Histology and Lectin Histochemistry in the Development of Female Germ Cells in Seahorse (Hippocampus kuda)
Abstract
The present research aimed to study on feature histological and histochemical of the female germ cellsIn the seahorse (Hippocampus kuda) during development stages by using paraffin methods. The ovarian samples were taken from animal bodies and fixed in Bouin’s solution. The paraffin embed samples were sectioned at 7 µm-thickness which were stained with Hematoxylin and Eosin (H-E), Periodic-acid Schiff and hematoxylin (PAS/H), alcian blue pH2.5 (AB pH2.5) and lectin. The ovarian cells in seahorse ovary were characterized into various stages (including oogonia, primary growth, oil droplet, cortical alveolus, vitellogenic and maturation). Those of the observed oocytes showed a wide range of diameters 10 mm to 675 mm. Lectin histochemistry was also applied to distribution of glycoconjugates during the initiation of cortical alveolus stage, an appearance of cortical alveoli alveoli containing neutral and carboxylated glycoconjugates was obviously seen around the peripheral area of cytoplasm. Both of glycoconjugates within cortical alveoli were specially composed of α/β-acetyl-D-galactosamine, α-acetyl-D glucosamine, α-mannose and sialic acid. The zona radiata positively reacted to all lectins, which indicated the complex polysaccharides in the surface of oocytes. Keywords : Hippocampus kuda, oocyte growth, lectinsReferences
Abou-seedo, F., Dadzie S. Kanaan A. (2003). Histology of ovarian development and maturity stages in the
yellowfin seabream, Acanthopagrus ltus (Teleostei: Sparidae) (Hottuyn, 1782) reared in cages. Kuwait
Journal of Science, 30, 121-135.
Babin, P.J., Cerdà, J. Lubzens, E. (2007). The Fish Oocyte: From Basic Studies to Biotechnological
applications. Dordrecht. Springer.
Begovac, P.C. Wallace, R. (1989). Major vitelline envelope proteins in pipefish oocytes originate within the
follicle and are associated with Z3 layer. Journal of experimental Zoology, 251, 56-73.
Casadevall, M., Bonet, S. Matallanas, J. (1993). Description of different stages in Ophiodon barbatum (Pisces,
Ophiidae). Environmental Biology of Fish. 36, 127-133.
Dell, A., Morris, H. R., Easton, R. L., Patankar, M. & Clark, G. F. (1999). The glycobiology of gametes and
fertilization. Biochimca et Biophysica Acta,1473, 196–205.
Grier, H.J. (2012). Development of the follicle complex and oocyte staging in red drum, Sciaenops ocellatus
Linnaeus,1776 (Perciformes, Sciaenidae). Journal of Morphology, 273, 801–829.
Guraya, S. S. (1979). Recent advances in the morphology, cytochemistry and function of Balbiani’s vitelline body in
animal oocytes. International Review of Cytology, 59, 249-321
Guraya, S.S. (1986). The Cell and Molecular Biology of Fish Oogenesis. In: Sauer HW (ed). Karger, New York.
Gutiérrez, M., Sarasquete C. Rodríguez R.B. (1985). Caracteres citohistoquímicos de carbohidratos
proteínas durante la ovogénesis del lenguado, Solea senegalensis (Kaup, 1858). Investigacion pesquera,
49, 353-363.
Hamlet, W.C., Jezior, M. Spieler, R. (1999). Ultrastructural analysis folliculogenesis in the ovary of yellow spotted
stingray Urolophus jamaicensis. Annals of anatomy, 181,159-172.
Humason, G.L. (1962). Animal tissue technique. San Francisco, W.H. Freeman.
Aquatoyou.com (2015). Retrieved January 2,2016, from http://www.aquatoyou.com/index.php/2013-02-20-13-43- 43/719-seahorse
Inoue, S. Inoue, Y. (1986). Fertilization (activation)-induced 200 to 9-kDa depolymerization of
polysialoglycoprotein, a distinct component of cortical alveoli of rainbow trout eggs. Journal of Biological
Chemistry, 261,5256-5261.
