Telomeres shorten in response to oxidative stress in mouse skeletal muscle fibers

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 69, Issue 7, 2014, Pages 821-830

  Ludlow, Andrew T ^a   Spangenburg, Espen E ^a   Chin, Eva R ^a   Cheng, Wen Hsing ^b,c   Roth, Stephen M ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

Low oxygen tissue culture; Oxidative stress; Skeletal muscle fibers; Telomere length; Telomere binding proteins

Indexed keywords

HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; TELOMERASE; TELOMERE BINDING PROTEIN; TELOMERIC REPEAT BINDING FACTOR 1; TELOMERIC REPEAT BINDING FACTOR 2; TRF2 PROTEIN, MOUSE;

AGING; ANIMAL; ARTICLE; C57BL MOUSE; CELL CULTURE; DNA DAMAGE; DRUG EFFECT; GENETICS; LOW OXYGEN TISSUE CULTURE; MALE; METABOLISM; MOUSE; OXIDATIVE STRESS; OXIDATIVE STRESS.; SKELETAL MUSCLE; SPECIES DIFFERENCE; TELOMERE LENGTH; TELOMERE SHORTENING;

LOW OXYGEN TISSUE CULTURE; OXIDATIVE STRESS.; SKELETAL MUSCLE FIBERS; TELOMERE LENGTH; TELOMERE-BINDING PROTEINS;

AGING; ANIMALS; CELLS, CULTURED; DNA DAMAGE; HYDROGEN PEROXIDE; MALE; MICE; MICE, INBRED C57BL; MUSCLE FIBERS, SKELETAL; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SPECIES SPECIFICITY; TELOMERASE; TELOMERE SHORTENING; TELOMERIC REPEAT BINDING PROTEIN 1; TELOMERIC REPEAT BINDING PROTEIN 2;

EID: 84902242629     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glt211     Document Type: Article

References (67)

