The p53-p21-DREAM-CDE/CHR pathway regulates G2/M cell cycle genes

Nucleic Acids Research

Volumn 44, Issue 1, 2016, Pages 164-174

  Fischer, Martin ^a,c   Quaas, Marianne ^a   Steiner, Lydia ^a,b   Engeland, Kurt ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALSENILIN; CELL CYCLE DEPENDENT ELEMENT; CELL CYCLE GENE HOMOLOGY REGION; DOXORUBICIN; MESSENGER RNA; PROTEIN P21; PROTEIN P53; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; CYCLIN DEPENDENT KINASE INHIBITOR 1A; KCNIP3 PROTEIN, HUMAN; KV CHANNEL INTERACTING PROTEIN; PROTEIN BINDING; REPRESSOR PROTEIN;

ARTICLE; BINDING AFFINITY; BUB1 GENE; CCNA2 GENE; CCNB1 GENE; CELL CYCLE ARREST; CHEK2 GENE; DOWN REGULATION; G2 PHASE CELL CYCLE CHECKPOINT; GENE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE TARGETING; HUMAN; IN VITRO STUDY; MELK GENE; MITOSIS; MYBL2 GENE; NONHUMAN; PHYLOGENY; POLDI1 GENE; PRIORITY JOURNAL; PROTEIN BINDING; RAD18 GENE; RAD54L GENE; TUMOR SUPPRESSOR GENE; ANIMAL; BINDING SITE; DNA RESPONSIVE ELEMENT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; PROMOTER REGION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; BINDING SITES; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; G2 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION; HUMANS; KV CHANNEL-INTERACTING PROTEINS; MICE; MITOSIS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRESSOR PROTEINS; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84958184651     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv927     Document Type: Article

References (65)

1. Vousden,K.H. and Prives,C. (2009) Blinded by the light: the growing complexity of p53. Cell, 137, 413-431.
2. Levine,A.J. and Oren,M. (2009) The first 30 years of p53: growing ever more complex. Nat. Rev. Cancer, 9, 749-758.
3. el-Deiry,W.S., Tokino,T., Velculescu,V.E., Levy,D.B., Parsons,R., Trent,J.M., Lin,D., Mercer,W.E., Kinzler,K.W. and Vogelstein,B. (1993) WAF1, a potential mediator of p53 tumor suppression. Cell, 75, 817-825.
4. Spitkovsky,D., Schulze,A., Boye,B. and Jansen-Durr,P. (1997) Down-regulation of cyclin A gene expression upon genotoxic stress correlates with reduced binding of free E2F to the promoter. Cell Growth Differ., 8, 699-710.
5. Azzam,E.I., deToledo,S.M., Pykett,M.J., Nagasawa,H. and Little,J.B. (1997) CDC2 is down-regulated by ionizing radiation in a p53-dependent manner. Cell Growth Differ., 8, 1161-1169.
6. de Toledo,S.M., Azzam,E.I., Keng,P., Laffrenier,S. and Little,J.B. (1998) Regulation by ionizing radiation of CDC2, cyclin A, cyclin B, thymidine kinase, topoisomerase IIalpha, and RAD51 expression in normal human diploid fibroblasts is dependent on p53/p21Waf1. Cell Growth Differ., 9, 887-896.
7. Chang,B.D., Watanabe,K., Broude,E.V., Fang,J., Poole,J.C., Kalinichenko,T.V. and Roninson,I.B. (2000) Effects of p21(Waf1/Cip1/Sdi1) on cellular gene expression: Implications for carcinogenesis, senescence, and age-related diseases. Proc. Natl. Acad. Sci. U.S.A., 97, 4291-4296.
8. Flatt,P.M., Tang,L.J., Scatena,C.D., Szak,S.T. and Pietenpol,J.A. (2000) p53 regulation of G(2) checkpoint is retinoblastoma protein dependent. Mol. Cell Biol., 20, 4210-4223.
