PROKR2 and PROK2 mutations cause isolated congenital anosmia without gonadotropic deficiency

European Journal of Endocrinology

Volumn 168, Issue 1, 2013, Pages 31-37

  Moya Plana, Antoine ^a   Villanueva, Carine ^b   Laccourreye, Ollivier ^a   Bonfils, Pierre ^a   De Roux, Nicolas ^b,c,d  

^a HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INSERM   (France)

^d HÔPITAL ROBERT DEBRÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTOR RECEPTOR 1; GONADORELIN;

ADULT; ANOSMIA; ARTICLE; CLINICAL ARTICLE; CODON; DISEASE ASSOCIATION; DNA SEQUENCE; FEMALE; FGF8 GENE; FGFR1 GENE; GENE; GENE ACTIVITY; GENE FUNCTION; GENE MUTATION; GENETIC ANALYSIS; GENETIC SCREENING; GONADOTROPIN DEFICIENCY; HUMAN; ISOLATED CONGENITAL ANOSMIA; KAL1 GENE; KALLMANN SYNDROME; MALE; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROK2 GENE; PROKR2 GENE;

ADOLESCENT; ADULT; CHILD; FEMALE; GASTROINTESTINAL HORMONES; GENOTYPE; HUMANS; KALLMANN SYNDROME; MALE; MIDDLE AGED; NEUROPEPTIDES; OLFACTION DISORDERS; OLFACTORY BULB; PEDIGREE; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, PEPTIDE;

EID: 84871965463     PISSN: 08044643     EISSN: 1479683X     Source Type: Journal    
DOI: 10.1530/EJE-12-0578     Document Type: Article

References (32)

