Thermal sensitivity of mitochondrial metabolism in two distinct mitotypes of drosophila simulans: Evaluation of mitochondrial plasticity

Journal of Experimental Biology

Volumn 213, Issue 10, 2010, Pages 1665-1675

  Pichaud, Nicolas ^a   Chatelain, Etienne Hébert ^a   Ballard, J William O ^b   Tanguay, Robert ^c   Morrow, Geneviève ^c   Blier, Pierre U ^a  

^a UNIVERSITÉ DU QUÉBEC À RIMOUSKI   (Canada)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITÉ LAVAL   (Canada)

Author keywords

Drosophila simulans; Metabolism; Mitochondrial dna; Mitochondrial respiration; Temperature; Thermal sensitivity

Indexed keywords

CYTOCHROME C OXIDASE; SODIUM AZIDE;

ANIMAL; ARTICLE; CELL RESPIRATION; DROSOPHILA; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; KINETICS; METABOLISM; MITOCHONDRION; TEMPERATURE;

ANIMALS; CELL RESPIRATION; DROSOPHILA; ELECTRON TRANSPORT COMPLEX IV; KINETICS; MITOCHONDRIA; SODIUM AZIDE; TEMPERATURE;

DROSOPHILA SIMULANS;

EID: 77951715188     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.040261     Document Type: Article

References (54)

