Oogenesis and Localization of Progesterone Receptors in Ovary of Oratosquilla nepa
Abstract
The objective of this study was to describe histological characteristics of the female germ cells and to characterize progesterone receptors expression in the ovary of Oratosquilla nepa. The histology of the ovary demonstrated subsequent stages of development of the oocytes. According to their cellular characteristics, oogonia and 5 types of oocytes were classified : early chromatin nucleolus (Oc1), late chromatin nucleolus (Oc2), previtellogenic oocyte (Oc3), vitellogenic oocyte (Oc4) and mature oocyte (Oc5). Oogonium has condensed basophilic heterochromatin which is usually located near the nuclear membrane. Oc1 has a round nucleus containing dispersed heterochromatin. Oc2 has a round nucleus with 1-2 nucleoli, basophilic cytoplasm. Oc3 are larger, cytoplasm fill with vacuolated globules. Oc4 is characterized by the appearance of yolk granules in cytoplasm. Oc5 is the largest of the germ cells. The cytoplasm is filled with yolk plates stained orange color with hematoxylin-eosin. Progesterone receptor y immunoreactivity was detected in cytoplasm of Oc2 and follicular cells of Oc3, Oc4 and Oc5. In contrast, there was no progesterone receptor immunoreactivity was observed in oogonia and Oc1. Keywords: Oratosquilla nepa, oocyte development, progesterone receptorReferences
Abdu,U., Yehezkel, G., Saki, A. (2000). Oocyte development and polypeptide dynamics during ovarian maturation
in the red-claw crayfish Cherax quadricarinatus. Invertebrate Reproduction and Development, 37, 75-83.
Ando, H. Makioka, T. (1998). Structure of the ovary and mode of oogenesis in a fresh water crayfish,
Procambarus clarkii (Girard). Zoological Science, 15, 893-901.
Ando, H. Makioka, T. (1999). Structure of the ovary and Mode of oogenesis in a freshwater crab (Potamon
dehaani. Journal of morphology, 239, 107-114.
Braga, A.A. Nunes , E.T. López-Grecco, L.S. Camargo-Mathias, M.I., Fransozo, V. (2016). Histological and
histochemical features of the oogenesis in the simultaneous protandric hermaphrodite shrimp
Exhippolysmata oplophoroides (Decapoda: Caridea). Micron, 88,60-67.
Chang, C.F. Shih, T.W. (1995). Reproductive cycle of ovarian development and vitellogenin profiles in the
freshwater prawns, Macrobrachium rosenbergii. Invertebrate Reproduction and Development, 27,
11–20.
Costa, T.M.C. Negreiros-Fransozo, M.L. (1998). The reproductive cycle of Callinectes danae Smith, 1869
(Decapoda, Portunidae) in the Ubatuba region, Brazil. Crustaceana, 71, 615-627.
Couch, E.F.,Hagino, N., Lee, J.W. (1987). Changes in estradiol and progesterone immunoreactivity in tissues of
the lobster, Homarus americanus, with developing and immature ovaries. Comparative Biochemistry
Physiollogy, 85A, 765-770.
Desouza, L.P., Silva, J.R.F. (2009). Morphology of the female reproductive system of the red clawed
mangrove tree crab (Goniopsis cruentata Latreille, 1803). Scientia Marina, 73, 527-539.
Di Cosmo, A., Paolucci, M., Di Cristo, C., Botte V. Ciarcia,G. 1998. Progesterone and 17β -estradiol involment in
the yolk protein synthesis in the ovary of Octopus vulgaris. Molecular Reproduction and Development,
50,451-460
El-Sherifa ,S, S., El-Khodary, G.M., Ghonimb A.M. (2012). Ovarian cycle and scanning electron micrographs
of the spawned egg of female mantis shrimp Oratosquilla massavensis (Alexandria, Egypt).
The Journal of Basic and Applied Zoology, 65, 116-124.
Fairs, N., Quinlan, P., Goad, L. (1990) Changes in ovarian unconjugated and conjugated steroid titers during
vitellogenesis in Penaeus monodon. Aquaculture, 89, 83-99.
