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Gonadotrophin Receptors

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Endocrinology of the Testis and Male Reproduction

Part of the book series: Endocrinology ((ENDOCR))

Abstract

The two gonadotrophin receptors (GnRs), luteinizing hormone receptor (LHCGR) and follicle-stimulating receptor (FSHR), belong to the glycoprotein hormone receptor subgroup of type A G protein-coupled receptors (GPCRs). LHCGR binds specifically the two structurally similar gonadotrophins, luteinizing hormone (LH) and human chorionic gonadotrophin (hCG), and FSHR binds follicle-stimulating hormone (FSH). The receptors reside on plasma membrane and transmit the gonadotrophin signal to target cells using the classical Gs/adenylyl cyclase/cyclic AMP/protein kinase A signaling cascade. Other signaling pathways (e.g., inositol phosphate, calcium) are activated at pharmacological hormone concentrations or at high receptor density. LHCGR is expressed in testicular Leydig cells and in ovarian theca, luteinizing granulosa and luteal cells. FSHR is expressed in testicular Sertoli cells and ovarian granulosa cells. LHCGR activation stimulated Leydig cell steroidogenesis, in particular testosterone production, while FSHR maintains Sertoli cell metabolism, thereby indirectly stimulating spermatogenesis. Recent basic research, using GnR, expressing cells in vitro and genetically modified mice in vivo, has elucidated novel aspects of the molecular mechanisms of gonadotrophin receptor function. The crystal structure of GnRs has also been partly resolved. Numerous inactivating and activating GnR mutations that have been discovered in patients have unraveled the molecular basis of hypogonadism and other aberrations of reproductive endocrine functions. The purpose of this chapter is to review the recent trends of GnR research and how it has elucidated the molecular mechanisms of GnR function and the role of GnR in human reproductive physiology and pathophysiology.

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References

  • Abel MH, Wootton AN, Wilkins V, Huhtaniemi I, Knight PG, Charlton HM. The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology [Internet]. 2000;141(5):1795–803. Cited 2 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10803590.

    Google Scholar 

  • Agrawal G, Dighe RR. Critical involvement of the hinge region of the follicle-stimulating hormone receptor in the activation of the receptor. J Biol Chem. 2009;284(5):2636–47.

    Article  CAS  PubMed  Google Scholar 

  • Agrawal V, Jaiswal MK, Jaiswal YK. Gonadal and nongonadal FSHR and LHR dysfunction during lipopolysaccharide induced failure of blastocyst implantation in mouse. J Assist Reprod Genet [Internet]. 2012;29(2):163–73. Cited 29 June 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22193751.

    Google Scholar 

  • Aittomäki K, Lucena JL, Pakarinen P, Sistonen P, Tapanainen J, Gromoll J, et al. Mutation in the follicle-stimulating hormone receptor gene causes hereditary hypergonadotropic ovarian failure. Cell [Internet]. 1995;82(6):959–68. Cited 5 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/7553856.

    Google Scholar 

  • Aivatiadou E, Ripolone M, Brunetti F, Berruti G. cAMP-Epac2-mediated activation of Rap1 in developing male germ cells: RA-RhoGAP as a possible direct down-stream effector- PubMed – NCBI. Mol Reprod Dev. 2009;76(4):407–16.

    Google Scholar 

  • Allan CM, Garcia A, Spaliviero J, Zhang F-P, Jimenez M, Huhtaniemi I, et al. Complete Sertoli cell proliferation induced by follicle-stimulating hormone (FSH) independently of luteinizing hormone activity: evidence from genetic models of isolated FSH action. Endocrinology [Internet]. 2004;145(4):1587–93. Cited 19 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/14726449.

    Google Scholar 

  • Allen LA, Achermann JC, Pakarinen P, Kotlar TJ, Huhtaniemi IT, Jameson JL, et al. A novel loss of function mutation in exon 10 of the FSH receptor gene causing hypergonadotrophic hypogonadism: clinical and molecular characteristics. Hum Reprod [Internet]. 2003;18(2):251–6. Cited 5 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12571157.

    Google Scholar 

  • Angelova K, de Jonge H, Granneman JCM, Puett D, Bogerd J. Functional differences of invariant and highly conserved residues in the extracellular domain of the glycoprotein hormone receptors. J Biol Chem. 2010;285(45):34813–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Apaja PM, Harju KT, Aatsinki JT, Petaja-Repo UE, Rajaniemi HJ. Identification and structural characterization of the neuronal luteinizing hormone receptor associated with sensory systems. J Biol Chem [Internet]. 2004;279(3):1899–906. Cited 23 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/14581462.

    Google Scholar 

  • Apaja PM, Tuusa JT, Pietilä EM, Rajaniemi HJ, Petäjä-Repo UE. Luteinizing hormone receptor ectodomain splice variant misroutes the full-length receptor into a subcompartment of the endoplasmic reticulum. Mol Biol Cell [Internet]. 2006;17(5):2243–55. Cited 25 May 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1446094&tool=pmcentrez&rendertype=abstract.

  • Ascoli M, Segaloff D. On the structure of the luteinizing hormone/chorionic gonadotropin receptor*. Endocr Rev [Internet]. 1989;10(1):27–44. Cited 28 June 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/2666109.

    Google Scholar 

  • Ascoli M, Fanelli F, Segaloff DL. The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr Rev. 2002;23(2):141–74.

    Article  CAS  PubMed  Google Scholar 

  • Ayoub MA, Landomiel F, Gallay N, Jégot G, Poupon A, Crépieux P, et al. Assessing gonadotropin receptor function by resonance energy transfer-based assays. Front Endocrinol (Lausanne) [Internet]. 2015;6:130. Cited 4 July 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4550792&tool=pmcentrez&rendertype=abstract.

  • Birdsall NJM. Can different receptors interact directly with each other? Trends Neurosci. 1982;5:137–8.

    Article  CAS  Google Scholar 

  • Boot AM, Lumbroso S, Verhoef-Post M, Richter-Unruh A, Looijenga LHJ, Funaro A, et al. Mutation analysis of the LH receptor gene in Leydig cell adenoma and hyperplasia and functional and biochemical studies of activating mutations of the LH receptor gene. J Clin Endocrinol Metab [Internet]. 2011;96(7):E1197–205. Cited 4 July 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3135199&tool=pmcentrez&rendertype=abstract.

  • Bousfield GR, Butnev VY, Butnev VY, Hiromasa Y, Harvey DJ, May JV. Hypo-glycosylated human follicle-stimulating hormone (hFSH(21/18)) is much more active in vitro than fully-glycosylated hFSH (hFSH(24)). Mol Cell Endocrinol. 2014;382(2):989–97.

    Article  CAS  PubMed  Google Scholar 

  • Bramble MS, Goldstein EH, Lipson A, Ngun T, Eskin A, Gosschalk JE, et al. A novel follicle-stimulating hormone receptor mutation causing primary ovarian failure: a fertility application of whole exome sequencing. Hum Reprod [Internet]. 2016;31(4):905–14. Cited 6 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26911863.

    Google Scholar 

  • Brokken LJS, Lundberg-Giwercman Y, Rajpert De-Meyts E, Eberhard J, StÃ¥hl O, Cohn-Cedermark G, et al. Association of polymorphisms in genes encoding hormone receptors ESR1, ESR2 and LHCGR with the risk and clinical features of testicular germ cell cancer. Mol Cell Endocrinol [Internet]. 2012;351(2):279–85. Cited 3 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22245602.

    Google Scholar 

  • Bukovsky A, Indrapichate K, Fujiwara H, Cekanova M, Ayala ME, Dominguez R, et al. Multiple luteinizing hormone receptor (LHR) protein variants, interspecies reactivity of anti-LHR mAb clone 3B5, subcellular localization of LHR in human placenta, pelvic floor and brain, and possible role for LHR in the development of abnormal pregnancy. Reprod Biol Endocrinol [Internet]. 2003;1:46. Cited 25 May 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=161821&tool=pmcentrez&rendertype=abstract.

