Genomic profiling of acquired resistance to apoptosis in cells derived from human atherosclerotic lesions: Potential role of STATs, cyclinD1, BAD, and Bcl-XL

Journal of Molecular and Cellular Cardiology

Volumn 39, Issue 3, 2005, Pages 453-465

  Gagarin, Dmitry ^a,b   Yang, Zhaoqing ^a,b   Butler, Jason ^a,b   Wimmer, Monika ^a,b   Du, Baoheng ^c   Cahan, Patrick ^a,b   McCaffrey, Timothy A ^a,b  

^a GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

^b Catherine Birch McCormick Genomics Center   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Apoptosis; Atherosclerosis; BAD; Bcl xL; Caspase; Cyclin D1; Restenosis; STAT; Transcript profiling

Indexed keywords

CYCLIN D1; FAS ANTIGEN; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEIN BAD; PROTEIN BCL XL; STAT PROTEIN; VOLTAGE GATED CHANNEL FORMING PROTEIN;

ANGINA PECTORIS; APOPTOSIS; ARTERY LIGATION; ARTERY RUPTURE; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD VESSEL REACTIVITY; CELL ACTIVITY; CLONE; CONTROLLED STUDY; DNA MICROARRAY; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INFARCTION; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; RESTENOSIS; WESTERN BLOTTING;

ANTIGENS, CD95; APOPTOSIS; ARTERIOSCLEROSIS; BCL-ASSOCIATED DEATH PROTEIN; BCL-X PROTEIN; BLOTTING, WESTERN; CARRIER PROTEINS; CELL SURVIVAL; CYCLIN D1; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENOME, HUMAN; HUMANS; MODELS, ANATOMIC; MODELS, BIOLOGICAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PORINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, MESSENGER; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; STAT6 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS; VOLTAGE-DEPENDENT ANION CHANNEL 2; VOLTAGE-DEPENDENT ANION CHANNELS;

EID: 23644448750     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2005.01.015     Document Type: Article

References (72)

