Chronic exercise modifies age-related telomere dynamics in a tissue-specific fashion

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 67 A, Issue 9, 2012, Pages 911-926

  Ludlow, Andrew T ^a   Witkowski, Sarah ^a,b   Marshall, Mallory R ^a   Wang, Jenny ^a   Lima, Laila C J ^a,c   Guth, Lisa M ^a   Spangenburg, Espen E ^a   Roth, Stephen M ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c UNIVERSIDADE CATÓLICA DE BRASÍLIA   (Brazil)

Author keywords

Aging; Cast Ei mice; Shelterin; Telomerase; Telomere length

Indexed keywords

ANIMALIA; MUS;

PRIMER DNA; TELOMERASE; TELOMERIC REPEAT BINDING FACTOR 1;

AGING; ANIMAL; ARTICLE; DNA REPAIR; EXERCISE; FEMALE; GENE EXPRESSION; GENETICS; HEART MUSCLE; LIVER; MALE; METABOLISM; MOUSE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SKELETAL MUSCLE; TELOMERE SHORTENING; TISSUE DISTRIBUTION;

AGING; ANIMALS; BASE SEQUENCE; DNA PRIMERS; DNA REPAIR; FEMALE; GENE EXPRESSION; LIVER; MALE; MICE; MUSCLE, SKELETAL; MYOCARDIUM; PHYSICAL EXERTION; TELOMERASE; TELOMERE SHORTENING; TELOMERIC REPEAT BINDING PROTEIN 1; TISSUE DISTRIBUTION;

EID: 84865738522     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/gls002     Document Type: Article

References (55)

1. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 2005; 19: 2100-2110.
2. Oh H, Taffet GE, Youker KA, et al. Telomerase reverse transcriptase promotes cardiac muscle cell proliferation, hypertrophy, and survival. Proc Natl Acad Sci USA. 2001; 98: 10308-10313.
3. Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature. 1990; 345: 458-460.
4. Shay JW, Wright WE. Senescence and immortalization: role of telomeres and telomerase. Carcinogenesis. 2005; 26: 867-874.
5. Greider CW, Blackburn EH. Tracking telomerase. Cell. 2004; 116: S83-S86, 81 p following S86.
6. Ludlow AT, Roth SM. Physical activity and telomere biology: exploring the link with aging-related disease prevention. J Aging Res. 2011; 2011: 790378.
7. 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.
8. Ludlow AT, Zimmerman JB, Witkowski S, Hearn JW, Hatfi eld BD, Roth SM. Relationship between physical activity level, telomere length, and telomerase activity. Med Sci Sports Exerc. 2008; 40: 1764-1771.
9. Werner C, Furster T, Widmann T, et al. Physical exercise prevents cellular senescence in circulating leukocytes and in the vessel wall. Circulation. 2009; 120: 2438-2447.
10. Werner C, Hanhoun M, Widmann T, et al. Effects of physical exercise on myocardial telomere-regulating proteins, survival pathways, and apoptosis. J Am Coll Cardiol. 2008; 52: 470-482.
11. Holloszy JO. Exercise and longevity: studies on rats. J Gerontol. 1988; 43: B149-B151.
12. Navarro A, Gomez C, Lopez-Cepero JM, Boveris A. Benefi cial effects of moderate exercise on mice aging: survival, behavior, oxidative stress, and mitochondrial electron transfer. Am J Physiol Regul Integr Comp Physiol. 2004; 286: R505-R511.
13. Blair SN, Kohl HW 3rd, Paffenbarger RS Jr, Clark DG, Cooper KH, Gibbons LW. Physical fitness and all-cause mortality. A prospective study of healthy men and women. JAMA. 1989; 262: 2395-2401.
14. Cherkas LF, Aviv A, Valdes AM, et al. The effects of social status on biological aging as measured by white-blood-cell telomere length. Aging Cell. 2006; 5: 361-365.
15. LaRocca TJ, Seals DR, Pierce GL. Leukocyte telomere length is preserved with aging in endurance exercise-trained adults and related to maximal aerobic capacity. Mech Ageing Dev. 2010; 131: 165-167.
16. Ponsot E, Lexell J, Kadi F. Skeletal muscle telomere length is not impaired in healthy physically active old women and men. Muscle Nerve. 2008; 37: 467-472.
17. Collins M, Renault V, Grobler LA, et al. Athletes with exerciseassociated fatigue have abnormally short muscle DNA telomeres. Med Sci Sports Exerc. 2003; 35: 1524-1528.
18. Rae DE, Vignaud A, Butler-Browne GS, et al. Skeletal muscle telomere length in healthy, experienced, endurance runners. Eur J Appl Physiol. 2010; 109: 323-330.
19. Cooke HJ, Smith BA. Variability at the telomeres of the human X/Y pseudoautosomal region. Cold Spring Harb Symp Quant Biol. 1986; 51 (Pt 1): 213-219.
20. de Lange T. How shelterin solves the telomere end-protection problem. Cold Spring Harb Symp Quant Biol. 2010; 75: 167-177.
21. Palm W, de Lange T. How shelterin protects mammalian telomeres. Annu Rev Genet. 2008; 42: 301-334.
22. Smogorzewska A, van Steensel B, Bianchi A, et al. Control of human telomere length by TRF1 and TRF2. Mol Cell Biol. 2000; 20: 1659-1668.
23. Nojima H. Protein kinases that regulate chromosome stability and their downstream targets. Genome Dyn. 2006; 1: 131-148.
24. Wang Y, Ghosh G, Hendrickson EA. Ku86 represses lethal telomere deletion events in human somatic cells. Proc Natl Acad Sci USA. 2009; 106: 12430-12435.
25. Hemann MT, Greider CW. Wild-derived inbred mouse strains have short telomeres. Nucleic Acids Res. 2000; 28: 4474-4478.
26. Callicott RJ, Womack JE. Real-time PCR assay for measurement of mouse telomeres. Comp Med. 2006; 56: 17-22.
27. Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res. 2002; 30: e47.
28. 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.
29. Ponsot E, Kadi F. Signal modelization for improved precision of assessment of minimum and mean telomere lengths. Electrophoresis. 2008; 29: 542-544.
30. Wright WE, Shay JW, Piatyszek MA. Modifi cations of a telomeric repeat amplifi cation protocol (TRAP) result in increased reliability, linearity and sensitivity. Nucleic Acids Res. 1995; 23: 3794-3795.
31. Cattan V, Mercier N, Gardner JP, et al. Chronic oxidative stress induces a tissue-specifi c reduction in telomere length in CAST/Ei mice. Free Radic Biol Med. 2008; 44: 1592-1598.
32. Wu H, Rothermel B, Kanatous S, et al. Activation of MEF2 by muscle activity is mediated through a calcineurin-dependent pathway. EMBO J. 2001; 20: 6414-6423.
33. Martinez P, Blasco MA. Role of shelterin in cancer and aging. Aging Cell. 2010; 9: 653-666.
34. Samper E, Goytisolo FA, Slijepcevic P, van Buul PP, Blasco MA. Mammalian Ku86 protein prevents telomeric fusions independently of the length of TTAGGG repeats and the G-strand overhang. EMBO Rep. 2000; 1: 244-252.
35. 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.
36. Cherif H, Tarry JL, Ozanne SE, Hales CN. Ageing and telomeres: a study into organ-and gender-specifi c telomere shortening. Nucleic Acids Res. 2003; 31: 1576-1583.
37. Hastings R, Li NC, Lacy PS, et al. Rapid telomere attrition in cardiac tissue of the ageing Wistar rat. Experimental gerontology. 2004; 39: 855-857.
38. Levy MZ, Allsopp RC, Futcher AB, Greider CW, Harley CB. Telomere end-replication problem and cell aging. J Mol Biol. 1992; 225: 951-960.
39. 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.
40. Kajstura J, Pertoldi B, Leri A, et al. Telomere shortening is an in vivo marker of myocyte replication and aging. Am J Pathol. 2000; 156: 813-819.
41. Decary S, Mouly V, Hamida CB, Sautet A, Barbet JP, Butler-Browne GS. Replicative potential and telomere length in human skeletal muscle: implications for satellite cell-mediated gene therapy. Hum Gene Ther. 1997; 8: 1429-1438.
42. Renault V, Thornell LE, Eriksson PO, Butler-Browne G, Mouly V. Regenerative potential of human skeletal muscle during aging. Aging Cell. 2002; 1: 132-139.
43. Kawanishi S, Oikawa S. Mechanism of telomere shortening by oxidative stress. Ann N Y Acad Sci. 2004; 1019: 278-284.
44. 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.
45. Limon-Pacheco J, Gonsebatt ME. The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress. Mutat Res. 2009; 674: 137-147.
46. Radak Z, Taylor AW, Sasvari M, et al. Telomerase activity is not altered by regular strenuous exercise in skeletal muscle or by sarcoma in liver of rats. Redox Rep. 2001; 6: 99-103.
47. Nozawa K, Maehara K, Isobe K. Mechanism for the reduction of telomerase expression during muscle cell differentiation. J Biol Chem. 2001; 276: 22016-22023.
48. Wernig A, Schafer R, Knauf U, et al. On the regenerative capacity of human skeletal muscle. Artif Organs. 2005; 29: 192-198.
49. Yi X, Shay JW, Wright WE. Quantitation of telomerase components and hTERT mRNA splicing patterns in immortal human cells. Nucleic Acids Res. 2001; 29: 4818-4825.
50. Ahmed S, Passos JF, Birket MJ, et al. Telomerase does not counteract telomere shortening but protects mitochondrial function under oxidative stress. J Cell Sci. 2008; 121: 1046-1053.
51. Buchner N, Zschauer TC, Lukosz M, Altschmied J, Haendeler J. Downregulation of mitochondrial telomerase reverse transcriptase induced by H2O2 is Src kinase dependent. Exp Gerontol. 2010; 45: 558-562.
52. Holloszy JO. Regulation by exercise of skeletal muscle content of mitochondria and GLUT4. J Physiol Pharmacol. 2008; 59 (suppl 7): 5-18.
53. Anversa P, Nadal-Ginard B. Myocyte renewal and ventricular remodelling . Nature. 2002; 415: 240-243.
54. Kim YH, Heo JS, Han HJ. High glucose increase cell cycle regulatory proteins level of mouse embryonic stem cells via PI3-K/Akt and MAPKs signal pathways. J Cell Physiol. 2006; 209: 94-102.
55. Mehrabian M, Allayee H, Wong J, et al. Identifi cation of 5-lipoxygenase as a major gene contributing to atherosclerosis susceptibility in mice. Circ Res. 2002; 91: 120-126.