Environmental Biology of Fishes

, Volume 38, Issue 1–3, pp 197–208 | Cite as

Gonadotropin-releasing hormone in cartilaginous fishes: structure, location, and transport

  • Nancy M. Sherwood
  • David A. Lovejoy


Gonadotropin-releasing hormone (GnRH) is thought to play a fundamental role in the reproduction of cartilaginous fishes. The primary structures of the only form of GnRH in ratfish,Hydrolagus colliei, and one of four forms of GnRH in dogfish,Squalus acanthias, have recently been shown to be identical to a form originally isolated from birds (chicken GnRH-II). Phylogenetic studies indicate that this chicken GnRH-II molecule is the most highly conserved GnRH family member in vertebrates; it is present in animals from cartilaginous fishes to marsupials. However, the presence of four immunoreactive forms of GnRH inS. acanthias, but only one form inH. colliei suggests that the two subclasses of these species diverged a long time ago. Immunocytochemical localization of GnRH shows that it is found in the brains of all chondrichthyans examined to date. GnRH cell bodies and fibers were found in specific patterns throughout the brain in our studies of dogfish shark and black skate,Bathyraja kincaidii. The lack of immunoreactive GnRH fibers in the median eminence and the unique arrangement of the pituitary in Chondrichthyes suggest that transport of GnRH from the brain to the pituitary gonadotropes occurs in the systemic circulation. The use of this unconventional route is further supported by markedly higher levels of serum GnRH in ratfish compared with other vertebrates.

Key words

Elasmobranchs Holocephalans Neuropeptides Brain Immunohistochemistry Reproduction Vertebrates Evolution Chondrichthyes Sharks Skates Ratfish 


