Endothelial krüppel-like factor 4 mediates the protective effect of statins against ischemic AKI

Journal of the American Society of Nephrology

Volumn 27, Issue 5, 2016, Pages 1379-1388

  Yoshida, Tadashi ^a   Yamashita, Maho ^a   Iwai, Mieko ^a   Hayashi, Matsuhiko ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CREATININE; FLUINDOSTATIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; KRUPPEL LIKE FACTOR 4; TUMOR NECROSIS FACTOR; VASCULAR CELL ADHESION MOLECULE 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; KRUPPEL LIKE FACTOR;

ACUTE KIDNEY FAILURE; ARTICLE; BREEDING; CELL CULTURE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; INFLAMMATORY CELL; KIDNEY ISCHEMIA; LYMPHOCYTE COUNT; MACROPHAGE; MALE; MONOCYTE; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; REPERFUSION INJURY; UREA NITROGEN BLOOD LEVEL; ACUTE KIDNEY INJURY; ANIMAL; BIOSYNTHESIS; ENDOTHELIUM; KIDNEY; METABOLISM; PHYSIOLOGY; VASCULARIZATION;

ACUTE KIDNEY INJURY; ANIMALS; ENDOTHELIUM; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; KIDNEY; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MICE; REPERFUSION INJURY;

EID: 84983786606     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2015040460     Document Type: Article

References (39)

