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An overview of functional and stereological evaluation of spermatogenesis and germ cell transplantation in fish

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Abstract

Although there are almost thirty-thousand species of fish living in a great variety of habitats and utilizing vast reproductive strategies, our knowledge of morphofunctional and quantitative aspects of testis structure and spermatogenesis is still incipient for this group of vertebrates. In this review, we discuss aspects that are important to better understanding of testis structure and function, and of the development of germ cells (GC) during spermatogenesis. To achieve this, we have recently completed a number of studies presenting morphometric and functional data related to the numbers of GC and Sertoli cells (SC) per each type of spermatogenic cyst, the number of spermatogonial generations, the SC efficiency, and the magnitude of GC loss that normally occurs during spermatogenesis. We also investigated SC proliferation and the relationship of this important event to early spermatogenic cysts. The available data strongly suggest that SC proliferation in sexually mature tilapia is the primary factor responsible for the increase in testis size and for determination of the magnitude of sperm production. The influence of temperature on the duration of spermatogenesis in tilapia was also evaluated and we have used this knowledge to deplete endogenous spermatogenesis in this teleost, in order to develop an experimental system for GC transplantation. This exciting technique results in new possibilities for investigation of spermatogenesis and spermatogonial stem cell biology, creating also an entirely new and promising scenario in biotechnology—transgenic animal production and the preservation of the genetic stocks of valuable animals or endangered species.

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References

  • Almeida FF, Kristoffersen C, Taranger GL, Schulz RW (2008) Spermatogenesis in Atlantic cod (Gadus morhua): a novel model of cystic germ cell development. Biol Reprod 78(1):27–34

    Article  PubMed  CAS  Google Scholar 

  • Alvarenga ER, Bazzoli N, Santos GB, Rizzo E (2006) Reproductive biology and feeding of Curimatella lepidura (Eigenmann & Eigenmann) (Pisces, Curimatidae) in Juramento reservoir, Minas Gerais, Brazil. Rev Braz Zool 23(2):314–322

    Google Scholar 

  • Ando N, Miura T, Nader MR, Miura C, Yamauchi K (2000) A method for estimating the number of mitotic divisions in fish testis. Fish Sci 66:299–303

    Article  CAS  Google Scholar 

  • Batlouni SR, Romagosa E, Borella MI (2006) The reproductive cycle of male catfish Pseudoplatystoma fasciatum (Teleostei, Pimelodidae) revealed by changes of the germinal epithelium. An approach addressed to aquaculture. Anim Reprod Sci 96(1–2):116–132

    Article  PubMed  CAS  Google Scholar 

  • Baum JS, George JPS, McCall K (2005) Programmed cell death in germline. Semin Cell Dev Biol 16:245–259

    Article  PubMed  CAS  Google Scholar 

  • Billard R (1969) La spermatogenèse de Poecilia reticulata I. Estimation du nombre de generations goniales et rendement de la spermatogenèse. Ann Biol Biochem Biophys 9:251–271

    Article  Google Scholar 

  • Bizzotto PM, Godinho HP (2007) Morphometric evaluation of the spermatogenesis in trahira Hoplias malabaricus (Bloch) (Characiformes, Erythrinidae). Rev Braz Zool 24(3):541–544

    Google Scholar 

  • Braat AK, Zandbergen T, Water SVD, Goos HJTh, Zivkovic D (1999) Characterization of zebrafish primordial germ cells: morphology and early distribution of vasa RNA. Dev Dyn 216(2):153–167

    Article  PubMed  CAS  Google Scholar 

  • Brinster RL, Avarbock MR (1994) Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci USA 91:11303–11307

    Article  PubMed  CAS  Google Scholar 

  • Brinster RL, Zimmermann JW (1994) Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci USA 91:11298–11302

    Article  PubMed  CAS  Google Scholar 

  • Chaves-Pozo E, Mulero V, Meseguer J, Ayala AG (2005) An overview of cell renewal in the testis throughout the reproductive cycle of a seasonal breeding teleost, the gilthead seabream (Sparus aurata L.). Biol Reprod 72:593–601

