Russian Journal of Genetics

, Volume 53, Issue 1, pp 21–38 | Cite as

The evolution of heat shock genes and expression patterns of heat shock proteins in the species from temperature contrasting habitats

  • D. G. GarbuzEmail author
  • M. B. Evgen’ev
Reviews and Theoretical Articles


Heat shock genes are the most evolutionarily ancient among the systems responsible for adaptation of organisms to a harsh environment. The encoded proteins (heat shock proteins, Hsps) represent the most important factors of adaptation to adverse environmental conditions. They serve as molecular chaperones, providing protein folding and preventing aggregation of damaged cellular proteins. Structural analysis of the heat shock genes in individuals from both phylogenetically close and very distant taxa made it possible to reveal the basic trends of the heat shock gene organization in the context of adaptation to extreme conditions. Using different model objects and nonmodel species from natural populations, it was demonstrated that modulation of the Hsps expression during adaptation to different environmental conditions could be achieved by changing the number and structural organization of heat shock genes in the genome, as well as the structure of their promoters. It was demonstrated that thermotolerant species were usually characterized by elevated levels of Hsps under normal temperature or by the increase in the synthesis of these proteins in response to heat shock. Analysis of the heat shock genes in phylogenetically distant organisms is of great interest because, on one hand, it contributes to the understanding of the molecular mechanisms of evolution of adaptogenes and, on the other hand, sheds the light on the role of different Hsps families in the development of thermotolerance and the resistance to other stress factors.


heat shock genes heat shock proteins evolution of multigene families adaptation thermotolerance 


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  1. 1.
    Craig, E.A., The heat shock response, CRC Crit. Rev. Biochem., 1985, vol. 18, no. 3, pp. 239–280.PubMedCrossRefGoogle Scholar
  2. 2.
    Easton, D.P., Kaneko, Y., and Subjeck, J.R., The hsp110 and Grp170 stress proteins: newly recognized relatives of the Hsp70s, Cell Stress Chaperones, 2000, vol. 5, no. 4, pp. 276–290.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Kampinga, H.H., Hageman, J., Vos, M.J., et al., Guidelines for the nomenclature of the human heat shock proteins, Cell Stress Chaperones, 2009, vol. 14, no. 1, pp. 105–111. doi 10.1007/s12192-008-0068-7PubMedCrossRefGoogle Scholar
  4. 4.
    Heat Shock Proteins: from Bacteria to Man, Schlesinger M.J., Tissires A., and Ashburner M., Eds., Cold Spring Harbor: Cold Spring Harbor Lab., 1982.Google Scholar
  5. 5.
    Feder, M.E. and Hofmann, G.E., Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology, Annu. Rev. Physiol., 1999, vol. 61, pp. 243–282.PubMedCrossRefGoogle Scholar
  6. 6.
    Rinehart, J.P., Hayward, S.A., Elnitsky, M.A., et al., Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 38, pp. 14223–14227. doi 10.1073/pnas.0606840103PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Amin, J., Ananthan, J., and Voellmy, R., Key features of heat shock regulatory elements, Mol. Cell. Biol., 1988, vol. 8, no. 9, pp. 3761–3769.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Åkerfelt, M., Morimoto, R.I., and Sistonen, L., Heat shock factors: integrators of cell stress, development and lifespan, Nat. Rev. Mol. Cell. Biol., 2010, vol. 11, no. 8, pp. 545–555. doi 10.1038/nrm2938PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Ish-Horowicz, D. and Leigh Brown, A.J., Evolution of the 87A and 87C heat-shock loci in Drosophila, Nature, 1981, vol. 290, no. 5808, pp. 677–682.PubMedCrossRefGoogle Scholar
  10. 10.
    Parsell, D.A. and Lindquist, S., The function of heatshock proteins in stress tolerance: degradation and reactivation of damaged proteins, Annu. Rev. Genet., 1993, vol. 27, pp. 437–496.PubMedCrossRefGoogle Scholar
  11. 11.
    Lindquist, S., The heat-shock response, Annu. Rev. Biochem., 1986, vol. 55, pp. 1151–1191.PubMedCrossRefGoogle Scholar
  12. 12.
    Bracher, A. and Verghese, J., The nucleotide exchange factors of Hsp70 molecular chaperones, Front. Mol. Biosci., 2015, vol. 2, p. 10. doi 10.3389/fmolb. 2015.00010PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Margulis, B.A. and Guzhova, I.V., Stress proteins in eukaryotic cells, Tsitologiya, 2000, vol. 42, no. 4, pp. 323–341.Google Scholar
  14. 14.
    Tian, S., Haney, R.A., and Feder, M.E., Phylogeny disambiguates the evolution of heat-shock cis-regulatory elements in Drosophila, PLoS One, 2010, vol. 5, no. 5. e10669. doi 10.1371/journal.pone.0010669PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Ayme, A. and Tissieres, A., Locus 67B of Drosophila melanogaster contains seven, not four, closely related heat shock genes, EMBO J., 1985, vol. 4, no. 11, pp. 2949–2954.PubMedPubMedCentralGoogle Scholar
  16. 16.
