Evidence that FGFR1 loss-of-function mutations may cause variable skeletal malformations in patients with Kallmann syndrome

Advances in Medical Sciences

Volumn 57, Issue 2, 2012, Pages 314-321

  Jarzabek, K ^a,b   Wolczynski, S ^a,b   Lesniewicz, R ^a   Plessis, G ^c   Kottler M L , ^c,d  

^a MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

^b INSTITUTE OF ANIMAL REPRODUCTION AND FOOD RESEARCH   (Poland)

^c CAEN UNIVERSITY HOSPITAL   (France)

^d Biology and Innovative Therapeutics for Ovarian Cancers group   (France)

Author keywords

FGFR1; KAL2; Kallmann syndrome; Skeletal malformations

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 1;

ADULT; ARTICLE; AUDIOMETRY; CLINICAL ARTICLE; COHORT ANALYSIS; DNA SEQUENCE; FEMALE; GENE MUTATION; HUMAN; KALLMANN SYNDROME; KNOCKOUT MOUSE; MALE; METACARPAL BONE; MOUSE; NONHUMAN; PHENOTYPE; SKELETON MALFORMATION;

EID: 84879682789     PISSN: 18961126     EISSN: 18984002     Source Type: Journal    
DOI: 10.2478/v10039-012-0036-4     Document Type: Article

References (58)

