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The Reproductive Hypothalamic-Pituitary Axis in Lampreys

  • Stacia A. SowerEmail author
Chapter
Part of the Fish & Fisheries Series book series (FIFI, volume 37)

Abstract

This chapter reviews the knowledge of the hypothalamic-pituitary axis in the control of reproduction in lampreys. In gnathostomes, the hypothalamus and pituitary have well-defined roles in the control of reproduction. Up until the late 1970s, it was thought that the agnathan lampreys did not have the same neuroendocrine control of reproduction seen in the jawed vertebrates, in part due to their lack of the typical anatomical hypothalamic-pituitary connection. Since then and during the past three decades, there have been rapid advances in our knowledge of the structure and function of the hypothalamic and pituitary hormones and respective receptors in lampreys. This chapter highlights the delineation of the neuroendocrine system that has come from 30 years of research on the biochemical, molecular, anatomical, immunohistochemical, and functional studies that have established that lampreys, similar to the jawed vertebrates, have a hypothalamic-pituitary-gonadal axis and that there is a high conservation of the mechanisms of gonadotropin-releasing hormone action. These findings also show that the neuroendocrine factors share common functional and developmental features compared to later evolved vertebrates.

Keywords

Estradiol GABA Glycoprotein receptors Gonadotropin Gonadotropin inhibiting hormone Gonadotropin-releasing hormone GnIH GnRH GnRH receptors Hypothalamus Hypothalamic-pituitary-gonadal axis Kisspeptin Neuropeptide Y NPY Pituitary Pituitary glycoprotein hormones Petromyzon marinus RFamide peptides Thyrostimulin 

Notes

Acknowledgments

I dedicate this chapter to Professor Aubrey Gorbman (1914–2003) who laid the groundwork for agnathan comparative endocrinology and inspired many of his former students/postdocs/associates such as Professor Masumi Nozaki, Dr. Erika Plisetskaya, and myself to pursue agnathan endocrinology. The research in this chapter would not have been done without his mentorship and support over many years. It was an honor and privilege to have been his postdoctoral associate and then to continue as collaborators throughout my career. I also particularly thank the Great Lakes Fishery Commission and personnel, particularly Lee H. Hanson at Hammond Bay Biological Station, where many of the studies were done over a 20-year period. Funding has been provided during the past 30 years from the National Science Foundation, Great Lakes Fishery Commission, New Hampshire Agricultural Experiment Station, and National Institutes of Health. I would also like to thank personnel of the New Hampshire Fish and Game. The majority of the cited studies are from the laboratory of Dr. Stacia A. Sower, her colleagues, and students. There are many, many wonderful colleagues (in particular, Professors Hiroshi Kawauchi, Jean Joss, John Youson, Erika Plisetskaya, Masumi Nozaki) former students, postdoctoral research associates, and staff who have made many significant contributions to various aspects of the lamprey research and are greatly thanked for their contributions.

References

  1. Adams BA, Tello JA, Erchegyi J et al (2003) Six novel gonadotropin-releasing hormones are encoded as triplets on each of two genes in the protochordate, Ciona intestinalis. Endocrinology 144:1907–1919PubMedGoogle Scholar
  2. Akutsu S, Takada M, Ohki-Hamazaki H, Murakami S, Arai Y (1992) Origin of luteinizing hormone-releasing hormone (LHRH) neurons in the chick embryo: effect of the olfactory placode ablation. Neurosci Lett 142:241–244PubMedGoogle Scholar
  3. Amano M, Iigo M, Ikuta K et al (2004) Disturbance of plasma melatonin profile by high dose melatonin administration inhibits testicular maturation of precocious male masu salmon. Zool Sci 24:79–85Google Scholar
  4. Anadόn R, Melendez-Ferro M, Perez-Costas E, Pombal MA, Rodicio MC (1998) Centrifugal fibers are the only GABAergic structures of the retina of the larval sea lamprey: an immunocytochemical study. Brain Res 782(1–2):297–302Google Scholar
  5. Andersson E, Borg B, de Leeuw R (1989) Characterization of gonadotropin-releasing hormone binding sites in the pituitary of the three-spined stickleback, Gasterosteus aculeatus. Gen Comp Endocrinol 76:41–45PubMedGoogle Scholar
  6. 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 114:181–190PubMedGoogle Scholar
  7. Anglade I, Mazurais D, Douard V et al (1999) Distribution of glutamic acid decarboxylase mRNA in the forebrain of the rainbow trout as studied by in situ hybridization. J Comp Neurol 410:277–289PubMedGoogle Scholar
  8. Applegate VC (1950) Natural history of the sea lamprey, Petromyzon marinus, in Michigan. US Fish and Wildlife Service Special Scientific Report 55, Washington, DCGoogle Scholar
  9. Arora KK, Sakai A, Catt KJ (1995) Effects of second intracellular loop mutations on signal transduction and internalization of the gonadotropin-releasing hormone receptor. J Biol Chem 270:22820–22826PubMedGoogle Scholar
  10. Arora KK, Cheng Z, Catt KJ (1997) Mutations of the conserved DRS motif in the second intracellular loop of the gonadotropin-releasing hormone receptor affect expression, activation, and internalization. Mol Endocrinol 11:1203–1212PubMedGoogle Scholar
  11. Arora KK, Krsmanovic LZ, Mores N, O’Farrell H, Catt KJ (1998) Mediation of cyclic AMP signaling by the first intracellular loop of the gonadotropin-releasing hormone receptor. J Biol Chem 273:25581–25586PubMedGoogle Scholar
  12. Ascoli M, Fanelli F, Segaloff DL (2002) The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr Rev 23:141–174PubMedGoogle Scholar
  13. Barale E, Fasolo A, Girardi E, Artero C, Franzoni MF (1996) Immunohistochemical investigation of gamma-aminobutyric acid ontogeny and transient expression in the central nervous system of Xenopus laevis tadpoles. J Comp Neurol 368:285–294PubMedGoogle Scholar
  14. Barannikova IA, Boev AA, Arshavskaya SV, Dyubin VP (1995) Feature of hormonal regulation of the reproduction of lamprey, Lampetra fluviatilis, during the final period of the sexual cycle. J Ichthyol 35:184–197Google Scholar
  15. Barreiro-Iglesias A, Villar-Cervino V, AnadÏn R, Rodicio M (2009) Dopamine and γ-aminobutyric acid are colocalized in restricted groups of neurons in the sea lamprey brain: insights into the early evolution of neurotransmitter colocalization in vertebrates. J Anat 215:601–610PubMedCentralPubMedGoogle Scholar
  16. Bennis M, Calas A, Geffard M, Gamrani H (1991) Distribution of GABA immunoreactive systems in the forebrain and midbrain of the chameleon. Brain Res Bull 26:891–898PubMedGoogle Scholar
  17. Bless EP, Westaway WA, Schwarting GA, Tobet SA (2000) Effects of gamma-aminobutyric acid(A) receptor manipulation on migrating gonadotropin-releasing hormone neurons through the entire migratory route in vivo and in vitro. Endocrinology 141:1254–1262PubMedGoogle Scholar
  18. Blomenrohr M, Heding A, Sellar R et al (1999) Pivotal role for the cytoplasmic carboxyl-terminal tail of a nonmammalian gonadotropin-releasing hormone receptor in cell surface expression, ligand binding, and receptor phosphorylation and internalization. Mol Pharmacol 56:1229–1237PubMedGoogle Scholar
  19. Bogerd J, Diepenbroek WB, Hund E et al (2002) Two gonadotropin-releasing hormone receptors in the African catfish: no differences in ligand selectivity, but differences in tissue distribution. Endocrinology 143:4673–4682PubMedGoogle Scholar
  20. Bolduc TG, Sower SA (1992) Changes in brain gonadotropin-releasing hormone, plasma estradiol 17-β, and progesterone during the final reproductive cycle of the female sea lamprey, Petromyzon marinus. J Exp Zool 264:55–63PubMedGoogle Scholar
  21. Bonnard E, Burlet-Schiltz O, Frances B et al (2001) Identification of neuropeptide FF-related peptides in rodent spinal cord. Peptides 22:1085–1092PubMedGoogle Scholar
