Candidate gene resequencing to identify rare, pedigree-specific variants influencing healthy aging phenotypes in the long life family study

BMC Geriatrics

Volumn 16, Issue 1, 2016, Pages

  Druley, Todd E ^a   Wang, Lihua ^a   Lin, Shiow J ^a   Lee, Joseph H ^b,c,d   Zhang, Qunyuan ^a   Daw, E Warwick ^a   Abel, Haley J ^a   Chasnoff, Sara E ^a   Ramos, Enrique I ^a   Levinson, Benjamin T ^a   Thyagarajan, Bharat ^e   Newman, Anne B ^f   Christensen, Kaare ^g   Mayeux, Richard ^b   Province, Michael A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Vagelos College of Physicians and Surgeons   (United States)

^c New York Presbyterian Columbia University Medical Center   (United States)

^d Graduate School of Public Health ^*  (United States)

^e UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^f UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^g UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Aging; Family; Genetics; Genomics; Geriatrics; Pedigrees; Sequencing

Indexed keywords

AGED; FEMALE; GENETIC ASSOCIATION STUDY; GENETIC SCREENING; GENETIC VARIATION; GENETICS; HIGH THROUGHPUT SEQUENCING; HUMAN; LONGEVITY; MALE; PEDIGREE; PHENOTYPE;

AGED; FEMALE; GENETIC ASSOCIATION STUDIES; GENETIC TESTING; GENETIC VARIATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; LONGEVITY; MALE; PEDIGREE; PHENOTYPE;

EID: 84966267489     PISSN: None     EISSN: 14712318     Source Type: Journal    
DOI: 10.1186/s12877-016-0253-y     Document Type: Article

References (62)

