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[1]Xu F, Sun Y, Chen Y, Sun Y, Li R. Endothelial cell apoptosis is responsible for the formation of coronary thrombotic atherosclerotic plaques. Tohoku J Exp Med 218(1), 25-33 (2009)
[2]Galle J, Hansen-Hagge T, Wanner C, Seibold S. Impact of oxidized low density lipoprotein on vascular cells. Atherosclerosis 185(2), 219-26 (2006)
[3]Kamota T, Li TS, Morikage N, Murakami M, Ohshima M. Ischemic pre-conditioning enhances the mobilization and recruitment of bone marrow stem cells to protect against ischemia/reperfusion injury in the late phase. J Am Coll Cardiol 53(19), 1814-22 (2009)
[4]Wei DH, Jia XY, Liu YH, Guo FX. Cathepsin L stimulates autophagy and inhibits apoptosis of ox-LDL-induced endothelial cells: potential role in atherosclerosis. Int J Mol Med 31(2), 400-6 (2013)
[5]Salvayre R, Auge N, Benoist H, Negre-Salvayre A. Oxidized low-density lipoprotein-induced apoptosis. Biochim Biophys Acta 1585(2-3), 213-21 (2002)
[6]Colles SM, Maxson JM, Carlson SG, Chisolm GM. Oxidized LDL-induced injury and apoptosis in atherosclerosis. Potential roles for oxysterols. Trends Cardiovasc Med 11(3-4), 131-8 (2001)
[7]Cheng J, Cui R, Chen CH, Du J. Oxidized low-density lipoprotein stimulates p53-dependent activation of proapoptotic Bax leading to apoptosis of differentiated endothelial progenitor cells. Endocrinology 148(5), 2085-94 (2007)
[8]Lu J, Yang JH, Burns AR, Chen HH, Tang D. Mediation of electronegative low-density lipoprotein signaling by LOX-1: a possible mechanism of endothelial apoptosis. Circ Res 104(5), 619-27 (2009)
[9]Bai YP, Hu CP, Yuan Q, Peng J, Shi RZ. Role of VPO1, a newly identified heme-containing peroxidase, in ox-LDL induced endothelial cell apoptosis. Free Radic Biol Med 51(8), 1492-500 (2011)
[10]Liu S, Shen H, Xu M, Liu O. FRP inhibits ox-LDL-induced endothelial cell apoptosis through an Akt-NF-{kappa}B-Bcl-2 pathway and inhibits endothelial cell apoptosis in an apoE-knockout mouse model. Am J Physiol Endocrinol Metab 299(3), E351-63 (2010)
[11]Takahashi M, Okazaki H, Ogata Y, Takeuchi K. Lysophosphatidylcholine induces apoptosis in human endothelial cells through a p38-mitogen-activated protein kinase-dependent mechanism. Atherosclerosis 161(2), 387-94 (2002)
[12]N’Guessan PD, Schmeck B, Ayim A, Hocke AC. Streptococcus pneumoniae R6x induced p38 MAPK and JNK-mediated caspase-dependent apoptosis in human endothelial cells. Thromb Haemost 94(2), 295-303 (2005)
[13]Steinberg D. Low density lipoprotein oxidation and its pathobiological significance. J Biol Chem 272(34), 20963-6 (1997)
[14]Holvoet P, Vanhaecke J, Janssens S. Oxidized LDL and malondialdehyde-modified LDL in patients with acute coronary syndromes and stable coronary artery disease. Circulation 98(15), 1487-94 (1998)
[15]Massy ZA, Kim Y, Guijarro C, Kasiske BL. Low-density lipoprotein-induced expression of interleukin-6, a marker of human mesangial cell inflammation: effects of oxidation and modulation by lovastatin. Biochem Biophys Res Commun 267(2), 536-40 (2000)
[16]Tekin IO, Orem A, Shiri-Sverdlov R. Oxidized LDL in inflammation: from bench to bedside. Mediators Inflamm 2013, 762759 (2013)
[17]Hulthe J, Fagerberg B. Circulating oxidized LDL is associated with subclinical atherosclerosis development and inflammatory cytokines (AIR Study). Arterioscler Thromb Vasc Biol 22(7), 1162-7 (2002)
[18]Adcock IM. HDAC inhibitors as anti-inflammatory agents. Br J Pharmacol 150(7), 829-31 (2007)
[19]Glauben R, Sonnenberg E, Zeitz M, Siegmund B. HDAC inhibitors in models of inflammation-related tumorigenesis. Cancer Lett 280(2), 154-9 (2009)
[20]Shakespear MR1, Halili MA, Irvine KM. Histone deacetylases as regulators of inflammation and immunity. Trends Immunol 32(7), 335-43 (2011)
[21]Shakespear MR, Halili MA, Irvine KM. Histone deacetylases as regulators of inflammation and immunity. Trends Immunol 32(7), 335-43 (2011)
