Abstract
1. This work deals with a family of neuropeptides, gonadotropin-releasing hormone (GnRH), that play a key role in the development and maintenance of reproductive function in vertebrates.
2. Until now, a total of 16 GnRH structural variants have been isolated and characterized from vertebrate and protochordate nervous tissue. All vertebrate species already investigated have at least two GnRH forms coexisting in the central nervous system. However, it is now well accepted that three forms of GnRH in early and late evolved bony fishes are present.
3. In these cases, cGnRH-II is expressed by midbrain neurons, a species-specific GnRH is present mainly in the preoptic area and the hypothalamus, and sGnRH is localized in the terminal nerve ganglion (TNG). In this context it is possible to think that three GnRH forms and three GnRH receptor (GnRH-R) subtypes are expressed in the central nervous system of a given species.
4. Then it is possible to propose three different GnRH lineages expressed by distinct brain areas in vertebrates: (1) the conserved cGnRH-II or mesencephalic lineage; or (2) the hypothalamic or “releasing” lineage whose primary structure has diverged by point mutations (mGnRH and its orthologous forms: hrGnRH, wfGnRH, cfGnRH, sbGnRH, and pjGnRH); and (3) the telencephalic sGnRH form. Also different GnRH nomenclatures are discussed.
Similar content being viewed by others
REFERENCES
Adams, B. A., Vickers, E. D., Warby, C., Park, M., Fischer, W. H., Grey Craig, A., Rivier, J. E., and Sherwood, N. M. (2002). Three forms of gonadotropin-releasing hormone, including a novel form, in a basal salmonid, Coregonus clupeaformis. Biol. Reprod. 67:232–239.
Adelman, J. P., Mason, A. J., Hayflick, J. S., and Seeburg, P. H. (1986). Isolation of the gene and hypothalamic cDNA for the common precursor of gonadotropin-releasin hormone and prolactin releaseinhibiting factor in human and rat. Proc. Natl. Acad. Sci. U.S.A. 83:179–183.
Amano, M., Aida, K., Okumoto, N., and Hasegawa, Y. (1992). Changes in salmon GnRH and chicken GnRH-II in the brain and pituitary, and GTH contents in the pituitary in female masu salmon, Oncorhynchus masou, from hatching through ovulation. Zool. Sci. 9:375–386.
Amano, M., Hyodo, S., Kitamura, S., Ikuta, K., Suzuki, Y., Urano, A., and Aida, K. (1995). Salmon GnRH synthesis in the preoptic area and the ventral telencephalon is activated during gonadal maturation in female masu salmon. Gen. Comp. Endocrinol. 99:13–21.
Amano, M., Takahashi, A., Yamanome, T., Okubo, K., Aida, K., and Yamamori, K. (2002). Molecular cloning of three cDNAs encoding different GnRHs in the brain of barfin flounder. Gen. Comp. Endocrinol. 126:325–333.
Amores, A., Force, A., Yan, Y.-L., Joly, L., Ameniya, C., Frits, A., Ho, R. K., Langeland, J., Prince, V., Westerfield, M., Ekker, M., and Postlehwait, J. H. (1998). Zebrafish hox clusters and vertebrate genome evolution. Science 282:1711–1714.
Anctil, M. (2000). Evidence for gonadotropin-releasing hormone-like peptides in a cnidarian nervous system. Gen. Comp. Endocrinol. 119:317–328.
Andersen, A. C., Tonon, M. C., Pelletier, G., Conlon, J. M., Fasolo, A., and Vaudry, H. (1992). Neuropeptides in the amphibian brain. Int. Rev. Cytol. 138:89–210.
Anderson, E., Fjelldal, P. G., Klenke, U., Vikingstad, E., Taranger, G. L., Zohar, Y., and Stefansson, S. O. (2001). Three forms of GnRH in the brain and pituitary of the turbot, Scophthalmus maximus: Immunological characterization and seasonal variation. Comp. Biochem. Physiol. B 129:551–558.
Ashihara, M., Suzuki, M., Kubokawa, K., Yoshiura, Y., Kobayashi, M., Urano, A., and Aida, K. (1995). Two differing genes for the salmon-type gonadotropin-releasing hormone exists in salmonids. J. Mol. Endocrinol. 15:1–9.
Bogerd, J., Zanderbergen, T., Andersson, E., and Goss, H. (1994). Isolation, characterization and expression of cDNAs encoding the catfish-type and chicken-II-type gonadotropin-releasing hormone precursors in the African catfish. Eur. J. Biochem. 222:541–549.
Burgus, R., Butcher, M., Amoss, M., Ling, N., Monahan, M., Rivier, J., Fellows, R., Blackwell, R., Vale,W., and Guillemin, R. (1972). Primary structure of ovine luteinizing hormone-releasing factor (LRF). Proc. Natl. Acad. Sci. U.S.A. 69:278–282.
Cameron, C.B., Mackie, G.O., Powell, J. F. F., Lescheid, D.W., and Sherwood, N. M. (1999). Gonadotropinreleasinghormonein Mulberry cells of Saccoglossus and Ptychodera (Hemichordata: Enteropneusta). Gen. Comp. Endocrinol. 114:2–10.
Carolsfeld, J., Powell, J. F. F., Park, M., Fischer, W. H., Craig, A.G., Chang, J. P., Rivier, J. E., and Sherwood, N. M. (2000). A novel form of gonadotropin-releasing hormone (GnRH) in herring sheds light on evolutionary pressures. Endocrinology 141:505–512.
Cassará, M. C., Guilgur, L. G., and Somoza, G. M. (2001). Identification of gonadotropin-releasing hormone (GnRH) variants in the South American lungfish Lepidosiren paradoxa: Phylogentic implications. Biocell 25:44.
Chen, A., Yahalom, D., Ben-Aroya, N., Kaganovsky, E., Okon, E., and Koch, Y. (1998). A second isoform of gonadotropin-releasing hormone is present in the brain of human and rodents. FEBS Lett. 435:199–203.
