Heat shock protein (hsp70) expression and thermal tolerance in sublethally heat-shocked eastern oysters Crassostrea virginica infected with the parasite Perkinsus marinus

Diseases of Aquatic Organisms

Volumn 76, Issue 3, 2007, Pages 251-260

  Encomio, V G ^a   Chu, F L E ^b  

^a FLORIDA GULF COAST UNIVERSITY   (United States)

^b VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

Author keywords

Crassostrea virginica; Heat shock protein; Hsp70; Perkinsus marinus; Thermal tolerance

Indexed keywords

BIVALVE; HEAT SHOCK; PARASITE; PROTEIN; SUBLETHAL EFFECT; SURVIVAL; TEMPERATURE TOLERANCE;

CRASSOSTREA VIRGINICA; OSTREIDAE; PERKINSUS MARINUS;

HEAT SHOCK PROTEIN 70; ISOPROTEIN;

ANIMAL; ANIMAL DISEASE; ANIMAL PARASITOSIS; ARTICLE; BIOSYNTHESIS; GROWTH, DEVELOPMENT AND AGING; HEAT SHOCK RESPONSE; IMMUNOLOGY; KAPLAN MEIER METHOD; METABOLISM; OYSTER; PARASITOLOGY; PHYSIOLOGY; PROTOZOON; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CRASSOSTREA; HEAT-SHOCK RESPONSE; HSP70 HEAT-SHOCK PROTEINS; KAPLAN-MEIERS ESTIMATE; PROTEIN ISOFORMS; PROTOZOA; PROTOZOAN INFECTIONS, ANIMAL;

EID: 35748933484     PISSN: 01775103     EISSN: 16161580     Source Type: Journal    
DOI: 10.3354/dao076251     Document Type: Article

References (56)

