The igf 1 p2 promoter is an epigenetic qtl for circulating igf 1 and human growth

Clinical Epigenetics

Volumn 7, Issue 1, 2015, Pages 2-12

  Ouni, Meriem ^a   Gunes, Yasemin ^a   Belot, Marie Pierre ^a   Castell, Anne Laure ^b   Fradin, Delphine ^a   Bougnères, Pierre ^a,b  

^a INSERM   (France)

^b BICÊTRE HOSPITAL   (France)

Author keywords

DNA methylation; Epigenetics; Growth; Height; IGF1; QTLepi; Short stature; T DMR

Indexed keywords

SOMATOMEDIN C;

ARTICLE; BODY GROWTH; BODY HEIGHT; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DEMETHYLATION; EPIGENETICS; GENE; GENE EXPRESSION; GENE LOCUS; GENETIC VARIABILITY; GROWTH INHIBITION; HUMAN; HUMAN CELL; IGF1 GENE; LEUKOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN METHYLATION; QUANTITATIVE TRAIT LOCUS; REPORTER GENE;

EID: 84927168063     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-015-0062-8     Document Type: Article

References (76)

1. Cohen P, Rogol AD, Deal CL, Saenger P, Reiter EO, Ross JL, et al. Consensus statement on the diagnosis and treatment of children with idiopathic short stature: a summary of the Growth Hormone Research Society, the Lawson Wilkins Pediatric Endocrine Society, and the European Society for Paediatric Endocrinology Workshop. J Clin Endocrinol Metab. 2007;2008(93):4210–7.
2. Rosenfeld RG. The molecular basis of idiopathic short stature. Growth Horm IGF Res. 2005;15(Suppl A):S3–5.
3. Cole TJ. The secular trend in human physical growth: a biological view. Econ Hum Biol. 2003;1:161–8.
4. Galton F, Dickson JDH. Family likeness in stature. Proc R Soc Lond. 1886;40:42–73.
5. Visscher PM, McEvoy B, Yang J. From Galton to GWAS: quantitative genetics of human height. Genet Res. 2010;92:371–9.
6. Hirschhorn JN, Gajdos ZKZ. Genome-wide association studies: results from the first few years and potential implications for clinical medicine. Annu Rev Med. 2011;62:11–24.
7. Fisher RA. XV. - The correlation between relatives on the supposition of Mendelian inheritance. Earth Environ Sci Trans R Soc Edinb. 1919;52:399–433.
8. Silventoinen K, Sammalisto S, Perola M, Boomsma DI, Cornes BK, Davis C, et al. Heritability of adult body height: a comparative study of twin cohorts in eight countries. Twin Res. 2003;6:399–408.
9. Wood AR, Esko T, Yang J, Vedantam S, Pers TH, Gustafsson S, et al. Defining the role of common variation in the genomic and biological architecture of adult human height. Nat Genet. 2014;46:1173–86.
10. Lango Allen H, Estrada K, Lettre G, Berndt SI, Weedon MN, Rivadeneira F, et al. Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature. 2010;467:832–8.
11. Yang J, Benyamin B, McEvoy BP, Gordon S, Henders AK, Nyholt DR, et al. Common SNPs explain a large proportion of the heritability for human height. Nat Genet. 2010;42:565–9.
12. Murrell A, Rakyan VK, Beck S. From genome to epigenome. Hum Mol Genet. 2005;14(Spec No 1):R3–10.
13. Johannes F, Colot V, Jansen RC. Epigenome dynamics: a quantitative genetics perspective. Nat Rev Genet. 2008;9:883–90.
14. Rakyan VK, Down TA, Balding DJ, Beck S. Epigenome-wide association studies for common human diseases. Nat Rev Genet. 2011;12:529–41.
15. Woods KA, Camacho-Hübner C, Savage MO, Clark AJ. Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N Engl J Med. 1996;335:1363–7.
16. Lupu F, Terwilliger JD, Lee K, Segre GV, Efstratiadis A. Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth. Dev Biol. 2001;229:141–62.
17. Rogers I, Metcalfe C, Gunnell D, Emmett P, Dunger D, Holly J, et al. Insulin-like growth factor-I and growth in height, leg length, and trunk length between ages 5 and 10 years. J Clin Endocrinol Metab. 2006;91:2514–9.
