Aspirin-triggered resolvin D1 down-regulates inflammatory responses and protects against endotoxin-induced acute kidney injury

Toxicology and Applied Pharmacology

Volumn 277, Issue 2, 2014, Pages 118-123

  Chen, Jiao ^a   Shetty, Sreerama ^b   Zhang, Ping ^c   Gao, Rong ^a   Hu, Yuxin ^a   Wang, Shuxia ^d   Li, Zhenyu ^a   Fu, Jian ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF TEXAS HEALTH CENTER   (United States)

^c SICHUAN UNIVERSITY   (China)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Acute kidney injury; Aspirin triggered resolvin D1; Endotoxemia; Inflammation; Sepsis

Indexed keywords

ANTIINFLAMMATORY AGENT; ASPIRIN TRIGGERED RESOLVIN D1; CLAUDIN 4; CREATININE; ENDOTOXIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; STAT3 PROTEIN; UNCLASSIFIED DRUG; UREA; VASCULAR CELL ADHESION MOLECULE 1;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DOWN REGULATION; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; KIDNEY; KIDNEY CORTEX; KIDNEY MEDULLA; KIDNEY TUBULE DAMAGE; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; RENAL PROTECTION; SIGNAL TRANSDUCTION; UREA NITROGEN BLOOD LEVEL;

ACUTE KIDNEY INJURY; ASPIRIN-TRIGGERED RESOLVIN D1; ENDOTOXEMIA; INFLAMMATION; SEPSIS;

ACUTE KIDNEY INJURY; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ASPIRIN; BIOLOGICAL MARKERS; BLOOD UREA NITROGEN; CLAUDIN-4; CREATININE; CYTOPROTECTION; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; ENDOTOXINS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; INFLAMMATION MEDIATORS; INTERCELLULAR ADHESION MOLECULE-1; INTERLEUKIN-6; KIDNEY; MALE; MICE; MICE, INBRED C57BL; NEUTROPHIL INFILTRATION; NF-KAPPA B; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TIME FACTORS; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84899151178     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.03.017     Document Type: Article

References (59)

