In vivo and in vitro analysis of age-associated changes and somatic cellular senescence in renal epithelial cells

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Berkenkamp, Birgit ^a   Susnik, Nathan ^a   Baisantry, Arpita ^a   Kuznetsova, Inna ^a   Jacobi, Christoph ^a   Sor̈ensen Zender, Inga ^a   Broecker, Verena ^a   Haller, Hermann ^a   Melk, Anette ^a   Schmitt, Roland ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 2A; HISTONE H2AX; KI 67 ANTIGEN; LEAD ACETATE;

AGE DISTRIBUTION; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL AGING; CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; GAMMA IRRADIATION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; KIDNEY TUBULE CELL; MALE; MOUSE; NONHUMAN; SENESCENCE; SOMATIC CELL;

ACUTE KIDNEY INJURY; AGING; ANIMALS; BETA-GALACTOSIDASE; CELL AGING; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P16; EPITHELIAL CELLS; EPITHELIUM; HISTONES; KI-67 ANTIGEN; KIDNEY TUBULES; MALE; MICE; MICE, INBRED C57BL; REGENERATION;

EID: 84896892826     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088071     Document Type: Article

References (45)

1. Braun H, Schmidt BM, Raiss M, Baisantry A, Mircea-Constantin D, et al. (2012) Cellular Senescence Limits Regenerative Capacity and Allograft Survival. J Am Soc Nephrol. 2012 Sep;23(9):1467-73.
2. Schmitt R, Marlier A, Cantley LG (2008) Zag expression during aging suppresses proliferation after kidney injury. J Am Soc Nephrol 19: 2375-2383.
3. Humphreys BD, Valerius MT, Kobayashi A, Mugford JW, Soeung S, et al. (2008) Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2: 284-291. (Pubitemid 351298594)
4. Melk A, Schmidt BM, Braun H, Vongwiwatana A, Urmson J, et al. (2009) Effects of donor age and cell senescence on kidney allograft survival. Am J Transplant 9: 114-123.
5. Witzgall R, Brown D, Schwarz C, Bonventre JV (1994) Localization of proliferating cell nuclear antigen, vimentin, c-Fos, and clusterin in the postischemic kidney. Evidence for a heterogenous genetic response among nephron segments, and a large pool of mitotically active and dedifferentiated cells. J Clin Invest 93: 2175-2188.
6. Melk A, Schmidt BM, Takeuchi O, Sawitzki B, Rayner DC, et al. (2004) Expression of p16INK4a and other cell cycle regulator and senescence associated genes in aging human kidney. Kidney Int 65: 510-520. (Pubitemid 38130645)
7. Westhoff JH, Schildhorn C, Jacobi C, Homme M, Hartner A, et al. (2010) Telomere shortening reduces regenerative capacity after acute kidney injury. J Am Soc Nephrol 21: 327-336.
8. Melk A (2003) Senescence of renal cells: molecular basis and clinical implications. Nephrol Dial Transplant 18: 2474-2478.
9. Naesens M (2011) Replicative senescence in kidney aging, renal disease, and renal transplantation. Discov Med 11: 65-75.
10. Schmitt R, Melk A (2012) New Insights on Molecular Mechanisms of Renal Aging. Am J Transplant. 2012 Nov;12(11):2892-900.
11. Melk A, Kittikowit W, Sandhu I, Halloran KM, Grimm P, et al. (2003) Cell senescence in rat kidneys in vivo increases with growth and age despite lack of telomere shortening. Kidney Int 63: 2134-2143. (Pubitemid 36605824)
12. Melk A, Ramassar V, Helms LM, Moore R, Rayner D, et al. (2000) Telomere shortening in kidneys with age. J Am Soc Nephrol 11: 444-453. (Pubitemid 30115074)
13. Verzola D, Gandolfo MT, Gaetani G, Ferraris A, Mangerini R, et al. (2008) Accelerated senescence in the kidneys of patients with type 2 diabetic nephropathy. Am J Physiol Renal Physiol 295: F1563-1573.
14. Westhoff JH, Hilgers KF, Steinbach MP, Hartner A, Klanke B, et al. (2008) Hypertension induces somatic cellular senescence in rats and humans by induction of cell cycle inhibitor p16INK4a. Hypertension 52: 123-129.
15. Joosten SA, van Ham V, Nolan CE, Borrias MC, Jardine AG, et al. (2003) Telomere shortening and cellular senescence in a model of chronic renal allograft rejection. Am J Pathol 162: 1305-1312. (Pubitemid 36350674)
16. Miura K, Goldstein RS, Morgan DG, Pasino DA, Hewitt WR, et al. (1987) Age-related differences in susceptibility to renal ischemia in rats. Toxicol Appl Pharmacol 87: 284-296. (Pubitemid 17019113)
17. Qiao X, Chen X, Wu D, Ding R,Wang J, et al. (2005) Mitochondrial pathway is responsible for aging-related increase of tubular cell apoptosis in renal ischemia/reperfusion injury. J Gerontol A Biol Sci Med Sci 60: 830-839. (Pubitemid 41098626)
18. Choie DD, Richter GW (1972) Cell proliferation in rat kidneys after prolonged treatment with lead. Am J Pathol 68: 359-370.
19. Choie DD, Richter GW (1972) Cell proliferation in rat kidney induced by lead acetate and effects of uninephrectomy on the proliferation. Am J Pathol 66: 265-275.
