Telomere length as a biomarker of aging and diseases
Abstract
As research related to healthspan and lifespan has become a hot topic, the necessity for a reliable and practical biomarker of aging (BoA), which can provide information about mortality and morbidity risk, along with remaining life expectancy, has increased. The chromosome terminus non-coding protective structure that prevents genomic instability is called a telomere. The continual shortening of telomeres, which affects their structure as well as function, is a hallmark of agedness. The aforementioned process is a potential cause of age-related diseases (ARDs), leading to a bad prognosis and a low survival rate, which compromise health and longevity. Hence, studies scrutinizing the BoAs often include telomere length (TL) as a prospective candidate. The results of these studies suggest that TL measurement can only provide an approximate appraisal of the aging rate, and its implementation into clinical practice and routine use as a BoA has many limitations and challenges. Nevertheless, measuring TL while determining other biomarkers can be used to assess biological age. This review focuses on the importance of telomeres in health, senescence, and diseases, as well as on summarizing the results and conclusions of previous studies evaluating TL as a potential BoA.
References
Lee J, Lau S, Meijer E, Hu P. Living Longer, With or Without Disability? A Global and Longitudinal Perspective. J Gerontol A Biol. 2020;75(1):162–7.
Chang AY, Skirbekk VF, Tyrovolas S, Kassebaum NJ, Dieleman JL. Measuring population ageing: an analysis of the Global Burden of Disease Study 2017. Lancet Public Health. 2019;4(3):e159–67.
Teixeira MZ. Telomere length: Biological marker of cellular vitality, aging, and health-disease process. Rev Assoc Med Bras. 2021;67(2):173–7.
Mather KA, Jorm AF, Parslow RA, Christensen H. Is telomere length a biomarker of aging? A review. J Gerontol A Biol Sci Med Sci. 2011;66 A(2):202–13.
Baker GT, Sprott RL. Biomarkers of aging. Exp Gerontol. 1988;23(4–5):223–39.
Vaiserman A, Krasnienkov D. Telomere Length as a Marker of Biological Age: State-of-the-Art, Open Issues, and Future Perspectives. Front Genet. 2021;1:630186.
Lohman T, Bains G, Berk L, Lohman E. Predictors of Biological Age: The Implications for Wellness and Aging Research. J Gerontol Geriatr Med. 2021; 7:23337214211046419.
Herrmann M, Pusceddu I, März W, Herrmann W. Telomere biology and age-related diseases. Clin Chem Lab Med. 2018;56(8):1210–22.
Shammas MA. Telomeres, lifestyle, cancer, and aging. Curr Opin Clin Nutr Metab Care. 2011;14(1):28–34.
Bertuch AA. The molecular genetics of the telomere biology disorders. RNA Biol. 2016;13(8):696–706.
Benetos A, Okuda K, Lajemi M, Kimura M, Thomas F, Skurnick J, 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(2):381–5.
Feurstein S, Adegunsoye A, Mojsilovic D, Vij R, West DePersia AH, Rajagopal PS, et al. Telomere biology disorder prevalence and phenotypes in adults with familial hematologic and/or pulmonary presentations. Blood Adv. 2020;4(19):4873–86.
Hastings WJ, Shalev I, Belsky DW. Translating Measures of Biological Aging to Test Effectiveness of Geroprotective Interventions: What Can We Learn from Research on Telomeres? Front Genet. 2017;8:164.
Sanders JL, Newman AB. Telomere Length in Epidemiology: A Biomarker of Aging, Age-Related Disease, Both, or Neither? Epidemiol Rev. 2013;35:112–31.
Gruber HJ, Semeraro MD, Renner W, Herrmann M. Telomeres and age-related diseases. Biomedicines. 2021;9(10):1335.
Notterman DA, Schneper L. Telomere Time-Why We Should Treat Biological Age Cautiously. JAMA Netw Open. 2020;3(5):e204352.
Gorenjak V. The future of telomere length in personalized medicine. Front Biosci. 1629;23:1628–54.
Meynell HA. The Remaking of the Remaking. Theology. 1975;78(661):338–45.
Mcclintock B. The stability of broken ends of chromosomes in zea mays. Genetics. 1940;26:234.
Tomita K. How long does telomerase extend telomeres? Regulation of telomerase release and telomere length homeostasis. Curr Genet. 2018;64:1177–81.
