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Identification and Characterization of Three Differentially Expressed Ovarian Genes Associated with Ovarian Maturation in Yesso Scallop, Patinopecten yessoensis

  • Kim, Young-Ju (Department of Marine Biology, Pukyong National University) ;
  • Kang, Hye-Eun (Department of Marine Biology, Pukyong National University) ;
  • Cho, Gyu-Tae (Aquaculture Department, East Sea Fisheries Research Institute) ;
  • Suh, Young-Sang (Ecology and Oceanography Division, National Fisheries Research and Development Institute) ;
  • Yoo, Myong-Suk (Department of Marine Biology, Pukyong National University) ;
  • Kim, Hyun-Woo (Department of Marine Biology, Pukyong National University)
  • Published : 2009.12.31

Abstract

Despite great commercial interest, relatively little has been described about molecular mechanism of bivalve reproduction. We investigated genes involved in ovarian maturation of the Yesso scallop, Patinopecten yessoensis. GSI index and histological analysis revealed that maturation of ovary begin in February and spawning period is from April to June which is similar to the previous study in the East Sea. As result of combination analysis of differential display RTPCR (DDRT-PCR) and histological examination, vitellogenin (Vg), ferritin (Ft) and ADT/ATP carrier protein (ACC) were identified as differently expressed genes in maturating ovary. Endpoint RT-PCR results showed that Vg is ovary-specific genes whereas Ft and ACC are expressed ubiquitously suggesting that Vg can be good molecular markers for ovarian development and sex determination in bivalves. Quantitative PCR results revealed that Vg were expressed highest during growth stage and appears to play a major role in oocyte maturation. On the contrary, expression of Ft was highest after spawning stage, which suggests that up-regulation may be involved in spawning and inactive stages in which the scallops recover from spawning. In addition, high level of the mitochondrial gene, ACC, may play a role in energy metabolism in maturating oocytes. Isolation and molecular studies of these key genes will expand our knowledge of the physiological changes from various exogenous factors including temperature, salinity, pH, even or numerous endocrine disrupting chemicals (EDCs) during reproductive cycle. In addition, further study of these genes implicates various industrial applications including the stable seed production, increased food quality, or economic aquaculture system.

Keywords

References

  1. Abdelmajid H, Rivailler P, Krantic S and Guerrier P. 1994. Differences in tyrosine phosphorylation of oocyte key proteins during 5HT-inducedmεiosis reinitiation in two bivalve species. Exp Cell Res 212, 422-5 https://doi.org/10.1006/excr.1994.1163
  2. Abdu U, Davis C, Khalaila I and Sagi A. 2002. The vitellogenin cDNA of Cherax quadricarinatus encodes a lipoprotein with calcium binding ability, and its expression is induced following the removal of the androgenic gland in a sexually plastic system. Gen Comp Endocrinol 27, 263-72 https://doi.org/10.1016/S0016-6480(02)00053-9
  3. Beck G, Ellis TW, Habicht GS, Schluter SF and Marchalonis JJ. 2002. Evolution of the acute phase response: iron release by echinoderm (Astenas forbesi) coelomocytes, and cloning of an echinoderm ferritin molecule. Dev Comp Immunol 26, 11-26 https://doi.org/10.1016/S0145-305X(01)00051-9
  4. Boutet I, Moraga D, Marinovic L, Obreque J and ChavezCrooker P. 2008. Characterization of reproductionspecific genes in a marine bivalve mollusc: influence of maturation stage and sex on mRNA expression. Gene 407, 130-8 https://doi.org/10.1016/j.gene.2007.10.005
