Heat shock response to hypoxia and its attenuation during recovery in the flesh fly, Sarcophaga crassipalpis

Journal of Insect Physiology

Volumn 57, Issue 1, 2011, Pages 203-210

  Michaud, M Robert ^a   Teets, Nicholas M ^a   Peyton, Justin T ^a   Blobner, Brandon M ^a   Denlinger, David L ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Heat shock factor; Heat shock proteins; Hypoxia; Sirtuin

Indexed keywords

HEAT SHOCK PROTEIN; INSECT PROTEIN; OXYGEN;

ADULT; FLY; GENE EXPRESSION; HEAT SHOCK; HYPOXIA; OBSERVATIONAL METHOD; OXYGEN; PHYSIOLOGICAL RESPONSE; POLYMERASE CHAIN REACTION; PROTEIN; SURVIVAL;

ANIMAL; ARTICLE; CELL HYPOXIA; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HEAT SHOCK RESPONSE; MALE; METABOLISM; PHYSIOLOGY; SARCOPHAGIDAE;

ANIMALS; CELL HYPOXIA; FEMALE; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; INSECT PROTEINS; MALE; OXYGEN; SARCOPHAGIDAE;

SARCOPHAGA CRASSIPALPIS; SARCOPHAGIDAE;

EID: 78650215944     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2010.11.007     Document Type: Article

References (47)