1. Blackburn EH, Greider CW, Szostak JW. Telomeres and telomerase: The path from maize, Tetrahymena and yeast to human cancer and aging. Nat Med. 2006;12:1133-1138. doi:10.1038/nm1006-1133 (Pubitemid 44527346
2. Daniali L, Benetos A, Susser E, et al. Telomeres shorten at equivalent rates in somatic tissues of adults. Nat Commun. 2013;4:1597. doi:10.1038/ncomms2602
3. Gomes NM, Ryder OA, Houck ML, et al. Comparative biology of mammalian telomeres: Hypotheses on ancestral states and the roles of telomeres in longevity determination. Aging Cell. 2011;10:761-768. doi:10.1111/j.1474-9726. 2011.00718.x
4. Shay JW, Wright WE. Senescence and immortalization: Role of telomeres and telomerase. Carcinogenesis. 2005;26:867-874. doi:10.1093/ carcin/bgh296 (Pubitemid 41214314
5. Martinez P, Thanasoula M, Carlos AR, et al. Mammalian Rap1 controls telomere function and gene expression through binding to telomeric and extratelomeric sites. Nat Cell Biol. 2010;12:768-780. doi:10.1038/ncb2081
6. Perrod S, Gasser SM. Long-range silencing and position effects at telomeres and centromeres: Parallels and differences. Cell Mol Life Sci. 2003;60:2303-2318. doi:10.1007/s00018-003-3246-x (Pubitemid 37487252
7. Stadler G, Rahimov F, King OD, et al. Telomere position effect regulates DUX4 in human facioscapulohumeral muscular dystrophy. Nat Struct Mol Biol. 2013;20:671-678. doi:10.1038/nsmb.2571
8. Greider CW. Telomeres, telomerase and senescence. Bioessays. 1990;12:363-369. doi:10.1002/bies.950120803 (Pubitemid 120034478
9. Greider CW. Telomerase RNA levels limit the telomere length equilibrium. Cold Spring Harb Symp Quant Biol. 2006;71:225-229. doi:10.1101/sqb.2006.71.063
10. Lee HW, Blasco MA, Gottlieb GJ, Horner JW 2nd, Greider CW, DePinho RA. Essential role of mouse telomerase in highly proliferative organs. Nature. 1998;392:569-574. doi:10.1038/33345 (Pubitemid 28207706
11. Levy MZ, Allsopp RC, Futcher AB, Greider CW, Harley CB. Telomere end-replication problem and cell aging. J Mol Biol. 1992;225:951-960. doi:10.1016/0022-2836(92)90096-3
12. Ludlow AT, Roth SM. Physical activity and telomere biology: Exploring the link with aging-related disease prevention. J Aging Res. 2011;2011:790378. doi:10.4061/2011/790378
13. van der Harst P, van der Steege G, de Boer RA, et al.; MERIT-HF Study Group. Telomere length of circulating leukocytes is decreased in patients with chronic heart failure. J Am Coll Cardiol. 2007;49:1459-1464. doi:10.1016/j.jacc.2007.01.027 (Pubitemid 46482923
14. 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. doi:10.1001/archinternmed.2007.39 (Pubitemid 351185881
15. Ludlow AT, Zimmerman JB, Witkowski S, Hearn JW, Hatfield BD, Roth SM. Relationship between physical activity level, telomere length, and telomerase activity. Med Sci Sports Exerc. 2008;40:1764-1771. doi:10.1249/MSS. 0b013e31817c92aa
16. 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. doi:10.1161/CIRCULATIONAHA.109.861005
17. 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. doi:10.1016/j. jacc.2008.04.034
18. Decary S, Hamida CB, Mouly V, Barbet JP, Hentati F, Butler-Browne GS. Shorter telomeres in dystrophic muscle consistent with extensive regeneration in young children. Neuromuscul Disord. 2000;10:113-120. doi:10.1016/S0960-8966(99) 00093-0 (Pubitemid 30050623
19. 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. doi:10.1089/hum.1997.8.12-1429 (Pubitemid 27393998
20. Ludlow AT, Witkowski S, Marshall MR, et al. Chronic exercise modifies age-related telomere dynamics in a tissue-specific fashion. J Gerontol A Biol Sci Med Sci. 2012;67:911-926. doi:10.1093/gerona/gls002
21. Mouly V, Aamiri A, Bigot A, et al. The mitotic clock in skeletal muscle regeneration, disease and cell mediated gene therapy. Acta Physiol Scand. 2005;184:3-15. doi:10.1111/j.1365-201X.2005.01417.x (Pubitemid 40646734
22. Renault V, Thornell LE, Butler-Browne G, Mouly V. Human skeletal muscle satellite cells: Aging, oxidative stress and the mitotic clock. Exp Gerontol. 2002;37:1229-1236. doi:S0531556502001298 [pii]
23. Renault V, Thornell LE, Eriksson PO, Butler-Browne G, Mouly V, Thorne LE. Regenerative potential of human skeletal muscle during aging. Aging Cell. 2002;1:132-139