1. K. Walsh, R. Smith, and H. Kim Vascular cell apoptosis in remodeling, restenosis, and plaque rupture Circ. Res. 87 2000 184 188
2. M.L. Huynh, V.A. Fadok, and P.M. Henson Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation J. Clin. Invest. 109 2002 41 50
3. D.J. Falcone, and D.J. Salisbury Fibronectin stimulates macrophage uptake of low density lipoprotein-heparin-collagen complexes Arterioscler. Thromb. Vasc. Biol. 8 1988 263 273
4. S. Bjorkerud, and B. Bjorkerud Apoptosis is abundant in human atherosclerotic lesions, especially in inflammatory cells (macrophages and T cells), and may contribute to the accumulation of gruel and plaque instability Am. J. Pathol. 149 1996 367 380
5. M.L. Bochaton-Piallat, F. Gabbiani, M. Redard, A. Desmouliere, and G. Gabbiani Apoptosis participates in cellularity regulation during rat aortic intimal thickening Am. J. Pathol. 146 5 1995 1059 1064
6. V.Y. Mehta, M.B. Jorgensen, A.E. Raizner, G. Wolde-Tsadik, P.R. Mahrer, and P. Mansukhani Spontaneous regression of restenosis: an angiographic study J. Am. Coll. Cardiol. 26 1995 696 702
7. G. Bauriedel, S. Schluckebier, R. Hutter, U. Welsch, R. Kandolf, B. Luderitz, and M.F. Prescott Apoptosis in restenosis versus stable-angina atherosclerosis-implications for the pathogenesis of restenosis Arterioscler. Thromb. Vasc. Biol. 18 1998 1132 1139
8. C. Rembold Could atherosclerosis originate from defective smooth muscle cell death? Perspect. Biol. Med. 39 3 1996 405 408
9. J. Boyle, D. Bowyer, P. Weissberg, and M. Bennett Human blood-derived macrophages induce apoptosis in human plaque-derived vascular smooth muscle cells fas-ligand/fas interactions Arterioscler. Thromb. Vasc. Biol. 21 2001 1402 1407
10. M.R. Bennett, G.I. Evan, and S.M. Schwartz Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques J. Clin. Invest. 95 5 1995 2266 2274
11. S. Chan, L. Hegyi, S. Scott, N. Cary, P. Weissberg, and M. Bennett Sensitivity to fas-mediated apoptosis is determined below receptor level in human vascular smooth muscle cells Circ. Res. 86 2000 1038 1046
12. T.A. McCaffrey, S. Consigli, B. Du, D.J. Falcone, T.A. Sanborn, A.M. Spokojny, and H. Bush Decreased Type II/Type I TGF-β1 receptor ratio in cells derived from human atherosclerotic lesions: conversion from an antiproliferative to profibrotic response to TGF-β1 J. Clin. Invest. 96 1995 2667 2675
13. P. Bray, B. Du, V. Mejia, S. Hao, E. Deutsch, C. Fu, R. Wilson, H. Hanauske-Abel, and T. McCaffrey Glucocorticoid resistance due to reduced expression of the glucocorticoid receptor in cells from human vascular lesions Arterioscler. Thromb. Vasc. Biol. 19 1999 1180 1189
14. T. McCaffrey, B. Du, P. Bray, C. Fu, T. Sanborn, E. Deutsch, N. Tarazona, A. Shaknovitch, G. Newman, C. Patterson, and H. Bush The expression of TGF-β receptors in human atherosclerosis: evidence for acquired resistance due to receptor imbalance J. Mol. Cell. Cardiol. 31 1999 1627 1642
15. B. Du, C. Fu, C. Kent, H. Bush, A. Schulick, K. Kreiger, T. Collins, and T. McCaffrey Elevated Egr-1 in human atherosclerotic cells transcriptionally represses the Type II TGF-β receptor and confers resistance to TGF-β J. Biol. Chem. 275 50 2000 39039 39047
16. A.K. Robertson, M. Rudling, X. Zhou, L. Gorelik, R.A. Flavell, and G.K. Hansson Disruption of TGF-beta signaling in T cells accelerates atherosclerosis J. Clin. Invest. 112 2003 1342 1350
17. D.S. Heo, J.G. Park, K. Hata, R. Day, R.B. Herberman, and T.L. Whiteside Evaluation of tetrazolium-based semiautomatic colorimetric assay for measurement of human antitumor cytotoxicity Cancer Res. 50 1990 3681 3690
18. B. Breitkreutz, C. Stark, and M. Tyers Osprey: a network visualization system Gen. Biol. 4 2003 R22
19. C.M. Counter, M. Meyerson, E.N. Eaton, L.W. Ellisen, S.D. Caddle, D.A. Haber, and R.A. Weinberg Telomerase activity is restored in human cells by ectopic expression of hTERT (hEST2), the atalytic subunit of telomerase Oncogene 16 1998 1217 1222