Chow, M. M., Kight, K. E., Gothilf, Y., Alok, D., Stubblefield, J., and Zohar, Y. (1998). Multiple GnRHs present in a teleost species are encoded by separate genes: Analysis of the sbGnRH and cGnRH-II genes from the striped bass: Morone saxatilis. J. Mol. Endocrinol. 21:277–289.
Coe, I. R., Grier, H. J., and Sherwood, N. M. (1992). Gonadotropin-releasing hormone in the molly Poecilia latipinna: Molecular form, quantity, and location. J. Exp. Zool. 261:414–423.
Coe, I. R., Von Schalburg, K. R., and Sherwood, N. M. (1995). Characterization of the pacific salmon gonadotropin-releasing hormone gene, copy number and transcription start site. Mol. Cell. Endocrinol. 115:113–122.
Collins, P. M., O'Neill, D. F., Barron, B. R., Moore, R. K., and Sherwood, N. M. (2001). Gonadotropinreleasing 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.
Conlon, J. M., Collin, F., Chiang, Y.-C., Sower, S. A., and Vaudry, H. (1993). Two molecular forms of gonadotropin-releasing hormone from the brain of the frog, Rana ridibunda: Purification, characterization, and distribution. Endocrinology 132:2117–2120.
Dellovade, T. L., King, J. A., Millar, R. P., and Rissman, E. F. (1993).. Presence and differential distribution of distinct forms of immunoreactive onadotropin-releasing hormone in the musk shrew brain Neuroendocrinology 58:166–177.
Demski, L. S., Beaver, J. A., Sudberry, J. J., and Curtis, J. R. (1997). GnRH systems in cartilaginous fishes. In Parhar, I. S., and Sakuma, Y.(eds.), GnRH Neurons. Gene to Behavior, Brain Shuppan, Tokyo, pp. 123–143.
Di Cosmo, A., and Cristo, C. (1998). Neuropeptidergic control of the optic gland of Octopus vulgaris: FMRF-amide and GnRH immunoreactivity. J. Comp. Neurol. 398:1–12.
Dubois, E. A., Zandbergen, M. A., Peute, J., and Goos, H. J. Th. (2002). Evolutionary development of three gonadotropin-releasing hormone (GnRH) systems in vertebrates. Brain Res. Bull. 57:413–418.
Dufour, S., Montero, M., Le Belle, N., Bassom-Pierre, M., King, J. A., Millar, R. P., Peter, R. E., and Fontaine, Y. A. (1993). Differential distribution and response to experimental sexual maturation of two forms of gonadotropin-releasing hormone (GnRH) in the European eel, Anguilla anguilla. Fish Physiol. Biochem. 11:19–29.
Dunn, I., Chen, Y., Hook, C., Sharp, P., and Sang, H. (1993). Characterization of the chicken preprogonadotrophin-releasing hormone-I gene. J. Mol. Endocrinol.11:19–29.
Fernald, R. D., and White, R. B. (1999). Gonadotropin-releasing hormone genes: Phylogeny, structure, and functions. Front. Neuroendocrinol. 20:224–240.
Fink, G. (1988). Gonadotropin secretion and its control. In Knobil, E., and Neill, J. (eds.), The Physiology of Reproduction, Raven Press, New York, pp. 1349–1377.
Forlano, P. M., Maruska, K. P., Sower, S. A., King, J. A., and Tricas, T. C. (2000). Differential distribution of gonadotropin-releasing hormone-immunoreactive neurons in the stingray brain: Functional and evolutionary considerations. Gen. Comp. Endocrinol. 118:226–248.
Gautron, J. P., Pattou, E., Bauer, K., and Kordon, C. (1991). (Hydroxyproline9) luteinizing hormonereleasing hormone: A novel peptide in mammalian and frog hypothalamus. Neurochem. Int. 18:221–235.
Gestrin, E. D., White, R. B., and Fernald, R. D. (1999). Second form of gonadotropin-releasing hormone in mouse: Immunocytochemistry reveals hippocampal and periventricular distribution. FEBS Lett. 448:289–291.
Goldberg, J., Garofalo, R., Price, Ch., and Chang, J. P. (1993). Presence and biological activity of a GnRHlike factor in the nervous system of Helisoma trivolvis. J. Comp. Neurol. 336:571–582.
González-Martínez, D., Madigou,T., Zmora,N., Anglade, I., Zanuy, S., Zohar,Y., Elizur, A., Muñoz-Cueto, J. A., and Kah, O. (2001). Differential expression of three different prepro-GnRH (gonadotrophinreleasing hormone) messengers in the brain of the European sea bass (Dicentrarchus labrax). J. Comp. Neurol. 429:144–155.
González-Martínez, D., Zmora, N., Zanuy, S., Sarasquete, C., Elizur, A., Kah, O., and Muñoz-Cueto, J. A. (2002). 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.
Gothilf, Y., Muñoz-Cueto, J. A., Sagrillo, C. A., Selmanoff, M., Chen, T. T., Kah, O., Elizur, A., and Zohar,Y. (1996). Three forms of gonadotropin-releasing hormone in a perciform fish (Sparus aurata): Complementary deoxyribonucleic acid characterization and brain localization. Biol. Reprod. 55:636–645.
Hayes, P.W., Wray, S., and Battey, J. (1994). The frog gonadotropin-releasing hormone-I (GnRH-I) gene has a mammalian-like expression pattern and conserved domains in GnRH-associated peptide, but brain onset is delayed until metamorphosis. Endocrinology 4:1835–1845.
Holland, M. C., Hassin, S., and Zohar,Y. (2001). Seasonal fluctuations in pituitary levels of the three froms of gonadotropin-releasing hormone in striped bass, Morone saxatilis (Teleostei), during juvenile and pubertal development. J. Endocrinol. 169:527–538.
Iela, L., Powell, J.F.F., Sherwood, N. M., D'Aniello, B., Rastogi, R., and Bagnara, J.T. (1986). Reproduction in the Mexican leaf frog, Pachymedusa dacnicolor. VI. Presence and distribution of multiple GnRH forms in the brain. Gen. Comp. Endocrinol. 103:235–243.