9. Gottifredi,V., Karni-Schmidt,O., Shieh,S.S. and Prives,C. (2001) p53 down-regulates CHK1 through p21 and the retinoblastoma protein. Mol. Cell Biol., 21, 1066-1076.
10. Zhu,H., Chang,B.D., Uchiumi,T. and Roninson,I.B. (2002) Identification of promoter elements responsible for transcriptional inhibition of polo-like kinase 1 and topoisomerase IIalpha genes by p21(WAF1/CIP1/SDI1). Cell Cycle, 1, 59-66.
11. Löhr,K., Möritz,C., Contente,A. and Dobbelstein,M. (2003) p21/CDKN1A mediates negative regulation of transcription by p53. J. Biol. Chem., 278, 32507-32516.
12. Shats,I., Milyavsky,M., Tang,X., Stambolsky,P., Erez,N., Brosh,R., Kogan,I., Braunstein,I., Tzukerman,M., Ginsberg,D. et al. (2004) p53-dependent down-regulation of telomerase is mediated by p21waf1. J. Biol. Chem., 279, 50976-50985.
13. Litovchick,L., Sadasivam,S., Florens,L., Zhu,X., Swanson,S.K., Velmurugan,S., Chen,R., Washburn,M.P., Liu,X.S. and DeCaprio,J.A. (2007) Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol. Cell, 26, 539-551.
14. Schmit,F., Korenjak,M., Mannefeld,M., Schmitt,K., Franke,C., von Eyss,B., Gagrica,S., Hanel,F., Brehm,A. and Gaubatz,S. (2007) LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle, 6, 1903-1913.
15. Müller,G.A., Quaas,M., Schümann,M., Krause,E., Padi,M., Fischer,M., Litovchick,L., DeCaprio,J.A. and Engeland,K. (2012) The CHR promoter element controls cell cycle-dependent gene transcription and binds the DREAM and MMB complexes. Nucleic Acids Res., 40, 1561-1578.
16. Mannefeld,M., Klassen,E. and Gaubatz,S. (2009) B-MYB is required for recovery from the DNA damage-induced G2 checkpoint in p53 mutant cells. Cancer Res., 69, 4073-4080.
17. Calvisi,D.F., Simile,M.M., Ladu,S., Frau,M., Evert,M., Tomasi,M.L., Demartis,M.I., Daino,L., Seddaiu,M.A., Brozzetti,S. et al. (2011) Activation of v-Myb avian myeloblastosis viral oncogene homolog-like2 (MYBL2)-LIN9 complex contributes to human hepatocarcinogenesis and identifies a subset of hepatocellular carcinoma with mutant p53. Hepatology, 53, 1226-1236.
18. Sadasivam,S. and DeCaprio,J.A. (2013) The DREAM complex: master coordinator of cell cycle-dependent gene expression. Nat. Rev. Cancer, 13, 585-595.
19. Quaas,M., Müller,G.A. and Engeland,K. (2012) p53 can repress transcription of cell cycle genes through a p21(WAF1/CIP1)-dependent switch from MMB to DREAM protein complex binding at CHR promoter elements. Cell Cycle, 11, 4661-4672.
20. Müller,G.A. and Engeland,K. (2010) The central role of CDE/CHR promoter elements in the regulation of cell cycle-dependent gene transcription. FEBS J., 277, 877-893.
21. Müller,G.A., Wintsche,A., Stangner,K., Prohaska,S.J., Stadler,P.F. and Engeland,K. (2014) The CHR site: definition and genome-wide identification of a cell cycle transcriptional element. Nucleic Acids Res., 42, 10331-10350.
22. Chen,X., Müller,G.A., Quaas,M., Fischer,M., Han,N., Stutchbury,B., Sharrocks,A.D. and Engeland,K. (2013) The forkhead transcription factor FOXM1 controls cell cycle-dependent gene expression through an atypical chromatin binding mechanism. Mol. Cell Biol., 33, 227-236.