    Morrow, G., Heikkila, J.J., and Tanguay, R.M., Differences in the chaperone-like activities of the four main small heat shock proteins of Drosophila melanogaster, Cell Stress Chaperones, 2006, vol. 11, no. 1, pp. 51–60.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Horwitz, J., Some properties of the low molecular weight alpha-crystallin from normal human lens: comparison with bovine lens, Exp. Eye. Res., 1976, vol. 23, no. 5, pp. 471–481.PubMedCrossRefGoogle Scholar
  18. 18.
    Carver, J.A., Guerreiro, N., Nicholls, K.A., and Truscott, R.J., On the interaction of alpha-crystallin with unfolded proteins, Biochim. Biophys. Acta, 1995, vol. 1252, no. 2, pp. 251–260.PubMedCrossRefGoogle Scholar
  19. 19.
    Kazemi-Esfarjani, P. and Seymour Benzer, Genetic suppression of polyglutamine toxicity in Drosophila, Science, 2000, vol. 287, no. 5459, pp. 1837–1840.PubMedCrossRefGoogle Scholar
  20. 20.
    Brackley, K.I. and Grantham, J., Activities of the chaperonin containing TCP-1 (CCT): implications for cell cycle progression and cytoskeletal organization, Cell Stress Chaperones, 2009, vol. 14, no. 1, pp. 23–31. doi 10.1007/s12192-008-0057-xPubMedCrossRefGoogle Scholar
  21. 21.
    Sarkar, S. and Lakhotia, S.C., The Hsp60C gene in the 25F cytogenetic region in Drosophila melanogaster is essential for tracheal development and fertility, J. Genet., 2005, vol. 84, no. 3, pp. 265–281.PubMedCrossRefGoogle Scholar
  22. 22.
    Hartl, F.U., Bracher, A., and Hayer-Hartl, M., Molecular chaperones in protein folding and proteostasis, Nature, 2011, vol. 475, no. 7356, pp. 324–332. doi 10.1038/nature10317PubMedCrossRefGoogle Scholar
  23. 23.
    Kaul, S.C., Deocaris, C.C., and Wadhwa, R., Three faces of mortalin: a housekeeper, guardian and killer, Exp. Gerontol., 2007, vol. 42, no. 4, pp. 263–274. doi 10.1016/j.exger.2006.10.020PubMedCrossRefGoogle Scholar
  24. 24.
    Milner, C.M. and Campbell, R.D., Structure and expression of the three MHC-linked HSP70 genes, Immunogenetics, 1990, vol. 32, no. 4, pp. 242–251.PubMedCrossRefGoogle Scholar
  25. 25.
    Milner, C.M. and Campbell, R.D., Polymorphic analysis of three MHC-linked HSP70 genes, Immunogenetics, 1992, vol. 36, no. 6, pp. 357–362.PubMedCrossRefGoogle Scholar
  26. 26.
    Rubin, D.M., Mehta, A.D., Zhu, J., et al., Genomic structure and sequence analysis of Drosophila melanogaster HSC70 genes, Gene, 1993, vol. 128, no. 2, pp. 155–163.PubMedCrossRefGoogle Scholar
  27. 27.
    Lee-Yoon, D., Easton, D., Murawski, M., et al., Identification of a major subfamily of large hsp70-like proteins through the cloning of the mammalian 110-kDa heat shock protein, J. Biol. Chem., 1995, vol. 270, no. 26, pp. 15725–15733.PubMedCrossRefGoogle Scholar
  28. 28.
    Xu, X., Sarbeng, E.B., Vorvis, C., et al., Unique peptide substrate binding properties of 110-kDa heatshock protein (Hsp110) determine its distinct chaperone activity, J. Biol. Chem., 2012, vol. 287, no. 8, pp. 5661–5672. doi 10.1074/jbc.M111.275057PubMedCrossRefGoogle Scholar
  29. 29.
    Sorger, P.K. and Pelham, H.R., The glucose-regulated protein grp94 is related to heat shock protein hsp90, J. Mol. Biol., 1987, vol. 194, no. 2, pp. 341–344.PubMedCrossRefGoogle Scholar
  30. 30.
    Felts, S.J., Owen, B.A., Nguyen, P., et al., The hsp90-related protein TRAP1 is a mitochondrial protein with distinct functional properties, J. Biol. Chem., 2000, vol. 275, no. 5, pp. 3305–3312.PubMedCrossRefGoogle Scholar
  31. 31.
    Chen, B., Zhong, D., and Monteiro, A., Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms, BMC Genomics, 2006, vol. 7, p. 156. doi 10.1186/1471-2164-7-156PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Abravaya, K., Myers, M.P., Murphy, S.P., and Morimoto, R.I., The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression, Genes Dev., 1992, vol. 6, no. 7, pp. 1153–1164.PubMedCrossRefGoogle Scholar
  33. 33.