Feng, L., Wu, X.G., Lu, J.F., Liu Z.J., Cheng, Y.X. (2009). Changes of progesterone and 17β-estradiol
concentrations in ovary, hepatopancreas, and hemolymph of swimming crab Portunus trituberculatus
during the reproductive cycle. Journal of Fish China, 33, 86.
Ferreira, M.A.P., Resende, B.M., Lima, M.Y.S., Santos, S.S.D., Rocha, R.M. ( 2012). The stages of ovarian
development affects organ expression of vitellogenin as well as the morphometry and ultrastructure of
germ cells in the freshwater prawn Macrobrachium amazonicum (Heller, 1862), Theriogenology 78,
981–990.
Fingerman , M., Nagahshanam, R., Sarojini R. (1993). Vertebrate-type hormones in crustaceans: localization,
identification and functional significance. Zoolological Science, 10,13–29.
Fyhn, M.E.H. Costlow, J.D. (1977). Histology and histochemistry of the ovary and oogenesis in Balanus amphitrite L
and Balanus eburneus Gould (Cirripedia: Crustacea). Biological Bulletin, 152, 351-359.
Gunamalai, V., Kirubagaran, R., Subramoniam, T. (2006). Vertebrate steroids and the control of female reproduction in
two decapod crustaceans, Emerita asiatica and Macrobrachium rosenbergii. Current Science India, 90,119–123.
Humason, G.L. (1972) Animal tissue technique. W.H. Freeman, San Franscisco.641pp.
Kessel, R.G. (1968). Mechanisms of protein yolk synthesis and deposition in crustacean oocytes. Zeitschrift für
Zellforschung Mikroskopische Anatomie, 89, 17-38.
King, J.E.(1948). A study reproductive organs of the common marine shrimp, Peneaus sertiferus (Linnaeus). Biological
Bulletin, 94, 224-262.
Ko¨ hler, H. R.,Kloas, W., Schirling, M., Lutz, L., Reye, A.L., Langen, J., Triebskorn, R., Nagel, R., Scho¨ nfelder, G.
(2007). Sex steroid receptor evolution and signalling in aquatic invertebrates. Ecotoxicology, 16, 131–143.
Kulkarni, G.K., Nagabhushanam, R., Joshi, P.K. (1979). Effect of progesterone on ovarian maturation in a marine
penaeid prawn, Parapenaeopsis hardwickii. Indian Journal of Experimental Biology, 17, 986–987.
Kulkarni, G.K., Glade, L., Fingerman, M. (1991). Oogenesis and effects of neuroendocrine tissues on in vitro
synthesis of protein by the ovary of the red swamp crayfish Procambarus clarkii, Journal of Crustacean
Biology, 11, 513–522
Krol, R.M., Hawkins, W.E., Overstreet R.M. Reproductive components. F.W. Harrison, F.W., Humes A.G.,
(Eds.), Microscopic Anatomy of Invertebrates Vol 10: Decapod Crustacea, Wiley-Liss, New York (1992),
pp. 259-343.
LaFont , R., Mathieu, M. (2007). Steroids in aquatic invertebrate. Ecotoxicology, 16,109-130.
Meunpol, O., Iam-Pai, S., Suthikrai, W., Piyatiratitivorakul, S. (2007). Identification of progesterone and 17β-
hydroxyprogesterone in polychaetes (Perinereis sp.) and the effects of hormone extracts on penaeid
oocyte development in vitro. Aquaculture, 270, 485–492.
Minagawa, M., J.-R. Chiu, J.-R. Kudo, F. Ito, F. Takashima, F. (1993). Female reproductive biology and oocyte
development of the red frog crab, Ranina ranina, off Hachijojima, Izu Islands, Japan. Marine
Biology,115, 613–623.
Nicolau, C.F., Nascimento, A.A., Machado-Santos, C., Sales, A. Oshiro, L.M.Y. (2012). Gonads of males and
females of the mangrove tree crab Aratus pisonii (Grapsidae: Brachyura: Decapoda): a histological and
histochemical view. Acta Zoolology, 93, 222–230.
O’Donovan, P., Abraham, M., Cohen D. (1984). The ovarian cycle during the intermoult in ovigerous
Macrobrachium rosenbergii. Aquaculture, 36, 347-358.