  22. Bonnard E, Burlet-Schiltz O, Monsarrat B, Girard JP, Zajac JM (2003) Identification of proNeuropeptide FFA peptides processed in neuronal and non-neuronal cells and in nervous tissue. Eur J Biochem 270:4187–4199PubMedGoogle Scholar
  23. Braun CB, Wicht H, Northcutt RGJ (1995) Distribution of gonadotropin-releasing hormone immunoreactivity in the brain of the Pacific hagfish, Eptatretus stouti (Craniata: Myxinoidea). Comp Neurol 353:464–476Google Scholar
  24. Brudel M, Kertscher U, Berger H, Mehlis B (1994) Liquid chromatographic-mass spectrometric studies on the enzymatic degradation of gonadotropin-releasing hormone. J Chromatogr A 661:55–60PubMedGoogle Scholar
  25. Bryan MB, Scott AP, Cerny I, Young BA, Li W (2004) 15α-Hydroxyprogesterone in male sea lampreys, Petromyzon marinus L. Steroids 69:473–481PubMedGoogle Scholar
  26. Bryan MB, Young BA, Close DA et al (2006) Comparison of synthesis of 15α-hydroxylated steroids in males of four North American lamprey species. Gen Comp Endocrinol 146:149–156PubMedGoogle Scholar
  27. Bryan MB, Scott AP, Li W (2008) Sex steroids and their receptors in lampreys. Steroids 73:1–12PubMedGoogle Scholar
  28. Burlet-Schiltz O, Mazarguil H, Sol JC et al (2002) Identification of neuropeptide FF-related peptides in human cerebrospinal fluid by mass spectrometry. FEBS Lett 532:313–318PubMedGoogle Scholar
  29. Butler AB, Hodos W (1996) Comparative vertebrate neuroanatomy: evolution and adaptation. Wiley-Liss, New YorkGoogle Scholar
  30. Butler AB, Hodos W (2005) Comparative vertebrate neuroanatomy: evolution and adaptation, 2nd edn. Wiley, HobokenGoogle Scholar
  31. Byrne B, McGregor A, Taylor PL et al (1999) Isolation and characterisation of the marmoset gonadotrophin releasing hormone receptor: Ser140 of the DRS motif is substituted by Phe. J Endocrinol 163:447–456PubMedGoogle Scholar
  32. Chang JP, Cook AF, Peter RE (1983) Influence of catecholamines on gonadotropin secretion in goldfish, Carassius auratus. Gen Comp Endocrinol 49:22–31PubMedGoogle Scholar
  33. Chartrel N, Dujardin C, Leprince J et al (2002) Isolation, characterization, and distribution of a novel neuropeptide, Rana RFamide (R-RFa), in the brain of the European green frog Rana esculenta. J Comp Neurol 448:111–127PubMedGoogle Scholar
  34. Chartrel N, Dujardin C, Anouar Y et al (2003) Identification of 26RFa, a hypothalamic neuropeptide of the RFamide peptide family with orexigenic activity. Proc Natl Acad Sci U S A 100:15247–15252PubMedCentralPubMedGoogle Scholar
  35. Chen C-C, Fernald RD (2008) GnRH and GnRH receptors: distribution, function and evolution. J Fish Biol 73:1099–1120Google Scholar
  36. Cherubini E, Conti F (2001) Generating diversity at GABAergic synapses. Trends Neurosci 24:155–162PubMedGoogle Scholar
  37. Combarnous Y (1992) Molecular basis of the specificity of binding of glycoprotein hormones to their receptors. Endocr Rev 13:670–691PubMedGoogle Scholar
  38. Conlon JM, Bjornholm B, Jorgensen FS, Youson JH, Schwartz TW (1991) Primary structure and conformational analysis of peptide methionine-tyrosine, a peptide related to neuropeptide Y and peptide YY isolated from lamprey intestine. Eur J Biochem 199:293–298PubMedGoogle Scholar
  39. Conlon JM, Balasubramaniam A, Sower SA (1994) Purification of a neuropeptide Y-related peptide from the brain of the sea lamprey and its effect on steroidogenesis. Regul Pept 50:167–175PubMedGoogle Scholar
  40. Copeland P, Thomas P (1989) Control of gonadotropin release in the Atlantic croaker (Micropogonias undulatus): evidence for lack of dopaminergic inhibition. Gen Comp Endocrinol 74:474–483PubMedGoogle Scholar
  41. Cosowsky L, Lin W, Han Y et al (1997) Influence of subunit interactions on lutropin specificity. Implications for studies of glycoprotein hormone function. J Biol Chem 272:3309–3314PubMedGoogle Scholar
  42. Crim JW (1981) Immunoreactive luteinizing hormone releasing hormone and cerebral spinal fluid-contacting neurons in the preoptic nucleus of lamprey. In: Farner DS, Lederis K (eds) Neurosecretion: molecules, cells and systems. Plenum, London, pp 424–433Google Scholar
  43. Crim J, Urano A, Gorbman A (1979a) lmmunocytochemical studies of luteinizing hormone-releasing hormone in brains of agnathan fishes. II. Patterns of immunoreactivity in larval and maturing Western brook lamprey (Lampetra richardsoni). Gen Comp Endocrinol 38:290–299Google Scholar
  44. Crim JW, Urano A, Gorbman A (1979b) Immunocytochemical studies of luteinizing hormone-releasing hormone in brains of agnathan fishes. I. Comparisons of adult Pacific lamprey (Entosphenus tridentata) and the Pacific hagfish (Eptatretus stouti). Gen Comp Endocrinol 37(3):294–305Google Scholar
  45. Crim LW, St Arnaud R, Lavoie M, Labrie F (1988) A study of LH-RH receptors in the pituitary gland of the winter flounder (Pseudopleuronectes americanus Walbaum). Gen Comp Endocrinol 69:372–377PubMedGoogle Scholar
  46. Crow KD, Wagner GP (2006) What is the role of genome duplication in the evolution of complexity and diversity? Mol Biol Evol 23:887–892PubMedGoogle Scholar
  47. Daukss D, Gazda K, Kosugi T et al (2012) Effects of lamprey PQRFamide peptides on brain gonadotropin-β mRNA expression. Gen Comp Endocrinol 177:215–219PubMedGoogle Scholar
  48. De Andrés M, Anadón R, Manso MJ, González MJ (2002) Distribution of thyrotropin-releasing hormone immunoreactivity in the brain of larval and adult sea lampreys, Petromyzon marinus L. J Comp Neurol 453:323–335Google Scholar
  49. Decatur WA, Hall JA, Smith JJ, Li W, Sower SA (2013) Insight from the lamprey genome: glimpsing early vertebrate development via neuroendocrine-associated genes and shared synteny of gonadotropin-releasing hormone (GnRH). Gen Comp Endocrinol 192:237–245PubMedGoogle Scholar
  50. De Leeuw R, Conn P, Van’t Veer C, Goos H, Van Ordt P (1988) Characterization of the receptor for gonadotropin-releasing hormone in the pituitary of the African catfish, Clarias gariepinus. Fish Physiol Biochem 5:99–107PubMedGoogle Scholar
  51. Deragon KL, Sower SA (1994) Effects of lamprey gonadotropin-releasing hormone-III on steroidogenesis and spermiation in male sea lampreys. Gen Comp Endocrinol 95:363–367PubMedGoogle Scholar
  52. Docker MF (2009) A review of the evolution of nonparasitism in lampreys and an update of the paired species concept. In: Brown LR, Chase SD, Mesa MG, Beamish RJ, Moyle PB (eds) Biology, management, and conservation of lampreys in North America. American Fisheries Society, Symposium 72, Bethesda, pp 71–114Google Scholar
  53. Docker MF, Potter IC (in press) Life history variation in lampreys: alternate feeding and migratory types. In: Docker MF (ed) Lampreys: biology, conservation and control, vol 2. Springer, DordrechtGoogle Scholar
  54. Docker MF, Beamish FWH, Bryan MB, Spice EK (in press) The lamprey gonad. In: Docker MF (ed) Lampreys: biology, conservation and control, vol 2. Springer, DordrechtGoogle Scholar
  55. Doldan MJ, Prego B, Holmqvist BI, de Miguel E (1999) Distribution of GABA-immunolabeling in the early zebrafish (Danio rerio) brain. Eur J Morphol 37:126–129PubMedGoogle Scholar
  56. Domenici L, Waldvogel HJ, Matute C, Streit P (1988) Distribution of GABA-like immunoreactivity in the pigeon brain. Neuroscience 25:931–950PubMedGoogle Scholar
  57. Dos Santos S, Bardet C, Bertrand S et al (2009) Distinct expression patterns of glycoprotein hormone-α2 and -β5 in a basal chordate suggest independent developmental functions. Endocrinology 150:3815–3822PubMedGoogle Scholar
  58. Dos Santos S, Mazan S, Venkatesh B, Cohen-Tannoudji J, Querat B (2011) Emergence and evolution of the glycoprotein hormone and neurotrophin gene families in vertebrates. BMC Evol Biol 11:332PubMedGoogle Scholar
  59. Dufau ML (1998) The luteinizing hormone receptor. Annu Rev Physiol 60:461–496PubMedGoogle Scholar