    Xu, Y. and Lindquist, S., Heat-shock protein hsp90 governs the activity of pp60v-src kinase, Proc. Natl. Acad. Sci. U.S.A., 1993, vol. 90, no. 15, pp. 7074–7078.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Whitesell, L., Sutphin, P.D., Pulcini, E.J., et al., The physical association of multiple molecular chaperone proteins with mutant p53 is altered by geldanamycin, an HSP90-binding agent, Mol. Cell. Biol., 1998, vol. 18, no. 3, pp. 1517–1524.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Kosano, H., Stensgard, B., Charlesworth, M.C., et al., The assembly of progesterone receptor-hsp90 complexes using purified proteins, J. Biol. Chem., 1998, vol. 273, no. 49, pp. 32973–32979.PubMedCrossRefGoogle Scholar
  36. 36.
    Sato, S., Fujita, N., and Tsuruo, T., Modulation of Akt kinase activity by binding to Hsp90, Proc. Natl. Acad. Sci. U.S.A., 2000, vol. 97, no. 20, pp. 10832–10837.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Chen, Y. and Brandizzi, F., IRE1: ER stress sensor and cell fate executor, Trends Cell. Biol., 2013, vol. 23, no. 11, pp. 547–555. doi 10.1016/j.tcb.2013.06.005PubMedCrossRefGoogle Scholar
  38. 38.
    Hunt, C. and Morimoto, R.I., Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70, Proc. Natl. Acad. Sci. U.S.A., 1985, vol. 82, no. 19, pp. 6455–6459.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Lindquist, S. and Craig, E.A., The heat-shock proteins, Annu. Rev. Genet., 1988, vol. 22, pp. 631–677.PubMedCrossRefGoogle Scholar
  40. 40.
    Southgate, R., Mirault, M., Ayme, A., and Tissieres, A., Organization, sequences and induction of heat shock genes, in Changes in Eukaryotic Gene Expression in Response to Environmental Stress, New York: Academic, 1985, pp. 3–30.CrossRefGoogle Scholar
  41. 41.
    Lindquist, S. and Kim, G., Heat-shock protein 104 expression is sufficient for thermotolerance in yeast, Proc. Natl. Acad. Sci. U.S.A., 1996, vol. 93, no. 11, pp. 5301–5306.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Heschl, M.F. and Baillie, D.L., Characterization of the hsp70 multigene family of Caenorhabditis elegans, DNA, 1989, vol. 8, no. 4, pp. 233–243.PubMedCrossRefGoogle Scholar
  43. 43.
    Heschl, M.F. and Baillie, D.L., The HSP70 multigene family of Caenorhabditis elegans, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1990, vol. 96, no. 4, pp. 633–637.CrossRefGoogle Scholar
  44. 44.
    Hansen, J.J., Bross, P., Westergaard, M., et al., Genomic structure of the human mitochondrial chaperonin genes: HSP60 and HSP10 are localized head to head on chromosome 2 separated by a bidirectional promoter, Hum. Genet., 2003, vol. 112, no. 1, pp. 71–77.PubMedCrossRefGoogle Scholar
  45. 45.
    Maside, X., Bartolome, C., and Charlesworth, B., S-element insertions are associated with the evolution of the Hsp70 genes in Drosophila melanogaster, Curr. Biol., 2002, vol. 12, no. 19, pp. 1686–1691.PubMedCrossRefGoogle Scholar
  46. 46.
    Dragon, E., Sias, S., Kato, E., and Gabe, J., The genome of Trypanosoma cruzi containes a constitutively expressed, tandemly arranged multicopy gene homologous to a major heat shock protein, Mol. Cell. Biol., 1978, vol. 7, no. 3, pp. 1271–1275.CrossRefGoogle Scholar
  47. 47.
    Shapira, M. and Pinelli, E., Heat-shock protein 83 of Leishmania mexicana amazonensis is an abundant cytoplasmic protein with a tandemly repeated genomic arrangement, Eur. J. Biochem., 1989, vol. 185, no. 2, pp. 231–236.PubMedCrossRefGoogle Scholar
  48. 48.
    Benedict, M.Q., Levine, B.J., Ke, Z.X., et al., Precise limitation of concerted evolution to ORFs in mosquito Hsp82 genes, Insect Mol. Biol., 1996, vol. 5, no. 1, pp. 73–79.PubMedCrossRefGoogle Scholar
  49. 49.
    Evgen’ev, M.B., Zatsepina, O.G., Garbuz, D., et al., Evolution and arrangement of the hsp70 gene cluster in two closely related species of the virilis group of Drosophila, Chromosoma, 2004, vol. 113, no. 5, pp. 223–232.PubMedCrossRefGoogle Scholar
  50. 50.
    Segal, G. and Ron, E.Z., Regulation of heat-shock response in bacteria, Ann. N.Y. Acad. Sci., 1998, vol. 851, pp. 147–151.PubMedCrossRefGoogle Scholar
  51. 51.
    Flaherty, K.M., DeLuca-Flaherty, C., and McKay, D.B., Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein, Nature, 1990, vol. 346, no. 6285, pp. 623–628.PubMedCrossRefGoogle Scholar
  52. 52.
