Lipoxins attenuate renal fibrosis by inducing let-7c and suppressing TGFβR1

Journal of the American Society of Nephrology

Volumn 24, Issue 4, 2013, Pages 627-637

  Brennan, Eoin P ^a   Nolan, Karen A ^a   Börgeson, Emma ^a   Gough, Oisín S ^a   McEvoy, Caitríona M ^a,c   Docherty, Neil G ^b   Higgins, Debra F ^a   Murphy, Madeline ^a   Sadlier, Denise M ^a,c   Ali Shah, Syed Tasadaque ^a   Guiry, Patrick J ^a   Savage, David A ^d   Maxwell, Alexander P ^d   Martin, Finian ^a   Godson, Catherine ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c MATER MISERICORDIAE UNIVERSITY HOSPITAL   (Ireland)

^d QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; JAGGED1; LIPOXIN A; MICRORNA; MICRORNA LET 7C; NERVE CELL ADHESION MOLECULE; THROMBOSPONDIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG TARGETING; EPITHELIUM CELL; HUMAN; HUMAN CELL; KIDNEY BIOPSY; KIDNEY EPITHELIUM; KIDNEY FIBROSIS; KIDNEY PROXIMAL TUBULE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84875711412     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2012060550     Document Type: Article

References (47)

1. Serhan CN: Lipoxins and aspirin-triggered 15-epi-lipoxins are the first lipid mediators of endogenous anti-inflammation and resolution. Prostaglandins Leukot Essent Fatty Acids 73: 141-162, 2005
2. Serhan CN: Lipoxins and aspirin-triggered 15-epi-lipoxins are endogenous components of antiinflammation: Emergence of the counterregulatory side. Arch Immunol Ther Exp (Warsz) 49: 177-188, 2001
3. Serhan CN: Lipoxins and novel aspirin-triggered 15-epi-lipoxins (ATL): A jungle of cell-cell interactions or a therapeutic opportunity? Prostaglandins 53: 107-137, 1997
4. Serhan CN, Chiang N: Lipid-derived mediators in endogenous antiinflammation and resolution: Lipoxins and aspirin-triggered 15-epilipoxins. Scientific World Journal 2: 169-204, 2002
5. Börgeson E, Docherty NG, Murphy M, Rodgers K, Ryan A, O'Sullivan TP, Guiry PJ, Goldschmeding R, Higgins DF, Godson C: Lipoxin A4 and benzo-lipoxin A4 attenuate experimental renal fibrosis. FASEB J 25: 2967-2979, 2011
6. Grumbach Y, Quynh NV, Chiron R, Urbach V: LXA4 stimulates ZO-1 expression and transepithelial electrical resistance in human airway epithelial (16HBE14o-) cells. Am J Physiol Lung Cell Mol Physiol 296: L101-L108, 2009
7. Kalluri R, Neilson EG: Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 112: 1776-1784, 2003
8. Zeisberg M, Duffield JS: Resolved: EMT produces fibroblasts in the kidney. J Am Soc Nephrol 21: 1247-1253, 2010
9. Croce CM, Calin GA: miRNAs, cancer, and stem cell division. Cell 122: 6-7, 2005
10. Lee YS, Dutta A: MicroRNAs in cancer. Annu Rev Pathol 4: 199-227, 2009
11. Urbich C, Kuehbacher A, Dimmeler S: Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 79: 581-588, 2008
12. Kartha RV, Subramanian S: MicroRNAs in cardiovascular diseases: Biology and potential clinical applications. J Cardiovasc Transl Res 3: 256-270, 2010
13. Kato M, Zhang J, Wang M, Lanting L, Yuan H, Rossi JJ, Natarajan R: MicroRNA-192 in diabetic kidney glomeruli and its function in TGFbeta-induced collagen expression via inhibition of E-box repressors. Proc Natl Acad Sci U S A 104: 3432-3437, 2007
14. Wang Q, Wang Y, Minto AW, Wang J, Shi Q, Li X,Quigg RJ:MicroRNA-377 is up-regulated and can lead to increased fibronectinproduction in diabetic nephropathy. FASEB J 22: 4126-4135, 2008
