Proximal tubule-specific overexpression of netrin-1 suppresses acute kidney injury-induced interstitial fibrosis and glomerulosclerosis through suppression of IL-6/STAT3 signaling

American Journal of Physiology - Renal Physiology

Volumn 304, Issue 8, 2013, Pages 1054-1065

  Ranganathan, Punithavathi ^a   Jayakumar, Calpurnia ^a   Ramesh, Ganesan ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Acute kidney injury; Glomerular sclerosis; Interstitial fibrosis; Netrin 1; STAT3

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 4; CREATININE; INTERLEUKIN 6; NETRIN 1; STAT3 PROTEIN;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY DENSITY; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CYTOKINE PRODUCTION; DISEASE EXACERBATION; EPITHELIUM CELL; FIBROGENESIS; GLOMERULOSCLEROSIS; HISTOLOGY; IN VIVO STUDY; KIDNEY BLOOD FLOW; KIDNEY CORTEX; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY ISCHEMIA; KIDNEY MEDULLA; KIDNEY PROXIMAL TUBULE; MACROPHAGE MIGRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; WILD TYPE;

EID: 84878658824     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00650.2012     Document Type: Article

References (31)

1. Bonner JC. Regulation of PDGF and its receptors in fibrotic diseases. Cytokine Growth Factor Rev 15: 255-273, 2004.
2. Chertow GM, Soroko SH, Paganini EP, Cho KC, Himmelfarb J, Ikizler TA, Mehta RL. Mortality after acute renal failure: models for prognostic stratification and risk adjustment. Kidney Int 70: 1120-1126, 2006.
3. Chow F, Ozols E, Nikolic-Paterson DJ, Atkins RC, Tesch GH. Macrophages in mouse type 2 diabetic nephropathy: correlation with diabetic state and progressive renal injury. Kidney Int 65: 116-128, 2004.
4. de Borst MH, Prakash J, Sandovici M, Klok PA, Hamming I, Kok RJ, Navis G, van Goor H. c-Jun NH2-terminal kinase is crucially involved in renal tubulo-interstitial inflammation. J Pharmacol Exp Ther 331: 896-905, 2009.
5. Furuichi K, Wada T, Iwata Y, Kitagawa K, Kobayashi K, Hashimoto H, Ishiwata Y, Asano M, Wang H, Matsushima K, Takeya M, Kuziel WA, Mukaida N, Yokoyama H. CCR2 signaling contributes to ischemia-reperfusion injury in kidney. J Am Soc Nephrol 14: 2503-2515, 2003.
6. Galkina E, Ley K. Leukocyte recruitment and vascular injury in diabetic nephropathy. J Am Soc Nephrol 17: 368-377, 2006.
7. Gandolfo MT, Jang HR, Bagnasco SM, Ko GJ, Agreda P, Satpute SR, Crow MT, King LS, Rabb H. Foxp3 + regulatory T cells participate in repair of ischemic acute kidney injury. Kidney Int 76: 717-729, 2009.
8. 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.
9. Harcourt BE, Forbes JM, Matthews VB. Obesity-induced renal impairment is exacerbated in interleukin-6-knockout mice. Nephrology 17: 257-262, 2012.
10. Himmelfarb J, Joannidis M, Molitoris B, Schietz M, Okusa MD, Warnock D, Laghi F, Goldstein SL, Prielipp R, Parikh CR, Pannu N, Lobo SM, Shah S, D'Intini V, Kellum JA. Evaluation and initial management of acute kidney injury. Clin J Am Soc Nephrol 3: 962-967, 2008.
11. Jayakumar C, Mohamed R, Ranganathan PV, Ramesh G. Intracellular kinases mediate increased translation and secretion of netrin-1 from renal tubular epithelial cells. PLoS ONE 6: e26776, 2011.
12. Kielar ML, John R, Bennett M, Richardson JA, Shelton JM, Chen L, Jeyarajah DR, Zhou XJ, Zhou H, Chiquett B, Nagami GT, Lu CY. Maladaptive role of IL-6 in ischemic acute renal failure. J Am Soc Nephrol 16: 3315-3325, 2005.
