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Molecular mechanisms underlying thermal adaptation of xeric animals

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Abstract

For many years, we and our collaborators have investigated the adaptive role of heat shock proteins in different animals, including the representatives of homothermic and poikilothermic species that inhabit regions with contrasting thermal conditions. Adaptive evolution of the response to hyperthermia has led to different results depending upon the species. The thermal threshold of induction of heat shock proteins in desert thermophylic species is, as a rule, higher than in the species from less extreme climates. In addition, thermoresistant poikilothermic species often exhibit a certain level of heat shock proteins in cells even at a physiologically normal temperature. Furthermore, there is often a positive correlation between the characteristic temperature of the ecological niche of a given species and the amount of Hsp70-like proteins in the cells at normal temperature. Although in most cases adaptation to hyperthermia occurs without changes in the number of heat shock genes, these genes can be amplified in some xeric species. It was shown that mobile genetic elements may play an important role in the evolution and fine-tuning of the heat shock response system, and can be used for direct introduction of mutations in the promoter regions of these genes.

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References

  • Belikov S V and Karpov V L 1996 Mapping Protein-DNA Interaction with CIS-DDP: Chromatine Structure of Promoter Region of Hsp70 Gene; Biochem. Mol. Biol. Int. 38 997–1002

    PubMed  CAS  Google Scholar 

  • Bettencourt B R and Feder M E 2002 Rapid concerted evolution via gene conversion at the Hsp70 genes; J. Mol. Evol. 54 569–586

    Article  PubMed  CAS  Google Scholar 

  • Buckley B A and Hofmann G E 2002 Thermal acclimation changes DNA-binding activity of heat shock factor 1 (HSF1) in the goby: implications for plasticity in the heat-shock response in natural populations; J. Exp. Biol. 205 3231–3240

    PubMed  CAS  Google Scholar 

  • Diamant S, Eliahu N, Rosenthal D and Goloubinoff P 2001 Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat sresses; J. Biol. Chem. 276 39586–39591

    Article  PubMed  CAS  Google Scholar 

  • Duncan R F 2005 Inhibition of Hsp90 function delays and impairs recovery from heat shock; FEBS J. 272 5244–5256

    Article  PubMed  CAS  Google Scholar 

  • Evgen’ev M B, Kolchinski A, Levin A, Preobrazhenskaya A L and Sarkisova E 1978 Heat-shock DNA homology in distantly related species of Drosophila; Chromosoma 68 357–365

    Article  PubMed  CAS  Google Scholar 

  • Evgen’ev M B, Sheinker V S and Levin A V, et al 1987 Molecular Mechanisms of Adaptation to Hyperthermia in Higher Organisms. Synthesis of Heat-Shock Proteins in Cell Cultures and Larvae of Certain Silkworm Species; Mol. Biol. 21 484–494

    CAS  Google Scholar 

  • Evgen’ev M B, Zatsepina O G, Garbuz D G, Lerman D, Velikodvorskaya V, Zelentsova E and Feder M E 2004 Evolution and arrangement of the Hsp70 gene cluster in two closely related species of the virilis group of Drosophila; Chromosoma 113 223–232

    Article  PubMed  CAS  Google Scholar 

  • Evgen’ev M B, Garbuz D G, Zatsepina O G 2005 Heat shock proteins: functions and role in adaptation to hyperthermia; Ontogenez (Rus.) 36 265–273

    CAS  Google Scholar 

  • Feder M E and Hofmann G E 1998 Evolutionary and ecological physiology of heat-shock proteins and the heat-shock response: A comprehensive bibliography; Suppl. Annu. Rev. Physiol. 61 http://www.annurev.arg/sup/material.htm

  • Feder M E and Hofmann G E 1999 Heat-Shock Proteins, Molecular Chaperones, and the Stress Response, Evolutionary and Ecological Phisiology; Annu. Rev. Physiol. 61 243–282