1. Abele, D., Burlando, B., Viarengo, A. and Pörtner, H. O. (1998). Exposure to elevated temperatures and hydrogen peroxide elicits oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 120, 425-435. (Pubitemid 28386796)
2. Abele, D., Heise, K., Pörtner, H. O. and Puntarelo, S. (2002). Temperature-dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria. J. Exp. Biol. 205, 1831-1841. (Pubitemid 34853435)
3. Andreyev, A. Y., Kushnareva, Y. E. and Starkov, A. A. (2005). Mitochondrial metabolism of reactive oxygen species. Biochemistry 70, 200-214. (Pubitemid 40512329)
4. Ballard, J. W. O. (2000a) Comparative genomics of mitochondrial DNA in members of the Drosophila melanogaster subgroup. J. Mol. Evol. 51, 48-63.
5. Ballard, J. W. O. (2000b) When one is not enough: introgression of mitochondrial DNA in Drosophila. Mol. Biol. Evol. 17, 1126-1130.
6. Ballard, J. W. O. (2004) Sequential evolution of a symbiont inferred from the host: Wolbachia and Drosophila simulans. Mol. Biol. Evol. 21, 428-442.
7. Ballard, J. W. O. (2005). Drosophila simulans as a novel model for studying mitochondrial metabolism and aging. Exp. Geront. 40, 763-773. (Pubitemid 41416539)
8. Ballard, J. W. O., Chernoff, B. and James, A. C. (2002). Divergence of mitochondrial DNA is not corroborated by nuclear DNA, morphology, or behaviour in Drosophila simulans. Evolution 56, 527-545. (Pubitemid 34299829)
9. Ballard, J. W. O., Melvin, R. G., Katewa, S. D. and Maas, K. (2007) Mitochondrial DNA variation is associated with measurable differences in life-history traits and mitochondrial metabolism in Drosophila simulans. Evolutions 61, 1735-1747.
10. Barja, G. and Herrero, A. (2000). Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J. 14, 312-318. (Pubitemid 30086068)
11. Beckman, K. B. and Ames, B. N. (1998) The free radical theory of aging matures. Physiol. Rev. 78, 548-571.
12. Berrigan, D. (1997) Acclimation of metabolic rate in response to developmental temperature in Drosophila melanogaster. J. Therm. Biol. 22, 213-218.
13. Berrigan, D. and Partridge, L. (1997) Influence of temperature and activity on the metabolic rate of adult Drosophila melanogaster. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 118, 1301-1307.
14. Blier, P. U. and Guderley, H. E. (1993) Mitochondrial activity in Rainbow Trout red muscle: effect of temperature on the ADP-dependence of ATP synthesis. J. Exp. Biol. 176, 145-157.
15. Blier, P. U. and Lemieux, H. (2001) The impact of the thermal sensitivity of cytochrome c oxidase on the respiration rate of Artic charr red muscle mitochondria. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 171, 247-253.
16. Blier, P. U., Dufresne, F. and Burton, R. S. (2001). Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends Genet. 17, 400-406. (Pubitemid 32545386)
17. Blier, P. U., Breton, S., Desrosiers, V. and Lemieux, H. (2006). Functional conservatism in mitochondrial evolution: Insight from hybridization of Artic and Brook charrs. J. Exp. Zool. B. Mol. Dev. Evol. 306, 1-8. (Pubitemid 44483139)
18. Bogenhagen, D. F. (1999) Repair of mtDNA in vertebrates. Am. J. Hum. Gen. 64, 1276-1281.
19. Bokov, A., Chaudhurib, A. and Richardson, A. (2004). The role of oxidative damage and stress in aging. Mech. Ageing Dev. 125, 811-826. (Pubitemid 39482409)
20. Chamberlin, M. E. (2004) Top-down control analysis of the effect of temperature on ectotherm oxidative phosphorylation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, 794-800.
21. Chance, B. and Williams, C. M. (1956) The respiratory chain and oxidative phosphorylation. Adv. Enzymol. Relat. Areas Biochem. 17, 65-134.
22. Chen, Q., Vazquez, E. J., Moghaddas, S., Hoppel, C. L. and Lesnefsky, E. J. (2003). Production of reactive oxygen species by mitochondria: central role of complex III. J Biol. Chem. 278, 36027-36031. (Pubitemid 37139922)
23. Das, J. (2006). The role of mitochondrial respiration in physiological and evolutionary adaptation. BioEssays 28, 890-901.
24. Das, N., Levine, R. L., Orr, W. C. and Sohal, R. S. (2001) Selectivity of protein oxidative damage during aging in Drosophila melanogaster. Biochem. J. 360, 209-216.
25. David, J. R. (1988) Temperature. In Drosophila as a Model Organism for Ageing Studies (ed. F. H. Lints and M. H. Soliman), pp. 33-45. London: Blackie.
26. Dean, M. D., Ballard, K. J., Glass, A. and Ballard, J. W. O. (2003) Influence of two Wolbachia strains on population structure of east African Drosophila simulans. Genetics 65, 1959-1969.
27. Farge, G., Touraille, S., Debise, R. and Alziari, S. (2003). The respiratory chain complex thresholds in mitochondria of a Drosophila subobscura mutant strain. Biochimie, 84, 1189-1197. (Pubitemid 36372167)
28. Fontanillas, P., Depraz, A., Giorgi, M. S. and Perrin, N. (2005). Nonshivering thermogenesis capacity associated to mitochondrial DNA haplotypes and gender in the greater white-toothed shrew, Crocidura russula. Mol. Ecol. 14, 661-670. (Pubitemid 40210693)