    Bork, P., Sander, C., and Valencia, A., An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins, Proc. Natl. Acad. Sci. U.S.A. 1992, vol. 89, no. 16, pp. 7290–7294.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Smith, T.M. and Kirley, T.L., Site-directed mutagenesis of a human brain ecto-apyrase: evidence that the E-type ATPases are related to the actin/heat shock 70/sugar kinase superfamily, Biochemistry, 1999, vol. 38, no. 1, pp. 321–328.PubMedCrossRefGoogle Scholar
  54. 54.
    Flajnik, M.F., Canel, C., Kramer, J., and Kasahara, M., Which came first, tMHC class I or class II?, {iImmunogenetics,} 1991, vol. 33, pp. 295–300.CrossRefGoogle Scholar
  55. 55.
    Evgen’ev, M.B., Sheinker, V.Sh., and Levin, A.V., Molecular mechanisms of adaptation to hyperthermia in higher organisms: 1. Synthesis of heat-shock proteins in cell cultures of different species of silkworms and in caterpillars, Mol. Biol. (Moscow), 1987, vol. 21, no. 2, pp. 484–494.Google Scholar
  56. 56.
    Gehring, W.J. and Wehner, R., Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert, Proc. Natl. Acad. Sci. U.S.A., 1995, vol. 92, no. 7, pp. 2994–2998.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Garbuz, D.G., Zatsepina, O.G., Przhiboro, A.A., et al., Larvae of related Diptera species from thermally contrasting habitats exhibit continuous up-regulation of heat shock proteins and high thermotolerance, Mol. Ecol., 2008, vol. 17, no. 21, pp. 4763–4777. doi 10.1111/j.1365-294X.2008.03947.xPubMedCrossRefGoogle Scholar
  58. 58.
    Zatsepina, O.G., Przhiboro, A.A., Yushenova, I.A., et al., A Drosophila heat shock response represents an exception rather than a rule among Diptera species, Insect Mol. Biol., 2016, vol. 25, no. 4, pp. 431–449. doi 10.1111/imb.12235PubMedCrossRefGoogle Scholar
  59. 59.
    Konstantopoulou, I., Nikolaidis, N., and Scouras, Z.G., The hsp70 locus of Drosophila auraria (montium subgroup) is single and contains copies in a conserved arrangement, Chromosoma, 1998, vol. 107, no. 8, pp. 577–586.PubMedCrossRefGoogle Scholar
  60. 60.
    Bettencourt, B.R. and Feder, M.E., Hsp70 duplication in the Drosophila melanogaster species group: how and when did two become five?, Mol. Biol. Evol., 2001, vol. 18, no. 7, pp. 1272–1282.PubMedCrossRefGoogle Scholar
  61. 61.
    Bettencourt, B.R. and Feder, M.E., Rapid concerted evolution via gene conversion at the Drosophila hsp70 genes, J. Mol. Evol., 2002, vol. 54, no. 5, pp. 569–586.PubMedCrossRefGoogle Scholar
  62. 62.
    Evgen’ev, M.B., Kolchinski, A., Levin, A., et al., Heat-shock DNA homology in distantly related species of Drosophila, Chromosoma, 1978, vol. 68, no. 4, pp. 357–365.PubMedCrossRefGoogle Scholar
  63. 63.
    Garbuz, D., Evgenev, M.B., Feder, M.E., and Zatsepina, O.G., Evolution of thermotolerance and the heat-shock response: evidence from inter/intraspecific comparison and interspecific hybridization in the virilis species group of Drosophila: 1. Thermal phenotype, J. Exp. Biol., 2003, vol. 206, no. 14, pp. 2399–2408.PubMedCrossRefGoogle Scholar
  64. 64.
    Miller, W.J., Nagel, A., Bachmann, J., and Bachmann, L., Evolutionary dynamics of the SGM transposon family in the Drosophila obscura species group, Mol. Biol. Evol., 2000, vol. 17, no. 11, pp. 1597–1609.PubMedCrossRefGoogle Scholar
  65. 65.
    Feder, J.H., Rossi, J.M., Solomon, J., et al., The consequences of expressing hsp70 in Drosophila cells at normal temperatures, Genes Dev., 1992, vol. 6, no. 8, pp. 1402–1413.PubMedCrossRefGoogle Scholar
  66. 66.
    Feder, M.E. and Krebs, R.A., Ecological and evolutionary physiology of heat shock proteins and the stress response in Drosophila: complementary insights from genetic engineering and natural variation, in Stress, Adaptation, and Evolution, Bijlsma, R. and Loeschcke, V., Eds., Basel: Birkha User, 1997, pp. 155–173.CrossRefGoogle Scholar
  67. 67.
    Feder, M.E. and Krebs, R.A., Natural and genetic engineering of thermotolerance in Drosophila melanogaster: consequence for thermotolerance, Am. Zool., 1998, vol. 38, pp. 503–517.CrossRefGoogle Scholar
  68. 68.