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References cited

  1. Araki, S., N. Takanashi, K. Chikazawa, M. Motoyama, A. Akabori, S. Konuma & T. Tamada. 1986. Reevaluation of immunoreactive gonadotropin-releasing hormone (GnRH) levels in general circulation in women: changes in levels and episodic patterns before, during and after gonadotropin surges. Endocrinol. Jap. 55: 457–468.Google Scholar
  2. Barry, J. 1979. Immunohistochemistry of luteinizing hormone-releasing hormone-producing neurons of the vertebrates. Int. Rev. Cytol. 60: 179–221.Google Scholar
  3. Bennis, M., P. Dubourg, H. Gamrani, A. Calas & O. Kah. 1989. Existence of a GnRH immunoreactive nucleus in the dorsal midbrain tegmentum of the chameleon. Gen. Comp. Endocrinol. 75: 195–203.Google Scholar
  4. Burgus, R., M. Butcher, M. Amoss, N. Ling, M. Monahan, R. Fellows, R. Blackwell, W. Vale & R. Guillemin. 1972. Primary structure of the ovine hypothalamic luteinizing hormone-releasing factor (LRF). Proc. Natl. Acad. Sci. USA 69: 278–282.Google Scholar
  5. Chan, R.L. & M.D. Chaplin. 1985. Plasma binding of LHRH and nafarelin acetate, a highly potent LHRH agonist. Biochem. Biophys. Res. Communic. 127: 673–679.Google Scholar
  6. Chiba,A. & Y. Honma. 1989. Somatostatin- and luteinizing hormone-releasing hormone like immunoreactivities in the brains of the arctic lamprey and the gummy shark. Eleventh International Symposium on Comparative Endocrinology, Malaga Spain, abstract P-78.Google Scholar
  7. Clarke, B.L. & J.T. Cummins. 1982. The temporal relationship between gonadotropin releasing hormone (GnRH) and luteinizing hormone (LH) secretion in ovariectomized ewes. J. Endocrinol. 111: 1737–1739.Google Scholar
  8. Davis, M.R., J.D. Veldhuis, A.D. Rogol, M.L. Dufau & K.J. Catt. 1987. Sustained inhibitory actions of a potent antagonist of gonadotropin-releasing hormone in postmenopausal women. J. Clin. Endocrinol. Metabol. 64: 1268–1274.Google Scholar
  9. Deery, D.J. 1974. Determination by radioimmunoassay of the luteinizing hormone-releasing hormone (LHRH) content of the hypothalamus of the rat and some lower vertebrates. Gen. Comp. Endocrinol. 24: 280–285.Google Scholar
  10. Demski, L. S. 1989. Pathways for GnRH control of elasmobranch reproductive physiology and behavior. J. Exp. Zool. Suppl. 2: 4–11.Google Scholar
  11. Dodd, J.M., M.H.I. Dodd, J.P. Sumpter & N. Jenkins. 1982. Gonadotrophic activity in the buccal lobe (Rachendachhypophyse) of the pituitary gland of the rabbit fish Hydrolagus colliei (Chondrichthyes: Holocephali). Gen. Comp. Endocrinol. 48: 174–180.Google Scholar
  12. Dufour, S., F. Monniot, C. Monniot, S. Baloche, B. Kerdelhue & Y-A Fontaine. 1988. Dosage radioimmunologique, chez Ascidella aspersa, d"un facteur de type gonadoliberine (GnRH) de poids moleculaire apparent supérieur à celui du decapeptide mammalien. C.R. Acad. Sci. Paris, Serie III, 306: 253–256.Google Scholar
  13. Folkers, K., C.Y. Bowers, P-F.L. Tang & M. Kubota. 1986. Decapeptides as effective agonists from L-amino acids biologically equivalent to the luteinizing hormone-releasing hormone. Proc. Natl. Acad. Sci. USA 82: 1070–1074.Google Scholar
  14. Forey, P.L. 1988. Golden jubilee for the coelacanth Latimeria chalumnae. Nature 336: 727–732.Google Scholar
  15. Georges, D. & M.P. Dubois. 1980. Mise en évidence par les techniques d"immunofluorescence d"un antigene de type LH-RH dans le système nerveux de Ciona intestinalis (Tunicier ascidiace). C.R. Acad. Sci. Paris, Ser. D. 290: 29–31.Google Scholar
  16. Gunter, G., L.L. Sulya & B.E. Box. 1961. Some evolutionary patterns in fishes" blood. Biol. Bull. 121: 302–306.Google Scholar
  17. Hasegawa, Y., K. Miyamota, M. Igarashi, N. Chino & S. Sakakibara. 1984. Biological properties of chicken luteinizing hormone-releasing hormone: gonadotropin release from rat and chicken cultured anterior pituitary cells and radioligand analysis. Endocrinology 114: 1441–1447.Google Scholar
