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An Updated Version of Histological and Ultrastructural Studies of Oogenesis in the Siberian Sturgeon Acipenser baerii

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The Siberian Sturgeon (Acipenser baerii, Brandt, 1869) Volume 1 - Biology

Abstract

Oogenesis of Siberian sturgeon Acipenser baerii is studied on farm fish using light and electron microscopy. We have identified five stages correlated with physiological state of the ovarian follicle constituted by the oocyte surrounded by its cellular (theca and granulosa) and a-cellular (zona radiata) layers: Stages I and II before vitellogenesis, Stages III and IV during vitellogenesis, and Stage V during maturational processes.

Following the oogonial stage, Stage I presents an elevated nucleoplasmic index, and the nucleus contains only one nucleolus. In this early stage, lipid globules were identified. Stage II is characterized by nucleoli multiplication and their migration toward the nuclear periphery. During this stage, the number of lipid globules increases in the oocyte cytoplasm. At the end of this stage, cortical alveoli get synthesized. The beginning of Stage III, called sub-Stage IIIa, corresponds to the first features of vitellogenin incorporation simultaneously with the elaboration of the zona radiata externa. During sub-Stage IIIb the zona radiata interna 1 is built. Stage IV is characterized by the first apparition of pigment granules and the elaboration of the zona radiata interna 2. Yolk accumulation increases and the oocyte volume grows considerably. Stage V corresponds to maturation with the beginning of nucleus migration toward the oocyte membrane. The zona radiata is completely synthesized, and a “jelly coat” is deposited on the outer surface of the zona radiata externa by synthesis of granulosa cells. Yolk accumulation ends at this stage.

In conclusion, ultrastructural data allow accurate determination of oogenesis stages.

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References

  • Abraham M et al (1984) The cellular envelope of oocytes in Teleosts. Cell Tissue Res 235:403–410

    Article  CAS  PubMed  Google Scholar 

  • Agulleiro M et al. (2007) High transcript level of fatty acid-protein but not very low-density lipoprotein receptor is correlated to ovarian follicle in teleost fish (Solea senegalensis). Biol Reprod PMID: 17554079

    Google Scholar 

  • Akimova NB et al. (1979) Growth and gametogenesis of the Siberian sturgeon (Acipenser baerii B.) under experimental and natural conditions. Proc. 7th Japan Soviet joint Symp Aquacult Tokyo: 179

    Google Scholar 

  • Amanze D, Lyengar A (1990) The micropyle: a sperm guidance system in teleost fertilization. Development 109:495–500

    CAS  PubMed  Google Scholar 

  • Anderson E (1967) The formation of the primary envelope during oocyte differentiation in teleosts. J Cell Biol 35:193–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badenko LV et al (1981) Method for evaluating the quality of sturgeon spawners as exemplified in the sevryuga (Acipenser stellatus) from the Kuban river. J Ichthyol 21:96–103

    Google Scholar 

  • Besseau L, Giraud-Guille MM (1995) Stabilization of fluid cholesteric phases of collagen to ordered gelateed matrices. J Mol Biol 251:197–202

    Article  CAS  PubMed  Google Scholar 

  • Bouligand Y (1972) Twisted fibrous arrangements in biological materials and cholesteric mesophases. Tissue Cell 4:189–217

    Article  CAS  PubMed  Google Scholar 

  • Breton B et al (1983) Maturational glycoprotein gonadotropin and estradiol-17ß during the reproductive cycle of the female brown tour (Salmo trutta). Gen Comp Endocrinol 49:220–231

    Article  CAS  PubMed  Google Scholar 

  • Bruslé S (1980) Fine structure of early previtellogenic oocytes in Mugil (Lisa) auratus Risso, 1810 (Teleostei, Mugilidae). Cell Tissue Res 207:121–134

    Article  Google Scholar 

  • Bruslé S, Bruslé J (1978) An ultrastructural study of early germs cells in Mugil (Liza) auratus Risso, 1810 (Teleostei, Mugilidae). Ann Biol Anim Biophys 18:1141–1153

    Article  Google Scholar 

  • Busson-Mabillot S (1969) Données récentes sur la vitellogénèse. Ann Biol 8:199–227

    CAS  Google Scholar 

  • Busson-Mabillot S (1973) Evolution des enveloppes de l’ovocyte et de l’œuf chez un poisson téléostéen. J Microscopie 18:23–44

