Updating the Mitochondrial Free Radical Theory of Aging: An Integrated View, Key Aspects, and Confounding Concepts
Publication: Antioxidants & Redox Signaling
Volume 19, Issue Number 12
Abstract
An updated version of the mitochondrial free radical theory of aging (MFRTA) and longevity is reviewed. Key aspects of the theory are emphasized. Another main focus concerns common misconceptions that can mislead investigators from other specialties, even to wrongly discard the theory. Those different issues include (i) the main reactive oxygen species (ROS)-generating site in the respiratory chain in relation to aging and longevity: complex I; (ii) the close vicinity or even contact between that site and the mitochondrial DNA, in relation to the lack of local efficacy of antioxidants and to sub-cellular compartmentation; (iii) the relationship between mitochondrial ROS production and oxygen consumption; (iv) recent criticisms on the MFRTA; (v) the widespread assumption that ROS are simple “by-products” of the mitochondrial respiratory chain; (vi) the unnecessary postulation of “vicious cycle” hypotheses of mitochondrial ROS generation which are not central to the free radical theory of aging; and (vii) the role of DNA repair concerning endogenous versus exogenous damage. After considering the large body of data already available, two general characteristics responsible for the high maintenance degree of long-lived animals emerge: (i) a low generation rate of endogenous damage: and (ii) the possession of tissue macromolecules that are highly resistant to oxidative modification. Antioxid. Redox Signal. 19, 1420–1445.
Abstract
I. Introduction
II. An Integrated View on the MFRTA
A. Antioxidants do not control longevity
B. mtROSp and oxidative damage in mtDNA are low in long-lived animal species
C. The membrane fatty acid unsaturation degree is low in long-lived animals
D. DR lowers mtROSp and oxidative damage in mtDNA because it decreases the methionine dietary intake
III. MFRTA. Key Aspects and Confounding Concepts
A. The rate of mtROSp. The first known factor with capacity to explain longevity
1. mtROSp. What to measure or not and its meaning for MFRTA
2. mtROSp is not necessarily proportional to mitochondrial oxygen consumption
B. Criticisms on MFRTA: why they are unfounded
1. Failure to increase longevity by increasing antioxidants does not discredit the theory. It is mtROS generation, not elimination, that matters
2. ROS cannot cause degenerative diseases only, and not aging
3. Studies in naked-mole rats
4. Studies in birds and bats
C. ROS are not “by-products” of the respiratory chain: mtROSp and %FRL are regulated in each species at a level related to its longevity
D. The vicious cycle, an unnecessary hypothesis: mtROS generation does not need to increase with age to cause aging
E. DNA damage
1. Repair of endogenous DNA oxidative damage seems to be low in long-lived animals
IV. Conclusions
Get full access to this article
View all available purchase options and get full access to this article.
References
1.
Andziak BBuffenstein R. Disparate patterns of age-related changes in lipid peroxidation in long-lived naked mole-rats and shorter-lived miceAging Cell5525-5322006. 1. Andziak B and Buffenstein R. Disparate patterns of age-related changes in lipid peroxidation in long-lived naked mole-rats and shorter-lived mice. Aging Cell 5: 525–532, 2006.
2.
Andziak BO'Connor TPBuffenstein R. Antioxidants do not explain the disparate longevity between mice and the longest-living rodent, the naked mole-ratMech Ageing Dev1261206-12122005. 2. Andziak B, O'Connor TP, and Buffenstein R. Antioxidants do not explain the disparate longevity between mice and the longest-living rodent, the naked mole-rat. Mech Ageing Dev 126: 1206–1212, 2005.
3.
Andziak BO'Connor TPQi WDeWaal EMPierce AChaudhuri ARVan Remmen HBuffenstein R. High oxidative damage levels in the longest-living rodent, the naked mole-ratAging Cell5463-4712006. 3. Andziak B, O'Connor TP, Qi W, DeWaal EM, Pierce A, Chaudhuri AR, Van Remmen H, and Buffenstein R. High oxidative damage levels in the longest-living rodent, the naked mole-rat. Aging Cell 5: 463–471, 2006.
4.
Back PBraeckman BPMatthijssens F. ROS in aging Caenorhabditis elegans: damage or signaling?Oxid Med Cell Longev6084782012. 4. Back P, Braeckman BP, and Matthijssens F. ROS in aging Caenorhabditis elegans: damage or signaling? Oxid Med Cell Longev 608478, 2012.
5.
Barja G. Oxygen radicals, a failure or a success of evolution?Free Rad Res1863-701993. 5. Barja G. Oxygen radicals, a failure or a success of evolution? Free Rad Res 18: 63–70, 1993.
6.
Barja G. The flux of free radical attack through mitochondrial DNA is related to aging rateAging (Milano)12342-3552000. 6. Barja G. The flux of free radical attack through mitochondrial DNA is related to aging rate. Aging (Milano) 12: 342–355, 2000.
7.
Barja G. The quantitative measurement of H2O2 generation in isolated mitochondriaJ Bioenerg Biomembr34227-2332002. 7. Barja G. The quantitative measurement of H2O2 generation in isolated mitochondria. J Bioenerg Biomembr 34: 227–233, 2002.
8.
Barja G. Aging in vertebrates and the effect of caloric restriction: a mitochondrial free radical production-DNA damage mechanism?Biol Rev79235-2512004. 8. Barja G. Aging in vertebrates and the effect of caloric restriction: a mitochondrial free radical production-DNA damage mechanism? Biol Rev 79: 235–251, 2004.
9.
Barja G. Free radicals and agingTrends Neurosci27595-6002004. 9. Barja G. Free radicals and aging. Trends Neurosci 27: 595–600, 2004.
10.
Barja G. Mitochondrial oxygen consumption and ROS production are independently modulated. Implications for aging studiesRejuvenation Res10215-2232007. 10. Barja G. Mitochondrial oxygen consumption and ROS production are independently modulated. Implications for aging studies. Rejuvenation Res 10: 215–223, 2007.
11.
Barja G. The gene cluster hypothesis of aging and longevityBiogerontology957-662008. 11. Barja G. The gene cluster hypothesis of aging and longevity. Biogerontology 9: 57–66, 2008.
12.
Barja GLongevity and EvolutionNew YorkNova Science Publishers, Inc.20111-194. 12. Barja G. Longevity and Evolution. New York: Nova Science Publishers, Inc., 2011, pp. 1–194.
13.
Barja GCadenas SRojas CLópez-Torres MPérez-Campo R. A decrease of free radical production near critical sites as the main cause of maximum longevity in animalsComp Biochem Physiol108B501-5121994. 13. Barja G, Cadenas S, Rojas C, López-Torres M, and Pérez-Campo R. A decrease of free radical production near critical sites as the main cause of maximum longevity in animals. Comp Biochem Physiol 108B: 501–512, 1994.
14.
Barja GCadenas SRojas CPérez-Campo RLópez-Torres M. Low mitochondrial free radical production per unit O2 consumption can explain the simultaneous presence of high longevity and high metabolic rates in birdsFree Radic Res21317-3281994. 14. Barja G, Cadenas S, Rojas C, Pérez-Campo R, and López-Torres M. Low mitochondrial free radical production per unit O2 consumption can explain the simultaneous presence of high longevity and high metabolic rates in birds. Free Radic Res 21: 317–328, 1994.
15.
Barja GHerrero A. Localization at complex I and mechanism of the higher free radical production of brain non-synaptic mitochondria in the short-lived rat than in the longevous pigeonJ Bioenerg Biomembr30235-2431998. 15. Barja G and Herrero A. Localization at complex I and mechanism of the higher free radical production of brain non-synaptic mitochondria in the short-lived rat than in the longevous pigeon. J Bioenerg Biomembr 30: 235–243, 1998.
16.
Barja GHerrero A. Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammalsFASEB J14312-3182000. 16. Barja G and Herrero A. Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J 14: 312–318, 2000.
17.
Bender AKishnan KMorris MCTaylor GAReeve AKPerry RHJaros EHersheson JSBetts JKlopstock TTaylor RWTurnbull DM. High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson diseaseNature Genet38515-5172006. 17. Bender A, Kishnan K, Morris MC, Taylor GA, Reeve AK, Perry RH, Jaros E, Hersheson JS, Betts J, Klopstock T, Taylor RW, and Turnbull DM. High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nature Genet 38: 515–517, 2006.
18.
Berg BN. Study of vitamin E supplements in relation to muscular dystrophy and other diseases in aging ratsJ Gerontol14174-1801959. 18. Berg BN. Study of vitamin E supplements in relation to muscular dystrophy and other diseases in aging rats. J Gerontol 14: 174–180, 1959.
19.
Boveris ACadenas E. Mitochondrial production of hydrogen peroxide regulation by nitric oxide and the role of ubisemiquinoneIUBMB Life50245-2502000. 19. Boveris A and Cadenas E. Mitochondrial production of hydrogen peroxide regulation by nitric oxide and the role of ubisemiquinone. IUBMB Life 50: 245–250, 2000.
20.
