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Molecular Coordinated Regulation of Gene Expression During Ovarian Development in the Penaeid Shrimp

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Abstract

To understand the molecular events of ovarian development in penaeid shrimp, RNA arbitrarily primed polymerase chain reaction (RAP-PCR) was used to identify differentially expressed genes during ovarian maturation in Metapenaeus ensis. From a screening of 700 clones in a cDNA library of the shrimp ovary by the products of RAP-PCR of different maturation stages, 91 fragments with differentially expressed pattern as revealed by dot-blot hybridization were isolated and sequenced. Forty-two of these fragments show significant sequence similarity to known gene products and the differentially expressed pattern of 10 putative genes were further characterized via Northern hybridization. Putative glyceraldehyde–3–phosphate dehydrogenase and arginine kinase are related to provision of energy for active cellular function in oocyte development. Translationally controlled tumor protein, actin, and keratin are related to the organization of cytoskeleton to accomplish growth and development of oocytes. High mobility group protein DSP1, heat shock protein 70, and nucleoside diphosphate kinase may act as repressors before the onset of ovarian maturation. Peptidyl-prolyl cis-trans isomerase and glutathione peroxidase are related to the stabilization of proteins and oocytes. This study provides new insights on the molecular events in the ovarian development in the shrimp.

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References

  • Agou F, Raveh S, Veron M (2000) The binding mode of human nucleoside diphosphate kinase B to single-strand DNA. J Bioenerg Biomembranes 32, 285–292

    Article  Google Scholar 

  • 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  Google Scholar 

  • Benzie JAH (1998) Penaeid genetics and biotechnology. Aquaculture 164, 23–47

    Article  Google Scholar 

  • Bessman SP, Carpenter CL (1985) The creatine-creatine phosphate energy shuttle. Annu Res Biochem 54, 831–862

    Article  Google Scholar 

  • Bommer UA, Thiele BJ (2004) The translationally controlled tumour protein (TCTP). Int J Biochem Cell Biol 36, 379–385

    Article  Google Scholar 

  • Bongrazio M, Gräfe M, Pries AR, Gaehtgens P, Zakrzewicz A (2001) Improvement of RNA fingerprinting efficiency for the analysis of differential gene expression in human cardiac macro- and microvascular endothelial cells. Pharmacol Res 43, 553–560

    Article  Google Scholar 

  • Canaple L, Decoville M, Leng M, Locker D (1997) The Drosophia DSP1 gene encoding an HMG 1-like protein, genome organization, evolutionary conservation and expression. Gene 184, 285–290

    Article  Google Scholar 

  • Cariolou MA, Flytzanis CN (1993) Biochemical characterization of gonadal development in the shrimp Penaeus vannamei. Comp Biochem Physiol B 105, 579–584

    Article  Google Scholar 

  • Charmantier G, Charmantier-Daures M, Van Herp F (1997) Hormonal regulation of growth and reproduction in crustaceans. In: Recent Advances in Marine Biotechnology, Vol. I. Fingerman M, Nagabhushanam R, Thompson, MF, eds. (New York: Science Publishers), pp 109–161

    Google Scholar 

  • Chiou TT, Wu JL, Chen TT, Lu JK (2005) Molecular cloning and characterization of cDNA of penaeidin–like antimicrobial peptide from tiger shrimp (Penaeus monodon). Mar Biotechnol 7, 119–127

    Article  Google Scholar 

  • 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 

  • Das D, Scovell WM (2001) The binding interaction of HMG–1 with the TATA-binding protein/TATA complex. J Biol Chem 276, 32597–32605

    Article  Google Scholar 

  • Fingerman M (1997) Roles of neurotransmitters in regulating reproductive hormone release and gonadal maturation in decapod crustaceans. Invert Reprod Dev 31, 47–54

    Google Scholar 

  • Fingerman M, Nagabhushanam R (1997) Roles of neuroregulators in controlling the release of the growth and reproductive hormones in Crustacea. In: Recent Advances in Marine Biotechnology, Vol. I. Fingerman M, Nagabhushanam R, Thompson MF, eds. (New York: Science Publishers) pp 179–201

