Glycoconjugates of the ovary of Genypterus Blacodes and its importance in the reproductive biology
Abstract
The pink cuskeel, Genypterus blacodes, is a widely distributed ophidiiform inhabiting waters from 22 ° 35'S (Rio de Janeiro, Brazil) to about 43 ° S (Argentina). This species is one of the most valuable demersal fish resources in the Argentine Sea, mainly due its large size and flesh quality. The ovaries of G. blacodes present an elongated shape and are suspended by mesenteries from the dorsal body wall. When fish are in reproductive condition, the lamellae contain oocytes at different developmental stages: previtellogenic, primary growth and vitellogenic oocytes. A single-layer flat epithelium lines the lamellae, and the epitelial cells present variations in size and morphology depending on the gonad maturity stage. In most teleost fishes this epithelium is involved in the formation of ovarian fluid. Particularly, the ovary of G. blacodes secretes large quantities of glycoconjugates, not only at the epithelium of the lamellae, but also in different oocyte structures. The aim of this research is to review literature of the ovary of G. blacodes in relation to the synthesis of glycoconjugates and their importance in the reproductive biology of this species.
Keywords: Genypterus blacodes, ovary, reproductive strategies, glycoconjugates.
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References
Baker LL, Wiff R, Quiroz JC, Flores A, Céspedes R, Barrientos MA, Ojeda V, Gatica C (2014) Reproductive ecology of the female pink cuskeel (Genypterus blacodes): evaluating differences between fishery management zones in the Chilean austral zone. Environ Biol Fish 97: 1083-1093.
Brown-Peterson N, Wyanskib DM, Saborido-Rey F, Macewicz BJ, Lowerre-Barbierie SK (2011) A Standardized Terminology for Describing Reproductive Development in Fishes. Mar Coast Fish Dynam Manag Ecosys S 3(1): 52-70.
Calabro C, Albanese MP, Bertuccio C, Licata A, Gentile (2008) Histological, histochemical and immunohistochemical study on the growing oocytes of the abyssal teleost Hoplostethus mediterraneus (V). Folia Histochem Cytobiol 46 (1): 97-102.
Cohen S, Petcoff GM, Freijo RO, Portiansky EL, Barbeito CG, Macchi GJ, Díaz AO (2015) Histochemical characterization of oocytes in the pink cuskeel (Genypterus blacodes). Zool Sci 32(4): 383-388.
Cordo HD, Machinandiarena L, Macchi GJ, Villarino MF (2002) Talla de primera madurez del abadejo (Genypterus blacodes) en el Atlántico Sudoccidental. INIDEP Inf Téc 47, 5p.
Cousseau MB, Perrota RG (2000) Peces marinos de Argentina. Biología, distribución, pesca. Publicaciones Especiales INIDEP, Mar del Plata, Argentina.
Desantis S, Ventriglia G, Suban D, Deflorio M, Megalofonou P, Acone F, Zarrilli A, Palmieri G, De Metrio G (2006) Histochemical analysis of glycoconjugates in the domestic cat testis. Histol Histopathol 21: 11-22.
Díaz AO, Freijo RO, García AM, Portiansky EL, Barbeito CG, Macchi GJ (2012) Lectin histochemical aspects of the ovarian lamellae epithelium of Genypterus blacodes (Schneider, 1801). Pes Vet Bras 32(6): 547-552.
Díaz AO, García AM, Escalante AH, Goldemberg AL (2010) Glycoprotein histochemistry of the gills of Odontesthes bonariensis (Teleostei, Atherinopsidae). J Fish Biol 77: 1665-1673.
Díaz AO, García AM, Goldemberg AL (2005) Glycoconjugates in the branchial mucous cells of Cynoscion guatucupa (Cuvier, 1830) (Pisces: Sciaenidae). Sci Mar 69: 545-553.
Díaz AO, García AM, Goldemberg AL (2008) Glycoconjugates in the mucosa of the digestive tract of Cynoscion guatucupa: A histochemical study. Acta Histochem 110: 76-85.
Ehrlich MD (1998) Composición y abundancia de la fauna acompañante de merluza (Merluccius hubbsi) a través de datos de la flota comercial. INIDEP Inf Téc, 125, 24p.
Erickson D, Pikitch E (1993) A histological description of shortspine thornyhead, Sebastolopus alascanus, ovaries: structures associated with the production of gelatinous egg masses. Environ Biol Fish 36: 273-282.
