Feline chronic kidney disease is associated with shortened telomeres and increased cellular senescence

American Journal of Physiology - Renal Physiology

Volumn 305, Issue 3, 2013, Pages

  Quimby, Jessica M ^a   Maranon, David G ^a   Battaglia, Christine L R ^a   McLeland, Shannon M ^a   Brock, William T ^a   Bailey, Susan M ^a  

^a Department of Ecosystem Science and Sustainability   (United States)

Author keywords

Aging; Feline; Kidney; Senescence; Telomere

Indexed keywords

BETA GALACTOSIDASE;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAT; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; EPITHELIUM CELL; FLUORESCENCE IN SITU HYBRIDIZATION; HISTOGRAM; IMMUNOHISTOCHEMISTRY; KIDNEY; LIVER; NONHUMAN; PRIORITY JOURNAL; SENESCENCE; SKIN; TELOMERE; TELOMERE HOMEOSTASIS;

EID: 84880999356     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00527.2012     Document Type: Article

References (50)

1. Aikata H, Takaishi H, Kawakami Y, Takahashi S, Kitamoto M, Nakanishi T, Nakamura Y, Shimamoto F, Kajiyama G, Ide T. Telomere reduction in human liver tissues with age and chronic inflammation. Exp Cell Res 256: 578-582, 2000.
2. Boyd LM, Langston C, Thompson K, Zivin K, Imanishi M. Survival in cats with naturally occurring chronic kidney disease (2000-2002). J Vet Intern Med 22: 1111-1117, 2008.
3. Brandt LE, Bohn AA, Charles JB, Ehrhart EJ. Localization of canine, feline, and mouse renal membrane proteins. Vet Pathol 49: 693-703, 2011.
4. Cadile CD, Kitchell BE, Biller BJ, Hetler ER, Balkin RG. Telomerase activity as a marker for malignancy in feline tissues. Am J Vet Res 62: 1578-1581, 2001.
5. Cottliar A, Fundia A, Boerr L, Sambuelli A, Negreira S, Gil A, Gomez JC, Chopita N, Bernedo A, Slavutsky I. High frequencies of telomeric associations, chromosome aberrations, and sister chromatid exchanges in ulcerative colitis. Am J Gastroenterol 95: 2301-2307, 2000.
6. DiBartola SP, Rutgers HC, Zack PM, Tarr MJ. Clinicopathologic findings associated with chronic renal disease in cats: 74 cases (1973-1984). J Am Vet Med Assoc 190: 1196-1202, 1987.
7. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 92: 9363-9367, 1995.
8. Feng X, Wang L, Li Y. Change of telomere length in angiotensin II-induced human glomerular mesangial cell senescence and the protective role of losartan. Mol Med Report 4: 255-260, 2011.
9. Fusaro L, Panarese S, Brunetti B, Zambelli D, Benazzi C, Sarli G. Quantitative analysis of telomerase in feline mammary tissues. J Vet Diagn Invest 21: 369-373, 2009.
10. Goldberg-Bittman L, Kitay-Cohen Y, Quitt M, Hadary R, Fejgin MD, Yukla M, Amiel A. Telomere aggregates in non-Hodgkin lymphoma patients at different disease stages. Cancer Genet Cytogen 184: 105-108, 2008.
11. Hamet P, Thorin-Trescases N, Moreau P, Dumas P, Tea BS, deBlois D, Kren V, Pravenec M, Kunes J, Sun Y, Tremblay J. Workshop: excess growth and apoptosis: is hypertension a case of accelerated aging of cardiovascular cells? Hypertension 37: 760-766, 2001.
12. Harris RC, Neilson EG. Toward a unified theory of renal progression. Annu Rev Med 57: 365-380, 2006.
13. Herbert BS, Hochreiter AE, Wright WE, Shay JW. Nonradioactive detection of telomerase activity using the telomeric repeat amplification protocol. Nat Protoc 1: 1583-1590, 2006.
14. Hirota J, Usui R, Satoh T, Ikemoto S. Telomere position on the cat chromosome. J Vet Med Sci 58: 1025-1026, 1996.
15. Hou M, Xu D, Bjorkholm M, Gruber A. Real-time quantitative telomeric repeat amplification protocol assay for the detection of telomerase activity. Clin Chem 47: 519-524, 2001.
16. Houben JM, Moonen HJ, van Schooten FJ, Hageman GJ. Telomere length assessment: biomarker of chronic oxidative stress? Free Radic Biol Med 44: 235-246, 2008.
17. Jaskelioff M, Muller FL, Paik JH, Thomas E, Jiang S, Adams AC, Sahin E, Kost-Alimova M, Protopopov A, Cadinanos J, Horner JW, Maratos-Flier E, Depinho RA. Telomerase reactivation reverses tissue degeneration in aged telomerase-deficient mice. Nature 469: 102-106, 2011.
18. Jiang H, Ju Z, Rudolph KL. Telomere shortening and ageing. Z Gerontol Geriatr 40: 314-324, 2007.
19. Joosten SA, van Ham V, Nolan CE, Borrias MC, Jardine AG, Shiels PG, van Kooten C, Paul LC. Telomere shortening and cellular senescence in a model of chronic renal allograft rejection. Am J Pathol 162: 1305-1312, 2003.
20. Kao MP, Ang DS, Pall A, Struthers AD. Oxidative stress in renal dysfunction: mechanisms, clinical sequelae and therapeutic options. J Hum Hypertens 24: 1-8, 2010.
21. Keegan RF, Webb CB. Oxidative stress and neutrophil function in cats with chronic renal failure. J Vet Intern Med 24: 514-519, 2010.
22. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PLC, Coviello GM, Wright WE, Weinrich SL, Shay JW. Specific association of human telomerase activity with immortal cells and cancer. Science 266: 2011-2015, 1994.
