Bcl-2 inhibits retinoic acid-induced apoptosis during the neural differentiation of embryonal stem cells

Journal of Cell Biology

Volumn 132, Issue 5, 1996, Pages 955-968

  Okazawa, Hitoshi ^a   Shimizu, Jun ^a   Kamei, Masaki ^a   Imafuku, Ichiro ^a   Hamada, Hiroshi ^b   Kanazawa, Ichiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; CYCLOHEXIMIDE; DACTINOMYCIN; RETINOIC ACID; RETINOIC ACID RECEPTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CELL DIFFERENTIATION; DNA CLEAVAGE; EMBRYO; GENE DISRUPTION; NERVE DEGENERATION; NONHUMAN; PLASMID; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; BASE SEQUENCE; BLOTTING, NORTHERN; BRAIN; CELL DIFFERENTIATION; CELL LINE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VECTORS; MICE; MOLECULAR SEQUENCE DATA; NERVOUS SYSTEM; NERVOUS SYSTEM PHYSIOLOGY; NEURONS; OLIGONUCLEOTIDES, ANTISENSE; POLYMERASE CHAIN REACTION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; STEM CELLS; TRETINOIN;

EID: 0029991311     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.132.5.955     Document Type: Article

References (97)

1. Akhtar, S , R Kohle, and R.L. Juliano. 1991. Stability of antisense DNA oligonucleotide analogs in cellular extracts and sera. Life Sci. 49:1793-1801.
2. Allsopp, T.E., S. Wyatt, H.F. Patterson, and A.M. Davies. 1993. The protooncogene bcl-2 can selectively rescue neurotrophic factor-dependent neurons from apoptosis. Cell. 73:295-307.
3. Askew, D.S., R.A. Ashmun, B.C. Simmons, and J.L. Cleveland. 1991. Constitutive c-myc expression in an IL-3-dependent myeloid cell line supresses cell cycle arrest and accelerates apoptosis. Oncogene. 6.1915-1922.
4. Atencia, R., M Garcia-Sanz, F. Unda, and J. Arechaga. 1994. Apoptosis during retinoic acid-induced F9 embryonal carcinoma cells. Exp Cell Res. 214:663-667
5. Bafy, G., T. Miyashita, J.R. Williamson, and J.C. Reed. 1993. Apoptosis induced by withdrawal of Interleukin-3 [IL-3] from an IL-3 dependent hematopoietic cell line is associated with repartitioning of intracellular calcium and is blocked by enforced Bcl-2 oncoprotein production. J. Biol. Chem 268 6511-6519.
6. Bain, G., and D.I. Gottlieb. 1994. Expression of retinoid X receptors in 19 embryonal carcinoma cells and embryonic system cells. Biochem. Biophys. Res. Commun. 200:1252-1256.
7. H on chromosome 14 and near a transcription unit on 18. Cell. 41:899-906.
8. Barde, Y.-A. 1989. Trophic factors and neuronal survival. Neuron. 2:1525-1534.
9. Batistatou, A., and L.A. Greene. 1991. Aurintricarboxylic acid rescues PC12 cells and sympathetic neurons from death caused by nerve growth factor deprivation, correlation with suppression, of endonuclease activity. J. Cell Biol. 115:461-471
10. Bissonnette, R.P., F. Echeverri, A. Mahboubi, and D.R. Green 1992. Apoptotic cell death induced by c-Myc is inhibited by bcl-2. Nature (Lond ). 359: 552-554.
11. Boise, L.H., M. Gonzalez-Garcia, C.E. Posteme, L. Ding, T. Lindsten, L.A. Turka, X. Mao, G. Nunez, and C.B. Thompson. 1993. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell. 74: 597-308.
12. Burton, K. 1956. A study of the conditions and mechanism of diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem. J. 62:315-323.
13. Castren, E., Y. Ohga, M.P. Berzaghi, G. Tzimagiorgis, H. Thoenen, and D. Lindholm. 1994. bcl-2 messenger RNA is localized in neurons and adult rat brain. Neuroscience. 61:165-177.
14. Chante, J., W. de Graaff, S. Shen, and J. Deschamps. 1994. Ectopic expression of Hoxb-8 causes duplication of the ZPA in the forelimb and homeotic transformation of axial structures. Cell. 78.589-601.
15. Chambaut-Guerin, A.-M., M.-C. Martinez, C. Hamimi, X. Gauthereau, and J. Nunez. 1995. Tumor necrosis factor receptors in neuroblastoma SKNBE cells and their regulation by retinoic acid. J. Neurochem. 65:537-544.
