Annexin 1 mimetic peptide protects against renal ischemia/reperfusion injury in rats

Journal of Molecular Medicine

Volumn 89, Issue 1, 2011, Pages 51-63

  Facio Jr , Fernando N ^a   Sena, Angela A ^b   Araújo, Leandro P ^b   Mendes, Gloria E ^a   Castro, Isac ^c   Luz, Marcus A M ^a   Yu, Luis ^c   Oliani, Sonia Maria ^b   Burdmann, Emmanuel A ^a,c  

^a Sao Jose do Rio Preto Medical School   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Acute kidney injury; Acute tubular necrosis; Annexin A1; Ischemia reperfusion injury; Kidney; Neutrophils

Indexed keywords

AC 226; LIPOCORTIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; GLOMERULUS FILTRATION RATE; IMMUNITY; IMMUNOREGULATION; KIDNEY ISCHEMIA; KIDNEY PERFUSION; KIDNEY TUBULE NECROSIS; MACROPHAGE; MALE; NEUTROPHIL; NONHUMAN; RAT; RENAL PROTECTION; REPERFUSION INJURY; TREATMENT OUTCOME;

ANIMALS; ANNEXIN A1; ANTI-INFLAMMATORY AGENTS; BIOMIMETICS; GENE EXPRESSION REGULATION; KIDNEY; KIDNEY TUBULES, PROXIMAL; MALE; MODELS, ANIMAL; RATS; REPERFUSION INJURY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 78651351012     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-010-0684-4     Document Type: Article

References (54)

