Advertisement

Cell Stress and Chaperones

, Volume 14, Issue 4, pp 439–443 | Cite as

Differences in heat shock protein 70 expression during larval and early spat development in the Eastern oyster, Crassostrea virginica (Gmelin, 1791)

  • Nobuo Ueda
  • Anne BoettcherEmail author
Short Communication

Abstract

For a variety of species, changes in the expression of heat shock proteins (HSP) have been linked to key developmental changes, i.e., gametogenesis, embryogenesis, and metamorphosis. Many marine invertebrates are known to have a biphasic life cycle where pelagic larvae go through settlement and metamorphosis as they transition to the benthic life stage. A series of experiments were run to examine the expression of heat shock protein 70 (HSP 70) during larval and early spat (initial benthic phase) development in the Eastern oyster, Crassostrea virginica. In addition, the impact of thermal stress on HSP 70 expression during these early stages was studied. C. virginica larvae and spat expressed three HSP 70 isoforms, two constitutive, HSC 77 and HSC 72, and one inducible, HSP 69. We found differences in the expression of both the constitutive and inducible forms of HSP 70 among larval and early juvenile stages and in response to thermal stress. Low expression of HSP 69 during early larval and spat development may be associated with the susceptibility of these stages to environmental stress. Although developmental regulation of HSP 70 expression has been widely recognized, changes in its expression during settlement and metamorphosis of marine invertebrates are still unknown. The results of the current study demonstrated a reduction of HSP 70 expression during settlement and metamorphosis in the Eastern oyster, C. virginica.

Keywords

Eastern oyster Heat shock protein 70 Larvae Settlement and metamorphosis Spat 

Abbreviations

DNA

Deoxyribonucleic acid

HSC

Heat shock cognate/constitutive

HSP

Heat shock protein

PCR

Polymerase chain reaction

SDS

Sodium dodecyl sulfate

Notes

Acknowledgments

The authors would like to thank the Auburn University Shellfish Laboratory, particularly Scott Rikard, for providing oyster larvae and spat samples. We thank John Freeman, Tim Sherman, Richard Wallace, and Kevin Fielman for valuable suggestions and stimulating discussions of our manuscript. We would also like to thank Dan Martin and two anonymous reviewers for valuable comments on this paper. This research was made possible by funding from the Alabama Oyster Reef Restoration Program, National Marine Fisheries Service.

