Targeted disruption of the MYC antagonist MAD1 inhibits cell cycle exit during granulocyte differentiation

EMBO Journal

Volumn 17, Issue 3, 1998, Pages 774-785

  Foley, Kevin P ^a   McArthur, Grant A ^a   Quéva, Christophe ^a   Hurlin, Peter J ^a   Soriano, Philippe ^a   Eisenman, Robert N ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Cell cycle exit; Granulocyte; MAD1; MYC; Terminal differentiation

Indexed keywords

TRANSCRIPTION FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; BONE MARROW CELL; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; COLONY FORMING UNIT; CONTROLLED STUDY; EMBRYO; GENE DISRUPTION; GENETIC RECOMBINATION; GRANULOCYTE; HOMOZYGOTE; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY;

ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BONE MARROW; BONE MARROW CELLS; CELL CYCLE; CELL DIFFERENTIATION; CELLS, CULTURED; CYTOKINES; DNA-BINDING PROTEINS; FLUOROURACIL; GENES; GRANULOCYTES; HUMANS; MACROPHAGES; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MONOCYTES; MULTIGENE FAMILY; MUTAGENESIS, SITE-DIRECTED; PROTO-ONCOGENE PROTEINS C-MYC; REPRESSOR PROTEINS; SENSITIVITY AND SPECIFICITY;

ANIMALIA;

EID: 0032472914     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.3.774     Document Type: Article

References (82)

