Is telomere length a biomarker of aging? A review

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 66 A, Issue 2, 2011, Pages 202-213

  Mather, Karen Anne ^a,b   Jorm, Anthony Francis ^c   Parslow, Ruth Adeline ^d   Christensen, Helen ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d LA TROBE UNIVERSITY   (Australia)

Author keywords

Biomarker of aging; Telomere length

Indexed keywords

BIOLOGICAL MARKER; TELOMERASE;

AGING; ANIMAL; CELL AGING; COGNITION; GENETICS; HUMAN; LONGITUDINAL STUDY; MALE; METABOLISM; MOUSE; REVIEW; TELOMERE;

AGING; ANIMALS; BIOLOGICAL MARKERS; CELL AGING; COGNITION; HUMANS; LONGITUDINAL STUDIES; MALE; MICE; TELOMERASE; TELOMERE;

EID: 79951780180     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glq180     Document Type: Review

References (110)

1. Christensen H, Mackinnon A, Jorm AF, Henderson AS, Scott LR, Korten AE. Age differences and interindividual variation in cognition in community-dwelling elderly. Psychol Aging. 1994;9:381-390. (Pubitemid 24301671)
2. Christensen H, Mackinnon AJ, Korten AE, Jorm AF, Henderson AS, Jacomb P. Dispersion in cognitive ability as a function of age: a longitudinal study of an elderly community sample. Aging Neuropsychol Cognition. 1999;6:214-228. (Pubitemid 30108397)
3. Harris JR, Pedersen NL, McClearn GE, Plomin R, Nesselroade JR. Age differences in genetic and environmental influences for health from the Swedish Adoption/Twin Study of Aging. J Gerontol. 1992;47:P213-P220.
4. Hultsch DF, MacDonald SW, Dixon RA. Variability in reaction time performance of younger and older adults. J Gerontol Psychol Sci. 2002;57:P101-P115. (Pubitemid 34203264)
5. Karasik D, Hannan MT, Cupples LA, Felson DT, Kiel DP. Genetic contribution to biological aging: the Framingham Study. J Gerontol A Biol Sci Med Sci. 2004;59:218-226. (Pubitemid 38375334)
6. Morse CK. Does variability increase with age? An archival study of cognitive measures. Psychol Aging. 1993;8:156-164.
7. Butler RN, Sprott R, Warner H, et al. Biomarkers of aging: from primitive organisms to humans. J Gerontol A Biol Sci Med Sci. 2004;59:B560-B567.
8. Karasik D, Demissie S, Cupples LA, Kiel DP. Disentangling the genetic determinants of human aging: biological age as an alternative to the use of survival measures. J Gerontol A Biol Sci Med Sci. 2005;60:574-587. (Pubitemid 40847918)
9. Crimmins E, Vasunilashorn S, Kim JK, Alley D. Biomarkers related to aging in human populations. In: G Makowski (ed). Advances in Clinical Chemistry; Burlington, VA: Academic Press; 2008:161-216.
10. Simm A, Nass N, Bartling B, Hofmann B, Silber RE, Navarrete Santos A. Potential biomarkers of ageing. Biol Chem. 2008;389:257-265. (Pubitemid 351329032)
11. Johnson TE. Recent results: biomarkers of aging. Exp Gerontol. 2006;41:1243-1246. (Pubitemid 44848393)
12. Warner HR. Current status of efforts to measure and modulate the biological rate of aging. J Gerontol A Biol Sci Med Sci. 2004;59:692-696. (Pubitemid 39063241)
13. Bekaert S, De Meyer T, Van Oostveldt P. Telomere attrition as ageing biomarker. Anticancer Res. 2005;25:3011-3021.
14. Guralnik JM. Successful aging: is it in our future? Arch Intern Med. 2008;168:131-132. (Pubitemid 351185877)
15. Koppelstaetter C, Kern G, Mayer G. Biomarkers of aging with prognostic and predictive value in non-oncological diseases. Curr Med Chem. 2009;16:3469-3475.
16. von Zglinicki T, Martin-Ruiz CM. Telomeres as biomarkers for ageing and age-related diseases. Curr Mol Med. 2005;5:197-203. (Pubitemid 40601647)
17. von Zglinicki T, Serra V, Lorenz M, et al. Short telomeres in patients with vascular dementia: an indicator of low antioxidative capacity and a possible risk factor? Lab Invest. 2000;80:1739-1747.
18. Cawthon RM, Smith KR, O'Brien E, Sivatchenko A, Kerber RA. Association between telomere length in blood and mortality in people aged 60 years or older. Lancet. 2003;361:393-395. (Pubitemid 36164975)
