Genome-wide analysis reveals DNA methylation markers that vary with both age and obesity

Gene

Volumn 548, Issue 1, 2014, Pages 61-67

  Almén, Markus Sällman ^a   Nilsson, Emil K ^a   Jacobsson, Josefin A ^a   Kalnina, Ineta ^b   Klovins, Janis ^b   Fredriksson, Robert ^a   Schiöth, Helgi B ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF LATVIA   (Latvia)

Author keywords

Aging; Epigenetics; Microarray; Obesity

Indexed keywords

TELOMERASE;

ADCY1 GENE; ADULT; AGE; AGED; AGING; AGPAT4 GENE; AQPEP GENE; ARTICLE; ATP8A2 GENE; BLOOD ANALYSIS; BODY MASS; BODY WEIGHT; BRUNOL6 GENE; CECR6 GENE; CLINICAL ARTICLE; CPG ISLAND; CXADR GENE; DNA METHYLATION; DNA PROBE; ENZYME ACTIVE SITE; EPIGENETICS; FBLIM1 GENE; FEMALE; FNDC4 GENE; FOXE3 GENE; GENE; GENETIC ANALYSIS; GENETIC SUSCEPTIBILITY; GENOTYPE; HBQ1 GENE; HTR7 GENE; HUMAN; INTRON; KCNS2 GENE; LIFESTYLE; LMX1B GENE; MALE; MLNR GENE; NAGS GENE; NAT8L GENE; NHLRC1 GENE; NNAT GENE; OBESITY; PIGC GENE; PRIORITY JOURNAL; RNH1 GENE; SERHL GENE; STATISTICAL MODEL; ZNF154 GENE;

AGING; EPIGENETICS; MICROARRAY; OBESITY;

ADULT; AGED; AGING; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENETIC MARKERS; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MIDDLE AGED; OBESITY; PROTEINS; TELOMERASE;

EID: 84904731621     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2014.07.009     Document Type: Article

References (53)

