Human longevity and variation in GH/IGF-1/insulin signaling, DNA damage signaling and repair and pro/antioxidant pathway genes: Cross sectional and longitudinal studies

Experimental Gerontology

Volumn 47, Issue 5, 2012, Pages 379-387

  Soerensen, Mette ^a,b   Dato, Serena ^a,c   Tan, Qihua ^a,b   Thinggaard, Mikael ^a   Kleindorp, Rabea ^d   Beekman, Marian ^e   Jacobsen, Rune ^a   Suchiman, Eka H D ^e   de Craen, Anton J M ^e   Westendorp, Rudi G J ^e   Schreiber, Stefan ^d   Stevnsner, Tinna ^f   Bohr, Vilhelm A ^g,h   Slagboom, P Eline ^e   Nebel, Almut ^d   Vaupel, James W ^a,h   Christensen, Kaare ^a,b   McGue, Matt ^a,i   Christiansen, Lene ^a,b  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b ODENSE UNIVERSITY HOSPITAL   (Denmark)

^c UNIVERSITY OF CALABRIA   (Italy)

^d UNIVERSITY OF KIEL   (Germany)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^f AARHUS UNIVERSITY   (Denmark)

^g NATIONAL INSTITUTE ON AGING   (United States)

^h MAX PLANCK INSTITUTE FOR DEMOGRAPHIC RESEARCH   (Germany)

ⁱ UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Association study; Candidate study; Case control data; Human longevity; Longitudinal data

Indexed keywords

DNA; GROWTH HORMONE; INSULIN; SOMATOMEDIN C;

ADULT; AGE DISTRIBUTION; AGED; ARTICLE; CASE CONTROL STUDY; COHORT ANALYSIS; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DENMARK; DNA DAMAGE; DNA REPAIR; FEMALE; FOLLOW UP; GENE; GENE LOCUS; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GERMANY; GHRHR GENE; GHSR GENE; GSR GENE; HUMAN; IGF2R GENE; INS GENE; KL GENE; LONGEVITY; LONGITUDINAL STUDY; MALE; NTHL1 GENE; POLB GENE; PRIORITY JOURNAL; RAD23 GENE; RAD52 GENE; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SURVIVAL RATE; WRN GENE; XDH GENE;

AGED; AGED, 80 AND OVER; ANTIOXIDANTS; CASE-CONTROL STUDIES; DNA DAMAGE; DNA REPAIR; FEMALE; HUMAN GROWTH HORMONE; HUMANS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; LONGEVITY; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; OXIDATION-REDUCTION; POLYMORPHISM, SINGLE NUCLEOTIDE; SIGNAL TRANSDUCTION;

EID: 84859853540     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2012.02.010     Document Type: Article

References (63)