  60. Eisthen HL, Northcutt RG (1996) Silver lampreys (Ichthyomyzon unicuspis) lack a gonadotropin-releasing hormone- and FMRFamide-immunoreactive terminal nerve. J Comp Neurol 370:159–172PubMedGoogle Scholar
  61. Ekstrom P, Ohlin LM (1995) Ontogeny of GABA-immunoreactive neurons in the central nervous system in a teleost, Gasterosteus aculeatus L. J Chem Neuroanat 9:271–288PubMedGoogle Scholar
  62. Fahien CM, Sower SA (1990) Relationship between brain gonadotropin-releasing hormone and final reproductive period of the adult male sea lamprey, Petromyzon marinus. Gen Comp Endocrinol 80:427–437PubMedGoogle Scholar
  63. Felip A, Zanuy S, Pineda R et al (2009) Evidence for two distinct KiSS genes in non-placental vertebrates that encode kisspeptins with different gonadotropin-releasing activities in fish and mammals. Mol Cell Endocrinol 312:61–71PubMedGoogle Scholar
  64. Fernald RD, White RB (1999) Gonadotropin-releasing hormone genes: phylogeny, structure, and functions. Front Neuroendocrinol 20:224–240PubMedGoogle Scholar
  65. Forey P, Janvier P (1994) Evolution of the early vertebrates. Am Sci 82:554–566Google Scholar
  66. Franzoni MF, Morino P (1989) The distribution of GABA-like-immunoreactive neurons in the brain of the newt, Triturus cristatus carnifex, and the green frog, Rana esculenta. Cell Tissue Res 255:155–166PubMedGoogle Scholar
  67. Freamat M, Sower SA (2008a) A sea lamprey glycoprotein hormone receptor similar with gnathostome thyrotropin hormone receptor. J Mol Endocrinol 41:219–228Google Scholar
  68. Freamat M, Sower SA (2008b) Glycoprotein hormone receptors in sea lamprey Petromyzon marinus. Zool Sci 25:1037–1044Google Scholar
  69. Freamat M, Sower SA (2010) Functional divergence of glycoprotein hormone receptors. Integr Comp Biol 50:110–123PubMedGoogle Scholar
  70. Freamat M, Kawauchi H, Nozaki M, Sower SA (2006) Identification and cloning of a glycoprotein hormone receptor from sea lamprey, Petromyzon marinus. J Mol Endocrinol 37:135–146PubMedGoogle Scholar
  71. Fueshko SM, Key S, Wray S (1998) GABA inhibits migration of luteinizing hormone-releasing hormone neurons in embryonic olfactory explants. J Neurosci 18:2560–2569PubMedGoogle Scholar
  72. Fujimoto M, Takeshita K, Wang X et al (1998) Isolation and characterization of a novel bioactive peptide, Carassius RFamide (C-RFa), from the brain of the Japanese crucian carp. Biochem Biophys Res Commun 242:436–440PubMedGoogle Scholar
  73. Fukamachi S, Meyer A (2007) Evolution of receptors for growth hormone and somatolactin in fish and land vertebrates: lessons from the lungfish and sturgeon orthologues. J Mol Evol 65:359–372PubMedGoogle Scholar
  74. Fukayama S, Takahashi H (1985) Changes in serum levels of estradiol-17b and testosterone in the Japanese river lamprey, Lampetra japonica, in the course of sexual maturation. Bull Fac Fish Hokkaido Univ 36:163–169Google Scholar
  75. Fukusumi S, Habata Y, Yoshida H et al (2001) Characteristics and distribution of endogenous RFamide-related peptide-1. Biochim Biophys Acta 1540:221–232PubMedGoogle Scholar
  76. Fukusumi S, Yoshida H, Fujii R et al (2003) A new peptidic ligand and its receptor regulating adrenal function in rats. J Biol Chem 278:46387–46395PubMedGoogle Scholar
  77. Gazourian L, Sower SA (1994) Pituitary responsiveness to perifused lamprey GnRH-I or -III analogs in the adult sea lamprey, Petromyzon marinus. Am Zool 34:23AGoogle Scholar
  78. Gazourian L, Deragon KL, Chase CF et al (1997) Characteristics of GnRH binding in the gonads and effects of lamprey GnRH-I and -III on reproduction in the adult sea lamprey. Gen Comp Endocrinol 108:327–339PubMedGoogle Scholar
  79. Gazourian L, Evans EL, Hanson L, Chase CF, Sower SA (2000) The effects of lamprey GnRH-I, III and analogs on steroidogenesis in the sea lamprey (Petromyzon marinus). Aquaculture 188:147–165Google Scholar
  80. Gorbman A (1965) Vascular relations between the neurohypophysis and adenohypophysis of cyclostomes and the problem of evolution of hypothalamic neuroendrocrine control. Arch Anat Microsc Morphol Exp 54:163–194PubMedGoogle Scholar
  81. Gorbman A, Dickhoff WW (1978) Endocrine control of reproduction in hagfish. In: Gaillard PJ, Boer HH (eds) Comparative endocrinology. Elsevier, Amsterdam, pp 49–54Google Scholar
  82. Gorbman A, Sower SA (2003) Evolution of the role of GnRH in animal (metazoan) biology. Gen Comp Endocrinol 134:207–213PubMedGoogle Scholar
  83. Gorbman A, Dickoff WW, Vigna SR, Clark NB, Ralph CL (1983) Comparative endocrinology. Wiley, New YorkGoogle Scholar
  84. Gore AC (2002) GnRH: the master molecule of reproduction. Kluwer, New YorkGoogle Scholar
  85. Goren A, Zohar Y, Fridkin M, Elhanati E, Koch Y (1990) Degradation of gonadotropin-releasing hormones in the gilthead seabream, Sparus aurata. I. Cleavage of native salmon GnRH and mammalian LHRH in the pituitary. Gen Comp Endocrinol 79:291–305PubMedGoogle Scholar
  86. Grober MS, Myers TR, Marchaterre MA, Bass AH, Myers DA (1995) Structure, localization, and molecular phylogeny of a GnRH cDNA from a paracanthopterygian fish, the plainfin midshipman (Porichthys notatus). Gen Comp Endocrinol 99:85–99PubMedGoogle Scholar
  87. Grosse R, Roelle S, Herrlich A, Hohn J, Gudermann T (2000) Epidermal growth factor receptor tyrosine kinase mediates Ras activation by gonadotropin-releasing hormone. J Biol Chem 275:12251–12260PubMedGoogle Scholar
  88. Grossmann M, Weintraub BD, Szkudlinski MW (1997) Novel insights into the molecular mechanisms of human thyrotropin action: structural, physiological, and therapeutic implications for the glycoprotein hormone family. Endocr Rev 18:476–501PubMedGoogle Scholar
  89. Guilgur LG, Moncaut NP, Canario AV, Somoza GM (2006) Evolution of GnRH ligands and receptors in gnathostomata. Comp Biochem Physiol A Mol Integr Physiol 144:272–283PubMedGoogle Scholar
  90. Guillemin R (1978) Peptides in the brain: the new endocrinology of the neuron. Science 202:390–402PubMedGoogle Scholar
  91. Hagelin L-O, Steffner N (1958) Notes on the spawning habits of the river lamprey (Petromyzon fluviatilis). Oikos 9:221–238Google Scholar
  92. Hall JA, Decatur WA, Daukss DM et al (2013) Expression of three GnRH receptors in specific tissues in male and female sea lampreys Petromyzon marinus at three distinct life stages. Front Neurosci 28:7–88Google Scholar
  93. Hardisty MW, Potter IC, Hilliard RW (1986) Gonadogenesis and sex differentiation in the southern hemisphere lamprey, Geotria australis. J Zool Lond (A) 209:477–499Google Scholar
  94. Harvey B, Carolsfeld J (1993) Induced breeding in tropical fish culture. International Development Research Centre, OttawaGoogle Scholar
  95. Heding A, Vrecl M, Bogerd J et al (1998) Gonadotropin-releasing hormone receptors with intracellular carboxyl-terminal tails undergo acute desensitization of total inositol phosphate production and exhibit accelerated internalization kinetics. J Biol Chem 273:11472–11477PubMedGoogle Scholar
  96. Heimberg A, Cowper-Sallari R, Sémon M, Donoghue P, Peterson K (2010) microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc Natl Acad Sci U S A 107:19379–19383PubMedCentralPubMedGoogle Scholar
  97. Heinig JA, Keeley FW, Robson P, Sower SA, Youson JH (1995) The appearance of proopiomelanocortin early in vertebrate evolution: cloning and sequencing of POMC from a lamprey pituitary cDNA library. Gen Comp Endocrinol 99:137–144PubMedGoogle Scholar
  98. Hinuma S, Habata Y, Fujii R et al (1998) A prolactin-releasing peptide in the brain. Nature 393:272–276PubMedGoogle Scholar
  99. Hislop J, Caunt C, Sedgley K et al (2005) Internalization of gonadotropin-releasing hormone receptors (GnRHRs): does arrestin binding to the C-terminal tail target GnRHRs for dynamin-dependent internalization? J Mol Endocrinol 35:177–189PubMedGoogle Scholar
  100. Ho SM, Press D, Liang LC, Sower S (1987) Identification of an estrogen receptor in the testis of the sea lamprey, Petromyzon marinus. Gen Comp Endocrinol 67:119–125PubMedGoogle Scholar