1. Almen M.S., Jacobsson J.A., Moschonis G., Benedict C., Chrousos G.P., Fredriksson R., et al. Genome wide analysis reveals association of a FTO gene variant with epigenetic changes. Genomics 2012, 99(3):132-137. (Mar, PubMed PMID: 22234326. Epub 2012/01/12. eng).
2. Alves M.K., Faria M.H., Neves Filho E.H., Ferrasi A.C., Pardini M.I., de Moraes Filho M.O., et al. CDKN2A promoter hypermethylation in astrocytomas is associated with age and sex. Int. J. Surg. 2013, 11(7):549-553. (PubMed PMID: 23721661. Epub 2013/06/01. eng).
3. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 2000, 25(1):25-29. (May, PubMed PMID: 10802651. Pubmed Central PMCID: PMC3037419. Epub 2000/05/10. eng).
4. Benjamini Y., Drai D., Elmer G., Kafkafi N., Golani I. Controlling the false discovery rate in behavior genetics research. Behav. Brain Res. 2001, 125(1-2):279-284.
5. Bergman O., Hakansson A., Westberg L., Belin A.C., Sydow O., Olson L., et al. Do polymorphisms in transcription factors LMX1A and LMX1B influence the risk for Parkinson's disease?. J. Neural Transm. 2009, 116(3):333-338. (Mar, PubMed PMID: 19189040. Epub 2009/02/04. eng).
6. Beydoun M.A., Beydoun H.A., Wang Y. Obesity and central obesity as risk factors for incident dementia and its subtypes: a systematic review and meta-analysis. Obes. Rev. 2008, 9(3):204-218. (May, PubMed PMID: 18331422. Epub 2008/03/12. eng).
7. Bibikova M., Le J., Barnes B., Saedinia-Melnyk S., Zhou L., Shen R., et al. Genome-wide DNA methylation profiling using Infinium® assay. Epigenomics 2009, 1(1):177-200.
8. Bird A., Taggart M., Frommer M., Miller O.J., Macleod D. A fraction of the mouse genome that is derived from islands of nonmethylated, CpG-rich DNA. Cell 1985, 40(1):91-99. (Jan, PubMed PMID: 2981636. Epub 1985/01/01. eng).
9. Bjornsson H.T., Sigurdsson M.I., Fallin M.D., Irizarry R.A., Aspelund T., Cui H., et al. Intra-individual change over time in DNA methylation with familial clustering. JAMA 2008, 299(24):2877-2883. (June 25).
10. Bocklandt S., Lin W., Sehl M.E., Sánchez F.J., Sinsheimer J.S., Horvath S., et al. Epigenetic predictor of age. PLoS One 2011, 6(6):e14821.
11. Bollati V., Galimberti D., Pergoli L., Dalla Valle E., Barretta F., Cortini F., et al. DNA methylation in repetitive elements and Alzheimer disease. Brain Behav. Immun. 2011, 25(6):1078-1083.
12. Calabrese R., Zampieri M., Mechelli R., Annibali V., Guastafierro T., Ciccarone F., et al. Methylation-dependent PAD2 upregulation in multiple sclerosis peripheral blood. Mult. Scler. 2011, 18(3):299-304. (August 30).
13. Calle E.E., Rodriguez C., Walker-Thurmond K., Thun M.J. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N. Engl. J. Med. 2003, 348(17):1625-1638. (Apr 24, PubMed PMID: 12711737. Epub 2003/04/25. eng).
14. Campion J., Milagro F.I., Martinez J.A. Individuality and epigenetics in obesity. Obes. Rev. 2009, 10(4):383-392. (Jul, PubMed PMID: 19413700. Epub 2009/05/06. eng).
15. Chouliaras L., van den Hove D.L., Kenis G., Dela Cruz J., Lemmens M.A., van Os J., et al. Caloric restriction attenuates age-related changes of DNA methyltransferase 3a in mouse hippocampus. Brain Behav. Immun. 2011, 25(4):616-623. (May, PubMed PMID: 21172419. Epub 2010/12/22. eng).
16. Colman R.J., Anderson R.M., Johnson S.C., Kastman E.K., Kosmatka K.J., Beasley T.M., et al. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science (New York, N.Y.) 2009, 325(5937):201-204. (Jul 10, PubMed PMID: 19590001. Pubmed Central PMCID: 2812811. Epub 2009/07/11. eng).
17. Dempster E.L., Pidsley R., Schalkwyk L.C., Owens S., Georgiades A., Kane F., et al. Disease-associated epigenetic changes in monozygotic twins discordant for schizophrenia and bipolar disorder. Hum. Mol. Genet. 2011, 20(24):4786-4796.
18. Ehrlich M., Gama-Sosa M.A., Huang L.H., Midgett R.M., Kuo K.C., McCune R.A., et al. Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Res. 1982, 10(8):2709-2721. (Apr 24, PubMed PMID: 7079182. Pubmed Central PMCID: 320645. Epub 1982/04/24. eng).
