Genetic control of pubertal timing

Current Opinion in Pediatrics

Volumn 20, Issue 4, 2008, Pages 458-464

  Kaminski, Beth A ^a   Palmert, Mark R ^b  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Genetic regulation; Genetics; Hypogonadotropic hypogonadism; Kallmann syndrome; Pubertal timing; Puberty

Indexed keywords

LEPTIN;

GENE; GENETIC ASSOCIATION; GENETIC DISORDER; GENETIC REGULATION; GENETIC VARIABILITY; HUMAN; HYPOGONADOTROPIC HYPOGONADISM; IDIOPATHIC DISEASE; KALLMANN SYNDROME; NONHUMAN; PRIORITY JOURNAL; PUBERTY; QUANTITATIVE TRAIT LOCUS; REVIEW; ADOLESCENT; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; HYPOGONADISM; TIME;

ADOLESCENT; ANIMALS; GENE EXPRESSION REGULATION; HUMANS; HYPOGONADISM; KALLMANN SYNDROME; LEPTIN; PUBERTY; QUANTITATIVE TRAIT LOCI; TIME FACTORS; VARIATION (GENETICS);

EID: 52449092757     PISSN: 10408703     EISSN: None     Source Type: Journal    
DOI: 10.1097/MOP.0b013e3283060ed4     Document Type: Review

References (85)