    Petesch, S.J. and Lis, J.T., Rapid, transcription-independent loss of nucleosomes over a large chromatin domain at Hsp70 loci, Cell, 2008, vol. 134, no. 1, pp. 74–84. doi 10.1016/j.cell.2008.05.029PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Hart, C., Zhao, K., and Laemmli, U., The scs’ boundary element: characterization of boundary elementassociated factors, Mol. Cell. Biol., 1997, vol. 17, no. 2, pp. 999–1009.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Kellett, M. and McKechnie, S.W., A cluster of diagnostic Hsp68 amino acid sites that are identified in Drosophila from the melanogaster species group are concentrated around beta-sheet residues involved with substrate binding, Genome, 2005, vol. 48, no. 2, pp. 226–233. doi 10.1139/g04-113PubMedCrossRefGoogle Scholar
  71. 71.
    Garbuz, D.G., Yushenova, I., Bettencourt, B.G., et al., Organization and evolution of hsp70 clusters strikingly differ in two species of Stratiomyidae (Diptera) inhabiting thermally contrasting environments, BMC Evol. Biol., 2011, vol. 11, no. 1, p. 74. doi 10.1186/1471-2148-11-74PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Glass, D., Polvere, R.I., and Van der Ploeg, L.H.T., Conserved sequences and transcription of the hsp70 gene family in Trypanosoma brucei, Mol. Cell. Biol., 1986, vol. 6, no. 12, pp. 4657–4666.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Muhich, M.L. and Boothroyd, J.C., Synthesis of trypanosome hsp70 mRNA is resistant to disruption of trans-splicing by heat shock, J. Biol. Chem., 1989, vol. 264, no. 13, pp. 7107–7110.PubMedGoogle Scholar
  74. 74.
    Fiori, A., Kucharíková, S., Govaert, G., et al., The heat-induced molecular disaggregase Hsp104 of Candida albicans plays a role in biofilm formation and pathogenicity in a worm infection model, Eukaryotic Cell, 2012, vol. 11, no. 8, pp. 1012–1020. doi 10.1128/EC.00147-12PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Carrión, J., Folgueira, C., Soto, M., et al., Leishmania infantum HSP70-II null mutant as candidate vaccine against leishmaniasis: a preliminary evaluation, Parasites Vectors, 2011, vol. 4, p. 150. doi 10.1186/1756-3305-4-150PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Michalak, P., Minkov, I., Helin, A., et al., Genetic evidence for adaptation-driven incipient speciation of Drosophila melanogaster along a microclimatic contrast in “Evolution Canyon,” Israel, Proc. Natl. Acad. Sci. U.S.A., 2001, vol. 98, no. 23, pp. 13195–13200.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Zatsepina, O.G., Velikodvorskaia, V.V., Molodtsov, V.B., et al., A Drosophila melanogaster strain from sub-equatorial Africa has exceptional thermotolerance but decreased Hsp70 expression, J. Exp. Biol., 2001, vol. 204, no. 11, pp. 1869–1881.PubMedGoogle Scholar
  78. 78.
    Lerman, D.N., Michalak, P., Helin, A.B., et al., Modification of heat-shock gene expression in Drosophila melanogaster populations via transposable elements, Mol. Biol. Evol., 2003, vol. 20, no. 1, pp. 135–144.PubMedCrossRefGoogle Scholar
  79. 79.
    Lerman, D.N. and Feder, M.E., Naturally occurring transposable elements disrupt hsp70 promoter function in Drosophila melanogaster, Mol. Biol. Evol., 2005, vol. 22, no. 3, pp. 776–783. doi 10.1093/molbev/msi063PubMedCrossRefGoogle Scholar
  80. 80.
    Walser, J.C., Chen, B., and Feder, M.E., Heat-shock promoters: targets for evolution by P transposable elements in Drosophila, PLoS Genet., 2006, vol. 2, no. 10. e165. doi 10.1371/journal.pgen.0020165PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Karpov, V.L., Preobrazhenskaya, O.V., and Mirzabekov, A.D., Chromatin structure of hsp70 genes, activated by heat shock: selective removal of histones from the coding region and their absence from the 5' region, Cell, 1984, vol. 36, pp. 423–431.PubMedCrossRefGoogle Scholar
  82. 82.
    Tsukiyama, T., Becker, P.B., and Wu, C., ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor, Nature, 1994, vol. 367, no. 6463, pp. 525–532.PubMedCrossRefGoogle Scholar
  83. 83.
    Shopland, L.S., Hirayoshi, K., Fernandes, M., and Lis, J.T., HSF access to heat shock elements in vivo depends critically on promoter architecture defined by GAGA-factor, TFIID, and RNA-polymerase II binding sites, Genes Dev., 1995, vol. 9, no. 22, pp. 2756–2769.PubMedCrossRefGoogle Scholar
  84. 84.
    Shilova, V.Y., Garbuz, D.G., Myasyankina, E.N., et al., Remarkable site specificity of local transposition into the Hsp70 promoter of Drosophila melanogaster, Genetics, 2006, vol. 173, no. 2, pp. 809–820. doi 10.1534/genetics.105.053959PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Lee, H., Kraus, K., Wolfner, M., and Lis, J., DNA sequence requirements for generating paused polymerase at the start of hsp70, Genes. Dev., 1992, vol. 6, no. 2, pp. 284–295.PubMedCrossRefGoogle Scholar
  86. 86.