19. Martin-Ruiz CM, Gussekloo J, van Heemst D, von Zglinicki T, Westendorp RG. Telomere length in white blood cells is not associated with morbidity or mortality in the oldest old: a population-based study. Aging Cell. 2005;4:287-290.
20. Bischoff C, Petersen HC, Graakjaer J, et al. No association between telomere length and survival among the elderly and oldest old. Epidemiology. 2006;17:190-194.
21. Harris SE, Deary IJ, Maclntyre A, et al. The association between telomere length, physical health, cognitive ageing, and mortality in non-demented older people. Neurosci Lett. 2006;406:260-264. (Pubitemid 44311375)
22. Fitzpatrick AL, Kronmal RA, Gardner JP, et al. Leukocyte telomere length and cardiovascular disease in the cardiovascular health study. Am J Epidemiol. 2007;165:14-21. (Pubitemid 46026204)
23. Bakaysa SL, Mucci LA, Slagboom PE, et al. Telomere length predicts survival independent of genetic influences. Aging Cell. 2007;6:769-774. (Pubitemid 350131045)
24. Kimura M, Hjelmborg JV, Gardner JP, et al. Telomere length and mortality: a study of leukocytes in elderly Danish twins. Am J Epidemiol. 2008;167:799-806. (Pubitemid 351451747)
25. Epel ES, Merkin SS, Cawthon R, et al. The rate of leukocyte telomere shortening predicts mortality from cardiovascular disease in elderly men. Aging (Albany NY). 2009;1:81-88.
26. Njajou OT, Hsueh W-C, Blackburn EH, et al. Association between telomere length, specific causes of death, and years of healthy life in health, aging, and body composition, a population-based cohort study. J Gerontol A Biol Sci Med Sci. 2009;64A:860-864.
27. Ehrlenbach S, Willeit P, Kiechl S, et al. Influences on the reduction of relative telomere length over 10 years in the population-based Bruneck Study: introduction of a well-controlled high-throughput assay. Int J Epidemiol. 2009;38:1725-1734.
28. Mather KA, Jorm AF, Milburn PJ, Tan X, Easteal S, Christensen H. No associations between telomere length and age-sensitive indicators of physical function in mid and later life. J Gerontol A Biol Sci Med Sci. 2010;65A:792-799.
29. Bekaert S, Van Pottelbergh I, De Meyer T, et al. Telomere length versus hormonal and bone mineral status in healthy elderly men. Mech Ageing Dev. 2005;126:1115-1122. (Pubitemid 41253863)
30. Bekaert S, De Meyer T, Rietzschel ER, et al. Telomere length and cardiovascular risk factors in a middle-aged population free of overt cardiovascular disease. Aging Cell. 2007;6:639-647. (Pubitemid 47400046)
31. Brouilette SW, Moore JS, McMahon AD, et al. Telomere length, risk of coronary heart disease, and statin treatment in the West of Scotland Primary Prevention Study: a nested case-control study. Lancet. 2007;369:107-114. (Pubitemid 46073129)
32. Benetos A, Okuda K, Lajemi M, et al. Telomere length as an indicator of biological aging-the gender effect and relation with pulse pressure and pulse wave velocity. Hypertension. 2001;37:381-385. (Pubitemid 32198997)
33. Valdes AM, Deary IJ, Gardner J, et al. Leukocyte telomere length is associated with cognitive performance in healthy women. Neurobiol Aging. 2010;31:986-992.
34. Yaffe K, Lindquist K, Kluse M, et al.; for the Health ABCS. Telomere length and cognitive function in community-dwelling elders: findings from the Health ABC Study. Neurobiol Aging. 2009. In press.
35. Canela A, Vera E, Klatt P, Blasco MA. High-throughput telomere length quantification by FISH and its application to human population studies. Proc Natl Acad Sci U S A. 2007;104:5300-5305. (Pubitemid 47175675)
36. Aviv A, Valdes AM, Spector TD. Human telomere biology: pitfalls of moving from the laboratory to epidemiology. Int J Epidemiol. 2006;35:1424-1429. (Pubitemid 46178916)
37. Halaschek-Wiener J, Vulto I, Fornika D, et al. Reduced telomere length variation in healthy oldest old. Mech Ageing Dev. 2008;129:638-641.