[22]de Zoeten EF, Wang L, Sai H, Dillmann WH. Inhibition of HDAC9 increases T regulatory cell function and prevents colitis in mice. Gastroenterology 138(2), 583-94 (2010)
[23]Cao Q, Rong S, Repa JJ, St Clair R. Histone deacetylase 9 represses cholesterol efflux and alternatively activated macrophages in atherosclerosis development. Arterioscler Thromb Vasc Biol 34(9), 1871-9 (2014)
[24]Sata M, Walsh K. Oxidized LDL activates fas-mediated endothelial cell apoptosis. J Clin Invest 102(9), 1682-9 (1998)
[25]Li D, Yang B, Mehta JL. Ox-LDL induces apoptosis in human coronary artery endothelial cells: role of PKC, PTK, bcl-2, and Fas. Am J Physiol 275(2 Pt 2), H568-76 (1998)
[26]Sata M, Walsh K. TNFalpha regulation of Fas ligand expression on the vascular endothelium modulates leukocyte extravasation. Nat Med 4(4), 415-20 (1998)
[27]Yla-Herttuala S, Palinski W, Rosenfeld ME, Parthasarathy S. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J Clin Invest 84(4), 1086-95 (1989)
[28]Lacronique V, Mignon A, Fabre M, Viollet B, Rouquet N. Bcl-2 protects from lethal hepatic apoptosis induced by an anti-Fas antibody in mice. Nat Med 2(1), 80-6 (1996)
[29]Itoh N, Tsujimoto Y, Nagata S. Effect of bcl-2 on Fas antigen-mediated cell death. J Immunol 151(2), 621-7 (1993)
[30]Rehemtulla A, Hamilton CA, Chinnaiyan AM. Ultraviolet radiation-induced apoptosis is mediated by activation of CD-95 (Fas/APO1). J Biol Chem 272(41), 25783-6 (1997)
[31]Okura T, Gong L, Kamitani T, Wada T, Okura I. Protection against Fas/APO-1-and tumor necrosis factor-mediated cell death by a novel protein, sentrin. J Immunol 157(10), 4277-81 (1996)
[32]De Maria R, Lenti L, Malisan F. Requirement for GD3 ganglioside in CD95-and ceramide-induced apoptosis. Science 277 (5332), 1652-5 (1997)
[33]Mannick JB, Miao XQ, Stamler JS. Nitric oxide inhibits Fas-induced apoptosis. J Biol Chem 272(39), 24125-8 (1997)
[34]Uzui H, Harpf A, Liu M, Doherty TM. Increased expression of membrane type 3-matrix metalloproteinase in human atherosclerotic plaque: role of activated macrophages and inflammatory cytokines. Circulation 106(24), 3024-30 (2002)
[35]Doria A, Sherer Y, Meroni PL, Shoenfeld Y. Inflammation and accelerated atherosclerosis: basic mechanisms. Rheum Dis Clin North Am 31(2), 355-62 (2005)
[36]Mackness B, Hine D, Liu Y, Mastorikou M, Mackness M. Paraoxonase-1 inhibits oxidised LDL-induced MCP-1 production by endothelial cells. Biochem Biophys Res Commun 318(3), 680-3 (2004)
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Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
HDAC9 regulates ox-LDL-induced endothelial cell apoptosis by participating in inflammatory reactions
1 Department of Neurology, Huashan Hospital, State Key Laboratory of Medical Neurobiology of Fudan University, Shanghai, 200040, China
2 Department of Rehabilitatipn, Suzhou Municipal Hospital, No.26 Daoqian Road, Suzhou, Jiangsu, 215000, China
Abstract
Atherosclerosis is the most common cause of cardiovascular diseases worldwide. The endothelial cell apoptosis elicited by oxidized low-density lipoprotein (ox-LDL), which contributes to endothelial damage and inflammation, is a particularly important event in the early stage of atherosclerosis. However, the mechanism underlying ox-LDL-induced endothelial cell apoptosis remains unclear. Here we found that HDAC9 expression was increased at both the mRNA and protein levels accompanied by dose-dependent ox-LDL-induced endothelial cell apoptosis. Depletion of HDAC9 by its specific shRNA significantly antagonized ox-LDL-induced cell apoptosis and suppressed the expression of ox-LDL-induced inflammatory factors, such as TNF-α and MCP1. These data suggest that HDAC9 is an important epigenetic factor regulating ox-LDL-induced endothelial cell apoptosis and inflammatory factor expression. These results suggest that HDAC9 may participate in ox-LDL-induced endothelial damage and inflammation during atherosclerosis development.