13. Lee S, Huen S, Nishio H, Nishio S, Lee HK, Choi BS, Ruhrberg C, Cantley LG. Distinct macrophage phenotypes contribute to kidney injury and repair. J Am Soc Nephrol 22: 317-326, 2011.
14. 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.
15. 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.
16. Ly NP, Komatsuzaki K, Fraser IP, Tseng AA, Prodhan P, Moore KJ, Kinane TB. Netrin-1 inhibits leukocyte migration in vitro and in vivo. Proc Natl Acad Sci USA 102: 14729-14734, 2005.
17. Mazelin L, Bernet A, Bonod-Bidaud C, Pays L, Arnaud S, Gespach C, Bredesen DE, Scoazec JY, Mehlen P. Netrin-1 controls colorectal tumorigenesis by regulating apoptosis. Nature 431: 80-84, 2004.
18. Mirakaj V, Thix CA, Laucher S, Mielke C, Morote-Garcia JC, Schmit MA, Henes J, Unertl KE, Köhler D, Rosenberger P. Netrin-1 dampens pulmonary inflammation during acute lung injury. Am J Respir Crit Care Med 181: 815-824, 2010.
19. Mohamed R, Jayakumar C, Ranganathan PV, Ganapathy V, Ramesh G. Kidney proximal tubular epithelial-specific overexpression of netrin-1 suppresses inflammation and albuminuria through suppression of COX-2-mediated PGE2 production in streptozotocin-induced diabetic mice. Am J Pathol 181: 1991-2002, 2012.
20. Navarro-Gonzalez JF, Mora-Fernandez C. The role of inflammatory cytokines in diabetic nephropathy. J Am Soc Nephrol 19: 433-442, 2008.
21. Pang M, Ma L, Gong R, Tolbert E, Mao H, Ponnusamy M, Chin YE, Yan H, Dworkin LD, Zhuang S. A novel STAT3 inhibitor, S3I-201, attenuates renal interstitial fibroblast activation and interstitial fibrosis in obstructive nephropathy. Kidney Int 78: 257-268, 2010.
22. Ramesh G, Reeves WB. p38 MAP kinase inhibition ameliorates cisplatin nephrotoxicity in mice. Am J Physiol Renal Physiol 289: F166-F174, 2005.
23. Rosenberger P, Schwab JM, Mirakaj V, Masekowsky E, Mager A, Morote-Garcia JC, Unertl K, Eltzschig HK. Hypoxia-inducible factor-dependent induction of netrin-1 dampens inflammation caused by hypoxia. Nat Immunol 10: 195-202, 2009.
24. Squarize CH, Castilho RM, Sriuranpong V, Pinto DS Jr, Gutkind JS. Molecular cross-talk between the NFkappaB and STAT3 signaling pathways in head and neck squamous cell carcinoma. Neoplasia 8: 733-746, 2006.
25. Tadagavadi RK, Wang W, Ramesh G. Netrin-1 regulates Th1/Th2/Th17 cytokine production and inflammation through UNC5B receptor and protects kidney against ischemia-reperfusion injury. J Immunol 185: 3750-3758, 2010.
26. Waikar SS, Liu KD, Chertow GM. Diagnosis, epidemiology and outcomes of acute kidney injury. Clin J Am Soc Nephrol 3: 844-861, 2008.
27. Wang W, Reeves WB, Pays L, Mehlen P, Ramesh G. Netrin-1 over-expression protects kidney from ischemia reperfusion injury by suppressing apoptosis. Am J Pathol 175: 1010-1018, 2009.
28. Wang W, Reeves WB, Ramesh G. Netrin-1 and kidney injury. I. Netrin-1 protects against ischemia-reperfusion injury of the kidney. Am J Physiol Renal Physiol 294: F739-F747, 2008.
29. Wang W, Reeves WB, Ramesh G. Netrin-1 increases proliferation and migration of renal proximal tubular epithelial cells via the UNC5B receptor. Am J Physiol Renal Physiol 296: F723-F729, 2009.
30. Wang Y, Harris DCH. Macrophages in renal disease. J Am Soc Nephrol 22: 21-27, 2011.
31. 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.