  • Butnev VY, Gotschall RR, Baker VL, Moore WT, Bousfield GR. Negative influence of O-linked oligosaccharides of high molecular weight equine chorionic gonadotropin on its luteinizing hormone and follicle-stimulating hormone receptor-binding activities. Endocrinology. 1996;137(6):2530–42.

    Article  CAS  PubMed  Google Scholar 

  • Canto P, Soderlund D, Ramon G, Nishimura E, Mendez JP. Mutational analysis of the luteinizing hormone receptor gene in two individuals with Leydig cell tumors. Am J Med Genet [Internet]. 2002;108(2):148–52. 2002/02/22 ed. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=11857565.

  • Casarini L, Pignatti E, Simoni M. Effects of polymorphisms in gonadotropin and gonadotropin receptor genes on reproductive function. Rev Endocr Metab Disord [Internet]. 2011;12(4):303–21. Cited 28 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21912887.

    Google Scholar 

  • Casarini L, Lispi M, Longobardi S, Milosa F, La Marca A, Tagliasacchi D, et al. LH and hCG action on the same receptor results in quantitatively and qualitatively different intracellular signalling. PLoS ONE [Internet]. Public Library of Science. 2012;7(10):e46682. Cited 22 Apr 2016. Available from: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0046682.

  • Casarini L, Moriondo V, Marino M, Adversi F, Capodanno F, Grisolia C, et al. FSHR polymorphism p.N680S mediates different responses to FSH in vitro. Mol Cell Endocrinol [Internet]. 2014;393(1–2):83–91. Cited 29 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24970684.

  • Casas-González P, Scaglia HE, Pérez-Solís MA, Durand G, Scaglia J, Zariñán T, et al. Normal testicular function without detectable follicle-stimulating hormone. A novel mutation in the follicle-stimulating hormone receptor gene leading to apparent constitutive activity and impaired agonist-induced desensitization and internalization. Mol Cell Endocrinol [Internet]. 2012;364(1–2):71–82. Cited 6 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22954680.

    Google Scholar 

  • Chauhan AR, Prasad M, Chamariya S, Achrekar S, Mahale SD, Mittal K. Novel FSH receptor mutation in a case of spontaneous ovarian hyperstimulation syndrome with successful pregnancy outcome. J Hum Reprod Sci [Internet]. 2015;8(4):230–3. Cited 17 Mar 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4691976&tool=pmcentrez&rendertype=abstract.

  • Chen Z-J, Zhao H, He L, Shi Y, Qin Y, Shi Y, et al. Genome-wide association study identifies susceptibility loci for polycystic ovary syndrome on chromosome 2p16.3, 2p21 and 9q33.3. Nat Genet [Internet]. 2011;43(1):55–9. Cited 28 Mar 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21151128.

    Google Scholar 

  • Choi J, Smitz J. Luteinizing hormone and human chorionic gonadotropin: origins of difference. Mol Cell Endocrinol. 2014;383(1–2):203–13.

    Article  CAS  PubMed  Google Scholar 

  • Chrusciel M, Vuorenoja S, Mohanty B, Rivero-Müller A, Li X, Toppari J, et al. Transgenic GATA-4 expression induces adrenocortical tumorigenesis in C57Bl/6 mice. J Cell Sci [Internet]. The Company of Biologists Ltd; 2013;126(8):1845–57. Cited 25 Sept 2015. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3678410&tool=pmcentrez&rendertype=abstract.

  • Chu L, Li J, Liu Y, Hu W, Cheng CH. Targeted gene disruption in zebrafish reveals noncanonical functions of LH signaling in reproduction. Mol Endocrinol. 2014;28(11):1785–95.

    Article  PubMed  Google Scholar 

  • Cohen BD, Bariteau JT, Magenis LM, Dias JA. Regulation of follitropin receptor cell surface residency by the ubiquitin-proteasome pathway. Endocrinology [Internet]. Endocr Soc. 2011. Cited 26 May 2016. Available from: http://press.endocrine.org/doi/full/10.1210/en.2002-0063.

  • Cole LA. hCG, the wonder of today’s science. Reprod Biol Endocrinol. 2012;10:24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conti M. Specificity of the cyclic adenosine 3′,5′-monophosphate signal in granulosa cell function. Biol Reprod [Internet]. 2002;67(6):1653–61. Cited 26 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12444038.

    Google Scholar 

  • Costagliola S, Panneels V, Bonomi M, Koch J, Many MC, Smits G, et al. Tyrosine sulfation is required for agonist recognition by glycoprotein hormone receptors. EMBO J. 2002;21(4):504–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costagliola S, Urizar E, Mendive F, Vassart G. Specificity and promiscuity of gonadotropin receptors. Reproduction [Internet]. 2005;130(3):275–81. Cited 25 May 2016. Available from: http://www.reproduction-online.org/content/130/3/275.full.

    Google Scholar 

  • De Leener A, Caltabiano G, Erkan S, Idil M, Vassart G, Pardo L, et al. Identification of the first germline mutation in the extracellular domain of the follitropin receptor responsible for spontaneous ovarian hyperstimulation syndrome. Hum Mutat [Internet]. 2008 ;29(1):91–8. Cited 4 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17721928.

  • Desai SS, Achrekar SK, Pathak BR, Desai SK, Mangoli VS, Mangoli R V, et al. Follicle-stimulating hormone receptor polymorphism (G-29A) is associated with altered level of receptor expression in granulosa cells. J Clin Endocrinol Metab [Internet]. 2011;96(9):2805–12. Cited 29 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21752882.

    Google Scholar 

  • Desai SS, Roy BS, Mahale SD. Mutations and polymorphisms in FSH receptor: functional implications in human reproduction. Reproduction [Internet]. 2013;146(6):R235–48. Cited 4 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24051057.

    Google Scholar 

  • Doherty E, Pakarinen P, Tiitinen A, Kiilavuori A, Huhtaniemi I, Forrest S, et al. A Novel mutation in the FSH receptor inhibiting signal transduction and causing primary ovarian failure. J Clin Endocrinol Metab [Internet]. 2002;87(3):1151–5. Cited 6 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11889179.

    Google Scholar 

  • Donadeu FX, Ascoli M. The differential effects of the gonadotropin receptors on aromatase expression in primary cultures of immature rat granulosa cells are highly dependent on the density of receptors expressed and the activation of the inositol phosphate cascade. Endocrinology [Internet]. 2005;146(9):3907–16. Cited 23 May 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1262674&tool=pmcentrez&rendertype=abstract.

  • Dupakuntla M, Mahale SD. Accessibility of the extracellular loops of follicle stimulating hormone receptor and their role in hormone-receptor interaction. Mol Cell Endocrinol. 2010;315(1–2):131–7.

    Article  CAS  PubMed  Google Scholar 

  • Dupakuntla M, Pathak B, Roy BS, Mahale SD. Extracellular loop 2 in the FSH receptor is crucial for ligand mediated receptor activation. Mol Cell Endocrinol. 2012;362(1–2):60–8.

    Article  CAS  PubMed  Google Scholar 

  • Eikvar L, Taskén KA, Eskild W, Hansson V. Protein kinase C activation and positive and negative agonist regulation of 3′,5′-cyclic adenosine monophosphate levels in cultured rat Sertoli cells. Acta Endocrinol (Copenh) [Internet]. 1993;128(6):568–72. Cited 27 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/7687809.

    Google Scholar 

  • El-Gehani F, Zhang FP, Pakarinen P, Rannikko A, Huhtaniemi I. Gonadotropin-independent regulation of steroidogenesis in the fetal rat testis. Biol Reprod [Internet]. 1998;58(1):116–23. Cited 11 July 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9472931.

    Google Scholar 

  • Fan QR, Hendrickson WA. Structure of human follicle-stimulating hormone in complex with its receptor. Nature [Internet]. 2005;433(7023):269–77. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=15662415.