Papathanassiou, E., King, P.E. (1984). Ultrastructural Studies on Gametogenesis of the Prawn Puhemon
serratus (Pennant). I. Oogenesis. Acta Zoologica (Stockh.), 65, 17-31.
Paolucci, M., Cristo, C, D., Cosmo, A.D. (2002). Immunological evidence for progesterone and estradiol
receptors in the freshwater crayfish Austropotamobius pallipes. Molecular reproduction and
development. 63, 55-62.
Pearse, A,G, E. (1960). Histochemistry theoretical and applied. Vol. 2. London: Jet. Churchill Ltd. p. 965.
Quadros, P.S,, Lopez, V., De Vries, G.J., Chung, W.C., Wagner, C.K. (2002). Progesterone receptors and the
sexual differentiation of the medial preoptic nucleus. Journal Neurobiology, 51, 24-32.
Ravi , R., Manisseri, M. K., Sanil, N, K. (2012). Ovarian maturation and oogenesis in the blue swimmer crab,
Portunus pelagicus (Decapoda: Portunidae). Acta Zoologica (Stockholm), 94, 291–299.
Robinson, R.S., Mann, G.E., Lamming, G.E., Wathes, D.C. (2001). Expression of oxytocin, oestrogen and
progesterone receptors in uterine biopsy samples throughout the estrous cycle and early pregnancy in
cows. Reproduction, 122, 965–979.
Santos S. Negreiros-Fransozo, M.L. (1999). Reproductive cycle of the swimming crab Portunus spinimanus
Latreille (Crustacea, Decapoda, Brachyura) from the Ubatuba, São Paulo, Brazil. Revista Brasileira de
Zoologia, 16, 1183-1193.
Sharifian, S., Kamrani, E., Safaie, M., Sharifian, S. (2015). Oogenesis and ovarian development in the
freshwater Crab Sodhiana iranica (Decapoda: Gecarcinuaidae) from the south of Iran. Tissue and
cell, 47, 213-220.
Soroka, Y., Milner, Y. Sagi, A. (2000). The hepatopancreas as a site of yolk protein synthesis in the prawn,
Macrobrachium rosenbergii. Invertebrate Reproductive Development, 37, 61–68.
Souza ,T.L., .Bragaa, A.A., López, L.S., Nunesa, G,E. (2017). Dynamics of oogenesis in ghost shrimp
Callichirus major (Crustacea: Axiidea): a morphofunctional and histochemical study. Acta Histochemica,
119,769-777.
Stewart, M.J., Soonklang, N., Stewart, P., Hanna, P.J., Wanichanon, C., Parratt, A., Duan, W., Sobhon, P., 2007.
Histological studies of the ovaries of two tropical portunid crabs, Portunus pelagicus (L.) and Scylla serrata
(F.). Invertebrate Reproduction Development, 50, 85–97.
Suzuki, S., Yamasaki, K., Katakura, Y., (1989) Vitellogenin synthesis by fat body and ovary in the terrestial
isopod, Armadillidium vulgare. Gereneral Comparative Endocrinology, 74, 120-126.
Thongbuakaew,T., Siangcham,T., Suwansa-ard, S., Elizur, A., Cummins, S.F., Sobhon, P., Sretarugsa, P.
(2016). Steroids and genes related to steroid biosynthesis in the female giant freshwater prawn, Macrobrachium rosenbergii. Steroids, 107, 149-160.
Thomas, P., TubbsHakan C., Berg, H., Dressing, G. (2007) Sex steroid hormone receptors in fish ovaries.
Dordrecht, the Netherlands: Springer. p. 203–232.
Warrier, S.R., Tirumalai, R., Subramoniam, T. (2001) Occurence of vertebrate steroids, estradiole 17β and
progesterone in the reproducing females of the mud crab Scylla serrata. Comparative Biochemistry
Physiology A Molecular Integrate Physiology, 130, 283-294.
Wolin, E.M., Laufer, H., Albertini, D.F. (1973) Uptake of yolk protein lipovitelline by developing crustacean
oocytes. Developmetal Biology, 35, 160-170.
