Skip to main content
SpringerLink
Log in

Cell junctions in fish seminiferous epithelium

Fish Physiology and Biochemistry volume 35, pages 207–217 (2009)Cite this article

Abstract

Similar to mammals, in fish the cellular interactions between Sertoli cells (SC) and germ cells (GC) in the seminiferous epithelium have important structural and functional roles. In this review, we give a brief summary of these interactions, in particular those on the cell junctions. Despite the scarcity of detailed empirical data, it appears that both basic types of adhesive junctions (actin- and intermediate filaments-related) are present between SC. However, the actin-related multifunctional junction known as the “ectoplasmic specialization” is seemingly present only in some cartilaginous fish. Conversely, SC in other fish species are joined by actin-related junctions similar to typical zonulae or puncta adherens found in other epithelia. Adhesive junctions are also found between SC and GC and between GC and GC, and due to their particular characteristics these junctions are known as “desmosome-like junctions”. In terms of intercellular communication, connexins and gap junctions have been shown to occur between SC in fish, and they may be involved in the coordination of the synchronous development of GC within the cysts. It is also possible that gap junctions may form an interconnected network between SC and GC within a cyst. Concerning the SC barrier, tight junctions between fish SC apparently form a functional barrier only in cysts containing haploid GC, and different from mammals, meiotic GC in fish are not shielded from the vascular system. In summary, although still not well investigated, cell–cell interactions in the seminiferous epithelium of fish seem to be crucial for GC development, and their disturbance, for example by changing environmental conditions, will probably affect GC survival and fertility.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (Canada)

Fig. 1
Fig. 2

References

  • Abraham M, Rahamin E, Tibika H, Golenser E, Kieselstein M (1980) The blood-testis barrier in Aphamus dlspar (Teleostei). Cell Tissue Res 211:207–214. doi:10.1007/BF00236443

    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 

  • Arenas MI, Fraile B, De Miguel MP, Paniagua R (1995) Cytoskeleton in Sertoli cells of the mosquito fish (Gambusia afiinis holbrooki). Anat Rec 24:225–234. doi:10.1002/ar.1092410209

    Article  Google Scholar 

  • Batias C, Defamie N, Lablack A, Thepot D, Fenichel P, Segretain D et al (1999) Modified expression of testicular gap junction connexin 43 during normal spermatogenic cycle and in altered spermatogenesis. Cell Tissue Res 298:113–121. doi:10.1007/s004419900076

    Article  PubMed  CAS  Google Scholar 

  • Batias C, Siffroi JP, Fénichel P, Pointis G, Segretain D (2000) Connexin43 gene expression and regulation in the rodent seminiferous epithelium. Histochem Cytochem 48(6):793–805

    CAS  Google Scholar 

  • Batlouni SR, Carreño FR, Romagosa E, Borella MI (2005) Cell junctions in the seminiferous epithelium may play an important role in spermatogenesis of the catfish P. fasciatum (Pisces, Siluriformes). J Mol Histol 36(1–2):97–110

    Article  PubMed  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 seminiferous epithelium An approach addressed to aquaculture. Anim Reprod Sci 96(1–2):116–132. doi:10.1016/j.anireprosci.2005.11.012

    Article  PubMed  CAS  Google Scholar 

  • Bergmann M, Schindelmeiser M, Greven H (1984) The blood- testis barrier in vertebrates having different testicular organization. Cell Tissue Res 238:145–150. doi:10.1007/BF00215155

    Article  Google Scholar 

  • Billard R (1983) Spermiogenesis in the rainbow trout (Salmo gairdneri) An ultrastructural study. Cell Tissue Res 233(2):265–284. doi:10.1007/BF00238295

    Article  PubMed  CAS  Google Scholar 

  • Billard R (1984) Ultrastructural changes in the spermatogonia and spermatocytes of Poecilia reticulata during spermatogenesis. Cell Tissue Res 237(2):219–226. doi:10.1007/BF00217139

    Article  PubMed  CAS  Google Scholar 

  • Brehm R, Zeiler M, Rüttinger C, Herde K, Kibschull M, Winterhager E et al (2007) A Sertoli cell-specific knockout of connexins 43 prevents initiation of spermatogenesis. Am J Pathol 171(1):19–31. doi:10.2353/ajpath.2007.061171

    Article  PubMed  CAS  Google Scholar 

  • Brown-Peterson NJ, Grier HJ, Overstreet RM (2002) Annual changes in the seminiferous epithelium determines reproductive classes in male cobia, Rachycentron canadum. J Fish Biol 60:178–202. doi:10.1111/j.1095-8649.2002.tb02397.x

    Article  Google Scholar 

  • Cerdà J, Reidenbach S, Pratzel S, Franke WW (1999) Cadherin–catenin complexes during zebrafish oogenesis: heterotypic junctions between oocytes and follicle cells. Biol Reprod 61:692–704

    Article  PubMed  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 

  • Clérot JC (1971) Intercellular bridges in the testis of Gardonus: syncitial organization and synchrony in the differentiation of germ cells. J Ultrastruc Res 37(5):690–703