    Timakov, B., Liu, X., Turgut, I., and Zhang, P., Timing and targeting of P-element local transposition in the male germline Cells of Drosophila melanogaster, Genetics, 2002, vol. 160, no. 3, pp. 1011–1022.PubMedPubMedCentralGoogle Scholar
  87. 87.
    Krebs, R.A. and Feder, M.E., Hsp70 and larval thermotolerance in Drosophila melanogaster: how much is enough and when is more too much?, J. Insect. Physiol., 1998, vol. 44, no. 11, pp. 1091–1101.PubMedCrossRefGoogle Scholar
  88. 88.
    Walter, L., Rauh, F., and Gunther, E., Comparative analysis of the three major histocompatibility complex-linked heat shock protein 70 (hsp70) genes of the rat, Immunogenetics, 1994, vol. 40, no. 5, pp. 325–330.PubMedCrossRefGoogle Scholar
  89. 89.
    Salter-Cid, L., Kasahara, M., and Flajnik, M.F., Hsp70 genes are linked to the Xenopus major histocompatibility complex, Immunogenetics, 1994, vol. 39, no. 1, pp. 1–7.PubMedCrossRefGoogle Scholar
  90. 90.
    Garbuz, D.G., Astakhova, N.L., Zatsepina, O.G., et al., Functional organization of hsp70 cluster in camel (Camelus dromedarius) and other mammals, PLoS One, 2011, vol. 6, no. 11. e27205. doi 10.1371/journal.pone.0027205PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Hunt, C.R., Gasser, D.L., Chaplin, D.D., et al., Chromosomal localization of five murine HSP70 gene family members: Hsp70-1, Hsp70-2, Hsp70-3, Hsp70t and Grp78, Genomics, 1993, vol. 16, no. 1, pp. 193–198.PubMedCrossRefGoogle Scholar
  92. 92.
    Cameron, P.U., Tabarias, H.A., Pulendran, B., et al., Conservation of the central MHC genome: PFGE mapping and RFLP analysis of complement, HSP70, and TNF genes in the goat, Immunogenetics, 1990, vol. 31, no. 4, pp. 253–264.PubMedCrossRefGoogle Scholar
  93. 93.
    Berger, E.M., Marino, G., and Torrey, D., Expression of Drosophila hsp 70-CAT hybrid gene in Aedes cells induced by heat shock, Somat. Cell. Mol. Genet., 1985, vol. 11, no. 4, pp. 371–377.PubMedCrossRefGoogle Scholar
  94. 94.
    McMahon, A.P., Novak, T.J., Britten, R.J., and Davidson, E.H., Inducible expression of a cloned heat shock fusion gene in sea urchin embryos, Proc. Natl. Acad. Sci. U.S.A., 1984, vol. 81, no. 23, pp. 7490–7494.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Uhlirova, M., Asahina, M., Riddiford, L.M., and Jindra, M., Heat-inducible transgenic expression in the silkmoth Bombyx mori, Dev. Genes Evol., 2002, vol. 212, no. 3, pp. 145–151.PubMedCrossRefGoogle Scholar
  96. 96.
    Bienz, M. and Pelham, H.R.B., Heat shock regulatory elements function as an inducible enhancer in the Xenopus hsp70 gene and when linked to a heterologous promoter, Cell, 1986, vol. 45, no. 5, pp. 753–760.PubMedCrossRefGoogle Scholar
  97. 97.
    Voellmy, R. and Rungger, D., Transcription of a Drosophila heat shock gene is heat-induced in Xenopus oocytes, Proc. Natl. Acad. Sci. U.S.A., 1982, vol. 79, no. 6, pp. 1776–1780.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Burke, J.E. and Ish-Horowicz, D., Expression of Drosophila heat-shock genes is regulated in Rat-1 cells, Nucleic Acids Res., 1982, vol. 10, no. 13, pp. 3821–3830.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Mirault, M.E., Southgate, R., and Delwart, E., Regulation of heat shock genes: a DNA sequence up-stream of Drosphila hsp70 genes is essential for their induction in monkey cells, EMBO J., 1982, vol. 1, no. 10, pp. 1279–1285.PubMedPubMedCentralGoogle Scholar
  100. 100.
    Atkinson, P.W. and O’Brochta, D.A., In vivo expression of two highly conserved Drosophila genes in Australian sheep blowfly, Lucilia cuprina, Insect Biochem. Mol. Biol., 1992, vol. 22, pp. 423–431.CrossRefGoogle Scholar
  101. 101.
    Kalosaka, K., Chrysanthis, G., Rojas-Gill, A.P., et al., Evaluation of the activities of the medfly and Drosophila hsp70 promoters in vivo in germ-line transformed medflies, Insect Mol. Biol., 2006, vol. 15, no. 3, pp. 373–382. doi 10.1111/j.1365-2583.2006.00650.xPubMedCrossRefGoogle Scholar
  102. 102.
