Skip to main content
SpringerLink
Log in

MnHSP90 cDNA characterization and its expression during the ovary development in oriental river prawn, Macrobrachium nipponense

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Heat shock protein 90 (HSP90) is not only involved in environmental stress but also plays roles in the ovary development in some vertebrates. To understand its role in crustacean, we examined the HSP90 cDNA for the first time in the ovary and hepatopancreas of the oriental river prawn, Macrobrachium nipponense and designated this protein as MnHSP90 in this study. The MnHSP90 was cloned by the methods of degenerated oligonucleotide primers and rapid amplification of the cDNA ends (RACE). Bioinformatics analysis showed that the MnHSP90 cDNA was 2,684 bp in length, containing a 126 bp 5′ untranslated region (UTR), a 359 bp 3′ UTR, and an open reading frame (ORF) of 2,199 bp encoding a 732-amino acid polypeptide with predicted molecular mass of 84.3 KDa. Sequence alignment showed that the MnHSP90 shared 72–79% identity with other animals. Real-time quantitative PCR (qPCR) analysis demonstrated that the MnHSP90 mRNA was ubiquitously detected in all tested tissues, with the highest expression in the thoracic ganglia, the mediate in heart, muscle and intestine, and the lowest in haemocytes and gills. The MnHSP90 mRNA levels in the hepatopancreas and ovary of M. nipponense reached a maximum at the stage III (early vitellogenic stage) and stage IV (later vitellogenic stage) ovaries, respectively, and then decreased significantly in both tissues as the ovarian development proceeded. The level of MnHSP90 expression in the hepatopancreas was higher than that in the ovary when compared with in the same ovarian developmental stage. Our results indicate that MnHSP90 is involved in ovarian development in oriental river prawn and may play a regulatory role in ovary maturation.

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

Similar content being viewed by others

References

  1. Picard D (2002) Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 59(10):1640–1648

    Article  CAS  PubMed  Google Scholar 

  2. Csermely P, Schnaider T, Soti C, Prohászka Z, Nardai G (1998) The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther 79(2):129–168

    Article  CAS  PubMed  Google Scholar 

  3. Wiech H, Buchner J, Zimmermann R, Jakob U (1992) Hsp90 chaperones protein folding in vitro. Nature 358(6382):169–170

    Article  CAS  PubMed  Google Scholar 

  4. Miyata Y, Yahara I (1992) The 90-kDa heat shock protein, HSP90, binds and protects casein kinase II from self-aggregation and enhances its kinase activity. J Biol Chem 267(10):7042–7047

    CAS  PubMed  Google Scholar 

  5. Miyata Y, Yahara I (1995) Interaction between casein kinase II and the 90-kDa stress protein, HSP90. Biochemistry 34(25):8123–8129

    Article  CAS  PubMed  Google Scholar 

  6. Schumacher RJ, Hurst R, Sullivan WP, McMahon NJ, Toft DO, Matts RL (1994) ATP-dependent chaperoning activity of reticulocyte lysate. J Biol Chem 269(13):9493–9499

    CAS  PubMed  Google Scholar 

  7. Nathan DF, Vos MH, Lindquist S (1997) In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc Natl Acad Sci USA 94(24):12949–12956

    Article  CAS  PubMed  Google Scholar 

  8. Freeman BC, Morimoto RI (1996) The human cytosolic molecular chaperones hsp90, hsp70 (hsc70) and hdj-1 have distinct roles in recognition of a non-native protein and protein refolding. EMBO J 15(12):2969–2979

    CAS  PubMed  Google Scholar 

  9. Du SJ, Li HQ, Bian YH, Zhong YW (2008) Heat-shock protein 90alpha1 is required for organized myofibril assembly in skeletal muscles of zebrafish embryos. Proc Natl Acad Sci USA 105(2):554–559

    Article  CAS  PubMed  Google Scholar 

  10. Yeyati PL, Bancewicz RM, Maule J, Van Heyningen V (2007) Hsp90 selectively modulates phenotype in vertebrate development. PLoS Genet 3(3):0431–0447

