Physiological Entomology

Volume 41, Issue 1 p. 59-66

Original Article

Probable mechanism of sexual dimorphism in insulin control of Drosophila heat stress resistance

Nataly E. Gruntenko,

Corresponding Author

Nataly E. Gruntenko

Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

Correspondence: Nataly E. Gruntenko, Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Lavrentyeva 10, Novosibirsk 630090, Russia. Tel.: +7191319341814; e-mail: [email protected]Search for more papers by this author

Evgenia K. Karpova,

Evgenia K. Karpova

Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

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Elena V. Burdina,

Elena V. Burdina

Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

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Natalya V. Adonyeva,

Natalya V. Adonyeva

Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

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Olga V. Andreenkova,

Olga V. Andreenkova

Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

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Alexander A. Alekseev,

Alexander A. Alekseev

Institute of Chemical Kinetics and Combustion, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

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Inga Y. Rauschenbach,

Inga Y. Rauschenbach

Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

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Nataly E. Gruntenko,

Corresponding Author

Nataly E. Gruntenko

Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

Evgenia K. Karpova,

Evgenia K. Karpova

Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

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Elena V. Burdina,

Elena V. Burdina

Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

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Natalya V. Adonyeva,

Natalya V. Adonyeva

Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

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Olga V. Andreenkova,

Olga V. Andreenkova

Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

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Alexander A. Alekseev,

Alexander A. Alekseev

Institute of Chemical Kinetics and Combustion, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

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Inga Y. Rauschenbach,

Inga Y. Rauschenbach

Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia

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First published: 26 December 2015

https://doi.org/10.1111/phen.12125

Citations: 9

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Abstract

Adult males of Drosophila species (Drosophila melanogaster L. and Drosophila virilis) show a lower tolerance to heat stress compared with females. The present study investigates the effects of RNA interference (RNAi) knockdown of the insulin-like receptor in the corpus allatum of D. melanogaster males on dopamine metabolism and content, heat stress resistance and juvenile hormone metabolism. In male flies, the knockdown of insulin-like receptor in the corpus allatum is shown to change metabolism of juvenile hormone but not dopamine. It is also shown that knockdown of the insulin-like receptor in the corpus allatum results in a decrease of heat stress resistance in females but not males, and that juvenile hormone rescues this decrease. The results suggest that at least one of the ways in which insulin-like growth factors affect heat stress resistance is by successive mediation through juvenile hormone and dopamine, which could lead to sexual dimorphism in the trait.

