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Endocrinology

Clinical Manifestations, Genetic Variants and Therapeutic Evaluation in Sporadic Chinese Patients with Idiopathic Hypogonadotropic Hypogonadism

ORCID Icon, , , , , , & ORCID Icon show all
Pages 4429-4439 | Received 16 Jul 2023, Accepted 18 Sep 2023, Published online: 29 Sep 2023

References

  • Boehm U, Bouloux PM, Dattani MT, et al. Expert consensus document: European Consensus Statement on congenital hypogonadotropic hypogonadism--pathogenesis, diagnosis and treatment. Nat Rev Endocrinol. 2015;11(9):547–564. doi:10.1038/nrendo.2015.112
  • Bonomi M, Vezzoli V, Krausz C, et al. Characteristics of a nationwide cohort of patients presenting with isolated hypogonadotropic hypogonadism (IHH). Eur J Endocrinol. 2018;178(1):23–32. doi:10.1530/EJE-17-0065
  • Good DJ. New gene targets in the study of hypogonadotropic hypogonadism. Mol Cell Endocrinol. 2021;520:111077. doi:10.1016/j.mce.2020.111077
  • Mitchell AL, Dwyer A, Pitteloud N, Quinton R. Genetic basis and variable phenotypic expression of Kallmann syndrome: towards a unifying theory. Trends Endocrinol Metab. 2011;22(7):249–258. doi:10.1016/j.tem.2011.03.002
  • Bassi I, Luzzani F, Marelli F, et al. Knocking-down of the Prokineticin receptor 2 affects reveals its complex role in the regulation of the hypothalamus-pituitary-gonadal axis in the zebrafish model. Sci Rep. 2020;10(1):7632. doi:10.1038/s41598-020-64077-2
  • Maione L, Dwyer AA, Francou B, et al. Genetics in endocrinology: genetic counseling for congenital hypogonadotropic hypogonadism and Kallmann syndrome: new challenges in the era of oligogenism and next-generation sequencing. Eur J Endocrinol. 2018;178(3):R55–R80. doi:10.1530/EJE-17-0749
  • Amato LGL, Montenegro LR, Lerario AM, et al. New genetic findings in a large cohort of congenital hypogonadotropic hypogonadism. Eur J Endocrinol. 2019;181(2):103–119. doi:10.1530/EJE-18-0764
  • Cangiano B, Swee DS, Quinton R, Bonomi M. Genetics of congenital hypogonadotropic hypogonadism: peculiarities and phenotype of an oligogenic disease. Hum Genet. 2021;140(1):77–111. doi:10.1007/s00439-020-02147-1
  • Bianco SD, Kaiser UB. The genetic and molecular basis of idiopathic hypogonadotropic hypogonadism. Nat Rev Endocrinol. 2009;5(10):569–576. doi:10.1038/nrendo.2009.177
  • Butz H, Nyiro G, Kurucz PA, Liko I, Patocs A. Molecular genetic diagnostics of hypogonadotropic hypogonadism: from panel design towards result interpretation in clinical practice. Hum Genet. 2021;140(1):113–134. doi:10.1007/s00439-020-02148-0
  • Mao JF, Xu HL, Duan J, et al. Reversal of idiopathic hypogonadotropic hypogonadism: a cohort study in Chinese patients. Asian J Androl. 2015;17(3):497–502. doi:10.4103/1008-682X.145072
  • Turan I, Hutchins BI, Hacihamdioglu B, et al. CCDC141 mutations in idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 2017;102(6):1816–1825. doi:10.1210/jc.2016-3391
  • Pitteloud N, Hayes FJ, Dwyer A, Boepple PA, Lee H, Crowley WF. Predictors of outcome of long-term GnRH therapy in men with idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 2002;87(9):4128–4136. doi:10.1210/jc.2002-020518
  • Xu D, Lu L, Xi L, et al. Efficacy and safety of percutaneous administration of dihydrotestosterone in children of different genetic backgrounds with micropenis. J Pediatr Endocrinol Metab. 2017;30(12):1285–1291. doi:10.1515/jpem-2016-0400
  • Richards S, Aziz N, Bale S, et al. Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genet Med. 2015;17(5):405–424. doi:10.1038/gim.2015.30
  • Zhang LL, Bao L, Li YQ, et al. Age at menopause, body mass index, and risk of type 2 diabetes mellitus in postmenopausal Chinese women: the Henan Rural Cohort study. Nutr Metab Cardiovas. 2020;30(8):1347–1354. doi:10.1016/j.numecd.2020.04.003
  • Israel E, Attie KM, Bengtsson BA, et al. Consensus guidelines for the diagnosis and treatment of growth hormone (GH) deficiency in childhood and adolescence: summary statement of the GH Research Society. J Clin Endocr Metab. 2000;85(11):3990–3993.
  • Isojima T, Shimatsu A, Yokoya S, et al. Standardized centile curves and reference intervals of serum insulin-like growth factor-I (IGF-I) levels in a normal Japanese population using the LMS method. Endocr J. 2012;59(9):771–780. doi:10.1507/endocrj.EJ12-0110
  • Raivio T, Falardeau J, Dwyer A, et al. Reversal of idiopathic hypogonadotropic hypogonadism. New Engl J Med. 2007;357(9):863–873. doi:10.1056/NEJMoa066494
  • Stamou MI, Georgopoulos NA. Kallmann syndrome: phenotype and genotype of hypogonadotropic hypogonadism. Metabolism. 2018;86:124–134. doi:10.1016/j.metabol.2017.10.012
