Neurobiology of Aging
Volume 32, Issue 12 , Pages 2190-2197 , December 2011

Telomere shortening is associated to TRF1 and PARP1 overexpression in Duchenne muscular dystrophy

  • M’Hammed Aguennouz

      Affiliations

    • Department of Neurosciences, Psychiatry and Anaesthesiology, University of Messina, AOU Policlinico, Messina 98125, Italy
    • Both authors equally contributed to this study.
  • ,
  • Gian Luca Vita

      Affiliations

    • Department of Neurosciences, Psychiatry and Anaesthesiology, University of Messina, AOU Policlinico, Messina 98125, Italy
    • Both authors equally contributed to this study.
  • ,
  • Sonia Messina

      Affiliations

    • Department of Neurosciences, Psychiatry and Anaesthesiology, University of Messina, AOU Policlinico, Messina 98125, Italy
  • ,
  • Annamaria Cama

      Affiliations

    • Department of Neurosciences, Psychiatry and Anaesthesiology, University of Messina, AOU Policlinico, Messina 98125, Italy
  • ,
  • Natalia Lanzano

      Affiliations

    • Department of Neurosciences, Psychiatry and Anaesthesiology, University of Messina, AOU Policlinico, Messina 98125, Italy
  • ,
  • Annamaria Ciranni

      Affiliations

    • Department of Neurosciences, Psychiatry and Anaesthesiology, University of Messina, AOU Policlinico, Messina 98125, Italy
  • ,
  • Carmelo Rodolico

      Affiliations

    • Department of Neurosciences, Psychiatry and Anaesthesiology, University of Messina, AOU Policlinico, Messina 98125, Italy
  • ,
  • Rosa Maria Di Giorgio

      Affiliations

    • Department of Biochemical, Physiological and Nutritional Sciences, University of Messina, AOU Policlinico, Messina 98125, Italy
  • ,
  • Giuseppe Vita

      Affiliations

    • Department of Neurosciences, Psychiatry and Anaesthesiology, University of Messina, AOU Policlinico, Messina 98125, Italy
    • Corresponding Author InformationCorresponding author. Unit of Neurology and Neuromuscular Diseases, AOU Policlinico, Via Consolare Valeria 1, 98125 Messina, Italy. Tel.: +39 090 2212793; fax: +39 090 2212789.

Received 23 July 2009 ,Revised 30 October 2009 ,Accepted 14 January 2010.

