Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

GnRH systems of Cichlasoma dimerus (Perciformes, Cichlidae) revisited: a localization study with antibodies and riboprobes to GnRH-associated peptides

  • 126 Accesses

  • 40 Citations


The distribution of cells that express three prepro-gonadotropin-releasing hormones (GnRH), corresponding to salmon GnRH, sea bream GnRH (sbGnRH), and chicken II GnRH, was studied in the brain and pituitary of the South American cichlid fish, Cichlasoma dimerus. Although the ontogeny and distribution of GnRH neuronal systems have previously been examined immunohistochemically with antibodies and antisera against the various GnRH decapeptides, we have used antisera against various perciform GnRH-associated peptides (GAPs) and riboprobes to various perciform GnRH+GAPs. The results demonstrate that: (1) the GnRH neuronal populations in the forebrain (salmon and sea bream GAPs; sGAP and sbGAP, respectively) show an overlapping pattern along the olfactory bulbs, nucleus olfacto-retinalis, ventral telencephalon, and preoptic area; (2) projections with sGAP are mainly located in the forebrain and contribute to the pituitary innervation, with projections containing chicken GAP II being mainly distributed along the mid and hindbrain and not contributing to pituitary innervation, whereas sbGAP projections are restricted to the ventral forebrain, being the most important molecular form in relation to pituitary innervation; (3) sbGnRH (GnRH I) neurons have an olfactory origin; (4) GAP antibodies and GAP riboprobes are valuable tools for the study of various GnRH systems, by avoiding the cross-reactivity problems that occur when using GnRH antibodies and GnRH riboprobes alone.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9


  1. Adams BA, Vickres ED, Warby C, Park M, Fischer WH, Craig AG, Rivier JE, Sherwood NM (2002) Three forms of gonadotropin-releasing hormone, including a novel form, in a basal salmonid, Coregonus clupeaformis. Biol Reprod 67:232–239

  2. Amano M, Oka Y, Aida K, Okumoto N, Kawashima S, Hasegawa Y (1991) Immunocytochemical demonstration of salmon GnRH and chicken GnRH II in the brain of the masu salmon, Oncorhynchus masou. J Comp Neurol 314:587–585

  3. Andersson E, Fjelldal PG, Klende U, Vikingstad E, Taranger GL, Zohar Y, Stefansson SO (2001) Three forms of GnRH in the brain and pituitary of the turbot, Scophthalmus maximus: immunological characterization and seasonal variation. Comp Biochem Physiol 129B:551–558

  4. Bennis M, Dubourg P, Gamrani H, Calas A, Kah O (1989) Existence of a GnRH immunoreactive nucleus in the dorsal midbrain tegmentum of the chameleon. Gen Comp Endocrinol 75:195–203

  5. Carolsfeld J, Powell JF, Park M, Fischer WH, Craig AG, Chang JP, Rivier JE, Sherwood NM (2000) Primary structure and function of three gonadotropin-releasing hormones, including a novel form, from an ancient teleost, herring. Endocrinology 141:505–512

  6. Cerdá-Reverter JM, Zanuy S, Muñoz-Cueto JA (2001a) Cytoarchitectonic study of the brain of a perciform species, the sea bass (Dicentrarchus labrax). I. The telencephalon. J Morphol 247:217–228

  7. Cerdá-Reverter JM, Zanuy S, Muñoz-Cueto JA (2001b). Cytoarchitectonic study of the brain of a perciform species, the sea bass (Dicentrarchus labrax). II. The diencephalon. J Morphol 247:229–251

  8. Collins PM, O’Neill DF, Barron BR, Moore RK, Sherwood NM (2001) Gonadotropin-releasing hormone content in the brain and pituitary of male and female grass rockfish (Sebastes rastrelliger) in relation to seasonal changes in reproductive status. Biol Reprod 65:173–179

  9. Eisthen HL, Delay RJ, Wirsig-Wiechmann CR, Dionne VE (2000) Neuromodulatory effects of gonadotropin releasing hormone on olfactory receptor neurons. J Neurosci 20:3947–3955

  10. Fernald RD, Shelton LC (1985) The organization of the diencephalon and the pretectum in the cichlid fish, Haplochromis burtoni. J Comp Neurol 238:202–217

  11. Fiorentino M, Pinelli C, D’Aniello B, Iela L, Meglio M di, Rastogi RK (2001) Development and distribution of FMRF-amide-like immunoreactivity in the toad (Bufo bufo) brain. J Chem Neuroanat 21:201–213