38. Terry DF, Nolan VG, Andersen SL, Perls TT, Cawthon R. Association of longer telomeres with better health in centenarians. J Gerontol A Biol Sci Med Sci. 2008;63:809-812.
39. Aviv A, Chen W, Gardner JP, et al. Leukocyte telomere dynamics: longitudinal findings among young adults in the Bogalusa Heart Study. Am J Epidemiol. 2009;169:323-329.
40. Olovnikov AM. Telomeres, telomerase, and aging: origin of the theory. Exp Gerontol. 1996;31:443-448. (Pubitemid 126745166)
41. Baird DM, Rowson J, Wynford-Thomas D, Kipling D. Extensive allelic variation and ultrashort telomeres in senescent human cells. Nat Genet. 2003;33:203-207. (Pubitemid 36177075)
42. Bendix L, Horn PB, Jensen UB, Rubelj I, Kolvraa S. The load of short telomeres, estimated by a new method, Universal STELA, correlates with number of senescent cells. Aging Cell. 2010;9:383-397.
43. Lansdorp PM. Major cutbacks at chromosome ends. Trends Biochem Sci. 2005;30:388-395. (Pubitemid 40942034)
44. Petersen S, Saretzki G, von Zglinicki T. Preferential accumulation of single-stranded regions in telomeres of human fibroblasts. Exp Cell Res. 1998;239:152-160. (Pubitemid 28368486)
45. Hemann MT, Strong MA, Hao LY, Greider CW. The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell. 2001;107:67-77. (Pubitemid 32972038)
46. Blackburn EH. Switching and signaling at the telomere. Cell. 2001;106:661-673. (Pubitemid 32900658)
47. Campisi J, d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol. 2007;8:729-740. (Pubitemid 47312822)
48. Deng Y, Chang S. Role of telomeres and telomerase in genomic instability, senescence and cancer. Lab Invest. 2007;87:1071-1076. (Pubitemid 47609025)
49. Shay JW, Wright WE. Hallmarks of telomeres in ageing research. J Pathol. 2007;211:114-123. (Pubitemid 46195510)
50. Abdallah P, Luciano P, Runge KW, et al. A two-step model for senescence triggered by a single critically short telomere. Nat Cell Biol. 2009;11:988-993.
51. Zou Y, Sfeir A, Gryaznov SM, Shay JW, Wright WE. Does a sentinel or a subset of short telomeres determine replicative senescence? Mol Biol Cell. 2004;15:3709-3718. (Pubitemid 38989708)
52. Kipling D. Telomeres, replicative senescence and human ageing. Maturitas. 2001;38:25-37.
53. Rodier F, Kim SH, Nijjar T, Yaswen P, Campisi J. Cancer and aging: the importance of telomeres in genome maintenance. Int J Biochem Cell Biol. 2005;37:977-990. (Pubitemid 40311740)
54. Garcia CK, Wright WE, Shay JW. Human diseases of telomerase dysfunction: insights into tissue aging. Nucleic Acids Res. 2007;35:7406-7416.
55. Anstey KJ, Lord SR, Smith GA. Measuring human functional age: a review of empirical findings. Exp Aging Res. 1996;22:245-266. (Pubitemid 26275444)
56. Nakamura E, Miyao K. Further evaluation of the basic nature of the human biological aging process based on a factor analysis of age-related physiological variables. J Gerontol A Biol Sci Med Sci. 2003;58:196-204. (Pubitemid 36307589)
57. Chyou PH, White LR, Yano K, et al. Pulmonary function measures as predictors and correlates of cognitive functioning in later life. Am J Epidemiol. 1996;143:750-756. (Pubitemid 26119818)
58. Beaty TH, Cohen BH, Newill CA, Menkes HA, Diamond EL, Chen CJ. Impaired pulmonary function as a risk factor for mortality. Am J Epidemiol. 1982;116:102-113. (Pubitemid 12087727)
59. Lee DC, Im JA, Kim JH, Lee HR, Shim JY. Effect of long-term hormone therapy on telomere length in postmenopausal women. Yonsei Med J. 2005;46:471-479.
60. Wechsler D. Wechsler Adult Intelligence Scale-Third Edition (WAIS-III); San Antonio, TX: The Psychological Corporation; 1997.
61. 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;12:189-198.
62. Teng EL, Chui HC. The Modified Mini-Mental State (3MS) examination. J Clin Psychiatry. 1987;48:314-318. (Pubitemid 17138128)
