Proteasome-mediated reduction in proapoptotic molecule bim renders CD4+CD28null T cells resistant to apoptosis in acute coronary syndrome

Circulation

Volumn 131, Issue 8, 2015, Pages 709-720

  Kovalcsik, Edit ^a   Antunes, Ricardo F ^a   Baruah, Paramita ^a   Kaski, Juan Carlos ^a   Dumitriu, Ingrid E ^a  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Allergy and immunology; Apoptosis; Atherosclerosis; T lymphocytes

Indexed keywords

BIM PROTEIN; CD28 ANTIGEN; CD4 ANTIGEN; FAS ANTIGEN; PROTEASOME; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; ANTIIDIOTYPIC ANTIBODY; APOPTOSIS REGULATORY PROTEIN; BCL-2-LIKE PROTEIN 11; FAS ASSOCIATED DEATH DOMAIN PROTEIN; MEMBRANE PROTEIN; ONCOPROTEIN;

ACUTE CORONARY SYNDROME; APOPTOSIS; ARTICLE; CONTROLLED STUDY; HOMEOSTASIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; CD4+ T LYMPHOCYTE; CELL CULTURE; CELL PROLIFERATION; COMPARATIVE STUDY; DEFICIENCY; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHENOTYPE; PHYSIOLOGY; RECURRENT DISEASE; RISK FACTOR; SIGNAL TRANSDUCTION;

ACUTE CORONARY SYNDROME; ANTIBODIES, ANTI-IDIOTYPIC; ANTIGENS, CD28; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; HOMEOSTASIS; HUMANS; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; PHENOTYPE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS; RECURRENCE; RISK FACTORS;

EID: 84923658523     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.114.013710     Document Type: Article

References (39)

