Abstract
Land snails are subject to daily and seasonal variations in temperature and in water availability and depend on a range of behavioral and physiological adaptations for coping with problems of maintaining water, ionic, and thermal balance. Heat shock proteins (HSPs) are a multigene family of proteins whose expression is induced by a variety of stress agents. We used experimental desiccation to test whether adaptation to different habitats affects HSP expression in two closely related Sphincterochila snail species, a desiccation-resistant, desert species Sphincterochila zonata, and a Mediterranean-type, desiccation-sensitive species Sphincterochila cariosa. We examined the HSP response in the foot, hepatopancreas, and kidney tissues of snails exposed to normothermic desiccation. Our findings show variations in the HSP response in both timing and magnitude between the two species. The levels of endogenous Hsp72 in S. cariosa were higher in all the examined tissues, and the induction of Hsp72, Hsp74, and Hsp90 developed earlier than in S. zonata. In contrary, the induction of sHSPs (Hsp25 and Hsp30) was more pronounced in S. zonata compared to S. cariosa. Our results suggest that land snails use HSPs as part of their survival strategy during desiccation and as important components of the aestivation mechanism in the transition from activity to dormancy. Our study underscores the distinct strategy of HSP expression in response to desiccation, namely the delayed induction of Hsp70 and Hsp90 together with enhanced induction of sHSPs in the desert-dwelling species, and suggests that evolution in harsh environments will result in selection for reduced Hsp70 expression.
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Adhikari AS, Sridhar Rao K, Rangaraj N, Parnaik VK, Mohan Rao C (2004) Heat stress-induced localization of small heat shock proteins in mouse myoblasts: intranuclear lamin A/C speckles as target for alpha B-crystallin and Hsp25. Exp Cell Res 299:393–403
Alastalo TP, Hellesuo M, Sandqvist A, Hietakangas V, Kallio M, Sistonen L (2003) Formation of nuclear stress granules involves HSF2 and coincides with the nucleolar localization of Hsp70. J Cell Sci 116:3557–3570
Arad Z (2001) Desiccation and rehydration in land snails—a test for distinct set points in Theba pisana. Isr J Zool 47:41–53
Arad Z, Goldenberg S, Heller J (1989) Comparative water economy in five species of Sphincterochila. J Zool (Lond) 218:353–364
Arad Z, Goldenberg S, Heller J (1992) Intraspecific variation in resistance to desiccation and climatic gradients in the distribution of the land snail Xeropicta vestalis. J Zool (Lond) 226:643–656
Arad Z, Goldenberg S, Heller J (1993) Intraspecific variation in resistance to desiccation and climatic gradients in the distribution of the bush-dwelling land snail Trochoidea simulata. J Zool (Lond) 229:249–265
Aufricht C, Ardito T, Thulin G, Kashgarian M, Siegel NJ, Van Why SK (1998) Heat-shock protein 25 induction and redistribution during actin reorganization after renal ischemia. Am J Physiol 274:F215–F222
Beck FX, Neuhofer W, Muller E (2000) Molecular chaperones in the kidney: distribution, putative roles, and regulation. Am J Physiol Renal Physiol 279:F203–F215
Bettencourt BR, Feder ME, Cavicchi S (1999) Experimental evolution of HSP70 expression and thermotolerance in Drosophila melanogaster. Evolution 53:484–492
Boon-Niermeijer EK, Tuyl M, van de Scheur H (1986) Evidence for two states of thermotolerance. Int J Hyperthermia 2:93–105
Boon-Niermeijer EK, Souren JE, Van Wijk R (1987) Thermotolerance induced by 2, 4-dinitrophenol. Int J Hyperthermia 3:133–141
Boon-Niermeijer EK, Souren JE, De Waal AM, Van Wijk R (1988) Thermotolerance induced by heat and ethanol. Int J Hyperthermia 4:211–222
Brooks SP, Storey KB (1995) Evidence for aestivation specific proteins in Otala lactea. Mol Cell Biochem 143:15–20
Bryantsev AL, Loktionova SA, Ilyinskaya OP, Tararak EM, Kampinga HH, Kabakov AE (2002) Distribution, phosphorylation, and activities of Hsp25 in heat-stressed H9c2 myoblasts: a functional link to cytoprotection. Cell Stress Chaperones 7:146–155
