263
Views
4
CrossRef citations to date
0
Altmetric
Retina/Optic Nerve

Annexin A1 Promotes Reparative Angiogenesis and Ameliorates Neuronal Injury in Ischemic Retinopathy

, , & ORCID Icon
Pages 791-801 | Received 20 Aug 2021, Accepted 12 Jan 2022, Published online: 22 Mar 2022

References

  • Osborne NN, Casson RJ, Wood JP, Chidlow G, Graham M, Melena J. Retinal ischemia: mechanisms of damage and potential therapeutic strategies. Prog Retin Eye Res. 2004;23:91–147. doi:10.1016/j.preteyeres.2003.12.001.
  • Duh EJ, Sun JK, Stitt AW. Diabetic retinopathy: current understanding, mechanisms, and treatment strategies. JCI Insight. 2017;2:e93751. doi:10.1172/jci.insight.93751.
  • Zhou TE, Rivera JC, Bhosle VK, Lahaie I, Shao Z, Tahiri H, Zhu T, Polosa A, Dorfman A, Beaudry-Richard A, et al. Choroidal involution is associated with a progressive degeneration of the outer retinal function in a model of retinopathy of prematurity: early role for IL-1β. Am J Pathol. 2016;186:3100–3116. doi:10.1016/j.ajpath.2016.08.004.
  • Gardiner TA, Gibson DS, de Gooyer TE, de la Cruz VF, McDonald DM, Stitt AW. Inhibition of tumor necrosis factor-alpha improves physiological angiogenesis and reduces pathological neovascularization in ischemic retinopathy. Am J Pathol. 2005;166:637–644. doi:10.1016/S0002-9440(10)62284-5.
  • Szade A, Grochot-Przeczek A, Florczyk U, Jozkowicz A, Dulak J. Cellular and molecular mechanisms of inflammation-induced angiogenesis. IUBMB Life. 2015;67:145–159. doi:10.1002/iub.1358.
  • Jelinic M, Kahlberg N, Leo CH, Ng HH, Rosli S, Deo M, Li M, Finlayson S, Walsh J, Parry LJ, et al. Annexin-A1 deficiency exacerbates pathological remodelling of the mesenteric vasculature in insulin-resistant, but not insulin-deficient, mice. Br J Pharmacol. 2020;177:1677–1691. doi:10.1111/bph.14927.
  • Qin CX, Finlayson SB, Al-Sharea A, Tate M, De Blasio MJ, Deo M, Rosli S, Prakoso D, Thomas CJ, Kiriazis H, et al. Endogenous annexin-A1 regulates haematopoietic stem cell mobilisation and inflammatory response post myocardial infarction in mice in vivo. Sci Rep. 2017;7:16615. doi:10.1038/s41598-017-16317-1.
  • Liao WI, Wu SY, Wu GC, Pao HP, Tang SE, Huang KL, Chu SJ. Ac2-26, an annexin A1 peptide, attenuates ischemia-reperfusion-induced acute lung injury. Int J Mol Sci. 2017;18:1771.
  • Guido BC, Zanatelli M, Tavares-de-Lima W, Oliani SM, Damazo AS. Annexin-A1 peptide down-regulates the leukocyte recruitment and up-regulates interleukin-10 release into lung after intestinal ischemia-reperfusion in mice. J Inflamm (Lond). 2013;10:10. doi:10.1186/1476-9255-10-10.
  • Lacerda JZ, Drewes CC, Mimura KKO, Zanon CF, Ansari T, Gil CD, Greco KV, Farsky SHP, Oliani SM. Annexin A1(2-26) treatment improves skin heterologous transplantation by modulating inflammation and angiogenesis processes. Front Pharmacol. 1015;9:1015.
  • Smith LE, Wesolowski E, McLellan A, Kostyk SK, D'Amato R, Sullivan R. D'Amore PA. Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci. 1994;35:101–111.
  • Connor KM, Krah NM, Dennison RJ, Aderman CM, Chen J, Guerin KI, Sapieha P, Stahl A, Willett KL, Smith LE. Quantification of oxygen-induced retinopathy in the mouse: a model of vessel loss, vessel regrowth and pathological angiogenesis. Nat Protoc. 2009;4:1565–1573. doi:10.1038/nprot.2009.187.
  • Wei Y, Gong J, Xu Z, Duh EJ. Nrf2 promotes reparative angiogenesis through regulation of NADPH oxidase-2 in oxygen-induced retinopathy. Free Radic Biol Med. 2016;99:234–243. (doi:10.1016/j.freeradbiomed.2016.08.013.
  • Soucy KG, Attarzadeh DO, Ramachandran R, Soucy PA, Romer LH, Shoukas AA, Berkowitz DE. Single exposure to radiation produces early anti-angiogenic effects in mouse aorta. Radiat Environ Biophys. 2010;49:397–404. doi:10.1007/s00411-010-0287-z.
  • Qiu F, Meng T, Chen Q, Zhou K, Shao Y, Matlock G, Ma X, Wu W, Du Y, Wang X, et al. Fenofibrate-loaded biodegradable nanoparticles for the treatment of experimental diabetic retinopathy and neovascular age-related macular degeneration. Mol Pharm. 2019;16:1958–1970. doi:10.1021/acs.molpharmaceut.8b01319.
  • Facio FN, Jr., Sena AA, Araújo LP, Mendes GE, Castro I, Luz MA, Yu L, Oliani SM, Burdmann EA. Annexin 1 mimetic peptide protects against renal ischemia/reperfusion injury in rats. J Mol Med (Berl). 2011;89:51–63. doi:10.1007/s00109-010-0684-4.