Wu, X., Chen, H., Liu, Z., Cheng, Y., (2014.) Immunorecognition and distribution of progesterone receptors in the
Chinese mitten crab Eriocheir sinensis during ovarian development. Journal of Shellfish Research,
33, 35-43
Yano, I. (1985). Induced ovarian maturation and spawning in greasyback shrimp, Metapenaeus ensis. By
progesterone, Aquaculture, 47, 223-229,
Ye, H., Songa, P., Mab,J., Huanga H., Wanga ,G. (2010). Changes in progesterone levels and distribution of
progesterone receptor during vitellogenesis in the female mud crab (Scylla paramamosain). Marine
and Freshwater Behaviour and Physiology, 43, 25-35.
in the red-claw crayfish Cherax quadricarinatus. Invertebrate Reproduction and Development, 37, 75-83.
Ando, H. Makioka, T. (1998). Structure of the ovary and mode of oogenesis in a fresh water crayfish,
Procambarus clarkii (Girard). Zoological Science, 15, 893-901.
Ando, H. Makioka, T. (1999). Structure of the ovary and Mode of oogenesis in a freshwater crab (Potamon
dehaani. Journal of morphology, 239, 107-114.
Braga, A.A. Nunes , E.T. López-Grecco, L.S. Camargo-Mathias, M.I., Fransozo, V. (2016). Histological and
histochemical features of the oogenesis in the simultaneous protandric hermaphrodite shrimp
Exhippolysmata oplophoroides (Decapoda: Caridea). Micron, 88,60-67.
Chang, C.F. Shih, T.W. (1995). Reproductive cycle of ovarian development and vitellogenin profiles in the
freshwater prawns, Macrobrachium rosenbergii. Invertebrate Reproduction and Development, 27,
11–20.
Costa, T.M.C. Negreiros-Fransozo, M.L. (1998). The reproductive cycle of Callinectes danae Smith, 1869
(Decapoda, Portunidae) in the Ubatuba region, Brazil. Crustaceana, 71, 615-627.
Couch, E.F.,Hagino, N., Lee, J.W. (1987). Changes in estradiol and progesterone immunoreactivity in tissues of
the lobster, Homarus americanus, with developing and immature ovaries. Comparative Biochemistry
Physiollogy, 85A, 765-770.
Desouza, L.P., Silva, J.R.F. (2009). Morphology of the female reproductive system of the red clawed
mangrove tree crab (Goniopsis cruentata Latreille, 1803). Scientia Marina, 73, 527-539.
Di Cosmo, A., Paolucci, M., Di Cristo, C., Botte V. Ciarcia,G. 1998. Progesterone and 17β -estradiol involment in
the yolk protein synthesis in the ovary of Octopus vulgaris. Molecular Reproduction and Development,
50,451-460
El-Sherifa ,S, S., El-Khodary, G.M., Ghonimb A.M. (2012). Ovarian cycle and scanning electron micrographs
of the spawned egg of female mantis shrimp Oratosquilla massavensis (Alexandria, Egypt).
The Journal of Basic and Applied Zoology, 65, 116-124.
Fairs, N., Quinlan, P., Goad, L. (1990) Changes in ovarian unconjugated and conjugated steroid titers during
vitellogenesis in Penaeus monodon. Aquaculture, 89, 83-99.
Feng, L., Wu, X.G., Lu, J.F., Liu Z.J., Cheng, Y.X. (2009). Changes of progesterone and 17β-estradiol
concentrations in ovary, hepatopancreas, and hemolymph of swimming crab Portunus trituberculatus
during the reproductive cycle. Journal of Fish China, 33, 86.
Ferreira, M.A.P., Resende, B.M., Lima, M.Y.S., Santos, S.S.D., Rocha, R.M. ( 2012). The stages of ovarian
development affects organ expression of vitellogenin as well as the morphometry and ultrastructure of
germ cells in the freshwater prawn Macrobrachium amazonicum (Heller, 1862), Theriogenology 78,
981–990.
Fingerman , M., Nagahshanam, R., Sarojini R. (1993). Vertebrate-type hormones in crustaceans: localization,
identification and functional significance. Zoolological Science, 10,13–29.