Khoo K.H. (1979). The histochemistry and endocrine control of vitellogenesis in goldfish ovaries. Canadian
Journal of Zoology, 57,617-626.
Kunz, Y.W. (2004). Developmental biology of teleost fishes. Netherlands: Springer, 636 p.
Kress, A. (1996). A comparison of oocyte organelles in Monodelphis domestica with those of other Marsupials
and Eutherians. Reproduction Fertility and Development, 8, 521-533.
LaFleur, G.J. Jr., Raldúa, D., Fabra, M., Carnevali, O., Denslow, N., Wallace, R.A. Cerdá, J. (2005).
Derivation of major yolk proteins from parental vitellogenins and alternative processing during
oocyte maturation in Fundulus heteroclitus. Biological Reproduction, 73, 815-824.
Lee M.F., Huang J.D. Chang C.F. (2008). Development of ovarian tissue and female germ cells in the
protandrous black porgy, Acanthopagrus schlegeli (Perciformes, Sparidae). Zoological Studies, 47, 302-316.
Lis H. Sharon N. (1986). Lectins as molecules and as tools. Annual Review Biochemistry, 55, 35-67,
Maria A.N., Laura H. Orfão, L.H., Rizzo E. Ninhaus-Silveira, A. (2014). Histochemical and morphological features of
biopsied and stripped oocytes from the Brazilian endangered teleost pirapitinga, Brycon nattereri
(Characiformes). Zygote, 23, 1-7.
Mayer, I., Schackley, S.E. Ryland, J.S. (1988). Aspects of reproductive biology of the bass, Dicentrarchus labrax L. I.
A histological and histochemical study of oocyte development. Journal of Fish Biology, 33, 609-622.
Miller, D. J. AX R.L. (1990). Carbohydrate and fertilization in animals. Molecular Reproduction Development, 26,184-192.
Mommsen, T.P. Walsh, P.J. (1988). Vitellogenesis and oocyte assembly. In: Fish physiology. Vol.1A. Hoar
W.S. and Randall D.J. (eds). Academic Press. New York. pp 347-406.
Mourente G., Megina, G. Diaz-Salvago, E. (2002). Lipids in female northern Bluefin tuna (Thunnus thynnus L.) during
sexual maturation. Fish Physiology Biochemistry, 24,351-363.
Ortiz-Delgado, J.B., Porcelloniม S., Fossi C. Sarasquete, C. (2008). Histochemical characterisation of oocytes of
the swordfih Xiphias gladius. Scientia Marina, 72, 549-564.
Ohta T., Iwamatsu T., Tanaka M., Yoshimoto, Y. (1990). Cortical alveolus breakdown in the eggs of the
freshwater teleost Rhodeus oceltatus, Anatomy Record, 227,486-496.
Parillo, F., Fagioli O., Dall’Aglio C. & Verini-Supplizi, A. (2000). Lectin histochemical detection of sulfoglycans in
the zona pellucida of mammalian antral oocytes. Acta Histochemistry, 10,:193-202.
Pearse, A.G.E. (1985). Histochemistry. Theoretical and applied. Vol. 2. Analytic technology. 4th ed. Churchill
Livingstone. New York, NY, 1055 pp.
Ramezani-Fard E., Kamarudin, M.S. Harmin, S.A. (2013). Endocrine control of oogenesis in teleosts. Asian
Journal of Animal and Veterinary Advances, 8, 205-215.
Sarasquete, C., Cárdenas S., González de Canales, M.L., Pascua E. (2002). Oogenesis in the bluefin tuna,
Thunnus thynnus L., A histological and histochemical study. Histology Histopathology, 17, 775-788
Selman, K. Wallace, R.A. (1986). Gametogenesis in Fundulus heteroclitus. Americal Zoologist. 26, 173-192.
Selman, K., Wallace, R.A., Sarka, A. Xiaoping, Q. (1993). Stages of oocyte development in the zebrafish,
Brachydanio rerio. Journal of Morphology, 218, 203-24.
