Activation of cyclin-dependent kinases by Myc mediates induction of cyclin A, but not apoptosis

EMBO Journal

Volumn 15, Issue 12, 1996, Pages 3065-3076

  Rudolph, Bettina ^a   Saffrich, Rainer ^b   Zwicker, Jörk ^c   Henglein, Berthold ^d   Müller, Rolf ^c   Ansorge, Wilhelm ^b   Eilers, Martin ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c Inst Molekularbiol/Tumorforsch   (Germany)

^d CNRS   (France)

Author keywords

Apoptosis; c myc; Cell cycle; Cyclin dependent kinases

Indexed keywords

CYCLIN A; CYCLIN DEPENDENT KINASE;

APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE S PHASE; GENE INDUCTION; ONCOGENE MYC; PRIORITY JOURNAL;

EID: 0029888119     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00669.x     Document Type: Article

References (92)

1. Abraham,R.T., Acquarone,M., Andersen,A., Asensi,A., Bellé,R., Berger,F. Bergounioux,C., Brunn,G., Buquet-Fagot,C., Fagot,D., Glab,N., Goudeau,H., Goudeau,M., Guerrier,P., Houghton,P.J., Hendriks,H., Kloareg,B.,Lippai,M., Marie,D., Maro,B., Meijer,L., Mester,J., Mulner-Lorillon,O., Poulet,S.A., Schierenberg,E., Schutte,B., Vaulot,D. and Verlhac,M.H. (1995) Cellular effects of olomoucine, an inhibitor of cyclin-dependent kinases. Biol. Cell, 83, 105-120.
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. Amati,B., Brooks,M.W., Levy,N., Littlewood,T.D., Evan,G.I. and Land,H. (1993a) Oncogenic activity of the c-Myc protein requires dimerization with Max. Cell, 72, 233-245.
4. Amati,B., Littlewood,T.D., Evan,G.I. and Land,H. (1993b) The c-Myc protein induces cell cycle progression and apoptosis through dimerization with Max. EMBO J., 13, 5083-5087.
5. Amin,C., Wagner,A.J. and Hay,N. (1993) Sequence-specific transcriptional activation by Myc and repression by Max. Mol. Cell. Biol., 13, 383-390.
6. 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.
7. 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.
8. Ayer,D.E., Lawrence,Q.A. and Eisenman,R.N. (1995) Mad-Myc transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell, 80, 767-776.
9. Beijersbergen,R.L., Hijmans,E.M., Zhu,L. and Bernards,R. (1994) Interaction of c-Myc with the pRb-related protein p107 results in inhibition of c-Myc-mediated transactivation. EMBO J., 13, 4080-4086.
10. Bello-Fernandez,C., Packham,G. and Cleveland,J.L. (1993) The ornithine decarboxylase gene is a transcriptional target of c-MYC. Proc. Natl Acad. Sci. USA, 90, 7804-7808.
11. Benvenisty,N., Leder,A., Kuo,A. and Leder,P. (1992) An embryonically expressed gene is a target for c-Myc regulation via the c-Myc-binding sequence. Genes Dev. 6, 2513-2524.
12. Berry,M., Metzger,D. and Chambon,P. (1990) Role of the two activating domains of the oestrogen receptor in the cell-type and promotor-context dependent agonistic activity of the anti-oestrogen4-hydroxy-tamoxifen. EMBO J., 9, 2811-2818.
13. Blackwell,T.K., Kretzner,L., Blackwood,E.M., Eisenman,R.N. and Weintraub,H. (1990) Sequence-specific DNA binding by the c-myc protein. Science, 250, 1149-1151.
14. 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.
15. Blackwood,E.M., Lüscher,B. and Eisenman,R.N. (1992) Myc and Max associate in vivo. Genes Dev., 6, 71-80.