29. Forman, J. H. and Boveris, A. (1982) Superoxide radical and hydrogen peroxide in mitochondria. In Free Radicals in Biology (ed. W. A. Pryor), pp. 65-90. New York: Academic Press.
30. Gardner, P. R. (2002) Aconitase: sensitive target and measure of superoxide. Methods Enzymol. 349, 9-23.
31. Gnaiger, E. and Kuznetsov, A. V. (2002) Mitochondrial respiration at low levels of oxygen and cytochrome c. Biochem. Soc. Trans. 30, 252-258.
32. Gnaiger, E., Lassnig, B., Kuznetsov, A., Reiger, G. and Margreiter, R. (1998). Mitochondrial oxygen affinity, respiratory flux control and excess capacity of cytochrome c oxidase. J. Exp. Biol. 201, 1129-1139. (Pubitemid 28278318)
33. Guderley, H. (2004) Metabolic responses to low temperature in fish. Biol. Rev. 79, 409-427.
34. Guderley, H., St. Pierre, J., Couture, P. and Hulbert, A. J. (1997). Plasticity of the properties of mitochondria from rainbow trout red muscle with seasonal acclimatization. Fish Physiol. Biochem. 16, 531-541. (Pubitemid 127505775)
35. James, A. C. and Ballard, J. W. O. (2000) Expression of cytoplasmic incompatibility in Drosophila simulans and its impact on infection frequencies and distribution of Wolbachia pipientis. Evolution 54, 1661-1672.
36. Katewa, S. D. and Ballard, J. W. O. (2007). Sympatric Drosophila simulans flies with distinct mtDNA show difference in mitochondrial respiration and electron transport. Ins. Bioch. Mol. Biol. 37, 213-222. (Pubitemid 46217953)
37. Keller, M., Sommer, A. M., Pörtner, H. O. and Abele, D. (2004). Seasonality of energetic functioning and production of reactive oxygen species by lugworm (Arenicola marina) mitochondria exposed to acute temperature changes. J. Exp. Biol. 207, 2529-2538. (Pubitemid 39009288)
38. Kuznetsov, A. V., Clark, J. F., Winkler, K. and Kunz, W. S. (1996). Increase of flux control of cytochrome c oxidase in copper-deficient mottled brindled mice. J. Biol. Chem. 271, 283-288. (Pubitemid 26026591)
39. Kuznetsov, A. V., Veksler, V., Gellerich, F. N., Saks, V., Margreiter, R. and Kunz, W. S. (2008). Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat. Protoc. 3, 965-976. (Pubitemid 351818685)
40. Letellier, T., Heinrich, R., Malgat, M. and Mazat, J.-P. (1994). The kinetic basis of threshold effects observed in mitochondrial diseases: a systemic approach. Biochem. J 302, 171-174. (Pubitemid 24256350)
41. Miwa, S. and Brand, M. D. (2005). The topology of superoxide production by complex III and glycerol 3-phosphate dehydrogenase in Drosophila mitochondria. Biochim. Biophys. Acta 1709, 214-219. (Pubitemid 41254214)
42. Miwa, S., St-Pierre, J., Partridge, L. and Brand, M. D. (2003). Superoxide and hydrogen peroxide production by Drosophila mitochondria. Free Rad. Biol. Med. 35, 938-948. (Pubitemid 37211448)
43. Orr, W. C. and Sohal, R. (1992) The effects of catalase gene overexpression on life-span and resistance to oxidative stress in transgenic Drosophila melanogaster. Arch. Biochem. Biophys. 297, 35-41.
44. Pörtner, H. O. (2002) Physiological basis of temperature-dependent biogeography: trade-offs in muscle design and performance in polar ectotherms. J. Exp. Biol. 205, 2217-2230.
45. Rossignol, R., Malgat, M., Mazat, J.-P. and Letellier, T. (1999) Threshold effect and tissue specificity. J. Biol. Chem. 274, 33426-33432.
46. Sastre, J., Pallardo, F. V. and Vina, J. (2000). Mitochondrial oxidative stress plays a key role in aging and apoptosis. IUBMB Life 49, 427-435. (Pubitemid 30436178)
47. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J. and Klenk, M. D. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
48. Thibeault, M., Blier, P. U. and Guderley, H. (1997) Seasonal variation of muscle metabolic organization in rainbow trout (Oncorhynchus mykiss). Fish Physiol. Biochem. 16, 139-155.
49. Villani, G. and Attardi, G. (1997). In vivo control of respiration by cytochrome c oxidase in wild-type and mitochondrial DNA mutation-carrying human cells. Proc. Natl. Acad. Sci. USA 94, 1166-1171. (Pubitemid 27087822)
50. Watada, M., Ohba, S. and Tobari, Y. N. (1986) Genetic differentiation in Japanese populations of Drosophila simulans and Drosophila melanogaster. II. Morphological variation. Jap. J. Genet. 61, 469-480.
51. Wei, Y. H., Lu, C. Y., Lee, H. C., Pang, C. Y. and Ma, Y. S. (1998) Oxidative damage and mutation to mitochondrial DNA and age-dependent decline of mitochondrial respiratory function. Ann. NYAcad. Sci. 854, 155-170.
52. Yan, L. J. and Sohal, R. S. (1998) Mitochondrial adenine nucleotide translocase is oxidatively modified during aging. Proc. Natl. Acad. Sci. USA 95, 12896-12901.
53. Yan, L. J., Levine R. and Sohal, R. S. (1997). Oxidative damage during aging targets mitochondrial aconitase. Proc. Natl. Acad. Sci. USA 94, 11168-11172. (Pubitemid 27450969)
54. Yarian, C. S. and Sohal, R. S. (2005) In the aging housefly aconitase is the only citric acid cycle enzyme to decline significantly. J. Bioenerg. Biomembr. 37, 91-96.