Impaired fibroblast growth factor receptor 1 signaling as a cause of normosmic idiopathic hypogonadotropic hypogonadism

Journal of Clinical Endocrinology and Metabolism

Volumn 94, Issue 11, 2009, Pages 4380-4390

  Raivio, Taneli ^a,h   Sidis, Yisrael ^a   Plummer, Lacey ^a   Chen, Huaibin ^c   Ma, Jinghong ^c   Mukherjee, Abir ^a   Jacobson Dickman, Elka ^a   Quinton, Richard ^d   Van Vliet, Guy ^e   Lavoie, Helene ^f   Hughes, Virginia A ^a   Dwyer, Andrew ^a   Hayes, Frances J ^a   Xu, Shuyun ^b   Sparks, Susan ^g   Kaiser, Ursula B ^b   Mohammadi, Moosa ^c   Pitteloud, Nelly ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e UNIVERSITY OF MONTREAL   (Canada)

^f CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^g CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^h UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 1; PROTEIN TYROSINE KINASE;

ADULT; ALLELE; ARTICLE; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVITY; FAMILY; FEMALE; GENE LOCUS; GENE SEQUENCE; GENETIC DISORDER; GENOTYPE; GLYCOSYLATION; HETEROZYGOSITY; HUMAN; HYPOGONADOTROPIC HYPOGONADISM; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; MUTANT; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; RECEPTOR AFFINITY; REPRODUCTION; SIGNAL TRANSDUCTION;

EID: 70449103248     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2009-0179     Document Type: Article

References (53)