1. S Uchino JA Kellum R Bellomo GS Doig H Morimatsu S Morgera M Schetz I Tan C Bouman E Macedo, et al. 2005 Beginning and ending supportive therapy for the kidney (BEST Kidney) investigators. Acute renal failure in critically ill patients: a multinational, multicenter study JAMA 294 813 818 1:CAS:528:DC%2BD2MXos1WnsL0%3D 10.1001/jama.294.7.813 16106006
2. W Gwinner K Hinzmann U Erdbruegger I Scheffner V Broecker B Vaske H Kreipe H Haller A Schwarz M Mengel 2000 Acute tubular injury in protocol biopsies of renal grafts: prevalence, associated factors and effect on long-term function Am J Transplant 8 1684 1693 10.1111/j.1600-6143.2008.02293.x
3. CY Lu J Hartono M Senitko J Chen 2007 The inflammatory response to ischemic acute kidney injury: a result of the 'right stuff' in the 'wrong place'? Curr Opin Nephrol Hypertens 16 83 89 10.1097/MNH.0b013e3280403c4e 17293682
4. JV Bonventre 2007 Pathophysiology of acute kidney injury: roles of potential inhibitors of inflammation Contrib Nephrol 156 39 46 1:CAS:528:DC%2BD1cXhsFaru7bK 10.1159/000102069 17464114
5. P Devarajan 2006 Update on mechanisms of ischemic acute kidney injury J Am Soc Nephrol 17 503 1520 10.1681/ASN.2006010017
6. CC Willinger H Schramek K Pfaller W Pfaller 1992 Tissue distribution of neutrophils in postischemic acute renal failure Virchows Arch B Cell Pathol Incl Mol Pathol 62 237 243 1:STN:280:DyaK3s%2FmvF2ktg%3D%3D 10.1007/BF02899687 1359696
7. DD Koo KI Welsh JA Roake PJ Morris SV Fuggle 1998 Ischemia/reperfusion injury in human kidney transplantation: an immunohistochemical analysis of changes after reperfusion Am J Pathol 153 557 566 1:CAS:528:DyaK1cXls1ejtLo%3D 9708815
8. DK Ysebaert KE De Greef SR Vercauteren M Ghielli GA Verpooten EJ Eyskens ME De Broe 2000 Identification and kinetics of leukocytes after severe ischaemia/reperfusion renal injury Nephrol Dial Transplant 15 1562 1574 1:STN:280:DC%2BD3M%2FktVWrsw%3D%3D 10.1093/ndt/15.10.1562 11007823
9. JJ Friedewald H Rabb 2004 Inflammatory cells in ischemic acute renal failure Kidney Int 66 486 491 10.1111/j.1523-1755.2004.761-3.x 15253694
10. K Singbartl K Ley 2004 Leukocyte recruitment and acute renal failure J Mol Med 82 91 101 10.1007/s00109-003-0498-8 14669001
11. M Riera J Torras I Herrero J Valles M Paubert-Braquet JM Cruzado J Alsina JM Grinyo 1997 Neutrophils accentuate renal cold ischemia-reperfusion injury. Dose-dependent protective effect of a platelet-activating factor receptor antagonist J Pharmacol Exp Ther 280 786 794 1:CAS:528:DyaK2sXivVWktbk%3D 9023292
12. P Park M Haas PN Cunningham L Bao JJ Alexander RJ Quigg 2002 Injury in renal ischemia-reperfusion is independent from immunoglobulins and T lymphocytes Am J Physiol Renal Physiol 282 F352 F357 11788450
13. H Rabb F Daniels M O'Donnell M Haq SR Saba W Keane WW Tang 2000 Pathophysiological role of T lymphocytes in renal ischemia-reperfusion injury in mice Am J Physiol Renal Physiol 279 F525 F531 1:CAS:528:DC%2BD3cXmvFSjsLY%3D 10966932
14. SK Jo SA Sung WY Cho KJ Go HK Kim 2006 Macrophages contribute to the initiation of ischaemic acute renal failure in rats Nephrol Dial Transplant 21 1231 1239 1:CAS:528:DC%2BD28XjslKru78%3D 10.1093/ndt/gfk047 16410269
15. H Rabb 2006 Immune modulation of acute kidney injury J Am Soc Nephrol 17 604 606 1:CAS:528:DC%2BD28XislCruro%3D 10.1681/ASN.2006010060 16481410
16. Y Huang H Rabb KL Womer 2007 Ischemia-reperfusion and immediate T cell responses Cell Immunol 248 4 11 1:CAS:528:DC%2BD2sXhtlWqurrN 17942086
17. M Perretti RJ Flower 2004 Annexin 1 and the biology of the neutrophil J Leukoc Biol 76 25 29 1:CAS:528:DC%2BD2cXlsVOisrg%3D 10.1189/jlb.1103552 14966195
18. SM Oliani HC Christian J Manston RJ Flower M Perretti 2000 An immunocytochemical and in situ hybridization analysis of annexin 1 expression in rat mast cells: modulation by inflammation and dexamethasone Lab Invest 80 1429 1438 1:CAS:528:DC%2BD3cXnt1Kgu78%3D 11005211
19. SM Oliani MJ Paul-Clark H Christian RJ Flower M Perretti 2001 Neutrophil interaction with inflamed post-capillary venule endothelium alters annexin 1 expression Am J Phatol 158 603 615 1:CAS:528:DC%2BD3MXhsFWmtL8%3D