  5. Cummins JM. 2000. Fertilization and elimination of the patemal mitochondrial genome. Hum Reprod 15 SuppI 2, 92-101 https://doi.org/10.1093/humrep/15.suppl_2.92
  6. Davis GP and Hetzel DJS. 2000. Integrating molecular genetic technology with traditional approaches for genetic improvement in aquaculture species. Aqua Res. 31, 3-10 https://doi.org/10.1046/j.1365-2109.2000.00438.x
  7. Dukeman AK, Blake NJ and Amold WS. 2005. The reproductive cycle of the flame scallop, Ctenoides scaber (Bom 1778), from the lower Florida keys and its relationship with environmental conditions. J.shell. Res. 24, 341-351 https://doi.org/10.2983/0730-8000
  8. FAO. 2003. Fishery Statistics, Aquaculture Production. WWW.jao.org
  9. Fissore RA, Kurokawa M, Knott J, Zhang M and Smyth J. 2002. Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction 124, 745-54 https://doi.org/10.1530/rep.0.1240745
  10. Fleury E, Fabioux C, Lelong C, Favrel P and Huvet A. 2008. Characterization of a gonad-specific transforming growth factor-beta superfamily member differentially expressed during the reproductive cycle of the oyster Crassostrea gigas. Gene 410, 187-96 https://doi.org/10.1016/j.gene.2007.12.017
  11. Fong PP, Huminski PT and D'Urso LM. 1998. Induction and potentiation of parturition in fingemail clams (Sphaerium striatinum) by selective serotonin reuptake inhibitors (SSRIs). J Exp Zool 280, 260-4 https://doi.org/10.1002/(SICI)1097-010X(19980215)280:3<260::AID-JEZ7>3.0.CO;2-L
  12. Gagne F, Blaise C, Salazar M, Salazar S and Hansen PD. 2001. Evaluation of estrogenic effects of municipal effluents to the freshwatermussel Elliptio complanata. Comp Biochem Physiol C Toxicol Pharmacol 128, 213-25 https://doi.org/10.1016/S1532-0456(00)00189-7
  13. Gaulejac Bd, Henry M and Vicente N. 1995. An Ultrastructural study of gametogenesis of the marine bivalve Pinna novilis (LINNAEUS 1758).oogenesis J Moll. Stud. 61, 375-392 https://doi.org/10.1093/mollus/61.3.375
  14. Hirai S, Kishimoto T, Kadam AL, Kanatani H and Koide SS. 1988. Induction of spawning and oocyte maturation by 5-hydroxytryptamine in the surfclam. J Exp. Zool. 245, 318-321 https://doi.org/10.1002/jez.1402450312
  15. Hunt PA and Hassold TJ. 2002. Sex matters in meiosis. Science 296, 2181-3 https://doi.org/10.1126/science.1071907
  16. Jansen RP and de Boer K. 1998. The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate. Mol Cell Endocrinol 145, 81-8 https://doi.org/10.1016/S0303-7207(98)00173-7
  17. Kajiwara M, Kuraku S, Kurokawa T, Kato K, Toda S, Hirose H, Takahashi S, Shibata Y, Iguchi T, Matsumoto T et al. 2006. Tissue preferential expression of estrogεn receptor gene in the marine snail, Thais clavigera. Gen Comp Endocrinol 148, 315-26 https://doi.org/10.1016/j.ygcen.2006.03.016
  18. Kanda A, Takahashi T, Satake H and Minakata H. 2006. Molecular and functional characterization of a novel gonadotropin-releasing-hormone receptor isolatedfrom the common octopus (Octopus vulgaris). Biochem J 395, 125-35 https://doi.org/10.1042/BJ20051615
  19. Keay J, Bridgham JT and Thomton Jw. 2006. The Octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications. Endocrinolohgy 147, 3861-9 https://doi.org/10.1210/en.2006-0363
  20. Kim HW, Chang ES and Mykles DL. 2005. Three calpains and ecdysone receptor in the land crab Gecarcinus lateralis: sequences, expression and effects of elevated ecdysteroid induced by eyestalk ablation. J Exp Biol 208, 3177-97 https://doi.org/10.1242/jeb.01754