References

Aggarwal, D.D. (2014) Physiological basis of starvation resistance in Drosophila leontia: analysis of sexual dimorphism. Journal of Experimental Biology, 217, 1849–1859.
10.1242/jeb.096792
CASPubMedWeb of Science®Google Scholar
Altaratz, M., Applebaum, Sh.W., Richard, D.S. et al. (1991) Regulation of juvenile hormone synthesis in wild-type and apterous mutant Drosophila. Molecular and Cellular Endocrinology, 81, 205–216.
10.1016/0303-7207(91)90219-I
CASPubMedWeb of Science®Google Scholar
Argue, K.J., Yun, A.J. & Neckameyer, W.S. (2013) Early manipulation of juvenile hormone has sexually dimorphic effects on mature adult behavior in Drosophila melanogaster. Hormones and Behavior, 64, 589–597.
10.1016/j.yhbeh.2013.08.018
CASPubMedWeb of Science®Google Scholar
Belgacem, Y.H. & Martin, J.-R. (2006) Disruption of insulin pathways alters trehalose level and abolishes sexual dimorphism in locomotor activity in Drosophila. Journal of Neurobiology, 66, 19–32.
10.1002/neu.20193
CASPubMedWeb of Science®Google Scholar
Belgacem, Y.H. & Martin, J.-R. (2007) HMGCR in the corpus allatum controls sexual dimorphism of locomotor activity and body size via the insulin pathway in Drosophila. PLoS ONE, 2, e187.
10.1371/journal.pone.0000187
CASPubMedWeb of Science®Google Scholar
Bogomolova, E.V., Rauschenbach, I.Yu., Adonyeva, N.V. et al. (2010) Dopamine down-regulates activity of alkaline phosphatase in Drosophila: the role of D2-Like receptors. Journal of Insect Physiology, 56, 1155–1159.
10.1016/j.jinsphys.2010.03.014
CASPubMedWeb of Science®Google Scholar
Gruntenko, N.E., Chentsova, N.A., Andreenkova, E.V. et al. (2003) Stress response in a juvenile hormone deficient Drosophila melanogaster mutant apterous^56f. Insect Molecular Biology, 12, 353–363.
10.1046/j.1365-2583.2003.00419.x
CASPubMedWeb of Science®Google Scholar
Gruntenko, N.E., Chentsova, N.A., Bogomolova, E.V. et al. (2004) The effect of mutations altering biogenic amine metabolism in Drosophila on viability and the response to environmental stresses. Archives of Insect Biochemistry and Physiology, 55, 55–67.
10.1002/arch.10123
CASPubMedWeb of Science®Google Scholar
Gruntenko, N.E., Karpova, E.K., Alekseev, A.A. et al. (2005) Effects of dopamine on juvenile hormone metabolism and fitness in Drosophila virilis. Journal of Insect Physiology, 51, 959–968.
10.1016/j.jinsphys.2005.04.010
CASPubMedWeb of Science®Google Scholar
Gruntenko, N.E., Karpova, E.K., Chentsova, N.A. et al. (2009) 20-hydroxyecdysone and juvenile hormone influence tyrosine hydroxylase activity in Drosophila females under normal and heat stress conditions. Archives of Insect Biochemistry and Physiology, 72, 263–272.
10.1002/arch.20337
CASPubMedWeb of Science®Google Scholar
Gruntenko, N.E., Wen, D., Karpova, E.K. et al. (2010) Altered juvenile hormone metabolism, reproduction and stress response in Drosophila adults with genetic ablation of the corpus allatum cells. Insect Biochemistry and Molecular Biology, 40, 891–897.
10.1016/j.ibmb.2010.09.001
CASPubMedWeb of Science®Google Scholar
Gruntenko, N.E., Bogomolova, E.V., Adonyeva, N.V. et al. (2012a) Decrease in juvenile hormone level as a result of genetic ablation of the corpus allatum cells affects the synthesis and metabolism of stress related hormones in Drosophila. Journal of Insect Physiology, 58, 49–55.
10.1016/j.jinsphys.2011.09.015
CASPubMedWeb of Science®Google Scholar
Gruntenko, N.E., Laukhina, O.V., Bogomolova, E.V. et al. (2012b) Downregulation of the dopamine D2-like receptor in corpus allatum affects juvenile hormone synthesis in Drosophila melanogaster females. Journal of Insect Physiology, 58, 348–355.
10.1016/j.jinsphys.2011.12.006
CASWeb of Science®Google Scholar
Hodgetts, R.B. & Konopka, R.J. (1973) Tyrosine and catecholamine metabolism in wild-type Drosophila melanogaster and a mutant, ebony. Journal of Insect Physiology, 19, 1211–1220.
10.1016/0022-1910(73)90205-9
CASPubMedWeb of Science®Google Scholar
Matzkin, L.M., Watts, T.D. & Markow, T.A. (2009) Evolution of stress resistance in Drosophila: interspecific variation in tolerance to desiccation and starvation. Functional Ecology, 23, 521–527.
10.1111/j.1365-2435.2008.01533.x
Web of Science®Google Scholar
Mirth, C., Truman, J.W. & Riddiford, L.M. (2005) The role of the prothoracic gland in determining critical weight for metamorphosis in Drosophila melanogaster. Current Biology, 15, 1796–1807.
10.1016/j.cub.2005.09.017
CASPubMedWeb of Science®Google Scholar
Nässel, D.R., Liu, Y. & Luo, J. (2015) Insulin/IGF signaling and its regulation in Drosophila. General and Comparative Endocrinology, 221, 255–266.
10.1016/j.ygcen.2014.11.021
CASPubMedWeb of Science®Google Scholar
Neckameyer, W.S. & Quinn, W.G. (1989) Isolation and characterization of the gene for Drosophila tyrosine hydroxylase. Neuron, 2, 1167–1175.
10.1016/0896-6273(89)90183-9
CASPubMedWeb of Science®Google Scholar
Parkash, R., Singh, D. & Lambhod, C. (2014) Sex-specific differences in desiccation resistance and the use of energy metabolites as osmolytes in Drosophila melanogaster flies acclimated to dehydration stress. Journal of Comparative Physiology B, 184, 193–204.
10.1007/s00360-013-0790-z
CASPubMedWeb of Science®Google Scholar
Rauschenbach, I.Y., Sukhanova, M.Z., Shumnaya, L.V. et al. (1997) Role of dopa decarboxylase and N-acetyltransferase in regulation of dopamine content in Drosophila virilis under normal and heat stress conditions. Insect Biochemistry and Molecular Biology, 27, 729–734.
10.1016/S0965-1748(97)00051-9
CASPubMedWeb of Science®Google Scholar
Rauschenbach, I.Yu., Bogomolova, E.V., Karpova, E.K. et al. (2011) Mechanisms of age-specific regulation of dopamine metabolism by juvenile hormone and 20-hydroxyecdysone in Drosophila females. Journal of Comparative Physiology B, 181, 19–26.
10.1007/s00360-010-0512-8
CASPubMedWeb of Science®Google Scholar
Rauschenbach, I.Yu., Karpova, E.K., Adonyeva, N.V. et al. (2014) Disruption of insulin signalling affects the neuroendocrine stress reaction in Drosophila females. The Journal of Experimental Biology, 217, 3733–3741.
10.1242/jeb.106815
PubMedWeb of Science®Google Scholar
Tatar, M., Kopelman, A., Epstein, D. et al. (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science, 292, 107–110.
10.1126/science.1057987
CASPubMedWeb of Science®Google Scholar
Tu, M.-P., Yin, C.-M. & Tatar, M. (2005) Mutations in insulin signaling pathway alter juvenile hormone synthesis in Drosophila melanogaster. General and Comparative Endocrinology, 142, 347–356.
10.1016/j.ygcen.2005.02.009
CASPubMedWeb of Science®Google Scholar
Wright, T.R.F. (1987) Genetic of biogenic amines metabolism, sclerotisation and melanisation in Drosophila melanogaster. Advances in Genetics, 24, 127–221.
10.1016/S0065-2660(08)60008-5
CASPubMedWeb of Science®Google Scholar

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Volume41, Issue1

March 2016

Pages 59-66

Probable mechanism of sexual dimorphism in insulin control of Drosophila heat stress resistance

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Probable mechanism of sexual dimorphism in insulin control of Drosophila heat stress resistance

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