Skip to main content
SpringerLink
Log in

Characterization of gonadotropic cells during continuous and seasonal spermatogenesis of two freshwater fish species: a histochemical and immunohistochemical study

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

This work describes gonadotropic (GtH) cells and their morphological and immunohistochemical changes during the spermatogenic cycle of Serrasalmus maculatus (continuous spermatogenesis) and Pimelodus maculatus (seasonal spermatogenesis). GtH cells, widely distributed in the proximal pars distalis of the adenohypophysis, were characterized as round-shaped cells with eccentric nucleus, and cytoplasm with basophilic secretory granules and a variable number of vacuoles for both species. Immunohistochemistry against β-follicle-stimulating hormone (Fsh) and β-luteinizing hormone (Lh) in adjacent sections showed two separated GtH-producing cell populations, and a third population where both GtHs are expressed in the same cell for both species. In the seasonal spermatogenesis of P. maculatus, GtH cells seemed to be more abundant during developing and spawning capable phases. In contrast, no cyclic changes were detected in the continuous spermatogenesis of S. maculatus, except for the strong immunoreaction for Fsh and Lh in males with intense spermiogenesis. We conclude that changes reported here might reflect the type of spermatogenic cycle (seasonal or continuous) which are under different regulatory mechanisms (environmental and internal cues) controlling the reproduction in these species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agulleiro B, Garcia-Hernández MP, García-Ayala A (2006) Teleost adenohypophysis: morphofunctional and development aspects. In: Reinecke M, Zaccone G, Kapoor BG (eds) Fish endocrinology. Science Publishers, Enfield, pp 289–323

    Google Scholar 

  • Aizen J, Kasuto H, Golan M, Zakay H, Levavi-Sivan B (2007) Tilapia follicle-stimulating hormone (FSH): immunochemistry, stimulation by gonadotropin-releasing hormone, and effect of biologically active recombinant FSH on steroid secretion. Biol Reprod 76:692–700

    Article  CAS  PubMed  Google Scholar 

  • Arantes FP, Borçato FL, Sato Y, Rizzo E, Bazzoli N (2013) Reproduction and embryogenesis of the mandi-amarelo catfish, Pimelodus maculatus (Pisces, Pimelodidae), in captivity. Anat Histol Embryol 42:30–39

    Article  CAS  PubMed  Google Scholar 

  • Borella MI, Gazola R, Val-Sella MV, Fava-De-Moraes F (1997) Histochemical and immunohistochemical study of the pituitary gland of the South-American teleost pacu fish Piaractus mesopotamicus (Cypriniformes, Characidae). Braz J Morphol Sci 14:219–225

    Google Scholar 

  • Borella MI, Venturieri R, Mancera JM (2009) Immunocytochemical identification of adenohypophyseal cells in the pirarucu (Arapaima gigas), an Amazonian basal teleost. Fish Physiol Biochem 35:3–16

    Article  CAS  PubMed  Google Scholar 

  • Brown-Peterson NJ, Wyanski DM, Saborido-Rey F, Macewicz BJ, Lowerre-Barbieri SK (2011) A standardized terminology for describing reproductive development in fishes. Mar Coast Fish Dynam Manag Ecosys Sci 2011:52–70

    Article  Google Scholar 

  • Calman B, Lin YW, Wallace RA (2001) Preparation and use of specific antibodies to the β-I and β-II subunits of Gonadotropic hormone from Fundulus heteroclitus pituitary. Gen Comp Endocrinol 123:203–209

    Article  CAS  PubMed  Google Scholar 

  • Cambré ML, Verdonck W, Ollevier F, Vandesande F, Batten TF, Kühn ER (1986) Immunocytochemical identification and localization of the different cell types in the pituitary of the seabass (Dicentrarchus labrax). Gen Comp Endocrinol 61:368–375

    Article  PubMed  Google Scholar 

  • Chauvigné F, Zapater C, Gasol JM, Cerdà J (2014) Germ-line activation of the luteinizing hormone receptor directly drives spermiogenesis in a nonmammalian vertebrate. Proc Natl Acad Sci USA 111:1427–1432

    Article  PubMed  PubMed Central  Google Scholar 

  • Cinquetti R, Dramis L (2006) Identification and localization of hormone-producing cells in the pituitary of male Padogobius martensi (Pisces, Gobiidae): a histochemical and immunocytochemical study. J Fish Biol 68:235–250