23. Kim NW, Wu F. Advances in quantification and characterization of telomerase activity by the telomeric repeat amplification protocol (TRAP). Nucleic Acids Res 25: 2595-2597, 1997.
24. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25: 402-408, 2001.
25. Locatelli F, Canaud B, Eckardt KU, Stenvinkel P, Wanner C, Zoccali C. Oxidative stress in end-stage renal disease: an emerging threat to patient outcome. Nephrol Dial Transplant 18: 1272-1280, 2003.
26. Lopez-Diazguerrero NE, Perez-Figueroa GE, Martinez-Garduno CM, Alarcon-Aguilar A, Luna-Lopez A, Gutierrez-Ruiz MC, Konigsberg M. Telomerase activity in response to mild oxidative stress. Cell Biol Int 36: 409-413, 2012.
27. Mai S, Garini Y. The significance of telomeric aggregates in the interphase nuclei of tumor cells. J Cell Biochem 97: 904-915, 2006.
28. Masi S, Salpea KD, Li K, Parkar M, Nibali L, Donos N, Patel K, Taddei S, Deanfield JE, D'Aiuto F, Humphries SE. Oxidative stress, chronic inflammation, and telomere length in patients with periodontitis. Free Radic Biol Med 50: 730-735, 2011.
29. McKevitt TP, Nasir L, Wallis CV, Argyle DJ. A cohort study of telomere and telomerase biology in cats. Am J Vet Res 64: 1496-1499, 2003.
30. Meeker AK, Gage WR, Hicks JL, Simon I, Coffman JR, Platz EA, March GE, De Marzo AM. Telomere length assessment in human archival tissues: combined telomere fluorescence in situ hybridization and immunostaining. Am J Pathol 160: 1259-1268, 2002.
31. 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.
32. 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.
33. Melk A, Schmidt BM, Vongwiwatana A, Rayner DC, Halloran PF. Increased expression of senescence-associated cell cycle inhibitor p16INK4a in deteriorating renal transplants and diseased native kidney. Am J Transplant 5: 1375-1382, 2005.
34. Naesens M. Replicative senescence in kidney aging, renal disease, and renal transplantation. Discov Med 11: 65-75, 2011.
35. Nangaku M. Chronic hypoxia and tubulointerstitial injury: a final common pathway to end-stage renal failure. J Am Soc Nephrol 17: 17-25, 2006.
36. Oeseburg H, de Boer RA, van Gilst WH, van der Harst P. Telomere biology in healthy aging and disease. Pflügers Arch 459: 259-268, 2010.
37. Perico N, Remuzzi G, Benigni A. Aging and the kidney. Curr Opin Nephrol Hypertens 20: 312-317, 2011.
38. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45, 2001.
39. Popolo A, Autore G, Pinto A, Marzocco S. Oxidative stress in patients with cardiovascular disease and chronic renal failure. Free Radic Res 47: 346-356, 2013.
40. Reyes JL, Lamas M, Martin D, del Carmen Namorado M, Islas S, Luna J, Tauc M, Gonzalez-Mariscal L. The renal segmental distribution of claudins changes with development. Kidney Int 62: 476-487, 2002.
41. Risques RA, Lai LA, Brentnall TA, Li L, Feng Z, Gallaher J, Mandelson MT, Potter JD, Bronner MP, Rabinovitch PS. Ulcerative colitis is a disease of accelerated colon aging: evidence from telomere attrition and DNA damage. Gastroenterology 135: 410-418, 2008.
42. Rodriguez-Iturbe B, Garcia Garcia G. The role of tubulointerstitial inflammation in the progression of chronic renal failure. Nephron Clin Pract 116: 81-88, 2010.
43. 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.
44. Smith JA, Park S, Krause JS, Banik NL. Oxidative stress, DNA damage, and the telomeric complex as therapeutic targets in acute neurodegeneration. Neurochem Int 62: 764-775, 2013.
45. Takubo K, Aida J, Izumiyama-Shimomura N, Ishikawa N, Sawabe M, Kurabayashi R, Shiraishi H, Arai T, Nakamura K. Changes of telomere length with aging. Geriatr Gerontol Int 10, Suppl 1: S197-S206, 2010.
46. Tarry-Adkins JL, Ozanne SE, Norden A, Cherif H, Hales CN. Lower antioxidant capacity and elevated p53 and p21 may be a link between gender disparity in renal telomere shortening, albuminuria, and longevity. Am J Physiol Renal Physiol 290: F509-F516, 2006.
47. Tchakmakjian L, Gardner JP, Wilson PD, Kimura M, Skurnick J, Zielke HR, Aviv A. Age-dependent telomere attrition as a potential indicator of racial differences in renal growth patterns. Nephron Exp Nephrol 98: 82-88, 2004.
48. Verzola D, Gandolfo MT, Gaetani G, Ferraris A, Mangerini R, Ferrario F, Villaggio B, Gianiorio F, Tosetti F, Weiss U, Traverso P, Mji M, Deferrari G, Garibotto G. Accelerated senescence in the kidneys of patients with type 2 diabetic nephropathy. Am J Physiol Renal Physiol 295: F1563-F1573, 2008.
49. von Figura G, Hartmann D, Song Z, Rudolph KL. Role of telomere dysfunction in aging and its detection by biomarkers. J Mol Med 87: 1165-1171, 2009.
50. Yu S, Paetau-Robinson I. Dietary supplements of vitamins E and C and beta-carotene reduce oxidative stress in cats with lprenal insufficiency. Vet Res Commun 30: 403-413, 2006.