Application of heat shock protein expression for detecting natural adaptation and exposure to stress in natural populations

Current Zoology

Volumn 56, Issue 6, 2010, Pages 703-713

  Sørensen, Jesper Givskov ^a  

^a AARHUS UNIVERSITY   (Denmark)

Author keywords

Biomarker; Hsp; Molecular chaperone; Thermal adaptation; Thermal stress

Indexed keywords

EID: 78649409939     PISSN: 16745507     EISSN: None     Source Type: Journal    
DOI: 10.1093/czoolo/56.6.703     Document Type: Article

References (95)

1. Arriero E, Moreno J, Merino S, Martinez J, 2008. Habitat effects on physiological stress response in nestling blue tits are mediated through parasitism. Physiol. Biochem. Zool. 81: 195-203.
2. Asea A, 2007. Mechanisms of HSP72 release. J. Biosciences 32: 579-584.
3. Ayroles JF, Carbone MA, Stone EA, Jordan KW, Lyman RF et al., 2009. Systems genetics of complex traits in Drosophila melanogaster. Nat. Genet. 41: 299-307.
4. Bahrndorff S, Mariën J, Loeschcke V, Ellers J, 2009. Dynamics of heat-induced thermal stress resistance and hsp70 expression in the springtail Orchesella cincta. Funct. Ecol. 23: 233-239.
5. Basu N, Todgham AE, Ackerman PA, Bibeau MR, Nakano K et al., 2002. Heat shock protein genes and their functional significance in fish. Gene 295: 173-183.
6. Bijlsma R, Loeschcke V, 1997. Environmental Stress, Adaptation and Evolution. Basel: Birkhäuser Verlag.
7. Blanco G, Frias O, Martinez J, Lemus JA, Merino R et al., 2006. Sex and rank in competitive brood hierarchies influence stress levels in nestlings of a sexually dimorphic bird. Biol. J. Linn. Soc. 88: 383-390.
8. Chown SL, Jumbam KR, Sørensen JG, Terblanche JS, 2009. Phenotypic variance, plasticity and heritability estimates of critical thermal limits depend on methodological context. Funct. Ecol. 23: 133-140.
9. Collier RJ, Collier JL, Rhoads RP, Baumgard LH, 2008. Genes involved in the bovine heat stress response. J. Dairy Sci. 91: 445-454.
10. David JR, Araripe LO, Chakir M, Legout H, Lemos B et al., 2005. Male sterility at extreme temperatures: A significant but neglected phenomenon for understanding Drosophila climatic adaptations. J. Evolution. Biol. 18: 838-846.
11. Delaney MA, Klesius PH, 2004. Hypoxic conditions induce Hsp70 production in blood, brain and head kidney of juvenile Nile tilapia Oreochromis niloticus (L.). Aquaculture 236: 633-644.
12. Dyer SD, Brooks GL, Dickson KL, Sanders BM, Zimmerman EG, 1993. Synthesis and accumulation of stress proteins in tissues of arsenite-exposed fathead minnows Pimephales promelas. Environ. Toxicol. Chem. 12: 913-924.
13. Evgen'ev MB, Garbuz DG, Shilova VY, Zatsepina OG, 2007. Molecular mechanisms underlying thermal adaptation of xeric animals. J. Biosciences 32: 489-499.
14. Fader SC, Yu Z, Spotila JR, 1994. Seasonal variation in heat shock proteins (hsp70) in stream fish under natural conditions. J. Therm. Biol. 19: 335-341.
15. Fasolo AG, Krebs RA, 2004. A comparison of behavioural change in Drosophila during exposure to thermal stress. Biol. J. Linn. Soc. 83: 197-205.
16. Feder ME, Blair N, Figueras H, 1997. Natural thermal stress and heat-shock protein expression in Drosophila larvae and pupae. Funct. Ecol. 11: 90-100.
17. Feder ME, Hofmann GE, 1999. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annu. Rev. Physiol. 61: 243-282.