16. Danielian,P.S., White,R., Hoare,S.A., Fawell,S.E. and Parker,M.G. (1993) Identification of residues in the estrogen receptor that confer differential sensitivity to estrogen and hydroxytamoxifen. Mol. Endocrinol., 7, 232-240.
17. Debbas,M. and White,E. (1993) Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev, 7, 546-554.
18. 1/S-regulatory genes. Mol. Cell. Biol., 15, 4215-4224.
19. Desbarats,L., Gaubatz,S. and Eilers,M. (1996) Discrimination between different E-box binding proteins at an endogenous target gene of Myc. Genes Dev., 10, 447-460.
20. Deuschle,U., Pepperkok,R., Wang,F.B., Giordano,T.J., McAllister,W.T., Ansorge,W. and Bujard,H. (1989) Regulated expression of foreign genes in mammalian cells under the control of coliphage T3 RNA polymerase and lac repressor. Proc. Natl Acad. Sci. USA, 86, 5400-5404.
21. Dou,Q.P., Levin,A.H., Zhao,S. and Pardee,A.B. (1993) Cyclin E and cyclin A as candidates for the restriction point protein. Cancer Res., 53, 1493-1497.
22. Dulic,V., Kaufmann,W.K., Wilson,S.J., Tlsty,T.D., Lees,E., Harper,J.W., Elledge,S.J. and Reed,S.I. (1994) p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell, 76, 1013-1023.
23. Eilers,M., Picard,D., Yamamoto,K. and Bishop,J.M. (1989) Chimaeras between the MYC oncoprotein and steroid receptors cause hormone-dependent transformation of cells. Nature, 340, 66-68.
24. Eilers,M., Schirm,S. and Bishop,J.M. (1991) The MYC protein activates transcription of the α-prothymosin gene. EMBO J., 10, 133-141.
25. El Deiry,W.S., Harper,J.W., O'Connor,P.M., Velculescu,V.E., Canman, C.E., Jackman,J., Pietenpol,J.A., Burrell,M., Hill,D.E. and Wang,Y. (1994) WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res., 54, 1169-1174.
26. 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.
27. Freytag,S.O. and Geddes,T.J. (1992) Reciprocal regulation of adipogenesis by Myc and C/EBPα. Science, 256, 379-382.
28. Galaktionov,K., Lee,A.K., Eckstein,J., Draetta,G., Meckler,J., Loda,M. and Beach,D. (1995) CDC25 phosphatases as potential human oncogenes. Science, 269, 1575-1577.
29. Gaubatz,S., Meichle,A. and Eilers,M. (1994) An E-box element localized in the first intron mediates regulation of the prothymosin α gene by c-myc. Mol. Cell. Biol., 14, 3853-3862.
30. Gaubatz,S., Imhof,A., Dosch,R., Werner,O., Mitchell,P., Buettner,R. and Eilers,M. (1995) Transcriptional activation by Myc is under negative control by the transcription factor AP-2. EMBO J., 14, 1508-1529.
31. Girard,F., Strausfeld,U., Fernandez,A. and Lamb,N.J. (1991) Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell, 67, 1169-1179.
32. Glab,N., Labidi,H., Qin,L.-X., Trehin,C., Bergounioux,C. and Meijer,L. (1994) Olomoucine an inhibitor of the cdc2/cdk2 kinases, blocks plant cells at the G1 to S and G2 to M cell cycle transitions. FEBS Lett., 353, 207-211.
33. Gu,W., Bhatia,K., Magrath,I.T., Dang,C.V. and Dalla-Favera,R. (1994) Binding and suppression of the Myc transcriptional activation domain by p107. Science, 264, 251-254.
34. Guadagno,T.M., Ohtsubo,M., Roberts,J.M. and Assoian,R.K. (1993) A link between cyclin A expression and adhesion-dependent cell cycle progression. Science, 262, 1572-1575.
35. Hann,S.R., Dixit,M., Sears,R.C. and Sealy,L. (1994) The alternatively initiated c-Myc proteins differentially regulate transcription through a noncanonical DNA-binding site. Genes Dev., 15, 2441-2452.
