THE DISCOVERY OF ESTROGEN RECEPTOR-BETA IN REPRODUCTIVE TISSUE OF MARINE POLYCHAETE, Perinereis nuntia BROODSTOCK

Main Article Content

Chotip Phoim
Patamaporn Sukplang
Acharawan Thongmee
Gun Anantasomboon

Abstract

The polychaete Perinereis nuntia, a tropical segmented marine worm species in Thailand, has been cultured and wildly used in commercial shrimp live-feed, especially for the penaeid shrimp broodstock. Study of reproductive tissue of the marine worm is necessary to improve its culturing procedure. The presumption of this study is that the reproductive sandworm may generate and use estrogen to control inter-cellular group for reproductive functions as was reported in Korean lugworm, P. aibuhitensis and other vertebrate species. Actions of estrogen at its target cells are commonly known since it binds with the estrogen receptor (ER). Six brooders of female and male P. nuntia at 5-6 months of age and 3 pre-reproductive animals at 3-4 months old were examined for sites of ERβ protein synthesis and deposition by using indirect immunohistochemistry. A tissue distribution analysis of ERβ revealed positive immunoreactions in various tissues of the female and male broodstock, including cytoplasm of oocytes, cluster of cells at the parapodia and the intestinal mucosa corresponding to their reproductive age as was characterized by histological analysis. This report describes the first tissue-specific ERβ expression in P. nuntia broodstock. The expressed ER in reproductive tissues was likely related to the process of reproductive cell generation and the completion of reproductive cells of the polychaete.

Article Details

How to Cite
1.
Phoim C, Sukplang P, Thongmee A, Anantasomboon G. THE DISCOVERY OF ESTROGEN RECEPTOR-BETA IN REPRODUCTIVE TISSUE OF MARINE POLYCHAETE, Perinereis nuntia BROODSTOCK. Interprof J Health Sci [Internet]. 2020 Jan. 31 [cited 2024 Dec. 22];18(2):59-68. Available from: https://li05.tci-thaijo.org/index.php/IJHS/article/view/38
Section
Research Articles

References

Bannister R, Beresford N, May D, Routledge EJ, Jobling S, Weaver MR. 2007. Novel estrogen receptor-related transcripts in Marisa coronaritis: a freshwater snail with reported sensitivity to estrogenic chemicals. Environ. Sci. Technol. 41: 2643-2650.

Bell TA, Lightner DV. 1988. A handbook of normal penaeid shrimp histology. World Aquaculture Society, Baton Rouge, LA.

Bhattacharya M, Peri K, Ribeiro-da-Silva A, Almazan G, Shichi H, Hou X, Chemtob S. 1999. Localization of functional prostaglandin E2 receptors EP3 and EP4 in the nuclear envelope. J. Biol. Chem. 274(22): 15719-24.

Bridgham JT, Brown JE, Rodriguez-Mari A, Catchen JM, Thomton JW. 2008. Evolution of a new function by degenerative mutation in cephalochordate steroid receptors. PLoS Genet 4:e1000191.

Browdy CL. 1992. A review of the reproductive biology of Penaeus species: perspectives on controlled shrimp maturation systems for high quality naupli production. In: Wyban, J. (Ed.), Proceedings of the Special Session on Shrimp Farming. The World Aquaculture Society, Baton Rouge, LA, USA, pp. 22–51.

Buhring SI, Christiansen B. 2001. Lipids in selected abyssal benthopelagic animals: link to the epipealagic zone prog. Oceanogr. 50: 369-82.

Cho SJ, Valles Y, Weisblat DA. 2015. Differential expression of conserved germ line markers and delayed segregation of male and female primordial germ cells in a hermaphrodite, the leech helobdella. Mol. Biol. Evol. 32(3): 833-4.

Darvas B, Szekacs A, Fonagy A, Szecsi M, Toth I. 1997. Progesterone in Periplaneta americana and Neobellieria bullata adults from the procuticle phase until first progeny production. Gen. Comp. Endocrinol. 107: 450–60.

Fingerman M, Nagabhushanam R, Sarojini R. 1993. Vertebrate-type hormones in crustaceans: localization, identification and functional significance. Zool. Sci. 18: 13–29.

