Genetic analysis of TOR complex gene variation with human longevity: A nested case-control study of American men of Japanese ancestry

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 70, Issue 2, 2015, Pages 133-142

  Morris, Brian J ^a,b,c   Donlon, Timothy A ^a   He, Qimei ^a   Grove, John S ^a,b   Masaki, Kamal H ^a,b   Elliott, Ayako ^a   Craig Willcox, D ^a,b,d   Allsopp, Richard ^b   Willcox, Bradley J ^a,b  

^a KUAKINI MEDICAL CENTER   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c UNIVERSITY OF SYDNEY   (Australia)

^d OKINAWA INTERNATIONAL UNIVERSITY   (Japan)

Author keywords

Genetic association analysis; Health span; Life span; Longevity; Target of rapamycin

Indexed keywords

CARRIER PROTEIN; MTOR PROTEIN, HUMAN; RICTOR PROTEIN, HUMAN; RPS6KA1 PROTEIN, HUMAN; RPTOR PROTEIN, HUMAN; S6 KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TARGET OF RAPAMYCIN KINASE;

AGED; ASIAN AMERICAN; CASE CONTROL STUDY; ETHNOLOGY; GENE FREQUENCY; GENETICS; GENOTYPE; HUMAN; JAPAN; LONGEVITY; LONGITUDINAL STUDY; MALE; SINGLE NUCLEOTIDE POLYMORPHISM; UNITED STATES; VERY ELDERLY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AGED; AGED, 80 AND OVER; ASIAN AMERICANS; CARRIER PROTEINS; CASE-CONTROL STUDIES; GENE FREQUENCY; GENOTYPE; HAWAII; HUMANS; JAPAN; LONGEVITY; LONGITUDINAL STUDIES; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; TOR SERINE-THREONINE KINASES;

EID: 84922463485     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glu021     Document Type: Article

References (50)