19. Feighner S.D., Tan C.P., McKee K.K., Palyha O.C., Hreniuk D.L., Pong S.-S., et al. Receptor for motilin identified in the human gastrointestinal system. Science 1999, 284(5423):2184-2188. (June 25).
20. Feinberg A.P., Irizarry R.A. Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. Proc. Natl. Acad. Sci. 2010, 107(Suppl. 1):1757-1764. (January 26).
21. Fraga M.F., Ballestar E., Paz M.F., Ropero S., Setien F., Ballestar M.L., et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(30):10604-10609. (July 26).
22. Franks P.W., Ling C. Epigenetics and obesity: the devil is in the details. BMC Med. 2010, 8:88. (PubMed PMID: 21176136. Pubmed Central PMCID: 3019199. Epub 2010/12/24. eng).
23. Frayling T.M., Timpson N.J., Weedon M.N., Zeggini E., Freathy R.M., Lindgren C.M., et al. A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science 2007, 316(5826):889-894. (May 11, PubMed PMID: 17434869. Pubmed Central PMCID: 2646098. Epub 2007/04/17. eng).
24. Gentleman R., Carey V., Bates D., Bolstad B., Dettling M., Dudoit S., et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004, 5(10):R80. (PubMed PMID). 10.1186/gb-2004-5-10-r80.
25. Haslam D.W., James W.P. Obesity. Lancet 2005, 366(9492):1197-1209. (Oct 1, PubMed PMID: 16198769. Epub 2005/10/04. eng).
26. Heijmans B.T., Kremer D., Tobi E.W., Boomsma D.I., Slagboom P.E. Heritable rather than age-related environmental and stochastic factors dominate variation in DNA methylation of the human IGF2/H19 locus. Hum. Mol. Genet. 2007, 16(5):547-554. (March 1).
27. Heyn H., Li N., Ferreira H.J., Moran S., Pisano D.G., Gomez A., Diez J., Sanchez-Mut J.V., Setien F., Carmona F.J., Puca A.A., Sayols S., Pujana M.A., Serra-Musach J., Iglesias-Platas I., Formiga F., Fernandez A.F., Fraga M.F., Health S.C., Valencia A., Gut I.G., Wang J., Esteller M. Distinct DNA methylomes of newborns and centenarians. Proc. Natl. Acad. Sci. 2012, 109(26):10522-10527. (jun;26).
28. Hindorff L.A., Sethupathy P., Junkins H.A., Ramos E.M., Mehta J.P., Collins F.S., et al. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc. Natl. Acad. Sci. 2009, 106(23):9362-9367. (June 9).
29. Horvath S., Zhang Y., Langfelder P., Kahn R.S., Boks M.P., van Eijk K., et al. Aging effects on DNA methylation modules in human brain and blood tissue. Genome Biol. 2012, 13(10):R97. (Oct 3, PubMed PMID: 23034122. Epub 2012/10/05. Eng.).
30. Hotamisligil G.S. Inflammation and metabolic disorders. Nature 2006, 444(7121):860-867. (Dec 14, PubMed PMID: 17167474. Epub 2006/12/15. eng).
31. Jacobsson J.A., Danielsson P., Svensson V., Klovins J., Gyllensten U., Marcus C., et al. Major gender difference in association of FTO gene variant among severely obese children with obesity and obesity related phenotypes. Biochem. Biophys. Res. Commun. 2008, 368(3):476-482.
32. Kamburov A., Wierling C., Lehrach H., Herwig R. ConsensusPathDB-a database for integrating human functional interaction networks. Nucleic Acids Res. 2009, 37(Database issue):D623-D628. (Jan, PubMed PMID: 18940869. Pubmed Central PMCID: PMC2686562. Epub 2008/10/23. eng).
33. Kamburov A., Pentchev K., Galicka H., Wierling C., Lehrach H., Herwig R. ConsensusPathDB: toward a more complete picture of cell biology. Nucleic Acids Res. 2011, 39(Database issue):D712-D717. (Jan, PubMed PMID: 21071422. Pubmed Central PMCID: PMC3013724. Epub 2010/11/13. eng).
34. Kanehisa M., Goto S., Kawashima S., Okuno Y., Hattori M. The KEGG resource for deciphering the genome. Nucleic Acids Res. 2004, 32(Suppl. 1):D277-D280. (January 1).
35. Kim T.Y., Lee H.J., Hwang K.S., Lee M., Kim J.W., Bang Y.J., et al. Methylation of RUNX3 in various types of human cancers and premalignant stages of gastric carcinoma. Lab. Invest. 2004, 84(4):479-484. (Apr, PubMed PMID: 14968123. Epub 2004/02/18. eng).
36. Koch C.M., Wagner W. Epigenetic-aging-signature to determine age in different tissues. Aging (Albany NY) 2011, 3(10):1018-1027. (20111026).
