Skip to main content

Advertisement

SpringerLink
Log in

Comparative proteomic profiling during ovarian development of the shrimp Metapenaeus ensis

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Two-dimensional electrophoresis and mass spectrometry were used to identify proteins that are differentially expressed during ovarian maturation in Metapenaeus ensis. 87 spots with consistently significant quantitative differences (≥1.5-fold for vol%) among stage I, III and V ovaries were chosen for MS/MS analysis. 45 spots were significantly matched to known proteins in the database (Mascot score >40). Half of them were down-regulated, in contrast to 9 out of 45 proteins that were up-regulated as ovarian maturation proceeded. Functionally, these identified proteins could be classified into five major groups, including cytoskeleton (11 %), metabolism (18 %), signal transduction (32 %), gene expression (14 %) and immune response (7 %). Among the differentially expressed reproduction-related proteins, the mRNA expression level of cellular retinoic acid/retinol binding protein in M. ensis (MeCRABP) during ovarian maturation was further characterized by quantitative real-time PCR. It was down-regulated during ovarian maturation. In situ hybridization further revealed that MeCRABP transcript was localized in ooplasm of previtellogenic oocytes but not in vitellogenic oocytes. These results demonstrate the application of proteomic analysis for identification of proteins involved in shrimp ovarian maturation and they provide new insights into ovarian development.

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. Khayat M, Babin PJ, Funkenstein B, Sammar M, Nagasawa H, Tietz A, Lubzens E (2001) Molecular characterization and high expression during oocyte development of a shrimp ovarian cortical rod protein homologous to insect intestinal peritrophins. Biol Reprod 64:1090–1099

    Article  CAS  PubMed  Google Scholar 

  2. 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 71:863–870

    Article  CAS  PubMed  Google Scholar 

  3. 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 73:424–436

    Article  CAS  PubMed  Google Scholar 

  4. Lo TS, Cui Z, Mong JL, Wong QW, Chan SM, Kwan HS, Chu KH (2007) Molecular coordinated regulation of gene expression during ovarian development in the penaeid shrimp. Mar Biotechnol (NY) 9:459–468

    Article  CAS  Google Scholar 

  5. Loongyai W, Phongdara A, Chotigeat W (2007) Cloning and expression of a TCTP homolog from the ovaries of banana prawn. Mar Biol 150:455–462

    Article  CAS  Google Scholar 

  6. 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 75:952–959

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  8. Zhou F, Jiang S, Huang J, Qiu L, Zhang D, Su T (2011) Molecular analysis of the QM gene from Penaeus monodon and its expression on the different ovarian stages of development. Mol Biol Rep 38:1921–1927

    Article  CAS  PubMed  Google Scholar 

  9. Karoonuthaisiri N, Sittikankeaw K, Preechaphol R, Kalachikov S, Wongsurawat T, Uawisetwathana U, Russo JJ, Ju J, Klinbunga S, Kirtikara K (2009) ReproArray(GTS): a cDNA microarray for identification of reproduction-related genes in the giant tiger shrimp Penaeus monodon and characterization of a novel nuclear autoantigenic sperm protein (NASP) gene. Comp Biochem Physiol D 4:90–99

    Google Scholar 

  10. Vitale AM, Calvert ME, Mallavarapu M, Yurttas P, Perlin J, Herr J, Coonrod S (2007) Proteomic profiling of murine oocyte maturation. Mol Reprod Dev 74:608–616

    Article  CAS  PubMed  Google Scholar 

  11. Bhojwani M, Rudolph E, Kanitz W, Zuehlke H, Schneider F, Tomek W (2006) Molecular analysis of maturation processes by protein and phosphoprotein profiling during in vitro maturation of bovine oocytes: a proteomic approach. Cloning Stem Cells 8:259–274

    Article  CAS  PubMed  Google Scholar 

  12. Ellederova Z, Halada P, Man P, Kubelka M, Motlik J, Kovarova H (2004) Protein patterns of pig oocytes during in vitro maturation. Biol Reprod 71:1533–1539

    Article  CAS  PubMed  Google Scholar 

  13. Sato K, Iwasaki T, Sakakibara K, Itakura S, Fukami Y (2002) Towards the molecular dissection of fertilization signaling: our functional genomic/proteomic strategies. Proteomics 2:1079–1089