  • Fang L, Yu Y, Zhang R, He J, Sun Y-P. Amphiregulin mediates hCG-induced StAR expression and progesterone production in human granulosa cells. Sci Rep [Internet]. Nature Publishing Group. 2016;6:24917. Cited 5 May 2016. Available from: http://www.nature.com/srep/2016/160426/srep24917/full/srep24917.html.

  • Foulkes NS, Mellström B, Benusiglio E, Sassone-Corsi P. Developmental switch of CREM function during spermatogenesis: from antagonist to activator. Nature [Internet]. 1992;355(6355):80–4. Cited 23 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/1370576.

    Google Scholar 

  • Furtado PS, Moraes F, Lago R, Barros LO, Toralles MB, Barroso U. Gender dysphoria associated with disorders of sex development. Nat Rev Urol [Internet]. Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.; 2012;9(11):620–7. Cited 30 May 2016. Available from: http://dx.doi.org/10.1038/nrurol.2012.182.

    Google Scholar 

  • García-López A, de Jonge H, Nóbrega RH, de Waal PP, van Dijk W, Hemrika W, et al. Studies in zebrafish reveal unusual cellular expression patterns of gonadotropin receptor messenger ribonucleic acids in the testis and unexpected functional differentiation of the gonadotropins. Endocrinology [Internet]. 2010;151(5):2349–60. Cited 27 May 2014. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2869266&tool=pmcentrez&rendertype=abstract.

  • Garverick HA, Baxter G, Gong J, Armstrong DG, Campbell BK, Gutierrez CG, et al. Regulation of expression of ovarian mRNA encoding steroidogenic enzymes and gonadotrophin receptors by FSH and GH in hypogonadotrophic cattle. Reproduction [Internet]. 2002;123(5):651–61. Cited 25 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12006093.

    Google Scholar 

  • Geng Y, Tsai-Morris CH, Zhang Y, Dufau ML. The human luteinizing hormone receptor gene promoter: activation by Sp1 and Sp3 and inhibitory regulation.- PubMed - NCBI. Biochem Biophys Res Commun. 1999;263(2):366–71.

    Google Scholar 

  • George JW, Dille EA, Heckert LL. Current concepts of follicle-stimulating hormone receptor gene regulation. Biol Reprod [Internet]. 2011;84(1):7–17. Cited 10 Feb 2016. Available from: http://www.biolreprod.org/content/84/1/7.full.

    Google Scholar 

  • Ghinea N, Mai T V, Groyer-Picard MT, Milgrom E. How protein hormones reach their target cells. Receptor-mediated transcytosis of hCG through endothelial cells. J Cell Biol [Internet]. 1994;125(1):87–97. Cited 25 May 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2120011&tool=pmcentrez&rendertype=abstract.

  • Gloaguen P, Crépieux P, Heitzler D, Poupon A, Reiter E. Mapping the follicle-stimulating hormone-induced signaling networks. Front Endocrinol (Lausanne) [Internet]. 2011;2:45. Cited 26 Apr 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3364461&tool=pmcentrez&rendertype=abstract.

  • Greb RR, Behre HM, Simoni M. Pharmacogenetics in ovarian stimulation – current concepts and future options. Reprod BioMed Online [Internet]. 2005;11(5):589–600. Cited 28 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16409708.

    Google Scholar 

  • Grigorova M, Punab M, Poolamets O, Sõber S, Vihljajev V, ŽilaitienÄ— B, et al. Study in 1790 Baltic men: FSHR Asn680Ser polymorphism affects total testes volume. Andrology [Internet]. 2013;1(2):293–300. Cited 11 July 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3674532&tool=pmcentrez&rendertype=abstract.

  • Grigorova M, Punab M, Punab AM, Poolamets O, Vihljajev V, ZilaitienÄ— B, et al. Reproductive physiology in young men is cumulatively affected by FSH-action modulating genetic variants: FSHR -29G/A and c.2039 A/G, FSHB -211G/T. PLoS ONE [Internet]. 2014;9(4):e94244. Cited 11 July 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3981791&tool=pmcentrez&rendertype=abstract.

  • Gromoll J, Pekel E, Nieschlag E. The structure and organization of the human follicle-stimulating hormone receptor (FSHR) gene. Genomics [Internet]. 1996a;35(2):308–11. Cited 5 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8661143.

  • Gromoll J, Simoni M, Nieschlag E. An activating mutation of the follicle-stimulating hormone receptor autonomously sustains spermatogenesis in a hypophysectomized man. J Clin Endocrinol Metab [Internet]. 1996/04/01 ed. 1996b;81(4):1367–70. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=8636335.

  • Gromoll J, Simoni M, Nordhoff V, Behre HM, De Geyter C, Nieschlag E. Functional and clinical consequences of mutations in the FSH receptor. Mol Cell Endocrinol [Internet]. 1996c;125(1–2):177–82. Cited 4 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9027356.

    Google Scholar 

  • Gromoll J, Eiholzer U, Nieschlag E, Simoni M. Male hypogonadism caused by homozygous deletion of exon 10 of the luteinizing hormone (LH) receptor: differential action of human chorionic gonadotropin and LH. J Clin Endocrinol Metab [Internet]. 2000/06/14 ed. 2000;85(6):2281–6. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=10852464.

  • Gromoll J, Schulz A, Borta H, Gudermann T, Teerds KJ, Greschniok A, et al. Homozygous mutation within the conserved Ala-Phe-Asn-Glu-Thr motif of exon 7 of the LH receptor causes male pseudohermaphroditism. Eur J Endocrinol [Internet]. 2002;147(5):597–608. Cited 4 July 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12444891.

  • Gromoll J, Wistuba J, Terwort N, Godmann M, Müller T, Simoni M, et al. A new subclass of the luteinizing hormone/chorionic gonadotropin receptor lacking exon 10 messenger RNA in the New World monkey (Platyrrhini) lineage. Biol Reprod [Internet]. 2003/02/28 ed. 2003;69(1):75–80. Cited 20 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12606382.

  • Grzesik P, Teichmann A, Furkert J, Rutz C, Wiesner B, Kleinau G, et al. Differences between lutropin-mediated and choriogonadotropin-mediated receptor activation. FEBS J. 2014;281(5):1479–92.

    Article  CAS  PubMed  Google Scholar 

  • Grzesik P, Kreuchwig A, Rutz C, Furkert J, Wiesner B, Schuelein R, et al. Differences in signal activation by LH and hCG are mediated by the LH/CG receptor’s extracellular hinge region. Front Endocrinol (Lausanne). 2015;6:140.

    Google Scholar 

  • Guillou F, Combarnous Y. Purification of equine gonadotropins and comparative study of their acid-dissociation and receptor-binding specificity. Biochim Biophys Acta [Internet]. 1983/01/25 ed. 1983;755(2):229–36.Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=6299370.

  • Hamalainen T, Poutanen M, Huhtaniemi I. Promoter function of different lengths of the murine luteinizing hormone receptor gene 5′-flanking region in transfected gonadal cells and in transgenic mice. Endocrinology [Internet]. 2001;142(6):2427–34.Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=11356691.

  • Haywood M, Tymchenko N, Spaliviero J, Koch A, Jimenez M, Gromoll J, et al. An activated human follicle-stimulating hormone (FSH) receptor stimulates FSH-like activity in gonadotropin-deficient transgenic mice. Mol Endocrinol [Internet]. Endocrine Society. 2002 ;16(11):2582–91. Cited 3 May 2016. Available from: http://press.endocrine.org/doi/10.1210/me.2002-0032?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub%3dpubmed.

  • Heckert LL, Daley IJ, Griswold MD. Structural organization of the follicle-stimulating hormone receptor gene. Mol Endocrinol [Internet]. 1992;6(1):70–80. Available from: http://www.ncbi.nlm.nih.gov/pubmed/1738373.

