1932

Abstract

Insect heat shock proteins include ATP-independent small heat shock proteins and the larger ATP-dependent proteins, Hsp70, Hsp90, and Hsp60. In concert with cochaperones and accessory proteins, heat shock proteins mediate essential activities such as protein folding, localization, and degradation. Heat shock proteins are synthesized constitutively in insects and induced by stressors such as heat, cold, crowding, and anoxia. Synthesis depends on the physiological state of the insect, but the common function of heat shock proteins, often working in networks, is to maintain cell homeostasis through interaction with substrate proteins. Stress-induced expression of heat shock protein genes occurs in a background of protein synthesis inhibition, but in the course of diapause, a state of dormancy and increased stress tolerance, these genes undergo differential regulation without the general disruption of protein production. During diapause, when ATP concentrations are low, heat shock proteins may sequester rather than fold proteins.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-011613-162107
2015-01-07
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/ento/60/1/annurev-ento-011613-162107.html?itemId=/content/journals/10.1146/annurev-ento-011613-162107&mimeType=html&fmt=ahah

Literature Cited

  1. Arrigo A-P. 1.  2013. Human small heat shock proteins: protein interactomes of homo- and hetero-oligomeric complexes; an update. FEBS Lett. 587:1959–69 [Google Scholar]
  2. Atungulu E, Tanaka H, Fujita K, Yamamoto K, Sakata M. 2.  et al. 2006. A double chaperone function of the sHsp genes against heat-based environmental adversity in the soil-dwelling leaf beetles. J. Insect Biotechnol. Sericol. 75:15–22 [Google Scholar]
  3. Azad P, Ryu J, Haddad GG. 3.  2011. Distinct role of Hsp70 in Drosophila hemocytes during severe hypoxia. Free Rad. Biol. Med. 51:530–38 [Google Scholar]
  4. Bao B, Xu W-H. 4.  2011. Identification of gene expression changes associated with the initiation of diapause in the brain of the cotton bollworm, Helicoverpa armigera. BMC Genomics 12:224 [Google Scholar]
  5. Basha E, O'Neill H, Vierling E. 5.  2012. Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends Biochem. Sci. 37:106–17Describes sHsp structure and its function in protein protection during stress. [Google Scholar]
  6. Benoit JB, Lopez-Martinez G, Phillips ZP, Patrick KR, Denlinger DL. 6.  2010. Heat shock proteins contribute to mosquito dehydration tolerance. J. Insect Physiol. 56:151–56 [Google Scholar]
  7. Brackley KI, Grantham J. 7.  2009. Activities of the chaperonin containing TCP-1 (CCT): implications for cell cycle progression and cytoskeletal organisation. Cell Stress Chaperones 14:23–31 [Google Scholar]
  8. Burton V, Mitchell HK, Young P, Petersen NS. 8.  1988. Heat shock protection against cold stress of Drosophila melanogaster. Mol. Cell. Biol. 8:3550–52 [Google Scholar]
  9. Carrigan PE, Riggs DL, Chinkers M, Smith DF. 9.  2005. Functional comparison of human and Drosophila Hop reveals novel role in steroid receptor maturation. J. Biol. Chem. 280:8906–11 [Google Scholar]
  10. Chapuis M-P, Simpson SJ, Blondin L, Sword GA. 10.  2011. Taxa-specific heat shock proteins are over-expressed with crowding in the Australian plague locust. J. Insect Physiol. 57:1562–67 [Google Scholar]
