BioFactors

Volume 43, Issue 4 p. 567-576

Research Communication

Anti-inflammatory, antioxidant, and immunomodulatory effects of curcumin in ovalbumin-sensitized rat

Farzaneh Shakeri,

Farzaneh Shakeri

Neurogenetic Inflammation Research Centre, Mashhad University of Medical Sciences, Mashhad, Iran

Department of Physiology, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

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Mohammad Hossein Boskabady,

Corresponding Author

Mohammad Hossein Boskabady

orcid.org/0000-0001-5736-9755

Neurogenetic Inflammation Research Centre, Mashhad University of Medical Sciences, Mashhad, Iran

Department of Physiology, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

Address for correspondence: Mohammad Hossein Boskabady, Neurogenic Inflammation Research Center and Department of Physiology, School of Medicine, Mashhad University of Medical Sciences, Mashhad 9177948564, Iran. Tel.: +98 51 38828565; Fax: +98 51 38828564; E-mail: [email protected] and [email protected]Search for more papers by this author

Farzaneh Shakeri,

Farzaneh Shakeri

Neurogenetic Inflammation Research Centre, Mashhad University of Medical Sciences, Mashhad, Iran

Department of Physiology, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

Search for more papers by this author

Mohammad Hossein Boskabady,

Corresponding Author

Mohammad Hossein Boskabady

orcid.org/0000-0001-5736-9755

Neurogenetic Inflammation Research Centre, Mashhad University of Medical Sciences, Mashhad, Iran

Department of Physiology, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

First published: 16 May 2017

https://doi.org/10.1002/biof.1364

Citations: 53

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Abstract

Background: Anti-inflammatory and antioxidant properties of curcumin have been shown. In this study, anti-inflammatory, antioxidant, and immunomodulatory effects of curcumin in sensitized rat were evaluated. Methods: Six groups of rats including control (C), ovalbumin-sensitized (as a rat model of asthma, S), S groups treated with curcumin (Cu 0.15, 0.30, and 0.60 mg/mL), and 1.25 μg/mL dexamethasone (S + D) were studied. Curcumin and dexamethasone were given in animals' drinking water during sensitization period. Total and differential WBC count, PLA2, TP, IFN-γ, IL-4, IgE, oxidant, and antioxidant biomarker levels in bronchoalveolar lavage fluid (BALF) were examined. Results: Total WBC, neutrophil and eosinophil counts, levels of PLA2, TP, IgE, IL-4, NO₂, NO₃, and MDA in BALF were increased but lymphocyte percentage, SOD, CAT, thiol, and IFN-γ levels and IFN-γ/IL-4 ratio decreased in S animals compared to controls (P < 0.001 for all cases). Treatment with all concentrations of curcumin significantly improved total WBC, PLA2, TP, IgE, IL-4, IFN-γ, IFN-γ/IL-4 ratio, SOD, thiol, NO₂, and NO₃ compared to S group (P < 0.01 to P < 0.001). Two higher concentrations of curcumin significantly decreased neutrophil and eosinophil counts and MDA level but increased IFN-γ, CAT and lymphocyte values compared to S group (P < 0.001 for all cases). Dexamethasone treatment also significantly improved most of the measured parameters (P < 0.05 to P < 0.001) but it did not change IL-4 and IFN-γ levels and IFN-γ/IL-4 ratio. Conclusion: Anti-inflammatory, antioxidant, and immunomodulatory effects of curcumin with more specific immunomodulatory effect on Th1/Th2 balance compared to dexamethasone in sensitized rats was shown. © 2017 BioFactors, 43(4):567–576, 2017

References

1 Jurenka, J. S. (2009) Anti-inflammatory properties of curcumin, a major constituent of Curcuma longa: a review of preclinical and clinical research. Altern. Med. Rev. 14, 141–153.