  • Wen Y, Zhang ZZ, Li Z, et al. The PROK2/PROKR2 signaling pathway is required for the migration of most olfactory bulb interneurons. J Comp Neurol. 2019;527(18):2931–2947. doi:10.1002/cne.24719
  • Dode C, Rondard P. PROK2/PROKR2 signaling and Kallmann syndrome. Front Endocrinol. 2013;4:19. doi:10.3389/fendo.2013.00019
  • Matsumoto S, Yamazaki C, Masumoto KH, et al. Abnormal development of the olfactory bulb and reproductive system in mice lacking prokineticin receptor PKR2. P Natl Acad Sci USA. 2006;103(11):4140–4145. doi:10.1073/pnas.0508881103
  • Sbai O, Monnier C, Dode C, Pin JP, Hardelin JP, Rondard P. Biased signaling through G-protein-coupled PROKR2 receptors harboring missense mutations. FASEB J. 2014;28(8):3734–3744. doi:10.1096/fj.13-243402
  • Wang Y, Qin M, Fan LJ, Gong CX. Correlation analysis of genotypes and phenotypes in Chinese male pediatric patients with congenital hypogonadotropic hypogonadism. Front Endocrinol. 2022;13:846801. doi:10.3389/fendo.2022.846801
  • Monnier C, Dode C, Fabre L, et al. PROKR2 missense mutations associated with Kallmann syndrome impair receptor signalling activity. Hum Mol Genet. 2009;18(1):75–81. doi:10.1093/hmg/ddn318
  • Martinez-Mayer J, Perez-Millan MI. Phenotypic and genotypic landscape of PROKR2 in neuroendocrine disorders. Front Endocrinol. 2023;14:1132787. doi:10.3389/fendo.2023.1132787
  • Wang XY, Chen DN, Zhao YG, et al. A functional spectrum of PROKR2 mutations identified in isolated hypogonadotropic hypogonadism. Hum Mol Genet. 2023;32(10):1722–1729. doi:10.1093/hmg/ddad014
  • Cho HJ, Shan YF, Whittington NC, Wray S. Nasal placode development, GNRH neuronal migration and Kallmann syndrome. Front Cell Dev Biol. 2019;7:121.
  • Brajadenta GS, Bilan F, Gilbert-Dussardier B, Kitzis A, Thoreau V. A functional assay to study the pathogenicity of CHD7 protein variants encountered in CHARGE syndrome patients. Eur J Hum Genet. 2019;27(11):1683–1691. doi:10.1038/s41431-019-0465-7
  • Li JD, Wu JY, Zhao YG, et al. Phenotypic spectrum of idiopathic hypogonadotropic hypogonadism patients with CHD7 variants from a large Chinese cohort. J Clin Endocr Metab. 2020;105(5):1515–1526.
  • Balasubramanian R, Crowley WF. Reproductive endocrine phenotypes relating to CHD7 mutations in humans. Am J Med Genet C. 2017;175(4):507–515. doi:10.1002/ajmg.c.31585
  • Zentner GE, Layman WS, Martin DM, Scacheri PC. Molecular and phenotypic aspects of CHD7 mutation in CHARGE syndrome. Am J Med Genet A. 2010;152A(3):674–686. doi:10.1002/ajmg.a.33323
  • Pingault V, Zerad L, Bertani-Torres W, Bondurand N. SOX10: 20 years of phenotypic plurality and current understanding of its developmental function. J Med Genet. 2022;59(2):105–114. doi:10.1136/jmedgenet-2021-108105
  • Dai WT, Wu JY, Zhao YG, et al. Functional analysis of SOX10 mutations identified in Chinese patients with Kallmann syndrome. Gene. 2019;702:99–106. doi:10.1016/j.gene.2019.03.039
  • Rojas RA, Kutateladze AA, Plummer L, et al. Phenotypic continuum between Waardenburg syndrome and idiopathic hypogonadotropic hypogonadism in humans with SOX10 variants. Genet Med. 2021;23(4):629–636. doi:10.1038/s41436-020-01051-3
  • Barraud P, St John JA, Stolt CC, Wegner M, Baker CVH. Olfactory ensheathing glia are required for embryonic olfactory axon targeting and the migration of gonadotropin-releasing hormone neurons. Biol Open. 2013;2(7):750–759. doi:10.1242/bio.20135249
  • Pingault V, Bodereau V, Baral V, et al. Loss-of-Function mutations in SOX10 cause Kallmann syndrome with deafness. Am J Hum Genet. 2013;92(5):707–724. doi:10.1016/j.ajhg.2013.03.024
  • Kim HG, Ahn JW, Kurth I, et al. WDR11, a WD protein that interacts with transcription factor EMX1, is mutated in idiopathic hypogonadotropic hypogonadism and Kallmann syndrome. Am J Hum Genet. 2010;87(4):465–479. doi:10.1016/j.ajhg.2010.08.018
  • Valdes-Socin H, Almanza MR, Fernandez-Ladreda MT, Debray FG, Bours V, Beckers A. Reproduction, smell, and neurodevelopmental disorders: genetic defects in different hypogonadotropic hypogonadal syndromes. Front Endocrinol. 2014;5:109. doi:10.3389/fendo.2014.00109
  • Men MC, Wu JY, Zhao YG, et al. Genotypic and phenotypic spectra of FGFR1, FGF8, and FGF17 mutations in a Chinese cohort with idiopathic hypogonadotropic hypogonadism. Fertil Steril. 2020;113(1):158–166. doi:10.1016/j.fertnstert.2019.08.069
  • Yang L, Zhang SX, Dong Q, Xiong ZB, Li X. Application of hormonal treatment in hypogonadotropic hypogonadism: more than ten years experience. Int Urol Nephrol. 2012;44(2):393–399. doi:10.1007/s11255-011-0065-0