  11. Chen B, Kayukawa T, Monteiro A, Ishikawa Y. 11.  2005. The expression of the HSP90 gene in response to winter and summer diapauses and thermal-stress in the onion maggot, Delia antiqua. Insect Mol. Biol. 14:697–702 [Google Scholar]
  12. Chen B, Kayukawa T, Monteiro A, Ishikawa Y. 12.  2006. Cloning and characterization of the HSP70 gene, and its expression in response to diapauses and thermal stress in the onion maggot, Delia antiqua. J. Biochem. Mol. Biol. 39:749–58 [Google Scholar]
  13. Chen L, Ma W, Wang X, Niu C, Lei C. 13.  2009. Analysis of pupal head proteome and its alteration in diapausing pupae of Helicoverpa armigera. J. Insect Physiol. 56:247–52 [Google Scholar]
  14. Clare DK, Saibil HR. 14.  2013. ATP-driven molecular chaperone machines. Biopolymers 99:846–59Provides a description of the structure and function of ATP-dependent HSPs. [Google Scholar]
  15. Colinet H, Hoffmann A. 15.  2010. Gene and protein expression of Drosophila Starvin during cold stress and recovery from chill coma. Insect Biochem. Mol. Biol. 40:425–28 [Google Scholar]
  16. Colinet H, Hoffmann AA. 16.  2012. Comparing phenotypic effects and molecular correlates of developmental, gradual and rapid cold acclimation responses in Drosophila melanogaster. Funct. Ecol. 26:84–93 [Google Scholar]
  17. Colinet H, Lee SF, Hoffmann A. 17.  2010. Knocking down expression of Hsp22 and Hsp23 by RNA interference affects recovery from chill coma in Drosophila melanogaster. J. Exp. Biol. 213:4146–50 [Google Scholar]
  18. Colinet H, Lee SF, Hoffmann A. 18.  2010. Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. FEBS J. 277:174–85 [Google Scholar]
  19. Colinet H, Muratori F, Hance T. 19.  2010. Cold-induced expression of diapause in Praon volucre: fitness cost and morpho-physiological characterization. Physiol. Entomol. 35:301–7 [Google Scholar]
  20. Colinet H, Renault D, Charoy-Guével B, Com E. 20.  2012. Metabolic and proteomic profiling of diapause in the aphid parasitoid Praon volucre. PLoS ONE 7:2e32606 [Google Scholar]
  21. Cui Y-D, Du Y-Z, Lu M-X, Qiang C-K. 21.  2010. Cloning of the heat shock protein 60 gene from the stem borer, Chilo suppressalis, and analysis of expression characteristics under heat stress. J. Insect Sci. 10:100 http://insectscience.org/10.100 [Google Scholar]
  22. Ehrnsperger M, Gräber S, Gaestel M, Buchner J. 22.  1997. Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J. 16:221–29Depicts sHsps as platforms that bind denaturing proteins and enable subsequent refolding. [Google Scholar]
  23. Fan L, Lin J, Zhong Y, Liu J. 23.  2013. Shotgun proteomic analysis on the diapause and non-diapause eggs of domesticated silkworm Bombyx mori. PLOS ONE 8:4e60386 [Google Scholar]
  24. Fremdt H, Amendt J, Zehner R. 24.  2014. Diapause-specific gene expression in Calliphora vicina (Diptera: Calliphoridae)—a useful diagnostic tool for forensic entomology. Int. J. Legal Med. 1281001–11 [Google Scholar]
  25. Gkouvitsas T, Kontogiannatos D, Kourti A. 25.  2008. Differential expression of two small Hsps during diapause in the corn stalk borer Sesamia nonagrioides (Lef.). J. Insect Physiol. 54:1503–10 [Google Scholar]
  26. Gkouvitsas T, Kontogiannatos D, Kourti A. 26.  2009. Cognate Hsp70 gene is induced during deep larval diapause in the moth Sesamia nonagrioides. Insect Mol. Biol. 18:253–64 [Google Scholar]