PubMedWeb of Science®Google Scholar
2 Trujillo, J., Chirino, Y. I., Molina-Jijón, E., Andérica-Romero, A. C., Tapia, E., et al. (2013) Renoprotective effect of the antioxidant curcumin: recent findings. Redox Biol. 1, 448–456.
10.1016/j.redox.2013.09.003
CASPubMedWeb of Science®Google Scholar
3 Park, E. J., Jeon, C. H., Ko, G., Kim, J., and Sohn, D. H. (2000) Protective effect of curcumin in rat liver injury induced by carbon tetrachloride. J. Pharm. Pharmacol. 52, 437–440.
10.1211/0022357001774048
CASPubMedWeb of Science®Google Scholar
4 Chainani-Wu, N. (2003) Safety and anti-inflammatory activity of curcumin: a component of tumeric (Curcuma longa). J. Altern. Complement Med. 9, 161–168.
10.1089/107555303321223035
PubMedWeb of Science®Google Scholar
5 Kim, J., Jeong, S. W., Quan, H., Jeong, C. W., Choi, J. I., et al. (2016) Effect of curcumin (Curcuma longa extract) on LPS-induced acute lung injury is mediated by the activation of AMPK. J. Anaesth. 30, 100–108.
10.1007/s00540-015-2073-1
Web of Science®Google Scholar
6 Rao, M. (1997) Nitric oxide scavenging by curcuminoids. J. Pharm. Pharmacol. 49, 105–107.
10.1111/j.2042-7158.1997.tb06761.x
PubMedWeb of Science®Google Scholar
7 Rao, M. (1994) Curcuminoids as potent inhibitors of lipid peroxidation. J. Pharm. Pharmacol. 46, 1013–1016.
10.1111/j.2042-7158.1994.tb03258.x
CASPubMedWeb of Science®Google Scholar
8 Elias, J. A., Lee, C. G., Zheng, T., Ma, B., Homer, R. J., et al. (2003) New insights into the pathogenesis of asthma. J. Clin. Invest. 111, 291–297.
10.1172/JCI17748
CASPubMedWeb of Science®Google Scholar
9 Louis, R., Lau, L. C., Bron, A. O., Roldaan, A. C., Radermecker, M., et al. (2000) The relationship between airways inflammation and asthma severity. Am. J. Respir. Crit. Care Med. 161, 9–16.
10.1164/ajrccm.161.1.9802048
CASPubMedWeb of Science®Google Scholar
10 Bowton, D. L., Dmitrienko, A. A., Israel, E., Zeiher, B. G., and Sides, G. D. (2005) Impact of a soluble phospholipase A2 inhibitor on inhaled allergen challenge in subjects with asthma. J. Asthma 42, 65–71.
10.1081/JAS-200044748
CASPubMedWeb of Science®Google Scholar
11 Caramori, G., and Papi, A. (2004) Oxidants and asthma. Thorax 59, 170–173.
10.1136/thorax.2002.002477
CASPubMedWeb of Science®Google Scholar
12 Barnes, P. J., Chung, K. F., and Page, C. P. (1998) Inflammatory mediators of asthma: an update. Pharmacol. Rev. 50, 515–596.