Freijo R (2003) Determinación de glicoproteínas en epitelio germinal de Genypterus blacodes (abadejo manchado). Tesis de grado, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata.
Freijo RO, García AM, Portiansky EL, Barbeito CG, Macchi GJ, Díaz AO (2009) Morphological and histochemical characteristics of the epithelium of ovarian lamellae of Genypterus blacodes (Schneider, 1801). Fish Physiol Biochem 35 (3): 359-367.
Gasparini C, Andreatta G, Pilastro A (2012) Ovarian fluid of receptive females enhances sperm velocity. Naturwissenschaften 99 (5): 417-420.
Gasparini C, Evans JP (2013) Ovarian Fluid Mediates the Temporal Decline in Sperm Viability in a Fish with Sperm Storage. PloS One 8 (5): e64431.
Gimeno EJ, Barbeito CG (2004) La glicobiología, una nueva dimensión para el estudio de la biología y la patología celular y tisular. Anales de la Academia Nacional de Agronomía y Veterinaria 58: 6-34.
Grier HJ (2000) Ovarian germinal epithelium and folliculogenesis in common snook, Centropomus undecimalis (Teleostei: Centropomidae). J Morphol 243: 265-281.
Grier HJ (2012) Development of the follicle complex and oocyte staging in red drum, Sciaenops ocellatus Linnaeus, 1776 (Perciformes, Sciaenidae). J Morphol 273 (8): 801-829.
Lahnsteiner F (2002) The influence of ovarian fluid on the gamete physiology in the Salmonidae. Fish Physiol Biochem 27: 49-59.
Lahnsteiner F (2007) First results on a relation between ovarian fluid and egg proteins of Salmo trutta and egg quality. Aquacult Res 38: 131-139.
Macchi GJ (1998) Preliminary estimates of spawning frequency and batch fecundity of striped weakfish, Cynoscion striatus, in coastal waters off Buenos Aires province. Fish Bull 96: 375-381.
Macchi G, Díaz AO, Goldemberg AL (1998) Aparato genital femenino en los peces. En: Temas de Histología y Embriología Animal (Parte 3), Nessi A et al. (eds) Ed Inarbite, Buenos Aires, Argentina, pp. 199-206.
Macchi GJ, Díaz AO (2013) Aparato genital femenino en peces. En: Histología y Embriología Humana y Comparada (Parte 3), Nessi A et al. (eds) (eds) Inarbite, Buenos Aires, Argentina, pp. 250-256.
Machinandiarena L, Villarino MF, Macchi GJ (1998) Descripción del estadio de desove del abadejo manchado Genypterus blacodes (Schneider, 1801) (Pisces, Ophidiidae) en el mar Argentino. Bol Inst Esp Oceanogr 14: 49-55.
Mansour N, Lahnsteiner F, Patzner RA (2009) Ovarian fluid plays an essential role in attachment of Eurasian perch, Perca fluviatilis eggs. Theriogen 71: 586-593.
Marchetti L, Capacchietti M, Sabbieti MG, Accili D, Materazzi G, Menghi G (2006) Histology and carbohydrate histochemistry of the alimentary canal in the rainbow trout Oncorhynchus mykiss. J Fish Biol 68: 1808-1821.
Mittal AK, Ueda T, Fujimori O, Yamada K (1994a) Histochemical analysis of glycoproteins in the unicellular glands in the epidermis of an Indian freshwater fish Mastacembelus pancalus (Hamilton). Histochem J 26: 666-677.
Mittal AK, Ueda T, Fujimori O, Yamada K (1994b) Carbohydrates in the epdiermal mucous cells of a freshwater fish Mastacembelus pancalus (Mastacembelidae, Pisces) as studied by electron-microscopic cytochemical methods. Cell Tissue Res 280: 531-539.
Morris Jr JA, Sullivan CV, Govoni JJ (2011) Oogenesis and spawn formation in the invasive lionfish, Pterois miles and Pterois volitans. Scien Mar 75 (1): 147-154.
Munehara H (1989) Studies on the reproductive biology of the masked greenling, Hexagrammos octogramus. Ph.D. thesis, Hokkaido University.
Muñoz M, Casadevall M, Bonet S (1999) Annual reproductive cycle of Helicolenus dactylopterus dactylopterus (Teleostei: Scorpaeniformes) with special reference to the ovaries sperm storage. J Mar Biol Assoc UK 79: 521-529.
Neutra MR, Forstner JF (1987) Gastrointestinal mucus - synthesis, secretion and function. In Physiology of the Gastrointestinal Tract, 2nd Edn) Johnson LR (eds) Raven, New York, pp. 975-1009.