1. Amasheh S., Fromm M., Gunzel D. Claudins of intestine and nephron-a correlation of molecular tight junction structure and barrier function. Acta Physiol. 2011, 201:133-140.
2. Angus D.C., Linde-Zwirble W.T., Lidicker J., Clermont G., Carcillo J., Pinsky M.R. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 2001, 29:1303-1310.
3. Bagshaw S.M., Laupland K.B., Doig C.J., Mortis G., Fick G.H., Mucenski M., Godinez-Luna T., Svenson L.W., Rosenal T. Prognosis for long-term survival and renal recovery in critically ill patients with severe acute renal failure: a population-based study. Crit. Care 2005, 9:R700-R709.
4. Balkovetz D.F. Claudins at the gate: determinants of renal epithelial tight junction paracellular permeability. Am. J. Physiol. Ren. Physiol. 2006, 290:F572-F579.
5. Bento A.F., Claudino R.F., Dutra R.C., Marcon R., Calixto J.B. Omega-3 fatty acid-derived mediators 17(R)-hydroxy docosahexaenoic acid, aspirin-triggered resolvin D1 and resolvin D2 prevent experimental colitis in mice. J. Immunol. 2011, 187:1957-1969.
6. Burne-Taney M.J., Kofler J., Yokota N., Weisfeldt M., Traystman R.J., Rabb H. Acute renal failure after whole body ischemia is characterized by inflammation and T cell-mediated injury. Am. J. Physiol. Ren. Physiol. 2003, 285:F87-F94.
7. Calder P.C. Dietary modification of inflammation with lipids. Proc. Nutr. Soc. 2002, 61:345-358.
8. Coldewey S.M., Khan A.I., Kapoor A., Collino M., Rogazzo M., Brines M., Cerami A., Hall P., Sheaff M., Kieswich J.E., Yaqoob M.M., Patel N.S., Thiemermann C. Erythropoietin attenuates acute kidney dysfunction in murine experimental sepsis by activation of the beta-common receptor. Kidney Int. 2013, 84:482-490.
9. Cunningham P.N., Wang Y., Guo R., He G., Quigg R.J. Role of Toll-like receptor 4 in endotoxin-induced acute renal failure. J. Immunol. 2004, 172:2629-2635.
10. Deng Y., Edin M.L., Theken K.N., Schuck R.N., Flake G.P., Kannon M.A., DeGraff L.M., Lih F.B., Foley J., Bradbury J.A., Graves J.P., Tomer K.B., Falck J.R., Zeldin D.C., Lee C.R. Endothelial CYP epoxygenase overexpression and soluble epoxide hydrolase disruption attenuate acute vascular inflammatory responses in mice. FASEB J. 2011, 25:703-713.
11. Doi K., Leelahavanichkul A., Yuen P.S., Star R.A. Animal models of sepsis and sepsis-induced kidney injury. J. Clin. Invest. 2009, 119:2868-2878.
12. Donnahoo K.K., Meng X., Ayala A., Cain M.P., Harken A.H., Meldrum D.R. Early kidney TNF-alpha expression mediates neutrophil infiltration and injury after renal ischemia-reperfusion. Am. J. Physiol. 1999, 277:R922-R929.
13. Duffield J.S., Forbes S.J., Constandinou C.M., Clay S., Partolina M., Vuthoori S., Wu S., Lang R., Iredale J.P. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J. Clin. Invest. 2005, 115:56-65.
14. Duffield J.S., Hong S., Vaidya V.S., Lu Y., Fredman G., Serhan C.N., Bonventre J.V. Resolvin D series and protectin D1 mitigate acute kidney injury. J. Immunol. 2006, 177:5902-5911.
15. Eadon M.T., Hack B.K., Xu C., Ko B., Toback F.G., Cunningham P.N. Endotoxemia alters tight junction gene and protein expression in the kidney. Am. J. Physiol. Ren. Physiol. 2012, 303:F821-F830.
16. Eickmeier O., Seki H., Haworth O., Hilberath J.N., Gao F., Uddin M., Croze R.H., Carlo T., Pfeffer M.A., Levy B.D. Aspirin-triggered resolvin D1 reduces mucosal inflammation and promotes resolution in a murine model of acute lung injury. Mucosal Immunol. 2013, 6:256-266.
17. Fang Z., Tang Y., Fang J., Zhou Z., Xing Z., Guo Z., Guo X., Wang W., Jiao W., Xu Z., Liu Z. Simvastatin inhibits renal cancer cell growth and metastasis via AKT/mTOR, ERK and JAK2/STAT3 pathway. PLoS One 2013, 8:e62823.
18. Gabay C. Interleukin-6 and chronic inflammation. Arthritis Res. Ther. 2006, 8(Suppl. 2):S3.
19. Grigoryev D.N., Liu M., Hassoun H.T., Cheadle C., Barnes K.C., Rabb H. The local and systemic inflammatory transcriptome after acute kidney injury. J. Am. Soc. Nephrol. 2008, 19:547-558.
