Anti-inflammatory mechanisms of the annexin A1 protein and its mimetic peptide Ac2-26 in models of ocular inflammation in vivo and in vitro

Journal of Immunology

Volumn 190, Issue 11, 2013, Pages 5689-5701

  Girol, Ana P ^a,b   Mimura, Kallyne K O ^c   Drewes, Carine C ^d   Bolonheis, Simone M ^d   Solito, Egle ^e   Farsky, Sandra H P ^d   Gil, Cristiane D ^c   Oliani, Sonia Maria ^a,c  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b Padre Albino Foundation College of Nursing   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

^e QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL ALANYLMETHIONYLVALYLSERYLPHENYLALANYLLEUCYLLYSYLGLUTAMINYLALANYLTRYPTOPHYLPHENYLALANYLISOLEUCYLGLUTAMYLASPARAGINYLGLUTAMYLGLUTAMYLGLUTAMINYLGLUTAMINYLGLUTAMYLTYROSYLVALYLGLUTAMINYLTHREONYLVALYLLYSINE; ANTIINFLAMMATORY AGENT; CYCLOOXYGENASE 2; FORMYLPEPTIDE RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOCORTIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL COUNT; CELL INFILTRATION; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFICACY; DRUG MECHANISM; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LEUKOCYTE; MALE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RAT; TREATMENT RESPONSE; UVEITIS;

ANIMALS; ANNEXIN A1; ANTI-INFLAMMATORY AGENTS; AQUEOUS HUMOR; CYCLOOXYGENASE 2; CYTOKINES; DISEASE MODELS, ANIMAL; ENDOTOXINS; GENE EXPRESSION REGULATION; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NEUTROPHIL INFILTRATION; NEUTROPHILS; NF-KAPPA B; OLIGOPEPTIDES; PEPTIDES; PHOSPHORYLATION; PROTEIN TRANSPORT; RATS; RECEPTORS, FORMYL PEPTIDE; UVEITIS;

EID: 84878087706     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202030     Document Type: Article

References (51)