1. Santoro N, Filicori M, Crowley Jr WF 1986 Hypogonadotropic disorders in men and women: diagnosis and therapy with pulsatile gonadotropin-releasing hormone. Endocr Rev 7:11-23
2. Seminara SB, Hayes FJ, Crowley Jr WF 1998 Gonadotropin-releasing hormone deficiency in the human (idiopathic hypogonadotropic hypogonadism and Kallmann's syndrome): pathophysiological and genetic considerations. Endocr Rev 19:521-539
3. Quinton R, Duke VM, Robertson A, Kirk JM, Matfin G, de Zoysa PA, Azcona C, MacColl GS, Jacobs HS, Conway GS, Besser M, Stanhope RG, Bouloux PM 2001 Idiopathic gonadotrophin deficiency: genetic questions addressed through phenotypic characterization. Clin Endocrinol (Oxf) 55:163-174 (Pubitemid 32868580)
4. Sato N, Katsumata N, Kagami M, Hasegawa T, Hori N, Kawakita S, Minowada S, Shimotsuka A, Shishiba Y, Yokozawa M, Yasuda T, Nagasaki K, Hasegawa D, Hasegawa Y, Tachibana K, Naiki Y, Horikawa R, Tanaka T, Ogata T 2004 Clinical assessment and mutation analysis of Kallmann syndrome 1 (KAL1) and fibroblast growth factor receptor 1 (FGFR1, or KAL2) in five families and 18 sporadic patients. J Clin Endocrinol Metab 89:1079-1088 (Pubitemid 38368394)
5. Kim SH, Hu Y, Cadman S, Bouloux P 2008 Diversity in fibroblast growth factor receptor 1 regulation: learning from the investigation of Kallmann syndrome. J Neuroendocrinol 20:141-163 (Pubitemid 351147002)
6. Chung WC, Moyle SS, Tsai PS 2008 Fibroblast growth factor 8 signaling through fibroblast growth factor receptor 1 is required for the emergence of gonadotropin-releasing hormone neurons. Endocrinology 149:4997-5003
7. Legouis R, Hardelin JP, Levilliers J, Claverie JM, Compain S, Wunderle V, Millasseau P, Le Paslier D, Cohen D, Caterina D, Bougueleret L, Delemarre-van de Waal HA, Lutfalla G, Weissenbach J, Petit C 1991 The candidate gene for the X-linked Kallmann syndrome encodes a protein related to adhesion molecules. Cell 67: 423-435 (Pubitemid 121001457)
8. Franco B, Guioli S, Pragliola A, Incerti B, Bardoni B, Tonlorenzi R, Carrozzo R, Maestrini E, Pieretti M, Taillon-Miller P, Brown CJ, Willard HF, Lawrence C, Persico MG, Camerino G, Ballabio A 1991 A gene deleted in Kallmann's syndrome shares homology with neural cell adhesion and axonal path-finding molecules. Nature 353: 529-536 (Pubitemid 21912544)
9. Dodé C, Levilliers J, Dupont JM, De Paepe A, Le Dû N, Soussi- Yanicostas N, Coimbra RS, Delmaghani S, Compain-Nouaille S, Baverel F, Pêcheux C, Le Tessier D, Cruaud C, Delpech M, Speleman F, Vermeulen S, Amalfitano A, Bachelot Y, Bouchard P, Cabrol S, Carel JC, Delemarre-van de Waal H, Goulet-Salmon B, Kottler ML, Richard O, Sanchez-Franco F, Saura R, Young J, Petit C, Hardelin JP 2003 Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nat Genet 33:463-465 (Pubitemid 36390006)
10. Falardeau J, Chung WC, Beenken A, Raivio T, Plummer L, Sidis Y, Jacobson-Dickman EE, Eliseenkova AV, Ma J, Dwyer A, Quinton R, Na S, Hall JE, Huot C, Alois N, Pearce SH, Cole LW, Hughes V, Mohammadi M, Tsai P, Pitteloud N 2008 Decreased FGF8 signaling causes deficiency of gonadotropin-releasing hormone in humans and mice. J Clin Invest 118:2822-2831
11. de Roux N, Young J, Misrahi M, Genet R, Chanson P, Schaison G, Milgrom E 1997 A family with hypogonadotropic hypogonadism and mutations in the gonadotropin-releasing hormone receptor. N Engl J Med 337:1597-1602 (Pubitemid 27509763)
12. Pitteloud N, Quinton R, Pearce S, Raivio T, Acierno J, Dwyer A, Plummer L, Hughes V, Seminara S, Cheng YZ, Li WP, Maccoll G, Eliseenkova AV, Olsen SK, Ibrahimi OA, Hayes FJ, Boepple P, Hall JE, Bouloux P, Mohammadi M ,Crowley W 2007 Digenic mutations account for variable phenotypes in idiopathic hypogonadotropic hypogonadism. J Clin Invest 117:457-463 (Pubitemid 46203974)
13. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E 2003 Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 100:10972-10976 (Pubitemid 37140137)
14. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno Jr JS, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O'Rahilly S, Carlton MB, Crowley Jr WF, Aparicio SA, Colledge WH 2003 The GPR54 gene as a regulator of puberty. N Engl J Med 349:1614-1627
15. Dode C, Teixeira L, Levilliers J, Fouveaut C, Bouchard P, Kottler ML, Lespinasse J, Lienhardt-Roussie A, Mathieu M, Moerman A, Morgan G, Murat A, Toublanc JE, Wolczynski S, Delpech M, Petit C, Young J, Hardelin JP 2006 Kallmann syndrome: mutations in the genes encoding prokineticin-2 and prokineticin receptor-2. PLoS Genet 2:e175 (Pubitemid 44656538)