1. Parent AS, Teilmann G, Juul A, et al. The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev 2003; 24:668-693.
2. Palmert MR, Hirschhorn JN. Genetic approaches to stature, pubertal timing, and other complex traits. Mol Genet Metab 2003; 80:1-10.
3. Plant TM, Barker-Gibb ML. Neurobiological mechanisms of puberty in higher primates. Hum Reprod Update 2004; 10:67-77.
4. Towne B, Czerwinski SA, Demerath EW, et al. Heritability of age at menarche in girls from the Fels longitudinal study. Am J Phys Anthropol 2005; 128:210- 219.
5. Darvasi A. Experimental strategies for the genetic dissection of complex traits in animal models. Nat Genet 1998; 18:19-24.
6. Palmert MR, Boepple PA. Variation in the timing of puberty: clinical spectrum and genetic investigation. J Clin Endocrinol Metab 2001; 86:2364-2368.
7. Kalantaridou SN, Chrousos GP. Clinical review 148: monogenic disorders of puberty. J Clin Endocrinol Metab 2002; 87:2481-2494.
8. Silveira LF, MacColl GS, Bouloux PM. Hypogonadotropic hypogonadism. Semin Reprod Med 2002; 20:327-338.
9. de Roux N, Young J, Misrahi M, et al. A family with hypogonadotropic hypo-gonadism and mutations in the gonadotropin-releasing hormone receptor. N Engl J Med 1997; 337:1597-1602.
10. De Roux N, Genin E, Carel JC, et al. Hypogonadotropic hypogonadism due to lossof functionof the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci U S A 2003; 100:10972-10976.
11. Messager S, Chatzidaki EE, Ma D, et al. Kisspeptin directly stimulates gonado-tropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci U S A 2005; 102:1761-1766.
12. Seminara SB, Messager S, Chatzidaki EE, et al. The GPR54 gene as a regulator of puberty. N Engl J Med 2003; 349:1614-1627.
13. Shahab M, Mastronardi C, Seminara SB, et al. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci U S A 2005; 102:2129-2134.
14. Bedecarrats GY, Linher KD, Janovick JA, et al. Four naturally occurring mutations in the human GnRH receptor affect ligand binding and receptor function. Mol Cell Endocrinol 2003; 205:51-64.
15. Bedecarrats GY, Linher KD, Kaiser UB. Two common naturally occurring mutations in the human gonadotropin-releasing hormone (GnRH) receptor have differential effects on gonadotropin gene expression and on GnRH-mediated signal transduction. J Clin Endocrinol Metab 2003; 88:834-843.
16. Wolczynski S, Laudanski P, Jarzabek K, et al. A case of complete hypogo-nadotropic hypogonadism with a mutation in the gonadotropin-releasing hormone receptor gene. Fertil Steril 2003; 79:442-444.
17. Karges B, Karges W, Mine M, et al. Mutation ala(171)thr stabilizes the gonadotropin-releasing hormone receptor in its inactive conformation, causing familial hypogonadotropic hypogonadism. J Clin Endocrinol Metab 2003; 88:1873-1879.
18. Layman LC, Cohen DP, Jin M, et al. Mutations in gonadotropin-releasing hormone receptor gene cause hypogonadotropic hypogonadism. Nat Genet 1998; 18:14-15.
19. Bhagavath B, Ozata M, Ozdemir IC, et al. The prevalence of gonadotropin-releasing hormone receptor mutations in a large cohort of patients with hypogonadotropic hypogonadism. Fertil Steril 2005; 84:951-957.
20. Beranova M, Oliveira LM, Bedecarrats GY, et al. Prevalence, phenotypic spectrum, and modes of inheritance of gonadotropin-releasing hormone receptor mutations in idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab 2001; 86:1580-1588.
21. Lin L, Conway GS, Hill NR, et al. A homozygous r262q mutation in the gonadotropin-releasing hormone receptor presenting as constitutional delay of growth and puberty with subsequent borderline oligospermia. J Clin Endocrinol Metab 2006; 91:5117-5121.
22. Sedlmeyer IL, Pearce CL, Trueman JA, et al. Determination of sequence variation and haplotype structure for the gonadotropin-releasing hormone (GnRH) and GnRH receptor genes: investigation of role in pubertal timing. J Clin Endocrinol Metab 2005; 90:1091-1099.
23. Irwig MS, Fraley GS, Smith JT, et al. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mrna in the male rat. Neuroendocrinology 2004; 80:264-272.
24. Gottsch ML, Cunningham MJ, Smith JT, et al. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004; 145:4073-4077.
25. Navarro VM, Castellano JM, Fernandez-Fernandez R, et al. Developmental and hormonally regulated messenger ribonucleic acid expression of kKiSS-1 and its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KiSS-1 peptide. Endocrinology 2004; 145:4565-4574.
26. Navarro VM, Fernandez-Fernandez R, Castellano JM, et al. Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol 2004; 561:379-386.
27. Plant TM. The role of KiSS-1 in the regulation of puberty in higher primates. Eur J Endocrinol 2006; 155 (Suppl 1):S11 -S16.
28. Funes S, Hedrick JA, Vassileva G, et al. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 2003; 312:1357-1363.