1. Arking D.E., Atzmon G., Arking A., Barzilai N., Dietz H.C. Association between a functional variant of the KLOTHO gene and high-density lipoprotein cholesterol, blood pressure, stroke, and longevity. Circ. Res. 2005, 96:412-418.
2. Barrett J.C., Fry B., Maller J., Daly M.J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005, 21:263-265.
3. Bartke A. Minireview: role of the growth hormone/insulin-like growth factor system in mammalian aging. Endocrinology 2005, 146:3718-3723.
4. Beekman M., Nederstigt C., Suchiman H.E., Kremer D., van der B.R., Lakenberg N., Alemayehu W.G., de Craen A.J., Westendorp R.G., Boomsma D.I., de Geus E.J., Houwing-Duistermaat J.J., Heijmans B.T., Slagboom P.E. Genome-wide association study (GWAS)-identified disease risk alleles do not compromise human longevity. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:18046-18049.
5. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 1995, 57:289-300.
6. Berthold H.K., Giannakidou E., Krone W., Tregouet D.A., Gouni-Berthold I. Influence of ghrelin gene polymorphisms on hypertension and atherosclerotic disease. Hypertens. Res. 2010, 33:155-160.
7. Bonafe M., Barbieri M., Marchegiani F., Olivieri F., Ragno E., Giampieri C., Mugianesi E., Centurelli M., Franceschi C., Paolisso G. Polymorphic variants of insulin-like growth factor I (IGF-I) receptor and phosphoinositide 3-kinase genes affect IGF-I plasma levels and human longevity: cues for an evolutionarily conserved mechanism of life span control. J. Clin. Endocrinol. Metab. 2003, 88:3299-3304.
8. Bootsma-van der Wiel A., Van Exel E., de Craen A.J., Gussekloo J., Lagaay A.M., Knook D.L., Westendorp R.G. A high response is not essential to prevent selection bias: results from the Leiden 85-plus study. J. Clin. Epidemiol. 2002, 55:1119-1125.
9. Burtner C.R., Kennedy B.K. Progeria syndromes and ageing: what is the connection?. Nat. Rev. Mol. Cell Biol. 2010, 11:567-578.
10. Cabelof D.C., Ikeno Y., Nyska A., Busuttil R.A., Anyangwe N., Vijg J., Matherly L.H., Tucker J.D., Wilson S.H., Richardson A., Heydari A.R. Haploinsufficiency in DNA polymerase beta increases cancer risk with age and alters mortality rate. Cancer Res. 2006, 66:7460-7465.
11. Candore G., Balistreri C.R., Listi F., Grimaldi M.P., Vasto S., Colonna-Romano G., Franceschi C., Lio D., Caselli G., Caruso C. Immunogenetics, gender, and longevity. Ann. N. Y. Acad. Sci. 2006, 1089:516-537.
12. Castro E., Edland S.D., Lee L., Ogburn C.E., Deeb S.S., Brown G., Panduro A., Riestra R., Tilvis R., Louhija J., Penttinen R., Erkkola R., Wang L., Martin G.M., Oshima J. Polymorphisms at the Werner locus: II. 1074Leu/Phe, 1367Cys/Arg, longevity, and atherosclerosis. Am. J. Med. Genet. 2000, 95:374-380.
13. Christensen K., Johnson T.E., Vaupel J.W. The quest for genetic determinants of human longevity: challenges and insights. Nat. Rev. Genet. 2006, 7:436-448.
14. Christiansen L., Bathum L., Frederiksen H., Christensen K. Paraoxonase 1 polymorphisms and survival. Eur. J. Hum. Genet. 2004, 12:843-847.
15. Cluett C., Melzer D. Human genetic variations: beacons on the pathways to successful ageing. Mech. Ageing Dev. 2009, 130:553-563.
16. Deelen J., Uh H.W., Monajemi R., van H.D., Thijssen P.E., Bohringer S., van den Akker E.B., de Craen A.J., Rivadeneira F., Uitterlinden A.G., Westendorp R.G., Goeman J.J., Slagboom P.E., Houwing-Duistermaat J.J., Beekman M. Gene set analysis of GWAS data for human longevity highlights the relevance of the insulin/IGF-1 signaling and telomere maintenance pathways. Age (Dordr). 2011, 2011 Nov 24. doi:10.1007/s11357-011-9340-3.