  12. González-Martínez D, Madigou T, Zmora N, Anglade I, Zanuy S, Zohar Y, Elizur A, Muñoz-Cueto JA, Kah O (2001) Differential expression of three different prepro-GnRH (gonadotrophin-releasing hormone) messengers in the brain of the European sea bass (Dicentrarchus labrax). J Comp Neurol 429:144–155

  13. González-Martínez D, Zmora N, Mañanos E, Saligaut D, Zauny S, Zohar Y, Elizur A, Kah O, Muñoz-Cueto JA (2002a) Immunohistochemical localization of three different prepro-GnRHs (gonadotrophin-releasing hormone) in the brain and pituitary of the European sea bass Dicentrarchus labrax using antibodies to the corresponding GnRH-associated peptides. J Comp Neurol 446:95–113

  14. González-Martínez D, Zmora N, Zanuy S, Sarasquete C, Elizur A, Kah O, Muñoz-Cueto JA (2002b) Developmental expression of three different prepro-GnRH (gonadotrophin-releasing hormone) messengers in the brain of the European sea bass (Dicentrarchus labrax). J Chem Neuroanat 23:255–267

  15. Gothlif Y, Muñoz-Cueto JA, Sagrillo CA, Selamanoff M, Chen TT, Elizur A, Kah O, Zohar Y (1996) Three forms of gonadotrophin-releasing hormone in a teleost fish: cDNA characterization and brain localization. Biol Reprod 55:636–645

  16. Kah O, Breton B, Dulka JG, Núñez-Rodriguez J, Peter RE, Corrigan A, Rivier JE, Vale WW (1986) A reinvestigation of the GnRH (gonadotropin-releasing hormone) systems in the goldfish brain using antibodies to salmon GnRH. Cell Tissue Res 244:327–333

  17. Kim MH, Oka Y, Amano M, Kobayashi M, Okuzawa K, Hasegawa Y, Kawashima S, Suzuki Y, Aida K (1995) Immunocytochemical localization of sGnRH and cGnRH II in the brain of goldfish Carassius auratus. J Comp Neurol 356:72–82

  18. Lescheid DW, Terasawa E, Abler LA, Urbanski HF, Warby CM, Millar RP, Sherwood NM (1997) A second form of gonadotropin-releasing hormone (GnRH) with characteristics of chicken GnRH-II is present in the primate brain. Endocrinology 138:5618–5629

  19. Marchant TA, Chang JP, Nahorniak CS, Peter RE (1989) Evidence that gonadotrophin-releasing hormone also functions as a growth hormone-releasing factor in the goldfish. Endocrinology 124:2509–2518

  20. Montero M, Vidal B, Vandesande F, King JA, Tramu G, Dufour S, Kah O (1994) Comparative distribution of mammalian GnRH (gonadotropin-releasing hormone) and chicken GnRH II in the brain of the European eel. J Chem Neuroanat 7:227–241

  21. Münz HP, Stumpf WE, Jennes L (1981) LHRH systems in the brain of platyfish. Brain Res 221:1–13

  22. Murakami S, Kikuyama S, Arai Y (1992) The origin of luteinizing hormone-releasing hormone (LHRH) neurons in newts (Cynops pyrrhogaster): the effect of olfactory placode ablation. Cell Tissue Res 269:21–27

  23. Muske LE (1993) Evolution of gonadotrophin-releasing hormone (GnRH) neuronal systems. Brain Behav Evol 42:215–230

  24. Muske LE, Moore FL (1994) Antibodies against different forms of GnRH distinguish different populations of cells and axonal pathways in a urodele amphibian, Taricha granulosa. J Comp Neurol 345:139–147

  25. Muske LE, Moore FL (1998) The amphibian nervus terminalis: anatomy, chemistry and relationship with the hypothalamic LHRH system. Brain Behav Evol 32:141–150

  26. Norgen RB, Gao C (1994) LHRH neuronal subtypes have multiple origins in chickens. Dev Biol 165:735–738

  27. Oka Y, Ichikawa M (1990) Gonadotropin-releasing hormone (GnRH) immunoreactive system in the brain of the dwarf gourami (Colisa laila) as revealed by light microscopy using a monoclonal antibody to common amino acid sequences of GnRH. J Comp Neurol 300:511–522

  28. Okubo K, Sakai F, Lau E, Aida K, Nagahama Y (2004) Characterization of embryonic development of forebrain gonadotropin-releasing hormone neurons using transgenic medaka. Fifth International Symposium on Fish Endocrinology, Castellón, Spain. Abstract 83