Lazzerini-Denchi E, Sfeir A. Stop pulling my strings - what telomeres taught us about the DNA damage response. Nat Rev Mol Cell Biol. 2016;17(6):364–78.
Blasco MA. Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet. 2005;6(8):611–22.
Blackburn EH. Review Switching and Signaling at the Telomere. Cell. 2001;106:661–73.
Blackburn EH. Telomeres and Telomerase: The Means to the End (Nobel Lecture). Angew Chem Int Ed. 2010;49(41):7405–21.
de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 2005;19(18):2100–10.
Blasco MA. Telomere length, stem cells and aging. Nat Chem Biol. 2007;3(10):640–9.
Srinivas N, Rachakonda S, Kumar R. cancers Telomeres and Telomere Length: A General Overview. Cancers. 2020;12:558.
Blasco MA. The epigenetic regulation of mammalian telomeres. Nat Rev Genet. 2007;8(4):299–309.
Allsopp RC, Vaziri H, Pat C, Goldsteint S, Younglai EV, Bruce Futcher A, et al. Telomere length predicts replicative capacity of human fibroblasts. Proc Natl Acad Sci U S A. 1992;89:10114–8.
Saretzki G. Telomeres, Telomerase and Ageing. Biochem Cell Biol. 2018;90:221–308.
Oikawa S, Kawanishi S. Site-specifc DNA damage at GGG sequence by oxidative stress may accelerate telomere shortening. FEBS Lett. 1999;453:365–8.
von Zglinicki T, Wan T, Miwa S. Senescence in Post-Mitotic Cells: A Driver of Aging? Antioxid Redox Signal. 2021;34(4):308–23.
von Zglinicki T, Wan T, Miwa S. Senescence in Post-Mitotic Cells: A Driver of Aging? Antioxid Redox Signal. 2021;34(4):308–23.
Sanders JL, Newman AB. Telomere Length in Epidemiology: A Biomarker of Aging, Age-Related Disease, Both, or Neither? Epidemiol Rev. 2013;35(1):112-31.
Gardner M, Bann D, Wiley L, Cooper R, Hardy R, Nitsch D, et al. Gender and telomere length: Systematic review and meta-analysis. Exp Gerontol. 2014;51:15–27.
Lapham K, Kvale MN, Lin J, Connell S, Croen LA, Dispensa BP, et al. Automated Assay of Telomere Length Measurement and Informatics for 100,000 Subjects in the Genetic Epidemiology Research on Adult Health and Aging (GERA) Cohort. Genetics. 2015;200(4):1061–72.
Calado RT, Dumitriu B. Telomere Dynamics in Mice and Humans. Semin Hematol. 2013;50(2):165–74.
Boccardi M, Boccardi V. Psychological Wellbeing and Healthy Aging: Focus on Telomeres. Geriatrics. 2019;4:25.
Arai Y, Martin-Ruiz CM, Takayama M, Abe Y, Takebayashi T, Koyasu S, et al. Inflammation, But Not Telomere Length, Predicts Successful Ageing at Extreme Old Age: A Longitudinal Study of Semi-supercentenarians. EBioMedicine. 2015;2(10):1549–58.
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(9355):393–5.
Andreassi MG. DNA damage, vascular senescence and atherosclerosis. J Mol Med. 2008;86:1033–43.
Samani NJ, van der Harst P. Biological ageing and cardiovascular disease. Heart. 2008;94(5):537–9.
Shay JW, van der Haegen BA, Ying Y, Wright WE. The Frequency of Immortalization of Human Fibroblasts and Mammary Epithelial Cells Transfected with SV40 Large T-Antigen. Exp Cell Res. 1993;209(1):45–52.
Wang Y, Sušac L, Feigon J. Structural Biology of Telomerase. Cold Spring Harb Perspect Biol. 2019;11:a032383.
Wong MS, Wright WE, Shay JW. Alternative splicing regulation of telomerase: a new paradigm? Trends Genet. 2014;30(10):430–8.
Dunham MA, Neumann AA, Fasching CL, Reddel RR. Telomere maintenance by recombination in human cells. Nat Genet. 2000;26(4):447–50.
Maciejowski J, de Lange T. Telomeres in cancer: tumour suppression and genome instability. Nat Rev Mol Cell Biol. 2017;18(3):175–86.