1. Hardelin JP, Dodé C. The complex genetics of Kallmann syndrome: KAL1, FGFR1, FGF8, PROKR2, PROK2, et al. Sex Dev. 2008;2(4-5):181-93.
2. Wegenke JD, Uehling DT, Wear JB Jr, Gordon ES, Bargman JG, Deacon JS, Herrmann JP, Opitz JM. Familial Kallmann syndrome with unilateral renal aplasia. Clin Genet. 1975 May-Jun;7(5):368-81.
3. Conrad B, Kriebel J, Hetzel WD. Hereditary bimanual synkinesis combined with hypogonadotropic hypogonadism and anosmia in four brothers. J Neurol. 1978 Aug 25;218(4):263-74. (Pubitemid 8381534)
4. Schwankhaus JD, Currie J, Jaffe MJ, Rose SR, Sherins RJ. Neurologic findings in men with isolated hypogonadotropic hypogonadism. Neurology. 1989 Feb;39(2 Pt 1):223-6. (Pubitemid 19059309)
5. Hill J, Elliott C, Colquhoun I. Audiological, vestibular and radiological abnormalities in Kallman's syndrome. J Laryngol Otol. 1992 Jun;106(6):530-4.
6. de Zegher F, Lagae L, Declerck D, Vinckier F. Kallmann syndrome and delayed puberty associated with agenesis of lateral maxillary incisors. J Craniofac Genet Dev Biol. 1995 Apr-Jun;15(2):87-9.
7. Mølsted K, Kjaer I, Giwercman A, Vesterhauge S, Skakkebaek NE. Craniofacial morphology in patients with Kallmann's syndrome with and without cleft lip and palate. Cleft Palate Craniofac J. 1997 Sep;34(5):417-24. (Pubitemid 27408725)
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, Graziella Persico M, Camerino G, Ballabio A. A gene deleted in Kallmann's syndrome shares homology with neural cell adhesion and axonal path-finding molecules. Nature. 1991 Oct 10;353(6344):529-36. (Pubitemid 21912544)
9. Legouis R, Hardelin JP, Leyilliers J, Claverle JM, Compain S, Wunderle V, Millasseau P, Le Paslier D, Cohen D, Caterina D, Bougueleret L, Delemarre-Van De Waal H, Lutfalla G, Weissenbach J, Petit C. The candidate gene for the X-linked Kallmann syndrome encodes a protein related to adhesion molecules. Cell. 1991 Oct 18;67(2):423-35.
10. Hardelin JP, Levilliers J, Del Castillo I, Cohen- Salmon M, Legouis R, Blanchard S, Compain S, Bouloux P, Kirk J, Moraine C, Chaussain, JL, Weissenbach J, Petit C. X chromosome-linked Kallmann syndrome: stop mutations validate the candidate gene. Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8190-4.
11. 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. Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nat Genet. 2003 Apr;33(4):463-5. (Pubitemid 36390006)
12. 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. Decreased FGF8 signaling causes deficiency of gonadotropin-releasing hormone in humans and mice. J Clin Invest. 2008 Aug;118(8):2822-31.
13. Dodé 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. Kallmann syndrome: mutations in the genes encoding prokineticin-2 and prokineticin receptor-2. PLoS Genet. 2006 Oct 20;2(10):e175.
14. Kim HG, Ahn JW, Kurth I, Ullmann R, Kim HT, Kulharya A, Ha KS, Itokawa Y, Meliciani I, Wenzel W, Lee D, Rosenberger G, Ozata M, Bick DP, Sherins RJ, Nagase T, Tekin M, Kim SH, Kim CH, Ropers HH, Gusella JF, Kalscheuer V, Choi CY, Layman LC. WDR11, a WD protein that interacts with transcription factor EMX1, is mutated in idiopathic hypogonadotropic hypogonadism and Kallmann syndrome. Am J Hum Genet. 2010 Oct 8;87(4):465-79.
15. Tornberg J, Sykiotis GP, Keefe K, Plummer L, Hoang X, Hall JE, Quinton R, Seminara SB, Hughes V, Van Vliet G, Van Uum S, Crowley WF, Habuchi H, Kimata K, Pitteloud N, Bülow HE. Heparan sulfate 6-O-sulfotransferase 1, a gene involved in extracellular sugar modifications, is mutated inpatients with idiopathic hypogonadotrophic hypogonadism. Proc Natl Acad Sci U S A. 2011 Jul 12;108(28):11524-9.
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. Mutations in CHD7, encoding a chromatinremodeling protein, cause idiopathic hypogonadotropic hypogonadism and Kallmann syndrome. Am J Hum Genet. 2008 Oct;83(4):511-9.
17. Hardelin JP, Julliard AK, Moniot B, Soussi- Yanicostas N, Verney C, Schwanzel-Fukuda M, Ayer-Le Lievre C, Petit C. Anosmin-1 is a regionally restricted component of basement membranes and interstitial matrices during organogenesis: implications for the developmental anomalies of X chromosome-linked Kallmann syndrome. Dev Dyn. 1999 May;215(1):26-44. (Pubitemid 29215701)
18. Albuisson J, Pêcheux C, Carel JC, Lacombe D, Leheup B, Lapuzina P, Bouchard P, Legius E, Matthijs G, Wasniewska M, Delpech M, Young J, Hardelin JP, Dodé C. Kallmann syndrome: 14 novel mutations in KAL1 and FGFR1 (KAL2). Hum Mutat. 2005 Jan;25(1):98-9.
