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Research Article

Spermine oxidase inhibitor, MDL 72527, reduced neovascularization, vascular permeability, and acrolein-conjugated proteins in a mouse model of ischemic retinopathy

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Article: 2347070 | Received 28 Dec 2023, Accepted 19 Apr 2024, Published online: 29 Apr 2024

References

  • Kempen JH, O’Colmain BJ, Leske MC, Haffner SM, Klein R, Moss SE, Taylor HR, Hamman RF. Eye Diseases prevalence research G: The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol. 2004;122:552–15.
  • Gilbert C, Rahi J, Eckstein M, O’Sullivan J, Foster A. Retinopathy of prematurity in middle-income countries. Lancet. 1997;350:12–14. doi:10.1016/S0140-6736(97)01107-0.
  • Yang L, Wu L, Wang D, Li Y, Dou H, Tso MO, Ma, Z. Role of endoplasmic reticulum stress in the loss of retinal ganglion cells in diabetic retinopathy. Neural Regen Res. 2013;8:3148–3158. doi:10.3969/j.issn.1673-5374.2013.33.009.
  • Aouiss A, Anka Idrissi D, Kabine M, Zaid Y. Update of inflammatory proliferative retinopathy: ischemia, hypoxia and angiogenesis. Curr Res Transl Med. 2019;67(2):62–71. doi:10.1016/j.retram.2019.01.005.
  • McLeod DS, Brownstein R, Lutty GA. Vaso-obliteration in the canine model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci. 1996;37(2):300–311.
  • Penn JS, Henry MM, Tolman BL. Exposure to alternating hypoxia and hyperoxia causes severe proliferative retinopathy in the newborn rat. Pediatr Res. 1994;36(6):724–731. doi:10.1203/00006450-199412000-00007.
  • Kubota Y, Suda T. Feedback mechanism between blood vessels and astrocytes in retinal vascular development. Trends Cardiovasc Med. 2009;19(2):38–43. doi:10.1016/j.tcm.2009.04.004.
  • Al-Shabrawey M, Elsherbiny M, Nussbaum J, Othman A, Megyerdi S, Tawfik, A. Targeting neovascularization in Ischemic Retinopathy: recent advances. Expert Rev Ophthalmol. 2013;8:267–286. doi:10.1586/eop.13.17.
  • Peng S, Gan G, Rao VS, Adelman RA, Rizzolo LJ. Effects of proinflammatory cytokines on the claudin-19 rich tight junctions of human retinal pigment epithelium. Invest Ophthalmol Vis Sci. 2012;53(8):5016–5028. doi:10.1167/iovs.11-8311.
  • Eichler W, Yafai Y, Keller T, Wiedemann P, Reichenbach A. PEDF derived from glial müller cells: a possible regulator of retinal angiogenesis. Exp Cell Res. 2004;299(1):68–78. doi:10.1016/j.yexcr.2004.05.020.
  • Duh EJ, Yang HS, Suzuma I, Miyagi M, Youngman E, Mori K, Katai M, Yan L, Suzuma K, West K. et al. Pigment epithelium-derived factor suppresses ischemia-induced retinal neovascularization and VEGF-induced migration and growth. Invest Ophthalmol Vis Sci. 2002;43(3):821–829.
  • Runkle EA, Antonetti DA. The blood-retinal barrier: structure and functional significance. Methods Mol Biol. 2011;686:133–148.
  • Weiger TM, Hermann A. Cell proliferation, potassium channels, polyamines and their interactions: a mini review. Amino Acids. 2014;46(3):681–688. doi:10.1007/s00726-013-1536-7.
  • Casero RA, Pegg AE. Polyamine catabolism and disease. Biochem J. 2009;421(3):323–338. doi:10.1042/BJ20090598.
  • Narayanan SP, Shosha E, C DP. Spermine oxidase: a promising therapeutic target for neurodegeneration in diabetic retinopathy. Pharmacol Res. 2019;147:104299. doi:10.1016/j.phrs.2019.104299.
  • Moghe A, Ghare S, Lamoreau B, Mohammad M, Barve S, McClain C, Joshi-Barve S. Molecular mechanisms of acrolein toxicity: relevance to human disease. Toxicol Sci. 2015;143(2):242–255. doi:10.1093/toxsci/kfu233.
