Stress-induced accumulation of glycerol in the flesh fly, Sarcophaga bullata: Evidence indicating anti-desiccant and cryoprotectant functions of this polyol and a role for the brain in coordinating the response

Journal of Insect Physiology

Volumn 52, Issue 2, 2006, Pages 202-214

  Yoder, Jay A ^a   Benoit, Joshua B ^a   Denlinger, David L ^b   Rivers, David B ^c  

^a WITTENBERG UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c LOYOLA UNIVERSITY MARYLAND   (United States)

Author keywords

Brain; Cold shock injury; Polyol; Rapid cold hardening; Water balance

Indexed keywords

GLYCEROL; TREHALOSE;

DEHYDRATION; ENVIRONMENTAL STRESS; PHYSIOLOGICAL RESPONSE;

ANIMAL; ANOXIA; ARTICLE; COLD; DEHYDRATION; FLY; HEAT; METABOLISM; PHYSIOLOGY; STRESS;

ANIMALS; ANOXIA; COLD; DEHYDRATION; DIPTERA; GLYCEROL; HEAT; STRESS; TREHALOSE;

SARCOPHAGA BULLATA; SARCOPHAGIDAE;

EID: 31144445335     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2005.10.005     Document Type: Article

References (66)

1. T.A. Adedokun, and D.L. Denlinger Metabolic reserves associated with pupal diapause in the flesh fly, Sarcophaga crassipalpis Journal of Insect Physiology 31 1985 229 233
2. T. Arakawa, and S.E. Timasheff Stabilization of protein structure by sugars Biochemistry 21 1982 6536 6544
3. L.G. Arlian, and I.A. Ekstrand Water balance in Drosophilia pseudoobscura, and its ecological implications Annals of the Entomological Society of America 68 1975 827 832
4. J.S. Bale Insects and low temperatures: from molecular biology to distributions and abundance Philosophical Transactions of the Royal Society of London B: Biological Sciences 29 2002 849 862
5. W. Block Cold or drought-the lesser of two evils for terrestrial arthropods European Journal of Entomology 93 1996 325 339
6. W. Block Water or ice? The challenge for invertebrate cold survival Science Progress 86 2003 77 101
7. V. Burton, H.K. Mitchell, P. Young, and N.S. Petersen Heat shock protection against cold stress of Drosophila melanogaster Molecular and Cellular Biology 8 1988 3550 3552
8. C.-P. Chen, and D.L. Denlinger Activation of phosphorylase in response to cold and heat stress in the flesh fly, Sarcophaga crassipalpis Journal of Insect Physiology 36 1990 549 553
9. C.-P. Chen, R.E. Lee, and D.L. Denlinger Cold shock and heat shock: a comparison of the protection generated by brief pretreatment at less severe temperatures Physiological Entomology 16 1987 19 26
10. C.-P. Chen, R.E. Lee, and D.L. Denlinger A comparison of the responses of tropical and temperate flies (Diptera: Sarcophagidae) to cold and heat stress Journal of Comparative Physiology B 160 1990 543 547
11. S.J. Coulson, and J.S. Bale Characterization and limitations of the rapid cold hardening response in the housefly Musca domestica (Diptera: Muscidae) Journal of Insect Physiology 36 1990 207 211
12. S.J. Coulson, and J.S. Bale Anoxia induces rapid cold hardening in the housefly Musca domestica (Diptera: Muscidae) Journal of Insect Physiology 37 1991 497 501
13. M.C. Czajka, and R.E. Lee A rapid cold-hardening response protecting against cold-shock injury in Drosophila melanogaster Journal of Experimental Biology 148 1990 245 254
14. H.V. Danks Dehydration in dormant insects Journal of Insect Physiology 46 2000 837 852
15. J.R. David, P. Gibert, B. Moreteau, G.W. Gilchrist, and R.B. Huey The fly that came in from the cold: geographic variation of recovery time from low-temperature exposure in Drosophila subobscura Journal of Thermal Biology 23 2003 291 299
16. D.L. Denlinger Induction and termination of pupal diapause in Sarcophaga (Diptera: Sarcophagidae) Biological Bulletin 142 1972 11 24
17. D.L. Denlinger Regulation of diapause Annual Review of Entomology 47 2002 93 122
18. D.L. Denlinger, and R.E. Lee Physiology of cold sensitivity G.J. Hallman D.L. Denlinger Temperature Sensitivity in Insects and Application in Integrated Pest Management 1998 Westview Press Boulder, CO 55 95
19. D.L. Denlinger, R.E. Lee, G.D. Yocum, and O. Kukal Role of chilling in the acquisition of cold tolerance and the capacitation to express stress proteins in diapausing pharate larvae of the gypsy moth, Lymantria dispar Archives of Insect Biochemistry and Physiology 21 1992 271 280
20. M.E. Feder, and G.E. Hoffman Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology Annual Review of Physiology 61 1999 242 282
