Environmental Biology of Fishes

, Volume 93, Issue 3, pp 333–342 | Cite as

Starvation reduces the heat shock protein responses in white sturgeon larvae

  • Dong Han
  • Susie S. Y. Huang
  • Wei-Fang Wang
  • Dong-Fang Deng
  • Silas S. O. Hung
Article

Abstract

This study investigates the responses of white sturgeon larvae (Acipenser transmontanus) to starvation and thermal stress, through the measurement of nutritional status (i.e. growth performances) and cellular biomarkers: heat shock proteins (Hsp) 70 and 90. White sturgeon larvae (25 day post hatch; initial weight 179.0 ± 5.1 mg) were fed (20% body weight per day) or starved for 24, 48 or 72 hrs. Every 24 hrs, five larvae from each of the starved or fed treatment replicates were exposed to heat shock resulting from an increase in water temperature from 19°C to 26°C, at a rate of 1°C per 15 min, and maintained at 26°C for 4 hrs. No mortality was observed in this study. Starvation significantly (p < 0.05) decreased the body weight and body contents of energy, protein, and lipid of the experimental larvae, compared to the fed larvae. Heat shock induced the expressions of Hsp70 and Hsp90 in both the fed and starved group; however, starvation reduced the induction at all sampling points. The current study demonstrates that poor larval nutritional status, assessed by the aforementioned parameters, reduced heat shock responses to thermal stress, as measured by heat shock protein levels. Furthermore, Hsp70 and 90 are more sensitive to heat shock and starvation, respectively. This may be, in part, a result of the different functioning of the heat shock proteins in cellular stress response and warrants further study.