Keywords
- Ox-LDL
- TNF-α
- HUVECs
References
- [1] Xu F, Sun Y, Chen Y, Sun Y, Li R. Endothelial cell apoptosis is responsible for the formation of coronary thrombotic atherosclerotic plaques. Tohoku J Exp Med 218(1), 25-33 (2009)
- [2] Galle J, Hansen-Hagge T, Wanner C, Seibold S. Impact of oxidized low density lipoprotein on vascular cells. Atherosclerosis 185(2), 219-26 (2006)
- [3] Kamota T, Li TS, Morikage N, Murakami M, Ohshima M. Ischemic pre-conditioning enhances the mobilization and recruitment of bone marrow stem cells to protect against ischemia/reperfusion injury in the late phase. J Am Coll Cardiol 53(19), 1814-22 (2009)
- [4] Wei DH, Jia XY, Liu YH, Guo FX. Cathepsin L stimulates autophagy and inhibits apoptosis of ox-LDL-induced endothelial cells: potential role in atherosclerosis. Int J Mol Med 31(2), 400-6 (2013)
- [5] Salvayre R, Auge N, Benoist H, Negre-Salvayre A. Oxidized low-density lipoprotein-induced apoptosis. Biochim Biophys Acta 1585(2-3), 213-21 (2002)
- [6] Colles SM, Maxson JM, Carlson SG, Chisolm GM. Oxidized LDL-induced injury and apoptosis in atherosclerosis. Potential roles for oxysterols. Trends Cardiovasc Med 11(3-4), 131-8 (2001)
- [7] Cheng J, Cui R, Chen CH, Du J. Oxidized low-density lipoprotein stimulates p53-dependent activation of proapoptotic Bax leading to apoptosis of differentiated endothelial progenitor cells. Endocrinology 148(5), 2085-94 (2007)
- [8] Lu J, Yang JH, Burns AR, Chen HH, Tang D. Mediation of electronegative low-density lipoprotein signaling by LOX-1: a possible mechanism of endothelial apoptosis. Circ Res 104(5), 619-27 (2009)
- [9] Bai YP, Hu CP, Yuan Q, Peng J, Shi RZ. Role of VPO1, a newly identified heme-containing peroxidase, in ox-LDL induced endothelial cell apoptosis. Free Radic Biol Med 51(8), 1492-500 (2011)
- [10] Liu S, Shen H, Xu M, Liu O. FRP inhibits ox-LDL-induced endothelial cell apoptosis through an Akt-NF-{kappa}B-Bcl-2 pathway and inhibits endothelial cell apoptosis in an apoE-knockout mouse model. Am J Physiol Endocrinol Metab 299(3), E351-63 (2010)Cited within: 0Google Scholar
- [11] Takahashi M, Okazaki H, Ogata Y, Takeuchi K. Lysophosphatidylcholine induces apoptosis in human endothelial cells through a p38-mitogen-activated protein kinase-dependent mechanism. Atherosclerosis 161(2), 387-94 (2002)
- [12] N’Guessan PD, Schmeck B, Ayim A, Hocke AC. Streptococcus pneumoniae R6x induced p38 MAPK and JNK-mediated caspase-dependent apoptosis in human endothelial cells. Thromb Haemost 94(2), 295-303 (2005)
- [13] Steinberg D. Low density lipoprotein oxidation and its pathobiological significance. J Biol Chem 272(34), 20963-6 (1997)
- [14] Holvoet P, Vanhaecke J, Janssens S. Oxidized LDL and malondialdehyde-modified LDL in patients with acute coronary syndromes and stable coronary artery disease. Circulation 98(15), 1487-94 (1998)
- [15] Massy ZA, Kim Y, Guijarro C, Kasiske BL. Low-density lipoprotein-induced expression of interleukin-6, a marker of human mesangial cell inflammation: effects of oxidation and modulation by lovastatin. Biochem Biophys Res Commun 267(2), 536-40 (2000)
- [16] Tekin IO, Orem A, Shiri-Sverdlov R. Oxidized LDL in inflammation: from bench to bedside. Mediators Inflamm 2013, 762759 (2013)