References 

  1. Aguilar-Quesada R, Muñoz-Gámez JA, Martín-Oliva D, Peralta-Leal A, Quiles-Pérez R, Rodríguez-Vargas JM, et al. Modulation of transcription by PARP-1: consequences in carcinogenesis and inflammation. Curr. Med. Chem. 2007;14:1179–1187
  2. Bellon M, Datta A, Brown M, Pouliquen JF, Couppie P, Kazanji M, et al. Increased expression of telomere length regulating factors TRF1, TRF2 and TIN2 in patients with adult T-cell leukemia. Int. J. Cancer. 2006;119:2090–2097
  3. Benetos A, Gardner JP, Zureik M, Labat C, Xiaobin L, Adamopoulos C, et al. Short telomeres are associated with increased carotid atherosclerosis in hypertensive subjects. Hypertension. 2004;43:182–185
  4. Blasco MA. Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 2005;6:611–622
  5. Brouilette S, Singh RK, Thompson JR, Goodall AH, Samani NJ. White cell telomere length and risk of premature myocardial infarction. Arterioscler. Thromb. Vasc. Biol. 2003;23:842–846
  6. Cong YS, Wright WE, Shay JW. Human telomerase and its regulation. Microbiol. Mol. Biol. Rev. 2002;66:407–425
  7. Cook BD, Dynek JN, Chang W, Shostak G, Smith S. Role for the related poly(ADP-Ribose) polymerases tankyrase 1 and 2 at human telomeres. Mol. Cell. Biol. 2002;22:332–342
  8. Dantzer F, Giraud-Panis MJ, Jaco I, Amé JC, Schultz I, Blasco M, et al. Functional interaction between poly(ADP-Ribose) polymerase 2 (PARP-2) and TRF2: PARP activity negatively regulates TRF2. Mol. Cell. Biol. 2004;24:1595–1607
  9. De Boeck G, Forsyth RG, Praet M, Hogendoorn PC. Telomere-associated proteins: cross-talk between telomere maintenance and telomere-lengthening mechanisms. J. Pathol. 2009;217:327–344
  10. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 2005;19:2100–2110
  11. 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
  12. 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
  13. Di Donna S, Mamchaoui K, Cooper RN, Seigneurin-Venin S, Tremblay J, Butler-Browne GS, et al. Telomerase can extend the proliferative capacity of human myoblasts, but does not lead to their immortalization. Mol. Cancer Res. 2003;1:643–653
  14. Dubowitz V, Sewry CA. Muscle Biopsy. third ed.. Edinburgh: Saunders Elsevier; 2007;
  15. Flores I, Benetti R, Blasco MA. Telomerase regulation and stem cell behaviour. Curr. Opin. Cell. Biol. 2006;18:254–260
  16. García S, Bodaño A, González A, Forteza J, Gómez-Reino JJ, Conde C. Partial protection against collagen antibody-induced arthritis in PARP-1 deficient mice. Arthritis Res. Ther. 2006;8:R14
  17. García S, Bodaño A, Pablos JL, Gómez-Reino JJ, Conde C. Poly(ADP-ribose) polymerase inhibition reduces tumor necrosis factor-induced inflammatory response in rheumatoid synovial fibroblasts. Ann. Rheum. Dis. 2008;67:631–637
  18. Ghaffari SH, Shayan-Asl N, Jamialahmadi AH, Alimoghaddam K, Ghavamzadeh A. Telomerase activity and telomere length in patients with acute promyelocytic leukemia: indicative of proliferative activity, disease progression, and overall survival. Ann. Oncol. 2008;19:1927–1934
  19. Hansson M, Zendehrokh N, Ohyashiki J, Ohyashiki K, Westman UB, Roos G, et al. Telomerase activity in effusions: a comparison between telomere repeat amplification protocol in situ and conventional telomere repeat amplification protocol assay. Arch. Pathol. Lab. Med. 2008;132:1896–1902
  20. Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature. 1990;345:458–460
  21. Hashimoto Y, Murakami Y, Uemura K, Hayashidani Y, Sudo T, Ohge H, et al. Detection of human telomerase reverse transcriptase (hTERT) expression in tissue and pancreatic juice from pancreatic cancer. Surgery. 2008;143:113–125
  22. Hnia K, Gayraud J, Hugon G, Ramonatxo M, De La Porte S, Matecki S, et al. L-arginine decreases inflammation and modulates the nuclear factor-kappaB/matrix metalloproteinase cascade in mdx muscle fibers. Am. J. Pathol. 2008;172:1509–1519
  23. Honig LS, Schupf N, Lee JH, Tang MX, Mayeux R. Shorter telomeres are associated with mortality in those with APOE epsilon4 and dementia. Ann. Neurol. 2006;60:181–187
  24. 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. 2009;(September):[Epub ahead of print]
  25. Kim NW. Clinical implications of telomerase in cancer. Eur. J. Cancer. 1997;33:781–786
  26. Kim MK, Kang MR, Nam HW, Bae YS, Kim YS, Chung IK. Regulation of telomeric repeat binding factor 1 binding to telomeres by casein kinase 2-mediated phosphorylation. J. Biol. Chem. 2008;283:14144–14152
  27. Lord CJ, Ashworth A. Targeted therapy for cancer using PARP inhibitors. Curr. Opin. Pharmacol. 2008;8:363–369