Chapple JP, Smerdon GR, Hawkins AJS (1997) Stress-70 protein induction in Mytilus edulis: tissue-specific responses to elevated temperature reflect relative vulnerability and physiological function. J Exp Mar Biol Ecol 217:225–235
Clegg JS, Jackson SA, Warner AH (1994) Extensive intracellular translocations of a major protein accompany anoxia in embryos of Artemia franciscana. Exp Cell Res 212:77–83
Csermely P, Schnaider T, Soti C, Prohaszka Z, Nardai G (1998) The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther 79:129–168
Dasgupta S, Hohman TC, Carper D (1992) Hypertonic stress induces alpha B-crystallin expression. Exp Eye Res 54:461–470
Dastoor Z, Dreyer J (2000) Nuclear translocation and aggregate formation of heat shock cognate protein 70 (Hsc70) in oxidative stress and apoptosis. J Cell Sci 113(Pt 16):2845–2854
Dietz TJ, Somero GN (1992) The threshold induction temperature of the 90-kDa heat shock protein is subject to acclimatization in eurythermal goby fishes (genus Gillichthys). Proc Natl Acad Sci U S A 89:3389–3393
Dong Y, Miller LP, Sanders JG, Somero GN (2008) Heat-shock protein 70 (Hsp70) expression in four limpets of the genus Lottia: interspecific variation in constitutive and inducible synthesis correlates with in situ exposure to heat stress. Biol Bull 215:173–181
Easton DP, Rutledge PS, Spotila JR (1987) Heat shock protein induction and induced thermal tolerance are independent in adult salamanders. J Exp Zool 241:263–267
Edgerly JS, Tadimalla A, Dahlhoff EP (2005) Adaptation to thermal stress in lichen-eating web spinners (Embioptera): habitat choice, domicile construction and the potential role of heat shock proteins. Funct Ecol 19:255–262
Evgen’ev MB, Garbuz DG, Shilova VY, Zatsepina OG (2007) Molecular mechanisms underlying thermal adaptation of xeric animals. J Biosci 32:489–499
Feder ME (1999) Organismal, ecological, and evolutionary aspects of heat-shock proteins and the stress response: established conclusions and unresolved issues. Am Zool 39:857–864
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282
Feder ME, Bedford TB, Albright DR, Michalak P (2002) Evolvability of Hsp70 expression under artificial election for inducible thermotolerance in independent populations of Drosophila melanogaster. Physiol Biochem Zool 75:325–334
Ferreira AS, Totola MR, Kasuya MCM, Araujo EF, Borges AC (2005) Small heat shock proteins in the development of thermotolerance in Pisolithus sp. J Therm Biol 30:595–602
Flanagan SW, Ryan AJ, Gisolfi CV, Moseley PL (1995) Tissue-specific HSP70 response in animals undergoing heat stress. Am J Physiol 268:R28–R32
Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12:842–846
Hayward SA, Rinehart JP, Denlinger DL (2004) Desiccation and rehydration elicit distinct heat shock protein transcript responses in flesh fly pupae. J Exp Biol 207:963–971
Heikkila JJ (2004) Regulation and function of small heat shock protein genes during amphibian development. J Cell Biochem 93:672–680
Hofmann GE, Somero GN (1996) Interspecific variation in thermal denaturation of proteins in the congeneric mussels Mytilus trossulus and M. galloprovincialis: evidence from the heat-shock response and protein ubiquitination. Mar Biol 126:65–75
Jakob U, Gaestel M, Engel K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517–1520
Jiang S, Qiu L, Zhou F, Huang J, Guo Y, Yang K (2009) Molecular cloning and expression analysis of a heat shock protein (Hsp90) gene from black tiger shrimp (Penaeus monodon). Mol Biol Rep 36:127–134
King YT, Lin CS, Lin JH, Lee WC (2002) Whole-body hyperthermia-induced thermotolerance is associated with the induction of heat shock protein 70 in mice. J Exp Biol 205:273–278
Krebs RA, Feder ME (1997a) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2:60–71
Krebs RA, Feder ME (1997b) Tissue-specific variation in Hsp70 expression and thermal damage in Drosophila melanogaster larvae. J Exp Biol 200:2007–2015
Lavoie JN, Gingras-Breton G, Tanguay RM, Landry J (1993) Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock. HSP27 stabilization of the microfilament organization. J Biol Chem 268:3420–3429
Lee S, Owen HA, Prochaska DJ, Barnum SR (2000) HSP16.6 is involved in the development of thermotolerance and thylakoid stability in the unicellular cyanobacterium, Synechocystis sp. PCC 6803. Curr Microbiol 40:283–287