1. Smith SC Jr, Collins A, Ferrari R, Holmes DR Jr, Logstrup S, McGhie DV, Ralston J, Sacco RL, Stam H, Taubert K, Wood DA, Zoghbi WA; World Heart Federation; American Heart Association; American College of Cardiology Foundation; European Heart Network; European Society of Cardiology. Our time: a call to save preventable death from cardiovascular disease (heart disease and stroke). J Am Coll Cardiol. 2012;60:2343-2348. doi: 10.1016/j.jacc.2012.08.962.
2. Libby P, Lichtman AH, Hansson GK. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity. 2013;38:1092-1104. doi: 10.1016/j.immuni.2013.06.009.
3. Dumitriu IE, Kaski JC. The role of T and B cells in atherosclerosis: potential clinical implications. Curr Pharm Des. 2011;17:4159-4171.
4. Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Immunol. 2011;12:204-212. doi: 10.1038/ni.2001.
5. Hansson GK, Holm J, Jonasson L. Detection of activated T lymphocytes in the human atherosclerotic plaque. Am J Pathol. 1989;135:169-175.
6. Dumitriu IE, Baruah P, Finlayson CJ, Loftus IM, Antunes RF, Lim P, Bunce N, Kaski JC. High levels of costimulatory receptors OX40 and 4-1BB characterize CD4+CD28null T cells in patients with acute coronary syndrome. Circ Res. 2012;110:857-869. doi: 10.1161/CIRCRESAHA.111.261933.
7. Liuzzo G, Goronzy JJ, Yang H, Kopecky SL, Holmes DR, Frye RL, Weyand CM. Monoclonal T-cell proliferation and plaque instability in acute coronary syndromes. Circulation. 2000;101:2883-2888.
8. Liuzzo G, Kopecky SL, Frye RL, O'Fallon WM, Maseri A, Goronzy JJ, Weyand CM. Perturbation of the T-cell repertoire in patients with unstable angina. Circulation. 1999;100:2135-2139.
9. Giubilato S, Liuzzo G, Brugaletta S, Pitocco D, Graziani F, Smaldone C, Montone RA, Pazzano V, Pedicino D, Biasucci LM, Ghirlanda G, Crea F. Expansion of CD4+CD28null T-lymphocytes in diabetic patients: exploring new pathogenetic mechanisms of increased cardiovascular risk in diabetes mellitus. Eur Heart J. 2011;32:1214-1226. doi: 10.1093/eurheartj/ehq499.
10. Nakajima T, Schulte S, Warrington KJ, Kopecky SL, Frye RL, Goronzy JJ, Weyand CM. T-cell-mediated lysis of endothelial cells in acute coronary syndromes. Circulation. 2002;105:570-575.
11. Lee HW, Nam KO, Seo SK, Kim YH, Kang H, Kwon BS. 4-1BB crosslinking enhances the survival and cell cycle progression of CD4 T lymphocytes. Cell Immunol. 2003;223:143-150.
12. Rogers PR, Song J, Gramaglia I, Killeen N, Croft M. OX40 promotes Bcl-xL and Bcl-2 expression and is essential for long-term survival of CD4 T cells. Immunity. 2001;15:445-455.
13. Liuzzo G, Biasucci LM, Trotta G, Brugaletta S, Pinnelli M, Digianuario G, Rizzello V, Rebuzzi AG, Rumi C, Maseri A, Crea F. Unusual CD4+CD28null T lymphocytes and recurrence of acute coronary events. J Am Coll Cardiol. 2007;50:1450-1458. doi: 10.1016/j.jacc.2007.06.040.
14. Krammer PH, Arnold R, Lavrik IN. Life and death in peripheral T cells. Nat Rev Immunol. 2007;7:532-542. doi: 10.1038/nri2115.
15. Krammer PH. CD95's deadly mission in the immune system. Nature. 2000;407:789-795. doi: 10.1038/35037728.
16. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-ordeath switch. Nat Rev Cancer. 2002;2:647-656. doi: 10.1038/nrc883.
17. Antonsson B, Conti F, Ciavatta A, Montessuit S, Lewis S, Martinou I, Bernasconi L, Bernard A, Mermod JJ, Mazzei G, Maundrell K, Gambale F, Sadoul R, Martinou JC. Inhibition of Bax channel-forming activity by Bcl-2. Science. 1997;277:370-372.
18. O'Connor L, Strasser A, O'Reilly LA, Hausmann G, Adams JM, Cory S, Huang DC. Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 1998;17:384-395. doi: 10.1093/emboj/17.2.384.
19. Willis SN, Adams JM. Life in the balance: how BH3-only proteins induce apoptosis. Curr Opin Cell Biol. 2005;17:617-625. doi: 10.1016/j. ceb.2005.10.001.
20. Dumitriu IE, Dunbar DR, Howie SE, Sethi T, Gregory CD. Human dendritic cells produce TGF-beta 1 under the influence of lung carcinoma cells and prime the differentiation of CD4+CD25+Foxp3+ regulatory T cells. J Immunol. 2009;182:2795-2807. doi: 10.4049/jimmunol.0712671.
