Blockade of cysteine-rich protein 61 attenuates renal inflammation and fibrosis after ischemic kidney injury

American Journal of Physiology - Renal Physiology

Volumn 307, Issue 5, 2014, Pages

  Lai, Chun Fu ^a,b   Lin, Shuei Liong ^a,b   Chiang, Wen Chih ^b   Chen, Yung Ming ^b   Wu, Vin Cent ^b   Young, Guang Huar ^b   Ko, Wen Jo ^b   Kuo, Min Liang ^c   Tsai, Tun Jun ^b   Wu, Kwan Dun ^b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Acute kidney injury; Cysteine rich protein 61; Fibrosis; Inflammation; Macrophages

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; CYSTEINE RICH PROTEIN 61; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 2; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PLASMINOGEN ACTIVATOR INHIBITOR 1; TRANSFORMING GROWTH FACTOR BETA; ANTIIDIOTYPIC ANTIBODY; CCL2 PROTEIN, MOUSE; CYR61 PROTEIN, MOUSE; PROTEASE NEXIN I; SERPINE2 PROTEIN, MOUSE;

ACUTE KIDNEY FAILURE; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL CULTURE; CELL INFILTRATION; CLINICAL ARTICLE; COLLAGEN FIBRIL; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; HUMAN; KIDNEY CELL; KIDNEY FIBROSIS; KIDNEY ISCHEMIA; KIDNEY TUBULE EPITHELIUM; MACROPHAGE; MALE; MOUSE; NEPHRITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; UPREGULATION; URINARY EXCRETION; ANIMAL; ANOXIA; ANTAGONISTS AND INHIBITORS; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; FIBROSIS; IMMUNOLOGY; IN VITRO STUDY; INSTITUTE FOR CANCER RESEARCH MOUSE; KIDNEY; KIDNEY PROXIMAL TUBULE; METABOLISM; PATHOLOGY;

ACUTE KIDNEY INJURY; ANIMALS; ANOXIA; ANTIBODIES, ANTI-IDIOTYPIC; CELLS, CULTURED; CHEMOKINE CCL2; CYSTEINE-RICH PROTEIN 61; DISEASE MODELS, ANIMAL; FIBROSIS; IN VITRO TECHNIQUES; INTERLEUKIN-6; KIDNEY; KIDNEY TUBULES, PROXIMAL; MALE; MICE; MICE, INBRED ICR; NEPHRITIS; REPERFUSION INJURY; SERPIN E2; TRANSFORMING GROWTH FACTOR BETA;

EID: 84906901606     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00670.2013     Document Type: Article

References (50)

1. Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res 97: 512-523, 2005.
2. Bai T, Chen CC, Lau LF. Matricellular protein CCN1 activates a proinflammatory genetic program in murine macrophages. J Immunol 184: 3223-3232, 2010.
3. Basile DP. The endothelial cell in ischemic acute kidney injury: implications for acute and chronic function. Kidney Int 72: 151-156, 2007.
4. Basile DP, Fredrich K, Chelladurai B, Leonard EC, Parrish AR. Renal ischemia reperfusion inhibits VEGF expression and induces ADAMTS-1, a novel VEGF inhibitor. Am J Physiol Renal Physiol 294: F928-F936, 2008.
5. Basile DP, Friedrich JL, Spahic J, Knipe N, Mang H, Leonard EC, Changizi-Ashtiyani S, Bacallao RL, Molitoris BA, Sutton TA. Impaired endothelial proliferation and mesenchymal transition contribute to vascular rarefaction following acute kidney injury. Am J Physiol Renal Physiol 300: F721-F733, 2011.
6. Bonventre JV, Vaidya VS, Schmouder R, Feig P, Dieterle F. Next-generation biomarkers for detecting kidney toxicity. Nat Biotechnol 28: 436-440, 2010.
7. Bonventre JV, Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest 121: 4210-4221, 2011.
8. Castaño AP, Lin SL, Surowy T, Nowlin BT, Turlapati SA, Patel T, Singh A, Li S, Lupher ML Jr, Duffield JS. Serum amyloid P inhibits fibrosis through Fc R-dependent monocyte-macrophage regulation in vivo. Sci Transl Med 1: 5ra13, 2009.
9. Chen CC, Lau LF. Functions and mechanisms of action of CCN matricellular proteins. Int J Biochem Cell Biol 41: 771-783, 2009.
10. Chen CC, Mo FE, Lau LF. The angiogenic factor Cyr61 activates a genetic program for wound healing in human skin fibroblasts. J Biol Chem 276: 47329-47337, 2001.
11. Chen Y, Du XY. Functional properties and intracellular signaling of CCN1/Cyr61. J Cell Biochem 100: 1337-1345, 2007.
12. Chen YM, Lin SL, Chen CW, Chiang WC, Tsai TJ, Hsieh BS. Tumor necrosis factor-stimulates fractalkine production by mesangial cells and regulates monocyte transmigration: down-regulation by cAMP. Kidney Int 63: 474-486, 2003.
13. Chertow GM, Burdick E, Honour M, Bonventre JV, Bates DW. Acute kidney injury, mortality, length of stay, and costs in hospitalized patients. J Am Soc Nephrol 16: 3365-3370, 2005.
14. Chevalier RL, Forbes MS, Thornhill BA. Ureteral obstruction as a model of renal interstitial fibrosis and obstructive nephropathy. Kidney Int 75: 1145-1152, 2009.
15. Duffield JS. Macrophages and immunologic inflammation of the kidney. Semin Nephrol 30: 234-254, 2010.
16. Gammelager H, Christiansen CF, Johansen MB, Tonnesen E, Jespersen B, Sorensen HT. Five-year risk of end-stage renal disease among intensive care patients surviving dialysis-requiring acute kidney injury: a nationwide cohort study. Crit Care 17: R145, 2013.
17. Geng H, Lan R, Wang G, Siddiqi AR, Naski MC, Brooks AI, Barnes JL, Saikumar P, Weinberg JM, Venkatachalam MA. Inhibition of autoregulated TGF signaling simultaneously enhances proliferation and differentiation of kidney epithelium and promotes repair following renal ischemia. Am J Pathol 174: 1291-1308, 2009.
18. Grgic I, Campanholle G, Bijol V, Wang C, Sabbisetti VS, Ichimura T, Humphreys BD, Bonventre JV. Targeted proximal tubule injury triggers interstitial fibrosis and glomerulosclerosis. Kidney Int 82: 172-183, 2012.
19. Haase M, Bellomo R, Matalanis G, Calzavacca P, Dragun D, Haase-Fielitz A. A comparison of the RIFLE and Acute Kidney Injury Network classifications for cardiac surgery-associated acute kidney injury: a prospective cohort study. J Thorac Cardiovasc Surg 138: 1370-1376, 2009.