18. Feder ME, Walser J-C, 2005. The biological limitations of transcriptomics in elucidating stress and stress responses. J. Evolution. Biol. 18: 901-910.
19. Ferguson IB, Snelgar W, Lay Yee M, Watkins CB, Bowen JH, 1998. Expression of heat shock protein genes in apple fruit in the field. Aust. J. Plant Physiol. 25: 155-163.
20. Fleshner M, Campisi J, Amiri L, Diamond DM, 2004. Cat exposure induces both intra- and extracellular Hsp72: The role of adrenal hormones. Psychoneuroendocrino. 29: 1142-1152.
21. Fonager J, Beedholm R, Clark BFC, Rattan SIS, 2002. Mild stress-induced stimulation of heat-shock protein synthesis and improved functional ability of human fibroblasts undergoing aging in vitro. Exp. Gerontol. 37: 1223-1228.
22. Frydenberg J, Hoffmann AA, Loeschcke V, 2003. DNA sequence variation and latitudinal associations in hsp23, hsp26 and hsp27 from natural populations of Drosophila melanogaster. Mol. Ecol. 12: 2025-2032.
23. Gehring WJ, Wehner R, 1995. Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert. P. Natl. Acad. Sci. USA 92: 2994-2998.
24. Gregersen N, Bolund L, Bross P, 2003. Protein misfolding, aggregation and degradation in disease. 232: 3-16.
25. Grime JP, 1979. Plant Strategies and Vegetation Processes. Chichester: John Wiley.
26. Heckmann LH, Baas J, Jager T, 2010. Time is of the essence. Environ. Toxicol. Chem. 29: 1396-1398.
27. Hemmer-Hansen J, Nielsen EE, Frydenberg J, Loeschcke V, 2007. Adaptive divergence in a high gene flow environment: Hsc70 variation in the European flounder (Platichthys flesus L.). Heredity 99: 592-600.
28. Herring G, Gawlik DE, 2007. The role of stress proteins in the study of allostatic overload in birds: Use and applicability to current studies in avian ecology. TheScientificWorldJo. 7: 1596-1602.
29. Herring G, Gawlik DE, Rumbold DG, 2009. Feather mercury concentrations and physiological condition of great egret and white ibis nestlings in the Florida Everglades. Sci. Total Environ. 407: 2641-2649.
30. Hoffmann AA, Parsons PA, 1991. Evolutionary Genetics and Environmental Stress. New York: Oxford University Press.
31. Hoffmann AA, Sørensen JG, Loeschcke V, 2003. Adaptation of Drosophila to temperature extremes: Bringing together quantitative and molecular approaches. J. Therm. Biol. 28: 175-216.
32. Hofmann GE, Somero GN, 1995. Evidence for protein damage at environmental temperatures: Seasonal changes in levels of ubiquitin conjugates and Hsp70 in the intertidal mussel Mytilus trossulus. J. Exp. Biol. 198: 1509-1518.
33. Holmstrup M, Overgaard J, Bindesbøl AM, Pertoldi C, Bayley M, 2007. Adaptations to overwintering in the earthworm Dendrobaena octaedra: Genetic differences in glucose mobilisation and freeze tolerance. Soil Biol. Biochem. 39: 2640-2650.
34. Iwama GK, Afonso LOB, Todgham A, Ackerman P, Nakano K, 2004. Are hsps suitable for indicating stressed states in fish? J. Exp. Biol. 207: 15-19.
35. Jedlicka P, Mortin MA, Wu C, 1997. Multiple functions of Drosophila heat shock transcription factor in vivo. Embo J. 16: 2452-2462.
36. Jensen LT, Cockerell FE, Kristensen TN, Rako L, Loeschcke V et al., 2009. Adult heat tolerance variation in Drosophila melanogaster is not related to Hsp70 expression. J. Exp. Zool. Part A 313: 35-44.