    Google Scholar 

  • Hong H, Yan Y, Shi S, Graves SA, Krasteva LK, Nickles RJ, et al. PET of follicle-stimulating hormone receptor: broad applicability to cancer imaging. Mol Pharm [Internet]. 2015;12(2):403–10. Cited 25 May 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4351720&tool=pmcentrez&rendertype=abstract.

  • Huhtaniemi I. A short evolutionary history of FSH-stimulated spermatogenesis. Hormones (Athens) [Internet]. 2015;14(4):468–78. Cited 28 June 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26732152.

  • Huhtaniemi IT, Catt KJ. Differential binding affinities of rat testis luteinizing hormone (LH) receptors for human chorionic gonadotropin, human LH, and ovine LH. Endocrinology [Internet]. 1981;108(5):1931–8. Cited 28 June 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/6260468.

    Google Scholar 

  • Huhtaniemi IT, Eskola V, Pakarinen P, Matikainen T, Sprengel R. The murine luteinizing hormone and follicle-stimulating hormone receptor genes: transcription initiation sites, putative promoter sequences and promoter activity. Mol Cell Endocrinol. 1992;88(1):55–66.

    Article  CAS  PubMed  Google Scholar 

  • Hunzicker-Dunn M, Barisas G, Song J, Roess DA. Membrane organization of luteinizing hormone receptors differs between actively signaling and desensitized receptors. J Biol Chem [Internet] 2003;278(44):42744–9. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12930832.

  • Insel PA, Zhang L, Murray F, Yokouchi H, Zambon AC. Cyclic AMP is both a pro-apoptotic and anti-apoptotic second messenger. Acta Physiol (Oxf) [Internet]. 2012;204(2):277–87. Cited 27 Apr 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3125423&tool=pmcentrez&rendertype=abstract.

  • Jeoung M, Lee C, Ji I, Ji TH. Trans-activation, cis-activation and signal selection of gonadotropin receptors. Mol Cell Endocrinol [Internet]. 2007;260–262:137–43. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=17055146.

  • Jeppesen JV, Kristensen SG, Nielsen ME, Humaidan P, Dal Canto M, Fadini R, et al. LH-receptor gene expression in human granulosa and cumulus cells from antral and preovulatory follicles. J Clin Endocrinol Metab [Internet]. The Endocrine Society. 2012;97(8):E1524–31. Cited 25 May 2016. Available from: /pmc/articles/PMC3410279/?report=abstract.

    Google Scholar 

  • Ji I, Lee C, Jeoung M, Koo Y, Sievert GA, Ji TH. Trans-activation of mutant follicle-stimulating hormone receptors selectively generates only one of two hormone signals. Mol Endocrinol [Internet]. 2004;18(4):968–78. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=14726491.

  • Jiang X, Liu H, Chen X, Chen P-H, Fischer D, Sriraman V, et al. Structure of follicle-stimulating hormone in complex with the entire ectodomain of its receptor. Proc Natl Acad Sci USA. 2012;109(31):12491–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang X, Dias JA, He X. Structural biology of glycoprotein hormones and their receptors: insights to signaling. Mol Cell Endocrinol. 2014a;382(1):424–51.

    Article  CAS  PubMed  Google Scholar 

  • Jiang X, Fischer D, Chen X, McKenna SD, Liu H, Sriraman V, et al. Evidence for follicle-stimulating hormone receptor as a functional trimer. J Biol Chem [Internet]. 2014b;289(20):14273–82. Cited 28 June 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4022893&tool=pmcentrez&rendertype=abstract.

  • Jiang C, Hou X, Wang C, May JV, Butnev VY, Bousfield GR, et al. Hypoglycosylated hFSH has greater bioactivity than fully glycosylated recombinant hFSH in human granulosa cells. J Clin Endocrinol Metab. 2015;100(6):E852–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jo Y, King SR, Khan SA, Stocco DM. Involvement of protein kinase C and cyclic adenosine 3′,5′-monophosphate-dependent kinase in steroidogenic acute regulatory protein expression and steroid biosynthesis in Leydig cells. Biol Reprod [Internet]. 2005;73(2):244–55. Cited 27 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15814901.

    Google Scholar 

  • Jonas KC, Rivero-Müller A, Huhtaniemi IT, Hanyaloglu AC. G protein-coupled receptor transactivation: from molecules to mice. Methods Cell Biol [Internet]. 2012;117:433–50. Cited 6 Oct 2014. Available from: http://www.sciencedirect.com/science/article/pii/B9780124081437000232.

  • Jonas KC, Fanelli F, Huhtaniemi IT, Hanyaloglu AC. Single molecule analysis of functionally asymmetric G protein-coupled receptor (GPCR) oligomers reveals diverse spatial and structural assemblies. J Biol Chem [Internet]. 2015;290(7):3875–92. Cited 15 Feb 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4326798&tool=pmcentrez&rendertype=abstract.

  • Kawate N, Menon KM. Palmitoylation of luteinizing hormone/human choriogonadotropin receptors in transfected cells. Abolition of palmitoylation by mutation of Cys-621 and Cys-622 residues in the cytoplasmic tail increases ligand-induced internalization of the receptor. J Biol Chem. 1994;269(48):30651–8.

    CAS  PubMed  Google Scholar 

  • Kawate N, Kletter GB, Wilson BE, Netzloff ML, Menon KM. Identification of constitutively activating mutation of the luteinising hormone receptor in a family with male limited gonadotrophin independent precocious puberty (testotoxicosis). J Med Genet [Internet]. 1995;32(7):553–4. Cited 28 June 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1050550&tool=pmcentrez&rendertype=abstract.

  • Kendall SK, Samuelson LC, Saunders TL, Wood RI, Camper SA. Targeted disruption of the pituitary glycoprotein hormone alpha-subunit produces hypogonadal and hypothyroid mice. Genes Dev [Internet]. 1995;9(16):2007–19. Cited 26 May 2016. Available from: http://genesdev.cshlp.org/content/9/16/2007.abstract.

    Google Scholar 

  • Klarenbeek JB, Goedhart J, Hink MA, Gadella TWJ, Jalink K. A mTurquoise-based cAMP sensor for both FLIM and ratiometric read-out has improved dynamic range. PLoS ONE [Internet]. 2011 ed. 2011 Jan 29;6(4):e19170. Cited 31 Oct 2012. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=21559477.

  • Kobe B, Deisenhofer J. Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. Nature. 1993;366(6457):751–6.

    Article  CAS  PubMed  Google Scholar 

  • Kossack N, Simoni M, Richter-Unruh A, Themmen APN, Gromoll J. Mutations in a novel, cryptic exon of the luteinizing hormone/chorionic gonadotropin receptor gene cause male pseudohermaphroditism. PLoS Med. 2008;5(4):e88.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kremer H, Kraaij R, Toledo SP, Post M, Fridman JB, Hayashida CY, et al. Male pseudohermaphroditism due to a homozygous missense mutation of the luteinizing hormone receptor gene. Nat Genet [Internet]. 1995;9(2):160–4. Cited 19 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/7719343.

    Google Scholar 

  • Krishnamurthy H, Danilovich N, Morales CR, Sairam MR. Qualitative and quantitative decline in spermatogenesis of the follicle-stimulating hormone receptor knockout (FORKO) mouse. Biol Reprod [Internet]. 2000;62(5):1146–59. Cited 28 June 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10775161.

    Google Scholar 

  • Kuechler A, Hauffa BP, Köninger A, Kleinau G, Albrecht B, Horsthemke B, et al. An unbalanced translocation unmasks a recessive mutation in the follicle-stimulating hormone receptor (FSHR) gene and causes FSH resistance. Eur J Hum Genet [Internet]. 2010;18(6):656–61. Cited 6 May 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2987335&tool=pmcentrez&rendertype=abstract.

  • Kumar TR. Mouse models for gonadotropins: a 15-year saga. Mol Cell Endocrinol [Internet]. 2007;260–262:249–54. Cited 26 May 2016. Available from: http://www.sciencedirect.com/science/article/pii/S0303720706004229.

