The heritability of leucocyte telomere length dynamics

Journal of Medical Genetics

Volumn 52, Issue 5, 2015, Pages 297-302

  Hjelmborg, Jacob B ^a   Dalgård, Christine ^a   Möller, Soren ^a   Steenstrup, Troels ^a   Kimura, Masayuki ^b   Christensen, Kaare ^a,c   Kyvik, Kirsten O ^a   Aviv, Abraham ^b  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b University of Medicine and Dentistry of New Jersey Medical School   (United States)

^c ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGE; ARTICLE; CONTROLLED STUDY; DIZYGOTIC TWINS; ENVIRONMENTAL FACTOR; FEMALE; FOLLOW UP; HEREDITY; HERITABILITY; HUMAN; LEUCOCYTE TELOMERE LENGTH; LEUKOCYTE; LONGITUDINAL STUDY; MALE; MONOZYGOTIC TWINS; PRIORITY JOURNAL; SEX; TELOMERE HOMEOSTASIS; BIOMETRY; GENETICS; METABOLISM; MIDDLE AGED; REGISTER; TELOMERE; TWINS; YOUNG ADULT;

ADULT; BIOMETRY; FEMALE; FOLLOW-UP STUDIES; HUMANS; LEUKOCYTES; MALE; MIDDLE AGED; REGISTRIES; TELOMERE; TELOMERE HOMEOSTASIS; TWINS; YOUNG ADULT;

EID: 84930675596     PISSN: 00222593     EISSN: 14686244     Source Type: Journal    
DOI: 10.1136/jmedgenet-2014-102736     Document Type: Article

References (49)