  • Patel C, Xu Z, Shosha E, Xing J, Lucas R, Caldwell RW, Caldwell RB, Narayanan SP. Treatment with polyamine oxidase inhibitor reduces microglial activation and limits vascular injury in ischemic retinopathy. Biochim Biophys Acta. 2016;1862(9):1628–1639. doi:10.1016/j.bbadis.2016.05.020.
  • Narayanan SP, Xu Z, Putluri N, Sreekumar A, Lemtalsi T, Caldwell RW, Caldwell RB. Arginase 2 deficiency reduces hyperoxia-mediated retinal neurodegeneration through the regulation of polyamine metabolism. Cell Death Disease. 2014;5(2):e1075. doi:10.1038/cddis.2014.23.
  • Pichavaram P, Palani CD, Patel C, Xu Z, Shosha E, Fouda AY, Caldwell RB, Narayanan SP. Targeting polyamine oxidase to prevent excitotoxicity-induced retinal neurodegeneration. Front Neurosci. 2018;12:956. doi:10.3389/fnins.2018.00956.
  • Liu F, Saul AB, Pichavaram P, Xu Z, Rudraraju M, Somanath PR, Smith SB, Caldwell RB, Narayanan SP. Pharmacological inhibition of spermine oxidase reduces neurodegeneration and improves retinal function in diabetic mice. J Clin Med. 2020;9(2):9(2. doi:10.3390/jcm9020340.
  • Wang Y, Hacker A, Murray-Stewart T, Fleischer J, Woster P, Casero R. Induction of human spermine oxidase SMO(PAOh1) is regulated at the levels of new mRNA synthesis, mRNA stabilization and newly synthesized protein. Biochem J. 2005;386(3):543–547. doi:10.1042/BJ20041084.
  • Babbar N, Casero RA. Tumor necrosis factor-alpha increases reactive oxygen species by inducing spermine oxidase in human lung epithelial cells: a potential mechanism for inflammation-induced carcinogenesis. Cancer Res. 2006;66(23):11125–11130. doi:10.1158/0008-5472.CAN-06-3174.
  • Seghieri G, Gironi A, Niccolai M, Mammini P, Alviggi L, Giorgio LA, Caselli P, Bartolomei G. Serum spermidine oxidase activity in patients with insulin-dependent diabetes mellitus and microvascular complications. Acta Diabetol Lat. 1990;27(4):303–308. doi:10.1007/BF02580934.
  • Shan S, Liu F, Ford E, Caldwell RB, Narayanan SP, Somanath PR. Triciribine attenuates pathological neovascularization and vascular permeability in a mouse model of proliferative retinopathy. Biomed Pharmacother. 2023;162:114714. doi:10.1016/j.biopha.2023.114714.
  • Patel C, Narayanan SP, Zhang W, Xu Z, Sukumari-Ramesh S, Dhandapani KM, Caldwell RW, Caldwell RB. Activation of the endothelin system mediates pathological angiogenesis during ischemic retinopathy. Am J Pathol. 2014;184(11):3040–3051. doi:10.1016/j.ajpath.2014.07.012.
  • Stahl A, Connor KM, Sapieha P, Willett KL, Krah NM, Dennison RJ, Chen J, Guerin KI, Smith LEH. Computer-aided quantification of retinal neovascularization. Angiogenesis. 2009;12(3):297–301. doi:10.1007/s10456-009-9155-3.
  • Palani CD, Fouda AY, Liu F, Xu Z, Mohamed E, Giri S, Smith SB, Caldwell RB, Narayanan SP. Deletion of Arginase 2 ameliorates retinal neurodegeneration in a mouse Model of multiple sclerosis. Mol Neurobiol. 2019;56(12):8589–8602. doi:10.1007/s12035-019-01691-w.
  • Candadai AA, Liu F, Fouda AY, Alfarhan M, Palani CD, Xu Z, Caldwell RB, Narayanan SP. Deletion of arginase 2 attenuates neuroinflammation in an experimental model of optic neuritis. PLOS ONE. 2021;16(3):e0247901. doi:10.1371/journal.pone.0247901.