Smith-Sonneborn J. Telomerase Biology Associations Offer Keys to Cancer and Aging Therapeutics. Curr Aging Sci. 2020;13(1):11–21.
Roake CM, Artandi SE. Regulation of human telomerase in homeostasis and disease. Nat Rev Mol Cell Biol. 2020;21(7):384–97.
Armanios M. Review series Telomeres and age-related disease: how telomere biology informs clinical paradigms. J Clin Investig. 2013;123(3):996–1002.
Paul L. Diet, nutrition and telomere length. J Nutr Biochem. 2011;22(10):895–901.
Pusceddu I, Herrmann M, Kirsch SH, Werner C, Hübner U, Bodis M, et al. Prospective study of telomere length and LINE-1 methylation in peripheral blood cells: the role of B vitamins supplementation. Eur J Nutr. 2016;55(5):1863–73.
Borras M, Panizo S, Sarró F, Valdivielso JM, Fernandez E. Assessment of the Potential Role of Active Vitamin D Treatment in Telomere Length: A Case-Control Study in Hemodialysis Patients. Clin Ther. 2012;34(4):849–56.
Zhu H, Guo D, Li K, Pedersen-White J, Stallmann-Jorgensen IS, Huang Y, et al. Increased telomerase activity and vitamin D supplementation in overweight African Americans. Int J Obes. 2012;36(6):805–9.
Hoffecker BM, Raffield LM, Kamen DL, Nowling TK, Johnson RH. Systemic Lupus Erythematosus and Vitamin D Deficiency Are Associated with Shorter Telomere Length among African Americans: A Case-Control Study. PLoS ONE. 2013;8(5):e63725.
Lulkiewicz M, Bajsert J, Kopczynski P, Barczak W, Rubis B. Telomere length: how the length makes a difference. Mol Biol Rep. 2020;47:7181–8.
Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, Morrow JD, et al. Accelerated telomere shortening in response to life stress. PNAS. 2004;101(49):17312–5.
Ornish D, Lin J, Daubenmier J, Weidner G, Epel E, Kemp C, et al. Increased telomerase activity and comprehensive lifestyle changes: a pilot study. Lancet Oncol. 2008;9(11):1048–57.
Werner C, Fürster T, Widmann T, Pöss J, Roggia C, Hanhoun M, et al. Physical Exercise Prevents Cellular Senescence in Circulating Leukocytes and in the Vessel Wall. Circulation. 2009;120:2438–47.
Freitas-Simoes T-M, Ros E, Sala-Vila A. Nutrients, foods, dietary patterns and telomere length: Update of epidemiological studies and randomized trials. Metab. 2016;65(4):406–15.
Pusceddu I, Farrell C-JL, di Pierro AM, Jani E, Herrmann W, Herrmann M. The role of telomeres and vitamin D in cellular aging and age-related diseases. Clin Chem Lab. 2015;53(11):1661-78.
Pusceddu I, Herrmann M, Kirsch SH, Werner C, Hübner U, Bodis M, et al. One-carbon metabolites and telomere length in a prospective and randomized study of B- and/or D-vitamin supplementation. Eur J Nutr. 2017;56(5):1887–98.
Arsenis NC, You T, Ogawa EF, Tinsley GM, Zuo L. Physical activity and telomere length: Impact of aging and potential mechanisms of action. Oncotarget. 2017;8(27):45008–19.
Balan E, Decottignies A, Deldicque L. Physical Activity and Nutrition: Two Promising Strategies for Telomere Maintenance? Nutrients. 2018;10:1942.
Maugeri A, Barchitta M, Magnano R, Lio S, Clara M, Rosa L, et al. The Effect of Alcohol on Telomere Length: A Systematic Review of Epidemiological Evidence and a Pilot Study during Pregnancy. Int J Environ Res Public Health. 2021;18:5038.
Astuti Y, Wardhana A, Watkins J, Wulaningsih W. Cigarette smoking and telomere length: A systematic review of 84 studies and meta-analysis. Environ. 2017;158:480–9.
Vulliamy T, Marrone A, Szydlo R, Walne A, Mason PJ, Dokal I. Disease anticipation is associated with progressive telomere shortening in families with dyskeratosis congenita due to mutations in TERC. Nat Genet. 2004;36(5):447–9.
Demanelis K, Jasmine F, Chen LS, Chernoff M, Tong L, Delgado D, et al. Determinants of telomere length across human tissues. Science. 2020;369(6509):eaaz6876.