  18. Hildebrand, M. 1988. Analysis of vertebrate structure. John Wiley & Sons, Toronto. 701 pp.Google Scholar
  19. Huang,Y-P. 1990. gonadotropin-releasing hormone serum binding protein and metabolism in goldfish. Ph.D. Dissertation, University of Alberta, Edmonton, 179pp.Google Scholar
  20. Huang, Y-P. & R.E. Peter. 1988. Evidence for a gonadotropin-releasing hormone binding protein in goldfish (Carassius auratus) serum. Gen. Comp. Endocrinol. 69: 308–316.Google Scholar
  21. Jenkins, N. & J.M. Dodd. 1980. Effects of synthetic mammalian gonadotropin releasing hormone and dogfish hypothalamic extracts on levels of androgens and oestradiol in the circulation of the dogfish (Scyliorhinus canicula L.). J. Endocrinol. 86: 171–177.Google Scholar
  22. Jenkins, N., J.P. Sumpter & B.K. Follet. 1978. The effects of vertebrate gonadotrophins on androgen release in vitro from testicular cells of Japanese quail and a comparison with their radioimmunoassay activities. Gen. Comp. Endocrinol. 35: 309–321.Google Scholar
  23. Kelsall, R., I.R. Coe & N.M. Sherwood. 1990. Phylogeny and ontogeny of gonadotropin-releasing hormone: comparison of guinea pig, rat and a protochordate. Gen. Comp. Endocrinol. 78: 479–494.Google Scholar
  24. King, J.A. & R.P. Millar. 1980. Comparative aspects of luteinizing hormone-releasing hormone structure and function in vertebrate phylogeny. Endocrinology 106: 707–717.Google Scholar
  25. King, J.A. & R.P. Millar. 1982a. Structure of chicken hypothalamic luteinizing hormone-releasing hormone. I. Structural determination on partially purified material. J. Biol. Chem. 257: 10722–10728.Google Scholar
  26. King, J.A. & R.P. Millar. 1982b. Structure of chicken hypothalamic luteinizing hormone-releasing hormone. II. Isolation and characterization. J. Biol. Chem. 257: 10729–10732.Google Scholar
  27. King, J.A., A.E.I. Mehl, C.H. Tyndale-Biscoe, L. Hinds & R.P. Millar. 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.Google Scholar
  28. Lagios, M.D. 1975. The pituitary gland of the coelacanth Latimeria chalumnae Smith. Gen. Comp. Endocrinol. 25: 126–146.Google Scholar
  29. Lance, V. & I.P. Callard. 1978. Gonadotropic activity in pituitary extracts from an elasmobranch (Squalus acanthias). J. Endocrinol. 78: 149–150.Google Scholar
  30. Liu, Q. & L.S. Demski. 1993. Clasper control in the round stingray, Urolophus halleri: lower sensorimotor pathways. Env. Biol. Fish. 38: 219–230 (this volume).Google Scholar
  31. Lovejoy, D.A. 1991. Gonadotropin-releasing hormone: structure and function in cartilaginous fish and radiation in the vertebrata. Ph.D. Dissertation, University of Victoria, Victoria. 272pp.Google Scholar
  32. Lovejoy, D.A. & N.M. Sherwood. 1989. Gonadotropin-releasing hormone in ratfish (Hydrolagus colliei): distribution between the sexes and possible relationship with chicken II and salmon II forms. Comp. Biochem. Physiol. 92B: 111–118.Google Scholar
  33. Lovejoy, D.A., B.J. Ashmead, I.R. Coe & N.M. Sherwood. 1992c. Presence of gonadotropin-releasing hormone immunoreactivity in dogfish and skate brains. J. Exp. Zool. 263: 272–283.Google Scholar
  34. Lovejoy, D.A., W.H. Fischer, S. Ngamvongchon, A.G. Craig, C.S. Nahorniak, R.E. Peter, J.E. Rivier & N.M. Sherwood. 1992b. Distinct sequence of gonadotropin-releasing hormone (GnRH) in dogfish brain provides insight into GnRH evolution. Proc. Natl. Acad. Sci. USA 89: 6373–6377.Google Scholar
  35. Lovejoy, D.A., W.H. Fischer, D.B. Parker, J.E. McRory, M. Park, V. Lance, P. Swanson, J.E. Rivier & N.M. Sherwood. 1991b. Primary structure of two forms of GnRH from brains of the American alligator (Alligator mississippiensis). Regulatory Peptides 33: 105–116.Google Scholar
  36. Lovejoy, D.A., N.M. Sherwood, W.H. Fischer, B.C. Jackson, J.E. Rivier & T. Lee. 1991a. Primary structure of gonadotropin-releasing hormone from the brain of a holocephalan (ratfish; Hydrolagus colliei). Gen. Comp. Endocrinol. 82: 152–161.Google Scholar