Ortiz-Delgado JB, Porcelloni S, Fossi, Sarasquete C (2008) Histochemical characterisation of oocytes of the swordfish Xiphias gladius. Sci Mar 72 (3): 549-564.
Pajak B, Danguy A (1993) Characterization of sugar moieties and oligosaccharide sequences in the distal intestinal epithelium of the rainbow trout by means of lectin histochemistry. J Fish Biol 43: 709-722.
Parrillo F, Arias MP, Verini Supplizi A (2009) Glycoprofile of the different cell types present in the mucosa of the horse guttural pouches. Tissue Cell 41: 257-265.
Patiño R, Sullivan CV (2002) Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol Biochem 26: 57-70.
Riehl R, Patzner RA (1998) Minireview: the modes of egg attachment in teleost fishes. Ital J Zool (Modena) 65: 415-420.
Rosengrave P, Taylor H, Montgomerie R, Metcalf A, McBride K, Gemmell NJ (2009) Chemical composition of seminal and ovarian fluids of chinook salmon (Oncorhynchus tshawytscha) and their effects on sperm motility traits. Comp Biochem Physiol Part A: Mol Integr Physiol 152 (1): 123-129.
Sáez FG, Madrid JF, Alonso E, Hernández F (2001) Glycan composition of follicle (Sertoli) cells of the amphibian Pleurideles waltl: A lectin histochemical study. J Anat 198: 673-681.
Sales NG, dos Santos SA, Arantes FP, Hojo RES, dos Santos JE (2012) Ovarian Structure and Oogenesis of Catfish Pimelodella vittata (Lütken, 1874) (Siluriformes, Heptapteridae). Anat Histol Embryol 42 (3): 213-219.
Sarasquete C, González de Canales ML, Piñuela C, Muñoz Cueto JA, Rendón C, Mañanós EL, Rodríguez Gómez FJ, Pascual E (2002) Histochemical characteristics of the vitellogenic oocytes of the bluefin tuna, Thunnus thynnus L. Cienc Mar 28(4): 419-431.
Turner E, Montgomerie R (2002) Ovarian fluid enhances sperm movement in Arctic char. J Fish Biol 60 (6): 1570-1579.
Yoneda M, Tokimura M, Fujita H, Takeshita N, Matsuyama M, Matsuura (1998) Reproductive cycle and sexual maturity of the anglerfish Lophiomus setigerus in the East China Sea with a note on specialized spermatogenesis. J Fish Biol 53: 164-178.
Zimmer G, Reuter G, Schauer R (1992) Use of influenza C virus for detection of 9-O-acetylated sialic acids on immobilized glycoconjugates by esterase activity. Eur J Biochem 204: 209-215.
Brown-Peterson N, Wyanskib DM, Saborido-Rey F, Macewicz BJ, Lowerre-Barbierie SK (2011) A Standardized Terminology for Describing Reproductive Development in Fishes. Mar Coast Fish Dynam Manag Ecosys S 3(1): 52-70.
Calabro C, Albanese MP, Bertuccio C, Licata A, Gentile (2008) Histological, histochemical and immunohistochemical study on the growing oocytes of the abyssal teleost Hoplostethus mediterraneus (V). Folia Histochem Cytobiol 46 (1): 97-102.
Cohen S, Petcoff GM, Freijo RO, Portiansky EL, Barbeito CG, Macchi GJ, Díaz AO (2015) Histochemical characterization of oocytes in the pink cuskeel (Genypterus blacodes). Zool Sci 32(4): 383-388.
Cordo HD, Machinandiarena L, Macchi GJ, Villarino MF (2002) Talla de primera madurez del abadejo (Genypterus blacodes) en el Atlántico Sudoccidental. INIDEP Inf Téc 47, 5p.
Cousseau MB, Perrota RG (2000) Peces marinos de Argentina. Biología, distribución, pesca. Publicaciones Especiales INIDEP, Mar del Plata, Argentina.
Desantis S, Ventriglia G, Suban D, Deflorio M, Megalofonou P, Acone F, Zarrilli A, Palmieri G, De Metrio G (2006) Histochemical analysis of glycoconjugates in the domestic cat testis. Histol Histopathol 21: 11-22.
Díaz AO, Freijo RO, García AM, Portiansky EL, Barbeito CG, Macchi GJ (2012) Lectin histochemical aspects of the ovarian lamellae epithelium of Genypterus blacodes (Schneider, 1801). Pes Vet Bras 32(6): 547-552.