23. Fischer,M., Grundke,I., Sohr,S., Quaas,M., Hoffmann,S., Knörck,A., Gumhold,C. and Rother,K. (2013) p53 and cell cycle dependent transcription of kinesin family member 23 (KIF23) is controlled via a CHR promoter element bound by DREAM and MMB complexes. PLoS One, 8, e63187.
24. Fischer,M., Quaas,M., Wintsche,A., Müller,G.A. and Engeland,K. (2014) Polo-like kinase 4 transcription is activated via CRE and NRF1 elements, repressed by DREAM through CDE/CHR sites and deregulated by HPV E7 protein. Nucleic Acids Res., 42, 163-180.
25. 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.
26. Wasner,M., Tschöp,K., Spiesbach,K., Haugwitz,U., Johne,C., Mössner,J., Mantovani,R. and Engeland,K. (2003) Cyclin B1 transcription is enhanced by the p300 coactivator and regulated during the cell cycle by a CHR-dependent repression mechanism. FEBS Lett., 536, 66-70.
27. Liu,N., Lucibello,F.C., Zwicker,J., Engeland,K. and Müller,R. (1996) Cell cycle-regulated repression of B-myb transcription: cooperation of an E2F site with a contiguous corepressor element. Nucleic Acids Res., 24, 2905-2910.
28. Fischer,M., Steiner,L. and Engeland,K. (2014) The transcription factor p53: Not a repressor, solely an activator. Cell Cycle, 13, 3037-3058.
29. Nikulenkov,F., Spinnler,C., Li,H., Tonelli,C., Shi,Y., Turunen,M., Kivioja,T., Ignatiev,I., Kel,A., Taipale,J. et al. (2012) Insights into p53 transcriptional function via genome-wide chromatin occupancy and gene expression analysis. Cell Death. Differ., 19, 1992-2002.
30. Böhlig,L., Friedrich,M. and Engeland,K. (2011) p53 activates the PANK1/miRNA-107 gene leading to downregulation of CDK6 and p130 cell cycle proteins. Nucleic Acids Res., 39, 440-453.
31. Rashi-Elkeles,S., Elkon,R., Shavit,S., Lerenthal,Y., Linhart,C., Kupershtein,A., Amariglio,N., Rechavi,G., Shamir,R. and Shiloh,Y. (2011) Transcriptional modulation induced by ionizing radiation: p53 remains a central player. Mol. Oncol., 5, 336-348.
32. Rozenblatt-Rosen,O., Deo,R.C., Padi,M., Adelmant,G., Calderwood,M.A., Rolland,T., Grace,M., Dricot,A., Askenazi,M., Tavares,M. et al. (2012) Interpreting cancer genomes using systematic host network perturbations by tumour virus proteins. Nature, 487, 491-495.
33. Kracikova,M., Akiri,G., George,A., Sachidanandam,R. and Aaronson,S.A. (2013) A threshold mechanism mediates p53 cell fate decision between growth arrest and apoptosis. Cell Death Differ., 20, 576-588.
34. Goldstein,I., Ezra,O., Rivlin,N., Molchadsky,A., Madar,S., Goldfinger,N. and Rotter,V. (2012) p53, a novel regulator of lipid metabolism pathways. J. Hepatol., 56, 656-662.
35. Siepel,A., Bejerano,G., Pedersen,J.S., Hinrichs,A.S., Hou,M., Rosenbloom,K., Clawson,H., Spieth,J., Hillier,L.W., Richards,S. et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res., 15, 1034-1050.
36. Blanchette,M., Kent,W.J., Riemer,C., Elnitski,L., Smit,A.F., Roskin,K.M., Baertsch,R., Rosenbloom,K., Clawson,H., Green,E.D. et al. (2004) Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res., 14, 708-715.
37. Huang,d.W., Sherman,B.T. and Lempicki,R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
38. Waldman,T., Kinzler,K.W. and Vogelstein,B. (1995) p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res., 55, 5187-5190.