  101. Holland PW, Garcia-Fernandez J, Williams NA, Sidow A (1994) Gene duplications and the origins of vertebrate development. Development 1994(Suppl):125–133Google Scholar
  102. Huhtaniemi I (2005) Focus on gonadotrophin signalling. Reproduction 130:261–262PubMedGoogle Scholar
  103. Illing N, Troskie BE, Nahorniak CS et al (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 96:2526–2531PubMedCentralPubMedGoogle Scholar
  104. Jackson IM, Reichlin S (1977) Thyrotropin-releasing hormone: abundance in the skin of the frog, Rana pipiens. Science 198:414–415PubMedGoogle Scholar
  105. Jang M-H, Lucas MC (2005) Reproductive ecology of the river lamprey. J Fish Biol 66:499–512Google Scholar
  106. Janvier P (2010) microRNAs revive old views about jawless vertebrate divergence and evolution. Proc Natl Acad Sci U S A 107:19137–19138PubMedCentralPubMedGoogle Scholar
  107. Joseph NT, Aquilina-Beck A, MacDonald C et al (2012) Molecular cloning and pharmacological characterization of two novel GnRH receptors in the lamprey (Petromyzon marinus). Endocrinology 153:3345–3356PubMedCentralPubMedGoogle Scholar
  108. Kah O, Dufour S (2010) Conserved and divergent features of reproductive neuroendocrinology in teleost fishes. In: Norris DO, Lopez KH (eds) Hormones and reproduction of vertebrates, vol 1, fishes. Academic Press, Boston, pp 15–42Google Scholar
  109. Kah O, Dubourg P, Martinoli MG et al (1987) Central GABAergic innervation of the pituitary in goldfish: a radioautographic and immunocytochemical study at the electron microscope level. Gen Comp Endocrinol 67:324–332PubMedGoogle Scholar
  110. Kah O, Trudeau VL, Sloley BD et al (1992) Influence of GABA on gonadotrophin release in the goldfish. Neuroendocrinology 55:396–404PubMedGoogle Scholar
  111. Kah O, Lethimonier C, Somoza G et al (2007) GnRH and GnRH receptors in metazoa: a historical, comparative, and evolutive perspective. Gen Comp Endocrinol 153:346–364PubMedGoogle Scholar
  112. Kauffman AS, Rissman EF (2004a) A critical role for the evolutionarily conserved gonadotropin-releasing hormone II: mediation of energy status and female sexual behavior. Endocrinology 145:3639–3646Google Scholar
  113. Kauffman AS, Rissman EF (2004b) The evolutionarily conserved gonadotropin-releasing hormone II modifies food intake. Endocrinology 145:686–691Google Scholar
  114. Kavanaugh SI, Nozaki M, Sower SA (2008) Origins of gonadotropin-releasing hormone (GnRH) in vertebrates: identification of a novel GnRH in a basal vertebrate, the sea lamprey. Endocrinology 149:3860–3869PubMedCentralPubMedGoogle Scholar
  115. Kawauchi H, Sower SA (2006) The dawn and evolution of hormones in the adenohypophysis. Gen Comp Endocrinol 148:3–14PubMedGoogle Scholar
  116. Kawauchi H, Suzuki K, Itho H et al (1989) The duality of teleost gonadotropins. Fish Physiol Biochem 7:29–38PubMedGoogle Scholar
  117. Kawauchi H, Suzuki K, Yamazaki T et al (2002) Identification of growth hormone in the sea lamprey, an extant representative of a group of the most ancient vertebrates. Endocrinology 143:4916–4921PubMedGoogle Scholar
  118. Kim DK, Cho EB, Moon MJ et al (2011) Revisiting the evolution of gonadotropin-releasing hormones and their receptors in vertebrates: secrets hidden in genomes. Gen Comp Endocrinol 170:68–78PubMedGoogle Scholar
  119. King JA, Millar RP (1991) Gonadotropin-releasing hormones. In: Pang PKT, Schreibman MP (eds) Vertebrate endocrinology: fundamentals and biomedical implications, vol 4. Academic Press, San Diego, pp 1–32Google Scholar
  120. King JC, Sower SA, Anthony EL (1988) Neuronal systems immunoreactive with antiserum to lamprey gonadotropin- releasing hormone in the brain of Petromyzon marinus. Cell Tissue Res 253:1–8PubMedGoogle Scholar
  121. Kitahashi T, Ogawa S, Parhar IS (2009) Cloning and expression of kiss2 in the zebrafish and medaka. Endocrinology 150:821–831PubMedGoogle Scholar
  122. Kleinau G, Krause G (2009) Thyrotropin and homologous glycoprotein hormone receptors: structural and functional aspects of extracellular signaling mechanisms. Endocr Rev 30:133–151PubMedGoogle Scholar
  123. Knox CJ, Boyd SK, Sower SA (1994) Characterization and localization of gonadotropin-releasing hormone receptors in the adult female sea lamprey, Petromyzon marinus. Endocrinology 134:492–498PubMedGoogle Scholar
  124. Koda A, Ukena K, Teranishi H et al (2002) A novel amphibian hypothalamic neuropeptide: isolation, localization, and biological activity. Endocrinology 143:411–419PubMedGoogle Scholar
  125. Kosugi T, Sower SA (2010) A role of Histidine151 in the lamprey gonadotropin-releasing hormone receptor-1 (lGnRHR-1): functional insight of diverse amino acid residues in the position of Tyr of the DRY motif in GnRHR from an ancestral type II receptor. Gen Comp Endocrinol 166:498–503PubMedCentralPubMedGoogle Scholar
  126. Kotani M, Detheux M, Vandenbogaerde A et al (2001) The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 276:34631–34636PubMedGoogle Scholar
  127. Kuo MW, Lou SW, Postlethwait J, Chung BC (2005) Chromosomal organization, evolutionary relationship, and expression of zebrafish GnRH family members. J Biomed Sci 12:629–639PubMedGoogle Scholar
  128. Kuraku S, Meyer A, Kuratani S (2009) Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after? Mol Biol Evol 26:47–59PubMedGoogle Scholar
  129. Kuratani S, Kuraku S, Murakami Y (2002) Lamprey as an evo-devo model: lessons from comparative embryology and molecular phylogenetics. Genesis 34:175–183PubMedGoogle Scholar
  130. Kusano K, Fueshko S, Gainer H, Wray S (1995) Electrical and synaptic properties of embryonic luteinizing hormone- releasing hormone neurons in explant cultures. Proc Natl Acad Sci U S A 92:3918–3922PubMedCentralPubMedGoogle Scholar
  131. Lagios MD (1970) The median eminence of the bowfin, Amia calva L. Gen Comp Endocrinol 15:453–463PubMedGoogle Scholar
  132. Larhammar D (1996) Evolution of neuropeptide Y, peptide YY and pancreatic polypeptide. Regul Pept 62:1–11PubMedGoogle Scholar
  133. Lariviere K, MacEachern L, Greco V et al (2002) GAD65 and GAD67 isoforms of the glutamic acid decarboxylase gene originated before the divergence of cartilaginous fishes. Mol Biol Evol 19:2325–2329PubMedGoogle Scholar
  134. Larsen LO (1965) Effects of hypophysectomy in the cyclostome, Lampetra fluviatilis (L.) Gray. Gen Comp Endocrinol 5:16–30Google Scholar
  135. Larsen LO (1973) Development in adult, freshwater river lampreys and its hormonal control: starvation, sexual maturation and natural death. PhD thesis, University of Copenhagen, CopenhagenGoogle Scholar
  136. Lauder JM (1993) Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci 16:233–240PubMedGoogle Scholar
  137. Lauder JM, Han VK, Henderson P, Verdoorn T, Towle AC (1986) Prenatal ontogeny of the GABAergic system in the rat brain: an immunocytochemical study. Neuroscience 19:465–493PubMedGoogle Scholar
  138. Lee YR, Tsunekawa K, Moon MJ et al (2009) Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology 150:2837–2846PubMedGoogle Scholar
  139. Leranth C, MacLusky NJ, Sakamoto H, Shanabrough M, Naftolin F (1985) Glutamic acid decarboxylase-containing axons synapse on LHRH neurons in the rat medial preoptic area. Neuroendocrinology 40:536–539PubMedGoogle Scholar
  140. Linville JE, Hanson LH, Sower SA (1987) Endocrine events associated with spawning behavior in the sea lamprey (Petromyzon marinus). Horm Behav 21:105–117PubMedGoogle Scholar
  141. Liu F, Usui I, Evans LG et al (2002) Involvement of both Gq/11 and Gs proteins in gonadotropin-releasing hormone receptor-mediated signaling in LβT2 cells. J Biol Chem 277:32099–32108PubMedCentralPubMedGoogle Scholar
  142. Lovejoy DA, Fischer WH, Ngamvongchon S et al (1992) Distinct sequence of gonadotropin-releasing hormone (GnRH) in dogfish brain provides insight into GnRH evolution. Proc Natl Acad Sci U S A 89:6373–6377PubMedCentralPubMedGoogle Scholar
