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PMID: 26355015 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, N.I.H., Extramural

A Genetic Network Associated With Stress Resistance, Longevity, and Cancer in Humans.

Levine ME, Crimmins EM

Abstract

Human longevity and diseases are likely influenced by multiple interacting genes within a few biologically conserved pathways. Using long-lived smokers as a phenotype (n = 90)-a group whose survival may signify innate resilience-we conducted a genome-wide association study comparing them to smokers at ages 52-69 (n = 730). These results were used to conduct a functional interaction network and pathway analysis, to identify single nucleotide polymorphisms that collectively related to smokers' longevity. We identified a set of 215 single nucleotide polymorphisms (all of which had p <5×10(-3) in the genome-wide association study) that were located within genes making-up a functional interaction network. These single nucleotide polymorphisms were then used to create a weighted polygenic risk score that, using an independent validation sample of nonsmokers (N = 6,447), was found to be significantly associated with a 22% increase in the likelihood of being aged 90-99 (n = 253) and an over threefold increase in the likelihood of being a centenarian (n = 4), compared with being at ages 52-79 (n = 4,900). Additionally, the polygenic risk score was also associated with an 11% reduction in cancer prevalence over up to 18 years (odds ratio: 0.89, p = .011). Overall, using a unique phenotype and incorporating prior knowledge of biological networks, this study identified a set of single nucleotide polymorphisms that together appear to be important for human aging, stress resistance, cancer, and longevity.