    Google Scholar 

  • Kumar TR, Wang Y, Lu N, Matzuk MM. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet [Internet]. 1997;15(2):201–4. Cited 14 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9020850.

    Google Scholar 

  • Latronico AC, Anasti J, Arnhold IJ, Rapaport R, Mendonca BB, Bloise W, et al. Brief report: testicular and ovarian resistance to luteinizing hormone caused by inactivating mutations of the luteinizing hormone-receptor gene. N Engl J Med [Internet]. 1996;334(8):507–12. Cited 19 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8559204.

    Google Scholar 

  • Lee C, Ji I, Ryu K, Song Y, Conn PM, Ji TH. Two defective heterozygous luteinizing hormone receptors can rescue hormone action. J Biol Chem [Internet]. 2002a;277(18):15795–800. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=11859079.

  • Lee PSN, Buchan AMJ, Hsueh AJW, Yuen BH, Leung PCK. Intracellular calcium mobilization in response to the activation of human wild-type and chimeric gonadotropin receptors. Endocrinology. 2002b;143(5):1732–40.

    Article  CAS  PubMed  Google Scholar 

  • Lei Y, Hagen GM, Smith SML, Liu J, Barisas G, Roess DA. Constitutively-active human LH receptors are self-associated and located in rafts. Mol Cell Endocrinol [Internet]. 2007;260–262:65–72. Cited 1 Mar 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1904512&tool=pmcentrez&rendertype=abstract.

  • Lend AK, Belousova A, Haller-Kikkatalo K, Punab M, Poolamets O, Peters M, et al. Follicle-stimulating hormone receptor gene haplotypes and male infertility in Estonian population and meta-analysis. Syst Biol Reprod Med [Internet]. 2010;56(1):84–90. Cited 4 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20170288.

    Google Scholar 

  • Liu G, Duranteau L, Carel JC, Monroe J, Doyle DA, Shenker A. Leydig-cell tumors caused by an activating mutation of the gene encoding the luteinizing hormone receptor. N Engl J Med [Internet]. 1999/12/02 ed. 1999;341(23):1731–6. Cited 17 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10580072.

    Google Scholar 

  • Lohse MJ, Benovic JL, Codina J, Caron MG, Lefkowitz RJ. Beta-arrestin: a protein that regulates beta-adrenergic receptor function. Science [Internet]. 1990;248(4962):1547–50. Cited 27 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/2163110.

    Google Scholar 

  • Loss ES, Jacobus AP, Wassermann GF. Rapid signaling responses in Sertoli cell membranes induced by follicle stimulating hormone and testosterone: calcium inflow and electrophysiological changes. Life Sci [Internet]. 2011. ;89(15–16):577–83. Cited 26 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21703282.

    Google Scholar 

  • Ma X, Dong Y, Matzuk MM, Kumar TR. Targeted disruption of luteinizing hormone beta-subunit leads to hypogonadism, defects in gonadal steroidogenesis, and infertility. Proc Natl Acad Sci U S A [Internet]. 2004;101(49):17294–9. Cited 26 May 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=535369&tool=pmcentrez&rendertype=abstract.

  • Manna PR, Stocco DM. The role of specific mitogen-activated protein kinase signaling cascades in the regulation of steroidogenesis. J Signal Transduct [Internet]. 2011;2011:821615. Cited 27 Apr 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3100650&tool=pmcentrez&rendertype=abstract.

  • Mazurkiewicz JE, Herrick-Davis K, Barroso M, Ulloa-Aguirre A, Lindau-Shepard B, Thomas RM, et al. Single-molecule analyses of fully functional fluorescent protein-tagged follitropin receptor reveal homodimerization and specific heterodimerization with lutropin receptor. Biol Reprod [Internet]. 2015;92(4):100. Cited 1 Mar 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25761594.

  • McAllister JM, Legro RS, Modi BP, Strauss JF. Functional genomics of PCOS: from GWAS to molecular mechanisms. Trends Endocrinol Metab [Internet]. 2015;26(3):118–24. Cited 3 May 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4346470&tool=pmcentrez&rendertype=abstract.

  • McFarland KC, Sprengel R, Phillips HS, Köhler M, Rosemblit N, Nikolics K, et al. Lutropin-choriogonadotropin receptor: an unusual member of the G protein-coupled receptor family. Science. 1989;245(4917):494–9.

    Article  CAS  PubMed  Google Scholar 

  • Menon KMJ, Menon B. Structure, function and regulation of gonadotropin receptors – a perspective. Mol Cell Endocrinol [Internet]. 2012;356(1–2):88–97. Cited 25 May 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3327826&tool=pmcentrez&rendertype=abstract.

  • Menon KMJ, Munshi UM, Clouser CL, Nair AK. Regulation of luteinizing hormone/human chorionic gonadotropin receptor expression: a perspective. Biol Reprod [Internet]. 2004;70(4):861–6. Cited 23 May 2016. Available from: http://www.biolreprod.org/content/70/4/861.abstract.

    Google Scholar 

  • Menon B, Franzo-Romain M, Damanpour S, Menon KMJ. Luteinizing hormone receptor mRNA down-regulation is mediated through ERK-dependent induction of RNA binding protein. Mol Endocrinol [Internet]. 2011 ;25(2):282–90. Cited 26 Apr 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3386540&tool=pmcentrez&rendertype=abstract.

  • Meroni SB, Riera MF, Pellizzari EH, Cigorraga SB. Regulation of rat Sertoli cell function by FSH: possible role of phosphatidylinositol 3-kinase/protein kinase B pathway.- PubMed - NCBI. J Endocrinol [Internet]. 2002;174(2):195–204. Cited 26 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12176658.

    Google Scholar 

  • Mertens-Walker I, Bolitho C, Baxter RC, Marsh DJ. Gonadotropin-induced ovarian cancer cell migration and proliferation require extracellular signal-regulated kinase 1/2 activation regulated by calcium and protein kinase C{delta}. Endocr Relat Cancer [Internet]. 2010;17(2):335–49. Cited 27 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20215102.

    Google Scholar 

  • Minegishi T, Nakamura K, Takakura Y, Miyamoto K, Hasegawa Y, Ibuki Y, et al. Cloning and sequencing of human LH/hCG receptor cDNA. Biochem Biophys Res Commun. 1990;172(3):1049–54.

    Article  CAS  PubMed  Google Scholar 

  • Minegishi T, Nakamura K, Takakura Y, Ibuki Y, Igarashi M, Minegish T [corrected to Minegishi T]. Cloning and sequencing of human FSH receptor cDNA. Biochem Biophys Res Commun. 1991;175(3):1125–30.

    Google Scholar 

  • Minegishi T, Tano M, Abe Y, Nakamura K, Ibuki Y, Miyamoto K. Expression of luteinizing hormone/human chorionic gonadotrophin (LH/HCG) receptor mRNA in the human ovary. Mol Hum Reprod [Internet]. 1997;3(2):101–7. Cited 28 June 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9239715.

    Google Scholar 

  • Mitri F, Bentov Y, Behan LA, Esfandiari N, Casper RF. A novel compound heterozygous mutation of the luteinizing hormone receptor -implications for fertility. J Assist Reprod Genet [Internet]. 2014;31(7):787–94. Cited 18 May 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4096877&tool=pmcentrez&rendertype=abstract.

  • Montanelli L, Van Durme JJJ, Smits G, Bonomi M, Rodien P, Devor EJ, et al. Modulation of ligand selectivity associated with activation of the transmembrane region of the human follitropin receptor. Mol Endocrinol [Internet]. 2004;18(8):2061–73. Cited 6 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15166252.

    Google Scholar 

  • Monticone S, Auchus RJ, Rainey WE. Adrenal disorders in pregnancy. Nat Rev Endocrinol [Internet]. 2012;8(11):668–78. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22965163.

