Telomerase Reverse Transcriptase Synergizes with Calorie Restriction to Increase Health Span and Extend Mouse Longevity

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Vera, Elsa ^a   Bernardes de Jesus, Bruno ^a   Foronda, Miguel ^a   Flores, Juana M ^b   Blasco, Maria A ^a  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

TELOMERASE REVERSE TRANSCRIPTASE;

AGING; ANALYSIS OF VARIANCE; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; CALORIC RESTRICTION; CONTROLLED STUDY; DNA DEGRADATION; DNA REPAIR; GENE OVEREXPRESSION; HISTONE PHOSPHORYLATION; HOMEOSTASIS; INSULIN SENSITIVITY; LEUKOCYTE; LIFESPAN; LONGEVITY; MALE; MASKING; MOUSE; NONHUMAN; TELOMERE; TISSUE DISTRIBUTION; TRANSGENIC MOUSE; WEIGHT REDUCTION;

AGING; ANIMALS; BIOLOGICAL MARKERS; BODY WEIGHT; CALORIC RESTRICTION; CHROMOSOME ABERRATIONS; HEALTH; HUMANS; LONGEVITY; LONGITUDINAL STUDIES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; TELOMERASE; TELOMERE; TELOMERE SHORTENING;

MUS; MUS MUSCULUS; RODENTIA;

EID: 84872767063     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053760     Document Type: Article

References (61)

1. Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, et al. (2009) Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325: 201-204.
2. Mattison JA, Roth GS, Beasley TM, Tilmont EM, Handy AM, et al. (2012) Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 489: 318-321.
3. Kenyon C, (2005) The plasticity of aging: insights from long-lived mutants. Cell 120: 449-460.
4. Fontana L, Klein S, (2007) Aging, adiposity, and calorie restriction. JAMA 297: 986-994.
5. Anderson RM, Shanmuganayagam D, Weindruch R, (2009) Caloric restriction and aging: studies in mice and monkeys. Toxicol Pathol 37: 47-51.
6. Hamrick MW, Ding KH, Ponnala S, Ferrari SL, Isales CM, (2008) Caloric restriction decreases cortical bone mass but spares trabecular bone in the mouse skeleton: implications for the regulation of bone mass by body weight. J Bone Miner Res 23: 870-878.
7. Hempenstall S, Picchio L, Mitchell SE, Speakman JR, Selman C, (2010) The impact of acute caloric restriction on the metabolic phenotype in male C57BL/6 and DBA/2 mice. Mech Ageing Dev 131: 111-118.
8. Liao CY, Rikke BA, Johnson TE, Diaz V, Nelson JF, (2010) Genetic variation in the murine lifespan response to dietary restriction: from life extension to life shortening. Aging Cell 9: 92-95.
9. Turturro A, Witt WW, Lewis S, Hass BS, Lipman RD, et al. (1999) Growth curves and survival characteristics of the animals used in the Biomarkers of Aging Program. J Gerontol A Biol Sci Med Sci 54: B492-501.
10. Dhahbi JM, Kim HJ, Mote PL, Beaver RJ, Spindler SR, (2004) Temporal linkage between the phenotypic and genomic responses to caloric restriction. Proc Natl Acad Sci U S A 101: 5524-5529.
11. Weindruch R, Walford RL, (1982) Dietary restriction in mice beginning at 1 year of age: effect on life-span and spontaneous cancer incidence. Science 215: 1415-1418.
12. Weindruch R, Walford RL, Fligiel S, Guthrie D, (1986) The retardation of aging in mice by dietary restriction: longevity, cancer, immunity and lifetime energy intake. J Nutr 116: 641-654.
13. Spindler SR, (2010) Caloric restriction: from soup to nuts. Ageing Res Rev 9: 324-353.
14. Bordone L, Guarente L, (2005) Calorie restriction, SIRT1 and metabolism: understanding longevity. Nat Rev Mol Cell Biol 6: 298-305.
15. Koubova J, Guarente L, (2003) How does calorie restriction work? Genes Dev 17: 313-321.
16. Herrera E, Samper E, Martin-Caballero J, Flores JM, Lee HW, et al. (1999) Disease states associated with telomerase deficiency appear earlier in mice with short telomeres. EMBO J 18: 2950-2960.
17. Chan SW, Blackburn EH, (2002) New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene 21: 553-563.
18. Flores I, Benetti R, Blasco MA, (2006) Telomerase regulation and stem cell behaviour. Curr Opin Cell Biol 18: 254-260.
19. Harley CB, Futcher AB, Greider CW, (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345: 458-460.
20. Collado M, Blasco MA, Serrano M, (2007) Cellular senescence in cancer and aging. Cell 130: 223-233.
21. Blasco MA, (2007) Telomere length, stem cells and aging. Nat Chem Biol 3: 640-649.
22. Mitchell JR, Wood E, Collins K, (1999) A telomerase component is defective in the human disease dyskeratosis congenita. Nature 402: 551-555.
23. Armanios MY, Chen JJ, Cogan JD, Alder JK, Ingersoll RG, et al. (2007) Telomerase mutations in families with idiopathic pulmonary fibrosis. N Engl J Med 356: 1317-1326.
24. Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, et al. (2004) Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci U S A 101: 17312-17315.
25. Tomas-Loba A, Flores I, Fernandez-Marcos PJ, Cayuela ML, Maraver A, et al. (2008) Telomerase reverse transcriptase delays aging in cancer-resistant mice. Cell 135: 609-622.
26. Bernardes de Jesus B, Vera E, Schneeberger K, Tejera AM, Ayuso E, et al. (2012) Telomerase gene therapy in adult and old mice delays aging and increases longevity without increasing cancer. EMBO Mol Med 4: 1-14.
27. Gonzalez-Suarez E, Geserick C, Flores JM, Blasco MA, (2005) Antagonistic effects of telomerase on cancer and aging in K5-mTert transgenic mice. Oncogene 24: 2256-2270.
28. Canela A, Vera E, Klatt P, Blasco MA, (2007) High-throughput telomere length quantification by FISH and its application to human population studies. Proc Natl Acad Sci U S A 104: 5300-5305.
29. Hemann MT, Strong MA, Hao LY, Greider CW, (2001) The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107: 67-77.
30. Argentino DP, Dominici FP, Munoz MC, Al-Regaiey K, Bartke A, et al. (2005) Effects of long-term caloric restriction on glucose homeostasis and on the first steps of the insulin signaling system in skeletal muscle of normal and Ames dwarf (Prop1df/Prop1df) mice. Exp Gerontol 40: 27-35.
