Id2 promotes apoptosis by a novel mechanism independent of dimerization to basic helix-loop-helix factors

Molecular and Cellular Biology

Volumn 18, Issue 9, 1998, Pages 5435-5444

  Florio, Monica ^a   Hernandez, Maria Clemencia ^a   Yang, Hui ^b   Shu, Hui Kuo ^a,d   Cleveland, John L ^a,c   Israel, Mark A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELIX LOOP HELIX PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DIMERIZATION; DNA BINDING; GENE ACTIVATION; GENE EXPRESSION REGULATION; GROWTH REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION;

ANIMALIA;

EID: 0031841824     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.9.5435     Document Type: Article

References (79)

1. Almasan, A., Y. Yin, Y. E. Kelly, E. Y.-H. P. Lee, A. Bradley, W. Li, J. R. Bertino, and G. M. Wahl. 1995. Deficiency of retinoblastoma protein leads to inappropriate S-phase entry, activation of E2F-responsive genes, and apoptosis. Proc. Natl. Acad. Sci. USA 92:5436-5440.
2. Andres-Barquin, P. J., M. C. Hernandez, T. E. Haves, R. D. McKay, and M. A. Israel. 1997. Id genes encoding inhibitors of transcription are expressed during in vitro astrocyte differentiation and in cell lines derived from astrocytic tumors. Cancer Res. 57:215-220.
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 suppresses cell cycle arrest and accelerates apoptosis. Oncogene 6:1915-1922.
4. Barone, M. V., R. Pepperkok, F. A. Peverali, and L. Philipson. 1994. Id proteins control growth induction in mammalian cells. Proc. Natl. Acad. Sci. USA 91:4985-4988.
5. Benezra, R., R. L. Davis, D. Lockshon, D. L. Turner, and H. Weintraub. 1990. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61:40-61.
6. Biggs, J. R., E. V. Murphy, and M. A. Israel. 1992. A human Id-like helix-loop-helix protein expressed during early development. Proc. Natl. Acad. Sci. USA 89:1512-1516.
7. Bossy-Wetzel, E., L. Bakiri, and M. Yaniv. 1997. Induction of apoptosis by the transcription factor c-Jun. EMBO J. 16:1695-1709.
8. Chen, B., B. H. Ban, X. H. Sun, and R. W. Lim. 1997. Inhibition of muscle-specific gene expression by Id3: requirement of the C-terminal region of the protein for stable expression and function. Nucleic Acids Res. 25:423-430.
9. Chen, X., L. J. Ko, L. Jayaraman, and C. Prives. 1996. p53 levels, functional domains, and DNA damage determine the extent of the apoptotic response of tumor cells. Genes Dev. 10:2438-2451.
10. Christy, B. A., L. K. Sanders, L. F. Lau, N. G. Copeland, N. A. Jenkins, and D. Nathans. 1991. An Id-related helix-loop-helix protein encoded by a growth factor-inducible gene. Proc. Natl. Acad. Sci. USA 88:1815-1819.
11. Cleveland, J. Unpublished data.
12. Cleveland, J. L., J. Troppmair, G. Packham, D. S. Askew, P. Lloyd, M. Gonzalez-Garcia, G. Nunez, J. N. Ihle, and U. R. Rapp. 1994. v-raf suppresses apoptosis and promotes growth of interleukin-3-dependent myeloid cells. Oncogene 9:2217-2226.
13. Condorelli, G. L., A. Tocci, R. Botta, F. Facchiano, U. Testa, L. Vitelli, M. Valtieri, C. M. Croce, and C. Peschle. 1997. Ectopic TAL-1/SCL expression in phenotypically normal or leukemic myeloid precursors: proliferative and antiapoptotic effects coupled with a differentiation blockade. Mol. Cell. Biol. 17:2954-2969.
14. Cordle, S. R., E. Henderson, H. Masuoka, P. A. Weil, and R. Stein. 1991. Pancreatic beta-cell-type-specific transcription of the insulin gene is mediated by basic helix-loop-helix DNA-binding proteins. Mol. Cell. Biol. 11: 1734-1738.
