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Involvement of GnRH, PACAP and PRP in the Reproduction of Blue Gourami Females (Trichogaster trichopterus)

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Abstract

In vertebrates, gonadotropin-releasing hormone (GnRH) and pituitary adenylate cyclase-activating polypeptide (PACAP) are key hormones regulating growth and reproduction in the brain–pituitary axis. The regulating hormonal interactions are of great interest, therefore, the aim of this study is to provide novel insights into the involvement of brain GnRH and PACAP in oogensis and spermatogenesis in a fish model, the blue gourami (Trichogaster trichopterus). cDNA cloning of two GnRH forms combined with phylogenetic analysis revealed that three paralogous GnRH forms exist in blue gourami and evolve as a result of genome duplication. GnRH1 mRNA levels are related to final oocyte maturation (FOM), and this peptide stimulated β follicle-stimulating hormone (βFSH) and growth hormone (GH) gene expression; GnRH2 stimulated β gonadotropins (GtH) gene expression and GnRH analog combined with PACAP-38 synergistically upregulate GH and βFSH gene expression. The data presented, together with previous studies in our lab, enable suggesting mechanisms explaining the physiological relevance of these peptides in the regulation of gametogenesis and steroidogenesis in blue gourami females. These findings support the biological importance of the GnRH and PACAP hormones family, enabling them to stimulate differential biological functions in the regulation of growth and reproduction.

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References

  • Amano M, Okubo K, Yamanome T, Yamada H, Aida K, Yamamori K (2004) Changes in brain GnRH mRNA and pituitary GnRH peptide during testicular maturation in barfin flounder. Comp Biochem Physiol B Biochem Mol Biol 138:435–443

    Article  PubMed  Google Scholar 

  • Amano M, Pham KX, Amiya N, Yamanome T, Yamamori K (2008) Changes in brain seabream GnRH mRNA and pituitary seabream GnRH peptide levels during ovarian maturation in female barfin flounder. Gen Comp Endocrinol 158:168–172

    Article  PubMed  CAS  Google Scholar 

  • An KW, Nelson ER, Habibi HR, Choi CY (2008) Molecular characterization and expression of three GnRH forms mRNA during gonad sex-change process, and effect of GnRHa on GTH subunits mRNA in the protandrous black porgy (Acanthopagrus schlegeli). Gen Comp Endocrinol 159:38–45

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Becker D, Galili N, Degani G (1992) GCMS-indentified steroids and steroid glucoronides in gonads and holding water of Trichogaster trichopterus (Anabantidae, Pallas 1770). Comp Biochem Phys Part B: Comp Biochem 103:15–19

    Article  Google Scholar 

  • Bosma PT, Rebers FE, Dijk W, Willems PH, Goos HJ, Schulz RW (2000) Inhibitory and stimulatory interactions between endogenous gonadotropin-releasing hormones in the African catfish (Clarias gariepinus). Biol Reprod 62:731–738

    Article  PubMed  CAS  Google Scholar 

  • Canosa LF, Stacey N, Peter RE (2008) Changes in brain mRNA levels of gonadotropin-releasing hormone, pituitary adenylate cyclase activating polypeptide, and somatostatin during ovulatory luteinizing hormone and growth hormone surges in goldfish. Am J Physiol Regul Integr Comp Physiol 295:R1815–1821

    Article  PubMed  CAS  Google Scholar 

  • Chang JP, Wirachowsky NR, Kwong P, Johnson JD (2001) Pacap stimulation of gonadotropin-II secretion in goldfish pituitary cells: mechanisms of action and interaction with gonadotropin releasing hormone signalling. J Neuroendocrinol 13:540–550

    Article  PubMed  CAS  Google Scholar 

  • Chang JP, Johnson JD, Sawisky GR, Grey CL, Mitchell G, Booth M, Volk MM, Parks SK, Thompson E, Goss GG, Klausen C, Habibi HR (2009) Signal transduction in multifactorial neuroendocrine control of gonadotropin secretion and synthesis in teleosts-studies on the goldfish model. Gen Comp Endocrinol 161:42–52

    Article  PubMed  CAS  Google Scholar 

  • Cheng GF, Yuen CW, Ge W (2007) Evidence for the existence of a local activin follistatin negative feedback loop in the goldfish pituitary and its regulation by activin and gonadal steroids. J Endocrinol 195:373–384

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Degani G (1990) The effect of human chorionic gonadotropin on steroid changes in trichogaster trichopterus (B & S 1801). Comp Biochem Physiol 96A

  • Degani G (1993a) The effect of sexual behavior on oocyte development and steroid changes in Trichogaster trichopterus. Copeia 4, 1091-1091-1096

