Resolvins E1 and D1 inhibit interstitial fibrosis in the obstructed kidney via inhibition of local fibroblast proliferation

Journal of Pathology

Volumn 228, Issue 4, 2012, Pages 506-519

  Qu, Xinli ^a   Zhang, Xueming ^a,b   Yao, Jun ^a   Song, Jiangning ^a   Nikolic Paterson, David J ^a   Li, Jinhua ^a  

^a MONASH UNIVERSITY   (Australia)

^b INNER MONGOLIA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

AKT; ChemR23; ERK; Fibroblast; PDGF; Proliferation; Renal fibrosis; Resolvin; UUO

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ANTIFIBROTIC AGENT; ANTIINFLAMMATORY AGENT; CYCLIN D; MYC PROTEIN; PLATELET DERIVED GROWTH FACTOR BB; RESOLVIN D1; RESOLVIN E1; UNCLASSIFIED DRUG; 5S,12R,18R-TRIHYDROXY-6Z,8E,10E,14Z,16E-EICOSAPENTAENOIC ACID; DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID; PLATELET DERIVED GROWTH FACTOR B; PLATELET-DERIVED GROWTH FACTOR BB; CELL RECEPTOR; CHEMR23 PROTEIN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; CYCLIN DEPENDENT KINASE INHIBITOR 1; FIBRONECTIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGENIC AGENT; PLATELET DERIVED GROWTH FACTOR; PROTEIN KINASE B; PROTEIN P21; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; DOWN REGULATION; KIDNEY DISEASE; KIDNEY FIBROSIS; MALE; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION; URETER OBSTRUCTION; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; DRUG EFFECTS; FIBROBLAST; FIBROSIS; KIDNEY; MACROPHAGE; PATHOLOGY; PRIMARY CELL CULTURE; URETERAL OBSTRUCTION; ANIMAL TISSUE; CONTROLLED STUDY; ENZYME ACTIVATION; IN VITRO STUDY; PROTEIN EXPRESSION;

ANIMALS; CELL PROLIFERATION; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; FIBROBLASTS; FIBROSIS; KIDNEY; MACROPHAGES; MALE; MICE, INBRED C57BL; PRIMARY CELL CULTURE; PROTO-ONCOGENE PROTEINS C-SIS; URETERAL OBSTRUCTION;

EID: 84871217601     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4050     Document Type: Article

References (61)