18. Cohen P. Controversy in clinical endocrinology: problems with reclassification of insulin-like growth factor I production and action disorders. J Clin Endocrinol Metab. 2006;91:4235–6.
19. Frayling TM, Hattersley AT, McCarthy A, Holly J, Mitchell SMS, Gloyn AL, et al. A putative functional polymorphism in the IGF-I gene association studies with type 2 diabetes, adult height, glucose tolerance, and fetal growth in U.K. Populations. Diabetes. 2002;51:2313–6.
20. Lettre G, Butler JL, Ardlie KG, Hirschhorn JN. Common genetic variation in eight genes of the GH/IGF1 axis does not contribute to adult height variation. Hum Genet. 2007;122:129–39.
21. Kim J-J, Lee H-I, Park T, Kim K, Lee J-E, Cho NH, et al. Identification of 15 loci influencing height in a Korean population. J Hum Genet. 2009;55:27–31.
22. Okada Y, Kamatani Y, Takahashi A, Matsuda K, Hosono N, Ohmiya H, et al. A genome-wide association study in 19 633 Japanese subjects identified LHX3-QSOX2 and IGF1 as adult height loci. Hum Mol Genet. 2010;19:2303–12.
23. Harrela M, Koistinen H, Kaprio J, Lehtovirta M, Tuomilehto J, Eriksson J, et al. Genetic and environmental components of interindividual variation in circulating levels of IGF-I, IGF-II, IGFBP-1, and IGFBP-3. J Clin Invest. 1996;98:2612–5.
24. Kao PC, Matheny AP, Lang CA. Insulin-like growth factor-I comparisons in healthy twin children. J Clin Endocrinol Metab. 1994;78:310–2.
25. Verhaeghe J, Loos R, Vlietinck R, Van Herck E, van Bree R, DSchutter AM. C-peptide, insulin-like growth factors I and II, and insulin-like growth factor binding protein-1 in cord serum of twins: genetic versus environmental regulation. Am J Obstet Gynecol. 1996;175:1180–8.
26. Palles C, Johnson N, Coupland B, Taylor C, Carvajal J, Holly J, et al. Identification of genetic variants that influence circulating IGF1 levels: a targeted search strategy. Hum Mol Genet. 2008;17:1457–64.
27. Al-Zahrani A, Sandhu MS, Luben RN, Thompson D, Baynes C, Pooley KA, et al. IGF1 and IGFBP3 tagging polymorphisms are associated with circulating levels of IGF1, IGFBP3 and risk of breast cancer. Hum Mol Genet. 2006;15:1–10.
28. Wong H-L, DeLellis K, Probst-Hensch N, Koh W-P, Berg DVD, Lee H-P, et al. A new single nucleotide polymorphism in the insulin-like growth factor I regulatory region associates with colorectal cancer risk in Singapore Chinese. Cancer Epidemiol Biomarkers Prev. 2005;14:144–51.
29. Ester WA, Hokken-Koelega ACS. Polymorphisms in the IGF1 and IGF1R genes and children born small for gestational age: results of large population studies. Best Pract Res Clin Endocrinol Metab. 2008;22:415–31.
30. Vaessen N, Janssen JA, Heutink P, Hofman A, Lamberts SWJ, Oostra BA, et al. Association between genetic variation in the gene for insulin-like growth factor-I and low birthweight. Lancet. 2002;359:1036–7.
31. Rotwein P. Mapping the growth hormone - Stat5b - IGF-I transcriptional circuit. Trends Endocrinol Metab. 2012;23:186–93.
32. Bock C, Walter J, Paulsen M, Lengauer T. Inter-individual variation of DNA methylation and its implications for large-scale epigenome mapping. Nucleic Acids Res. 2008;36:e55.
33. Kuroda A, Rauch TA, Todorov I, Ku HT, Al-Abdullah IH, Kandeel F, et al. Insulin gene expression is regulated by DNA methylation. PLoS ONE. 2009;4:e6953.
34. Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmühl Y, Fischer D, et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci. 2009;12:1559–66.