20. AM Kamal RJ Flower M Perretti 2005 An overview of the effects of annexin 1 on cells involved in the inflammatory process Mem Inst Oswaldo Cruz 100 Suppl 1 39 47 1:CAS:528:DC%2BD2MXktVOgtr4%3D 15962097
21. S Cuzzocrea A Tailor B Zingarelli AL Salzman RJ Flower C Szabó M Perretti 1997 Lipocortin 1 protects against splanchnic artery occlusion and reperfusion injury by affecting neutrophil migration J Immunol 159 5089 5097 1:CAS:528:DyaK2sXntlKrtLk%3D 9366438
22. M D'Amico C Di Filippo M La E Solito PG McLean RJ Flower SM Oliani M Perretti 2000 Lipocortin 1 reduces myocardial ischemia-reperfusion injury by affecting local leukocyte recruitment FASEB J 14 1867 1869 11023969
23. M La M D'Amico S Bandiera C Di Filippo SM Oliani FN Gavins RJ Flower M Perretti 2001 Annexin 1 peptides protect against experimental myocardial ischemia-reperfusion: analysis of their mechanism of action FASEB J 15 2247 2256 1:CAS:528:DC%2BD3MXnsV2mtrY%3D 10.1096/fj.01-0196com 11641252
24. FN Gavins J Dalli RJ Flower DN Granger M Perretti 2007 Activation of the annexin 1 counter-regulatory circuit affords protection in the mouse brain microcirculation FASEB J 21 1751 1758 1:CAS:528:DC%2BD2sXmsVWksr8%3D 10.1096/fj.06-7842com 17317721
25. NC Teoh Y Ito J Field NW Bethea D Amr MK McCuskey RS McCuskey GC Farrell AC Allison 2007 Diannexin, a novel annexin V homodimer, provides prolonged protection against hepatic ischemia-reperfusion injury in mice Gastroenterology 133 632 646 1:CAS:528:DC%2BD2sXhtVWqsr3J 10.1053/j.gastro.2007.05.027 17681182
26. XD Shen B Ke Y Zhai SI Tsuchihashi F Gao S Duarte A Coito RW Busuttil AC Allison JW Kupiec-Weglinski 2007 Diannexin, a novel annexin V homodimer, protects rat liver transplants against cold ischemia-reperfusion injury Am J Transplant 7 2463 2471 1:CAS:528:DC%2BD2sXhtlakt7zE 10.1111/j.1600-6143.2007. 01967.x 17868064
27. Ahluwalia A, Buckingham JC, Croxtall JD, Flower RJ, Goulding NJ, Perretti M (1996) Biology of annexin 1. In: Seaton BA (ed) Annexins: molecular structure to cellular function. Landes, Austin, pp 161-199
28. V Gerke CE Creutz SE Moss 2005 Annexins: linking Ca2+ signalling to membrane dynamics Nat Rev Mol Cell Biol 6 449 461 1:CAS:528:DC%2BD2MXks1Gmtbo%3D 10.1038/nrm1661 15928709
29. E Solito A Kamal F Russo-Marie JC Buckingham S Marullo M Perretti 2003 A novel calcium-dependent proapoptotic effect of annexin 1 on human neutrophils FASEB J 17 1544 1546 1:CAS:528:DC%2BD3sXmtVKns70%3D 12824302
30. F Mancuso RJ Flower M Perretti 1995 Leukocyte transmigration, but not rolling or adhesion, is selectively inhibited by dexamethasone in the hamster post-capillary venule. Involvement of endogenous lipocortin 1 J Immunol 155 377 386 1:CAS:528:DyaK2MXmsFKhtb4%3D 7602112
31. LH Lim E Solito F Russo-Marie RJ Flower M Perretti 1998 Promoting detachment of neutrophils adherent to murine postcapillary venules to control inflammation: effect of lipocortin 1 Proc Natl Acad Sci USA 95 14535 14539 1:CAS:528:DyaK1cXns1Gltrs%3D 10.1073/pnas.95.24.14535 9826735
32. FN Gavins S Yona AM Kamal RJ Flower M Perretti 2003 Leukocyte antiadhesive actions of annexin 1: ALXR- and FPR-related anti-inflammatory mechanisms Blood 101 4140 4147 1:CAS:528:DC%2BD3sXktVGmsr0%3D 10.1182/blood-2002-11-3411 12560218
33. JA McKanna A Chuncharunee KA Munger JA Breyer S Cohen RC Harris 1992 Localization of p35 (annexin I, lipocortin I) in normal adult rat kidney and during recovery from ischemia J Cell Physiol 153 467 476 1:CAS:528: DyaK3sXjslWisA%3D%3D 10.1002/jcp.1041530305 1447309
34. RM Soubhia GE Mendes FZ Mendonça MA Baptista JP Cipullo EA Burdmann 2005 Tacrolimus and nonsteroidal anti-inflammatory drugs: an association to be avoided Am J Nephrol 25 327 334 1:CAS:528:DC%2BD2MXnvFynsr8%3D 10.1159/000086569 15976495
35. L Yu PE Gengaro M Niederberger TJ Burke RW Schrier 1994 Nitric oxide: a mediator in rat tubular hypoxia/reoxygenation injury Proc Natl Acad Sci USA 91 1691 1695 1:CAS:528:DyaK2cXhvVyrtrk%3D 10.1073/pnas.91.5.1691 7510405
36. AS Damazo S Yona RJ Flower M Perretti SM Oliani 2006 Spatial and temporal profiles for anti-inflammatory gene expression in leukocytes during a resolving model of peritonitis J Immunol 176 4410 4418 1:CAS:528:DC%2BD28Xis1eqsLw%3D 16547279