  27. Gkouvitsas T, Kontogiannatos D, Kourti A. 27.  2009. Expression of the HSP83 gene in response to diapause and thermal stress in the moth Sesamia nonagrioides. Insect Mol. Biol. 18:759–68 [Google Scholar]
  28. Goto SG, Kimura MT. 28.  1998. Heat- and cold-shock responses and temperature adaptations in subtropical and temperate species of Drosophila. J. Insect Physiol. 44:1233–39 [Google Scholar]
  29. Goto SG, Kimura MT. 29.  2004. Heat-shock-responsive genes are not involved in the adult diapause of Drosophila triauraria. Gene 326:117–22 [Google Scholar]
  30. Goto SG, Yoshida KM, Kimura MT. 30.  1998. Accumulation of Hsp70 mRNA under environmental stresses in diapausing and nondiapausing adults of Drosophila triauraria. J. Insect Physiol. 44:1009–15Reveals that Hsp70 is not required for adult diapause in Drosophila (see also Ref. 29). [Google Scholar]
  31. Hahn DA, Denlinger DL. 31.  2011. Energetics of insect diapause. Annu. Rev. Entomol. 56:103–21 [Google Scholar]
  32. Hao Y-J, Li W-S, He Z-B, Si F-L, Ishikawa Y, Chen B. 32.  2012. Differential gene expression between summer and winter diapause pupae of the onion maggot Delia antiqua, detected by suppressive subtractive hybridization. J. Insect Physiol. 58:1444–49 [Google Scholar]
  33. Hayward SAL, Pavlides SC, Tammariello SP, Rinehart JP, Denlinger DL. 33.  2005. Temporal expression patterns of diapause-associated genes in flesh fly pupae from the onset of diapause through post-diapause quiescence. J. Insect Physiol. 51:631–40 [Google Scholar]
  34. Hayward SAL, Rinehart JP, Denlinger DL. 34.  2004. Desiccation and rehydration elicit distinct heat shock protein transcript responses in flesh fly pupae. J. Exp. Biol. 207:963–71 [Google Scholar]
  35. Huang L-H, Chen B, Kang L. 35.  2007. Impact of mild temperature hardening on thermotolerance, fecundity, and Hsp gene expression in Liriomyza huidobrensis. J. Insect Physiol. 53:1199–205 [Google Scholar]
  36. Huang L-H, Kang L. 36.  2007. Cloning and interspecific altered expression of heat shock protein genes in two leafminer species in response to thermal stress. Insect Mol. Biol. 16:491–500 [Google Scholar]
  37. Huang L-H, Wang C-Z, Kang L. 37.  2009. Cloning and expression of five heat shock protein genes in relation to cold hardening and development in the leafminer, Liriomyza sativa. J. Insect Physiol. 55:279–85 [Google Scholar]
  38. Hwang J-S, Go H-J, Goo T-W, Yun E-Y, Choi K-H. 38.  et al. 2005. The analysis of differentially expressed novel transcripts in diapausing and diapause-activated eggs of Bombyx mori. Arch. Insect Biochem. Physiol. 59:197–201 [Google Scholar]
  39. Joplin KH, Yocum GD, Denlinger DL. 39.  1990. Cold shock elicits expression of heat shock proteins in the flesh fly, Sarcophaga crassipalpis. J. Insect Physiol. 36:825–34 [Google Scholar]
  40. Kankare M, Salminen T, Laiho A, Vesala L, Hoikkala A. 40.  2010. Changes in gene expression linked with adult reproductive diapause in a northern malt fly species: a candidate gene microarray study. BMC Ecol. 10:3 [Google Scholar]
  41. Kayukawa T, Chen B, Miyazaki S, Itoyama K, Shinoda T, Ishikawa Y. 41.  2005. Expression of mRNA for the t-complex polypeptide–1, a subunit of chaperonin CCT, is upregulated in association with increased cold hardiness in Delia antiqua. Cell Stress Chaperones 10:204–10 [Google Scholar]