1. Alland, L., Muhle, R., Hou, Jr. H., Potes, J., Chin, L., Schreiber-Agus, N. and DePinho, R.A. (1997) Role for N-CoR and histone deacetylase in Sin3-mediated transcriptional repression. Nature, 387, 49-55.
2. Amati, B., Dalton, S., Brooks, M.W., Littlewood, T.D., Evan, G.I. and Land, H. (1992) Transcriptional activation by the human c-Myc oncoprotein in yeast requires interaction with Max. Nature, 359, 423-426.
3. Askew, D.S., Ashmun, R.A., Simmons, B.C. and Cleveland, J.L. (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. Ayer, D.E. and Eisenman, R.N. (1993) A switch from Myc:Max to Mad:Max heterocomplexes accompanies monocyte/macrophage differentiation. Genes Dev., 7, 2110-2119.
5. Ayer, D.E., Kretzner, L. and Eisenman, R.N. (1993) Mad: a heterodimeric partner for Max that antagonizes Myc transcriptional activity. Cell, 72, 211-222.
6. Ayer, D.E., Lawrence, Q.A. and Eisenman, R.N. (1995) Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell, 80, 767-776.
7. Blackwood, E.M. and Eisenman, R.N. (1991) Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc. Science, 251, 1211-1217.
8. Blackwood, E.M., Lüscher, B. and Eisenman, R.N. (1992) Myc and Max associate in vivo. Genes Dev., 6, 71-80.
9. Kip1. Genes Dev., 11, 2335-2346.
10. Cerni, C., Bousset, K., Seelos, C., Burkhardt, H., Henriksson, M. and Lüscher, B. (1995) Differential effects by Mad and Max on transformation by cellular and viral oncoproteins. Oncogene, 11, 587-596.
11. Chen, J., Willingham, T., Margraf, L.R., Schreiber-Agus, N., DePinho, R.A. and Nisen, P.D. (1995) Effects of the MYC oncogene antagonist, MAD, on proliferation, cell cycling and the malignant phenotype of human brain tumor cells. Nature Med., 1, 638-643.
12. Chen, Z., Friedrich, G.A. and Soriano, P. (1994) Transcriptional enhancer factor 1 disruption by a retroviral gene trap leads to heart defects and embryonic lethality in mice. Genes Dev., 8, 2293-2301.
13. Chin, L., Schreiber-Agus, N., Pellicer, I., Chen, K., Lee, H.-W., Dudast, M., Cordon-Cardo, C. and DePinho, R.A. (1995) Contrasting roles for Myc and Mad proteins in cellular growth and differentiation. Proc. Natl Acad. Sci. USA, 92, 8488-8492.
14. Clarke, A.R., Maandag, E.R., van Roon, M., van der Lugt, N.M.T., van der Valk, M., Hooper, M.L., Berns, A. and te Riele, H. (1992) Requirement for a functional Rb-1 gene in murine development. Nature, 359, 328-330.
15. Coppola, J.A. and Cole, M.D. (1986) Constitutive c-myc oncogene expression blocks mouse erythroleukaemia cell differentiation but not commitment. Nature, 320, 760-763.
16. Cultraro, C.M., Bino, T. and Segal, S. (1997) Function of the c-Myc antagonist Mad1 during a molecular switch from proliferation to differentiation. Mol. Cell. Biol., 17, 2353-2359.
17. Delgado, M.D., Lerga, A., Cañelles, M., Ǵmez-Casares, M.T. and León, J. (1995) Differential regulation of Max and role of c-Myc during erythroid and myelomonocytic differentiation of K562 cells. Oncogene, 10, 1659-1665.
18. de Nooij J.C., Letendre, M.A. and Hariharan, I.K. (1996) A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell, 87, 1237-1247.
19. Eilers, M., Schirm, S. and Bishop, J.M. (1991) The MYC protein activates transcription of the α-prothymosin gene. EMBO J., 10, 133-141.
20. Endo, T. and Nadal-Ginard, B. (1986) Transcriptional and posttranscriptional control of c-myc during myogenesis: its mRNA remains inducible in differentiated cells and does not suppress the differentiated phenotype. Mol. Cell. Biol., 6, 1412-1421.
21. 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.
22. 1. Mol. Cell. Biol., 8, 1614-1624.
23. Gandarillas, A. and Watt, F.M. (1995) Changes in expression of members of the fos and jun families and myc network during terminal differentiation of human keratinocytes. Oncogene, 11, 1403-1407.
24. Grandori, C. and Eisenman, R.N. (1997) Myc target genes. Trends Biochem. Sci., 22, 177-181.
25. Hassig, C.A., Fleischer, T.C. Billin, A.N., Schreiber, S.L. and Ayer, D.E. (1997) Histone deacetylase activity is required for full transcriptional repression by mSin3A. Cell, 89, 341-347.
26. 1. Nature, 328, 445-449.
27. Heinzel, T. et al. (1997) A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature, 387, 43-48.
28. Henriksson, M. and Lüscher, B. (1996) Proteins of the Myc network: essential regulators of cell growth and differentiation. Adv. Cancer Res., 68, 109-182.
29. Hurlin, P.J., Foley, K.P. Ayer, D.E., Eisenman, R.N., Hanahan, D. and Arbeit, J.M. (1995a) Regulation of Myc and Mad during epidermal differentiation and HPV-associated tumorigenesis. Oncogene, 11, 2487-2501.