Keywords
Cancer Genetic network HRS Longevity Polygenic risk score Resilience
MeSH Terms
Aged Aged, 80 and over Aging/genetics Alleles Case-Control Studies Gene Regulatory Networks Genome-Wide Association Study Genotype Humans Longevity/genetics Longitudinal Studies Middle Aged Neoplasms/genetics Phenotype Polymorphism, Single Nucleotide Smoking Stress, Physiological/genetics United States
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Levine Morgan E
Department of Human Genetics, David Geffen School of Medicine, University of California Los Angeles. [email protected].
Crimmins Eileen M
Davis School of Gerontology, University of Southern California, Los Angeles.
References (48)
48 references, click to expand
  1. Evolutionary medicine: from dwarf model systems to healthy centenarians?
    Science. 2003 Feb 28;299(5611):1342-6 PMID: 12610293
  2. Population structure and eigenanalysis.
    PLoS Genet. 2006 Dec;2(12):e190 PMID: 17194218
  3. Cohort Profile: the Health and Retirement Study (HRS).
    Int J Epidemiol. 2014 Apr;43(2):576-85 PMID: 24671021
  4. Joint influence of small-effect genetic variants on human longevity.
    Aging (Albany NY). 2010 Sep;2(9):612-20 PMID: 20834067
  5. Speed-bumps ahead for the genetics of later-life diseases.
    Trends Genet. 2011 Oct;27(10):387-8 PMID: 21824675
  6. Genetic influence on human lifespan and longevity.
    Hum Genet. 2006 Apr;119(3):312-21 PMID: 16463022
  7. Oxidative stress and accelerated vascular aging: implications for cigarette smoking.
    Front Biosci (Landmark Ed). 2009 Jan 01;14:3128-44 PMID: 19273262
  8. The Reactome pathway knowledgebase.
    Nucleic Acids Res. 2014 Jan;42(Database issue):D472-7 PMID: 24243840
  9. GWAS of longevity in CHARGE consortium confirms APOE and FOXO3 candidacy.
    J Gerontol A Biol Sci Med Sci. 2015 Jan;70(1):110-8 PMID: 25199915
  10. Prediction of individual genetic risk to disease from genome-wide association studies.
    Genome Res. 2007 Oct;17(10):1520-8 PMID: 17785532
  11. Cytoscape: a software environment for integrated models of biomolecular interaction networks.
    Genome Res. 2003 Nov;13(11):2498-504 PMID: 14597658
  12. Power and predictive accuracy of polygenic risk scores.
    PLoS Genet. 2013 Mar;9(3):e1003348 PMID: 23555274
  13. Network analysis of GWAS data.
    Curr Opin Genet Dev. 2013 Dec;23(6):602-10 PMID: 24287332
  14. Prospects for the genetics of human longevity.
    Hum Genet. 1993 Jul;91(6):519-26 PMID: 8340104
  15. Lifestyle factors of people with exceptional longevity.
    J Am Geriatr Soc. 2011 Aug;59(8):1509-12 PMID: 21812767
  16. Substantial health and economic returns from delayed aging may warrant a new focus for medical research.
    Health Aff (Millwood). 2013 Oct;32(10):1698-705 PMID: 24101058
  17. A bad rap: Rap1 signaling and oncogenesis.
    Cancer Cell. 2003 Jul;4(1):3-4 PMID: 12892706
  18. Association of FOXO3A variation with human longevity confirmed in German centenarians.
    Proc Natl Acad Sci U S A. 2009 Feb 24;106(8):2700-5 PMID: 19196970
  19. Obesity, cigarette smoking, and telomere length in women.
    Lancet. 2005 Aug 20-26;366(9486):662-4 PMID: 16112303
  20. Calorie restriction in humans inhibits the PI3K/AKT pathway and induces a younger transcription profile.
    Aging Cell. 2013 Aug;12 (4):645-51 PMID: 23601134
  21. Cell resilience in species life spans: a link to inflammation?
    Aging Cell. 2010 Aug;9(4):519-26 PMID: 20415721
  22. FOXO3A genotype is strongly associated with human longevity.
    Proc Natl Acad Sci U S A. 2008 Sep 16;105(37):13987-92 PMID: 18765803
  23. Finding missing heritability in less significant Loci and allelic heterogeneity: genetic variation in human height.
    PLoS One. 2012;7(12):e51211 PMID: 23251454
  24. Cancer Prevention Study II. The American Cancer Society Prospective Study.
    Stat Bull Metrop Insur Co. 1992 Oct-Dec;73(4):21-9 PMID: 1475748
  25. Hundreds of variants clustered in genomic loci and biological pathways affect human height.
    Nature. 2010 Oct 14;467(7317):832-8 PMID: 20881960
  26. A new DAF-16 isoform regulates longevity.
    Nature. 2010 Jul 22;466(7305):498-502 PMID: 20613724
  27. Genome-wide linkage analysis for human longevity: Genetics of Healthy Aging Study.
    Aging Cell. 2013 Apr;12(2):184-93 PMID: 23286790
  28. Ageing as a risk factor for disease.
    Curr Biol. 2012 Sep 11;22(17):R741-52 PMID: 22975005
  29. Genetic signatures of exceptional longevity in humans.
    PLoS One. 2012;7(1):e29848 PMID: 22279548
  30. Understanding Ras: 'it ain't over 'til it's over'.
    Trends Cell Biol. 2000 Apr;10(4):147-54 PMID: 10740269
  31. Untangling genetic influences on smoking, body mass index and longevity: a multivariate study of 2464 Danish twins followed for 28 years.
    Hum Genet. 1996 Oct;98(4):467-75 PMID: 8792824
  32. Genetics of longevity in model organisms: debates and paradigm shifts.
    Annu Rev Physiol. 2013;75:621-44 PMID: 23190075
  33. Genome-wide association meta-analysis of human longevity identifies a novel locus conferring survival beyond 90 years of age.
    Hum Mol Genet. 2014 Aug 15;23(16):4420-32 PMID: 24688116
  34. Genomic instability--an evolving hallmark of cancer.
    Nat Rev Mol Cell Biol. 2010 Mar;11(3):220-8 PMID: 20177397
  35. Prediction of individual genetic risk of complex disease.
    Curr Opin Genet Dev. 2008 Jun;18(3):257-63 PMID: 18682292
  36. Emerging roles of PDGF-D signaling pathway in tumor development and progression.
    Biochim Biophys Acta. 2010 Aug;1806(1):122-30 PMID: 20434526
  37. Annotating cancer variants and anti-cancer therapeutics in reactome.
    Cancers (Basel). 2012 Nov 08;4(4):1180-211 PMID: 24213504
  38. Aging and DNA damage in humans: a meta‐analysis study.
    Aging (Albany NY). 2014 Jun;6(6):432-9 PMID: 25140379
  39. Discovery of functional gene variants associated with human longevity: opportunities and challenges.
    J Gerontol A Biol Sci Med Sci. 2012 Apr;67(4):376-83 PMID: 22156437
  40. PLINK: a tool set for whole-genome association and population-based linkage analyses.
    Am J Hum Genet. 2007 Sep;81(3):559-75 PMID: 17701901
  41. Projecting the effect of changes in smoking and obesity on future life expectancy in the United States.
    Demography. 2014 Feb;51(1):27-49 PMID: 24272710
  42. Genetics of longevity and aging.
    Annu Rev Med. 2005;56:193-212 PMID: 15660509
  43. Unique lipoprotein phenotype and genotype associated with exceptional longevity.
    JAMA. 2003 Oct 15;290(15):2030-40 PMID: 14559957
  44. Longevity genes in the nematode Caenorhabditis elegans also mediate increased resistance to stress and prevent disease.
    J Inherit Metab Dis. 2002 May;25(3):197-206 PMID: 12137228
  45. Genetic risk sum score comprised of common polygenic variation is associated with body mass index.
    Hum Genet. 2011 Feb;129(2):221-30 PMID: 21104096
  46. The aging process: major risk factor for disease and death.
    Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5360-3 PMID: 2052612
  47. Not all smokers die young: a model for hidden heterogeneity within the human population.
    PLoS One. 2014 Feb 10;9(2):e87403 PMID: 24520332
  48. Functionally significant insulin-like growth factor I receptor mutations in centenarians.
    Proc Natl Acad Sci U S A. 2008 Mar 4;105(9):3438-42 PMID: 18316725
Article Info
Journal
The journals of gerontology. Series A, Biological sciences and medical sciences
Abbr.
J Gerontol A Biol Sci Med Sci
ISSN
1758-535X
Published
2016-00-00
Epub
2015-00-09
Pages
703-12
Language
English
Region
United States
NLM ID
9502837
PMCID
PMC4888382
Subset
IM
Grants
NIA NIH HHS · P30 AG017265 · United States
NIA NIH HHS · T32 AG000037 · United States
NIA NIH HHS · U01 AG009740 · United States
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