Fujino H, Pierce K L, Srinivasan D, Protzman CE, Krauss AH, Woodward DF, Regan JW. 2000. Delayed reversal of shape change in cells expressing fpb prostanoid receptors possible role of receptor resensitization. J. Biol. Chem. 275(38): 29907-14.

Graeve M, Kattner G, Piepenburg D. 1997. Lipids in Arctic benthos: does the fatty acid and alcohol composition reflect feedingand trophic interactions Polar. Biol. 18: 53-61.

García-Alonso JAVIER, Rebscher N. 2005. Estradiol signaling in Nereis virens reproduction. Invertebr. Reprod. Dev. 48(1-3): 95-100.

Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Gustafsson JA. 2007. Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 87(3): 905-31.

Helliwell RJA, Berry EBE, O’Carroll SJ, Mitchell MD. 2004. Nuclear prostaglandin receptors: role in pregnancy and parturition? Prostaglandins, Leukot. Essent. Fatty Acids. 70(2): 149-65.

Hułas-Stasiak M, Gawron A. 2007. Immunohistochemical localization of estrogen receptors ERα and ERβ in the spiny mouse (Acomys cahirinus) ovary during postnatal development. J. Mol. Histol. 38(1): 25-32.

Kajiwara M, Kuraku S, Kurokawa T, Kato K, Toda S, Hirose H, Takahashi S, Shibata Y, Iguchi T, Matsumoto T, Miyata T, Miura T, Takahashi Y. 2006. Tissue preferential expression of estrogen receptor gene in the marine snail, Thais Clavigera. Gen. Comp. Endocrinol. 148: 315-26.

Katsu Y, Kubokawa K, Urushitani H, Iguchi T. 2010. Estrogen-dependent transactivation of amphioxus steroid hormone receptor via both estrogen and androgen response elements. Endocrinology. 151: 639-48.

Keay J, Bridgham JT, Thornton JW. 2006. The octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications. Endocrinology. 147: 3861-9.

Keay J, Thornton JW. 2009. Hormone-activated estrogen receptors in annelid invertebrates: implications for evolution and endocrine disruption. Endocrinology. 150: 1731-8.

LaFont R. 2000. The endocrinology of invertebrates. Ecotoxicology. 9(1–2): 41–57.

Li Q, Osada M, Suzuki T, Mori K. 1998. Changes in vitellin during oogenesis and effect of estradiol on vitellogenesis in the Pacific oyster Crassostrea gigas. Invert. Reprod. Dev. 33: 87-93.

Luis OJ, Passos AM. 1995. Seasonal changes in lipid content and composition of the polychaete Nereis (Hediste) diversicolor. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 111(4): 579-86.

Lv L, Dong X, Lv F, Zhao W, Yu Y, Yang W. 2017. Molecular cloning and characterization of an estrogen receptor gene in the marine polychaete Perinereis aibuhitensis. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 207: 15-21.

Lytle JS, Lytle TF, Ogle JT. 1990. Polyunsaturated fatty acid profiles as a comparative tool in assessing maturation diets of Penaeus vannamei. Aquaculture. 89(3): 287-99.

Maceren-Pates M, Kurita Y, Pates G, Yoshikuni M. 2015. A model for germ cell development in a fully segmented worm. Zoological Lett. 1(1): 34.

Marsden GE, McGuren JJ, Hansford SW, Burke MJ. 1997. A moist artificial diet for prawn broodstock: its effect on the variable reproductive performance of wild caught Penaeus monodon. Aquaculture. 149(1-2): 145-56.

Matozzo V, Marin MG. 2008. Can 17 β-estradiol inducevitellogenin-like proteins in the clam Tapes philippinarum. Environ. Toxicol. Pharmacol. 26: 38-44.

Matsumoto T, Nakamura AM, Mori K, Akiyama I, Hirose H, Takahashi Y. 2007. Oyster estrogen receptor: cDNA cloning and immunolocalization. Gen. Comp. Endocrinol. 151: 195-201.

Meunpol O, Meejing P, Piyatiratitivorakul S. 2005(b). Maturation diet based on fatty acid content for male Penaeus monodon (Fabricius) broodstock. Aquac. Res. 36(12): 1216-25.