20. M.R. Bennett, T.D. Littlewood, S.M. Schwartz, and P.L. Weissberg Increased sensitivity of human vascular smooth muscle cells from atherosclerotic plaques to p53-mediated apoptosis Circ. Res. 81 1997 591 599
21. Y.J. Geng, L.E. Henderson, E.B. Levesque, M. Muszynski, and P. Libby Fas is expressed in human atherosclerotic intima and promotes apoptosis of cytokine-primed human vascular smooth muscle cells Arterioscler. Thromb. Vasc. Biol. 17 1997 2200 2208
22. G. Dennis Jr., B.T. Sherman, D.A. Hosack, J. Yang, W. Gao, H.C. Lane, and R.A. Lempicki DAVID: database for annotation, visualization, and integrated discovery Gen. Biol. 4 2003 3
23. D.A. Hosack, G. Dennis Jr., B.T. Sherman, H.C. Lane, and R.A. Lempicki Identifying biological themes within lists of genes with EASE Gen. Biol. 4 2003 R70
24. S.Y. Seo, Y.B. Chen, I. Ivanovska, A.M. Ranger, S.J. Hong, V.L. Dawson, S.J. Korsmeyer, D.S. Bellows, Y. Fannjiang, and J.M. Hardwick BAD is a pro-survival factor prior to activation of its pro-apoptotic function J. Biol. Chem. 279 2004 42240 42249
25. C.W. Chiang, C. Kanies, K.W. Kim, W.B. Fang, C. Parkhurst, M. Xie, T. Henry, and E. Yang Protein phosphatase 2A dephosphorylation of phosphoserine 112 plays the gatekeeper role for BAD-mediated apoptosis Mol. Cell. Biol. 23 2003 6350 6362
26. L.H. Boise, and C.B. Thompson Bcl-x(L) can inhibit apoptosis in cells that have undergone Fas-induced protease activation Proc. Natl. Acad. Sci. USA 94 1997 3759 3764
27. N. Van Houten, S.F. Blake, E.J. Li, T.A. Hallam, D.G. Chilton, W.K. Gourley, L.H. Boise, C.B. Thompson, and E.B. Thompson Elevated expression of Bcl-2 and Bcl-x by intestinal intraepithelial lymphocytes: resistance to apoptosis by glucocorticoids and irradiation Int. Immunol. 9 1997 945 953
28. E.H. Cheng, T.V. Sheiko, J.K. Fisher, W.J. Craigen, and S.J. Korsmeyer VDAC2 inhibits BAK activation and mitochondrial apoptosis Science 301 2003 513 517
29. M.R. Jensen, T. Audolfsson, V.M. Factor, and S.S. Thorgeirsson In vivo expression and genomic organization of the mouse cyclin I gene (Ccni) Gene 256 2000 59 67
30. T. Li, A. Inoue, J.M. Lahti, and V.J. Kidd Failure to proliferate and mitotic arrest of CDK11(p110/p58)-null mutant mice at the blastocyst stage of embryonic cell development Mol. Cell. Biol. 24 2004 3188 3197
31. I. Maeda, T. Ohta, H. Koizumi, and M. Fukuda In vitro ubiquitination of cyclin D1 by ROC1-CUL1 and ROC1-CUL3 FEBS Lett. 494 2001 181 185
32. R.F. Hennigan, and P.J. Stambrook Dominant negative c-jun inhibits activation of the cyclin D1 and cyclin E kinase complexes Mol. Biol. Cell 12 2001 2352 2363
33. J.W. Soh, and I.B. Weinstein Roles of specific isoforms of protein kinase C in the transcriptional control of cyclin D1 and related genes J. Biol. Chem. 278 2003 34709 34716
34. J.B. Weitzman, L. Fiette, K. Matsuo, and M. Yaniv JunD protects cells from p53-dependent senescence and apoptosis Mol. Cell 6 2000 1109 1119
35. C. Takahashi, Z. Sheng, T.P. Horan, H. Kitayama, M. Maki, K. Hitomi, Y. Kitaura, S. Takai, R.M. Sasahara, A. Horimoto, Y. Ikawa, B.J. Ratzkin, T. Arakawa, and M. Noda Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK Proc. Natl. Acad. Sci. USA 95 1998 13221 13226
36. S.S. Huang, T.Y. Ling, W.F. Tseng, Y.H. Huang, F.M. Tang, S.M. Leal, and J.S. Huang Cellular growth inhibition by IGFBP-3 and TGF-beta1 requires LRP-1 FASEB J. 17 2003 2068 2081
37. X. Lin, M. Liang, and X.H. Feng Smurf2 is a ubiquitin E3 ligase mediating proteasome-dependent degradation of Smad2 in transforming growth factor-beta signaling J. Biol. Chem. 275 2000 36818 36822
38. P. Kavsak, R.K. Rasmussen, C.G. Causing, S. Bonni, H. Zhu, G.H. Thomsen, and J.L. Wrana Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation Mol. Cell 6 2000 1365 1375
39. H. Zhang, and S.N. Cohen Smurf2 up-regulation activates telomere-dependent senescence Genes Dev. 18 2004 3028 3040