29. Lapatto R, Pallais JC, Zhang D, et al. KiSS1 -/- mice exhibit more variable hypogonadism than GPR54-/- mice. Endocrinology 2007; 148:4927-4936.
30. Gottsch ML, Clifton DK, Steiner RA. Kisspepeptin-GPR54 signaling in the neuro.
31. Han SK, Gottsch ML, Lee KJ, et al. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 2005; 25:11349-11356.
32. Teles MG, Bianco SD, Brito VN, et al. A GPR54-activating mutation in a patient with central precocious puberty. N Engl J Med 2008; 358:709-715.
33. Seminara SB. Converging at puberty's hub. Endocrinology 2007; 148:5145-5146.
34. Roth CL, Mastronardi C, Lomniczi A, et al. Expression of a tumor-related gene network increases in the mammalian hypothalamus at the time of female puberty. Endocrinology 2007; 148:5147-5161.
35. Franco B, Guioli S, Pragliola A, et al. A gene deleted in Kallmann's syndrome shares homology with neural cell adhesion and axonal path-finding molecules. Nature 1991; 353:529-536.
36. Hardelin JP, Levilliers J, Blanchard S, et al. Heterogeneity in the mutations responsible for x chromosome-linked Kallmann syndrome. Hum Mol Genet 1993; 2:373-377.
37. Legouis R, Hardelin JP, Levilliers J, et al. The candidate gene for the x-linked Kallmann syndrome encodes a protein related to adhesion molecules. Cell 1991; 67:423-435.
38. Dode C, Levilliers J, Dupont JM, et al. Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nat Genet 2003; 33:463-465.
39. DodeC,TeixeiraL, Levilliers J, et al. Kallmann syndrome: mutations in the genes encoding prokineticin-2 and prokineticin receptor-2. PLoS Genet 2006; 2:e175.
40. Kramer PR, Wray S. Novel gene expressed in nasal region influences outgrowth of olfactory axons and migration of luteinizing hormone-releasing hormone (lhrh) neurons. Genes Dev 2000; 14:1824-1834.
41. Miura K, Acierno JS Jr, Seminara SB. Characterization of the human nasal embryonic LHRH factor gene, NELF, and a mutation screening among 65 patients with idiopathic hypogonadotropic hypogonadism (IHH). J Hum Genet 2004; 49:265-268.
42. Pitteloud N, Quinton R, PearceS, et al. Digenic mutations account for variable phenotypes in idiopathic hypogonadotropic hypogonadism. J Clin Invest 2007; 117:457-463.
43. Pitteloud N, Acierno JS Jr, Meysing A, et al. Mutations in fibroblast growth factor receptor 1 cause both Kallmann syndrome and normosmic idiopathic hypogonadotropic hypogonadism. Proc Natl Acad Sci USA 2006; 103:6281 -6286.
44. Pitteloud N, Zhang C, Pignatelli D, et al. Loss-of-function mutation in the prokineticin 2 gene causes Kallmann syndrome and normosmic idiopathic hypogonadotropic hypogonadism. Proc Natl Acad Sci USA 2007; 104: 17447-17452.
45. Pitteloud N, Acierno JS Jr, Meysing AU, et al. 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 2005; 90:1317-1322.
46. RaivioT, Falardeau J, Dwyer A, et al. Reversal of idiopathic hypogonadotropic hypogonadism. N Engl J Med 2007; 357:863-873.
47. Mantzoros CS, Flier JS, Rogol AD. A longitudinal assessment of hormonal and physical alterations during normal puberty in boys. V. Rising leptin levels may signal the onset of puberty. J Clin Endocrinol Metab 1997; 82:1066-1070.
48. Smith JT, Acohido BV, Clifton DK, et al. Kiss-1 neurones are direct targets for leptin in the ob/ob mouse. J Neuroendocrinol 2006; 18:298-303.
49. Banerjee I, Trueman JA, Hall CM, et al. Phenotypic variation in constitutional delay of growth and puberty: relationship to specific leptin and leptin receptor gene polymorphisms. Eur J Endocrinol 2006; 155:121-126.
50. Habiby RL, Boepple P, Nachtigall L, et al. Adrenal hypoplasia congenita with hypogonadotropic hypogonadism: evidence that DAX1 mutations lead to combined hypothalmic and pituitary defects in gonadotropin production [see comments]. J Clin Invest 1996; 98:1055-1062.
51. Seminara SB, Achermann JC, Genel M, et al. X-linked adrenal hypoplasia congenita: a mutation in DAX1 expands the phenotypic spectrum in males and females. J Clin Endocrinol Metab 1999; 84:4501 -4509.
52. Parker KL, Schimmer BP. Steroidogenic factor 1: a key determinant of endocrine development and function. Endocr Rev 1997; 18:361-377.
53. Bakke M,ZhaoL, Parker KL. Approaches to define the role of SF-1 at different levels of the hypothalamic-pituitary-steroidogenic organ axis. Mol Cell Endocrinol 2001; 179:33-37.
54. Jackson RS, Creemers JW, Ohagi S, et al. Obesity and impaired prohormone processing associated with mutations in the human prohormone convertase 1 gene. Nat Genet 1997; 16:303-306.
55. Reindollar RH, McDonough PG. Delayed sexual development: common causes and basic clinical approach. Pediatr Ann 1981; 10:30-39.
56. ToublancJE, Roger M,ChaussainJL Etiologies of late puberty. Horm Res 1991; 36:136-140.
57. Sperlich M, Butenandt O,Schwarz HP. Final height and predicted height in boys with untreated constitutional growth delay. Eur J Pediatr 1995; 154:627-632.