Lerman DN, Michalak P, Helin AB, Bettencourt BR, Feder ME (2003) Modification of heat-shock gene expression in Drosophila melanogaster populations via transposable elements. Mol Biol Evol 20:135–144
Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191
Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631–677
Lopez-Martinez G, Benoit JB, Rinehart JP, Elnitsky MA, Lee RE Jr, Denlinger DL (2009) Dehydration, rehydration, and overhydration alter patterns of gene expression in the Antarctic midge, Belgica antarctica. J Comp Physiol B 179:481–491
Machin J (1967) Structural adaptation for reducing water-loss in three species of terrestrial snails. J Zool Lond 152:55–65
Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684
Mehlen P, Preville X, Chareyron P, Briolay J, Klemenz R, Arrigo AP (1995) Constitutive expression of human hsp27, Drosophila hsp27, or human alpha B-crystallin confers resistance to TNF- and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts. J Immunol 154:363–374
Mirkes PE, Little SA, Cornel L, Welsh MJ, Laney TN, Wright FH (1996) Induction of heat shock protein 27 in rat embryos exposed to hyperthermia. Mol Reprod Dev 45:276–284
Morrow G, Heikkila JJ, Tanguay RM (2006) Differences in the chaperone-like activities of the four main small heat shock proteins of Drosophila melanogaster. Cell Stress Chaperones 11:51–60
Moseley PL (1997) Heat shock proteins and heat adaptation of the whole organism. J Appl Physiol 83:1413–1417
Mulligan-Tuttle A, Heikkila JJ (2007) Expression of the small heat shock protein gene, hsp30, in Rana catesbeiana fibroblasts. Comp Biochem Physiol A Mol Integr Physiol 148:308–316
Nakano K, Iwama G (2002) The 70-kDa heat shock protein response in two intertidal sculpins, Oligocottus maculosus and O. snyderi: relationship of hsp70 and thermal tolerance. Comp Biochem Physiol A Mol Integr Physiol 133:79–94
Neuhofer W, Muller E, Burger-Kentischer A, Beck FX (1998) Hypertonicity affects heat shock protein 27 and F-actin localization in Madin-Darby canine kidney cells. Kidney Int Suppl 67:S165–S167
Neuhofer W, Fraek ML, Ouyang N, Beck FX (2005) Differential expression of heat shock protein 27 and 70 in renal papillary collecting duct and interstitial cells—implications for urea resistance. J Physiol 564:715–722
Nollen EA, Brunsting JF, Roelofsen H, Weber LA, Kampinga HH (1999) In vivo chaperone activity of heat shock protein 70 and thermotolerance. Mol Cell Biol 19:2069–2079
Norris CE, diIorio PJ, Schultz RJ, Hightower LE (1995) Variation in heat shock proteins within tropical and desert species of poeciliid fishes. Mol Biol Evol 12:1048–1062
Norris CE, Brown MA, Hickey E, Weber LA, Hightower LE (1997) Low-molecular-weight heat shock proteins in a desert fish (Poeciliopsis lucida): homologs of human Hsp27 and Xenopus Hsp30. Mol Biol Evol 14:1050–1061
Ohno A, Muller E, Fraek ML, Thurau K, Beck F (1997) Solute composition and heat shock proteins in rat renal medulla. Pflugers Arch 434:117–122
Pakay JL, Withers PC, Hobbs AA, Guppy M (2002) In vivo downregulation of protein synthesis in the snail Helix aspersa during estivation. Am J Physiol Regul Integr Comp Physiol 283:R197–204
Parcellier A, Schmitt E, Brunet M, Hammann A, Solary E, Garrido C (2005) Small heat shock proteins HSP27 and alpha B-crystallin: cytoprotective and oncogenic functions. Antioxid Redox Signal 7:404–413
Pratt WB, Toft DO (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med (Maywood) 228:111–133
Ramirez V, Uribe N, Garcia-Torres R, Castro C, Rubio J, Gamba G, Bobadilla NA (2004) Upregulation and intrarenal redistribution of heat shock proteins 90alpha and 90beta by low-sodium diet in the rat. Cell Stress Chaperones 9:198–206
Ramnanan CJ, Groom AG, Storey KB (2007) Akt and its downstream targets play key roles in mediating dormancy in land snails. Comp Biochem Physiol B Biochem Mol Biol 148:245–255
Ramnanan CJ, Allan ME, Groom AG, Storey KB (2009) Regulation of global protein translation and protein degradation in aerobic dormancy. Mol Cell Biochem 323:9–20
Ravindran RK, Tablin F, Crowe JH, Oliver AE (2005) Resistance to dehydration damage in hela cells correlates with the presence of endogenous heat shock proteins. Cell Preserv Technol 3:155–164
