Effect of thermal stress on protein expression in the mussel Mytilus galloprovincialis Lmk

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 147, Issue 3, 2007, Pages 531-540

  Gonzalez Riopedre M ^a   Novas A ^a   Dobano E ^a   Ramos Martinez J I ^a   Barcia, R ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

Biomarker; Electrophoretic profile; Haemocytes; HSP60; HSP70; Mytilus; Protein expression; Stress

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD CELL; CELL CULTURE; CONTROLLED STUDY; EXTRACTION; HEMOLYMPH; HOMEOSTASIS; MYTILUS GALLOPROVINCIALIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; SENSITIVITY ANALYSIS; TEMPERATURE STRESS; TISSUE REACTION;

MYTILUS; MYTILUS GALLOPROVINCIALIS;

EID: 34249279522     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2007.03.006     Document Type: Article

References (70)

1. Barcia R., Cao A., Arbeteta J., and Ramos-Martínez J.I. The IL-2 receptor in hemocytes of the sea mussel Mytilus galloprovincialis Lmk. IUBMB Life 48 (1999) 419-423
2. Bosch T.C.G., Krylow S.M., Bode H.R., and Steele R.E. Thermotolerance and synthesis of heat shock proteins: these responses are present in Hydra attenuata but absent in Hydra oligactis. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 7927-7931
3. Bradford M.M. A rapid and sensitive method for the quantification of micrograms quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
4. Buchner J., Schmidt M., Fuchs M., Jaenicke R., Rudolph R., Schmid F.X., and Kiefhaber T. GroE facilitates refolding of citrate synthase by suppressing aggregation. Biochemistry 30 (1991) 1586-1591
5. Buckley B.A., Owen M.E., and Hofmann G.E. Adjusting the thermostat: the threshold induction temperature for the heat-shock response in intertidal mussels (genus Mytilus) changes as a function of thermal history. J. Exp. Biol. 204 (2001) 3571-3579
6. Cao A., Mercado L., Ramos-Martínez J.I., and Barcia R. Primary cultures of hemocytes from Mytilus galloprovincialis Lmk.: expression of IL-2Rα. Aquaculture 216 (2003) 1-8
7. Cao A., Novás A., Ramos-Martínez J.I., and Barcia R. Seasonal variations in haemocyte response in the mussel Mytilus galloprovincialis Lmk. Aquaculture 263 (2007) 310-319
8. Chapple J.P., Smerdon G.R., and Hawkins A.J.S. 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 (1997) 225-235
9. Chapple J.P., Smerdon G.R., Barry R.J., and Hawkins A.J.S. Seasonal changes in stress-70 protein levels reflect thermal tolerance in the marine bivalve Mytilus edulis L. J. Exp. Mar. Biol. Ecol. 229 (1998) 53-68
10. Cheng M.Y., Hartl F.U., Martin J., Pollock R.A., Kalousek F., Neupert W., Hallberg E.M., Hallberg R.L., and Horwich A.L. Mitochondrial heat shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337 (1989) 620-624
11. Clegg J.S., Uhlinger K.R., Jackson S.A., Cherr G.N., Rifkin E., and Friedman C.S. Induced thermotolerance and the heat shock protein-70 family in the Pacific oyster Crassostrea gigas. Mol. Mar. Biol. Biotechnol. 7 (1998) 21-30
12. Coles J.A., Farley S.R., and Pipe R.K. Alteration of the immune response of the common marine mussel Mytilus edulis resulting from exposure to cadmium. Dis. Aquat. Org. 22 (1995) 59-65
13. Craig E.A., and Gross C.A. Is hsp70 the cellular thermometer?. Trends Biochem. Sci. 16 (1991) 135-140
14. Dietz T.J., and Somero G.N. 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 (1992) 3389-3393
15. Dyer S.D., Dickson K.L., Zimmerman E.G., and Sanders B.M. Tissue-specific patterns of synthesis of heat-shock proteins and thermal tolerance of the fathead minnow (Pimephales promelas). Can. J. Zool 69 (1991) 2021-2027
16. Ellis R.J. The molecular chaperon concept. Semin. Cell Biol. 1 (1990) 1-9
17. Ellis R.J. Discovery of molecular chaperones. Cell Stress Chaperones 1 (1996) 155-160
18. Ellis R.J. Do molecular chaperones have to be proteins?. Biochem. Biophys. Res. Commun. 238 (1997) 687-692
19. Ellis R.J., and van der Vies S.M. Molecular chaperones. Annu. Rev. Biochem. 60 (1991) 321-347
20. Gatenby A.A., Donaldson G.K., Goloubinoff P., LaRossa R.A., Lorimer G.H., Lubben T.H., Van Dyk T.K., and Viitanen P. The cellular functions of chaperonins. In: Schlesinger M.J., Santoro M.G., and Garaci E. (Eds). Stress Proteins, Induction and Function (1991), Springer-Verlag, New York 57-70