39. Wolter,P., Schmitt,K., Fackler,M., Kremling,H., Probst,L., Hauser,S., Gruss,O.J. and Gaubatz,S. (2012) GAS2L3, a target gene of the DREAM complex, is required for proper cytokinesis and genomic stability. J. Cell Sci., 125, 2393-2406.
40. Jackson,J.G. and Pereira-Smith,O.M. (2006) Primary and compensatory roles for RB family members at cell cycle gene promoters that are deacetylated and downregulated in doxorubicin-induced senescence of breast cancer cells. Mol. Cell. Biol., 26, 2501-2510.
41. Li,B.Q. and Lee,M.Y.W. (2001) Transcriptional regulation of the human DNA polymerase delta catalytic subunit gene POLD1 by p53 tumor suppressor and Sp1. J. Biol. Chem., 276, 29729-29739.
42. Innocente,S.A. and Lee,J.M. (2005) p53 is a NF-Y- and p21-independent, Sp1-dependent repressor of cyclin B1 transcription. FEBS Lett., 579, 1001-1007.
43. Ceribelli,M., Alcalay,M., Vigano,M.A. and Mantovani,R. (2006) Repression of new p53 targets revealed by ChIP on chip experiments. Cell Cycle, 5, 1102-1110.
44. Lipski,R., Lippincott,D.J., Durden,B.C., Kaplan,A.R., Keiser,H.E., Park,J.H. and Levesque,A.A. (2012) p53 Dimers associate with a head-to-tail response element to repress cyclin B transcription. PLoS One, 7, e42615.
45. Jackson,M.W., Agarwal,M.K., Yang,J., Bruss,P., Uchiumi,T., Agarwal,M.L., Stark,G.R. and Taylor,W.R. (2005) p130/p107/p105Rb-dependent transcriptional repression during DNA-damage-induced cell-cycle exit at G2. J. Cell Sci., 118, 1821-1832.
46. Mirza,A., Wu,Q., Wang,L., McClanahan,T., Bishop,W.R., Gheyas,F., Ding,W., Hutchins,B., Hockenberry,T., Kirschmeier,P. et al. (2003) Global transcriptional program of p53 target genes during the process of apoptosis and cell cycle progression. Oncogene, 22, 3645-3654.
47. Banerjee,T., Nath,S. and Roychoudhury,S. (2009) DNA damage induced p53 downregulates Cdc20 by direct binding to its promoter causing chromatin remodeling. Nucleic Acids Res., 37, 2688-2698.
48. Dalvai,M., Mondesert,O., Bourdon,J.C., Ducommun,B. and Dozier,C. (2011) Cdc25B is negatively regulated by p53 through Sp1 and NF-Y transcription factors. Oncogene, 30, 2282-2288.
49. Le Gac,G., Esteve,P.O., Ferec,C. and Pradhan,S. (2006) DNA damage-induced down-regulation of human Cdc25C and Cdc2 is mediated by cooperation between p53 and maintenance DNA (cytosine-5) methyltransferase 1. J. Biol. Chem., 281, 24161-24170.
50. Li,C., Lin,M. and Liu,J. (2004) Identification of PRC1 as the p53 target gene uncovers a novel function of p53 in the regulation of cytokinesis. Oncogene, 23, 9336-9347.
51. Kho,P.S., Wang,Z., Zhuang,L., Li,Y., Chew,J.L., Ng,H.H., Liu,E.T. and Yu,Q. (2004) p53-regulated transcriptional program associated with genotoxic stress-induced apoptosis. J. Biol. Chem., 279, 21183-21192.
52. Wei,C.L., Wu,Q., Vega,V.B., Chiu,K.P., Ng,P., Zhang,T., Shahab,A., Yong,H.C., Fu,Y., Weng,Z. et al. (2006) A global map of p53 transcription-factor binding sites in the human genome. Cell, 124, 207-219.