1. Herskind AM, McGue M, Holm NV, Sorensen TI, Harvald B, Vaupel JW. The heritability of human longevity: a population-based study of 2872 Danish twin pairs born 1870-1900. Hum Genet. 1996;97:319-23.
2. Schachter F, Faure-Delanef L, Guenot F, Rouger H, Froguel P, Lesueur-Ginot L, Cohen D. Genetic associations with human longevity at the APOE and ACE loci. Nat Genet. 1994;6:29-32.
3. van Bockxmeer FM. ApoE and ACE genes: impact on human longevity. Nat Genet. 1994;6:4-5.
4. Christensen K, Johnson TE, Vaupel JW. The quest for genetic determinants of human longevity: challenges and insights. Nat Rev Genet. 2006;7:436-48.
5. Deelen J, Beekman M, Uh HW, Helmer Q, Kuningas M, Christiansen L, Kremer D, 500 van der Breggen R, Suchiman HE, Lakenberg N, et al. Genome-wide association study identifies a single major locus contributing to survival into old age; the APOE locus revisited. Aging Cell. 2011;10:686-98.
6. 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;88:3299-304.
7. Willcox BJ, Donlon TA, He Q, Chen R, Grove JS, Yano K, Masaki KH, Willcox DC, Rodriguez B, Curb JD. FOXO3A genotype is strongly associated with human longevity. Proc Natl Acad Sci USA. 2008;105:13987-92.
8. Pawlikowska L, Hu D, Huntsman S, Sung A, Chu C, Chen J, Joyner AH, Schork NJ, Hsueh WC, Reiner AP, et al. Association of common genetic variation in the insulin/IGF1 signaling pathway with human longevity. Aging Cell. 2009;8:460-72.
9. Sebastiani P, Solovieff N, Dewan AT, Walsh KM, Puca A, Hartley SW, Melista E, Andersen S, Dworkis DA, Wilk JB, et al. Genetic signatures of exceptional longevity in humans. PLoS One. 2012;7:e29848.
10. Sebastiani P, Sun FX, Andersen SL, Lee JH, Wojczynski MK, Sanders JL, Yashin A, Newman AB, Perls TT. Families Enriched for Exceptional Longevity also have Increased Health-Span: Findings from the Long Life Family Study. Front Public Health. 2013;1:38.
11. Newman AB, Glynn NW, Taylor CA, Sebastiani P, Perls TT, Mayeux R, Christensen K, Zmuda JM, Barral S, Lee JH, et al. Health and function of participants in the Long Life Family Study: A comparison with other cohorts. Aging (Albany NY). 2011;3:63-76.
12. Barral S, Cosentino S, Costa R, Andersen SL, Christensen K, Eckfeldt JH, Newman AB, Perls TT, Province MA, Hadley EC, et al. Exceptional memory performance in the Long Life Family Study. Neurobiol Aging. 2013;34:2445-8.
13. Sanders JL, Minster RL, Barmada MM, Matteini AM, Boudreau RM, Christensen K, Mayeux R, Borecki IB, Zhang Q, Perls T, et al. Heritability of and mortality prediction with a longevity phenotype: the healthy aging index. J Gerontol A Biol Sci Med Sci. 2014;69:479-85.
14. Sebastiani P, Hadley EC, Province M, Christensen K, Rossi W, Perls TT, Ash AS. A family longevity selection score: ranking sibships by their longevity, size, and availability for study. Am J Epidemiol. 2009;170:1555-62.
15. An P, Miljkovic I, Thyagarajan B, Kraja AT, Daw EW, Pankow JS, Selvin E, Kao WH, Maruthur NM, Nalls MA, et al. Genome-wide association study identifies common loci influencing circulating glycated hemoglobin (HbA) levels in non-diabetic subjects: The Long Life Family Study (LLFS). Metabolism. 2013;63:461-8.
16. Lee JH, Cheng R, Honig LS, Feitosa M, Kammerer CM, Kang MS, Schupf N, Lin SJ, Sanders JL, Bae H, et al. Genome wide association and linkage analyses identified three loci-4q25, 17q23.2, and 10q11.21-associated with variation in leukocyte telomere length: the Long Life Family Study. Front Genet. 2013;4:310.
17. Wu J, Province MA, Coon H, Hunt SC, Eckfeldt JH, Arnett DK, Heiss G, Lewis CE, Ellison RC, Rao DC, et al. An investigation of the effects of lipid-lowering medications: genome-wide linkage analysis of lipids in the HyperGEN study. BMC Genet. 2007;8:60.
18. Wu J, Kraja AT, Oberman A, Lewis CE, Ellison RC, Arnett DK, Heiss G, Lalouel JM, Turner ST, Hunt SC, Province MA, Rao DC. A summary of the effects of antihypertensive medications on measured blood pressure. Am J Hypertens. 2005;18:935-42.
19. Folstein MF, Folstein SE, McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189-98.
20. Ramos E, Levinson BT, Chasnoff S, Hughes A, Young AL, Thornton K, Li A, Vallania FL, Province M, Druley TE. Population-based rare variant detection via pooled exome or custom hybridization capture with or without individual indexing. BMC Genomics. 2012;13:683.