  42. Kayukawa T, Ishikawa Y. 42.  2009. Chaperonin contributes to cold hardiness of the onion maggot Delia antiqua through repression of depolymerization of actin at low temperatures. PLOS ONE 4:12e8277 [Google Scholar]
  43. Kihara F, Niimi T, Yamashita O, Yaginuma T. 43.  2011. Heat shock factor binds to heat shock elements upstream of heat shock protein 70a and Samui genes to confer transcriptional activity in Bombyx mori diapause eggs exposed to 5°C. Insect Biochem. Mol. Biol. 41:843–51 [Google Scholar]
  44. Kim B-G, Shim J-K, Kim D-W, Kwon YJ, Lee K-Y. 44.  2008. Tissue-specific variation of heat shock protein gene expression in relation to diapause in the bumblebee Bombus terrestris. Entomolog. Res. 38:10–16 [Google Scholar]
  45. Koštál V. 45.  2006. Eco-physiological phases of insect diapause. J. Insect Physiol. 52:113–27Presents a thorough account of different phases throughout insect diapause. [Google Scholar]
  46. Koštál V, Tollarová-Borovanská M. 46.  2009. The 70 kDa heat shock protein assists during the repair of chilling injury in the insect, Pyrrhocoris apterus. PLoS ONE 4:2e4546 [Google Scholar]
  47. Lee GJ, Vierling E. 47.  2000. A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol. 122:189–97 [Google Scholar]
  48. Li A, Denlinger DL. 48.  2008. Rapid cold hardening elicits changes in brain protein profiles of the flesh fly, Sarcophaga crassipalpis. Insect Mol. Biol. 17:565–72 [Google Scholar]
  49. Li A, Denlinger DL. 49.  2009. Pupal cuticle protein is abundant during early adult diapause in the mosquito Culex pipiens. J. Med. Entomol. 46:1382–86 [Google Scholar]
  50. Li AQ, Popova-Butler A, Dean DH, Denlinger DL. 50.  2007. Proteomics of the flesh fly brain reveals an abundance of upregulated heat shock proteins during pupal diapause. J. Insect Physiol. 53:385–91Illustrates an early use of proteomics to examine HSPs during diapause. [Google Scholar]
  51. Li H-B, Du Y-Z. 51.  2013. Molecular cloning and characterization of an Hsp90/70 organizing protein gene from Frankliniella occidentalis (Insecta: Thysanoptera, Thripidae). Gene 520:148–55 [Google Scholar]
  52. Li J, Moghaddam HH, Du X, Zhong B, Chen Y-Y. 52.  2012. Comparative analysis on the expression of inducible HSPs in the silkworm, Bombyx mori. Mol. Biol. Rep. 39:3915–23 [Google Scholar]
  53. Li Z-W, Li X, Yu Q-Y, Xiang Z-H, Kishino H, Zhang Z. 53.  2009. The small heat shock protein (sHSP) genes in the silkworm, Bombyx mori, and comparative analysis with other insect sHSP genes. BMC Evol. Biol. 9:215 [Google Scholar]
  54. Liu G, Roy J, Johnson EA. 54.  2006. Identification and function of hypoxia-response genes in Drosophila melanogaster. Physiol. Genomics 25:134–41 [Google Scholar]
  55. Liu Z, Xi D, Kang M, Guo X, Xu B. 55.  2012. Molecular cloning and characterization of Hsp27.6: the first reported small heat shock protein from Apis cerana cerana. Cell Stress Chaperones 17:539–51 [Google Scholar]
  56. Lopez-Martinez G, Benoit JB, Rinehart JP, Elnitsky MA, Lee RE Jr, Denlinger DL. 56.  2009. Dehydration, rehydration, and overhydration alter patterns of gene expression in the Antarctic midge, Belgica antarctica. J. Comp. Physiol. B 179:481–91 [Google Scholar]
  57. Lopez-Martinez G, Denlinger DL. 57.  2008. Regulation of heat shock proteins in the apple maggot Rhagoletis pomonella during hot summer days and overwintering diapause. Physiol. Entomol. 33:346–52 [Google Scholar]
