Skip to main content
SpringerLink
Log in

Molecular characterization and expression analysis of a heat shock protein 90 gene from disk abalone (Haliotis discus)

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Heat shock protein 90s (hsp90s) are chaperones that contribute to the proper folding of cellular proteins and help animals cope with the cellular protein damages in stress conditions. In this study, an hsp90 gene was isolated from disc abalone (Haliotis discus). The complete nucleotide sequence of the hsp90 gene contains an open reading frame of 2,184 base pairs, encoding an 84 kDa protein. Disk abalone hsp90 shares high sequence similarity with other hsp90 family proteins. Although the phylogenetic analysis did not classify it into the hsp90α group, the inductivity of this gene was confirmed by heat shock and lipopolysaccharide (LPS) challenge test. Disk abalone hsp90 gene displayed a rapid and reversible induction response to both an exposure of typical heat shock and the LPS challenge. Once given the sublethal heat shock treatment, the transcription of disk abalone hsp90 gene was significantly up-regulated. With a recovery of 12 h, the transcription of disk abalone hsp90 gene gradually attenuated to the control level. These observations reflected the feedback regulation of abalone heat shock responses faithfully. In response to LPS challenge, the transcription of disk abalone hsp90 gene was significantly increased within 2 h and it approached maximum induction at 4 h later and recovered finally the reference level in 24 h. Take all together, the cloning and expression analysis of disk abalone hsp90 gene provided useful molecular information of abalone responses in stress conditions and potential ways to monitor the chronic stressors in abalone culture environments and diagnose the animal health status.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Csermeley P, Schnaider T, Soti C, Prohaszka Z, Nardai G (1998) The 90-kDa molecular chaperone family: structure, function and clinical applications—a comprehensive review. Pharmacol Ther 79:129–168

    Article  Google Scholar 

  2. Lindquist S, Craig E (1988) The heat shock proteins. Annu Rev Genet 22:631–677

    Article  PubMed  CAS  Google Scholar 

  3. Scholz GM, Hartson SD, Cartledge K, Volk L, Matts RL, Dunn AR (2001) The molecular chaperone hsp90 is required for signal transduction by wild-type Hck and maintenance of its constitutively active counterpart. Cell Growth Differ 12:409–417

    PubMed  CAS  Google Scholar 

  4. Buchner J (1999) Hsp90 & Co.: a holding for folding. Trends Biochem Sci 24:136–141

    Article  PubMed  CAS  Google Scholar 

  5. Iwama GK, Vijayan MM, Forsyth RB, Ackerman PA (1999) Heat shock proteins and physiological stress in fish. Am Zool 39:901–909

    CAS  Google Scholar 

  6. Sanders BM (1993) Stress proteins in aquatic organisms: an environmental perspective. Crit Rev Toxicol 23:49–75

    Article  PubMed  CAS  Google Scholar 

  7. Ojima N, Yamashita M, Watabe S (2005) Quantitative mRNA expression profiling of heat shock protein families in rainbow trout cells. Biochem Biophys Res Commun 329:51–57

    Article  PubMed  CAS  Google Scholar 

  8. Multhoff G (2006) Heat shock proteins in immunity. Handb Exp Pharmacol 172:279–304

    Article  PubMed  CAS  Google Scholar 

  9. Farcy E, Serpentini A, Fiévet B, Lebel JM (2007) Identification of cDNAs encoding HSP70 and HSP90 in the abalone Haliotis tuberculata: transcriptional induction in response to thermal stress in hemocyte primary culture. Comp Biochem and Physiol 146 B:540–550

    Article  Google Scholar 

  10. Manchado M, Salas-Leiton E, Infante C, Ponce M, Asensio E, Crespo A, Zuasti E, Canavate JP (2008) Molecular characterization, gene expression and transcriptional regulation of cytosolic HSP90 genes in the flatfish Senegalese sole (Solea senegalensis Kaup). Gene 416:77–84

    Article  PubMed  CAS  Google Scholar 

  11. Jiang S, Qiu L, Zhou F, Huang J, Guo Y, Yang K (2009) Molecular cloning and expression analysis of a heat shock protein (Hsp90) gene from black tiger shrimp (Penaeus monodon). Mol Biol Rep 36:127–134