37. Johnson TK, Cockerell FE, Carrington LB, Rako L, Hoffmann AA et al., 2009. The capacity of Drosophila to heat harden associates with low rates of heat-shocked protein synthesis. J. Therm. Biol. 34: 327-331.
38. Jørgensen KT, Sørensen JG, Bundgaard J, 2006. Heat tolerance and the effect of mild heat stress on reproductive characters in Drosophila buzzatii males. J. Therm. Biol. 31: 280-286.
39. Kalmar B, Greensmith L, 2009. Induction of heat shock proteins for protection against oxidative stress. Adv. Drug Deliver. Rev. 61: 310-318.
40. Kelty JD, Lee RE, 1999. Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster. J. Insect Physiol. 45: 719-726.
41. Köhler HR, Zanger M, Eckwert H, Einfeldt I, 2000. Selection favours low Hsp70 levels in chronically metal-stressed soil arthropods. J. Evolution. Biol. 13: 569-582.
42. Koorsloot A, van Gestel CAM, van Straalen NM, 2004. Environmental Stress and Cellular Response in Artropods. Boca Ratton, Florida: CRC Press.
43. Koštál V, Berková P, Šimek P, 2003. Remodelling of membrane phospholipids during transition to diapause and cold-acclimation in the larvae of Chymomyza costata (Drosophilidae). Comp. Biochem. Phys. B 135: 407-419.
44. Koštál V, Tollarová-Borovanská M, 2009. The 70 kDa heat shock protein assists during the repair of chilling injury in the insect Pyrrhocoris apterus. PLoS ONE 4: e4546. doi:4510.1371/ journal.pone.0004546.
45. Krebs RA, Thompson KA, 2006. Direct and correlated effects of selection on flight after exposure to thermal stress in Drosophila melanogaster. Genetica 128: 217-225.
46. Kristensen TN, Hoffmann AA, Overgaard J, Sørensen JG, Hallas R et al., 2008. Costs and benefits of cold acclimation in field-released Drosophila. P. Natl. Acad. Sci. USA 105: 216-221.
47. Kristensen TN, Løvendahl P, 2006. Physiological responses to heat stress and their potential use as indicators of reduced welfare in Jersey calves. Acta Zool. Sinica 52: 681-689.
48. Kristensen TN, Løvendahl P, Berg P, Loeschcke V, 2004. Hsp72 is present in plasma from Holstein-Friesian dairy cattle, and the concentration level is repeatable across days and age classes. Cell Stress Chaperon. 9: 143-149.
49. Lakhotia SC, Prasanth KV, 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.
50. Leemans R, Egger B, Loop T, Kammermeier L, Haiqiong H et al., 2000. Quantitative transcript imaging in normal and heat-shocked Drosophila embryos by using high-density oligonucleotide arrays. P. Natl. Acad. Sci. USA 97: 12138-12143.
51. Lindquist S, Craig EA, 1988. The heat-shock proteins. Annu. Rev. Genet. 22: 631-677.
52. Lindquist SL, 1986. The heat-shock response. Annu. Rev. Biochem. 55: 1151-1191.
53. Malmendal A, Overgaard J, Bundy JG, Sørensen JG, Nielsen NC et al., 2006. Metabolomic profiling of heat stress: Hardening and recovery of homeostasis in Drosophila. Am. J. Physiol.-Reg I 291: R205-R212.
54. Martinez-Padilla J, Martinez J, Davila JA, Merino S, Moreno J et al., 2004. Within-brood size differences, sex and parasites determine blood stress protein levels in Eurasian Kestrel nestlings. Funct. Ecol. 18: 426-434.
55. Matzkin LM, Markow TA, 2009. Transcriptional regulation of metabolism associated with the increased desiccation resistance of the cactophilic Drosophila mojavensis. Genetics 182: 1279-1288.
56. McMillan DM, Fearnley SL, Rank NE, Dahlhoff EP, 2005. Natural temperature variation affects larval survival, development and Hsp70 expression in a leaf beetle. Funct. Ecol. 19: 844-852.