  37. Lovejoy, D.A., W.K. Stell & N.M. Sherwood. 1992a. Partial characterization of four forms of immunoreactive gonadotropin-releasing hormone in the brain and terminal nerve of the spiny dogfish (Elasmobranchii; Squalus acanthias). Regulatory Peptides 37: 39–48.Google Scholar
  38. Matsuo, H., Y. Baba, R.M.G. Nair, A. Arimura & A.V. Schally. 1971. Structure of porcine LH- and FSH-releasing hormone. I. The proposed amino acid sequence. Biochem. Biophys. Res. Communic. 43: 1334–1339.Google Scholar
  39. Matthews, L.H. 1950. Reproduction in the basking shark, Cetorhinus maximus (Gunnar). Phil. Trans. Roy. Soc. London 234B: 247–316.Google Scholar
  40. Millar, R.P., R.C. deL. Milton, B.K. Follett & J.A. King. 1986. Receptor binding and gonadotropin-releasing activity of a novel chicken gonadotropin-releasing hormone ([His5, Trp7, Tyr8]GnRH) and a D-Arg6 analog. Endocrinology 119: 224–231.Google Scholar
  41. Millem, J.R., C.B. Craig-Veit, T.E. Adams & B.M. Adams. 1989. Avian gonadotropin-releasing hormones I and II in the brain and other tissues in turkey hens. Comp. Biochem. Physiol. 94A: 771–776.Google Scholar
  42. Miyamoto, K., Y. Hasegawa, M. Igarashi, S. Sakakibara, K. Kangawa & H. Matsuo. 1983. Evidence that chicken hypothalamic luteinizing hormone-releasing hormone is (Gln8)-LH-RH. Life Sci. 32: 1341–1347.Google Scholar
  43. Miyamoto, K., Y. Hasegawa, T. Minegishi, M. Nomura, Y. Takahashi, M. Igarashi, K. Kangawa & H. Matsuo. 1982. Isolation and characterization of chicken hypothalamic luteinizing hormone-releasing hormone. Biochem. Biophys. Res. Communic. 107: 820–827.Google Scholar
  44. Miyamoto, K., Y. Hasegawa, M. Nomura, M. Igarashi, K. Kangawa & H. Matsuo. 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. USA 81: 3874–3878.Google Scholar
  45. Ngamvongchon, S., D.A. Lovejoy, W.H. Fischer, A.G. Craig, C.S. Nahorniak, R.E. Peter, J.E. Rivier & N.M. Sherwood. 1992. Primary structures of two forms of gonadotropin-releasing hormone, one distinct and one conserved, from catfish brain. Mol. Cell. Neurosci. 3: 17–22.Google Scholar
  46. Northcutt, R.G. 1977. Elasmobranch central nervous system organization and its possible evolutionary significance. Amer. Zool. 17: 411–429.Google Scholar
  47. Northcutt, R.G. 1981. Evolution of the telencephalon in nonmammals. Ann. Rev. Neurosci. 4: 301–350.Google Scholar
  48. Northcutt, R.G. 1989. Brain variation and phylogenetic trends in elasmobranch fishes. J. Exp. Zool. Suppl. 2: 83–100.Google Scholar
  49. Nozaki, M. 1985. Tissue distribution of hormonal peptides in primitive fishes. pp. 433–454. In: R.E. Foreman, A. Gorbman, J.M. Dodd & R. Olsson (ed.) Evolutionary Biology of Primitive Fishes, Plenum Press, New York.Google Scholar
  50. Nozaki, M. & H. Kobayashi. 1979. Distribution of LHRH-like substance in the vertebrates brain as revealed by immunohistochemistry. Arch. Histol. Japon. 42: 201–219.Google Scholar
  51. Nozaki, M., T. Tsukahara & H. Kobayashi. 1984. Neuronal systems producing LHRH in vertebrates. pp. 3–27. In: K. Ochiai (ed.) Endocrine Correlates of Reproduction, Japan. Sci. Soc. Press, Tokyo.Google Scholar
  52. Pierantoni, R., M. D"Antonio & S. Fasano. 1993. Morpho-functional aspects of the hypothalamus-pituitary-gonadal axis of elasmobranch fishes. Env. Biol. Fish. 38: 187–196 (this volume).Google Scholar
  53. Peter, R.E., C.S. Nahorniak, S. Shih, J.A. King & R.P. Millar. 1987. Activity of position-8-substituted analogs of mammalian gonadotropin-releasing hormone (mGnRH) and chicken and lamprey gonadotropin-releasing hormones in goldfish. Gen. Comp. Endocrinol. 65: 385–393.Google Scholar
  54. Powell, R.C., R.P. Millar & J.A. King. 1986. Diverse molecular forms of gonadotropin-releasing hormone in an elasmobranch and a teleost fish. Gen. Comp. Endocrinol. 63: 77–85.Google Scholar
  55. Rivier, J., C. Rivier, D. Branton, R. Millar, J. Spiess & W. Vale. 1981. HPLC purification of ovine CRF, rat extrahypothalamic brain somatostatin and frog brain GnRH. pp. 771–776. In: D.H. Rich & E. Gross (ed.) Peptides: Synthesis-Structure-Function, Proc 7th American Peptide Symposium, Pierce Chemical Co., Rockford.Google Scholar