  143. MacIntyre JK, Chase C, Tobet SA, Sower SA (1997) The interrelationship of PMY, GABA, and GnRH in the sea lamprey, Petromyzon marinus. XIII Int Congr Comp Endocrinol 1:721–724Google Scholar
  144. Manion PJ, Hanson LH (1980) Spawning behavior and fecundity of lampreys from the upper three Great Lakes. Can J Fish Aquat Sci 37:1635–1640Google Scholar
  145. Marchant TA, Chang JP, Nahorniak CS, Peter RE (1989) Evidence that gonadotropin-releasing hormone also functions as a growth hormone-releasing factor in the goldfish. Endocrinology 124:2509–2518PubMedGoogle Scholar
  146. Martinoli M, Dubourg P, Geffard M, Calas A, Kah O (1990) Distribution of GABA-immunoreactive neurons in the forebrain of the goldfish, Carassius auratus. Cell Tissue Res 260:77–84PubMedGoogle Scholar
  147. Materne OL, Gazourian L, Chase C et al (1997) Characterization of the gonadotropin-releasing hormone binding sites in the pituitary and gonads of the sexually maturing adult lamprey. XIII Int Congr Comp Endocrinol 1:743–746Google Scholar
  148. McArdle CA, Davidson JS, Willars GB (1999) The tail of the gonadotrophin-releasing hormone receptor: desensitization at, and distal to, G protein-coupled receptors. Mol Cell Endocrinol 151:129–136PubMedGoogle Scholar
  149. Medina M, Reperant J, Dufour S et al (1994) The distribution of GABA-immunoreactive neurons in the brain of the silver eel (Anguilla anguilla L.). Anat Embryol 189:25–39PubMedGoogle Scholar
  150. Melendez-Ferro M, Perez-Costas E, Rodriguez-Munoz R et al (2001) GABA immunoreactivity in the olfactory bulbs of the adult sea lamprey Petromyzon marinus L. Brain Res 893:253–260PubMedGoogle Scholar
  151. Melendez-Ferro M, Villar-Cheda B, Manoel Abalo X et al (2002) Early development of the retina and pineal complex in the sea lamprey: comparative immunocytochemical study. J Comp Neurol 442:250–265PubMedGoogle Scholar
  152. Mesa M, Bayer J, Bryan M, Sower S (2010) Annual sex steroid and other physiological profiles of Pacific lampreys (Entosphenus tridentatus). Comp Biochem Physiol A 155:56–63Google Scholar
  153. Millar RP, King JA (1987) Structural and functional evolution of gonadotropin-releasing hormone. Int Rev Cytol 106:149–182PubMedGoogle Scholar
  154. Millar R, Lowe S, Conklin D et al (2001) A novel mammalian receptor for the evolutionarily conserved type II GnRH. Proc Natl Acad Sci U S A 98:9636–9641PubMedCentralPubMedGoogle Scholar
  155. Millar RP, Lu ZL, Pawson AJ et al (2004) Gonadotropin-releasing hormone receptors. Endocr Rev 25:235–275PubMedGoogle Scholar
  156. Moriyama S, Ito T, Takahashi A et al (2002) A homolog of mammalian PRL-releasing peptide (fish arginyl-phenylalanyl-amide peptide) is a major hypothalamic peptide of PRL release in teleost fish. Endocrinology 143:2071–2079PubMedGoogle Scholar
  157. Moyle WR, Xing Y, Lin W et al (2004) Model of glycoprotein hormone receptor ligand binding and signaling. J Biol Chem 279:44442–44459PubMedGoogle Scholar
  158. Moyle WR, Lin W, Myers RV et al (2005) Models of glycoprotein hormone receptor interaction. Endocrine 26:189–205PubMedGoogle Scholar
  159. Murakami S, Arai Y (1994) Direct evidence for the migration of LHRH neurons from the nasal region to the forebrain in the chick embryo: a carbocyanine dye analysis. Neurosci Res 19:331–338PubMedGoogle Scholar
  160. Murakami S, Kikuyama S, Arai Y (1992) The origin of the luteinizing hormone-releasing hormone (LHRH) neurons in newts (Cynops pyrrhogaster): the effect of olfactory placode ablation. Cell Tissue Res 269:21–27PubMedGoogle Scholar
  161. Muske LE (1993) Evolution of gonadotropin-releasing hormone (GnRH) neuronal system. Brain Behav Evol 42:224–230Google Scholar
  162. Myburgh DB, Millar RP, Hapgood JP (1998) Alanine-261 in intracellular loop III of the human gonadotropin-releasing hormone receptor is crucial for G-protein coupling and receptor internalization. Biochem J 331:893–896PubMedCentralPubMedGoogle Scholar
  163. Nakabayashi K, Matsumi H, Bhalla A et al (2002) Thyrostimulin, a heterodimer of two new human glycoprotein hormone subunits, activates the thyroid-stimulating hormone receptor. J Clin Invest 109:1445–1452PubMedCentralPubMedGoogle Scholar
  164. Near TJ (2009) Conflict and resolution between phylogenies inferred from molecular and phenotypic data sets for hagfish, lampreys, and gnathostomes. J Exp Zool Mol Dev Evol 312B:749–761Google Scholar
  165. Neill JD, Duck LW, Sellers JC, Musgrove LC (2001) A gonadotropin-releasing hormone (GnRH) receptor specific for GnRH II in primates. Biochem Biophys Res Commun 282:1012–1018PubMedGoogle Scholar
  166. Nieuwenhuys R (1977) The brain of the lamprey in a comparative perspective. Ann N Y Acad Sci 299:97–145PubMedGoogle Scholar
  167. Norgren RB, Jr, Gao C (1994) LHRH neuronal subtypes have multiple origins in chickens. Dev Biol 165:735–738PubMedGoogle Scholar
  168. Norris DO, Carr JA (2013) Vertebrate endocrinology, 5th edn. Academic Press, WalthamGoogle Scholar
  169. Northcutt RG, Muske LE (1994) Multiple embryonic origins of gonadotropin-releasing hormone (GnRH) immunoreactive neurons. Dev Brain Res 78:279–290Google Scholar
  170. Nozaki M, Gorbman A (1984) Distribution of immunoreactive sites for several components of pro-opiocortin in the pituitary and brain of adult lampreys, Petromyzon marinus and Entosphenus tridentatus. Gen Comp Endocrinol 53:335–352PubMedGoogle Scholar
  171. Nozaki M, Kobayashi H (1979) Distribution of LHRH-like substance in the vertebrate brain as revealed by immunohistochemistry. Arch Histol Jpn 42:201–219PubMedGoogle Scholar
  172. Nozaki M, Fernholm B, Kobayashi H (1975) Ependymal absorption of peroxidase in the third ventricle of the hagfish Eptatretus burgeri (Girard). Acta Zool 56:265–269Google Scholar
  173. Nozaki M, Tsukahara T, Kobayashi H (1984) An immunocytological study of the distribution of neuropeptides in the brain of fish. Biomed Res-Tokyo 4(Suppl S):135–145Google Scholar
  174. Nozaki M, Gorbman A, Sower SA (1994) Diffusion between the neurohypophysis and the adenohypophysis of lampreys, Petromyzon marinus. Gen Comp Endocrinol 96:385–391PubMedGoogle Scholar
  175. Nozaki M, Takahashi A, Amemiya Y, Kawauchi H, Sower SA (1995) Distribution of lamprey adrenocorticotropin and melanotropins in the pituitary of the adult sea lamprey, Petromyzon marinus. Gen Comp Endocrinol 98:147–156PubMedGoogle Scholar
  176. Nozaki M, Ominato K, Takahashi A, Kawauchi H, Sower SA (1999) Possible gonadotropin cells in the lamprey pituitary: colocalization of mammalian LH-like immunoreactivity and glycoconjugate in adult sea lampreys (Petromyzon marinus). Gen Comp Endocrinol 113:23–31PubMedGoogle Scholar
  177. Nozaki M, Ominato K, Gorbman A, Sower SA (2000) The distribution of lamprey GnRH-III in brains of adult sea lampreys (Petromyzon marinus). Gen Comp Endocrinol 118:57–67PubMedGoogle Scholar
  178. 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 Biochem Mol Biol 129:303–309PubMedGoogle Scholar
  179. Nozaki M, Ominato K, Shimotani T et al (2008) Identity and distribution of immunoreactive adenohypophysial cells in the pituitary during the life cycle of sea lampreys, Petromyzon marinus. Gen Comp Endocrinol 155:403–412PubMedGoogle Scholar
  180. Oh DY, Song JA, Moon JS et al (2005) Membrane-proximal region of the carboxyl terminus of the gonadotropin-releasing hormone receptor (GnRHR) confers differential signal transduction between mammalian and nonmammalian GnRHRs. Mol Endocrinol 19:722–731PubMedGoogle Scholar
  181. Ohno S (1970) Evolution by gene duplication. Allen and Unwin Springer, New YorkGoogle Scholar
  182. Ohtaki T, Shintani Y, Honda S et al (2001) Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 411:613–617PubMedGoogle Scholar
  183. Okubo K, Nagahama Y (2008) Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiol 193:3–15Google Scholar
  184. Okubo K, Nagata S, Ko R et al (2001) Identification and characterization of two distinct GnRH receptor subtypes in a teleost, the medaka Oryzias latipes. Endocrinology 142:4729–4739PubMedGoogle Scholar