36. Harrington,E.A., Bennett,M.R., Fanidi,A. and Evan,G.I. (1994) c-Myc-induced apoptosis in fibroblasts is inhibited by specific cytokines. EMBO J., 13, 3286-3295.
37. Henglein,B., Chenivesse,X., Wang,J., Eick,D. and Bréchot,C. (1994) Structure and cell cycle-regulated transcription of the human cyclin A gene. Proc. Natl Acad Sci. USA, 91, 5490-5494.
38. Hermeking,H. and Eick,D. (1994) Myc-induced apoptosis is mediated by p53 protein. Science, 265, 2091-2093.
39. Hermeking,H., Wolf,D.A., Kohlhuber,F., Dickmanns,A., Billeaud,M., Fanning,E. and Eick,D. (1994) Role of c-myc in simian virus 40 large tumor antigen-induced DNA synthesis in quiescent 3T3-L1 mouse fibroblasts. Proc. Natl Acad. Sci. USA, 91, 10412-10416.
40. Hoang,A.T., Cohen,K.J., Barrett,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.
41. Jansen-Dürr,P., Meichle,A., Steiner,P., Pagano,M., Finke,K., Botz,J., Wessbecher,J., Draetta,G. and Eilers,M. (1993) Differential modulation of cyclin gene expression by MYC. Proc. Natl Acad. Sci. USA, 90, 3685-3689.
42. Jiang,W., Kahn,S.M., Zhou,P., Zhang,Y.-J., Cacace,A.M., Infante,A.S., Doi,S., Santella,R.M. and Weinstein,I.B. (1993) Overexpression of cyclin D1 in rat fibroblasts causes abnormalities in growth control, cell cycle progression and gene expression. Oncogene, 8, 3447-3457.
43. Kato,G., Lee,W.M.F., Chen,L. and Dang,C.V. (1992) Max: functional domains and interaction with c-myc. Genes Dev., 6, 81-92.
44. Katz,S., Kowenz-Leutz,E., Müller,C., Meese,K., Ness,S.A. and Leutz,A. (1993) The NF-M transcription factor is related to C/EBP β and plays a role in signal transduction, differentiation and leukemogenesis of avian myelomonocytic cells. EMBO J., 12, 1321-1332.
45. Keath,E.J., Caimi,P.G. and Cole,M.D. (1984) Fibroblast lines expressing activated c-myc oncogenes are tumorigenic in nude mice and syngeneic animals. Cell, 39, 339-348.
46. Kerkhoff,E., Bister,K. and Klempnauer,K.-H. (1991) Sequence-specific DNA-binding by Myc proteins. Proc. Natl Acad. Sci. USA, 88, 4323-4327.
47. Klefstrom,J., Vastrik,I., Saksela,E., Valle,J., Eilers,M. and Alitalo,K. (1994) c-Myc induces cellular susceptibility to the cytotoxic action of TNF-α. EMBO J., 13, 5442-5450.
48. 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.
49. Kretzner,L., Blackwood,E.M. and Eisenmann,R.N. (1992) Myc and Max proteins possess distinct transcriptional activities. Nature, 359, 426-429.
50. Land,H., Parada,L.F. and Weinberg,R.A. (1983) Cellular oncogenes and multistep carcinogenesis. Science, 222, 771-778.
51. Lin,D., Fiscella,M., O'Connor,P.M., Jackman,J., Chen,M., Luo,L.L., Sala,A., Travali,S., Appella,E. and Mercer,W.E. (1994) Constitutive expression of B-myb can bypass p53-induced Waf1/Cip1-mediated G1 arrest. Proc. Natl Acad. Sci. USA, 91, 10079-10083.
52. Littlewood,T.D., Hancock,D.C., Danielian,P.S., Parker,M.G. and Evan,G.I. (1995) A modified oestrogen receptor ligand binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res., 23, 1686-1690.
53. Lovec,H., Sewing,A., Lucibello,F.C., Muller,R. and Moroy,T. (1994) Oncogenic activity of cyclin D1 revealed through cooperation with Ha-ras: link between cell cycle control and malignant transformation. Oncogene, 9, 323-326.