Riddle WA (1983) Physiological ecology of land snails and slugs. In: Russell-Hunter WD (ed) The Mollusca, vol 6. Academic, London, pp 431–461
Rollet E, Lavoie JN, Landry J, Tanguay RM (1992) Expression of Drosophila’s 27 kDa heat shock protein into rodent cells confers thermal resistance. Biochem Biophys Res Commun 185:116–120
Sanders BM, Hope C, Pascoe VM, Martin LS (1991) Characterization of the stress protein response in two species of Collisella limpets with different temperature tolerances. Physiol Zool 64:1471–1489
Schill RO, Steinbruck GH, Kohler HR (2004) Stress gene (hsp70) sequences and quantitative expression in Milnesium tardigradum (Tardigrada) during active and cryptobiotic stages. J Exp Biol 207:1607–1613
Schmidt-Nielsen K, Taylor CR, Shkolnik A (1971) Desert snails: problems of heat, water and food. J Exp Biol 55:385–398
Schmidt-Nielsen K, Taylor CR, Shkolnik A (1972) Desert snail: problems of survival. Symp Zool Soc Lond 31:1–13
Schober A, Muller E, Thurau K, Beck FX (1997) The response of heat shock proteins 25 and 72 to ischaemia in different kidney zones. Pflugers Arch 434:292–299
Scott MA, Locke M, Buck LT (2003) Tissue-specific expression of inducible and constitutive Hsp70 isoforms in the western painted turtle. J Exp Biol 206:303–311
Shabtay A, Arad Z (2005) Ectothermy and endothermy: evolutionary perspectives of thermoprotection by HSPs. J Exp Biol 208:2773–2781
Shilova VY, Garbuz DG, Evgen’ev MB, Zatsepina OG (2006) Small heat shock proteins and adaptation of various Drosophila species to hyperthermia. Mol Biol 40:235–239
Smith BJ, Yaffe MP (1991) Uncoupling thermotolerance from the induction of heat shock proteins. Proc Natl Acad Sci U S A 88:11091–11094
Somero GN (1995) Proteins and temperature. Annu Rev Physiol 57:43–68
Sorensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037
Sorte CJB, Hofmann GE (2005) Thermotolerance and heat-shock protein expression in Northeastern Pacific Nucella species with different biogeographical ranges. Mar Biol 146:985–993
Storey KB (2002) Life in the slow lane: molecular mechanisms of estivation. Comp Biochem Physiol A Mol Integr Physiol 133:733–754
Storey KB, Storey JM (1990) Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. Q Rev Biol 65:145–174
Tammariello SP, Rinehart JP, Denlinger DL (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 45:933–938
Tomanek L, Somero GN (1999) Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography. J Exp Biol 202:2925–2936
Tomanek L, Somero GN (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 Tegula): implications for regulation of hsp gene expression. J Exp Biol 205:677–685
Torok Z, Goloubinoff P, Horvath I, Tsvetkova NM, Glatz A, Balogh G, Varvasovszki V, Los DA, Vierling E, Crowe JH, Vigh L (2001) Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proc Natl Acad Sci U S A 98:3098–3103
Ulmasov HA, Karaev KK, Lyashko VN, Evgen’ev MB (1993) Heat-shock response in camel (Camelus dromedarius) blood cells and adaptation to hyperthermia. Comp Biochem Physiol B 106:867–872
Widelitz RB, Magun BE, Gerner EW (1986) Effects of cycloheximide on thermotolerance expression, heat shock protein synthesis, and heat shock protein mRNA accumulation in rat fibroblasts. Mol Cell Biol 6:1088–1094
Zatsepina OG, Ulmasov KA, Beresten SF, Molodtsov VB, Rybtsov SA, Evgen’ev MB (2000) Thermotolerant desert lizards characteristically differ in terms of heat-shock system regulation. J Exp Biol 203:1017–1025
Zatsepina OG, Velikodvorskaia VV, Molodtsov VB, Garbuz D, Lerman DN, Bettencourt BR, Feder ME, Evgenev MB (2001) A Drosophila melanogaster strain from sub-equatorial Africa has exceptional thermotolerance but decreased Hsp70 expression. J Exp Biol 204:1869–1881
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We thank Dr. Ariel Shabtay for his comments. This work was supported by the Israel Science Foundation grant no. 1125/07.
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Mizrahi, T., Heller, J., Goldenberg, S. et al. Heat shock proteins and resistance to desiccation in congeneric land snails. Cell Stress and Chaperones 15, 351–363 (2010). https://doi.org/10.1007/s12192-009-0150-9
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DOI: https://doi.org/10.1007/s12192-009-0150-9