    Google Scholar 

  • Busson-Mabillot S (1977) Un type particulier de sécrétion exocrine, celui de l’appareil adhésif de l’oeuf d’un poisson téléostéen. Biol Cell 30:233–244

    Google Scholar 

  • Caloianu-Yordachel M (1971) L’ovogénèse chez les poissons Acipenséridés, la morphogénèse et la constitution histochimique des membranes externes. Rev Roum Biol Zool 16(2):113–120

    Google Scholar 

  • Caporiccio B, Connes R (1977) Etude ultrastructurale des enveloppes périovocytaires et périovulaires de Dicentrarchus labrax L. (Poisson téléostéen). Ann Sei Nat Zool Paris 19(12ème série):351–368

    Google Scholar 

  • Carnaveli O et al (1999) Yolk formation and degradation during oocyte maturation in bream, Sparus aurata: involvement of two lysosomal proteinases. Biol Reprod 60:140–146

    Article  Google Scholar 

  • Chan L et al (1991) Vitellogenin purification and development of assay for vitellogenin receptor in oocyte membranes of the tilapia (Oreochromis niloticus Linnaeus) 1766. J Exp Zool 257:96–109

    Article  CAS  Google Scholar 

  • Cherr GN, Clark WH Jr (1982) Fine structure of the envelope and the micropyles of the eggs of the white sturgeon Acipenser transmontanus. Develop Growth Differ 24:341–352

    Article  Google Scholar 

  • Cherr GN, Clark WH Jr (1984) Jelly release in the eggs of the white sturgeon Acipenser transmontanus: an enzymatically mediated event. J Exp Zool 230:145–149

    Article  CAS  Google Scholar 

  • Clérot JC (1976) Les groupements mitochondriaux des cellules germinales de poissons Téléostéens Cyprinidés. 1. Etude ultrastructurale. J Ultrastruct Res 54:461–475

    Article  PubMed  Google Scholar 

  • Clérot JC, Wegnez M (1977) Etude ultrastructurale et biochimique de l’ovocyte en prévitellogénèse de vertébrés inférieurs. Biol Cell 29:23a

    Google Scholar 

  • Davail B et al (1998) Evolution of oogenesis: the receptor fot vitellogenin from the rainbow trout. J Lipid Res 39:1929–1937

    CAS  PubMed  Google Scholar 

  • De Vlaming VL et al (1980) Golsfish Carassius auratus vitellogenin: induction, isolation, properties and relationship to yolk proteins. Comp Biochem Physiol 67 b:613–623

    Google Scholar 

  • Droller MJ, Roth TF (1966) An electron microscope study of yolk formation during oogenesis in Lebistes reticulatus Guppyi. J Cell Biol 28:209–232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dumont JN, Brummet AR (1980) The viteline envelope, chorion and micropyle of Fundulus heteroclitus eggs. Gamete Res 3:25–44

    Article  Google Scholar 

  • Fedorova LS (1976) Physiological and biochemical characteristics of the reproductive products and larvae of sturgeons during artificial rearing. J Ichthyol 16:427–436

    Google Scholar 

  • Flynn SR, Benfey TJ (2007) Sex differentiation and aspects of gametogenesis in shortnose sturgeon Acipenser brevirostrum Lesueur. J Fish Biol 70:1027–1044

    Article  Google Scholar 

  • Fontana F et al (2008) Evidence of hexaploid karyotype in shortnose sturgeon. Genome 51(2):113–119

    Article  CAS  PubMed  Google Scholar 

  • Fridel G (1922) Les états mésomorphes de la matière. Ann Phys 18:273–474

    Article  Google Scholar 

  • Ginzburg AS (1968) Fertilisation in fishes and the problem of polyspermy. N O A A and National Scientific Foundation Translation, Silver Spring, p 290

    Google Scholar 

  • Ginzburg AS, Detlaf TA (1969) Razvitie Osetrovykh Ryb. Sozrevanie yats, oplodotvorenie i embriogenez. Izdatel’stvo “NAUKA”, Moskva, p 134

    Google Scholar 

  • Giraud-Guille MM (1996) Twisted liquid crystalline supramolecular arrangements in morphogenesis. Int Rev Cytol 166:59–101

    Article  CAS  PubMed  Google Scholar 

  • Grandi G, Chicca M (2008) Histological and ultrastructural investigation of early gonad development and sex differentiation in Adriatic sturgeon Acipenser nacarii, (Acipenseriformes, Chondrostei). J Morphol 269:1238–1262