20. Vogetseder A, Palan T, Bacic D, Kaissling B, Le Hir M (2007) Proximal tubular epithelial cells are generated by division of differentiated cells in the healthy kidney. Am J Physiol Cell Physiol 292: C807-813.
21. Vogetseder A, Picard N, Gaspert A, Walch M, Kaissling B, et al. (2008) Proliferation capacity of the renal proximal tubule involves the bulk of differentiated epithelial cells. Am J Physiol Cell Physiol 294: C22-28.
22. Witzgall R (2008) Are renal proximal tubular epithelial cells constantly prepared for an emergency? Focus on "the proliferation capacity of the renal proximal tubule involves the bulk of differentiated epithelial cells". Am J Physiol Cell Physiol 294: C1-3.
23. Yang L, Besschetnova TY, Brooks CR, Shah JV, Bonventre JV (2010) Epithelial cell cycle arrest in G2/M mediates kidney fibrosis after injury. Nat Med 16: 535-543, 531p following 143.
24. Diehl JA (2002) Cycling to cancer with cyclin D1. Cancer Biol Ther 1: 226-231.
25. Lawless C, Wang C, Jurk D, Merz A, Zglinicki T, et al. (2010) Quantitative assessment of markers for cell senescence. Exp Gerontol 45: 772-778.
26. Villeda SA, Luo J, Mosher KI, Zou B, Britschgi M, et al. (2011) The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 477: 90-94.
27. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, et al. (2005) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433: 760-764. (Pubitemid 40292986)
28. Davalos AR, Kawahara M, Malhotra GK, Schaum N, Huang J, et al. (2013) p53-dependent release of Alarmin HMGB1 is a central mediator of senescent phenotypes. J Cell Biol 201: 613-629.
29. Coppe JP, Patil CK, Rodier F, Krtolica A, Beausejour CM, et al. (2010) A human-like senescence-associated secretory phenotype is conserved in mouse cells dependent on physiological oxygen. PLoS One 5: e9188.
30. Liu J, Xu K, Chase M, Ji Y, Logan JK, et al. (2012) Tiam1-regulated osteopontin in senescent fibroblasts contributes to the migration and invasion of associated epithelial cells. J Cell Sci 125: 376-386.
31. Freund A, Laberge RM, Demaria M, Campisi J (2012) Lamin B1 loss is a senescence-associated biomarker. Mol Biol Cell 23: 2066-2075.
32. Miya M, Maeshima A, Mishima K, Sakurai N, Ikeuchi H, et al. (2012) Age-related decline in label-retaining tubular cells: implication for reduced regenerative capacity after injury in the aging kidney. Am J Physiol Renal Physiol 302: F694-702.
33. Deng Q, Liao R, Wu BL, Sun P (2004) High intensity ras signaling induces premature senescence by activating p38 pathway in primary human fibroblasts. J Biol Chem 279: 1050-1059. (Pubitemid 38082626)
34. Sherr CJ, DePinho RA (2000) Cellular senescence: mitotic clock or culture shock? Cell 102: 407-410.
35. Kuilman T, Michaloglou C, Mooi WJ, Peeper DS (2010) The essence of senescence. Genes Dev 24: 2463-2479.
36. Rodier F, Coppe JP, Patil CK, Hoeijmakers WA, Munoz DP, et al. (2009) Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat Cell Biol 11: 973-979.
37. Rodier F, Munoz DP, Teachenor R, Chu V, Le O, et al. (2011) DNA-SCARS: distinct nuclear structures that sustain damage-induced senescence growth arrest and inflammatory cytokine secretion. J Cell Sci 124: 68-81.
38. Han EK, Ng SC, Arber N, Begemann M, Weinstein IB (1999) Roles of cyclin D1 and related genes in growth inhibition, senescence and apoptosis. Apoptosis 4: 213-219. (Pubitemid 29378789)
39. Burton DG, Sheerin AN, Ostler EL, Smith K, Giles PJ, et al. (2007) Cyclin D1 overexpression permits the reproducible detection of senescent human vascular smooth muscle cells. Ann N Y Acad Sci 1119: 20-31. (Pubitemid 350191243)
40. Ledda-Columbano GM, Pibiri M, Cossu C, Molotzu F, Locker J, et al. (2004) Aging does not reduce the hepatocyte proliferative response of mice to the primary mitogen TCPOBOP. Hepatology 40: 981-988. (Pubitemid 39288132)
41. Suzuki A, Sakaguchi T, Inaba K, Suzuki S, Konno H (2012) Impact of cell cycle disruption on impaired hepatic regeneration in aged livers with ischemic insult. J Surg Res 173: 267-277.
42. Leontieva OV, Lenzo F, Demidenko ZN, Blagosklonny MV (2012) Hypermitogenic drive coexists with mitotic incompetence in senescent cells. Cell Cycle 11: 4642-4649.
43. Sorensen I, Rong S, Susnik N, Gueler F, Shushakova N, et al. (2011) Bbeta(15-42) attenuates the effect of ischemia-reperfusion injury in renal transplantation. J Am Soc Nephrol 22: 1887-1896.
44. Debacq-Chainiaux F, Erusalimsky JD, Campisi J, Toussaint O (2009) Protocols to detect senescence-associated beta-galactosidase (SA-betagal) activity, a biomarker of senescent cells in culture and in vivo. Nat Protoc 4: 1798-1806.
45. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. (Pubitemid 34164012)