30. Hurlin, P.J., Quéva, C., Koskinen, P.J., Steingrimsson, E., Ayer, D.E., Copeland, N.G., Jenkins, N.A. and Eisenman, R.N. (1995b) Mad3 and Mad4: novel Max-interacting transcriptional repressors that suppress c-myc dependent transformation and are expressed during neural and epidermal differentiation. EMBO J., 14, 5646-5659.
31. Hurlin, P.J., Quéva, C. and Eisenman, R.N. (1997) Mnt, a novel Max-interacting protein is coexpressed with Myc in proliferating cells and mediates repression at Myc binding sites. Genes Dev., 11, 44-58.
32. Jacks, T. Fazeli, A., Schmitt, E.M., Bronson, R.T., Goodell, M.A. and Weinberg, R.A. (1992) Effects of an Rb mutation in the mouse. Nature, 359, 295-300.
33. Jacobsen, K.A., Prasad, V.S., Sidman, C.L. and Osmond, D.G. (1994) Apoptosis and macrophage-mediated deletion of precursor B cells in the bone marrow of Eμ-myc transgenic mice. Blood, 84, 2784-2794.
34. Kelly, K., Cochran, B.H., Stiles, C.D. and Leder, P. (1982) Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor. Cell 35, 603-610.
35. Koskinen, P.J., Ayer, D.E and Eisenman, R.N. (1995) Repression of Myc-Ras cotransformation by Mad is mediated by multiple protein-protein interactions. Cell Growth Differ., 6, 623-629.
36. Kretzner, L., Blackwood, E.M. and Eisenman, R.N. (1992) Myc and Max proteins possess distinct transcriptional activities. Nature, 359, 426-429.
37. Lachman, H.M. and Skoultchi, A.I. (1984) Expression of c-myc changes during differentiation of mouse erythroleukaemia cells. Nature, 310, 592-594.
38. Laherty, C.D., Yang, W.-M., Sun, J.-M., Davie, J.R., Seto, E. and Eisenman, R.N. (1997) Histone deacetylases associated with the mSin3 corepressor mediate Mad transcriptional repression. Cell, 89, 349-356.
39. Lahoz, E.G., Xu, L., Schreiber-Agus, N. and DePinho, R.A. (1994) Suppression of Myc, but not E1a, transformation activity by Max-associated proteins. Mad and Mxil. Proc. Natl Acad. Sci. USA, 91, 5503-5507.
40. Lane, M.E., Sauer, K., Wallace, K., Nung Jan, Y., Lehner, C.F. and Vaessin, H. (1996) Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during Drosophila development. Cell, 87, 1225-1235.
41. Langdon, W.Y., Harris, A.W., Cory, S. and Adams, J.M. (1986) The c-myc oncogene perturbs B lymphocyte development in Eμ-myc transgenic mice. Cell, 47, 11-18.
42. Larsson, L.-G., Pettersson, M., Öberg, F., Nilsson, K. and Lüscher, B. (1994) Expression of mad, mxil, max and c-myc during induced differentiation of hematopoietic cells: opposite regulation of mad and c-myc. Oncogene, 9, 1247-1252.
43. Lee, E.Y.-H.P, Chang, C.-Y., Hu, N., Wang, Y.-C.J., Lai, C.-C., Herrup, K., Lee, W.-H. and Bradley, A. (1992) Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature, 359, 288-294.
44. Lee, E.Y.-H.P., Hu, N., Yuan, S.-S.F., Cox, L.A, Bradley, A., Lee, W.-H. and Herrup, K. (1994) Dual roles of the retinoblastoma protein in cell cycle regulation and neuron differentiation. Genes Dev., 8, 2008-2021.
45. Leonard, M.W., Lim, K.-C. and Engel, J.D. (1993) Expression of the chicken GATA factor family during early erythroid development and differentiation. Development, 119, 519-531.
46. Liu, F., Wu, H.-Y., Wesselschmidt, R., Kornaga, T. and Link, D.C. (1996) Impaired production and increased apoptosis of neutrophils in granulocyte colony-stimulating factor receptor-deficient mice. Immunity, 5, 491-501.
47. Lowell, C.A. and Soriano, P. (1996) Knockouts of Src-family kinases: stiff bones, wimpy T cells, and bad memories. Genes Dev., 10, 1845-1857.
48. Lymboussaki, A., Kaipainen, A., Hatva, E., Västrik, I., Jeskanen, L., Jalkanen, M., Werner, S., Stenbäck, F. and Alitalo, R. (1996) Expression of Mad, an antagonist of Myc oncoprotein function, in differentiating keratinocytes during tumorigenesis of the skin. Br. J. Cancer, 73, 1347-1355.
49. Lyons, A.B. and Parish, C.R. (1994) Determination of lymphocyte division by flow cytometry. J. Immunol. Methods, 171, 131-137.
50. Macleod, K.F., Hu, Y. and Jacks, T. (1996) Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J., 15, 6178-6188.
51. Marcu, K.B., Bossone, S.A. and Patel, A.J. (1992) myc function and regulation. Annu. Rev. Biochem., 61, 809-860.
52. McKenna, S.L. and Cotter, T.G. (1997) Functional aspects of apoptosis in hematopoiesis and consequences of failure. Adv. Cancer Res., 71, 121-164.
53. Meroni, G. et al. (1997) Rox, a novel bHLHZip protein expressed in quiescent cells that heterodimerizes with Max, binds a non-canonical E box and acts as a transcriptional repressor. EMBO J., 16, 2892-2906.
