Annexin A1 and resolution of inflammation: tissue repairing properties and signalling signature

References

Abramson, S.N., Martin, M.W., Hughes, A.R., Harden, T.K., Neve, K.A., Barrett, D.A., and Molinoff, P.B. (1988). Interaction of β-adrenergic receptors with the inhibitory guanine nucleotide-binding protein of adenylate cyclase in membranes prepared from cyc- s49 lymphoma cells. Biochem Pharmacol. 37, 4289–4297.10.1016/0006-2952(88)90609-0Search in Google Scholar

Akasheh, R.T., Pini, M., Pang, J., and Fantuzzi, G. (2013). Increased adiposity in annexin a1-deficient mice. PLoS One 8, e82608.10.1371/journal.pone.0082608Search in Google Scholar

Ambrose, M.P. and Hunninghake, G.W. (1990). Corticosteroids increase lipocortin i in alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 3, 349–353.10.1165/ajrcmb/3.4.349Search in Google Scholar

Arur, S., Uche, U.E., Rezaul, K., Fong, M., Scranton, V., Cowan, A.E., Mohler, W., and Han, D.K. (2003). Annexin i is an endogenous ligand that mediates apoptotic cell engulfment. Dev. Cell 4, 587–598.10.1016/S1534-5807(03)00090-XSearch in Google Scholar

Babbin, B.A., Laukoetter, M.G., Nava, P., Koch, S., Lee, W.Y., Capaldo, C.T., Peatman, E., Severson, E.A., Flower, R.J., Perretti, M., et al. (2008). Annexin a1 regulates intestinal mucosal injury, inflammation, and repair. J. Immunol. 181, 5035–5044.10.4049/jimmunol.181.7.5035Search in Google Scholar

Babbin, B.A., Lee, W.Y., Parkos, C.A., Winfree, L.M., Akyildiz, A., Perretti, M., and Nusrat, A. (2006). Annexin i regulates skco-15 cell invasion by signaling through formyl peptide receptors. J. Biol. Chem. 281, 19588–19599.10.1074/jbc.M513025200Search in Google Scholar

Bao, L., Gerard, N.P., Eddy, Jr., R.L., Shows, T.B., and Gerard, C. (1992). Mapping of genes for the human c5a receptor (c5ar), human fmlp receptor (fpr), and two fmlp receptor homologue orphan receptors (fprh1, fprh2) to chromosome 19. Genomics 13, 437–440.10.1016/0888-7543(92)90265-TSearch in Google Scholar

Bena, S., Brancaleone, V., Wang, J.M., Perretti, M., and Flower, R.J. (2012). Annexin a1 interaction with the fpr2/alx receptor: Identification of distinct domains and downstream associated signaling. J. Biol. Chem. 287, 24690–24697.10.1074/jbc.M112.377101Search in Google Scholar PubMed PubMed Central

Bensalem, N., Ventura, A.P., Vallee, B., Lipecka, J., Tondelier, D., Davezac, N., Dos Santos, A., Perretti, M., Fajac, A., Sermet-Gaudelus, I., et al. (2005). Down-regulation of the anti-inflammatory protein annexin a1 in cystic fibrosis knock-out mice and patients. Mol. Cell Proteomics 4, 1591–1601.10.1074/mcp.M500019-MCP200Search in Google Scholar PubMed

Bizzarro, V., Fontanella, B., Franceschelli, S., Pirozzi, M., Christian, H., Parente, L., and Petrella, A. (2010). Role of annexin a1 in mouse myoblast cell differentiation. J. Cell Physiol. 224, 757–765.10.1002/jcp.22178Search in Google Scholar PubMed

Bizzarro, V., Belvedere, R., Dal Piaz, F., Parente, L., and Petrella, A. (2012a). Annexin a1 induces skeletal muscle cell migration acting through formyl peptide receptors. PLoS One 7, e48246.10.1371/journal.pone.0048246Search in Google Scholar

Bizzarro, V., Petrella, A., and Parente, L. (2012b). Annexin a1: Novel roles in skeletal muscle biology. J. Cell Physiol. 227, 3007–3015.10.1002/jcp.24032Search in Google Scholar

Bizzarro, V., Belvedere, R., Milone, M.R., Pucci, B., Lombardi, R., Bruzzese, F., Popolo, A., Parente, L., Budillon, A., and Petrella, A. (2015). Annexin a1 is involved in the acquisition and maintenance of a stem cell-like/aggressive phenotype in prostate cancer cells with acquired resistance to zoledronic acid. Oncotarget 6, 25076–25092.10.18632/oncotarget.4725Search in Google Scholar

Bozinovski, S., Uddin, M., Vlahos, R., Thompson, M., McQualter, J.L., Merritt, A.S., Wark, P.A., Hutchinson, A., Irving, L.B., Levy, B.D., et al. (2012). Serum amyloid a opposes lipoxin a(4) to mediate glucocorticoid refractory lung inflammation in chronic obstructive pulmonary disease. Proc. Natl. Acad Sci. USA 109, 935–940.10.1073/pnas.1109382109Search in Google Scholar

Brunt, E.M. (2010). Pathology of nonalcoholic fatty liver disease. Nat. Rev. Gastroenterol. Hepatol. 7, 195–203.10.1038/nrgastro.2010.21Search in Google Scholar