Silveira, R.B. Fontoura, N.F. (2010). Fecundity and fertility of the longsnout seahorse, Hippocampus reidi (Teleostei: Syngnathidae), in tropical Brazil. Revista Brasileira de Biociências. Brazilian Journal of
Biosciences, 8,362-367.
Skutelsky, E., Ranen, E. Shalgi, R. (1994). Variations in the distribution of sugar in the zona pellucida
as possible species specific determinants of mammalian oocytes. Journal of Reproduction and Fertility,
100, 35-41.
Sogabe, A., Matsumoto, K., Ohashi M., Watanabe A., Takata H., Murakami Y., Omor, I K. Yanagisawa, Y.
(2008). A monogamous pipefish has the same type of ovary as observed in monogamous seahorses.
Biology Letter, 4, 362-365.
Spicer, S.S. Schulte, B. A. (1992). Diversity of cell glycoconjugates shown histochemically: a perspective.
Journal of Histochemistry and Cytochemistry, 40, 1-38.
Stehr, C.M. Hawkes J.W. (1979). The comparative ultrastructure of the egg membrane and associated pore
structures in the starry flounder, Platichthys stellatus (Pallas), and pink salmon, Oncorhynchus
gorbuscha (Walbaum). Cell Tissue Research, 200, 347-356.
Stölting, K.N. Wilson, A.B. (2007). Male pregnancy in seahorses and pipefish: beyond the mammalian model.
Bioassays, 29, 884-96.
Tiralongo, J. Duncker, I.M. (2015). Sialobiology: structure, biosynthesis and function. Sialic acid
glycoconjugates in health and disease. Glycoconjugate Journal, 77-78.
Tyler, C.R. Sumpter J.P. (1996). Oocyte growth and development in teleosts. Reviews in Fish Biology and
Fisheries, 6,287-318.
Uribe M.C., Grier, H.J. Parenti L.R. (2012). Ovarian structure and oogenesis of the oviparous goodeids
Crenichthys baileyi (Gilbert, 1893) and Empetrichthys latos Miller, 1948 (Teleostei, Cyprinodontiformes).
Journal of Morphology, 273,371–387.
Wallace,R.A. Selman K. (1990). Ultrastructural aspects of oogenesis and oocyte growth in fish and
amphibians. Journal of Electron Microscopy Technique, 16,175–201.
Wiegand, M.D. (1996). Composition, accumulation and utilization of yolk lipids in teleost fish. Review in Fish
Biology and Fisheries, 6,259–286.
Zelazowska, M., Kilarski, W., Bilinski, S. M., Podder, D. D. Kloc, M. (2007). Balbiani cytoplasm in oocytes of a
primitive fish, the sturgeon Acipenser gueldenstaedtii, and its potential homology to the Balbiani’s body
(mitochondrial cloud) of Xenopus laevis oocytes. Cell Tissue Research, 329, 137-145.
yellowfin seabream, Acanthopagrus ltus (Teleostei: Sparidae) (Hottuyn, 1782) reared in cages. Kuwait
Journal of Science, 30, 121-135.
Babin, P.J., Cerdà, J. Lubzens, E. (2007). The Fish Oocyte: From Basic Studies to Biotechnological
applications. Dordrecht. Springer.
Begovac, P.C. Wallace, R. (1989). Major vitelline envelope proteins in pipefish oocytes originate within the
follicle and are associated with Z3 layer. Journal of experimental Zoology, 251, 56-73.
Casadevall, M., Bonet, S. Matallanas, J. (1993). Description of different stages in Ophiodon barbatum (Pisces,
Ophiidae). Environmental Biology of Fish. 36, 127-133.
Dell, A., Morris, H. R., Easton, R. L., Patankar, M. & Clark, G. F. (1999). The glycobiology of gametes and
fertilization. Biochimca et Biophysica Acta,1473, 196–205.
Grier, H.J. (2012). Development of the follicle complex and oocyte staging in red drum, Sciaenops ocellatus
Linnaeus,1776 (Perciformes, Sciaenidae). Journal of Morphology, 273, 801–829.