  58. Lopez-Martinez G, Elnitsky MA, Benoit JB, Lee RE Jr, Denlinger DL. 58.  2008. High resistance to oxidative damage in the Antarctic midge Belgica antarctica, and developmentally linked expression of genes encoding superoxide dismutase, catalase and heat shock proteins. Insect Biochem. Mol. Biol. 38:796–804 [Google Scholar]
  59. Lu M-X, Hua J, Cui Y-D, Du Y-Z. 59.  2014. Five small heat shock protein genes from Chilo suppressalis: characteristics of gene, genomic organization, structural analysis, and transcription profiles. Cell Stress Chaperones 19:91–104 [Google Scholar]
  60. Lu Y-X, Xu W-H. 60.  2010. Proteomic and phosphoproteomic analysis at diapause initiation in the cotton bollworm, Helicoverpa armigera. J. Proteome Res. 9:5053–64 [Google Scholar]
  61. MacRae TH. 61.  2010. Gene expression, metabolic regulation and stress tolerance during diapause. Cell. Mol. Life Sci. 67:2405–24Molecular analysis of diapause in several organisms, including insects. [Google Scholar]
  62. Mayer MP. 62.  2010. Gymnastics of molecular chaperones. Mol. Cell 39:321–31 [Google Scholar]
  63. Meyer AS, Gillespie JR, Walther D, Millet IS, Doniach S, Frydman J. 63.  2003. Closing the folding chamber of the eukaryotic chaperonin requires the transition state of ATP hydrolysis. Cell 113:369–81 [Google Scholar]
  64. Michaud MB, Teets NM, Peyton JT, Blobner BM, Denlinger DL. 64.  2011. Heat shock response to hypoxia and its attenuation during recovery in the flesh fly, Sarcophaga crassipalpis. J. Insect Physiol. 57:203–10 [Google Scholar]
  65. Moribe Y, Niimi T, Yamashita O, Yaginuma T. 65.  2001. Samui, a novel cold-inducible gene, encoding a protein with a BAG domain similar to silencer of death domains (SODD/BAG-4), isolated from Bombyx diapause eggs. Eur. J. Biochem. 268:3432–42 [Google Scholar]
  66. Moribe Y, Oka K, Niimi T, Yamashita O, Yaginuma T. 66.  2010. Expression of heat shock protein 70a mRNA in Bombyx mori diapause eggs. J. Insect Physiol. 56:1246–52 [Google Scholar]
  67. Pavlides SC, Pavlides SA, Tammariello SP. 67.  2011. Proteomic and phosphoproteomic profiling during diapause entrance in the flesh fly, Sarcophaga crassipalpis. J. Insect Physiol. 57:635–44 [Google Scholar]
  68. Poelchau MF, Reynolds JA, Elsik CG, Denlinger DL, Armbruster PA. 68.  2013. Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus. Proc. R. Soc. B 280:20130143 [Google Scholar]
  69. Ragland GJ, Denlinger DL, Hahn DA. 69.  2010. Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly. Proc. Natl. Acad. Sci. USA 107:14909–14 [Google Scholar]
  70. Reynolds JA, Hand SC. 70.  2009. Decoupling development and energy flow during embryonic diapause in the cricket, Allonemobius scolus. J. Exp. Biol. 212:2065–74 [Google Scholar]
  71. Reynolds JA, Hand SC. 71.  2009. Embryonic diapause highlighted by differential expression of mRNAs for ecdysteroidogenesis, transcription and lipid sparing in the cricket Allonemobius socius. J. Exp. Biol. 212:2075–84 [Google Scholar]
  72. Rinehart JP, Denlinger DL. 72.  2000. Heat-shock protein 90 is down-regulated during pupal diapause in the flesh fly, Sarcophaga crassipalpis, but remains responsive to thermal stress. Insect Mol. Biol. 9:641–45 [Google Scholar]
