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Differential Gene Expression in Hepatopancreas of the Shrimp Metapenaeus ensis During Ovarian Maturation

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Abstract

Differentially expressed genes were identified in the hepatopancreas of Metapenaeus ensis during ovarian maturation via differential display reverse transcription-polymerase chain reaction (DDRT-PCR). They are G-protein signaling modulator 2 (GPSM2), glutamate carboxypeptide II (GCPII), ligatin, C-type lectin, O-linked N-acetylglucosamine transferase (O-GlcNAc transferase), 1-acylglycerol-3-phosphate O-acyltransferase 4 (AGPAT4), vitellogenin (Vg), and hemocyanin. The hepatopancreas Vg gene identified in this study shows 92% and 49% amino acid sequence homology, respectively, to MeVg1 and MeVg2 previously isolated from this species, suggesting the identification of a new Vg gene in M. ensis. Vg gene expression was highest when the ovary was actively developing. The two metabolic enzymes, O-GlcNAc transferase and AGPAT4, exhibited a similar trend of expression to Vg gene, suggesting their involvement in Vg synthesis. The signal transduction related genes (GPSM2, GCPII, ligatin, and C-type lectin) were highly expressed in the hepatopancreas in the initial phase of maturation. These genes may be important for the signaling in the hepatopancreas for synthesis and mobilization of vitellogenin and nutrients to the developing ovary. The present work provides candidate genes for further investigation on the role of hepatopancreas in shrimp reproduction.

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References

  • Ayub Z, Ahmed M (2002) A description of the ovarian development stages of penaeid shrimps from the coast of Pakistan. Aquac Res 33, 767–776

    Article  Google Scholar 

  • Chan SM, Gu PL, Chu KH, Tobe SS (2003) Crustacean neuropeptide genes of the CHH/MIH/GIH family: implications from molecular studies. Gen Comp Endocr 134, 214–219

    Article  PubMed  CAS  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 

  • Dall W, Moriarty DJ (1983) “Functional aspects of nutrition and digestion”. In: The Biology of Crustacea, Volume 5, Bliss DE, Mantel LH, eds. (New York: Academic Press) pp 215–261

    Google Scholar 

  • Daniela M-D, Zdenek T, Vladimir V (1997) Assignment of the mouse ligatin gene (Lgtn) to chromosome 1F by in situ hybridization. Genomics 40, 192–193

    Article  Google Scholar 

  • Frost MR, Guggenheim JA (1999) Prevention of depurination during elution facilitates the reamplification of DNA from differential display gels. Nucleic Acids Res 27, e6

    Article  PubMed  CAS  Google Scholar 

  • Gibson R, Barker PL (1979) The decapod hepatopancreas. Oceanogr Mar Biol Ann Rev 17, 519–523

    Google Scholar 

  • Gross PS, Bartlett TC, Browdy CL, Chapman RW, Warr GW (2001) Immune gene discovery by expressed sequence tag analysis of hemocytes and hepatopancreas in the Pacific white shrimp, Litopenaeus vannamei, and the Atlantic white shrimp, L. setiferus. Dev Comp Immunol 25, 565–577

    Article  PubMed  CAS  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

    CAS  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  PubMed  CAS  Google Scholar 

  • Humason GL (1967) Animal Tissue Techniques. (San Francisco: WH Freeman), 569 pp

    Google Scholar 

  • Ivanova AV, Ivanov SV (2002) Differential display analysis of gene expression in yeast. Cell Mol Life Sci 59, 1241–1245

    Article  PubMed  CAS  Google Scholar 

  • Jayasankar V, Tsutsui N, Jasmani S, Saido-Sakanaka H, Yang W-J, Okuno A, Hien TTT, Aida K, Wilder MN (2002) Dynamics of vitellogenin mRNA expression and changes in hemolymph vitellogenin levels during ovarian maturation in the giant freshwater prawn Macrobrachium rosenbergii. J Exp Zool 293, 675–682

    Article  PubMed  CAS  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

    CAS  Google Scholar 

  • Khayat M, Funkenstein B, Tietz A, Lubzens E (1995) In vivo, in vitro and cell-free synthesis of hemocyanin in the shrimp Penaeus semisulcatus (de Haan). Comp Biochem Physiol B 112, 31–38

    Article  Google Scholar 

  • Khayat M, Yang W-J, Aida K, Nagasawa H, Tietz A, Funkenstein B, Lubzens E (1998) Hyperglycaemic hormones inhibit protein and mRNA synthesis in in vitro-incubated ovarian fragments of the marine shrimp Penaeus semisulcatus. Gen Comp Endocrinol 110, 307–318

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Liang P, Pardee AB (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 52, 6966–6988

    CAS  Google Scholar 

  • Lo TS, Cui ZX, Mong JLY, Wong QWL, Chan SM, Kwan HS, Chu KH (2007) Molecular coordinated regulation of gene expression during ovarian development in the penaeid shrimp. Mar Biotechnol 9, 459–468

    Google Scholar 

  • 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 

  • Maughan NJ, Lewis FA, Smith V (2001) An introduction to arrays. J Pathol 195, 3–6