    Article  PubMed  CAS  Google Scholar 

  • Fujikake N, Nagai Y, Popiel H A, Kano H, Yamaguchi M and Toda T 2005 Alternative splicing regulates the transcriptional activity of heat shock factor in response to heat/cold stress; FEBS Lett. 579 3842–3848

    Article  PubMed  CAS  Google Scholar 

  • Garbuz D G, Molodtsov V B, Velikodvorskaya V V, Evgen’ev M B and Zatsepina O G 2002 Evolution of the response to heat shock in genus; Genetika (Rus.) 38 1097–1109

    CAS  Google Scholar 

  • Garbuz D G, Evgenev M B, Feder M E and Zatsepina O G 2003 Evolution of thermotolerance and the heat-shock response: evidence from inter/intraspecific comparison and interspecific hybridization in the species group of I. Thermal phenotype; J. Exp. Biol. 206 2399–2408

    Article  PubMed  CAS  Google Scholar 

  • Gehring W J and Wehner R 1995 Heat shock protein synthesis and thermotolerance in, an ant from the Sahara desert; Proc. Natl. Acad. Sci. USA 92 2994–2998

    Article  PubMed  CAS  Google Scholar 

  • Gong W J and Golic K G 2006 Loss of Hsp70 in is pleiotropic, with effects on thermotolerance, recovery from heat shock and neurodegeneration; Proc. Natl. Acad. Sci. USA 172 275–286

    CAS  Google Scholar 

  • Ish-Horowicz D S, Pinchin J, Gausz H, Gyurkovics G and Bencze G et al 1979 Deletion mapping of two loci that code for the 70,000 dalton heat-induced protein; Cell 17 565–571

    Article  PubMed  CAS  Google Scholar 

  • Krebs RA and Feder M E 1997 Deleterious consequences of Hsp70 overexpression in larvae; Cell Stress Chaperones 2 60–71

    Article  PubMed  CAS  Google Scholar 

  • Lakhotia S C and Prasanth K V 2002 Tissue-and development-specific induction and turnover of Hsp70 transcripts from loci 87A and 87C after heat shock and during recovery in Drosophila melanogaster; J. Exp. Biol. 205 345–358

    PubMed  CAS  Google Scholar 

  • Lebedeva L A, Nabirochkina E N, Kurshakova M M, Flavie R, Krasnov A N, Evgen’ev M B, Kadonaga J T, Georgieva S G and La’szlo’ Tora 2005 Occupancy of the Hsp70 promoter by a subset of basal transcription factors diminishes upon transcriptional activation; Proc. Natl. Acad. Sci. USA 102 18087–18092

    Article  PubMed  CAS  Google Scholar 

  • Leigh Brown A J and Ish-Horowicz D 1981 Evolution of the 87A and 87C heat-shock loci in Drosophila; Nature (London) 290 677–682

    Article  CAS  Google Scholar 

  • Lerman D N, Michalak P, Helin A B, Bettencourt B R and Feder M E 2003 Modification of Heat-Shock Gene Expression in Populations via Transposable Elements; Mol. Biol. Evol. 20 135–144

    Article  PubMed  CAS  Google Scholar 

  • Lewis M J, Helmsing P and Ashburner M 1975 Parallel changes in puffing activity and patterns of protein synthesis in salivary glands of Drosophila; Proc. Natl. Acad. Sci. USA 72 3604–36608

    Article  PubMed  CAS  Google Scholar 

  • Lindquist S 1986 The heat-shock response; Annu. Rev. Biochem. 55 1151–1191

    Article  PubMed  CAS  Google Scholar 

  • Lindquist S and Kim G 1996 Heat-shock protein 104 expression is sufficient for thermotolerance in yeast; Proc. Natl. Acad. Sci. USA 93 5301–5306