19. 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. 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. 2004 Mar;89(3):1079-88. (Pubitemid 38368394)
20. Pitteloud N, Meysing A, Quinton R, Acierno JS Jr, Dwyer AA, Plummer L, Fliers E, Boepple P, Hayes F, Seminara S, Hughes VA, Ma J, Bouloux P, Mohammadi M, Crowley WF Jr. Mutations in fibroblast growth factor receptor 1 cause Kallmann syndrome with a wide spectrum of reproductive phenotypes. Mol Cell Endocrinol. 2006 Jul 25;254-255:60-9.
21. Zenaty D, Bretones P, Lambe C, Guemas I, David M, Léger J, de Roux N. Paediatric phenotype of Kallmann syndrome due to mutations of fibroblast growth factor receptor 1 (FGFR1). Mol Cell Endocrinol. 2006 Jul 25;254- 255:78-83.
22. 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. Idiopathic gonadotrophin deficiency: genetic questions addressed through phenotypic characterization. Clin Endocrinol (Oxf). 2001 Aug;55(2):163-74. (Pubitemid 32868580)
23. Dodé C, Hardelin JP. Kallmann syndrome: fibroblast growth factor signaling insufficiency? J Mol Med. 2004 Nov;82(11):725-34. (Pubitemid 40022266)
24. Salenave S, Chanson P, Bry H, Pugeat M, Cabrol S, Carel JC, Murat A, Lecomte P, Brailly S, Hardelin JP, Dodé C, Young J. Kallmann's syndrome: a comparison of the reproductive phenotypes in men carrying KAL1 and FGFR1/KAL2 mutations. J Clin Endocrinol Metab. 2008 Mar;93(3):758-63. (Pubitemid 351398550)
25. McKeehan WL, Kan M. Heparan sulfate fibroblast growth factor receptor complex: structure-function relationships. Mol Reprod Dev. 1994 Sep;39(1):69-81; discusison 81-2.
26. Ibrahimi OA, Zhang F, Hrstka SC, Mohammadi M, Linhardt RJ. Kinetic model for FGF, FGFR, and proteoglycan signal transduction complex assembly. Biochemistry. 2004 Apr 27;43(16):4724-30. (Pubitemid 38509093)
27. González-Martínez D, Kim SH, Hu Y, Guimond S, Schofield J, Winyard P, Vannelli GB, Turnbull J, Bouloux PM. Anosmin-1 modulates fibroblast growth factor receptor 1 signaling in human gonadotropin-releasing hormone olfactory neuroblasts through a heparan sulfate-dependent mechanism. J Neurosci. 2004 Nov 17;24(46):10384-92. (Pubitemid 39552623)
28. Ohkubo Y, Uchida AO, Shin D, Partanen J, Vaccarino FM. Fibroblast growth factor receptor 1 is required for the proliferation of hippocampal progenitor cells and for hippocampal growth in mouse. J Neurosci. 2004 Jul 7;24(27):6057-69. (Pubitemid 38891096)
29. Reuss B, von Bohlen und Halbach O. Fibroblast growth factors and their receptors in the central nervous system. Cell Tissue Res. 2003 Aug;313(2):139-57. (Pubitemid 37129946)
30. Gill JC, Moenter SM, Tsai PS. Developmental regulation of gonadotropin-releasing hormone neurons by fibroblast growth factor signaling. Endocrinology. 2004 Aug;145(8):3830-9. (Pubitemid 39037571)
31. Pirvola U, Ylikoski J, Trokovic R, Hébert JM, McConnell SK, Partanen J. FGFR1 is required for the development of the auditory sensory epithelium. Neuron. 2002 Aug;35(4):671-80. (Pubitemid 35223027)
32. Kim SH, Hu Y, Cadman S, Bouloux P. Diversity in fibroblast growth factor receptor 1 regulation: learning from the investigation of Kallmann syndrome. J Neuroendocrinol. 2008 Feb;20(2):141-63. (Pubitemid 351147002)
33. Hébert JM, Lin M, Partanen J, Rossant J, McConnell SK. FGF signaling through FGFR1 is required for olfactory bulb morphogenesis. Development. 2003 Mar;130(6):1101-11. (Pubitemid 36395692)
34. Tsai PS, Moenter SM, Postigo HR, El Majdoubi M, Pak TR, Gill JC, Paruthiyil S, Werner S, Weiner RI. 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. 2005 Jan;19(1):225-36. (Pubitemid 40065972)
35. Hajihosseini MK, Lalioti MD, Arthaud S, Burgar HR, Brown JM, Twigg SR, Wilkie AO, Heath JK. Skeletal development is regulated by fibroblast growth factor receptor 1 signalling dynamics. Development. 2004 Jan;131(2):325-35. (Pubitemid 38181372)
36. Horton WA, Degnin CR. FGFs in endochondral skeletal development. Trends Endocrinol Metab. 2009 Sep;20(7):341-8.
37. Sewell W, Kusumi K. Genetic analysis of molecular oscillators in mammalian somitogenesis: clues for studiesof human vertebral disorders. Birth Defects Res C Embryo Today. 2007 Jun;81(2):111-20. (Pubitemid 47052610)
38. White KE, Cabral JM, Davis SI, Fishburn T, Evans WE, Ichikawa S, Fields J, Yu X, Shaw NJ, McLellan NJ, McKeown C, Fitzpatrick D, Yu K, Ornitz DM, Econs MJ. Mutations that cause osteoglophonic dysplasia define novel roles for FGFR1 in bone elongation. Am J Hum Genet. 2005 Feb;76(2):361-7. (Pubitemid 40129563)