  29. Okuzawa K, Granneman J, Bogerd J, Goos HJ, Zohar Y, Kagawa H (1997) Distinct expression of GnRH genes in the red seabream brain. Fish Physiol Biochem 17:71–79

  30. Ookura T, Okuzawa K, Tanaka H, Gen K, Kagawa H (1999) The ontogeny of gonadotropin-releasing hormone neurons in the red seabream. In: Abstracts of the Sixth International Symposium on Reproductive Physiology of Fish. University of Bergen, Bergen, pp 12

  31. Pandolfi M, Parhar IS, Ravaglia MA, Meijide FJ, Maggese MC, Paz DA (2002) Ontogeny and distribution of gonadotropin-releasing hormone (GnRH) neuronal systems in the brain of the cichlid fish Cichlasoma dimerus. Anat Embryol 205:271–281

  32. Parhar IS (1997) GnRH in tialpia: three genes, three origins and their roles. In: Parhar IS (ed) GnRH neurons: gene to behaviour. Brain Shuppan, Tokyo, pp 99–116

  33. Parhar IS, Soga T, Ishikawa Y, Nagahama Y, Sakuma Y (1998) Neurons synthesizing gonadotropin-releasing hormone mRNA subtypes have multiple developmental origins in the medaka. J Comp Neurol 401:217–226

  34. Polkowska J, Przekop F (1993) Effect of protein deficiency on luteinizing hormone releasing hormone (LHRH), gonadotropoin releasing hormone associated peptide (GAP) and luteinizing hormone (LH) immunocytochemistry in the hypothalamus and pituitary gland of prepubertal ewes. Exp Clin Endocrinol 101:230–237

  35. Powell JF, Zohar Y, Elizur A, Park M, Fischer WH, Craig AG, Rivier JE, Lovejoy DA, Sherwood NM (1994) Three forms of gonadotrophin-releasing hormone characterized from brains of one species. Proc Natl Acad Sci USA 91:12081–12085

  36. Powell JFF, Standen EM, Carolsfeld J, Borella M, Gazola R, Fischer WH, Park M, Craig AG, Warby CM, Rivier JE, Val-Sella M, Sherwood NM (1997) Primary structure of three forms of gonadotropin-releasing hormone (GnRH) from the pacu brain. Regul Pept 68:189–195

  37. Ronchi E, Aoki C, Krey LC, Pfaff DW (1992) Immunocytochemical study of GnRH and GnRH-associated peptide in male Syrian hamsters as a function of photoperiod and gonadal alterations. Neuroendocrinology 55:134–145

  38. Schulz RW, Bosma PT, Zanderbergen MA, Van der Sanden MC, Van Dijk W, Peute J, Bogerd J, Goos HJTh (1993) Two gonadotropin-releasing hormones in the African catfish, Clarias gariepinus: localization, pituitary receptor binding, and gonadotropin release activity. Endocrinology 133:1569–1577

  39. Schwanzel-Fukuda M (1999) Origin and migration of luteinizing hormone releasing hormone in mammals. Microsc Res Technol 44:2–10

  40. Schwanzel-Fukuda M, Pfaff DW (1989) Origin of luteinizing hormone-releasing hormone neurons. Nature 338:161–164

  41. Senthilkumaran B, Okuzawa K, Gen K, Ookura T, Kagawa H (1999) Distribution and seasonal variations in levels of three native GnRHs in the brain and pituitary of perciform fish. J Neuroendocrinol 11:181–186

  42. Silverman A, Livne Y, Witkin JM (1994) The gonadotrophin-releasing hormone (GnRH) neuronal system: immunocytochemistry and in situ hybridization. In: Knobil E, Neil J (eds) The physiology of reproduction. Raven, New York, pp 1683–1709

  43. Somoza GM, Lescheid DW, Miranda LA, Lo Nostro FL, Magliulo-Cepriano L, Montaner AD, Schreibman MP, Rivier JE, Sherwood NM (2002) Expression of pejerrey gonadotropin-releasing hormone in three orders of fish. Biol Reprod 67:1864–1871

  44. Stefano AV, Vissio PG, Paz DA, Somoza GM, Maggese MC, Barrantes G (1999) Colocalization of GnRH binding sites with gonadotropin-, somatotropin-, somatolactin- and prolactin-expressing pituitary cells of the pejerrey, Odonthestes bonariensis, in vitro. Gen Comp Endocrinol 116:133–139