    Article  PubMed  CAS  Google Scholar 

  • Lozovskaya E R and Evgen’ev M B 1984 Heat Shock in and Regulation of Genome Activity; Mol. Bio. (Russian) 20 142–185

    Google Scholar 

  • Lyashko V N, Vikulova V K, Chernicov V G, Ivanov V I, Ulmasov K A, Zatsepina O G and Evgen’ev M B 1994 Comparison of the heat shock response in ethnically and ecologically different human populations; Proc. Natl. Acad. Sci. USA 91 12492–12495

    Article  PubMed  CAS  Google Scholar 

  • Margulis B A and Guzhova I V 2000 Stress Proteins in Eukaryotic Cell; Cytology (Russian) 42 323–342

    CAS  Google Scholar 

  • Morimoto R J, Jolly C, Satyal S, Mathew A, Shi Y and Kitagawa K 1999 Molecular chaperones and the heat shock response; Br. J. Cancer 80 S19

    Google Scholar 

  • Morrow G, Heikkila J J and Tanguay RM 2006 Differences in the chaperone-like activities of the four main small heat shock proteins of; Cell Stress Chaperones 11 51–60

    Article  PubMed  CAS  Google Scholar 

  • Neal S J, Karunanithy S, Best A, Ken-Choy-So A, Tanguay R M, Atwood H L and Westwood J T 2005 Thermoprotection of synaptic transmission in a heat shock factor mutant is accompanied by increased expression of Hsp83 and DnaJ-1; Physiol. Genomics 25 493–501

    Google Scholar 

  • Norris C E, diTorio P J, Schultz R J and Hightower L 1995 Variation in heat shock proteins within tropical and desert species of poeciliid fishes; Mol. Biol. Evol. 12 1048–1062

    PubMed  CAS  Google Scholar 

  • Podrabsky J E and Somero G N 2004 Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish; J. Exp. Biol. 207 2237–2254

    Article  PubMed  CAS  Google Scholar 

  • Rinehart J P, Hayward S A, Elnitsky M A, Sandro L H, Lee R E Jr and Denlinger D L. 2006 Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect; Proc. Natl. Acad. Sci. USA 38 14223–14227

    Article  Google Scholar 

  • Schlesinger M J et al (eds) 1982 Heat Shock: from bacteria to man; (New York: Cold Spring Harbor Lab) pp 440

    Google Scholar 

  • Shilova V Y, Garbuz D G, Myasyankina E N, Chen B, Evgen’ev M B, Feder M E and Zatsepina O G 2006 Remarkable site specificity of local transposition into the Hsp70 promoter of Drosophila melanogaster; Genetics 173 809–820

    Article  PubMed  CAS  Google Scholar 

  • Sorensen J G, Dahlgaard J and Loeschke V 2001 Genetic variation in thermal tolerance among natural populations of Drosophila buzzatii: down regulation of Hsp70 expression and variation in heat stress resistance traits; Funct. Ecol. 15 289–296

    Article  Google Scholar 

  • Sorensen J G, Kristensen T N and Loeschke V 2003 The evolutionary and ecological role of heat shock proteins; Ecol. Lett. 6 1025–1037

    Article  Google Scholar 

  • Tissieres A, Mitchel H K and Tracy U 1974 Protein synthesis in salivary glands of relation to chromosome puffs; J. Mol. Biol. 84 389–398

    Article  PubMed  CAS  Google Scholar 

  • Timakov B, Liu X, Turgut I and Zhang P 2002 Timing and Targeting of P-Element Local Transposition in the Male Germline Cells of Drosophila melanogaster; Genetics 160 1011–1022

    PubMed  CAS  Google Scholar 

  • Tomanek L 2005 Two-dimensional gel analysis of the heat-shock response in marine snails (genus): interspecific variation in protein expression and acclimation ability; J. Exp. Biol. 208 3133–3143

    Article  PubMed  CAS  Google Scholar 

  • Tomanek L and Somero G N 1999 Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus) from different thermal habitats: implications for limits of thermotolerance and biogeography; J. Exp. Biol. 202 2925–2936