  21. Kim KS, Kim BK, Kim HJ, Yoo MS, Mykles DL and Kim HW. 2008. Pancreatic lipase-related protein (PYPLRP) highly expressed in the vitellogenic ovary of the scallop, Patinopecten yessoensis. Comp Biochem Physiol B Biochem Mol Biol 151, 52-8 https://doi.org/10.1016/j.cbpb.2008.05.009
  22. Kim YJ, Kwak CI, Gu YY, Hwang IT and Chun JY. 2004. Annealing control primer system for identification of diflìerentially expressed genes on agarose gels. Biotechniques 36, 424-6, 428, 430 passim
  23. Klee CB, Ren H and Wang X. 1998. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J Biol Chem 273, 13367-70 https://doi.org/10.1074/jbc.273.22.13367
  24. Le NT and Richardson DR. 2002. Thε role of iron in cell cycle progression and the proliferation of neoplastic cells. Biochim Biophys Acta 1603, 31-46 https://doi.org/10.1016/S0304-419X(02)00068-9
  25. Li Q, Osada M, Suzuki R and Mori K. 1998. Changes in vitellin during oogenesis and effect of estradiol-17$\beta$ on vitellogenesis in the Pacific oyster Crassostrea gigas. Invert. Reprod. Deν. 33, 87-89 https://doi.org/10.1080/07924259.1998.9652345
  26. Matsumoto T, Nakamura AM, Mori K, Akiyama I, Hirose H and Takahashi Y. 2007. Oyster estrogen receptor: cDNA cloning and immunolocalization. Gen Comp EndocrinoI 151, 195-201 https://doi.org/10.1016/j.ygcen.2007.01.016
  27. Matsumoto T, Nakamura AM, Mori K and Kayano T. 2003. Molecular characterization of a cDNA encoding putative vitellogenin from the Pacific oyster Crassostrea gigas. Zoolog Sci 20, 37-42 https://doi.org/10.2108/zsj.20.37
  28. Matsumoto T, Yamano K, Kitamura M and Hara A. 2008. Ovarian follicle cells are the site of vitellogenin synthesis in the Pacific abalone Haliotis discus hannai. Comp Biochem Physiol A Mol Integr Physiol 149, 293-8 https://doi.org/10.1016/j.cbpa.2008.01.003
  29. Okuno A, Yang WJ, Jayasankar V, Saido-Sakanaka H, Huong DT, Jasmani S, Atmomarsono M, Subramoniam T, Tsutsui N, Ohira T et al. 2002. Deduced primary structure of vitellogenin in thε giant freshwater prawn, Macrobrachium rosenbergii, and yolk processing during ovarian maturation. J Exp Zool 292, 417-29 https://doi.org/10.1002/jez.10083
  30. Osada M, Harata M, Kishida M and Kijima A. 2004a Molecular cloning and expression analysis of vitellogenin in scallop, Patinopecten yessoensis (Bivalvia, Mollusca). Mol Reprod Dev 67, 273-81 https://doi.org/10.1002/mrd.20020
  31. Osada M, Tawarayama H and Mori K. 2004b. Estrogεn synthesis in relation to gonadal development of Japanese scallop, Patinopecten yεssoensis: gonadalprofile and immunolocalization of P450 aromatase and estrogen. Comp Biochem Physiol B Biochem Mol Biol 139, 123-8 https://doi.org/10.1016/j.cbpc.2004.07.002
  32. Petersen-Mahrt SK, Han'is RS and Neubζrger MS. 2002. AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418, 99-103 https://doi.org/10.1038/nature00862
  33. Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP and Amaral A. 2009. Mitochondrial functionality in reproduction: from gonads and gametes to embryos and εmbryonic stem cells. Hum Reprod Update https://doi.org/10.1093/humupd/dmp016
  34. Raviv S, Pames S, Segall C, Davis C and Sagi A. 2006. Complete sequence of Litopenaeus vannamei (Crustacea: Decapoda) vitellogenin cDNA and its expression in endocrinologically induced sub-adult females. Gen Comp EndocrinoI 145, 39-50 https://doi.org/10.1016/j.ygcen.2005.06.009
  35. Rodet F, Lelong C, Dubos MP, Costil K and Favrel P. 2005. Molecular cloning of a molluscan gonadotropinreleasing hormone receptor orthologue specifically expressed in the gonad. Biochim Biophys Acta 1730, 187-95 https://doi.org/10.1016/j.bbaexp.2005.05.012