Chiang, N., Fierro, I.M., Gronert, K., and Serhan, C.N. (2000). Activation of lipoxin a(4) receptors by aspirin-triggered lipoxins and select peptides evokes ligand-specific responses in inflammation. J. Exp. Med. 191, 1197–1208.10.1084/jem.191.7.1197Search in Google Scholar

Christmas, P., Callaway, J., Fallon, J., Jones, J., and Haigler, H.T. (1991). Selective secretion of annexin 1, a protein without a signal sequence, by the human prostate gland. J. Biol. Chem. 266, 2499–2507.10.1016/S0021-9258(18)52272-9Search in Google Scholar

Chung, Y.W., Oh, H.Y., Kim, J.Y., Kim, J.H., and Kim, I.Y. (2004). Allergen-induced proteolytic cleavage of annexin-1 and activation of cytosolic phospholipase a2 in the lungs of a mouse model of asthma. Proteomics 4, 3328–3334.10.1002/pmic.200400895Search in Google Scholar

Cooray, S.N., Gobbetti, T., Montero-Melendez, T., McArthur, S., Thompson, D., Clark, A.J., Flower, R.J., and Perretti, M. (2013). Ligand-specific conformational change of the g-protein-coupled receptor alx/fpr2 determines proresolving functional responses. Proc. Natl. Acad. Sci. USA 110, 18232–18237.10.1073/pnas.1308253110Search in Google Scholar

Creutz, C.E., Pazoles, C.J., and Pollard, H.B. (1978). Identification and purification of an adrenal medullary protein (synexin) that causes calcium-dependent aggregation of isolated chromaffin granules. J. Biol. Chem. 253, 2858–2866.10.1016/S0021-9258(17)40901-XSearch in Google Scholar

Cristante, E., McArthur, S., Mauro, C., Maggioli, E., Romero, I.A., Wylezinska-Arridge, M., Couraud, P.O., Lopez-Tremoleda, J., Christian, H.C., Weksler, B.B., et al. (2013). Identification of an essential endogenous regulator of blood-brain barrier integrity, and its pathological and therapeutic implications. Proc. Natl. Acad. Sci. USA 110, 832–841.10.1073/pnas.1209362110Search in Google Scholar

Crumpton, M.J. and Dedman, J.R. (1990). Protein terminology tangle. Nature 345, 212.10.1038/345212a0Search in Google Scholar

D’Acquisto, F., Merghani, A., Lecona, E., Rosignoli, G., Raza, K., Buckley, C.D., Flower, R.J., and Perretti, M. (2007). Annexin-1 modulates t-cell activation and differentiation. Blood 109, 1095–1102.10.1182/blood-2006-05-022798Search in Google Scholar

D’Acunto, C.W., Gbelcova, H., Festa, M., and Ruml, T. (2014). The complex understanding of annexin a1 phosphorylation. Cell Signal. 26, 173–178.10.1016/j.cellsig.2013.09.020Search in Google Scholar

D’Amico, M., Di Filippo, C., La, M., Solito, E., McLean, P.G., Flower, R.J., Oliani, S.M., and Perretti, M. (2000). Lipocortin 1 reduces myocardial ischemia-reperfusion injury by affecting local leukocyte recruitment. FASEB J. 14, 1867–1869.10.1096/fj.99-0602fjeSearch in Google Scholar

Dalli, J., Norling, L.V., Renshaw, D., Cooper, D., Leung, K.Y., and Perretti, M. (2008). Annexin 1 mediates the rapid anti-inflammatory effects of neutrophil-derived microparticles. Blood 112, 2512–2519.10.1182/blood-2008-02-140533Search in Google Scholar

Dalli, J., Rosignoli, G., Hayhoe, R.P., Edelman, A., and Perretti, M. (2010). Cftr inhibition provokes an inflammatory response associated with an imbalance of the annexin a1 pathway. Am. J. Pathol. 177, 176–186.10.2353/ajpath.2010.091149Search in Google Scholar

Dalli, J., Consalvo, A.P., Ray, V., Di Filippo, C., D’Amico, M., Mehta, N., and Perretti, M. (2013). Proresolving and tissue-protective actions of annexin a1-based cleavage-resistant peptides are mediated by formyl peptide receptor 2/lipoxin a4 receptor. J. Immunol. 190, 6478–6487.10.4049/jimmunol.1203000Search in Google Scholar

Damazo, A.S., Yona, S., D’Acquisto, F., Flower, R.J., Oliani, S.M., and Perretti, M. (2005). Critical protective role for annexin 1 gene expression in the endotoxemic murine microcirculation. Am. J. Pathol. 166, 1607–1617.10.1016/S0002-9440(10)62471-6Search in Google Scholar

Damazo, A.S., Sampaio, A.L., Nakata, C.M., Flower, R.J., Perretti, M., and Oliani, S.M. (2011). Endogenous annexin a1 counter-regulates bleomycin-induced lung fibrosis. BMC Immunol. 12, 59.10.1186/1471-2172-12-59Search in Google Scholar PubMed PubMed Central

de Boer, A.G. and Gaillard, P.J. (2006). Blood-brain barrier dysfunction and recovery. J. Neural. Transm. (Vienna) 113, 455–462.10.1007/s00702-005-0375-4Search in Google Scholar