54. Lowe,S.W., Jacks,T., Housman,D.E. and Ruley,H.E. (1994) Abrogation of oncogene-associated apoptosis allows transformation of p53-deficient cells. Proc. Natl Acad. Sci. USA, 91, 2026-2030.
55. Lukas,J., Muller,H., Bartkova,J., Spitkovksy,D., Kjerulff,A.A., Jansen-Dürr,P., Strauss,M. and Bartek,J. (1994) DNA tumor virus oncoproteins and retinoblastoma gene mutations share the ability to relieve the cell's requirement for cyclin D1 function in G1. J. Cell Biol., 125, 625-638.
56. Matsushime,H., Quelle,D.E., Shurtleff,S.A.A., Shibuya,M., Sherr,C.J. and Kato,J.-Y. (1994) D-type cyclin-dependent kinase activity in mammalian cells. Mol. Cell. Biol., 14, 2066-2076.
57. Meichle,A., Philipp,A. and Eilers,M. (1992) The functions of Myc proteins. Biochim. Biophys. Acta, 1114, 129-146.
58. Meijer,L. (1995) Chemical inhibitors of cyclin-dependent kinases. In Meijer,L., Guidet,S. and Tung,H.Y.L. (eds). Progress in Cell Cycle Research. Plenum Press, New York, Vol. 1, in press.
59. 1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. Biol., 14, 2077-2086.
60. Oswald,F., Lovec,H., Möröy,T. and Lipp,M. (1994) E2F-dependent regulation of human MYC: trans-activation by cyclins D1 and A overrides tumour suppressor protein functions. Oncogene, 9, 2029-2036.
61. Packham,G. and Cleveland,J.L. (1994) Ornithine decarboxylase is a mediator of c-Myc-induced apoptosis. Mol. Cell Biol., 14, 5741-5747.
62. Pagano,M., Pepperkok,R., Verde,F., Ansorge,W. and Draetta,G. (1992) Cyclin A is required at two points in the human cell cycle. EMBO J., 11, 961-971.
63. Philipp,A., Schneider,A., Väsrik,I., Finke,K., Xiong,Y., Beach,D., Alitalo,K. and Eilers,M. (1994) Repression of cyclin D1: a novel function of MYC. Mol. Cell. Biol., 14, 4032-4043.
64. Polyak,K., Lee,M.-H., Erdjument-Bromage,H., Koff,A., Roberts,J.M., Tempst,P. and Massague,J. (1994) Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell, 78, 59-66.
65. Prendergast,G.C. and Ziff,E.B. (1991) Methylation-sensitive sequence-specific DNA binding by the c-myc basic region. Science, 251, 186-189.
66. 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.
67. Qin,X.Q., Livingston,D.M., Kaelin,W.G.,Jr 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.
68. Rao,L., Debbas,M., Sabbatini,P., Hockenbery,D., Korsmeyer,S. and White,E. (1992) The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc. Natl Acad. Sci. USA, 89, 7742-7746.
69. Reisman,D., Elkind,N.B., Roy,B., Beamon,J. and Rotter,V. (1993) c-Myc trans-activates the p53 promoter through a required downstream CACGTG motif. Cell Growth Differ., 4, 57-65.
70. Reynisdóttir,I., Polyak,K., Iavarone,A. and Massagué,J. (1995) Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-β. Genes Dev., 9, 1831-1845.
71. Roussel,M.F., Theodoras,A.M., Pagano,M. and Sherr,C.J. (1995) Rescue of defective mitogenic signaling by D-type cyclins. Proc. Natl Acad. Sci. USA, 92, 6837-6841.
72. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, NY.
73. Sawyers,C.L., Callahan,W. and Witte,O.N. (1992) Dominant negative MYC blocks transformation by ABL oncogenes. Cell, 70, 901-910.
