Skip to main content
Log in

A systematic immunohistochemical survey of the distribution patterns of GH, prolactin, somatolactin, β–TSH, β–FSH, β–LH, ACTH, and α–MSH in the adenohypophysis of Oreochromis niloticus, the Nile tilapia

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Fish pituitary plays a central role in the control of growth, development, reproduction and adaptation to the environment. Several types of hormone–secreting adenohypophyseal cells have been characterised and localised in diverse teleost species. The results suggest a similar distribution pattern among the species investigated. However, most studies deal with a single hormone or hormone family. Thus, we studied adjacent sections of the pituitary of Oreochromis niloticus, the tilapia, by conventional staining and immunohistochemistry with specific antisera directed against growth hormone (GH), prolactin (PRL), somatolactin (SL), thyrotropin (β–TSH), follicle–stimulating hormone (β–FSH), luteinising hormone (β–LH), adrenocorticotropic hormone (ACTH) and melanocyte–stimulating hormone (α–MSH). The pituitary was characterised by a close interdigitating neighbourhood of neurohypophysis (PN) and adenohypophysis. PRL–immunoreactive and ACTH–immunoreactive cells were detected in the rostral pars distalis. GH–immunoreactive cells were present in the proximal pars distalis (PPD). A small region of the PPD contained β–TSH–immunoreactive cells, and β–LH–immunoreactive cells covered approximately the remaining parts. Centrally, β–FSH–immunoreactive cells were detected in the vicinity of the GH–containing cells. Some of these cells also displayed β–LH immunoreactivity. The pars intermedia was characterised by branches of the PN surrounded by SL–containing and α–MSH–immunoreactive cells.The ACTH and α–MSH antisera were observed to cross-react with the respective antigens. This cross–reactivity was abolished by pre–absorption. We present a complete map of the distinct localisation sites for the classical pituitary hormones, thereby providing a solid basis for future research on teleost pituitary.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agulleiro B, García-Hernández MP, García Ayala A (2006) Teleost adenohypophysis: morphofunctional and developmental aspects. In: Reinecke M, Zaccone G, Kapoor BG (eds) Fish endocrinology. Science Publishers, New Hampshire, pp 290–324

    Google Scholar 

  • Amemiya Y, Sogabe Y, Nozaki M, Takahashi A, Kawauchi H (1999) Somatolactin in the white sturgeon and African lungfish and its evolutionary significance. Gen Comp Endocrinol 114:181–190

    Article  PubMed  CAS  Google Scholar 

  • Amano M, Takahashi A, Yamanome T, Oka Y, Amiya N, Kawauchi H, Yamamori K (2005) Immunocytochemical localization and ontogenic development of α–melanocyte–stimulating hormone (α–MSH) in the brain of a pleuronectiform fish, barfin flounder. Cell Tissue Res 320:127–134

    Article  PubMed  CAS  Google Scholar 

  • Baroiller JF, Guiguen Y (2001) Endocrine and environmental aspects of sex differentiation in gonochoristic fish. EXS 91:177–201

    PubMed  CAS  Google Scholar 

  • Caelers A, Maclean N, Hwang G, Eppler E, Reinecke M (2005) Expression of endogenous and exogenous growth hormone (GH) in a GH–transgenic tilapia (Oreochromis niloticus). Transgen Res 14:95–104

    Article  CAS  Google Scholar 

  • Dores RM, Hoffman NE, Chilcutt-Ruth T, Lancha A, Brown C, Marra L, Youson J (1996) A comparative analysis of somatolactin-related immunoreactivity in the pituitaries of four neopterygian fishes and one chondrostean fish: an immunohistochemical study. Gen Comp Endocrinol 102:79–87

    Article  PubMed  CAS  Google Scholar 

  • Dores RM, Lecaude S (2005) Trends in the evolution of the proopiomelanocortin gene. Gen Comp Endocrinol 142:81–93