  73. Rinehart JP, Li A, Yocum GD, Robich RM, Hayward SAL, Denlinger DL. 73.  2007. Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proc. Natl. Acad. Sci. USA 104:11130–37HSP production and function during diapause and cold tolerance in several insects. [Google Scholar]
  74. Rinehart JP, Robich RM, Denlinger DL. 74.  2006. Enhanced cold and desiccation tolerance in diapausing adults of Culex pipiens, and a role for Hsp70 in response to cold shock but not as a component of the diapause program. J. Med. Entomol. 43:713–22 [Google Scholar]
  75. Rinehart JP, Robich RM, Denlinger DL. 75.  2010. Isolation of diapause-regulated genes from the flesh fly, Sarcophaga crassipalpis by suppressive subtractive hybridization. J. Insect Physiol. 56:603–9 [Google Scholar]
  76. Rinehart JP, Yocum GD, Denlinger DL. 76.  2000. Developmental regulation of inducible hsp70 transcripts, but not the cognate form, during pupal diapause in the flesh fly, Sarcophaga crassipalpis. Insect Biochem. Mol. Biol. 30:515–21 [Google Scholar]
  77. Robich RM, Rinehart JP, Kitchen LJ, Denlinger DL. 77.  2007. Diapause-specific gene expression in the northern house mosquito, Culex pipiens L., identified by suppressive subtractive hybridization. J. Insect Physiol. 53:235–45 [Google Scholar]
  78. Röhl A, Rohrberg J, Buchner J. 78.  2013. The chaperone Hsp90: changing partners for demanding clients. Trends Biochem. Sci. 38:253–62 [Google Scholar]
  79. Sakano D, Li B, Xia Q, Yamamoto K, Fujii H, Aso Y. 79.  2006. Genes encoding small heat shock proteins of the silkworm, Bombyx mori. Biosci. Biotechnol. Biochem. 70:2443–50 [Google Scholar]
  80. Saravanakumar R, Ponnuvel KM, Qadri SMH. 80.  2008. Expression of metabolic enzyme genes and heat-shock protein genes during embryonic development in diapause and non-diapause egg of multivoltine silkworm Bombyx mori. Biologia 63:737–44 [Google Scholar]
  81. Sasibhushan S, Ponnuvel KM, Vijayaprakash NB. 81.  2012. Diapause specific gene expression in the eggs of multivoltine silkworm Bombyx mori, identified by suppressive subtractive hybridization. Comp. Biochem. Physiol. B 161:371–79 [Google Scholar]
  82. Sasibhushan S, Rao CGP, Ponnuvel KM. 82.  2013. Genome wide microarray based expression profiles during early embryogenesis in diapause induced and non-diapause eggs of polyvoltine silkworm Bombyx mori. Genomics 102:379–87 [Google Scholar]
  83. Sejerkilde M, Sørensen JG, Loeschcke V. 83.  2003. Effects of cold- and heat hardening on thermal resistance in Drosophila melanogaster. J. Insect Physiol. 49:719–26 [Google Scholar]
  84. Shorter J. 84.  2011. The mammalian disaggregase machinery: Hsp110 synergizes with Hsp70 and Hsp40 to catalyze protein disaggregation and reactivation in a cell-free system. PLOS ONE 6:10e26319 [Google Scholar]
  85. Sinclair BJ, Gibbs AG, Roberts SP. 85.  2007. Gene transcription during exposure to, and recovery from, cold and desiccation stress in Drosophila melanogaster. Insect Mol. Biol. 16:435–43 [Google Scholar]
  86. Sonoda S, Fukumoto K, Izumi Y, Yoshida H, Tsumuki H. 86.  2006. Cloning of heat shock protein genes (hsp90 and hsc70) and their expression during larval diapause and cold tolerance acquisition in the rice stem borer, Chilo suppressalis Walker. Arch. Insect Biochem. Physiol. 63:36–47 [Google Scholar]
