Kisspeptin receptor, GPR54, as a candidate for the regulation of testicular activity in the frog rana esculenta

Biology of Reproduction

Volumn 88, Issue 3, 2013, Pages

  Chianese, Rosanna ^a   Ciaramella, Vincenza ^a   Fasano, Silvia ^a   Pierantoni, Riccardo ^a   Meccariello, Rosaria ^b  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b UNIVERSITY OF NAPLES PARTHENOPE   (Italy)

Author keywords

Amphibians; GPR54; Kisspeptin; Reproduction; Spermatogenesis; Testis

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; G PROTEIN COUPLED RECEPTOR 54; KISSPEPTIN 10; MESSENGER RNA;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; FEMALE; GERM CELL; GONAD; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RANA ESCULENTA; SEASONAL VARIATION; SERTOLI CELL; SPERMATOCYTE; TESTIS FUNCTION; TISSUE DISTRIBUTION; UPREGULATION; WINTER;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; KISSPEPTINS; MALE; MOLECULAR SEQUENCE DATA; PITUITARY GLAND; RANA ESCULENTA; RECEPTORS, G-PROTEIN-COUPLED; SEASONS; TESTIS;

AMPHIBIA; ANURA; RANA ESCULENTA;

EID: 84877053098     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.103515     Document Type: Article

References (66)