Del Gaudio, P., De Cicco, F., Aquino, R.P., Picerno, P., Russo, P., Dal Piaz, F., Bizzarro, V., Belvedere, R., Parente, L., and Petrella, A. (2015). Evaluation of in situ injectable hydrogels as controlled release device for anxa1 derived peptide in wound healing. Carbohydr. Polym. 115, 629–635.10.1016/j.carbpol.2014.09.040Search in Google Scholar

Drechsler, M., de Jong, R., Rossaint, J., Viola, J.R., Leoni, G., Wang, J.M., Grommes, J., Hinkel, R., Kupatt, C., Weber, C., et al. (2015). Annexin a1 counteracts chemokine-induced arterial myeloid cell recruitment. Circ. Res. 116, 827–835.10.1161/CIRCRESAHA.116.305825Search in Google Scholar

Dreier, R., Schmid, K.W., Gerke, V., and Riehemann, K. (1998). Differential expression of annexins i, ii and iv in human tissues: an immunohistochemical study. Histochem. Cell Biol. 110, 137–148.10.1007/s004180050275Search in Google Scholar

El Kebir, D., Jozsef, L., Khreiss, T., Pan, W., Petasis, N.A., Serhan, C.N., and Filep, J.G. (2007). Aspirin-triggered lipoxins override the apoptosis-delaying action of serum amyloid a in human neutrophils: a novel mechanism for resolution of inflammation. J. Immunol. 179, 616–622.10.4049/jimmunol.179.1.616Search in Google Scholar

Ernst, S., Lange, C., Wilbers, A., Goebeler, V., Gerke, V., and Rescher, U. (2004). An annexin 1 n-terminal peptide activates leukocytes by triggering different members of the formyl peptide receptor family. J. Immunol. 172, 7669–7676.10.4049/jimmunol.172.12.7669Search in Google Scholar

Errasfa, M., Rothhut, B., Fradin, A., Billardon, C., Junien, J.L., Bure, J., and Russo-Marie, F. (1985). The presence of lipocortin in human embryonic skin fibroblasts and its regulation by anti-inflammatory steroids. Biochim. Biophys. Acta 847, 247–254.10.1016/0167-4889(85)90027-8Search in Google Scholar

Fargin, A., Raymond, J.R., Regan, J.W., Cotecchia, S., Lefkowitz, R.J., and Caron, M.G. (1989). Effector coupling mechanisms of the cloned 5-ht1a receptor. J. Biol. Chem. 264, 14848–14852.10.1016/S0021-9258(18)63778-0Search in Google Scholar

Flower, R.J. and Blackwell, G.J. (1979). Anti-inflammatory steroids induce biosynthesis of a phospholipase a2 inhibitor which prevents prostaglandin generation. Nature 278, 456–459.10.1038/278456a0Search in Google Scholar PubMed

Fredman, G., Kamaly, N., Spolitu, S., Milton, J., Ghorpade, D., Chiasson, R., Kuriakose, G., Perretti, M., Farokhzad, O., and Tabas, I. (2015). Targeted nanoparticles containing the proresolving peptide ac2-26 protect against advanced atherosclerosis in hypercholesterolemic mice. Sci. Transl. Med. 7, 275ra220.10.1126/scitranslmed.aaa1065Search in Google Scholar PubMed PubMed Central

Gastardelo, T.S., Cunha, B.R., Raposo, L.S., Maniglia, J.V., Cury, P.M., Lisoni, F.C., Tajara, E.H., and Oliani, S.M. (2014). Inflammation and cancer: Role of annexin a1 and fpr2/alx in proliferation and metastasis in human laryngeal squamous cell carcinoma. PLoS One 9, e111317.10.1371/journal.pone.0111317Search in Google Scholar PubMed PubMed Central

Gavins, F.N. and Hickey, M.J. (2012). Annexin a1 and the regulation of innate and adaptive immunity. Front. Immunol. 3, 354.10.3389/fimmu.2012.00354Search in Google Scholar PubMed PubMed Central

Gavins, F.N., Yona, S., Kamal, A.M., Flower, R.J., and Perretti, M. (2003). Leukocyte antiadhesive actions of annexin 1: Alxr- and fpr-related anti-inflammatory mechanisms. Blood 101, 4140–4147.10.1182/blood-2002-11-3411Search in Google Scholar PubMed

Gavins, F.N., Leoni, G., and Getting, S.J. (2006). Annexin 1 and melanocortin peptide therapy for protection against ischaemic-reperfusion damage in the heart. Sci. World J. 6, 1008–1023.10.1100/tsw.2006.196Search in Google Scholar PubMed PubMed Central

Gavins, F.N., Dalli, J., Flower, R.J., Granger, D.N., and Perretti, M. (2007). Activation of the annexin 1 counter-regulatory circuit affords protection in the mouse brain microcirculation. FASEB J. 21, 1751–1758.10.1096/fj.06-7842comSearch in Google Scholar PubMed

Gerke, V. and Moss, S.E. (2002). Annexins: from structure to function. Physiol. Rev. 82, 331–371.10.1152/physrev.00030.2001Search in Google Scholar PubMed

Gerke, V., Creutz, C.E., and Moss, S.E. (2005). Annexins: Linking ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 6, 449–461.10.1038/nrm1661Search in Google Scholar PubMed