21. 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. 92 (1995) 2994-2998
22. Gething M.J., and Sambrook J. Protein folding in the cell. Nature 355 (1992) 33-45
23. Gómez-Mendikute A., and Cajaraville M.P. Comparative effects of cadmium, copper, paraquat and benzo[a]pyrene on the actin cytoskeleton and production of reactive oxygen species (ROS) in mussel haemocytes. Toxicol. In Vitro 17 (2003) 539-546
24. Hartl F.U., Martin J., and Neupert W. Protein folding in the cell: the role of molecular chaperones Hsp70 and Hsp60. Annu. Rev. Biophys. Biomol. Struct. 21 (1992) 293-322
25. Helmuth B.S.T., and Hofmann G.E. Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol. Bull. 201 (2001) 374-384
26. Heugens E.H.W., Hendriks A.J., Dekker T., van Straalen N.M., and Admiraal W. A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Crit. Rev. Toxicol. 31 (2001) 247-284
27. Hofmann G.E. Ecologically relevant variation in induction and function of heat shock proteins in marine organisms. Am. Zool. 39 (1999) 889-900
28. Hofmann G.E., and Somero G.N. 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 (1995) 1509-1518
29. Hofmann G.E., and Somero G.N. 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 (1996) 65-75
30. Jaenicke R. Protein stability and molecular adaptation to extreme conditions. Eur. J. Biochem. 202 (1991) 715-728
31. Kerambrun P., and Guerin J.P. Electrophoresis in study of stress effects in marine invertebrates. Bull. Soc. Zool. Fr. 109 (1984) 333-341
32. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
33. Lekube X., Cajaraville M.P., and Marigómez I. Use of polyclonal antibodies for the detection of changes induced by cadmium in lysosomes of aquatic organisms. Sci.Total Environ. 247 (2000) 201-212
34. Li G.C., Li L.G., Liu Y.K., Mak J.Y., and Chen L.L. Thermal response of rat fibroblasts stably transfected with the human 70-kDa heat shock protein-encoding gene. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 1681-1685
35. Lindquist S. The heat-shock response. Annu. Rev. Biochem. 55 (1986) 1151-1191
36. Lindquist S., and Craig E.A. The heat-shock proteins. Annu. Rev. Genet. 22 (1988) 631-677
37. Lis J., and Wu C. Protein traffic on the heat shock promoter: parking, stalling, and trucking along. Cell 74 (1993) 1-4
38. Lyons C., Dowling V., Tedengren N., Gardestrom J., Hartl M.G.J., O'Brien N., van Pelt F.N.A.M., O'Halloran J., and Sheehan D. Variability of heat shock proteins and glutathione S-transferase in gill and digestive gland of blue mussel, Mytilus edulis. Mar. Environ. Res. 56 (2003) 585-597
39. Martin J., Langer T., Boteva R., Schramel A., Horwich A.L., and Hartl F.U. Chaperonin-mediated protein folding at the surface of groEL through a "molten globule"-like intermediate. Nature 352 (1991) 36-42
40. McMullin T.W., and Hallberg R.L. A highly evolutionarily conserved mitochondrial protein is structurally related to the protein encoded by the Escherichia groEL gene. Mol. Cell. Biol 8 (1988) 371-380
41. Minier C., Borghi V., Moore M.N., and Porte C. Seasonal variation of MRX and stress proteins in the common mussel, Mytilus galloprovincialis. Aquat. Toxicol. 50 (2000) 167-176
42. Mizzen L.A., and Welch W.J. Characterization of the thermotolerant cell. I. Effects on protein synthesis activity and the regulation of heat-shock protein 70 expression. J. Biol. Chem. 106 (1988) 1105-1116
43. Morimoto R.I., Tissières A., and Georgopoulos C. The stress response, function of the proteins, and perspectives. In: Morimoto R.I., Tissières A., and Georgopoulos C. (Eds). Stress Proteins in Biology and Medicine (1990), Cold Spring Harbor Laboratory Press, New York 1-36
44. Nover L. The Heat Shock Response (1991), CRC Press, Boca Raton, FL
45. Ostermann J., Horwich A.L., Neupert W., and Hartl F.U. Protein folding in mitochondria requires complex formation with hsp60 and ATP hydrolysis. Nature 341 (1989) 125-130
46. Parsell D.A., Taulien J., and Lindquist S. The role of heat-shock proteins in thermotolerance. Philos. Trans. R. Soc. Lond., B Biol. Sci. 339 (1993) 279-286