21. Pinheiro JC, Bates DB. Mixed-effects models in S and S-Plus. New York, NY: Springer; 2000.
22. Abrahantes JC, Burzykowski T. A version of the EM algorithm for proportional hazard model with random effects. Biom J. 2005;47:847-62.
23. Li B, Leal SM. Methods for detecting associations with rare variants for common diseases: application to analysis of sequence data. Am J Hum Genet. 2008;83:311-21.
24. Madsen BE, Browning SR. A groupwise association test for rare mutations using a weighted sum statistic. PLoS Genet. 2009;5:e1000384.
25. Zhang Q, Irvin MR, Arnett DK, Province MA, Borecki I. A data-driven method for identifying rare variants with heterogeneous trait effects. Genet Epidemiol. 2011;35:679-85.
26. Chen H, Meigs JB, Dupuis J. Sequence kernel association test for quantitative traits in family samples. Genet Epidemiol. 2013;37:196-204.
27. Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010;38:e164.
28. Lee S, Abecasis GR, Boehnke M, Lin X. Rare-variant association analysis:study designs and statistical tests. Am J Hum Genet. 2014;95:5-23.
29. Dato S, Crocco P, D'Aquila P, de Rango F, Bellizzi D, Rose G, Passarino G. et al. Exploring the role of genetic variability and lifestyle in oxidative stress response for healthy aging and longevity. Int J Mol Sci. 2013;14:16443-72.
30. Atzmon G, Rincon M, Schechter CB, Shuldiner AR, Lipton RB, Bergman A, Barzilai N. Lipoprotein genotype and conserved pathway for exceptional longevity in humans. PLoS Biol. 2006;4(4):e113.
31. Trahan G. Mitochondrial-nuclear epistasis: implications for human aging and longevity. Ageing Res Rev. 2011;10:238-52.
32. Geesaman BJ, Benson E, Brewster SJ, Kunkel LM, Blanche H, Thomas G, et al. Haplotype-based identification of a microsomal transfer protein marker associated with the human lifespan. Proc Natl Acad Sci USA. 2003;100:14115-20.
33. Gondo Y, Hirose N, Arai Y, Yamamura K, Shimizu K, Takayama M, Ebihara Y, Nakazawa S, Inagaki H, Masui Y, et al. Contribution of an affect-associated gene to human longevity: prevalence of the long-allele genotype of the serotonin transporter-linked gene in Japanese centenarians. Mech Ageing Dev. 2005;126:1178-84.
34. Atzmon G, Barzilai N, Surks MI, Gabriely I. Genetic predisposition to elevated serum thyrotropin is associated with exceptional longevity. J Clin Endocrinol Metab. 2009;94:4768-75.
35. Budovsky A, Craig T, Wang J, Tacutu R, Csordas A, Lourenco J, Fraifeld VE, de Magalhaes JP. LongevityMap: a database of human genetic variants associated with longevity. Trends Genet. 2013;29:559-60.
36. Li Y, Wang WJ, Cao H, Lu J, Wu C, et al. Genetic association of FOXO1A and FOXO3A with longevity trait in Han Chinese populations. Hum Mol Genet. 2009;18:4897-904.
37. Broer L, Buchman AS, Deelen J, Evans DS, Faul JD, Lunetta KL, Sebastiani P, Smith JA, Smith AV, Tanaka T, Yu L, Arnold AM, Aspelund T, Benjamin EJ, De Jager PL, Eirkisdottir G, Evans DA, Garcia ME, Hofman A, Kaplan RC, Kardia SL, Kiel DP, Oostra BA, Orwoll ES, Parimi N, Psaty BM, Rivadeneira F, Rotter JI, Seshadri S, Singleton A, Tiemeier H, Uitterlinden AG, Zhao W, Bandinelli S, Bennett DA, Ferrucci L, Gudnason V, Harris TB, Karasik D, Launer LJ, Perls TT, Slagboom PE, Tranah GJ, Weir DR, Newman AB, van Duijn CM, Murabito JM. GWAS of Longevity in CHARGE Consortium Confirms APOE and FOXO3 Candidacy. J Gerontol A Biol Sci Med Sci. 2015;70:110-8.
38. Soerensen M, Dato S, Christensen K, McGue M, Stevnsner T, Bohr VA, 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;9:1010-7.
39. Zeng Y, Cheng L, Chen H, Cao H, Hauser ER, Liu Y, Xiao Z, Tan Q, Tian XL, Vaupel JW. Effects of FOXO genotypes on longevity: a biodemographic analysis. J Gerontol A Biol Sci Med Sci. 2010;65:1285-99.
40. Haisa M. The type 1 insulin-like growth factor receptor signalling system and targeted tyrosine kinase inhibition in cancer. J Int Med Res. 2013;41:253-64.
41. Rader DJ, deGoma EM. Future of cholesteryl ester transfer protein inhibitors. Annu Rev Med. 2014;65:385-403.
42. Reilly D, Hao K, Jensen MK, Girman CJ, Rimm EB. Use of systems biology approaches to analysis of genome-wide association studies of myocardial infarction and blood cholesterol in the nurses' health study and health professionals' follow-up study. PLoS One. 2013;8:e85369.