    Article  PubMed  CAS  Google Scholar 

  • Cinquetti R, Dramis L (2003) Histological, histochemical, enzyme histochemical and ultrastructural investigations of the testis of Padogobius martensi between annual breeding seasons. J Fish Biol 63:1402–1428

    Article  CAS  Google Scholar 

  • Cooke PS, Hess RA, Kirby JD (1994) A model for increasing testis size and sperm production: potential application to animal science. J Anim Sci 72:43–54

    Google Scholar 

  • De Rooij DG (2006a) Rapid expansion of the spermatogonial stem cell tool box. Proc Natl Acad Sci USA 103(21):7939–7940

    Article  PubMed  Google Scholar 

  • De Rooij DG (2006b) Regulation of spermatogonial stem cell behavior in vivo and in vitro. Anim Reprod 3(2):130–134

    Google Scholar 

  • De Rooij DG, Russell LD (2000) All you wanted to know about spermatogonia but were afraid to ask. J Androl 21:776–798

    PubMed  Google Scholar 

  • Fishelson L (2003) Comparison of testes structure, spermatogenesis, and spermatocytogenesis in young, aging, and hybrid cichlid fish (Cichlidae, Teleostei). J Morphol 256:285–300

    Article  PubMed  Google Scholar 

  • Fishelson L, Delarea Y, Gon O (2006) Testis structure, spermatogenesis, spermatocytogenesis, and sperm structure in cardinal fish (Apogonidae, Perciformes). Anat Embryol 211:31–46

    Article  PubMed  Google Scholar 

  • Fishelson L, Gon O, Holdengreber V, Delarea Y (2007) Comparative spermatogenesis, spermatocytogenesis, and spermatozeugmata formation in males of viviparous species of clinid fishes (Teleostei:Clinidae, Blennioidei). Anat Record 290:311–323

    Article  Google Scholar 

  • França LR, Russell LD (1998) The testis of domestic animals. In: Martínez-García F, Regadera J (eds) Male reproduction: a multidisciplinary overview. Churchill Communications, Madrid, pp 198–219

    Google Scholar 

  • França LR, Ogawa T, Avarbock MR, Brinster RL, Russell LD (1998) Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod 59(6):1371–1377

    Article  PubMed  Google Scholar 

  • Godinho HP (2007) Reproductive strategies of fishes applied to aquaculture: bases for development of production technologies. Rev Bras Reprod Anim 31(3):351–360

    Google Scholar 

  • Grier HJ (1993) Comparative organization of Sertoli cells including the Sertoli cell barrier. In: Russell LD, Griswold MD (eds) The Sertoli cell. Cache River Press, Clearwater, FL, pp 704–739

    Google Scholar 

  • Grier HJ, Taylor RG (1998) Testicular maturation and regression in the common snook. J Fish Biol 53:521–542

    Article  Google Scholar 

  • Gusmão P, Foresti F, Quagio-Grassiotto I (2002) The ultrastructure of the pre-meiotic and meiotic stages of spermatogenesis in Plagioscion squamosissimus (Teleostei, Perciformes, Sciaenidae). J Submicrosc Cytol Pathol 34(2):159–165

    PubMed  Google Scholar 

  • Hess RA, França LR (2007) Spermatogenesis and cycle of the seminiferous epithelium. In: Cheng CY (ed) Molecular mechanisms in spermatogenesis. Landes Bioscience, pp 1–15

  • Hoar WS (1969) Reproduction. In: Hoar WS, Randall DJ (eds) Fish physiology, Chap 1, vol 111. Academic Press, New York

    Google Scholar 

  • Kobayashi T, Takeuchi Y, Takeuchi T, Yoshizaki G (2006) Generation of viable fish from cryopreserved primordial germ cells. Mol Reprod Dev 74(2):207–213

