Mutations in fibroblast growth factor receptor 1 cause Kallmann syndrome with a wide spectrum of reproductive phenotypes

Molecular and Cellular Endocrinology

Volumn 254-255, Issue , 2006, Pages 60-69

  Pitteloud, Nelly ^a   Meysing, Astrid ^a   Quinton, Richard ^b   Acierno Jr , James S ^a   Dwyer, Andrew A ^a   Plummer, Lacey ^a   Fliers, Eric ^c   Boepple, Paul ^a   Hayes, Frances ^a   Seminara, Stephanie ^a   Hughes, Viriginia A ^a   Ma, Jinghong ^d   Bouloux, Pierre ^b   Mohammadi, Moosa ^d   Crowley Jr , William F ^a  

^a Reproductive Endocrine Unit   (United States)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

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

Author keywords

FGFR1 mutation; Idiopathic hypogonadotropic hypogonadism; Kallmann syndrome; Pubertal development

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 1; GONADOTROPIN; IMMUNOGLOBULIN; INHIBIN B; PROTEIN TYROSINE KINASE; TESTOSTERONE;

ARTICLE; CONTROLLED STUDY; CRYPTORCHISM; EXON; FEMALE; GONADOTROPIN BLOOD LEVEL; HUMAN; HYPOGONADOTROPIC HYPOGONADISM; KALLMANN SYNDROME; MAJOR CLINICAL STUDY; MALE; MICROPENIS; MISSENSE MUTATION; MUTATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; REPRODUCTION; SPERMATOGENESIS; TESTOSTERONE BLOOD LEVEL;

EID: 33745948557     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2006.04.021     Document Type: Article

References (33)