58. Sedlmeyer IL, Hirschhorn JN, Palmert MR. Pedigree analysis of constitutional delay of growth and maturation: determination of familial aggregation and inheritance patterns. J Clin Endocrinol Metab 2002; 87:5581 -5586.
59. Sedlmeyer IL, Palmert MR. Delayed puberty: analysis of a large case series from an academic center. J Clin Endocrinol Metab 2002; 87:1613-1620.
60. Kaminski BA, Palmert MR. Human puberty: physiology, progression, and genetic regulation of variation in onset. In: Pfaff D, Arnold A, Etgen A, et al., editors. Hormones, brain, and behavior. 2nd ed. San Diego, CA: Elsevier Science 2008.
61. Romeo S, Pennacchio LA, Fu Y, et al. Population-based resequencing of angptl4 uncovers variations that reduce triglycerides and increase hdl. Nat Genet 2007; 39:513-516.
62. Topol EJ, Frazer KA.The resequencing imperative. Nat Genet 2007; 39:439-440.
63. Ambrosone CB, Moysich KB, Furberg H, et al. CYP17 genetic polymorphism, breast cancer, and breast cancer risk factors. Breast Cancer Res 2003; 5:R45-R51.
64. Dunning AM, Healey CS, Pharoah PD, et al. No association between a polymorphism in the steroid metabolism gene CYP17 and risk of breast cancer. Br J Cancer 1998; 77:2045-2047.
65. Feigelson HS, Coetzee GA, Kolonel LN, et al. A polymorphism in the CYP17 gene increases the risk of breast cancer. Cancer Res 1997; 57:1063-1065.
66. Gorai I, Tanaka K, Inada M, et al. Estrogen-metabolizing gene polymorphisms, but not estrogen receptor-alpha gene polymorphisms, are associated with the onset of menarche in healthy postmenopausal Japanese women. J Clin Endocrinol Metab 2003; 88:799-803.
67. Haiman CA, Hankinson SE, Spiegelman D, et al. The relationship between a polymorphism in CYP17 with plasma hormone levels and breast cancer. Cancer Res 1999; 59:1015-1020.
68. Lai J, Vesprini D,Chu W, et al. CYPgene polymorphisms and early menarche. Mol Genet Metab 2001; 74:449-457.
69. Weston A, Pan CF, Bleiweiss IJ, et al. CYP1 7 genotype and breast cancer risk. Cancer Epidemiol Biomarkers Prev 1998; 7:941-944.
70. Eriksson AL, Suuriniemi M, Mahonen A, et al. The comt val158met polymorphism is associated with early pubertal development, height and cortical bone mass in girls. Pediatr Res 2005; 58:71 -77.
71. Boot AM, van der Sluis IM, de Muinck Keizer-Schrama SM, et al. Estrogen receptor alpha gene polymorphisms and bone mineral density in healthy children and young adults. Calcif Tissue Int 2004; 74:495-500.
72. Long JR, Xu H, Zhao LJ, et al. The oestrogen receptor alpha gene is linked and/or associated with age of menarche in different ethnic groups. J Med Genet 2005; 42:796-800.
73. Stavrou I, Zois C, Ioannidis JP, et al. Association of polymorphisms of the oestrogen receptor alpha gene with the age of menarche. Hum Reprod 2002; 17:1101 -1105.
74. Weel AE, Uitterlinden AG, Westendorp IC, et al. Estrogen receptor polymorphism predicts the onset of natural and surgical menopause. J Clin Endocrinol Metab 1999; 84:3146-3150.
75. Xita N,Tsatsoulis A, Stavrou I, et al. Association of SHBG gene polymorphism with menarche. Mol Hum Reprod 2005; 11:459-462.
76. Comings DE, Muhleman D, Johnson JP, et al. Parent-daughter transmission of the androgen receptor gene as an explanation of the effect of father absence on age of menarche. Child Dev 2002; 73:1046-1051.
77. Jorm AF, Christensen H, Rodgers B, et al. Association of adverse childhood experiences, age of menarche, and adult reproductive behavior: does the androgen receptor gene play a role? Am J Med Genet B Neuropsychiatr Genet 2004; 125:105-111.
78. Gajdos Z, DeLellis Henderson K, Butler J, et al. Is age at menarche in the Hawaii and Los Angeles multiethnic cohort influenced by common sequence variation in genes that cause hypogonadotropic hypogonadism? Proceedings of the 89th Annual Meeting of the Endocrine Society; 2-5 June 2007; Toronto, Canada: Endocrine Society; 2007.
79. Guo Y, Shen H, Xiao P, et al. Genomewide linkage scan for quantitative trait loci underlying variation in age at menarche. J Clin Endocrinol Metab 2006; 91:1009-1014.
80. Rothenbuhler A, Fradin D, Heath S, et al. Weight-adjusted genome scan analysis for mapping quantitative trait loci for menarchal age. J Clin Endocrinol Metab 2006; 91:3534-3537.
81. Nathan BM, Hodges CA, Supelak PJ, et al. A quantitative trait locus on chromosome 6 regulates the onset of puberty in mice. Endocrinology 2006; 147:5132-5138.
82. Krewson TD, Supelak PJ, Hill AE, et al. Chromosomes 6 and 13 harbor genes that regulate pubertal timing in mouse chromosome substitution strains. Endocrinology 2004; 145:4447-4451.
83. Ojeda SR, Lomniczi A, Mastronardi C, et al. Minireview: the neuroendocrine regulation of puberty - is the time ripe for a systems biology approach? Endocrinology 2006; 147:1166-1174.
84. The Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 2007; 447:661 -678.
85. Frayling TM. Genome-wide association studies provide new insights into type 2 diabetes aetiology. Nat Rev Genet 2007; 8:657-662.