Telomere shortening reduces regenerative capacity after acute kidney injury

Journal of the American Society of Nephrology

Volumn 21, Issue 2, 2010, Pages 327-336

  Westhoff, Jens H ^a   Schildhorn, Carolin ^a,b   Jacobi, Christoph ^b   Hömme, Meike ^b   Hartner, Andrea ^c   Braun, Heidi ^a   Kryzer, Christine ^a   Wang, Chunfang ^d   Zglinicki, Thomas Von ^d   Kränzlin, Bettina ^e   Gretz, Norbert ^e   Melk, Anette ^b  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 2A; PROTEIN P53; CYCLIN DEPENDENT KINASE INHIBITOR 1A; RNA; TELOMERASE; TELOMERASE RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL AGING; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; GLOMERULUS; HISTOPATHOLOGY; KIDNEY CELL; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY INTERSTITIUM; KIDNEY ISCHEMIA; KIDNEY TUBULE ABSORPTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; TELOMERE; WILD TYPE; ACUTE KIDNEY FAILURE; ANIMAL; DISEASE MODEL; GENETICS; KIDNEY; METABOLISM; MOUSE MUTANT; NEPHRECTOMY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REGENERATION; ULTRASTRUCTURE;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; CONNECTIVE TISSUE GROWTH FACTOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DISEASE MODELS, ANIMAL; KIDNEY; KIDNEY FAILURE, ACUTE; MALE; MICE; MICE, KNOCKOUT; NEPHRECTOMY; REGENERATION; REPERFUSION INJURY; RNA; TELOMERASE; TELOMERE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77949377276     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2009010072     Document Type: Article

References (40)