    Article  PubMed  Google Scholar 

  • Grier H (2000) Ovarian germinal epithelium and folliculogenesis in the common snook Centropomus undecimalis (Teleostei, Centropomidae). J Morphol 243:265–281

    Article  CAS  PubMed  Google Scholar 

  • Guraya SS (1986) The cell and molecular biology of fish oogenesis. In: Sauer HW (ed) Monographs in developmental biology, vol 18. Karger, Basel, pp 1–223

    Google Scholar 

  • Hamagushi S (1985) Changes in the morphology of the germinal dense bodies in primordial germ cells of the teleost Oryzias latipes. Cell Tissue Res 240:669–673

    Article  Google Scholar 

  • Hascall VC, Hascall GK (1981) Proteoglycans. In: Hay ED (ed) Cell biology of extracellular matrix. Plenum Press, New York, pp 39–60

    Chapter  Google Scholar 

  • Havelka M et al (2014) Fertility of a spontaneous hexaploid male Siberian sturgeon, Acipenser baerii. BMC Genet 15:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Hay ED (1981) Cell biology of extracellular matrix. In: Hay ED (ed) . Plenum Press, New York, p 417

    Google Scholar 

  • Hiramatsu N et al (2004) Molecular characterisation and expression of vitellogenin receptor from the white perch (Morone Americana). Biol Reprod 70:1720–1730

    Article  CAS  PubMed  Google Scholar 

  • Hogan JC (1978) An ultrastructural analysis of “cytoplasmic maker” in germ cells of Oryzias latipes. J Ulrastruct Res 62:237–250

    Article  Google Scholar 

  • Iwamatsu T et al (1997) Effect of micropylar morphology and size on rapid sperm entry into the eggs of medaka. Zool Sci 14:626–628

    Article  Google Scholar 

  • Kagawa H (1985) Ultrastructural and histochemical observations regarding the ovarian follicles of the amago salmon (Oncorhynchus rhodurus). J UOEH 7:27–35

    Article  CAS  PubMed  Google Scholar 

  • Kagawa H et al (1981) Correlation of plasma estradiol-17-β and progesterone levels with ultrastructure and histochemistry of ovarian follicles in the spoted char, Salvenilus leucomaenis. Cell Tissue Res 218:315–329

    Article  CAS  PubMed  Google Scholar 

  • Karasaki S (1967) An electron microscope study on the crystalline structure of the yolk platelets of the lamprey egg. J Ultrastruct Res 18:377–390

    Article  CAS  PubMed  Google Scholar 

  • Kijima T, Maruyama T (1985) Histological research for the development of the gonad of the hybrid sturgeon bester (Acipenser ruthenus male x Huso huso female). Bull Nati Res Inst Aquacult 8:23–29

    Google Scholar 

  • Kondrat’yev AK (1977) The functional morphology of oocytes in the period of previtellogenesis in the Siberian sterlet Acipenser ruthenus M. At different time of its annual biological cycle. J Ichthyol 17:769–778

    Google Scholar 

  • Kornienko GG (1975) Early degenerative changes in the oocyte of the Kuban sevryuga Acipenser stellatus. J Ichthyol 15:503–507

    Google Scholar 

  • Le Menn F (1984) Aspects ultrastructuraux, biochimiques et endocriniens de la vitellogénèse d’un poisson téléostéen Gobius niger L. Thèse de Doctorat d’Etat, Univ. Bordeaux I, n° 814

    Google Scholar 

  • Le Menn F, Burzawa-Gerard E (1985) Effect of carp gonadotrophin (cGTH) and a fraction unadsorbed on concavalin A-sepharose obtained from c-GTH on vitellogenesis in the hypophysectomized marine teleost Gobius niger. Gen Comp Endocrinol 57:23–36

    Article  PubMed  Google Scholar 

  • Le Menn F, Pelissero C (1991) Histological and ultrastructural studies of oogenesis of the Siberian sturgeon (Acipenser baerii). In: Williot P (ed) , vol 57. CEMAGREF, Antony, France, pp 23–36

    Google Scholar 

  • Le Menn F et al. (1999) A new approach to fish oocyte vitellogenesis. Proc 6th Int. Symp Reprod Physiol Fish, Bergen, Norway: 281–284

    Google Scholar 

  • Le Menn F et al. (2007) Ultrastructural aspects of the ontogeny and differentiation of ray-finned fish ovarian follicles. In: Babin PJ et al (eds) The fish oocyte: from basic studies to biochemical applications, p 1–37