20. Han WK, Waikar SS, Johnson A, Betensky RA, Dent CL, Devarajan P, Bonventre JV. Urinary biomarkers in the early diagnosis of acute kidney injury. Kidney Int 73: 863-869, 2008.
21. Huang TM, Wu VC, Young GH, Lin YF, Shiao CC, Wu PC, Li WY, Yu HY, Hu FC, Lin JW, Chen YS, Lin YH, Wang SS, Hsu RB, Chang FC, Chou NK, Chu TS, Yeh YC, Tsai PR, Huang JW, Lin SL, Chen YM, Ko WJ, Wu KD; National Taiwan University Hospital Study Group of Acute Renal Failure. Preoperative proteinuria predicts adverse renal outcomes after coronary artery bypass grafting. J Am Soc Nephrol 22: 156-163, 2011.
22. Jun JI, Lau LF. The matricellular protein CCN1 induces fibroblast senescence and restricts fibrosis in cutaneous wound healing. Nat Cell Biol 12: 676-685, 2010.
23. Kim KH, Chen CC, Monzon RI, Lau LF. Matricellular protein CCN1 promotes regression of liver fibrosis through induction of cellular senescence in hepatic myofibroblasts. Mol Cell Biol 33: 2078-2090, 2013.
24. Ko GJ, Boo CS, Jo SK, Cho WY, Kim HK. Macrophages contribute to the development of renal fibrosis following ischaemia/reperfusion-induced acute kidney injury. Nephrol Dial Transplant 23: 842-852, 2008.
25. Ko GJ, Grigoryev DN, Linfert D, Jang HR, Watkins T, Cheadle C, Racusen L, Rabb H. Transcriptional analysis of kidneys during repair from AKI reveals possible roles for NGAL and KIM-1 as biomarkers of AKI-to-CKD transition. Am J Physiol Renal Physiol 298: F1472-F1483, 2010.
26. Kular L, Pakradouni J, Kitabgi P, Laurent M, Martinerie C. The CCN family: a new class of inflammation modulators? Biochimie 93: 377-388, 2011.
27. Lai CF, Chen YM, Chiang WC, Lin SL, Kuo ML, Tsai TJ. Cysteinerich protein 61 plays a proinflammatory role in obstructive kidney fibrosis. PLOS ONE 8: e56481, 2013.
28. Lai CF, Wu VC, Huang TM, Yeh YC, Wang KC, Han YY, Lin YF, Jhuang YJ, Chao CT, Shiao CC, Tsai PR, Hu FC, Chou NK, Ko WJ, Wu KD; and the National Taiwan University Hospital Study Group on Acute Renal Failure. Kidney function decline after a non-dialysis-requiring acute kidney injury is associated with higher long-term mortality in critically ill survivors. Crit Care 16: R123, 2012.
29. Lech M, Rommele C, Grobmayr R, Eka Susanti H, Kulkarni OP, Wang S, Grone HJ, Uhl B, Reichel C, Krombach F, Garlanda C, Mantovani A, Anders HJ. Endogenous and exogenous pentraxin-3 limits postischemic acute and chronic kidney injury. Kidney Int 83: 647-661, 2013.
30. Li PK, Burdmann EA, Mehta RL. Acute kidney injury: global health alert. Acta Nephrologica 27: 5-10, 2013.
31. Liangos O, Perianayagam MC, Vaidya VS, Han WK, Wald R, Tighiouart H, MacKinnon RW, Li L, Balakrishnan VS, Pereira BJ, Bonventre JV, Jaber BL. Urinary N-acetyl--(D)-glucosaminidase activity and kidney injury molecule-1 level are associated with adverse outcomes in acute renal failure. J Am Soc Nephrol 18: 904-912, 2007.
32. Lin SL, Chang FC, Schrimpf C, Chen YT, Wu CF, Wu VC, Chiang WC, Kuhnert F, Kuo CJ, Chen YM, Wu KD, Tsai TJ, Duffield JS. Targeting endothelium-pericyte cross talk by inhibiting VEGF receptor signaling attenuates kidney microvascular rarefaction and fibrosis. Am J Pathol 178: 911-923, 2011.
33. Lin SL, Chen RH, Chen YM, Chiang WC, Lai CF, Wu KD, Tsai TJ. Pentoxifylline attenuates tubulointerstitial fibrosis by blocking Smad3/4-activated transcription and profibrogenic effects of connective tissue growth factor. J Am Soc Nephrol 16: 2702-2713, 2005.
34. Lin SL, Chen YM, Chien CT, Chiang WC, Tsai CC, Tsai TJ. Pentoxifylline attenuated the renal disease progression in rats with remnant kidney. J Am Soc Nephrol 13: 2916-2929, 2002.
