Bax-mediated cell death by the Gax homeoprotein requires mitogen activation but is independent of cell cycle activity

EMBO Journal

Volumn 17, Issue 13, 1998, Pages 3576-3586

  Perlman, Harris ^a,b   Sata, Masataka ^a   Le Roux, Aude ^c   Sedlak, Thomas W ^d   Branellec, Didier ^c   Walsh, Kenneth ^a,b  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TUFTS UNIVERSITY   (United States)

^c SANOFI   (France)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Bax; Cell cycle; Homeobox gene; Mitogen regulated transcription factor

Indexed keywords

HOMEODOMAIN PROTEIN; MITOGENIC AGENT; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P21; PROTEIN P53;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; FIBROBLAST; HOMEOSTASIS; HOMOZYGOTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL CYCLE; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; G1 PHASE; HOMEODOMAIN PROTEINS; HYDROXYUREA; MALE; MICE; MITOGENS; MUSCLE PROTEINS; MUSCLE, SMOOTH, VASCULAR; PHENOTYPE; POLYENES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; S PHASE; SERUM ALBUMIN, BOVINE; SIROLIMUS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0032127486     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.13.3576     Document Type: Article

References (59)

1. Batistatou, A. and Greene, L.A. (1993) Internucleosomal DNA cleavage and neuronal cell survival/death. J. Cell Biol., 122, 523-532.
2. Bochaton-Piallat, M.L., Gabbiani, F., Redard, M., Desmouliere, A. and Gabbiani, G. (1995) Apoptosis participates in cellularity regulation during rat aortic intimal thickening. Am. J. Pathol., 146, 1059-1064.
3. Boyd, J.M. et al. (1995) Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins. Oncogene, 11, 1921-1928.
4. Chittenden, T.C., Flemington, C., Houghton, A.B., Ebb, R.G., Gallo, G.J., Elangtovan, B., Chinnadurai, G. and Lutz, R.J. (1995) A conserved domain in Bak, distinct from BH1 and BH2, mediates cell death and protein binding functions. EMBO J., 14, 5589-5596.
5. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162, 156-159.
6. Clayman, G.L., Liu, T.J., Overholt, S.M., Mobley, S.R., Wang, M., Janot, F. and Goepfert, H. (1996) Gene therapy for head and neck cancer. Comparing the tumor suppressor gene p53 and a cell cycle regulator WAF/CIP (p21). Arch. Otolaryngol., 122, 489-493.
7. Clowes, A.W., Reidy, M.A. and Clowes, M.M. (1983) Kinetics of cellular proliferation after arterial injury I: smooth muscle cell growth in the absence of endothelium. Lab. Invest., 49, 327-333.
8. Colombel, M., Olsson, C.A., Ng, P.Y. and Buttyan, R. (1992) Hormone-regulated apoptosis results from reentry of differentiated prostate cells onto a defective cell cycle. Cancer Res., 52, 4313-4319.
9. Dear, T.N. et al. (1995) The Hox11 gene is essential for cell survival during spleen development. Development, 121, 2909-2915.
10. Deckwerth, T.L., Elliott, J.L., Knudson, C.M., Johnson, E.M., Snider, W.D. and Korsmeyer, S.J. (1996) BAX is required for neuronal death after trophic factor deprivation and during development. Neuron, 17, 401-411.
11. Del Sal, G., Ruaro, M.E., Philipson, L. and Schneider, C. (1992) The growth-arrest-specific gene gas1 is involved in growth suppression. Cell. 70, 595-607.
12. 1 checkpoint control. Cell, 82, 675-684.
13. Evan, G.I., Wyllie, A.H., Gilbert, C.S., Littlewood, T.D., Land, H., Brooks, M., Waters, C.M., Penn, L.Z. and Hancock, D.C. (1992) Induction of apoptosis in fibroblasts by c-myc protein. Cell, 69, 119-128.
14. Fabbretti, E., Edomi, P., Brancolini, C. and Schneider, C. (1995) Apoptotic phenotype induced by overexpression of wild-type gas3/PMP22: its relation to the demylinating peripheral neuropathy CMT1A. Genes Dev., 9, 1846-1856.
15. Farinelli, S.E. and Greene, L.A. (1996) Cell cycle blockers mimosine, ciclopirox, and deferoxamine prevent the death of PC12 cells and postmitotic sympathetic neurons after removal of trophic support. J. Neurosci., 16, 1150-1162.