    Google Scholar 

  • Fischer G, Schmid F-X (1990) The mechanism of protein folding Implications of in vitro refolding models for de novo protein folding and translocation in the cell. Biochemistry 29, 2205–2212

    Article  Google Scholar 

  • Gachet Y, Tournier S, Lee M, Lazaris-Karatzas A, Poulton T, Bommer UA (1999) The growth–related, translationally controlled protein P23 has properties of a tubulin binding protein and associates transiently with microtubules during the cell cycle. J Cell Sci 112, 1257–1271

    Google Scholar 

  • Gard DL (1999) Confocal microscopy and 3-D reconstruction of the cytoskeleton of Xenopus oocytes. Microsc Res Tech 44, 388–414

    Article  Google Scholar 

  • Ge H, Roeder RG (1994) The high mobility group protein HMG1 can reversibly inhibit class II gene transcription by interaction with the TATA-binding protein. J Biol Chem 269, 17136–17140

    Google Scholar 

  • Gu P-L, Chan S-M (1998) Cloning of a cDNA encoding a putative molt–inhibiting hormone from the eyestalk of the sand shrimp Metapenaeus ensis. Mol Mar Biol Biotech 7, 214–220

    Google Scholar 

  • Gu P-L, Tobe SS, Chow BKC, Chu KH, He J-G, Chan S-M (2002) Characterization of an additional molt inhibiting hormone-like neuropeptide from the shrimp Metapenaeus ensis. Peptides 23, 1875–1883

    Article  Google Scholar 

  • Hamalainen HK, Tubman JC, Vikman S, Kyrölä T, Ylikoski E, Warrington JA, Lahesmaa R (2001) Identification and validation of endogenous reference genes for expression profiling of T helper cell differentiation by quantitative real-time RT-PCR. Anal Biochem 299, 63–70

    Article  Google Scholar 

  • Huberman A (2000) Shrimp endocrinology: a review. Aquaculture 191, 191–208

    Article  Google Scholar 

  • Kawazoe I, Jasmani S, Shih TW, Suzuki Y, Aida K (2000) Purification and characterization of vitellin from the ovary of kuruma prawn, Penaeus japonicus. Fish Res 66, 390–396

    Google Scholar 

  • Kim SY, Ferrell JE Jr, Chae SK, Lee KJ (2000) Inhibition of progesterone-induced Xenopus oocyte maturation by Nm23. Cell Growth Differ 11, 485–490

    Google Scholar 

  • Krol RM, Hawkins WE, Overstreet RM (1992) Reproductive components. In: Microscopic Anatomy of Invertebrates, Vol. 10. Harrison FW, Humes, AG eds. (New York: Wiley-Liss) pp 295–343

    Google Scholar 

  • Lee DO’C, Wickins JF (1992) Crustacean Farming. (Oxford: Blackwell), pp 132–133

    Google Scholar 

  • Liu F, Liu Y, Li F, Dong B, Xiang J (2005) Molecular cloning and expression profile of putative antilipopolysaccharide factor in Chinese shrimp (Fenneropenaeus chinensis). Mar Biotechnol 7, 600–608

    Article  Google Scholar 

  • Longyant S, Sithigorngul P, Thammapalerd N, Sithigorngul W, Menasveta P (2000) Characterization of vitellin and vitellogenin of giant tiger prawn Penaeus monodon using monoclonal antibodies specific to vitellin subunits. Invert Reprod Dev 37, 211–221

    Google Scholar 

  • Makinouchi S, Primavera JH (1987) Maturation and spawning of Penaeus indicus using different ablation method. Aquaculture 62, 73–81

    Article  Google Scholar 

  • Martinez-Gonzalez J, Hegardt FG (1995) Characterization of a cDNA encoding a cytosolic peptidylprolyl cis-trans-isomerase from Blattella germanica. Eur J Biochem 234, 284–292