Boveris ACadenas EStoppani AOM. Role of ubiquinone in the mitochondrial generation of hydrogen peroxideBiochem J156435-4441976. 20. Boveris A, Cadenas E, and Stoppani AOM. Role of ubiquinone in the mitochondrial generation of hydrogen peroxide. Biochem J 156: 435–444, 1976.
21.
Boveris AChance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygenBiochem J134707-7161973. 21. Boveris A and Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134: 707–716, 1973.
22.
Bovers AOshino NChance B. The cellular production of hydrogen peroxideBiochem J128617-6301972. 22. Bovers A, Oshino N, and Chance B. The cellular production of hydrogen peroxide. Biochem J 128: 617–630, 1972.
23.
Brunet-Rossinni AK. Reduced free-radical production and extreme longevity in the little brown bat (Myotis lucifugus) versus two non-flying mammalsMech Ageing Dev12511-202004. 23. Brunet-Rossinni AK. Reduced free-radical production and extreme longevity in the little brown bat (Myotis lucifugus) versus two non-flying mammals. Mech Ageing Dev 125: 11–20, 2004.
24.
Buffenstein REdrey YHYang TMele J. The oxidative stress theory of aging: embattled or invincible? Insights from non-traditional model organismsAge3099-1092008. 24. Buffenstein R, Edrey YH, Yang T, and Mele J. The oxidative stress theory of aging: embattled or invincible? Insights from non-traditional model organisms. Age 30: 99–109, 2008.
25.
Burch HBLowry OHBradley MEMax PF Jr. Hepatic metabolites and cofactors in riboflavin deficiency and calorie restrictionAm J Physiol219409-4151970. 25. Burch HB, Lowry OH, Bradley ME, and Max PF Jr. Hepatic metabolites and cofactors in riboflavin deficiency and calorie restriction. Am J Physiol 219: 409–415, 1970.
26.
Caro PGómez JArduini AGonzález-Sánchez MGonzález-García MBorrás CViña JPuertas MJSastre JBarja G. Mitochondrial DNA sequences are present inside nuclear DNA in rat tissues and increase with ageMitochondrion10479-4862010. 26. Caro P, Gómez J, Arduini A, González-Sánchez M, González-García M, Borrás C, Viña J, Puertas MJ, Sastre J, and Barja G. Mitochondrial DNA sequences are present inside nuclear DNA in rat tissues and increase with age. Mitochondrion 10: 479–486, 2010.
27.
Caro PGómez JLópez-Torres MSánchez INaudí AJove MPamplona RBarja G. Forty percent and eighty percent methionine restriction decrease mitochondrial ROS generation and oxidative stress in rat liverBiogerontology9183-1962008. 27. Caro P, Gómez J, López-Torres M, Sánchez I, Naudí A, Jove M, Pamplona R, and Barja G. Forty percent and eighty percent methionine restriction decrease mitochondrial ROS generation and oxidative stress in rat liver. Biogerontology 9: 183–196, 2008.
28.
Caro PGomez JSanchez IGarcia RLópez-Torres MNaudí APortero-Otin MPamplona RBarja G. Effect of 40% restriction of dietary amino acids -except methionine- on mitochondrial oxidative stress and biogenesis, AIF and SIRT1 in rat liverBiogerontology10579-5922009. 28. Caro P, Gomez J, Sanchez I, Garcia R, López-Torres M, Naudí A, Portero-Otin M, Pamplona R, and Barja G. Effect of 40% restriction of dietary amino acids -except methionine- on mitochondrial oxidative stress and biogenesis, AIF and SIRT1 in rat liver. Biogerontology 10: 579–592, 2009.
29.
Chaudhary AKNokubo MReddy GRYeola SNMorrow JDBlair IAMarnett LJ. Detection of endogenous malondialdehyde-deoxyguanosine adducts in human liverScience2651580-15821994. 29. Chaudhary AK, Nokubo M, Reddy GR, Yeola SN, Morrow JD, Blair IA, and Marnett LJ. Detection of endogenous malondialdehyde-deoxyguanosine adducts in human liver. Science 265: 1580–1582, 1994.
30.
Clapp NKSatterfield LCBowles ND. Effects of the antioxidant butylated hydroxytoluene (BHT) on mortality in BALB/c miceJ Gerontol34497-5011979. 30. Clapp NK, Satterfield LC, and Bowles ND. Effects of the antioxidant butylated hydroxytoluene (BHT) on mortality in BALB/c mice. J Gerontol 34: 497–501, 1979.
31.
Cochemé HMQuin CMcQuaker SJCabreiro FLogan APrime TAAbakumova IPatel JVFearnley IMJames AMPorteous CMSmith RASaeed SCarré JESinger MGems DHartley RCPartridge LMurphy MP. Measurement of H2O2 within living Drosophila during aging using a ratiometric mass spectrometry probe targeted to the mitochondrial matrixCell Metab13340-3502011. 31. Cochemé HM, Quin C, McQuaker SJ, Cabreiro F, Logan A, Prime TA, Abakumova I, Patel JV, Fearnley IM, James AM, Porteous CM, Smith RA, Saeed S, Carré JE, Singer M, Gems D, Hartley RC, Partridge L, and Murphy MP. Measurement of H2O2 within living Drosophila during aging using a ratiometric mass spectrometry probe targeted to the mitochondrial matrix. Cell Metab 13: 340–350, 2011.
32.
Colman JRAnderson RMJohnson SCKastman EKKosmatka KJBeasley TMAllison DBCruzen CSimmons HAKemnitz JWWeindruch R. Caloric restriction delays disease onset and mortality in rhesus monkeysScience325201-2042009. 32. Colman JR, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, Beasley TM, Allison DB, Cruzen C, Simmons HA, Kemnitz JW, and Weindruch R. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325: 201–204, 2009.
33.
Comfort AYouhotsky-Gore IPathmanathan K. Effect of ethoxyquin on the longevity of C3H miceNature229254-2551971. 33. Comfort A, Youhotsky-Gore I, and Pathmanathan K. Effect of ethoxyquin on the longevity of C3H mice. Nature 229: 254–255, 1971.
34.
Cortopassi GAWang E. There is substantial agreement among interspecies estimates of DNA repair activityMech Ageing Dev91211-2181996. 34. Cortopassi GA and Wang E. There is substantial agreement among interspecies estimates of DNA repair activity. Mech Ageing Dev 91: 211–218, 1996.
35.
Csiszar APodlutsky APodlutskaya NSonntag WEMerlin SZPhilipp EEDoyle KDavila ARecchia FABallabh PPinto JTUngvari Z. Testing the oxidative stress hypothesis of aging in primate fibroblasts: is there a correlation between species longevity and cellular ROS production?J Gerontol A67841-8522012. 35. Csiszar A, Podlutsky A, Podlutskaya N, Sonntag WE, Merlin SZ, Philipp EE, Doyle K, Davila A, Recchia FA, Ballabh P, Pinto JT, and Ungvari Z. Testing the oxidative stress hypothesis of aging in primate fibroblasts: is there a correlation between species longevity and cellular ROS production? J Gerontol A 67: 841–852, 2012.
36.
Dani DShimokawa IKomatsu THigami YWarnken USchokraie ESchnölzer MKrause FSugawa MDDencher NA. Modulation of oxidative phosphorylation machinery signifies a prime mode of anti-ageing mechanism of calorie restriction in male rat liver mitochondriaBiogerontology11321-3342010. 36. Dani D, Shimokawa I, Komatsu T, Higami Y, Warnken U, Schokraie E, Schnölzer M, Krause F, Sugawa MD, and Dencher NA. Modulation of oxidative phosphorylation machinery signifies a prime mode of anti-ageing mechanism of calorie restriction in male rat liver mitochondria. Biogerontology 11: 321–334, 2010.
37.
De AKChipalkatti SAiyar AS. Some biochemical parameters of ageing in relation to dietary proteinMech Ageing Dev2137-481983. 37. De AK, Chipalkatti S, and Aiyar AS. Some biochemical parameters of ageing in relation to dietary protein. Mech Ageing Dev 21: 37–48, 1983.
38.
Dlasková AHlavatá LJezek P. Oxidative stress caused by blocking of mitochondrial complex I H(+) pumping as a link in aging/disease vicious cycleInt J Biochem Cell Biol401792-18052008. 38. Dlasková A, Hlavatá L, and Jezek P. Oxidative stress caused by blocking of mitochondrial complex I H(+) pumping as a link in aging/disease vicious cycle. Int J Biochem Cell Biol 40: 1792–1805, 2008.
39.
Doonan RMcElwee JJMatthijssens FWalker GAHouthoofd KBack PMatscheski AVanfleteren JRGems D. Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegansGenes Dev223236-32412008. 39. Doonan R, McElwee JJ, Matthijssens F, Walker GA, Houthoofd K, Back P, Matscheski A, Vanfleteren JR, and Gems D. Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev 22: 3236–3241, 2008.
40.
Dufour EBoulay JRincheval VSainsard-Chanet A. A causal link between respiration and senescence in Podospora anserinaPNAS974138-41432000. 40. Dufour E, Boulay J, Rincheval V, and Sainsard-Chanet A. A causal link between respiration and senescence in Podospora anserina. PNAS 97: 4138–4143, 2000.