    Google Scholar 

  • Magnin E (1967) Recherches sur les cycles de reproduction des esturgeons Acipenser fulvescens Raf. de la rivière Nottaway tributaire de la Baie James. Verh Int Ver Limnol 16:1018–1024

    Google Scholar 

  • Markov KP (1975) Scanning electron microscope study of the microstructure of the egg membrane in the Russian sturgeon Acipenser gueldenstaedtii B. J Ichthyol 15:739–749

    Google Scholar 

  • Matova N, Cooley L (2001) Comparative aspects of animal oogenesis. Dev Biol 231:291–320

    Article  CAS  PubMed  Google Scholar 

  • Mazabraud A et al (1975) Biochemical research on oogenesis. RNA accumulation in the oocytes of teleosts. Dev Biol 44:326–332

    Article  CAS  PubMed  Google Scholar 

  • Nagahama Y (1983) The functional morphology of teleost gonad. In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish physiology. Acad Press, NY IX A, pp 223–275

    Google Scholar 

  • Nagahama Y (1997) 17-20ß-dihydroxy-pregnen-3-one, a maturation inducing hormone in fish oocytes: mechanisms of synthesis and action. Steroids 62:190–196

    Article  CAS  PubMed  Google Scholar 

  • Nagahama Y et al (1995) Regulation of oocyte growth and maturation in fish. Curr Yop Dev Biol 30:103–145

    Article  CAS  Google Scholar 

  • Nakamura M, Nagahama Y (1985) Steroid producing cells during ovarian differentiation of the tilapia, Sarotherodon niloticus. Dev Growth Diffr 27:701–708

    Article  Google Scholar 

  • Nakamura M et al (1993) Ultrastructural analysis of the developing follicle during early vitellogenesis in tilapia, Oreochromis niloticus, with special references in the steroid-producing cells. Cell Tissue Res 272:33–39

    Article  CAS  Google Scholar 

  • Nunez Rodriguez J (1985) Contribution à l’étude de la biologie de la reproduction de la sole (Solea vulgaris Quensel 1806). Approche ultrastructurale et physiologique. Thèse 3ème Cycle, Université de Bordeaux I, n° 2061

    Google Scholar 

  • Parry EW (1973) Methylene blue and azure-2 as stains for lipid in osmium-fixed tissues embeded in araldite. J Clin Pathol 16:546–548

    Article  Google Scholar 

  • Pearse (1976) Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles. Proc Natl Acad Sc USA 73:1255–1259

    Article  CAS  Google Scholar 

  • Pelissero C (1988) Mise en place des bases méthodologiques pour l’étude de la reproduction chez l’esturgeon Acipenser baerii femelle. Thèse de 3ème cycle, Université de Bordeaux I, n° 2229

    Google Scholar 

  • Pelissero C et al (1985) Ultrastructural characteristic features of the oocyte of the sturgeon Acipenser baerii B, 7th Conf Fish Culture Europ Soc Comp Physiol Biochem Barcelona, vol A3, Promociones Publicationes Universitarias, Barcelona, p 8

    Google Scholar 

  • Perazzolo LM et al (1999) Expression and localization of messenger ribonucleic acid for the vitellogenin receptor in ovarian follicles throughout oogenesis in the rainbow trout, Oncorhynchus mykiss. Biol Reprod 60:1057–1068

    Article  CAS  PubMed  Google Scholar 

  • Raïkova EV (1976) Evolution of the nuclear apparatus during oogenesis in Acipenseridae. J Embryol Exp Morphol 35(8):667–687

    PubMed  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at hight pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riehl R (1978) Electronen mikroskopische und autoradiographische Untersuchungen an den Dotterkernen in den Oocyten von Noemacheilus barbatulus L. und Phoxinus phoxinus L. (Pisces, Teleostei). Cytobiologie 17:137–145

    CAS  PubMed  Google Scholar 

  • Rzepkowska M, Ostaszewska T (2013) Proliferating cell nuclear antigen and Vasa protein expression during gonadal development and sexual differentiation in cultured Siberian (Acipenser baerii Brandt, 1869) and Russian (Acipenser gueldenstaedtii Brandt, Ratzeburg, 1833) sturgeon. Rev Aquac 5:1–14

    Article  Google Scholar 

  • Selman K, Wallace RA (1982) The inter- and intracellular passage of protein through the ovarian follicle in teleosts. In: Proc. Int Symp Reprod Physiol Fish. Wageningen, The Netherlands, p 57

    Google Scholar 

  • Selman K, Wallace RA (1989) Cellular aspects of oocyte growth in teleost. Zool Sci 6:211–231