    Article  PubMed  CAS  Google Scholar 

  12. Pan F, Zarate JM, Tremblay GC, Bradley TM (2000) Cloning and characterization of salmon hsp90 cDNA: upregulation by thermal and hyperosmotic stress. J Exp Zool 287:199–212

    Article  PubMed  CAS  Google Scholar 

  13. Li F, Luan W, Zhang C, Zhang J, Wang B, Xie Y, Li S, Xiang J (2009) Cloning of cytoplasmic heat shock protein 90 (FcHSP90) from Fenneropenaeus chinensis and its expression response to heat shock and hypoxia. Cell Stress Chaperones 14:161–172

    Article  PubMed  CAS  Google Scholar 

  14. Chang ES, Chang SA, Keller R, Reddy PS, Snyder MJ, Spees JL (1999) Quantification of stress in lobsters: crustacean hyperglycemic hormone, stress proteins, and gene expression. Am Zool 39:487–495

    CAS  Google Scholar 

  15. Gao Q, Song L, Ni D, Wu L, Zhang H, Chang Y (2007) cDNA cloning and mRNA expression of heat shock protein 90 gene in the haemocytes of Zhikong scallop Chlamys farreri. Comp Biochem Physiol 147 B:704–715

    Google Scholar 

  16. 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 91:245–254

    Article  PubMed  CAS  Google Scholar 

  17. Snyder MJ, Girvetz E, Mulder EP (2001) Induction of marine mollusc stress proteins by chemical or physical Stress. Arch Environ Contam Toxicol 41:22–29

    Article  PubMed  CAS  Google Scholar 

  18. Venn AA, Quinn J, Jones R, Bodnar A (2009) P-glycoprotein (multi-xenobiotic resistance) and heat shock protein gene expression in the reef coral Montastraea franksi in response to environmental toxicants. Aquat Toxicol 93:188–195

    Article  PubMed  CAS  Google Scholar 

  19. Cho WJ, Cha SJ, Do JW, Choi JY, Lee JY, Jeong CS, Cho KJ, Choi WS, Kang HS, Kim HD, Park JW (1997) A novel 90-kDa stress protein induced in fish cells by fish rhabdovirus infection. Biochem Biophys Res Commun 233:316–319

    Article  PubMed  CAS  Google Scholar 

  20. Young RA (1990) Stress proteins and immunology. Annu Rev Immunol 8:401–420

    Article  PubMed  CAS  Google Scholar 

  21. Gornati R, Papis E, Rimoldi S, Terova G, Saroglia M, Bernardini G (2004) Rearing density influences the expression of stress-related genes in sea bass (Dicentrarchus labrax L.). Gene 341:111–118

    Article  PubMed  CAS  Google Scholar 

  22. Cheng P, Liu X, Zhang G, He J (2007) Cloning and expression analysis of a HSP70 gene from Pacific abalone (Haliotis discus hannai). Fish Shellfish Immunol 22:77–87

    Article  PubMed  CAS  Google Scholar 

  23. Hooper C, Day R, Slocombe R, Handlinger J, Benkendorff K (2007) Stress and immune responses in abalone: limitations in current knowledge and investigative methods based on other models. Fish Shellfish Immunol 22:363–379

    Article  PubMed  CAS  Google Scholar 

  24. Pepin K, Momose F, Ishida N, Nagata K (2000) Molecular cloning of horse hsp90 cDNA and its comparative analysis with other vertebrate hsp90 sequences. J Vet Med Sci 63:115–124

    Article  Google Scholar 

  25. Csermely P, Kahn CR (1991) The 90-kDa heat shock protein (hsp-90) possesses an ATP binding site and autophoshporylating activity. J Biol Chem 266:4943–4950

    PubMed  CAS  Google Scholar 

  26. Prodromou C, Roe SM, O’Brien R, Ladbury JE, Piper PW, Pearl LH (1997) Identification and structural characterization of the ATP/ADP-binding site in the hsp90 molecular chaperone. Cell 90:65–75