40. A. Rivard, L. Berthou-Soulie, N. Principe, M. Kearney, C. Curry, D. Branellec, G.L. Semenza, and J.M. Isner Age-dependent defect in vascular endothelial growth factor expression is associated with reduced hypoxia-inducible factor 1 activity J. Biol. Chem. 275 2000 29643 29647
41. D. Zohlnhofer, T. Richter, F. Neumann, T. Nuhrenberg, R. Wessely, R. Brandl, A. Murr, C. Klein, and P. Baeuerle Transcriptome analysis reveals a role of interferon-γ in human neointima formation Mol. Cell 7 2001 1059 1069
42. P. Rajan, D.M. Panchision, L.F. Newell, and R.D. McKay BMPs signal alternately through a SMAD or FRAP-STAT pathway to regulate fate choice in CNS stem cells J. Cell Biol. 161 2003 911 921
43. T. Gotoh, K. Terada, S. Oyadomari, and M. Mori hsp70-DnaJ chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria Cell Death Differ. 11 2004 390 402
44. J.A. Hutt, J.P. O'Rourke, and J. DeWille Signal transducer and activator of transcription 3 activates CCAAT enhancer-binding protein delta gene transcription in G0 growth-arrested mouse mammary epithelial cells and in involuting mouse mammary gland J. Biol. Chem. 275 2000 29123 29131
45. T.L. Sander, K.F. Stringer, J.L. Maki, P. Szauter, J.R. Stone, and T. Collins The SCAN domain defines a large family of zinc finger transcription factors Gene 310 2003 29 38
46. T. McCaffrey, C. Fu, B. Du, S. Eksinar, K. Kent, H. Bush, K. Kreiger, T. Rosengart, M. Cybulsky, E. Silverman, and T. Collins High-level expression of Egr-1, and Egr-1 inducible genes, in mouse and human atherosclerosis J. Clin. Invest. 105 5 2000 653 662
47. J.F. Bromberg, M.H. Wrzeszczynska, G. Devgan, Y. Zhao, R.G. Pestell, C. Albanese, and J.E. Darnell Jr. STAT3 as an oncogene Cell 98 1999 295 303
48. G. Niu, K.L. Wright, M. Huang, L. Song, E. Haura, J. Turkson, S. Zhang, T. Wang, D. Sinibaldi, D. Coppola, R. Heller, L.M. Ellis, J. Karras, J. Bromberg, D. Pardoll, R. Jove, and H. Yu Constitutive STAT3 activity up-regulates VEGF expression and tumor angiogenesis Oncogene 21 2002 2000 2008
49. Y. Shen, G. Devgan, J.E. Darnell Jr., and J.F. Bromberg Constitutively activated Stat3 protects fibroblasts from serum withdrawal and UV-induced apoptosis and antagonizes the proapoptotic effects of activated Stat1 Proc. Natl. Acad. Sci. USA 98 2001 1543 1548
50. J.F. Bromberg, C.M. Horvath, Z. Wen, R.D. Schreiber, and J.E. Darnell Jr. Transcriptionally active Stat1 is required for the antiproliferative effects of both interferon alpha and interferon gamma Proc. Natl. Acad. Sci. USA 93 1996 7673 7678
51. L.F. Stancato, M. David, C. Carter-Su, A.C. Larner, and W.B. Pratt Preassociation of STAT1 with STAT2 and STAT3 in separate signalling complexes prior to cytokine stimulation J. Biol. Chem. 271 1996 4134 4137
52. A. Stephanou, B.K. Brar, R.A. Knight, and D.S. Latchman Opposing actions of STAT-1 and STAT-3 on the Bcl-2 and Bcl-x promoters Cell Death Differ. 7 2000 329 330
53. A.L. Wurster, V.L. Rodgers, M.F. White, T.L. Rothstein, and M.J. Grusby Interleukin-4-mediated protection of primary B cells from apoptosis through Stat6-dependent up-regulation of Bcl-xL J. Biol. Chem. 277 2002 27169 27175
54. C. Albanese, M. D'Amico, A.T. Reutens, M. Fu, G. Watanabe, R.J. Lee, R.N. Kitsis, B. Henglein, M. Avantaggiati, K. Somasundaram, B. Thimmapaya, and R.G. Pestell Activation of the cyclin D1 gene by the E1A-associated protein p300 through AP-1 inhibits cellular apoptosis J. Biol. Chem. 274 1999 34186 34195
55. K. Wu, C. Wang, M. D'Amico, R. Lee, C. Albanese, R. Pestell, and S. Mani Flavopiridol and trastuzumab syntergistically inhibit proliferation of breast cancer cells: association with selective cooperative inhibition of cyclin D1-dependent kinase and Akt signaling pathways Mol. Canc. Ther. 1 2002 695 706
56. A. Okamoto, W. Jiang, S.J. Kim, E.A. Spillare, G.D. Stoner, and I.B.H. Weinstein Overexpression of human cyclin D1 reduces the transforming growth factor β (TGF-β) type II receptor and growth inhibition by TGF-β1 in an immortalized human esophageal epithelial cell line Proc. Natl. Acad. Sci. USA 91 1994 11576 11580