1. Slagboom PE, Droog S, Boomsma DI. Genetic determination of telomere size in humans: a twin study of three age groups. Am J Hum Genet 1994;55:876-82.
2. 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.
3. Vasa-Nicotera M, Brouilette S, Mangino M, Thompson JR, Braund P, Clemitson JR, Mason A, Bodycote CL, Raleigh SM, Louis E, Samani NJ. Mapping of a major locus that determines telomere length in humans. Am J Hum Genet 2005;76:147-51.
4. Andrew T, Aviv A, Falchi M, Surdulescu GL, Gardner JP, Lu X, Kimura M, Kato BS, Valdes AM, Spector TD. Mapping genetic loci that determine leukocyte telomere length in a large sample of unselected female sibling pairs. Am J Hum Genet 2006;78:480-6.
5. Lee JH, Cheng R, Honig LS, Feitosa M, Kammerer CM, Kang MS, Schupf N, Lin SJ, Sanders JL, Bae H, Druley T, Perls T, Christensen K, Province M, Mayeux R. 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 2014;4:310.
6. Nawrot TS, Staessen JA, Gardner JP, Aviv A. Telomere length and possible link to X chromosome. Lancet 2004;363:507-10.
7. Vasan RS, Demissie S, Kimura M, Cupples LA, Rifai N, White C, Wang TJ, Gardner JP, Cao X, Benjamin EJ, Levy D, Aviv A. Association of leukocyte telomere length with circulating biomarkers of the renin-angiotensin-aldosterone system: the Framingham Heart Study. Circulation 2008;117:1138-44.
8. Hunt SC, Chen W, Gardner JP, Kimura M, Srinivasan SR, Eckfeldt JH, Berenson GS, Aviv A. 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;7:451-8.
9. Unryn BM, Cook LS, Riabowol KT. Paternal age is positively linked to telomere length of children. Aging Cell 2005;4:97-101.
10. De Meyer T, Rietzschel ER, De Buyzere ML, De Bacquer D, Van Criekinge W, De Backer GG, Gillebert TC, Van Oostveldt P, Bekaert S. Paternal age at birth is an important determinant of offspring telomere length. Hum Mol Genet 2007;16:3097-102.
11. Kimura M, Cherkas LF, Kato BS, Demissie S, Hjelmborg JB, Brimacombe M, Cupples A, Hunkin JL, Gardner JP, Lu X, Cao X, Sastrasinh M, Province MA, Hunt SC, Christensen K, Levy D, Spector TD, Aviv A. Offspring's leukocyte telomere length, paternal age, and telomere elongation in sperm. PLoS Genet 2008;4:e37.
12. Broer L, Codd V, Nyholt DR, Deelen J, Mangino M, Willemsen G, Albrecht E, Amin N, Beekman M, de Geus EJ, Henders A, Nelson CP, Steves CJ, Wright MJ, de Craen AJ, Isaacs A, Matthews M, Moayyeri A, Montgomery GW, Oostra BA, Vink JM, Spector TD, Slagboom PE, Martin NG, Samani NJ, van Duijn CM, Boomsma DI. Meta-analysis of telomere length in 19,713 subjects reveals high heritability, stronger maternal inheritance and a paternal age effect. Eur J Hum Genet 2013;21:1163-8.
13. 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;366:662-4.
14. Vasan RS, Demissie S, Kimura M, Cupples LA, Rifai N, White C, Wang TJ, Gardner JP, Cao X, Benjamin EJ, Aviv A. Association of leukocyte telomere length with circulating biomarkers of the renin-angiotensin-aldosterone system: the Framingham Heart Study. Circulation 2008;117:1138-44.
15. Gardner JP, Li S, Srinivasan SR, Chen W, Kimura M, Lu X, Berenson GS, Aviv A. Rise in insulin resistance is associated with escalated telomere attrition. Circulation 2005;111:2171-7.
16. Kark JD, Goldberger N, Kimura M, Sinnreich R, Aviv A. Energy intake and leukocyte telomere length in young adults. Am J Clin Nutr 2012;95:479-87.
17. Cherkas LF, Hunkin JL, Kato BS, Richards JB, Gardner JP, Surdulescu GL, Kimura M, Lu X, Spector TD, Aviv A. The association between physical activity in leisure time and leukocyte telomere length. Arch Intern Med 2008;168:154-8.
18. Werner C, Fürster T, Widmann T, Pöss J, Roggia C, Hanhoun M, Scharhag J, Büchner N, Meyer T, Kindermann W, Haendeler J, Böhm M, Laufs U. Physical exercise prevents cellular senescence in circulating leukocytes and in the vessel wall. Circulation 2009;120:2438-47.
