Phosphorylation of CHOP (C/EBP Homologous Protein) by the AMP-Activated Protein Kinase Alpha 1 in Macrophages Promotes CHOP Degradation and Reduces Injury-Induced Neointimal Disruption in Vivo

Circulation Research

Volumn 119, Issue 10, 2016, Pages 1089-1100

  Dai, Xiaoyan ^a   Ding, Ye ^a   Liu, Zhaoyu ^a   Zhang, Wencheng ^b,c   Zou, Ming Hui ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b Qilu Hospital of Shandong University   (China)

^c SHANDONG UNIVERSITY   (China)

Author keywords

AMPK; apoptosis; CHOP; degradation; macrophage; neointima; ubiquitination

Indexed keywords

C EBP HOMOLOGOUS PROTEIN; CASEIN KINASE II; CASPASE 3; CCAAT ENHANCER BINDING PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; AMPK ALPHA1 SUBUNIT, MOUSE; AMPK ALPHA2 SUBUNIT, MOUSE; APOLIPOPROTEIN E; DDIT3 PROTEIN, MOUSE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; PHOSPHOSERINE; PROTEASOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATHEROSCLEROTIC PLAQUE; BONE MARROW DERIVED MACROPHAGE; CAROTID ATHEROSCLEROSIS; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; GENE DELETION; IN VIVO STUDY; MALE; MOUSE; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; UBIQUITINATION; UPREGULATION; ANIMAL; CAROTID ARTERY OBSTRUCTION; CELL CULTURE; COMMON CAROTID ARTERY; DEFICIENCY; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOLIPOPROTEINS E; APOPTOSIS; CAROTID ARTERY, COMMON; CAROTID STENOSIS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; MACROPHAGES; MALE; MICE; MICE, KNOCKOUT; NEOINTIMA; PHOSPHORYLATION; PHOSPHOSERINE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; RNA, SMALL INTERFERING; TRANSCRIPTION FACTOR CHOP;

EID: 84991492445     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.309463     Document Type: Article

References (41)

