Seasonal Effect of Gonadotrophin Inhibitory Hormone on Gonadotrophin‐Releasing Hormone‐induced Gonadotroph Functions in the Goldfish Pituitary

We have shown that native goldfish gonadotrophin inhibitory hormone (gGnIH) differentially regulates luteinsing hormone (LH)‐β and follicle‐stimulating hormone (FSH)‐β expression. To further understand the functions of gGnIH, we examined its interactions with two native goldfish gonadotrophin‐releasing hormones, salmon gonadotrophin‐releasing hormone (sGnRH) and chicken (c)GnRH‐II in vivo and in vitro. Intraperitoneal injections of gGnIH alone reduced serum LH levels in fish in early and mid gonadal recrudescence; this inhibition was also seen in fish co‐injected with either sGnRH or cGnRH‐II during early recrudescence. Injection of gGnIH alone elevated pituitary LH‐β and FSH‐β mRNA levels at early and mid recrudescence, and FSH‐β mRNA at late recrudescence. Co‐injection of gGnIH attenuated the stimulatory influences of sGnRH on LH‐β in early recrudescence, and LH‐β and FSH‐β mRNA levels in mid and late recrudescence, as well as the cGnRH‐II‐elicited increase in LH‐β, but not FSH‐β, mRNA expression at mid and late recrudescence. sGnRH and cGnRH‐II injection increased pituitary gGnIH‐R mRNA expression in mid and late recrudescence but gGnIH reduced gGnIH‐R mRNA levels in late recrudescence. gGnIH did not affect basal LH release from perifused pituitary cells and continual exposure to gGnIH did not alter the LH responses to acute applications of GnRH. However, a short 5‐min GnIH treatment in the middle of a 60‐min GnRH perifusion selectively reduced the cGnRH‐II‐induced release of LH. These novel results indicate that, in goldfish, gGnIH and GnRH modulate pituitary GnIH‐R expression and gGnIH differentially affects sGnRH and cGnRH‐II regulation of LH secretion and gonadotrophin subunit mRNA levels. Furthermore, these actions are manifested in a reproductive stage‐dependent manner.

[1]  J. P. Chang,et al.  Seasonal effect of GnIH on gonadotrope functions in the pituitary of goldfish , 2012, Molecular and Cellular Endocrinology.

[2]  K. Tsutsui,et al.  Gonadotropin-inhibitory hormone inhibits GnRH-induced gonadotropin subunit gene transcriptions by inhibiting AC/cAMP/PKA-dependent ERK pathway in LβT2 cells. , 2012, Endocrinology.

[3]  L. Kriegsfeld,et al.  Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. , 2012, Endocrinology.

[4]  R. Zann,et al.  Potential roles for GNIH and GNRH-II in reproductive axis regulation of an opportunistically breeding songbird. , 2011, General and comparative endocrinology.

[5]  I. Clarke Control of GnRH secretion: One step back , 2011, Frontiers in Neuroendocrinology.

[6]  G. Roch,et al.  Evolution of GnRH: diving deeper. , 2011, General and comparative endocrinology.

[7]  K. Ukena,et al.  Synchronised Expressions of LPXRFamide Peptide and its Receptor Genes: Seasonal, Diurnal and Circadian Changes During Spawning Period in Grass Puffer , 2011, Journal of neuroendocrinology.

[8]  L. Kriegsfeld,et al.  Discovery and Evolutionary History of Gonadotrophin‐Inhibitory Hormone and Kisspeptin: New Key Neuropeptides Controlling Reproduction , 2010, Journal of neuroendocrinology.

[9]  L. Kriegsfeld,et al.  Gonadotropin-inhibitory hormone (GnIH) and its control of central and peripheral reproductive function , 2010, Frontiers in Neuroendocrinology.

[10]  G. Bédécarrats,et al.  Activation of the chicken gonadotropin-inhibitory hormone receptor reduces gonadotropin releasing hormone receptor signaling. , 2010, General and comparative endocrinology.

[11]  Yong Zhang,et al.  Structural diversity of the gnih/gnih receptor system in teleost: Its involvement in early development and the negative control of LH release , 2010, Peptides.

[12]  Jeremy T. Smith,et al.  Gonadotropin inhibitory hormone function in mammals , 2010, Trends in Endocrinology & Metabolism.