16. Chambon, P. 1994. The retinoid pathway: molecular and genetic analyses. Semin. Cell Biol. 5:115-125.
17. Chittenden, T., E.A. Harrington, R. O'Conner, C. Flemington, R.J. Lutz, G.I. Evan, and B.C. Guild. 1995. Induction of apoptosis by the Bcl-2 homologue Bak. Nature (Lond.). 374:733-736.
18. Clarke, A.R., C.A Purdie, D.J. Harrison, R.G. Morris, C.C. Bird, M L. Hooper, and A H. Wyllie. 1993. Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature (Lond.). 362:849-852.
19. Cleary, M.L., and J. Sklar. 1985. Nucleotide sequence of a t(14;18) chromosomal breakpoint in follicular lymphoma and demonstration of a breakpoint-cluster region near a transcriptionally active locus on chromosome 18. Proc. Natl. Acad. Sci. USA. 82:7439-7443.
20. Culotta, E., and D.E. Koshland. 1993. p53 sweeps through cancer reseach. Science (Wash DC). 262:1958-1961.
21. de-The, H , M.M. Vivanco-Ruiz, P. Tiollais, H. Stunnenberg, and A. Dejean. 1990. Identification of a retinoic acid responsive element in the retinoic acid beta gene. Nature (Lond.). 343:177-180.
22. Dispasquale, B., A.M Marini, and R.J. Youle. 1991. Apoptosis and DNA degradation induced by 1-methyl-4-phenylpyridinium in neurons. Biochem. Biophys. Res. Commun. 181:1442-1448.
23. Dolle, P., A. Dierich, M. LeMeur, T. Schimmang, B. Schuhbaur, P. Chambon, and D. Double. 1993. Disruption of the Hox-13 gene induces localized heterochrony leading to mice with neotenic limbs. Cell. 75:431-441
24. Dolle, P., V. Fraulob, P. Kastner, and P. Chambon. 1994. Developmental expression of murine retinoid X receptor (RXR) genes. Mech Dev. 45:91-104.
25. Echelard, Y., D.J. Epstein, B. St-Jacques, L. Shen, J Mohler, J A. McMahon, and A.P. McMahon 1993. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity Cell. 75: 1417-1430.
26. Edwards, S N., A.E. Buckmaster, and A.M. Tolkovsky. 1991. The death program in cultured sympathetic neurons can be suppressed at post-translational level by nerve growth factor, cyclic AMP and depolarization. J. Neurochem. 57.2140-2143
27. Estus, S., W.J. Zaks, R.S. Freeman, M Gruda, R. Bravo, and E.M. Johnson, Jr. 1994 Altered gene expression in neurons during programmed cell death: identification of c-Jun as necessary for neuronal apoptosis. J. Cell Biol. 127 1717-1727.
28. Evan, G.I., A.H. Wyllie, C.S. Gilbert, T.D. Littlewood, H. Land, M Brooks, C.M. Waters, L.Z Penn, and D.C. Hancock 1992. Induction of apoptosis in fibroblasts by c-Myc protein. Cell. 69:119-128.
29. Fanidi, A , E.A. Harrington, and G.I. Evan. 1992. Cooperative interaction between c-myc and bcl-2 proto-oncogenes. Nature (Lond.). 359:554-556.
30. Ferrer, I., A. Tortosa, E. Condom, R. Blanco, A. Macaya, and A. Planas. 1994. Increased expression of bcl-2 immunoreactivity in the developing cerebral cortex of the rat. Neurosci. Lett. 179:3-16.
31. Francis, P.H., M.K. Richardson, P M. Brickell, and C Tickle. 1994. Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. Development. 120:209-218.
32. Garcia, I., I. Martinou, Y. Tsujimoto, and J.-C. Martinou. 1992 Prevention of programmed cell death of sympathetic neurons by the bcl-2 protooncogene Science (Wash. DC). 258:302-304
33. Giguere, V , M. Shago, R. Zirngibl, P. Tate, J Rossant, and S. Varmuza. 1990. Identification of a novel isoform of the retinoic acid receptor γ expressed in mouse embryo Mol. Cell. Biol. 10 2335-2340.
34. Greene, L.A., and A.S. Tischler. 1976. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad Sci. USA. 73:2424-2428.
35. Greene, L.A. 1978. Nerve growth factor prevents the death and stimulates neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-free medium. J. Cell Biol. 78:747-755.