CASPubMedWeb of Science®Google Scholar
13 Henricks, P. A., and Nijkamp, F. P. (2001) Reactive oxygen species as mediators in asthma. Pulm. Pharmacol. Ther. 14, 409–421.
10.1006/pupt.2001.0319
CASPubMedWeb of Science®Google Scholar
14 Sackesen, C., Ercan, H., Dizdar, E., Soyer, O., Gumus, P., et al. (2008) A comprehensive evaluation of the enzymatic and nonenzymatic antioxidant systems in childhood asthma. J. Allergy Clin. Immunol. 122, 78–85.
10.1016/j.jaci.2008.03.035
CASPubMedWeb of Science®Google Scholar
15 Talati, M., Meyrick, B., Peebles, R. S., Davies, S. S., Dworski, R., et al. (2006) Oxidant stress modulates murine allergic airway responses. Free Radic. Biol. Med. 40, 1210–1219.
10.1016/j.freeradbiomed.2005.11.012
CASPubMedWeb of Science®Google Scholar
16 Terada, L. S. (2006) Specificity in reactive oxidant signaling: think globally, act locally. J. Cell Biol. 174, 615–623.
10.1083/jcb.200605036
CASPubMedWeb of Science®Google Scholar
17 Salmon, M., Walsh, D. A., Huang, T. J., Barnes, P. J., Leonard, T. B., et al. (1999) Involvement of cysteinyl leukotrienes in airway smooth muscle cell DNA synthesis after repeated allergen exposure in sensitized Brown Norway rats. Br. J. Pharmacol. 127, 1151–1158.
10.1038/sj.bjp.0702669
CASPubMedWeb of Science®Google Scholar
18 Iwamoto, I., Nakajima, H., Endo, H., and Yoshida, S. (1993) Interferon gamma regulates antigen-induced eosinophil recruitment into the mouse airways by inhibiting the infiltration of CD4+ T cells. J. Exp. Med. 177, 573–576.
10.1084/jem.177.2.573
CASPubMedWeb of Science®Google Scholar
19 Akbari, O., Freeman, G. J., Meyer, E. H., Greenfield, E. A., Chang, T. T., et al. (2002) Antigen-specific regulatory T cells develop via the ICOS–ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat. Med. 8, 1024–1032.
10.1038/nm745
CASPubMedWeb of Science®Google Scholar
20 Platts-Mills, T. A. (2001) The role of immunoglobulin E in allergy and asthma. Am. J. Respir. Crit. Care Med. 164, 1–5.
10.1164/ajrccm.164.supplement_1.2103024
CASPubMedWeb of Science®Google Scholar
21 Salama, A. A., Zaki, H. F., El-Shenawy, S. M., EL-Denshary, E. S. M., and Ismaiel, I. (2012) Effects of fish oil and dexamethasone in experimentally-induced bronchial asthma. Aust. J. Basic Appl. Sci. 13, 497–506.

Google Scholar
22 Tang, X. Y., Yu, H. P., Deng, H. J., Chen, X., Fan, H. Z., et al. (2011) Pathogenic mechanism of CD8(+) CD28(-) T cell and the effect of dexamethasone in asthmatic mouse. Zhonghua Yi. Xue. Za. Zhi. 91, 1861–1865.

CASPubMedGoogle Scholar
23 Yousefniapasha, Y., Jorsaraei, G., Gholinezhadchari, M., Mahjoub, S., Hajiahmadi, M., et al. (2015) Nitric oxide levels and total antioxidant capacity in the seminal plasma of infertile smoking men. Cell J. 17, 129–136.

PubMedWeb of Science®Google Scholar
24 Janero, D. R. (1990) Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic. Biol. Med. 9, 515–540.
10.1016/0891-5849(90)90131-2
CASPubMedWeb of Science®Google Scholar
25 Madesh, M., and Balasubramanian, K. (1998) Microtiter plate assay for superoxide dismutase using MTT reduction by superoxide. Indian J. Biochem. Biophys. 35, 184–188.

CASPubMedWeb of Science®Google Scholar
26 Beers, R. F., and Sizer, I. W. (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 195, 133–140.
10.1016/S0021-9258(19)50881-X
CASPubMedWeb of Science®Google Scholar
27 Hosseinzadeh, H., and Sadeghnia, H. R. (2005) Safranal, a constituent of Crocus sativus (saffron), attenuated cerebral ischemia induced oxidative damage in rat hippocampus. J. Pharm. Pharm. Sci. 8, 394–399.