  185. Osugi T, Ukena K, Bentley GE et al (2004) Gonadotropin-inhibitory hormone in Gambel’s white-crowned sparrow (Zonotrichia leucophrys gambelii): cDNA identification, transcript localization and functional effects in laboratory and field experiments. J Endocrinol 182:33–42PubMedGoogle Scholar
  186. Osugi T, Ukena K, Sower SA, Kawauchi H, Tsutsui K (2006) Evolutionary origin and divergence of PQRFamide peptides and LPXRFamide peptides in the RFamide peptide family: insights from novel lamprey RFamide peptides. FEBS J 273:1731–1743PubMedGoogle Scholar
  187. Osugi T, Daukss D, Gazda K et al (2012) Evolutionary origin of the structure and function of gonadotropin-inhibitory hormone: insights from lampreys. Endocrinology 153:2362–2374PubMedGoogle Scholar
  188. Ota KG, Kuraku S, Kuratani S (2007) Hagfish embryology with reference to the evolution of the neural crest. Nature 446:672–675PubMedGoogle Scholar
  189. Pagelson G, Zohar Y (1992) Characterization of gonadotropin-releasing hormone binding to pituitary receptors in the gilthead seabream (Sparus aurata). Biol Reprod 47:1004–1008PubMedGoogle Scholar
  190. Paris M, Pettersson K, Schubert M et al (2008) An amphioxus orthologue of the estrogen receptor that does not bind estradiol: insights into estrogen receptor evolution. Curr Biol 18:825–830PubMedGoogle Scholar
  191. Pawson AJ, Katz A, Sun YM et al (1998) Contrasting internalization kinetics of human and chicken gonadotropin- releasing hormone receptors mediated by C-terminal tail. J Endocrinol 156:R9–R12PubMedGoogle Scholar
  192. Peter RE, Paulencu CR (1980) Involvement of the preoptic region in gonadotropin release-inhibition in goldfish, Carassius auratus. Neuroendocrinology 31:133–141PubMedGoogle Scholar
  193. Peter RE, Crim LW, Goos H, Crim JW (1978) Lesioning studies on the gravid goldfish: neuroendocrine regulation of ovulation. Gen Comp Endocrinol 35:391–401PubMedGoogle Scholar
  194. Peter RE, Yu KL, Marchant TA, Rosenblum PM (1990) Direct neural regulation of the teleost adenophypophysis. J Exp Zool Suppl 4:84–89Google Scholar
  195. Pombal MA, Puelles L (1999) Prosomeric map of the lamprey forebrain based on calretinin immunocytochemistry, Nissl stain, and ancillary markers. J Comp Neurol 414:391–422PubMedGoogle Scholar
  196. Pombal MA, El Manira A, Grillner S (1997) Organization of the lamprey striatum—transmitters and projections. Brain Res 766:249–254PubMedGoogle Scholar
  197. Quérat B, Sellouk A, Salmon C (2000) Phylogenetic analysis of the vertebrate glycoprotein hormone family including new sequences of sturgeon (Acipenser baeri) β-subunits of the two gonadotropins and the thyroid-stimulating hormone. Biol Reprod 63:222–228PubMedGoogle Scholar
  198. Quérat B, Tonnerre-Doncarli C, Genies F, Salmon C (2001) Duality of gonadotropins in gnathostomes. Gen Comp Endocrinol 124:308–314PubMedGoogle Scholar
  199. Quérat B, Arai Y, Henry A et al (2004) Pituitary glycoprotein hormone β subunits in the Australian lungfish and estimation of the relative evolution rate of these subunits within vertebrates. Biol Reprod 70:356–363PubMedGoogle Scholar
  200. Reed KL, MacIntyre JK, Tobet SA et al (2002) The spatial relationship of gamma-aminobutyric acid (GABA) neurons and gonadotropin-releasing hormone (GnRH) neurons in larval and adult sea lamprey, Petromyzon marinus. Brain Behav Evol 60:1–12PubMedGoogle Scholar
  201. Rissman EF, Alones VE, Craig-Veit CB, Millam JR (1995) Distribution of chicken-II gonadotropin-releasing hormone in mammalian brain. J Comp Neurol 357:524–531PubMedGoogle Scholar
  202. Roa J, Castellano JM, Navarro VM et al (2009) Kisspeptins and the control of gonadotropin secretion in male and female rodents. Peptides 30:57–66PubMedGoogle Scholar
  203. Roberts A, Dale N, Ottersen OP, Storm-Mathisen J (1987) The early development of neurons with GABA immunoreactivity in the CNS of Xenopus laevis embryos. J Comp Neurol 261:435–449PubMedGoogle Scholar
  204. Root AR, Sanford JD, Kavanaugh SI, Sower SA (2004) In vitro and in vivo effects of GABA, muscimol, and bicuculline on lamprey GnRH concentration in the brain of the sea lamprey (Petromyzon marinus). Comp Biochem Physiol A Mol Integr Physiol 138:493–501PubMedGoogle Scholar
  205. Root AR, Nucci NV, Sanford JD et al (2005) In situ characterization of gonadotropin-releasing hormone-I, -III, and glutamic acid decarboxylase expression in the brain of the sea lamprey, Petromyzon marinus. Brain Behav Evol 65:60–70PubMedGoogle Scholar
  206. Rovati GE, Capra V, Neubig RR (2007) The highly conserved DRY motif of class A G protein-coupled receptors: beyond the ground state. Mol Pharmacol 71:959–964PubMedGoogle Scholar
  207. Rowe ML, Elphick MR (2012) The neuropeptide transcriptome of a model echinoderm, the sea urchin Strongylocentrous purpuratus. Gen Comp Endocrinol 179:331–344PubMedGoogle Scholar
  208. Satake H, Hisada M, Kawada T et al (2001) Characterization of a cDNA encoding a novel avian hypothalamic neuropeptide exerting an inhibitory effect on gonadotropin release. Biochem J 354:379–385PubMedCentralPubMedGoogle Scholar
  209. Sawada K, Ukena K, Satake H et al (2002) Novel fish hypothalamic neuropeptide. Eur J Biochem 269:6000–6008PubMedGoogle Scholar
  210. Schally AV (1978) Aspects of hypothalamic regulation of the pituitary gland. Science 202:18–28PubMedGoogle Scholar
  211. Schwanzel-Fukuda M, Pfaff DW (1989) Origin of luteinizing hormone-releasing hormone neurons. Nature 338:161–164PubMedGoogle Scholar
  212. Seale AP, Itoh T, Moriyama S et al (2002) Isolation and characterization of a homologue of mammalian prolactin-releasing peptide from the tilapia brain and its effect on prolactin release from the tilapia pituitary. Gen Comp Endocrinol 125:328–339PubMedGoogle Scholar
  213. Seminara S, Crowley J, WF (2008) Kisspeptin and GPR54: discovery of a novel pathway in reproduction. J Neuroendocrinol 20:727–731PubMedCentralPubMedGoogle Scholar
  214. Seminara S, Messager S, Chatzidaki E et al (2003) The GPR54 gene as a regulator of puberty. N Engl J Med 349:16114–16127Google Scholar
  215. Seong JY, Wang L, Oh da Y et al (2003) Ala/Thr201 in extracellular loop 2 and Leu/Phe290 in transmembrane domain 6 of type 1 frog gonadotropin-releasing hormone receptor confer differential ligand sensitivity and signal transduction. Endocrinology 144:454–466PubMedGoogle Scholar
  216. Sherwood NM, Sower SA, Marshak DR, Fraser BA, Brownstein MJ (1986) Primary structure of gonadotropin-releasing hormone in lamprey brain. J Biol Chem 15:4812–4819Google Scholar
  217. Sidow A (1996) Gen(om)e duplications in the evolution of early vertebrates. Curr Opin Genet Dev 6:715–722PubMedGoogle Scholar
  218. Silver MR, Sower SA (2006) Functional characterization and kinetic studies of an ancestral lamprey GnRH-III selective type II GnRH receptor from the sea lamprey, Petromyzon marinus. J Mol Endocrinol 36:601–610PubMedGoogle Scholar
  219. Silver MR, Kawauchi H, Nozaki M, Sower SA (2004) Cloning and analysis of the lamprey GnRH-III cDNA from eight species of lamprey representing the three families of Petromyzoniformes. Gen Comp Endocrinol 139:85–94PubMedGoogle Scholar
  220. Silver MR, Nucci NV, Root AR, Reed KL, Sower SA (2005) Cloning and characterization of a functional type II gonadotropin-releasing hormone receptor with a lengthy carboxy-terminal tail from an ancestral vertebrate, the sea lamprey. Endocrinology 146:3351–3361PubMedGoogle Scholar
  221. Sloley BD, Kah O, Trudeau VL, Dulka JG, Peter RE (1992) Amino acid neurotransmitters and dopamine in brain and pituitary of the goldfish: involvement in the regulation of gonadotropin secretion. J Neurochem 58:2254–2262PubMedGoogle Scholar
  222. Smith JJ, Kuraku S, Holt C et al (2013) Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat Genet 45:415–421PubMedCentralPubMedGoogle Scholar
  223. Sower SA (1987) Biological action of lamprey gonadotropin-releasing hormone in lampreys. Proceedings of the 3rd international symposium of the reproductive physiology of fish, St. John’s, NL, pp 40–41Google Scholar