37. BA Babbin CA Parkos KJ Mandell LM Winfree O Laur AI Ivanov A Nusrat 2007 Annexin 2 regulates intestinal epithelial cell spreading and wound closure through Rho-related signaling Am J Pathol 170 951 966 1:CAS:528: DC%2BD2sXjs1WlsLg%3D 10.2353/ajpath.2007.060647 17322380
38. BA Babbin MG Laukoetter P Nava S Koch WY Lee CT Capaldo E Peatman EA Severson RJ Flower M Perretti CA Parkos A Nusrat 2008 Annexin A1 regulates intestinal mucosal injury, inflammation, and repair J Immunol 181 5035 5544 1:CAS:528:DC%2BD1cXhtFaru7%2FK 18802107
39. B McMahon D Mitchell R Shattock F Martin HR Brady C Godson 2002 Lipoxin, leukotriene, and PDGF receptors cross-talk to regulate mesangial cell proliferation FASEB J 16 1817 1819 1:CAS:528:DC%2BD38XoslOgt74%3D 12223454
40. JV Bonventre A Zuk 2004 Ischemic acute renal failure: an inflammatory disease? Kidney Int 66 480 485 1:CAS:528:DC%2BD2cXmvVegs78%3D 10.1111/j.1523-1755.2004.761-2.x 15253693
41. BE Chatterjee S Yona G Rosignoli RE Young S Nourshargh RJ Flower M Perretti 2005 Annexin 1-deficient neutrophils exhibit enhanced transmigration in vivo and increased responsiveness in vitro J Leukoc Biol 78 639 646 1:CAS:528:DC%2BD2MXhtVSksb3M 10.1189/jlb.0405206 16000391
42. MS Paller 1989 Effect of neutrophil depletion on ischemic renal injury in the rat J Lab Clin Med 113 379 386 1:STN:280:DyaL1M7ns1Kmtg%3D%3D 2926243
43. B Vries J Köhl WK Leclercq TG Wolfs AA van Bijnen P Heeringa WA Buurman 2003 Complement factor C5a mediates renal ischemia-reperfusion injury independent from neutrophils J Immunol 170 3883 3889 12646657
44. SL Linas PF Shanley D Whittenburg E Berger JE Repine 1988 Neutrophils accentuate ischemia-reperfusion injury in isolated perfused rat kidneys Am J Physiol 255 F728 F735 1:CAS:528:DyaL1cXmt1ynt7w%3D 2845813
45. KJ Kelly WW Williams Jr RB Colvin SM Meehan TA Springer JC Gutierrez-Ramos JV Bonventre 1996 Intercellular adhesion molecule-1-deficient mice are protected against ischemic renal injury J Clin Invest 97 1056 1063 1:CAS:528:DyaK28XhvVais7o%3D 10.1172/JCI118498 8613529
46. M Perretti FNE Gavins 2003 Annexin 1: an endogenous anti-inflammatory protein News Physiol Sci 18 60 64 1:CAS:528:DC%2BD3sXjt1ejsro%3D 12644621
47. ML Kielar R John M Bennett JA Richardson JM Shelton L Chen DR Jeyarajah XJ Zhou H Zhou B Chiquett, et al. 2005 Maladaptive role of IL-6 in ischemic acute renal failure J Am Soc Nephrol 16 3315 3325 1:CAS:528:DC%2BD2MXht1Cnsr3N 10.1681/ASN.2003090757 16192425
48. YJ Day L Huang H Ye J Linden MD Okusa 2005 Renal ischemia-reperfusion injury and adenosine 2A receptor-mediated tissue protection: role of macrophages Am J Physiol Renal Physiol 288 F722 F731 1:CAS:528:DC%2BD2MXjtlOqt7g%3D 10.1152/ajprenal.00378.2004 15561971
49. GJ Ko CS Boo SK Jo WY Cho HK Kim 2008 Macrophages contribute to the development of renal fibrosis following ischaemia/reperfusion-induced acute kidney injury Nephrol Dial Transplant 23 842 852 1:CAS:528:DC%2BD1cXivVOrtL8%3D 10.1093/ndt/gfm694 17984109
50. E Vinuesa G Hotter M Jung I Herrero-Fresneda J Torras A Sola 2008 Macrophage involvement in the kidney repair phase after ischaemia/reperfusion injury J Pathol 214 104 113 1:CAS:528:DC%2BD1cXhtlyms78%3D 10.1002/path.2259 17973244
51. M Suleiman PM Cury JO Pestana EA Burdmann V Bueno 2005 FTY720 prevents renal T-cell infiltration after ischemia/reperfusion injury Transplant Proc 37 373 374 1:CAS:528:DC%2BD2MXivFSntr8%3D 10.1016/j.transproceed.2004.12.280 15808648
52. S Faubel D Ljubanovic B Poole B Dursun Z He S Cushing H Somerset RG Gill CL Edelstein 2005 Peripheral CD4 T-cell depletion is not sufficient to prevent ischemic acute renal failure Transplantation 80 643 649 10.1097/01.tp. 0000173396.07368.55 16177639
53. N Yokota M Burne-Taney L Racusen H Rabb 2003 Contrasting roles for STAT4 and STAT6 signal transduction pathways in murine renal ischemia-reperfusion injury Am J Physiol Renal Physiol 285 F319 F325 1:CAS:528:DC%2BD3sXmsVagu7w%3D 12709397
54. KK Donnahoo X Meng A Ayala MP Cain AH Harken DR Meldrum 1999 Early kidney TNF-alpha expression mediates neutrophil infiltration and injury after renal ischemia-reperfusion Am J Physiol 277 R922 R929 1:CAS:528:DyaK1MXmt1Gis7c%3D 10484513