Illing, N., Troskie, B., Nahorniak, C. S., Hapgood, J. P., Peter, R. E., and Millar, R. P. (1999). Two gonadotropin-releasing hormone receptor subtypes with distinct ligand selectivity and differential distribution in brain and pituitary in the goldfish (Carassius auratus). Proc. Natl. Acad. Sci. U.S.A. 96:2526–2531.
Jiménez-Liñan, M., Rubin, B. S., and King, J. C. (1997). Examination of guinea pig luteinizing hormonereleasing hormone gene reveals a unique decapeptide and existence of two transcripts in the brain. Endocrinology 138:4123–4130.
Joss, J.M. P., King, J. A., and Millar, R. P. (1994). Identification of the molecular forms of and steroid hormone response to gonadotropin-releasing hormone in the Australian lungfish, Neoceratodus forsteri. Gen. Comp. Endocrinol. 96:392–400.
Kakizawa, S., Kaneko, T., and Hirano, T. (1997). Effects of hypothalamic factors on somatolactin secretion from the organ-cultured pituitary of rainbow trout. Gen. Comp. Endocrinol. 105:71–78.
Kasten, T. L., White, S. A., Norton, T. T., Bond, C. T., Adelman, J. P., and Fernald, R.D. (1996). Characterization of two new preproGnRH mRNAs in the tree shrew: First direct evidence for mesencephalic GnRH gene expression in a placental mammal. Gen. Comp. Endocrinol. 104:7–19.
Kim, M.-H., Kobayashi, M., Oka, Y., Amano, M., Kawashima, S., and Aida, K. (2001). Effects of olfactory tract section on the immunohistochemical distribution of brain GnRH fibers in the female goldfish, Carassius auratus. Zool. Sci. 18:241–248.
King, J. A., Dufour, S., Fotaine, Y.-A., and Millar, R. P. (1990a). Chromatographic and immunological evidence for mammalian GnRH and chicken GnRH-II in eel (Anguilla anguilla) brain and pituitary. Peptides 11:507–514.
King, J. A., Hinds, L. A., Mehl, A. E., Saunders, N. R., and Millar, R. P. (1990b). Chicken GnRH II occurs together with mammalian GnRH in a South American species of marsupial (Monodelphis domestica). Peptides 11:521–525.
King, J. A., Mehl, A. E. I., Tyndale-Biscoe, C. H., Hinds, L., and Millar, R. P. (1989). A second form of gonadotropin-releasing hormone (GnRH), with chicken GnRH II-like properties, occurs together with mammalian GnRH in marsupial brains. Endocrinology 125:2244–2252.
King, J. A., and Millar, R. P. (1982). Structure of chicken hypothalamic luteinizing hormone-releasing hormone II. Isolation and characterization. J. Biol. Chem. 257:10729–10732.
King, J. A., and Millar, R. P. (1986). Identification of His5, Trp7, Tyr8-GnRH (chicken GnRH II) in amphibian brain. Peptides 7:827–834.
King, J. A., and Millar, R. P. (1997). Coordinated evolution of GnRHs and their receptors. In Parhar, I.S., and Sakuma, Y. (eds.), GnRH Neurons. Gene to Behavior, Brain Shuppan, Tokyo, pp. 145–180.
King, J. A., Millar, R. P., Vallarino, M., and Pierantoni, R. (1995). Localization and characterization of gonadotropin-releasing hormones in the brain, gonads and plasma of a dipnoi (lungfish, Protopterus annectens). Regul. Pept. 57:163–174.
King, J. A., Steneveld, A. A., Curlewis, J. D., Rissman, E. F., and Millar, R. P. (1994a). Identification of chicken GnRH II in brains of metatherian and early-evolved eutherian species of mammals. Regul. Pept. 54:467–477.
King, J. A., Steneveld, A. A., and Millar, R. P. (1994b). Differential regional distribution of gonadotropinreleasing hormones in amphibian (clawed toad, Xenopus laevis) brain. Regul. Pept. 50:277–289.
Kobayashi, M., Amano, M., Kim, M.-H., Furukawa, K., Hasegawa,Y., and Aida, K. (1994). Gonadotropinreleasing hormones of terminal nerve origin are not essential to ovarian development and ovulation in goldfish. Gen. Comp. Endocrinol. 95:192–200.
Kobayashi, M., Amano, M., Kim, M.-H., Yoshiura, Y., Sohn, Y. C., Suetake, H., and Aida, K. (1997). Gonadotropin releasing hormone and gonadotropin in goldfish and masou salmon. Fish Physiol. Biochem. 17:1–8.
Kudo, H., Hyodo, S., Ueda, H., Hiroi, O., Aida, K., Hany, I., Hasegawa, Y., and Miyamoto, K. (1996). Cytophysiology of gonadotropin-releasing hormone neurons in chum salmon (Oncorhynchus keta) forebrain before and after upstream migration. Cell Tissue Res. 284:261–267.
Latimer, V. S., Rodrigues, S. M., Garyfallou, V.T., Kohama, S.G., White, R.B., Fernald, R.D., and Urbanski, H. F. (2000). Two molecular forms of gonadotropin-releasing hormone (GnRH-I and GnRH-II) are expressed by two separate populations of cells in the rhesus macaque hypothalamus. Mol. Brain Res. 75:287–292.
Lescheid, D. W., Powell, J. F. F., Fischer, W. H., Park, M., Craig, A. G., Bukovskaya, O., Barannikova, I. A., and Sherwood, N. M. (1995). Mammalian gonadotropin-releasing hormone (GnRH) identified by primary structure in russian strugeon, Acipenser gueldenstaedti. Regul. Pept. 55:299–309.
Lescheid, D. W., Rosen, G. J., Bridge, A. E., Jones, R. E., Warby, C. M., and Sherwood, N. M. (1997a). Immunoreactive gonadotropin-releasing hormone (GnRH) is detected only in the form of chicken GnRH-II within the brain of the green anole, Anolis carolinensis. Gen. Comp. Endocrinol. 108:247–257.