17. Di Bona D., Vasto S., Capurso C., Christiansen L., Deiana L., Franceschi C., Hurme M., Mocchegiani E., Rea M., Lio D., Candore G., Caruso C. Effect of interleukin-6 polymorphisms on human longevity: a systematic review and meta-analysis. Ageing Res. Rev. 2009, 8:36-42.
18. Flachsbart F., Caliebe A., Kleindorp R., Blanche H., von Eller-Eberstein H., Nikolaus S., Schreiber S., Nebel A. Association of FOXO3A variation with human longevity confirmed in German centenarians. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2700-2705.
19. Flachsbart F., Franke A., Kleindorp R., Caliebe A., Blanche H., Schreiber S., Nebel A. Investigation of genetic susceptibility factors for human longevity - a targeted nonsynonymous SNP study. Mutat. Res. 2010, 694:9-13.
20. Flurkey K., Papaconstantinou J., Miller R.A., Harrison D.E. Lifespan extension and delayed immune and collagen aging in mutant mice with defects in growth hormone production. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:6736-6741.
21. Franceschi C., Motta L., Valensin S., Rapisarda R., Franzone A., Berardelli M., Motta M., Monti D., Bonafe M., Ferrucci L., Deiana L., Pes G.M., Carru C., Desole M.S., Barbi C., Sartoni G., Gemelli C., Lescai F., Olivieri F., Marchegiani F., Cardelli M., Cavallone L., Gueresi P., Cossarizza A., Troiano L., Pini G., Sansoni P., Passeri G., Lisa R., Spazzafumo L., Amadio L., Giunta S., Stecconi R., Morresi R., Viticchi C., Mattace R., De B.G., Baggio G. Do men and women follow different trajectories to reach extreme longevity? Italian Multicenter Study on Centenarians (IMUSCE). Aging (Milano) 2000, 12:77-84.
22. Giannakou M.E., Goss M., Junger M.A., Hafen E., Leevers S.J., Partridge L. Long-lived Drosophila with overexpressed dFOXO in adult fat body. Science 2004, 305:361.
23. Gueorguiev M., Lecoeur C., Meyre D., Benzinou M., Mein C.A., Hinney A., Vatin V., Weill J., Heude B., Hebebrand J., Grossman A.B., Korbonits M., Froguel P. Association studies on ghrelin and ghrelin receptor gene polymorphisms with obesity. Obesity 2009, 17:745-754. (Silver.Spring).
24. Hampe J., Wollstein A., Lu T., Frevel H.J., Will M., Manaster C., Schreiber S. An integrated system for high throughput TaqMan based SNP genotyping. Bioinformatics 2001, 17:654-655.
25. Harman D. Free radical theory of aging. Triangle 1973, 12:153-158.
26. Herskind A.M., McGue M., Holm N.V., Sorensen T.I., Harvald B., Vaupel J.W. The heritability of human longevity: a population-based study of 2872 Danish twin pairs born 1870-1900. Hum. Genet. 1996, 97:319-323.
27. Hjelmborg J.Vb., Iachine I., Skytthe A., Vaupel J.W., McGue M., Koskenvuo M., Kaprio J., Pedersen N.L., Christensen K. Genetic influence on human lifespan and longevity. Hum. Genet. 2006, 119:312-321.
28. Holzenberger M., Dupont J., Ducos B., Leneuve P., Geloen A., Even P.C., Cervera P., Le B.Y. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 2003, 421:182-187.
29. Hubacek J.A., Bohuslavova R., Skodova Z., Adamkova V. Variants within the ghrelin gene-association with HDL-cholesterol, but not with body mass index. Folia Biol. (Praha) 2007, 53:202-206.
30. Jacobsen R., Martinussen T., Christiansen L., Jeune B., ndersen-Ranberg K., Vaupel J.W., Christensen K. Increased effect of the ApoE gene on survival at advanced age in healthy and long-lived Danes: two nationwide cohort studies. Aging Cell 2010, 9:1004-1009.
31. Kawano T., Ito Y., Ishiguro M., Takuwa K., Nakajima T., Kimura Y. Molecular cloning and characterization of a new insulin/IGF-like peptide of the nematode Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 2000, 273:431-436.
32. Kenyon C.J. The genetics of ageing. Nature 2010, 464:504-512.
33. Kim D.J., Yi S.M., Lee S.Y., Kang H.S., Choi Y.H., Song Y.W., Park S.C. Association between the MLH1 gene and longevity. Hum. Genet. 2006, 119:353-354.