1. Pierantoni R, Cobellis G, Meccariello R, Fasano S. Evolutionary aspects of cellular communication in the vertebrate hypothalamo-hypophysiogonadal axis. Int Rev Cytol 2002; 218:69-141.
2. Fink G. Neuroendocrine regulation of pituitary function: general principles. In: Conn PM, Freeman ME (eds.), Neuroendocrinology in Physiology and Medicine. Totowa NJ: Humana Press; 2000:107-134.
3. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci U S A 2005; 102:2129-2134.
4. Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, Ghatei MA, Bloom SR. Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 2004; 16:850-858.
5. Ukena K, Tsutsui K. A new member of the hypothalamic RF-amide peptide family, LPXRF-amide peptides: structure, localization, and function. Mass Spectrom Rev 2005; 24:469-486.
6. Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E, Brezillon S, Tyldesley R, Suarez-Huerta N, Vandeput F, Blanpain C, Schiffmann SN, et al. The metastasis suppressor gene KISS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 2001; 276:34631-34636.
7. Hameed S, Jayasena CN, Dhillo WS. Kisspeptin and fertility. J Endocrinol 2011; 208:97-105.
8. Novaira HJ, Ng Y, Wolfe A, Radovick S. Kisspeptin increases GnRH mRNA expression and secretion in GnRH secreting neuronal cell lines. Mol Cell Endocrinol 2009; 311:126-134.
9. Oakley AE, Clifton DK, Steiner RA. Kisspeptin signaling in the brain. Endocr Rev 2009; 30:713-743.
10. Revel FG, Ansel L, Klosen P, Saboureau M, Pévet P, Mikkelsen JD, Simonneaux V. Kisspeptin: a key link to seasonal breeding. Rev Endocr Metab Disord 2007; 8:57-65.
11. Fernandez-Fernandez R, Martini AC, Navarro VM, Castellano JM, Dieguez C, Aguilar E, Pinilla L, Tena-Sempere M. Novel signals for the integration of energy balance and reproduction. Mol Cell Endocrinol 2006; 254-255:127-132.
12. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A. Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci Lett 2006; 401:225-230.
13. Herbison AE. Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: the case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev 2008; 57:277-287.
14. Clarkson J, Herbison AE. Postnatal development of kisspeptin neurons in mouse hypothalamus: sexual dimorphism and projections to gonadotropinreleasing hormone (GnRH) neurons. Endocrinology 2006; 147:5817-5825.
15. Navarro VM, Castellano JM, Fernandez-Fernandez R, Barreiro ML, Roa J, Sanchez-Criado JE, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. Developmental and hormonally regulated messenger ribonucleic acid expression of KISS-1 and its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KISS-1 peptide. Endocrinology 2004; 145:4565-4574.
16. Colledge WH. Kisspeptins and GnRH neuronal signalling. Trends Endocrinol Metab 2009; 20:115-121.
17. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci U S A 2003; 100:10972-10976.
18. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, et al. The GPR54 gene as a regulator of puberty. N Engl J Med 2003; 349:1614-1627.
19. Biran J, Ben-Dor S, Levavi-Sivan B. Molecular identification and functional characterization of the kisspeptin/kisspeptin receptor system in lower vertebrates. Biol Reprod 2008; 79:776-786.
20. Martinez-Chavez CC, Minghetti M, Migaud H. GPR54 and rGnRHI gene expression during the onset of puberty in Nile tilapia. Gen Comp Endocrinol 2008; 156:224-233.
21. Beck BH, Fuller SA, Peatman E, McEntire ME, Darwish A, Freeman DW. Chronic exogenous kisspeptin administration accelerates gonadal development in basses of the genus Morone. Comp Biochem Physiol A Mol Integr Physiol 2012; 162:265-273.
22. Richard N, Corvaiser S, Camacho E, Kottler ML. KISS-1 and GPR54 at the pituitary level: overview and recent insights. Peptides 2009; 30:123-129.
23. Yang B, Jing Q, Chan T, Ko WKW, Wong AOL. Goldfish kisspeptin: molecular cloning, tissue distribution of transcript expression, and stimulatory effects on prolactin, growth hormone and luteinizing hormone secretion and gene expression via direct actions at the pituitary level. Gen Comp Endocrinol 2010; 165:60-71.
24. Lee YR, Tsunekawa K, Moon MJ, Um HN, Hwang JI, Osugi T, Otaki N, Sunakawa Y, Kim K, Vaudry H, Kwon HB, Seong JY, et al. Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology 2009; 150:2837-2846.
25. Moon JS, Lee YR, Oh DY, Hwang JI, Lee JY, Kim JI, Vaudry H, Kwon HB, Seong JY. Molecular cloning of the bullfrog kisspeptin receptor GPR54 with high sensitivity to Xenopus kisspeptin. Peptides 2009; 30:171-179.
