Focal adhesion kinase signaling mediates acute renal injury induced by ischemia/reperfusion

American Journal of Pathology

Volumn 179, Issue 6, 2011, Pages 2766-2778

  Qin, Yu ^a   Alderliesten, Maaike C ^a   Stokman, Geurt ^a   Pennekamp, Petra ^b   Bonventre, Joseph V ^c   De Heer, Emile ^d   Ichimura, Takaharu ^c   De Graauw, Marjo ^a   Price, Leo S ^a   Van De Water, Bob ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE; HYDROGEN PEROXIDE; INTERLEUKIN 6; KIDNEY INJURY MOLECULE 1; MONOCYTE CHEMOTACTIC PROTEIN 1; PAXILLIN; SERINE; STRESS ACTIVATED PROTEIN KINASE; TAMOXIFEN;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FOCAL ADHESION; GENE DELETION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC RECOMBINATION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CELL; KIDNEY ISCHEMIA; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; KIDNEY TUBULE DAMAGE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REPERFUSION INJURY;

ACUTE KIDNEY INJURY; ANIMALS; CELL ADHESION; CYTOKINES; ENZYME INHIBITORS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HYDROGEN PEROXIDE; KIDNEY TUBULES, PROXIMAL; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; NEPHRITIS; OXIDANTS; OXIDATIVE STRESS; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TAMOXIFEN;

EID: 81255157523     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.08.025     Document Type: Article

References (40)