    Google Scholar 

  • Müller T, Simoni M, Pekel E, Luetjens CM, Chandolia R, Amato F, et al. Chorionic gonadotrophin beta subunit mRNA but not luteinising hormone beta subunit mRNA is expressed in the pituitary of the common marmoset (Callithrix jacchus). J Mol Endocrinol [Internet]. 2004 ed. 2004 Feb;32(1):115–28. Cited 28 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=14765996.

  • Munier M, Grouleff J, Gourdin L, Fauchard M, Chantreau V, Henrion D, et al. In vitro effects of the endocrine disruptor p,p’DDT on human follitropin receptor. Environ Health Perspect [Internet]. 2016;124(7):991–9. Cited 11 July 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26895433.

    Google Scholar 

  • O’Shaughnessy PJ, Fleming LM, Jackson G, Hochgeschwender U, Reed P, Baker PJ. Endocrinology [Internet]. 2003;144(8):3279–84. Cited 15 Feb 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12865302.

    Google Scholar 

  • Oba Y, Hirai T, Yoshiura Y, Yoshikuni M, HNY K. The duality of fish gonadotropin receptors: cloning and functional characterization of a second gonadotropin receptor cDNA expressed in the ovary and testis of amago salmon (Oncorhynchus rhodurus). Biochem Biophys Res Commun. 1999;265(2):366–71.

    Article  CAS  PubMed  Google Scholar 

  • Osuga Y, Hayashi M, Kudo M, Conti M, Kobilka B, Hsueh AJ. Co-expression of defective luteinizing hormone receptor fragments partially reconstitutes ligand-induced signal generation. J Biol Chem [Internet]. 1997;272(40):25006–12. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=9312107.

  • Pakarainen T, Zhang FP, Poutanen M, Huhtaniemi I. Fertility in luteinizing hormone receptor-knockout mice after wild-type ovary transplantation demonstrates redundancy of extragonadal luteinizing hormone action. J Clin Invest [Internet] 2005;115(7):1862–8. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=15951841.

  • Pakarainen T, Ahtiainen P, Zhang F-P, Rulli S, Poutanen M, Huhtaniemi I. Extragonadal LH/hCG action—not yet time to rewrite textbooks. Mol Cell Endocrinol [Internet]. 2007;269(1–2):9–16. Cited 2016 Jun 28. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17350753.

    Google Scholar 

  • Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, et al. Crystal structure of rhodopsin: a G protein-coupled receptor. Science. 2000;289(5480):739–45.

    Article  CAS  PubMed  Google Scholar 

  • Paramonov VM, Mamaeva V, Sahlgren C, Rivero-Müller A. Genetically-encoded tools for cAMP probing and modulation in living systems. Front Pharmacol [Internet]. 2015;6:196. Cited 30 Oct 2015. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4569861&tool=pmcentrez&rendertype=abstract.

  • Peltoketo H, Rivero-Muller A, Ahtiainen P, Poutanen M, Huhtaniemi I, Rivero-Müller Consequences of genetic manipulations of gonadotrophins and gonadotrophin receptors in mice. Ann Endocrinol [Internet]. 2010/04/07 ed. 2010;71(3):170–6. Cited 30 May 2012. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20362970.

    Google Scholar 

  • Piersma D, Berns EM, Verhoef-Post M, Uitterlinden AG, Braakman I, Pols HA, et al. A common polymorphism renders the luteinizing hormone receptor protein more active by improving signal peptide function and predicts adverse outcome in breast cancer patients. J Clin Endocrinol Metab [Internet]. 2006;91(4):1470–6. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16464948.

  • Pietilä EM, Tuusa JT, Apaja PM, Aatsinki JT, Hakalahti AE, Rajaniemi HJ, et al. Inefficient maturation of the rat luteinizing hormone receptor. A putative way to regulate receptor numbers at the cell surface. J Biol Chem [Internet]. 2005;280(28):26622–9. Cited 26 May 2016. Available from: http://www.jbc.org/content/280/28/26622.full.

    Google Scholar 

  • Pitcher JA, Tesmer JJ, Freeman JL, Capel WD, Stone WC, Lefkowitz RJ. Feedback inhibition of G protein-coupled receptor kinase 2 (GRK2) activity by extracellular signal-regulated kinases. J Biol Chem [Internet]. 1999;274(49):34531–4. Cited 27 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10574913.

    Google Scholar 

  • Powell BL, Piersma D, Kevenaar ME, van Staveren IL, Themmen APN, Iacopetta BJ, et al. Luteinizing hormone signaling and breast cancer: polymorphisms and age of onset. J Clin Endocrinol Metab [Internet]. 2003;88(4):1653–7. Cited 3 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12679452.

    Google Scholar 

  • Premont RT, Macrae AD, Stoffel RH, Chung N, Pitcher JA, Ambrose C, et al. Characterization of the G protein-coupled receptor kinase GRK4. Identification of four splice variants. J Biol Chem [Internet]. 1996 ed. 1996 Mar 15;271(11):6403–10. Cited 25 May 2016. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=8626439.

  • Qanbar R, Bouvier M. Role of palmitoylation/depalmitoylation reactions in G-protein-coupled receptor function. Pharmacol Ther [Internet]. 2003;97(1):1–33. Cited 23 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12493533.

    Google Scholar 

  • Radu A, Pichon C, Camparo P, Antoine M, Allory Y, Couvelard A, et al. Expression of follicle-stimulating hormone receptor in tumor blood vessels. N Engl J Med [Internet]. 2010/10/22 ed. 2010;363(17):1621–30. Cited 13 Feb 2016. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=20961245.

  • Reiter E, Lefkowitz RJ. GRKs and beta-arrestins: roles in receptor silencing, trafficking and signaling. Trends Endocrinol Metab [Internet]. 2006;17(4):159–65. Cited 1 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16595179.

  • Richter-Unruh A, Verhoef-Post M, Malak S, Homoki J, Hauffa BP, Themmen APN. Leydig cell hypoplasia: absent luteinizing hormone receptor cell surface expression caused by a novel homozygous mutation in the extracellular domain. J Clin Endocrinol Metab [Internet]. 2004;89(10):5161–7. Cited 25 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15472221.

    Google Scholar 

  • Risma KA, Clay CM, Nett TM, Wagner T, Yun J, Nilson JH. Targeted overexpression of luteinizing hormone in transgenic mice leads to infertility, polycystic ovaries, and ovarian tumors. Proc Natl Acad Sci U S A [Internet]. National Academy of Sciences. 1995;92(5):1322–6. Cited 11 July 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/7877975.

  • Rivero-Müller A, Chou Y-YY-Y, Ji I, Lajic S, Hanyaloglu AC, Jonas K, et al. Rescue of defective G protein-coupled receptor function in vivo by intermolecular cooperation. Proc Natl Acad Sci U S A [Internet]. 2010 ed. National Acad Sciences. 2010;107(5):2319–24. Cited 16 Mar 2012. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=20080658.

  • Rivero-Müller A, Potorac I, Pintiaux A, Daly AF, Thiry A, Rydlewski C, et al. A novel inactivating mutation of the LH/chorionic gonadotrophin receptor with impaired membrane trafficking leading to Leydig cell hypoplasia type 1. Eur J Endocrinol [Internet]. 2015;172(6):K27–36. Cited 25 Sept 2015. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25795638.

    Google Scholar 

  • Rodien P, Cetani F, Costagliola S, Tonacchera M, Duprez L, Minegishi T, et al. Evidences for an allelic variant of the human LC/CG receptor rather than a gene duplication: functional comparison of wild-type and variant receptors. J Clin Endocrinol Metab [Internet]. 1998;83(12):4431–4. Cited 3 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9851790.

    Google Scholar 

  • Roess DA, Horvat RD, Munnelly H, Barisas BG. Luteinizing hormone receptors are self-associated in the plasma membrane. Endocrinology [Internet]. 2000;141(12):4518–23. Cited 1 Mar 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11108263.