37. Ladd A.N., Nguyen N.H., Malhotra K., Cooper T.A. CELF6, a member of the CELF family of RNA-binding proteins, regulates muscle-specific splicing enhancer-dependent alternative splicing. J. Biol. Chem. 2004, 279(17):17756-17764. (April 23).
38. Liau J.Y., Liao S.L., Hsiao C.H., Lin M.C., Chang H.C., Kuo K.T. Hypermethylation of the CDKN2A gene promoter is a frequent epigenetic change in periocular sebaceous carcinoma and is associated with younger patient age. Hum. Pathol. 2014, 45(3):533-539. (Mar, PubMed PMID: 24440092. Epub 2014/01/21. eng).
39. Liu L., Wylie R.C., Andrews L.G., Tollefsbol T.O. Aging, cancer and nutrition: the DNA methylation connection. Mech. Ageing Dev. 2003, 124(10-12):989-998.
40. Liu F., Arias-Vasquez A., Sleegers K., Aulchenko Y.S., Kayser M., Sanchez-Juan P., et al. A genomewide screen for late-onset Alzheimer disease in a genetically isolated Dutch population. Am. J. Hum. Genet. 2007, 81(1):17-31. (Jul, PubMed PMID: 17564960. Pubmed Central PMCID: 1950931. Epub 2007/06/15. eng).
41. Milagro F.I., Campion J., Cordero P., Goyenechea E., Gomez-Uriz A.M., Abete I., et al. A dual epigenomic approach for the search of obesity biomarkers: DNA methylation in relation to diet-induced weight loss. FASEB J. 2011, 25(4):1378-1389. (Apr, PubMed PMID: 21209057. Epub 2011/01/07. eng).
42. Mohn F., Weber M., Rebhan M., Roloff T.C., Richter J., Stadler M.B., et al. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell 2008, 30(6):755-766. (Jun 20, PubMed PMID: 18514006. Epub 2008/06/03. eng).
43. Rando T.A. Epigenetics and aging. Exp. Gerontol. 2010, 45(4):253-254.
44. Smyth G. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 2004, 3(1):25.
45. Stein R., Razin A., Cedar H. In vitro methylation of the hamster adenine phosphoribosyltransferase gene inhibits its expression in mouse L cells. Proc. Natl. Acad. Sci. U. S. A. 1982, 79(11):3418-3422. (Jun, PubMed PMID: 6954487. Pubmed Central PMCID: 346431. Epub 1982/06/01. eng).
46. Storey J.D., Tibshirani R. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(16):9440-9445. (Aug 5, PubMed PMID: 12883005. Pubmed Central PMCID: 170937. Epub 2003/07/29. eng).
47. Toyota M., Ahuja N., Ohe-Toyota M., Herman J.G., Baylin S.B., Issa J.P. CpG island methylator phenotype in colorectal cancer. Proc. Natl. Acad. Sci. U. S. A. 1999, 96(15):8681-8686. (Jul 20, PubMed PMID: 10411935. Pubmed Central PMCID: 17576. Epub 1999/07/21. eng).
48. Tra J., Kondo T., Lu Q., Kuick R., Hanash S., Richardson B. Infrequent occurrence of age-dependent changes in CpG island methylation as detected by restriction landmark genome scanning. Mech. Ageing Dev. 2002, 123(11):1487-1503. (Sep, PubMed PMID: 12425956. Epub 2002/11/12. eng).
49. Vrang N., Meyre D., Froguel P., Jelsing J., Tang-Christensen M., Vatin V., et al. The imprinted gene neuronatin is regulated by metabolic status and associated with obesity. Obesity (Silver Spring) 2010, 18(7):1289-1296. (Jul, Pubmed Central PMCID: 2921166. Epub 2009/10/24. eng).
50. Wang X., Zhu H., Snieder H., Su S., Munn D., Harshfield G., et al. Obesity related methylation changes in DNA of peripheral blood leukocytes. BMC Med. 2010, 8:87. (PubMed PMID: 21176133. Pubmed Central PMCID: 3016263. Epub 2010/12/24. eng).
51. Weng N.P., Levine B.L., June C.H., Hodes R.J. Regulated expression of telomerase activity in human T lymphocyte development and activation. J. Exp. Med. 1996, 183(6):2471-2479. (Jun 1, PubMed PMID: 8676067. Pubmed Central PMCID: 2192611. Epub 1996/06/01. eng).
52. Wilson V.L., Jones P.A. DNA methylation decreases in aging but not in immortal cells. Science (New York, N.Y.) 1983, 220(4601):1055-1057. (Jun 3, PubMed PMID: 6844925. Epub 1983/06/03. eng).
53. Wilson V.L., Smith R.A., Ma S., Cutler R.G. Genomic 5-methyldeoxycytidine decreases with age. J. Biol. Chem. 1987, 262(21):9948-9951. (Jul 25, PubMed PMID: 3611071. Epub 1987/07/25. eng).