    Article  Google Scholar 

  • Defamie N, Berthaut I, Mograbi B, Chevallier D, Dadoune JP, Fénichel P, Segretain D, Pointis G (2003) Impaired gap junction connexin43 in Sertoli cells of patients with secretory azoospermia: a marker of undifferentiated Sertoli cells. Lab Invest 83(3):449–456

    PubMed  CAS  Google Scholar 

  • de Montgolfier B, Dufresne J, Letourneau M, Nagler JJ, Fournier A, Audet C, Cyr DG (2007) The expression of multiple connexins throughout spermatogenesis in the rainbow trout testis suggests a role for complex intercellular communication. Biol Reprod 76(1):2–8

    Article  PubMed  CAS  Google Scholar 

  • de Montgolfier B, Fournier M, Audet C, Marcogliese DJ, Cyr DG (2008) Influence of municipal effluents on the expression of connexins in the brook trout (Salvelinus fontinalis) testis. Aquat Toxicol 20 86(1):38–48

    Article  CAS  Google Scholar 

  • Dym M, Fawcett DW (1970) The blood testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 3(3):308–326

    PubMed  CAS  Google Scholar 

  • Eusebi F, Ziparo E, Fratamico G, Russo MA, Stefanini M (1983) Intercellular communication in rat seminiferous tubules. Dev Biol 100(1):249–255

    Article  PubMed  CAS  Google Scholar 

  • Farquhar MG, Palade GE (1963) Junctional complexes in various epithelia. J Cell Biol 17:375–412

    Article  PubMed  CAS  Google Scholar 

  • Fawcett DW, Leak LV, Heidger PM Jr (1970) Electron microscopic observations on the structural components of the blood-testis barrier. J Reprod Fert 10:105–122

    CAS  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 

  • Fraile B, Sáez FJ, Vicentini CA, de Miguel MP, Paniagua R (1992) The testicular cycle of Gambusia affinis holbrooki (Teleostei Poeciliidae). J Zool Lond 228:115–126

    Article  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, 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 

  • Guttman JA, Vaid KS, Vogl AW (2007) Enrichment and disassembly of ectoplasmic specializations in the rat testis. Method Mol Biol 392:159–170

    Article  CAS  Google Scholar 

  • Herrenknecht K, Ozawa M, Eckerskorn C, Lottspeich F, Lenter M, Kemler R (1991) The uvomorulin-anchorage protein alpha catenin is a vinculin homologue. Proc Natl Acad Sci USA 88(20):9156–9160

    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 

  • Marina P, Annamaria L, Barbara D, Loredana R, Piero A, Francesco A (2002) Fine structure of Leydig and Sertoli cells in the testis of immature and mature spotted ray Torpedo marmorata. Mol Reprod Dev 63(2):192–201

    Article  PubMed  CAS  Google Scholar 

  • McClusky LM (2006) Stage-dependency of apoptosis and the blood-testis barrier in the dogfish shark (Squalus acanthias): cadmium-induced changes as assessed by vital fluorescence techniques. Cell Tissue Res 325(3):541–553

    Article  PubMed  CAS  Google Scholar 

  • McGinley D, Posalaky Z, Provaznik M (1977) Intercellular junctional complexes of the rat seminiferous tubules: a freeze-fracture study. Anat Rec 189(2):211–231

    Article  PubMed  CAS  Google Scholar 

  • McGinley DM, Posalaky Z, Porvaznik M, Russell LD (1979) Gap junctions between Sertoli and germ cells of rat seminiferous tubules. Tissue Cell 11(4):741–754

    Article  PubMed  CAS  Google Scholar 

  • Miller MG, Mulholland DJ, Vogl AW (1999) Rat testis motor proteins associated with spermatid translocation (dynein) and spermatid flagella (kinesin-II). Biol Reprod 60(4):1047–1056

    Article  PubMed  CAS  Google Scholar 

  • Neaves WB (1973) Permeability of Sertoli cell tight junctions to lanthanum after ligation of ductus deferens and ductuli efferentes. J Cell Biol 59(3):559–572

    Article  PubMed  CAS  Google Scholar 

  • Ozawa M, Kemler R (1992) Molecular organization of the uvomorulin-catenin complex. J Cell Biol 116(4):989–996

    Article  PubMed  CAS  Google Scholar 

  • Pelletier MR (2004) The tight junction in the testis. Recent Res Dev Endocrinol 4:29–51

    Google Scholar 

  • Pfeiffer DC, Vogl AW (1994) Actin-related intercellular junctions in the germinal compartment of the testis in Poecilia reticulata (Teleostei, Poeciliidae). Zoomorphology 114:177–184

    Article  Google Scholar 

  • Pfeiffer DC, Vogl AW (2002) Actin-related intercellular adhesion junctions in the germinal compartment of the testis in the hagfish (Eptatetrus stouti) and lamprey (Lampetra tridentatus). Tissue Cell 34(6):450–459

    Article  PubMed  CAS  Google Scholar 

  • Points G, Fiorini C, Norah D, Segretain D (2005) Gap junctional communication in the male reproductive system. Biochem Biophys Acta 1719:102–116

