Epithelial cell cycle arrest in G2/M mediates kidney fibrosis after injury

Nature Medicine

Volumn 16, Issue 5, 2010, Pages 535-543

  Yang, Li ^a,b   Besschetnova, Tatiana Y ^a,c   Brooks, Craig R ^a   Shah, Jagesh V ^a,c,d   Bonventre, Joseph V ^a,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b PEKING UNIVERSITY FIRST HOSPITAL   (China)

^c HARVARD MEDICAL SCHOOL   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; MITOGEN ACTIVATED PROTEIN KINASE 9; PIFITHRIN ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CYTOKINE PRODUCTION; ENZYME ACTIVATION; EPITHELIUM CELL; HUMAN; KIDNEY FIBROSIS; KIDNEY ISCHEMIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

ADULT; CELL CYCLE; EPITHELIAL CELLS; FIBROSIS; GLOMERULONEPHRITIS; HUMANS; KIDNEY; KIDNEY DISEASES; KIDNEY FAILURE, ACUTE; MITOGEN-ACTIVATED PROTEIN KINASE 9; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77952174830     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2144     Document Type: Article

References (52)

1. Humphreys, B.D. et al. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2, 284-291 (2008).
2. Wynn, T.A. Cellular and molecular mechanisms of fbrosis. J. Pathol. 214, 199-210 (2008).
3. Coresh, J., Astor, B.C., Greene, T., Eknoyan, G. & Levey, A.S. Prevalence of chronic kidney disease and decreased kidney function in the adult US population: Third National Health and Nutrition Examination Survey. Am. J. Kidney Dis. 41, 1-12 (2003).
4. Lameire, N., Jager, K., Van Biesen, W., de Bacquer, D. & Vanholder, R. Chronic kidney disease: a European perspective. Kidney Int. Suppl. S30-S38 (2005).
5. Forbes, J.M., Hewitson, T.D., Becker, G.J. & Jones, C.L. Ischemic acute renal failure: long-term histology of cell and matrix changes in the rat. Kidney Int. 57, 2375-2385 (2000).
6. Macedo, E., Bouchard, J. & Mehta, R.L. Renal recovery following acute kidney injury. Curr. Opin. Crit. Care 14, 660-665 (2008).
7. Kalluri, R. & Neilson, E.G. Epithelial-mesenchymal transition and its implications for fbrosis. J. Clin. Invest. 112, 1776-1784 (2003).
8. Liu, Y. Epithelial to mesenchymal transition in renal fbrogenesis: pathologic signifcance, molecular mechanism, and therapeutic intervention. J. Am. Soc. Nephrol. 15, 1-12 (2004).
9. Burns, W.C., Kantharidis, P. & Thomas, M.C. The role of tubular epithelial-mesenchymal transition in progressive kidney disease. Cells Tissues Organs 185, 222-231 (2007).
10. Humphreys, B.D. et al. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fbrosis. Am. J. Pathol. 176, 85-97 (2010).
11. Nguyen, T.Q. & Goldschmeding, R. Bone morphogenetic protein-7 and connective tissue growth factor: novel targets for treatment of renal fbrosis? Pharm. Res. 25, 2416-2426 (2008).
12. Qi, W., Chen, X., Poronnik, P. & Pollock, C.A. Transforming growth factor-β/connective tissue growth factor axis in the kidney. Int. J. Biochem. Cell Biol. 40, 9-13 (2008).
13. Bonventre, J.V. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J. Am. Soc. Nephrol. 14 Suppl 1, S55-S61 (2003).
14. Price, P.M., Megyesi, J. & Safrstein, R.L. Cell cycle regulation: repair and regeneration in acute renal failure. Kidney Int. 66, 509-514 (2004).
15. Tanaka, H. et al. Role of the E2F1-p19-p53 pathway in ischemic acute renal failure. Nephron Physiol. 101, 27-34 (2005).
16. Chkhotua, A.B., Abendroth, D., Froeba, G. & Schelzig, H. Up-regulation of cell cycle regulatory genes after renal ischemia/reperfusion: differential expression of p16(INK4a), p21(WAF1/CIP1) and p27(Kip1) cyclin-dependent kinase inhibitor genes depending on reperfusion time. Transpl. Int. 19, 72-77 (2006).
17. Melk, A., Schmidt, B.M., Vongwiwatana, A., Rayner, D.C. & Halloran, P.F. Increased expression of senescence-associated cell cycle inhibitor p16INK4a in deteriorating renal transplants and diseased native kidney. Am. J. Transplant. 5, 1375-1382 (2005).
18. Jiang, M. & Dong, Z. Regulation and pathological role of p53 in cisplatin nephrotoxicity. J. Pharmacol. Exp. Ther. 327, 300-307 (2008).
19. Price, P.M., Safrstein, R.L. & Megyesi, J. The cell cycle and acute kidney injury. Kidney Int. 76, 604-613 (2009).
20. Molitoris, B.A. et al. siRNA targeted to p53 attenuates ischemic and cisplatin-induced acute kidney injury. J. Am. Soc. Nephrol. 20, 1754-1764 (2009).
21. Yu, C.C., Woods, A.L. & Levison, D.A. The assessment of cellular proliferation by immunohistochemistry: a review of currently available methods and their applications. Histochem. J. 24, 121-131 (1992).
