Abstract
Hypogonadotropic hypogonadism is defined as a deficiency of the pituitary secretion of follicle-stimulating hormone and luteinizing hormone, which results in the impairment of pubertal maturation and of reproductive function. In the absence of pituitary or hypothalamic anatomical lesions and of anosmia (Kallmann syndrome), hypogonadotropic hypogonadism is referred to as isolated hypogonadotropic hypogonadism (IHH). A limited number of IHH cases are due to loss-of-function mutations of the gonadotropin-releasing hormone receptor. To identify additional gene defects leading to IHH, a large consanguineous family with five affected siblings and with a normal gonadotropin-releasing hormone receptor coding sequence was studied. Homozygosity whole-genome mapping allowed the localization of a new locus within the short arm of chromosome 19 (19p13). Sequencing of several genes localized within this region showed that all affected siblings of the family carried a homozygous deletion of 155 nucleotides in the GPR54 gene. This deletion encompassed the splicing acceptor site of intron 4-exon 5 junction and part of exon 5. The deletion was absent or present on only one allele in unaffected family members. GPR54 has been initially identified as an orphan G protein-coupled receptor with 40% homology to galanin receptors. Recently, a 54-aa peptide derived from the KiSS1 protein was identified as a ligand of GPR54. The present study shows that loss of function of GPR54 is a cause of IHH, and it identifies GPR54 and possibly KiSS1 protein-derived peptide as playing a major and previously unsuspected role in the physiology of the gonadotropic axis.
MeSH Terms
Base Sequence
Consanguinity
DNA Primers
Female
Genotype
Humans
Hypogonadism/genetics,physiopathology
Male
Pedigree
Receptors, G-Protein-Coupled
Receptors, Kisspeptin-1
Receptors, Neuropeptide/genetics,physiology
Chemicals
DNA Primers
KISS1R protein, human
Receptors, G-Protein-Coupled
Receptors, Kisspeptin-1
Receptors, Neuropeptide
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
de Roux Nicolas
Institut National de la Santé et de la Recherche Médicale Unité 135, Unité de Recherches Hormones Gènes et Reproduction, Hôpital de Bicêtre, 94275 Le Kremlin-Bicêtre, France. deroux@necker.fr
Genin Emmanuelle
Carel Jean-Claude
Matsuda Fumihiko
Chaussain Jean-Louis
Milgrom Edwin
References (29)
29 references, click to expand
-
Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function.
Endocr Rev. 2000 Oct;21(5):551-83
PMID: 11041448
-
Uncovering molecular mechanisms involved in activation of G protein-coupled receptors.
Endocr Rev. 2000 Feb;21(1):90-113
PMID: 10696571
-
Prevalence, phenotypic spectrum, and modes of inheritance of gonadotropin-releasing hormone receptor mutations in idiopathic hypogonadotropic hypogonadism.
J Clin Endocrinol Metab. 2001 Apr;86(4):1580-8
PMID: 11297587
-
Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor.
Nature. 2001 May 31;411(6837):613-7
PMID: 11385580
-
AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1.
J Biol Chem. 2001 Aug 3;276(31):28969-75
PMID: 11387329
-
The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54.
J Biol Chem. 2001 Sep 14;276(37):34631-6
PMID: 11457843
-
Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits.
Nature. 2002 Feb 14;415(6873):793-8
PMID: 11823786
-
Genetic causes of human reproductive disease.
J Clin Endocrinol Metab. 2002 Jun;87(6):2447-54
PMID: 12050198
-
Clinical review 148: Monogenic disorders of puberty.
J Clin Endocrinol Metab. 2002 Jun;87(6):2481-94
PMID: 12050203
-
Molecular basis of combined pituitary hormone deficiencies.
Endocr Rev. 2002 Aug;23(4):431-42
PMID: 12202459
-
Optimization of genome search strategies for homozygosity mapping: influence of marker spacing on power and threshold criteria for identification of candidate regions.
Ann Hum Genet. 1998 Sep;62(Pt 5):419-29
PMID: 10088039
-
Discovery of a receptor related to the galanin receptors.
FEBS Lett. 1999 Mar 5;446(1):103-7
PMID: 10100623
-
Transcriptional expression of genes involved in cell invasion and migration by normal and tumoral trophoblast cells.
J Clin Endocrinol Metab. 2002 Nov;87(11):5336-9
PMID: 12414911
-
Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome.
Nat Genet. 2003 Apr;33(4):463-5
PMID: 12627230
-
The candidate gene for the X-linked Kallmann syndrome encodes a protein related to adhesion molecules.
Cell. 1991 Oct 18;67(2):423-35
PMID: 1913827
-
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
PMID: 1922361
-
Faster sequential genetic linkage computations.
Am J Hum Genet. 1993 Jul;53(1):252-63
PMID: 8317490
-
Avoiding recomputation in linkage analysis.
Hum Hered. 1994 Jul-Aug;44(4):225-37
PMID: 8056435
-
A comprehensive genetic map of the human genome based on 5,264 microsatellites.
Nature. 1996 Mar 14;380(6570):152-4
PMID: 8600387
-
Parametric and nonparametric linkage analysis: a unified multipoint approach.
Am J Hum Genet. 1996 Jun;58(6):1347-63
PMID: 8651312
-
Physical and genetic mapping of novel microsatellite polymorphisms on human chromosome 19.
Genomics. 1996 Oct 1;37(1):125-30
PMID: 8921379
-
KiSS-1, a novel human malignant melanoma metastasis-suppressor gene.
J Natl Cancer Inst. 1996 Dec 4;88(23):1731-7
PMID: 8944003
-
A family with hypogonadotropic hypogonadism and mutations in the gonadotropin-releasing hormone receptor.
N Engl J Med. 1997 Nov 27;337(22):1597-602
PMID: 9371856
-
The Eph family in the patterning of neural development.
Curr Biol. 1997 Dec 1;7(12):R799-807
PMID: 9382835
-
Overexpression of mouse follistatin causes reproductive defects in transgenic mice.
Mol Endocrinol. 1998 Jan;12(1):96-106
PMID: 9440814
-
Expression of basigin, a member of the immunoglobulin superfamily, in the mouse central nervous system.
Neurosci Res. 1998 Jan;30(1):53-63
PMID: 9572580
-
A prolactin-releasing peptide in the brain.
Nature. 1998 May 21;393(6682):272-6
PMID: 9607765
-
Gonadotropin-releasing hormone deficiency in the human (idiopathic hypogonadotropic hypogonadism and Kallmann's syndrome): pathophysiological and genetic considerations.
Endocr Rev. 1998 Oct;19(5):521-39
PMID: 9793755
-
Characterization of a cDNA encoding a novel avian hypothalamic neuropeptide exerting an inhibitory effect on gonadotropin release.
Biochem J. 2001 Mar 1;354(Pt 2):379-85
PMID: 11171117