    Article  CAS  PubMed  Google Scholar 

  14. Knoll-Gellida A, Andre M, Gattegno T, Forgue J, Admon A, Babin PJ (2006) Molecular phenotype of zebrafish ovarian follicle by serial analysis of gene expression and proteomic profiling, and comparison with the transcriptomes of other animals. BMC Genomics 7:46

    Article  PubMed Central  PubMed  Google Scholar 

  15. Cardoen D, Ernst UR, Boerjan B, Bogaerts A, Formesyn E, de Graaf DC, Wenseleers T, Schoofs L, Verleyen P (2012) Worker honeybee sterility: a proteomic analysis of suppressed ovary activation. J Proteome Res 11:2838–2850

    Article  CAS  PubMed  Google Scholar 

  16. Talakhun W, Roytrakul S, Phaonakrop N, Kittisenachai S, Khamnamtong B, Klinbunga S, Menasveta P (2012) Identification of reproduction-related proteins and characterization of the protein disulfide isomerase A6 cDNA in ovaries of the giant tiger shrimp Penaeus monodon. Comp Biochem Physiol D 7:180–190

    CAS  Google Scholar 

  17. Wilhelm D, Huang E, Svingen T, Stanfield S, Dinnis D, Koopman P (2006) Comparative proteomic analysis to study molecular events during gonad development in mice. Genesis 44:168–176

    Article  CAS  PubMed  Google Scholar 

  18. Chu KH, Tam YK, Chung CK, Ng WL (1993) Morphometric relationships and reproductive maturation of the shrimp, Metapenaeus ensis, from commercial catches in Hong Kong. Fish Res 18:187–197

    Article  Google Scholar 

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

    Article  Google Scholar 

  20. Teshima S, Kanazawa A (1983) Variation in lipid compositions during the ovarian maturation of the prawn. Jap Soc Sci Fish 49:957–962

    Article  CAS  Google Scholar 

  21. Tan-Fermin JD, Pudadera RA (1989) Ovarian maturation stages of the wild giant tiger prawn, Penaeus monodon Fabricius. Aquaculture 77:229–242

    Article  Google Scholar 

  22. Sakaji H, Tsuchiya K, Segawa S (2000) Oocyte development of Metapenaeopsis dalei (Penaeidae, Decapoda, Crustacea). Invertebr Reprod Dev 38:7–12

    Article  Google Scholar 

  23. Tada T, Endo M, Hirono I, Takashima F, Aoki T (2002) Differential expression and cellular localization of activin and inhibin mRNA in the rainbow trout ovary and testis. Gen Comp Endocrinol 125:142–149

    Article  CAS  PubMed  Google Scholar 

  24. Zhong MQ (2005) Alteration in cellular defense and metabolism in diabetes and virus infection: a proteomic approach. Thesis, The Chinese University of Hong Kong: P, 36

  25. Cariolou MA, Flytzanis CN (1993) Biochemical characterization of gonadal development in the shrimp Penaeus vannamei. Comp Biochem Physiol B 105:570–684

    Google Scholar 

  26. Clark TG, Merriam RW (1977) Diffusible and bound actin nuclei of Xenopus laevis oocytes. Cell 12:883–891

    Article  CAS  PubMed  Google Scholar 

  27. Bohnsack MT, Stuven T, Kuhn C, Cordes VC, Gorlich D (2006) A selective block of nuclear actin export stabilizes the giant nuclei of Xenopus oocytes. Nat Cell Biol 8:257–263

    Article  CAS  PubMed  Google Scholar 

  28. Allworth AE, Albertini DF (1993) Meiotic maturation in cultured bovine oocytes is accompanied by remodeling of the cumulus cell cytoskeleton. Dev Biol 158:101–112

    Article  CAS  PubMed  Google Scholar 

  29. Uawisetwathana U, Leelatanawit R, Klanchui A, Prommoon J, Klinbunga S, Karoonuthaisiri N (2011) Insights into eyestalk ablation mechanism to induce ovarian maturation in the black tiger shrimp. PLoS One 6:e24427

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Yano I (1987) Effect of 17β-hydroxy-progesterone on vitellogenin secretion in kuruma prawn, Penaeus japonicus. Aquaculture 61:49–57