15. Long J, Wang Y, Wang W, Chang BH, Danesh FR: Identification of microRNA-93 as a novel regulator of vascular endothelial growth factor in hyperglycemic conditions. J Biol Chem285: 23457-23465, 2010
16. Fiore S, Ryeom SW, Weller PF, Serhan CN: Lipoxin recognition sites. Specific binding of labeled lipoxin A4 with human neutrophils. J Biol Chem 267: 16168-16176, 1992
17. Mitchell D, Rodgers K, Hanly J, McMahon B, Brady HR, Martin F, Godson C: Lipoxins inhibit Akt/PKB activation and cell cycle progression in human mesangial cells. Am J Pathol 164: 937-946, 2004
18. Rodgers K, McMahon B, Mitchell D, Sadlier D, Godson C: Lipoxin A4 modifies platelet-derived growth factor-induced pro-fibrotic gene expression in human renal mesangial cells. Am J Pathol 167: 683-694, 2005
19. Ahn SH, Susztak K: Getting a notch closer to understanding diabetic kidney disease. Diabetes 59: 1865-1867, 2010
20. Murea M, Park JK, Sharma S, Kato H, Gruenwald A, Niranjan T, Si H, Thomas DB, Pullman JM, Melamed ML, Susztak K: Expression of Notch pathway proteins correlates with albuminuria, glomerulosclerosis, and renal function. Kidney Int 78: 514-522, 2010
21. Walsh DW, Roxburgh SA, McGettigan P, Berthier CC, Higgins DG, Kretzler M, Cohen CD, Mezzano S, Brazil DP,Martin F: Co-regulation of Gremlin and Notch signalling in diabetic nephropathy. Biochim Biophys Acta 1782: 10-21, 2008
22. Le Y, Yazawa H, Gong W, Yu Z, Ferrans VJ, Murphy PM, Wang JM: The neurotoxic prion peptide fragment PrP(106-126) is a chemotactic agonist for theGprotein-coupled receptor formyl peptide receptor-like 1. J Immunol 166: 1448-1451, 2001
23. Sun Y, Koo S, White N, Peralta E, Esau C, Dean NM, Perera RJ: Development of a micro-array to detect human and mouse microRNAs and characterization of expression in human organs. Nucleic Acids Res 32: e188, 2004
24. Roush S, Slack FJ: The let-7 family of microRNAs. Trends Cell Biol 18: 505-516, 2008
25. Krupa A, Jenkins R, Luo DD, Lewis A, Phillips A, Fraser D: Loss of MicroRNA-192 promotes fibrogenesis in diabetic nephropathy. J Am Soc Nephrol 21: 438-447, 2010
26. Wang B, Herman-Edelstein M, Koh P, Burns W, Jandeleit-Dahm K, Watson A, Saleem M, Goodall GJ, Twigg SM, Cooper ME, Kantharidis P: E-cadherin expression is regulated by miR-192/215 by a mechanism that is independent of the profibrotic effects of transforming growth factor-beta. Diabetes 59: 1794-1802, 2010
27. Brennan EP, Morine MJ, Walsh DW, Roxburgh SA, Lindenmeyer MT, Brazil DP, Gaora PO, Roche HM, Sadlier DM, Cohen CD, Godson C, Martin F; GENIE Consortium: Next-generation sequencing identifies TGF-b1-associated gene expression profiles in renal epithelial cells reiterated in human diabetic nephropathy. Biochim Biophys Acta 1822: 589-599, 2012
28. Ozsolak F, Poling LL,Wang Z, Liu H, Liu XS, Roeder RG, Zhang X, Song JS, Fisher DE: Chromatin structure analyses identify miRNA promoters. Genes Dev 22: 3172-3183, 2008
29. Corcoran DL, Pandit KV, Gordon B, Bhattacharjee A, Kaminski N, Benos PV: Features of mammalian microRNA promoters emerge from polymerase II chromatin immunoprecipitation data. PLoS ONE 4: e5279, 2009
30. Thuault S, Valcourt U, Petersen M, Manfioletti G, Heldin CH, Moustakas A: Transforming growth factor-beta employs HMGA2 to elicit epithelialmesenchymal transition. J Cell Biol 174: 175-183, 2006