35. Yang H, Adamo ML, Koval AP, McGuinness MC, Ben-Hur H, Yang Y, et al. Alternative leader sequences in insulin-like growth factor I mRNAs modulate translational efficiency and encode multiple signal peptides. Mol Endocrinol. 1995;9:1380–95.
36. Adamo ML, Ben-Hur H, Roberts CT, LeRoith D. Regulation of start site usage in the leader exons of the rat insulin-like growth factor-I gene by development, fasting, and diabetes. Mol Endocrinol. 1991;5:1677–86.
37. Oberbauer AM. The regulation of IGF-1 gene transcription and splicing during development and aging. Front Endocrinol. 2013;4:39.
38. Weedon MN, Lettre G, Freathy RM, Lindgren CM, Voight BF, Perry JRB, et al. A common variant of HMGA2 is associated with adult and childhood height in the general population. Nat Genet. 2007;39:1245–50.
39. Sanna S, Jackson AU, Nagaraja R, Willer CJ, Chen W-M, Bonnycastle LL, et al. Common variants in the GDF5-UQCC region are associated with variation in human height. Nat Genet. 2008;40:198–203.
40. Weedon MN, Lango H, Lindgren CM, Wallace C, Evans DM, Mangino M, et al. Genome-wide association analysis identifies 20 loci that influence adult height. Nat Genet. 2008;40:575–83.
41. Bogin B. Secular changes in childhood, adolescent and adult stature. Nestlé Nutr Inst Workshop Ser. 2013;71:115–26.
42. Clemmons DR, Underwood LE. Nutritional regulation of IGF-I and IGF binding proteins. Annu Rev Nutr. 1991;11:393–412.
43. Bird A. Putting the DNA back into DNA methylation. Nat Genet. 2011;43:1050–1.
44. Knight JC. Allele-specific gene expression uncovered. Trends Genet TIG. 2004;20:113–6.
45. Meaburn EL, Schalkwyk LC, Mill J. Allele-specific methylation in the human genome: implications for genetic studies of complex disease. Epigenetics. 2010;5:578–82.
46. Fradin D, Le Fur S, Mille C, Naoui N, Groves C, Zelenika D, et al. Association of the CpG methylation pattern of the proximal insulin gene promoter with type 1 diabetes. PLoS ONE. 2012;7:e36278.
47. Richards EJ. Population epigenetics. Curr Opin Genet Dev. 2008;18:221–6 [Chromosomes and Expression Mechanisms].
48. Bell JT, Pai AA, Pickrell JK, Gaffney DJ, Pique Regi R, Degner JF, et al. DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biol. 2011;12:R10.
49. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA. 2005;102:10604–9.
50. Kaminsky ZA, Tang T, Wang S-C, Ptak C, Oh GHT, Wong AHC, et al. DNA methylation profiles in monozygotic and dizygotic twins. Nat Genet. 2009;41:240–5.
51. Petronis A. Epigenetics and twins: three variations on the theme. Trends Genet TIG. 2006;22:347–50.
52. Yakar S, Pennisi P, Wu Y, Zhao H, LeRoith D. Clinical relevance of systemic and local IGF-I. In: Cianfarani S, Clemmons DR, Savage MO, editors. Endocrine Development. Basel: KARGER; 2005. p. 11–6.
53. Liu JL, Yakar S, LeRoith D. Conditional knockout of mouse insulin-like growth factor-1 gene using the Cre/loxP system. Proc Soc Exp Biol Med. 2000;223:344–51.
54. Feinberg AP, Irizarry RA, Fradin D, Aryee MJ, Murakami P, Aspelund T, et al. Personalized epigenomic signatures that are stable over time and covary with body mass index. Sci Transl Med. 2010;2:4967.
55. Talens RP, Boomsma DI, Tobi EW, Kremer D, Jukema JW, Willemsen G, et al. Variation, patterns, and temporal stability of DNA methylation: considerations for epigenetic epidemiology. FASEB J. 2010;24:3135–44.
56. Mill J, Heijmans BT. From promises to practical strategies in epigenetic epidemiology. Nat Rev Genet. 2013;14:585–94.