[13]  Adam J Pawson,et al.  Identification of Human GnIH Homologs, RFRP-1 and RFRP-3, and the Cognate Receptor, GPR147 in the Human Hypothalamic Pituitary Axis , 2009, PloS one.

[14]  K. Tsutsui,et al.  Gonadotropin‐inhibitory hormone identification, cDNA cloning, and distribution in rhesus macaque brain , 2009, The Journal of comparative neurology.

[15]  Jeremy T. Smith,et al.  Effect of RF-amide-related peptide-3 on luteinizing hormone and follicle-stimulating hormone synthesis and secretion in ovine pituitary gonadotropes. , 2009, Endocrinology.

[16]  A. Herbison,et al.  RFamide-related peptide-3, a mammalian gonadotropin-inhibitory hormone ortholog, regulates gonadotropin-releasing hormone neuron firing in the mouse. , 2009, Endocrinology.

[17]  H. Habibi,et al.  Signal transduction in multifactorial neuroendocrine control of gonadotropin secretion and synthesis in teleosts-studies on the goldfish model. , 2009, General and comparative endocrinology.

[18]  L. Kriegsfeld,et al.  Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. , 2008, Endocrinology.

[19]  L. Kriegsfeld,et al.  Alterations in RFamide-related peptide expression are coordinated with the preovulatory luteinizing hormone surge. , 2008, Endocrinology.

[20]  S. Krzysik-Walker,et al.  Gonadotrophin‐Inhibitory Hormone Receptor Expression in the Chicken Pituitary Gland: Potential Influence of Sexual Maturation and Ovarian Steroids , 2008, Journal of neuroendocrinology.

[21]  K. Tsutsui,et al.  Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and -II neurons in European starling brain. , 2008, Endocrinology.

[22]  Adam J Pawson,et al.  Potent action of RFamide-related peptide-3 on pituitary gonadotropes indicative of a hypophysiotropic role in the negative regulation of gonadotropin secretion. , 2008, Endocrinology.

[23]  Cameron M. Hand,et al.  p38 mitogen-activated protein kinase is critical for synergistic induction of the FSH(beta) gene by gonadotropin-releasing hormone and activin through augmentation of c-Fos induction and Smad phosphorylation. , 2007, Molecular endocrinology.

[24]  Adam J Pawson,et al.  Reciprocal cross talk between gonadotropin-releasing hormone (GnRH) and prostaglandin receptors regulates GnRH receptor expression and differential gonadotropin secretion. , 2007, Molecular endocrinology.

[25]  Adam J Pawson,et al.  Bovine and ovine gonadotropin-releasing hormone (GnRH)-II ligand precursors and type II GnRH receptor genes are functionally inactivated. , 2006, Endocrinology.

[26]  K. Ukena,et al.  Gonadotropin-inhibitory hormone inhibits gonadal development and maintenance by decreasing gonadotropin synthesis and release in male quail. , 2006, Endocrinology.

[27]  K. Ukena,et al.  Novel fish hypothalamic neuropeptides stimulate the release of gonadotrophins and growth hormone from the pituitary of sockeye salmon. , 2006, The Journal of endocrinology.

[28]  L. Kriegsfeld,et al.  Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[29]  J. P. Chang,et al.  Intracellular Calcium Involvement in Pituitary Adenylate Cyclase‐Activating Polypeptide Stimulation of Growth Hormone and Gonadotrophin Secretion in Goldfish Pituitary Cells , 2005, Journal of neuroendocrinology.

[30]  Tadahiro Ikemoto,et al.  Chicken RFamide-related peptide (GnIH) and two distinct receptor subtypes: identification, molecular characterization, and evolutionary considerations. , 2005, The Journal of reproduction and development.

[31]  K. Ukena,et al.  A novel G protein-coupled receptor for gonadotropin-inhibitory hormone in the Japanese quail (Coturnix japonica): identification, expression and binding activity. , 2005, The Journal of endocrinology.

[32]  K. Ukena,et al.  Gonadotrophin Inhibitory Hormone Depresses Gonadotrophin α and Follicle‐Stimulating Hormone β Subunit Expression in the Pituitary of the Domestic Chicken , 2004 .

[33]  J. Wingfield,et al.  Gonadotropin-inhibitory hormone in Gambel's white-crowned sparrow (Zonotrichia leucophrys gambelii): cDNA identification, transcript localization and functional effects in laboratory and field experiments. , 2004, The Journal of endocrinology.