19. Levy D, Neuhausen SL, Hunt SC, Kimura M, Hwang SJ, Chen W, Bis JC, Fitzpatrick AL, Smith E, Johnson AD, Gardner JP, Srinivasan SR, Schork N, Rotter JI, Herbig U, Psaty BM, Sastrasinh M, Murray SS, Vasan RS, Province MA, Glazer NL, Lu X, Cao X, Kronmal R, Mangino M, Soranzo N, Spector TD, Berenson GS, Aviv A. Genome-wide association identifies OBFC1 as a locus involved in human leukocyte telomere biology. Proc Nat Acad Sci 2010;107:9293-8.
20. Codd V, Mangino M, van der Harst P, Braund PS, Kaiser M, Beveridge AJ, Rafelt S, Moore J, Nelson C, Soranzo N, Zhai G, Valdes AM, Blackburn H, Mateo Leach I, de Boer RA, Kimura M, Aviv A; Wellcome Trust Case Control Consortium, Goodall AH, Ouwehand W, van Veldhuisen DJ, van Gilst WH, Navis G, Burton PR, Tobin MD, Hall AS, Thompson JR, Spector T, Samani NJ. Common variants near TERC are associated with mean telomere length. Nat Genet 2010;42:197-9.
21. Mangino M, Hwang SJ, Spector TD, Hunt SC, Kimura M, Fitzpatrick AL, Christiansen L, Petersen I, Elbers CC, Harris T, Chen W, Srinivasan SR, Kark JD, Benetos A, El Shamieh S, Visvikis-Siest S, Christensen K, Berenson GS, Valdes AM, Viñuela A, Garcia M, Arnett DK, Broeckel U, Province MA, Pankow JS, Kammerer C, Liu Y, Nalls M, Tishkoff S, Thomas F, Ziv E, Psaty BM, Bis JC, Rotter JI, Taylor KD, Smith E, Schork NJ, Levy D, Aviv A. Genome-wide meta-analysis points to CTC1 and ZNF676 as genes regulating telomere homeostasis in humans. Hum Mol Genet 2012;21:5385-94.
22. Codd V, Nelson CP, Albrecht E, Mangino M, Deelen J, Buxton JL, Hottenga JJ, Fischer K, Esko T, Surakka I, Broer L, Nyholt DR, Mateo Leach I, Salo P, Hägg S, Matthews MK, Palmen J, Norata GD, O'Reilly PF, Saleheen D, Amin N, Balmforth AJ, Beekman M, de Boer RA, Böhringer S, Braund PS, Burton PR, de Craen AJ, Denniff M, Dong Y, Douroudis K, Dubinina E, Eriksson JG, Garlaschelli K, Guo D, Hartikainen AL, Henders AK, Houwing-Duistermaat JJ, Kananen L, Karssen LC, Kettunen J, Klopp N, Lagou V, van Leeuwen EM, Madden PA, Mägi R, Magnusson PK, Männistö S, McCarthy MI, Medland SE, Mihailov E, Montgomery GW, Oostra BA, Palotie A, Peters A, Pollard H, Pouta A, Prokopenko I, Ripatti S, Salomaa V, Suchiman HE, Valdes AM, Verweij N, Viñuela A, Wang X, Wichmann HE, Widen E, Willemsen G, Wright MJ, Xia K, Xiao X, van Veldhuisen DJ, Catapano AL, Tobin MD, Hall AS, Blakemore AI, van Gilst WH, Zhu H, Consortium C, Erdmann J, Reilly MP, Kathiresan S, Schunkert H, Talmud PJ, Pedersen NL, Perola M, Ouwehand W, Kaprio J, Martin NG, van Duijn CM, Hovatta I, Gieger C, Metspalu A, Boomsma DI, Jarvelin MR, Slagboom PE, Thompson JR, Spector TD, van der Harst P, Samani NJ. Identification of seven loci affecting mean telomere length and their association with disease. Nat Genet 2012;45:422-7.
23. Aubert G, Baerlocher GM, Vulto I, Poon SS, Lansdorp PM. Collapse of telomere homeostasis in hematopoietic cells caused by heterozygous mutations in telomerase genes. PLoS Genet 2012;8:e1002696.
24. Sidorov I, Kimura M, Yashin A, Aviv A. Leukocyte telomere dynamics and human hematopoietic stem cell kinetics during somatic growth. Exp Hematol 2009;37:514-24.
25. Kimura M, Gazitt Y, Cao X, Zhao X, Lansdorp PM, Aviv A. Synchrony of telomere length among hematopoietic cells. Exp Hematol 2010;38:854-9.
26. Shepherd BE, Guttorp P, Lansdorp PM, Abkowitz JL. Estimating human hematopoietic stem cell kinetics using granulocyte telomere lengths. Exp Hematol 2004;32:1040-50.
27. Daniali L, Benetos A, Susser E, Kark JD, Labat C, Kimura M, Desai K, Granick M, Aviv A. Telomeres shorten at equivalent rates in somatic tissues of adults. Nat Commun 2013;4:1597.
28. Yui J, Chiu CP, Lansdorp PM. Telomerase activity in candidate stem cells from fetal liver and adult bone marrow. Blood 1998;91:3255-62.