1. Serhan CN, Yacoubian S, Yang R. Anti-inflammatory and proresolving lipid mediators. Annu Rev Pathol 2008; 3: 279-312.
2. Serhan CN, Clish CB, Brannon J, et al. Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from ω-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. J Exp Med 2000; 192: 1197-1204.
3. Schwab JM, Chiang N, Arita M, et al. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 2007; 447: 869-874.
4. Arita M, Yoshida M, Hong S, et al. Resolvin E1, an endogenous lipid mediator derived from ω-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis. Proc Natl Acad Sci USA 2005; 102: 7671-7676.
5. Hasturk H, Kantarci A, Ohira T, et al. RvE1 protects from local inflammation and osteoclast mediated bone destruction in periodontitis. FASEB J 2006; 20: 401-403.
6. Dona M, Fredman G, Schwab JM, et al. Resolvin E1, an EPAderived mediator in whole blood, selectively counterregulates leukocytes and platelets. Blood 2008; 112: 848-855.
7. Haworth O, Cernadas M, Yang R, et al. Resolvin E1 regulates interleukin 23, interferon-γ and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat Immunol 2008; 9: 873-9.
8. Arita M, Bianchini F, Aliberti J, et al. Stereochemical assignment, anti-inflammatory properties, and receptor for the ω-3 lipid mediator resolvin E1. J Exp Med 2005; 201: 713-722.
9. Arita M, Ohira T, Sun YP, et al. Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation. J Immunol 2007; 178: 3912-3917.
10. Ohira T, Arita M, Omori K, et al. Resolvin E1 receptor activation signals phosphorylation and phagocytosis. J Biol Chem 2010; 285: 3451-3461.
11. Kinsey GR, Li L, Okusa MD. Inflammation in acute kidney injury. Nephron Exp Nephrol 2008; 109: E102-107.
12. Duffield JS, Hong S, Vaidya VS, et al. Resolvin D series and protectin D1 mitigate acute kidney injury. J Immunol 2006; 177: 5902-5911.
13. Serhan CN, Hong S, Gronert K, et al. Resolvins: A family of bioactive products of ω-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med 2002; 196: 1025-1037.
14. Hong S, Gronert K, Devchand PR, et al. Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. Autacoids in anti-inflammation. J Biol Chem 2003; 278: 14677-14687.
15. Sun YP, Oh SF, Uddin J, et al. Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, antiinflammatory properties, and enzymatic inactivation. J Biol Chem 2007; 282: 9323-9334.
16. Grande MT, Ĺopez-Novoa JM. Fibroblast activation and myofibroblast generation in obstructive nephropathy. Nat Rev Nephrol 2009; 5: 319-328.
17. Chevalier RL, Forbes MS, Thornhill BA. Ureteral obstruction as a model of renal interstitial fibrosis and obstructive nephropathy. Kidney Int 2009; 75: 1145-1152.
18. Han Y, Masaki T, Hurst LA, et al. Extracellular signal-regulated kinase-dependent interstitial macrophage proliferation in the obstructed mouse kidney. Nephrology (Carlton) 2008; 13: 411-418.
19. Rajasagi NK, Reddy PB, Suryawanshi A, et al. Controlling herpes simplex virus-induced ocular inflammatory lesions with the lipidderived mediator resolvin E1. J Immunol 2011; 186: 1735-1746.
20. Oh SF, Pillai PS, Recchiuti A, et al. Pro-resolving actions and stereoselective biosynthesis of 18S E-series resolvins in human leukocytes and murine inflammation. J Clin Invest 2011; 121: 569-581.
21. Kasuga K, Yang R, Porter TF, et al. Rapid appearance of resolvin precursors in inflammatory exudates: Novel mechanisms in resolution. J Immunol 2008; 181: 8677-8687.
22. Ariel A, Serhan CN. Resolvins and protectins in the termination program of acute inflammation. Trends Immunol 2007; 28: 176-183.
23. Floege J, Eng E, Young BA, et al. Infusion of platelet-derived growth factor or basic fibroblast growth factor induces selective glomerular mesangial cell proliferation and matrix accumulation in rats. J Clin Invest 1993; 92: 2952-2962.
24. Uehara G, Suzuki D, Toyoda M, et al. Glomerular expression of platelet-derived growth factor (PDGF)-A, -B chain and PDGF receptor-α, -β in human diabetic nephropathy. Clin Exp Nephrol 2004; 8: 36-42.
25. Tang WW, Ulich TR, Lacey DL, et al. Platelet-derived growth factor-BB induces renal tubulointerstitial myofibroblast formation and tubulointerstitial fibrosis. Am J Pathol 1996; 148: 1169-1180.
26. Wang S, Wilkes MC, Leof EB, et al. Imatinib mesylate blocks a non-Smad TGFβ pathway and reduces renal fibrogenesis in vivo. FASEB J 2005; 19: 1-11.
27. Chen YT, Chang FC, Wu CF, et al. Platelet-derived growth factor receptor signaling activates pericyte-myofibroblast transition in obstructive and post-ischemic kidney fibrosis. Kidney Int 2011; 80: 1170-1181.
28. Kinoshita K, Nakagawa K, Hamada J, et al. Imatinib mesylate inhibits the proliferation-stimulating effect of human lung cancerassociated stromal fibroblasts on lung cancer cells. Int J Oncol 2010; 37: 869-977.
29. Millette E, Rauch BH, Defawe O, et al. Platelet-derived growth factor-BB-induced human smooth muscle cell proliferation depends on basic FGF release and FGFR-1 activation. Circ Res 2005; 96: 172-179.
30. Lin Z, Sugai JV, Jin Q, et al. Platelet-derived growth factor- B gene delivery sustains gingival fibroblast signal transduction. J Periodontal Res 2008; 43: 440-449.
31. Jones SM, Klinghoffer R, Prestwich GD, et al. PDGF induces an early and a late wave of PI 3-kinase activity, and only the late wave is required for progression through G1. Curr Biol 1999; 9: 512-521.