41.
Drew BPhaneuf SDirks ASelman CGredilla RLezza ABarja GLeeuwenburgh C. Effects of aging and caloric restriction on mitochondrial energy production in gastrocnemius muscle and heartAm J Physiol284R474-R4802003. 41. Drew B, Phaneuf S, Dirks A, Selman C, Gredilla R, Lezza A, Barja G, and Leeuwenburgh C. Effects of aging and caloric restriction on mitochondrial energy production in gastrocnemius muscle and heart. Am J Physiol 284: R474–R480, 2003.
42.
Dutton PLMoser CCSled VDDaldal FOhnishi T. A reductant-induced oxidation mechanism for complex IBiochim Biophys Acta1364245-2571998. 42. Dutton PL, Moser CC, Sled VD, Daldal F, and Ohnishi T. A reductant-induced oxidation mechanism for complex I. Biochim Biophys Acta 1364: 245–257, 1998.
43.
Fleming JEMiquel JCottrell SFYengoyan LSEconomos AC. Is cell aging caused by respiration-dependent injury to the mitochondrial genome?Gerontology2844-531982. 43. Fleming JE, Miquel J, Cottrell SF, Yengoyan LS, and Economos AC. Is cell aging caused by respiration-dependent injury to the mitochondrial genome? Gerontology 28: 44–53, 1982.
44.
Fontana LPartridge LLongo VD. Extending healthy life span—from yeast to humansScience328321-3262010. 44. Fontana L, Partridge L, and Longo VD. Extending healthy life span—from yeast to humans. Science 328: 321–326, 2010.
45.
Genova MLVentura BGiuliano GBovina CFormiggini GParenti Castelli GLenaz G. The state of production of superoxide radical in mitochondrial complex I is not a bound semiquinone but presumably iron-sulphur cluster N2FEBS Lett505364-3682001. 45. Genova ML, Ventura B, Giuliano G, Bovina C, Formiggini G, Parenti Castelli G, and Lenaz G. The state of production of superoxide radical in mitochondrial complex I is not a bound semiquinone but presumably iron-sulphur cluster N2. FEBS Lett 505: 364–368, 2001.
46.
Goodrick CL. Effects of long-term voluntary wheel exercise on male and female Wistar rats. I. Longevity, body weight, and metabolic rateGerontology2622-331980. 46. Goodrick CL. Effects of long-term voluntary wheel exercise on male and female Wistar rats. I. Longevity, body weight, and metabolic rate. Gerontology 26: 22–33, 1980.
47.
Grandison RCPiper MDPartridge L. Amino-acid imbalance explains extension of lifespan by dietary restriction in DrosophilaNature4621061-10642009. 47. Grandison RC, Piper MD, and Partridge L. Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462: 1061–1064, 2009.
48.
Gredilla RBarja G. The role of oxidative stress in relation to caloric restriction and longevityEndocrinology1463713-37172005. 48. Gredilla R and Barja G. The role of oxidative stress in relation to caloric restriction and longevity. Endocrinology 146: 3713–3717, 2005.
49.
Gredilla RBarja GLópez-Torres M. Effect of short-term caloric restriction on H2O2 production and oxidative DNA damage in rat liver mitochondria and location of the free radical sourceJ Bioenerg Biomembr33279-2872001. 49. Gredilla R, Barja G, and López-Torres M. Effect of short-term caloric restriction on H2O2 production and oxidative DNA damage in rat liver mitochondria and location of the free radical source. J Bioenerg Biomembr 33: 279–287, 2001.
50.
Gredilla RSanz ALopez-Torres MBarja G. Caloric restriction decreases mitochondrial free radical generation at complex I and lowers oxidative damage to mitochondrial DNA in the rat heartFASEB J151589-15912001. 50. Gredilla R, Sanz A, Lopez-Torres M, and Barja G. Caloric restriction decreases mitochondrial free radical generation at complex I and lowers oxidative damage to mitochondrial DNA in the rat heart. FASEB J 15: 1589–1591, 2001.
51.
Hamilton MLGuo ZFuller CDVan Remmen HWard WFAustad SNTroyer DAThompson IRichardson A. A reliable assessment of 8-oxo-2-deoxyguanosine levels in nuclear and mitochondrial DNA using the sodium iodide method to isolate DNANucleic Acids Res292117-21262001. 51. Hamilton ML, Guo Z, Fuller CD, Van Remmen H, Ward WF, Austad SN, Troyer DA, Thompson I, and Richardson A. A reliable assessment of 8-oxo-2-deoxyguanosine levels in nuclear and mitochondrial DNA using the sodium iodide method to isolate DNA. Nucleic Acids Res 29: 2117–2126, 2001.
52.
Harman D. Aging: a theory based on free radical and radiation chemistryJ Gerontol11298-3001956. 52. Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol 11: 298–300, 1956.
53.
Harman D. Free radical theory of aging: effect of free radical reaction inhibitors on the mortality rate of male LAF1 miceJ Gerontol23476-4821968. 53. Harman D. Free radical theory of aging: effect of free radical reaction inhibitors on the mortality rate of male LAF1 mice. J Gerontol 23: 476–482, 1968.
54.
Harman D. The biological clock: the mitochondria?J Am Geriatr Soc20145-1471972. 54. Harman D. The biological clock: the mitochondria? J Am Geriatr Soc 20: 145–147, 1972.
55.
Harris SBWeindruch RSmith GSMickey MRWalford RL. Dietary restriction alone and in combination with oral ethoxyquine/2-mercaptoethylamine in miceJ Gerontol45B141-B1471990. 55. Harris SB, Weindruch R, Smith GS, Mickey MR, and Walford RL. Dietary restriction alone and in combination with oral ethoxyquine/2-mercaptoethylamine in mice. J Gerontol 45: B141–B147, 1990.
56.
Hashizume OShimizu AYokota MSugiyama ANakada KMiyoshi HItami MOhira MNagase HTakenaga KHayashi J-I. Specific mitochondrial DNA mutation in mice regulates diabetes and linfoma developmentProc Natl Acad Sci U S A10910528-105332012. 56. Hashizume O, Shimizu A, Yokota M, Sugiyama A, Nakada K, Miyoshi H, Itami M, Ohira M, Nagase H, Takenaga K, and Hayashi J-I. Specific mitochondrial DNA mutation in mice regulates diabetes and linfoma development. Proc Natl Acad Sci U S A 109: 10528–10533, 2012.
57.
Hayflick L. Theories of biological agingExp Gerontol20145-1591985. 57. Hayflick L. Theories of biological aging. Exp Gerontol 20: 145–159, 1985.
58.
Heidrick MLHendircks LCCook DE. Effect of dietary 2-mercaptoethanol on the life span, immune system, tumor incidence and lipid peroxidation damage in spleen lymphocytes of aging BC3F1 miceMech Aging Dev27341-3581984. 58. Heidrick ML, Hendircks LC, and Cook DE. Effect of dietary 2-mercaptoethanol on the life span, immune system, tumor incidence and lipid peroxidation damage in spleen lymphocytes of aging BC3F1 mice. Mech Aging Dev 27: 341–358, 1984.
59.
Herrero ABarja G. Sites and mechanisms responsible for the low rate of free radical production of heart mitochondria in the long-lived pigeonMech Ageing Dev9895-1111997. 59. Herrero A and Barja G. Sites and mechanisms responsible for the low rate of free radical production of heart mitochondria in the long-lived pigeon. Mech Ageing Dev 98: 95–111, 1997.
60.
Herrero A. and Barja G. ADP regulation of mitochondrial free radical production is different with complex I- or complex II-linked substrates: implications for the exercise paradox and brain hypermetabolismJ Bioenerg Biomembr29241-2491997. 60. Herrero A. and Barja G. ADP regulation of mitochondrial free radical production is different with complex I- or complex II-linked substrates: implications for the exercise paradox and brain hypermetabolism. J Bioenerg Biomembr 29: 241–249, 1997.
61.
Herrero ABarja G. H2O2 production of heart mitochondria and aging rate are slower in canaries and parakeets than in mice: sites of free radical generation and mechanisms involvedMech Ageing Dev103133-1461998. 61. Herrero A and Barja G. H2O2 production of heart mitochondria and aging rate are slower in canaries and parakeets than in mice: sites of free radical generation and mechanisms involved. Mech Ageing Dev 103: 133–146, 1998.
62.
Herrero ABarja G. 8-oxodeoxyguanosine levels in heart and brain mitochondrial and nuclear DNA of two mammals and three birds in relation to their different rates of agingAging Clin Exp Res11294-3001999. 62. Herrero A and Barja G. 8-oxodeoxyguanosine levels in heart and brain mitochondrial and nuclear DNA of two mammals and three birds in relation to their different rates of aging. Aging Clin Exp Res 11: 294–300, 1999.
63.