    Article  Google Scholar 

  • McClelland M, Honeycutt R, Mathieu-Daude F, Vogt T, Welsh J (1997) Fingerprinting by arbitrarily primed PCR. In: Methods in Molecular Biology, Vol. 85. Liang P, Pardee AB, eds. (Totowa, NJ: Humana Press) pp 13–24

    Google Scholar 

  • Mohamed KS, Diwan AD (1994) Vitellogenesis in the Indian white prawn Penaeus indicus (Crustacea, Decapoda, Penaeidae). J Aquac Trop 9, 157–172

    Google Scholar 

  • Murakoshi M, Ikada R, Tagawa M (2003) Expression of prostatic glutathione-peroxidase (GSH–PO) in the rat treated with a combination of testosterone and 17β-estradiol. Tokai J Exp Clin Med 28, 45–50

    Google Scholar 

  • Plancha CE (1996) Cytokeratin dynamics during oocyte maturation in the hamster requires reaching of metaphase I. Differentiation 60, 87–98

    Article  Google Scholar 

  • Postel EH, Berberich SJ, Rooney JW, Kaetzel DM (2000) Human NM23/nucleoside diphosphate kinase regulates gene expression through DNA binding to nuclease-hypersensitive transcriptional elements. J Bioenerg Biomembranes 32, 277–284

    Article  Google Scholar 

  • Rapoport HS, Shadwick RE (2002) Mechanical characterization of an unusual elastic biomaterial from the egg capsules of marine snails (Busycon spp). Biomacromolecules 3, 42–50

    Article  Google Scholar 

  • Ravid T, Tietz A, Khayat M, Boehm E, Michelis R, Lubzens E (1999) Lipid accumulation in the ovaries of a marine shrimp Penaeus semisulcatus (De Haan). J Exp Biol 202, 1819–1829

    Google Scholar 

  • Richards JS, Russell DL, Ochsner SO, Espey LL (2002) Ovulation, new dimensions and new regulations of the inflammatory-like response. Annu Rev Physiol 64, 69–92

    Article  Google Scholar 

  • Rothschild CB, Brewer CS, Bowden DW (1997) DD/AP-PCR, combination of differential display and arbitrarily primed PCR of oligo(dT) cDNA. Anal Biochem 245, 48–54

    Article  Google Scholar 

  • Sakaji H, Tsuchiya K, Wa SS (2000) Oocyte development of Metapenaeus dalei (Penaeidae, Decapoda, Crustacea). Invert Reprod Dev 38, 7–12

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press)

    Google Scholar 

  • Silva Gunawardene YIN, Chow BKM, He JG, Chan SM (2001) The shrimp FAMeT cDNA is encoded for a putative enzyme involved in the methylfarnesoate (MF) biosynthetic pathway and is temporally expressed in the eyestalk of different sexes. Insect Biochem Mol Biol 31, 1115–1124

    Article  Google Scholar 

  • 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 

  • 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  Google Scholar 

  • Tseng DY, Chen YN, Kou GH, Lo CF, Kuo CM (2001) Hepatopancreas is the extraovarian site of vitellogenin synthesis in black tiger shrimp, Penaeus monodon. Comp Biochem Physiol A 129, 909–917

    Article  Google Scholar 

  • Tsukimura B, Kamemoto FJ (1991) In vitro stimulation of oocytes by presumptive mandibular organ secretions in the shrimp, Penaeus vannamei. Aquaculture 92, 59–66

    Article  Google Scholar 

  • Tsutsui N, Kawazoe I, Ohira T, Jasmani S, Yang WJ, 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, 651–660

    Article  Google Scholar 

  • Wang B, Li F, Dong B, Zhang X, Zhang C, Xiang J (2006) Discovery of the genes in response to white spot syndrome virus (WSSV) infection in Fenneropenaeus chinensis through cDNA microarray. Mar Biotechnol 8, 491–500