  36. Rodet F, Lelong C, Dubos MP and Favrel P. 2008. Altemative splicing of a single precursor mRNA generates two subtypes of Oonadotropin-Releasing Hormone receptor orthologues and their variants in the bivalve mollusc Crassostrea gigas. Gene 414, 1-9 https://doi.org/10.1016/j.gene.2008.01.022
  37. Salisbury JL, Suino KM, Busby R and Springett M. 2002. Centrin-2 is required for cεntriole duplication in mammalian cells. Curr Biol 12, 1287-92 https://doi.org/10.1016/S0960-9822(02)01019-9
  38. Sappington TW and Raikhel AS. 1998. Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochem Mol Bio128, 277-300 https://doi.org/10.1016/S0965-1748(97)00110-0
  39. Tanabε T, Osada M, Kyozuka K, Inaba K and Kijima A. 2006. A novel oocyte maturation arresting factor in the central nervous system of scallops inhibits serotonin-induced oocyte maturation and spawning of bivalve mollusks. Gen Comp Endocrinol 147, 352-61 https://doi.org/10.1016/j.ygcen.2006.02.004
  40. Thouas GA, Trounson AO, Wolvetang EJ and Jones GM. 2004. Mitochondral dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro. Biol Reprod 71, 1936-42 https://doi.org/10.1095/biolreprod.104.033589
  41. Tiu SH, Hui JH, He JO, Tobe SS and Chan SM. 2006. Characterization of vitellogenin in the shrimp Metapenaeus ensis: exprεssion studies and hormonal regulation of MeVg1 transcription in vitro. Mol Reprod Dev 73, 424-36 https://doi.org/10.1002/mrd.20433
  42. Tsutsui N, Kawazoe I, Ohira T, Jasmani S, Yang WJ, Wilder MN and 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. Zoolog Sci 17, 651-60 https://doi.org/10.2108/zsj.17.651
  43. Tsutsui N, Saido-Sakanaka H, Yang WJ, Jayasankar V, Jasmani S, Okuno A, Ohira T, Okumura T, Aida K and Wilder MN. 2004. Molecular characterization of a cDNA encoding vitellogenin in the coonstriped shrimp, Pandalus hypsinotus and site of vitellogenin mRNA exprεssion. J Exp Zoolog A Comp Exp Biol 301 , 802-14
  44. Uddin MJ, Park K-I, Kang D-H, Park Y-J and Choi K-S. 2007. Comparative reproductive biology of Yezo scallop, Patinopecten yessoensis, under two diffierent culture systems on the east coast of Korea. Aquaculture 265, 139-147 https://doi.org/10.1016/j.aquaculture.2007.01.047
  45. Uryu M, Nakatomi A, Watanabe M, Hatsuse R and Yazawa M. 2000. Molecular cloning of cDNA encoding two subunits of calcineurin from scallop testis: demonstration of stage-specific expression during maturation ofthe testis. J Biochem 127, 739-46 https://doi.org/10.1093/oxfordjournals.jbchem.a022665
  46. Varaksina GS and Varaksin AA. 1991. Effects of estradiol, progesterone,and testosterone on oogenesis of yezo scallop. Bio. Mora. 3, 61-68
  47. Wallace RA and Selman K. 1978. Oogenesis in Fundulus heteroclitus. I. Preliminary observations on oocyte maturation in vivo and in vitro. Dev Biol 62, 354-69 https://doi.org/10.1016/0012-1606(78)90222-1
  48. Wedekind JE, Dance OS, Sowden MP and Smith HC. 2003. Messenger RNA editing in mammals: newmembers of the APOBEC family seeking roles in the family business. Trends Gnet 19, 207-16 https://doi.org/10.1016/S0168-9525(03)00054-4
  49. Wolfrum U. 1995. Centrin in the photoreceptor cells of mammalian retinae. CeII Motil Cytoskeleton 32, 55-64 https://doi.org/10.1002/cm.970320107
  50. Wong H and Schotz MC. 2002. The lipase gene family. J Lipid Res 43, 993-9 https://doi.org/10.1194/jlr.R200007-JLR200
  51. Yoshikawa K, Okazaki IM, Eto T, Kinoshita K, Muramatsu M, Nagaoka H and Honjo. 2002. AID enzymeinduced hypermutation in an activeIy transcribedgene in fibroblasts. Science 296, 2033-6 https://doi.org/10.1126/science.1071556