1. Baird N.A., Turnbull D.W., Johnson E.A. Induction of the heat shock pathway during hypoxia requires regulation of heat shock factor by hypoxia-inducible factor-1. Journal of Biological Chemistry 2006, 281:38675-38681.
2. Basson H.C., Terblanche J.S. Metabolic responses of Glossina pallidipes (Diptera: Glossinidae) puparia exposed to oxygen and temperature variation: implications for population dynamics and the subterranean life. Journal of Insect Physiology 2010, 56:1787-1789.
3. Bultmann H. Induction of a heat shock puff by hypoxia in polytene foot pad chromosomes of Sarcophaga bullata. Chromosoma 1986, 93:358-366.
4. Bunn H.F., Poyton R.O. Oxygen sensing and molecular adaptation to hypoxia. Physiological Reviews 1996, 76:839-885.
5. Bustin S.A., Benes V., Garson J.A., Hellemans J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesomple J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 2009, 55:611-622.
6. Chang J., Knowlton A.A., Wasser J.S. Expression of heat shock proteins in turtle and mammal hearts: relationship to anoxia tolerance. American Journal of Physiology Regulatory Integrative and Comparative Physiology 2000, 278:R209-R214.
7. Clegg J.S. Embryos of Artemia franciscana survive four years of continuous anoxia: the case for complete metabolic rate depression. Journal of Experimental Biology 1997, 200:467-475.
8. Colinet H., Lee S.F., Hoffman A. Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. FEBS Journal 2010, 277:174-185.
9. Concannon C.G., Gorman A.M., Samali A. On the role of Hsp27 in regulating apoptosis. Apoptosis 2003, 8:61-70.
10. David E., Tanguy A., Pichavant K., Moraga D. Response of the pacific oyster Crassostrea gigas to hypoxia exposure under experimental conditions. FEBS Journal 2005, 272:5635-5652.
11. Denlinger D.L. Induction and termination of pupal diapause in Sarcophaga (Diptera: Sarcophagidae). Biological Bulletin 1972, 142:11-24.
12. Denlinger D.L., Willis J.H., Fraenkel G. Rates and cycles of oxygen consumption during pupal diapause in Sarcophaga flesh flies. Journal of Insect Physiology 1972, 18:871-882.
13. Feder M.E., Hoffman G.E. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology 1999, 61:243-282.
14. Hahn D.A., Ragland G.J., Shoemaker D.D., Denlinger D.L. Gene discovery using massively parallel pyrosequencing to develop ESTs for the flesh fly, Sarcophaga crassipalpis. BMC Genomics 2009, 10:234.
15. Hayward S.A.L., Rinehart J.P., Denlinger D.L. Desiccation and rehydration elicit distinct heat shock protein transcript responses in flesh fly pupae. Journal of Experimental Biology 2004, 207:963-971.
16. Hermes-Lima M., Zenteno-Savin T. Animal responses to drastic changes in oxygen availability and physiological oxidative stress. Comparative Biochemistry and Physiology Part C 2002, 133:537-556.
17. Hoback W.W., Podrabsky J.E., Higley L.G., Stanley D.W., Hand S.C. Anoxia tolerance of con-familial tiger beetle larvae is associated with differences in energy flow and anaerobiosis. Journal of Comparative Physiology Part B 2000, 170:307-314.
18. Hoback W.W., Stanley D.W. Insects in hypoxia. Journal of Insect Physiology 2001, 47:533-542.
19. Hochachka P.W., Lutz P.L. Mechanism, origin, and evolution of anoxia tolerance in animals. Comparative Biochemistry and Physiology Part B 2001, 130:435-459.
20. Hugler W., O'Connor K.C., Landry C.J., Bivins J.E. Induction of stress proteins in anoxic and hyperthermic Spodoptera frugiperda cells. Cytotechnology 1995, 17:91-101.
21. Kolsch G., Jakobi K., Wegener G., Braune H.J. Energy metabolism and metabolic rate of the adler leaf beetle Agelastica alni (L.) (Coleoptera, Chrysomelidae) under aerobic and anaerobic conditions: a microcalorimetric study. Journal of Insect Physiology 2002, 48:143-151.
22. Krishnan S.N., Sun Y., Mohsenin A., Wyman R.J., Haddad G.G. Behavioral and electrophysiologic responses of Drosophila melanogaster to prolonged periods of anoxia. Journal of Insect Physiology 1997, 43:203-210.
23. Krivoruchko A., Storey K.B. Regulation of the heat shock response under anoxia in the turtle, Trachemys scripta elegans. Journal of Comparative Physiology B 2010, 180:403-414.
24. Kukal O., Denlinger D., Lee R.E. Developmental and metabolic changes induced by anoxia in diapausing and non-diapausing flesh fly pupae. Journal of Comparative Physiology B 1991, 160:683-689.
25. Land S.C., Buck L.T., Hochachka P.W. Response of protein synthesis to anoxia and recovery in anoxia-tolerant hepatocytes. American Journal of Physiology Regulatory Integrative and Comparative Physiology 1993, 265:41-48.
26. Lasanthi-Kudahettige R., Magneschi L., Loretti E., Gonzali S., Licausi F., Novi G., Beretta O., Vitulli F., Alpi A., Perata P. Transcript profiling of the anoxia rice coleoptile. Plant Physiology 2007, 144:218-231.
27. Liu G., Roy J., Johnson E.A. Identification and function of hypoxia-response genes in Drosophila melanogaster. Physiological Genomics 2006, 25:134-141.
28. Ma E., Haddad G.G. Anoxia regulates gene expression in the central nervous system of Drosophila melanogaster. Molecular Brain Research 1997, 46:325-328.
29. Marchler G., Wu C. Modulation of Drosophila heat shock transcription factor activity by the molecular chaperone DROJ1. EMBO Journal 2001, 20:499-509.
30. Mayer M.P., Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cellular and Molecular Life Sciences 2005, 62:670-684.
31. Morimoto R.I. Cells in stress: transcriptional activation of heat shock genes. Science 1993, 259:1409-1410.
32. Neupert W. Protein import into mitochondria. Annual Reviews of Biochemistry 1998, 66:863-917.
33. Prentice H.M., Milton S.L., Scheurle D., Lutz P.L. The upregulation of cognate and inducible heat shock proteins in the anoxic turtle brain. Journal of Cerebral Blood Flow and Metabolism 2004, 24:826-828.
34. Qiu X.-B., Shao Y.-M., Wang L. The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cellular and Molecular Life Sciences 2006, 63:2560-2570.
35. Ramaglia V., Buck L.T. Time-dependent expression of heat shock proteins 70 and 90 in tissues of the anoxic wester painted turtle. Journal of Experimental Biology 2004, 207:3775-3784.
36. Rinehart J.P., Denlinger D.L. Heat-shock protein 90 is down-regulated during pupal diapause in the flesh fly, Sarcophaga crassipalpis, but remains responsive to thermal stress. Insect Molecular Biology 2000, 9:641-645.
37. Rinehart J.P., Li A., Yocum G.D., Robich R.M., Hayward S.A.L., Denlinger D.L. Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:11130-11137.
38. Rinehart J.P., Yocum G.D., Denlinger D.L. Developmental upregulation of indicible hsp70 transcripts, but not the cognate form, during pupal diapause in the flesh fly, Sarcophaga crassipalpis. Insect Biochemistry and Molecular Biology 2000, 30:515-521.
39. Sharma S., Reddy P.V.J., Rohilla M.S., Tiwari P.K. Expression of HSP60 homologue in sheep blowfly Lucilia cuprina during development and heat stress. Journal of Thermal Biology 2006, 31:546-555.
40. Snyder C.M., Chandel N.S. Mitochondrial regulation of cell survival and death during low-oxygen conditions. Antioxidants and Redox Signaling 2009, 11:2673-2683.
41. Sorensen J.G., Nielsen M.M., Kruhoffer M., Justesen J., Loeschcke V. Full genome gene expression analysis of the heat stress response in Drosophila melanogaster. Cell Stress and Chaperones 2005, 10:312-328.
42. Storey K.B., Storey J.M. Metabolic rate depression in animals: transcriptional and translation controls. Biological Reviews 2004, 79:207-233.
43. Sun Y., MacRae T.H. The small heat shock proteins and their role in human disease. FEBS Journal 2005, 272:2613-2627.
44. Turman M.A., Kahn D.A., Rosenfeld S.L., Apple C.A., Bates C.M. Characterization of human proximal tubular cells after hypoxic preconditioning: constitutive and hypoxia-induced expression of heat shock proteins hsp70 (A, B, and C), HSC70, and HSP90. Biochemical and Molecular Medicine 1997, 60:49-58.
45. Westerheide S.D., Anckar J., Stevens S.M., Sistonen L., Morimoto R.I. Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 2009, 323:1063-1066.
46. Yocum G.D., Denlinger D.L. Anoxia blocks thermotolerance and the induction of rapid cold hardening in the flesh fly, Sarcophaga crassipalpis. Physiological Entomology 1994, 19:152-158.
47. Yocum G.D., Joplin K.H., Denlinger D.L. Upregulation of a 23kDa small heat shock protein transcript during pupal diapause in the flesh fly, Sarcophaga crassipalpis. Insect Biochemistry and Molecular Biology 1998, 28:677-682.