1. Sebastiani P, Perls TT. The genetics of extreme longevity: lessons from the New England centenarian study. Front Genet. 2012; 3: 277. doi: 10.3389/fgene
2. Beekman M, Blanche H, Perola M, et al.; GEHA consortium. Genome-wide linkage analysis for human longevity: Genetics of Healthy Aging Study. Aging Cell. 2013; 12: 184-193. doi: 10.1111/acel.12039
3. Murabito JM, Yuan R, Lunetta KL. The search for longevity and healthy aging genes: insights from epidemiological studies and samples of long-lived individuals. J Gerontol A Biol Sci Med Sci. 2012; 67: 470-479. doi: 10.1093/gerona/gls089
4. Mair W, Dillin A. Aging and survival: the genetics of life span extension by dietary restriction. Annu Rev Biochem. 2008; 77: 727-754. doi: 10.1146/annurev.biochem.77.061206.171059
5. Willcox BJ, Donlon TA, He Q, et al. FOXO3A genotype is strongly associated with human longevity. Proc Natl Acad Sci U S A. 2008; 105: 13987-13992. doi: 10.1073/pnas.0801030105
6. Gems D, Partridge L. Genetics of longevity in model organisms: debates and paradigm shifts. Annu Rev Physiol. 2013; 75: 621-644. doi: 10.1146/annurev-physiol-030212-183712
7. Curran SP, Ruvkun G. Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet. 2007; 3: e56.
8. Pan Y, Nishida Y, Wang M, Verdin E. Metabolic regulation, mitochondria and the life-prolonging effect of rapamycin: a mini-review. Gerontology. 2012; 58: 524-530. doi: 10.1159/000342204
9. Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, Benzer S. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol. 2004; 14: 885-890.
10. Kaeberlein M, Powers RW 3rd, Steffen KK, et al. Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science. 2005; 310: 1193-1196.
11. Fadini GP, Ceolotto G, Pagnin E, de Kreutzenberg S, Avogaro A. At the crossroads of longevity and metabolism: the metabolic syndrome and lifespan determinant pathways. Aging Cell. 2011; 10: 10-17. doi: 10.1111/j.1474-9726.2010.00642.x
12. Wu JJ, Liu J, Chen EB, et al. Increased mammalian lifespan and a segmental and tissue-specific slowing of aging after genetic reduction of mTOR expression. Cell Rep. 2013; 4: 913-920. doi: 10.1016/j. celrep.2013.07.030
13. Yang Z, Ming XF. mTOR signalling: the molecular interface connecting metabolic stress, aging and cardiovascular diseases. Obes Rev. 2012; 13 (Suppl 2): 58-68. doi: 10.1111/j.1467-789X.2012.01038.x
14. Dibble CC, Manning BD. Signal integration by mTORC1 coordinates nutrient input with biosynthetic output. Nat Cell Biol. 2013; 15: 555-564. doi: 10.1038/ncb2763
15. Mendelsohn AR, Larrick JW. Dissecting mammalian target of rapamycin to promote longevity. Rejuvenation Res. 2012; 15: 334-337. doi: 10.1089/rej.2012.1347
16. Yang H, Rudge DG, Koos JD, Vaidialingam B, Yang HJ, Pavletich NP. mTOR kinase structure, mechanism and regulation. Nature. 2013; 497: 217-223. doi: 10.1038/nature12122
17. Harrison DE, Strong R, Sharp ZD, et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature. 2009; 460: 392-395. doi: 10.1038/nature08221
18. Zhang Y, Bokov A, Gelfond J, et al. Rapamycin extends life and health in C57BL/6 mice. J Gerontol A Biol Sci Med Sci. 2014; 69: 119-130. doi: 10.1093/gerona/glt056
19. Hara K, Maruki Y, Long X, et al. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell. 2002; 110: 177-189.
20. Sarbassov DD, Ali SM, Kim DH, et al. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptorindependent pathway that regulates the cytoskeleton. Curr Biol. 2004; 14: 1296-1302.
21. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell. 2012; 149: 274-293. doi: 10.1016/j.cell.2012.03.017
22. Yip CK, Murata K, Walz T, Sabatini DM, Kang SA. Structure of the human mTOR complex I and its implications for rapamycin inhibition. Mol Cell. 2010; 38: 768-774. doi: 10.1016/j. molcel.2010.05.017
23. Magnuson B, Ekim B, Fingar DC. Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem J. 2012; 441: 1-21. doi: 10.1042/BJ20110892
24. Um SH, D'Alessio D, Thomas G. Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab. 2006; 3: 393-402.
25. Selman C, Tullet JM, Wieser D, et al. Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science. 2009; 326: 140-144. doi: 10.1126/science.1177221
26. Worth RM, Kagan A. Ascertainment of men of Japanese ancestry in Hawaii through World War II Selective Service registration. J Chronic Dis. 1970; 23: 389-397.