43. Ridker PM, Pare G, Parker AN, Zee RY, Miletich JP, Chasman DI. Polymorphism in the CETP gene region, HDL cholesterol, and risk of future myocardial infarction: Genomewide analysis among 18 245 initially healthy women from the Women's Genome Health Study. Circ Cardiovasc Genet. 2009;2:26-33.
44. van Dijk KW, Rensen PC, Voshol PJ, Havekes LM. The role and mode of action of apolipoproteins CIII and AV: synergistic actors in triglyceride metabolism? Curr Opin Lipidol. 2004;15:239-46.
45. Smith CE, Tucker KL, Scott TM, Van Rompay M, Mattei J, Lai CQ, Parnell LD, Junyent M, Lee YC, Garcia-Bailo B, et al. Apolipoprotein C3 polymorphisms, cognitive function and diabetes in Caribbean origin Hispanics. PLoS One. 2009;4:e5465.
46. Ronald J, Rajagopalan R, Ranchalis JE, Marshall JK, Hatsukami TS, Heagerty PJ, Jarvik GP. Analysis of recently identified dyslipidemia alleles reveals two loci that contribute to risk for carotid artery disease. Lipids Health Dis. 2009;8:52.
47. Talmud PJ, Drenos F, Shah S, Shah T, Palmen J, Verzilli C, Gaunt TR, Pallas J, Lovering R, Li K, et al. Gene-centric association signals for lipids and apolipoproteins identified via the HumanCVD BeadChip. Am J Hum Genet. 2009;85:628-42.
48. Maruszak A, Peplonska B, Safranow K, Chodakowska-Zebrowska M, Barcikowska M, Zekanowski C. TOMM40 rs10524523 polymorphism's role in late-onset Alzheimer's disease and in longevity. J Alzheimers Dis. 2012;28:309-22.
49. Kwok JB, Loy CT, Hamilton G, Lau E, Hallupp M, Williams J, Owen MJ, Broe GA, Tang N, Lam L, Powell JF, Lovestone S, Schofield PR. Glycogen synthase kinase-3 beta and tau genes interact in Alzheimer's disease. Ann Neurol. 2008;64:446-54.
50. Forlenza OV, Torres CA, Talib LL, de Paula VJ, Joaquim HP, Diniz BS, Gattaz WF. Increased platelet GSK3B activity in patients with mild cognitive impairment and Alzheimer's disease. J Psychiatr Res. 2011;45:220-4.
51. Dill MT, Rothweiler S, Djonov V, Hlushchuk R, Tornillo L, Terracciano L, Meili-Butz S, Radtke F, Heim MH, Semela D. Disruption of Notch1 induces vascular remodeling, intussusceptive angiogenesis, and angiosarcomas in livers of mice. Gastroenterology. 2012;142:967-77.
52. Zhao W, Guan J, Horswell R, Li W, Wang Y, Wu X, Hu G. HDL Cholesterol and Cancer Risk Among Patients With Type 2 Diabetes. Diabetes Care. 2014;37:3196-203.
53. Kulminski AM, Arbeev KG, Culminskaya I, Arbeeva L, Ukraintseva SV, Stallard E, Christensen K, Schupf N, Province MA, Yashin AI. Age, gender, and cancer but not neurodegenerative and cardiovascular diseases strongly modulate systemic effect of the Apolipoprotein E4 allele on lifespan. PLoS Genet. 2014;10:e1004141.
54. Kirkwood TB, Melev S. On the programmed/non-programmed nature of ageing within the life history. Curr Biol. 2011;21:R701-7.
55. Shi G, Simino J, Rao DC. Enriching rare variants using family-specific linkage information. BMC Proc. 2011;Suppl 9:S82.
56. Bowden DW, An SS, Palmer ND, Brown WM, Norris JM, Haffner SM, Hawkins GA, Guo X, Rotter JI, Chen YD, et al. Molecular basis of a linkage peak: exome sequencing and family-based analysis identify a rare genetic variant in the ADIPOQ gene in the IRAS Family Study. Hum Mol Genet. 2010;19:4112-20.
57. Jope RS, Johnson GV. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci. 2004;29:95-102.
58. Schaffer BA, Bertram L, Miller BL, Mullin K, Weintraub S, Johnson N, Bigio EH, Mesulam M, Wiedau-Pazos M, Jackson GR, et al. Association of GSK3B with Alzheimer disease and frontotemporal dementia. Arch Neurol. 2008;65:1368-74.
59. Atzmon G, Rincon M, Rabizadeh P, Barzilai N. Biological evidence for inheritance of exceptional longevity. Mech Ageing Dev. 2005;26:341-5.
60. Barzilai N, Atzmon G, Schechter C, Schaefer EJ, Cupples AL, Lipton R, Cheng S, Shuldiner AR. Unique lipoprotein phenotype and genotype associated with exceptional longevity. JAMA. 2003;290:2030-40.
61. Chen JJ, Li YM, Zou WY, Fu JL. Relationships between CETP genetic polymorphisms and Alzheimer's disease risk: a meta-analysis. DNA Cell Biol. 2014;33:807-15.
62. Ukraintseva S, Yashin A, Arbeev K, Kulminski A, Akushevich I, Wu D, Joshi G, Land, KC, Stallard,E (2015) Puzzling role of genetic risk factors in human longevity:"risk alleles" as pro-longevity variants. Biogerontology. [Epub ahead of print]