21. R.D. Flannagan, S.P. Tammariello, K.H. Joplin, R.A. Cikra-Ireland, G.D. Yocum, and D.L. Denlinger Diapause-specific gene expressionin pupae of the flesh fly, Sarcophaga crassipalpis Proceedings of the National Academy of Sciences 79 1998 2360 2364
22. G. Gade Activation of fat body glycogen phosphorylase in Locusta migratoria by corpus cardiacum extract and synthetic adipokinetic hormone Journal of Insect Physiology 27 1981 155 161
23. K. Gekko, and S.E. Timasheff Mechanism of protein stabilization by glycerol: preferential hydration in glycerol-water mixtures Biochemistry 20 1981 4667 4676
24. G.J. Goldsworthy The action of hyperglycaemic factors from the corpus cardiacum of Locusta migratoria on glucogen phosphorylase General and Comparative Endocrinology 14 1970 78 85
25. S.G. Goto, K.M. Yoshida, and M.T. Kimura Accumulation of Hsp70 mRNA under environmental stresses in diapausing and nondiapausing adults of Drosophila triauraria Journal of Insect Physiology 44 1998 1009 1015
26. D.R. Guzman, and J.J. Petersen Cold acclimation and prolonged low temperature survival of filth fly parasites (Hymenoptera: Pteromalidae) Environmental Entomology 15 1986 936 942
27. N.F. Hadley Water Relations of Terrestrial Arthropods 1994 Academic Press New York, NY
28. S.A.L. Hayward, J.P. Rinehart, and D.L. Denlinger Desiccation and rehydration elicit distinct heat shock protein transcript responses in flesh fly pupae Journal of Experimental Biology 207 2004 963 971
29. P.W. Hochachka, and G.N. Somero Biochemical Adaptation 1984 Princeton University Press Princeton
30. M. Hodkova, P. Berkova, and H. Zahradnickova Photoperiodic regulation of the phospholipid molecular species composition in thoracic muscles and fat body of Pyrrhocoris apterus (Heteroptera) via an endocrine gland, corpus allatum Journal of Insect Physiology 48 2002 1009 1019
31. K.H. Joplin, and D.L. Denlinger Cycles of protein synthesis during pupal diapause in the flesh fly, Sarcophaga crassipalpis Archives of Insect Biochemistry and Physiology 12 1989 111 122
32. K.H. Joplin, G.D. Yocum, and D.L. Denlinger Cold shock elicits expression of heta shock proteins in the flesh fly Sarcophaga crassipalpis Journal of Insect Physiology 36 1990 825 834
33. J.D. Kelty, and R.E. Lee Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster Journal of Insect Physiology 45 1999 719 726
34. A. Korsloot, C. van Gestel, and N. van Straalen Environmental Stress and Cellular Response in Arthropods 2004 CRC Press Boca Raton, FL
35. V. Kostal, M. Slachta, and P. Simek Cryoprotective role of polyols independent of the increase in supercooling capacity in diapausing adults of Pyrrhocoris apterus (Heteroptera: Insecta) Comparative Biochemistry and Physiology B 130 2001 365 374
36. O. Kukal, D.L. Denlinger, and R.E. Lee Developmental and metabolic changes induced by anoxia in diapausing and non-diapausing flesh fly pupae Journal of Comparative Physiology B 160 1991 683 689
37. K.-Y. Lee, F.M. Horodyski, A.P. Valaitis, and D.L. Denlinger Molecular characterization of the insect immune protein hemolin and its high induction during embryonic diapause in the gypsy moth, Lymantria dispar Insect Biochemistry and Molecular Biology 32 2002 1457 1467
38. R.E. Lee Principles of insect low temperature tolerance R.E. Lee D.L. Denlinger Insects at Low Temperature 1991 Chapman and Hall New York 17
39. R.E. Lee, and D.L. Denlinger Cold tolerance in diapausing and non-diapausing stages of the flesh fly, Sarcophaga crassipalpis Physiological Entomology 10 1985 309 315
40. R.E. Lee, C.-P. Chen, and D.L. Denlinger A rapid cold-hardening process in insects Science 238 1987 1415 1417
41. Y.-P. Li, M. Goto, L. Ding, and H. Tsumuki Diapause development and acclimation regulating enzymes associated with glycerol synthesis in the Shonai ecotype of the rice stem borer larva, Chilo suppressalis walker Journal of Insect Physiology 48 2002 303 310
42. S.S. Macdonald, L. Rako, P. Batterham, and A.A. Hoffman Dissecting chill coma recovery as a measure of cold resistance: evidence for a biphasic response in Drosophila melanogaster Journal of Insect Physiology 50 2004 695 700
43. S.R. Misener, C.-P. Chen, and V.K. Walker Cold tolerance and proline metabolic gene expression in Drosophila melanogaster Journal of Insect Physiology 47 2001 393 400