Vaziri H, Schachter F, Uchida I, Weit L, Zhu X, Effros R, et al. Loss of Telomeric DNA during Aging of Normal and Trisomy 21 Human Lymphocytes. Am J Hum Genet. 1993;52:661–7.
Eline Slagboom P, Droog S. Genetic Determination of Telomere Size in Humans: A Twin Study of Three Age Groups. Am J Hum Genet. 1994;55:876–82.
Kam MLW, Nguyen TTT, Ngeow JYY. Telomere biology disorders. Genomic Med. 2021;6:36.
Zhang X, Lin S, Funk WE, Hou L. Environmental and occupational exposure to chemicals and telomere length in human studies. Occup Environ Med. 2013;70(10):743–9.
Epel ES. Can Childhood Adversity Affect Telomeres of the Next Generation? Possible Mechanisms, Implications, and Next-Generation Research. Am J Psychiat. 2020;177(1):7–9.
Mendoza-Núñez VM, Martínez-Maldonado M de la L, Vivaldo-Martínez M. What Is the Onset Age of Human Aging and Old Age? Int J Gerontol. 2016;10(1):56.
Mahmoodpoor A, Sanaie S, Roudbari F, Sabzevari T, Sohrabifar N, Kazeminasab S. Understanding the role of telomere attrition and epigenetic signatures in COVID-19 severity. Gene. 2022;811:146069.
Ridout KK, Levandowski M, Ridout SJ, Gantz L, Goonan K, Palermo D, et al. Early life adversity and telomere length: a meta-analysis. Mol Psychiatry. 2018;23(4):858–71.
Wadhwa PD, Entringer S, de Punder K, Buss C. The fetal programming of telomere biology hypothesis: an update. Philos Trans R Soc Lond, B Biol Sci. 2018;373(1741):20170151.
Aviv A, Shay JW. Reflections on telomere dynamics and ageing-related diseases in humans. Philos Trans R Soc Lond, B Biol Sci. 2018;373(1741):20160436.
Haycock PC, Heydon EE, Kaptoge S, Butterworth AS, Thompson A, Willeit P. Leucocyte telomere length and risk of cardiovascular disease: systematic review and meta-analysis. BMJ. 2014;349(3):g4227–g4227.
Tellechea ML, Pirola CJ. The impact of hypertension on leukocyte telomere length: a systematic review and meta-analysis of human studies. J Hum Hypertens. 2016;31:99–105.
Jin X, Pan B, Dang X, Wu H, Xu D. Relationship between short telomere length and stroke A meta-analysis. Medicine. 2018;97(39):e12489.
Martínez P, Blasco MA. Telomere-driven diseases and telomere-targeting therapies. J Cell Biol. 2017 Apr 3;216(4):875–87.
Müezzinler A, Mons U, Dieffenbach AK, Butterbach K, Saum K-U, Schick M, et al. Body mass index and leukocyte telomere length dynamics among older adults: Results from the ESTHER cohort. Exp Gerontol. 2016;74:1–8.
Welzl K, Kern G, Mayer G, Weinberger B, Säemann MD, Sturm G, et al. Effect of Different Immunosuppressive Drugs on Immune Cells from Young and Old Healthy Persons. Gerontology. 2014;60(3):229–38.
Yepuri G, Sukhovershin R, Nazari-Shafti TZ, Petrascheck M, Ghebre YT, Cooke JP. Proton Pump Inhibitors Accelerate Endothelial Senescence. Circ Res. 2016;118(12).
Zeng J, Liu H, Ping F, Li W, Li Y. Insulin treatment affects leukocyte telomere length in patients with type 2 diabetes: 6-year longitudinal study. J Diabetes Complicat. 2019;33(5):363–7.
Prasad KN, Wu M, Bondy SC. Telomere shortening during aging: Attenuation by antioxidants and anti-inflammatory agents. Mech Ageing Dev. 2017;164:61–6.
Haycock PC, Hemani G, Aviv A. Telomere Length and Risk of Cancer and Non-neoplastic Diseases: Is Survivin the Ariadne’s Thread? Reply. JAMA Oncol. 2017 Dec 1;3(12):1741.
Gavia-García G, Rosado-Pérez J, Arista-Ugalde TL, Aguiñiga-Sánchez I, Santiago-Osorio E, Mendoza-Núñez VM. Telomere length and oxidative stress and its relation with metabolic syndrome components in the aging. Biology. 2021;10(4):253.