Lescheid, D.W., Terasawa, E., Abler, L., Urbanski, H. F., Warby, C. M., Millar, R. P., and Sherwood, N. M. (1997b). A second form of gonadotropin-releasing hormone (GnRH) with characteristics of chicken GnRH-II is present in the primate brain. Endocrinology 138:5618–5629.
Li, W. S., Lin, H. R., and Wong, A. O. (2002). Effects of gonadotropin-releasing hormone on growth hormone secretion and gene expression in common carp pituitary. Comp. Biochem. Physiol. 132:335–341.
Licht, P., Porter, D., and Millar, R. P. (1987). Specificity of amphibian and reptilian pituitaries for various forms of gonadotropin releasing hormones in vitro. Gen. Comp. Endocrinol. 66:248–255.
Lin, X.-W., and Peter, R. E. (1996). Expession of salmon gonadotropin-releasing hormone (GnRH) and chicken GnRH-II precursor messenger ribonucleic acid in the brain and ovary of goldfish. Gen. Comp. Endocrinol. 101:282–296.
Lovejoy, D. A., Fischer, W. H., Ngamvongchon, S., Craig, A. G., Nahorniak, C. S., Peter, R. E., Rivier, J. E., and Sherwood, N. M. (1992). Distinct sequence of gonadotropin-releasing hormone (GnRH) in dogfish brain provides insight into GnRH evolution. Proc. Natl. Acad. Sci. U.S.A. 89:6373–6377.
Lovejoy, D. A., Fischer, W. H., Parker, D. B., McRory, J. E., Park, M., Lance, V., Swanson, P., Rivier, J. E., and Sherwood, N. M. (1991a). Primary structure of two forms of gonadotropin-releasing hormone from brains of the American alligator (Alligator mississippiensis). Regul. Pept. 33:105–116.
Lovejoy, D. A., Sherwood, N. M., Fischer, W. H., Jackson, B. C., Rivier, J. E., and Lee, T. (1991b). Primary structure of gonadotropin-releasing hormone from the brain of a holocephalan (ratfish: Hydrolagus colliei). Gen. Comp. Endocrinol. 82:152–161.
MacColl, G., Quinton, R., and Bouloux, P. M. G. (2002). GnRH neuronal development: Insights into hypogonadotrophic hypogonadism. Trends Endocrinol. Metab. 13:112–118.
Marchant, T. A., Chang, J. P., Nahorniak, C. S., and Peter, R. E. (1989). Evidence that gonadotropinreleasing hormone also functions as a growth hormone-releasing factor in the goldfish. Endocrinology 124:2509–2518.
Mason, A. J., Hayflick, J. S., Zoeller, R. T., Young, W. S., III, Phillips, H. S., Nikolics, K., and Seeburg, P. H. (1986). A deletion truncating the gonadotropin-releasing hormone gene is responsible for hypogonadism in the hpg mouse. Science 234:1366–1371.
Matsuo, H., Baba, Y., Nair, R.M. G., Arimura, A., and Schally, A. V. (1971). Structure of the porcine LH and FSH-releasing hormone. I. The proposed amino acid sequence. Biochem. Biophys. Res. Commun. 43:1334–1339.
Millam, J. R., Craig-Veit, C. B., Adams, T. E., and Adams, B. M. (1989). Avian gonadotropin-releasing hormones I and II in brain and other tissues in turkey hens. Comp. Biochem. Physiol. A 94:771–776.
Millam, J. R., Ottinger, M. A., Craig-Veit, C. B., Fan, Y., Chiseha, Y., and E. l. Halawani, M. E. (1998). Multiple forms of GnRH are released from perifused medial basal hypothalamic/preoptic area (MBH/POA) explants in birds. Gen. Comp. Endocrinol. 111:95–101.
Millar, R. P., Lowe, S., Conklin, D., Pawson, A., Maudsley, S., Troskie, B., Ott, T., Millar, M., Lincoln, G., Sellar, R., Faurholm, B., Scobie, G., Kuestner, R., Terasawa, E., and Katz, A. (2001). A novel mammalian receptor for the evolutionarily conserved type II GnRH. Proc. Natl. Acad. Sci. U.S.A. 98:9636–9641.
Miranda, L. A., Montaner, A.D., Ansaldo, M., Affanni, J. M., and Somoza, G. M. (1999). Characterization of brain gonadotropin-releasing hormona (GnRH) molecular variants in brain extracts from different perciform fishes from Antartic waters. Polar Biol. 21:122–127.
Miranda, L. A., Paz, D. A., Affanni, J. M., and Somoza, G. M. (1998). Identification and neuroanatomical distribution of immunoreactive mammalian gonadotropin-releasing hormone (mGnRH) in the brain and neural hypophyseal lobe of the toad Bufo arenarum. Cell Tissue Res. 293:419–425.
Miyamoto, K., Hasegawa, Y., Igarashi, M., Chino, N., Sakakibara, S., Kangawa, K., and Matsuo,H. (1983). Evidence that chicken hypothalamic luteinizing hormone-releasing hormone is [Gln8]LHRH. Life Sci. 32:1341–1347.
Miyamoto, K., Hasegawa,Y., Nomura, M., Igarashi, M., Kangawa, K., and Matsuo,H. (1984). Identification of the second gonadotropin releasing hormone in chicken hypothalamus: Evidence that gonadotropin secretion is probably controlled by two distinct gonadotropin-releasing hormones in avian species. Proc. Natl. Acad. Sci. U.S.A. 81:3874–3878.
Montaner, A. D., Affanni, J. M., King, J. A., Bianchini, J. J., Tonarelli, G., and Somoza, G. M. (1999). Differential distribution of gonadotropin-releasing hormone variants in the brain of Hydrochaeris hydrochaeris. Cell. Mol. Neurobiol. 19:635–651.
Montaner, A. D., González, O., Paz, D. A., Affanni, J. M., and Somoza, G. M. (2000). Gonadotropinreleasing hormone (GnRH) variants in a lizard brain. Is mammalian GnRH being expressed? Gen. Comp. Endocrinol. 119:121–131.