Herrero ABarja G. Localization of the site of oxygen radical generation inside the Complex I of heart and non-synaptic brain mammalian mitochondriaJ Bioenerg Biomembr32609-6152000. 63. Herrero A and Barja G. Localization of the site of oxygen radical generation inside the Complex I of heart and non-synaptic brain mammalian mitochondria. J Bioenerg Biomembr 32: 609–615, 2000.
64.
Hoffman DLSalter JDBrooks PS. The response of mitochondrial reactive oxygen species generation to steady-state oxygen tension: implications for hypoxic cell signallingAm J Physiol291H101-H1082007. 64. Hoffman DL, Salter JD, and Brooks PS. The response of mitochondrial reactive oxygen species generation to steady-state oxygen tension: implications for hypoxic cell signalling. Am J Physiol 291: H101–H108, 2007.
65.
Holloszy JOSmith EKVining MAdams SA. Effect of voluntary exercise on longevity in ratsJ Appl Physiol59826-8311985. 65. Holloszy JO, Smith EK, Vining M, and Adams SA. Effect of voluntary exercise on longevity in rats. J Appl Physiol 59: 826–831, 1985.
66.
Houtfood KBraeckman BPLenaerts IBrys KDe Vreese AVan Eygen SVanfleteren JR. No reduction of metabolic rate in food restricted Caenorhabditis elegansExp Gerontol371359-13692002. 66. Houtfood K, Braeckman BP, Lenaerts I, Brys K, De Vreese A, Van Eygen S, and Vanfleteren JR. No reduction of metabolic rate in food restricted Caenorhabditis elegans. Exp Gerontol 37: 1359–1369, 2002.
67.
Hulbert TPamplona RBuffenstein RButtemer WA. Life and death: metabolic rate, membrane composition and lifespan of animalsPhysiol Rev871175-12132007. 67. Hulbert T, Pamplona R, Buffenstein R, and Buttemer WA. Life and death: metabolic rate, membrane composition and lifespan of animals. Physiol Rev 87: 1175–1213, 2007.
68.
Hulbert AJ. The links between membrane composition, metabolic rate and lifespanComp Biochem Physiol A150196-2032008. 68. Hulbert AJ. The links between membrane composition, metabolic rate and lifespan. Comp Biochem Physiol A 150: 196–203, 2008.
69.
Hütter ESkobro MLener BPrats CRabol RDela FJansen-Dürr P. Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged skeletal muscleAging Cell6245-2562007. 69. Hütter E, Skobro M, Lener B, Prats C, Rabol R, Dela F, and Jansen-Dürr P. Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged skeletal muscle. Aging Cell 6: 245–256, 2007.
70.
Judge SJang YMSmith AHagen TLeeuwenburgh C. Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of agingFASEB J19419-4212005. 70. Judge S, Jang YM, Smith A, Hagen T, and Leeuwenburgh C. Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of aging. FASEB J 19: 419–421, 2005.
71.
Judge SJang YMSmith ASelman CPhillips TSpeakman JRHagen TLeeuwenburgh C. Exercise by long-life voluntary running reduces subsarcolemmal and interfibrilar hydrogen peroxide production in the rat heartAm J Physiol89R1564-R15722005. 71. Judge S, Jang YM, Smith A, Selman C, Phillips T, Speakman JR, Hagen T, and Leeuwenburgh C. Exercise by long-life voluntary running reduces subsarcolemmal and interfibrilar hydrogen peroxide production in the rat heart. Am J Physiol 89: R1564–R1572, 2005.
72.
Keaney MGems D. No increase in lifespan in Caenorhabditis elegans upon treatment with the superoxide dismutase mimetic EUK-8Free Radic Biol Med34277-2822003. 72. Keaney M and Gems D. No increase in lifespan in Caenorhabditis elegans upon treatment with the superoxide dismutase mimetic EUK-8. Free Radic Biol Med 34: 277–282, 2003.
73.
Kirkwood TBL. A systematic look to an old problem: as life expectancy increases, a systems-biology approach is needed to ensure that we have a healthy old ageNature451644-6472008. 73. Kirkwood TBL. A systematic look to an old problem: as life expectancy increases, a systems-biology approach is needed to ensure that we have a healthy old age. Nature 451: 644–647, 2008.
74.
Kohn RR. Effect of antioxidants on life-span of C57BL miceJ Gerontol26378-3801971. 74. Kohn RR. Effect of antioxidants on life-span of C57BL mice. J Gerontol 26: 378–380, 1971.
75.
Kraytsberg YKudryavtseva EMcKee ACGeula CKowall NWKhrapko K. Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neuronsNat Genet38518-5202006. 75. Kraytsberg Y, Kudryavtseva E, McKee AC, Geula C, Kowall NW, and Khrapko K. Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat Genet 38: 518–520, 2006.
76.
Kregel KCZhang HJ. An integrated view of oxidative stress in aging: basic mechanisms, functional effects, and pathological considerationsAm J Physiol292R18-R362007. 76. Kregel KC and Zhang HJ. An integrated view of oxidative stress in aging: basic mechanisms, functional effects, and pathological considerations. Am J Physiol 292: R18–R36, 2007.
77.
Ku HHBrunk UTSohal RS. Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian speciesFree Radic Biol Med15621-6271993. 77. Ku HH, Brunk UT, and Sohal RS. Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species. Free Radic Biol Med 15, 621–627, 1993.
78.
Kudin APMalinska DKunz WS. Sites of generation of reactive oxygen species in homogenates of brain tissue determined with the use of respiratory substrates and inhibitorsBiochim Biophys Acta1777689-6952008. 78. Kudin AP, Malinska D, and Kunz WS. Sites of generation of reactive oxygen species in homogenates of brain tissue determined with the use of respiratory substrates and inhibitors. Biochim Biophys Acta 1777: 689–695, 2008.
79.
Kujoth GCHiona APugh TDSomeya SPanzer KWohlgemuth SEHofer TSeo AYSullivan RJobling WAMorrow JDVan Remmen HSedivy JMYamasoba TTanokura MWeindruch RLeeuwenburgh CProlla TA. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian agingScience309481-4842005. 79. Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K, Wohlgemuth SE, Hofer T, Seo AY, Sullivan R, Jobling WA, Morrow JD, Van Remmen H, Sedivy JM, Yamasoba T, Tanokura M, Weindruch R, Leeuwenburgh C, and Prolla TA. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309: 481–484, 2005.
80.
Kushnareva YMurphy AAndreyev A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P+) oxidation-reduction stateBiochem J368545-5532002. 80. Kushnareva Y, Murphy A, and Andreyev A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P+) oxidation-reduction state. Biochem J 368: 545–553, 2002.
81.
Lambert ABrand M. Inhibitors of the quinine-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I)J Biol Chem27939414-394202004. 81. Lambert A and Brand M. Inhibitors of the quinine-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Biol Chem 279: 39414–39420, 2004.
82.
Lambert ABoysen HBuckingham JAYang TPodlutsky AAustad SNKunz THBuffenstein RBrand D. Low rates of hydrogen peroxide production by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeothermsAging Cell6607-6182007. 82. Lambert A, Boysen H, Buckingham JA, Yang T, Podlutsky A, Austad SN, Kunz TH, Buffenstein R, and Brand D. Low rates of hydrogen peroxide production by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeotherms. Aging Cell 6: 607–618, 2007.
83.
Lambert AJPortero-Otin MPamplona RMerry BJ. Effect of ageing and caloric restriction on specific markers of protein oxidative damage and membrane peroxidizability in rat liver mitochondriaMech Ageing Dev125529-5382004. 83. Lambert AJ, Portero-Otin M, Pamplona R, and Merry BJ. Effect of ageing and caloric restriction on specific markers of protein oxidative damage and membrane peroxidizability in rat liver mitochondria. Mech Ageing Dev 125: 529–538, 2004.
84.
Lawrence ABurk RF. Species, tissue and subcellular distribution of non-Se dependent glutathione peroxidasa activityJ Nutr108211-2151978. 84. Lawrence A and Burk RF. Species, tissue and subcellular distribution of non-Se dependent glutathione peroxidasa activity. J Nutr 108: 211–215, 1978.
85.
Ledvina MHodánová M. The effect of simultaneous administration of tocopherol and sunflower oil on the life-span of female miceExp Gerontol1567-711980. 85. Ledvina M and Hodánová M. The effect of simultaneous administration of tocopherol and sunflower oil on the life-span of female mice. Exp Gerontol 15: 67–71, 1980.
86.
Lee IMSieh CCHPaffenbarger RS. Exercise intensity and longevity in men. The Harvard Alumni Health StudyJAMA2731179-11841995. 86. Lee IM, Sieh CCH, and Paffenbarger RS. Exercise intensity and longevity in men. The Harvard Alumni Health Study. JAMA 273: 1179–1184, 1995.
87.
Lee KPSimpson SJClissold FJBrooks RBallard JWTaylor PWSoran NRaubenheimer D. Lifespan and reproduction in Drosophila: new insights from nutritional geometryPNAS1052498-25032008. 87. Lee KP, Simpson SJ, Clissold FJ, Brooks R, Ballard JW, Taylor PW, Soran N, and Raubenheimer D. Lifespan and reproduction in Drosophila: new insights from nutritional geometry. PNAS 105: 2498–2503, 2008.