Go, K.G., Zuiderveen, F., De Ley, L., Ter Haar, J.G., Parente, L., Solito, E., and Molenaar, W.M. (1994). Effect of steroids on brain lipocortin immunoreactivity. Acta Neurochir. Suppl. (Wien) 60, 101–103.10.1007/978-3-7091-9334-1_26Search in Google Scholar PubMed

Gobbetti, T., Coldewey, S.M., Chen, J., McArthur, S., le Faouder, P., Cenac, N., Flower, R.J., Thiemermann, C., and Perretti, M. (2014). Nonredundant protective properties of fpr2/alx in polymicrobial murine sepsis. Proc. Natl. Acad. Sci. USA 111, 18685–18690.10.1073/pnas.1410938111Search in Google Scholar PubMed PubMed Central

Guo, C., Liu, S., and Sun, M.Z. (2013). Potential role of anxa1 in cancer. Future Oncol. 9, 1773–1793.10.2217/fon.13.114Search in Google Scholar PubMed

Hannon, R., Croxtall, J.D., Getting, S.J., Roviezzo, F., Yona, S., Paul-Clark, M.J., Gavins, F.N., Perretti, M., Morris, J.F., Buckingham, J.C., et al. (2003). Aberrant inflammation and resistance to glucocorticoids in annexin 1^-/- mouse. FASEB J. 17, 253–255.10.1096/fj.02-0239fjeSearch in Google Scholar

Hayhoe, R.P., Kamal, A.M., Solito, E., Flower, R.J., Cooper, D., and Perretti, M. (2006). Annexin 1 and its bioactive peptide inhibit neutrophil-endothelium interactions under flow: indication of distinct receptor involvement. Blood 107, 2123–2130.10.1182/blood-2005-08-3099Search in Google Scholar

Headland, S.E., Jones, H.R., Norling, L.V., Kim, A., Souza, P.R., Corsiero, E., Gil, C.D., Nerviani, A., Dell’Accio, F., Pitzalis, C., et al. (2015). Neutrophil-derived microvesicles enter cartilage and protect the joint in inflammatory arthritis. Sci. Transl. Med. 7, 315ra190.10.1126/scitranslmed.aac5608Search in Google Scholar

Huang, K.S., Wallner, B.P., Mattaliano, R.J., Tizard, R., Burne, C., Frey, A., Hession, C., McGray, P., Sinclair, L.K., Chow, E.P., et al. (1986). Two human 35 kDa inhibitors of phospholipase a2 are related to substrates of pp60v-src and of the epidermal growth factor receptor/kinase. Cell 46, 191–199.10.1016/0092-8674(86)90736-1Search in Google Scholar

Hullin, F., Raynal, P., Ragab-Thomas, J.M., Fauvel, J., and Chap, H. (1989). Effect of dexamethasone on prostaglandin synthesis and on lipocortin status in human endothelial cells. Inhibition of prostaglandin i2 synthesis occurring without alteration of arachidonic acid liberation and of lipocortin synthesis. J. Biol. Chem. 264, 3506–3513.10.1016/S0021-9258(18)94095-0Search in Google Scholar

Jia, Y., Morand, E.F., Song, W., Cheng, Q., Stewart, A., and Yang, Y.H. (2013). Regulation of lung fibroblast activation by annexin a1. J. Cell Physiol. 228, 476–484.10.1002/jcp.24156Search in Google Scholar

Kenakin, T. (1995). Agonist-receptor efficacy. Ii. Agonist trafficking of receptor signals. Trends Pharmacol. Sci. 16, 232–238.10.1016/S0165-6147(00)89032-XSearch in Google Scholar

Khau, T., Langenbach, S.Y., Schuliga, M., Harris, T., Johnstone, C.N., Anderson, R.L., and Stewart, A.G. (2011). Annexin-1 signals mitogen-stimulated breast tumor cell proliferation by activation of the formyl peptide receptors (FPRS) 1 and 2. FASEB J. 25, 483–496.10.1096/fj.09-154096Search in Google Scholar PubMed

Kosicka, A., Cunliffe, A.D., Mackenzie, R., Zariwala, M.G., Perretti, M., Flower, R.J., and Renshaw, D. (2013). Attenuation of plasma annexin a1 in human obesity. FASEB J. 27, 368–378.10.1096/fj.12-213728Search in Google Scholar PubMed

Kotas, M.E. and Medzhitov, R. (2015). Homeostasis, inflammation, and disease susceptibility. Cell 160, 816–827.10.1016/j.cell.2015.02.010Search in Google Scholar PubMed PubMed Central

Kusters, D.H., Chatrou, M.L., Willems, B.A., De Saint-Hubert, M., Bauwens, M., van der Vorst, E., Bena, S., Biessen, E.A., Perretti, M., Schurgers, L.J., et al. (2015). Pharmacological treatment with annexin a1 reduces atherosclerotic plaque burden in LDLR^-/- mice on western type diet. PLoS One 10, e0130484.10.1371/journal.pone.0130484Search in Google Scholar

La, M., D’Amico, M., Bandiera, S., Di Filippo, C., Oliani, S.M., Gavins, F.N., Flower, R.J., and Perretti, M. (2001). Annexin 1 peptides protect against experimental myocardial ischemia-reperfusion: analysis of their mechanism of action. FASEB J. 15, 2247–2256.10.1096/fj.01-0196comSearch in Google Scholar