    Article  CAS  Google Scholar 

  • García-Ayala A, Villaplana M, Garcia-Hernández MP, Chaves Pozo E, Agulleiro B (2003) FSH-, LH-, and TSH-expressing cells during development of Sparus aurata L. (Teleostei). An immunocytochemical study. Gen Comp Endocrinol 134:72–79

    Article  PubMed  Google Scholar 

  • Garcia-Hernández MP, García-Ayala A, Elbal MT, Agulleiro B (1996) The adenohypophysis of Mediterranean yellowtail, Seriola dumerilii (Risso, 1810): an immunocytochemical study. Tissue Cell 28:577–585

    Article  PubMed  Google Scholar 

  • Garcia-Hernández MP, García-Ayala A, Zandbergen MA, Agulleiro B (2002) Investigation into the duality of gonadotropic cells of Mediterranean yellowtail (Seriola dumerilii, Risso 1810): immunocytochemical and ultrastructural studies. Gen Comp Endocrinol 128:25–35

    Article  Google Scholar 

  • Golan M, Biran J, Levavi-Sivan B (2014) A novel model for development, organization, and function of gonadotropes in fish pituitary. Front Endocrinol 5:182

    Article  Google Scholar 

  • Grandi G, Marchetti MG, Lanzoni M, Chicca M (2014) Immunocytochemical and ultrastructural identification of adenohypophyseal cells in Ctenopharyngodon idella (Cypriniformes: Cyprinidae) during gonadal differentiation. Fish Physiol Biochem 40:1115–1139

    CAS  PubMed  Google Scholar 

  • Grier H, Lo Nostro F (2000) The germinal epithelium in fish gonads: the unifying concept. In: Norberg B, Kjesbu OS, Taranger GL, Andersson E, Stefansson SO (eds) Proceedings of the 6th international symposium on the reproductive physiology of fish. University of Bergen, Norway, pp 233–236

    Google Scholar 

  • Honji RM, Nobrega RH, Pandolfi M, Shimizu A, Borella MI, Moreira RG (2013) Immunohistochemical study of pituitary cells in wild and captive Salminus hilarii (Characiformes: Characidae) females during the annual reproductive cycle. Springerplus 2:460

    Article  PubMed  PubMed Central  Google Scholar 

  • Horie Y, Shimizu A, Adachi S, Kobayashi T (2014) Expression and localization of gonadotropic hormone subunits (Gpa, βFsh, and βLh) in the pituitary during gonadal differentiation in medaka. Gen Comp Endocrinol 204:173–180

    Article  CAS  PubMed  Google Scholar 

  • Jesus LWO, Chehade C, Costa FG, Borella MI (2014) Pituitary gland morphogenesis and ontogeny of adenohypophyseal cells of Salminus brasiliensis (Teleostei, Characiformes). Fish Physiol Biochem 40:897–909

    PubMed  Google Scholar 

  • Kagawa H, Kawazoe I, Tanaka H, Okuzawa K (1998) Immunocytochemical identification of two distinct Gonadotropic cells (GTI and GTHII) in the pituitary of Bluefin Tuna, Thunnus thynnus. Gen Comp Endocrinol 110:11–18

    Article  CAS  PubMed  Google Scholar 

  • Kaneko T, Aida K, Hanyu I (1986) Ultrastructural changes in the pituitary gonadotropes during the annual reproductive cycle of the female chichibugoby Tridentiger obscurus. Cell Tissue Res 246:137–144

    Article  Google Scholar 

  • Kasper RS, Shved N, Takahashi A, Reinecke M, Eppler E (2006) A systematic immunohistochemical survey of the distribution patterns of GH, prolactin, somatolactin, β-TSH, β-FSH, β-LH, ACTH, and alpha-MSH in the adenohypophysis of Oreochromis niloticus, the Nile tilapia. Cell Tissue Res 325:303–313

    Article  CAS  PubMed  Google Scholar 

  • Lamas IR, Godinho AL (1996) Reproduction in the piranha Serrasalmus spilopleura, a neotropical fish with an usual pattern of sexual maturity. Environ Biol Fishes 45:161–168

    Article  Google Scholar 

  • Levavi-Sivan B, Bogerd J, Mananos EL, Gomez A, Lareyre JJ (2010) Perspectives on fish gonadotropins and their receptors. Gen Comp Endocrinol 165:412–437