    Article  Google Scholar 

  • Koulish S, Kramer CR, Grier HJ (2002) Organization of the male gonad in a protogynous fish, Thalassoma bifasciatum (Teleostei: Labridae). J Morphol 254:292–311

    Article  PubMed  Google Scholar 

  • Krovel AV, Olsen LC (2002) Expression of vas::EGFP transgene in primordial germ cells of the zebrafish. Mech Dev 116:141–150

    Article  PubMed  CAS  Google Scholar 

  • Jamieson BGM (1991) Fish evolution and systematics: evidence from spermatozoa. Cambridge University Press, Cambridge

    Google Scholar 

  • Lacerda SMSN, Batlouni SR, Silva SBG, Homem CSP, França LR (2006) Germ cells transplantation in fish: the Nile-tilapia model. Anim Reprod 3(2):146–159

    Google Scholar 

  • Lacerda SMSN, Batlouni SR, Assis LH, Resende FM, Campos-Silva SM, Campos-Silva R, Segatelli TM, França LR (2008) Germ cell transplantation in tilapias (Oreochromis niloticus). Cybium (in press)

  • Le Gac F, Loir M (1999) Male reproductive system, fish. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction, vol 3. Academic Press, San Diego, pp 20–30

    Google Scholar 

  • Leal MC, França LR (2006) The seminiferous epithelium cycle length in the black tufted-ear marmoset (Callithrix penicillata) is similar to humans. Biol Reprod 74(4):616–624

    Article  PubMed  CAS  Google Scholar 

  • Lo Nostro FL, Grier H, Meijide FJ, Guerrero GA (2003) Ultrastructure of the testis in Synbranchus marmoratus (Teleostei, Synbranchidae): the germinal compartment. Tissue Cell 35:121–132

    Article  PubMed  CAS  Google Scholar 

  • Loir M, Sourdaine P, Mendis-Handagama SMLC, Jégou B (1995) Cell–cell interactions in the testis of teleosts and elasmobranchs. Microsc Res Tech 32:533–552

    Article  PubMed  CAS  Google Scholar 

  • Matta SLP, Vilela DAR, Godinho HP, França LR (2002) The goitrogen 6-n-propyl-2-thiouracil (PTU) given during testis development increases Sertoli and germ cell numbers per cyst in fish: the tilapia (Oreochromis niloticus) model. Endocrinology 143:970–978

    Article  PubMed  CAS  Google Scholar 

  • McClusky LM (2005) Stage and season effects on cell cycle and apoptotic activities of germ cells and Sertoli cells during spermatogenesis in the spiny dogfish (Squalus acanthias). Reproduction (129):89–102

  • Miura T (1999) Spermatogenic cycle in fish. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction, vol 4. Academic Press, San Diego, pp 571–578

    Google Scholar 

  • Miura T, Miura CI (2003) Molecular control mechanisms of fish spermatogenesis. Fish Physiol Biochem 28:181–186

    Article  CAS  Google Scholar 

  • Miura C, Kuwahara R, Miura T (2006) Transfer of spermatogenesis-related cDNAs into eel testis germ-somatic cell coculture pellets by electroporation: methods for analysis of gene function. Mol Reprod Dev 74(4):420–427

    Article  Google Scholar 

  • Moyle PB, Cech JJ (2004) Fishes: an introduction to ichthyology, 5th edn. Prentice Hall, Englewood Cliffs, NJ, p 726

    Google Scholar 

  • Nagahama Y (1983) The functional morphology of teleost gonads. In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish physiology, Chap 6, vol IXA. Academic Press, New York, pp 223–275

    Google Scholar 

  • Nakatani K, Agostinho AA, Baumgartner G, Bialetzki A, Sanches PV, Makrakis MC, Pavanelli CS (2001) Ovos e larvas de peixes de água doce: desenvolvimento e manual de identificação. EDUEM, Maringá