    Article  PubMed  CAS  Google Scholar 

  27. Guerriero JP, Sullivan WP, Fadden P, Haystead TAJ, Clark J, Mimnaugh E, Krutzsch H, Ochel H, Schulte TW, Sausville E, Neckers LM, Toft DO (1997) The amino-terminal domain of heat shock protein 90 (hsp90) that binds geldanamycin is an ATP/ADP switch domain that regulates hsp90 conformation. J Biol Chem 272:23843–23850

    Article  Google Scholar 

  28. Stebbins CE, Russo AA, Schneider C, Rosen N, Hartl FU, Pavletich NP (1997) Crystal structure of an hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89:239–250

    Article  PubMed  CAS  Google Scholar 

  29. Carrello A, Ingley E, Minchin RF, Tsai S, Ratajczak T (1999) The common tetratricopeptide repeat acceptor site for steroid receptor-associated immunophilins and hop is located in the dimerization domain of hsp90. J Biol Chem 274:2682–2689

    Article  PubMed  CAS  Google Scholar 

  30. Gupta RS (1995) Phylogenetic analysis of the 90 kDa heat shock family of protein sequences and examination of the relationship among animals, plants, and fungi species. Mol Biol Evol 12:1063–1073

    PubMed  CAS  Google Scholar 

  31. Lees-Miller SP, Anderson CW (1989) The human double-stranded DNA-activated protein kinase phosphorylates the 90-kDa heat-shock protein, hsp90α at two NH2-terminal threonine residues. J Biol Chem 264:17275–17280

    PubMed  CAS  Google Scholar 

  32. Krone PH, Sass JB (1994) Hsp 90α and hsp 90β genes are present in the zebrafish and are differentially regulated in developing embryos. Biochem Biophys Res Commun 204:746–752

    Article  PubMed  CAS  Google Scholar 

  33. Voellmy R (2006) Feedback regulation of the heat shock response. Handb Exp Pharmacol 172:43–68

    Article  PubMed  CAS  Google Scholar 

  34. Pirkkala L, Nykanen P, Sistonen L (2001) Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J 15:1118–1131

    Article  PubMed  CAS  Google Scholar 

  35. Ahmed R, Duncan RF (2004) Translational regulation of hsp90 mRNA. J Biol Chem 279:49919–49930

    Article  PubMed  CAS  Google Scholar 

  36. Heine H, Delude RL, Monks BG, Espevik T, Golenbock DT (1999) Bacterial lipopolysaccharide induces expression of the stress response genes hop and H411. J Biol Chem 274:21049–21055

    Article  PubMed  CAS  Google Scholar 

  37. Triantafilou K, Triantafilou M, Dedrick RL (2001) A CD14-independent LPS receptor cluster. Nat Immunol 2:338–345

    Article  PubMed  CAS  Google Scholar 

  38. Triantafilou M, Triantafilou K (2004) Heat-shock protein 70 and heat-shock protein 90 associate with toll-like receptor 4 in response to bacterial lipopolysaccharide. Biochem Soc Trans 32:636–640

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Marine and Extreme Genome Research Center Program of Ministry of Marine time of land, Transportation and Marine time Affairs, Republic of Korea.

Author information

Authors and Affiliations

  1. Department of Marine Life Sciences, College of Ocean Science, Jeju National University, Jeju-si, 690-756, Republic of Korea

    Ning Wang & Jehee Lee

  2. Department of Life Science, Jeju National University, 66 Jejudaehakno, Ara-Dong, Jeju-si, 690-756, Republic of Korea

    Ilson Whang

  3. Department of Chemistry, College of Natural Sciences, Hanyang University, Seoul, 133-791, Republic of Korea

    Jae-Seong Lee

  4. Marine and Environmental Institute, Jeju National University, Jeju Special Self-Governing Province, Jeju-si, 690-814, Republic of Korea

    Jehee Lee

  5. Department of Marine Life Sciences, College of Ocean Science, Jeju National University, Jeju-si, 690-756, Republic of Korea

    Jehee Lee

Authors
  1. Ning Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ilson Whang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jae-Seong Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jehee Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jehee Lee.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 26 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, N., Whang, I., Lee, JS. et al. Molecular characterization and expression analysis of a heat shock protein 90 gene from disk abalone (Haliotis discus). Mol Biol Rep 38, 3055–3060 (2011). https://doi.org/10.1007/s11033-010-9972-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-010-9972-x

Keywords

Search

Navigation