  • Alfarhan M, Liu F, Shan S, Pichavaram P, Somanath PR, Narayanan SP. Pharmacological inhibition of spermine oxidase suppresses excitotoxicity induced neuroinflammation in Mouse Retina. Int J Mol Sci. 2022;23(4):23(4. doi:10.3390/ijms23042133.
  • Rudraraju M, Narayanan SP, Somanath PR. Distinct mechanisms of human retinal endothelial barrier modulation in vitro by mediators of diabetes and uveitis. Life (Basel). 2021;12(1):33. doi:10.3390/life12010033.
  • Chen S, Zhang J, Sun D, Wu Y, Fang J, Wan X, Li S, Zhang S, Gu Q, Shao Q. et al. SYVN1 promotes STAT3 protein ubiquitination and exerts antiangiogenesis effects in retinopathy of prematurity development. Invest Ophthalmol Vis Sci. 2023;64(11):8. doi:10.1167/iovs.64.11.8.
  • Gui F, You Z, Fu S, Wu H, Zhang Y. Endothelial dysfunction in Diabetic Retinopathy. Front Endocrinol (Lausanne). 2020;11:591. doi:10.3389/fendo.2020.00591.
  • Alfarhan M, Jafari E, Narayanan SP. Acrolein: a potential Mediator of oxidative damage in diabetic retinopathy. Biomolecules. 2020;10(11):10(11. doi:10.3390/biom10111579.
  • Patel AK, Syeda S, Hackam AS. Signal transducer and activator of transcription 3 (STAT3) signaling in retinal pigment epithelium cells. JAKSTAT. 2013;2(4):e25434. doi:10.4161/jkst.25434.
  • Gong K, Jiao J, Xu C, Dong Y, Li D, He D, Zhao D, Yu J, Sun Y, Zhang W. et al. The targetable nanoparticle BAF312@cRGD-CaP-NP represses tumor growth and angiogenesis by downregulating the S1PR1/P-STAT3/VEGFA axis in triple-negative breast cancer. J Nanobiotechnol. 2021;19(1):165. doi:10.1186/s12951-021-00904-6.
  • Gao P, Yi J, Chen W, Gu J, Miao S, Wang X, Huang Y, Jiang T, Li Q, Zhou W. et al. Pericyte-derived exosomal miR-210 improves mitochondrial function and inhibits lipid peroxidation in vascular endothelial cells after traumatic spinal cord injury by activating JAK1/STAT3 signaling pathway. J Nanobiotechnol. 2023;21(1):452. doi:10.1186/s12951-023-02110-y.
  • Zahedi K, Huttinger F, Morrison R, Murray-Stewart T, Casero RA, Strauss KI. Polyamine catabolism is enhanced after traumatic brain injury. J Neurotrauma. 2010;27(3):515–525. doi:10.1089/neu.2009.1097.
  • Fouda AY, Xu Z, Suwanpradid J, Rojas M, Shosha E, Lemtalsi T, Patel C, Xing J, Zaidi SA, Zhi W. et al. Targeting proliferative retinopathy: Arginase 1 limits vitreoretinal neovascularization and promotes angiogenic repair. Cell Death Disease. 2022;13(8):745. doi:10.1038/s41419-022-05196-8.
  • Rao AM, Hatcher JF, Dogan A, Dempsey RJ. Elevated N1-acetylspermidine levels in gerbil and rat brains after CNS injury. J Neurochem. 2000;74(3):1106–1111. doi:10.1046/j.1471-4159.2000.741106.x.
  • Liu F, Alfarhan M, Baker L, Shenoy N, Liao Y, Henry-Ojo HO, Somanath PR, Narayanan SP. Treatment with MDL 72527 ameliorated clinical symptoms, retinal ganglion cell loss, optic nerve inflammation, and improved visual acuity in an experimental Model of multiple sclerosis. Cells. 2022;11(24):11(24. doi:10.3390/cells11244100.
  • Desjarlais M, Ruknudin P, Wirth M, Lahaie I, Dabouz R, Rivera JC, Habelrih T, Omri S, Hardy P, Rivard A. et al. Tyrosine-Protein Phosphatase Non-receptor type 9 (PTPN9) negatively regulates the paracrine vasoprotective activity of bone-marrow derived Pro-angiogenic cells: impact on vascular degeneration in Oxygen-Induced Retinopathy. Front Cell Dev Biol. 2021;9:679906. doi:10.3389/fcell.2021.679906.