    Chen, B., Jia, T., Ma, R., et al., Evolution of hsp70 gene expression: a role for changes in AT-richness within promoters, PLoS One, 2011, vol. 6, no. 5. e20308. doi 10.1371/journal.pone.0020308PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Astakhova, L.N., Zatsepina, O.G., Przhiboro, A.A., et al., Novel arrangement and comparative analysis of hsp90 family genes in three thermotolerant species of Stratiomyidae (Diptera), Insect Mol. Biol., 2013, vol. 22, no. 3, pp. 284–296. doi 10.1111/imb.12020PubMedCrossRefGoogle Scholar
  104. 104.
    Astakhova L.N., Zatsepina O.G., Funikov S.Yu. et al. Activity of heat shock genes’ promoters in thermally contrasting animal species, PLoS One, 2015, vol. 10, no. 2. e0115536. doi 10.1371/journal.pone.0115536PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Kostyuchenko, M., Savitskaya, E., Koryagina, E., et al., Zeste can facilitate long-range enhancer–promoter communication and insulator bypass in Drosophila melanogaster, Chromosoma, 2009, vol. 118, no. 5, pp. 665–674. doi 10.1007/s00412-009-0226-4PubMedCrossRefGoogle Scholar
  106. 106.
    Ulmasov, H.A., Karaev, K.K., Lyashko, V.N., and Evgen’ev, M.B., Heat-shock response in camel (Camelus dromedarius) blood cells and adaptation to hyperthermia, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1993, vol. 106, no. 4, pp. 867–872.CrossRefGoogle Scholar
  107. 107.
    Evgen’ev, M.B., Garbuz, D.G., and Zatsepina, O.G., Heat Shock Proteins and Whole Body Adaptation to Extreme Environments, Springer-Verlag, 2014.CrossRefGoogle Scholar
  108. 108.
    Garbuz, D.G., Zatsepina, O.G., Yushenova, I., et al., Different mechanisms responsible for stress resistance operate in the same insect order (Diptera), in Handbook of Molecular Chaperones: Roles, Structures and Mechanisms, New York: Nova, 2010, pp. 479–495.Google Scholar
  109. 109.
    Velazquez, J.M., Sonoda, S., Bugaisky, G., and Lindquist, S., Is the major Drosophila heat shock protein present in cells that have not been heat shocked?, J. Cell. Biol., 1983, vol. 96, no. 1, pp. 286–290.PubMedCrossRefGoogle Scholar
  110. 110.
    Krebs, R.A., A comparison of Hsp70 expression and thermotolerance in adults and larvae of three Drosophila species, Cell Stress Chaperones, 1999, vol. 4, no. 4, pp. 243–249.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Papadimitriou, E., Kritikou, D., Mavroidis, M., et al., The heat shock 70 gene family in the Mediterranean fruit fly Ceratitis capitata, Insect Mol. Biol., 1998, vol. 7, no. 3, pp. 279–290.PubMedCrossRefGoogle Scholar
  112. 112.
    Karouna-Renier, N.K. and Zehr, J.P., Short-term exposures to chronically toxic copper concentrations induce HSP70 proteins in midge larvae (Chironomus tentans), Sci. Tot. Environ., 2003, vol. 312, nos. 1–3, pp. 267–272.CrossRefGoogle Scholar
  113. 113.
    Tachibana, S., Numata, H., and Goto, S.G., Gene expression of heat-shock proteins (Hsp23, Hsp70 and Hsp90) during and after larval diapause in the blow fly Lucilia sericata, J. Insect. Physiol., 2005, vol. 51, no. 6, pp. 641–647. doi 10.1016/j.jinsphys.2004.11.012PubMedCrossRefGoogle Scholar
  114. 114.
    Lee, S.M., Lee, S.B., Park, C.H., and Choi, J., Expression of heat shock protein and hemoglobin genes in Chironomus tentans (Diptera, Chironomidae) larvae exposed to various environmental pollutants: a potential biomarker of freshwater monitoring, Chemosphere, 2006, vol. 65, no. 6, pp. 1074–1081. doi 10.1016/j.chemosphere.2006.02.042PubMedCrossRefGoogle Scholar
  115. 115.
    Michaud, M.R., Teets, N.M., Peyton, J.T., et al., Heat shock response to hypoxia and its attenuation during recovery in the flesh fly, Sarcophaga crassipalpis, J. Insect. Physiol., 2011, vol. 57, no. 1, pp. 203–210. doi 10.1016/j.jinsphys.2010.11.007PubMedCrossRefGoogle Scholar
  116. 116.
    Delrio, G. and Cocco, A., Tephritidae, in Integrated Cotrol of Citrus Pests in the Mediterranean Region, Vacante, V. and Gerson, U., Eds., Bentham E-book, 2011, pp. 206–222.Google Scholar
  117. 117.
    King, A.M. and MacRae, T.H., Insect heat shock proteins during stress and diapauses, Annu. Rev. Entomol., 2015, vol. 60, pp. 59–75. doi 10.1146/annurev-ento-011613-162107PubMedCrossRefGoogle Scholar
  118. 118.
    Barua, D. and Heckathorn, S.A., Acclimation of the temperature set-points of the heat-shock response, J. Thermal Biol., 2004, vol. 29, pp. 185–193.CrossRefGoogle Scholar
  119. 119.