  • Rulli SB, Kuorelahti A, Karaer O, Pelliniemi LJ, Poutanen M, Huhtaniemi I. Reproductive disturbances, pituitary lactotrope adenomas, and mammary gland tumors in transgenic female mice producing high levels of human chorionic gonadotropin. Endocrinology [Internet]. 2002;143(10):4084–95. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12239120.

  • Sangkhathat S, Kanngurn S, Jaruratanasirikul S, Tubtawee T, Chaiyapan W, Patrapinyokul S, et al. Peripheral precocious puberty in a male caused by Leydig cell adenoma harboring a somatic mutation of the LHR gene: report of a case. J Med Assoc Thail [Internet]. 2010;93(9):1093–7. Cited 28 June 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20873084.

  • Schubert RL, Narayan P, Puett D. Specificity of cognate ligand-receptor interactions: fusion proteins of human chorionic gonadotropin and the heptahelical receptors for human luteinizing hormone, thyroid-stimulating hormone, and follicle-stimulating hormone. Endocrinology. 2003;144(1):129–37.

    Article  CAS  PubMed  Google Scholar 

  • Shetty G, Weng CCY, Porter KL, Zhang Z, Pakarinen P, Kumar TR, et al. Spermatogonial differentiation in juvenile spermatogonial depletion (jsd) mice with androgen receptor or follicle-stimulating hormone mutations. Endocrinology [Internet]. 2006;147(7):3563–70. Cited 28 June 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16627582.

    Google Scholar 

  • Shi Y, Zhao H, Shi Y, Cao Y, Yang D, Li Z, et al. Genome-wide association study identifies eight new risk loci for polycystic ovary syndrome. Nat Genet [Internet]. 2012;44(9):1020–1025. Cited 3 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22885925.

    Google Scholar 

  • Simoni M, Casarini L. Mechanisms in endocrinology: genetics of FSH action: a 2014-and-beyond view. Eur J Endocrinol [Internet]. 2014;170(3):R91–107. Cited 28 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24288354.

    Google Scholar 

  • Simoni M, Gromoll J, Nieschlag E. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr Rev. 1997;18(6):739–73.

    CAS  PubMed  Google Scholar 

  • Simoni M, Gromoll J, Höppner W, Kamischke A, Krafft T, Stähle D, et al. Mutational analysis of the follicle-stimulating hormone (FSH) receptor in normal and infertile men: identification and characterization of two discrete FSH receptor isoforms. J Clin Endocrinol Metab [Internet]. 1999;84(2):751–5. Cited 29 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10022448.

    Google Scholar 

  • Simoni M, Tüttelmann F, Michel C, Böckenfeld Y, Nieschlag E, Gromoll J. Polymorphisms of the luteinizing hormone/chorionic gonadotropin receptor gene: association with maldescended testes and male infertility. Pharmacogenet Genomics [Internet]. 2008;18(3):193–200. Cited 3 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18300940.

    Google Scholar 

  • Simoni M, Santi D, Negri L, Hoffmann I, Muratori M, Baldi E, et al. Treatment with human, recombinant FSH improves sperm DNA fragmentation in idiopathic infertile men depending on the FSH receptor polymorphism p.N680S: a pharmacogenetic study. Hum Reprod. 2016;31:1960.

    Article  PubMed  Google Scholar 

  • Smith SM, Lei Y, Liu J, Cahill ME, Hagen GM, Barisas BG, et al. Luteinizing hormone receptors translocate to plasma membrane microdomains after binding of human chorionic gonadotropin. Endocrinology [Internet] 2006;147(4):1789–95. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16410308.

  • Smits G, Campillo M, Govaerts C, Janssens V, Richter C, Vassart G, et al. Glycoprotein hormone receptors: determinants in leucine-rich repeats responsible for ligand specificity. EMBO J. 2003a;22(11):2692–703.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smits G, Olatunbosun O, Delbaere A, Pierson R, Vassart G, Costagliola S. Ovarian hyperstimulation syndrome due to a mutation in the follicle-stimulating hormone receptor. N Engl J Med [Internet]. 2003b;349(8):760–6. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12930928.

  • So W-K, Kwok H-F, Ge W. Zebrafish gonadotropins and their receptors: II. Cloning and characterization of zebrafish follicle-stimulating hormone and luteinizing hormone subunits – their spatial-temporal expression patterns and receptor specificity. Biol Reprod [Internet]. 2005;72(6):1382–96. Cited 1 July 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15728794.

  • Sprengel R, Braun T, Nikolics K, Segaloff DL, Seeburg PH. The testicular receptor for follicle stimulating hormone: structure and functional expression of cloned cDNA. Mol Endocrinol. 1990;4(4):525–30.

    Article  CAS  PubMed  Google Scholar 

  • Stewart F, Allen WR. The binding of FSH, LH and PMSG to equine gonadal tissues. J Reprod Fertil Suppl [Internet]. 1979 ed. 1979;(27):431–40. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=225496.

  • Stewart F, Allen WR. Biological functions and receptor binding activities of equine chorionic gonadotrophins. J Reprod Fertil [Internet]. 1981 ed. 1981;62(2):527–36. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=6265633.

  • Tano M, Minegishi T, Nakamura K, Karino S, Ibuki Y, Miyamoto K. Transcriptional and post-transcriptional regulation of FSH receptor in rat granulosa cells by cyclic AMP and activin. J Endocrinol [Internet]. 1997;153(3):465–73. Cited 23 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9204001.

    Google Scholar 

  • Tao Y-XX, Johnson NB, Segaloff DL. Constitutive and agonist-dependent self-association of the cell surface human lutropin receptor. J Biol Chem [Internet]. 2004;279(7):5904–14. Cited 1 Mar 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/14594799.

  • Tapanainen JS, Aittomäki K, Min J, Vaskivuo T, Huhtaniemi IT. Men homozygous for an inactivating mutation of the follicle-stimulating hormone (FSH) receptor gene present variable suppression of spermatogenesis and fertility. Nat Genet [Internet]. 1997;15(2):205–6. Cited 28 Mar 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9020851.

    Google Scholar 

  • Teo AED, Garg S, Shaikh LH, Zhou J, Karet Frankl FE, Gurnell M, et al. Pregnancy, primary aldosteronism, and adrenal CTNNB1 mutations. N Engl J Med [Internet]. Massachusetts Medical Society; 2015;373(15):1429–36. Cited 26 May 2016. Available from: http://www.nejm.org/doi/full/10.1056/NEJMoa1504869?rss=searchAndBrowse#t=article.

    Google Scholar 

  • Thomas RM, Nechamen CA, Mazurkiewicz JE, Muda M, Palmer S, Dias JA. Follice-stimulating hormone receptor forms oligomers and shows evidence of carboxyl-terminal proteolytic processing. Endocrinology [Internet]. 2007 ed. 2007;148(5):1987–95. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=17272391.

  • Thomas RM, Nechamen CA, Mazurkiewicz JE, Ulloa-Aguirre A, Dias JA. The adapter protein APPL1 links FSH receptor to inositol 1,4,5-trisphosphate production and is implicated in intracellular Ca(2+) mobilization. Endocrinology [Internet]. 2011. Cited 27 Apr 2016;152(4):1691–701. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3060640&tool=pmcentrez&rendertype=abstract.

  • Timossi C, Maldonado D, Vizcaino A, Lindau-Shepard B, Conn PM, Ulloa-Aguirre A. Structural determinants in the second intracellular loop of the human follicle-stimulating hormone receptor are involved in nnnn(s) protein activation. Mol Cell Endocrinol [Internet]. 2002 ed. 2002;189(1–2):157–68. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12039074.

  • Tranchant T, Durand G, Gauthier C, Crépieux P, Ulloa-Aguirre A, Royère D, et al. Preferential β-arrestin signalling at low receptor density revealed by functional characterization of the human FSH receptor A189 V mutation. Mol Cell Endocrinol [Internet]. 2011.;331(1):109–18. Cited 27 Apr 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20801186.