    PubMed  Google Scholar 

  • Tomanek L and Somero G N 2002 Interspecific-and acclimation-induced variation in levels of heat-shock proteins 70 (Hsp70) and 90 (Hsp90) and heat-shock transcription factor-1 (HSF1) in congeneric marine snails (genus): implications for regulations of Hsp gene expression; J. Exp. Biol. 205 677–685

    PubMed  CAS  Google Scholar 

  • Udvardy A, Maine E and Schedl P 1985 The 87A7 chromomere. Identification of novel chromatin structures flanking the heat shock locus that may define the boundaries of higher order domains; J. Mol. Biol. 185 341–358

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov K A, Ovezmukhammedov A, Karaev K K and Evgen’ev M B 1988 Molecular Mechanisms of Adaptation to Hypothermia in Higher Organisms. 3. Induction of Heat Shock Proteins in Two Species; Mol. Biol. (Russian) 22 1583–1589

    CAS  Google Scholar 

  • Ulmasov KA, Shammakov S, Karavaev K and Evgen’ev M B 1992 Heat shock proteins and thermoresistance in lizards; Proc. Natl. Acad. Sci. USA 89 1666–1670

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov H A, Karaev K K, Lyashko V N and Evgen’ev M B 1993 Heat-shock response in camel 0 blood cells and adaptation to hyperthermia; Comp. Biochem. Physiol. 106 867–872

    Article  CAS  Google Scholar 

  • Ulmasov K A, Zatsepina O G, Molodtsov V B and Evgen’ev M B 1999 Natural body temperature and kinetics of heat shock protein synthesis in the toad-heated agamid lizard; Amphibia-Reptilia 20 1–9

    Article  Google Scholar 

  • Walser J C, Chen B and Feder M E 2006 Heat-Shock Promoters: Targets for Evolution by P Transposable Elements in; PLoS Genet 2 (in press)

  • Wu C 1995 Heat Shock Transcription Factors: Structure and Regulation; Annu. Rev. Cell. Dev. Biol. 11 441–469

    Article  PubMed  CAS  Google Scholar 

  • Zatsepina O G, Ulmasov K A, Beresten S F et al 2000 Thermotolerant desert lizards characteristically differ in terms of heat-shock system regulation; J. Exp. Biol. 203 1017–1025

    PubMed  CAS  Google Scholar 

  • Zatsepina O G, Velikodvorskaia V V, Molodtsov V B, Garbuz D G, Lerman D N, Bettencourt B R, Feder M E and Evgenev M B 2001 A strain from sub-equatorial Africa has exceptional thermotolerance but decreased Hsp70 expression; J. Exp. Biol. 204 1869–1881

    PubMed  CAS  Google Scholar 

  • Zatsepina O G, Karavanov A A, Garbuz D G, Shilova V, Tornatore P and Evgen’ev M B 2005 Use of surface-enhanced laser desorption ionization-time-of-flight to identify heat shock protein 70 isoforms in closely related species of the virilis group of Drosophila; Cell Stress Chaperones 10 12–16

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Vavilov Street 32, Moscow, 199991, Russia

    M B Evgen’ev, D G Garbuz, V Y Shilova & O G Zatsepina

  2. Institute of Cell Biophysics, Russian Academy of Sciences, Pushchino, Moscow Region, 142292, Russia

    M B Evgen’ev

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  1. M B Evgen’ev
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  2. D G Garbuz
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  3. V Y Shilova
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  4. O G Zatsepina
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Correspondence to M B Evgen’ev.

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Evgen’ev, M.B., Garbuz, D.G., Shilova, V.Y. et al. Molecular mechanisms underlying thermal adaptation of xeric animals. J Biosci 32, 489–499 (2007). https://doi.org/10.1007/s12038-007-0048-6

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