Meunpol O, Iam-Pai S, Suthikrai W, Piyatiratitivorakul S. 2007. Identification of progesterone and 17α-hydroxyprogesterone in polychaetes (Perinereis sp.) and the effects of hormone extracts on penaeid oocyte development in vitro. Aquaculture. 270(1-4): 485-92.

Middleditch BS, Missler SR, Hines HB, McVey JP, Brown A, Ward DG, Lawrence AL. 1980. Metabolic profiles of penaied shrimp: dietary lipids and ovarian maturation. J. Chromatogr. 195(3): 359-68.

Nagasawa K, Treen N, Kondo R, Otoki Y, Itoh N, Rotchell JM, Osada M. 2015. Molecular characterization of an estrogen receptor and estrogen-related receptor and their autoregulatory capabilities in two Mytilus species. Gene. 564: 153–9.

Naessens E, Lavens P, Gomez L, Browdy CL, McGovern-Hopkins K, Spencer A, Kawahigashi D, Sorgeloos P. 1997. Maturation performance of Penaeus vannamei co-fed Artemia biomass preparations. Aquaculture. 155: 87–101.

Nelson ER. Habibi HR, 2013. Estrogen receptor function and regulation in fish and other vertebrates. Gen. Comp. Endocr. 192: 15-24.

Ni JB, Zeng Z, Ke CH. 2013. Sex steroid levels and expression patterns of estrogen receptor gene in the oyster Crassostrea angulata during reproductive cycle. Aquaculture. 376–379: 105-16.

Olive PJ. 1999. Polychaete aquaculture and polychaete science: a mutual synergism. Hydrobiologia. 402: 177-86.

Osada M, Takamura T, Sato H, Mori K. 2003. Vitellogenin synthesis in the ovary of scallop Patinopecten yessoensis: control by estradiol-17βand the central nervous system. J. Exp. Zool. 299: 172-9.

Paris M, Pettersson K, Schubert M, Bertrand S, Pongratz I, Escriva H, Laudet V. 2008. An amphioxus orthologue of the estrogen receptor that does not bind estradiol: insights into estrogen receptor evolution. BMC Evol. Biol. 8: 219.

Poltana P. 2005. Development of the polychaete Perinereis nuntia brevicirrus and its prostaglandin F2 alpha content in the atokous stage. 10th International Congress on Invertebrate Reproduction and Development 18-23 July 2004. Newcastle upon Tyne, UK. Abstract. (pp. 18-23).

Rebscher N, Zelada-Gonzalez F, Banishch TU, Raible F, Arendt D. 2007. Vasa unveils a common origin of germ cells and of somatic stem cells from the posterior growth zone in the polychaete Platynereis dumerilii. Dev. Biol. 306: 599-611.

Sar M, Welsch F. 1999. Differential expression of estrogen receptor-β and estrogen receptor-α in the rat ovary. Endocrinology. 140(2): 963-71.

Skipper JK, Hamilton TH. 1977. Regulation by estrogen of the vitellogenin gene. Proc. Natl Acad. Sci. 74(6): 2384-8.

Spaziani EP, Hinsch GW, Edwards SC. 1993. Changes in prostaglandin E 2 and F 2α during vitellogenesis in the Florida crayfish Procambarus paeninsulanus. J. Comp. Physiol. 163(7): 541-5.

Stange D, Sieratowicz A, Horres R,Oehimann J. 2011. Freshwater mud snail (Potamopyrgus antipodarum) estrogen receptor: identification and expression analysis under exposure to (xeno-) hormones. Ecotox. Environ. Safe. 75: 94-101.

Tran TKA, MacFarlane GR, Kong RYC, O’Connor WA, Yu RMK. 2016(b). Mechanistic insights into induction of vitellogenin gene expression by estrogens in Sydney rock oysters, Saccostrea glomerata. Aquat. Toxicol. 174: 146-58.

Wallen K. 2005. Hormonal influences on sexually differentiated behavior in nonhuman primates. Front. Neuroendocr. 26: 7-26.

Withyachumnarnkul B, Plodphai P, Nash G, Fegan D. 2002. Growth rate and reproductive performance of F4 domesticated Penaeus monodon broodstock. In The 3rd National Symposium of Marine Shrimp, November 8-9, 2001, Sirikit National Convention Center, Bangkok, Thailand, Biotechnology, National Science and Technology Development Agency, 33-40.