Chang ACY, Chang ACH, Kirillova A, Sasagawa K, Su W, Weber G, et al. Telomere shortening is a hallmark of genetic cardiomyopathies. PNAS. 2018;115(37):9276–81.
Frati G, Versaci F, Sciarretta S. A novel signalling mechanism regulating telomere length in cardiomyocytes. Cardiovasc Res. 2021;117:13–4.
Morgan RG, Donato AJ, Walker AE. Telomere uncapping and vascular aging. Am J Physiol - Heart Circ Physiol. 2018;315(1):H1–5.
Brouilette SW, Moore JS, McMahon AD, Thompson JR, Ford I, Shepherd J, 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. The Lancet. 2007;369(9556):107–14.
Ogami M, Ikura Y, Ohsawa M, Matsuo T, Kayo S, Yoshimi N, et al. Telomere Shortening in Human Coronary Artery Diseases. Arterioscler Thromb Vasc Biol. 2004;24(3):546–50.
Sawhney V, Campbell NG, Brouilette SW, Coppen SR, Harbo M, Baker V, et al. Telomere shortening and telomerase activity in ischaemic cardiomyopathy patients – Potential markers of ventricular arrhythmia. Int J Cardiol. 2016;207:157–63.
Sharifi-Sanjani M, Oyster NM, Tichy ED, Bedi Jr KC, Harel O, Margulies KB, et al. Cardiomyocyte-Specific Telomere Shortening is a Distinct Signature of Heart Failure in Humans. J Am Heart Assoc. 2017;6(9):e005086.
Willeit P, Willeit J, Brandstätter A, Ehrlenbach S, Mayr A, Gasperi A, et al. Clinical and Population Studies Cellular Aging Reflected by Leukocyte Telomere Length Predicts Advanced Atherosclerosis and Cardiovascular Disease Risk. Arterioscler Thromb Vasc Biol. 2010;30:1649–56.
Vukašinović A, Ostanek B, Klisic A, Kafedžić S, Zdravković M, Ilić I, et al. Telomere-telomerase system status in patients with acute myocardial infarction with ST-segment elevation (STEMI) - relationship with oxidative stress. Arch Med Sci. doi: 10.5114/aoms/136074.
Gao D, Zhang R, Ji G, Li C, Guo D, Jin T, et al. Relative Telomere Length and Stroke Risk in a Chinese Han Population. J Mol Neurosci. 2018;66(4):475–81.
Allende M, Molina E, González-Porras JR, Toledo E, Lecumberri R, Hermida J. Short Leukocyte Telomere Length Is Associated With Cardioembolic Stroke Risk in Patients With Atrial Fibrillation. Stroke. 2016;47(3):863–5.
Ding H, Chen C, Shaffer JR, Liu L, Xu Y, Wang X, et al. Telomere Length and Risk of Stroke in Chinese. Stroke. 2012;43(3):658–63.
Jiang X, Dong M, Cheng J, Huang S, He Y, Ma K, et al. Decreased Leukocyte Telomere Length (LTL) Is Associated with Stroke but Unlikely to Be Causative. PLoS ONE. 2013;8(7):e68254.
Zhang W, Chen Y, Wang Y, Liu P, Zhang M, Zhang C, et al. Short telomere length in blood leucocytes contributes to the presence of atherothrombotic stroke and haemorrhagic stroke and risk of post-stroke death. Clin Sci. 2013;125(1):27–36.
Martin-Ruiz C, Dickinson HO, Keys B, Rowan E, Kenny RA, von Zglinicki T. Telomere length predicts poststroke mortality, dementia, and cognitive decline. Ann Neurol. 2006;60(2):174–80.
Haycock PC, Heydon EE, Kaptoge S, Butterworth AS, Thompson A, Willeit P. Leucocyte telomere length and risk of cardiovascular disease: systematic review and meta-analysis. BMJ. 2014;349:g4227.
Hoffmann J, Richardson G, Haendeler J, Altschmied J, Andrés V. Arteriosclerosis, Thrombosis, and Vascular Biology Telomerase as a Therapeutic Target in Cardiovascular Disease. Arterioscler Thromb Vasc Biol. 2021;41:1047–61.