36. Ham, J., C. Babij, J. Whitfield, C.M. Pfarr, M. Lallemand, and L.L. Rubin. 1995. A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron. 14:927-939.
37. Hamburger, V., and R.W. Oppenheim. 1982. Naturally occuring neuronal death in vertebrates. Neurosci. Commun. 1:39-55.
38. Hockenbery, D., G. Nunez, C. Milliman, R.D. Schreber, and S.J. Korsmeyer. 1990. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature (Lond ). 348:334-336.
39. Hockenbery, D , Z. Oltavai, X -M. Yin, C. Milliman, and S.J. Korsmeyer. 1993. Bcl-2 functions in an antioxident pathway apoptosis. Cell. 75:241-251.
40. Hogan, B.L.M., C. Thaller, and O. Eichele. 1992 Evidence that Hensen's node is a site of retinoic acid synthesis. Nature (Lond.). 359:237-241
41. Jones-Velleneuve, E.M., M A. Rudnicki, J.F. Harris, and M.W. McBurney. 1983. Retinoic acid-induced neural differentiation of embryonal carcinoma cells. Mol. Cell. Biol. 3:2271-2279
42. Jonk, L.J.C., M.E.J. de Jonge, F A E. Kruyt, C.L Mummery, P.T. van der Saag, and W. Kruijer 1992. Aggregation and cell cycle dependent retinoic acid receptor mRNA expression in P19 embryonal carcinoma cells. Mech. Dev. 36:165-172.
43. Kane, D.J., T.A. Sarafin, S. Auton, H. Hahn, F.B. Gralla, J.C. Valentine, T Ord, and D.E. Bredesen. 1993. Bcl-2 inhibition of neural cell death: decreased generation of reative oxygen species. Science (Wash. DC). 262:1274-1276.
44. Kiefer, M.C., M.J. Brauer, V.C Powers, J.J. Wu, S.R. Umansky, L.D. Tomei, and P.J. Barr. 1995. Modulation of apoptosis by the widely distributed homologue Bak. Nature (Lond.). 374:736-739.
45. Kozopas, K.M., T. Yang, H.L. Buchan, P Zhou, and R W. Craig. 1993. MCL-1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL-2. Proc Natl. Acad. Sci. USA. 90:3516-3520.
46. Kure, S., T. Tominaga, T. Yoshimoto, K. Tada, and K. Narisawa. 1991. Glutamate triggers internucleosomal DNA cleavage in neuronal cells. Biochem. Biophys Res Commun. 179:39-45.
47. LaSpada, A.R., E.M. Wilson, D.B. Lubahn, A.E. Harding, and K.H. Fischbeck. 1991. Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature (Lond.). 352:77-79.
48. Leroy, P., A. Krust, A. Zelent, C Mendelsohn, J.-M. Garnier, P. Kastner, A. Dierich, and P. Chambon. 1991. Multiple isoforms of the retinoic acid receptor α are generated by alternative splicing and differential induction by retinoic acid. EMBO J. 10:59-69.
49. Lin, E.Y., A Orlofsky, M.S. Berger, and M.B. Prystowsky. 1993. Characterization of A1, a novel hemopoietic-specific early-response gene with sequence similarity to bcl-2. J. Immunol. 151:1979-1988.
50. Lowe, S.W., E.M. Schmitt, S.W. Smith, B.A. Osborne, and T. Jacks 1993. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature (Lond.). 362:847-849.
51. Luckow, B., and G. Schutz 1987. CAT constructions with multiple unique restriction sites for the functional analysis of eukaryotic promoters and regulatory elements Nucleic Acid Res. 15:5490.
52. Mah, S P., L.T. Zhong, Y. Liu, A. Roghani, R.H. Edwards, and D.E. Bredesen. 1993. The protooncogene bcl-2 inhibits apoptosis in PC12 cells. J. Neurochem 60:1183-1186.
53. Maden, M., D.E. Ong, and F. Chytil. 1990. Retinoid-binding protein distribution in the developing mammalian nervous system. Development 109:75-80.
54. Maden, M. 1994. The limb bud - part two. Nature (Lond.). 371:560-561.
55. Mangelsdorf, D.J., U. Borgmeyer, R.A Heyman, J.Y. Zhou, E.S. Ong, A.E. Oro, A. Kakizuka, and R M. Evans. 1992. Characterization of three RXR genes that mediate the action of 9-cis retinoic acid. Genes & Dev 6:329-344.