    Article  PubMed  CAS  Google Scholar 

  • Elizur A, Zmora N, Meiri I, Kasuto H, Rosenfeld H, Chaouat S, Kobayashi M, Zohar Y, Yaron Z (2000) Gonadotropins—from genes to recombinant proteins. In: Norberg B, Kjesbu OS, Taranger GI, Andersson E, Stefansson SO (eds) Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish 1999. University of Bergen, Bergen, Norway, pp 462–465

  • García Ayala A, Villaplana M, García-Hernández MP, Chavez 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  CAS  Google Scholar 

  • García-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 

  • Grandi G, Chicca M (2004) Early development of the pituitary gland in Acipenser naccarii (Chondrostei, Acipenseriformes): an immunocytochemical study. Anat Embryol 208:311–321

    Article  PubMed  CAS  Google Scholar 

  • Grandi G, Colombo G, Chicca M (2003) Immunocytochemical studies on the pituitary gland of Anguilla anguilla L., in relation to early growth stages and diet-induced sex differentiation. Gen Comp Endocrinol 131:66–76

    Article  PubMed  CAS  Google Scholar 

  • Holmes RL, Ball JN (1974) The pituitary gland—a comparative account. Cambridge University Press, London, New York

    Google Scholar 

  • Huang L, Specker JL (1994) Growth hormone– and prolactin–producing cells in the pituitary gland of striped bass (Morone saxatilis): immunocytochemical characterization at different life stages. Gen Comp Endocrinol 94:225–236

    Article  PubMed  CAS  Google Scholar 

  • Inoue K, Iwatani H, Takei Y (2003) Growth hormone and insulin–like growth factor I of a euryhaline fish Cottus kazika: cDNA cloning and expression after seawater acclimation. Gen Comp Endocrinol 131:77–84

    Article  PubMed  CAS  Google Scholar 

  • Joss JMP, Dores RM, Crim JW, Beshaw M (1990) Immunocytochemical location of pituitary cells containing ACTH, α–MSH, and β–endorphin in Acipenser transmontanus, Lepisosteus spatula, and Amia calva. Gen Comp Endocrinol 78:459–468

    Article  PubMed  CAS  Google Scholar 

  • Joy KP, Sathyanesan AG (1980) Pituitary cytology of the teleost fish Tilapia mossambica (Peters). Z Mikrosk Anat Forsch Leipzig 94:337–344

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kawauchi H, Moriyama S, Yasuda A, Yamaguchi K, Shirahata K, Kubota J, Hirano T (1986) Isolation and characterization of chum salmon growth hormone. Arch Biochem Biophys 244:542–552

    Article  PubMed  CAS  Google Scholar 

  • Kawauchi H, Suzuki K, Itoh H, Swanson P, Naito N, Nagahama Y, Nozaki M (1989) The duality of teleost gonadotropins. Fish Physiol Biochem 7:29–38

    Article  CAS  Google Scholar 

  • Laiz-Carrión R, Segura-Noguera MM, Martín del Río MP, Mancera JM (2003) Ontogeny of adenohypophyseal cells in the pituitary of the American shad (Alosa sapidissima). Gen Comp Endocrinol 132:454–464

    Article  PubMed  CAS  Google Scholar 

  • Leatherland JF, Ball JN, Hyder M (1974) Structure and fine structure of the hypophyseal pars distalis in endigenous African species of the genus tilapia. Cell Tissue Res 149:245–266

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Danielson P, Sollars C, Alrubaian J, Balm P, Dores RM (1999) Cloning of a neoteleost (Oreochromis mossambicus) pro–opiomelanocortin (POMC) cDNA reveals a deletion of the γ–melanotropin region and most of the joining peptide region: implications for POMC processing. Peptides 20:1391–1399

    Article  PubMed  CAS  Google Scholar 

  • Li C-J, Zhou L, Wang Y, Hong Y-H, Gui J-F (2005) Molecular and expression characterization of three gonadotropin subunits common α, FSHβ and LHβ in groupers. Mol Cell Endocrinol 233:33–46

    Article  PubMed  CAS  Google Scholar 

  • Matsuda K, Nagano Y, Uchiyama M, Takahashi A, Kawauchi H (2005) Immunohistochemical observation of pituitary adenylate cyclase–activating polypeptide (PACAP) and adenohypophysial hormones in the pituitary of a teleost, Uranoscopus japonicus. Zool Sci 22:71–76