Kuo C, Pilling LC, Kuchel GA, Ferrucci L, Melzer D. Telomere length and aging‐related outcomes in humans: A Mendelian randomization study in 261,000 older participants. Aging Cell. 2019;18(6):e13017.
Yeh J-K, Wang C-Y. Telomeres and Telomerase in Cardiovascular Diseases. Genes. 2016;7(9):58.
Calvert PA, Liew T-V, Gorenne I, Clarke M, Costopoulos C, Obaid DR, et al. Leukocyte Telomere Length Is Associated With High-Risk Plaques on Virtual Histology Intravascular Ultrasound and Increased Proinflammatory Activity. Arterioscler Thromb Vasc Biol. 2011;31(9):2157–64.
Armstrong EJ, Xing L, Zhang J, Zheng Y, Shunk KA, Yeh RW, et al. Association between leukocyte telomere length and drug-eluting stent strut coverage by optical coherence tomography. J Am Coll Cardiol. 2012;59(24):2218–9.
Adaikalakoteswari A, Balasubramanyam M, Mohan V. Telomere shortening occurs in Asian Indian Type 2 diabetic patients. Diabet Med. 2005;22(9):1151–6.
Adaikalakoteswari A, Balasubramanyam M, Ravikumar R, Deepa R, Mohan V. Association of telomere shortening with impaired glucose tolerance and diabetic macroangiopathy. Atherosclerosis. 2007;195(1):83–9.
Salpea KD, Talmud PJ, Cooper JA, Maubaret CG, Stephens JW, Abelak K, et al. Association of telomere length with type 2 diabetes, oxidative stress and UCP2 gene variation. Atherosclerosis. 2010;209(1):42–50.
Shen Q, Zhao X, Yu L, Zhang Z, Zhou D, Kan M, et al. Association of Leukocyte Telomere Length with Type 2 Diabetes in Mainland Chinese Populations. J Clin Endocrinol Metab. 2012;97(4):1371–4.
Tentolouris N, Nzietchueng R, Cattan V, Ga¨el Poitevin G, Lacolley P, Papazafiropoulou A, et al. White Blood Cells Telomere Length Is Shorter in Males With Type 2 Diabetes and Microalbuminuria. Diabetes Care. 2007;30:2909–15.
Testa R, Olivieri F, Sirolla C, Spazzafumo L, Rippo MR, Marra M, et al. Leukocyte telomere length is associated with complications of Type 2 diabetes mellitus. Diabet Med. 2011 Nov;28(11):1388–94.
Xiao F, Zheng X, Cui M, Shi G, Chen X, Li R, et al. Telomere Dysfunction–Related Serological Markers Are Associated With Type 2 Diabetes. Diabetes Care. 2011 Oct 1;34(10):2273–8.
Zhao J, Zhu Y, Lin J, Matsuguchi T, Blackburn E, Zhang Y, et al. Short Leukocyte Telomere Length Predicts Risk of Diabetes in American Indians: the Strong Heart Family Study. Diabetes. 2014;63(1):354–62.
Hovatta I, de Mello VDF, Kananen L, Lindströ MJ, Eriksson JG. Leukocyte Telomere Length in the Finnish Diabetes Prevention Study. PLoS ONE. 2012;7(4):34948.
Tamura Y, Izumiyama-Shimomura N, Kimbara Y, Nakamura K, Ishikawa N, Aida J, et al. β-Cell Telomere Attrition in Diabetes: Inverse Correlation Between HbA1c and Telomere Length. J Clin Endocrinol Metab. 2014;99(8):2771–7.
You NY, Chen BH, Song Y, Lu X, Chen Y, Manson JE, et al. A Prospective Study of Leukocyte Telomere Length and Risk of Type 2 Diabetes in Postmenopausal Women. Diabetes. 2012;61(11):2998–3004.
Hou L, Zhang X, Gawron AJ, Liu J. Surrogate tissue telomere length and cancer risk: Shorter or Longer? Cancer Lett. 2012;319(2):130–5.
Hou L, Joyce BT, Gao T, Liu L, Zheng Y, Penedo FJ, et al. Blood Telomere Length Attrition and Cancer Development in the Normative Aging Study Cohort. EBioMedicine. 2015;2(6):591–6.
Vinagre J, Almeida A, Pópulo H, Batista R, Lyra J, Pinto V, et al. Frequency of TERT promoter mutations in human cancers. Nat Commun. 2013;4:2185.