24. Benetos A, Kimura M, Labat C, et al. A model of canine leukocyte telomere dynamics. Aging Cell. 2011;10:991-995. doi:10.1111/j.1474-9726.2011.00744.x
25. Fano G, Mecocci P, Vecchiet J, et al. Age and sex influence on oxidative damage and functional status in human skeletal muscle. J Muscle Res Cell Motil. 2001;22:345-351. doi:10.1023/A:1013122805060 (Pubitemid 34043033
26. Fulle S, Di Donna S, Puglielli C, et al. Age-dependent imbalance of the antioxidative system in human satellite cells. Exp Gerontol. 2005;40:189-197. doi:10.1016/j.exger.2004.11.006 (Pubitemid 40343010
27. Kawanishi S, Oikawa S. Mechanism of telomere shortening by oxidative stress. Ann N Y Acad Sci. 2004;1019:278-284. doi:10.1196/ annals.1297.047 (Pubitemid 38951320
28. Narciso L, Fortini P, Pajalunga D, et al. Terminally differentiated muscle cells are defective in base excision DNA repair and hypersensitive to oxygen injury. Proc Natl Acad Sci USA. 2007;104:17010-17015. doi:10.1073/pnas.0701743104 (Pubitemid 350210982
29. Oikawa S, Tada-Oikawa S, Kawanishi S. Site-specific DNA damage at the GGG sequence by UVA involves acceleration of telomere shortening. Biochemistry. 2001;40:4763-4768. doi:10.1021/bi002721g (Pubitemid 32374664
30. Rochette PJ, Brash DE. Human telomeres are hypersensitive to UV-induced DNA Damage and refractory to repair. PLoS Genet. 2010;6:e1000926. doi:10.1371/journal.pgen.1000926
31. Bilaud T, Brun C, Ancelin K, Koering CE, Laroche T, Gilson E. Telomeric localization of TRF2, a novel human telobox protein. Nat Genet. 1997;17:236-239. doi:10.1038/ng1097-236
32. de Lange T. How shelterin solves the telomere end-protection problem. Cold Spring Harb Symp Quant Biol. 2010;75:167-177. doi:10.1101/ sqb.2010.75.017
33. de Lange T. Shelterin: The protein complex that shapes and safeguards human telomeres. Genes Dev. 2005;19:2100-2110. doi:10.1101/ gad.1346005 (Pubitemid 41330312
34. Brown LD, Schneider MF. Delayed dedifferentiation and retention of properties in dissociated adult skeletal muscle fibers in vitro. In Vitro Cell Dev Biol Anim. 2002;38:411-422. doi:10.1290/1071-2690(2002)038<0411: DDAROP>2.0.CO;2 (Pubitemid 36150678
35. Chakravarthy MV, Spangenburg EE, Booth FW. Culture in low levels of oxygen enhances in vitro proliferation potential of satellite cells from old skeletal muscles. Cell Mol Life Sci. 2001;58:1150-1158. (Pubitemid 32756525
36. Richardson RS, Noyszewski EA, Leigh JS, Wagner PD. Lactate efflux from exercising human skeletal muscle: Role of intracellular PO2. J Appl Physiol. 1998;85:627-634. doi:10.1113/jphysiol.2005.102327 (Pubitemid 28365832
37. Wright WE, Shay JW. Inexpensive low-oxygen incubators. Nat Protoc. 2006;1:2088-2090. doi:10.1038/nprot.2006.374 (Pubitemid 46773331
38. Palomero J, Pye D, Kabayo T, Spiller DG, Jackson MJ. In situ detection and measurement of intracellular reactive oxygen species in single isolated mature skeletal muscle fibers by real time fluorescence microscopy. Antioxid Redox Signal. 2008;10:1463-1474. doi:10.1089/ ars.2007.2009
39. Brandl A, Meyer M, Bechmann V, Nerlich M, Angele P. Oxidative stress induces senescence in human mesenchymal stem cells. Exp Cell Res. 2011;317:1541-1547. doi:10.1016/j.yexcr.2011.02.015
40. Ludlow AT, Lima LC, Wang J, et al. Exercise alters mRNA expression of telomere-repeat binding factor 1 in skeletal muscle via p38 MAPK. J Appl Physiol. 2012;113:1737-1746. doi:10.1152/ japplphysiol.00200.2012
41. Rasband WS. ImageJ. U. S. National Institutes of Health 1997-2011. Retrieved from http://imagej.nih.gov/ij/.
42. Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res. 2002;30:e47. doi:10.1093/nar/30.10.e47
43. Parrinello S, Samper E, Krtolica A, Goldstein J, Melov S, Campisi J. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat Cell Biol. 2003;5:741-747. doi:10.1038/ncb1024 (Pubitemid 36986782
44. Greider CW. Telomeres do D-loop-T-loop. Cell. 1999;97:419-422. doi:10.1016/S0092-8674(00)80750-3 (Pubitemid 29231163
45. Griffith JD, Comeau L, Rosenfield S, et al. Mammalian telomeres end in a large duplex loop. Cell. 1999;97:503-514. doi:10.1016/ S0092-8674(00)80760-6
46. Nandakumar J, Cech TR. Finding the end: Recruitment of telomerase to telomeres. Nat Rev Mol Cell Biol. 2013;14:69-82. doi:10.1038/ nrm3505