56. Mangelsdorf, D.J., K. Umesono, and R.M. Evans. 1994. The retinoid receptors. In The retinoids, 2nd edition. M B. Sporn, A.B Roberts, and D.S. Goodman, editors. Raven Press, New York. 319-349.
57. Merry, D.E., D.J. Veis, W.F. Hickey, and S.J. Korsmeyer. 1994. bcl-2 protein expression is widespread in the developing nervous system and retained in the adult PNS. Development. 120:301-311.
58. Miyashita, T , and J.C Reed. 1993. Bcl-2 oncoprotein blocks chemotherapyinduced apoptosis in human leukemia cell line. Blood 81:151-157.
59. Miyashita, T , S. Krajewski, M. Krajewska, H.G. Wang, H.K. Lin, D.A. Liebermann, B. Hoffman, and J.C Reed 1994. Tumor suppressor p53 is a regulator of bcl-2 and box gene expression in vitro and in vivo Oncogene. 9.1799-1805.
60. Miyashita, T., and J.C. Reed. 1995. Tumor Suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80:293-299
61. Morgan, R.G., J.-C. Izpisua-Belmonte, D. Duboule, and C J, Tabin. 1992. Targeted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature (Lond.). 358:236-239.
62. Morgenbesser, S.D , B.O Williams, T. Jacks, and R.A. DePinho. 1994. p53-dependent apoptosis produced by Rb-deficiency in the developing mouse lens. Nature (Lond.). 371:72-74.
63. Niswander, L., and G.R. Martin. 1992. Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development, 114: 755-768
64. Niswander, L., and G.R. Martin. 1993. Fgf4 and BMP-2 have opposite effects on limb growth. Nature (Lond.). 361:68-71.
65. Niswander, L , S. Jeffrey, G.R. Martin, and C. Tickle. 1994. A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature (Lond.) 371:609-611.
66. Negrini, M., E. Silini, C. Kozak, Y. Tsujimoto, and C.M. Croce. 1987. Molecular analysis of mbcl-2: structure and expression of the murine gene homologous to the human gene involved in follicular lymphoma. Cell. 49:455-463.
67. Okamoto, K., H. Okazawa, A. Okuda, M. Sakai, M. Muramatsu, and H. Hamada. 1990. A novel octamer binding transcription factor is differentially expressed in mouse embryonic cells. Cell. 60:461-472.
68. Okazawa, H., K. Okamoto, T. Ishino-Kaneko, S. Takeda, Y. Toyoda, M. Muramatsu, and H. Hamada. 1991. The oct-3 gene, a gene for an embryonic transcription factor is controlled by aretinoic acid repressible enhancer. EMBO J. 10:2997-3005.
69. Oltvai, Z.N., C.L. Milliman, and S.J. Korsmeyer. 1993. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell. 74:609-619.
70. Oppenheim, R.W. 1991. Cell death during development of the nervous system Annu. Rev. Neurosci. 14:453-501.
71. Pan, H., and A.E. Griep 1994. Altered cell cycle regulation in the lens of HPV-16 E6 or E7 transgenic mice: implications for tumor suppressor gene function in development. Genes & Dev. 8:1285-1299.
72. Park, J.R., K. Robertson, D.D. Hickstein, S Tsai, D.M. Hockenbery, and S.J. Collins. 1994. Dysregulated bcl-2 expression inhibits apoptosis but not differentiation of retinoic acid-induced HL-60 granulocytes. Blood 84:440-445.
73. Pratt, M.A., J. Kralova, and M.W. Mcburney. 1990. A dominant negative mutation of the alpha retinoic acid receptor gene in a retinoic acid-nonresponsive embryonal carcinoma cell. Mol. Cell. Biol 10:6445-6453.
74. Ray, W.J., and D.I. Gottlieb. 1994 Expression of ionotropic glutamate receptor genes by P19 embryonal carcinoma cells. Biochem. Biophys. Res. Commun. 197:1475-1482.
75. Reed, J.C. 1994. Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124:1-6.
76. Riddle, R.D., R.L. Johnson, E. Laufer, and C. Tabin. 1993. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell. 75:1401-1416.
77. Ruberte, E., V. Friederich, G. Morris-Kay, and P. Chambon. 1992. Differential distribution patterns of CRABP I and CRABP II transcripts during mouse embryogenesis. Development. 115:973-987.
78. Ruberte, E., V. Friederich, P. Chambon, and G. Morriss-Kay. 1993. Retionic acid receptors and cellular retinoid binding proteins. III. Their differential transcript distribution during mouse nervous system development. Development 118:267-282.