Horn S, Figl A, Rachakonda PS, Fischer C, Sucker A, Gast A, et al. TERT Promoter Mutations in Familial and Sporadic Melanoma. Science. 2013;339(6122):959–61.
Killela PJ, Reitman ZJ, Jiao Y, Bettegowda C, Agrawal N, Diaz LA, et al. TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. PNAS. 2013;110(15):6021–6.
Kinde I, Munari E, Faraj SF, Hruban RH, Schoenberg M, Bivalacqua T, et al. TERT Promoter Mutations Occur Early in Urothelial Neoplasia and Are Biomarkers of Early Disease and Disease Recurrence in Urine. Cancer Res. 2013;73(24):7162–7.
Kawai-Kitahata F, Asahina Y, Tanaka S, Kakinuma S, Murakawa M, Nitta S, et al. Comprehensive analyses of mutations and hepatitis B virus integration in hepatocellular carcinoma with clinicopathological features. J Gastroenterol. 2016;51(5):473–86.
Dilley RL, Greenberg RA. ALTernative Telomere Maintenance and Cancer. Trends Cancer. 2015;1(2):145–56.
Fordyce CA, Heaphy CM, Bisoffi M, Wyaco JL, Joste NE, Mangalik A, et al. Telomere content correlates with stage and prognosis in breast cancer. Breast Cancer Res Treat. 2006;99(2):193–202.
Weischer M, Nordestgaard BG, Cawthon RM, Freiberg JJ, Tybjærg-Hansen A, Bojesen SE. Short Telomere Length, Cancer Survival, and Cancer Risk in 47102 Individuals. J Natl Cancer Inst. 2013;105(7):459–68.
Julin B, Shui I, Heaphy CM, Joshu CE, Meeker AK, Giovannucci E, et al. Circulating leukocyte telomere length and risk of overall and aggressive prostate cancer. B J Cancer. 2015;112:769–76.
Wentzensen IM, Mirabello L, Pfeiffer RM, Savage SA. The Association of Telomere Length and Cancer: a Meta-analysis. Cancer Epidemiol Biomarkers Prev. 2011;20(6):1238–50.
Zhang X, Zhao Q, Zhu W, Liu T, Xie S-H, Zhong L-X, et al. The Association of Telomere Length in Peripheral Blood Cells with Cancer Risk: A Systematic Review and Meta-analysis of Prospective Studies. Cancer Epidemiol Biomark Prev. 2017;26(9):1381–90.
Jang JS, Choi YY, Lee WK, Choi JE, Cha SI, Kim YJ, et al. Telomere length and the risk of lung cancer. Cancer Science. 2008;99(7):1385–9.
Doherty JA, Grieshober L, Houck JR, Barnett MJ, Tapsoba JDD, Thornquist M, et al. Telomere Length and Lung Cancer Mortality among Heavy Smokers. Cancer Epidemiol Biomark Prev. 2018;27(7):829–37.
Jebaraj BMC, Stilgenbauer S. Telomere Dysfunction in Chronic Lymphocytic Leukemia. Front Oncol. 2021;10:612665.
Ruden M, Puri N. Novel anticancer therapeutics targeting telomerase. Cancer Treat Rev. 2013;39(5):444–56.
Valdes AM, Richards JB, Gardner JP, Swaminathan R, Kimura M, Xiaobin L, et al. Telomere length in leukocytes correlates with bone mineral density and is shorter in women with osteoporosis. Osteoporos Int. 2007;18(9):1203–10.
Tang NLS, Woo J, Suen EWC, Liao CD, Leung JCS, Leung PC. The effect of telomere length, a marker of biological aging, on bone mineral density in elderly population. Osteoporos Int. 2010;21(1):89–97.
Pignolo RJ, Suda RK, McMillan EA, Shen J, Lee S-H, Choi Y, et al. Defects in telomere maintenance molecules impair osteoblast differentiation and promote osteoporosis. Aging Cell. 2008;7(1):23–31.
Sanders JL, Cauley JA, Boudreau RM, Zmuda JM, Strotmeyer ES, Opresko PL, et al. Leukocyte Telomere Length Is Not Associated With BMD, Osteoporosis, or Fracture in Older Adults: Results From the Health, Aging and Body Composition Study Jason. J Bone Miner Res. 2009;24(9):1531–6.