57. Minier C, Borghi V, Moore MN, Porte C, 2000. Seasonal variation of MXR and stress proteins in the common mussel Mytilus galloprovincialis. Aquat. Toxicol. 50: 167-176.
58. Morales J, Moreno J, Lobato E, Merino S, Tomas G et al., 2006. Higher stress protein levels are associated with lower humoral and cell-mediated immune responses in pied flycatcher females. Funct. Ecol. 20: 647-655.
59. Morgan TJ, Mackay TFC, 2006. Quantitative trait loci for thermotolerance phenotypes in Drosophila melanogaster. Heredity 96: 232-242.
60. Morimoto RI, Jolly C, Satyal S, Mathew A, Shi Y et al., 1999. Molecular chaperones and the heat shock response. Brit. J. Cancer 80: S18.
61. Nguyen HT, Joshi CP, Klueva N, Weng J, Hendershot KL et al., 1994. The heat-shock response and expression of heat-shock proteins in wheat under diurnal heat stress and field conditions. Aust. J. Plant Physiol. 21: 857-867.
62. Nielsen MM, Overgaard J, Sørensen JG, Holmstrup M, Justesen J et al., 2005. Role of HSF activation for resistance to heat, cold and high-temperature knock-down. J. Insect Physiol. 51: 1320-1329.
63. Nielsen MM, Sørensen JG, Kruhøffer M, Justesen J, Loeschcke V, 2006. Phototransduction genes are upregulated in a global gene expression study of Drosophila melanogaster selected for heat resistance. Cell Stress Chaperon. 11: 325-333.
64. Ohtsu T, Kimura MT, Katagiri C, 1998. How Drosophila species acquire cold tolerance-qualitative changes of phospholipids. Eur. J. Biochem. 252: 608-611.
65. Overgaard J, Sørensen JG, Petersen SO, Loeschcke V, Holmstrup M, 2006. Reorganization of membrane lipids during fast and slow cold hardening in Drosophila melanogaster. Physiol. Entomol. 31: 328-335.
66. Parsell DA, Lindquist S, 1993. The function of heat-shock proteins in stress tolerance: Degradation and reactivation of damaged proteins. Annu. Rev. Genet. 27: 437-496.
67. Pauwels K, Stoks R, De Meester L, 2005. Coping with predator stress: interclonal differences in induction of heat-shock proteins in the water flea Daphnia magna. J. Evol. Biol. 18: 867-872.
68. Pockley AG, 2003. Heat shock proteins as regulators of the immune response. Lancet 362: 469-476.
69. Pörtner HO, 2001. Climate change and temperature-dependent biogeography: Oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88: 137-146.
70. Pyza E, Mak P, Kramarz P, Laskowski R, 1997. Heat shock proteins (HSP70) as biomarkers in ecotoxicological studies. Ecotox. Environ. Safe. 38: 244-251.
71. Qin W, Neal SJ, Robertson RM, Westwood JT, Walker VK, 2005. Cold hardening and transcriptional change in Drosophila melanogaster. Insect Mol. Biol. 14: 607-613.
72. Queitsch C, Sangster TA, Lindquist S, 2002. Hsp90 as a capacitor of phenotypic variation. Nature 417: 618-624.
73. Rinehart JP, Hayward SAL, Elnitsky MA, Sandro LH, Lee RE et al., 2006. Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect. P. Natl. Acad. Sci. USA 103: 14223-14227.
74. Rodgers KJ, Ford JL, Brunk UT, 2009. Heat shock proteins: Keys to healthy ageing? Redox Rep. 14: 147-153.
75. Rutherford SL, 2003. Between genotype and phenotype: Protein chaperones and evolvability. Nat. Rev. Genet. 4: 263-274.
76. Rutherford SL, Lindquist S, 1998. Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342.