21. Morgan MJ, Kim YS, Liu ZG. Membrane-bound Fas ligand requires RIP1 for efficient activation of caspase-8 within the death-inducing signaling complex. J Immunol. 2009;183:3278-3284. doi: 10.4049/jimmunol.0803428.
22. Yonehara S, Ishii A, Yonehara M. A cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J Exp Med. 1989;169:1747-1756.
23. Ghafourifar P, Klein SD, Schucht O, Schenk U, Pruschy M, Rocha S, Richter C. Ceramide induces cytochrome c release from isolated mitochondria. Importance of mitochondrial redox state. J Biol Chem. 1999;274:6080-6084.
24. Link A, Selejan S, Hewera L, Walter F, Nickenig G, Böhm M. Rosuvastatin induces apoptosis in CD4(+)CD28 (null) T cells in patients with acute coronary syndromes. Clin Res Cardiol. 2011;100:147-158. doi: 10.1007/s00392-010-0225-8.
25. Shitara Y, Sugiyama Y. Pharmacokinetic and pharmacodynamic alterations of 3-hydroxy-3-methylglutaryl coenzyme A (HMG-CoA) reductase inhibitors: drug-drug interactions and interindividual differences in transporter and metabolic enzyme functions. Pharmacol Ther. 2006;112:71-105. doi: 10.1016/j.pharmthera.2006.03.003.
26. Refaeli Y, Van Parijs L, London CA, Tschopp J, Abbas AK. Biochemical mechanisms of IL-2-regulated Fas-mediated T cell apoptosis. Immunity. 1998;8:615-623.
27. Ley R, Balmanno K, Hadfield K, Weston C, Cook SJ. Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasomedependent degradation of the BH3-only protein, Bim. J Biol Chem. 2003;278:18811-18816. doi: 10.1074/jbc.M301010200.
28. Ley R, Ewings KE, Hadfield K, Howes E, Balmanno K, Cook SJ. Extracellular signal-regulated kinases . are serum-stimulated "Bim(EL) kinases" that bind to the BH3-only protein Bim(EL) causing its phosphorylation and turnover. J Biol Chem. 2004;279:8837-8847. doi: 10.1074/jbc. M311578200.
29. Squires MS, Nixon PM, Cook SJ. Cell-cycle arrest by PD184352 requires inhibition of extracellular signal-regulated kinases (ERK) . but not ERK5/BMK1. Biochem J. 2002;366(pt 2):673-680. doi: 10.1042/BJ20020372.
30. Strasser A. The role of BH3-only proteins in the immune system. Nat Rev Immunol. 2005;5:189-200. doi: 10.1038/nri1568.
31. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science. 2001;292:727-730. doi: 10.1126/science.1059108.
32. Koenen P, Heinzel S, Carrington EM, Happo L, Alexander WS, Zhang JG, Herold MJ, Scott CL, Lew AM, Strasser A, Hodgkin PD. Mutually exclusive regulation of T cell survival by IL-7R and antigen receptor-induced signals. Nat Commun. 2013;4:1735. doi: 10.1038/ncomms2719.
33. Ren D, Tu HC, Kim H, Wang GX, Bean GR, Takeuchi O, Jeffers JR, Zambetti GP, Hsieh JJ, Cheng EH. BID, BIM, and PUMA are essential for activation of the BAX- and BAK-dependent cell death program. Science. 2010;330:1390-1393. doi: 10.1126/science.1190217.
34. Hughes PD, Belz GT, Fortner KA, Budd RC, Strasser A, Bouillet P. Apoptosis regulators Fas and Bim cooperate in shutdown of chronic immune responses and prevention of autoimmunity. Immunity. 2008;28:197-205. doi: 10.1016/j.immuni.2007.12.017.
35. Weant AE, Michalek RD, Khan IU, Holbrook BC, Willingham MC, Grayson JM. Apoptosis regulators Bim and Fas function concurrently to control autoimmunity and CD8+ T cell contraction. Immunity. 2008;28:218-230. doi: 10.1016/j.immuni.2007.12.014.
36. Hutcheson J, Scatizzi JC, Siddiqui AM, Haines GK 3rd, Wu T, Li QZ, Davis LS, Mohan C, Perlman H. Combined deficiency of proapoptotic regulators Bim and Fas results in the early onset of systemic autoimmunity. Immunity. 2008;28:206-217. doi: 10.1016/j.immuni.2007.12.015.
37. Schirmer M, Vallejo AN, Weyand CM, Goronzy JJ. Resistance to apoptosis and elevated expression of Bcl-2 in clonally expanded CD4+CD28- T cells from rheumatoid arthritis patients. J Immunol. 1998;161:1018-1025.
38. Vallejo AN, Schirmer M, Weyand CM, Goronzy JJ. Clonality and longevity of CD4+CD28null T cells are associated with defects in apoptotic pathways. J Immunol. 2000;165:6301-6307.
39. Sabbagh L, Pulle G, Liu Y, Tsitsikov EN, Watts TH. ERK-dependent Bim modulation downstream of the 4-1BB-TRAF1 signaling axis is a critical mediator of CD8 T cell survival in vivo. J Immunol. 2008;180:8093-8101.