- [17] Hulthe J, Fagerberg B. Circulating oxidized LDL is associated with subclinical atherosclerosis development and inflammatory cytokines (AIR Study). Arterioscler Thromb Vasc Biol 22(7), 1162-7 (2002)
- [18] Adcock IM. HDAC inhibitors as anti-inflammatory agents. Br J Pharmacol 150(7), 829-31 (2007)
- [19] Glauben R, Sonnenberg E, Zeitz M, Siegmund B. HDAC inhibitors in models of inflammation-related tumorigenesis. Cancer Lett 280(2), 154-9 (2009)
- [20] Shakespear MR1, Halili MA, Irvine KM. Histone deacetylases as regulators of inflammation and immunity. Trends Immunol 32(7), 335-43 (2011)
- [21] Shakespear MR, Halili MA, Irvine KM. Histone deacetylases as regulators of inflammation and immunity. Trends Immunol 32(7), 335-43 (2011)
- [22] de Zoeten EF, Wang L, Sai H, Dillmann WH. Inhibition of HDAC9 increases T regulatory cell function and prevents colitis in mice. Gastroenterology 138(2), 583-94 (2010)
- [23] Cao Q, Rong S, Repa JJ, St Clair R. Histone deacetylase 9 represses cholesterol efflux and alternatively activated macrophages in atherosclerosis development. Arterioscler Thromb Vasc Biol 34(9), 1871-9 (2014)
- [24] Sata M, Walsh K. Oxidized LDL activates fas-mediated endothelial cell apoptosis. J Clin Invest 102(9), 1682-9 (1998)
- [25] Li D, Yang B, Mehta JL. Ox-LDL induces apoptosis in human coronary artery endothelial cells: role of PKC, PTK, bcl-2, and Fas. Am J Physiol 275(2 Pt 2), H568-76 (1998)
- [26] Sata M, Walsh K. TNFalpha regulation of Fas ligand expression on the vascular endothelium modulates leukocyte extravasation. Nat Med 4(4), 415-20 (1998)
- [27] Yla-Herttuala S, Palinski W, Rosenfeld ME, Parthasarathy S. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J Clin Invest 84(4), 1086-95 (1989)
- [28] Lacronique V, Mignon A, Fabre M, Viollet B, Rouquet N. Bcl-2 protects from lethal hepatic apoptosis induced by an anti-Fas antibody in mice. Nat Med 2(1), 80-6 (1996)
- [29] Itoh N, Tsujimoto Y, Nagata S. Effect of bcl-2 on Fas antigen-mediated cell death. J Immunol 151(2), 621-7 (1993)
- [30] Rehemtulla A, Hamilton CA, Chinnaiyan AM. Ultraviolet radiation-induced apoptosis is mediated by activation of CD-95 (Fas/APO1). J Biol Chem 272(41), 25783-6 (1997)
- [31] Okura T, Gong L, Kamitani T, Wada T, Okura I. Protection against Fas/APO-1-and tumor necrosis factor-mediated cell death by a novel protein, sentrin. J Immunol 157(10), 4277-81 (1996)
- [32] De Maria R, Lenti L, Malisan F. Requirement for GD3 ganglioside in CD95-and ceramide-induced apoptosis. Science 277 (5332), 1652-5 (1997)
- [33] Mannick JB, Miao XQ, Stamler JS. Nitric oxide inhibits Fas-induced apoptosis. J Biol Chem 272(39), 24125-8 (1997)
- [34] Uzui H, Harpf A, Liu M, Doherty TM. Increased expression of membrane type 3-matrix metalloproteinase in human atherosclerotic plaque: role of activated macrophages and inflammatory cytokines. Circulation 106(24), 3024-30 (2002)
- [35] Doria A, Sherer Y, Meroni PL, Shoenfeld Y. Inflammation and accelerated atherosclerosis: basic mechanisms. Rheum Dis Clin North Am 31(2), 355-62 (2005)
- [36] Mackness B, Hine D, Liu Y, Mastorikou M, Mackness M. Paraoxonase-1 inhibits oxidised LDL-induced MCP-1 production by endothelial cells. Biochem Biophys Res Commun 318(3), 680-3 (2004)