47. McKerlie M, Zhu XD. Cyclin B-dependent kinase 1 regulates human TRF1 to modulate the resolution of sister telomeres. Nat Commun. 2011;2:371. doi:10.1038/ncomms1372
48. Munoz P, Blanco R, Flores JM, Blasco MA. XPF nuclease-dependent telomere loss and increased DNA damage in mice overexpressing TRF2 result in premature aging and cancer. Nat Genet. 2005;37:1063-1071. doi:10.1038/ng1633 (Pubitemid 41486658
49. 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. doi:10.1128/MCB.20.5.1659-1668.2000 (Pubitemid 30100185
50. Hemann MT, Greider CW. Wild-derived inbred mouse strains have short telomeres. Nucleic Acids Res. 2000;28:4474-4478. doi:10.1093/ nar/28.22.4474
51. Prowse KR, Greider CW. Developmental and tissue-specific regulation of mouse telomerase and telomere length. Proc Natl Acad Sci USA. 1995;92:4818-4822. doi:10.1073/pnas.92.11.4818
52. Sahin E, Depinho RA. Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature. 2010;464:520-528. doi:10.1038/nature08982
53. 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. doi:10.1007/s00421-010-1353-6
54. Kadi F, Ponsot E. The biology of satellite cells and telomeres in human skeletal muscle: Effects of aging and physical activity. Scand J Med Sci Sports. 2010;20:39-48. doi:10.1111/j.1600-0838.2009.00966.x
55. Ponsot E, Echaniz-Laguna A, Delis AM, Kadi F. Telomere length and regulatory proteins in human skeletal muscle with and without ongoing regenerative cycles. Exp Physiol. 2012;97:774-784. doi:10.1113/ expphysiol.2011.063818
56. Makpol S, Zainuddin A, Rahim NA, Yusof YA, Ngah WZ. Alphatocopherol modulates hydrogen peroxide-induced DNA damage and telomere shortening of human skin fibroblasts derived from differently aged individuals. Planta Med. 2010;76:869-875. doi:10.1055/s-0029-1240812
57. Richter T, von Zglinicki T. A continuous correlation between oxidative stress and telomere shortening in fibroblasts. Exp Gerontol. 2007;42:1039-1042. doi:10.1016/j.exger.2007.08.005 (Pubitemid 47633455
58. Mehrabian M, Allayee H, Wong J, et al. Identification of 5-lipoxygenase as a major gene contributing to atherosclerosis susceptibility in mice. Circ Res. 2002;91:120-126. doi:10.1161/ 01.RES.0000028008.99774.7F (Pubitemid 34827222
59. Keane TM, Goodstadt L, Danecek P, et al. Mouse genomic variation and its effect on phenotypes and gene regulation. Nature. 2011;477:289-294. doi:10.1038/nature10413
60. 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. doi:10.1016/j.exger. 2010.03.003
61. Haendeler J, Drose S, Buchner N, et al. Mitochondrial telomerase reverse transcriptase binds to and protects mitochondrial DNA and function from damage. Arterioscler Thromb Vasc Biol. 2009;29:929-935. doi:10.1161/ATVBAHA.109.185546
62. Haendeler J, Hoffmann J, Diehl JF, et al. Antioxidants inhibit nuclear export of telomerase reverse transcriptase and delay replicative senescence of endothelial cells. Circ Res. 2004;94:768-775. doi:10.1161/ 01.RES.0000121104. 05977.F3 (Pubitemid 38451738
63. Strong MA, Vidal-Cardenas SL, Karim B, Yu H, Guo N, Greider CW. Phenotypes in mTERT+/- and mTERT-/- mice are due to short telomeres, not telomere-independent functions of telomerase reverse transcriptase. Mol Cell Biol. 2011;31:2369-2379. doi:10.1128/MCB.05312-11
64. Cattan V, Mercier N, Gardner JP, et al. Chronic oxidative stress induces a tissue-specific reduction in telomere length in CAST/ Ei mice. Free Radic Biol Med. 2008;44:1592-1598. doi:10.1016/j. freeradbiomed.2008.01.007
65. Spallarossa P, Altieri P, Aloi C, et al. Doxorubicin induces senescence or apoptosis in rat neonatal cardiomyocytes by regulating the expression levels of the telomere binding factors 1 and 2. Am J Physiol Heart Circ Physiol. 2009;297:H2169-H2181. doi:10.1152/ ajpheart.00068.2009
66. Zhang Y, Cao EH, Qin JF. Up-regulation of telomere-binding TRF1, TRF2 related to reactive oxygen species induced by As(2)O(3) in MGC-803 cells. Eur J Pharmacol. 2005;516:1-9. doi:10.1016/j. ejphar.2005.04.022
67. Aguennouz M, Vita GL, Messina S, et al. Telomere shortening is associated to TRF1 and PARP1 overexpression in Duchenne muscular dystrophy. Neurobiol Aging. 2011;32:2190-2197. doi:10.1016/j. neurobiolaging.2010.01.008.