    Article  CAS  Google Scholar 

  11. Toft DO (1998) Recent advances in the study of hsp90 structure and mechanism of action. Trends Endocrinol Metab 9(6):238–243

    Article  CAS  PubMed  Google Scholar 

  12. Pratt WB, Toft DO (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18(3):306–360

    Article  CAS  PubMed  Google Scholar 

  13. Beato M, Klug J (2000) Steroid hormone receptors: an update. Hum Reprod Update 6(3):225–236

    Article  CAS  PubMed  Google Scholar 

  14. Brown MA, Zhu L, Schmidt C, Tucker PW (2007) Hsp90—from signal transduction to cell transformation. Biochem Biophys Res Commun 363(2):241–246

    Article  CAS  PubMed  Google Scholar 

  15. Caruso JA, Laird DW, Batist G (1999) Role of HSP90 in mediating cross-talk between the estrogen receptor and the Ah receptor signal transduction pathways. Biochem Pharmacol 58(9):1395–1403

    Article  CAS  PubMed  Google Scholar 

  16. Fliss AE, Benzeno S, Rao J, Caplan AJ (2000) Control of estrogen receptor ligand binding by hsp90. J Steroid Biochem Mol Biol 72(5):223–230

    Article  CAS  PubMed  Google Scholar 

  17. Soverchia L, Ruggeri B, Palermo F, Mosconi G, Cardinaletti G, Scortichini G, Gatti G, Polzonetti-Magni AM (2005) Modulation of vitellogenin synthesis through estrogen receptor beta-1 in goldfish (Carassius auratus) juveniles exposed to 17-beta estradiol and nonylphenol. Toxicol Appl Pharmacol 209(3):236–243

    Article  CAS  PubMed  Google Scholar 

  18. Orn S, Yamani S, Norrgren L (2006) Comparison of vitellogenin induction, sex ratio, and gonad morphology between zebrafish and Japanese medaka after exposure to 17alpha-ethinylestradiol and 17beta-trenbolone. Arch Environ Contam Toxicol 51(2):237–243

    Article  CAS  PubMed  Google Scholar 

  19. Arukwe A, Goksøyr A (2003) Eggshell and egg yolk proteins in fish: hepatic proteins for the next generation: oogenetic, population, and evolutionary implications of endocrine disruption. Comp Hepatol 2(1):1–21

    Article  Google Scholar 

  20. Yano I (1985) Induced ovarian maturation and spawning in greasy back shrimp, Metapenaeus ensis, by progesterone. Aquaculture 47:223–229

    Article  Google Scholar 

  21. Yano I, Hoshino R (2006) Effects of 17 β-estradiol on the vitellogenin synthesis and oocyte development in the ovary of kuruma prawn (Marsupenaeus japonicus). Comp Biochem Physiol A 144(1):18–23

    Google Scholar 

  22. Tiu SH, Hui JH, He JG, Tobe SS, Chan SM (2006) Characterization of vitellogenin in the shrimp Metapenaeus ensis: expression studies and hormonal regulation of MeVg1 transcription in vitro. Mol Reprod Dev 73(4):424–436

    Article  CAS  PubMed  Google Scholar 

  23. Jiang SG, Qiu LH, Zhou FL, Huang JH, Guo YH, 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(1):127–134

    Article  CAS  PubMed  Google Scholar 

  24. Wu LT, Chu KH (2008) Characterization of heat shock protein 90 in the shrimp Metapenaeus ensis: evidence for its role in the regulation of vitellogenin synthesis. Mol Reprod Dev 75(5):952–959

    Article  CAS  PubMed  Google Scholar 

  25. Gao X, Liu H, Xu J, Cai S (2006) Study on site of vitellogenin synthesis in the freshwater prawn Macrobrachium Nipponese. Biotechnol Bull (z1):437–413 (in Chinese)

  26. Wu P, Qi D, Chen L, Zhang H, Zhang X, Qin J, Hu S (2009) Gene discovery from an ovary cDNA library of oriental river prawn Macrobrachium nipponense by ESTs annotation. Comp Biochem Physiol D 4:111–120