Díaz AO, García AM, Escalante AH, Goldemberg AL (2010) Glycoprotein histochemistry of the gills of Odontesthes bonariensis (Teleostei, Atherinopsidae). J Fish Biol 77: 1665-1673.
Díaz AO, García AM, Goldemberg AL (2005) Glycoconjugates in the branchial mucous cells of Cynoscion guatucupa (Cuvier, 1830) (Pisces: Sciaenidae). Sci Mar 69: 545-553.
Díaz AO, García AM, Goldemberg AL (2008) Glycoconjugates in the mucosa of the digestive tract of Cynoscion guatucupa: A histochemical study. Acta Histochem 110: 76-85.
Ehrlich MD (1998) Composición y abundancia de la fauna acompañante de merluza (Merluccius hubbsi) a través de datos de la flota comercial. INIDEP Inf Téc, 125, 24p.
Erickson D, Pikitch E (1993) A histological description of shortspine thornyhead, Sebastolopus alascanus, ovaries: structures associated with the production of gelatinous egg masses. Environ Biol Fish 36: 273-282.
Freijo R (2003) Determinación de glicoproteínas en epitelio germinal de Genypterus blacodes (abadejo manchado). Tesis de grado, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata.
Freijo RO, García AM, Portiansky EL, Barbeito CG, Macchi GJ, Díaz AO (2009) Morphological and histochemical characteristics of the epithelium of ovarian lamellae of Genypterus blacodes (Schneider, 1801). Fish Physiol Biochem 35 (3): 359-367.
Gasparini C, Andreatta G, Pilastro A (2012) Ovarian fluid of receptive females enhances sperm velocity. Naturwissenschaften 99 (5): 417-420.
Gasparini C, Evans JP (2013) Ovarian Fluid Mediates the Temporal Decline in Sperm Viability in a Fish with Sperm Storage. PloS One 8 (5): e64431.
Gimeno EJ, Barbeito CG (2004) La glicobiología, una nueva dimensión para el estudio de la biología y la patología celular y tisular. Anales de la Academia Nacional de Agronomía y Veterinaria 58: 6-34.
Grier HJ (2000) Ovarian germinal epithelium and folliculogenesis in common snook, Centropomus undecimalis (Teleostei: Centropomidae). J Morphol 243: 265-281.
Grier HJ (2012) Development of the follicle complex and oocyte staging in red drum, Sciaenops ocellatus Linnaeus, 1776 (Perciformes, Sciaenidae). J Morphol 273 (8): 801-829.
Lahnsteiner F (2002) The influence of ovarian fluid on the gamete physiology in the Salmonidae. Fish Physiol Biochem 27: 49-59.
Lahnsteiner F (2007) First results on a relation between ovarian fluid and egg proteins of Salmo trutta and egg quality. Aquacult Res 38: 131-139.
Macchi GJ (1998) Preliminary estimates of spawning frequency and batch fecundity of striped weakfish, Cynoscion striatus, in coastal waters off Buenos Aires province. Fish Bull 96: 375-381.
Macchi G, Díaz AO, Goldemberg AL (1998) Aparato genital femenino en los peces. En: Temas de Histología y Embriología Animal (Parte 3), Nessi A et al. (eds) Ed Inarbite, Buenos Aires, Argentina, pp. 199-206.
Macchi GJ, Díaz AO (2013) Aparato genital femenino en peces. En: Histología y Embriología Humana y Comparada (Parte 3), Nessi A et al. (eds) (eds) Inarbite, Buenos Aires, Argentina, pp. 250-256.
Machinandiarena L, Villarino MF, Macchi GJ (1998) Descripción del estadio de desove del abadejo manchado Genypterus blacodes (Schneider, 1801) (Pisces, Ophidiidae) en el mar Argentino. Bol Inst Esp Oceanogr 14: 49-55.
Mansour N, Lahnsteiner F, Patzner RA (2009) Ovarian fluid plays an essential role in attachment of Eurasian perch, Perca fluviatilis eggs. Theriogen 71: 586-593.
Marchetti L, Capacchietti M, Sabbieti MG, Accili D, Materazzi G, Menghi G (2006) Histology and carbohydrate histochemistry of the alimentary canal in the rainbow trout Oncorhynchus mykiss. J Fish Biol 68: 1808-1821.