1. Andrews JD (1965) Infection experiments in nature with Dermocystidium marinum in Chesapeake Bay. Chesap Sci 6: 60-67
2. Andrews JD (1988) Epizootiology of the disease caused by the oyster pathogen Perkinsus marinus and its effects on the oyster industry. In: Fisher WS (ed) Disease processes in marine bivalve molluscs, Vol 18. American Fisheries Society, Bethesda, MD, p 47-63
3. Bosch TCG, Krylow SM, Bode HR, Steele RE (1988) Thermotolerance and synthesis of heat shock proteins: These responses are present in Hydra attenuata but absent in Hydra oligactis. Proc Natl Acad Sci USA 85:7927-7931
4. Boutet I, Tanguy A, Rousseau S, Auffret M, Moraga D (2003) Molecular identification and expression of heat shock cognate 70 (hsc70) and heat shock protein 70 (hsp70) genes in the Pacific oyster Crassostrea gigas. Cell Stress Chaperones 8:76-85
5. Brown HM, Briden A, Stokell T, Griffin FJ, Cherr GN (2004) Thermotolerance and HSP70 profiles in adult and embryonic Californian native oysters, Ostreola conchaphila (Carpenter, 1857). J Shellfish Res 25:135-141
6. Burreson EM, Ragone-Calvo LM, La Peyre JF, Counts F, Paynter KT (1994) Acute osmotic tolerance of cultured cells of the oyster pathogen Perkinsus marinus (Apicomplexa: Perkinsada). Comp Biochem Physiol A 109:575-582
7. Bushek D, Ford SE, Allen SK Jr (1994) Evaluation of methods using Ray's fluid thioglycollate medium for diagnosis of Perkinsus marinus infection in the eastern oyster, Crassostrea virginica. Annu Rev Fish Dis 4:201-217
8. Calvo LMR, Calvo GW, Burreson EM (2003) Dual disease resistance in a selectively bred eastern oyster, Crassostrea virginica, strain tested in Chesapeake Bay. Aquaculture 220:69-87
9. Chappie 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
10. Choi KS, Wilson EA, Lewis DH, Powell EN, Ray SM (1989) The energetic cost of Perkinsus marinus parasitism in oysters: quantification of the thioglycollate method. J Shellfish Res 8:125-131
11. Chu FLE, La Peyre JF (1993) Perkinsus marinus susceptibility and defense-related activities in eastern oysters Crassostrea virginica: temperature effects. Dis Aquat Org 16: 223-234
12. Chu FLE, Volety AK (1997) Disease processes of the parasite Perkinsus marinus in eastern oyster Crassostrea virginica: minimum dose for infection initiation, and interaction of temperature, salinity and infective cell dose. Dis Aquat Org 28:61-68
13. Clegg JS, Uhlinger KR, Jackson SA, Cherr GN, Rifkin E, Friedman CS (1998) Induced thermotolerance and the heat shock protein-70 family in the Pacific oyster Crassostrea gigas. Mol Mar Biol Biotechnol 7:21-30
14. Cox DR, Oakes D (1984) Analysis of survival data. Chapman and Hall, New York
15. Craig A, Powell EN, Fay RR, Brooks JM (1989) Distribution of Perkinsus marinus in Gulf Coast oyster populations. Estuaries 12:82-91
16. Cruz-Rodriguez L, Chu FLE (2002) Heat shock protein (HSP70) response in the eastern oyster, Crassostrea virginica, exposed to PAHs sorbed to suspended artificial clay particles and to suspended field contaminated sediments. Aquat Toxicol 60:157-168
17. Dittman DE, Ford SE, Padilla DK (2001) Effects of Perkinsus marinus on reproduction and condition of the eastern oyster, Crassostrea virginica, depend on timing. J Shellfish Res 20:1025-1034
18. 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
19. Encomio VG (2004) A study of the eastern oyster, Crassostrea virginica. 1. Dermo tolerance, survival, growth, condition and hsp70 expression in different geographic stocks. 2. Heat tolerance and effects of sublethal heat shock on survival and hsp70 expression of infected and uninfected oysters. PhD dissertation, The College of William and Mary, Williamsburg, VA
20. Encomio V, Chu FLE (2004) Characterization of heat shock protein expression and induced thermotolerance in P. marinus parasitized oysters: lab and field studies. J Shellfish Res 23:289
21. Encomio VG, Chu FLE (2005) Seasonal variation of heat shock protein 70 in eastern oysters (Crassostrea virginica) infected with Perkinsus marinus (Dermo). J Shellfish Res 24:167-175
22. Encomio VG, Stickler SM, Chu FLE (2005) Performance of 'natural Dermo-resistant' oyster stocks: survival, disease, growth, condition and energy reserves. J Shellfish Res 24: 143-155
23. Feder ME, Hofmann GE (1999) Heat shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243-282
24. Fisher WS, Gauthier JD, Winstead JT (1992) Infection intensity of Perkinsus marinus disease in Crassostrea virginica (Gmelin, 1791) from the Gulf of Mexico maintained under different laboratory conditions. J Shellfish Res 11:363-369
25. Ford SE (1996) Range extension by the oyster parasite Perkinsus marinus into the northeastern United States: response to climate change? J Shellfish Res 15:45-56