26. Tena-Sempere M, Felip A, Gomez A, Zanuy S, Carillo M. Comparative insights of the kisspeptin/kisspeptin receptor system: lessons from nonmammalian vertebrates. Gen Comp Endocrinol 2012; 175:234-243.
27. Um HN, Han JM, Hwang JL, Hong SI, Vaudry H, Seong JY. Molecular coevolution of kisspeptins and their receptors from fish to mammals. Ann N Y Acad Sci 2010; 1200:67-74.
28. Terao Y, Kumano S, Takatsu Y, Hattori M, Nishimura A, Ohtaki T, Shintani Y. Expression of KISS-1, a metastasis suppressor gene, in trophoblast giant cells of the rat placenta. Biochim Biophys Acta 2004; 1678:102-110.
29. Pinto FM, Cejudo-Romàn A, Ravina CG, Fernàndez-Sànchez M, Martin-Lozano D, Illanes M, Tena-Sempere M, Candenas ML. Characterization of the kisspeptin system in human spermatozoa. Int J Androl 2012; 35:63-73.
30. Funes S, Hedrick JA, Vassleva G, Markowitz L, Abbondanzo S, Golovko A, Yang S, Monsma FJ, Gustafson EL. The KISS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 2003; 312:1357-1363.
31. Pierantoni R, Cobellis G, Meccariello R, Palmiero C, Fienga G, Minucci S, Fasano S. The amphibian testis as model to study germ cell progression during spermatogenesis. Comp Biochem Physiol B Biochem Mol Biol 2002; 132:131-139.
32. Rastogi RK, Iela L, Saxena PK, Chieffi G. The control of spermatogenesis in the green frog, Rana esculenta. J Exp Zool 1976; 169:151-166.
33. Chianese R, Ciaramella V, Fasano S, Pierantoni R, Meccariello R. Anandamide modulates the expression of GnRH-II and GnRHRs in frog, Rana esculenta, diencephalons. Gen Comp Endocrinol 2011; 173:389-395.
34. Chianese R, Ciaramella V, Scarpa D, Fasano S, Pierantoni R, Meccariello R. Anandamide regulates the expression of GnRH1, GnRH2 and GnRHRs in frog testis. Am J Physiol Endocrinol Metab 2012; 303:E475-E487.
35. De Rienzo G, Di Sena R, Ferrara D, Palmiero C, Chieffi Baccari G, Minucci S. Temporal and spatial localization of prothymosin a transcript in the Harderian gland of the frog, Rana esculenta. J Exp Zool 2002; 292:633-639.
36. Cobellis G, Pierantoni R, Minucci S, Pernas-Alonso R, Meccariello R, Fasano S. c-fos activity in Rana esculenta testis: seasonal and estradiolinduced changes. Endocrinology 1999; 140:3238-3244.
37. Luque RM, Cordoba-Chacon J, Gamete MD, Navarro VM, Tena-Sempere M, Kineman RD, Castano JP. Kisspeptin regulates gonadotroph and somatotroph function in nonhuman primate pituitary via common and distinct signalling mechanisms. Endocrinology 2011; 152:957-966.
38. Roseweir AK, Kauffman AS, Smith JT, Guerriero KA, Morgan K, Pielecka-Fortuna J, Pineda R, Gottsch ML, Tena-Sempere M, Moenter SM, Terasawa E, Clarke IJ, et al. Discovery of potent kisspeptin antagonists delineate physiological mechanisms of gonadotropin regulation. J Neurosci 2009; 29:3920-3929.
39. Servili A, Le Page Y, Leprince J, Caraty A, Escobar S, Parhar IS, Seong JY, Vaudry H, Kah O. Organization of two independent kisspeptin systems derived from evolutionary-ancient kiss genes in the brain of zebrafish. Endocrinology 2011; 152:1527-1540.
40. Oh DY, Kim K, Kwon HB, Seong JY. Cellular and molecular biology of orphan G protein-coupled receptors. Int Rev Cytol 2006; 252:163-218.
41. Tena-Sempere M. GPR54 and kisspeptin in reproduction. Hum Reprod Update 2006; 12:631-639.
42. Richard N, Galmiche G, Corvaisier S, Caraty A, Kottler ML. KiSS-1 and GPR54 genes are co-expressed in rat gonadotrophs and differentially regulated in vivo by oestradiol and gonadotrophin-releasing hormone. J Neuroendocrinol 2008; 20:381-393.
43. Smith JT, Rao A, Pereira A, Caraty A, Millar RP, Clarke IJ. Kisspeptin is present in ovine hypophysial portal blood but does not increase during the preovulatory luteinizing hormone surge: evidence that gonadotropes are not direct targets of kisspeptin in vivo. Endocrinology 2008; 149:1951-1959.
44. Chang JP, Mar A, Wlasichuk M, Wong AO. Kisspeptin-1 directly stimulates LH and GH secretion from goldfish pituitary cells in a Ca2+ dependent manner. Gen Comp Endocrinol 2012; 179:38-46.
45. Polzonetti-Magni AM, Mosconi G, Carnevali O, Yamamoto K, Hanaoka Y, Kikuyama S. Gonadotropins and reproductive function in the anuran amphibian, Rana esculenta. Biol Reprod 1998; 58:88-93.
46. Fasano S, Minucci S, Pierantoni R, Fasolo A, Di Matteo L, Basile C, Varriale B, Chieffi G. Hypothalamus-hypophysis and testicular GnRH control of gonadal activity in the frog, Rana esculenta: seasonal GnRH profiles and annual variations of in vitro androgen output by pituitarystimulated testes. Gen Comp Endocrinol 1988; 70:31-40.