    Google Scholar 

  27. Zhang F, Chen L, Wu P, Zhao W, Li E, Qin J (2009) cDNA cloning and expression of Ubc9 in the developing embryo and ovary of oriental river prawn, Macrobrachium nipponense. Comp Biochem Physiol B 155:288–293

    Article  PubMed  Google Scholar 

  28. Manchado M, Salas-Leiton E, Infante C, Ponce M, Asensio E, Crespo A, Zuasti E, Cañavate PJ (2008) Molecular characterization, gene expression and transcriptional regulation of cytosolic HSP90 genes in the flatfish Senegalese sole (Solea senegalensis Kaup). Gene 416(1–2):77–84

    Article  CAS  PubMed  Google Scholar 

  29. Li P, Zha J, Zhang ZH, Huang H, Sun HY, Song DX, Zhou KY (2009) Molecular cloning, mRNA expression, and characterization of HSP90 gene from Chinese mitten crab Eriocheir japonica sinensis. Comp Biochem Physiol B 153(3):229–235

    Article  PubMed  Google Scholar 

  30. Zhang XY, Zhang MZ, Zheng CJ, Liu J, Hu HJ (2009) Identification of two hsp90 genes from the marine crab, Portunus trituberculatus and their specific expression profiles under different environmental conditions. Comp Biochem Physiol C Toxicol Pharmacol 150(4):465–473

    Article  PubMed  Google Scholar 

  31. Li FH, Luan W, Zhang CS, Zhang JQ, Wang B, Xie YS, Li SH, Xiang JH (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(2):161–172

    Article  CAS  PubMed  Google Scholar 

  32. Buchner J (1999) HSP90 and Co.—a holding for folding. Trends Biochem Sci 24(4):136–141

    Article  CAS  PubMed  Google Scholar 

  33. Caplan AJ (1999) HSP90’s secrets unfold: new insights from structural and functional studies. Trends Cell Biol 9(7):262–268

    Article  CAS  PubMed  Google Scholar 

  34. 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(1):65–75

    Article  CAS  PubMed  Google Scholar 

  35. Gupta RS (1995) Phylogenetic analysis of the 90-kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. Mol Biol Evol 12(6):1063–1073

    CAS  PubMed  Google Scholar 

  36. Gao Q, Song LS, Ni DJ, Wu LT, Zhang H, Chang YQ (2007) cDNA cloning and mRNA expression of heat shock protein 90 gene in the haemocytes of Zhikong scallop Chlamys farreri. Comp Biochem Physiol B 147(4):704–715

    Article  PubMed  Google Scholar 

  37. Gao Q, Zhao JM, Song LS, Qiu LM, Yu YD, Zhang H, Ni DJ (2008) Molecular cloning, characterization and expression of heat shock protein 90 gene in the haemocytes of bay scallop Argopecten irradians. Fish Shellfish Immunol 24(4):379–385

    Article  CAS  PubMed  Google Scholar 

  38. Vamvakopoulos NO (1993) Tissue-specific expression of heat shock proteins 70 and 90: potential implication for differential sensitivity of tissues to glucocorticoids. Mol Cell Endocrinol 98(1):49–54

    Article  CAS  PubMed  Google Scholar 

  39. Itoh H, Toyoshima I, Mizunuma H, Kobayashi R, Tashima Y (1990) Three-step purification method and characterization of the bovine brain 90-kDa heat shock protein. Arch Biochem Biophys 282(2):290–296

    Article  CAS  PubMed  Google Scholar 

  40. Jin ZX, Ye HH, Li SJ, Huang HY, Wang GZ (2003) Role of nervous organs in stimulating ovarian maturation in the mud crab Scylla serrata: an in vitro study. Mar Sci 27(1):72–74 (in Chinese)

    CAS  Google Scholar 

  41. Kulkarni GK, Glade L, Fingerman M (1991) Oogensis and effects of neuroendocrine tissues on in vitro synthesis of protein by the ovary of the red swamp crayfish, Procambarus clarkii (Girard). J Crustac Biol 11(4):513–522