54. Metcalf, D. (1984) The Hemopoietic Colony Stimulating Factors. Elsevier, Amsterdam.
55. Metcalf, D., Lindeman, G.J. and Nicola, N.A. (1995) Analysis of hematopoiesis in max 41 transgenic mice that exhibit sustained elevations of blood granulocytes and monocytes. Blood, 85, 2364-2370.
56. Cip1/WAF1 alters keratinocyte growth and differentiation and promotes ras-tumor progression. Genes Dev., 10, 3065-3075.
57. Molkentin, J.D. and Olson, E.N. (1996) Defining the regulatory networks for muscle development. Curr. Opin. Genet. Dev., 6, 445-453.
58. Morgenbesser, S.D. and DePinho, R.A. (1994) Use of transgenic mice to study myc family gene function in normal mammalian development and in cancer. Semin. Cancer Biol., 5, 21-36.
59. Morgenbesser, S.D., Williams, B.O., Jacks, T. and DePinho, R.A. (1994) p53-dependent apoptosis produced by Rb-deficiency in the developing mouse lens. Nature, 371, 72-74.
60. Morrison, S.J., Shah, N.M and Anderson, D.J. (1997) Regulatory mechanisms in stem cell biology. Cell, 88, 287-298.
61. WAF1 is required for survival of differentiating neuroblastoma cells. Mol. Cell. Biol. 16, 1335-1341.
62. Prendergast, G.C., Lawe, D. and Ziff, E.B. (1991) Association of Myn, the murine homolog of Max, with c-Myc stimulates methylation-sensitive DNA binding and Ras cotransformation. Cell, 65, 395-407.
63. Quéva, C., Hurlin, P.J., Foley, K.P. and Eisenman, R.N. (1998) Sequential expression of the MAD family of transcriptional repressors during differentiation and development. Oncogene, in press.
64. Raff, M.C. (1992) Social controls on cell survival and cell death. Nature, 356, 397-400.
65. Raff, M.C. (1996) Size control: the regulation of cell numbers in animal development. Cell, 86, 173-175.
66. Rao, G. et al. (1996) Mouse Sin3A interacts with and can functionally substitute for the amino-terminal repression domain of the Myc antagonist Mxil. Oncogene, 12, 1165-1172.
67. Roussel, M.F., Ashmun, R.A., Sherr, C.J., Eisenman, R.N. and Ayer, D.E. (1996) Inhibition of cell proliferation by the Mad1 transcriptional repressor. Mol. Cell. Biol., 16, 2796-2801.
68. Sawyers, C.L., Denny, C.T. and Witte, O.N. (1991) Leukemia and the disruption of normal hematopoiesis. Cell, 64, 337-350.
69. -/- muscle cells. Science, 264, 1467-1471.
70. Schreiber-Agus, N., Chin, L., Chen, K., Torres, R., Rao, G., Guida, P., Skoultchi, A.I. and DePinho, R.A. (1995) An amino-terminal domain of Mxil mediates anti-Myc oncogenic activity and interacts with a homolog of the yeast transcriptional repressor SIN3. Cell, 80, 777-786.
71. Sommer, A., Hilfenhaus, S., Menkel, A., Kremmer, E., Seiser, C., Loidl, P. and Lüscher, B. (1997) Cell growth inhibition by the Mad/Max complex through recruitment of histone deacetylase activity. Curr. Biol., 7, 357-365.
72. Soriano, P., Montgomery, C., Geske, R. and Bradley, A. (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell, 64, 693-702.
73. Stanton, B.R., Perkins, A.S., Tessarollo, L., Sassoon, D.A. and Parada, L.F. (1992) Loss of N-myc-function results in embryonic lethality and failure of the epithelial component of the embryo to develop. Genes Dev., 6, 2235-2247.
74. Tsai, S. and Collins, S.J. (1993) A dominant negative retinoic acid receptor blocks neutrophil differentiation at the promyelocyte stage. Proc. Natl Acad. Sci. USA, 90, 7153-7157.
75. Vastrik, I., Kaipainen, A., Penttilä, T.-L., Lymboussakis, A., Alitalo, R., Parvinen, M. and Alitalo, K. (1995) Expression of the mad gene during cell differentiation in vivo and its inhibition of cell growth in vitro. J. Cell Biol., 128, 1197-1208.
76. Wang, J. and Walsh, K. (1996) Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science, 273, 359-361.
77. Westin, E.H. et al. (1982) Expression of cellular homologues of retroviral onc genes in human hematopoietic cells. Proc. Natl Acad. Sci. USA, 79, 2490-2494.
78. Kip2 results in increased apoptosis and delayed differentiation during mouse development. Genes Dev., 11, 973-983.
79. Zacksenhaus, E., Jiang, Z., Chung, D., Marth, J.D., Phillips, R.A. and Gallie, B.L. (1996) pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev., 10, 3051-3064.
80. Zervos, A.S., Gyuris, J. and Brent, R. (1993) Mxil, a protein that specifically interacts with Max to bind Myc-Max recognition sites. Cell, 72, 223-232.
81. KIP2 indicates a role in Beckwith-Wiedeman syndrome. Nature, 387, 151-158.
82. Zhuang, Y., Cheng, P. and Weintraub, H. (1996) B-lymphocyte development is regulated by the combined dosage of three basic helix-loop-helix genes, E2A, E2-2, and HEB. Mol. Cell. Biol., 16, 2898-2905.