1. Lindeman RD, Goldman R: Anatomic and physiologic age changes in the kidney. Exp Gerontol 21: 379-406, 1986
2. Goyal VK: Changes with age in the human kidney. Exp Gerontol 17: 321-331, 1982
3. Melk A, Schmidt BM, Takeuchi O, Sawitzki B, Rayner DC, Halloran PF: Expression of p16INK4a and other cell cycle regulator and senescence associated genes in aging human kidney. Kidney Int 65: 510-520, 2004
4. Schmitt R, Coca S, Kanbay M, Tinetti ME, Cantley LG, Parikh CR: Recovery of kidney function after acute kidney injury in the elderly: A systematic review and meta-analysis. Am J Kidney Dis 52: 262-271, 2008
5. US Renal Data System: USRDS 2007 Annual Data Report: Atlas of Chronic Kidney Disease and End-Stage Renal Disease in the United States, Bethesda, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, 2007
6. de Fijter JW, Mallat MJ, Doxiadis II, Ringers J, Rosendaal FR, Claas FH, Paul LC: Increased immunogenicity and cause of graft loss of old donor kidneys. J Am Soc Nephrol 12: 1538-1546, 2001
7. Blasco MA: Telomere length, stem cells and aging. Nat Chem Biol 3: 640-649, 2007
8. Choudhury AR, Ju Z, Djojosubroto MW, Schienke A, Lechel A, Schaet-zlein S, Jiang H, Stepczynska A, Wang C, Buer J, Lee HW, von Zglinicki T, Ganser A, Schirmacher P, Nakauchi H, Rudolph KL: Cdkn1a deletion improves stem cell function and lifespan of mice with dysfunctional telomeres without accelerating cancer formation. Nat Genet 39: 99-105, 2007
9. Greider CW, Blackburn EH: Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43: 405-413, 1985
10. Blasco MA, Lee HW, Hande MP, Samper E, Lansdorp PM, DePinho RA, Greider CW: Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91: 25-34, 1997
11. Flores I, Benetti R, Blasco MA: Telomerase regulation and stem cell behaviour. Curr Opin Cell Biol 18: 254-260, 2006
12. Melk A, Ramassar V, Helms LM, Moore R, Rayner D, Solez K, Halloran PF: Telomere shortening in kidneys with age. J Am Soc Nephrol 11: 444-453, 2000
13. 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 361: 393-395, 2003
14. Melk A, Kittikowit W, Sandhu I, Halloran KM, Grimm P, Schmidt BM, Halloran PF: Cell senescence in rat kidneys in vivo increases with growth and age despite lack of telomere shortening. Kidney Int 63: 2134-2143, 2003
15. Lee HW, Blasco MA, Gottlieb GJ, Horner JW 2nd, Greider CW, DePinho RA: Essential role of mouse telomerase in highly proliferative organs. Nature 392: 569-574, 1998
16. Rudolph KL, Chang S, Lee HW, Blasco M, Gottlieb GJ, Greider C, DePinho RA: Longevity, stress response, and cancer in aging telom-erase-deficient mice. Cell 96: 701-712, 1999
17. Satyanarayana A, Wiemann SU, Buer J, Lauber J, Dittmar KE, Wuste-feld T, Blasco MA, Manns MP, Rudolph KL: Telomere shortening impairs organ regeneration by inhibiting cell cycle re-entry of a sub-population of cells. EMBO J 22: 4003-4013, 2003
18. Melk A: Senescence of renal cells: Molecular basis and clinical implications. Nephrol Dial Transplant 18: 2474-2478, 2003
19. Melk A, Halloran PF: Cell senescence and its implications for nephrol-ogy. J Am Soc Nephrol 12: 385-393, 2001
20. Melk A, Schmidt BM, Braun H, Vongwiwatana A, Urmson J, Zhu LF, Rayner D, Halloran PF: Effects of donor age and cell senescence on kidney allograft survival. Am J Transplant 9: 114-123, 2009
21. Schmitt R, Marlier A, Cantley LG: Zag expression during aging suppresses proliferation after kidney injury. J Am Soc Nephrol 19: 2375-2383, 2008
22. Rudolph KL, Chang S, Millard M, Schreiber-Agus N, DePinho RA: Inhibition of experimental liver cirrhosis in mice by telomerase gene delivery. Science 287: 1253-1258, 2000
23. Lechel A, Satyanarayana A, Ju Z, Plentz RR, Schaetzlein S, Rudolph C, Wilkens L, Wiemann SU, Saretzki G, Malek NP, Manns MP, Buer J, Rudolph KL: The cellular level of telomere dysfunction determines induction of senescence or apoptosis in vivo. EMBO Rep 6: 275-281, 2005
24. Hemann MT, Rudolph KL, Strong MA, DePinho RA, Chin L, Greider CW: Telomere dysfunction triggers developmentally regulated germ cell apoptosis. Mol Biol Cell 12: 2023-2030, 2001
25. Kim KH, Park GT, Lim YB, Rue SW, Jung JC, Sonn JK, Bae YS, Park JW, Lee YS: Expression of connective tissue growth factor, a biomarker in senescence of human diploid fibroblasts, is up-regulated by a transforming growth factor-beta-mediated signaling pathway. Biochem Biophys Res Commun 318: 819-825, 2004
26. Campisi J: Senescent cells, tumor suppression, and organismal aging: Good citizens, bad neighbors. Cell 120: 513-522, 2005
27. Flores I, Blasco MA: A p53-dependent response limits epidermal stem cell functionality and organismal size in mice with short telomeres. PLoS One 4: e4934, 2009
28. Wang C, Jurk D, Maddick M, Nelson G, Martin-Ruiz C, von Zglinicki T: DNA damage response and cellular senescence in tissues of aging mice. Aging Cell 8: 311-323, 2009
29. d'Adda di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, Von Zglinicki T, Saretzki G, Carter NP, Jackson SP: A DNA damage checkpoint response in telomere-initiated senescence. Nature 426: 194-198, 2003
30. Megyesi J, Udvarhelyi N, Safirstein RL, Price PM: The p53-indepen-dent activation of transcription of p21 WAF1/CIP1/SDI1 after acute renal failure. Am J Physiol 271: F1211-F1216, 1996
31. Brown JP, Wei W, Sedivy JM: Bypass of senescence after disruption of p21CIP1/WAF1 gene in normal diploid human fibroblasts. Science 277: 831-834, 1997
32. Chin L, Artandi SE, Shen Q, Tam A, Lee SL, Gottlieb GJ, Greider CW, DePinho RA: p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcino-genesis. Cell 97: 527-538, 1999
33. Rodier F, Campisi J, Bhaumik D: Two faces of p53: Aging and tumor suppression. Nucleic Acids Res 35: 7475-7484, 2007
34. Collado M, Blasco MA, Serrano M: Cellular senescence in cancer and aging. Cell 130: 223-233, 2007
35. Alcorta DA, Xiong Y, Phelps D, Hannon G, Beach D, Barrett JC: Involvement of the cyclin-dependent kinase inhibitor p16 (INK4a) in replicative senescence of normal human fibroblasts. Proc Natl Acad Sci USA 93: 13742-13747, 1996
36. Shapiro GI, Edwards CD, Ewen ME, Rollins BJ: p16INK4A participates in a G1 arrest checkpoint in response to DNA damage. Mol Cell Biol 18: 378-387, 1998
37. Jacobs JJ, de Lange T: p16INK4a as a second effector of the telomere damage pathway. Cell Cycle 4: 1364-1368, 2005
38. Garcia-Cao I, Garcia-Cao M, Tomas-Loba A, Martin-Caballero J, Flores JM, Klatt P, Blasco MA, Serrano M: Increased p53 activity does not accelerate telomere-driven ageing. EMBO Rep 7: 546-552, 2006
39. Keppler A, Gretz N, Schmidt R, Kloetzer HM, Groene HJ, Lelongt B, Meyer M, Sadick M, Pill J: Plasma creatinine determination in mice and rats: An enzymatic method compares favorably with a high-performance liquid chromatography assay. Kidney Int 71: 74-78, 2007
40. Lechel A, Holstege H, Begus Y, Schienke A, Kamino K, Lehmann U, Kubicka S, Schirmacher P, Jonkers J, Rudolph KL: Telomerase deletion limits progression of p53-mutant hepatocellular carcinoma with short telomeres in chronic liver disease. Gastroenterology 132: 1465-1475, 2007