    Korol, A., Rashkovetsky, E., Iliadi, K., and Nevo, E., Drosophila flies in “Evolution Canyon” as a model for incipient sympatric speciation, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 48, pp. 18184–18189.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Shilova, V.Yu., Garbuz, D.G., Evgen’ev, M.B., and Zatsepina, O.G., Small heat shock proteins and adaptation of various Drosophila species to hyperthermia, Mol. Biol. (Moscow), 2006, vol. 40, no. 2, pp. 235–239.CrossRefGoogle Scholar
  121. 121.
    Hofmann, G.E., Buckley, B.A., Airaksinen, S., et al., Heat-shock protein expression is absent in the Antarctic fish Trematomus bernacchii (family Nototheniidae), J. Exp. Biol., 2000, vol. 203, no. 15, pp. 2331–2339.PubMedGoogle Scholar
  122. 122.
    LaTerza, A., Papa, G., Miceli, C., and Luporini, P., Divergence between two Antarctic species of the ciliate Euplotes, E. focardii and E. nobilii, in the expression of heat-shock protein 70 genes, Mol. Ecol., 2001, vol. 10, no. 4, pp. 1061–1067.CrossRefGoogle Scholar
  123. 123.
    Buckley, B.A., Place, S.P., and Hofmann, G.E., Regulation of heat shock genes in isolated hepatocytes from an Antarctic fish, Trematomus bernacchii, J. Exp. Biol., 2004, vol. 207, no. 21, pp. 3649–3656. doi 10.1242/jeb.01219PubMedCrossRefGoogle Scholar
  124. 124.
    Buckley, B.A. and Somero, G.N., cDNA microarray analysis reveals the capacity of the cold-adapted Antarctic fish Trematomus bernacchii to alter gene expression in response to heat stress, Polar Bio., 2009, vol. 32, no. 3, pp. 403–415. doi 10.1007/s00300-008-0533-xCrossRefGoogle Scholar
  125. 125.
    Place, S.P. and Hofmann, G.E., Comparison of Hsc70 orthologs from polar and temperate notothenioid fishes: differences in prevention of aggregation and refolding of denatured proteins, Am. J. Physiol. Regul. Integr. Comp. Physiol., 2005, vol. 288, no. 5, pp. 1195–1202. doi 10.1152/ajpregu.00660.2004CrossRefGoogle Scholar
  126. 126.
    Rinehart, J.P., Robich, R.M., and Denlinger, D.L., 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., 2006, vol. 43, no. 4, pp. 713–722. doi 10.1603/0022-2585(2006)43[713: ECADTI]2.0.CO;2PubMedCrossRefGoogle Scholar
  127. 127.
    Clark, M.S., Fraser, K.P., and Peck, L.S., Antarctic marine mollusks do have an HSP70 heat shock response, Cell Stress Chaperones, 2008, vol. 13, no. 1, pp. 39–49. doi 10.1007/s12192-008-0014-8PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Clarke, A. and Johnston, I.A., Evolution and adaptive radiation of Antarctic fishes, Trends Ecol. Evol., 1996, vol. 11, no. 5, pp. 212–218.PubMedCrossRefGoogle Scholar
  129. 129.
    Somero, G.N. and DeVries, A.L., Temperature tolerance of some Antarctic fishes, Science, 1967, vol. 156, no. 3772, pp. 257–258.PubMedCrossRefGoogle Scholar
  130. 130.
    Petricorena, Z.L. and Somero, G.N., Biochemical adaptations of notothenioid fishes: comparisons between cold temperate South American and New Zealand species and Antarctic species, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 2007, vol. 147, no. 3, pp. 799–807. doi 10.1016/j.cbpa.2006.09.028CrossRefGoogle Scholar
  131. 131.
    Privalov, P.L., Cold denaturation of proteins, Crit. Rev. Biochem. Mol. Biol., 1990, vol. 25, no. 4, pp. 281–305.PubMedCrossRefGoogle Scholar
  132. 132.
    Place, P., Mackenzie, L. and Zippay Hofmann, G., Constitutive roles for inducible genes: evidence for the alteration in expression of the inducible hsp70 gene in Antarctic notothenioid fishes, Am. J. Physiol. Regul. Integr. Comp. Physiol., 2004, vol. 287, no. 2, pp. 429–436. doi 10.1152/ajpregu.00223.2004CrossRefGoogle Scholar
  133. 133.
    Fraser, K.P., Clarke, A., and Peck, L.S., Growth in the slow lane: protein metabolism in the Antarctic limpet Nacella concinna (Strebel 1908), J. Exp. Biol., 2007, vol. 210, no. 15, pp. 2691–2699. doi 10.1242/jeb.003715PubMedCrossRefGoogle Scholar
  134. 134.
    Fraser, K.P. and Rogers, A.D., Protein metabolism in marine animals: the underlying mechanism of growth, Adv. Mar. Biol., 2007, vol. 52, pp. 267–362. doi 10.1016/S0065-2881(06)52003-6PubMedCrossRefGoogle Scholar

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© Pleiades Publishing, Inc. 2017

Authors and Affiliations

  1. 1.Engelhardt Institute of Molecular BiologyRussian Academy of SciencesMoscowRussia

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