Leikina, E., Defour, A., Melikov, K., Van der Meulen, J.H., Nagaraju, K., Bhuvanendran, S., Gebert, C., Pfeifer, K., Chernomordik, L.V., and Jaiswal, J.K. (2015). Annexin a1 deficiency does not affect myofiber repair but delays regeneration of injured muscles. Sci. Rep. 5, 18246.10.1038/srep18246Search in Google Scholar

Leoni, G., Alam, A., Neumann, P.A., Lambeth, J.D., Cheng, G., McCoy, J., Hilgarth, R.S., Kundu, K., Murthy, N., Kusters, D., et al. (2013). Annexin a1, formyl peptide receptor, and nox1 orchestrate epithelial repair. J. Clin. Invest. 123, 443–454.10.1172/JCI65831Search in Google Scholar

Leoni, G., Neumann, P.A., Kamaly, N., Quiros, M., Nishio, H., Jones, H.R., Sumagin, R., Hilgarth, R.S., Alam, A., Fredman, G., et al. (2015). Annexin a1-containing extracellular vesicles and polymeric nanoparticles promote epithelial wound repair. J. Clin. Invest. 125, 1215–1227.10.1172/JCI76693Search in Google Scholar

Locatelli, I., Sutti, S., Jindal, A., Vacchiano, M., Bozzola, C., Reutelingsperger, C., Kusters, D., Bena, S., Parola, M., Paternostro, C., et al. (2014). Endogenous annexin a1 is a novel protective determinant in nonalcoholic steatohepatitis in mice. Hepatology 60, 531–544.10.1002/hep.27141Search in Google Scholar

Maggioli, E., McArthur, S., Mauro, C., Kieswich, J., Kusters, D.H., Reutelingsperger, C.P., Yaqoob, M., and Solito, E. (2016). Estrogen protects the blood-brain barrier from inflammation-induced disruption and increased lymphocyte trafficking. Brain Behav. Immun. 51, 212–222.10.1016/j.bbi.2015.08.020Search in Google Scholar

Martin, G.R., Perretti, M., Flower, R.J., and Wallace, J.L. (2008). Annexin-1 modulates repair of gastric mucosal injury. Am. J. Physiol. Gastrointest. Liver. Physiol. 294, G764–G769.10.1152/ajpgi.00531.2007Search in Google Scholar

Morand, E.F., Hutchinson, P., Hargreaves, A., Goulding, N.J., Boyce, N.W., and Holdsworth, S.R. (1995). Detection of intracellular lipocortin 1 in human leukocyte subsets. Clin. Immunol. Immunopathol. 76, 195–202.10.1006/clin.1995.1115Search in Google Scholar

Moss, S.E. and Morgan, R.O. (2004). The annexins. Genome. Biol. 5, 219.10.1016/S0962-8924(96)10049-0Search in Google Scholar

Muesch, A., Hartmann, E., Rohde, K., Rubartelli, A., Sitia, R., and Rapoport, T.A. (1990). A novel pathway for secretory proteins? Trends Biochem. Sci. 15, 86–88.10.1016/B978-1-85166-512-9.50029-7Search in Google Scholar

Mulla, A., Leroux, C., Solito, E., and Buckingham, J.C. (2005). Correlation between the antiinflammatory protein annexin 1 (lipocortin 1) and serum cortisol in subjects with normal and dysregulated adrenal function. J. Clin. Endocrinol. Metab. 90, 557–562.10.1210/jc.2004-1230Search in Google Scholar PubMed

Neymeyer, H., Labes, R., Reverte, V., Saez, F., Stroh, T., Dathe, C., Hohberger, S., Zeisberg, M., Muller, G.A., Salazar, J., et al. (2015). Activation of annexin a1 signalling in renal fibroblasts exerts antifibrotic effects. Acta. Physiol. (Oxf). 215, 144–158.10.1111/apha.12586Search in Google Scholar PubMed

Ng, F.S., Wong, K.Y., Guan, S.P., Mustafa, F.B., Kajiji, T.S., Bist, P., Biswas, S.K., Wong, W.S., and Lim, L.H. (2011). Annexin-1-deficient mice exhibit spontaneous airway hyperresponsiveness and exacerbated allergen-specific antibody responses in a mouse model of asthma. Clin. Exp. Allergy. 41, 1793–1803.10.1111/j.1365-2222.2011.03855.xSearch in Google Scholar PubMed

Oliani, S.M., Christian, H.C., Manston, J., Flower, R.J., and Perretti, M. (2000). An immunocytochemical and in situ hybridization analysis of annexin 1 expression in rat mast cells: Modulation by inflammation and dexamethasone. Lab. Invest. 80, 1429–1438.10.1038/labinvest.3780150Search in Google Scholar PubMed

Oliani, S.M., Damazo, A.S., and Perretti, M. (2002). Annexin 1 localisation in tissue eosinophils as detected by electron microscopy. Mediat. Inflamm. 11, 287–292.10.1080/09629350210000015683Search in Google Scholar PubMed PubMed Central