    Google Scholar 

  • Trehan A, Rotgers E, Coffey ETE, Huhtaniemi I, Rivero-Müller A. CANDLES assay for monitoring GPCR induced cAMP generation in cell cultures. Cell Commun Signal [Internet]. 2014;12:70. Cited 25 Nov 2014. Available from: http://www.biosignaling.com/content/12/1/70.

  • Trehan A, KieÅ‚bus M, Czapinski J, Stepulak A, Huhtaniemi IT, Rivero-Müller A. REPLACR-mutagenesis, a one-step method for site-directed mutagenesis by recombineering. Sci Rep [Internet]. Macmillan Publishers Limited. 2015;5:19121. Available from: http://dx.doi.org/10.1038/srep19121.

  • Troppmann B, Kleinau G, Krause G, Gromoll J. Structural and functional plasticity of the luteinizing hormone/choriogonadotrophin receptor. Hum Reprod Update. 2013;19(5):583–602.

    Article  CAS  PubMed  Google Scholar 

  • Tüttelmann F, Laan M, Grigorova M, Punab M, Sõber S, Gromoll J. Combined effects of the variants FSHB −211G>T and FSHR 2039A>G on male reproductive parameters. J Clin Endocrinol Metab [Internet]. 2012;97(10):3639–47. Cited 28 June 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22791757.

  • Ulloa-Aguirre A, Dias JA, Bousfield G, Huhtaniemi I, Reiter E. Trafficking of the follitropin receptor. Methods Enzymol [Internet]. 2013;521:17–45. Cited 27 Apr 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4503599&tool=pmcentrez&rendertype=abstract.

  • Ulloa-Aguirre A, Reiter E, Bousfield G, Dias JA, Huhtaniemi I. Constitutive activity in gonadotropin receptors. Adv Pharmacol [Internet]. 2014;70:37–80. Cited 4 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24931192.

  • Uribe A, Zariñán T, Pérez-Solis MA, Gutiérrez-Sagal R, Jardón-Valadez E, Piñeiro A, et al. Functional and structural roles of conserved cysteine residues in the carboxyl-terminal domain of the follicle-stimulating hormone receptor in human embryonic kidney 293 cells. Biol Reprod [Internet]. 2008 ed. 2008 May 1 ;78(5):869–82. Cited 23 May 2016. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18199880.

  • Urizar E, Montanelli L, Loy T, Bonomi M, Swillens S, Gales C, et al. Glycoprotein hormone receptors: link between receptor homodimerization and negative cooperativity. EMBO J [Internet]. 2005;24(11):1954–64. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=15889138.

  • van Koppen CJ, Verbost PM, van de Lagemaat R, Karstens W-JF, Loozen HJJ, van Achterberg TAE, et al. Signaling of an allosteric, nanomolar potent, low molecular weight agonist for the follicle-stimulating hormone receptor. Biochem Pharmacol. 2013;85(8):1162–70.

    Article  PubMed  Google Scholar 

  • Vischer HF, Granneman JCM, Linskens MHK, Schulz RW, Bogerd J. Both recombinant African catfish LH and FSH are able to activate the African catfish FSH receptor. J Mol Endocrinol [Internet]. 2003;31(1):133–40. Cited 1 July 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12914531.

  • Vu Hai MT, Lescop P, Loosfelt H, Ghinea N. Receptor-mediated transcytosis of follicle-stimulating hormone through the rat testicular microvasculature. Biol Cell [Internet]. 2004;96(2):133–44. Cited 25 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15050368.

    Google Scholar 

  • Walker WH, Habener JF. Role of transcription factors CREB and CREM in cAMP-regulated transcription during spermatogenesis. Trends Endocrinol Metab. 1996 [Internet];7(4):133–8. Cited 23 Jan 2016. Available: fromhttp://www.ncbi.nlm.nih.gov/pubmed/18406739.

  • Watanabe AM, McConnaughey MM, Strawbridge RA, Fleming JW, Jones LR, Besch Jr. HR. Muscarinic cholinergic receptor modulation of beta-adrenergic receptor affinity for catecholamines. J Biol Chem [Internet]. 1978 ed. 1978;253(14):4833–6. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=209018.

  • Wu XQ, Xu SM, Wang YQ, Li Q, Wang ZQ, Zhang CL, et al. FSHR gene Thr307Ala and Asn680Ser polymorphisms in infertile men: an association study in North China and meta-analysis. Genet Mol Res [Internet]. 2015;14(2):5592–601. Cited 11 July 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26125757.

    Google Scholar 

  • Yang E-J, Nasipak BT, Kelley DB. Direct action of gonadotropin in brain integrates behavioral and reproductive functions. Proc Natl Acad Sci USA [Internet]. 2007;104(7):2477–82. Cited 23 May 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1893001&tool=pmcentrez&rendertype=abstract.

  • Yao Z, Petschnigg J, Ketteler R, Stagljar I. Application guide for omics approaches to cell signaling. Nat Chem Biol. Nature Publishing Group. 2015;11(6):387.

    Google Scholar 

  • Zhang Y, Dufau ML. Dual mechanisms of regulation of transcription of luteinizing hormone receptor gene by nuclear orphan receptors and histone deacetylase complexes. J Steroid Biochem Mol Biol [Internet]. 2003;85(2–5):401–414. Cited 25 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12943729.

    Google Scholar 

  • Zhang R, Xie X. Tools for GPCR drug discovery. Acta Pharmacol Sin [Internet]. Nature Publishing Group. 2012;33(3):372–84. Cited 3 July 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22266728.

    Google Scholar 

  • Zhang R, Cai H, Fatima N, Buczko E, Dufau ML. Functional glycosylation sites of the rat luteinizing hormone receptor required for ligand binding. J Biol Chem [Internet]. 1995;270(37):21722–8. Cited 26 May 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/7665591.

    Google Scholar 

  • Zhang FP, Rannikko AS, Manna PR, Fraser HM, Huhtaniemi IT. Cloning and functional expression of the luteinizing hormone receptor complementary deoxyribonucleic acid from the marmoset monkey testis: absence of sequences encoding exon 10 in other species. Endocrinology. 1997;138(6):2481–90.

    Article  CAS  PubMed  Google Scholar 

  • Zhang F-P, Pakarainen T, Poutanen M, Toppari J, Huhtaniemi I. The low gonadotropin-independent constitutive production of testicular testosterone is sufficient to maintain spermatogenesis. Proc Natl Acad Sci USA [Internet]. 2003;100(23):13692–7. Cited 14 May 2016. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=263875&tool=pmcentrez&rendertype=abstract.

  • Zhang Z, Lau S-W, Zhang L, Ge W. Disruption of zebrafish follicle-stimulating hormone receptor (fshr) But not luteinizing hormone receptor (lhcgr) gene by TALEN leads to failed follicle activation in females followed by sexual reversal to males. Endocrinology. 2015a;156:3747–62. http://dx.doi.org/10.1210/en.2015-1039. Endocrine Society Chevy Chase, MD.

    Google Scholar 

  • Zhang Z, Zhu B, Ge W. Genetic analysis of zebrafish gonadotropin (FSH and LH) functions by TALEN-mediated gene disruption. Mol Endocrinol [Internet]. 2015b;29(1):76–98. Cited 1 July 2016. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25396299.

    Google Scholar 

  • Ziecik AJ, Jedlinska M, Rzucidlo SJ. Effect of estradiol and progesterone on myometrial LH/hCG receptors in pigs. Eur J Endocrinol [Internet]. Eur Soc Endocrinol. 1992;127(2):185–8. Cited 28 June 2016. Available from: http://www.eje-online.org/cgi/doi/10.1530/acta.0.1270185.

    Google Scholar 

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Casarini, L., Huhtaniemi, I., Simoni, M., Rivero-Müller, A. (2016). Gonadotrophin Receptors. In: Simoni, M., Huhtaniemi, I. (eds) Endocrinology of the Testis and Male Reproduction. Endocrinology. Springer, Cham. https://doi.org/10.1007/978-3-319-29456-8_4-1

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