[34]  K. Ukena,et al.  Gonadotrophin Inhibitory Hormone Depresses Gonadotrophin α and Follicle‐Stimulating Hormone β Subunit Expression in the Pituitary of the Domestic Chicken , 2004, Journal of neuroendocrinology.

[35]  T. Martin Tuning exocytosis for speed: fast and slow modes. , 2003, Biochimica et biophysica acta.

[36]  J. Wingfield,et al.  Gonadotropin‐Inhibitory Peptide in Song Sparrows (Melospiza melodia) in Different Reproductive Conditions, and in House Sparrows (Passer domesticus) Relative to Chicken‐Gonadotropin‐Releasing Hormone , 2003, Journal of neuroendocrinology.

[37]  H. Minakata,et al.  Novel fish hypothalamic neuropeptide. , 2002, European journal of biochemistry.

[38]  H. Habibi,et al.  Time- and dose-related effects of gonadotropin-releasing hormone on growth hormone and gonadotropin subunit gene expression in the goldfish pituitary. , 2002, Canadian journal of physiology and pharmacology.

[39]  K. Ukena,et al.  A novel amphibian hypothalamic neuropeptide: isolation, localization, and biological activity. , 2002, Endocrinology.

[40]  H. Habibi,et al.  Multiplicity of gonadotropin-releasing hormone signaling: a comparative perspective. , 2002, Progress in brain research.

[41]  M. Kikuchi,et al.  A novel avian hypothalamic peptide inhibiting gonadotropin release. , 2000, Biochemical and biophysical research communications.

[42]  Warren K. Yunker,et al.  Signal transduction mechanisms mediating secretion in goldfish gonadotropes and somatotropes. , 2000, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[43]  B. Hille,et al.  Protein kinase C as a signal for exocytosis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[44]  J. P. Chang,et al.  Roles of calcium and calmodulin in the mediation of acute and sustained GnRH-stimulated gonadotropin secretion from dispersed goldfish pituitary cells. , 1996, General and comparative endocrinology.

[45]  F. van Goor,et al.  Interactions between protein kinase C and arachidonic acid in the gonadotropin response to salmon and chicken gonadotropin-releasing hormone-II in goldfish. , 1994, General and comparative endocrinology.

[46]  H. Habibi,et al.  Functional specificity for salmon gonadotropin-releasing hormone (GnRH) and chicken GnRH-II coupled to the gonadotropin release and subunit messenger ribonucleic acid level in the goldfish pituitary. , 1994, Endocrinology.

[47]  R. Peter,et al.  Dopamine stimulates growth hormone release from the pituitary of goldfish, Carassius auratus, through the dopamine D1 receptors. , 1992, Endocrinology.

[48]  V. Trudeau,et al.  Testosterone and estradiol potentiate the serum gonadotropin response to gonadotropin-releasing hormone in goldfish. , 1991, Biology of reproduction.

[49]  R. Peter,et al.  In vitro release of gonadotropin-releasing hormone from the brain preoptic-anterior hypothalamic region and pituitary of female goldfish. , 1991, General and comparative endocrinology.

[50]  G. Somoza,et al.  Use of a pituitary cell dispersion method and primary culture system for the studies of gonadotropin-releasing hormone action in the goldfish, Carassius auratus. I. Initial morphological, static, and cell column perifusion studies. , 1990, General and comparative endocrinology.

[51]  T. Marchant,et al.  Functional relationship between receptor binding and biological activity for analogs of mammalian and salmon gonadotropin-releasing hormones in the pituitary of goldfish (Carassius auratus). , 1989, Biology of reproduction.

[52]  R. J. Omeljaniuk,et al.  Alterations in pituitary GnRH and dopamine receptors associated with the seasonal variation and regulation of gonadotropin release in the goldfish (Carassius auratus). , 1989, General and comparative endocrinology.

[53]  G. Callard,et al.  Changes in brain aromatase and 5 alpha-reductase activities correlate significantly with seasonal reproductive cycles in goldfish (Carassius auratus). , 1988, Endocrinology.

[54]  R. Peter,et al.  Gonadotropin release from the pars distalis of goldfish, Carassius auratus, transplanted beside the brain or into the brain ventricles: additional evidence for gonadotropin-release-inhibitory factor. , 1984, General and comparative endocrinology.