Paschalidis, N., Iqbal, A.J., Maione, F., Wood, E.G., Perretti, M., Flower, R.J., and D’Acquisto, F. (2009). Modulation of experimental autoimmune encephalomyelitis by endogenous annexin a1. J. Neuroinflammation. 6, 33.10.1186/1742-2094-6-33Search in Google Scholar PubMed PubMed Central

Patel, H.B., Kornerup, K.N., Sampaio, A.L., D’Acquisto, F., Seed, M.P., Girol, A.P., Gray, M., Pitzalis, C., Oliani, S.M., and Perretti, M. (2012). The impact of endogenous annexin a1 on glucocorticoid control of inflammatory arthritis. Ann. Rheum. Dis. 71, 1872–1880.10.1136/annrheumdis-2011-201180Search in Google Scholar PubMed PubMed Central

Peers, S.H., Smillie, F., Elderfield, A.J., and Flower, R.J. (1993). Glucocorticoid-and non-glucocorticoid induction of lipocortins (annexins) 1 and 2 in rat peritoneal leucocytes in vivo. Br. J. Pharmacol. 108, 66–72.10.1111/j.1476-5381.1993.tb13441.xSearch in Google Scholar PubMed PubMed Central

Perretti, M. (2003). The annexin 1 receptor(s): is the plot unravelling? Trends Pharmacol. Sci. 24, 574–579.10.1016/j.tips.2003.09.010Search in Google Scholar PubMed

Perretti, M. (2015). The resolution of inflammation: new mechanisms in patho-physiology open opportunities for pharmacology. Semin. Immunol. 27, 145–148.10.1016/j.smim.2015.06.001Search in Google Scholar

Perretti, M. and D’Acquisto, F. (2009). Annexin a1 and glucocorticoids as effectors of the resolution of inflammation. Nat. Rev. Immunol. 9, 62–70.10.1038/nri2470Search in Google Scholar

Perretti, M., Croxtall, J.D., Wheller, S.K., Goulding, N.J., Hannon, R., and Flower, R.J. (1996). Mobilizing lipocortin 1 in adherent human leukocytes downregulates their transmigration. Nat. Med. 2, 1259–1262.10.1038/nm1196-1259Search in Google Scholar

Perretti, M., Christian, H., Wheller, S.K., Aiello, I., Mugridge, K.G., Morris, J.F., Flower, R.J., and Goulding, N.J. (2000). Annexin i is stored within gelatinase granules of human neutrophil and mobilized on the cell surface upon adhesion but not phagocytosis. Cell Biol. Int. 24, 163–174.10.1006/cbir.1999.0468Search in Google Scholar

Perretti, M., Chiang, N., La, M., Fierro, I.M., Marullo, S., Getting, S.J., Solito, E., and Serhan, C.N. (2002). Endogenous lipid- and peptide-derived anti-inflammatory pathways generated with glucocorticoid and aspirin treatment activate the lipoxin a4 receptor. Nat Med. 8, 1296–1302.10.1038/nm786Search in Google Scholar

Perretti, M., Leroy, X., Bland, E.J., and Montero-Melendez, T. (2015). Resolution pharmacology: Opportunities for therapeutic innovation in inflammation. Trends Pharmacol. Sci. 36, 737–755.10.1016/j.tips.2015.07.007Search in Google Scholar

Pitt, J.M., Kroemer, G., and Zitvogel, L. (2016). Extracellular vesicles: Masters of intercellular communication and potential clinical interventions. J. Clin. Invest. 126, 1139–1143.10.1172/JCI87316Search in Google Scholar

Qin, C., Buxton, K.D., Pepe, S., Cao, A.H., Venardos, K., Love, J.E., Kaye, D.M., Yang, Y.H., Morand, E.F., and Ritchie, R.H. (2013). Reperfusion-induced myocardial dysfunction is prevented by endogenous annexin-a1 and its n-terminal-derived peptide ac-anx-a1(2-26). Br. J. Pharmacol. 168, 238–252.10.1111/j.1476-5381.2012.02176.xSearch in Google Scholar

Qin, C., Yang, Y.H., May, L., Gao, X., Stewart, A.G., Tu, Y., Woodman, O.L., and Ritchie, R.H. (2015). Cardioprotective potential of annexin-a1 mimetics in myocardial infarction. Pharmacol. Ther. 148, 47–65.10.1016/j.pharmthera.2014.11.012Search in Google Scholar

Quehenberger, O., Prossnitz, E.R., Cavanagh, S.L., Cochrane, C.G., and Ye, R.D. (1993). Multiple domains of the n-formyl peptide receptor are required for high-affinity ligand binding. Construction and analysis of chimeric n-formyl peptide receptors. J. Biol. Chem. 268, 18167–18175.10.1016/S0021-9258(17)46825-6Search in Google Scholar

Raynal, P. and Pollard, H.B. (1994). Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim. Biophys. Acta 1197, 63–93.10.1016/0304-4157(94)90019-1Search in Google Scholar

Rescher, U., Goebeler, V., Wilbers, A., and Gerke, V. (2006). Proteolytic cleavage of annexin 1 by human leukocyte elastase. Biochim. Biophys. Acta 1763, 1320–1324.10.1016/j.bbamcr.2006.08.041Search in Google Scholar