47. Pavicic J., Smodis B., Skreblin M., Kregar I., and Stegnar P. Embryo-larval tolerance of Mytilus galloprovincialis, exposed to elevated seawater metal concentrations-II. Stage-specific fluctuations in sensitivity toward Zn and Cd and their bioaccumulation into veliger larvae. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 109C (1994) 37-46
48. Roberts D.A., Hofmann G.E., and Somero G.N. Heat-shock protein expression in Mytilus californianus: acclimatization (seasonal and tidal-height comparisons) and acclimation effects. Biol. Bull. 192 (1997) 309-320
49. Rothman J.E. Polypeptide chain binding proteins: Catalysts of protein folding and related processes in cells. Cell 59 (1989) 591-601
50. Sánchez Y., and Lindquist S.L. Hsp 104 required for induced thermotolerance. Science 248 (1990) 1112-1115
51. Sanders B.M. The role of stress protein response in physiological adaptation of marine molluscs. Mar. Environ. Res. 24 (1988) 207-210
52. Sanders B.M. Stress proteins: potential as multitiered biomarkers. In: Shugart L., and McCarthy J. (Eds). Biomarkers of Environmental Contamination (1990), Lewis, Boca Raton, FL 165-191
53. Sanders B.M. Stress proteins in aquatic organisms: an environmental perspective. Crit. Rev. Toxicol. 23 (1993) 49-75
54. Sanders B.M., and Martin L.S. Stress proteins as biomarkers of contaminant exposure in archived environmental samples. Sci. Total Environ. 139/149 (1993) 459-470
55. Sanders B.M., Martin L.S., Nelson W.G., Phelps D.K., and Welch W. Relationships between accumulation of a 60 kDa stress protein and scope-for-growth in Mytilus edulis exposed to a range of copper concentrations. Mar. Environ. Res. 31 (1991) 81-97
56. Sanders B.M., Pascoe V.M., Nakagawa P.A., and Martin L.S. Persistence of the heat-shock response over time in a common Mytilus mussel. Mol. Mar. Biol. Biotechnol. 1 (1992) 147-154
57. Sanders B.M., Martin L.S., Howe S.R., Nelson W.G., Hegre E.S., and Phelps D.K. Tissue-specific differences in accumulation of stress proteins in Mytilus edulis exposed to a range of copper concentrations. Toxicol. Appl. Pharmacol. 125 (1994) 206-213
58. Seckler R., and Jaenicke R. Protein folding and protein refolding. FASEB J. 6 (1992) 2545-2552
59. Sheehan D., and Power A. Effects of seasonality on xenobiotic and antioxidant defence mechanisms of bivalve molluscs. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 123C (1999) 193-199
60. Sherry J.P. The role of biomarkers in the health assessment of aquatic ecosystems. Aquat. Ecosyst. Health Manag. 6 (2003) 423-440
61. Snyder M.J., Girvetz E., and Mulder E.P. Induction of marine mollusc stress proteins by chemical or physical stress. Arch. Environ. Contam. Toxicol. 41 (2001) 22-29
62. Solomon J.M., Rossi J.M., Golic K., McGarry T., and Lindquist S. Changes in Hsp70 alter thermotolerance and heat-shock regulation in Drosophila. New Biol. 3 (1991) 1106-1120
63. Somero G.N. Proteins and temperature. Annu. Rev. Physiol. 57 (1995) 43-68
64. Steinert S.A., and Pickwell G.V. Induction of HSP70 proteins in mussels by ingestion of tributyltin. Mar. Environ. Res. 35 (1993) 89-93
65. Tirard C.T., Grossfeld R.M., Levine J.F., and Kennedy-Stoskopf S. Effect of hyperthermia in vitro on stress protein synthesis and accumulation in oyster hemocytes. Fish Shellfish Immunol. 5 (1995) 9-25
66. Veldhuizen-Tsoerkan M.B., Holwerda D.A., de Bont A.M.T., Smaal A.C., and Zandee D.I. A field study on stress indices in the sea mussel, Mytilus edulis: application of the "stress approach" in biomonitoring. Arch. Environ. Contam. Toxicol. 21 (1991) 497-504
67. Wagner M., Hermanns I., Bittinger F., and Kirkpatrick C.J. Induction of stress proteins in human endothelial cells by heavy metal ions and heat shock. Am. J. Physiol., Lung Cell Mol. Physiol. 21 (1999) 1026-1033
68. Welch W.J. The role of heat-shock proteins as molecular chaperones. Curr. Opin. Cell Biol. 3 (1991) 1033-1038
69. Welch W.J. How cells respond to stress. Sci. Am. 268 (1993) 56-64
70. Zinder M.J., Girvetz E., and Mulder E.P. Induction of marine mollusc stress proteins by chemical or physical stress. Arch. Environ. Contam. Toxicol. 41 (2001) 22-29