44. J.H. Nordin, Z. Cuiz, and C.-M. Yin. Cold-induced glycerol accumulation by Ostrinia nubilalis larvae is developmentally regulated Journal of Insect Physiology 30 1984 563 566
45. T. Ohtaki On the delayed pupation of the flesh fly, Sarcophaga peregrina Robineau-Desvoiday Japanese Journal of Medical Science and Biology 19 1966 97 104
46. Overgaard, J., Sorensen, J.G., Petersen, S.O., Loeschcke, V., Holmstrup, M., 2005. Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. Journal of Insect Physiology, in press.
47. D.B. Rivers, W.F. Hink, and D.L. Denlinger Toxicity of the venom from Nasonia vitripennis (Hymenoptera: Pteromalidae) toward fly hosts, nontarget insects, different developmental stages, and cultured insect cells Toxicon 31 1993 755 765
48. K. Slama, and D.L. Denlinger Infradian cycles of oxygen consumption in diapausing pupae of the flesh fly, Sarcophaga crassipalpis, monitored by a scanning microrespirographic method Archives of Insect Biochemistry and Physiology 20 1992 135 143
49. R.R. Sokal, and F.J. Rohlf Biometry: The Principles and Practice of Statistics in Biological Research third ed 1995 Freeman San Francisco, CA
50. J.M. Storey, and K.B. Storey Cold hardiness and freeze tolerance K.B. Storey Functional Metabolism: Regulation and Adaptation 2004 Wiley Hobocken, New Jersey 473 504
51. K.B. Storey Organic solutes in freezing tolerance Comparative Biochemistry and Physiology 117A 1997 319 326
52. K.B. Storey, and J.M. Storey Biochemistry of cryoprotectants R.E. Lee D.L. Denlinger Insects at Low Temperature 1991 Chapman and Hall New York 64 93
53. S.P. Tammariello Regulation of the cell cycle during diapause D.L. Denlinger J.M. Giebultowica D.S. Saunders Circadian Rhymicity to Seasonality 2001 Elsevier Amsterdam 173 184
54. 1 cell cycle arrest in the brain of Sarcophaga crassipalpis during pupal diapause and the expression pattern of the cell cycle regulator, proliferating cell nuclear antigen Insect Biochemistry and Molecular Biology 28 1998 83 89
55. E.C. Toolson Diffusion of water through the arthropod cuticle: thermodynamic consideration of the transition phenomenon Journal of Thermal Biology 3 1978 69 73
56. G.W. Wharton Water balance of insects G.A. Kerkut L.I. Gilbert Comprehensive Insect Physiology, Biochemistry, and Pharmacology vol. 4 1985 Pergamon Press Oxford 565 603
57. J.B. Williams, J.D. Shorthouse, and R.E. Lee Extreme resistance to desiccation and microclimate-related differences in cold-hardiness of gall wasps (Hymenoptera: Cynipidae) overwintering on roses in southern Canada Journal of Experimental Biology 205 2002 2115 2124
58. F.E. Wood, and J.H. Nordin Studies on the low-temperature induced biogenesis of glycerol by adult Protophormia terranovae Journal of Insect Physiology 22 1976 1665 1673
59. S.-X. Yi, and R.E. Lee In vivo and in vitro rapid cold-hardening protects cells from cold-shock injury in the flesh fly Journal of Comparative Physiology B 174 2004 611 615
60. G.D. Yocum, J. Zdarek, K.H. Joplin, R.E. Lee, D.C. Smith, K.D. Manter, and D.L. Denlinger Alteration of eclosion rhythm and eclosion behavior in the flesh fly, Sarcophaga crassipalpis by low and high temperature stress Journal of Insect Physiology 40 1994 13 21
61. G.D. Yocum, K.H. Joplin, and D.L. Denlinger Upregulation of a 23 kDa small heat shock protein transcript during pupal diapause in the flesh fly, Sarcophaga crassipalpis Insect Biochemistry and Molecular Biology 28 1998 677 682
62. J.A. Yoder, and D.L. Denlinger Water balance in flesh fly pupae and water vapor absorption associated with diapause Journal of Experimental Biology 157 1991 273 286
63. J.A. Yoder, D.L. Denlinger, M.W. Dennis, and P.E. Kolattukudy Enhancement of diapausing flesh fly puparia with additional hydrocarbons and evidence for alkane biosynthesis by a decarbonylation mechanism Insect Biochemistry and Molecular Biology 22 1992 37 243
64. K.E. Zachariassen Physiology of cold tolerance in insects Physiological Reviews 65 1985 799 832
65. J. Zdarek, and G. Fraenkel The mechanism of pupariation in flies Journal of Experimental Zoology 179 1972 315 324
66. J. Zdarek, G. Fraenkel, and S. Friedman Pupariation in flies: a tool for monitoring effects of drugs, venoms, and other neurotoxic compounds Archives of Insect Biochemistry and Physiology 4 1987 29 46