53. Menendez,D., Nguyen,T.A., Freudenberg,J.M., Mathew,V.J., Anderson,C.W., Jothi,R. and Resnick,M.A. (2013) Diverse stresses dramatically alter genome-wide p53 binding and transactivation landscape in human cancer cells. Nucleic Acids Res., 41, 7286-7301.
54. Schlereth,K., Heyl,C., Krampitz,A.M., Mernberger,M., Finkernagel,F., Scharfe,M., Jarek,M., Leich,E., Rosenwald,A. and Stiewe,T. (2013) Characterization of the p53 cistrome - DNA binding cooperativity dissects p53's tumor suppressor functions. PLoS Genet., 9, e1003726.
55. Rother,K., Kirschner,R., Sänger,K., Böhlig,L., Mössner,J. and Engeland,K. (2007) p53 downregulates expression of the G(1)/S cell cycle phosphatase Cdc25A. Oncogene, 26, 1949-1953.
56. Rother,K., Li,Y.Y., Tschöp,K., Kirschner,R., Müller,G.A., Mössner,J. and Engeland,K. (2007) Expression of cyclin-dependent kinase subunit 1 (Cks1) is regulated during the cell cycle by a CDE/CHR tandem element and is downregulated by p53 but not by p63 or p73. Cell Cycle, 6, 853-862.
57. Rother,K., Dengl,M., Lorenz,J., Tschöp,K., Kirschner,R., Mössner,J. and Engeland,K. (2007) Gene expression of cyclin-dependent kinase subunit Cks2 is repressed by the tumor suppressor p53 but not by the related proteins p63 or p73. FEBS Lett., 581, 1166-1172.
58. Sohr,S. and Engeland,K. (2008) RHAMM is differentially expressed in the cell cycle and downregulated by the tumor suppressor p53. Cell Cycle, 7, 3448-3460.
59. Tabach,Y., Milyavsky,M., Shats,I., Brosh,R., Zuk,O., Yitzhaky,A., Mantovani,R., Domany,E., Rotter,V. and Pilpel,Y. (2005) The promoters of human cell cycle genes integrate signals from two tumor suppressive pathways during cellular transformation. Mol. Syst. Biol., 1, 2005.0022.
60. Schvartzman,J.M., Duijf,P.H., Sotillo,R., Coker,C. and Benezra,R. (2011) Mad2 is a critical mediator of the chromosome instability observed upon Rb and p53 pathway inhibition. Cancer Cell, 19, 701-714.
61. Scian,M.J., Carchman,E.H., Mohanraj,L., Stagliano,K.E., Anderson,M.A., Deb,D., Crane,B.M., Kiyono,T., Windle,B., Deb,S.P. et al. (2008) Wild-type p53 and p73 negatively regulate expression of proliferation related genes. Oncogene, 27, 2583-2593.
62. Barsotti,A.M. and Prives,C. (2009) Pro-proliferative FoxM1 is a target of p53-mediated repression. Oncogene, 28, 4295-4305.
63. Benson,E.K., Mungamuri,S.K., Attie,O., Kracikova,M., Sachidanandam,R., Manfredi,J.J. and Aaronson,S.A. (2014) p53-dependent gene repression through p21 is mediated by recruitment of E2F4 repression complexes. Oncogene, 33, 3959-3969.
64. Klein,D.K., Hoffmann,S., Ahlskog,J.K., O'Hanlon,K., Quaas,M., Larsen,B.D., Rolland,B., Rosner,H.I., Walter,D., Kousholt,A.N. et al. (2015) Cyclin F suppresses B-Myb activity to promote cell cycle checkpoint control. Nat. Commun., 6, 5800.
65. Litovchick,L., Florens,L.A., Swanson,S.K., Washburn,M.P. and DeCaprio,J.A. (2011) DYRK1A protein kinase promotes quiescence and senescence through DREAM complex assembly. Genes Dev., 25, 801-813.