47. Cobellis G, Meccariello R, Fienga G, Pierantoni R, Fasano S. Cytoplasmic and nuclear Fos protein forms regulate resumption of spermatogenesis in the frog, Rana esculenta. Endocrinology 2002; 143:163-170.
48. Filby AL, van Aerle R, Duitman J, Tyler CR. The kisspeptin/gonadotropin-releasing hormone pathway and molecular signaling of puberty in fish. Biol Reprod 2008; 78:278-289.
49. Navarro VM, Fernández-Fernández R, Castellano JM, Roa J, Mayen A, Barreiro ML, Gaytan F, Aguilar E, Pinilla L, Dieguez C, Tena-Sempere M. Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol 2004; 561:379-386.
50. Ramzan F, Qureshi IZ. Intraperitoneal kisspeptin-10 administration induces dose-dependent degenerative changes in maturing rat testes. Life Sci 2011; 88:246-256.
51. Anjum S, Krishna A, Sridaran R, Tsutsui K. Localization of gonadotropinreleasing hormone (GnRH), gonadotropin-inhibitory hormone (GnIH), kisspeptin and GnRH receptor and their possible roles in testicular activities from birth to senescence in mice. J Exp Zool A Ecol Genet Physiol 2012; 317:630-644.
52. Cobellis G, Cacciola G, Chioccarelli T, Izzo G, Meccariello R, Pierantoni R, Fasano S. Estrogen regulation of the male reproductive tract in the frog, Rana esculenta: a role in Fra-1 activation in peritubular myoid cells and in sperm release. Gen Comp Endocrinol 2008; 155:838-846.
53. Minucci S, Di Matteo L, Chieffi Baccari G, Pierantoni R A gonadotropin releasing hormone analog induces spermiation in intact and hypophysectomized frogs, Rana esculenta. Experientia 1989; 45:1118-1121.
54. Sirianni R, Chimento A, Ruggiero C, De Luca A, Lappano R, Andò S, Maggiolini M, Pezzi V. The novel estrogen receptor, G protein-coupled receptor 30, mediates the proliferative effects induced by 17b-estradiol on mouse spermatogonial GC-1 cell line. Endocrinology 2008; 149:5043-5051.
55. Carreau S, Bois C, Zanatta L, Silva FR, Bouraima-Lelong H, Delalande C. Estrogen signaling in testicular cells. Life Sci 2011; 89:584-587.
56. Chianese R, Chioccarelli T, Cacciola G, Ciaramella V, Fasano S, Pierantoni R, Meccariello R, Cobellis G. The contribution of lower vertebrate animal models in human reproduction research. Gen Comp Endocrinol 2011; 171:17-27.
57. Fasano S, Minucci S, Di Matteo L, D'Antonio M, Pierantoni R. Intratesticular feedback mechanisms in the regulation of steroid profiles in the frog, Rana esculenta. Gen Comp Endocrinol 1989; 75:335-342.
58. Fasano S, D'Antonio M, Pierantoni R. Sites of action of local estradiol feedback mechanism in the frog (Rana esculenta) testis. Gen Comp Endocrinol 1991; 81:492-499.
59. Minucci S, Di Matteo L, Chieffi P, Pierantoni R, Fasano S. 17 betaestradiol effects on mast cell number and spermatogonial mitotic index in the testis of the frog, Rana esculenta. J Exp Zool 1997; 278:93-100.
60. Fasano S, Pierantoni R, Minucci S, Di Matteo L, Chieffi G. Seasonal fluctuations of estrogen binding activity in the testis of the frog, Rana esculenta. Gen Comp Endocrinol 1989; 75:157-161.
61. Clarkson J, Herbison AE. Oestrogen, kisspeptin, GPR54 and the preovulatory luteinising hormone surge. J Neuroendocrinol 2009; 21:305-311.
62. Meccariello R, Chianese R, Fasano S, Pierantoni R. Endocannabinoids and kisspeptins: two modulators in fight for the regulation of GnRH activity. In: J. Vizcarra (ed.), Gonadotropins. Rijeka, Croatia: Intech; 2013:dx.doi.org/10.5772/48443.
63. Tonsfeldt KJ, Goodall CP, Latham KL, Chappell PE. Oestrogen induces rhythmic expression of the Kisspeptin-1 receptor GPR54 in hypothalamic gonadotrophin-releasing hormone-secreting GT1-7 cells. J Neuroendocrinol 2011; 23:823-830.
64. Cobellis G, Meccariello R, Minucci S, Palmiero C, Pierantoni R, Fasano S. Cytoplasmic versus nuclear localization of Fos-related proteins in the frog, Rana esculenta, testis: in vivo and direct in vitro effect of a gonadotropinreleasing hormone agonist. Biol Reprod 2003; 68:954-960.
65. Pierantoni R, Cobellis G, Meccariello R, Cacciola G, Chianese R, Chioccareli T, Fasano S. Testicular GnRH activity, progression of spermatogenesis and sperm transport in vertebrates. Ann N Y Acad Sci 2009; 1163:279-291.
66. Cobellis G, Lombardi M, Scarpa D, Izzo G, Fienga G, Meccariello R, Pierantoni R, Fasano S. Fra1 activity in the frog, Rana esculenta, testis: a new potential role in sperm transport. Biol Reprod 2005; 72:1101-1108.