32. Jones SM, Kazlauskas A. Growth-factor-dependent mitogenesis requires two distinct phases of signalling. Nat Cell Biol 2001; 3: 165-172.
33. Gille H, Downward J. Multiple ras effector pathways contribute to G1 cell cycle progression. J Biol Chem 1999; 274: 22033-22040.
34. O'Keefe EJ, Pledger WJ. A model of cell cycle control: Sequential events regulated by growth factors. Mol Cell Endocrinol 1983; 31: 167-186.
35. Ho KJ, Spite M, Owens CD, et al. Aspirin-triggered lipoxin and resolvin E1 modulate vascular smooth muscle phenotype and correlate with peripheral atherosclerosis. Am J Pathol 2010; 177: 2116-2123.
36. Owman C, Lolait SJ, Sant́en S, et al. Molecular cloning and tissue distribution of cDNA encoding a novel chemoattractant-like receptor. Biochem Biophys Res Commun 1997; 241: 390-394.
37. Nagle RB, Johnson ME, Jervis HR. Proliferation of renal interstitial cells following injury induced by ureteral obstruction. Lab Invest 1976; 35: 18-22.
38. Grande MT, P'erez-Barriocanal F, L'opez-Novoa JM. Role of inflammation in tubulo-interstitial damage associated to obstructive nephropathy. J Inflamm (Lond) 2010; 7: 19.
39. Snelgrove SL, Kausman JY, Lo C, et al. Renal dendritic cells adopt a pro-inflammatory phenotype in obstructive uropathy to activate T cells but do not directly contribute to fibrosis. Am J Pathol 2012; 180: 91-103.
40. Shappell SB, Gurpinar T, Lechago J, et al. Chronic obstructive uropathy in severe combined immunodeficient (SCID) mice: Lymphocyte infiltration is not required for progressive tubulointerstitial injury. J Am Soc Nephrol 1998; 9: 1008-1017.
41. Tapmeier TT, Fearn A, Brown K, et al. Pivotal role of CD4+ T cells in renal fibrosis following ureteric obstruction. Kidney Int 2010; 78: 351-362.
42. Henderson NC, Mackinnon AC, Farnworth SL, et al. Galectin-3 expression and secretion links macrophages to the promotion of renal fibrosis. Am J Pathol 2008; 172: 288-298.
43. Sung SA, Jo SK, Cho WY, et al. Reduction of renal fibrosis as a result of liposome encapsulated clodronate induced macrophage depletion after unilateral ureteral obstruction in rats. Nephron Exp Nephrol 2007; 105: E1-9.
44. Nishida M, Okumura Y, Fujimoto S, et al. Adoptive transfer of macrophages ameliorates renal fibrosis in mice. Biochem Biophys Res Commun 2005; 332: 11-16.
45. Nishida M, Fujinaka H, Matsusaka T, et al. Absence of angiotensin II type 1 receptor in bone marrow-derived cells is detrimental in the evolution of renal fibrosis. J Clin Invest 2002; 110: 1859-1868.
46. Ma FY, Liu J, Kitching AR, et al. Targeting renal macrophage accumulation via c-fms kinase reduces tubular apoptosis but fails to modify progressive fibrosis in the obstructed rat kidney. Am J Physiol Renal Physiol 2009; 296: F177-F185.
47. Ma FY, Tesch GH, Flavell RA, et al. MKK3-p38 signaling promotes apoptosis and the early inflammatory response in the obstructed mouse kidney. Am J Physiol Renal Physiol 2007; 293: F1556-1563.
48. Morimoto Y, Gai Z, Tanishima H, et al. TNFα deficiency accelerates renal tubular interstitial fibrosis in the late stage of ureteral obstruction. Exp Mol Pathol 2008; 85: 207-213.
49. Jones LK, O'Sullivan KM, Semple T, et al. IL-1RI deficiency ameliorates early experimental renal interstitial fibrosis. Nephrol Dialysis Transpl 2009; 24: 3024-3032.
50. Zhang G, Kim H, Cai X, et al. Urokinase receptor modulates cellular and angiogenic responses in obstructive nephropathy. J Am Soc Nephrol 2003; 14: 1234-1253.
51. Nishida M, Okumura Y, Ozawa S, et al. MMP-2 inhibition reduces renal macrophage infiltration with increased fibrosis in UUO. Biochem Biophys Res Commun 2007; 354: 133-139.
52. Taneda S, Hudkins KL, Topouzis S, et al. Obstructive uropathy in mice and humans: Potential role for PDGF-D in the progression of tubulointerstitial injury. J Am Soc Nephrol 2003; 14: 2544-2555.
53. Oh SJ, Kurz H, Christ B, et al. Platelet-derived growth factor-B induces transformation of fibrocytes into spindle-shaped myofibroblasts in vivo. Histochem Cell Biol 1998; 109: 349-357.
54. Ludewig D, Kosmehl H, Sommer M, et al. PDGF receptor kinase blocker AG1295 attenuates interstitial fibrosis in rat kidney after unilateral obstruction. Cell Tissue Res 2000; 299: 97-103.
55. Floege J, Eitner F, Alpers CE. A new look at platelet-derived growth factor in renal disease. J Am Soc Nephrol 2008; 19: 12-23.
56. Ostendorf T, Eitner F, Floege J. The PDGF family in renal fibrosis. Pediat Nephrol, Online FirstTM, 20 May 2011.
57. Samson M, Edinger AL, Stordeur P, et al. ChemR23, a putative chemoattractant receptor, is expressed in monocyte-derived dendritic cells and macrophages and is a coreceptor for SIV and some primary HIV-1 strains. Eur J Immunol 1998; 28: 1689-1700.
58. Zhao RJ, Wang H. Chemerin/ChemR23 signaling axis is involved in the endothelial protection by K(ATP) channel opener iptakalim. Acta Pharmacol Sin 2011; 32: 573-580.
59. Kaneko K, Miyabe Y, Takayasu A, et al. Chemerin activates fibroblast-like synoviocytes in patients with rheumatoid arthritis. Arthritis Res Ther 2011; 13: R158.
60. Berg V, Sveinbjornsson B, Bendiksen S, et al. Human articular chondrocytes express ChemR23 and chemerin; ChemR23 promotes inflammatory signalling upon binding the ligand chemerin (21-157). Arthritis Res Ther 2010; 12: R228.
61. Krishnamoorthy S, Recchiuti A, Chiang N, et al. Resolvin D1 binds human phagocytes with evidence for proresolving receptors. Proc Natl Acad Sci USA 2010; 107: 1660-1665.