  56. Sarkar, D.K., S.A. Chiappa, G. Fink & N.M. Sherwood. 1976. Gonadotropin-releasing hormone surge in proestrus rats. Nature 264: 461–463.Google Scholar
  57. Schaeffer, B. & M. Williams. 1977. Relationships of fossil and living elasmobranchs. Amer. Zool. 17: 293–302.Google Scholar
  58. Sharpe, P.J., R.T. Talbot, G.M. Main, I.C. Dunn, H.M. Fraser & N.S. Huskisson. 1990. Physiological roles of chicken LHRH-I and -II in the control of gonadotropin release in the domestic chicken. J. Endocrinol. 124: 291–299.Google Scholar
  59. Sherwood, N.M. 1986. Evolution of a neuropeptide family: Gonadotropin-releasing hormone. Amer. Zool. 26: 1041–1054.Google Scholar
  60. Sherwood, N.M. & D.A. Lovejoy. 1989. The origin of the mammalian form of GnRH in primitive fishes. Fish Physiol. Biochem. 7: 85–93.Google Scholar
  61. Sherwood, N.M. & S.A. Sower. 1985. A new family member for gonadotropin-releasing hormone. Neuropeptides 6: 205–214.Google Scholar
  62. Sherwood, N.M., S.A. Chiappa, D.K. Sarkar & G. Fink. 1980. Gonadotropin-releasing hormone (GnRH) in pituitary stalk blood from proestrus rats: effects of anesthetics and relationship between stored and released GnRH and luteinizing hormone. Endocrinology 107: 1410–1417.Google Scholar
  63. Sherwood, N.M., L. Eiden, M. Brownstein, J. Spiess, J. Rivier & W. Vale. 1983. Characterization of a teleost gonadotropin-releasing hormone. Proc. Natl. Acad. Sci. USA 80: 2794–2798.Google Scholar
  64. Sherwood, N.M., S.A. Sower, D.R. Marshak, B.A. Fraser & M.J. Brownstein. 1986. Primary structure of a gonadotropin-releasing hormone from lamprey brain. J. Biol. Chem. 261: 4812–4819.Google Scholar
  65. Smeets, W.J.A.J., R. Nieuwenhuys & B.L. Roberts. 1983. The central nervous system of cartilaginous fishes: structure and functional correlations. Springer-Verlag, New York 266 pp.Google Scholar
  66. Sower, S.A., J.A. King, R.P. Millar, N.M. Sherwood & D.R. Marshak. 1987. Comparative biological properties of lamprey gonadotropin-releasing hormone in vertebrates. Endocrinology 120: 773–779.Google Scholar
  67. Sumpter, J.P., B.K. Follett, N. Jenkins & J.M. Dodd. 1978b. Studies on the purification and properties of gonadotropin from ventral lobes of the pituitary gland of the dogfish (Scyliorhinus canicula L.). Gen. Comp. Endocrinol. 36: 264–274.Google Scholar
  68. Sumpter, J.P., N. Jenkins & J.M. Dodd. 1978a. Gonadotrophic hormone in the pituitary gland of the dogfish (Scyliorhinus canicula L.): distribution and physiological significance. Gen. Comp. Endocrinol. 36: 275–285.Google Scholar
  69. Sumpter, J.P., N. Jenkins, R.T. Duggan & J.M. Dodd 1980. The steroidogenic effects of pituitary extracts from a range of elasmobranch species on isolated testicular cells of quail and their neutralisation by a dogfish anti-gonadotropin. Gen. Comp. Endocrinol. 40: 331 (abstract).Google Scholar
  70. Wourms, J. 1977. Reproduction and development in chondrichthyan fishes. Amer. Zool. 17: 379–410.Google Scholar
  71. Wright, D.E. & L.S. Demski. 1991. Gonadotropin hormone-releasing-hormone (GnRH) immunoreactivity in the mesencephalon of sharks and rays. J. Comp. Neurol. 307: 49–56.Google Scholar
  72. Wright, D.E. & L.S. Demski. 1993. Gonadotropin releasing hormone (GnRH) pathways and reproductive control in elasmobranchs. Env. Biol. Fish. 38: 209–218 (this volume).Google Scholar
  73. Yu, K.L., N.M. Sherwood & R.E. Peter. 1988. Differential distribution of two molecular forms of gonadotropin-releasing hormone in discrete areas of goldfish (Carassius auratus). Peptides 9: 625–630.Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • Nancy M. Sherwood
    • 1
  • David A. Lovejoy
    • 2
  1. 1.Biology DepartmentUniversity of VictoriaVictoriaCanada
  2. 2.The Clayton Foundation Laboratories for Peptide Biology, The Salk InstituteLa JollaU.S.A.

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