16. Kim HG, Kurth I, Lan F, Meliciani I, Wenzel W, Eom SH, Kang GB, Rosenberger G, Tekin M, Ozata M, Bick DP, Sherins RJ, Walker SL, Shi Y, Gusella JF, Layman LC 2008 Mutations in CHD7, encoding a chromatin-remodeling protein, cause idiopathic hypogonadotropic hypogonadism and Kallmann syndrome. Am J Hum Genet 83:511-519
17. Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, Porter KM, Serin A, Mungan NO, Cook JR, Ozbek MN, Imamoglu S, Akalin NS, Yuksel B, O'Rahilly S, Semple RK 2009 TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for Neurokinin B in the central control of reproduction. Nat Genet 41:354-358
18. Hébert JM, Lin M, Partanen J, Rossant J, McConnell SK 2003 FGF signaling through FGFR1 is required for olfactory bulb morphogenesis. Development 130:1101-1111 (Pubitemid 36395692)
19. Mohammadi M, Olsen SK, Ibrahimi OA 2005 Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev 16:107-137 (Pubitemid 40616111)
20. Parodi AJ 2000 Protein glucosylation and its role in protein folding. Annu Rev Biochem 69:69-93 (Pubitemid 30792204)
21. Partridge EA, Le Roy C, Di Guglielmo GM, Pawling J, Cheung P, Granovsky M, Nabi IR, Wrana JL, Dennis JW 2004 Regulation of cytokine receptors by Golgi N-glycan processing and endocytosis. Science 306:120-124 (Pubitemid 39451953)
22. Pitteloud N, Acierno Jr JS, Meysing A, Eliseenkova AV, Ma J, Ibrahimi OA,Metzger DL, Hayes FJ, Dwyer AA, Hughes VA, YialamasM,Hall JE, Grant E, Mohammadi M, Crowley Jr WF 2006 Mutations in fibroblast growth factor receptor 1 cause both Kallmann syndrome and normosmic idiopathic hypogonadotropic hypogonadism. Proc Natl Acad Sci USA 103:6281-6286
23. Kim HG, Herrick SR, Lemyre E, Kishikawa S, Salisz JA, Seminara S, MacDonald ME, Bruns GA, Morton CC, Quade BJ, Gusella JF 2005 Hypogonadotropic hypogonadism and cleft lip and palate caused by a balanced translocation producing haploinsufficiency for FGFR1. J Med Genet 42:666-672 (Pubitemid 41129040)
24. Trarbach EB, Costa EM, Versiani B, de Castro M, Baptista MT, Garmes HM, de Mendonca BB, Latronico AC 2006 Novel fibroblast growth factor receptor 1 mutations in patients with congenital hypogonadotropic hypogonadism with and without anosmia. J Clin Endocrinol Metab 91:4006-4012 (Pubitemid 44536878)
25. Xu N, Qin Y, Reindollar RH, Tho SP, McDonough PG, Layman LC 2007 A mutation in the fibroblast growth factor receptor 1 gene causes fully penetrant normosmic isolated hypogonadotropic hypogonadism. J Clin Endocrinol Metab 92:1155-1158 (Pubitemid 46465695)
26. Doty RL, Applebaum S, Zusho H, Settle RG 1985 Sex differences in odor identification ability: a cross-cultural analysis. Neuropsychologia 23:667-672 (Pubitemid 15011114)
27. Pitteloud N, Hayes FJ, Boepple PA, DeCruz S, Seminara SB, MacLaughlin DT, Crowley Jr WF 2002 The role of prior pubertal development, biochemical markers of testicular maturation, and genetics in elucidating the phenotypic heterogeneity of idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab 87:152-160 (Pubitemid 34084685)
28. Hayes FJ, McNicholl DJ, Schoenfeld D, Marsh EE, Hall JE 1999 Free α-subunit is superior to luteinizing hormone as a marker of gonadotropin-releasing hormone despite desensitization at fast pulse frequencies. J Clin Endocrinal Metab 1999:1028-1036 (Pubitemid 29138238)
29. Antonarakis SE 1998 Recommendations for a nomenclature system for human gene mutations. Nomenclature Working Group. Hum Mutat 11:1-3 (Pubitemid 128679142)
30. Beranova M, Oliveira LM, Bédécarrats GY, Schipani E, Vallejo M, Ammini AC, Quintos JB, Hall JE, Martin KA, Hayes FJ, Pitteloud N, Kaiser UB, Crowley Jr WF, Seminara SB 2001 Prevalence, phenotypic spectrum, and modes of inheritance of gonadotropin-releasing hormone receptor mutations in idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab 86:1580-1588 (Pubitemid 32374907)
31. Pitteloud N, Zhang C, Pignatelli D, Li JD, Raivio T, Cole LW, Plummer L, Jacobson-Dickman EE, Mellon PL, Zhou QY, Crowley Jr WF 2007 From the cover: loss-of-function mutation in the prokineticin 2 gene causes Kallmann syndrome and normosmic idiopathic hypogonadotropic hypogonadism. Proc Natl Acad Sci USA 104:17447-17452 (Pubitemid 350219858)
32. Cole LW, Sidis Y, Zhang C, Quinton R, Plummer L, Pignatelli D, Hughes VA, Dwyer AA, Raivio T, Hayes FJ, Seminara SB, Huot C, Alos N, Speiser P, Takeshita A, Van Vliet G, Pearce S, Crowley Jr WF, Zhou QY, Pitteloud N 2008 Mutations in prokineticin 2 and prokineticin receptor 2 genes in human gonadotrophin- releasing hormone deficiency: molecular genetics and clinical spectrum. J Clin Endocrinol Metab 93:3551-3559
33. Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova AV, Yeh BK, Yayon A, Linhardt RJ, Mohammadi M 2000 Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol Cell 6:743-750
34. Mohammadi M, Schlessinger J, Hubbard SR 1996 Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism. Cell 86:577-587 (Pubitemid 26299489)
35. Kiselyov VV, Bock E, Berezin V, Poulsen FM 2006 NMR structure of the first Ig module of mouse FGFR1. Protein Sci 15:1512-1515 (Pubitemid 43800023)
36. Chen H, Ma J, Li W, Eliseenkova AV, Xu C, Neubert TA, Miller WT, Mohammadi M 2007 A molecular brake in the kinase hinge region regulates the activity of receptor tyrosine kinases. Mol Cell 27:717-730 (Pubitemid 47333217)
37. DeLano WL 2002 The PyMOL user's manual. San Carlos, CA: DeLano Scientific
38. Mohammadi M, Dionne CA, Li W, Li N, Spivak T, Honegger AM, Jaye M, Schlessinger J 1992 Point mutation in FGF receptor eliminates phosphatidylinositol hydrolysis without affecting mitogenesis. Nature 358:681-684
39. Meysing AU, Kanasaki H, Bedecarrats GY, Acierno Jr JS, Conn PM, Martin KA, Seminara SB, Hall JE, Crowley Jr WF, Kaiser UB 2004 GNRHR mutations in a woman with idiopathic hypogonadotropic hypogonadism highlight the differential sensitivity of luteinizing hormone and follicle-stimulating hormone to gonadotropin-releasing hormone. J Clin Endocrinol Metab 89:3189-3198 (Pubitemid 38951883)
40. Lee C, Gardella TJ, Abou-Samra AB, Nussbaum SR, Segre GV, Potts Jr JT, Kronenberg HM, Jüppner H 1994 Role of the extracellular regions of the parathyroid hormone (PTH)/PTH-related peptide receptor in hormone binding. Endocrinology 135:1488-1495 (Pubitemid 24978276)
41. Olwin BB, Hauschka SD 1989 Cell type and tissue distribution of the fibroblast growth factor receptor. J Cell Biochem 39:443-454 (Pubitemid 19137351)
42. Roghani M, Mohammadi M, Schlessinger J, Moscatelli D 1996 Induction of urokinase-type plasminogen activator by fibroblast growth factor (FGF)-2 is dependent on expression of FGF receptors and does not require activation of phospholipase Cgamma1. J Biol Chem 271:31154-31159 (Pubitemid 26408556)
43. Barker SC, Kassel DB, Weigl D, Huang X, Luther MA, Knight WB 1995 Characterization of pp60c-src tyrosine kinase activities using a continuous assay: autoactivation of the enzyme is an intermolecular autophosphorylation process. Biochemistry 34:14843-14851 (Pubitemid 3002541)
44. Raivio T, Falardeau J, Dwyer A, Quinton R, Hayes FJ, Hughes VA, Cole LW, Pearce SH, Lee H, Boepple P, Crowley Jr WF, Pitteloud N 2007 Reversal of idiopathic hypogonadotropic hypogonadism. N Engl J Med 357:863-873
45. Maquat LE, Carmichael GG 2001 Quality control of mRNA function. Cell 104:173-176
46. Newberry EP, Boudreaux JM, Towler DA 1996 The rat osteocalcin fibroblast growth factor (FGF)-responsive element: an okadaic acidsensitive, FGF-selective transcriptional response motif. Mol Endocrinol 10:1029-1040
47. Pitteloud N, Meysing A, Quinton R, Acierno Jr JS, Dwyer AA, Plummer L, Fliers E, Boepple P, Hayes F, Seminara S, Hughes VA, Ma J, Bouloux P, Mohammadi M, Crowley Jr WF 2006 Mutations in fibroblast growth factor receptor 1 cause Kallmann syndrome with a wide spectrum of reproductive phenotypes. Mol Cell Endocrinol 254-255:60-69 (Pubitemid 44056268)
48. Dewailly D, Boucher A, Decanter C, Lagarde JP, Counis R, Kottler ML2002 Spontaneous pregnancy in a patientwhowas homozygous for the Q106R mutation in the gonadotropin-releasing hormone receptor gene. Fertil Steril 77:1288-1291
49. Pitteloud N, Boepple PA, DeCruz S, Valkenburgh SB, Crowley Jr WF, Hayes FJ 2001 The fertile eunuch variant of idiopathic hypogonadotropic hypogonadism: spontaneous reversal associated with a homozygous mutation in the gonadotropin-releasing hormone receptor. J Clin Endocrinol Metab 86:2470-2475 (Pubitemid 32545694)
50. González-Martinez D, Hu Y, Bouloux PM 2004 Ontogeny of GnRH and olfactory neuronal systems in man: novel insights from the investigation of inherited forms of Kallmann's syndrome. Front Neuroendocrinol 25:108-130 (Pubitemid 39572201)
51. Dode C, Fouveaut C, Mortier G, Janssens S, Bertherat J, Mahoudeau J, Kottler ML, Chabrolle C, Gancel A, Francois I, Devriendt K, Wolczynski S, Pugeat M, Pineiro-Garcia A, Murat A, Bouchard P, Young J, Delpech M, Hardelin JP 2007 Novel FGFR1 sequence variants in Kallmann syndrome, and genetic evidence that the FGFR1c isoform is required in olfactory bulb and palate morphogenesis. Hum Mutat 28:97-98
52. Hermanussen M, Sippell WG 1985 Heterogeneity of Kallmann's syndrome. Clin Genet 28:106-111
53. Hipkin LJ, Casson IF, Davis JC 1990 Identical twins discordant for Kallmann's syndrome. J Med Genet 27:198-199 (Pubitemid 20104750)