Xie H, Ma Y, Shao M, Kong J, Zhou T, Wang F, et al. Telomere length in patients with osteoarthritis: a systematic review and meta-analysis. Aging Clin Exp Res. 2021;34(3):495-503.
Forero DA, González-Giraldo Y, López-Quintero C, Castro-Vega LJ, Barreto GE, Perry G, et al. Meta-analysis of Telomere Length in Alzheimer’s Disease. J Gerontol A Biol Sci Med Sci. 2016;71(8):1069–73.
Hecker M, Bühring J, Fitzner B, Rommer PS, Zettl UK. Genetic, Environmental and Lifestyle Determinants of Accelerated Telomere Attrition as Contributors to Risk and Severity of Multiple Sclerosis. Biomolecules. 2021;11(10):1510.
Xia K, Zhang L, Zhang G, Wang Y, Huang T, Fan D. Leukocyte telomere length and amyotrophic lateral sclerosis: a Mendelian randomization study. Orphanet J Rare Dis. 2021;16(1):1–8.
Pousa PA, Souza RM, Melo PHM, Correa BHM, Mendonça TSC, Simões-e-Silva AC, et al. Telomere Shortening and Psychiatric Disorders: A Systematic Review. Cells. 2021;10(6):1423.
Heba AC, Toupance S, Arnone D, Peyrin-Biroulet L, Benetos A, Ndiaye NC. Telomeres: New players in immune-mediated inflammatory diseases? J Autoimmun. 2021;123:102699.
Wu K, Volke A, Lund M, Bang K, Thestrup-Pedersen K. Telomerase activity is spontaneously increased in lymphocytes from patients with atopic dermatitis and correlates with cellular proliferation. J Dermatol Sci. 1999;22(1):24–30.
Lee YH, Bae SC. Association between shortened telomere length and rheumatoid arthritis. Z Rheumatol. 2018;77(2):160–7.
Zeng Z, Zhang W, Qian Y, Huang H, Wu DJH, He Z, et al. Systematic Review and Meta Analysis Association of telomere length with risk of rheumatoid arthritis: a meta-analysis and Mendelian randomization. Rheumatology. 2020;59:940–7.
Fujii H, Shao L, Colmegna I, Goronzy JJ, Weyand CM. Telomerase insufficiency in rheumatoid arthritis. PNAS. 2009;106(11):4360–5.
Tsakiri KD, Cronkhite JT, Kuan PJ, Xing C, Raghu G, Weissler JC, et al. Adult-onset pulmonary fibrosis caused by mutations in telomerase. PNAS. 2007;104(18):7552–7.
Newton CA, Batra K, Torrealba J, Kozlitina J, Glazer CS, Aravena C, et al. Telomere-related lung fibrosis is diagnostically heterogeneous but uniformly progressive. Eur Respir J. 2016;48(6):1710–20.
Stock CJW, Renzoni EA, Bhattacharyya S. Clinical Medicine Telomeres in Interstitial Lung Disease. J Clin Med. 2021;10:1384.
Sanchez-Vazquez R, Guío-Carrión A, Zapatero-Gaviria A, Martínez P, A.Blasco M. Shorter telomere lengths in patients with severe COVID-19 disease. Aging. 2021;13(1):1–15.
dos Santos GA, Pimenta R, Viana NI, Guimarães VR, Romão P, Candido P, et al. Shorter leukocyte telomere length is associated with severity of COVID-19 infection. Biochem Biophys Rep. 2021;27:101056.
Mahmoodpoor A, Sanaie S, Roudbari F, Sabzevari T, Sohrabifar N, Kazeminasab S. Understanding the role of telomere attrition and epigenetic signatures in COVID-19 severity. Gene. 2022;811:146069.
Ledda C, Loreto C, Rapisarda V. Telomere length as a biomarker of biological aging in shiftworkers. Appl Sci. 2020;10(8):2764.
Kameda M, Mikawa T, Yokode M, Inagaki N, Kondoh H. Senescence research from historical theory to future clinical application. Geriatr Gerontol Int. 2021;21(2):125–30.
Der G, David Batty G, Benzeval M, Deary IJ, Green MJ, Mcglynn L, et al. Is Telomere Length a Biomarker for Aging: Cross-Sectional Evidence from the West of Scotland? PLoS ONE. 2012;7(9):e45166.
Weng N. Telomeres and immune competency. Curr Opin Immunol. 2012;24(4):470–5.