    Google Scholar 

  • Selman K et al (1993) Stages of oocyte development in the zebrafish, Brachidanio rerio. J Morphol 218:203–224

    Article  Google Scholar 

  • Senthilkumaran B et al (2004) A shift un steroidogenesis occurring in ovarian follicles prior to oocyte maturation. Mol Cell Endocrinol 215:11–18

    Article  CAS  PubMed  Google Scholar 

  • Sire MF et al (1994) Involvement of the lysosomal system in yolk protein deposit and degradation during vitellogenesis and embryonic development in trout. J Exp Zool 269:69–83

    Article  CAS  Google Scholar 

  • Stifani S et al (1990) Regulation of oogenesis: the piscine receptor for vitellognin. Biochem Biophys Acta 1045:271–279

    Article  CAS  PubMed  Google Scholar 

  • Tesoriero JV (1977) Formation of the chorion (zona pellucida) in the teleost Oryzias latipes. I. Morphology of early oogenesis. J Ultrastruct Res 59:282–291

    Article  CAS  PubMed  Google Scholar 

  • Toshimori K, Yasuzuni F (1979) Gap junctions between microvillosities of the oocyte and follicular cells in the teleost Plecoglossus altivelis. Z Mikrosk Anat Forsch 93:458–164

    CAS  PubMed  Google Scholar 

  • Trusov VZ (1975) Maturation in the gonads of the female sevryuga Acipenser stellatus during its life in the ocean. J Ichthyol 15:61–72

    Google Scholar 

  • Ulrich E (1969) Etude des ultrastructures au cours de l’ovogenèse d’un poisson téléostéen le Danio Brachydanio rerio. J Microsc 8:447–473

    Google Scholar 

  • Veshchev PV (1982) Reproduction of sterlet Acipenser ruthenus (Acipenseridae) in the lower volga. J Ichthyol 22:40–46

    Google Scholar 

  • Vrackq R (1974) Basal lamina scaffold: anatomy and significance for maintenance of orderly tissue structure. Am J Pathol 77:314–346

    Google Scholar 

  • Wallace RA, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleosts. Am Zool 21:325–343

    Article  Google Scholar 

  • Wallace RA et al. (1983) The oocyte as an endocytotic cell. In: Molecular biology of egg maturation. Ciba Found Symp Eds Pitman Books London: p 228–248

    Google Scholar 

  • Williot P, Brun R (1982a) Résultats sur la reproduction d’Acipenser baerii en 1982. Bull Fr Piscic 287:19–22

    Article  Google Scholar 

  • Williot P, Rouault T (1982b) Compte rendu d’une première reproduction en France de l’esturgeon sibérien Acipenser baerii. Bull Fr Piscic 286:255–261

    Article  Google Scholar 

  • Woods JW, Roth TF (1980) Selective protein transport: identity of the solubilized phosvitin receptor from chicken oocyte. J Supramol Struct 14:473–480

    Article  CAS  PubMed  Google Scholar 

  • Wourms JP (1976) Annual fish oogenesis. I. Differentiation of the mature oocyte and formation of the primary envelope. Dev Biol 50:338–354

    Article  CAS  PubMed  Google Scholar 

  • Wourms JP, Sheldon H (1976) Annual fish oogenesis. II. Formation of the secondary egg envelope. Dev Biol 50:355–366

    Article  CAS  PubMed  Google Scholar 

  • Yamashita M (1998) Molecular mechanisms of meiotic maturation and arrest in fish and amphibian oocytes. Semin Cell Dev Biol 9:569–579

    Article  CAS  PubMed  Google Scholar 

  • Yusko S et al (1981) Receptor-mediated vitellogenin binding to chicken oocytes. Biochem J 200:43–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zelazowska M et al. (2015) Ovarian nests in immature and mature sturgeons (Acipenser gueldenstaedtii) and paddlefish (Polyodon spathula) (Chondrostei, Acipenseriformes) comprise early previtellogenic oocytes. Tissue Cell

    Google Scholar 

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Le Menn, F., Benneteau-Pelissero, C., Le Menn, R. (2018). An Updated Version of Histological and Ultrastructural Studies of Oogenesis in the Siberian Sturgeon Acipenser baerii . In: Williot, P., Nonnotte, G., Vizziano-Cantonnet, D., Chebanov, M. (eds) The Siberian Sturgeon (Acipenser baerii, Brandt, 1869) Volume 1 - Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-61664-3_14

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