1. Cai, S., and C. R. Brandt. 2008. Induction of interleukin-6 in human retinal epithelial cells by an attenuated Herpes simplex virus vector requires viral replication and NFkappaB activation. Exp. Eye Res. 86: 178-188. (Pubitemid 351231882)
2. Leung, K. W., C. J. Barnstable, and J. Tombran-Tink. 2009. Bacterial endotoxin activates retinal pigment epithelial cells and induces their degeneration through IL-6 and IL-8 autocrine signaling. Mol. Immunol. 46: 1374-1386.
3. Brézin, A. P. 2012. [Uveitis]. Presse Med. 41: 10-20.
4. Srivastava, A., M. Rajappa, and J. Kaur. 2010. Uveitis: Mechanisms and recent advances in therapy. Clin. Chim. Acta 411: 1165-1171.
5. Larson, T., R. B. Nussenblatt, and H. N. Sen. 2011. Emerging drugs for uveitis. Expert Opin. Emerg. Drugs 16: 309-322.
6. Lee, R. W., and A. D. Dick. 2012. Current concepts and future directions in the pathogenesis and treatment of non-infectious intraocular inflammation. Eye (Lond.) 26: 17-28.
7. Mimura, K. K., R. C. Tedesco, K. S. Calabrese, C. D. Gil, and S. M. Oliani. 2012. The involvement of anti-inflammatory protein, annexin A1, in ocular toxoplasmosis. Mol. Vis. 18: 1583-1593.
8. Rosenbaum, J. T., H. O. McDevitt, R. B. Guss, and P. R. Egbert. 1980. Endotoxin-induced uveitis in rats as a model for human disease. Nature 286: 611-613. (Pubitemid 10015368)
9. Medeiros, R., G. B. Rodrigues, C. P. Figueiredo, E. B. Rodrigues, A. J. Grumman, Jr., O. J. Menezes-de-Lima, Jr., G. F. Passos, and J. B. Calixto. 2008. Molecular mechanisms of topical anti-inflammatory effects of lipoxin A (4) in endotoxin-induced uveitis. Mol. Pharmacol. 74: 154-161. (Pubitemid 351872166)
10. Li, S., H. Lu, X. Hu, W. Chen, Y. Xu, and J. Wang. 2010. Expression of TLR4-MyD88 and NF-κB in the iris during endotoxin-induced uveitis. Mediators Inflamm. 2010: 748218.
11. Chang, J. H., P. J. McCluskey, and D. Wakefield. 2006. Toll-like receptors in ocular immunity and the immunopathogenesis of inflammatory eye disease. Br. J. Ophthalmol. 90: 103-108. (Pubitemid 43029907)
12. Brito, B. E., D. O. Zamora, R. A. Bonnah, Y. Pan, S. R. Planck, and J. T. Rosenbaum. 2004. Toll-like receptor 4 and CD14 expression in human ciliary body and TLR-4 in human iris endothelial cells. Exp. Eye Res. 79: 203-208. (Pubitemid 39119409)
13. Kalariya, N. M., A. B. Reddy, N. H. Ansari, F. J. VanKuijk, and K. V. Ramana. 2011. Preventive effects of ethyl pyruvate on endotoxin-induced uveitis in rats. Invest. Ophthalmol. Vis. Sci. 52: 5144-5152.
14. Touchard, E., S. Omri, M. C. Naud, M. Berdugo, C. Deloche, C. Abadie, L. Jonet, J. C. Jeanny, P. Crisanti, Y. de Kozak, et al. 2010. A peptide inhibitor of c-Jun N-terminal kinase for the treatment of endotoxin-induced uveitis. Invest. Ophthalmol. Vis. Sci. 51: 4683-4693.
15. Rosenbaum, J. T. 2010. Future for biological therapy for uveitis. Curr. Opin. Ophthalmol. 21: 473-477.
16. Perretti, M., and R. J. Flower. 2004. Annexin 1 and the biology of the neutrophil. J. Leukoc. Biol. 76: 25-29. (Pubitemid 38857167)
17. Gavins, F. N., P. Sawmynaden, B. E. Chatterjee, and M. Perretti. 2005. A twist in anti-inflammation: annexin 1 acts via the lipoxin A4 receptor. Prostaglandins Leukot. Essent. Fatty Acids 73: 211-219. (Pubitemid 41253478)
18. Perretti, M., and F. D'Acquisto. 2009. Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat. Rev. Immunol. 9: 62-70.
19. Oliani, S. M., M. J. Paul-Clark, H. C. Christian, R. J. Flower, and M. Perretti. 2001. Neutrophil interaction with inflamed postcapillary venule endothelium alters annexin 1 expression. Am. J. Pathol. 158: 603-615. (Pubitemid 32158621)