Mittal AK, Ueda T, Fujimori O, Yamada K (1994a) Histochemical analysis of glycoproteins in the unicellular glands in the epidermis of an Indian freshwater fish Mastacembelus pancalus (Hamilton). Histochem J 26: 666-677.
Mittal AK, Ueda T, Fujimori O, Yamada K (1994b) Carbohydrates in the epdiermal mucous cells of a freshwater fish Mastacembelus pancalus (Mastacembelidae, Pisces) as studied by electron-microscopic cytochemical methods. Cell Tissue Res 280: 531-539.
Morris Jr JA, Sullivan CV, Govoni JJ (2011) Oogenesis and spawn formation in the invasive lionfish, Pterois miles and Pterois volitans. Scien Mar 75 (1): 147-154.
Munehara H (1989) Studies on the reproductive biology of the masked greenling, Hexagrammos octogramus. Ph.D. thesis, Hokkaido University.
Muñoz M, Casadevall M, Bonet S (1999) Annual reproductive cycle of Helicolenus dactylopterus dactylopterus (Teleostei: Scorpaeniformes) with special reference to the ovaries sperm storage. J Mar Biol Assoc UK 79: 521-529.
Neutra MR, Forstner JF (1987) Gastrointestinal mucus - synthesis, secretion and function. In Physiology of the Gastrointestinal Tract, 2nd Edn) Johnson LR (eds) Raven, New York, pp. 975-1009.
Ortiz-Delgado JB, Porcelloni S, Fossi, Sarasquete C (2008) Histochemical characterisation of oocytes of the swordfish Xiphias gladius. Sci Mar 72 (3): 549-564.
Pajak B, Danguy A (1993) Characterization of sugar moieties and oligosaccharide sequences in the distal intestinal epithelium of the rainbow trout by means of lectin histochemistry. J Fish Biol 43: 709-722.
Parrillo F, Arias MP, Verini Supplizi A (2009) Glycoprofile of the different cell types present in the mucosa of the horse guttural pouches. Tissue Cell 41: 257-265.
Patiño R, Sullivan CV (2002) Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol Biochem 26: 57-70.
Riehl R, Patzner RA (1998) Minireview: the modes of egg attachment in teleost fishes. Ital J Zool (Modena) 65: 415-420.
Rosengrave P, Taylor H, Montgomerie R, Metcalf A, McBride K, Gemmell NJ (2009) Chemical composition of seminal and ovarian fluids of chinook salmon (Oncorhynchus tshawytscha) and their effects on sperm motility traits. Comp Biochem Physiol Part A: Mol Integr Physiol 152 (1): 123-129.
Sáez FG, Madrid JF, Alonso E, Hernández F (2001) Glycan composition of follicle (Sertoli) cells of the amphibian Pleurideles waltl: A lectin histochemical study. J Anat 198: 673-681.
Sales NG, dos Santos SA, Arantes FP, Hojo RES, dos Santos JE (2012) Ovarian Structure and Oogenesis of Catfish Pimelodella vittata (Lütken, 1874) (Siluriformes, Heptapteridae). Anat Histol Embryol 42 (3): 213-219.
Sarasquete C, González de Canales ML, Piñuela C, Muñoz Cueto JA, Rendón C, Mañanós EL, Rodríguez Gómez FJ, Pascual E (2002) Histochemical characteristics of the vitellogenic oocytes of the bluefin tuna, Thunnus thynnus L. Cienc Mar 28(4): 419-431.
Turner E, Montgomerie R (2002) Ovarian fluid enhances sperm movement in Arctic char. J Fish Biol 60 (6): 1570-1579.
Yoneda M, Tokimura M, Fujita H, Takeshita N, Matsuyama M, Matsuura (1998) Reproductive cycle and sexual maturity of the anglerfish Lophiomus setigerus in the East China Sea with a note on specialized spermatogenesis. J Fish Biol 53: 164-178.
Zimmer G, Reuter G, Schauer R (1992) Use of influenza C virus for detection of 9-O-acetylated sialic acids on immobilized glycoconjugates by esterase activity. Eur J Biochem 204: 209-215.
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2016-06-29
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COHEN, S., FREIJO, R., PETCOFF, G. M., PORTIANSKY, E. L., BARBEITO, C. G., MACCHI, G. J., & DIAZ, A. O. (2016). Glycoconjugates of the ovary of Genypterus Blacodes and its importance in the reproductive biology. Revista Ciencias Morfológicas, 18(1). Retrieved from https://revistas.unlp.edu.ar/Morfol/article/view/2658
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