77. Sagarin RD, Somero GN, 2006. Complex patterns of expression of heat-shock protein 70 across the southern biogeographical ranges of the intertidal mussel Mytilus californianus and snail Nucella ostrina. J. Biogeogr. 33: 622-630.
78. Sarup P, Dahlgaard J, Norup AM, Jørgensen KT, Hebsgaard MB et al., 2004. Down regulation of Hsp70 expression level prolongs the duration of heat-induced male sterility in Drosophila buzzatii. Funct. Ecol. 18: 365-370.
79. Sarup P, Sørensen JG, Dimitrov K, Barker JSF, Loeschcke V, 2006. Climatic adaptation of Drosophila buzzatii populations in southeast Australia. Heredity 96: 479-486.
80. Schlesinger MJ, 1990. Heat shock proteins. J. Biol. Chem. 265: 12111-12114.
81. Selye H, 1956. The Stress of Life. New York: McGraw-Hill.
82. Shreve SM, Kelty JD, Lee RE, 2004. Preservation of reproductive behaviors during modest cooling: Rapid cold-hardening fine-tunes organismal response. J. Exp. Biol. 207: 1797-1802.
83. Sibly RM, Calow P, 1989. A life-cycle theory of responses to stress. Biol. J. Linn. Soc. 37: 101-116.
84. Sørensen JG, Kristensen TN, Loeschcke V, 2003. The evolutionary and ecological role of heat shock proteins. Ecol. Lett. 6: 1025-1037.
85. Sørensen JG, Loeschcke V, 2001. Larval crowding in Drosophila melanogaster induces Hsp70 expression, and leads to increased adult longevity and adult thermal stress resistance. J. Insect Physiol. 47: 1301-1307.
86. Sørensen JG, Loeschcke V, Kristensen TN, 2009a. Lessons from the use of genetically modified Drosophila melanogaster in ecological studies: Hsf mutant lines show highly trait-specific performance in field and laboratory thermal assays. Funct. Ecol. 23: 240-247.
87. Sørensen JG, Nielsen MM, Kruhoffer M, Justesen J, Loeschcke V, 2005a. Full genome gene expression analysis of the heat stress response, in Drosophila melanogaster. Cell Stress Chaperon. 10: 312-328.
88. Sørensen JG, Nielsen MM, Loeschcke V, 2007. Gene expression profile analysis of Drosophila melanogaster selected for resistance to environmental stressors. J. Evolution. Biol. 20: 1624-1636.
89. Sørensen JG, Norry FM, Scannapieco AC, Loeschcke V, 2005b. Altitudinal variation for stress resistance traits and thermal adaptation in adult Drosophila buzzatii from the New World. J. Evolution. Biol. 18: 829-837.
90. Sørensen JG, Pekkonen M, Lindgren B, Loeschcke V, Laurila A et al., 2009b. Complex patterns of geographic variation in heat tolerance and Hsp70 expression levels in the common frog Rana temporaria. J. Therm. Biol. 34: 49-54.
91. Sørensen JG, Sarup P, Kristensen TN, Loeschcke V, 2008. Temperature induced hormesis in Drosophila. In: Le Bourg E, Rattan SIS ed. Mild Stress and Healthy Aging. Netherlands: Springer Verlag, 65-79.
92. Stratman R, Markow TA, 1998. Resistance to thermal stress in desert Drosophila. Funct. Ecol. 12: 965-970.
93. Sun W, van Montagu M, Verbruggen N, 2002. Small heat shock proteins and stress tolerance in plants. Biochim. Biophys. Acta 1577: 1-9.
94. Sun Y, MacRae TH, 2005. Small heat shock proteins: Molecular structure and chaperone function. Cell. Mol. Life Sci. 62: 2460-2476.
95. Zatsepina OG, Ulmasov KA, Beresten SF, Molodtsov VB, Rybtsov SA et al., 2000. Thermotolerant desert lizards characteristically differ in terms of heat-shock system regulation. J. Exp. Biol. 203: 1017-1025.