  28. Lund TC, Grange RW, Lowe DA. Telomere shortening in diaphragm and tibialis anterior muscles of aged mdx mice. Muscle Nerve. 2007;36:387–390
  29. 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;60:174–180
  30. Mazzorana M, Pinna LA, Battistutta R. A structural insight into CK2 inhibition. Mol. Cell. Biochem. 2008;316:57–62
  31. Messina S, Altavilla D, Aguennouz M, Seminara P, Minutoli L, Monici MC, et al. Lipid peroxidation inhibition blunts nuclear factor-κB activation, reduces skeletal muscle degeneration, and enhances muscle function in mdx mice. Am. J. Pathol. 2006;168:918–926
  32. Messina S, Bitto A, Aguennouz M, Minutoli L, Monici MC, Altavilla D, et al. Nuclear factor kappa-B blockade reduces skeletal muscle degeneration and enhances muscle function in mdx mice. Exp. Neurol. 2006;198:234–241
  33. Messina S, Mazzeo A, Bitto A, Aguennouz M, Migliorato A, De Pasquale MG, et al. VEGF overexpression via adeno-associated virus gene transfer promotes skeletal muscle regeneration and enhances muscle function in mdx mice. FASEB J. 2007;21:3737–3746
  34. Messina S, Bitto A, Aguennouz M, Mazzeo A, Migliorato A, Polito F, et al. Flavocoxid counteracts muscle necrosis and improves functional properties in mdx mice: A comparison study with methylprednisolone. Exp. Neurol. 2009;220:349–358
  35. Morosetti R, Broccolini A, Sancricca C, Gliubizzi C, Gidaro T, Tonali PA, et al. Increased aging in primary muscle cultures of sporadic inclusion-body myositis. Neurobiol. Aging. 2008;
  36. Mota R, Sánchez-Bueno F, Berenguer-Pina JJ, Hernández-Espinosa D, Parrilla P, Yélamos J. Therapeutic treatment with poly(ADP-ribose) polymerase inhibitors attenuates the severity of acute pancreatitis and associated liver and lung injury. Br. J. Pharmacol. 2007;151:998–1005
  37. Muramatsu Y, Ohishi T, Sakamoto M, Tsuruo T, Seimiya H. Cross-species difference in telomeric function of tankyrase 1. Cancer Sci. 2007;98:850–857
  38. Oexle K, Zwirner A, Freudenberg K, Kohlschütter A, Speer A. Examination of telomere lengths in muscle tissue casts doubt on replicative aging as cause of progression in Duchenne muscular dystrophy. Pediatr. Res. 1997;42:226–231
  39. Oh H, Wang SC, Prahash A, Sano M, Moravec CS, Taffet GE, et al. Telomere attrition and Chk2 activation in human heart failure. Proc. Natl. Acad. Sci. U.S.A. 2003;100:5378–5383
  40. Peralta-Leal A, Rodríguez-Vargas JM, Aguilar-Quesada R, Rodríguez MI, Linares JL, de Almodóvar MR, et al. PARP inhibitors: new partners in the therapy of cancer and inflammatory diseases. Free Radic. Biol. Med. 2009;47:13–26
  41. 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
  42. Reddel RR. Alternative lengthening of telomeres, telomerase, and cancer. Cancer Lett. 2003;194:155–162
  43. Rodon J, Iniesta MD, Papadopoulos K. Development of PARP inhibitors in oncology. Expert Opin. Investig. Drugs. 2009;18:31–43
  44. Sánchez-Fidalgo S, Villegas I, Martín A, Sánchez-Hidalgo M, Alarcón de la Lastra C. PARP inhibition reduces acute colonic inflammation in rats. Eur. J. Pharmacol. 2007;563:216–223
  45. Schertzer JD, Gehrig SM, Ryall JG, Lynch GS. Modulation of insulin-like growth factor (IGF)-I and IGF-binding protein interactions enhances skeletal muscle regeneration and ameliorates the dystrophic pathology in mdx mice. Am. J. Pathol. 2007;171:1180–1188
  46. Seigneurin-Venin S, Bernard V, Tremblay JP. Telomerase allows the immortalization of T antigen-positive DMD myoblasts: a new source of cells for gene transfer application. Gene Ther. 2000;7:619–623
  47. Shay JW, Wright WE. Telomeres are double-strand DNA breaks hidden from DNA damage responses. Mol. Cell. 2004;14:420–421
  48. van Steensel B, de Lange T. Control of telomere length by the human telomeric protein TRF1. Nature. 1997;385:740–743
  49. von Zglinicki T. Oxidative stress shortens telomeres. Trends Biochem. Sci. 2002;27:339–344
  50. Webster C, Blau HM. Accelerated age-related decline in replicative life-span of Duchenne muscular dystrophy myoblasts: implications for cell and gene therapy. Somat. Cell. Mol. Genet. 1990;16:557–565
  51. 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
  52. Zhu CH, Mouly V, Cooper RN, Mamchaoui K, Bigot A, Shay JW, et al. Cellular senescence in human myoblasts is overcome by human telomerase reverse transcriptase and cyclin-dependent kinase 4: consequences in aging muscle and therapeutic strategies for muscular dystrophies. Aging Cell. 2007;6:515–523

PII: S0197-4580(10)00038-2

doi: 10.1016/j.neurobiolaging.2010.01.008

Neurobiology of Aging
Volume 32, Issue 12 , Pages 2190-2197 , December 2011