1. E.A. Hoste, and M. Schurgers Epidemiology of acute kidney injury: how big is the problem? Crit Care Med 36 2008 S146 S151
2. L.C. Racusen, B.A. Fivush, Y.L. Li, I. Slatnik, and K. Solez Dissociation of tubular cell detachment and tubular cell death in clinical and experimental "acute tubular necrosis" Lab Invest 64 1991 546 556
3. A. Zuk, J.V. Bonventre, D. Brown, and K.S. Matlin Polarity, integrin, and extracellular matrix dynamics in the postischemic rat kidney Am J Physiol 275 1998 C711 C731
4. D. Saenz-Morales, M.M. Escribese, K. Stamatakis, M. Garcia-Martos, L. Alegre, E. Conde, D. Perez-Sala, F. Mampaso, and M.L. Garcia-Bermejo Requirements for proximal tubule epithelial cell detachment in response to ischemia: role of oxidative stress Exp Cell Res 312 2006 3711 3727 (Pubitemid 44637176)
5. M. Alderliesten, M. de Graauw, J. Oldenampsen, Y. Qin, C. Pont, L. van Buren, and B. van de Water Extracellular signal-regulated kinase activation during renal ischemia/reperfusion mediates focal adhesion dissolution and renal injury Am J Pathol 171 2007 452 462 (Pubitemid 47344678)
6. A.L. Berrier, and K.M. Yamada Cell-matrix adhesion J Cell Physiol 213 2007 565 573 (Pubitemid 350058247)
7. D.S. Harburger, and D.A. Calderwood Integrin signalling at a glance J Cell Sci 122 2009 159 163
8. P.S. Kellerman, R.A. Clark, C.A. Hoilien, S.L. Linas, and B.A. Molitoris Role of microfilaments in maintenance of proximal tubule structural and functional integrity Am J Physiol 259 1990 F279 F285
9. J.M. Weinberg, M.A. Venkatachalam, N.F. Roeser, R.A. Senter, and I. Nissim Energetic determinants of tyrosine phosphorylation of focal adhesion proteins during hypoxia/reoxygenation of kidney proximal tubules Am J Pathol 158 2001 2153 2164 (Pubitemid 32545201)
10. D.J. Webb, K. Donais, L.A. Whitmore, S.M. Thomas, C.E. Turner, J.T. Parsons, and A.F. Horwitz FAK-Src signalling through paxillin ERK and MLCK regulates adhesion disassembly Nat Cell Biol 6 2004 154 161 (Pubitemid 38425715)
11. D.D. Schlaepfer, C.R. Hauck, and D.J. Sieg Signaling through focal adhesion kinase Prog Biophys Mol Biol 71 1999 435 478 (Pubitemid 29156312)
12. N.K. Zouq, J.A. Keeble, J. Lindsay, A.J. Valentijn, L. Zhang, D. Mills, C.E. Turner, C.H. Streuli, and A.P. Gilmore FAK engages multiple pathways to maintain survival of fibroblasts and epithelia: differential roles for paxillin and p130Cas J Cell Sci 122 2009 357 367
13. S.T. Lim, X.L. Chen, Y. Lim, D.A. Hanson, T.T. Vo, K. Howerton, N. Larocque, S.J. Fisher, D.D. Schlaepfer, and D. Ilic Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation Mol Cell 29 2008 9 22
14. M. Funakoshi-Tago, Y. Sonoda, S. Tanaka, K. Hashimoto, K. Tago, S. Tominaga, and T. Kasahara Tumor necrosis factor-induced nuclear factor kappaB activation is impaired in focal adhesion kinase-deficient fibroblasts J Biol Chem 278 2003 29359 29365 (Pubitemid 36935853)
15. D. Ilic, Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, and T. Yamamoto Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice Nature 377 1995 539 544
16. H.E. Beggs, D. Schahin-Reed, K. Zang, S. Goebbels, K.A. Nave, J. Gorski, K.R. Jones, D. Sretavan, and L.F. Reichardt FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies Neuron 40 2003 501 514 (Pubitemid 37494700)
17. B. Dworniczak, B. Skryabin, J. Tchinda, S. Heuck, F.J. Seesing, D. Metzger, P. Chambon, J. Horst, and P. Pennekamp Inducible Cre/loxP recombination in the mouse proximal tubule Nephron Exp Nephrol 106 2007 e11 e20
18. M. Vooijs, J. Jonkers, and A. Berns A highly efficient ligand-regulated Cre recombinase mouse line shows that LoxP recombination is position dependent EMBO Rep 2 2001 292 297 (Pubitemid 32401523)
19. T. Ichimura, J.V. Bonventre, V. Bailly, H. Wei, C.A. Hession, R.L. Cate, and M. Sanicola Kidney injury molecule-1 (KIM-1), a putative epithelial cell adhesion molecule containing a novel immunoglobulin domain, is up-regulated in renal cells after injury J Biol Chem 273 1998 4135 4142 (Pubitemid 28103282)
20. Q. Chen, T.W. Jones, P.C. Brown, and J.L. Stevens The mechanism of cysteine conjugate cytotoxicity in renal epithelial cells Covalent binding leads to thiol depletion and lipid peroxidation J Biol Chem 265 1990 21603 21611