Ritchie, R.H., Sun, X., Bilszta, J.L., Gulluyan, L.M., and Dusting, G.J. (2003). Cardioprotective actions of an n-terminal fragment of annexin-1 in rat myocardium in vitro. Eur J. Pharmacol. 461, 171–179.10.1016/S0014-2999(03)01314-1Search in Google Scholar

Ritchie, R.H., Gordon, J.M., Woodman, O.L., Cao, A.H., and Dusting, G.J. (2005). Annexin-1 peptide anx-1(2-26) protects adult rat cardiac myocytes from cellular injury induced by simulated ischaemia. Br. J. Pharmacol. 145, 495–502.10.1038/sj.bjp.0706211Search in Google Scholar

Romisch, J., Schuler, E., Bastian, B., Burger, T., Dunkel, F.G., Schwinn, A., Hartmann, A.A., and Paques, E.P. (1992). Annexins I to VI: quantitative determination in different human cell types and in plasma after myocardial infarction. Blood Coagul. Fibrinolysis. 3, 11–17.10.1097/00001721-199202000-00003Search in Google Scholar

Rosengarth, A., Gerke, V., and Luecke, H. (2001a). X-ray structure of full-length annexin 1 and implications for membrane aggregation. J. Mol. Biol. 306, 489–498.10.1006/jmbi.2000.4423Search in Google Scholar

Rosengarth, A., Rosgen, J., Hinz, H.J., and Gerke, V. (2001b). Folding energetics of ligand binding proteins ii. Cooperative binding of Ca²⁺ to annexin i. J. Mol. Biol. 306, 825–835.10.1006/jmbi.2000.4358Search in Google Scholar

Rothblum, E.D. (2009). An overview of same-sex couples in relation ships: a research area still at sea. Nebr. Symp. Motiv. 54, 113–139.10.1007/978-0-387-09556-1_5Search in Google Scholar

Rothhut, B., Russo-Marie, F., Wood, J., DiRosa, M., and Flower, R.J. (1983). Further characterization of the glucocorticoid-induced antiphospholipase protein “renocortin”. Biochem. Biophys. Res. Commun. 117, 878–884.10.1016/0006-291X(83)91678-9Search in Google Scholar

Ryan, G.B. and Majno, G. (1977). Acute inflammation. A review. Am. J. Pathol. 86, 183–276.10.1007/978-1-349-17334-1_13Search in Google Scholar

Sampey, A.V., Hutchinson, P., and Morand, E.F. (2000). Annexin i surface binding sites and their regulation on human fibroblast-like synoviocytes. Arthritis Rheum. 43, 2537–2542.10.1002/1529-0131(200011)43:11<2537::AID-ANR22>3.0.CO;2-MSearch in Google Scholar

Saris, C.J., Tack, B.F., Kristensen, T., Glenney, Jr. J.R., and Hunter, T. (1986). The cDNA sequence for the protein-tyrosine kinase substrate p36 (calpactin I heavy chain) reveals a multidomain protein with internal repeats. Cell 46, 201–212.10.1016/0092-8674(86)90737-3Search in Google Scholar

Sena, A., Grishina, I., Thai, A., Goulart, L., Macal, M., Fenton, A., Li, J., Prindiville, T., Oliani, S.M., Dandekar, S., et al. (2013). Dysregulation of anti-inflammatory annexin a1 expression in progressive crohns disease. PLoS One 8, e76969.10.1371/journal.pone.0076969Search in Google Scholar PubMed PubMed Central

Sinniah, A., Yazid, S., Perretti, M., Solito, E., and Flower, R.J. (2016). The role of the annexin-a1/fpr2 system in the regulation of mast cell degranulation provoked by compound 48/80 and in the inhibitory action of nedocromil. Int. Immunopharmacol. 32, 87–95.10.1016/j.intimp.2016.01.003Search in Google Scholar PubMed PubMed Central

Smith, S.F., Tetley, T.D., Guz, A., and Flower, R.J. (1990). Detection of lipocortin 1 in human lung lavage fluid: Lipocortin degradation as a possible proteolytic mechanism in the control of inflammatory mediators and inflammation. Environ. Health. Perspect. 85, 135–144.10.1289/ehp.85-1568329Search in Google Scholar

Smith, H.K., Gil, C.D., Oliani, S.M., and Gavins, F.N. (2015). Targeting formyl peptide receptor 2 reduces leukocyte-endothelial interactions in a murine model of stroke. FASEB J. 29, 2161–2171.10.1096/fj.14-263160Search in Google Scholar PubMed

Soehnlein, O., Zernecke, A., Eriksson, E.E., Rothfuchs, A.G., Pham, C.T., Herwald, H., Bidzhekov, K., Rottenberg, M.E., Weber, C., and Lindbom, L. (2008). Neutrophil secretion products pave the way for inflammatory monocytes. Blood 112, 1461–1471.10.1182/blood-2008-02-139634Search in Google Scholar PubMed PubMed Central

Solito, E., Raguenes-Nicol, C., de Coupade, C., Bisagni-Faure, A., and Russo-Marie, F. (1998). U937 cells deprived of endogenous annexin 1 demonstrate an increased pla2 activity. Br J. Pharmacol. 124, 1675–1683.10.1038/sj.bjp.0701991Search in Google Scholar PubMed PubMed Central