  87. Tachibana S-I, Numata H, Goto SG. 87.  2005. Gene expression of heat-shock proteins (Hsp23, Hsp70 and Hsp90) during and after larval diapause in the blow fly Lucilia sericata. J. Insect Physiol. 51:641–47 [Google Scholar]
  88. Tammariello SP, Denlinger DL. 88.  1998. G0/G1 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 Biochem. Mol. Biol. 28:83–89 [Google Scholar]
  89. Tammariello SP, Rinehart JP, Denlinger DL. 89.  1999. Desiccation elicits heat shock protein transcription in the flesh fly, Sarcophaga crassipalpis, but does not enhance tolerance to high or low temperatures. J. Insect Physiol. 45:933–38 [Google Scholar]
  90. Teixeira LAF, Polavarapu S. 90.  2005. Expression of heat shock protein 70 after heat stress during pupal diapause in Rhagoletis mendax (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 98:966–72 [Google Scholar]
  91. Tungjitwitayakul J, Tatun N, Singtripop T, Sakurai S. 91.  2008. Characteristic expression of three heat shock-responsive genes during larval diapause in the bamboo borer Omphisa fuscidentalis. Zool. Sci. 25:321–33 [Google Scholar]
  92. Wang H, Li K, Zhu J-Y, Fang Q, Ye G-Y. 92.  2012. Cloning and expression of heat shock protein genes from the endoparasitoid wasp, Pteromalus puparum in response to environmental stresses. Arch. Insect Biochem. Physiol. 79:247–63 [Google Scholar]
  93. Wang H-S, Wang X-H, Zhou C-S, Huang L-H, Zhang S-F. 93.  et al. 2007. cDNA cloning of heat shock proteins and their expression in the two phases of the migratory locust. Insect Mol. Biol. 16:207–19 [Google Scholar]
  94. Wolschin F, Gadau J. 94.  2009. Deciphering proteomic signatures of early diapause in Nasonia. PLOS ONE 4:7e6394 [Google Scholar]
  95. Yiangou M, Tsapogas P, Nikolaidis N, Scouras ZG. 95.  1997. Heat shock gene expression during recovery after transient cold shock in Drosophila auraria (Diptera: Drosophilidae). Cytobios 92:91–98 [Google Scholar]
  96. Yocum GD. 96.  2001. Differential expression of two HSP70 transcripts in response to cold shock, thermoperiod, and adult diapause in the Colorado potato beetle. J. Insect Physiol. 47:1139–45 [Google Scholar]
  97. Yocum GD, Kemp WP, Bosch J, Knoblett JN. 97.  2005. Temporal variation in overwintering gene expression and respiration in the solitary bee Megachile rotundata. J. Insect Physiol. 51:621–29 [Google Scholar]
  98. Zhang G, Storey JM, Storey KB. 98.  2011. Chaperone proteins and winter survival by a freeze tolerant insect. J. Insect Physiol. 57:1115–22 [Google Scholar]
  99. Zhang Q, Denlinger DL. 99.  2010. Molecular characterization of heat shock protein 90, 70 and 70 cognate cDNAs and their expression patterns during thermal stress and pupal diapause in the corn earworm. J. Insect Physiol. 56:138–50 [Google Scholar]
  100. Zhang Q, Lu Y-X, Xu W-H. 100.  2012. Integrated proteomic and metabolomic analysis of larval brain associated with diapause induction and preparation in the cotton bollworm, Helicoverpa armigera. J. Proteome Res. 11:1042–53 [Google Scholar]
  101. Zhang Q, Lu Y-X, Xu W-H. 101.  2013. Proteomic and metabolomic profiles of larval hemolymph associated with diapause in the cotton bollworm, Helicoverpa armigera. BMC Genomics 14:751 [Google Scholar]
/content/journals/10.1146/annurev-ento-011613-162107
Loading
/content/journals/10.1146/annurev-ento-011613-162107
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error