31. Schmid H, Boucherot A, Yasuda Y, Henger A, Brunner B, Eichinger F, Nitsche A, Kiss E, Bleich M, Gröne HJ, Nelson PJ, Schlöndorff D, Cohen CD, Kretzler M; European Renal cDNA Bank (ERCB) Consortium: Modular activation of nuclear factor-kappaB transcriptional programs in human diabetic nephropathy. Diabetes 55: 2993-3003, 2006
32. Woroniecka KI, Park AS,Mohtat D, Thomas DB, Pullman JM, Susztak K: Transcriptome analysis of human diabetic kidney disease. Diabetes 60: 2354-2369, 2011
33. Reich HN, Tritchler D, Cattran DC, Herzenberg AM, Eichinger F, Boucherot A, Henger A, Berthier CC, Nair V, Cohen CD, Scholey JW, Kretzler M: A molecular signature of proteinuria in glomerulonephritis. PLoS ONE 5: e13451, 2010
34. Hodgin JB, Borczuk AC, Nasr SH, Markowitz GS, Nair V, Martini S, Eichinger F, Vining C, Berthier CC, Kretzler M, D'Agati VD: Amolecular profile of focal segmental glomerulosclerosis from formalin-fixed, paraffin-embedded tissue. Am J Pathol 177: 1674-1686, 2010
35. Morrissey J, Guo G, Moridaira K, Fitzgerald M, McCracken R, Tolley T, Klahr S: Transforming growth factor-beta induces renal epithelial jagged-1 expression in fibrotic disease. J Am Soc Nephrol 13: 1499-1508, 2002
36. Hazan RB, Qiao R, Keren R, Badano I, Suyama K: Cadherin switch in tumor progression. Ann N Y Acad Sci 1014: 155-163, 2004
37. Gravdal K, Halvorsen OJ, Haukaas SA, Akslen LA: A switch from Ecadherin to N-cadherin expression indicates epithelial tomesenchymal transition and is of strong and independent importance for the progress of prostate cancer. Clin Cancer Res 13: 7003-7011, 2007
38. Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H, Harano T, Yatabe Y, Nagino M, Nimura Y, Mitsudomi T, Takahashi T: Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res 64: 3753-3756, 2004
39. Chang CJ, Hsu CC, Chang CH, Tsai LL, Chang YC, Lu SW, Yu CH, Huang HS, Wang JJ, Tsai CH, Chou MY, Yu CC, Hu FW: Let-7d functions as novel regulator of epithelial-mesenchymal transition and chemoresistant property in oral cancer. Oncol Rep 26: 1003-1010, 2011
40. Büssing I, Slack FJ, Grosshans H: let-7 microRNAs in development, stem cells and cancer. Trends Mol Med 14: 400-409, 2008
41. Lee YS, Dutta A: The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev 21: 1025-1030, 2007
42. Yamamoto T, Watanabe T, Ikegaya N, Fujigaki Y, Matsui K, Masaoka H, Nagase M, Hishida A: Expression of types I, II, and III TGF-beta receptors in human glomerulonephritis. J Am Soc Nephrol 9: 2253-2261, 1998
43. Chevalier RL, Forbes MS, Thornhill BA: Ureteral obstruction as a model of renal interstitial fibrosis and obstructive nephropathy. Kidney Int 75: 1145-1152, 2009
44. Higgins DF, Kimura K, Bernhardt WM, Shrimanker N, Akai Y, Hohenstein B, Saito Y, Johnson RS, Kretzler M, Cohen CD, Eckardt KU, Iwano M, Haase VH: Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest 117: 3810-3820, 2007
45. Corcoran DL, Feingold E, Dominick J, Wright M, Harnaha J, Trucco M, Giannoukakis N, Benos PV: Footer: A quantitative comparative genomics method for efficient recognition of cis-regulatory elements. Genome Res 15: 840-847, 2005
46. Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R: Fast and effective prediction of microRNA/target duplexes. RNA 10: 1507-1517, 2004
47. Papadopoulos GL, Alexiou P, Maragkakis M, Reczko M, Hatzigeorgiou AG: DIANA-mirPath: Integrating human and mouse microRNAs in pathways. Bioinformatics 25: 1991-1993, 2009