27. Kagan A, ed. The Honolulu Heart Program: An Epidemiological Study of Coronary Heart Disease and Stroke. Amsterdam, The Netherlands: Harwood Academic Publishers; 1996.
28. Arias E. United States Life Tables, 2003. Hyattsville, MD: National Center for Health Statistics; 2006: 54 (14).
29. Nordyke EC, Lee R, Gardner RW. A profile of Hawaii's elderly population. Papers East West Popul Inst. 1984; 91: 13-14.
30. White L, Petrovitch H, Ross GW, et al. Prevalence of dementia in older Japanese-American men in Hawaii: The Honolulu-Asia Aging Study. JAMA. 1996; 276: 955-960.
31. Shen R, Fan JB, Campbell D, et al. High-throughput SNP genotyping on universal bead arrays. Mutat Res. 2005; 573: 70-82.
32. Agresti A, Caffo B: Simple and effective confidence intervals for proportions and dfferences in proportions from adding two successes and two failures. Am Statist. 2000; 54: 280-288.
33. Statistical Analysis for the Social Sciences. SAS/STAT User's Guide, Version 6. Cary, NC: SAS Institute, 1990.
34. Michael Anson R, Willcox B, Austad S, Perls T. Within- and betweenspecies study of extreme longevity-comments, commonalities, and goals. J Gerontol A Biol Sci Med Sci. 2012; 67: 347-350. doi: 10.1093/gerona/gls010
35. Soerensen M. Genetic variation and human longevity. Dan Med J. 2012; 59: B4454.
36. Tazearslan C, Cho M, Suh Y. Discovery of functional gene variants associated with human longevity: opportunities and challenges. J Gerontol A Biol Sci Med Sci. 2012; 67: 376-383. doi: 10.1093/gerona/glr200
37. Tacutu R, Craig T, Budovsky A, et al. Human Ageing Genomic Resources: integrated databases and tools for the biology and genetics of ageing. Nucleic Acids Res. 2013; 41: D1027-D1033. doi: 10.1093/nar/gks1155
38. Passtoors WM, Beekman M, Deelen J, et al. Gene expression analysis of mTOR pathway: association with human longevity. Aging Cell. 2013; 12: 24-31. doi: 10.1111/acel.12015
39. Deelen J, Uh HW, Monajemi R, et al. Gene set analysis of GWAS data for human longevity highlights the relevance of the insulin/IGF-1 signaling and telomere maintenance pathways. Age (Dordr). 2013; 35: 235-249. doi: 10.1007/s11357-011-9340-3
40. Arias E. United States Life Tables, National Vital Statistics Reports. Hyattsville, MD: National Center for Health Statistics; 2008: 61 (3). http://www.cdc.gov/nchs/data/nvsr/nvsr61/nvsr61-03.pdf, 2012.
41. Deelen J, Beekman M, Uh HW, 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: 686-698.
42. Banasik K, Ribel-Madsen R, Gjesing AP, et al. The FOXO3A rs2802292 G-allele associates with improved peripheral and hepatic insulin sensitivity and increased skeletal muscle-FOXO3A mRNA expression in twins. J Clin Endocrinol Metab. 2011; 96: E119-E124. doi: 10.1210/jc.2010-0881
43. Evert J, Lawler E, Bogan H, Perls T. Morbidity profiles of centenarians: survivors, delayers, and escapers. J Gerontol A Biol Sci Med Sci. 2003; 58: 232-237.
44. Bernstein AM, Willcox BJ, Tamaki H, et al. First autopsy study of an Okinawan centenarian: absence of many age-related diseases. J Gerontol A Biol Sci Med Sci. 2004; 59: 1195-1199.
45. Willcox DC, Willcox BJ, Shimajiri S, Kurechi S, Suzuki M. Aging gracefully: a retrospective analysis of functional status in Okinawan centenarians. Am J Geriatr Psychiatry. 2007; 15: 252-256.
46. Johnson SC, Rabinovitch PS, Kaeberlein M. mTOR is a key modulator of ageing and age-related disease. Nature. 2013; 493: 338-345. doi: 10.1038/nature11861
47. Sakuma K, Yamaguchi A. Molecular mechanisms in aging and current strategies to counteract sarcopenia. Curr Aging Sci. 2010; 3: 90-101.
48. Flynn JM, O'Leary MN, Zambataro CA, et al. Late-life rapamycin treatment reverses age-related heart dysfunction. Aging Cell. 2013; 12: 851-862. doi: 10.1111/acel.12109
49. Wu P, Jiang C, Shen Q, Hu Y. Systematic gene expression profile of hypothalamus in calorie-restricted mice implicates the involvement of mTOR signaling in neuroprotective activity. Mech Ageing Dev. 2009; 130: 602-610. doi: 10.1016/j.mad.2009.07.005
50. Ganna A, Rivadeneira F, Hofman A, et al. Genetic determinants of mortality. Can findings from genome-wide association studies explain variation in human mortality? Hum Genet. 2013; 132: 553-561. doi: 10.1007/s00439-013-1267-6