  • Pegg AE. Functions of Polyamines in mammals. J Biol Chem. 2016;291(29):14904–14912. doi:10.1074/jbc.R116.731661.
  • Adil MS, Narayanan SP, Somanath PR. Cell-cell junctions: structure and regulation in physiology and pathology. Tissue Barriers. 2021;9(1):1848212. doi:10.1080/21688370.2020.1848212.
  • Rudraraju M, Narayanan SP, Somanath PR. Regulation of blood-retinal barrier cell-junctions in diabetic retinopathy. Pharmacol Res. 2020;161:105115. doi:10.1016/j.phrs.2020.105115.
  • Zhao L, Ling L, Lu J, Jiang F, Sun J, Zhang Z, Huang Y, Liu X, Zhu Y, Fu X. et al. Reactive oxygen species-responsive mitochondria-targeted liposomal quercetin attenuates retinal ischemia–reperfusion injury via regulating SIRT1 / FOXO3A and p38 MAPK signaling pathways. Bioeng Transl Med. 2023;8(3):e10460. doi:10.1002/btm2.10460.
  • Zou W, Zhang Z, Luo S, Cheng L, Huang X, Ding N, Yu J, Pan Y, Wu Z. p38 promoted retinal micro-angiogenesis through up-regulated RUNX1 expression in diabetic retinopathy. Biosci Rep. 2020;40(5):40(5. doi:10.1042/BSR20193256.
  • Redgate ES, Grudziak AG, Deutsch M, Boggs SS. Enhanced uptake of [3H] spermidine by 9L rat brain tumors after direct intratumoral infusion of inhibitors of enzymes of the polyamine biosynthetic pathway. J Neurooncol. 1999;42(2):123–130. doi:10.1023/A:1006108321223.
  • Dogan A, Rao AM, Baskaya MK, Hatcher J, Temiz C, Rao VLR, Dempsey RJ. Contribution of polyamine oxidase to brain injury after trauma. J Neurosurg. 1999;90(6):1078–1082. doi:10.3171/jns.1999.90.6.1078.
  • Dogan A, Rao AM, Hatcher J, Rao VLR, Baskaya MK, Dempsey RJ. Effects of MDL 72527, a specific inhibitor of polyamine oxidase, on brain edema, ischemic injury volume, and tissue polyamine levels in rats after temporary middle cerebral artery occlusion. J Neurochem. 1999;72(2):765–770. doi:10.1046/j.1471-4159.1999.0720765.x.
  • Hayashi Y, Baudry M. Effect of kainate-induced seizure activity on the polyamine interconversion pathway in juvenile rat brain. Brain Res Dev Brain Res. 1995;87(1):96–99. doi:10.1016/0165-3806(95)00053-G.
  • Liu W, Liu R, Schreiber SS, Baudry M. Role of polyamine metabolism in kainic acid excitotoxicity in organotypic hippocampal slice cultures. J Neurochem. 2001;79(5):976–984. doi:10.1046/j.1471-4159.2001.00650.x.
  • Baudry M, Najm I. Kainate-induced seizure activity stimulates the polyamine interconversion pathway in rat brain. Neurosci Lett. 1994;171(1–2):151–154. doi:10.1016/0304-3940(94)90627-0.
  • Bai Y, Bai X, Wang Z, Zhang X, Ruan C, Miao J. MicroRNA-126 inhibits ischemia-induced retinal neovascularization via regulating angiogenic growth factors. Exp Mol Pathol. 2011;91(1):471–477. doi:10.1016/j.yexmp.2011.04.016.
  • Roth S, Shaikh AR, Hennelly MM, Li Q, Bindokas V, Graham CE. Mitogen-activated protein kinases and retinal ischemia. Invest Ophthalmol Vis Sci. 2003;44(12):5383–5395. doi:10.1167/iovs.03-0451.
  • Chen M, Obasanmi G, Armstrong D, Lavery N-J, Kissenpfennig A, Lois N, Xu H. STAT3 activation in circulating myeloid-derived cells contributes to retinal microvascular dysfunction in diabetes. J Neuroinflammation. 2019;16(1):138. doi:10.1186/s12974-019-1533-1.