    Google Scholar 

  • Degani G (1993b) Reproduction control in multi-spawning asynchronic Trichogaster trichopterus (Pallas) as a model for the anabantidae family. Trends Comp Biochem Phys 1:1269–1275

    Google Scholar 

  • Degani G (1994) Effect of gonadotrpin and steroids on vitellogenesis during ovarian development in trichogaster trichopterus. J Aquacult Trop 9:15–23

    Google Scholar 

  • Degani G (2001) Blue gourami (Trichogaster trichopterus) model for labyrinth fish. Laser Pages Publishing, Israel

    Google Scholar 

  • Degani G, Boker R (1992a) Sensitivity to maturation-inducing steroids and gonadotropin in the oocytes of blue gourami Trichogaster trichopterus (Anabantidae, Pallas, 1770). Gen Comp Endocrinol 85:430–439

    Article  PubMed  CAS  Google Scholar 

  • Degani G, Boker R (1992b) Vitellogenesis level and the induction of maturation in the ovary of the blue gourami Trichogaster trichopterus (Anabantidae, Pallas 1770). J Exp Zool 263:330–337

    Article  CAS  Google Scholar 

  • Degani G, Gallagher ML (1996) Steroid and carp pituitary extract influenceon follicle frequency in vitellogenesis and maturation of Trichogaster trichopterus. J Aquacult Trop 11

  • Degani G, Schreibman MP (1993) Pheromone of males blue gourami and its effect on vitellogenesis and gonadotropin cells in pituitary of the females. J Fish Biol 43:475–485

    CAS  Google Scholar 

  • Degani G, Mananos EL, Jackson K, Abraham M, Zohar Y (1997) Changes in plasma and pituitary GtH-II levels in female blue gourami Trichogaster trichopterus during the end of vitellogenesis and final oocyte maturation. J Exp Zool 279:377–385

    Article  CAS  Google Scholar 

  • Degani G, Jackson K, Goldberg D, Sarfati R, Avtalion RR (2003) betaFSH, betaLH and growth hormone gene expression in blue gourami (Trichogaster trichopterus, Pallas 1770) during spermatogenesis and male sexual behavior. Zool Sci 20:737–743

    Article  PubMed  CAS  Google Scholar 

  • Foran CM, Bass AH (1999) Preoptic GnRH and AVT: axes for sexual plasticity in teleost fish. Gen Comp Endocrinol 116:141–152

    Article  PubMed  CAS  Google Scholar 

  • Goldberg D, Jackson K, Yom-Din S, Degani G (2004) Growth hormone of Trichogaster trichopterus: cDNA cloning, sequencing and analysis of mRNA expression during oogenesis. J Aquac Trop 19:215–229

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Martinez D, Zmora N, Mananos E, Saligaut D, Zanuy S, Zohar Y, Elizur A, Kah O, Munoz-Cueto JA (2002) Immunohistochemical localization of three different prepro-GnRHs in the brain and pituitary of the European sea bass (Dicentrarchus labrax) using antibodies to the corresponding GnRH-associated peptides. J Comp Neurol 446:95–113

    Article  PubMed  CAS  Google Scholar 

  • Guzman JM, Rubio M, Ortiz-Delgado JB, Klenke U, Kight K, Cross I, Sanchez-Ramos I, Riaza A, Rebordinos L, Sarasquete C, Zohar Y, Mananos EL (2009) Comparative gene expression of gonadotropins (FSH and LH) and peptide levels of gonadotropin-releasing hormones (GnRHs) in the pituitary of wild and cultured Senegalese sole (Solea senegalensis) broodstocks. Comp Biochem Physiol A Mol Integr Physiol 153:266–277

    Article  PubMed  CAS  Google Scholar 

  • Hull KL, Harvey S (2001) Growth hormone: roles in female reproduction. J Endocrinol 168:1–23

    Article  PubMed  CAS  Google Scholar 

  • Jackson K, Abraham M, Degani G (1994) Oocyte maturation triggered by the presence of male in the Blue Gourami (Trichogaster trichopterus). J Morphol 220:1–9

    Article  Google Scholar 

  • Jackson K, Goldberg D, Ofir M, Abraham M, Degani G (1999) Blue gourami (Trichogaster trichopterus) gonadotropic beta subunits (I and II) cDNA sequences and expression during oogenesis. J Mol Endocrinol 23:177–187

    Article  PubMed  CAS  Google Scholar 

  • Kah O, Lethimonier C, Lareyre JJ (2004) Gonadotrophin-releasing hormone (GnRH) in the animal kingdom. J Soc Biol 198:53–60