    Article  CAS  Google Scholar 

  31. Preechaphol R, Klinbunga S, Yamano K, Menasveta P (2010) Molecular cloning and expression of progestin membrane receptor component 1 (Pgmrc1) of the giant tiger shrimp Penaeus monodon. Gen Comp Endocrinol 168:440–449

    Article  CAS  PubMed  Google Scholar 

  32. Paolucci M, Di Cristo C, Di Cosmo A (2002) Immunological evidence for progesterone and estradiol receptors in the freshwater crayfish Austropotamobius pallipes. Mol Reprod Dev 63:55–62

    Article  CAS  PubMed  Google Scholar 

  33. Quinitio ET, Hara A, Yamauchi K, Nakao S (1994) Changes in the steroid hormone and vitellogenin levels during the gametogenic cycle of the giant tiger shrimp, Penaeus monodon. Comp Biochem Physiol C 109:21–26

    Google Scholar 

  34. Dugaiczyk A, Haron JA, Stone EM, Dennison OE, Rothblum KN, Schwartz RJ (1983) Cloning and sequencing of a deoxyribonucleic acid copy of glyceraldehyde-3-phosphate dehydrogenase messenger ribonucleic acid isolated from chicken muscle. Biochemistry 22:1605–1613

    Article  CAS  PubMed  Google Scholar 

  35. Ellington WR (2001) Evolution and physiological roles of phosphagen systems. Annu Rev Physiol 63:289–325

    Article  CAS  PubMed  Google Scholar 

  36. Liñá-Cabello MA, Medina-Zendejas R, Sánchez-Barajas M, Mena HA (2004) Effects of carotenoids and retinol in oocyte maturation of crayfish Cherax quadricarinatus. Aquac Res 35:905–911

    Article  Google Scholar 

  37. Gu PL, Gunawardene YI, Chow BC, He JG, Chan SM (2002) Characterization of a novel cellular retinoic acid/retinol binding protein from shrimp: expression of the recombinant protein for immunohistochemical detection and binding assay. Gene 288:77–84

    Article  CAS  PubMed  Google Scholar 

  38. Abrieu A, Doree M, Fisher D (2001) The interplay between cyclin-B-Cdc2 kinase (MPF) and MAP kinase during maturation of oocytes. J Cell Sci 114:257–267

    CAS  PubMed  Google Scholar 

  39. Ponza P, Yocawibun P, Sittikankaew K, Hiransuchalert R, Yamano K, Klinbunga S (2011) Molecular cloning and expression analysis of the mitogen-activating protein kinase 1 (MAPK1) gene and protein during ovarian development of the giant tiger shrimp Penaeus monodon. Mol Reprod Dev 78:347–360

    Article  CAS  PubMed  Google Scholar 

  40. Visudtiphole V, Klinbunga S, Kirtikara K (2009) Molecular characterization and expression profiles of cyclin A and cyclin B during ovarian development of the giant tiger shrimp Penaeus monodon. Comp Biochem Physiol A 152:535–543

    Article  Google Scholar 

Download references

Acknowledgments

We thank the staff of the Simon F. S. Li Marine Science Laboratory of The Chinese University of Hong Kong (CUHK) for their technical assistance. We are indebted to Dr. Arthur C. K. Chung and Dr. David Wilmshurst (CUHK) for their constructive comments on the drafts of this manuscript. The work described in this paper was supported by a Ph.D. Scientific Research Foundation of Beijing Hospital (BJ-2012-187) to J. C. and a grant from the Hong Kong Research Grants Council (CUHK4323/03M) to K.H.C.

Author information

Authors and Affiliations

  1. The Key Laboratory of Geriatrics, Beijing Hospital and Beijing Institute of Geriatrics, Ministry of Health, Da Hua Road, Beijing, 100730, China

    Ju Cui

  2. Simon F. S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Shatin, NT, Hong Kong SAR, China

    Ju Cui, Long Tao Wu & Ka Hou Chu

  3. Department of Medicine, Northwestern University, Chicago, IL, 60611, USA

    Long Tao Wu

Authors
  1. Ju Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Long Tao Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ka Hou Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ju Cui.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 27 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cui, J., Wu, L.T. & Chu, K.H. Comparative proteomic profiling during ovarian development of the shrimp Metapenaeus ensis . Mol Biol Rep 41, 519–528 (2014). https://doi.org/10.1007/s11033-013-2887-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-013-2887-6

Keywords

Search

Navigation