Keywords

Nutrient supply Thermal stress Hsp70 Hsp90 Sturgeon larvae 

References

  1. Apperson KA, Anders PJ (1991) Kootenai River white sturgeon investigations and experimental culture. Annual Progress Report FY 1990. Idaho Department of Fish and Game and the Bonneville Power Administration. Contract No. DE-AI79-88BP93497; Project No. 88–65. Portland, Oregon, pp 67.Google Scholar
  2. Buckiová D, Jelínek R (1995) Heat shock proteins and teratogenesis. Reprod Toxicol 9:501–511PubMedCrossRefGoogle Scholar
  3. Buckley LT, Caldarone E, Ong TL (1999) RNA-DNA ratio and other nucleic acid-based indicators for growth and condition of marine fishes. Hydrobiologia 401:265–277CrossRefGoogle Scholar
  4. Caldarone EM,Wagner M, St. Onge-Burns J, Buckley LJ (2001) Protocol and guide for estimating nucleic acids in larval fish using a fluorescence microplate reader. Northeast Fish Sci Cent Ref Doc 01–11, pp 22. Available from: National Marine Fisheries Service, 166 Water Street, Woods Hole, MA 02543–1026Google Scholar
  5. Cara JB, Aluru N, Moyano FJ, Vijayan MM (2005) Food-deprivation induces HSP70 and HSP90 protein expression in larval gilthead sea bream and rainbow trout. Comp Biochem Physiol 142B:426–431Google Scholar
  6. Cloern JE, Alpine AE, Cole BE, Wong RLJ, Arthur JF, Ball MD (1983) River discharge controls phytoplankton dynamics in the Northern San Francisco Bay Estuary. Estuar Coast Shelf Sci 16:415–429CrossRefGoogle Scholar
  7. CNDDB (California Natural Diversity Database) (2009) Department of Fish and Game, Biographic Data Branch, Special animals (883 taxa), July 2009. http://www.dfg.ca.gov/biogeodata/cnddb/pdfs/SPAnimals.pdf.
  8. Conceiçáo LE, Van der Meeren T, Verreth JA, Evjen MS, Houlihan DF, Fyhn HJ (1997) Amino acid metabolism and protein turnover in larval turbot, (Scophthalmus maximus) fed natural zooplankton or Artemia. Mar Biol 129:255–265CrossRefGoogle Scholar
  9. Cui YB, Hung SSO, Deng DF, Yang YX (1997) Growth of white sturgeon as affected by feeding regimen. Progressive Fish-Culturist 59:31–35CrossRefGoogle Scholar
  10. Deng DF, Koshio S, Yokoyama S, Bai SC, Shao QJ, Cui YB, Hung SSO (2003) Effects of feeding rate on growth performance of white sturgeon (Acipenser transmontanus) larvae. Aquaculture 217:589–598CrossRefGoogle Scholar
  11. Deng DF, Wang CF, Lee SH, Bai SC, Hung SSO (2009) Feeding rates affect heat shock protein levels in liver of larval white sturgeon (Acipenser transmontanus). Aquaculture 287:223–226CrossRefGoogle Scholar
  12. Duke S, Down T, Ptolemy J, Hammond J, Spence C (2004) Acipenser transmontanus. In: IUCN 2010. IUCN Red List of Threatened Species. Version 2010.2.Google Scholar
  13. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282PubMedCrossRefGoogle Scholar
  14. Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45PubMedCrossRefGoogle Scholar
  15. Gisbert E, Williot P (1997) Larval behavior and effect of the timing of initial feeding on growth and survival of Siberian sturgeon (Acipenser baeri) larvae under small scale hatchery production. Aquaculture 156:63–76CrossRefGoogle Scholar
  16. Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858PubMedCrossRefGoogle Scholar
  17. Hemre GI, Deng DF, Wilson RP, Berntssen MHG (2004) Vitamin A metabolism and early biological responses in juvenile sunshine bass (Morone chrysops×M. saxatilis) fed graded levels of vitamin A. Aquaculture 235:645–658CrossRefGoogle Scholar
  18. Heubach WR, Toth RJ, McCready AM (1963) Food of young-of-the-year striped bass (Roccus saxatilis) in the Sacramento-San Joaquin River system. Calif Fish Game 49:224–239Google Scholar
  19. Hightower LE (1991) Heat shock, stress proteins, chaperones and proteotoxicity. Cell 66:191–197PubMedCrossRefGoogle Scholar
  20. Ivanina AV, Taylor C, Sokolova IM (2009) Effects of elevated temperature and cadmium exposure on stress protein response in eastern oysters Crassostrea virginica (Gmelin). Aquat Toxicol 91:245–254PubMedCrossRefGoogle Scholar
  21. Iwama GK, Vijayan MM, Forsyth RB, Ackerman PA (1999) Heat shock proteins and physiological stress in fish. Am Zool 39:901–909Google Scholar
  22. Jelks HL, Walsh SJ, Burkhead NM, Contreras-Balderas S, Díaz-Pardo E, Hendrickson DA, Lyons J, Mandrak NE, McCormick F, Nelson JS, Platania SP, Porter BA, Renaud CB, Schmitter-Soto JJ, Taylor EB, Warren ML Jr (2008) Conservation status of imperiled North American freshwater and diadromous fishes. Fisheries 33:372–407CrossRefGoogle Scholar
  23. Jones CE (1984) Animal feed. In: Williams S (ed) Official methods of analysis of the Association of Official Analytical Chemists, 14th edn. Association of Official Analytical Chemists, Arlington, pp 152–160Google Scholar