22. Crosio, C. et al. Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol. Cell. Biol. 22, 874-885 (2002).
23. Silva, F.G., Nadasdy, T. & Laszik, Z. Immunohistochemical and lectin dissection of the human nephron in health and disease. Arch. Pathol. Lab. Med. 117, 1233-1239 (1993).
24. Ichimura, T., Hung, C.C., Yang, S.A., Stevens, J.L. & Bonventre, J.V. Kidney injury molecule-1: a tissue and urinary biomarker for nephrotoxicant-induced renal injury. Am. J. Physiol. Renal Physiol. 286, F552-F563 (2004).
25. Hendzel, M.J. et al. Mitosis-specifc phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348-360 (1997).
26. Abraham, R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15, 2177-2196 (2001).
27. Goodarzi, A.A., Block, W.D. & Lees-Miller, S.P. The role of ATM and ATR in DNA damage-induced cell cycle control. Prog. Cell Cycle Res. 5, 393-411 (2003).
28. Bencokova, Z. et al. ATM activation and signaling under hypoxic conditions. Mol. Cell. Biol. 29, 526-537 (2009).
29. Hickson, I. et al. Identifcation and characterization of a novel and specifc inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64, 9152-9159 (2004).
30. Komarov, P.G. et al. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 285, 1733-1737 (1999).
31. Vassilev, L.T. et al. Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc. Natl. Acad. Sci. USA 103, 10660-10665 (2006).
32. Horwitz, S.B. Mechanism of action of taxol. Trends Pharmacol. Sci. 13, 134-136 (1992).
33. Ishani, A. et al. Acute kidney injury increases risk of ESRD among elderly. J. Am. Soc. Nephrol. 20, 223-228 (2009).
34. Leask, A. & Abraham, D.J. TGF-β signaling and the fbrotic response. FASEB J. 18, 816-827 (2004).
35. Zeisberg, M. et al. Fibroblasts derive from hepatocytes in liver fbrosis via epithelial to mesenchymal transition. J. Biol. Chem. 282, 23337-23347 (2007).
36. Qi, W. et al. Integrated actions of transforming growth factor-β1 and connective tissue growth factor in renal fbrosis. Am. J. Physiol. Renal Physiol. 288, F800-F809 (2005).
37. Okada, H. et al. Connective tissue growth factor expressed in tubular epithelium has a pivotal role in renal fbrogenesis. J. Am. Soc. Nephrol. 16, 133-143 (2005).
38. Ikawa, Y. et al. Neutralizing monoclonal antibody to human connective tissue growth factor ameliorates transforming growth factor-β-induced mouse fbrosis. J. Cell. Physiol. 216, 680-687 (2008).
39. Shi-Wen, X., Leask, A. & Abraham, D. Regulation and function of connective tissue growth factor/CCN2 in tissue repair, scarring and fbrosis. Cytokine Growth Factor Rev. 19, 133-144 (2008).
40. Stark, G.R. & Taylor, W.R. Control of the G2/M transition. Mol. Biotechnol. 32, 227-248 (2006).
41. Taylor, W.R. & Stark, G.R. Regulation of the G2/M transition by p53. Oncogene 20, 1803-1815 (2001).
42. Bunz, F. et al. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282, 1497-1501 (1998).
43. Kailong, L. et al. P53-Rb signaling pathway is involved in tubular cell senescence in renal ischemia/reperfusion injury. Biocell 31, 213-223 (2007).
44. Megyesi, J., Price, P.M., Tamayo, E. & Safrstein, R.L. The lack of a functional p21(WAF1/CIP1) gene ameliorates progression to chronic renal failure. Proc. Natl. Acad. Sci. USA 96, 10830-10835 (1999).
45. Zahedi, K. et al. Stathmin-defcient mice develop fbrosis and show delayed recovery from ischemic-reperfusion injury. Am. J. Physiol. Renal Physiol. 290, F1559-F1567 (2006).
46. Hong, H. et al. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 460, 1132-1135 (2009).
47. Kawamura, T. et al. Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 460, 1140-1144 (2009).
48. Marion, R.M. et al. A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 460, 1149-1153 (2009).
49. Ma, F.Y., Sachchithananthan, M., Flanc, R.S. & Nikolic-Paterson, D.J. Mitogen activated protein kinases in renal fbrosis. Front. Biosci. (Schol. Ed.) 1, 171-187 (2009).
50. Park, K.M. et al. Inducible nitric oxide synthase is an important contributor to prolonged protective effects of ischemic preconditioning in the mouse kidney. J. Biol. Chem. 278, 27256-27266 (2003).
51. Hung, C.C., Ichimura, T., Stevens, J.L. & Bonventre, J.V. Protection of renal epithelial cells against oxidative injury by endoplasmic reticulum stress preconditioning is mediated by ERK1/2 activation. J. Biol. Chem. 278, 29317-29326 (2003).
52. Ichimura, T. et al. Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J. Clin. Invest. 118, 1657-1668 (2008).