CASPubMedWeb of Science®Google Scholar
28 Boskabady, M. H., Eslamizade, M. J., Tabatabaei, A., Nemati, H., and Mansouri, F. (2010) Effect of inhaled fluticasone on lung inflammation administered during and after guinea pig sensitization. Arch. Bronconeumol. 46, 215–222.
10.1016/S1579-2129(10)70056-2
PubMedWeb of Science®Google Scholar
29 Keyhanmanesh, R., Boskabady, M. H., Eslamizadeh, M. J., Khamneh, S., and Ebrahimi, M. A. (2010) The effect of thymoquinone, the main constituent of Nigella sativa on tracheal responsiveness and white blood cell count in lung lavage of sensitized guinea pigs. Planta Medica 76, 218–222.
10.1055/s-0029-1186054
CASPubMedWeb of Science®Google Scholar
30 Kashima, N., Nakajima, H., Fukaura, A., et al. (1993) Study of serum phospholipase A2 activity in bronchial asthmatic patients. Arerugi 42, 723–727.

CASPubMedGoogle Scholar
31 Boskabady, M. H., Jalali, S., Farkhondeh, T., and Byrami, G. (2014) The extract of Zataria multiflora affect tracheal responsiveness, serum levels of NO, nitrite, PLA2, TP and histamine in sensitized Guinea pigs. J. Ethnopharmacol. 156, 301–308.
10.1016/j.jep.2014.08.024
PubMedWeb of Science®Google Scholar
32 Barnes, P. J. (2008) Immunology of asthma and chronic obstructive pulmonary disease. Nat. Rev. Immunol. 8, 183–192.
10.1038/nri2254
CASPubMedWeb of Science®Google Scholar
33 Barnes, P. J. (2008) The cytokine network in asthma and chronic obstructive pulmonary disease. J. Clin. Invest. 118, 3546–3556.
10.1172/JCI36130
CASPubMedWeb of Science®Google Scholar
34 Ganas, K., Loukides, S., Papatheodorou, G., Panagou, P., and Kalogeropoulos, N. (2001) Total nitrite/nitrate in expired breath condensate of patients with asthma. Respir. Med. 95, 649–654.
10.1053/rmed.2001.1117
CASPubMedWeb of Science®Google Scholar
35 Ozaras, R., Tahan, V., Turkmen, S., Talay, F., Besirli, K., et al. (2000) Changes in malondialdehyde levels in bronchoalveolar fluid and serum by the treatment of asthma with inhaled steroid and beta2-agonist. Respirol. 5, 289–292.
10.1046/j.1440-1843.2000.00260.x
CASPubMedGoogle Scholar
36 De Raeve, H. R., Thunnissen, F., Kaneko, F. T., Guo, F. H., Lewis, M., et al. (1997) Decreased Cu, Zn-SOD activity in asthmatic airway epithelium: correction by inhaled corticosteroid in vivo. Am. J. Physiol. Lung Cell Mol. Physiol. 272, 148–154.
10.1152/ajplung.1997.272.1.L148
Google Scholar
37 Yang, L. L., Huang, M. S., Huang, C. C., Wang, T. H., Lin, M. C., et al. (2011) The association between adult asthma and superoxide dismutase and catalase gene activity. Int. Arch. Allergy Immunol. 156, 373–380.
10.1159/000324448
CASPubMedWeb of Science®Google Scholar
38 Kelly, F. J., Mudway, I., Blomberg, A., Frew, A., and Sandström, T. (1999) Altered lung antioxidant status in patients with mild asthma. The Lancet 354, 482–483.
10.1016/S0140-6736(99)01812-7
CASPubMedWeb of Science®Google Scholar
39 Sarkar, S., Srivastava, R., Dwivedi, P. K., Shukla, R., Srivastava, S., et al. (2015) Search for a herbal medicine: anti-asthmatic activity of methanolic extract of Curcuma longa. J. Pharmacogn. Phytochem. 3, 59–72.