Guraya, S. S. (1979). Recent advances in the morphology, cytochemistry and function of Balbiani’s vitelline body in
animal oocytes. International Review of Cytology, 59, 249-321
Guraya, S.S. (1986). The Cell and Molecular Biology of Fish Oogenesis. In: Sauer HW (ed). Karger, New York.
Gutiérrez, M., Sarasquete C. Rodríguez R.B. (1985). Caracteres citohistoquímicos de carbohidratos
proteínas durante la ovogénesis del lenguado, Solea senegalensis (Kaup, 1858). Investigacion pesquera,
49, 353-363.
Hamlet, W.C., Jezior, M. Spieler, R. (1999). Ultrastructural analysis folliculogenesis in the ovary of yellow spotted
stingray Urolophus jamaicensis. Annals of anatomy, 181,159-172.
Humason, G.L. (1962). Animal tissue technique. San Francisco, W.H. Freeman.
Aquatoyou.com (2015). Retrieved January 2,2016, from http://www.aquatoyou.com/index.php/2013-02-20-13-43- 43/719-seahorse
Inoue, S. Inoue, Y. (1986). Fertilization (activation)-induced 200 to 9-kDa depolymerization of
polysialoglycoprotein, a distinct component of cortical alveoli of rainbow trout eggs. Journal of Biological
Chemistry, 261,5256-5261.
Khoo K.H. (1979). The histochemistry and endocrine control of vitellogenesis in goldfish ovaries. Canadian
Journal of Zoology, 57,617-626.
Kunz, Y.W. (2004). Developmental biology of teleost fishes. Netherlands: Springer, 636 p.
Kress, A. (1996). A comparison of oocyte organelles in Monodelphis domestica with those of other Marsupials
and Eutherians. Reproduction Fertility and Development, 8, 521-533.
LaFleur, G.J. Jr., Raldúa, D., Fabra, M., Carnevali, O., Denslow, N., Wallace, R.A. Cerdá, J. (2005).
Derivation of major yolk proteins from parental vitellogenins and alternative processing during
oocyte maturation in Fundulus heteroclitus. Biological Reproduction, 73, 815-824.
Lee M.F., Huang J.D. Chang C.F. (2008). Development of ovarian tissue and female germ cells in the
protandrous black porgy, Acanthopagrus schlegeli (Perciformes, Sparidae). Zoological Studies, 47, 302-316.
Lis H. Sharon N. (1986). Lectins as molecules and as tools. Annual Review Biochemistry, 55, 35-67,
Maria A.N., Laura H. Orfão, L.H., Rizzo E. Ninhaus-Silveira, A. (2014). Histochemical and morphological features of
biopsied and stripped oocytes from the Brazilian endangered teleost pirapitinga, Brycon nattereri
(Characiformes). Zygote, 23, 1-7.
Mayer, I., Schackley, S.E. Ryland, J.S. (1988). Aspects of reproductive biology of the bass, Dicentrarchus labrax L. I.
A histological and histochemical study of oocyte development. Journal of Fish Biology, 33, 609-622.
Miller, D. J. AX R.L. (1990). Carbohydrate and fertilization in animals. Molecular Reproduction Development, 26,184-192.
Mommsen, T.P. Walsh, P.J. (1988). Vitellogenesis and oocyte assembly. In: Fish physiology. Vol.1A. Hoar
W.S. and Randall D.J. (eds). Academic Press. New York. pp 347-406.
Mourente G., Megina, G. Diaz-Salvago, E. (2002). Lipids in female northern Bluefin tuna (Thunnus thynnus L.) during
sexual maturation. Fish Physiology Biochemistry, 24,351-363.
Ortiz-Delgado, J.B., Porcelloniม S., Fossi C. Sarasquete, C. (2008). Histochemical characterisation of oocytes of
the swordfih Xiphias gladius. Scientia Marina, 72, 549-564.
Ohta T., Iwamatsu T., Tanaka M., Yoshimoto, Y. (1990). Cortical alveolus breakdown in the eggs of the
freshwater teleost Rhodeus oceltatus, Anatomy Record, 227,486-496.