    Article  CAS  Google Scholar 

  • Prisco M, Liguoro A, Ricchiari L, Angelini F, Andreuccetti P (2007) Cadherin in developing and maturing cysts of Torpedo marmorata testis. Mol Reprod Dev 74(2):242–248

    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, pp 612–657

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ren HP, Russell LD (1992) Quantitation of Sertoli cell–germ cell desmosome gap junctions in relation to meiotic divisions in the male rat. Tissue Cell 24(4):565–573

    Article  PubMed  CAS  Google Scholar 

  • Roscoe WA, Barr KJ, Mhawi AA, Pomerantz DK, Kidder GM (2001) Failure of spermatogenesis in mice lacking connexin 43. Biol Reprod 65(3):829–838

    Article  PubMed  CAS  Google Scholar 

  • Russell LD (1977a) Observations on rat Sertoli ectoplasmic (“junctional”) specializations in their association with germ cells of the rat testis. Tissue Cell 9:4754–4798

    Google Scholar 

  • Russell LD (1977b) Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 148(3):313–328

    Article  PubMed  CAS  Google Scholar 

  • Russell LD (1977c) Desmosome-like junctions between Sertoli and germ cells in the rat testis. Am J Anat 148(3):301–312

    Article  PubMed  CAS  Google Scholar 

  • Russell LD (1993) Morphological and functional evidence for Sertoli-germ cell relationship. In: Russell LD, Griswold MD (eds) The Sertoli cell. Cache River Press, Clearwater

    Google Scholar 

  • Russell LD, Peterson RN (1985) Sertoli cell junctions: morphological and functional correlates. Int Rev Cytol 94:177–211

    Article  PubMed  CAS  Google Scholar 

  • Setchell BP (2007) Blood-testis barrier, junctional and transport proteins and spermatogenesis. In: Cheng CY (ed) Molecular mechanisms in spermatogenesis. Landes Bioscience, Austin

  • Setchell BP, Voglmayr JK, Waites GMH (1969) A blood-testis barrier restricting passage from blood into rete testis fluid but not into lymph. J Physiol 200:73–85

    PubMed  CAS  Google Scholar 

  • Silva M, Godinho HP (1989) Blood-testis barrier in Oreochromis niloticus (Fish, teleost). Rev Bras Ciên Morfol 6:9–13

    Google Scholar 

  • Sprando RL, Russell LD (1987) Germ cell-somatic cell relationships: A comparative study of intercellular junctions during spermatogenesis in selected non-mammalian vertebrates. Scan Microsc 1:1249–1255

    CAS  Google Scholar 

  • Stanley HP, Lambert CC (1985) The role of a Sertoli cell actin-myosin system in sperm bundle formation in the ratfish Hydrolagus colliei (Chondrichthyes, Holocephali). J Morphol 186(2):223–236

    Article  PubMed  CAS  Google Scholar 

  • Vogl AW, Pfeiffer DC, Redenbach DM, Grove BD (1993) Sertoli cell cytoskeleton. In: Russell LD, Griswold MD (eds) The Sertoli cell. Cache River Press, Clearwater

    Google Scholar 

  • Vogl AW, Pfeiffer DC, Mulholland D, Kimel G, Guttman J (2000) Unique and multifunctional adhesion junctions in the testis: ectoplasmic specializations. Arch Histol Cytol 63:1–15

    Article  PubMed  CAS  Google Scholar 

  • Winterhager E, Pielensticker N, Freyer J, Ghanem A, Schrickel JW, Kim JS, Behr R, Grümmer R, Maass K, Urschel S, Lewalter T, Tiemann K, Simoni M, Willecke K (2007) Replacement of connexin43 by connexin26 in transgenic mice leads to dysfunctional reproductive organs and slowed ventricular conduction in the heart. BMC Dev Biol 4:7–26

    Google Scholar 

  • Ziparo E, Eusebi F, Fratamico G, Russo MA, Stefanini M (1983) Intercellular coupling during maturation of the rat seminiferous epithelium. Cell Biol Int Rep 7(3):190

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Author notes

  1. S. R. Batlouni

    Present address: Aquaculture Center, São Paulo State University (CAUNESP), Jaboticabal, SP, 14884-900, Brazil

Authors and Affiliations

  1. Laboratory of Cellular Biology, Department of Morphology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, MG, 31270-901, Brazil

    S. R. Batlouni, R. H. Nóbrega & L. R. França

Authors
  1. S. R. Batlouni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. H. Nóbrega
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. R. França
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. R. França.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Batlouni, S.R., Nóbrega, R.H. & França, L.R. Cell junctions in fish seminiferous epithelium. Fish Physiol Biochem 35, 207–217 (2009). https://doi.org/10.1007/s10695-008-9253-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-008-9253-y

Keywords

  • Seminiferous epithelium
  • Cell junctions
  • Adhesive junctions
  • Gap junctions
  • Sertoli cell barrier
  • Blood testis barrier

Search

Navigation