Fyhn, M.E.H. Costlow, J.D. (1977). Histology and histochemistry of the ovary and oogenesis in Balanus amphitrite L
and Balanus eburneus Gould (Cirripedia: Crustacea). Biological Bulletin, 152, 351-359.
Gunamalai, V., Kirubagaran, R., Subramoniam, T. (2006). Vertebrate steroids and the control of female reproduction in
two decapod crustaceans, Emerita asiatica and Macrobrachium rosenbergii. Current Science India, 90,119–123.
Humason, G.L. (1972) Animal tissue technique. W.H. Freeman, San Franscisco.641pp.
Kessel, R.G. (1968). Mechanisms of protein yolk synthesis and deposition in crustacean oocytes. Zeitschrift für
Zellforschung Mikroskopische Anatomie, 89, 17-38.
King, J.E.(1948). A study reproductive organs of the common marine shrimp, Peneaus sertiferus (Linnaeus). Biological
Bulletin, 94, 224-262.
Ko¨ hler, H. R.,Kloas, W., Schirling, M., Lutz, L., Reye, A.L., Langen, J., Triebskorn, R., Nagel, R., Scho¨ nfelder, G.
(2007). Sex steroid receptor evolution and signalling in aquatic invertebrates. Ecotoxicology, 16, 131–143.
Kulkarni, G.K., Nagabhushanam, R., Joshi, P.K. (1979). Effect of progesterone on ovarian maturation in a marine
penaeid prawn, Parapenaeopsis hardwickii. Indian Journal of Experimental Biology, 17, 986–987.
Kulkarni, G.K., Glade, L., Fingerman, M. (1991). Oogenesis and effects of neuroendocrine tissues on in vitro
synthesis of protein by the ovary of the red swamp crayfish Procambarus clarkii, Journal of Crustacean
Biology, 11, 513–522
Krol, R.M., Hawkins, W.E., Overstreet R.M. Reproductive components. F.W. Harrison, F.W., Humes A.G.,
(Eds.), Microscopic Anatomy of Invertebrates Vol 10: Decapod Crustacea, Wiley-Liss, New York (1992),
pp. 259-343.
LaFont , R., Mathieu, M. (2007). Steroids in aquatic invertebrate. Ecotoxicology, 16,109-130.
Meunpol, O., Iam-Pai, S., Suthikrai, W., Piyatiratitivorakul, S. (2007). Identification of progesterone and 17β-
hydroxyprogesterone in polychaetes (Perinereis sp.) and the effects of hormone extracts on penaeid
oocyte development in vitro. Aquaculture, 270, 485–492.
Minagawa, M., J.-R. Chiu, J.-R. Kudo, F. Ito, F. Takashima, F. (1993). Female reproductive biology and oocyte
development of the red frog crab, Ranina ranina, off Hachijojima, Izu Islands, Japan. Marine
Biology,115, 613–623.
Nicolau, C.F., Nascimento, A.A., Machado-Santos, C., Sales, A. Oshiro, L.M.Y. (2012). Gonads of males and
females of the mangrove tree crab Aratus pisonii (Grapsidae: Brachyura: Decapoda): a histological and
histochemical view. Acta Zoolology, 93, 222–230.
O’Donovan, P., Abraham, M., Cohen D. (1984). The ovarian cycle during the intermoult in ovigerous
Macrobrachium rosenbergii. Aquaculture, 36, 347-358.
Papathanassiou, E., King, P.E. (1984). Ultrastructural Studies on Gametogenesis of the Prawn Puhemon
serratus (Pennant). I. Oogenesis. Acta Zoologica (Stockh.), 65, 17-31.
Paolucci, M., Cristo, C, D., Cosmo, A.D. (2002). Immunological evidence for progesterone and estradiol
receptors in the freshwater crayfish Austropotamobius pallipes. Molecular reproduction and
development. 63, 55-62.
Pearse, A,G, E. (1960). Histochemistry theoretical and applied. Vol. 2. London: Jet. Churchill Ltd. p. 965.