15. Cubas, P., J. Modolell, and M. Ruiz-Gomez. 1994. The helix-loop-helix extramacrochaetae protein is required for proper specification of many cell types in the Drosophila embryo. Development 120:2555-2566.
16. Deed, R. W., S. M. Bianchi, G. T. Atherton, D. Johnston, M. Santibanez-Koref, J. J. Murphy, and J. D. Norton. 1993. An immediate early human gene encodes an Id-like helix-loop-helix protein and is regulated by protein kinase C activation in diverse cell types. Oncogene 8:599-607.
17. Deed, R. W., S. Armitage, and J. D. Norton. 1996. Nuclear localization and regulation of Id protein through an E protein-mediated chaperone mechanism. J. Biol. Chem. 271:23603-23606.
18. Desprez, P. Y., E. Hara, M. J. Bissell, and J. Campisi. 1995. Suppression of mammary epithelial cell differentiation by the helix-loop-helix protein Id1. Mol. Cell. Biol. 15:3398-3404.
19. Einarson, M. B., and M. V. Chao, 1995. Regulation of Idl and its association with basic helix-loop-helix proteins during nerve growth factor-induced differentiation of PC12 cells. Mol. Cell. Biol. 15:4175-4183.
20. Ellis, H. M., D. R. Spann, and J. W. Posakony. 1990. Extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of helix-loop-helix proteins. Cell 61:27-38.
21. Ellmeier, W., A. Aguzzi, E. Kleiner, R. Kurzbauer, and A. Weith. 1992. A mutually exclusive expression of a helix-loop-helix gene and N-myc in human neuroblastomas and in normal development. EMBO J. 11:2563-2571.
22. 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.
23. Fanidi, A., E. A. Harrington, and G. I. Evan. 1992. Cooperative interaction between c-myc and bcl-2 proto-oncogenes. Nature 359:554-556.
24. 23a.Florio, M. Unpublished data.
25. Garrell, J., and J. Modolell. 1990. The Drosophila extramacrochaetae locus, an antagonist of proneural genes that, like these genes, encode a helix-loop-helix protein. Cell 61:39-48.
26. Gavrieli, Y., Y. Sherman, and S. A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:443-501.
27. Gossen, M., S. Freundlieh. G. Bender, G. Muller, W. Hillen, and H. Bujard. 1995. Transcriptional activation by telracyclines in mammalian cells. Science 268:1766-1769.
28. Haas-Kogan, D., S. Kogan, D. Levi, P. Dazin, A. T. TAng, Y. Fung, and M. A. Israel. 1995. Inhibition of apoptosis by the retinoblastoma gene product. EMBO J. 14:461-472.
29. 1 progression and are repressed in senescent human fibroblasts. J. Biol. Chem. 269:2139-2145.
30. Hara, E., M. Hall, and G. Peters. 1997. Cdk2-dependent phosphorylation of Id2 modulates activity of E2A-related transcription factors. EMBO J. 16: 332-342.
31. Harrington, E. A., M. R. Bennett, A. Fanidi, and G. I. Evan. 1994. c-mycinduced apoptosis in fibroblasts is inhibited by specific cytokines. EMBO J. 13:3286-3295.
32. 30a.Hernandez, C. Unpublished data.
33. Hiebert, S. W., G. Packham, D. K. Strom, R. Haffner, M. Oren, G. Zambetti, and J. L. Cleveland. 1995. E2F-1:DP-1 induces p53 and overrides survival factors to trigger apoptosis. Mol. Cell. Biol. 15:6864-6874.
34. Hinds, P. W., and R. A. Weinberg. 1994. Tumor suppressor genes. Curr. Opin. Genet. Dev. 4:135-141.
35. Hsieh J. K., S. Fredersdorf, T. Kouzarides, K. Martin, and X. Lu. 1997. E2F-1-induced apoptosis requires DNA binding but not transactivation and is inhibited by the retinoblastoma protein through direct interaction. Genes Dev. 11:1840-1852.
36. Iavarone, A., P. Garg, A. Lasorella, J. Hsu, and M. A. Israel. 1994. The helix-loop-helix protein Id2 enhances cell proliferation and binds to the retinoblastoma protein. Genes Dev. 8:1270-1284.