    Article  Google Scholar 

  42. Meusy JJ, Payen GG (1988) Female reproduction in Malacostracan Crustacea. Zool Sci 5(22):217–265

    Google Scholar 

  43. Yang WJ, Ohira T, Tsutsui N, Subramoniam T, Huong DT, Aida K, Wilder MN (2000) Determination of amino acid sequence and site of mRNA expression of four vitellins in the giant freshwater prawn, Macrobrachium rosenbergii. J Exp Zool 287(6):413–422

    Article  CAS  PubMed  Google Scholar 

  44. Xie S, Sun L, Liu F, Dong B (2009) Molecular characterization and mRNA transcript profile of vitellogenin in Chinese shrimp, Fenneropenaeus chinensis. Mol Biol Rep 36(2):389–397

    Article  CAS  PubMed  Google Scholar 

  45. Tsutsui N, Kawazoe I, Ohira T, Jasmani S, Yang W, Wilder MN, Aida K (2000) Molecular characterization of a cDNA encoding vitellogenin and its expression in the hepatopancreas and ovary during vitellogenesis in the kuruma prawn, Penaeus japonicus. Zool Sci 17(5):651–660

    Article  CAS  PubMed  Google Scholar 

  46. Tsang WS, Quackenbush LS, Chow BK, Tiu SH, He JG, Chan SM (2003) Organization of the shrimp vitellogenin gene: evidence of multiple genes and tissue specific expression by the ovary and hepatopancreas. Gene 303:99–109

    Article  CAS  PubMed  Google Scholar 

  47. Kung SY, Chan SM, Hui JH, Tsang WS, Mak A, He JG (2004) Vitellogenesis in the sand shrimp, Metapenaeus ensis: the contribution from the hepatopancreas-specific vitellogenin gene (MeVg2). Biol Reprod 71(3):863–870

    Article  CAS  PubMed  Google Scholar 

  48. Wong QW, Mak WY, Chu KH (2008) Differential gene expression in hepatopancreas of the shrimp Metapenaeus ensis during ovarian maturation. Mar Biotechnol (NY) 10(1):91–98

    Article  CAS  Google Scholar 

  49. Fairs NJ, Quinlan PT, Goad LJ (1990) Changes in ovarian unconjugated and conjugated steroid titers during vitellogenesis in Penaeus monodon. Aquaculture 89(1):83–99

    Article  CAS  Google Scholar 

  50. Quinitio ET, Yamauchi K, Hara A, Fuji A (1991) Profiles of progesterone and estradiol-like substances in the hemolymph of female Pandalus kessleri during an annual reproductive cycle. Gen Comp Endocrinol 81(3):343–348

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research has been supported by grants from the Chinese Natural Science Foundation (No. 30771670), National Key Project of Scientific and Technical Supporting Programs Funded by Ministry of Science and Technology of China (No. 2006BAD01A13), Zhejiang Key Science and Technology Program of China (No. 2006C12005), Yancheng Institute of Technology (No. XKY2009017) and in part by the E-institute of the Shanghai Municipal Education Commission (Project number E03009). The authors would like to thank Chuanjie Qin for reviewing the manuscript and his helpful suggestions.

Author information

Authors and Affiliations

  1. Department of Biology, East China Normal University, 200062, Shanghai, People’s Republic of China

    Weihong Zhao, Liqiao Chen, Ping Wu, Fengying Zhang & Erchao Li

  2. School of Chemical and Biological Engineering, Yancheng Institute of Technology, 224051, Yancheng, People’s Republic of China

    Weihong Zhao

  3. School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, SA, 5001, Australia

    Jianguang Qin

  4. Jiangsu Provincial Key Laboratory of Coastal Wetland Bioresources and Environmental Protection, Yancheng Teachers University, 224002, Yancheng, People’s Republic of China

    Boping Tang

Authors
  1. Weihong Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liqiao Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianguang Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ping Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fengying Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Erchao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Boping Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Liqiao Chen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, W., Chen, L., Qin, J. et al. MnHSP90 cDNA characterization and its expression during the ovary development in oriental river prawn, Macrobrachium nipponense . Mol Biol Rep 38, 1399–1406 (2011). https://doi.org/10.1007/s11033-010-0243-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-010-0243-7

Keywords

Search

Navigation