Parillo, F., Fagioli O., Dall’Aglio C. & Verini-Supplizi, A. (2000). Lectin histochemical detection of sulfoglycans in
the zona pellucida of mammalian antral oocytes. Acta Histochemistry, 10,:193-202.
Pearse, A.G.E. (1985). Histochemistry. Theoretical and applied. Vol. 2. Analytic technology. 4th ed. Churchill
Livingstone. New York, NY, 1055 pp.
Ramezani-Fard E., Kamarudin, M.S. Harmin, S.A. (2013). Endocrine control of oogenesis in teleosts. Asian
Journal of Animal and Veterinary Advances, 8, 205-215.
Sarasquete, C., Cárdenas S., González de Canales, M.L., Pascua E. (2002). Oogenesis in the bluefin tuna,
Thunnus thynnus L., A histological and histochemical study. Histology Histopathology, 17, 775-788
Selman, K. Wallace, R.A. (1986). Gametogenesis in Fundulus heteroclitus. Americal Zoologist. 26, 173-192.
Selman, K., Wallace, R.A., Sarka, A. Xiaoping, Q. (1993). Stages of oocyte development in the zebrafish,
Brachydanio rerio. Journal of Morphology, 218, 203-24.
Silveira, R.B. Fontoura, N.F. (2010). Fecundity and fertility of the longsnout seahorse, Hippocampus reidi (Teleostei: Syngnathidae), in tropical Brazil. Revista Brasileira de Biociências. Brazilian Journal of
Biosciences, 8,362-367.
Skutelsky, E., Ranen, E. Shalgi, R. (1994). Variations in the distribution of sugar in the zona pellucida
as possible species specific determinants of mammalian oocytes. Journal of Reproduction and Fertility,
100, 35-41.
Sogabe, A., Matsumoto, K., Ohashi M., Watanabe A., Takata H., Murakami Y., Omor, I K. Yanagisawa, Y.
(2008). A monogamous pipefish has the same type of ovary as observed in monogamous seahorses.
Biology Letter, 4, 362-365.
Spicer, S.S. Schulte, B. A. (1992). Diversity of cell glycoconjugates shown histochemically: a perspective.
Journal of Histochemistry and Cytochemistry, 40, 1-38.
Stehr, C.M. Hawkes J.W. (1979). The comparative ultrastructure of the egg membrane and associated pore
structures in the starry flounder, Platichthys stellatus (Pallas), and pink salmon, Oncorhynchus
gorbuscha (Walbaum). Cell Tissue Research, 200, 347-356.
Stölting, K.N. Wilson, A.B. (2007). Male pregnancy in seahorses and pipefish: beyond the mammalian model.
Bioassays, 29, 884-96.
Tiralongo, J. Duncker, I.M. (2015). Sialobiology: structure, biosynthesis and function. Sialic acid
glycoconjugates in health and disease. Glycoconjugate Journal, 77-78.
Tyler, C.R. Sumpter J.P. (1996). Oocyte growth and development in teleosts. Reviews in Fish Biology and
Fisheries, 6,287-318.
Uribe M.C., Grier, H.J. Parenti L.R. (2012). Ovarian structure and oogenesis of the oviparous goodeids
Crenichthys baileyi (Gilbert, 1893) and Empetrichthys latos Miller, 1948 (Teleostei, Cyprinodontiformes).
Journal of Morphology, 273,371–387.
Wallace,R.A. Selman K. (1990). Ultrastructural aspects of oogenesis and oocyte growth in fish and
amphibians. Journal of Electron Microscopy Technique, 16,175–201.
Wiegand, M.D. (1996). Composition, accumulation and utilization of yolk lipids in teleost fish. Review in Fish
Biology and Fisheries, 6,259–286.
Zelazowska, M., Kilarski, W., Bilinski, S. M., Podder, D. D. Kloc, M. (2007). Balbiani cytoplasm in oocytes of a
primitive fish, the sturgeon Acipenser gueldenstaedtii, and its potential homology to the Balbiani’s body
(mitochondrial cloud) of Xenopus laevis oocytes. Cell Tissue Research, 329, 137-145.
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