16. 1 transition in vascular smooth muscle cells. Mol. Cell. Biol., 13, 3722-3733.
17. Gorski, D.H., LePage, D.F. and Walsh, K. (1994) Cloning and sequence analysis of homeobox transcription factor cDNAs with an inosine-containing probe. BioTechniques, 16, 856-865.
18. Han, D.K., Haudenschild, C.C., Hong, M.K., Tinkle, B.T., Leon, M.B. and Liau, G. (1995) Evidence for apoptosis in human atherogenesis and in a rat vascular injury model. Am. J. Pathol., 147, 267-277.
19. Harvey, D.M. and Levine, A.J. (1991) p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts. Genes Dev., 5, 2375-2385.
20. Hoang, A.T., Cohen, K.J., Barret, J.F., Bergstrom, D.A. and Dang, C.V. (1994) Participation of cyclin A in myc-induced apoptosis. Proc. Natl Acad. Sci. USA, 91, 6875-6879.
21. Hockenbery, D. (1995) Defining apoptosis. Am. J. Pathol., 146, 16-19.
22. Hockenbery, D., Nunez, G., Milliman, C., Schreiber, R.D. and Korsmeyer, S.J. (1990) Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature, 348, 334-336.
23. Hockenbery, D.M., Oltvai, Z.N., Yin, X.M., Milliman, C.L. and Korsmeyer, S.J. (1993) Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell, 75, 241-251.
24. Hoffman, B. and Liebermann, D.A. (1994) Molecular controls of apoptosis: differentiation/growth arrest primary response genes, protooncogenes, and tumor suppressor genes as positive and negative modulators. Oncogene, 9, 1807-1812.
25. Isner, J.M., Kearney, M., Bortman, S. and Passeri, J. (1995) Apoptosis in human atherosclerosis and restenosis. Circulation, 91, 2703-2711.
26. Kearney, M., Pieczek, A., Haley, L., Losordo, D.W., Andrés, V., Schainfeld, R., Rosenfield, K. and Isner, J.M. (1997) Histopathology of in-stent restenosis in patients with peripheral artery disease. Circulation, 95, 1998-2002.
27. Knudson, C.M., Tung, K.S., Tourtellotte, W.G., Brown, G.A. and Korsmeyer, S.J. (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science, 270, 96-99.
28. Ko, L.J. and Prives, C. (1996) p53: puzzle and paradigm. Genes Dev., 10, 1054-1072.
29. Kowalik, T.F., DeGregori, J., Schwarz, J.K. and Nevins, J.R. (1995) E2F1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J. Virol., 69, 2491-2500.
30. Liu, Y. and Kitsis, R.N. (1996) Induction of DNA synthesis and apoptosis in cardiac myocytes by E1A oncoprotein. J. Cell Biol., 133, 325-334.
31. Mader, S.L. (1992) Influence of clinical age on the β-adrenergic system in cultural rat aortic and mesenteric artery smooth muscle cells. J. Gerontol. Biol. Sci., 47, B32-B36.
32. Maillard, L. et al. (1997) Percutaneous delivery of the gax gene inhibits vessel stenosis in a rabbit model of balloon angioplasty. Cardiovasc. Res., 35, 536-546.
33. Marazzi, G., Wang, Y. and Sassoon, D. (1997) Msx2 is a transcriptional regulator in the BMP-4 mediated programmed cell death pathway. Dev. Biol., 186, 127-138.
34. Marcellus, R.C., Teodoro, J.G., Wu, T., Broug, D.E., Ketner, G., Shore, G.C. and Branton, P.E. (1996) Adenovirus type 5 early region 4 is responsible for E1A-induced p53-independent apoptosis. J. Virol., 70, 6207-6215.
35. Marx, S.O., Jayaraman, T., Go, L.O. and Marks, A.R. (1995) Rapamycin-FKBP inhibits cell cycle regulators of proliferation in vascular smooth muscle cells. Circ. Res., 76, 412-417.
36. McCurrach, M.E., Connor, T.M.F., Knudson, C.M., Korsmeyer, S.J. and Lowe, S.W. (1997) Bax-deficiency promotes drug resistance and oncogenic transformation by attenuating p53-dependent apoptosis. Proc. Natl Acad. Sci. USA, 94, 2345-2349.
37. Miura, M., Zhu, H., Rotello, R., Hartwieg, E.A. and Yuan, J. (1993) Induction of apoptosis in fibroblasts by IL-β-converting enzyme, a mammalian homolog of the C.elegans cell death gene ced-3. Cell, 75, 653-660.
38. Miyashita, T. and Reed, J.C. (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell, 80, 293-299.