  224. Sower SA (1989) Effects of lamprey gonadotropin-releasing hormone and analogs on steroidogenesis and spermiation in male sea lampreys. Fish Physiol Biochem 7:101–107PubMedGoogle Scholar
  225. Sower SA (1990) Neuroendocrine control of reproduction in lampreys. Fish Phys Biochem 8:365–374Google Scholar
  226. Sower SA (1997) Evolution of GnRH in fish of ancient origins. In: Parhar IS, Sakuma Y (eds) GnRH neurons: gene to behavior. Brain Shuppan, TokyoGoogle Scholar
  227. Sower SA (2003) The endocrinology of reproduction in lampreys and applications for male lamprey sterilization. J Great Lakes Res 29(Suppl 1):50–65Google Scholar
  228. Sower SA, Baron MP (2011) The interrelationship of estrogen receptor and GnRH in a basal vertebrate, the sea lamprey. Front Endocrinol 2:58Google Scholar
  229. Sower SA, Hanson LH (1992) Vertebrate sex determination/differentiation workshop. Report to the Great Lakes Fishery Commission. Ann Arbor, MIGoogle Scholar
  230. Sower SA, Kawauchi K (2011) Reproduction in agnathan fishes: lampreys and hagfishes. In: Norris DO, Lopez KH (eds) Hormones and reproduction of vertebrates, vol 1. Academic Press, New York, pp 193–208Google Scholar
  231. Sower SA, Larsen LO (1991) Plasma estradiol and progesterone after hypophysectomy and substitution with pituitary in female sea lampreys (Petromyzon marinus). Gen Comp Endocrinol 81:93–96PubMedGoogle Scholar
  232. Sower SA, Dickhoff WW, Gorbman A, Rivier JE, Vale WW (1983) Ovulatory and steroidal responses in the lamprey following administration of salmon gonadotropin and agonistic and antagonistic analogues of GnRH. Can J Zool 61:2653–2659Google Scholar
  233. Sower SA, Plisetskaya E, Gorbman A (1985a) Changes in plasma steroid and thyroid hormones and insulin during final maturation and spawning of the sea lamprey, Petromyzon marinus. Gen Comp Endocrinol 58:259–269Google Scholar
  234. Sower SA, Plisetskaya E, Gorbman A (1985b) Steroid and thyroid hormone profiles following a single injection of partly purified salmon gonadotropin or GnRH analogues in male and female sea lamprey. J Exp Zool 235:403–408Google Scholar
  235. Sower SA, King JA, Millar RP, Sherwood NM, Marshak DR (1987) Comparative biological properties of lamprey gonadotropin-releasing hormone in vertebrates. Endocrinology 120:773–779PubMedGoogle Scholar
  236. Sower SA, Chiang YC, Lovas S, Conlon JM (1993) Primary structure and biological activity of a third gonadotropin-releasing hormone from lamprey brain. Endocrinology 132:1125–1131PubMedGoogle Scholar
  237. Sower SA, Nozaki M, Knox CJ, Gorbman A (1995a) The occurrence and distribution of GnRH in the brain of Atlantic hagfish, an agnatha, determined by chromatography and immunocytochemistry. Gen Comp Endocrinol 97:300–307Google Scholar
  238. Sower SA, Goodman M, Nishiuchi Y (1995b) In vivo effects of lamprey GnRH-I and cyclized analogs: a structure-activity study. Neuropeptides 29:151–156Google Scholar
  239. Sower SA, McGregor AJ, Materne OL et al (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 120:168–175PubMedGoogle Scholar
  240. Sower SA, Nucci NV, Silver MR (2004) Family of gonadotropin-releasing hormone. In: Martini L (ed) Encyclopedia of endocrine diseases, vol 2. Elsevier, Amsterdam, pp 306–316Google Scholar
  241. Sower SA, Moriyama S, Kasahara M et al (2006) Identification of sea lamprey GTHβ-like cDNA and its evolutionary implications. Gen Comp Endocrinol 148:22–32PubMedGoogle Scholar
  242. Sower SA, Freamat M, Kavanaugh SI (2009) The origins of the vertebrate hypothalamic-pituitary-gonadal (HPG) and hypothalamic-pituitary-thyroid (HPT) endocrine systems: new insights from lampreys. Gen Comp Endocrinol 161:20–29PubMedGoogle Scholar
  243. Sower SA, Balz E, Aquilina-Beck A, Kavanaugh SI (2011) Seasonal changes of brain GnRH-I, -II, and -III during the final reproductive period in adult male and female sea lamprey. Gen Comp Endocrinol 170:276–282PubMedGoogle Scholar
  244. Stanislaus D, Ponder S, Ji TH, Conn PM (1998) Gonadotropin-releasing hormone receptor couples to multiple G proteins in rat gonadotrophs and in GGH3 cells: evidence from palmitoylation and overexpression of G proteins. Biol Reprod 59:579–586PubMedGoogle Scholar
  245. Stevenson TJ, Bentley GE, Ubuka T et al (2008) Effects of social cues on GnRH-I, GnRH-II, and reproductive physiology in female house sparrows (Passer domesticus). Gen Comp Endocrinol 156:385–394PubMedGoogle Scholar
  246. Struthers RS, Rivier J, Hagler AT (1985) Molecular dynamics and minimum energy conformations of GnRH and analogs. A methodology for computer-aided drug design. Ann N Y Acad Sci 439:81–96PubMedGoogle Scholar
  247. Sudo S, Kuwabara Y, Park JI, Hsu SY, Hsueh AJ (2005) Heterodimeric fly glycoprotein hormone-α2 (GPA2) and glycoprotein hormone-β5 (GPB5) activate fly leucine-rich repeat-containing G protein-coupled receptor-1 (DLGR1) and stimulation of human thyrotropin receptors by chimeric fly GPA2 and human GPB5. Endocrinology 146:3596–3604PubMedGoogle Scholar
  248. Sun B, Kavanaugh SI, Tsai P-S (2012) Gonadotropin-releasing hormone in protostomes: insights from functional studies on Aplysia californica. Gen Comp Endocrinol 176:321–326PubMedGoogle Scholar
  249. Suzuki K, Kawauchi H, Nagahama Y (1988) Isolation and characterization of subunits from two distinct salmon gonadotropins. Gen Comp Endocrinol 71:302–306PubMedGoogle Scholar
  250. Suzuki K, Gamble RL, Sower SA (2000) Multiple transcripts encoding lamprey gonadotropin releasing hormone-I precursors. J Mol Endocrinol 24:365–376PubMedGoogle Scholar
  251. Swanson P, Suzuki K, Kawauchi H, Dickhoff WW (1991) Isolation and characterization of two coho salmon gonadotropins, GTH I and GTH II. Biol Reprod 44:29–38PubMedGoogle Scholar
  252. Takahashi A, Amemiya Y, Nozaki M et al (1995a) Isolation and characterization of melanotropins from lamprey pituitary glands. Int J Pept Protein Res 46:197–204Google Scholar
  253. Takahashi A, Amemiya Y, Sarashi M, Sower SA, Kawauchi H (1995b) Melanotropin and corticotropin are encoded on two distinct genes in the lamprey, the earliest evolved extant vertebrate. Biochem Biophys Res Commun 213:490–498Google Scholar
  254. Tando Y, Kubokawa K (2009) Expression of the gene for ancestral glycoprotein hormone β subunit in the nerve cord of amphioxus. Gen Comp Endocrinol 162:329–339PubMedGoogle Scholar
  255. Temple JL, Millar RP, Rissman EF (2003) An evolutionarily conserved form of gonadotropin-releasing hormone coordinates energy and reproductive behavior. Endocrinology 144:13–19PubMedGoogle Scholar
  256. Thornton JW (2001) Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc Natl Acad Sci U S A 98:5671–5676PubMedCentralPubMedGoogle Scholar
  257. Tobet SA, Schwarting GA (2006) Minireview: recent progress in gonadotropin-releasing hormone neuronal migration. Endocrinology 147:1159–1165PubMedGoogle Scholar
  258. Tobet SA, Nozaki M, Youson JH, Sower SA (1995) Distribution of lamprey gonadotropin-releasing hormone-III (GnRH-III) in brains of larval lampreys (Petromyzon marinus). Cell Tissue Res 279:261–270Google Scholar
  259. Tobet SA, Chickering TW, Sower SA (1996) Relationship of gonadotropin-releasing hormone (GnRH) neurons to the olfactory system in developing lamprey (Petromyzon marinus). J Comp Neurol 376:97–111PubMedGoogle Scholar
  260. Tobet SA, Sower SA, Schwarting GA (1997) Gonadotropin-releasing hormone containing neurons and olfactory fibers during development: from lamprey to mammals. Brain Res Bull 44:479–486PubMedGoogle Scholar
  261. Tostivint H (2011) Evolution of the gonadotropin-releasing hormone (GnRH) gene family in relation to vertebrate tetraploidizations. Gen Comp Endocrinol 170:575–581PubMedGoogle Scholar
  262. Trudeau VL, Sloley BD, Peter RE (1993a) GABA stimulation of gonadotropin-II release in goldfish: involvement of GABAA receptors, dopamine, and sex steroids. Am J Physiol 265:R348–R355Google Scholar