20. Hopkins A.M., Baird A.W., Nusrat A. ICAM-1: targeted docking for exogenous as well as endogenous ligands. Adv. Drug Deliv. Rev. 2004, 56:763-778.
21. Hotchkiss R.S., Swanson P.E., Freeman B.D., Tinsley K.W., Cobb J.P., Matuschak G.M., Buchman T.G., Karl I.E. Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit. Care Med. 1999, 27:1230-1251.
22. Hou J., Renigunta A., Yang J., Waldegger S. Claudin-4 forms paracellular chloride channel in the kidney and requires claudin-8 for tight junction localization. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:18010-18015.
23. Ishida T., Yoshida M., Arita M., Nishitani Y., Nishiumi S., Masuda A., Mizuno S., Takagawa T., Morita Y., Kutsumi H., Inokuchi H., Serhan C.N., Blumberg R.S., Azuma T. Resolvin E1, an endogenous lipid mediator derived from eicosapentaenoic acid, prevents dextran sulfate sodium-induced colitis. Inflamm. Bowel Dis. 2010, 16:87-95.
24. Jeong M., Kim Y.W., Min J.R., Kwon M., Han B.S., Kim J.G., Jeong S.H. Change in kidney damage biomarkers after 13weeks of exposing rats to the complex of Paecilomyces sinclairii and its host Bombyx mori larvae. Food Chem. Toxicol. 2013, 59C:177-186.
25. Jiang M., Wei Q., Dong G., Komatsu M., Su Y., Dong Z. Autophagy in proximal tubules protects against acute kidney injury. Kidney Int. 2012, 82:1271-1283.
26. Kasuga K., Yang R., Porter T.F., Agrawal N., Petasis N.A., Irimia D., Toner M., Serhan C.N. Rapid appearance of resolvin precursors in inflammatory exudates: novel mechanisms in resolution. J. Immunol. 2008, 181:8677-8687.
27. Kim D.H., Jung Y.J., Lee A.S., Lee S., Kang K.P., Lee T.H., Lee S.Y., Jang K.Y., Moon W.S., Choi K.S., Yoon K.H., Sung M.J., Park S.K., Kim W. COMP-angiopoietin-1 decreases lipopolysaccharide-induced acute kidney injury. Kidney Int. 2009, 76:1180-1191.
28. Kiuchi-Saishin Y., Gotoh S., Furuse M., Takasuga A., Tano Y., Tsukita S. Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J. Am. Soc. Nephrol. 2002, 13:875-886.
29. Knotek M., Rogachev B., Wang W., Ecder T., Melnikov V., Gengaro P.E., Esson M., Edelstein C.L., Dinarello C.A., Schrier R.W. Endotoxemic renal failure in mice: role of tumor necrosis factor independent of inducible nitric oxide synthase. Kidney Int. 2001, 59:2243-2249.
30. Kremer J.M. n-3 fatty acid supplements in rheumatoid arthritis. Am. J. Clin. Nutr. 2000, 71:349S-351S.
31. Le Moellic C., Boulkroun S., Gonzalez-Nunez D., Dublineau I., Cluzeaud F., Fay M., Blot-Chabaud M., Farman N. Aldosterone and tight junctions: modulation of claudin-4 phosphorylation in renal collecting duct cells. Am. J. Physiol. Cell Physiol. 2005, 289:C1513-C1521.
32. Liano F., Pascual J. Epidemiology of acute renal failure: a prospective, multicenter, community-based study. Madrid Acute Renal Failure Study Group. Kidney Int. 1996, 50:811-818.
33. Liu S.F., Malik A.B. NF-kappa B activation as a pathological mechanism of septic shock and inflammation. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 290:L622-L645.
34. Lu C.Y., Hartono J., Senitko M., Chen J. The inflammatory response to ischemic acute kidney injury: a result of the 'right stuff' in the 'wrong place'?. Curr. Opin. Nephrol. Hypertens. 2007, 16:83-89.
35. Mehta R.L., Kellum J.A., Shah S.V., Molitoris B.A., Ronco C., Warnock D.G., Levin A., Acute Kidney Injury N. Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury. Crit. Care 2007, 11:R31.
36. Meloche S., Pouyssegur J. The ERK1/2 mitogen-activated protein kinase pathway as a master regulator of the G1- to S-phase transition. Oncogene 2007, 26:3227-3239.
37. Mitazaki S., Kato N., Suto M., Hiraiwa K., Abe S. Interleukin-6 deficiency accelerates cisplatin-induced acute renal failure but not systemic injury. Toxicology 2009, 265:115-121.
38. Mitazaki S., Hashimoto M., Matsuhashi Y., Honma S., Suto M., Kato N., Nakagawasai O., Tan-No K., Hiraiwa K., Yoshida M., Abe S. Interleukin-6 modulates oxidative stress produced during the development of cisplatin nephrotoxicity. Life Sci. 2013, 92:694-700.