88.
Lee YSChoi JYPark MKChoi EMKasai HChung MH. Induction of oh8Gua glycosylase in rat kidneys by potassium bromate (KBrO3), a renal carcinogenMutat Res364227-2331996. 88. Lee YS, Choi JY, Park MK, Choi EM, Kasai H, and Chung MH. Induction of oh8Gua glycosylase in rat kidneys by potassium bromate (KBrO3), a renal carcinogen. Mutat Res 364: 227–233, 1996.
89.
Lehninger ALPrinciples of BiochemistryNew YorkFreeman and Co.2005. 89. Lehninger AL. Principles of Biochemistry. New York: Freeman and Co., 2005.
90.
Liang SMele JWu YBuffenstein RHornsby PJ. Resistance to experimental tumorigenesis in cells of a long-lived mammal, the naked mole-rat (Heterocephalus glaber)Aging Cell9626-6352010. 90. Liang S, Mele J, Wu Y, Buffenstein R, and Hornsby PJ. Resistance to experimental tumorigenesis in cells of a long-lived mammal, the naked mole-rat (Heterocephalus glaber). Aging Cell 9: 626–635, 2010.
91.
Lin SJKaeberlein MAndalis AASturtz LADefossez PACulotta VCFink GRGuarante L. Caloric restriction extends Saccharomyces cerevisae life span by increasing respirationNature418344-3482002. 91. Lin SJ, Kaeberlein M, Andalis AA, Sturtz LA, Defossez PA, Culotta VC, Fink GR, and Guarante L. Caloric restriction extends Saccharomyces cerevisae life span by increasing respiration. Nature 418: 344–348, 2002.
92.
Linnane AWKios MMVitteta L. Healthy aging: regulation of the metabolome by cellular redox modulation and prooxidant signalling systems: the essential roles of superoxide anion and hydrogen peroxideBiogerontology8445-4672007. 92. Linnane AW, Kios MM, and Vitteta L. Healthy aging: regulation of the metabolome by cellular redox modulation and prooxidant signalling systems: the essential roles of superoxide anion and hydrogen peroxide. Biogerontology 8: 445–467, 2007.
93.
Liu YFiskum GSchubert D. Generation of reactive oxygen species by the electron transport chainJ Neurochem80780-7872002. 93. Liu Y, Fiskum G, and Schubert D. Generation of reactive oxygen species by the electron transport chain. J Neurochem 80: 780–787, 2002.
94.
Longo VDMitteldorf JSkulachev VP. Programmed and altruistic agingNat Rev Genet6866-8722005. 94. Longo VD, Mitteldorf J, and Skulachev VP. Programmed and altruistic aging. Nat Rev Genet 6: 866–872, 2005.
95.
López-Torres MBarja G. Lowered methionine ingestion as responsible for the decrease in rodent mitochondrial oxidative stress in protein and dietary restriction. Possible implications for humansBiochim Biophys Acta17801337-13472008. 95. López-Torres M and Barja G. Lowered methionine ingestion as responsible for the decrease in rodent mitochondrial oxidative stress in protein and dietary restriction. Possible implications for humans. Biochim Biophys Acta 1780: 1337–1347, 2008.
96.
López-Torres MGredilla RSanz ABarja G. Influence of aging and long-term caloric restriction on oxygen radical generation and oxidative DNA damage in rat liver mitochondriaFree Radic Biol Med32882-8892002. 96. López-Torres M, Gredilla R, Sanz A, and Barja G. Influence of aging and long-term caloric restriction on oxygen radical generation and oxidative DNA damage in rat liver mitochondria. Free Radic Biol Med 32: 882–889, 2002.
97.
López-Torres MPérez-Campo RRojas CCadenas SBarja G. Maximum life span in vertebrates: correlation with liver antioxidant enzymes, glutathione system, ascorbate, urate, sensitivity to peroxidation, true malondialdehyde, in vivo H2O2, and basal and maximum aerobic capacityMech Ageing Dev70177-1991993. 97. López-Torres M, Pérez-Campo R, Rojas C, Cadenas S, and Barja G. Maximum life span in vertebrates: correlation with liver antioxidant enzymes, glutathione system, ascorbate, urate, sensitivity to peroxidation, true malondialdehyde, in vivo H2O2, and basal and maximum aerobic capacity. Mech Ageing Dev 70: 177–199, 1993.
98.
López-Torres MPérez-Campo RRojas CCadenas SBarja de Quiroga G. Simultaneous induction of superoxide dismutase, glutathione reductase, GSH and ascorbate in liver and kidney correlates with survival throughout the life spanFree Radic Biol Med15133-1421993. 98. López-Torres M, Pérez-Campo R, Rojas C, Cadenas S, and Barja de Quiroga G. Simultaneous induction of superoxide dismutase, glutathione reductase, GSH and ascorbate in liver and kidney correlates with survival throughout the life span. Free Radic Biol Med 15: 133–142, 1993.
99.
Magalhães JPChurch GM. Cells discover fire: employing reactive oxygen species in development and consequences for agingExp Gerontol411-102006. 99. Magalhães JP and Church GM. Cells discover fire: employing reactive oxygen species in development and consequences for aging. Exp Gerontol 41: 1–10, 2006.
100.
Mattison JARoth GSBeasley TMTilmont EMHandy AMHerbert RLLongo DLAllison DBYoung JEBryant MBarnard DWard WFQi WIngram D. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA studyNature489318-3212012. 100. Mattison JA, Roth GS, Beasley TM, Tilmont EM, Handy AM, Herbert RL, Longo DL, Allison DB, Young JE, Bryant M, Barnard D, Ward WF, Qi W, and Ingram D. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 489: 318–321, 2012.
101.
McCarter RMasoro EJYu BP. Does food restriction retard aging by reducing metabolic rate?Am J Physiol248E488-E4901985. 101. McCarter R, Masoro EJ, and Yu BP. Does food restriction retard aging by reducing metabolic rate? Am J Physiol 248: E488–E490, 1985.
102.
Melov SRavenscroft JMalik SGill MSWalker DWClayton PEWallace DCMalfroy BDoctrow SRLithgow GJ. Extension of life-span with superoxide dismutase/catalase mimeticsScience2891567-15692000. 102. Melov S, Ravenscroft J, Malik S, Gill MS, Walker DW, Clayton PE, Wallace DC, Malfroy B, Doctrow SR, and Lithgow GJ. Extension of life-span with superoxide dismutase/catalase mimetics. Science 289: 1567–1569, 2000.
103.
Meyer AJDick TP. Fluorescent protein-based redox probesAntioxid Redox Signal13621-6502010. 103. Meyer AJ and Dick TP. Fluorescent protein-based redox probes. Antioxid Redox Signal 13: 621–650, 2010.
104.
Milgram NWRacine RJNellis PMendonca AIvy GO. Maintenance on l-deprenyl prolongs life in aged male ratsLife Sci47415-4201990. 104. Milgram NW, Racine RJ, Nellis P, Mendonca A, and Ivy GO. Maintenance on l-deprenyl prolongs life in aged male rats. Life Sci 47: 415–420, 1990.
105.
Miller RABuehner GChang YHarper JMSigler RSmith-Wheelock M. Methionine-deficient diet extends mouse lifespan, slows immune and lens aging, alters glucose, T4, IGF-I and insulin levels, and increases hepatocyte MIF levels and stress resistanceAging Cell4119-1252005. 105. Miller RA, Buehner G, Chang Y, Harper JM, Sigler R, and Smith-Wheelock M. Methionine-deficient diet extends mouse lifespan, slows immune and lens aging, alters glucose, T4, IGF-I and insulin levels, and increases hepatocyte MIF levels and stress resistance. Aging Cell 4: 119–125, 2005.
106.
Muller F. The nature and mechanism of superoxide production by the electron transport chain: its relevance to agingJ Am Aging Assoc23227-2532000. 106. Muller F. The nature and mechanism of superoxide production by the electron transport chain: its relevance to aging. J Am Aging Assoc 23: 227–253, 2000.
107.
Muller FLLustgarten MSJang YRichardson ARemmen HV. Trends in oxidative aging theoriesFree Radic Biol Med43477-5032007. 107. Muller FL, Lustgarten MS, Jang Y, Richardson A, and Remmen HV. Trends in oxidative aging theories. Free Radic Biol Med 43: 477–503, 2007.
108.
Muller FLSong WJang YCLiu YSabia MRichardson AVan Remmen H. Denervation-induced skeletal muscle atrophy is associated with increased mitochondrial ROS productionAm J Physiol293R1159-R11682007. 108. Muller FL, Song W, Jang YC, Liu Y, Sabia M, Richardson A, and Van Remmen H. Denervation-induced skeletal muscle atrophy is associated with increased mitochondrial ROS production. Am J Physiol 293: R1159–R1168, 2007.
109.
Munro DBlier PU. The extreme longevity of Arctica islandica is associated with increased peroxidation resistance in mitochondrial membranesAging Cell11845-8552012. 109. Munro D and Blier PU. The extreme longevity of Arctica islandica is associated with increased peroxidation resistance in mitochondrial membranes. Aging Cell 11: 845–855, 2012.