    Google Scholar 

  • Negrão JNC, Carvalho ED, Foresti F, Quagio-Grassiotto I (2002) Spermatogonia and spermatocyte ultrastructure in Hoplias malabaricus (Teleostei, Characiformes: Erythrinidae). J Zool Lond 257:287–293

    Article  Google Scholar 

  • Nóbrega RH (2003) Capacidade suporte das células de Sertoli e alterações do epitélio germinativo masculino e do tecido intersticial durante o ciclo reprodutivo de peixes neotropicais. Monograph. Universidade Estadual Paulista, Botucatu, Brazil

    Google Scholar 

  • Nóbrega RH (2006) Alterações do epitélio germinativo masculino, células endócrinas testiculares e células gonadotrópicas durante o ciclo reprodutivo de Serrasalmus spilopleura (Kner, 1859) e Pimelodus maculatus (Lacépède, 1803). Dissertation, Universidade Estadual de Campinas, Campinas, Brazil

  • Nóbrega RH, Quagio-Grassiotto I (2007) Morphofunctional changes in Leydig cells throughout the continuous spermatogenesis of the freshwater teleost fish, Serrasalmus spilopleura (Characiformes, Characidae): an ultrastructural and enzyme study. Cell Tissue Res 329(2):339–349

    Article  PubMed  Google Scholar 

  • Okutsu T, Suzuki K, Takeuchi Y, Takeuchi T, Yoshizaki G (2006a) Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional egg in fish. Proc Natl Acad Sci USA 103:2725–2729

    Article  PubMed  CAS  Google Scholar 

  • Okutsu T, Yano A, Nagasawa K, Shikina S, Kobayashi T, Takeuchi Y, Yoshizaki G (2006b) Manipulation of fish germ cell: visualization, cryopreservation and transplantation. J Reprod Dev 52:685–693

    Article  PubMed  Google Scholar 

  • Okutsu T, Shikina S, Kanno M, Takeuchi Y, Yoshizaki G (2007) Production of trout offspring from triploid salmon parents. Science 14:317(5844):1517

    Google Scholar 

  • Prisco M, Liguoro A, Comitato R, Cardone A, D’Onghia B, Ricchiari L, Angelini F, Andreuccetti P (2003) Apoptosis during spermatogenesis in the spotted ray Torpedo marmorata. Mol Reprod Dev 64(3):341–348

    Article  PubMed  CAS  Google Scholar 

  • Pudney J (1993) Comparative cytology of the non-mammalian vertebrate Sertoli cell. In: Russell LD, Griswold MD (eds) The Sertoli cell. Cache River Press, Clearwater, FL, pp 612–657

    Google Scholar 

  • Pudney J (1995) Spermatogenesis in nonmammalian vertebrates. Microsc Res Tech 32:459–497

    Article  PubMed  CAS  Google Scholar 

  • Pudney J (1996) Comparative cytology of the Leydig cell. In: Payne AH, Hardy MP, Russell LD (eds) The Leydig cell. Cache River Press, Vienna, IL, pp 98–142

    Google Scholar 

  • Pudney J (1999) Leydig and Sertoli cells, nonmammalian. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction, vol 2. Academic Press, San Diego, pp 1008–1020

    Google Scholar 

  • Quagio-Grassiotto I, Carvalho ED (1999) The ultrastructure of Sorubim lima (Teleostei, Siluriformes, Pimelodidae) spermatogenesis: premeiotic and meiotic periods. Tissue Cell 31(6):561–567

    Article  PubMed  CAS  Google Scholar 

  • Roosen-Runge EC (1977) The process of spermatogenesis in mammals. University Press, Cambridge

    Google Scholar 

  • Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED (1990) Mammalian spermatogenesis. In: Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED (eds) Histological and histopathological evaluation of the testis. Cache River Press, Clearwater, FL, pp 1–40

    Google Scholar 

  • Saito T, Goto-Kazeto R, Arai K, Yamaha E (2008) Xenogenesis in teleost fish through generation of germ-line chimeras by single primordial germ cell transplantation. Biol Reprod 78(1):159–166