  • Hong Y, Wang Y, Cui Y, Pan J, Mao S, Zhu Y, Wen T, Qi T, Wang A, Luo Y. et al. MicroRNA-124-3p attenuated retinal neovascularization in oxygen-induced retinopathy mice by inhibiting the dysfunction of retinal neuroglial cells through STAT3 pathway. Int J Mol Sci. 2023;24(14):24(14. doi:10.3390/ijms241411767.
  • Kong L, Li J, Yang Y, Tang H, Zou H. Paeoniflorin alleviates the progression of retinal vein occlusion via inhibiting hypoxia inducible factor-1α/vascular endothelial growth factor/STAT3 pathway. Bioengineered. 2022;13(5):13622–13631. doi:10.1080/21655979.2022.2081755.
  • Seiler N. Oxidation of polyamines and brain injury. Neurochem Res. 2000;25(4):471–490. doi:10.1023/A:1007508008731.
  • Uemura T, Watanabe K, Ishibashi M, Saiki R, Kuni K, Nishimura K, Toida T, Kashiwagi K, Igarashi K. Aggravation of brain infarction through an increase in acrolein production and a decrease in glutathione with aging. Biochem Biophys Res Commun. 2016;473(2):630–635. doi:10.1016/j.bbrc.2016.03.137.
  • Grigsby J, Betts B, Vidro-Kotchan E, Culbert R, Tsin A. A possible role of acrolein in Diabetic Retinopathy: involvement of a VEGF/TGFβ signaling pathway of the retinal pigment epithelium in hyperglycemia. Curr Eye Res. 2012;37(11):1045–1053. doi:10.3109/02713683.2012.713152.
  • Aldini G, Orioli M, Carini M. Protein modification by acrolein: relevance to pathological conditions and inhibition by aldehyde sequestering agents. Mol Nutr Food Res. 2011;55(9):1301–1319. doi:10.1002/mnfr.201100182.
  • Stevens JF, Maier CS. Acrolein: sources, metabolism, and biomolecular interactions relevant to human health and disease. Mol Nutr Food Res. 2008;52(1):7–25. doi:10.1002/mnfr.200700412.
  • Murata M, Noda K, Kawasaki A, Yoshida S, Dong Y, Saito M, Dong Z, Ando R, Mori S, Saito W. et al. Soluble vascular adhesion protein-1 mediates spermine oxidation as semicarbazide-sensitive amine oxidase: possible role in proliferative diabetic retinopathy. Curr Eye Res. 2017;42(12):1674–1683. doi:10.1080/02713683.2017.1359847.
  • Adams JD Jr., Klaidman LK. Acrolein-induced oxygen radical formation. Free Radic Biol Med. 1993;15(2):187–193. doi:10.1016/0891-5849(93)90058-3.
  • Murata M, Noda K, Yoshida S, Saito M, Fujiya A, Kanda A, Ishida S. Unsaturated aldehyde acrolein promotes retinal glial cell migration. Invest Ophthalmol Vis Sci. 2019;60(13):4425–4435. doi:10.1167/iovs.19-27346.
  • Dong Y, Noda K, Murata M, Yoshida S, Saito W, Kanda A, Ishida S. Localization of acrolein-lysine adduct in fibrovascular tissues of proliferative diabetic retinopathy. Curr Eye Res. 2017;42(1):111–117. doi:10.3109/02713683.2016.1150491.
  • Singh R, Letai A, Sarosiek K. Regulation of apoptosis in health and disease: the balancing act of BCL-2 family proteins. Nat Rev Mol Cell Biol. 2019;20(3):175–193. doi:10.1038/s41580-018-0089-8.
  • Fan J, Xu G, Jiang T, Qin Y. Pharmacologic induction of heme oxygenase-1 plays a protective role in diabetic retinopathy in rats. invest Ophthalmol Vis Sci. 2012;53(10):6541–6556. doi:10.1167/iovs.11-9241.
  • Arai-Gaun S, Katai N, Kikuchi T, Kurokawa T, Ohta K, Yoshimura N. Heme oxygenase-1 induced in muller cells plays a protective role in retinal ischemia–reperfusion injury in rats. Invest Ophthalmol Vis Sci. 2004;45(11):4226–4232. doi:10.1167/iovs.04-0450.

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