    PubMed  CAS  Google Scholar 

  • Kah O, Lethimonier C, Somoza G, Guilgur LG, Vaillant C, Lareyre JJ (2007) GnRH and GnRH receptors in metazoa: a historical, comparative, and evolutive perspective. Gen Comp Endocrinol 153:346–364

    Article  PubMed  CAS  Google Scholar 

  • Kanasaki H, Purwana IN, Mijiddorj T, Oride A, Miyazaki K (2011) Possible involvement of PACAP and PACAP type 1 receptor in GnRH-induced FSH beta-subunit gene expression. Regul Pept 167:227–232

    Article  PubMed  CAS  Google Scholar 

  • Kim DK, Cho EB, Moon MJ, Park S, Hwang JI, Kah O, Sower SA, Vaudry H, Seong JY (2011) Revisiting the evolution of gonadotropin-releasing hormones and their receptors in vertebrates: secrets hidden in genomes. Gen Comp Endocrinol 170:68–78

    Article  PubMed  CAS  Google Scholar 

  • Lethimonier C, Madigou T, Munoz-Cueto JA, Lareyre JJ, Kah O (2004) Evolutionary aspects of GnRHs, GnRH neuronal systems and GnRH receptors in teleost fish. Gen Comp Endocrinol 135:1–16

    Article  PubMed  CAS  Google Scholar 

  • Levy G, Degani G (2011) Evidence of a reproduction-related function for pituitary adenylate cyclase-activating polypeptide-related peptide in an Anabantidae fish. J Mol Endocrinol 46:101–110

    Article  PubMed  CAS  Google Scholar 

  • Levy G, Gothilf Y, Degani G (2009) Brain gonadotropin releasing hormone3 expression v ariation during oogenesis and sexual behavior and its effect on pituitary hormonal expression in the blue gourami. Comp Biochem Physiol A Mol Integr Physiol 154:241–248

    Article  PubMed  CAS  Google Scholar 

  • Levy G, Jackson K, Degani G (2010) Association between pituitary adenylate cyclase-activating polypeptide and reproduction in the blue gourami. Gen Comp Endocrinol 166:83–93

    Article  PubMed  CAS  Google Scholar 

  • Lin SW, Ge W (2009) Differential regulation of gonadotropins (FSH and LH) and growth hormone (GH) by neuroendocrine, endocrine, and paracrine factors in the zebrafish—an in vitro approach. Gen Comp Endocrinol 160:183–193

    Article  PubMed  CAS  Google Scholar 

  • Long Y, Tao M, Liu S, Zhong H, Chen L, Tao S, Liu Y (2009) Differential expression of Gnrh2, Gthbeta, and Gthr genes in sterile triploids and fertile tetraploids. Cell Tissue Res 338:151–159

    Article  PubMed  CAS  Google Scholar 

  • Mananos E, Zohar Y, Degani G (1997) The relationship between gonadotropin and sexual behavior of male Trichogaster trichopterus (Pallas). Indian J Fish 44:239–246

    Google Scholar 

  • Maruska KP, Tricas TC (2011) Gonadotropin-releasing hormone (GnRH) modulates auditory processing in the fish brain. Horm Behav 59:451–464

    Article  PubMed  CAS  Google Scholar 

  • Matsuda K, Nakamura K, Shimakura S, Miura T, Kageyama H, Uchiyama M, Shioda S, Ando H (2008) Inhibitory effect of chicken gonadotropin-releasing hormone II on food intake in the goldfish, Carassius auratus. Horm Behav 54:83–89

    Article  PubMed  CAS  Google Scholar 

  • Muller PY, Janovjak H, Miserez AR, Dobbie Z (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 32: 1372-1374, 1376, 1378-1379

    Google Scholar 

  • Nagahama Y (1994) Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38:217–229

    PubMed  CAS  Google Scholar 

  • Ogawa S, Akiyama G, Kato S, Soga T, Sakuma Y, Parhar IS (2006) Immunoneutralization of gonadotropin-releasing hormone type-III suppresses male reproductive behavior of cichlids. Neurosci Lett 403:201–205

    Article  PubMed  CAS  Google Scholar 

  • Okubo K, Nagahama Y (2008) Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiol (Oxf) 193:3–15

    Article  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  PubMed  CAS  Google Scholar 

  • Pincas H, Laverriere JN, Counis R (2001) Pituitary adenylate cyclase-activating polypeptide and cyclic adenosine 3′,5′-monophosphate stimulate the promoter activity of the rat gonadotropin-releasing hormone receptor gene via a bipartite response element in gonadotrope-derived cells. J Biol Chem 276:23562–23571