Montaner, A., Miranda, L. A., Vizziano, A. D., López, A., Okuzawa, K., and Somoza, G. M. (2001a). Gonadotropin-releasing hormone in two perciform fishes: Micropogonias furnieri and Pagrus pagrus. Fish Physiol. Biochem. 24:243–246.
Montaner, A. D., Mongiat, L., Lux-Lantos, V. A. R., Park, M. K., Fischer, W. H., Craig, A. G., Rivier, J. E., Lescheid,D., Lovejoy,D., Libertun, C., Sherwood, N. M., and Somoza, G. M. (2001b). Structure and biological activity of gonadotropin-releasing hormone (GnRH) isoforms isolated from rat and hamster brains. Neuroendocrinology 74:202–212.
Montaner, A. D., Mongiat, L., Lux-Lantos, V. A., Warby, C., Chewpoy, B., Bianchi, M. S., Libertun, C., Rivier, J. E., Sherwood, N. M., and Somoza, G. M. (2002). Guinea pig gonadotropin-releasing hormone (gpGnRH): Expression pattern, characterization and biological activity in rodents. Neuroendocrinology 75:326–338.
Montaner, A. D., Park, M., Fischer, W. H., Craig, A. G., Chang, J. P., Somoza, G. M., Rivier, J. E., and Sherwood, N. M. (2001c). Primary structure of a novel gonadotropin-releasing hormone (GnRH) variant in the brain of pejerrey (Odontesthes bonariensis). Endocrinology 142:1453–1460.
Montaner, A. D., Somoza, G. M., King, J. A., Bianchini, J. J., Bolis, G., and Affanni, J. M. (1998). Chromatographic and immunological identification of GnRH (Gonadotropin-releasing hormone) variants. Occurrence of mammalian and salmon-likeGnRHin the forebrain of an eutherian mammal: Hydrochaeris hydrochaeris (Mammalia, Rodentia). Regul. Pept. 73:197–204.
Muske, L. E. (1997). Organization of multiple molecular forms of GnRH. In Parhar, I. S., and Sakuma, Y. (eds.), GnRH Neurons. Gene to Behavior, Brain Shuppan, Tokyo, pp. 145–180.
Muske, L. E., and Moore, F. L. (1998). The amphibian nervous terminalis: Anatomy, chemistry and relationship with the hypothalamic LHRH system. Brain Behav. Evol. 32:141–150.
Mylonas, C. C., and Zohar, Y. (2001). Use of GnRHa-delivery systems for the control of reproduction in fish. Rev. Fish Biol. Fisher. 10:463–491.
Neill, J. D. (2002). GnRH and GnRH receptor genes in the human genome. Endocrinology 143:737–743.
Neill, J. D., Duck, L. W., Sellers, J. C., and Musgrove, L. C. (2001). A gonadotropin-releasing hormone (GnRH) receptor specific forGnRHII in primates. Biochem. Biophys. Res. Commun. 282:1012–1018.
Nelson, J. S. (1994). Fishes of the World,Wiley, Inc., Tokyo, p. 600.
Ngamvongchon, S., Lovejoy, D. A., Fischer, W. H., Craig, A.G., Nahorniak, C. S., Peter, R. E., Rivier, J. E., and Sherwood, N. M. (1992). Primary structures of two forms of gonadotropin-releasing hormone, one distinct and one conserved, from catfish brain. Mol. Cell. Neurosci. 3:7–22.
Oka, Y. (1992). Gonadotropin-releasing hormone (GnRH) cells of the terminal nerve as a model neuromodulator system. Neurosci. Lett. 142:119–122.
Oka,Y. (1997).GnRHneuronal system of fish brain as a model system for study of peptidergic neuromodulation. In Parhar, I. S., and Sakuma, Y. (eds.), GnRH Neurons. Gene to Behavior, Brain Shuppan, Tokyo, pp. 245–276.
Oka,Y., and Matsushima,T. (1993). Gonadotropin-releasing hormone (GnRH)-immunoreactive terminal nerve cells have intrinsic rhythmicity and project widely in the brain. J. Neurosci. 13:2161–2176.
Okubo, K., and Aida, K. (2001). Gonadotropin-releasing hormones (GnRHs) in a primitive teleost, the arowana: Phylogenetic evidence that three paralogous lineages of GnRH occurred prior to the emergence of teleosts. Gen. Comp. Endocrinol. 124:125–133.
Okubo, K., Amano, M., Yoshiura, Y., Suetake, H., and Aida, K. (2000). A novel form of gonadotropinreleasing hormone in the medaka, Oryzias latipes. Biochem. Biophys. Res. Commun. 276:298–303.
Okubo, K., Nagata, S., Ko, R., Kataoka, H., Yoshiura, Y., Mitani, H., Kondo, M., Naruse, K., Shima, A., and Aida, K. (2001). Identification and characterization of two distinct GnRH receptor subtypes in a teleost, the medaka Oryzias latipes. Endocrinology 142:4729–4739.
Okuzawa, K., Amano, M., Kobayashi, M., Aida, K., Hanyu, I., Hasegawa, Y., and Miyamoto, K. (1990). Differences in salmon GnRH and chicken GnRH-II contents in discrete brain areas of male and female rainbow trout according to age and stage of maturity. Gen. Comp. Endocrinol. 80:116–126.
Okuzawa, K., Furukawa, K., Aida, K., and Hanyu, I. (1994). The effect of water temperature on gonadotropin-releasing hormone contents in the discrete brain areas and pituitary of male honmoroko Gnathopogon cerulescens. Fish Sci. 60:155–158.
O'Neill, D. F., Powell, J. F. F., Standen, E. M., Youson, J. H., Warby, C. M., and Sherwood, N. M. (1998). Gonadotropin-releasing hormone (GnRH) in anciet teleosts, the bonytongue fishes: Putative origin of salmon GnRH. Gen. Comp. Endocrinol. 112:415–425.
Pandolfi, M., Parhar, I. S., Ravaglia, M. A., Meijide, F. J., Maggese, M. C., and Paz, D. A. (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.