26. Forsyth RB, Candido EPM, Babich SL, Iwama GK (1997) Stress protein expression in coho salmon with bacterial kidney disease. J Aquat Anim Health 9:18-25
27. Friedman CS, Cherr GN, Clegg JS, Hamdoun AH, Jacobsen JL, Jackson SA, Uhlinger KR (1999) Investigation of the stress response, summer mortality and disease resistance of oysters, Crassostrea spp. J Shellfish Res 18:297
28. Gething M, Sambrook J (1992) Protein folding in the cell. Nature 355:33-45
29. Gupta RS, Golding GB (1993) Evolution of HSP70 gene and its implications regarding relationships between archaebacteria, eubacteria and eukaryotes. J Mol Evol 37:573-582
30. Hamdoun AM, Cheney DP, Cherr GN (2003) Phenotypic plasticity of HSP70 and HSP70 gene expression in the Pacific oyster (Crassostrea gigas): implications for thermal limits and induction of thermal tolerance. Biol Bull (Woods Hole) 205:160-169
31. Handley SJ, Bergquist PR (1997) Spionid polychaete infestations of intertidal Pacific oysters Crassostrea gigas (Thunberg), Mahurangi Harbour, northern New Zealand. Aquaculture 153:191-205
32. Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, New York
33. Hofmann GE (1999) Ecologically relevant variation in induction and function of heat shock proteins in marine organisms. Am Zool 39:889-900
34. Huppert HW, Laudien H (1980) Influence of pretreatment with constant and changing temperatures on heat and freezing resistance in gill-epithelium of the mussel Mytilus edulis. Mar Ecol Prog Ser 3:113-120
35. Kleinschuster SJ, Parent J (1995) Sub-clinical infection of oysters (Crassostrea virginica, Gmelin, 1791) from Maine by species of the genus Perkinsus (Apicomplexa). J Shellfish Res 14:489-491
36. La Peyre JF (1996) Propagation and in vitro studies of Perkinsus marinus. J Shellfish Res 15:89-101
37. Lauckner G (1980) Diseases of Mollusca: Gastropoda. In: Kinne O (ed) Diseases of marine animals, Vol 1. Biologische Anstalt Helgoland, Hamburg, p 311-324
38. Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151-1191
39. Lindquist SC, Craig EA (1988) The heat shock proteins. Annu Rev Genet 22:631-677
40. Littlewood DTJ, Ford SE (1990) Physiological responses to acute temperature elevation in oysters, Crassostrea virginica (Gmelin, 1791), parasitized by Haplosporidium nelsoni (MSX) (Haskin, Stauber, and Mackin, 1966). J Shellfish Res 9:159-163
41. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265-275
42. Martinez J, Perez Serrano J, Bernadina WE, Rodriguez-Caabeiro F (1999) Influence of parasitization by Trichinella spiralis on the levels of heat shock proteins in rat liver and muscle. Parasitology 118:201-209
43. Mears HC (1993) Oyster disease research (ODR) program. J Shellfish Res 12:351-368
44. Merino SMJ, Barbosa A, Moller AP, De Lope F, Perez J, Rodriguez-Caabeiro F (1998) Increase in heat shock protein from blood cells in response of nestling house martins (Delichon urbica) to parasitism: an experimental approach. Oecologia 116:343-347
45. Morimoto RI, Tissieres A, Georgopoulos C (1990) The stress response, function of the proteins and perspectives. Stress Prot Biol Med 1:1-35
46. Newell RIE, Paynter KT, Burreson EM (1994) Physiological effects of protozoan parasitism on the eastern oyster Crassostrea virginica: feeding and metabolism. J Shellfish Res 13:294
47. Newman MC (1994) Quantitative methods in aquatic ecotoxicology. CRC Press, Boca Raton, FL
48. Piano A, Asirelli C, Caselli F, Fabbri E (2002) Hsp70 expression in thermally stressed Ostrea edulis, a commercially important oyster in Europe. Cell Stress Chaperones 7: 250-257
49. Ray SM (1966) A review of the culture method for detecting Dermocystidium marinum, with suggested modifications and precautions. Proc Nat Shellfish Assoc 54:55-69
50. Sanchez EH, Lindquist SL (1990) HSP 104 required for induced thermotolerance. Science 248:1112-1115
51. Sanders BM (1988) The role of stress protein response in physiological adaptation of marine molluscs. Mar Environ Res 24:207-210
52. Shamseldin AA, Clegg JS, Friedman CS, Cherr GN, Pillai MC (1997) Induced thermotolerance in the Pacific oyster, Crassostrea gigas. J Shellfish Res 16:487-491
53. Soudant P, Chu FLE, Lund ED (2005) Assessment of the cell viability of cultured Perkinsus marinus (Perkinsea), a parasitic protozoan of the eastern oyster, Crassostrea virginica, using sybrgreen-propidium iodide double staining and flow cytometry. J Eukaryot Microbiol 52(6):492-499
54. Tedengren M, Olsson B, Reimer O, Brown DC, Bradley BP (1999) Heat pretreatment increases cadmium resistance and HSP 70 levels in Baltic Sea mussels. Aquat Toxicol 48: 1-12
55. Tirard CT, Grossfeld RM, Levine JF, Kennedy-Stoskopf S (1995) Effect of hyperthermia in vitro on stress protein synthesis and accumulation in oyster haemocytes. Fish Shellfish Immunol 5:9-25
56. Ventilla RF (1984) Recent developments in the Japanese oyster culture industry. Adv Mar Biol 21:1-57