79. Rudnicki, M.A., and M.W. McBurney. 1987. Cell culture methods and induction of differentiation of embryonal carcinoma cell lines. In Teratocarcinomas and embryonic stem cells. J. Robertson, editor. IRL Press, Oxford, UK. 19-49.
80. Salvatore, A.M., M. Cozzolino, N. Gargano, S. Galanti, A. Levi, and S. Alema. 1995. Neuronal differentiation of P19 cells exhibits cell-specific regulation of neurotrophin receptors. Neuroreport. 6:873-877.
81. Sato, T., M. Hanada, S. Bodrug, S. Irie, N. Iwama, L.H. Boise, C.B. Thompson, E. Golemis, L. Fong, H.-G. Wang, and J.C. Reed. 1994. Interactions among members of the bcl-2 protein family analyzed with a two-hybrid system. Proc. Natl. Acad. Sci. USA. 91:9238-9242.
82. Sellins, K.S., and J.J. Cohen 1987. Gene induction by γ-irradiation leads to DNA fragmentation in lymphocytes. J. Immunol. 139:3199-3206.
83. Sentman, C.L., J.R. Shutter, D. Hockenbery, O. Kanagawa, and S J. Korsmeyer. 1991. Bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell. 67:879-888.
84. Shi, Y., J.M. Glynn, L.J. Guilbert, T.G. Cotter, R.P. Bissonnette, and D R. Green. 1994. Role for c-myc in activation-induced apoptotic cell death in T cell hybridomas Science (Wash. DC). 257:212-214.
85. Shimizu, S., Y. Eguchi, H. Kosaka, W. Kamiike, H. Matsuda, and Y. Tsujimoto. 1995. Prevention of hypoxia-induced cell death by Bcl-2 and Bcl-xL. Nature (Lond.). 374:811-813.
86. Staines, W.A., D.J. Morassutti, K.R. Reul, A.I. Ally, and M.W. McBurney. 1994. Neurons derived from embryonal carcinoma cells have varied morphologies and neurotransmitters. Neuroscience. 58:735-751.
87. Strasser, A., A.W. Harris, and S. Cory. 1991, Bcl-2 transgene inhibits T cell death and perturbs thymic self-sensorship. Cell. 67:889-899.
88. Tabin, C. 1995. The initiation of the limb bud: growth factors, Hox genes and retinoids. Cell. 80:671-674.
89. Takayama, S., T Sato, S. Krajewski, K. Kochel, S. Irie, J.A. Millan, and J.C. Reed. 1995. Cloning and functional analysis of BAG-1: a novel bcl-2-binding protein with anti-cell death activity. Cell. 80:279-284.
90. Tsujimoto, Y., J. Cossman, E. Jaffe, and C.M. Croce. 1985. Involvement of the bcl-2 gene in human follicular lymphoma. Science (Wash. DC). 228:1440-1443.
91. White, E. 1994. p53, guardian of Rb. Nature (Lond.). 371:21-22.
92. L and Bcl-2, displaces Bax and promotes cell death. Cell. 80:285-291.
93. Yin, X.-M., Z.N. Oltvai, and S.J. Korsmeyer. 1994. BH1 and BH2 domains are required for inhibition of apoptosis and heterodimerization with Bax. Nature (Lond). 369:321-323.
94. Yonish-Rouach, E., D. Resnitzky, J. Lotem, L. Sachs, A. Kimchi, and M. Oren. 1991. Wild-type p53 induces apoptosis of myeloid leukemic cells that is inhibited by interleukm-6 Nature (Lond.). 352:345-347.
95. Zelent, A., A. Krust, M. Petkovich, P. Kastner, and P. Chambon. 1989. Cloning of murine α and β retinoic acid receptors and novel receptor γ predominantly expressed in skin. Nature (Lond.). 339:714-717.
96. Zelent, A., C. Mendelssohn, P. Kastner, A. Krust, J.-M. Garnier, F. Ruffenach, and P. Chambon. 1991. Differentially expressed isoforms of the mouse retinoic acid receptor β are generated by usage of two promoters and alternative splicing. EMBO J. 10:71-81.
97. Zhong, L.T., T. Sarafian, D.J. Kane, A.C. Charles, S.P. Mah, R.H. Edwards, and D. E. Bredesen. 1993. Bcl-2 inhibits death of central neural cells induced by multiple agents. Proc Natl. Acad. Sci. USA. 90:4533-4537.