34. Kuningas M., Mooijaart S.P., van H.D., Zwaan B.J., Slagboom P.E., Westendorp R.G. Genes encoding longevity: from model organisms to humans. Aging Cell 2008, 7:270-280.
35. Kuro-o M., Matsumura Y., Aizawa H., Kawaguchi H., Suga T., Utsugi T., Ohyama Y., Kurabayashi M., Kaname T., Kume E., Iwasaki H., Iida A., Shiraki-Iida T., Nishikawa S., Nagai R., Nabeshima Y.I. Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 1997, 390:45-51.
36. Kurosu H., Yamamoto M., Clark J.D., Pastor J.V., Nandi A., Gurnani P., McGuinness O.P., Chikuda H., Yamaguchi M., Kawaguchi H., Shimomura I., Takayama Y., Herz J., Kahn C.R., Rosenblatt K.P., Kuro-o M. Suppression of aging in mice by the hormone Klotho. Science 2005, 309:1829-1833.
37. Li Y., Wang W.J., Cao H., Lu J., Wu C., Hu F.Y., Guo J., Zhao L., Yang F., Zhang Y.X., Li W., Zheng G.Y., Cui H., Chen X., Zhu Z., He H., Dong B., Mo X., Zeng Y., Tian X.L. Genetic association of FOXO1A and FOXO3A with longevity trait in Han Chinese populations. Hum. Mol. Genet. 2009, 18:4897-4904.
38. Lunetta K.L., D'Agostino R.B., Karasik D., Benjamin E.J., Guo C.Y., Govindaraju R., Kiel D.P., Kelly-Hayes M., Massaro J.M., Pencina M.J., Seshadri S., Murabito J.M. Genetic correlates of longevity and selected age-related phenotypes: a genome-wide association study in the Framingham Study. BMC Med. Genet. 2007, 8(Suppl. 1):S13.
39. Mockett R.J., Sohal R.S., Orr W.C. Overexpression of glutathione reductase extends survival in transgenic Drosophila melanogaster under hyperoxia but not normoxia. FASEB J. 1999, 13:1733-1742.
40. Montesanto A., Latorre V., Giordano M., Martino C., Domma F., Passarino G. The genetic component of human longevity: analysis of the survival advantage of parents and siblings of Italian nonagenarians. Eur. J. Hum. Genet. 2011, 19(8):882-886.
41. Nebel A., Croucher P.J., Stiegeler R., Nikolaus S., Krawczak M., Schreiber S. No association between microsomal triglyceride transfer protein (MTP) haplotype and longevity in humans. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:7906-7909.
42. Nebel A., Flachsbart F., Till A., Caliebe A., Blanche H., Arlt A., Hasler R., Jacobs G., Kleindorp R., Franke A., Shen B., Nikolaus S., Krawczak M., Rosenstiel P., Schreiber S. A functional EXO1 promoter variant is associated with prolonged life expectancy in centenarians. Mech. Ageing Dev. 2009, 130:691-699.
43. Nybo H., Gaist D., Jeune B., Bathum L., McGue M., Vaupel J.W., Christensen K. The Danish 1905 cohort: a genetic-epidemiological nationwide survey. J. Aging Health 2001, 13:32-46.
44. Pan J., Lin J., Izzo J.G., Liu Y., Xing J., Huang M., Ajani J.A., Wu X. Genetic susceptibility to esophageal cancer: the role of the nucleotide excision repair pathway. Carcinogenesis 2009, 30:785-792.
45. Park P.U., Defossez P.A., Guarente L. Effects of mutations in DNA repair genes on formation of ribosomal DNA circles and life span in Saccharomyces cerevisiae. Mol. Cell. Biol. 1999, 19:3848-3856.
46. Pawlikowska L., Hu D., Huntsman S., Sung A., Chu C., Chen J., Joyner A.H., Schork N.J., Hsueh W.C., Reiner A.P., Psaty B.M., Atzmon G., Barzilai N., Cummings S.R., Browner W.S., Kwok P.Y., Ziv E. Association of common genetic variation in the insulin/IGF1 signaling pathway with human longevity. Aging Cell 2009, 8:460-472.
47. Pawlikowska L., Hu D., Huntsman S., Sung A., Chu C., Chen J., Joyner A.H., Schork N.J., Hsueh W.C., Reiner A.P., Psaty B.M., Atzmon G., Barzilai N., Cummings S.R., Browner W.S., Kwok P.Y., Ziv E. Association of common genetic variation in the insulin/IGF1 signaling pathway with human longevity. Aging Cell 2009, 8:460-472.
48. Pedersen C.B., Gotzsche H., Moller J.O., Mortensen P.B. The Danish Civil Registration System. A cohort of eight million persons. Dan. Med. Bull. 2006, 53:441-449.
