HDAC inhibitor, MS-275, increases vascular permeability by suppressing Robo4 expression in endothelial cells

References

• Huminiecki L, Gorn M, Suchting S, Poulsom R, Bicknell R. Magic roundabout is a new member of the roundabout receptor family that is endothelial specific and expressed at sites of active angiogenesis. Genomics. 2002;79(4):1–11. doi:https://doi.org/10.1006/geno.2002.6745.
   PubMed Web of Science ®Google Scholar
• Park KW, Morrison CM, Sorensen LK, Jones CA, Rao Y, Chien CB, Wu JY, Urness LD, Li DY. Robo4 is a vascular-specific receptor that inhibits endothelial migration. Dev Biol. 2003;261(1):251–267. doi:https://doi.org/10.1016/S0012-1606(03)00258-6.
   PubMed Web of Science ®Google Scholar
• Shirakura K, Ishiba R, Kashio T, Funatsu R, Tanaka T, Fukada SI, Ishimoto K, Hino N, Kondoh M, Ago Y, et al. The Robo4-TRAF7 complex suppresses endothelial hyperpermeability in inflammation. J Cell Sci. 2019;132(1):jcs220228. doi:https://doi.org/10.1242/jcs.220228.
   PubMed Web of Science ®Google Scholar
• Koch AW, Mathivet T, Larrivee B, Tong RK, Kowalski J, Pibouin-Fragner L, Bouvrée K, Stawicki S, Nicholes K, Rathore N, et al. Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Dev Cell. 2011;20(1):33–46. doi:https://doi.org/10.1016/j.devcel.2010.12.001.
   PubMed Web of Science ®Google Scholar
• Jones CA, London NR, Chen H, Park KW, Sauvaget D, Stockton RA, Wythe JD, Suh W, Larrieu-Lahargue F, Mukouyama Y-S, et al. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat Med. 2008;14(4):448–453. doi:https://doi.org/10.1038/nm1742.
   PubMed Web of Science ®Google Scholar
• London NR, Zhu W, Bozza FA, Smith MC, Greif DM, Sorensen LK, Chen L, Kaminoh Y, Chan AC, Passi SF, et al. Targeting Robo4-dependent slit signaling to survive the cytokine storm in sepsis and influenza. Sci Transl Med. 2010;2(23):23ra19. doi:https://doi.org/10.1126/scitranslmed.3000678.
   PubMed Web of Science ®Google Scholar
• Okada Y, Yano K, Jin E, Funahashi N, Kitayama M, Doi T, Spokes K, Beeler DL, Shih S-C, Okada H, et al. A three-kilobase fragment of the human Robo4 promoter directs cell type-specific expression in endothelium. Circ Res. 2007;100(12):1712–1722. doi:https://doi.org/10.1161/01.RES.0000269779.10644.dc.
   PubMed Web of Science ®Google Scholar
• Okada Y, Jin E, Nikolova-Krstevski V, Yano K, Liu J, Beeler D, Spokes K, Kitayama M, Funahashi N, Doi T, et al. A GABP-binding element in the Robo4 promoter is necessary for endothelial expression in vivo. Blood. 2008;112(6):2336–2339. doi:https://doi.org/10.1182/blood-2008-01-135079.
   PubMed Web of Science ®Google Scholar
• Okada Y, Funahashi N, Tanaka T, Nishiyama Y, Yuan L, Shirakura K, Turjman AS, Kano Y, Naruse H, Suzuki A, et al. Endothelial cell-specific expression of roundabout 4 is regulated by differential DNA methylation of the proximal promoter. Arterioscler Thromb Vasc Biol. 2014;34(7):1531–1538. doi:https://doi.org/10.1161/ATVBAHA.114.303818.
   PubMed Web of Science ®Google Scholar
• Tanaka T, Izawa K, Maniwa Y, Okamura M, Okada A, Yamaguchi T, Shirakura K, Maekawa N, Matsui H, Ishimoto K, et al. ETV2-TET1/TET2 complexes induce endothelial Cell-Specific Robo4 expression via promoter demethylation. Sci Rep. 2018;8(1):5653. doi:https://doi.org/10.1038/s41598-018-23937-8.
   PubMedGoogle Scholar
• Izawa K, Shirakura K, Kakiuchi K, Funahashi N, Maekawa N, Hino N, Tanaka T, Doi T, Okada Y. PRC2 components maintain DNA hypermethylation of the upstream promoter and regulate Robo4 expression in endothelial cells. Biol Pharm Bull. 2020;43(4):742–746. doi:https://doi.org/10.1248/bpb.b19-01014.
   PubMed Web of Science ®Google Scholar
• Seto E, Yoshida M. Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb Perspect Biol. 2014;6(4):a018713. doi:https://doi.org/10.1101/cshperspect.a018713.
   PubMed Web of Science ®Google Scholar
• Adcock IM. HDAC inhibitors as anti-inflammatory agents. Br J Pharmacol. 2007;150(7):829–831. doi:https://doi.org/10.1038/sj.bjp.0707166.