1. Kinsey GR, Li L, Okusa MD: Inflammation in acute kidney injury. Nephron, Exp Nephrol 109: e102-e107, 2008
2. Molitoris BA: Therapeutic translation in acute kidney injury: The epithelial/endothelial axis. J Clin Invest 124: 2355-2363, 2014
3. Kelly KJ, Williams WW Jr, Colvin RB, Bonventre JV: Antibody to intercellular adhesion molecule 1 protects the kidney against ischemic injury. Proc Natl Acad Sci U S A 91: 812-816, 1994
4. Rabb H, Mendiola CC, Saba SR, Dietz JR, Smith CW, Bonventre JV, Ramirez G: Antibodies to ICAM-1 protect kidneys in severe ischemic reperfusion injury. Biochem Biophys Res Commun 211: 67-73, 1995
5. Kapitsinou PP, Sano H, Michael M, Kobayashi H, Davidoff O, Bian A, Yao B, Zhang MZ, Harris RC, Duffy KJ, Erickson-Miller CL, Sutton TA, Haase VH: Endothelial HIF-2 mediates protection and recovery from ischemic kidney injury. J Clin Invest 124: 2396-2409, 2014
6. Haller H, Dragun D, Miethke A, Park JK, Weis A, Lippoldt A, Gross V, Luft FC: Antisense oligonucleotides for ICAM-1 attenuate reperfusion injury and renal failure in the rat. Kidney Int 50: 473-480, 1996
7. Kelly KJ, Williams WW Jr, Colvin RB, Meehan SM, Springer TA, Gutiérrez-Ramos JC, Bonventre JV: Intercellular adhesion molecule-1-deficient mice are protected against ischemic renal injury. J Clin Invest 97: 1056-1063, 1996
8. Yoshida T, Hayashi M: Role of Krüppel-like factor 4 and its binding proteins in vascular disease. J Atheroscler Thromb 21: 402-413, 2014
9. Hamik A, Lin Z, Kumar A, Balcells M, Sinha S, Katz J, Feinberg MW, Gerzsten RE, Edelman ER, Jain MK: Kruppel-like factor 4 regulates endothelial inflammation. J Biol Chem282: 13769-13779, 2007
10. ZhouG,Hamik A, Nayak L, Tian H, Shi H, Lu Y, SharmaN, Liao X, Hale A, BoerboomL, Feaver RE, Gao H, Desai A, Schmaier A, Gerson SL,Wang Y, Atkins GB, Blackman BR, SimonDI, JainMK: Endothelial Kruppel-like factor 4 protects against atherothrombosis in mice. J Clin Invest 122: 4727-4731, 2012
11. Yoshida T, Yamashita M, Horimai C, Hayashi M: Deletion of Krüppellike factor 4 in endothelial and hematopoietic cells enhances neointimal formation following vascular injury. J Am Heart Assoc 3: e000622, 2014
12. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M: Tie2-Cre transgenic mice: A new model for endothelial cell-lineage analysis in vivo. Dev Biol 230: 230-242, 2001
13. Katz JP, Perreault N, Goldstein BG, Lee CS, Labosky PA, Yang VW, Kaestner KH: The zinc-finger transcription factor Klf4 is required for terminal differentiation of goblet cells in the colon. Development 129: 2619-2628, 2002
14. Gueler F, Rong S, Park JK, Fiebeler A, Menne J, Elger M, Mueller DN, Hampich F, Dechend R, Kunter U, Luft FC, Haller H: Postischemic acute renal failure is reduced by short-term statin treatment in a rat model. J Am Soc Nephrol 13: 2288-2298, 2002
15. Nesic Z, Todorovic Z, Stojanovic R, Basta-Jovanovic G,Radojevic-Skodric S, Velickovic R, Chatterjee PK, Thiemermann C, Prostran M: Single-dose intravenous simvastatin treatment attenuates renal injury in an experimental model of ischemia-reperfusion in the rat.JPharmacolSci 102: 413-417, 2006
16. Welten GM, Chonchol M, Schouten O, Hoeks S, Bax JJ, van Domburg RT, van Sambeek M, Poldermans D: Statin use is associated with early recovery of kidney injury after vascular surgery and improved long-term outcome. Nephrol Dial Transplant 23: 3867-3873, 2008
17. Molnar AO, Coca SG, Devereaux PJ, Jain AK, Kitchlu A, Luo J, Parikh CR, Paterson JM, Siddiqui N, Wald R, Walsh M, Garg AX: Statin use associates with a lower incidence of acute kidney injury after major elective surgery. J Am Soc Nephrol 22: 939-946, 2011
18. Homma K, Yoshida T, Yamashita M, Hayashida K, Hayashi M, Hori S: Inhalation of hydrogen gas is beneficial for preventing contrast-induced acute kidney injury in rats. Nephron, Exp Nephrol 128: 116-122, 2014
19. Kato N, Yuzawa Y, Kosugi T, Hobo A, Sato W, Miwa Y, Sakamoto K, Matsuo S, Kadomatsu K: The E-selectin ligand basigin/CD147 is responsible for neutrophil recruitment in renal ischemia/reperfusion. J Am Soc Nephrol 20: 1565-1576, 2009
20. Gueler F, Park JK, Rong S, Kirsch T, Lindschau C, Zheng W, Elger M, Fiebeler A, Fliser D, Luft FC, Haller H: Statins attenuate ischemiareperfusion injury by inducing heme oxygenase-1 in infiltrating macrophages. Am J Pathol 170: 1192-1199, 2007
21. Kentrup D, Reuter S, Schnöckel U, Grabner A, Edemir B, Pavenstädt H, Schober O, Schäfers M, Schlatter E, Büssemaker E: Hydroxyfasudilmediated inhibition of ROCK1 and ROCK2 improves kidney function in rat renal acute ischemia-reperfusion injury. PLoS One 6: e26419, 2011
22. Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T: Transcriptional regulation of endothelial cell adhesionmolecules:NF-k B and cytokine-inducible enhancers. FASEB J 9: 899-909, 1995
23. Kim YS, Ahn Y, Hong MH, Kim KH, Park HW, Hong YJ, Kim JH, Kim W, Jeong MH, Cho JG, Park JC, Kang JC: Rosuvastatin suppresses the inflammatory responses through inhibition of c-Jun N-terminal kinase and Nuclear Factor-kappaB in endothelial cells. J Cardiovasc Pharmacol 49: 376-383, 2007
24. Eccles KA, Sowden H, Porter KE, Parkin SM, Homer-Vanniasinkam S, Graham AM: Simvastatin alters human endothelial cell adhesion molecule expression and inhibits leukocyte adhesion under flow. Atherosclerosis 200: 69-79, 2008
25. Wu K, Tian S, Zhou H, Wu Y: Statins protect human endothelial cells from TNF-induced inflammation via ERK5 activation. Biochem Pharmacol 85: 1753-1760, 2013
26. Constien R, Forde A, Liliensiek B,Gröne HJ,Nawroth P, HämmerlingG, Arnold B: Characterization of a novel EGFP reporter mouse to monitor Cre recombination as demonstrated by a Tie2 Cremouse line. Genesis 30: 36-44, 2001
27. Feinberg MW, Wara AK, Cao Z, Lebedeva MA, Rosenbauer F, Iwasaki H, Hirai H, Katz JP, Haspel RL, Gray S, Akashi K, Segre J, Kaestner KH, Tenen DG, Jain MK: The Kruppel-like factor KLF4 is a critical regulator of monocyte differentiation. EMBO J 26: 4138-4148, 2007
28. Alder JK, Georgantas RW 3rd, Hildreth RL, Kaplan IM, Morisot S, Yu X, McDevitt M, Civin CI: Kruppel-like factor 4 is essential for inflammatory monocyte differentiation in vivo. J Immunol 180: 5645-5652, 2008
29. Thornton MA, Winn R, Alpers CE, Zager RA: An evaluation of the neutrophil as amediator of in vivo renal ischemic-reperfusion injury.Am J Pathol 135: 509-515, 1989
30. Sen-Banerjee S, Mir S, Lin Z, Hamik A, Atkins GB, Das H, Banerjee P, Kumar A, Jain MK: Kruppel-like factor 2 as a novel mediator of statin effects in endothelial cells. Circulation 112: 720-726, 2005
31. Ohnesorge N, Viemann D, Schmidt N, Czymai T, Spiering D, Schmolke M, Ludwig S, Roth J, Goebeler M, Schmidt M: Erk5 activation elicits a vasoprotective endothelial phenotype via induction of Kruppel-like factor 4 (KLF4). J Biol Chem285: 26199-26210, 2010
32. Maejima T, Inoue T, Kanki Y, Kohro T, LiG,Ohta Y, KimuraH, Kobayashi M, Taguchi A, Tsutsumi S, Iwanari H, Yamamoto S, Aruga H, Dong S, Stevens JF, Poh HM, Yamamoto K, Kawamura T, Mimura I, Suehiro J, Sugiyama A, Kaneki K, Shibata H, Yoshinaka Y, Doi T, Asanuma A, Tanabe S, Tanaka T, Minami T, Hamakubo T, Sakai J, Nozaki N, Aburatani H, Nangaku M, Ruan X, Tanabe H, Ruan Y, Ihara S, Endo A, Kodama T, Wada Y: Direct evidence for pitavastatin induced chromatin structure change in the KLF4 gene in endothelial cells. PLoS One 9: e96005, 2014
33. FeinbergMW, Cao Z,Wara AK, LebedevaMA, Senbanerjee S, Jain MK: Kruppel-like factor 4 is a mediator of proinflammatory signaling in macrophages. J Biol Chem 280: 38247-38258, 2005
34. Liao X, Sharma N, Kapadia F, Zhou G, Lu Y, Hong H, Paruchuri K, Mahabeleshwar GH, Dalmas E, Venteclef N, Flask CA, Kim J, Doreian BW, Lu KQ, Kaestner KH, Hamik A, Clément K, Jain MK: Krüppel-like factor 4 regulates macrophage polarization. J Clin Invest 121: 2736-2749, 2011
35. Yoshida T, Kaestner KH, Owens GK: Conditional deletion of Krüppellike factor 4 delays downregulation of smooth muscle cell differentiation markers but accelerates neointimal formation following vascular injury. Circ Res 102: 1548-1557, 2008
36. Yoshida T, Gan Q, Owens GK: Kruppel-like factor 4, Elk-1, and histone deacetylases cooperatively suppress smooth muscle cell differentiation markers in response to oxidized phospholipids. Am J Physiol Cell Physiol 295: C1175-C1182, 2008
37. Yoshida T, YamashitaM, Hayashi M: Kruppel-like factor 4 contributes to high phosphate-induced phenotypic switching of vascular smooth muscle cells into osteogenic cells. J Biol Chem 287: 25706-25714, 2012
38. Yoshida T, Sinha S, Dandré F, Wamhoff BR, HoofnagleMH, Kremer BE, Wang DZ,Olson EN, Owens GK:Myocardin is a key regulator of CArGdependent transcription of multiple smoothmusclemarker genes. Circ Res 92: 856-864, 2003
39. Yoshida T, Yamashita M, Horimai C, Hayashi M: Smooth muscleselective inhibition of nuclear factor-kB attenuates smooth muscle phenotypic switching and neointima formation following vascular injury. J Am Heart Assoc 2: e000230, 2013