  • Haridas V, Shetty P, Sarathkumar E, Bargale A, Vishwanatha JK, Patil V, Dinesh US. Reciprocal regulation of pro-inflammatory Annexin A2 and anti-inflammatory Annexin A1 in the pathogenesis of rheumatoid arthritis. Mol Biol Rep. 2019;46:83–95. doi:10.1007/s11033-018-4448-5.
  • Bai Y, Ma JX, Guo J, Wang J, Zhu M, Chen Y, Le YZ. Müller cell-derived VEGF is a significant contributor to retinal neovascularization. J Pathol. 2019;219:446–454. doi:10.1002/path.2611.
  • Watanabe D, Suzuma K, Matsui S, Kurimoto M, Kiryu J, Kita M, Suzuma I, Ohashi H, Ojima T, Murakami T, et al. Erythropoietin as a retinal angiogenic factor in proliferative diabetic retinopathy. N Engl J Med. 2005;353:782–792. doi:10.1056/NEJMoa041773.
  • Ferraro B, Leoni G, Hinkel R, Ormanns S, Paulin N, Ortega-Gomez A, Viola JR, de Jong R, Bongiovanni D, Bozoglu T, et al. Pro-angiogenic macrophage phenotype to promote myocardial repair. J Am Coll Cardiol. 2019;73:2990–3002. doi:10.1016/j.jacc.2019.03.503.
  • Stahl A, Connor KM, Sapieha P, Chen J, Dennison RJ, Krah NM, Seaward MR, Willett KL, Aderman CM, Guerin KI, et al. The mouse retina as an angiogenesis model. Invest Ophthalmol Vis Sci. 2010;51:2813–2826. doi:10.1167/iovs.10-5176.
  • Gimenes AD, Andrade BFD, Pinotti JVP, Oliani SM, Galvis-Alonso OY, Gil CD. Annexin A1-derived peptide Ac2-26 in a pilocarpine-induced status epilepticus model: anti-inflammatory and neuroprotective effects. J Neuroinflamm 2019;16:32. doi:10.1186/s12974-019-1414-7.
  • Vessey KA, Wilkinson-Berka JL, Fletcher EL. Characterization of retinal function and glial cell response in a mouse model of oxygen-induced retinopathy. J Comp Neurol. 2011;519:506–527. doi:10.1002/cne.22530.
  • Rivera JC, Sitaras N, Noueihed B, Hamel D, Madaan A, Zhou T, Honore JC, Quiniou C, Joyal JS, Hardy P, et al. Microglia and interleukin-1β in ischemic retinopathy elicit microvascular degeneration through neuronal semaphorin-3A. Arterioscler Thromb Vasc Biol 2013;33:1881–1891. doi:10.1161/ATVBAHA.113.301331.
  • Pan B, Kong J, Jin J, Kong J, He Y, Dong S, Ji L, Liu D, He D, Kong L, et al. A novel anti-inflammatory mechanism of high density lipoprotein through up-regulating annexin A1 in vascular endothelial cells. Biochim Biophys Acta. 2016;1861:501–512. doi:10.1016/j.bbalip.2016.03.022.
  • Koerdt SN, Gerke V. 2017. Annexin A2 is involved in Ca2+-dependent plasma membrane repair in primary human endothelial cells. Biochim Biophys Acta Mol Cell Res 1864:1046–1053. doi:10.1016/j.bbamcr.2016.12.007.
  • Machado MG, Tavares LP, Souza GVS, Queiroz-Junior CM, Ascenção FR, Lopes ME, Garcia CC, Menezes GB, Perretti M, Russo RC, et al. The Annexin A1/FPR2 pathway controls the inflammatory response and bacterial dissemination in experimental pneumococcal pneumonia. FASEB J. 2020;34:2749–2764. doi:10.1096/fj.201902172R.
  • Sakaguchi M, Murata H, Sonegawa H, Sakaguchi Y, Futami J, Kitazoe M, Yamada H, Huh NH. Truncation of annexin A1 is a regulatory lever for linking epidermal growth factor signaling with cytosolic phospholipase A2 in normal and malignant squamous epithelial cells. J Biol Chem. 2007;282:35679–35686. doi:10.1074/jbc.M707538200.
  • Han PF, Che XD, Li HZ, Gao YY, Wei XC, Li PC. Annexin A1 involved in the regulation of inflammation and cell signaling pathways. Chin J Traumatol. 2020;23:96–101. doi:10.1016/j.cjtee.2020.02.002.
  • Sitaras N, Rivera JC, Noueihed B, Bien-Aimé M, Zaniolo K, Omri S, Hamel D, Zhu T, Hardy P, Sapieha P, et al. Retinal neurons curb inflammation and enhance revascularization in ischemic retinopathies via proteinase-activated receptor-2. Am J Pathol. 2015;185:581–595. doi:10.1016/j.ajpath.2014.10.020.
  • Schultz GS, Grant MB. Neovascular growth factors. Eye (Lond). 1991;5:170–180. doi:10.1038/eye.1991.31.
  • Wei Y, Gong J, Xu Z, Thimmulappa RK, Mitchell KL, Welsbie DS, Biswal S, Duh EJ. Nrf2 in ischemic neurons promotes retinal vascular regeneration through regulation of semaphorin 6A. Proc Natl Acad Sci USA. 2015;112:E6927–6936. doi:10.1073/pnas.1512683112.
  • Yi M, Schnitzer JE. Impaired tumor growth, metastasis, angiogenesis and wound healing in annexin A1-null mice. Proc Natl Acad Sci USA. 2009;106:17886–17891. doi:10.1073/pnas.0901324106.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.