35. Lin SL, Kisseleva T, Brenner DA, Duffield JS. Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol 173: 1617-1627, 2008.
36. Lin SL, Li B, Rao S, Yeo EJ, Hudson TE, Nowlin BT, Pei H, Chen L, Zheng JJ, Carroll TJ, Pollard JW, McMahon AP, Lang RA, Duffield JS. Macrophage Wnt7b is critical for kidney repair and regeneration. Proc Natl Acad Sci USA 107: 4194-4199, 2010.
37. Lo LJ, Go AS, Chertow GM, McCulloch CE, Fan D, Ordonez JD, Hsu CY. Dialysis-requiring acute renal failure increases the risk of progressive chronic kidney disease. Kidney Int 76: 893-899, 2009.
38. Lobel M, Bauer S, Meisel C, Eisenreich A, Kudernatsch R, Tank J, Rauch U, Kuhl U, Schultheiss HP, Volk HD, Poller W, Scheibenbogen C. CCN1: a novel inflammation-regulated biphasic immune cell migration modulator. Cell Mol Life Sci 69: 3101-3113, 2012.
39. Ma LJ, Fogo AB. PAI-1 and kidney fibrosis. Front Biosci 14: 2028-2041, 2009.
40. Muramatsu Y, Tsujie M, Kohda Y, Pham B, Perantoni AO, Zhao H, Jo SK, Yuen PS, Craig L, Hu X, Star RA. Early detection of cysteine rich protein 61 (CYR61, CCN1) in urine following renal ischemic reperfusion injury. Kidney Int 62: 1601-1610, 2002.
41. Rao S, Lobov IB, Vallance JE, Tsujikawa K, Shiojima I, Akunuru S, Walsh K, Benjamin LE, Lang RA. Obligatory participation of macro-phages in an angiopoietin 2-mediated cell death switch. Development 134: 4449-4458, 2007.
42. Rother M, Krohn S, Kania G, Vanhoutte D, Eisenreich A, Wang X, Westermann D, Savvatis K, Dannemann N, Skurk C, Hilfiker-Kleiner D, Cathomen T, Fechner H, Rauch U, Schultheiss HP, Heymans S, Eriksson U, Scheibenbogen C, Poller W. Matricellular signaling molecule CCN1 attenuates experimental autoimmune myocarditis by acting as a novel immune cell migration modulator. Circulation 122: 2688-2698, 2010.
43. Saunders WB, Bohnsack BL, Faske JB, Anthis NJ, Bayless KJ, Hirschi KK, Davis GE. Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3. J Cell Biol 175: 179-191, 2006.
44. Semedo P, Donizetti-Oliveira C, Burgos-Silva M, Cenedeze MA, Avancini Costa Malheiros DM, Pacheco-Silva A, Câmara NO. Bone marrow mononuclear cells attenuate fibrosis development after severe acute kidney injury. Lab Invest 90: 685-695, 2010.
45. Suzuki T, Kimura M, Asano M, Fujigaki Y, Hishida A. Role of atrophic tubules in development of interstitial fibrosis in microembolism-induced renal failure in rat. Am J Pathol 158: 75-85, 2001.
46. Venkatachalam MA, Griffin KA, Lan R, Geng H, Saikumar P, Bidani AK. Acute kidney injury: a springboard for progression in chronic kidney disease. Am J Physiol Renal Physiol 298: F1078-F1094, 2010.
47. Wald R, Quinn RR, Luo J, Li P, Scales DC, Mamdani MM, Ray JG; University of Toronto Acute Kidney Injury Research Group. Chronic dialysis and death among survivors of acute kidney injury requiring dialysis. JAMA 302: 1179-1185, 2009.
48. Wu CF, Chiang WC, Lai CF, Chang FC, Chen YT, Chou YH, Wu TH, Linn GR, Ling H, Wu KD, Tsai TJ, Chen YM, Duffield JS, Lin SL. Transforming growth factor-1 stimulates profibrotic epithelial signaling to activate pericyte-myofibroblast transition in obstructive kidney fibrosis. Am J Pathol 182: 118-131, 2013.
49. Wu VC, Huang TM, Lai CF, Shiao CC, Lin YF, Chu TS, Wu PC, Chao CT, Wang JY, Kao TW, Young GH, Tsai PR, Tsai HB, Wang CL, Wu MS, Chiang WC, Tsai IJ, Hu FC, Lin SL, Chen YM, Tsai TJ, Ko WJ, Wu KD. Acute-on-chronic kidney injury at hospital discharge is associated with long-term dialysis and mortality. Kidney Int 80: 1222-1230, 2011.
50. Yang L, Besschetnova TY, Brooks CR, Shah JV, Bonventre JV. Epithelial cell cycle arrest in G2/M mediates kidney fibrosis after injury. Nat Med 16: 535-543, 2010.