   PubMed Web of Science ®Google Scholar
• Kovacs L, Kovacs-Kasa A, Verin AD, Fulton D, Lucas R, Su Y. Histone deacetylases in vascular permeability and remodeling associated with acute lung injury. Vessel Plus. 2018;2:2. doi:https://doi.org/10.20517/2574-1209.2018.06.
   Google Scholar
• Wang Y, Stowe RL, Pinello CE, Tian G, Madoux F, Li D, Zhao L, Li J-L, Wang Y, Wang Y, et al. Identification of histone deacetylase inhibitors with benzoylhydrazide scaffold that selectively inhibit class I histone deacetylases. Chem Biol. 2015;22(2):273–284. doi:https://doi.org/10.1016/j.chembiol.2014.12.015.
   PubMedGoogle Scholar
• Yang XJ, Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol. 2008;9(3):206–218. doi:https://doi.org/10.1038/nrm2346.
   PubMed Web of Science ®Google Scholar
• Yang WM, Tsai SC, Wen YD, Fejer G, Seto E. Functional domains of histone deacetylase-3. J Biol Chem. 2002;277(11):9447–9454. doi:https://doi.org/10.1074/jbc.M105993200.
   PubMed Web of Science ®Google Scholar
• Patton J, Block S, Coombs C, Martin ME. Identification of functional elements in the murine Gabp alpha/ATP synthase coupling factor 6 bi-directional promoter. Gene. 2006;369:35–44. doi:https://doi.org/10.1016/j.gene.2005.10.009.
   PubMed Web of Science ®Google Scholar
• Huang W, Tan D, Wang X, Han S, Tan J, Zhao Y, Lu J, Huang B. Histone deacetylase 3 represses p15(INK4b) and p21(WAF1/cip1) transcription by interacting with Sp1. Biochem Biophys Res Commun. 2006;339(1):165–171. doi:https://doi.org/10.1016/j.bbrc.2005.11.010.
   PubMed Web of Science ®Google Scholar
• Kim Y, Kim K, Park D, Lee E, Lee H, Lee YS, Choe J, Jeoung D. Histone deacetylase 3 mediates allergic skin inflammation by regulating expression of MCP1 protein. J Biol Chem. 2012;287(31):25844–25859. doi:https://doi.org/10.1074/jbc.M112.348284.
   PubMed Web of Science ®Google Scholar
• Leus NG, Van Den Bosch T, Van Der Wouden PE, Krist K, Ourailidou ME, Eleftheriadis N, Kistemaker LEM, Bos S, Gjaltema RAF, Mekonnen SA, et al. HDAC1-3 inhibitor MS-275 enhances IL10 expression in RAW264.7 macrophages and reduces cigarette smoke-induced airway inflammation in mice. Sci Rep. 2017;7(1):45047. doi:https://doi.org/10.1038/srep45047.
   PubMed Web of Science ®Google Scholar
• Dai Y, Rahmani M, Dent P, Grant S. Blockade of histone deacetylase inhibitor-induced RelA/p65 acetylation and NF-kappaB activation potentiates apoptosis in leukemia cells through a process mediated by oxidative damage, XIAP downregulation, and c-Jun N-terminal kinase 1 activation. Mol Cell Biol. 2005;25(13):5429–5444. doi:https://doi.org/10.1128/MCB.25.13.5429-5444.2005.
   PubMed Web of Science ®Google Scholar
• Rao-Bindal K, Koshkina NV, Stewart J, Kleinerman ES. The histone deacetylase inhibitor, MS-275 (entinostat), downregulates c-FLIP, sensitizes osteosarcoma cells to FasL, and induces the regression of osteosarcoma lung metastases. Curr Cancer Drug Targets. 2013;13(4):411–422. doi:https://doi.org/10.2174/1568009611313040005.
   PubMed Web of Science ®Google Scholar
• Srivastava RK, Kurzrock R, Shankar S. MS-275 sensitizes TRAIL-Resistant breast cancer cells, inhibits angiogenesis and metastasis, and reverses Epithelial-Mesenchymal transition in vivo. Mol Cancer Ther. 2010;9(12):3254–3266. doi:https://doi.org/10.1158/1535-7163.MCT-10-0582.
   PubMed Web of Science ®Google Scholar
• Gould RA, Aziz H, Woods CE, Seman-Senderos MA, Sparks E, Preuss C, Wünnemann F, Bedja D, Moats CR, McClymont SA, et al. ROBO4 variants predispose individuals to bicuspid aortic valve and thoracic aortic aneurysm. Nat Genet. 2019;51(1):42–50. doi:https://doi.org/10.1038/s41588-018-0265-y.
   PubMed Web of Science ®Google Scholar
• Gurzu S, Turdean S, Kovecsi A, Contac AO, Jung I. Epithelial-mesenchymal, mesenchymal-epithelial, and endothelial-mesenchymal transitions in malignant tumors: an update. World J Clin Cases. 2015;3(5):393–404. doi:https://doi.org/10.12998/wjcc.v3.i5.393.
   PubMed Web of Science ®Google Scholar