37. Ishiguro, A., K. S. Spirin, M. Shiohara, A. Tobler, A. F. Gombart, M. A. Israel, J. D. Norton, and H. P. Koeffler. 1996. Id2 expression increases with differentiation of human myeloid cells. Blood 87:5225-5231.
38. Ishiguro, A., K. Spirin, M. Shiohara, A. Tobler, J. D. Norton, M. Rigolet, T. Shimbo, and H. P. Koeffler. 1995. Expression of Id2 and Id3 mRNA in human lymphocytes. Leuk. Res. 19:989-996.
39. Jen, Y., K. Manova, and R. Benezra. 1996. Expression patterns of Idl. Id2, and Id3 are highly related but distinct from that of Id4 during mouse embryogenesis. Dev. Dyn. 207:235-252.
40. Jen, Y., H. Weintraub, and R. Benezra. 1992. Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of Id with E2A proteins. Genes Dev. 6:1466-1479.
41. Jen, Y., K. Manova, and R. Benezra. 1997. Each member of the Id gene family exhibits a unique expression pattern in mouse gastrulation and neurogenesis. Dev. Dyn. 208:92-106.
42. Kadesch, T. 1993. Consequences of heteromeric interactions among helix-loop-helix proteins. Cell Growth Differ. 4:49-55.
43. Kowalik, T. F., J. Degregori, J. K. Schwarz, and J. R. Nevins. 1995. E2F overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J. Virol. 69:2491-2500.
44. Kreider, B., R. Benezra, G. Rovera, and T. Kadesch. 1992. Inhibition of myeloid differentiation by the helix-loop-helix protein Id. Science 255:1700-1702.
45. Krek, W., G. Xu, and D. Livingston. 1995. Cyclin A-kinase regulation of E2F-1 DNA binding function underlies suppression of an S-phase check-point. Cell 83:1149-1158.
46. Kurabayashi, M., R. Jeyaseelan, and L. Kedes. 1993. Two distinct cDNA sequences encoding the human helix-loop-helix protein Id2. Gene 133:305-306.
47. Lasorella, A., A. Iavarone, and M. A. Israel. 1996. Id2 specifically alters regulation of the cell cycle by tumor suppressor proteins. Mol. Cell. Biol. 16:2570-2578.
48. Le Jossic C., G. P. Ilyin, P. Loyer, D. Glaise, S. Cariou, and C. Guguen-Guillouzo. 1994. Expression of helix-loop-helix factor Id-1 is dependent on the hepatocyte proliferation and differentiation status in rat liver and in primary culture. Cancer Res. 54:6065-6068.
49. Lister, J., W. C. Forrester, and M. H. Barron. 1995. Inhibition of an erythroid differentiation switch by the helix-loop-helix protein Idl. J. Biol. Chem. 270:17939-17946.
50. Littlewood, T. D., and G. I. Evan. 1995. Transcription factors 2: helix-loop-helix. Protein Profile 2:621-702.
51. McLeod, K. F., Y. Hu, and T. Jacks. 1996. Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J. 15:6178-6188.
52. Moldes, ML, F. Lasnier, B. Feve, J. Pairault, and P. Djian. 1997. Id3 prevents differentiation of preadipose cells. Mol. Cell. Biol. 17:1796-1804.
53. Morgen besser, S. IX, B. O. Williams, T. Jacks, and R. A. DePinho. 1904. p53-dependent apoptosis produced by Rb-deficiency in the developing mouse lens. Nature 371:72-74.
54. Murre, C., P. S. McCaw, and D. Baltimore. 1989. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56:777-783.
55. Nicoletti, I., G. Migliorati, M. C. Pagliacci, F. Grignani, and C. Riccardj. 1991. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139: 271-279.
56. Norton, J. D., and G. T. Atherton. 1998. Coupling of cell growth control and apoptosis functions of Id proteins. Mol. Cell. Biol. 18:2371-2381.
57. Paekham, G., C. Porter, and J. L. Cleveland. 1996. c-Mye induces apoptosis and cell cycle progression by separable, yet overlapping pathways. Oncogene 13:461-469.