20. Solito, E., H. C. Christian, M. Festa, A. Mulla, T. Tierney, R. J. Flower, and J. C. Buckingham. 2006. Post-translational modification plays an essential role in the translocation of annexin A1 from the cytoplasm to the cell surface. FASEB J. 20: 1498-1500.
21. da Silva, P. S., A. P. Girol, and S. M. Oliani. 2011. Mast cells modulate the inflammatory process in endotoxin-induced uveitis. Mol. Vis. 17: 1310-1319.
22. Solito, E., A. Mulla, J. F. Morris, H. C. Christian, R. J. Flower, and J. C. Buckingham. 2003. Dexamethasone induces rapid serine-phosphorylation and membrane translocation of annexin 1 in a human folliculostellate cell line via a novel nongenomic mechanism involving the glucocorticoid receptor, protein kinase C, phosphatidylinositol 3-kinase, and mitogen-activated protein kinase. Endocrinology 144: 1164-1174. (Pubitemid 36428456)
23. Dufton, N., R. Hannon, V. Brancaleone, J. Dalli, H. B. Patel, M. Gray, F. D'Acquisto, J. C. Buckingham, M. Perretti, and R. J. Flower. 2010. Anti-inflammatory role of the murine formyl-peptide receptor 2: ligand-specific effects on leukocyte responses and experimental inflammation. J. Immunol. 184: 2611-2619.
24. Gastardelo, T. S., A. S. Damazo, J. Dalli, R. J. Flower, M. Perretti, and S. M. Oliani. 2009. Functional and ultrastructural analysis of annexin A1 and its receptor in extravasating neutrophils during acute inflammation. Am. J. Pathol. 174: 177-183.
25. Perretti, M., S. J. Getting, E. Solito, P. M. Murphy, and J. L. Gao. 2001. Involvement of the receptor for formylated peptides in the in vivo anti-migratory actions of annexin 1 and its mimetics. Am. J. Pathol. 158: 1969-1973. (Pubitemid 32545181)
26. Patel, H. B., K. N. Kornerup, A. L. Sampaio, F. D'Acquisto, M. P. Seed, A. P. Girol, M. Gray, C. Pitzalis, S. M. Oliani, and M. Perretti. 2012. The impact of endogenous annexin A1 on glucocorticoid control of inflammatory arthritis. Ann. Rheum. Dis. 71: 1872-1880.
27. Damazo, A. S., S. Yona, R. J. Flower, M. Perretti, and S. M. Oliani. 2006. Spatial and temporal profiles for anti-inflammatory gene expression in leukocytes during a resolving model of peritonitis. J. Immunol. 176: 4410-4418. (Pubitemid 44264421)
28. Raynal, P., and H. B. Pollard. 1994. Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim. Biophys. Acta 1197: 63-93.
29. Yagci, F. C., O. Aslan, M. Gursel, G. Tincer, Y. Ozdamar, K. Karatepe, K. C. Akcali, and I. Gursel. 2010. Mammalian telomeric DNA suppresses endotoxin-induced uveitis. J. Biol. Chem. 285: 28806-28811.
30. Damazo, A. S., R. J. Flower, E. Solito, and S. M. Oliani. 2008. Annexin-A1 gene expression during liver development and post-translation modification after experimental endotoxemia. Inflamm. Res. 57: 97-103. (Pubitemid 351457936)
31. Dunn, K. C., A. E. Aotaki-Keen, F. R. Putkey, and L. M. Hjelmeland. 1996. ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp. Eye Res. 62: 155-169. (Pubitemid 26140102)
32. Paimela, T., T. Ryhänen, E. Mannermaa, J. Ojala, G. Kalesnykas, A. Salminen, and K. Kaarniranta. 2007. The effect of 17beta-estradiol on IL-6 secretion and NF-kappaB DNA-binding activity in human retinal pigment epithelial cells. Immunol. Lett. 110: 139-144. (Pubitemid 46829424)
33. Ju, W. K., and A. H. Neufeld. 2002. Cellular localization of cyclooxygenase-1 and cyclooxygenase-2 in the normal mouse, rat, and human retina. J. Comp. Neurol. 452: 392-399.
34. Damazo, A. S., S. Yona, F. D'Acquisto, R. J. Flower, S. M. Oliani, and M. Perretti. 2005. Critical protective role for annexin 1 gene expression in the endotoxemic murine microcirculation. Am. J. Pathol. 166: 1607-1617. (Pubitemid 40734384)