    Article  PubMed  CAS  Google Scholar 

  • Purwana IN, Kanasaki H, Oride A, Mijiddorj T, Shintani N, Hashimoto H, Baba A, Miyazaki K (2010) GnRH-induced PACAP and PAC1 receptor expression in pituitary gonadotrophs: a possible role in the regulation of gonadotropin subunit gene expression. Peptides 31:1748–1755

    Article  PubMed  CAS  Google Scholar 

  • Purwana IN, Kanasaki H, Oride A, Mijiddorj T, Miyazaki K (2011) Expression of the pituitary adenylate cyclase-activating polypeptide (PACAP) type 1 receptor (PAC1R) potentiates the effects of GnRH on gonadotropin subunit gene expression. Biochem Biophys Res Commun 410:295–300

    Article  PubMed  CAS  Google Scholar 

  • Reinecke M (2010) Insulin-like growth factors and fish reproduction. Biol Reprod 82:656–661

    Article  PubMed  CAS  Google Scholar 

  • Roch GJ, Busby ER, Sherwood NM (2011) Evolution of GnRH: diving deeper. Gen Comp Endocrinol 171:1–16

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Soverchia L, Carotti M, Andreu-Vieyra C, Mosconi G, Cannella N, Habibi H, Polzonetti-Magni AM (2007) Role of gonadotropin-releasing hormone (GnRH) in the regulation of gonadal differentiation in the gilthead seabream (Sparus aurata). Mol Reprod Dev 74:57–67

    Article  PubMed  CAS  Google Scholar 

  • 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 161:20–29

    Article  PubMed  CAS  Google Scholar 

  • Tostivint H (2011) Evolution of the gonadotropin-releasing hormone (GnRH) gene family in relation to vertebrate tetraploidizations. Gen Comp Endocrinol 170:575–581

    Article  PubMed  CAS  Google Scholar 

  • Volkoff H, Peter RE (1999) Actions of two forms of gonadotropin releasing hormone and a GnRH antagonist on spawning behavior of the goldfish Carassius auratus. Gen Comp Endocrinol 116:347–355

    Article  PubMed  CAS  Google Scholar 

  • White SA, Nguyen T, Fernald RD (2002) Social regulation of gonadotropin-releasing hormone. J Exp Biol 205:2567–2581

    PubMed  CAS  Google Scholar 

  • Winters SJ, Moore JP Jr (2011) PACAP, an autocrine/paracrine regulator of gonadotrophs. Biol Reprod 84:844–850

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Huang W, Zhong C, Luo D, Li S, Zhu Z, Hu W (2011) Defining global gene expression changes of the hypothalamic-pituitary-gonadal axis in female sGnRH-antisense transgenic common carp (Cyprinus carpio). PLoS One 6:e21057

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yaron Z, Gur G, Melamed P, Rosenfeld H, Levavi-Sivan B, Elizur A (2001) Regulation of gonadotropin subunit genes in tilapia. Comp Biochem Physiol B Biochem Mol Biol 129:489–502

    Article  PubMed  CAS  Google Scholar 

  • Yaron Z, Gur G, Melamed P, Rosenfeld H, Elizur A, Levavi-Sivan B (2003) Regulation of fish gonadotropins. Int Rev Cytol 225:131–185

    Article  PubMed  CAS  Google Scholar 

  • Zhou H, Wang X, Ko WK, Wong AO (2004) Evidence for a novel intrapituitary autocrine/paracrine feedback loop regulating growth hormone synthesis and secretion in grass carp pituitary cells by functional interactions between gonadotrophs and somatotrophs. Endocrinology 145:5548–5559

    Article  PubMed  CAS  Google Scholar 

  • Zhou H, Jiang Y, Ko WK, Li W, Wong AO (2005) Paracrine regulation of growth hormone gene expression by gonadotrophin release in grass carp pituitary cells: functional implications, molecular mechanisms and signal transduction. J Mol Endocrinol 34:415–432

    Article  PubMed  CAS  Google Scholar 

  • Zmora N, Gonzalez-Martinez D, Munoz-Cueto JA, Madigou T, Mananos-Sanchez E, Doste SZ, Zohar Y, Kah O, Elizur A (2002) The GnRH system in the European sea bass (Dicentrarchus labrax). J Endocrinol 172:105–116

    Article  PubMed  CAS  Google Scholar 

  • Zohar Y, Munoz-Cueto JA, Elizur A, Kah O (2010) Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol 165:438–455

    Article  PubMed  CAS  Google Scholar 

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Levy, G., Degani, G. Involvement of GnRH, PACAP and PRP in the Reproduction of Blue Gourami Females (Trichogaster trichopterus). J Mol Neurosci 48, 603–616 (2012). https://doi.org/10.1007/s12031-012-9730-8

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