29. Chiu CP, Dragowska W, Kim NW, Vaziri H, Yui J, Thomas TE, Harley CB, Lansdorp PM. Differential expression of telomerase activity in hematopoietic progenitors from adult human bone marrow. Stem Cells 1996;14:239-48.
30. Morrison SJ, Prowse KR, Ho P, Weissman IL. Telomerase activity in hematopoietic cells is associated with self-renewal potential. Immunity 1996;5:207-521.
31. Kimura M, Hjelmborg JV, Gardner JP, Bathum L, Brimacombe M, Lu X, Christiansen L, Vaupel JW, Aviv A, Christensen K. Telomere length and mortality: a study of leukocytes in elderly Danish twins. Am J Epidemiol 2008;167:799-806.
32. Bakaysa SL, Mucci LA, Slagboom PE, Boomsma DI, McClearn GE, Johansson B, Pedersen NL. Telomere length predicts survival independent of genetic influences. Aging Cell 2007;6:769-74.
33. 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;361:393-5.
34. Deelen J, Beekman M, Codd V, Trompet S, Broer L, Hägg S, Fischer K, Thijssen PE, Suchiman HE, Postmus I, Uitterlinden AG, Hofman A, de Craen AJ, Metspalu A, Pedersen NL, van Duijn CM, Jukema JW, Houwing-Duistermaat JJ, Samani NJ, Slagboom PE. Leukocyte telomere length associates with prospective mortality independent of immune-related parameters and known genetic markers. Int J Epidemiol 2014;43:878-86.
35. Aviv A. Genetics of leukocyte telomere length and its role in atherosclerosis. Mutat Res 2012;730:68-74.
36. Schousboe K, Visscher PM, Henriksen JE, Hopper JL, Sorensen TI, Kyvik KO. Twin study of genetic and environmental influences on glucose tolerance and indices of insulin sensitivity and secretion. Diabetologia 2003;46:1276-83.
37. Benyamin B, Sørensen TI, Schousboe K, Fenger M, Visscher PM, Kyvik KO. Are there common genetic and environmental factors behind the endophenotypes associated with the metabolic syndrome? Diabetologia 2007;50:1880-8.
38. Kimura M, Stone RC, Hunt SC, Skurnick J, Lu X, Cao X, Harley CB, Aviv A. Measurement of telomere length by the Southern blot analysis of terminal restriction fragment lengths. Nat Protoc 2010;5:596-607.
39. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988;16:1215.
40. Steenstrup T, Hjelmborg JV, Mortensen LH, Kimura M, Christensen K, Aviv A. Leukocyte telomere dynamics in the elderly. Eur J Epidemiol 2013;28:181-7.
41. Neale MC, Cardon LR. Methodology for genetic studies of twins and families. Dordrecht: Kluwer Academic Publishers, 1992.
42. Sham P. Statistics in human genetics. Chichester: John Wiley & Sons Ltd., 1998.
43. Okuda K, Bardeguez A, Gardner JP, Rodriguez P, Ganesh V, Kimura M, Skurnick J, Awad G, Aviv A. Telomere length in the newborn. Pediatr Res 2002;52:377-81.
44. Akkad A, Hastings R, Konje JC, Bell SC, Thurston H, Williams B. Telomere length in small-for-gestational-age babies. BJOG 2006;113:318-23.
45. Benetos A, Kark JD, Susser E, Kimura M, Sinnreich R, Chen W, Steenstrup T, Christensen K, Herbig U, von Bornemann Hjelmborg J, Srinivasan SR, Berenson GS, Labat C, Aviv A. Tracking and fixed ranking of leukocyte telomere length across the adult life course. Aging Cell 2013;12:615-21.
46. Benetos A, Dalgård C, Labat C, Kark JD, Verhulst S, Christensen K, Kimura M, Horvath K, Kyvik KO, Aviv A. Sex difference in leukocyte telomere length is ablated in opposite-sex co-twins. Int J Epidemiol 2014. Published Online First.
47. Cherkas LF, Aviv A, Valdes AM, Hunkin JL, Gardner JP, Surdulescu GL, Kimura M, Spector TD. The effects of social status on biological aging as measured by white-blood-cell telomere length. Aging Cell 2006;5:361-5.
48. Lin J, Epel E, Blackburn E. Telomeres and lifestyle factors: roles in cellular aging. Mutat Res 2012;730:85-9.
49. Tan Q, Christiansen L, Thomassen M, Kruse TA, Christensen K. Twins for epigenetic studies of human aging and development. Ageing Res Rev 2013;12:182-7.