CASGoogle Scholar
40 Zhang, Y., Liang, D., Dong, L., Ge, X., Xu, F., et al. (2015) Anti-inflammatory effects of novel curcumin analogs in experimental acute lung injury. Respir. Res. 16, 1–13.
10.1186/s12931-015-0199-1
PubMedWeb of Science®Google Scholar
41 Liju, V. B., Jeena, K., and Kuttan, R. (2011) An evaluation of antioxidant, anti-inflammatory, and antinociceptive activities of essential oil from Curcuma longa. L. Indian J Pharmacol. 43, 526–531.
10.4103/0253-7613.84961
CASPubMedWeb of Science®Google Scholar
42 Ma, C., Ma, Z., Fu, Q., and Ma, S. (2013) Curcumin attenuates allergic airway inflammation by regulation of CD4+ CD25+ regulatory T cells (Tregs)/Th17 balance in ovalbumin-sensitized mice. Fitoterapia 87, 57–64.
10.1016/j.fitote.2013.02.014
CASPubMedWeb of Science®Google Scholar
43 Chauhan, P. S., Dash, D., Paul, B., and Singh, R. (2016) Intranasal curcumin ameliorates airway inflammation and obstruction by regulating MAPKinase activation (p38, Erk and JNK) and prostaglandin D2 release in murine model of asthma. Int. Immunopharmacol. 31, 200–206.
10.1016/j.intimp.2015.12.025
CASPubMedWeb of Science®Google Scholar
44 Kurup, V. P., Barrios, C. S., Raju, R., Johnson, B. D., Levy, M. B., et al. (2007) Immune response modulation by curcumin in a latex allergy model. Clin. Mol. Allergy. 5, 1–12.
10.1186/1476-7961-5-1
CASPubMedGoogle Scholar
45 Yadav, R. S., Sankhwar, M. L., Shukla, R. K., Chandra, R., Pant, A. B., et al. (2009) Attenuation of arsenic neurotoxicity by curcumin in rats. Toxicol. Appl. Pharmacol. 240, 367–376.
10.1016/j.taap.2009.07.017
CASPubMedWeb of Science®Google Scholar
46 Reddy, A. C. P., and Lokesh, B. (1994) Effect of dietary turmeric (Curcuma longa) on iron-induced lipid peroxidation in the rat liver. Food Chem. Toxicol. 32, 279–283.
10.1016/0278-6915(94)90201-1
CASPubMedWeb of Science®Google Scholar
47 Zargari, M., Ahmadi, S., Shabani, S., and Mahrooz, A. (2013) Protective effect of curcumin on the superoxide dismutase and catalase activity in kidney of acetaminophen-exposed rats. J. Mazandaran Uni. Med. Sci. 22, 74–83.

Google Scholar
48 Liu, Y., Wu, Y., and Zhang, P. (2015) Protective effects of curcumin and quercetin during benzo (a) pyrene induced lung carcinogenesis in mice. Eur. Rev. Med. Pharmacol. Sci. 19, 1736–1743.

CASPubMedWeb of Science®Google Scholar
49 Chung, S. H., Choi, S. H., Choi, J. A., Chuck, R. S., and Joo, C. K. (2012) Curcumin suppresses ovalbumin-induced allergic conjunctivitis. Mol. Vis. 18, 1966–1972.

CASPubMedWeb of Science®Google Scholar
50 Dong, F., Wang, C., Duan, J., Zha, W., Xiang, D., et al. (2014) Puerarin attenuates ovalbumin-induced lung inflammation and hemostatic unbalance in rat asthma model. Evid. Based Complement Alternat. Med. 1–9.

PubMedGoogle Scholar
51 Kianmehr, M., Haghmorad, D., Nosratabadi, R., Rezaei, A., Alavinezhad, A., et al. The effect of Zataria multiflora on Th1/Th2 and Th17/Tregulatory in a mouse model of allergic asthma. Submitted to Forntiers in Pharmacology.

Google Scholar

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Volume43, Issue4

July/August 2017

Pages 567-576

Anti-inflammatory, antioxidant, and immunomodulatory effects of curcumin in ovalbumin-sensitized rat

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Anti-inflammatory, antioxidant, and immunomodulatory effects of curcumin in ovalbumin-sensitized rat

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