    Article  PubMed  CAS  Google Scholar 

  • Melamed P, Rosenfeld H, Elizur A, Yaron Z (1998) Endocrine regulation of gonadotropin and growth hormone gene transcription in fish. Comp Biochem Physiol C 119:325–338

    Article  CAS  PubMed  Google Scholar 

  • Mori T, Devlin RH (1999) Transgenic and host growth hormone expression in pituitary and nonpituitary tissues of normal and growth hormone transgenic salmon. Mol Cell Endocrinol 149:129–139

    Article  PubMed  CAS  Google Scholar 

  • Mousa MA, Mousa SA (1999a) Immunocytochemical and histological studies on the hypophyseal–gonadal system in the freshwater Nile tilapia, Oreochromis niloticus (L.), during sexual maturation and spawning in different habitats. J Exp Zool 284:343–354

    Article  PubMed  Google Scholar 

  • Mousa MA, Mousa SA (1999b) Immunocytochemical study on the localization and distribution of the somatolactin cells in the pituitary gland and the brain of Oreochromis niloticus (Teleostei, Cichlidae). Gen Comp Endocrinol 113:197–211

    Article  PubMed  CAS  Google Scholar 

  • Nagahama Y, Olivereau M, Farmer SW, Nishioka RS, Bern HA (1981) Immunocytochemical identification of the prolactin– and growth hormone–secreting cells in the teleost pituitary with antisera to tilapia prolactin and growth hormone. Gen Comp Endocrinol 44:389–395

    Article  PubMed  CAS  Google Scholar 

  • Naito N, Takahashi A, Nakai Y, Kawauchi H, Hirano T (1983) Immunocytochemical identification of the prolactin–secreting cells in the teleost pituitary with an antiserum to chum salmon prolactin. Gen Comp Endocrinol 50:282–291

    Article  PubMed  CAS  Google Scholar 

  • Naito N, de Jesus EG, Nakai Y, Hirano T (1993) Ontogeny of pituitary cell–types and the hypothalamo–hypophysial relationship during early development of chum salmon, Oncorhynchus keta. Cell Tissue Res 272:429–437

    Article  Google Scholar 

  • Nishioka RS, de Jesus EGT, Hyodo S (1993) Localization of mRNAs for a pair of prolactins and growth hormone in the tilapia pituitary using in situ hybridization with oligonucleotide probes. Gen Comp Endocrinol 89:72–81

    Article  PubMed  CAS  Google Scholar 

  • Nozaki M, Naito N, Swanson P, Miyata K, Nakai Y, Oota Y, Suzuki K, Kawauchi H (1990) Salmonid pituitary gonadotrophs. I. Distinct cellular distributions of two gonadotropins, GTH I and GTH II. Gen Comp Endocrinol 77:348–357

    Article  PubMed  CAS  Google Scholar 

  • Nozaki M, Ominato K, Takahashi A, Kawauchi H, Sower SA (2001) Adenohypophysial cell types in the lamprey pituitary: current state of the art. Comp Biochem Physiol B 129:303–309

    Article  PubMed  CAS  Google Scholar 

  • Olivereau M, Rand-Weaver M (1994) Immunocytochemical study of the somatolactin cells in the pituitary of Pacific salmon, Oncorhynchus nerka, and O. keta at some stages of the reproductive cycle. Gen Comp Endocrinol 93:28–35

    Article  PubMed  CAS  Google Scholar 

  • Ominato K, Nozaki M (2002) Distribution of growth hormone–like cells in the pituitary of adult sea lampreys, Petromyzon marinus. Zool Sci 19:1055–1059

    Article  PubMed  Google Scholar 

  • Ono M, Takayama Y, Rand-Weaver M, Sakata S, Yasunaga T, Noso T, Kawauchi H (1990) cDNA cloning of somatolactin, a pituitary protein related to growth hormone and prolactin. Proc Natl Acad Sci USA 87:4330–4334