    Article  PubMed  CAS  Google Scholar 

  • McCudden CR, Willard FS, Kimple RJ, Johnston CA, Hains MD, Jones MB, Siderovski DP (2005) Gα selectivity and inhibitor function of the multiple GoLoco motif protein GPSM2/LGN. Biochim Biophys Acta 1745, 254–264

    Article  PubMed  CAS  Google Scholar 

  • Millamena OM, Pascual FP (1990) Tissue lipid content and fatty acid composition of Penaeus monodon Fabricius broodstock from the wild. J World Aquac Soc 21, 116–121

    Article  Google Scholar 

  • Mourente G, Rodriguez A (1991) Variation in the lipid content of wild-caught females of the marine shrimp Penaeus kerathurus during sexual maturation. Mar Biol 110, 21–28

    Article  CAS  Google Scholar 

  • Qiu YW, Ng TB, Chu KH (1997) Purification and characterization of vitellin from the ovaries of the shrimp Metapenaeus ensis (Crustacea: Decapoda: Penaeidae). Invert Reprod Dev 31, 217–223

    CAS  Google Scholar 

  • Qiu G-F, Yamano K, Unuma T (2005) Cathepsin C transcripts are differentially expressed in the final stages of oocyte maturation in kuruma prawn Marsupenaeus japonicus. Comp Biochem Physiol B 140, 171–181

    Article  PubMed  CAS  Google Scholar 

  • Rainer J, Brouwer M (1993) Hemocyanin synthesis in the blue crab Callinectes sapidus. Comp Biochem Physiol B 104, 69–73

    Article  PubMed  CAS  Google Scholar 

  • Ruan H, Pownall HJ (2001) Overexpression of 1-acyl-glycerol-3-phosphate acyltransferase-alpha enhances lipid storage in cellular models of adipose tissue and skeletal muscle. Diabetes 50, 233–240

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch J, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press) 176 pp

    Google Scholar 

  • Simon HG (2002) Messenger RNA differential display strategies in birds and amphibians. Cell Mol Life Sci 59, 1264–1273

    Article  PubMed  CAS  Google Scholar 

  • Stein J, Liang P (2002) Differential display technology: a general guide. Cell Mol Life Sci 59, 1235–1240

    Article  PubMed  CAS  Google Scholar 

  • Sung YJ, Denman RB (1997) Use of two reverse transcriptases eliminates false-positive results in differential display. BioTechniques 23, 462–468

    PubMed  CAS  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  PubMed  CAS  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  CAS  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  CAS  PubMed  Google Scholar 

  • Tsutsui N, Ohira T, Kawazoe I, Takahashi A, Wilder MN (2007) Purification of sinus gland peptides having vitellogenesis-inhibiting activity from the whiteleg shrimp Litopenaeus vannamei. Mar Biotechnol 9, 360–369

    Google Scholar 

  • Virlon B, Cheval L, Buhler JM, Billon E, Doucet A, Elalouf JM (1999) Serial microanalysis of renal transcriptomes. Proc Natl Acad Sci USA 96, 15289–15292

    Article  Google Scholar 

  • Weis WI, Taylor ME, Drickamer K (1998) The C-type lectin superfamily in the immune system. Immunol Rev 163, 19–34

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Zegzouti H, Marty C, Jones B, Bouquin T, Latché A, Pech JC, Bouzayen M (1997) Improved screening of cDNAs generated by mRNA differential display enables the selection of true positives and the isolation of weakly expressed messages. Plant Mol Biol Rep 15, 236–245

    Article  CAS  Google Scholar 

  • Zhao Z-Y, Yin Z-X, Weng S-P, Guan H-J, Li S-D, Xing K, Chan S-M, He J-G (2007) Profiling of differentially expressed genes in hepatopancreas of white spot syndrome virus-resistant shrimp (Litopenaeus vannamei) by suppression subtractive hybridization. Fish Shellfish Immunol 22, 520–534

    Google Scholar 

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Acknowledgments

We thank K.C. Cheung and C.P. Li for technical assistance. The work described in this article was fully supported by a research grant from the Research Grants Council of the Hong Kong Special Administrative Region, China (Project No. CUHK4323/03M).

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Author notes

  1. Queenie W. L. Wong

    Present address: Department of Anatomical and Cellular Pathology, The Chinese University of Hong Kong, Shatin, Hong Kong, China

Authors and Affiliations

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

    Queenie W. L. Wong, Wai Yan Mak & Ka Hou Chu

  2. Department of Anatomical and Cellular Pathology, The Chinese University of Hong Kong, Shatin, Hong Kong, China

    Ka Hou Chu

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  1. Queenie W. L. Wong
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  2. Wai Yan Mak
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Correspondence to Ka Hou Chu.

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Wong, Q.W.L., Mak, W.Y. & Chu, K.H. Differential Gene Expression in Hepatopancreas of the Shrimp Metapenaeus ensis During Ovarian Maturation. Mar Biotechnol 10, 91–98 (2008). https://doi.org/10.1007/s10126-007-9042-0

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  • DOI: https://doi.org/10.1007/s10126-007-9042-0

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