  263. Trudeau VL, Sloley BD, Peter RE (1993b) Norepinephrine turnover in the goldfish brain is modulated by sex steroids and GABA. Brain Res 624:29–34Google Scholar
  264. Trudeau VL, Sloley BD, Peter RE (1993c) Testosterone enhances GABA and taurine but not N-methyl-D, L-aspartate stimulation of gonadotropin secretion in the goldfish: possible sex steroid feedback mechanisms. J Neuroendocrinol 5:129–136Google Scholar
  265. Trudeau VL, Spanswick D, Fraser EJ et al (2000) The role of amino acid neurotransmitters in the regulation of pituitary gonadotropin release in fish. Biochem Cell Biol 78:241–259PubMedGoogle Scholar
  266. Tsai PS, Zhang L (2008) The emergence and loss of gonadotropin-releasing hormone (GnRH) in protostomes: orthology, phylogeny, structure, and function. Biol Reprod 79:798–805PubMedGoogle Scholar
  267. Tsukahara T, Gorbman A, Kobayashi H (1986) Median eminence equivalence of the neurohypophysis of the hagfish, Eptatretus burgeri. Gen Comp Endocrinol 61:348–354PubMedGoogle Scholar
  268. Tsuneki K (1988) Neurohypophysis of cyclostomes as a primitive hypothalamic center of vertebrates. Zool Sci 5:21–32Google Scholar
  269. Tsuneki K, Gorbman A (1975) Ultrastructure of the anterior neurohypophysis and the pars distalis of the lamprey, Lampetra tridentata. Gen Comp Endocrinol 25:487–508PubMedGoogle Scholar
  270. Tsuneki K, Nozaki M (1989) Histological and immunohistochemical studies of the neurohypophysis of primitive teleosts, the Osteoglossidae. Acta Zool 70:47–52Google Scholar
  271. Tsutsui K, Saigoh E, Ukena K et al (2000) A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun 275:661–667PubMedGoogle Scholar
  272. Tsutsui K, Bentley G, Ubukab T et al (2007) The general and comparative biology of gonadotropin-inhibitory hormone (GnIH). Gen Comp Endocrinol 153:365–370PubMedGoogle Scholar
  273. Tsutsumi M, Zhou W, Millar RP et al (1992) Cloning and functional expression of a mouse gonadotropin-releasing hormone receptor. Mol Endocrinol 6:1163–1169PubMedGoogle Scholar
  274. Ubuka T, Ueno M, Ukena K, Tsutsui K (2003) Developmental changes in gonadotropin-inhibitory hormone in the Japanese quail (Coturnix japonica) hypothalamo-hypophysial system. J Endocrinol 178:311–318PubMedGoogle Scholar
  275. Uchida K, Moriyama S, Chiba H et al (2010) Evolutionary origin of a functional gonadotropin in the pituitary of the most primitive vertebrate, hagfish. Proc Natl Acad Sci U S A 107:15832–15837PubMedCentralPubMedGoogle Scholar
  276. Uchida K, Moriyama S, Sower SA, Nozaki M (2013) Glycoprotein hormone in the pituitary of hagfish and its evolutionary implications. Fish Physiol Biochem 39:75–83PubMedGoogle Scholar
  277. Ukena K, Iwakoshi E, Minakata H, Tsutsui K (2002) A novel rat hypothalamic RFamide-related peptide identified by immunoaffinity chromatography and mass spectrometry. FEBS Lett 512:255–258PubMedGoogle Scholar
  278. Ukena K, Koda A, Yamamoto K et al (2003a) Novel neuropeptides related to frog growth hormone-releasing peptide: isolation, sequence, and functional analysis. Endocrinology 144:3879–3884Google Scholar
  279. Ukena K, Ubuka T, Tsutsui K (2003b) Distribution of a novel avian gonadotropin-inhibitory hormone in the quail brain. Cell Tissue Res 312:73–79Google Scholar
  280. Vandepoele K, De Vos W, Taylor JS, Meyer A, Van de Peer Y (2004) Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proc Natl Acad Sci U S A 101:1638–1643PubMedCentralPubMedGoogle Scholar
  281. von Bartheld CS, Rubel EW (1989) Transient GABA immunoreactivity in cranial nerves of the chick embryo. J Comp Neurol 286:456–471PubMedGoogle Scholar
  282. Vrecl M, Heding A, Hanyaloglu A, Taylor PL, Eidne KA (2000) Internalization kinetics of the gonadotropin-releasing hormone (GnRH) receptor. Pflugers Arch 439:R19–R20PubMedGoogle Scholar
  283. Wald U, Selzer ME, Krieger NR (1981) Glutamic acid decarboxylase in sea lamprey (Petromyzon marinus): characterization, localization, and developmental changes. J Neurochem 36:363–368PubMedGoogle Scholar
  284. Wang L, Bogerd J, Choi HS et al (2001) Three distinct types of GnRH receptor characterized in the bullfrog. Proc Natl Acad Sci U S A 98:361–366PubMedCentralPubMedGoogle Scholar
  285. Willars GB, Heding A, Vrecl M et al (1999) Lack of a C-terminal tail in the mammalian gonadotropin-releasing hormone receptor confers resistance to agonist-dependent phosphorylation and rapid desensitization. J Biol Chem 274:30146–30153PubMedGoogle Scholar
  286. 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 placode. Proc Natl Acad Sci U S A 86:8132–8136Google Scholar
  287. Wray S, Nieburgs A, Elkabes S (1989b) Spatiotemporal cell expression of luteinizing hormone-releasing hormone in the prenatal mouse: evidence for an embryonic origin in the olfactory placode. Brain Res Dev Brain Res 46:309–318Google Scholar
  288. Wright DE, McBurney KM, Youson JH, Sower SA (1994) Distribution of lamprey gonadotropin-releasing hormone in the brain and pituitary gland of larval, metamorphic, and adult sea lampreys, Petromyzon marinus. Can J Zool 72:48–53Google Scholar
  289. Yang H-YT, Martin RM (1995) Isolation and characterization of a neuropeptide FF-like peptide from brain and spinal cord of rat. Soc Neurosci Abstr 21:760Google Scholar
  290. Yang HY, Fratta W, Majane EA, Costa E (1985) Isolation, sequencing, synthesis, and pharmacological characterization of two brain neuropeptides that modulate the action of morphine. Proc Natl Acad Sci U S A 82:7757–7761PubMedCentralPubMedGoogle Scholar
  291. Yoshida H, Habata Y, Hosoya M et al (2003) Molecular properties of endogenous RFamide-related peptide-3 and its interaction with receptors. Biochim Biophys Acta 1593:151–157PubMedGoogle Scholar
  292. Young BA, Bryan MB, Sower SA, Scott AP, Li W (2004) 15α-hydroxytestosterone induction by GnRH I and GnRH III in Atlantic and Great Lakes sea lamprey (Petromyzon marinus L.). Gen Comp Endocrinol 136:276–281PubMedGoogle Scholar
  293. Youngs LJ, Winokur A, Selzer ME (1985) Thyrotropin-releasing hormone in lamprey central nervous system. Brain Res 338:177–180PubMedGoogle Scholar
  294. Youson JH, Sower SA (1991) Concentration of brain gonadotropin-releasing hormone during metamorphosis in the lamprey, Petromyzon marinus. J Exp Zool 259:399–404Google Scholar
  295. Youson JH, Sower SA (2001) Theory on the evolutionary history of lamprey metamorphosis: role of reproductive and thyroid axes. Comp Biochem Physiol B Biochem Mol Biol 129:337–345PubMedGoogle Scholar
  296. Youson JH, Docker M, Sower SA (1995) Concentration of gonadotropin-releasing hormones in brain of larval and metamorphosing lampreys of two species with different adult life histories. In: Goetz FW, Thomas P (eds) 5th International Symposium of the Reproductive Physiology of Fish, Austin, TX, p 83Google Scholar
  297. Youson JH, Heinig JA, Khanam SF et al (2006) Patterns of proopiomelanotropin and proopiocortin gene expression and of immunohistochemistry for gonadotropin-releasing hormones (lGnRH-I and III) during the life cycle of a nonparasitic lamprey: relationship to this adult life history type. Gen Comp Endocrinol 148:54–71PubMedGoogle Scholar
  298. Yu KL, He ML, Chik CC et al (1998) mRNA expression of gonadotropin-releasing hormones (GnRHs) and GnRH receptor in goldfish. Gen Comp Endocrinol 112:303–311PubMedGoogle Scholar
  299. Zhang L, Tello JA, Zhang W, Tsai PS (2008) Molecular cloning, expression pattern, and immunocytochemical localization of a gonadotropin releasing hormone-like molecule in the gastropod mollusk, Aplysia californica. Gen Comp Endocrinol 156:201–209PubMedCentralPubMedGoogle Scholar

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© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Center for Molecular and Comparative Endocrinology, Department of Molecular, Cellular and Biomedical SciencesUniversity of New HampshireDurhamUSA

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