35. Yang, Y. H., D. Aeberli, A. Dacumos, J. R. Xue, and E. F. Morand. 2009. Annexin-1 regulates macrophage IL-6 and TNF via glucocorticoid-induced leucine zipper. J. Immunol. 183: 1435-1445.
36. -/- mouse. Prostaglandins Leukot. Essent. Fatty Acids 72: 95-103.
37. -/- mouse. FASEB J. 17: 253-255.
38. Damazo, A. S., N. Moradi-Bidhendi, S. M. Oliani, and R. J. Flower. 2007. Role of annexin 1 gene expression in mouse craniofacial bone development. Birth Defects Res. A Clin. Mol. Teratol. 79: 524-532. (Pubitemid 47068188)
39. Ayoub, S. S., S. Yazid, and R. J. Flower. 2008. Increased susceptibility of annexin-A1 null mice to nociceptive pain is indicative of a spinal antinociceptive action of annexin-A1. Br. J. Pharmacol. 154: 1135-1142. (Pubitemid 351915065)
40. Ooi, K. G., G. Galatowicz, V. L. Calder, and S. L. Lightman. 2006. Cytokines and chemokines in uveitis: is there a correlation with clinical phenotype? Clin. Med. Res. 4: 294-309. (Pubitemid 46166379)
41. de Coupade, C., M. N. Ajuebor, F. Russo-Marie, M. Perretti, and E. Solito. 2001. Cytokine modulation of liver annexin 1 expression during experimental endotoxemia. Am. J. Pathol. 159: 1435-1443. (Pubitemid 32947973)
42. Lim, L. H., and S. Pervaiz. 2007. Annexin 1: the new face of an old molecule. FASEB J. 21: 968-975. (Pubitemid 46495688)
43. Boulay, F., and M. J. Rabiet. 2005. The chemoattractant receptors FPR and C5aR: same functions - different fates. Traffic 6: 83-86.
44. Martin, G. R., M. Perretti, R. J. Flower, and J. L. Wallace. 2008. Annexin-1 modulates repair of gastric mucosal injury. Am. J. Physiol. Gastrointest. Liver Physiol. 294: G764-G769. (Pubitemid 351468762)
45. Huggins, A., N. Paschalidis, R. J. Flower, M. Perretti, and F. D'Acquisto. 2009. Annexin-1-deficient dendritic cells acquire a mature phenotype during differentiation. FASEB J. 23: 985-996.
46. Font-Nieves, M., M. G. Sans-Fons, R. Gorina, E. Bonfill-Teixidor, A. Salas-Perdomo, L. Marquez-Kisinousky, T. Santalucia, and A. M. Planas. 2012. Induction of COX-2 enzyme and down-regulation of COX-1 expression by lipopolysaccharide (LPS) control prostaglandin E2 production in astrocytes. J. Biol. Chem. 287: 6454-6468.
47. Xu, L. M., S. W. Jin, X. Y. Zhou, P. Wu, Y. S. Li, L. Zhang, Y. Y. Lin, Y. Chen, and D. Y. Ye. 2009. Effects of exogenous annexin-1 on lipopolysaccharide-induced proliferation and reactive oxygen species production partially through modulation of CRAC channels but independent of NF-kappaB pathway. Inflamm. Res. 58: 921-930.
48. Abdelwahab, S. I., L. E. Hassan, H. M. Sirat, S. M. Yagi, W. S. Koko, S. Mohan, M. M. Taha, S. Ahmad, C. S. Chuen, P. Narrima, et al. 2011. Anti-inflammatory activities of cucurbitacin E isolated from Citrullus lanatus var. citroides: role of reactive nitrogen species and cyclooxygenase enzyme inhibition. Fitoterapia 82: 1190-1197.
49. Wang, Z. M., S. G. Zhu, Z. W. Wu, Y. Lu, H. Z. Fu, and R. Q. Qian. 2011. Kirenol upregulates nuclear annexin-1 which interacts with NF-κB to attenuate synovial inflammation of collagen-induced arthritis in rats. J. Ethnopharmacol. 137: 774-782.
50. Bist, P., S. C. Leow, Q. H. Phua, S. Shu, Q. Zhuang, W. T. Loh, T. H. Nguyen, J. B. Zhou, S. C. Hooi, and L. H. Lim. 2011. Annexin-1 interacts with NEMO and RIP1 to constitutively activate IKK complex and NF-κB: implication in breast cancer metastasis. Oncogene 30: 3174-3185.
51. Zhang, Z., L. Huang, W. Zhao, and B. Rigas. 2010. Annexin 1 induced by anti-inflammatory drugs binds to NF-kappaB and inhibits its activation: anticancer effects in vitro and in vivo. Cancer Res. 70: 2379-2388.