39. Miyashita, T., Harigal, H., Hanada, M. and Reed, J.C. (1994a) Identification of a p53-dependent negative response element in the bcl-2 gene. Cancer Res., 54, 3131-3135.
40. Miyashita, T., Krajewski, S., Krajewska, H., Wang, H.G., Lin, H.K., Liebermann, D.A., Hoffman, B. and Reed, J.C. (1994b) Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene, 9, 1799-1805.
41. Oltvai, Z.N., Milliman, C.L. and Korsmeyer, S.J. (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell, 74, 609-619.
42. Perlman, H., Maillard, L., Krasinski, K. and Walsh, K. (1997) Evidence for the rapid onset of apoptosis in medial smooth muscle cells following balloon injury. Circulation, 95, 981-987.
43. Qin, X.-Q., Livingston, D., Kaelin, W.G. and Adams, P.D. (1994) Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl Acad. Sci. USA, 91, 10918-10922.
44. Quaggin, S.E., Yeger, H. and Igarashi, P. (1997) Antisense oligonucleotides to Cux-1 a Cut-related homeobox gene, cause increased apoptosis in mouse embryonic kidney cultures. J. Clin. Invest., 99, 718-724.
45. Raffo, A.J., Perlman, H., Chen, M.W., Day, M.L., Streitman, J.S. and Buttyan, R. (1995) Overexpression of bcl-2 protects prostate cancer cells from apoptosis in vitro and confers resistance to androgen depletion in vivo. Cancer Res., 55, 4438-4445.
46. Sata, M., Perlman, H., Muruve, D.A., Silver, M., Ikebe, M., Libermann, T.A., Oettgen, P. and Walsh, K. (1998) Fas ligand gene transfer to the vessel wall inhibits neointima formation and overrides the adenovirus-mediated T cell response. Proc. Natl Acad. Sci. USA, 95, 1213-1217.
47. Sharkey, M. Graba, Y. and Scott, M.P. (1997) Hox genes in evolution: proteins surfaces and paralog groups. Trends Genet., 13, 145-151.
48. Shi, L., Nishioka, W.K., Th'ng, J., Bradbury, E.M., Litchfield, D.W. and Greenberg, A.H. (1994) Premature p34cdc2 activation required for apoptosis. Science, 263, 1143-1145.
49. Smith, R.C. et al. (1997) p21CIP1-mediated inhibition of cell proliferation by overexpression of the gax homeodomain gene. Genes Dev., 11, 1674-1689.
50. Stratford-Perricaudet, L.D., Makeh, I., Perricaudet, M. and Briand, P. (1992) Widespread long-term gene transfer to mouse skeletal muscles and heart. J. Clin. Invest., 90, 626-630.
51. Walsh, K. and Perlman, H. (1996) Molecular strategies to inhibit restenosis: modulation of the vascular myocyte phenotype. Semin. Intervent. Cardiol., 1, 173-179.
52. Wang, J. and Walsh, K. (1996) Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science, 273, 359-361.
53. Wei, G.L., Krasinski, K., Kearney, M., Isner, J.M., Walsh, K. and Andrés, V. (1997) Temporally and spatially coordinated expression of cell cycle regulatory factors after angioplasty. Circ. Res., 80, 418-426.
54. Weir, L., Chen, D., Pastore, C., Isner, J.M. and Walsh, K. (1995) Expression of GAX, a growth-arrest homeobox gene, is rapidly down-regulated in the rat carotid artery during the proliferative response to balloon injury. J. Biol. Chem., 270, 5457-5461.
55. Xiong, W.C. and Montell, C. (1995) Defective glia induce neuronal apoptosis in the repo visual system of Drosophila. Neuron, 14, 581-590.
56. Yamashita, J. et al. (1997) Opposite regulation of Gax homeobox expression by angiotensin II and C-type natriuretic peptide. Hypertension, 29, 381-387.
57. Yang, E. and Korsmeyer, S.J. (1996) Molecular thanatopsis: a discourse on the BCL2 family and cell death. Blood. 88, 386-401.
58. Zhan, Q. et al. (1994) The gadd and MyD genes define a novel set of mammalian genes encoding acidic proteins that synergistically suppress cell growth. Mol. Cell. Biol., 14, 2361-2371.
59. Zoidl, G., Blass-Kampmann, S., D'Urso, D., Schmalenbach, C. and Muller, H.W. (1995) Retroviral-mediated gene transfer of the peripheral mylein protein PMP22 in Schwann cells: modulation of cell growth. EMBO J., 14, 1122-1128.