    Article  CAS  PubMed  Google Scholar 

  • Li CJ, Zhou L, Wang Y, Hong YH, Gui JF (2005) Molecular and expression characterization of three gonadotropin subunits common alpha, FSHβ and LHβ in groupers. Mol Cell Endocrinol 233:33–46

    Article  CAS  PubMed  Google Scholar 

  • Magliulo-Cepriano L, Schreibman MP, Blum V (1994) Distribution of variant forms of immunoreactive gonadotropin-releasing hormone and β-gonadotropins I and II in the platyfish, Xiphophorus maculatus, from birth to sexual maturity. Gen Comp Endocrinol 94:135–150

    Article  CAS  PubMed  Google Scholar 

  • Miranda LA, Strussmann CA, Somoza GM (2001) Immunocytochemical identification of GtH1 and GtH2 cells during the temperature-sensitive period for sex determination in pejerrey, Odontesthes bonariensis. Gen Comp Endocrinol 124:45–52

    Article  CAS  PubMed  Google Scholar 

  • Mukai T, Oota Y (1995) Histological changes in the pituitary, thyroid gland and gonads of the fourspine sculpin (Cottus kazika) during downstream migration. Zool Sci 12:91–97

    Article  CAS  PubMed  Google Scholar 

  • Naito N, Suzuki K, Nozaki M, Swanson P, Kawauchi H, Nakai Y (1993) Ultrastructural characteristics of two distinct gonadotropes (GTH I- and GTH II-cells) in the pituitary of rainbow trout Oncorhynchus mykiss. Fish Physiol Biochem 11:241–246

    Article  CAS  PubMed  Google Scholar 

  • 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 329:339–349

    Article  PubMed  Google Scholar 

  • Nóbrega RH, Morais RDVS, Crespo D, de Waal PP, França LR, Schulz RW, Bogerd J (2015) Fsh stimulates spermatogonial proliferation and differentiation in zebrafish via Igf3. Endocrinology 156:3804–3817

    Article  PubMed  Google Scholar 

  • Nozaki M, Naito N, Swanson P, Dickhoff WW, Nakai Y, Suzuki K, Kawauchi H (1990) Salmonid pituitary gonadotrophs. II. Ontogeny of GTH I and GTH II cells in the rainbow trout (Salmo gairdneri irideus). Gen Comp Endocrinol 77:358–367

    Article  CAS  PubMed  Google Scholar 

  • Pandolfi M, Paz DA, Maggese C, Meijide FJ, Vissio PG (2001) Immunocytochemical localization of different cell types in the adenohypophysis of the cichlid fish Cichlasoma dimerus (Heckel, 1840). Biocell 25:35–42

    CAS  PubMed  Google Scholar 

  • Pandolfi M, Lo Nostro FL, Shimizu A, Pozzi AG, Meijide FJ, Vazquez GR, Maggese MC (2006) Identification of immunoreactive FSH and LH cells in the cichlid fish Cichlasoma dimerus during the ontogeny and sexual differentiation. Anat Embryol 211:355–365

    Article  PubMed  Google Scholar 

  • Pierce JG, Parsons TF (1981) Glycoprotein hormones: structure and function. Annu Rev Biochem 50:465–495

    Article  CAS  PubMed  Google Scholar 

  • Quintero-Hunter I, Grier H, Muscato M (1991) Enhancement of histological detail using metanil yellow as counterstain in periodic acid Schiff’s hematoxylin staining of glycol methacrylate tissue sections. Biotech Histochem 66:169–172

    Article  CAS  PubMed  Google Scholar 

  • Santana JC, Quagio-Grassiotto I (2014) Extracellular matrix remodeling of the testes through the male reproductive cycle in Teleostei fish. Fish Physiol Biochem 40:1863–1875

    Article  CAS  PubMed  Google Scholar 

  • Schulz RW, de Franca LR, Lareyre JJ, Le Gac F, Chiarini-Garcia H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411

    Article  CAS  PubMed  Google Scholar 

  • Shimizu A, Kagawa H, Tanaka H (2003a) Immunocytochemical identification of gonadotrophs (FSH cells and LH cells) in various perciform fishes using antisera raised against synthetic peptides. Fish Physiol Biochem 28:109–110