57. Wu H-C, Delgado-Cruzata L, Flom JD, Kappil M, Ferris JS, Liao Y, et al. Global methylation profiles in DNA from different blood cell types. Epigenetics. 2011;6:76–85.
58. Xie W, Schultz MD, Lister R, Hou Z, Rajagopal N, Ray P, et al. Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell. 2013;153:1134–48.
59. Takai D, Jones PA. Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc Natl Acad Sci U S A. 2002;99:3740–5.
60. Han H, Cortez CC, Yang X, Nichols PW, Jones PA, Liang G. DNA methylation directly silences genes with non-CpG island promoters and establishes a nucleosome occupied promoter. Hum Mol Genet. 2011;20:4299–310.
61. Eckhardt F, Lewin J, Cortese R, Rakyan VK, Attwood J, Burger M, et al. DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet. 2006;38:1378–85.
62. Weber M, Hellmann I, Stadler MB, Ramos L, Pääbo S, Rebhan M, et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet. 2007;39:457–66.
63. Gal-Yam EN, Egger G, Iniguez L, Holster H, Einarsson S, Zhang X, et al. Frequent switching of polycomb repressive marks and DNA hypermethylation in the PC3 prostate cancer cell line. Proc Natl Acad Sci USA. 2008;105:12979–84.
64. Klug M, Rehli M. Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics. 2006;1:127–30.
65. Varco-Merth B, Mirza K, Alzhanov DT, Chia DJ, Rotwein P. Biochemical characterization of diverse Stat5b-binding enhancers that mediate growth hormone-activated insulin-like growth factor-I gene transcription. PLoS ONE. 2012;7:e50278.
66. Chia DJ, Young JJ, Mertens AR, Rotwein P. Distinct alterations in chromatin organization of the two IGF-I promoters precede growth hormone-induced activation of IGF-I gene transcription. Mol Endocrinol. 2010;24:779–89.
67. Chia DJ, Rotwein P. Defining the epigenetic actions of growth hormone: acute chromatin changes accompany GH-activated gene transcription. Mol Endocrinol. 2010;24:2038–49.
68. Slatkin M. Epigenetic inheritance and the missing heritability problem. Genetics. 2009;182:845–50.
69. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, et al. Finding the missing heritability of complex diseases. Nature. 2009;461:747–53.
70. Atchley WR, Zhu J. Developmental quantitative genetics, conditional epigenetic variability and growth in mice. Genetics. 1997;147:765–76.
71. Dos Santos C, Essioux L, Teinturier C, Tauber M, Goffin V, Bougnères P. A common polymorphism of the growth hormone receptor is associated with increased responsiveness to growth hormone. Nat Genet. 2004;36:720–4.
72. Alberti C, Chevenne D, Mercat I, Josserand E, Armoogum-Boizeau P, Tichet J, et al. Serum concentrations of insulin-like growth factor (IGF)-1 and IGF binding protein-3 (IGFBP-3), IGF-1/IGFBP-3 ratio, and markers of bone turnover: reference values for French children and adolescents and z-score comparability with other references. Clin Chem. 2011;57:1424–35.
73. Jansen E, Steenbergh PH, LeRoith D, Roberts CT, Sussenbach JS. Identification of multiple transcription start sites in the human insulin-like growth factor-I gene. Mol Cell Endocrinol. 1991;78:115–25.
74. Tost J, Gut IG. DNA methylation analysis by pyrosequencing. Nat Protoc. 2007;2:2265–75.
75. Cleveland RJ, Gammon MD, Edmiston SN, Teitelbaum SL, Britton JA, Terry MB, et al. IGF1 CA repeat polymorphisms, lifestyle factors and breast cancer risk in the Long Island Breast Cancer Study Project. Carcinogenesis. 2006;27:758–65.
76. Arends N, Johnston L, Hokken-Koelega A, van Duijn C, de Ridder M, Savage M, et al. Polymorphism in the IGF-I gene: clinical relevance for short children born small for gestational age (SGA). J Clin Endocrinol Metab. 2002;87:2720.