1. Antonarakis S.E. Recommendations for a nomenclature system for human gene mutations. Nomenclature Working Group. Hum. Mutat. 11 (1998) 1-3
2. Albuisson J., Pecheux C., Carel J.C., Lacombe D., Leheup B., Lapuzina P., Bouchard P., Legius E., Matthijs G., Wasniewska M., Delpech M., Young J., Hardelin J.P., and Dode C. Kallmann syndrome: 14 novel mutations in KAL1 and FGFR1 (KAL2). Hum. Mutat. 25 (2005) 98-99
3. Bick D.P., Schorderet D.F., Price P.A., Campbell L., Huff R.W., Shapiro L.J., and Moore C.M. Prenatal diagnosis and investigation of a fetus with Chondrodysplasia punctata, ichthyosis, and Kallmann syndrome due to an Xp deletion. Prenat. Diagn. 12 (1992) 19-29
4. Dode C., Levilliers J., Dupont J.M., De Paepe A., Le Du N., Soussi-Yanicostas N., Coimbra R.S., Delmaghani S., Compain-Nouaille S., Baverel F., Pecheux C., Le Tessier D., Cruaud C., Delpech M., Speleman F., Vermeulen S., Amalfitano A., Bachelot Y., Bouchard P., Cabrol S., Carel J.C., Delemarre-van de Waal H., Goulet-Salmon B., Kottler M.L., Richard O., Sanchez-Franco F., Saura R., Young J., Petit C., and Hardelin J.P. Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nat. Genet. 33 (2003) 463-465
5. Doty R.L., Applebaum S., Zusho H., and Settle R.G. Sex differences in odor identification ability: a cross-cultural analysis. Neuropsychologia 23 (1985) 667-672
6. Franco B., Guioli S., Pragliola A., Incerti B., Bardoni B., Tonlorenzi R., Carrozzo R., Maestrini E., Pieretti M., Taillon-Miller P., et al. A gene deleted in Kallmann's syndrome shares homology with neural cell adhesion and axonal path-finding molecules. Nature 353 (1991) 529-536
7. Grumbach M.M. A window of opportunity: the diagnosis of gonadotropin deficiency in the male infant. J. Clin. Endocrinol. Metab. 90 (2005) 3122-3127
8. Gonzalez-Martinez D., Kim S.H., Hu Y., Guimond S., Schofield J., Winyard P., Vannelli G.B., Turnbull J., and Bouloux P.M. Anosmin-1 modulates fibroblast growth factor receptor 1 signaling in human gonadotropin-releasing hormone olfactory neuroblasts through a heparan sulfate-dependent mechanism. J. Neurosci. 24 (2004) 10384-10392
9. Gill J.C., Moenter S.M., and Tsai P.S. Developmental regulation of gonadotropin-releasing hormone neurons by Fgf signaling. Endocrinology (2004)
10. Hardelin J.P., Levilliers J., Blanchard S., Carel J.-C., Leutenegger M., Pinard-Bertelletto J.-P., Bouloux P., and Petit C. Heterogeneity in the mutations responsible for X chromosome-linked Kallmann syndrome. Hum. Mol. Genet. 2 (1993) 373-377
11. Hoffman A.R., and Crowley Jr. W.F. Induction of puberty in men by long-term pulsatile administration of low-dose gonadotropin-releasing hormone. N. Engl. J. Med. 307 (1982) 1237-1241
12. Hayes F.J., McNicholl D.J., Schoenfeld D., Marsh E.E., and Hall J.E. Free alpha-subunit is superior to luteinizing hormone as a marker of gonadotropin-releasing hormone despite desensitization at fast pulse frequencies. J. Clin. Endocrinol. Metab. 1999 (1999) 1028-1036
13. Hebert J.M., Lin M., Partanen J., Rossant J., and McConnell S.K. FGF signaling through FGFR1 is required for olfactory bulb morphogenesis. Development 130 (2003) 1101-1111
14. Legouis R., Hardelin J.P., Levilliers J., Claverie J.M., Compain S., Wunderle V., Millasseau P., Le Paslier D., Cohen D., Caterina D., Bougueleret L., Delemarre-van de Waal H.A., Lutfalla G., Weissenbach J., and Petit C. The candidate gene for the X-linked Kallmann syndrome encodes a protein related to adhesion molecules. Cell 67 (1991) 423-435
15. Mohammadi M., Schlessinger J., and Hubbard S.R. Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism. Cell 86 (1996) 577-587
16. Maquat L.E., and Carmichael G.G. Quality control of mRNA function. Cell 104 (2001) 173-176
17. Muenke M., Schell U., Hehr A., Robin N.H., Losken H.W., Schinzel A., Pulleyn L.J., Rutland P., Reardon W., Malcolm S., et al. A common mutation in the fibroblast growth factor receptor 1 gene in Pfeiffer syndrome. Nat. Genet. 8 (1994) 269-274
18. Oliveira L.M., Seminara S.B., Beranova M., Hayes F.J., Valkenburgh S.B., Schipani E., Costa E.M., Latronico A.C., Crowley Jr. W.F., and Vallejo M. The importance of autosomal genes in Kallmann syndrome: genotype-phenotype correlations and neuroendocrine characteristics. J. Clin. Endocrinol. Metab. 86 (2001) 1532-1538
19. Pitteloud N., Hayes F.J., Boepple P.A., DeCruz S., Seminara S.B., MacLaughlin D.T., and Crowley Jr. W.F. 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 (2002) 152-160
20. Pitteloud N., Acierno Jr. J.S., Meysing A.U., Dwyer A.A., Hayes F.J., and Crowley Jr. W.F. Reversible Kallmann syndrome, delayed puberty, and isolated anosmia occurring in a single family with a mutation in the fibroblast growth factor receptor 1 gene. J. Clin. Endocrinol. Metab. 90 (2005) 1317-1322
21. Pirvola U., Ylikoski J., Trokovic R., Hebert J.M., McConnell S.K., and Partanen J. FGFR1 is required for the development of the auditory sensory epithelium. Neuron 35 (2002) 671-680
22. Quinton R., Duke V.M., Robertson A., Kirk J.M., Matfin G., de Zoysa P.A., Azcona C., MacColl G.S., Jacobs H.S., Conway G.S., Besser M., Stanhope R.G., and Bouloux P.M. Idiopathic gonadotrophin deficiency: genetic questions addressed through phenotypic characterization. Clin. Endocrinol. (Oxford) 55 (2001) 163-174
23. Quinton R., Cheow H.K., Tymms D.J., Bouloux P.M., Wu F.C., and Jacobs H.S. Kallmann's syndrome: is it always for life?. Clin. Endocrinol. (Oxford) 50 (1999) 481-485
24. Rice D.P., Rice R., and Thesleff I. Fgfr mRNA isoforms in craniofacial bone development. Bone 33 (2003) 14-27
25. Seminara S.B., Hayes F.J., and Crowley Jr. W.F. Gonadotropin-releasing hormone deficiency in the human (idiopathic hypogonadotropic hypogonadism and Kallmann's syndrome): pathophysiological and genetic considerations. Endocr. Rev. 19 (1998) 521-539
26. 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., and Ogata T. 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 (2004) 1079-1088
27. Schlessinger J., Plotnikov A.N., Ibrahimi O.A., Eliseenkova A.V., Yeh B.K., Yayon A., Linhardt R.J., and Mohammadi M. Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol. Cell. 6 (2000) 743-750
28. Spratt D.I., O'Dea L.S., Schoenfeld D., Butler J., Rao P.N., and Crowley Jr. W.F. Neuroendocrine-gonadal axis in men: frequent sampling of LH, FSH, and testosterone. Am. J. Physiol. 254 (1988) E658-E666
29. Schwanzel-Fukuda M., and Pfaff D. Origin of luteinizing hormone-releasing hormone neurons. Nature 338 (1989) 161-164
30. Tobet S.A., Bless E.P., and Schwarting G.A. Developmental aspect of the gonadotropin-releasing hormone system. Mol. Cell. Endocrinol. 185 (2001) 173-184
31. Tsai P.S., Moenter S.M., Postigo H.R., El Majdoubi M., Pak T.R., Gill J.C., Paruthiyil S., Werner S., and Weiner R.I. Targeted expression of a dominant-negative fibroblast growth factor (FGF) receptor in gonadotropin-releasing hormone (GnRH) neurons reduces FGF responsiveness and the size of GnRH neuronal population. Mol. Endocrinol. 19 (2005) 225-236
32. Wray S., Nieburgs A., and Elkabes S. Spatiotemporal cell expression of luteinizing hormone-releasing hormone in the prenatal mouse: evidence for an embryonic origin in the olfactory placode. Brain Res. Dev. Brain Res. 46 (1989) 309-318
33. Zitzmann M., and Nieschlag E. Hormone substitution in male hypogonadism. Mol. Cell. Endocrinol. 161 (2000) 73-88