  45. Umino O, Dowling JE (1991) Dopamine release from interplexiform cells in the retina. Effects of GnRH, FMRFamide, bicuculline and enkephalin on horizontal cell activity. Neuroscience 11:3034–3046

  46. Urbanski HF, White RB, Fernald RD, Kohama SG, Garyfallou VT, Densmore VS (1999) Regional expression of mRNA encoding a second form of gonadotrophin-releasing hormone in the macaque brain. Endocrinology 140:1945–1948

  47. Van Gils J, Absil P, Grauwels L, Moons L, Vandesande F, Balthazart J (1993) Distribution of luteinizing hormone-releasing hormones I and II (LHRH-I and -II) in the quail and chicken brain as demonstrated with antibodies directed against synthetic peptides. J Comp Neurol 334:304–323

  48. Vickers ED, Laberge F, Adams BA, Hara TJ, Sherwood NM (2004) Cloning and localization of three forms of gonadotropin-releasing hormone, including the novel whitefish form, in a salmonid, Coregonus clupeaformis. Biol Reprod 70:1136–1146

  49. Vissio PG, Stefano AV, Somoza GM, Maggese MC, Paz DA (1999) Close association of gonadotrophin-releasing hormone fibers and gonadotropins, growth hormone, somatolactin and prolactin expressing cells in pejerrey, Odonthestes bonariensis. Fish Physiol Biochem 21:121–127

  50. Walker S, Stell WK (1986) Gonadotropin-releasing hormone (GnRH), molluscan cardioexcitatory peptide (FMRFamide), enkephalin and related neuropeptides affect goldfish retinal ganglion cell activity. Brain Res 384:63–70

  51. Weber GM, Powell JFF, Park M, Fischer WH, Craig AG, Rivier JE, Nanakorn U, Parhar IS, Ngamvongchon S, Grau EG, Sherwood NM (1997) Evidence that gonadotrophin-releasing hormone (GnRH) functions as a prolactin-releasing factor in a teleost fish (Oreochromis mossambicus) and primary structures of three native GnRH molecules. J Endocrinol 155:121–132

  52. White RB, Fernald RD (1998) Genomic structure and expression sites of three gonadotropin-releasing hormone genes in one species. Gen Comp Endocrinol 112:17–25

  53. White SA, Kasten TL, Bond CT, Adelman JP, Fernald RD (1995) Three gonadotropin-releasing hormone genes in one organism suggest novel role for an ancient peptide. Proc Natl Acad Sci USA 92:8363–8367

  54. Wray S, Grant P, Gainer H (1989a) Evidence that cells expressing luteinizing hormone-releasing hormone mRNA in the mouse are derived from progenitor cells in the olfactory placodes. Proc Natl Acad Sci USA 86:8132–8136

  55. Wray S, Grant P, Gainer H (1989b) Spatiotemporal cell expression of luteinizing hormone-releasing hormone in the prenatal mouse:evidence for an embryonic origin in the olfactory placode. Dev Brain Res 46:309–318

  56. Yamamoto N, Oka Y, Kawashima S (1997) Lesions of gonadotropin-releasing hormone (GnRH)-immunoreactive terminal nerve cells: effects on reproductive behavior of male dwarf gouramis. Neuroendocrinology 65:403–412

  57. Yu KL, Sherwood NM, Peter RE (1998) Differential distribution of two molecular forms of gonadotropin-releasing hormone in discrete brain areas of goldfish (Carassius auratus). Peptides 9:625–630

  58. Zamora N, González-Martínez D, Muñoz-Cueto JA, Madigou T, Mañanos-Sanchez E, Doste SZ, Zohar Y, Kah O, Elizur A (2002) The GnRH sytem in the European sea bass (Dicentrarchus labrax). J Endocrinol 172:105–116

Download references

Author information

Correspondence to Matías Pandolfi.

Additional information

This work was supported by grants UBACYT X-217, Conicet PIP 0539/R188; NIH-HD-29186 and Fogarty International Fellowship TW00086.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pandolfi, M., Muñoz Cueto, J.A., Lo Nostro, F.L. et al. GnRH systems of Cichlasoma dimerus (Perciformes, Cichlidae) revisited: a localization study with antibodies and riboprobes to GnRH-associated peptides. Cell Tissue Res 321, 219–232 (2005). https://doi.org/10.1007/s00441-004-1055-7

Download citation


  • GAP
  • Brain
  • GnRH
  • Cichlids
  • Cichlasoma dimerus (Telestei)