31. Heikkinen S, Argmann CA, Champy MF, Auwerx J (2007) Evaluation of glucose homeostasis. Curr Protoc Mol Biol Chapter 29: Unit 29B 23.
32. Ferguson VL, Ayers RA, Bateman TA, Simske SJ, (2003) Bone development and age-related bone loss in male C57BL/6J mice. Bone 33: 387-398.
33. Ingram DK, Reynolds MA, (1986) Assessing the predictive validity of psychomotor tests as measures of biological age in mice. Exp Aging Res 12: 155-162.
34. Bartke A, (2005) Minireview: role of the growth hormone/insulin-like growth factor system in mammalian aging. Endocrinology 146: 3718-3723.
35. Fontana L, Partridge L, Longo VD, (2010) Extending healthy life span-from yeast to humans. Science 328: 321-326.
36. Wang C, Jurk D, Maddick M, Nelson G, Martin-Ruiz C, et al. (2009) DNA damage response and cellular senescence in tissues of aging mice. Aging Cell 8: 311-323.
37. Elyada E, Pribluda A, Goldstein RE, Morgenstern Y, Brachya G, et al. (2011) CKIalpha ablation highlights a critical role for p53 in invasiveness control. Nature 470: 409-413.
38. Herbig U, Ferreira M, Condel L, Carey D, Sedivy JM, (2006) Cellular senescence in aging primates. Science 311: 1257.
39. Herbig U, Jobling WA, Chen BP, Chen DJ, Sedivy JM, (2004) Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol Cell 14: 501-513.
40. Sedelnikova OA, Horikawa I, Redon C, Nakamura A, Zimonjic DB, et al. (2008) Delayed kinetics of DNA double-strand break processing in normal and pathological aging. Aging Cell 7: 89-100.
41. d'Adda di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, et al. (2003) A DNA damage checkpoint response in telomere-initiated senescence. Nature 426: 194-198.
42. Jaskelioff M, Muller FL, Paik JH, Thomas E, Jiang S, et al. (2011) Telomerase reactivation reverses tissue degeneration in aged telomerase-deficient mice. Nature 469: 102-106.
43. Finkel T, Holbrook NJ, (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408: 239-247.
44. Vera E, Bernardes de Jesus B, Foronda M, Flores JM, Blasco MA, (2012) The rate of increase of short telomeres predicts longevity in mammals. Cell Reports 2: 732-737.
45. Broccoli D, Young JW, de Lange T, (1995) Telomerase activity in normal and malignant hematopoietic cells. Proc Natl Acad Sci U S A 92: 9082-9086.
46. Blasco MA, (2005) Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet 6: 611-622.
47. de Lange T, (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19: 2100-2110.
48. Martinez P, Thanasoula M, Munoz P, Liao C, Tejera A, et al. (2009) Increased telomere fragility and fusions resulting from TRF1 deficiency lead to degenerative pathologies and increased cancer in mice. Genes Dev 23: 2060-2075.
49. McCay CM, Crowell MF, Maynard LA, (1935) The effect of retarded growth upon the length of life span and upon the ultimate body size. J Nutr 10: 63-79.
50. Guarente L, Picard F, (2005) Calorie restriction-the SIR2 connection. Cell 120: 473-482.
51. Canto C, Auwerx J, (2009) Caloric restriction, SIRT1 and longevity. Trends Endocrinol Metab 20: 325-331.
52. Burnett C, Valentini S, Cabreiro F, Goss M, Somogyvari M, et al. (2011) Absence of effects of Sir2 overexpression on lifespan in C. elegans and Drosophila. Nature 477: 482-485.
53. Longo VD, Fontana L, (2010) Calorie restriction and cancer prevention: metabolic and molecular mechanisms. Trends Pharmacol Sci 31: 89-98.
54. Dunn SE, Kari FW, French J, Leininger JR, Travlos G, et al. (1997) Dietary restriction reduces insulin-like growth factor I levels, which modulates apoptosis, cell proliferation, and tumor progression in p53-deficient mice. Cancer Res 57: 4667-4672.
55. von Zglinicki T, (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27: 339-344.
56. Calado RT, Young NS, (2009) Telomere diseases. N Engl J Med 361: 2353-2365.
57. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, et al. (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460: 392-395.
58. Pugh TD, Klopp RG, Weindruch R, (1999) Controlling caloric consumption: protocols for rodents and rhesus monkeys. Neurobiol Aging 20: 157-165.
59. Gonzalez-Suarez E, Samper E, Ramirez A, Flores JM, Martin-Caballero J, et al. (2001) Increased epidermal tumors and increased skin wound healing in transgenic mice overexpressing the catalytic subunit of telomerase, mTERT, in basal keratinocytes. EMBO J 20: 2619-2630.
60. Zijlmans JM, Martens UM, Poon SS, Raap AK, Tanke HJ, et al. (1997) Telomeres in the mouse have large inter-chromosomal variations in the number of T2AG3 repeats. Proc Natl Acad Sci U S A 94: 7423-7428.
61. McIlrath J, Bouffler SD, Samper E, Cuthbert A, Wojcik A, et al. (2001) Telomere length abnormalities in mammalian radiosensitive cells. Cancer Res 61: 912-915.