1. Quint C, Temmel AF, Schickinger B, Pabinger S, Ramberger P & Hummel T. Patterns of non-conductive olfactory disorders in eastern Austria: a study of 120 patients from the Department of Otorhinolaryngology at the University of Vienna. Wiener Klinische Wochenschrift 2001 113 52-57. (Pubitemid 32120894)
2. Karstensen HG & Tommerup N. Isolated and syndromic forms of congenital anosmia. Clinical Genetics 2012 81 210-215. (doi:10.1111/j.1399-0004. 2011.01776.x)
3. Feldmesser E, Bercovich D, Avidan N, Halbertal S, Haim L, Gross-Isseroff R, Goshen S & Lancet D. Mutations in olfactory signal transduction genes are not a major cause of human congenital general anosmia. Chemical Senses 2007 32 21-30. (doi:10.1093/chemse/bjl032)
4. Ghadami M, Majidzadeh AK, Morovvati S, Damavandi E, Nishimura G, Komatsu K, Kinoshita A, Najafi MT, Niikawa N & Yoshiura K. Isolated congenital anosmia with morphologically normal olfactory bulb in two Iranian families: a new clinical entity? American Journal of Medical Genetics. Part A 2004 127A 307-309. (doi:10.1002/ajmg.a.30025)
5. Temmel AF, Quint C, Schickinger-Fischer B, Klimek L, Stoller E & Hummel T. Characteristics of olfactory disorders in relation to major causes of olfactory loss. Archives of Otolaryngology - Head & Neck Surgery 2002 128 635-641. (Pubitemid 34665843)
6. Ghadami M, Morovvati S, Majidzadeh AK, Damavandi E, Nishimura G, Kinoshita A, Pasalar P, Komatsu K, Najafi MT, Niikawa N et al. Isolated congenital anosmia locus maps to 18p11.23-q12.2. Journal of Medical Genetics 2004 41 299-303. (doi:10.1136/jmg.2003.015313)
7. Dode C & Hardelin JP. Kallmann syndrome. European Journal of Human Genetics 2009 17 139-146. (doi:10.1038/ejhg.2008.206)
8. Hardelin JP, Levilliers J, del Castillo I, Cohen-Salmon M, Legouis R, Blanchard S, Compain S, Bouloux P, Kirk J, Moraine C et al. X chromosome-linked Kallmann syndrome: stop mutations validate the candidate gene. PNAS 1992 89 8190-8194. (doi:10.1073/pnas.89.17.8190)
9. Dode C, Levilliers J, Dupont JM, De Paepe A, Le Du N, Soussi-Yanicostas N, Coimbra RS, Delmaghani S, Compain-Nouaille S, Baverel F et al. Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nature Genetics 2003 33 463-465. (doi:10.1038/ng1122)
10. Dode C, Teixeira L, Levilliers J, Fouveaut C, Bouchard P, Kottler ML, Lespinasse J, Lienhardt-Roussie A, Mathieu M, Moerman A et al. Kallmann syndrome: mutations in the genes encoding prokineticin-2 and prokineticin receptor-2. PLoS Genetics 2006 2 e175. (doi:10.1371/journal.pgen.0020175)
11. Falardeau J, Chung WC, Beenken A, Raivio T, Plummer L, Sidis Y, Jacobson-Dickman EE, Eliseenkova AV, Ma J, Dwyer A et al. Decreased FGF8 signaling causes deficiency of gonadotropin-releasing hormone in humans and mice. Journal of Clinical Investigation 2008 118 2822-2831. (doi:10.1172/ JCI34538)
12. Pitteloud N, Zhang C, Pignatelli D, Li JD, Raivio T, Cole LW, Plummer L, Jacobson-Dickman EE, Mellon PL, Zhou QY et al. Loss-of-function mutation in the prokineticin 2 gene causes Kallmann syndrome and normosmic idiopathic hypogonadotropic hypogonadism. PNAS 2007 104 17447-17452. (doi:10.1073/pnas. 0707173104)
13. Tornberg J, Sykiotis GP, Keefe K, Plummer L, Hoang X, Hall JE, Quinton R, Seminara SB, Hughes V, Van Vliet G et al. Heparan sulfate 6-O-sulfotransferase 1, a gene involved in extracellular sugar modifications, is mutated in patients with idiopathic hypogonadotrophic hypogonadism. PNAS 2011 108 11524-11529. (doi:10.1073/pnas.1102284108)
14. Waldstreicher J, Seminara SB, Jameson JL, Geyer A, Nachtigall LB, Boepple PA, Holmes LB & Crowley WF Jr. The genetic and clinical heterogeneity of gonadotropin-releasing hormone deficiency in the human. Journal of Clinical Endocrinology and Metabolism 1996 81 4388-4395. (doi:10.1210/jc.81.12.4388)
15. Sykiotis GP, Plummer L, Hughes VA, Au M, Durrani S, Nayak-Young S, Dwyer AA, Quinton R, Hall JE, Gusella JF et al. Oligogenic basis of isolated gonadotropin-releasing hormone deficiency. PNAS 2010 107 15140-15144. (doi:10.1073/pnas.1009622107)
16. Bonfils P, Faulcon P & Avan P. Screening of olfactory function using the Biolfa olfactory test: investigations in patients with dysosmia. Acta Oto-Laryngologica 2004 124 1063-1071. (doi:10.1080/00016480410017990)