Parhar, I. S. (1997).GnRHin tilapia: Three genes, three origins and their roles. In Parhar, I. S., and Sakuma Y. (eds.), GnRH Neurons. Gene to Behavior, Brain Shuppan, Tokyo, pp. 99–122.
Parhar, I. S., Iwata, M., Pfaff, D. W., and Scwanzel-Fukuda, M. (1995). Embryonic development of gonadotropin-releasing hormone neurons in the sockeye salmon. J. Comp. Neurol. 362:256–270.
Parhar, I. S., Koibuchi, N., Saki, M., Iwata, M., and Yamoaka, S. (1994). Gonadotropin-releasing hormone (GnRH): Expression during salmon migration. Neurosci. Lett. 172:15–18.
Parhar, I. S., Soga, T., and Sakuma, Y. (1998). Quantitative in situ hybridization of three gonadotropinreleasing hormone-encodingmRNAs in castrated and progesterone-treated male tilapia. Gen. Comp. Endocrinol. 112:406–414.
Parhar, I. S., Soga, T., Sakuma, Y., and Millar, R. P. (2002). Spatio-temporal expresión of gonadotropinreleasing hormone receptor subtypes in gonadotropes, somatotropes and lactotropes in the cichlid fish. J. Neuroendocrinol. 14:657–665.
Pazos, A., and Mathieu, M. (1998). Effects of five natural gonadotropin-releasing hormones on cell suspensions of marine bivalve gonad: Stimulation of gonial DNA synthesis. Gen. Comp. Endocrinol. 113:112–120.
Penlington, M. C., Williams, M. A., Sumpter, J. P., Rand-Weaver, M., Hoole, D., and Arme, C. (1997). Isolation and characterisation of mRNA encoding the salmon-and chicken-II type gonadotropinreleasing hormones in the teleost fish Rutilus rutilus (Cyprinidae). J. Mol. Endocrinol. 19:337–346.
Peter, R. E., and Yu, K. L. (1997). Neuroendocrine regulation of ovulation in fishes: basic and applied aspects. Rev. Fish Bioler. Fisher 7:173–197.
Powell, R.C., Ciarcia,G., Lance,V., Millar, R. P., and King, J.A. (1986). Identification of diverse molecular forms of GnRH in reptile brain. Peptides 7:1101–1108.
Powell, J. F. F., Fischer, W. H., Park, M., Craig, A.G., Rivier, J. E., White, S. A., Francis, R.C., Fernald, R.D., Licht, P., Warby, C., and Sherwood, N. M. (1995). Primary structure of solitary form of gonadotropinreleasing hormone (GnRH) in cichlid pituitary; three forms of GnRH in brain of cichlid and pumpkinseed fish. Regul. Pept. 57:43–53.
Powell, R. C., Jach, H., Millar, R. P., and King, J. A. (1987). Identification of Gln8-GnRH and His5,Trp7,Tyr8-GnRH in the hypothalamus and extrahypothalamic brain of the ostrich (Struthio camelus). Peptides 8:185–190.
Powell, R.C., King, J. A., and Millar, R. P. (1985). [Trp7,Leu8]LH-RHin reptilian brain.Peptides 6:223–227.
Powell, J. F. F., Krueckl, S. L., Collins, P. M., and Sherwood, N. M. (1996a). Molecular forms of GnRH in three model fishes: Rockfish, medaka and zebrafish. J. Endocrinol. 150:17–23.
Powell, J. F. F., Reska-Skinner, S. M., Om Prakash, M., Fischer, W. H., Park, M., Rivier, J. E., Crai, A. G., Mackie, G. O., and Sherwood, N. M. (1996b). Two new forms of gonadotropin-releasing hormone in a protochordate and the evolutionary implications. Proc. Natl. Acad. Sci. U.S.A. 93:10461–10464.
Powell, J. F. F., Standen, E. M., Carolsfeld, J., Borella, M., Gazola, R., Fischer, W. H., Park, M., Craig, A.G., Warby, C. M., Rivier, J. E., Val-Sella, M., and Sherwood, N. M. (1997). Primary structure of three forms of gonadotropin-releasing hormone (GnRH) from the pacu brain. Regul. Pept. 68:189–195.
Powell, J. F. F., Zohar, Y., Elizur, A., Park, M., Fischer, W. H., Craig, A. G., Rivier, J. E., Lovejoy, D. A., and Sherwood, N. M. (1994). Three forms of gonadotropin-releasing hormone characterized from brains of one species. Proc. Natl. Acad. Sci. U.S.A. 91:12081–12085.
Quambeck, C., Sherwood, N. M., Millar, R. P., and Terasawa, E. (1997). Two populations of luteinizing hormone releasing hormone neurons in the forebrain of the rhesus macaque during embryonic development. J. Comp. Neurol. 380:293–309.
Rastogi, R. K., King, J. A., Di Fiore, M. M., D'Aniello, B., and Pinelli,C. (1997). Sex and reproductive status related brain content of mammalian and chicken-II GnRHs in Rana esculenta. J. Neuroendocrinol. 9:519–522.
Reinhart, J., Mertz, L. M., and Catt, K. J. (1992). Molecular cloning and expression of cDNA encoding the murine gonadotropin-releasing hormone receptor. J. Biol. Chem. 267:21281–21284.
Rissman, E. F. (1996). Behavioral regulation of gonadotropin-releasing hormone. Biol. Reprod. 54:413–419.
Rodríguez, L., Carrillo, M., Sorbera, L. A., Sourbrier, M. A., Mañanós, E., Holland, M. C. H., Yohar, Y., and Zanuy, S. (2000). Pituitary levels of three forms of GnRH in the male European sea bass (Dicentrarchus labrax, L.) during sex differentiation and first spawning season. Gen. Comp. Endocrinol. 120:67–74.
Roy, P., Datta, M., Dasgupta, S., and Bhattacharya, S. (2000). Gonadotropin-releasing hormona-stimulates thyroid activity in a freshwater Muriel, Channa gachau (ham.) and carps Catla catla (ham.) and Cirrhinus mrigala (ham.). Gen. Comp. Endocrinol. 117:456–463.