Quadros, P.S,, Lopez, V., De Vries, G.J., Chung, W.C., Wagner, C.K. (2002). Progesterone receptors and the
sexual differentiation of the medial preoptic nucleus. Journal Neurobiology, 51, 24-32.
Ravi , R., Manisseri, M. K., Sanil, N, K. (2012). Ovarian maturation and oogenesis in the blue swimmer crab,
Portunus pelagicus (Decapoda: Portunidae). Acta Zoologica (Stockholm), 94, 291–299.
Robinson, R.S., Mann, G.E., Lamming, G.E., Wathes, D.C. (2001). Expression of oxytocin, oestrogen and
progesterone receptors in uterine biopsy samples throughout the estrous cycle and early pregnancy in
cows. Reproduction, 122, 965–979.
Santos S. Negreiros-Fransozo, M.L. (1999). Reproductive cycle of the swimming crab Portunus spinimanus
Latreille (Crustacea, Decapoda, Brachyura) from the Ubatuba, São Paulo, Brazil. Revista Brasileira de
Zoologia, 16, 1183-1193.
Sharifian, S., Kamrani, E., Safaie, M., Sharifian, S. (2015). Oogenesis and ovarian development in the
freshwater Crab Sodhiana iranica (Decapoda: Gecarcinuaidae) from the south of Iran. Tissue and
cell, 47, 213-220.
Soroka, Y., Milner, Y. Sagi, A. (2000). The hepatopancreas as a site of yolk protein synthesis in the prawn,
Macrobrachium rosenbergii. Invertebrate Reproductive Development, 37, 61–68.
Souza ,T.L., .Bragaa, A.A., López, L.S., Nunesa, G,E. (2017). Dynamics of oogenesis in ghost shrimp
Callichirus major (Crustacea: Axiidea): a morphofunctional and histochemical study. Acta Histochemica,
119,769-777.
Stewart, M.J., Soonklang, N., Stewart, P., Hanna, P.J., Wanichanon, C., Parratt, A., Duan, W., Sobhon, P., 2007.
Histological studies of the ovaries of two tropical portunid crabs, Portunus pelagicus (L.) and Scylla serrata
(F.). Invertebrate Reproduction Development, 50, 85–97.
Suzuki, S., Yamasaki, K., Katakura, Y., (1989) Vitellogenin synthesis by fat body and ovary in the terrestial
isopod, Armadillidium vulgare. Gereneral Comparative Endocrinology, 74, 120-126.
Thongbuakaew,T., Siangcham,T., Suwansa-ard, S., Elizur, A., Cummins, S.F., Sobhon, P., Sretarugsa, P.
(2016). Steroids and genes related to steroid biosynthesis in the female giant freshwater prawn, Macrobrachium rosenbergii. Steroids, 107, 149-160.
Thomas, P., TubbsHakan C., Berg, H., Dressing, G. (2007) Sex steroid hormone receptors in fish ovaries.
Dordrecht, the Netherlands: Springer. p. 203–232.
Warrier, S.R., Tirumalai, R., Subramoniam, T. (2001) Occurence of vertebrate steroids, estradiole 17β and
progesterone in the reproducing females of the mud crab Scylla serrata. Comparative Biochemistry
Physiology A Molecular Integrate Physiology, 130, 283-294.
Wolin, E.M., Laufer, H., Albertini, D.F. (1973) Uptake of yolk protein lipovitelline by developing crustacean
oocytes. Developmetal Biology, 35, 160-170.
Wu, X., Chen, H., Liu, Z., Cheng, Y., (2014.) Immunorecognition and distribution of progesterone receptors in the
Chinese mitten crab Eriocheir sinensis during ovarian development. Journal of Shellfish Research,
33, 35-43
Yano, I. (1985). Induced ovarian maturation and spawning in greasyback shrimp, Metapenaeus ensis. By
progesterone, Aquaculture, 47, 223-229,
Ye, H., Songa, P., Mab,J., Huanga H., Wanga ,G. (2010). Changes in progesterone levels and distribution of
progesterone receptor during vitellogenesis in the female mud crab (Scylla paramamosain). Marine
and Freshwater Behaviour and Physiology, 43, 25-35.
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