110.
Murphy MP. How mitochondria produce reactive oxygen speciesBiochem J4171-132009. 110. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 417: 1–13, 2009.
111.
Naudi AJove MAyala VPortero-Otín MBarja GPamplona R. Regulation of membrane unsaturation as antioxidant adaptive mechanisms in long-lived animal speciesFree Radic Antiox13-122011. 111. Naudi A, Jove M, Ayala V, Portero-Otín M, Barja G, and Pamplona R. Regulation of membrane unsaturation as antioxidant adaptive mechanisms in long-lived animal species. Free Radic Antiox 1: 3–12, 2011.
112.
Nicholls DG. Mitochondrial membrane potential and agingAging Cell335-402004. 112. Nicholls DG. Mitochondrial membrane potential and aging. Aging Cell 3: 35–40, 2004.
113.
Nisoli ETonello CCardile ACozzi VBracale RTedesco LFalcone SValerio ACantoni OClementi EMoncada SCarruba MO. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOSScience310314-3172005. 113. Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, and Carruba MO. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310: 314–317, 2005.
114.
Nohl HHegner D. Do mitochondria produce oxygen radicals in vivo?Eur J Biochem82563-5671978. 114. Nohl H and Hegner D. Do mitochondria produce oxygen radicals in vivo? Eur J Biochem 82: 563–567, 1978.
115.
Oeriu SVochitu E. The effect of the administration of compounds which contain sulfhydryl groups on the survival rates of mice, rats, and guinea pigsJ Gerontol20417-4191965. 115. Oeriu S and Vochitu E. The effect of the administration of compounds which contain sulfhydryl groups on the survival rates of mice, rats, and guinea pigs. J Gerontol 20: 417–419, 1965.
116.
Paffenbarger RSHyde RTWing ALHsie C. Physical activity, all-cause mortality, and longevity of college alumniN Engl J Med314605-6131986. 116. Paffenbarger RS, Hyde RT, Wing AL, and Hsie C. Physical activity, all-cause mortality, and longevity of college alumni. N Engl J Med 314: 605–613, 1986.
117.
Page MMRichardson JWiens BFTiedtke FPeters CWFaure PABurness GStuart JA. Antioxidant enzyme activities are not broadly correlated with longevity in 14 vertebrate endothermic speciesAge32255-2702010. 117. Page MM, Richardson J, Wiens BF, Tiedtke F, Peters CW, Faure PA, Burness G, and Stuart JA. Antioxidant enzyme activities are not broadly correlated with longevity in 14 vertebrate endothermic species. Age 32: 255–270, 2010.
118.
Page MMStuart JA. Activities of DNA base excision repair enzymes in liver and brain correlate with body mass, but not with lifespanAge (Dordr)341195-12092011. 118. Page MM and Stuart JA. Activities of DNA base excision repair enzymes in liver and brain correlate with body mass, but not with lifespan. Age (Dordr) 34: 1195–1209, 2011.
119.
Pamplona RBarja G. Mitochondrial oxidative stress, aging and caloric restriction: the protein and methionine connectionBiochim Biophys Acta Bioenerg1757496-5082006. 119. Pamplona R and Barja G. Mitochondrial oxidative stress, aging and caloric restriction: the protein and methionine connection. Biochim Biophys Acta Bioenerg 1757: 496–508, 2006.
120.
Pamplona RBarja G. An evolutionary comparative scan for longevity-related oxidative stress resistance mechanisms in homeothermsBiogerontology12409-4352011. 120. Pamplona R and Barja G. An evolutionary comparative scan for longevity-related oxidative stress resistance mechanisms in homeotherms. Biogerontology 12: 409–435, 2011.
121.
Pamplona RBarja GPortero-Otín M. Membrane fatty acid unsaturation, protection against oxidative stress, and maximum life span: a homeoviscous-longevity adaptationAnn N Y Acad Sci959475-4902002. 121. Pamplona R, Barja G, and Portero-Otín M. Membrane fatty acid unsaturation, protection against oxidative stress, and maximum life span: a homeoviscous-longevity adaptation. Ann N Y Acad Sci 959: 475–490, 2002.
122.
Pamplona RConstantini D. Molecular and structural antioxidant defenses against oxidative stress in animalsAm J Physiol301R843-R8632011. 122. Pamplona R and Constantini D. Molecular and structural antioxidant defenses against oxidative stress in animals. Am J Physiol 301: R843–R863, 2011.
123.
Pamplona RPortero-Otín MRequena JGredilla RBarja G. Oxidative, glycoxidative and lipoxidative damage to rat heart mitochondrial proteins is lower after four months of caloric restriction than in age-matched controlsMech Ageing Dev1231437-14462002. 123. Pamplona R, Portero-Otín M, Requena J, Gredilla R, and Barja G. Oxidative, glycoxidative and lipoxidative damage to rat heart mitochondrial proteins is lower after four months of caloric restriction than in age-matched controls. Mech Ageing Dev 123: 1437–1446, 2002.
124.
Pamplona RPortero-Otín MRuiz CGredilla RHerrero ABarja G. Double bond content of phospholipids and lipid peroxidation negatively correlate with maximum longevity in the heart of mammalsMech Ageing Dev112169-1831999. 124. Pamplona R, Portero-Otín M, Ruiz C, Gredilla R, Herrero A, and Barja G. Double bond content of phospholipids and lipid peroxidation negatively correlate with maximum longevity in the heart of mammals. Mech Ageing Dev 112: 169–183, 1999.
125.
Pamplona RPortero-Otín MRuiz CPrat JBellmunt MJBarja G. Mitochondrial membrane peroxidizability index is inversely related to maximum life span in mammalsJ Lipid Res391989-19941998. 125. Pamplona R, Portero-Otín M, Ruiz C, Prat J, Bellmunt MJ, and Barja G. Mitochondrial membrane peroxidizability index is inversely related to maximum life span in mammals. J Lipid Res 39: 1989–1994, 1998.
126.
Pamplona RPrat JCadenas SRojas CPérez-Campo RLópez-Torres MBarja G. Low fatty acid unsaturation protects against lipid peroxidation in liver mitochondria from longevous species: the pigeon and human caseMech Ageing Dev8653-661996. 126. Pamplona R, Prat J, Cadenas S, Rojas C, Pérez-Campo R, López-Torres M, and Barja G. Low fatty acid unsaturation protects against lipid peroxidation in liver mitochondria from longevous species: the pigeon and human case. Mech Ageing Dev 86: 53–66, 1996.
127.
Pearl RThe Rate of LivingLondonUniversity of London Press1928. 127. Pearl R. The Rate of Living. London: University of London Press, 1928.
128.
Perez VIBokov AVan Remmen HMele JRan QIkeno YRichardson A. Is the oxidative stress theory of aging dead?Biochim Biophys Acta17901005-10142009. 128. Perez VI, Bokov A, Van Remmen H., Mele J, Ran Q, Ikeno Y, and Richardson A. Is the oxidative stress theory of aging dead? Biochim Biophys Acta 1790: 1005–1014, 2009.
129.
Pérez VIBuffenstein RMasamsetti VLeonard SSalmon ABMele JAndziak BYang TEdrey YFriguet BWard WRichardson AChaudhuri A. Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole-ratPNAS1063059-30642009. 129. Pérez VI, Buffenstein R, Masamsetti V, Leonard S, Salmon AB, Mele J, Andziak B, Yang T, Edrey Y, Friguet B, Ward W, Richardson A, and Chaudhuri A. Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole-rat. PNAS 106: 3059–3064, 2009.
130.
Pérez-Campo RLópez-Torres MCadenas SRojas CBarja G. The rate of free radical production as a determinant of the rate of aging: evidence from the comparative approachJ Comp Physiol B168149-1581998. 130. Pérez-Campo R, López-Torres M, Cadenas S, Rojas C, and Barja G. The rate of free radical production as a determinant of the rate of aging: evidence from the comparative approach. J Comp Physiol B 168: 149–158, 1998.
131.
Pérez-Campo RLópez-Torres MRojas CCadenas SBarja G. Longevity and antioxidant enzymes, non-enzymatic antioxidants, oxidative stress, malondialdehyde, and in vivo H2O2 levels in the vertebrate lung: a comparative studyJ Comp Physiol163682-6891994. 131. Pérez-Campo R, López-Torres M, Rojas C, Cadenas S, and Barja G. Longevity and antioxidant enzymes, non-enzymatic antioxidants, oxidative stress, malondialdehyde, and in vivo H2O2 levels in the vertebrate lung: a comparative study. J Comp Physiol 163: 682–689, 1994.
132.
Porta EAJoun NSNitta RT. Effects of the type of dietary fat at two levels of vitamin E in Wistar male rats during development and aging. I. Life span, serum biochemical parameters and pathological changesMech Aging Dev131-391980. 132. Porta EA, Joun NS, and Nitta RT. Effects of the type of dietary fat at two levels of vitamin E in Wistar male rats during development and aging. I. Life span, serum biochemical parameters and pathological changes. Mech Aging Dev 13: 1–39, 1980.