Schulz, R.W., Bosma, P. T., Zandbergen, M. A., Sanden, M. C., Dijk, Wv., Peute, J., Bogerd, J., and Goos, H. J. Th. (1993). Two gonadotropin releasing hormones in the African catfish, Clarias gariepinus: Localization, pituitary receptor binding, and gonadotropin release activity. Endocrinology 133:1569–1577.
Seeburg, P. H., and Adelman, J. P. (1984). Characterization of cDNA for precursor of human luteinizing hormone releasing hormone. Nature 83:666–668.
Senthilkumaran, B., Okuzawa, K., Gen, K., Ookura, T., and Kagawa, H. (1999). Distribution and seasonal variations in levels of three native GnRHs in the brain and pituitary of perciform fish. J. Neuroendocriol. 11:181–186.
Sharp, P. J., Dawson, A., and Lea, R. W. (1998). Control of luteinizing hormone and prolactin secretion in birds. Comp. Biochem. Physiol. C 119:275–282.
Sharp, P. J., Talbot, R. T., Main, G. M., Dunn, I. C., Fraser, H. M., and Huskisson, N. S. (1990). Physiological roles of chicken LHRH-I and-II in the control of gonadotropin release in the domestic chicken. J. Endocrinol. 124:291–299.
Sherwood, N. M., Doroshov, S., and Lance, V. (1991). Gonadotropin-releasing hormone (GnRH) in bony fish that are phylogenetically ancient: Reedfish (Calamoichthys calabaricus), sturgeon (Acipenser transmontanus) and Alligator Gar (Lepisosteus spepatula). Gen. Comp. Endocrinol. 84:44–57.
Sherwood, N. M., Eiden, L., Brownstein, M., Spiess, J., Rivier, J., and Vale,W. (1983). Characterization of a teleost gonadotropin-releasing hormone. Proc. Natl. Acad. Sci. U.S.A. 80:2794–2798.
Sherwood, N. M., Grier, H. J., Warby, C., Peute, J., and Taylor, R. J. (1993). Gonadotropin-releasing hormones, including a novel form, in snook Centropomus undecimalis, in comparison with forms in black sea bass Centropristis striata. Regul. Pept. 46:523–534.
Sherwood, N. M., Harvey,B., Brownstein, M. J., and Eiden, L. E. (1984). Gonadotropin-releasing hormone (Gn-RH) in stiped mullet (Mugil cephalus), milkfish (Chanos chanos), and rainbow trout (Salmo gairdneri): Comparison with salmon GnRH. Gen. Comp. Endocrinol. 55:174–181.
Sherwood, N. M., Sower, S. A., Marshak, D. R., Fraser, B. A., and Brownstein, M. J. (1986a). Primary structure of gonadotropin-releasing hormone from lamprey brain. J. Biol. Chem. 261:4812–4819.
Sherwood, N. M., von Schalburg, K., and Lescheid, D.W. (1997). Origin and evolution of GnRH in vertebrates and invertebrates. In Parhar, I. S., and Sakuma, Y. (eds.), GnRH Neurons. Gene to Behavior, Brain Shuppan, Tokyo, pp. 3–25.
Sherwood, N. M., and Whittier, J. M. (1988). Gonadotropin releasing hormone from brains of reptiles: Turtles (Pseudemys scripta) and snakes (Thamnophis sirtalis parietalis). Gen. Comp. Endocrinol. 69:319–327.
Sherwood, N. M., Wingfiled, J. C., Ball, G. F., and Dufty, A.M. (1988). Identity of gonadotropin-releasing hormone in passerine birds: Comparison of GnRH in song sparrow (Melospiza melodia) and starling (Sturnus vulgaris) with five vertebrate GnRHs. Gen. Comp. Endocrinol. 69:341–351.
Sherwood, N. M., Zoeller, R. T., and Moore, F. L. (1986b). Multiple forms of gonadotropin-releasing hormone in amphibian brains. Gen. Comp. Endocrinol. 61:313–322.
Silverman, A. J., Livne, Y., and Witkin, J. W. (1994). The gonadotropin-releasing hormone (GnRH), neuronal system: Immunocytochemistry and in situ hybridization. In Knobil, E., and Neil, J. (eds.), The Physiology of Reproduction, Raven Press, New York, pp. 1683–1709.
Somoza, G. M., Lescheid, D., Miranda, L. A., Lo Nostro, F. L., Magliulo-Cepriano, L., Montaner, A. D., Schreibman, M. P., Rivier, J. E., and Sherwood, N. M. (in press). Expression of pejerrey gonadotropinreleasing hormone (pjGnRH) in three orders of fish. Biol. Reprod.
Somoza, G. M., Stefano, A. V., D'Eramo, J. L., Canosa, L. F., and Fridman, O. (1994). Immunoreactive GnRH suggesting a third form of GnRH in addittion to cIIGnRH and sGnRH in the brain and pituitary gland of Prochilodus lineatus (Characiformes). Gen. Comp. Endocrinol. 94:44–52.
Sower, S. A. (1997). Evolution of GnRH in fish of ancient origins. In Parhar, I. S., and Sakuma, Y. (eds.), GnRH Neurons. Gene to Behavior, Brain Shuppan, Tokyo, pp. 27–49.
Sower, S. A., Chiang, Y.-C., Lovas, S., and Conlon, J. M. (1993). Primary structure and biological activity of a third gonadotropin-releasing hormone from lamprey brain. Endocrinology 132:1125–1131.
Sower, S.A., and Kawauchi, H. (2001). Update: Brain and pituitary hormones of lampreys.Comp. Biochem. Physiol. B 129:291–302.
Sower, S. A., McGregor, A. J., Materne, O. L., Chase,C., Potter, I., and Joss, J. (2000). Evidence for lamprey GnRH-I and-III-like molecules in the brains of the southern hemisphere lampreys Geotria australis and Mordacia mordax. Gen. Comp. Endocrinol. 120:168–175.
Sower, S. A., Nozaki, M., Knox, C. J., and Gorbman, A. (1995).The occurrence and distribution ofGnRHin the brain of Atlantic hagfish, an agnatha, determined by chromatography and immunocytochemistry. Gen. Comp. Endocrinol. 97:300–307.