    Article  PubMed  CAS  Google Scholar 

  • Parhar IS, Nagahama Y, Grau EG, Ross RM (1998) Immunocytochemical and ultrastructural identification of pituitary cell types in the protogynous Thalassoma duperrey during adult sexual ontogeny. Zool Sci 15:263–276

    Article  Google Scholar 

  • Parhar IS, Soga T, Sakuma Y, Millar RP (2002) Spatio–temporal expression of gonadotropin–releasing hormone receptor subtypes in gonadotropes, somatotropes and lactotropes in the cichlid fish. J Neuroendocrinol 14:657–665

    Article  PubMed  CAS  Google Scholar 

  • Parhar IS, Soga T, Ogawa S, Sakuma Y (2003) FSH and LH–β subunits in the preoptic nucleus: ontogenic expression in teleost. Gen Comp Endocrinol 132:369–378

    Article  PubMed  CAS  Google Scholar 

  • Power DM (1992) Immunocytochemical identification of growth hormone, prolactin, and gonadotropin cells in the pituitary of male plaice (Pleuronectes platessa) during gonadal maturation. Gen Comp Endocrinol 85:358–366

    Article  PubMed  CAS  Google Scholar 

  • Quérat B, Moumni M, Jutisz M, Fontaine YA, Counis R (1990) Molecular cloning and sequence analysis of the cDNA for the putative beta subunit of the type–II gonadotrophin from the European eel. J Mol Endocrinol 4:257–264

    Article  PubMed  Google Scholar 

  • Rand-Weaver M, Baker JB, Kawauchi H (1991) Cellular localization of somatolactin in the pars intermedia of some teleost fishes. Cell Tissue Res 263:207–215

    Article  CAS  Google Scholar 

  • Reinecke M, Collet C (1998) The phylogeny of the insulin–like growth factors. Int Rev Cytol 183:1–94

    Article  PubMed  CAS  Google Scholar 

  • Reinecke M, Björnsson BT, Dickhoff WW, McCormick SD, Navarro I, Power DM, Gutiérrez J (2005) Growth hormone and insulin–like growth factors in fish: where we are and where to go. Gen Comp Endocrinol 142:20–24

    Article  PubMed  CAS  Google Scholar 

  • Rosenfeld H, Levavi-Sivan B, Gur G, Melamed P, Meiri I, Yaron Z, Elizur A (2001) Characterization of tilapia FSHbeta gene and analysis of its 5’ flanking region. Comp Biochem Physiol B 129:389–398

    Article  PubMed  CAS  Google Scholar 

  • Saga T, Oota Y, Nozaki M, Swanson P (1993) Salmonid pituitary gonadotrophs. III. Chronological appearance of GTH I and other adenohypophysial hormones in the pituitary of the developing rainbow trout (Oncorhynchus mykiss irideus). Gen Comp Endocrinol 92:233–241

    Article  PubMed  CAS  Google Scholar 

  • Sánchez Cala F, Portillo A, Martín del Río MP, Mancera JM (2003) Immunocytochemical characterization of adenohypophyseal cells in the greater weever fish (Trachinus draco). Tissue Cell 35:169–178

    Article  PubMed  CAS  Google Scholar 

  • Santos EM, Rand-Weaver M, Tyler CR (2001) Follicle–stimulating hormone and its alpha and beta subunits in rainbow trout (Oncorhynchus mykiss): purification, characterization, development of specific radioimmunoassays, and their seasonal plasma and pituitary concentrations in females. Biol Reprod 65:288–294

    Article  PubMed  CAS  Google Scholar 

  • Schally AV, Chang RC, Huang WY, Coy DH, Kastin AJ, Redding TW (1980) Isolation, structure, biological characterization, and synthesis of beta–[Tyr9]melanotropin–(9–18) decapeptide from pig hypothalami. Proc Natl Acad Sci USA 77:3947–3951

    Article  PubMed  CAS  Google Scholar 

  • Segura-Noguera MM, Laiz-Carrión R, Martín del Río MP, Mancera JM (2000) An immunocytochemical study of the pituitary gland of the white seabream (Diplodus sargus). Histochem J 32:733–742