Solito, E., Romero, I.A., Marullo, S., Russo-Marie, F., and Weksler, B.B. (2000). Annexin 1 binds to u937 monocytic cells and inhibits their adhesion to microvascular endothelium: involvement of the α4 β1 integrin. J. Immunol. 165, 1573–1581.10.4049/jimmunol.165.3.1573Search in Google Scholar PubMed

Solito, E., Christian, H.C., Festa, M., Mulla, A., Tierney, T., Flower, R.J., and Buckingham, J.C. (2006). Post-translational modification plays an essential role in the translocation of annexin a1 from the cytoplasm to the cell surface. FASEB J. 20, 1498–1500.10.1096/fj.05-5319fjeSearch in Google Scholar PubMed PubMed Central

Souza, D.G., Fagundes, C.T., Amaral, F.A., Cisalpino, D., Sousa, L.P., Vieira, A.T., Pinho, V., Nicoli, J.R., Vieira, L.Q., Fierro, I.M., et al. (2007). The required role of endogenously produced lipoxin a4 and annexin-1 for the production of il-10 and inflammatory hyporesponsiveness in mice. J. Immunol. 179, 8533–8543.10.4049/jimmunol.179.12.8533Search in Google Scholar PubMed

Sugimoto, M.A., Vago, J.P., Teixeira, M.M., and Sousa, L.P. (2016). Annexin a1 and the resolution of inflammation: Modulation of neutrophil recruitment, apoptosis, and clearance. J. Immunol. Res. 2016, 8239258.10.1155/2016/8239258Search in Google Scholar PubMed PubMed Central

Tagoe, C.E., Marjanovic, N., Park, J.Y., Chan, E.S., Abeles, A.M., Attur, M., Abramson, S.B., and Pillinger, M.H. (2008). Annexin-1 mediates tnf-alpha-stimulated matrix metalloproteinase secretion from rheumatoid arthritis synovial fibroblasts. J. Immunol. 181, 2813–2820.10.4049/jimmunol.181.4.2813Search in Google Scholar

Tsao, F.H., Meyer, K.C., Chen, X., Rosenthal, N.S., and Hu, J. (1998). Degradation of annexin i in bronchoalveolar lavage fluid from patients with cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 18, 120–128.10.1165/ajrcmb.18.1.2808Search in Google Scholar

Vergnolle, N., Pages, P., Guimbaud, R., Chaussade, S., Bueno, L., Escourrou, J., and Comera, C. (2004). Annexin 1 is secreted in situ during ulcerative colitis in humans. Inflamm. Bowel. Dis. 10, 584–592.10.1097/00054725-200409000-00013Search in Google Scholar

Viiri, L.E., Full, L.E., Navin, T.J., Begum, S., Didangelos, A., Astola, N., Berge, R.K., Seppala, I., Shalhoub, J., Franklin, I.J., et al. (2013). Smooth muscle cells in human atherosclerosis: Proteomic profiling reveals differences in expression of annexin a1 and mitochondrial proteins in carotid disease. J. Mol. Cell Cardiol. 54, 65–72.10.1016/j.yjmcc.2012.11.002Search in Google Scholar

Vong, L., D’Acquisto, F., Pederzoli-Ribeil, M., Lavagno, L., Flower, R.J., Witko-Sarsat, V., and Perretti, M. (2007). Annexin 1 cleavage in activated neutrophils: a pivotal role for proteinase 3. J. Biol. Chem. 282, 29998–30004.10.1074/jbc.M702876200Search in Google Scholar

Vong, L., Ferraz, J.G., Dufton, N., Panaccione, R., Beck, P.L., Sherman, P.M., Perretti, M., and Wallace, J.L. (2012). Up-regulation of annexin-a1 and lipoxin a(4) in individuals with ulcerative colitis may promote mucosal homeostasis. PLoS One 7, e39244.10.1371/journal.pone.0039244Search in Google Scholar

Walther, A., Riehemann, K., and Gerke, V. (2000). A novel ligand of the formyl peptide receptor: Annexin I regulates neutrophil extravasation by interacting with the FPR. Mol. Cell 5, 831–840.10.1016/S1097-2765(00)80323-8Search in Google Scholar

Wein, S., Fauroux, M., Laffitte, J., de Nadai, P., Guaini, C., Pons, F., and Comera, C. (2004). Mediation of annexin 1 secretion by a probenecid-sensitive abc-transporter in rat inflamed mucosa. Biochem. Pharmacol. 67, 1195–1202.10.1016/j.bcp.2003.11.015Search in Google Scholar PubMed

Yang, Y.H., Morand, E.F., Getting, S.J., Paul-Clark, M., Liu, D.L., Yona, S., Hannon, R., Buckingham, J.C., Perretti, M., and Flower, R.J. (2004). Modulation of inflammation and response to dexamethasone by annexin 1 in antigen-induced arthritis. Arthritis Rheum. 50, 976–984.10.1002/art.20201Search in Google Scholar PubMed

Ye, R.D., Boulay, F., Wang, J.M., Dahlgren, C., Gerard, C., Parmentier, M., Serhan, C.N., and Murphy, P.M. (2009). International union of basic and clinical pharmacology. Lxxiii. Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol. Rev. 61, 119–161.10.1124/pr.109.001578Search in Google Scholar PubMed PubMed Central