133.
Rattan S. Targeting the age-related occurrence, removal, and accumulation of molecular damage by hormesisAnn N Y Acad Sci119728-322010. 133. Rattan S. Targeting the age-related occurrence, removal, and accumulation of molecular damage by hormesis. Ann N Y Acad Sci 1197: 28–32, 2010.
134.
Richie JP Jr.Leutzinger YParthasarathy SMalloy VOrentreich NZimmerman JA. Methionine restriction increases blood glutathione and longevity in F344 ratsFASEB J81302-13071994. 134. Richie JP, Jr., Leutzinger Y, Parthasarathy S, Malloy V, Orentreich N, and Zimmerman JA. Methionine restriction increases blood glutathione and longevity in F344 rats. FASEB J 8: 1302–1307, 1994.
135.
Ristow MZarse K. How increased oxidative stress promotes longevity and metabolic health: the concept of mitochondrial hormesis (mitohormesis)Exp Gerontol45410-4182010. 135. Ristow M and Zarse K. How increased oxidative stress promotes longevity and metabolic health: the concept of mitochondrial hormesis (mitohormesis). Exp Gerontol 45: 410–418, 2010.
136.
Robinson BH. Human complex I deficiency: clinical spectrum and involvement of oxygen free radicals in the pathogenicity of the defectBiochim Biophys Acta1364271-2861998. 136. Robinson BH. Human complex I deficiency: clinical spectrum and involvement of oxygen free radicals in the pathogenicity of the defect. Biochim Biophys Acta 1364: 271–286, 1998.
137.
Ruiz MCAyala VPortero-Otín MRequena JRBarja GPamplona R. Protein methionine content and MDA-lysine protein adducts are inversely related to maximum life span in the heart of mammalsMech Ageing Dev1261106-11142005. 137. Ruiz MC, Ayala V, Portero-Otín M, Requena JR, Barja G, and Pamplona R. Protein methionine content and MDA-lysine protein adducts are inversely related to maximum life span in the heart of mammals. Mech Ageing Dev 126: 1106–1114, 2005.
138.
Salway KDPage MMFaure PABurness GStuart JA. Enhanced protein repair and recycling are not correlated with longevity in 15 vertebrate endotherm speciesAge (Dordrecht)3333-472011. 138. Salway KD, Page MM, Faure PA, Burness G, and Stuart JA. Enhanced protein repair and recycling are not correlated with longevity in 15 vertebrate endotherm species. Age (Dordrecht) 33: 33–47, 2011.
139.
Sanchez-Roman IGomez AGomez JSuarez HSanchez CNaudi AAyala VPortero-Otin MLopez-Torres MPamplona RBarja G. Forty percent methionine restriction lowers DNA methylation, complex I ROS generation, and oxidative damage to mtDNA and mitochondrial proteins in rat heartJ Bioenerg Biomembr43699-7082011. 139. Sanchez-Roman I, Gomez A, Gomez J, Suarez H, Sanchez C, Naudi A, Ayala V, Portero-Otin M, Lopez-Torres M, Pamplona R, and Barja G. Forty percent methionine restriction lowers DNA methylation, complex I ROS generation, and oxidative damage to mtDNA and mitochondrial proteins in rat heart. J Bioenerg Biomembr 43: 699–708, 2011.
140.
Sanchez-Roman IGomez JNaudi AAyala VPortero-Otín MLopez-Torres MPamplona RBarja G. The β-blocker atenolol lowers the longevity-related degree of fatty acid unsaturation, decreases protein oxidative damage and increases ERK signaling in the heart of C57BL/6 miceRejuvenation Res13683-6932010. 140. Sanchez-Roman I, Gomez J, Naudi A, Ayala V, Portero-Otín M, Lopez-Torres M, Pamplona R, and Barja G. The β-blocker atenolol lowers the longevity-related degree of fatty acid unsaturation, decreases protein oxidative damage and increases ERK signaling in the heart of C57BL/6 mice. Rejuvenation Res 13: 683–693, 2010.
141.
Sanchez-Roman IGómez APérez ISanchez CSuarez HNaudí AJové MLopez-Torres MPamplona RBarja G. Effects of aging and methionine restriction applied at old age on ROS generation and oxidative damage in rat liver mitochondriaBiogerontology13399-4112012. 141. Sanchez-Roman I, Gómez A, Pérez I, Sanchez C, Suarez H, Naudí A, Jové M, Lopez-Torres M, Pamplona R, and Barja G. Effects of aging and methionine restriction applied at old age on ROS generation and oxidative damage in rat liver mitochondria. Biogerontology 13: 399–411, 2012.
142.
Sandhu SKBarlow HM. Strategies for successful agingClin Geriatr Med18643-6482002. 142. Sandhu SK and Barlow HM. Strategies for successful aging. Clin Geriatr Med 18: 643–648, 2002.
143.
Sanz ACaro PAyala VPortero-Otin MPamplona RBarja G. Methionine restriction decreases mitochondrial oxygen radical generation and leak as well as oxidative damage to mitochondrial DNA and proteinsFASEB J201064-10732006. 143. Sanz A, Caro P, Ayala V, Portero-Otin M, Pamplona R, and Barja G. Methionine restriction decreases mitochondrial oxygen radical generation and leak as well as oxidative damage to mitochondrial DNA and proteins. FASEB J 20: 1064–1073, 2006.
144.
Sanz ACaro PBarja G. Protein restriction without strong caloric restriction decreases mitochondrial oxygen radical production and oxidative DNA damage in rat liverJ Bioenerg Biomembr36545-5522004. 144. Sanz A, Caro P, and Barja G. Protein restriction without strong caloric restriction decreases mitochondrial oxygen radical production and oxidative DNA damage in rat liver. J Bioenerg Biomembr 36: 545–552, 2004.
145.
Sanz ACaro PGómez JBarja G. Testing the vicious cycle theory of mitochondrial ROS production: effects of H2O2 and cumene hydroperoxide treatment on heart mitochondriaJ Bioenerg Biomembr38121-1272006. 145. Sanz A, Caro P, Gómez J, and Barja G. Testing the vicious cycle theory of mitochondrial ROS production: effects of H2O2 and cumene hydroperoxide treatment on heart mitochondria. J Bioenerg Biomembr 38: 121–127, 2006.
146.
Sanz ACaro PIbáñez JGómez JGredilla RBarja G. Dietary restriction at old age lowers mitochondrial oxygen radical production and leak at complex I and oxidative DNA damage in rat brainJ Bioenerg Biomembr3783-902005. 146. Sanz A, Caro P, Ibáñez J, Gómez J, Gredilla R, and Barja G. Dietary restriction at old age lowers mitochondrial oxygen radical production and leak at complex I and oxidative DNA damage in rat brain. J Bioenerg Biomembr 37: 83–90, 2005.
147.
Sanz APamplona RBarja G. Is the mitochondrial free radical theory of aging intact?Antiox Redox Signal8582-5992006. 147. Sanz A, Pamplona R, and Barja G. Is the mitochondrial free radical theory of aging intact? Antiox Redox Signal 8: 582–599, 2006.
148.
Sanz AStefanatos RKA. The mitochondrial free radical theory of aging: a critical viewCurr Aging Sci110-212008. 148. Sanz A and Stefanatos RKA. The mitochondrial free radical theory of aging: a critical view. Curr Aging Sci 1: 10–21, 2008.
149.
Seluanov AHine CAzpurua JFeigenson MBozzella MMao ZCatania KCGorbunova V. Hypersensitivity to contact inhibition provides a clue to cancer resistance of naked mole-ratPNAS10619352-193572009. 149. Seluanov A, Hine C, Azpurua J, Feigenson M, Bozzella M, Mao Z, Catania KC, and Gorbunova V. Hypersensitivity to contact inhibition provides a clue to cancer resistance of naked mole-rat. PNAS 106: 19352–19357, 2009.
150.
Schriner SELinford NJMartin GMTreuting POgburn CEEmond MCoskun PELadiges WWolf NVan Remmen HWallace DCRabinovitch PS. Extension of murine life span by overexpression of catalase targeted to mitochondriaScience3081909-19112005. 150. Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, Coskun PE, Ladiges W, Wolf N, Van Remmen H, Wallace DC, and Rabinovitch PS. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308: 1909–1911, 2005.
151.
Skulachev VP. Aging is a specific biological function rather than a result of a disorder in complex living systems: evidence in support of the Weismann's hypothesisBiochemistry (Moscow)621191-11951997. 151. Skulachev VP. Aging is a specific biological function rather than a result of a disorder in complex living systems: evidence in support of the Weismann's hypothesis. Biochemistry (Moscow) 62: 1191–1195, 1997.
152.
Sohal RSFerguson MSohal BHForster MJ. Life span extension in mice by food restriction depends on an energy imbalanceJ Nutr139533-5392009. 152. Sohal RS, Ferguson M, Sohal BH, and Forster MJ. Life span extension in mice by food restriction depends on an energy imbalance. J Nutr 139: 533–539, 2009.
153.