21. V.S. Vaidya, V. Ramirez, T. Ichimura, N.A. Bobadilla, and J.V. Bonventre Urinary kidney injury molecule-1: a sensitive quantitative biomarker for early detection of kidney tubular injury Am J Physiol Renal Physiol 290 2006 F517 F529
22. M.R. Daha, and C. van Kooten Is the proximal tubular cell a proinflammatory cell? Nephrol Dial Transplant 15 Suppl 6 2000 41 43
23. C.C. Cao, X.Q. Ding, Z.L. Ou, C.F. Liu, P. Li, L. Wang, and C.F. Zhu In vivo transfection of NF-kappaB decoy oligodeoxynucleotides attenuate renal ischemia/reperfusion injury in rats Kidney Int 65 2004 834 845 (Pubitemid 38251059)
24. D. Huang, M. Khoe, M. Befekadu, S. Chung, Y. Takata, D. Ilic, and M. Bryer-Ash Focal adhesion kinase mediates cell survival via NF-kappaB and ERK signaling pathways Am J Physiol Cell Physiol 292 2007 C1339 C1352
25. M.H. van Miltenburg, R. Lalai, H. de Bont, E. van Waaij, H. Beggs, E.H. Danen, and B. van de Water Complete focal adhesion kinase deficiency in the mammary gland causes ductal dilation and aberrant branching morphogenesis through defects in Rho kinase-dependent cell contractility FASEB J 23 2009 3482 3493
26. K.H. Lee, S.E. Kim, and Y.S. Lee SP600125, a selective JNK inhibitor, aggravates hepatic ischemia-reperfusion injury Exp Mol Med 38 2006 408 416
27. J. DiMari, J. Megyesi, N. Udvarhelyi, P. Price, R. Davis, and R. Safirstein N-acetyl cysteine ameliorates ischemic renal failure Am J Physiol 272 1997 F292 F298
28. C. Huang, Z. Rajfur, C. Borchers, M.D. Schaller, and K. Jacobson JNK phosphorylates paxillin and regulates cell migration Nature 424 2003 219 223 (Pubitemid 36858692)
29. Z. Huang, D.P. Yan, and B.X. Ge JNK regulates cell migration through promotion of tyrosine phosphorylation of paxillin Cell Signal 20 2008 2002 2012
30. A. Kasorn, P. Alcaide, Y. Jia, K.K. Subramanian, B. Sarraj, Y. Li, F. Loison, H. Hattori, L.E. Silberstein, W.F. Luscinskas, and H.R. Luo Focal adhesion kinase regulates pathogen-killing capability and life span of neutrophils via mediating both adhesion-dependent and -independent cellular signals J Immunol 183 2009 1032 1043
31. B. Bisht, K. Srinivasan, and C.S. Dey In vivo inhibition of focal adhesion kinase causes insulin resistance J Physiol 586 2008 3825 3837
32. J.V. Bonventre Mechanisms of ischemic acute renal failure Kidney Int 43 1993 1160 1178 (Pubitemid 23137105)
33. Z.S. Hakim, L.A. DiMichele, M. Rojas, D. Meredith, C.P. Mack, and J.M. Taylor FAK regulates cardiomyocyte survival following ischemia/reperfusion J Mol Cell Cardiol 46 2009 241 248
34. C. Werno, H. Menrad, A. Weigert, N. Dehne, S. Goerdt, K. Schledzewski, J. Kzhyshkowska, and B. Brune Knockout of HIF-1alpha in tumor-associated macrophages enhances M2 polarization and attenuates their pro-angiogenic responses Carcinogenesis 31 2010 1863 1872
35. G. Stokman, J.C. Leemans, N. Claessen, J.J. Weening, and S. Florquin Hematopoietic stem cell mobilization therapy accelerates recovery of renal function independent of stem cell contribution J Am Soc Nephrol 16 2005 1684 1692 (Pubitemid 41716474)
36. A.B. Sanz, M.D. Sanchez-Nino, A.M. Ramos, J.A. Moreno, B. Santamaria, M. Ruiz-Ortega, J. Egido, and A. Ortiz NF-kappaB in renal inflammation J Am Soc Nephrol 21 2010 1254 1262
37. M.H. De Borst, J. Prakash, W.B. Melenhorst, M.C. van den Heuvel, R.J. Kok, G. Navis, and H. van Goor Glomerular and tubular induction of the transcription factor c-Jun in human renal disease J Pathol 213 2007 219 228 (Pubitemid 47612244)
38. M. de Graauw, I. Tijdens, R. Cramer, S. Corless, J.F. Timms, and B. van de Water Heat shock protein 27 is the major differentially phosphorylated protein involved in renal epithelial cellular stress response and controls focal adhesion organization and apoptosis J Biol Chem 280 2005 29885 29898 (Pubitemid 41177066)
39. T. Takino, M. Nakada, H. Miyamori, Y. Watanabe, T. Sato, D. Gantulga, K. Yoshioka, K.M. Yamada, and H. Sato JSAP1/JIP3 cooperates with focal adhesion kinase to regulate c-Jun N-terminal kinase and cell migration J Biol Chem 280 2005 37772 37781 (Pubitemid 41642387)
40. Q. Shi, A.B. Hjelmeland, S.T. Keir, L. Song, S. Wickman, D. Jackson, O. Ohmori, D.D. Bigner, H.S. Friedman, and J.N. Rich A novel low-molecular weight inhibitor of focal adhesion kinase TAE226, inhibits glioma growth Mol Carcinog 46 2007 488 496 (Pubitemid 46897053)