References

  1. Baker P (1995) Review of ecology and fishery of the Olympia oyster, Ostrea lurida with annotated bibliography. J Shellfish Res 14:501–518Google Scholar
  2. Bishop CD, Brandhorst BP (2001) NO/cGMP signaling and HSP90 activity represses metamorphosis in the sea urchin Lytechinus pictus. Biol Bull 201:394–404 doi: 10.2307/1543617 PubMedCrossRefGoogle Scholar
  3. Bishop CD, Bates WR, Brandhorst BP (2001) Regulation of metamorphosis in ascidians involves NO/cGMP signaling and HSP90. J Exp Zool 289:374–384 doi: 10.1002/jez.1019 PubMedCrossRefGoogle Scholar
  4. Brown HM, Bride A, Stokell T, Griffin FJ, Cherr GN (2004) Thrermotolerance and HSP70 profiles in adult and embryonic California native oyster, Ostreola conchaphila (Carpenter, 1857). J Shellfish Res 23:135–141Google Scholar
  5. Chang ES (2005) Stressed-out lobsters: Crustacean hyperglycemic hormone and stress proteins. Integr Comp Biol 45:43–50 doi: 10.1093/icb/45.1.43 CrossRefGoogle Scholar
  6. 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 7:21–30Google Scholar
  7. Davis HC, Chanley PE (1956) Spawning and egg production of oysters and clams. Biol Bull 110:117–128 doi: 10.2307/1538972 CrossRefGoogle Scholar
  8. Dix DJ (1997) Hsp70 expression and function during gametogenesis. Cell Stress Chap 2:73–77 doi: 10.1379/1466-1268(1997)002<0073:HEAFDG>2.3.CO;2 CrossRefGoogle Scholar
  9. Encomio VG, Chu F-LE (2005) Seasonal variation of heat shock protein 70 in Eastern oysters (Crassostrea virginica) infected with Perkinsus marinus (Dermo). J Shellfish Res 24:167–175Google Scholar
  10. Feder EM, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282 doi: 10.1146/annurev.physiol.61.1.243 PubMedCrossRefGoogle Scholar
  11. Gething M-J, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45 doi: 10.1038/355033a0 PubMedCrossRefGoogle Scholar
  12. Giudice G, Sconzo G, Roccheri MC (1999) Studies on heat shock proteins in sea urchin development. Dev Growth Differ 41:375–380 doi: 10.1046/j.1440-169x.1999.00450.x PubMedCrossRefGoogle Scholar
  13. Gunter HM, Degnan BM (2007) Developmental expression of Hsp90, Hsp70, and HSF during morphogenesis in the vetigastropod Haliotis asinina. Dev Genes Evol 217:603–612 doi: 10.1007/s00427-007-0171-2 PubMedCrossRefGoogle Scholar
  14. Hamdoun AH, 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 205:160–169 doi: 10.2307/1543236 PubMedCrossRefGoogle Scholar
  15. Hopkins AE (1936) Ecological observations on spawning and early larval development in the Olympia oyster (Ostrea lurida). Ecology 17:551–566 doi: 10.2307/1932760 CrossRefGoogle Scholar
  16. Karouna-Renier NK, Yang W-J, Rao KR (2003) Cloning and characterization of a 70 kDa heat shock cognate gene (HSC70) from two species of Chironomus. Insect Mol Biol 12:19–26 doi: 10.1046/j.1365-2583.2003.00383.x PubMedCrossRefGoogle Scholar
  17. Kennedy VS (1996) Biology of larvae and spat. In: Kennedy VS, Newell RIE, Eble AF (eds) The Eastern oyster, Crassostrea virginica. Maryland Seagrant, College Park, MD, pp 371–421Google Scholar
  18. Krebs RA, Feder ME (1998) Hsp70 and larval thermotolerance in Drosophila melanogaster: how much is enough and when is too much? J Insect Physiol 44:1091–1101 doi: 10.1016/S0022-1910(98)00059-6 PubMedCrossRefGoogle Scholar
  19. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the heat of bacteriophage T4. Nature 227:680–685 doi: 10.1038/227680a0 PubMedCrossRefGoogle Scholar
  20. Langdon CJ, Newell RIE (1996) Digestion and nutrition in larvae and adults. In: Kennedy VS, Newell RIE, Eble AF (eds) The Eastern oyster, Crassostrea virginica. Maryland Seagrant, College Park, MD, pp 231–269Google Scholar
  21. Mahroof R, Zhu KY, Neven L, Subramanyam Bh, Bai J (2005) Expression patterns of three heat shock protein 70 genes among developmental stages of the red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae). Comp Biochem Phys A 141:247–256 doi: 10.1016/j.cbpb.2005.05.044 CrossRefGoogle Scholar
  22. McEdward LR, Janies DA (1993) Life cycle evolution in asteroids: what is a larva? Biol Bull 184:255–268 doi: 10.2307/1542444 CrossRefGoogle Scholar
  23. Sanders BM (1993) Stress proteins in aquatic organisms: an environmental perspective. Crit Rev Toxicol 23:49–75 doi: 10.3109/10408449309104074 PubMedCrossRefGoogle Scholar
  24. Sarkis S, Boettcher A, Ueda N, Hohn C (2005) Simple transport procedure for juvenile Calico scallops, Argopecten gibbus (Linnaeus, 1758). J Shellfish Res 24:377–380Google Scholar
  25. Sorte CJB, Hofmann GE (2004) Changes in latitude, changes in aptitude: Nucella canaliculata (Mollusca: Gastropoda) is more stressed at its range edge. Mar Ecol Prog Ser 274:263–268 doi: 10.3354/meps274263 CrossRefGoogle Scholar
  26. Towbin H, Staechelin T, Gordon J (1979) Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354 doi: 10.1073/pnas.76.9.4350 PubMedCrossRefGoogle Scholar
  27. Wood LA, Brown IR, Youson JH (1999) Tissue and developmental variations in the heat shock response of sea lampreys (Petromyzon marinus): effects of an increase in acclimation temperature. Comp Biochem Phys A 123:35–42 doi: 10.1016/S1095-6433(99)00035-5 CrossRefGoogle Scholar
  28. Yeh F-L, Hsu T (2002) Differential regulation of spontaneous and heat-induced HSP 70 expression in developing zebrafish (Danio rerio). J Exp Zool 293:349–359 doi: 10.1002/jez.10093 PubMedCrossRefGoogle Scholar
  29. Zar JH (1984) Biostatistical analysis. Prentice Hall, NJGoogle Scholar

Copyright information

© Cell Stress Society International 2008

Authors and Affiliations

  1. 1.Department of Biological SciencesAuburn UniversityAuburnUSA
  2. 2.Department of Biology, LSCB 124University of South AlabamaMobileUSA

Personalised recommendations