39. Naugler W.E., Karin M. The wolf in sheep's clothing: the role of interleukin-6 in immunity, inflammation and cancer. Trends Mol. Med. 2008, 14:109-119.
40. Ricci Z., Ronco C. Pathogenesis of acute kidney injury during sepsis. Curr. Drug Targets 2009, 10:1179-1183.
41. Russell J.A., Singer J., Bernard G.R., Wheeler A., Fulkerson W., Hudson L., Schein R., Summer W., Wright P., Walley K.R. Changing pattern of organ dysfunction in early human sepsis is related to mortality. Crit. Care Med. 2000, 28:3405-3411.
42. Serhan C.N., Hong S., Gronert K., Colgan S.P., Devchand P.R., Mirick G., Moussignac R.L. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J. Exp. Med. 2002, 196:1025-1037.
43. Serhan C.N., Chiang N., Van Dyke T.E. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 2008, 8:349-361.
44. Silvester W., Bellomo R., Cole L. Epidemiology, management, and outcome of severe acute renal failure of critical illness in Australia. Crit. Care Med. 2001, 29:1910-1915.
45. Smith C.W., Entman M.L., Lane C.L., Beaudet A.L., Ty T.I., Youker K., Hawkins H.K., Anderson D.C. Adherence of neutrophils to canine cardiac myocytes in vitro is dependent on intercellular adhesion molecule-1. J. Clin. Invest. 1991, 88:1216-1223.
46. Spite M., Serhan C.N. Novel lipid mediators promote resolution of acute inflammation: impact of aspirin and statins. Circ. Res. 2010, 107:1170-1184.
47. Sun Y.P., Oh S.F., Uddin J., Yang R., Gotlinger K., Campbell E., Colgan S.P., Petasis N.A., Serhan C.N. Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J. Biol. Chem. 2007, 282:9323-9334.
48. Takada M., Nadeau K.C., Shaw G.D., Marquette K.A., Tilney N.L. The cytokine-adhesion molecule cascade in ischemia/reperfusion injury of the rat kidney. Inhibition by a soluble P-selectin ligand. J. Clin. Invest. 1997, 99:2682-2690.
49. Tanabe K., Matsushima-Nishiwaki R., Yamaguchi S., Iida H., Dohi S., Kozawa O. Mechanisms of tumor necrosis factor-alpha-induced interleukin-6 synthesis in glioma cells. J. Neuroinflammation 2010, 7:16.
50. Teitelbaum J.E., Allan Walker W. Review: the role of omega 3 fatty acids in intestinal inflammation. J. Nutr. Biochem. 2001, 12:21-32.
51. Thurman J.M. Triggers of inflammation after renal ischemia/reperfusion. Clin. Immunol. 2007, 123:7-13.
52. Tiwari M.M., Brock R.W., Megyesi J.K., Kaushal G.P., Mayeux P.R. Disruption of renal peritubular blood flow in lipopolysaccharide-induced renal failure: role of nitric oxide and caspases. Am. J. Physiol. Ren. Physiol. 2005, 289:F1324-F1332.
53. Van Itallie C., Rahner C., Anderson J.M. Regulated expression of claudin-4 decreases paracellular conductance through a selective decrease in sodium permeability. J. Clin. Invest. 2001, 107:1319-1327.
54. Wang W., Bansal S., Falk S., Ljubanovic D., Schrier R. Ghrelin protects mice against endotoxemia-induced acute kidney injury. Am. J. Physiol. Ren. Physiol. 2009, 297:F1032-F1037.
55. Wang B., Gong X., Wan J.Y., Zhang L., Zhang Z., Li H.Z., Min S. Resolvin D1 protects mice from LPS-induced acute lung injury. Pulm. Pharmacol. Ther. 2011, 24:434-441.
56. Wang S., Wei Q., Dong G., Dong Z. ERK-mediated suppression of cilia in cisplatin-induced tubular cell apoptosis and acute kidney injury. Biochim. Biophys. Acta 2013, 1832:1582-1590.
57. Wu Z., Liu M.C., Liang M., Fu J. Sirt1 protects against thrombomodulin down-regulation and lung coagulation after particulate matter exposure. Blood 2012, 119:2422-2429.
58. Yuan K., Huang C., Fox J., Gaid M., Weaver A., Li G., Singh B.B., Gao H., Wu M. Elevated inflammatory response in caveolin-1-deficient mice with Pseudomonas aeruginosa infection is mediated by STAT3 protein and nuclear factor kappaB (NF-kappaB). J. Biol. Chem. 2011, 286:21814-21825.
59. Zhang M.Z., Yao B., Yang S., Jiang L., Wang S., Fan X., Yin H., Wong K., Miyazawa T., Chen J., Chang I., Singh A., Harris R.C. CSF-1 signaling mediates recovery from acute kidney injury. J. Clin. Invest. 2012, 122:4519-4532.