    Article  PubMed  CAS  Google Scholar 

  • Schulz RW (2003) Endocrine regulation of spermatogenesis in teleost fish. ARBS Annu Rev Biomed Sci 5:57–68

    Article  CAS  Google Scholar 

  • Schulz RW, Miura T (2002) Spermatogenesis and its endocrine regulation. Fish Physiol Biochem 26:43–56

    Article  CAS  Google Scholar 

  • Schulz RW, van Dijk W, Bogerd J (2003) Sertoli cell proliferation and FSH signaling in African catfish, Clarias gariepinus. Fish Physiol Biochem 28:223–224

    Article  CAS  Google Scholar 

  • Schulz RW, Menting S, Bogerd J, França LR, Vilela DAR, Godinho HP (2005) Sertoli cell proliferation in the adult testis-evidence from two fish species belonging to different orders. Biol Reprod 73:891–898

    Article  PubMed  CAS  Google Scholar 

  • Setchell BP (2006) The effects of heat on the testis of mammals. Anim Reprod 3(2):81–91

    Google Scholar 

  • Shaha C (2007) Modulators of spermatogenic cell survival. Soc Reprod Fertil Suppl 63:173–186

    PubMed  CAS  Google Scholar 

  • Shikina S, Ihara S, Yoshizaki G (2008) Culture conditions for maintaining the survival and mitotic activity of rainbow trout transplantable type A spermatogonia. Mol Reprod Dev 75(3):529–537

    Article  PubMed  CAS  Google Scholar 

  • Silva M (1987) Morfologia ultra-estrutural do testículo, cinética da espermatogênese e barreira hemo-testicular da tilapia do Nilo, Oreochromis niloticus (Peixe, Ciclídeo). Thesis, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil

  • Takeuchi Y, Yoshizaki G, Kobayashi T, Takeuchi T (2002) Mass isolation of primordial germ cells from transgenic rainbow trout carrying the green fluorescent protein gene driven by the vasa gene promoter. Biol Reprod 67:1087–1092

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi Y, Yoshizaki G, Takeuchi T (2003) Generation of live fry from intraperitoneally transplanted primordial germ cells in rainbow trout. Biol Reprod 69:1142–1149

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi Y, Yoshizaki G, Takeuchi T (2004) Surrogate broodstock produces salmonids. Nature 430:629–630

    Article  PubMed  CAS  Google Scholar 

  • Vazzoler AEAM (1996) Biologia da reprodução de peixes teleósteos. Teoria e prática. EDUEM, Maringá

    Google Scholar 

  • Vilela DAR, Silva SGB, Peixoto MTD, Godinho HP, França LR (2003) Spermatogenesis in teleost: insights from Nile tilapia (Oreochromis niloticus) model. Fish Physiol Biochem 28:187–190

    Article  CAS  Google Scholar 

  • Yano A, Suzuki A, Yoshizaki G (2008) Flow-cytometric isolation of testicular germ cells from rainbow trout (Oncorhynchus mykiss) carrying the green fluorescent protein gene driven by trout vasa regulatory regions. Biol Reprod 78(1):151–158

    Article  PubMed  CAS  Google Scholar 

  • Yoshizaki G, Takeuchi Y, Sakatani S, Takeuchi T (2000) Germ cell-specific expression of green fluorescent protein in transgenic rainbow trout under control of the rainbow trout vasa-like gene promoter. Int J Dev Biol 44:323–326

    PubMed  CAS  Google Scholar 

  • Yu Q, Wu J (2008) Involvement of cyclins in mammalian spermatogenesis. Mol Cell Biochem. doi: 10.1007/s11010-008-9783-8

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Nóbrega, R.H., Batlouni, S.R. & França, L.R. An overview of functional and stereological evaluation of spermatogenesis and germ cell transplantation in fish. Fish Physiol Biochem 35, 197–206 (2009). https://doi.org/10.1007/s10695-008-9252-z

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