39. Muenke M, Schell U, Hehr A, Robin NH, Wolfgang Losken H, Schinzel A, Pulleyn LJ, Rutland P, Reardon W, Malcolm S, Winter RM A common mutation in the fibroblast growth factor receptor 1 gene in Pfeiffer syndrome. Nat Genet. 1994 Nov;8(3):269-74. (Pubitemid 24338739)
40. Dodé C, Fouveaut C, Mortier G, Janssens S, Bertherat J, Mahoudeau J, Kottler ML, Chabrolle C, Gancel A, François I, Devriendt K, Wolczynski S, Pugeat M, Pineiro-Garcia A, Murat A, Bouchard P, Young J, Delpech M, Hardelin JP. Novel FGFR1 sequence variants in Kallmann syndrome, and genetic evidence that the FGFR1c isoform is required in olfactory bulb and palate morphogenesis. Hum Mutat. 2007 Jan;28(1):97-8.
41. Deng CX, Wynshaw-Boris A, Shen MM, Daugherty C, Ornitz DM, Leder P. Murine FGFR-1 is required for early post-implantation growth and axial organization. Genes Dev. 1994 Dec;8(24):3045-57.
42. Raivio T, Sidis Y, Plummer L, Chen H, Ma J, Mukherjee A, Jacobson-Dickman E, Quinton R, Van Vliet G, Lavoie H, Hughes VA, Dwyer A, Hayes FJ, Xu S, Sparks S, Kaiser UB, Mohammadi M, Pitteloud N. Impaired fibroblast growth factor receptor 1 signaling as a cause of normosmic idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 2009 Nov;94(11):4380-90.
43. Müller F, O'Rahilly R, Benson DR. The early origin of vertebral anomalies, as illustrated by a 'butterfly vertebra'. J Anat. 1986 Dec;149:157-69. (Pubitemid 17006066)
44. Grimme JD, Castillo M. Congenital anomalies of the spine. Neuroimaging Clin N Am. 2007 Feb;17(1):1-16. (Pubitemid 46705490)
45. Li X, An HS, Ellman M, Phillips F, Thonar EJ, Park DK, Udayakumar RK, Im HJ. Action of fibroblast growth factor-2 on the intervertebral disc. Arthritis Res Ther. 2008 10(2):R48.
46. Ellman MB, An HS, Muddasani P, Im HJ. Biological impact of the fibroblast growth factor family on articular cartilage and intervertebral disc homeostasis. Gene. 2008 Aug 15;420(1):82-9.
47. Im HJ, Muddasani P, Natarajan V, Schmid TM, Block JA, Davis F, van Wijnen AJ, Loeser RF. Basic fibroblast growth factor stimulates matrix metalloproteinase-13 via the molecular cross-talk between the mitogen-activated protein kinases and protein kinase Cdelta pathways in human adult articular chondrocytes. J Biol Chem. 2007 Apr 13;282(15):11110-21. (Pubitemid 47100793)
48. Valverde-Franco G, Binette JS, Li W, Wang H, Chai S, Laflamme F, Tran-Khanh N, Quenneville E, Meijers T, Poole AR, Mort JS, Buschmann MD, Henderson JE. Defects in articular cartilage metabolism and early arthritis in fibroblast growth factor receptor 3 deficient mice. Hum Mol Genet. 2006 Jun 1;15(11):1783-92. (Pubitemid 43821768)
49. Li C, Xu X, Nelson DK, Williams T, Kuehn MR, Deng CX. FGFR1 function at the earliest stages of mouse limb development plays an indispensable role in subsequent autopod morphogenesis. Development. 2005 Nov;132(21):4755-64. (Pubitemid 41685285)
50. Verheyden JM, Lewandoski M, Deng C, Harfe BD, Sun X. Conditional inactivation of Fgfr1 in mouse defines its role in limb bud establishment, outgrowth and digit patterning. Development. 2005 Oct;132(19):4235-45. (Pubitemid 41576686)
51. Yu K, Ornitz DM. FGF signaling regulates mesenchymal differentiation and skeletal patterning along the limb bud proximodistal axis. Development. 2008 Feb;135(3):483-91.
52. Temtamy SA, McKusick VA. The genetics of hand malformations. Birth Defects Orig Artic Ser. 1978;14(3):i-xviii, 1-619.
53. Roscioli T, Flanagan S, Kumar P, Masel J, Gattas M, Hyland VJ, Glass IA. Clinical findings in a atient with FGFR1 P252R mutation and comparison with the literature. Am J Med Genet. 2000 Jul;93(1):22-8.
54. Hackett A, Rowe L. FGFR1 Pfeiffer syndrome without craniosynostosis: an additional case report. Clin Dysmorphol. 2006 Oct;15(4):207-10. (Pubitemid 44370558)
55. Rossi M, Jones RL, Norbury G, Bloch-Zupan A, Winter RM. The appearance of the feet in Pfeiffer syndrome caused by FGFR1 P252R mutation. Clin Dysmorphol. 2003 Oct;12(4):269-74. (Pubitemid 37267194)
56. Verloes A, David A, Ngô L, Bottani A. Stringent delineation of Pallister-Hall syndrome in two long surviving patients: importance of radiological anomalies of the hands. J Med Genet. 1995 Aug;32(8):605-11.
57. Doss BJ, Jolly S, Qureshi F, Jacques SM, Evans MI, Johnson MP, Lampinen J, Kupsky WJ. Neuropathologic findings in a case of OFDS type VI (Váradi syndrome). Am J Med Genet. 1998 Apr 28;77(1):38-42.
58. Stoll C, De Saint Martin A, Donato L, Alembik K, Sauvage P, Messer J. Pallister-Hall syndrome with stenosis of the cricoid cartilage and microphallus without hypopituitarism. Genet Couns. 2001;12(3):231-5. (Pubitemid 32938684)