63. Burns A, Brayne C, Folstein M. Key Papers in Geriatric Psychiatry: mini-mental state: a practical method for grading the cognitive status of patients for the clinician. M.Folstein, S. Folstein and P. McHugh, Journal of Psychiatric Research, 1975, 12, 189-198.
64. Int J Geriatr Psychiatr. 1998;13:285-294.
65. Sprott RL. Biomarkers of aging and disease: introduction and definitions. Exp Gerontol. 2010;45:2-4.
66. Fuster JJ, Andres V. Telomere biology and cardiovascular disease. Circ Res. 2006;99:1167-1180. (Pubitemid 44808653)
67. Friedrich U, Griese E, Schwab M, Fritz P, Thon K, Klotz U. Telomere length in different tissues of elderly patients. Mech Ageing Dev. 2000;119:89-99.
68. Thomas P, O'Callaghan N, Fenech M. Telomere length in white blood cells, buccal cells and brain tissue and its variation with ageing and Alzheimer's disease. Mech Ageing Dev. 2008;129:183-190.
69. Forsyth NR, Wright WE, Shay JW. Telomerase and differentiation in multicellular organisms: turn it off, turn it on, and turn it off again. Differentiation. 2002;69:188-197. (Pubitemid 41701542)
70. Prowse KR, Greider CW. Developmental and tissue-specific regulation of mouse telomerase and telomere length. Proc Natl Acad Sci U S A. 1995;92:4818-4822.
71. CovielloMcLaughlin GM, Prowse KR. Telomere length regulation during postnatal development and ageing in Mus spretus. Nucleic Acids Res. 1997;25:3051-3058. (Pubitemid 27331398)
72. Collado M, Blasco MA, Serrano M. Cellular senescence in cancer and aging. Cell. 2007;130:223-33. (Pubitemid 47081143)
73. Wong LSM, Oeseburg H, De Boer RA, Van Gilst WH, Van Veldhuisen DJ, Van Der Harst P. Telomere biology in cardiovascular disease: the TERC-/- mouse as a model for heart failure and ageing. Cardiovasc Res. 2009;81:244-252.
74. Leri A, Franco S, Zacheo A, et al. Ablation of telomerase and telomere loss leads to cardiac dilatation and heart failure associated with p53 upregulation. EMBO J. 2003;22:131-139. (Pubitemid 36091276)
75. Blasco MA. Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet. 2005;6:611-622. (Pubitemid 41044298)
76. Gonzalez-Suarez E, Geserick C, Flores JM, Blasco MA. Antagonistic effects of telomerase on cancer and aging in K5-mTert transgenic mice. Oncogene. 2005;24:2256-2270. (Pubitemid 40516592)
77. Gardner JP, Kimura M, Chai W, et al. Telomere dynamics in macaques and humans. J Gerontol A Biol Sci Med Sci. 2007;62:367-374. (Pubitemid 47065703)
78. De Meyer T, Rietzschel ER, De Buyzere ML, Van Criekinge W, Bekaert S. Studying telomeres in a longitudinal population based study. Front Biosci. 2008;13:2960-2970. (Pubitemid 351589212)
79. Nordfjall K, Svenson U, Norrback KF, Adolfsson R, Lenner P, Roos G. The individual blood cell telomere attrition rate is telomere length dependent. PLoS Genet. 2009;5:e1000375.
80. De Meyer T, Rietzschel ER, De Buyzere ML, et al. Paternal age at birth is an important determinant of offspring telomere length. Hum Mol Genet. 2007;16:3097-3102. (Pubitemid 350131328)
81. Kimura M, Cherkas LF, Kato BS, et al. Offspring's leukocyte telomere length, paternal age, and telomere elongation in sperm. PLoS Genet. 2008;4:e37.
82. Njajou OT, Cawthon RM, Damcott CM, et al. Telomere length is paternally inherited and is associated with parental lifespan. Proc Natl Acad Sci U S A. 2007;104:12135-12139. (Pubitemid 47185642)
83. Unryn BM, Cook LS, Riabowol KT. Paternal age is positively linked to telomere length of children. Aging Cell. 2005;4:97-101. (Pubitemid 41632908)
84. Richards JB, Valdes AM, Gardner JP, et al. Higher serum vitamin D concentrations are associated with longer leukocyte telomere length in women. Am J Clin Nutr. 2007;86:1420-1425. (Pubitemid 350126247)
85. McGrath M, Wong JY, Michaud D, Hunter DJ, De Vivo I. Telomere length, cigarette smoking, and bladder cancer risk in men and women. Cancer Epidemiol Biomarkers Prev. 2007;16:815-819. (Pubitemid 46650587)