    Article  CAS  Google Scholar 

  • Shimizu A, Sakai T, Nashida K, Honda H (2003b) Universal antisera for immunocytochemical identification of two different gonadotrophs in acanthopterygian fishes. Fish Physiol Biochem 29:275–287

    Article  CAS  Google Scholar 

  • Shimizu A, Tanaka H, Kagawa H (2003c) Immunocytochemical applications of specific antisera raised against synthetic fragment peptides of mummichog GtH subunits: examining seasonal variations of gonadotrophs (FSH cells and LH cells) in the mummichog and applications to other acanthopterygian fishes. Gen Comp Endocrinol 132:35–45

    Article  CAS  PubMed  Google Scholar 

  • Val-Sella MV, Sesso A (1980) Morphometric evaluation of the number of gonadotrophic cells of the teleost Rhamdia hilarii in the maturation, mature and spent stages of the gonadal cycle. Acta Zool 61:133–139

    Article  Google Scholar 

  • Vongvatcharanon U, Kirirat P, Suwanjarat J, Boonyoung P (2005) Alteration of gonadotrophs in the pituitary gland during the annual reproductive cycle of the adult female sand goby (Oxyeleotris marmoratus). J Sci Technol 27:437–445

    Google Scholar 

  • Weltzien FA, Andersson E, Andersen O, Shalchian-Tabrizi K, Norberg B (2004) The brain–pituitary–gonad axis in male teleosts, with special emphasis on flatfish (Pleuronectiformes). Comp Biochem Physiol A: Mol Integr Physiol 137:447–477

    Article  Google Scholar 

  • Wildner DD, Grier H, Quagio-Grassiotto I (2013) Female germ cell renewal during the annual reproductive cycle in Ostariophysians fish. Theriogenology 79:709–724

    Article  PubMed  Google Scholar 

  • Wu Y, He Z, Zhang L, Jiang H, Zhang W (2012) Ontogeny of immunoreactive Lh and Fsh cells in relation to early ovarian differentiation and development in protogynous hermaphroditic ricefield eel Monopterus albus. Biol Reprod 86(93):1–9

    CAS  Google Scholar 

  • Young G, Ball JN (1982) Ultrastructural changes in the adenohypophysis during the ovarian cycle of the viviparous teleost Poecilia latipinna. I. The gonadotrophic cells. Gen Comp Endocrinol 48:39–59

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr. H. Kawauchi (School of Fisheries Sciences, Kitasato University, Iwate, Japan) for the generous gift of antibodies, Mr. Cruz A. M. Rigonati (ICB/USP) and Antônio Vicente Salvador (IBB/UNESP) for technical support, Mr. Arno Juliano Butzge for technical help with the Figures, Dra. Irani Quagio-Grassioto (IBB/UNESP) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, 2003/11078-9).

Author information

Author notes

    Authors and Affiliations

    1. Department of Morphology, Institute of Biosciences, São Paulo State University, UNESP, Botucatu, Brazil

      Rafael Henrique Nóbrega

    2. Department of Cell and Developmental Biology, Institute of Biomedical Sciences, University of São Paulo, USP, São Paulo, Brazil

      Lázaro Wender Oliveira de Jesus & Maria Inês Borella

    3. Department of Physiology, Institute of Biosciences, University of São Paulo, USP, São Paulo, Brazil

      Renato Massaaki Honji

    4. Departamento de Biologia Celular e do Desenvolvimento, Instituto de Ciências Biomédicas, Universidade de São Paulo, Av. Professor Lineu Prestes 1524, São Paulo, SP, 05508-000, Brazil

      Maria Inês Borella

    Authors
    1. Rafael Henrique Nóbrega
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Lázaro Wender Oliveira de Jesus
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Renato Massaaki Honji
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Maria Inês Borella
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Maria Inês Borella.

    Ethics declarations

    Conflict of interest

    The author declares no conflict of interest.

    Additional information

    Rafael Henrique Nóbrega and Lázaro Wender Oliveira de Jesus have equally contributed to this paper.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Nóbrega, R.H., de Jesus, L.W.O., Honji, R.M. et al. Characterization of gonadotropic cells during continuous and seasonal spermatogenesis of two freshwater fish species: a histochemical and immunohistochemical study. Fish Physiol Biochem 43, 51–63 (2017). https://doi.org/10.1007/s10695-016-0267-6

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10695-016-0267-6

    Keywords

    Search

    Navigation