  24. Kampinga HH, Brunsting JF, Stege GJ, Burgman PW, Konings AW (1995) Thermal protein denaturation and protein aggregation in cells made thermotolerant by various chemicals: role of heat shock proteins. Exp Cell Res 219:536–546PubMedCrossRefGoogle Scholar
  25. Kiang JG, Tsokos GC (1998) Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacol Ther 80:183–201PubMedCrossRefGoogle Scholar
  26. Knutson AC Jr, Orsi JJ (1983) Factors regulating abundance and distribution of the shrimp Neomysis mercedis in the Sacramento-San Joaquin Estuary. Trans Am Fish Soc 112:476–485CrossRefGoogle Scholar
  27. McCabe GT Jr, Tracy CA (1994) Spawning and early life history of white sturgeon, Acipenser transmontanus, in the lower Columbia River. Fish B-NOAA 92:760–772Google Scholar
  28. Mourente G, Rodríguez A, Grau A, Pastor E (1999) Utilization of lipids by Dentex dentex L. (Osteichthyes, Sparidae) larvae during lecitotrophia and subsequent starvation. Fish Physiol Biochem 21:45–58CrossRefGoogle Scholar
  29. Moyle PB (2002) Inland fishes of California. University of California Press, BerkeleyGoogle Scholar
  30. Muir WD, Emmett RL, McConnell RJ (1988) Diet of juvenile and subadult white sturgeon in the lower Columbia River and its estuary. Calif Fish Game 74:49–54Google Scholar
  31. Muir WD, McCabe GT Jr, Parsley MJ, Hinton SA (2000) Diet of first-feeding larval and young-of-the-year white sturgeon in the lower Columbia River. NW Sci 74:25–33Google Scholar
  32. Neckers L, Ivy SP (2003) Heat shock protein 90. Curr Opin Oncol 15:419–424PubMedCrossRefGoogle Scholar
  33. Nichols FH, Cloern JE, Luoma SN, Peterson DH (1986) The modification of an estuary. Science 231:567–573PubMedCrossRefGoogle Scholar
  34. Pannevis MC, Houlihan DF (1992) The energetic cost of protein synthesis in isolated hepatocytes of rainbow trout (Oncorhynchus mykiss). J Comp Physiol 162B:393–400Google Scholar
  35. Raae AJ, Opstad I, Kvenseth P, Walther BT (1988) RNA, DNA and protein during early development in feeding and starved cod (Gadus morhua L.) larvae. Aquaculture 73:247–259CrossRefGoogle Scholar
  36. Rogers BA, Westin DT (1981) Laboratory studies on effects of temperature and delayed initial feeding on development of striped bass larvae. Trans Am Fish Soc 110:100–110CrossRefGoogle Scholar
  37. Tanaka Y, Satoh K, Yamada H, Takebe T, Nikaido H, Shiozawa S (2008) Assessment of the nutritional status of field-caught larval Pacific bluefin tuna by RNA/DNA ratio based on a starvation experiment of hatchery-reared fish. J Exp Mar Biol Ecol 354:56–64CrossRefGoogle Scholar
  38. Tomanek L, Somero GN (2000) Time course and magnitude of synthesis of heat-shock proteins in congeneric marine snails (genus Tegula) from different tidal heights. Physiol Biochem Zool 73:249–256PubMedCrossRefGoogle Scholar
  39. Van Eenennaam JP, Linares-Casenave J, Deng X, Doroshov SI (2005) Effect of incubation temperature on green sturgeon embryos, Acipenser medirostris. Environ Biol Fish 72:145–154CrossRefGoogle Scholar
  40. Watanabe T, Kiron V (1994) Prospects in larval fish dietetics. Aquaculture 124:223–251CrossRefGoogle Scholar
  41. Watanabe Y, Zenitani H, Kimura H (1995) Population decline of the Japanese Sardine Sardinops melanostictus owning to recruitment failures. Can J Fish Aquat Sci 52:1609–1616CrossRefGoogle Scholar
  42. Weber TE, Bosworth BG (2005) Effects of 28 day exposure to cold temperature or feed restriction on growth, body composition, and expression of genes related to muscle growth and metabolism in channel catfish. Aquaculture 246:483–492CrossRefGoogle Scholar
  43. Yengkokpam S, Pal AK, Sahu NP, Jain KK, Dalvi R, Misra S, Debnath D (2008) Metabolic modulation in Labeo rohita fingerlings during starvation: Hsp70 expression and oxygen consumption. Aquaculture 285:234–237CrossRefGoogle Scholar
  44. Yin MC, Blaxter JHS (1987) Temperature, salinity tolerance, and buoyancy during early development and starvation of Clyde and North Sea herring, cod, and flounder larvae. J Exp Mar Biol Ecol 107:279–290CrossRefGoogle Scholar
  45. Zarate J, Bradley TM (2003) Heat shock proteins are not sensitive indicators of hatchery stress in salmon. Aquaculture 223:175–187CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Dong Han
    • 1
  • Susie S. Y. Huang
    • 2
  • Wei-Fang Wang
    • 3
  • Dong-Fang Deng
    • 4
  • Silas S. O. Hung
    • 2
  1. 1.State Key Laboratory of Freshwater Ecology and BiotechnologyInstitute of Hydrobiology, Chinese Academy of SciencesWuhanPeople’s Republic of China
  2. 2.Department of Animal ScienceUniversity of California, DavisDavisUSA
  3. 3.Qingdao Key Laboratory for Marine Fish Breeding and BiotechnologyYellow Sea Fisheries Research Institute, Chinese Academy of Fishery SciencesQingdaoPeople’s Republic of China
  4. 4.Aquatic Feeds and Nutrition DepartmentOceanic InstituteHawaiiUSA

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