74. Schreiber-Agus,N., Chin,L., Chen,K., Torres,R., Rao,C., Guida,P., Skoultchi,A.I. and DePinho,R.A. (1995) An amino-terminal domain of Mxi1 mediates anti-Myconcogenic activity and interacts with a homolog of the yeast transcriptional repressor SIN1. Cell, 80, 777-786.
75. Schulze,A., Zerfass,K., Spitkovsky,D., Middendorp,S., Berges,J., Helin,C., Janssen-Dürr,P. and Henglein,B. (1995) Cell cycle regulation of the cyclin A promoter is mediated by a variant E2F site. Proc. Natl Acad. Sci. USA, 92, 11264-11268.
76. Serrano,M., Hannon,G.J. and Beach,D. (1993) A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature, 366, 704-707.
77. Shan,B. and Lee,W.H. (1994) Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol., 14, 8166-8173.
78. Sklar,M.D., Thompson,E., Welsh,M.J., Lienert,M., Harney,J., Brossman,H.B., Smith,M. and Prochownik,E.V. (1991) Depletion of c-myc with specific antisense sequences reverses the transformed phenotype in ras oncogene-transformed NIH 3T3 cells. Mol. Cell. Biol., 11, 3699-3710.
79. Solomon,D., Philipp,A., Land,H. and Eilers,M. (1995) Expression of cyclin D1 mRNA is not upregulated by Myc in rat fibroblasts. Oncogene. 11, 1893-1897.
80. 1 cyclin/cdk complexes. EMBO J., 14, 4814-4826.
81. Steinman,R.A., Hoffman,B., Iro,A., Guillouf,C., Liebermann,D. A. and El-Houseini,M.E. (1994) Induction of p21 (WAF-1/CIP1) during differentiation. Oncogene, 9, 3389-3396.
82. Stone,J., de Lange,T., Ramsay,G., Jakobovits,E., Bishop,J.M., Varmus,H. and Lee,B. (1987) Definition of regions in human c-myc that are involved in transformation and nuclear localization. Mol. Cell. Biol., 7, 1697-1709.
83. Thalmeier,K., Synovzik,H., Mertz,R., Winnacker,E.-L. and Lipp,M. (1989) Nuclear factor E2F mediates basic transcription and trans-activation by E1A of the human MYC promoter. Genes Dev., 3, 527-536.
84. van den Heuvel,S. and Harlow,E. (1993) Distinct roles for cyclin-dependent kinases in cell cycle control. Science, 262, 2050-2053.
85. Vesely,J., Havlicek,L., Strand,M., Blow,J.J., Donella-Deana,A., Pinna,L., Letham,D.S., Kato,J.Y., Deautivaud,L., Leclerc,S. and Meijer,L. (1994) Inhibition of cyclin-dependent kinases by purine derivatives. Eur. J. Biochem., 224, 771-786.
86. Wagner,A.J., Meyers,C., Laimins,L.A. and Hay,N. (1993a) c-myc induces the expression and activity of ornithine decarboxylase. Cell Growth Differ., 4, 879-883.
87. Wagner,A.J., Small,M.B. and Hay,N. (1993b) Myc-mediated apoptosis is blocked by ectopic expression of Bcl-2. Mol. Cell. Biol., 13, 2432-2440.
88. Wagner,A.J., Kokontis,J.M. and Hay,N. (1994) Myc-mediated apoptosis requires wild-type p53 in a manner independent of cell cycle arrest and the ability of p53 to induce p21Ruiz M.D.M.V.wafl/cipl. Genes Dev., 8, 2817-2830.
89. Wu,X. and Levine,A.J. (1994) p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl Acad. Sci. USA, 91, 3602-3606.
90. Zervos,A.S., Gyuris,J. and Brent,R. (1993) Mxi1, a protein that specifically interacts with Max to bind Myc-Max recognition sites. Cell, 72, 223-232.
91. CIP1-related domain to bind cyclin/cdk2 and regulate interactions with E2F. Genes Dev., 9, 1740-1752.
92. Zwicker,J., Lucibello,F.C., Wolfraim,L.A., Gross,C., Truss,M., Engeland,K. and Müller,R. (1995) Cell cycle-regulation of the cyclin A, cdc25C and cdc2 genes is based on a common mechanism of transcriptional repression. EMBO J., 14, 4514-4522.