57. T. Zhang, L.B. Nanney, M.O. Peeler, C.S. Williams, L. Lamps, K.J. Heppner, R.N. Du Bois, and R.D. Beauchamp Decreased transforming growth factor beta type II receptor expression in intestinal adenomas from Min/+ mice is associated with increased cyclin D1 and cyclin-dependent kinase 4 expression Cancer Res. 57 1997 1638 1643
58. S.K. Moon, B.Y. Cha, and C.H. Kim In vitro cellular aging is associated with enhanced proliferative capacity, G1 cell cycle modulation, and matrix metalloproteinase-9 regulation in mouse aortic smooth muscle cells Arch. Biochem. Biophys. 418 2003 39 48
59. J.C. Tsai, M.A. Perrella, M. Yoshizumi, C.M. Hsieh, E. Haber, R. Schlegel, and M. Lee Promotion of vascular smooth muscle cell growth by homocysteine: a link to atherosclerosis Proc. Natl. Acad. Sci. USA 91 1994 6369 6373
60. D. Zhao, J. Letterman, and B.M. Schreiber beta-Migrating very low density lipoprotein (beta VLDL) activates smooth muscle cell mitogen-activated protein (MAP) kinase via G protein-coupled receptor-mediated transactivation of the epidermal growth factor (EGF) receptor: effect of MAP kinase activation on beta VLDL plus EGF-induced cell proliferation J. Biol. Chem. 276 2001 30579 30588
61. J. Ruef, A.S. Meshel, Z. Hu, C. Horaist, C.A. Ballinger, L.J. Thompson, V.D. Subbarao, J.A. Dumont, and C. Patterson Flavopiridol inhibits smooth muscle cell proliferation in vitro and neointimal formation in vivo after carotid injury in the rat Circulation 100 1999 659 665
62. M.W. Chang, E. Barr, M.M. Lu, K. Barton, and J.M. Leiden Adenovirus-mediated over-expression of the cyclin/cyclin-dependent kinase inhibitor, p21 inhibits vascular smooth muscle cell proliferation and neointima formation in the rat carotid artery model of balloon angioplasty J. Clin. Invest. 96 1995 2260 2268
63. Z.Y. Yang, R.D. Simari, N.D. Perkins, H. San, D. Gordon, G.J. Nabel, and E.G. Nabel Role of the p21 cyclin-dependent kinase inhibitor in limiting intimal cell proliferation in response to arterial injury Proc. Natl. Acad. Sci. USA 93 1996 7905 7910
64. S. Hashemolhosseini, Y. Nagamine, S.J. Morley, S. Desrivieres, L. Mercep, and S. Ferrari Rapamycin inhibition of the G1 to S transition is mediated by effects on cyclin D1 mRNA and protein stability J. Biol. Chem. 273 1998 14424 14429
65. K. Tanabe, M. Degertekin, E. Regar, J. Ligthart, W. van der Giessen, and P. Serruys No delayed restenosis at 18:months after implantation of sirolimus-eluting stent Catheter. Cardiovasc. Interv. 57 2002 69 71
66. X. Pi, C. Yan, and B.C. Berk Big mitogen-activated protein kinase (BMK1)/ERK5 protects endothelial cells from apoptosis Circ. Res. 94 2004 362 369
67. S.R. Datta, A.M. Ranger, M.Z. Lin, J.F. Sturgill, Y.C. Ma, C.W. Cowan, P. Dikkes, S.J. Korsmeyer, and M.E. Greenberg Survival factor-mediated BAD phosphorylation raises the mitochondrial threshold for apoptosis Dev. Cell 3 2002 631 643
68. A. Garcia, X. Cayla, J. Guergnon, F. Dessauge, V. Hospital, M.P. Rebollo, A. Fleischer, and A. Rebollo Serine/threonine protein phosphatases PP1 and PP2A are key players in apoptosis Biochimie 85 2003 721 726
69. B.C. Kim, M. Mamura, K.S. Choi, B. Calabretta, and S.J. Kim Transforming growth factor beta 1 induces apoptosis through cleavage of BAD in a Smad3-dependent mechanism in FaO hepatoma cells Mol. Cell. Biol. 22 2002 1369 1378
70. Y.E. Chin, M. Kitagawa, K. Kuida, R.A. Flavell, and X.Y. Fu Activation of the STAT signaling pathway can cause expression of caspase 1 and apoptosis Mol. Cell. Biol. 17 1997 5328 5337
71. T. Tatsuta, A. Shiraishi, and J.D. Mountz The prodomain of caspase-1 enhances Fas-mediated apoptosis through facilitation of caspase-8 activation J. Biol. Chem. 275 2000 14248 14254
72. H.J. Ankersmit, T. Weber, J. Auer, G. Roth, M. Brunner, E. Kvas, B. Moser, S. Spreitzer, E. Lassnig, E. Maurer, P. Hartl, E. Wolner, G. Boltz-Nitulescu, and B. Eber Increased serum concentrations of soluble CD95/Fas and caspase 1/ICE in patients with acute angina Heart 90 2004 151 154