49. Purcell S., Neale B., Todd-Brown K., Thomas L., Ferreira M.A.R., Bender D., Maller J., Sklar P., de Bakker P.I.W., Daly M.J., Sham P.C. PLINK: a toolset for whole-genome association and population-based linkage analysis. Am. J. Hum. Genet. 2007, 81.
50. Scarpaci S., Frasca D., Barattini P., Guidi L., Doria G. DNA damage recognition and repair capacities in human naive and memory T cells from peripheral blood of young and elderly subjects. Mech. Ageing Dev. 2003, 124:517-524.
51. Schildkraut J.M., Iversen E.S., Wilson M.A., Clyde M.A., Moorman P.G., Palmieri R.T., Whitaker R., Bentley R.C., Marks J.R., Berchuck A. Association between DNA damage response and repair genes and risk of invasive serous ovarian cancer. PLoS One 2010, 5:e10061.
52. Shih D.M., Gu L., Xia Y.R., Navab M., Li W.F., Hama S., Castellani L.W., Furlong C.E., Costa L.G., Fogelman A.M., Lusis A.J. Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature 1998, 394:284-287.
53. Skytthe A., Kyvik K., Holm N.V., Vaupel J.W., Christensen K. The Danish Twin Registry: 127 birth cohorts of twins. Twin Res. 2002, 5:352-357.
54. Soerensen M., Dato S., Christensen K., McGue M., Stevnsner T., Bohr V.A., Christiansen L. Replication of an association of variation in the FOXO3A gene with human longevity using both case-control and longitudinal data. Aging Cell 2010, 9:1010-1017.
55. Tyner S.D., Venkatachalam S., Choi J., Jones S., Ghebranious N., Igelmann H., Lu X., Soron G., Cooper B., Brayton C., Hee P.S., Thompson T., Karsenty G., Bradley A., Donehower L.A. p53 mutant mice that display early ageing-associated phenotypes. Nature 2002, 415:45-53.
56. van der Horst G.T., van S.H., Berg R.J., van Gool A.J., de W.J., Weeda G., Morreau H., Beems R.B., van Kreijl C.F., de Gruijl F.R., Bootsma D., Hoeijmakers J.H. Defective transcription-coupled repair in Cockayne syndrome B mice is associated with skin cancer predisposition. Cell 1997, 89:425-435.
57. van Heemst D., Beekman M., Mooijaart S.P., Heijmans B.T., Brandt B.W., Zwaan B.J., Slagboom P.E., Westendorp R.G. Reduced insulin/IGF-1 signalling and human longevity. Aging Cell 2005, 4:79-85.
58. van Heemst D., Mooijaart S.P., Beekman M., Schreuder J., de Craen A.J., Brandt B.W., Slagboom P.E., Westendorp R.G. Variation in the human TP53 gene affects old age survival and cancer mortality. Exp. Gerontol. 2005, 40:11-15.
59. Van Ness B., Ramos C., Haznadar M., Hoering A., Haessler J., Crowley J., Jacobus S., Oken M., Rajkumar V., Greipp P., Barlogie B., Durie B., Katz M., Atluri G., Fang G., Gupta R., Steinbach M., Kumar V., Mushlin R., Johnson D., Morgan G. Genomic variation in myeloma: design, content, and initial application of the Bank On A Cure SNP Panel to detect associations with progression-free survival. BMC Med. 2008, 6:26.
60. Willcox B.J., Donlon T.A., He Q., Chen R., Grove J.S., Yano K., Masaki K.H., Wilcox D.C., Rodriguez B., Curb J.D. FOXO3A genotype is strongly associated with human longevity. Proc. Natl. Acad. Sci. 2008, 105:13987-13992.
61. Yang X.R., Pfeiffer R.M., Wheeler W., Yeager M., Chanock S., Tucker M.A., Goldstein A.M. Identification of modifier genes for cutaneous malignant melanoma in melanoma-prone families with and without CDKN2A mutations. Int. J. Cancer 2009, 125:2912-2917.
62. Yashin A.I., De B.G., Vaupel J.W., Tan Q., Andreev K.F., Iachine I.A., BonaFe M., Valensin S., De L.M., Carotenuto L., Franceschi C. Genes and longevity: lessons from studies of centenarians. J. Gerontol. A Biol. Sci. Med. Sci. 2000, 55:B319-B328.
63. Yashin A.I., Wu D., Arbeev K.G., Ukraintseva S.V. Joint influence of small-effect genetic variants on human longevity. Aging (Albany NY) 2010, 2:612-620.