86. Valdes AM, Andrew T, Gardner JP, Kimura M, Oelsner E, Cherkas LF, Aviv A, Spector TD. Obesity, cigarette smoking, and telomere length in women. Lancet. 2005;366:662-664. (Pubitemid 41176019)
87. Cherkas LF, Hunkin JL, Kato BS, et al. The association between physical activity in leisure time and leukocyte telomere length. Arch Intern Med. 2008;168:154-158. (Pubitemid 351185881)
88. Jeanclos E, Schork NJ, Kyvik KO, Kimura M, Skurnick JH, Aviv A. Telomere length inversely correlates with pulse pressure and is highly familial. Hypertension. 2000;36:195-200. (Pubitemid 30626988)
89. Nawrot TS, Staessen JA, Gardner JP, Aviv A. Telomere length and possible link to X chromosome. Lancet. 2004;363:507-510. (Pubitemid 38229449)
90. Samani NJ, Boultby R, Butler R, Thompson JR, Goodall AH. Telomere shortening in atherosclerosis. Lancet. 2001;358:472-473. (Pubitemid 32769858)
91. Woo J, Suen EW, Leung JC, Tang NL, Ebrahim S. Older men with higher self-rated socioeconomic status have shorter telomeres. Age Ageing. 2009;38:553-558.
92. Adams J, Martin-Ruiz C, Pearce MS, White M, Parker L, von Zglinicki T. No association between socio-economic status and white blood cell telomere length. Aging Cell. 2007;6:125-128. (Pubitemid 46140146)
93. Gardner JP, Li S, Srinivasan SR, et al. Rise in insulin resistance is associated with escalated telomere attrition. Circulation. 2005;111:2171-2172.
94. Vasan RS, Demissie S, Kimura M, et al. Association of leukocyte telomere length with circulating biomarkers of the renin-angiotensin-aldosterone system: the Framingham Heart Study. Circulation. 2008;117:1138-1144. (Pubitemid 351544068)
95. Hunt SC, Chen W, Gardner JP, et al. Leukocyte telomeres are longer in African Americans than in whites: the National Heart, Lung, and Blood Institute Family Heart Study and the Bogalusa Heart Study. Aging Cell. 2008;7:451-458. (Pubitemid 351998605)
96. Roux AV, Ranjit N, Jenny NS, et al. Race/ethnicity and telomere length in the Multi-Ethnic Study of Atherosclerosis. Aging Cell. 2009;8:251-257.
97. Aubert G, Lansdorp PM. Telomeres and aging. Physiol Rev. 2008;88:557-579. (Pubitemid 351522746)
98. Dokal I, Vulliamy T. Dyskeratosis congenita: its link to telomerase and aplastic anaemia. Blood Rev. 2003;17:217-225. (Pubitemid 37356392)
99. Andreassi MG. DNA damage, vascular senescence and atherosclerosis. J Mol Med. 2008;86:1033-1043.
100. Samani NJ, van der Harst P. Biological ageing and cardiovascular disease. Heart. 2008;94:537-539. (Pubitemid 351580115)
101. Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature. 1990;345:458-460.
102. Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res. 2002;30e47.
103. Baird DM. New developments in telomere length analysis. Exp Gerontol. 2005;40:363-368. (Pubitemid 40775728)
104. Lansdorp PM, Verwoerd NP, van de Rijke FM, et al. Heterogeneity in telomere length of human chromosomes. Hum Mol Genet. 1996;5:685-691. (Pubitemid 26141285)
105. Aviv A. The epidemiology of human telomeres: faults and promises. J Gerontol A Biol Sci Med Sci. 2008;63:979-983.
106. Richards JB, Valdes AM, Gardner JP, et al. Homocysteine levels and leukocyte telomere length. Atherosclerosis. 2008;200:271-277.
107. Petrie A, Sabin C. Medical Statistics at a Glance, 2nd ed: Oxford, UK: Blackwell Publishing Ltd; 2005.
108. Hofer SM, Sliwinski MJ. Understanding ageing. An evaluation of research designs for assessing the interdependence of ageing-related changes. Gerontology. 2001;47:341-352. (Pubitemid 33135811)
109. Hofer SM, Flaherty BP, Hoffman L. Cross-sectional analysis of time-dependent data: mean-induced association in age-heterogenous samples and an alternative method based on sequential narrow age-cohort samples. Multivariate Behav Res. 2006;41:165-187. (Pubitemid 44231226)
110. Epel ES, Blackburn EH, Lin J, et al. Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci U S A. 2004;101:17312-17315. (Pubitemid 39627816)