Sohal RSKu HHAgarwal SForster MJLal H. Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restrictionMech Ageing Dev74121-1331994. 153. Sohal RS, Ku HH, Agarwal S, Forster MJ, and Lal H. Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction. Mech Ageing Dev 74: 121–133, 1994.
154.
Sohal RSSohal BHBrunk UT. Relationship between antioxidant defenses and longevityMech Ageing Dev53217-2271990. 154. Sohal RS, Sohal BH, and Brunk UT. Relationship between antioxidant defenses and longevity. Mech Ageing Dev 53: 217–227, 1990.
155.
Sohal RSSvensson IBrunk UT. Hydrogen peroxide production by liver mitochondria in different speciesMech Ageing Dev53209-2151990. 155. Sohal RS, Svensson I, and Brunk UT. Hydrogen peroxide production by liver mitochondria in different species. Mech Ageing Dev 53: 209–215, 1990.
156.
Sohal RSSvensson ISohal BHBrunk UT. Superoxide anion radical production in different speciesMech Ageing Dev49129-1351989. 156. Sohal RS, Svensson I, Sohal BH, and Brunk UT. Superoxide anion radical production in different species. Mech Ageing Dev 49: 129–135, 1989.
157.
Sohal RSWeindruch R. Oxidative stress, caloric restriction, and agingScience27359-631996. 157. Sohal RS and Weindruch R. Oxidative stress, caloric restriction, and aging. Science 273: 59–63, 1996.
158.
Sohal RSOrr WC. The redox stress hypothesis of agingFree Rad Biol Med52539-5552012. 158. Sohal RS, and Orr WC. The redox stress hypothesis of aging. Free Rad Biol Med 52: 539–555, 2012.
159.
Soltow QAJones DPPromislow DE. A network perspective on metabolism and agingIntegr Comp Biol50844-8542010. 159. Soltow QA, Jones DP, and Promislow DE. A network perspective on metabolism and aging. Integr Comp Biol 50: 844–854, 2010.
160.
Someya SYu WHallows WCXu JVann JMLeeuwenburgh CTanokura MDenu JMProlla TA. Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restrictionCell143802-8122010. 160. Someya S, Yu W, Hallows WC, Xu J, Vann JM, Leeuwenburgh C, Tanokura M, Denu JM, and Prolla TA. Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 143: 802–812, 2010.
161.
Strehler BTime, Cells and AgingNew YorkAcademic Press1962. 161. Strehler B. Time, Cells and Aging. New York: Academic Press, 1962.
162.
Stuart JAKarahalil BHogue BASouza-Pinto NCBohr VC. Mitochondrial and nuclear DNA base excision repair are affected differently by caloric restrictionFASEB J18595-5972004. 162. Stuart JA, Karahalil B, Hogue BA, Souza-Pinto NC, and Bohr VC. Mitochondrial and nuclear DNA base excision repair are affected differently by caloric restriction. FASEB J 18: 595–597, 2004.
163.
Suliman HBCarraway MSVelsor LWDay BJGhio AJPinatadosi CA. Rapid mtDNA deletion by oxidants in rat liver mitochondria after hemin exposureFree Radic Biol Med32246-2562002. 163. Suliman HB, Carraway MS, Velsor LW, Day BJ, Ghio AJ, and Pinatadosi CA. Rapid mtDNA deletion by oxidants in rat liver mitochondria after hemin exposure. Free Radic Biol Med 32: 246–256, 2002.
164.
Sun LAmir AAkha SMillar RAHarper J. Life-span extension in mice by preweaning food restriction and by methionine restriction in middle ageJ Gerontol64A711-7222009. 164. Sun L, Amir A, Akha S, Millar RA, and Harper J. Life-span extension in mice by preweaning food restriction and by methionine restriction in middle age. J Gerontol 64A: 711–722, 2009.
165.
Takeshige KMinakami S. NADH- and NADPH-dependent formation of superoxide anions by bovine heart submitochondrial particles and NADH-ubiquinone reductase preparationBiochem J180129-1351979. 165. Takeshige K and Minakami S. NADH- and NADPH-dependent formation of superoxide anions by bovine heart submitochondrial particles and NADH-ubiquinone reductase preparation. Biochem J 180: 129–135, 1979.
166.
Tappel AFletcher BDeamer D. Effect of antioxidants and nutrients on lipid peroxidation fluorescent products and aging parameters in the mouseJ Gerontol28415-4241973. 166. Tappel A, Fletcher B, and Deamer D. Effect of antioxidants and nutrients on lipid peroxidation fluorescent products and aging parameters in the mouse. J Gerontol 28: 415–424, 1973.
167.
Tolmasoff JMOno TCutler RG. Superoxide dismutase: correlation with life span and specific metabolic rate in primate speciesProc Natl Acad Sci U S A772777-27811980. 167. Tolmasoff JM, Ono T, and Cutler RG. Superoxide dismutase: correlation with life span and specific metabolic rate in primate species. Proc Natl Acad Sci U S A 77: 2777–2781, 1980.
168.
Tranah GJ. Mitochondrial-nuclear epistasis: implications for human aging and longevityAgeing Res Rev10238-2522011. 168. Tranah GJ. Mitochondrial-nuclear epistasis: implications for human aging and longevity. Ageing Res Rev 10: 238–252, 2011.
169.
Turrens JFBoveris A. Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondriaBiochem J191421-4271980. 169. Turrens JF and Boveris A. Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 191: 421–427, 1980.
170.
Tyler DDThe Mitochondria in Health and DiseaseNew YorkVCH1992. 170. Tyler DD. The Mitochondria in Health and Disease. New York: VCH, 1992.
171.
Van de Bittner GCDubikovskaya EABertozzi CRChang CJ. In vivo imaging of hydrogen peroxide production in a murine tumor model with a chemoselective bioluminescent reporterPNAS U S A10721316-213212010. 171. Van de Bittner GC, Dubikovskaya EA, Bertozzi CR, and Chang CJ. In vivo imaging of hydrogen peroxide production in a murine tumor model with a chemoselective bioluminescent reporter. PNAS U S A 107: 21316–21321, 2010.
172.
Van Diepeningen ADMaas MFHuberts DHGoedbloed DJEngelmoer DJSlakhorst SMKoopmanschap ABKrause FDencher NASellem CHSainsard-Chanet AHoekstra RFDebets AJ. Calorie restriction causes healthy life span extension in the filamentous fungus Podospora anserinaMech Ageing Dev13160-682010. 172. Van Diepeningen AD, Maas MF, Huberts DH, Goedbloed DJ, Engelmoer DJ, Slakhorst SM, Koopmanschap AB, Krause F, Dencher NA, Sellem CH, Sainsard-Chanet A, Hoekstra RF, and Debets AJ. Calorie restriction causes healthy life span extension in the filamentous fungus Podospora anserina. Mech Ageing Dev 131: 60–68, 2010.
173.
Van Raamsdonk JMHekimi S. Reactive oxygen species and aging in Caenorhabditis elegans: causal or casual relationship?Antioxid Redox Signal131911-19532010. 173. Van Raamsdonk JM and Hekimi S. Reactive oxygen species and aging in Caenorhabditis elegans: causal or casual relationship? Antioxid Redox Signal 13: 1911–1953, 2010.
174.
Van Raamsdonk JMHekimi S. Superoxide dismutase is dispensable for normal animal lifespanPNAS1095785-57902012. 174. Van Raamsdonk JM and Hekimi S. Superoxide dismutase is dispensable for normal animal lifespan. PNAS 109: 5785–5790, 2012.
175.
Venditti PMasullo PDi Meo S. Effect of training on H2O2 release by mitochondria from rat skeletal muscleArch Biochem Biophys372315-3201999. 175. Venditti P, Masullo P, and Di Meo S. Effect of training on H2O2 release by mitochondria from rat skeletal muscle. Arch Biochem Biophys 372: 315–320, 1999.
176.
Zdanov SRemacle JToussaint O. Establishment of H2O2-induced premature senescence in human fibroblasts concomitant with increased cellular production of H2O2Ann N Y Acad Sci1067210-2162006. 176. Zdanov S, Remacle J, and Toussaint O. Establishment of H2O2-induced premature senescence in human fibroblasts concomitant with increased cellular production of H2O2. Ann N Y Acad Sci 1067: 210–216, 2006.
Information & Authors
Information
Published In
Antioxidants & Redox Signaling
Volume 19 • Issue Number 12 • October 20, 2013
Pages: 1420 - 1445
PubMed: 23642158
Copyright
Copyright 2013, Mary Ann Liebert, Inc.
History
Published in print: October 20, 2013
Published online: 4 October 2013
Published ahead of print: 3 July 2013
Published ahead of production: 5 May 2013
Accepted: 5 May 2013
Revision received: 11 April 2013
Received: 19 December 2012
Topics
Authors
Metrics & Citations
Metrics
Citations
Export Citation
Export citation
Select the format you want to export the citations of this publication.
View Options
Get Access
Access content
To read the fulltext, please use one of the options below to sign in or purchase access.⚠ Society Access
If you are a member of a society that has access to this content please log in via your society website and then return to this publication.