    Article  Google Scholar 

  • Warrier SR, Tirumalai R, Subramoniam T (2001) Occurrence of vertebrate steroids, estradiol 17β and progesterone in the reproducing females of the mud crab Scylla serrata. Comp Biochem Physiol A 130, 283–294

    Article  Google Scholar 

  • Welsh J, Chada K, Dalal SS, Cheng R, Ralph D, McClelland M (1992) Arbitrarily primed PCR fingerprinting of RNA. Nucleic Acids Res 20, 4965–4970

    Article  Google Scholar 

  • Williams K, Frayne J, Hall L (1998) Expression of extracellular glutathione peroxidase type 5 (GPX5) in the rat male reproductive tract. Mol Hum Reprod 4, 841–848

    Article  Google Scholar 

  • Wouters R, Molina C, Lavens P, Calderon J (2001) Lipid composition and vitamin content of wild female Litopenaeus vannamei in different stages of sexual maturation. Aquaculture 198, 307–323

    Article  Google Scholar 

  • Wuttke W, Pttzel L, Knoke I, Theiling K, Jarry H (1997) Immune–endocrine interactions affecting luteal function in pigs. J Reprod Fertil Suppl 52, 19–29

    Google Scholar 

  • Yamano K, Qiu GF, Unuma T (2004) Molecular cloning and ovarian expression profiles of thrombospondin, a major component of cortical rods in mature oocytes of penaeid shrimp, Marsupenaeus japonicus. Biol Reprod 70, 1670–1678

    Article  Google Scholar 

  • Yan L, Fei K, Bridge D, Sarras MP Jr (2000) A cnidarian homologue of translationally controlled tumor protein (P23/TCTP). Dev Genes Evol 210, 507–511

    Article  Google Scholar 

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Acknowledgments

We thank the staff of the Simon F.S. Li Marine Science Laboratory of The Chinese University of Hong Kong for their assistance in acquiring the shrimp for the present study. We also thank W.Y. Mak for technical assistance in preparing the manuscript and Grace S.W. Leung for reading the manuscript. The work described in this article was fully supported by grants from the Research Grants Council of the Hong Kong Special Administrative Region, China (Project nos. CUHK4323/03M, to K.H.C. and HKU7322/03M, to S.M.C.).

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Authors and Affiliations

  1. Department of Biology, The Chinese University of Hong Kong, Shatin, Hong Kong, China

    Ting Sze Lo, Zhaoxia Cui, Janice L.Y. Mong, Queenie W.L. Wong, Hoi Shan Kwan & Ka Hou Chu

  2. Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China

    Zhaoxia Cui

  3. Department of Zoology, The University of Hong Kong, Pokfulam Road, Hong Kong, China

    Siu-Ming Chan

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  1. Ting Sze Lo
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Correspondence to Ka Hou Chu.

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Addendum in proof

Since the submission of the manuscript, Loonygai et al. have reported a higher concentration of the translationally controlled tumor protein (TCTP, one of the genes isolated in the present study) at the early stage of ovarian development in Penaeus merguiensis, suggesting its role in shrimp ovarian maturation as implicated in the present study (see Loonygai et al., Cloning and expression of a TCTP homolog from the ovaries of banana prawn. Mar Biol 150, 455–462, 2007).

Present addresses:

T.S. Lo, Department of Applied Science, Hong Kong Institute of Vocational Education, Chai Wan, Hong Kong, China J.L.Y. Mong, Department of Biochemistry, The Chinese University of Hong Kong, Shatin, Hong Kong, China Q.W.L. Wong, Department of Anatomical and Cellular Pathology, The Chinese University of Hong Kong, Shatin, Hong Kong, China

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Lo, T.S., Cui, Z., Mong, J.L. et al. Molecular Coordinated Regulation of Gene Expression During Ovarian Development in the Penaeid Shrimp. Mar Biotechnol 9, 459–468 (2007). https://doi.org/10.1007/s10126-007-9006-4

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  • DOI: https://doi.org/10.1007/s10126-007-9006-4

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