58. Pan, H., and A. E. Griep. 1994. Altered cell cycle regulation in the lens of HPV-16 Eft or E7 transgenic mice: implications for tumor suppressor gene function in development. Genes Dev. 8:1285-1299.
59. Pesce, S., and R. Benezra. 1993. The loop region of the helix-loop-helix protein Id1 is critical for its dominant negative activity. Mol. Cell. Biol 13:7874-7880.
60. 1 progression by E2A and Id helix-loop-helix proteins. EMBO J. 13:4291-4301.
61. Phillips, A. C., S. Bates, K. M. Ryan, K. Helin, and K. H. Vousden. 1997. Induction of DNA synthesis and apoptosis are separable functions of E2F-1. Genes Dev. 11:1853-1863.
62. Prabhu, S., A. Ignatova, S. T. Park, and X.-H. Sun. 1997. Regulation of the expression of cyclin-dependent kinase inhibitor p21 by E2A and Id proteins, Mol. Cell. Biol. 17:5888-5895.
63. Qin, X. Q., D. M. Livingston, W. G. Kaelin, and P. D. Adams. 1994. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA 91:10918-10922.
64. Riechmann, V., I. Van Cruchten, and F. Sablitzky. 1994. The expression pattern of Id4, a novel dominant negative helix-loop-helix protein, is distinct from Id1, Id2 and Id3. Nucleic Acids Res. 22:749-755.
65. Rodriguez-Tarduchy, G. M., M. Collins, and A. Copez-Rivas. 1990. Regula- tion of apoptosis in interleukin-3-dependent hemopoietic cells by interleukin-3 and calcium ionophores. EMBO J. 9:2997-3002.
66. Rowan, S., R. L. Ludwig, Y. Haupt, S. Bates, X. Lu, M. Oren, and K. M. Vousden. 1996. Specific loss of apoptotic but not cell-cycle arrest function in a human tumor derived p53 mutant. EMBO J. 15:827-838.
67. Rudolph, B., R. Saffrich, J. Zwicker, B. Henglein, R. Muller, W. Ansorge, and M. Eilers. 1996. Activation of cyclin-dependent kinasesby Myc mediates induction of cyclin A, but not apoptosis. EMBO J. 15:3065-3076.
68. Schmitz, G. G., T. Walter, R. Seibl, and C. kessler. 1991. Nonradioactive labeling of oligonucleotides in vitro with the hapten digoxigenin by tailing with terminal transferase. Anal. Biochem. 192:222-231.
69. Shan, B., and W. H. Lee. 1994. Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol. 14:8166-8173.
70. Sheaff, R. J., M. Groudine, M. Gordon, J. Roberts, and B. E. Clurman. 1997. Cyclin E-Cdk2 is a regulator of p27kip1. Genes Dev. 11:1464-1478.
71. Steller, H. 1995. Mechanisms and genes of cellular suicide. Science 267: 1445-1449.
72. Sun, X.-H. 1994. Constitutive expression of the Idl gene impairs mouse B cell development. Cell 79:893-900.
73. Sun, X.-H., N. G. Copeland, N. A. Jenkins, and D. Baltimore. 1991. Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol. Cell. Biol. 11:5603-5611.
74. Szekely, L., E. Uzvolgyi, W.-Q. Jiang, M. Durko, K. G. Wiman, G. Klein, and J. Sumegi. 1991. Subcellular localization of the retinoblastoma protein. Cell Growth Differ. 2:287-295.
75. Wagner, A. J., J. M. Kokontis, and N. Hay. 1994. Myc-mediated apoptosis requires wild-type p53 in a manner independent of cell cycle arrest and the ability of p53 to induce p21(WAF-1/CIP-1). Genes Dev. 8:2817-2830.
76. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
77. Wu, X. W., and A. J. Levine. 1994. P53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA 91:3602-3606.
78. Zacksenhaus, E., Z. Jiang, D. Chung, J. D. Marth, R. A. Phillips, and B. L., Gallie. 1996. pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev. 10:3051-3064.
79. Zhu, W., J. Dahmen, A. Bulfone, M. Rigolet, M. C. Hernandez, W. L. Kuo, L. Puelles, J. L. Rubenstein, and M. A. Israel. 1995. Id gene expression during development and molecular cloning of the human Id-1 gene. Mol. Brain Res. 30:312-326.