1. Burke AP, Farb A, Malcom GT, Liang YH, Smialek J, Virmani R. Coronary risk factors and plaque morphology in men with coronary disease who died suddenly. N Engl J Med. 1997;336:1276-1282. doi: 10.1056/NEJM199705013361802.
2. Libby P. Infammation in atherosclerosis. Nature. 2002;420:868-874. doi: 10.1038/nature01323.
3. Libby P, Geng YJ, Aikawa M, Schoenbeck U, Mach F, Clinton SK, Sukhova GK, Lee RT. Macrophages and atherosclerotic plaque stability. Curr Opin Lipidol. 1996;7:330-335.
4. Kolodgie FD, Virmani R, Burke AP, Farb A, Weber DK, Kutys R, Finn AV, Gold HK. Pathologic assessment of the vulnerable human coronary plaque. Heart. 2004;90:1385-1391. doi: 10.1136/hrt.2004.041798.
5. Clarke M, Bennett M. The emerging role of vascular smooth muscle cell apoptosis in atherosclerosis and plaque stability. Am J Nephrol. 2006;26:531-535. doi: 10.1159/000097815.
6. Tabas I. Apoptosis and plaque destabilization in atherosclerosis: the role of macrophage apoptosis induced by cholesterol. Cell Death Differ. 2004;11(suppl 1):S12-S16. doi: 10.1038/sj.cdd.4401444.
7. Seimon T, Tabas I. Mechanisms and consequences of macrophage apop-tosis in atherosclerosis. J Lipid Res. 2009;50(suppl):S382-S387. doi: 10.1194/jlr.R800032-JLR200.
8. Kolodgie FD, Narula J, Burke AP, Haider N, Farb A, Hui-Liang Y, Smialek J, Virmani R. Localization of apoptotic macrophages at the site of plaque rupture in sudden coronary death. Am J Pathol. 2000;157:1259-1268. doi: 10.1016/S0002-9440(10)64641-X.
9. Ball RY, Stowers EC, Burton JH, Cary NR, Skepper JN, Mitchinson MJ. Evidence that the death of macrophage foam cells contributes to the lipid core of atheroma. Atherosclerosis. 1995;114:45-54.
10. Zhang Z, Yang XY, Cohen DM. Urea-associated oxidative stress and Gadd153/CHOP induction. Am J Physiol. 1999;276:F786-F793.
11. -/- mice lacking CHOP. Cell Metab. 2009;9:474-481. doi: 10.1016/j. cmet.2009.03.003.
12. Feng B, Yao PM, Li Y, Devlin CM, Zhang D, Harding HP, Sweeney M, Rong JX, Kuriakose G, Fisher EA, Marks AR, Ron D, Tabas I. The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nat Cell Biol. 2003;5:781-792. doi: 10.1038/ncb1035.
13. Myoishi M, Hao H, Minamino T, Watanabe K, Nishihira K, Hatakeyama K, Asada Y, Okada K, Ishibashi-Ueda H, Gabbiani G, Bochaton-Piallat ML, Mochizuki N, Kitakaze M. Increased endoplas-mic reticulum stress in atherosclerotic plaques associated with acute coronary syndrome. Circulation. 2007;116:1226-1233. doi: 10.1161/ CIRCULATIONAHA.106.682054.
14. Dorweiler B, Grechowa I, Wallrath A, Vahl CF, Horke S. Activation of the proapoptotic unfolded protein response in plaques of the human carotid artery. Eur J Vasc Endovasc Surg. 2014;48:248-257. doi: 10.1016/j. ejvs.2014.06.038.
15. Tsukano H, Gotoh T, Endo M, Miyata K, Tazume H, Kadomatsu T, Yano M, Iwawaki T, Kohno K, Araki K, Mizuta H, Oike Y. The endoplasmic re-ticulum stress-C/EBP homologous protein pathway-mediated apoptosis in macrophages contributes to the instability of atherosclerotic plaques. Arterioscler Thromb Vasc Biol. 2010;30:1925-1932. doi: 10.1161/ ATVBAHA.110.206094.
16. Schulz E, Anter E, Zou MH, Keaney JF Jr. Estradiol-mediated en-dothelial nitric oxide synthase association with heat shock protein 90 requires adenosine monophosphate-dependent protein kinase. Circulation. 2005;111:3473-3480. doi: 10.1161/CIRCULATIONAHA. 105.546812.
17. Chen Z, Peng IC, Sun W, Su MI, Hsu PH, Fu Y, Zhu Y, DeFea K, Pan S, Tsai MD, Shyy JY. AMP-activated protein kinase functionally phosphory-lates endothelial nitric oxide synthase Ser633. Circ Res. 2009;104:496- 505. doi: 10.1161/CIRCRESAHA.108.187567.
18. Sag D, Carling D, Stout RD, Suttles J. Adenosine 5'-monophosphate-activated protein kinase promotes macrophage polarization to an anti-infammatory functional phenotype. J Immunol. 2008;181:8633-8641.
19. Davis BJ, Xie Z, Viollet B, Zou MH. Activation of the AMP-activated ki-nase by antidiabetes drug metformin stimulates nitric oxide synthesis in vivo by promoting the association of heat shock protein 90 and endothelial nitric oxide synthase. Diabetes. 2006;55:496-505.
20. Nagata D, Takeda R, Sata M, Satonaka H, Suzuki E, Nagano T, Hirata Y. AMP-activated protein kinase inhibits angiotensin II-stimulated vascular smooth muscle cell proliferation. Circulation. 2004;110:444-451. doi: 10.1161/01.CIR.0000136025.96811.76.
21. Zou MH, Hou XY, Shi CM, Nagata D, Walsh K, Cohen RA. Modulation by peroxynitrite of Akt- and AMP-activated kinase-dependent Ser1179 phosphorylation of endothelial nitric oxide synthase. J Biol Chem. 2002;277:32552-32557. doi: 10.1074/jbc.M204512200.