    Article  PubMed  CAS  Google Scholar 

  • Shimizu A, Tanaka H, Kagawa H (2003) 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  PubMed  CAS  Google Scholar 

  • Siegmund I, Troncoso S, Caorsi CE, González CB (1987) Identification and distribution of the cell types in the pituitary gland of Austromenidia laticlavia (Teleostei, Atherinidae). Gen Comp Endocrinol 67:348–355

    Article  PubMed  CAS  Google Scholar 

  • Suzuki K, Kanamori A, Nagahama Y, Kawauchi H (1988) Development of salmon GTH I and GTH II radioimmunoassays. Gen Comp Endocrinol 71:459–467

    Article  PubMed  CAS  Google Scholar 

  • Takahashi A, Itoh T, Nakanishi A, Amemiya Y, Ida H, Meguro H, Kawauchi H (2004) Molecular cloning of proopiomelanocortin cDNA in the ratfish, a holocephalan. Gen Comp Endocrinol 135:159–165

    Article  PubMed  CAS  Google Scholar 

  • Villaplana M, García Ayala A, García-Hernández MP, Agulleiro B (1997) Ontogeny of immunoreactive somatolactin cells in the pituitary of gilthead seabream (Sparus aurata L., Teleostei). Anat Embryol 196:227–234

    Article  PubMed  CAS  Google Scholar 

  • Volckaert FAM, Mugoyo JWM, Lescroart O, Grisez L, Ollevier F (1999) Immunohistochemically detected ontogeny of prolactin and growth hormone cells in the African catfish Clarias gariepinus. Comp Biochem Physiol B 122:423–431

    Article  Google Scholar 

  • Weltzien FA, Kobayashi T, Andersson E, Norberg B, Andersen Ø (2003a) Molecular characterization and expression of FSHβ, LHβ, and common α–subunit in male Atlantic halibut (Hippoglossus hippoglossus). Gen Comp Endocrinol 131:87–96

    Article  PubMed  CAS  Google Scholar 

  • Weltzien FA, Norberg B, Helvik JV, Andersen Ø, Swanson P, Andersson E (2003b) Identification and localization of eight distinct hormone–producing cell types in the pituitary of male Atlantic halibut (Hippoglossus hippoglossus L.). Comp Biochem Physiol A 134:315–327

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yan HY, Thomas P (1991) Histochemical and immunocytochemical identification of the pituitary cell types in three sciaenid fishes: Atlantic croaker (Micropogonias undulatus), spotted seatrout (Cynoscion nebulosus), and red drum (Sciaenops ocellatus). Gen Comp Endocrinol 84:389–400

    Article  PubMed  CAS  Google Scholar 

  • Yang BY, Greene M, Chen TT (1999) Early embryonic expression of the growth hormone family protein genes in the developing rainbow trout, Oncorhynchus mykiss. Mol Reprod Dev 53:127–134

    Article  PubMed  CAS  Google Scholar 

  • Yaron Z, Gur G, Melamed P, Rosenfeld H, Levavi-Sivan B, Elizur A (2001) Regulation of gonadotropin subunit genes in tilapia. Comp Biochem Physiol B 129:489–502

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Prof. N. Maclean, School of Biological Sciences, University of Southampton, Southampton, UK, and Dr. Jean-François Baroiller and Mr. Frédéric Clota, CIRAD, Montpellier, France for providing fish, and Mrs. Elisabeth Katz and Mrs. Gunthild Krey for skilful technical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elisabeth Eppler.

Additional information

This work was supported by the SNF (NRP 50, project 4050–66580) and by the Hartmann Müller-Stiftung für Medizinische Forschung an der Universität Zürich (grant no. 972).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kasper, R.S., Shved, N., Takahashi, A. et al. A systematic immunohistochemical survey of the distribution patterns of GH, prolactin, somatolactin, β–TSH, β–FSH, β–LH, ACTH, and α–MSH in the adenohypophysis of Oreochromis niloticus, the Nile tilapia. Cell Tissue Res 325, 303–313 (2006). https://doi.org/10.1007/s00441-005-0119-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-005-0119-7

Keywords

Navigation