17. Cole LW, Sidis Y, Zhang C, Quinton R, Plummer L, Pignatelli D, Hughes VA, Dwyer AA, Raivio T, Hayes FJ et al. Mutations in prokineticin 2 and prokineticin receptor 2 genes in human gonadotrophin-releasing hormone deficiency: molecular genetics and clinical spectrum. Journal of Clinical Endocrinology and Metabolism 2008 93 3551-3559. (doi:10.1210/jc.2007-2654)
18. Sarfati J, Guiochon-Mantel A, Rondard P, Arnulf I, Garcia-Pinero A, Wolczynski S, Brailly-Tabard S, Bidet M, Ramos-Arroyo M, Mathieu M et al. A comparative phenotypic study of Kallmann syndrome patients carrying monoallelic and biallelic mutations in the prokineticin 2 or prokineticin receptor 2 genes. Journal of Clinical Endocrinology and Metabolism 2010 95 659-669. (doi:10.1210/jc.2009-0843)
19. Monnier C, Dode C, Fabre L, Teixeira L, Labesse G, Pin JP, Hardelin JP & Rondard P. PROKR2 missense mutations associated with Kallmann syndrome impair receptor signalling activity. Human Molecular Genetics 2009 18 75-81. (doi:10.1093/hmg/ddn318)
20. Abreu AP, Trarbach EB, de Castro M, Frade Costa EM, Versiani B, Matias Baptista MT, Garmes HM, Mendonca BB & Latronico AC. Loss-of-function mutations in the genes encoding prokineticin-2 or prokineticin receptor-2 cause autosomal recessive Kallmann syndrome. Journal of Clinical Endocrinology and Metabolism 2008 93 4113-4118. (doi:10.1210/jc.2008-0958)
21. Schwanzel-Fukuda M & Pfaff DW. Migration of LHRH-immunoreactive neurons from the olfactory placode rationalizes olfactohormonal relationships. Journal of Steroid Biochemistry and Molecular Biology 1991 39 565-572. (doi:10.1016/0960-0760(91)90254-3)
22. Teixeira L, Guimiot F, Dode C, Fallet-Bianco C, Millar RP, Delezoide AL & Hardelin JP. Defective migration of neuroendocrine GnRH cells in human arrhinencephalic conditions. Journal of Clinical Investigation 2010 120 3668-3672. (doi:10.1172/JCI43699)
23. Herbison AE, Porteous R, Pape JR, Mora JM & Hurst PR. Gonadotropin-releasing hormone neuron requirements for puberty, ovulation, and fertility. Endocrinology 2008 149 597-604. (doi:10.1210/en.2007-1139)
24. Bulow HE, Berry KL, Topper LH, Peles E & Hobert O. Heparan sulfate proteoglycan-dependent induction of axon branching and axon misrouting by the Kallmann syndrome gene kal-1. PNAS 2002 99 6346-6351. (doi:10.1073/pnas. 092128099)
25. Okubo K, Sakai F, Lau EL, Yoshizaki G, Takeuchi Y, Naruse K, Aida K & Nagahama Y. Forebrain gonadotropin-releasing hormone neuronal development: insights from transgenic medaka and the relevance to X-linked Kallmann syndrome. Endocrinology 2006 147 1076-1084. (doi:10.1210/en.2005-0468)
26. Hanchate NK, Giacobini P, Lhuillier P, Parkash J, Espy C, Fouveaut C, Leroy C, Baron S, Campagne C, Vanacker C et al. SEMA3A, a gene involved in axonal pathfinding, is mutated in patients with Kallmann syndrome. PLoS Genetics 2012 8 e1002896. (doi:10.1371/journal.pgen.1002896)
27. Quinton R, Duke VM, Robertson A, Kirk JM, Matfin G, de Zoysa PA, Azcona C, MacColl GS, Jacobs HS, Conway GS et al. Idiopathic gonadotrophin deficiency: genetic questions addressed through phenotypic characterization. Clinical Endocrinology 2001 55 163-174. (doi:10.1046/j.1365-2265.2001.01277.x)
28. 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. Developmental Dynamics 1999 215 26-44. (doi:10.1002/(SICI)1097-0177(199905)215:1〈26::AID-DVDY4〉3.0.CO;2-D)
29. Boulberdaa M, Turkeri G, Urayama K, Dormishian M, Szatkowski C, Zimmer L, Messaddeq N, Laugel V, Dolle P & Nebigil CG. Genetic inactivation of prokineticin receptor-1 leads to heart and kidney disorders. Arteriosclerosis, Thrombosis, and Vascular Biology 2011 31 842-850. (doi:10.1161/ATVBAHA.110. 222323)
30. Martin C, Balasubramanian R, Dwyer AA, Au MG, Sidis Y, Kaiser UB, Seminara SB, Pitteloud N, Zhou QY & Crowley WF Jr. The role of the prokineticin 2 pathway in human reproduction: evidence from the study of human and murine gene mutations. Endocrine Reviews 2011 32 225-246. (doi:10.1210/er.2010-0007)
31. Raivio T, Avbelj M, McCabe MJ, Romero CJ, Dwyer AA, Tommiska J, Sykiotis GP, Gregory LC, Diaczok D, Tziaferi V et al. Genetic overlap in Kallmann syndrome, combined pituitary hormone deficiency, and septo-optic dysplasia. Journal of Clinical Endocrinology and Metabolism 2012 97 E694-E699. (doi:10.1210/jc.2011-2938)
32. Reynaud R, Jayakody SA, Monnier C, Saveanu A, Bouligand J, Guedj AM, Simonin G, Lecomte P, Barlier A, Rondard P et al. PROKR2 variants in multiple hypopituitarism with pituitary stalk interruption. Journal of Clinical Endocrinology and Metabolism 2012 97 E1068-E1073. (doi:10.1210/jc.2011-3056)