22. Dong Y, Zhang M, Liang B, Xie Z, Zhao Z, Asfa S, Choi HC, Zou MH. Reduction of AMP-activated protein kinase alpha2 increases endoplasmic reticulum stress and atherosclerosis in vivo. Circulation. 2010;121:792- 803. doi: 10.1161/CIRCULATIONAHA.109.900928.
23. Nakamura K, Sasaki T, Cheng XW, Iguchi A, Sato K, Kuzuya M. Statin prevents plaque disruption in apoE-knockout mouse model through pleio-tropic effect on acute infammation. Atherosclerosis. 2009;206:355-361. doi: 10.1016/j.atherosclerosis.2009.02.014.
24. Sasaki T, Kuzuya M, Nakamura K, Cheng XW, Shibata T, Sato K, Iguchi A. A simple method of plaque rupture induction in apolipoprotein E-defcient mice. Arterioscler Thromb Vasc Biol. 2006;26:1304-1309. doi: 10.1161/01.ATV.0000219687.71607.f7.
25. Wang L, Zheng J, Bai X, Liu B, Liu CJ, Xu Q, Zhu Y, Wang N, Kong W, Wang X. ADAMTS-7 mediates vascular smooth muscle cell migration and neointima formation in balloon-injured rat arteries. Circ Res. 2009;104:688-698. doi: 10.1161/CIRCRESAHA.108.188425.
26. Han J, Back SH, Hur J, Lin YH, Gildersleeve R, Shan J, Yuan CL, Krokowski D, Wang S, Hatzoglou M, Kilberg MS, Sartor MA, Kaufman RJ. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol. 2013;15:481-490. doi: 10.1038/ ncb2738.
27. Wang XZ, Ron D. Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP Kinase. Science. 1996;272:1347-1349.
28. Ubeda M, Habener JF. CHOP transcription factor phosphorylation by casein kinase 2 inhibits transcriptional activation. J Biol Chem. 2003;278:40514-40520. doi: 10.1074/jbc.M306404200.
29. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell. 2008;30:214-226. doi: 10.1016/j. molcel.2008.03.003.
30. Qi Y, Xia P. Cellular inhibitor of apoptosis protein-1 (cIAP1) plays a critical role in β-cell survival under endoplasmic reticulum stress: promoting ubiquitination and degradation of C/EBP homologous protein (CHOP). J Biol Chem. 2012;287:32236-32245. doi: 10.1074/jbc. M112.362160.
31. Silvestre-Roig C, de Winther MP, Weber C, Daemen MJ, Lutgens E, Soehnlein O. Atherosclerotic plaque destabilization: mechanisms, models, and therapeutic strategies. Circ Res. 2014;114:214-226. doi: 10.1161/ CIRCRESAHA.114.302355.
32. Jackson CL, Bennett MR, Biessen EA, Johnson JL, Krams R. Assessment of unstable atherosclerosis in mice. Arterioscler Thromb Vasc Biol. 2007;27:714-720. doi: 10.1161/01.ATV.0000261873.86623.e1.
33. Tabas I. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phago-cytic effciency. Arterioscler Thromb Vasc Biol. 2005;25:2255-2264. doi: 10.1161/01.ATV.0000184783.04864.9f.
34. Schrijvers DM, De Meyer GR, Herman AG, Martinet W. Phagocytosis in atherosclerosis: Molecular mechanisms and implications for plaque progression and stability. Cardiovasc Res. 2007;73:470-480. doi: 10.1016/j.cardiores.2006.09.005.
35. Alexander MR, Moehle CW, Johnson JL, Yang Z, Lee JK, Jackson CL, Owens GK. Genetic inactivation of IL-1 signaling enhances atherosclerotic plaque instability and reduces outward vessel remodeling in advanced atherosclerosis in mice. J Clin Invest. 2012;122:70-79. doi: 10.1172/JCI43713.
36. Johnson J, Carson K, Williams H, Karanam S, Newby A, Angelini G, George S, Jackson C. Plaque rupture after short periods of fat feeding in the apolipoprotein E-knockout mouse: model characterization and effects of pravastatin treatment. Circulation. 2005;111:1422-1430. doi: 10.1161/01.CIR.0000158435.98035.8D.
37. Zang M, Xu S, Maitland-Toolan KA, Zuccollo A, Hou X, Jiang B, Wierzbicki M, Verbeuren TJ, Cohen RA. Polyphenols stimulate AMP-activated protein kinase, lower lipids, and inhibit accelerated atherosclerosis in diabetic LDL receptor-defcient mice. Diabetes. 2006;55:2180-2191. doi: 10.2337/db05-1188.
38. Dong Y, Zhang M, Wang S, Liang B, Zhao Z, Liu C, Wu M, Choi HC, Lyons TJ, Zou MH. Activation of AMP-activated protein kinase inhibits oxidized LDL-triggered endoplasmic reticulum stress in vivo. Diabetes. 2010;59:1386-1396. doi: 10.2337/db09-1637.
39. Wang S, Zhang M, Liang B, Xu J, Xie Z, Liu C, Viollet B, Yan D, Zou MH. AMPKalpha2 deletion causes aberrant expression and activation of NAD(P)H oxidase and consequent endothelial dysfunction in vivo: role of 26S proteasomes. Circ Res. 2010;106:1117-1128. doi: 10.1161/ CIRCRESAHA.109.212530.
40. Cai Z, Ding Y, Zhang M, Lu Q, Wu S, Zhu H, Song P, Zou MH. Ablation of ad-enosine monophosphate-activated protein kinase alpha1 in vascular smooth muscle cells promotes diet-induced atherosclerotic calcifcation in vivo. Circ Res. 2016;119:422-433. doi: 10.1161/CIRCRESAHA.116.308301.
41. Abbasi F, Chu JW, McLaughlin T, Lamendola C, Leary ET, Reaven GM. Effect of metformin treatment on multiple cardiovascular disease risk factors in patients with type 2 diabetes mellitus. Metabolism. 2004;53:159-164.