Stefano, A. V., Aldana-Marcos, H. J., Affanni, J. M., and Somoza, G. M. (2000). Gonadotropin-releasing hormone (GnRH) neuronal systems in the pejerrey Odontesthes bonariensis (Atheriniformes). Fish Physiol. Biochem. 23:215–223.
Stefano, A. V., Vissio, P.G., Paz, D. A., Somoza, G. M., Maggese, M. C., and Barrantes, G. E. (1999). Colocalization of GnRH binding sites with gonadotropin-, somatotropin-, somatolactin-and prolactinexpressing pituitary cells of the pejerrey Odontesthes bonariensis, in vitro. Gen. Comp. Endocrinol. 116:133–139.
Stojilkovic, S. S., Reinhart, J., and Catt, K. J. (1994). Gonadotropin-releasing hormone receptors: Structure and signal transduction pathways. Endocr. Rev. 15:462–499.
Suzuki, K., Gamble, R., and Sower, S. (2000). Multiple transcripts encoding lamprey gonadotropinreleasing hormone-I precursors. J. Mol. Endocrinol. 24:365–376.
Suzuki, M., Hyodo, S., Kobayashi, M., Aida, K., and Urano, A. (1992). Characterization and localization ofmRNAencoding the salmon-type gonadotropin-releasing hormone precursor of the masu salmon. J. Mol. Endocrinol. 9:73–82.
Troskie, B. E., Hapgood, J. P., Millar, R. P., and Illing, N. (2000). Complementary deoxyribonucleic acid cloning, gene expression, and ligand selectivity of a novel gonadotropin-releasing hormone receptor expressed in the pituitary and midbrain of Xenopus laevis. Endocrinology 141:1764–1771.
Troskie,B., Illing,N., Rumbak, E., Sun,. M., Hapgood, J., Sealfon, S., Conklin,D., and Millar, R. P. (1998). Identification of three putative GnRH receptor subtypes in vertebrates. Gen. Comp. Endocrinol. 112:296–302.
Tsai, P.-S., and Licht, P. (1993). In vivo responsiveness of LH secretion in the female turtle, Trachemys scripta, in relation to the reproductive stage. Gen. Comp. Endocrinol. 90:328–337.
Tsutsumi, M., Zhou,W., Millar, R. P., Mellon, P. L., Roberts, J. L., Flanagan, C. A., Dong, K., Gillo, B., and Sealfon, S. C. (1992). Cloning and functional expression of a mouse gonadotropin-releasing hormone receptor. Mol. Endocrinol. 6:1163–1169.
Wang, L., Bogerd, J., Choi, H. S., Seong, J. Y., Soh, J. M., Chun, S. Y., Blomenrohr, M., Troskie, B. E., Millar, R. P., Yu, W. H., McCann, S. M., and Kwon, H. B. (2001a). Three distinct types of GnRH receptor characterized in the bullfrog. Proc. Natl. Acad. Sci. U.S.A. 98:361–366.
Wang, L., Yoo, M. S., Kang, H. M., Im, W. B., Choi, H. S., Bogerd, J., and Kwon, H. B. (2001b). Cloning and characterization of cDNAs encoding the GnRH1 and GnRH2 precursors from bullfrog (Rana catesbeiana). J. Exp. Zool. 289:190–201.
Weber, G. M., Powell, J. F. F., Park, M., Fischer, W. H., Craig, A. G., Rivier, J. E., Nanakorn, U., Parhar, I. S., Ngamvongchon, S., Grau, E. G., and Sherwood, N. M. (1997). Evidence that gonadotropin releasing hormone (GnRH) functions as a prolactin releasing factor in a teleost fish (Oreochromis mossambicus) and primary structure for three native GnRH molecules. J. Endocrinol. 155:121–132.
White, R. B., Eisen, J. A., Kasten, T. L., and Fernald, R.D. (1998). Second gene for gonadotropin-releasing homone in humans. Proc. Natl. Acad. Sci. U.S.A. 95:305–309.
White, R. B., and Fernald, R. D. (1998). Genomic structure and expression sites of three gonadotropinreleasing hormone genes in one species. Gen. Comp. Endocrinol. 112:17–25.
White, S. A., Katen, T. L., Bond, C. T., Adelman, J. P., and Fernald, R. D. (1995). Three gonadotropin releasing hormone genes in one organism suggest novel roles for an ancient peptide. Proc. Natl. Acad. Sci. U.S.A. 92:8363–8367.
Yahalom,D., Chen, A., Ben-Aroya, N., Rahimipour, S., Kaganovsky, E., Okon, E., Fridkin, M., and Koch, Y. (1999). The gonadotroin-releasing hormone family of neuropeptides in the brain of human, bovine and rat: Identification of a third form. FEBS Lett. 463:289–294.
Yoo, M. S., Kang, H. M., Choi, H. S., Kim, J.W., Troskie, B. E., Millar, R. P., and Kwon, H. B. (2000). Molecular cloning, distribution and pharmacological characterization of a novel gonadotropin-releasing hormone ([Trp8] GnRH) in frog brain. Mol. Cell. Endocrinol. 164:197–204.
Yu, K. L., Sherwood, N. M., and Peter, R. E. (1988). Differential distribution of two molecular forms of gonadotropin-releasing hormone in discrete brain areas of goldfish (Carassius auratus). Peptides 9:625–630.
Zandbergen, M. A., Kah, O., Bogerd, J., Peute, J., and Goos, H. J. Th. (1995). Expression and distribution of two gonadotropin releasing hormone in the catfish brain. Neuroendocrinology 62:571–578.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Somoza, G.M., Miranda, L.A., Strobl-Mazzulla, P. et al. Gonadotropin-Releasing Hormone (GnRH): From Fish to Mammalian Brains. Cell Mol Neurobiol 22, 589–609 (2002). https://doi.org/10.1023/A:1021888420271
Issue Date:
DOI: https://doi.org/10.1023/A:1021888420271