A role for p38 in transcriptional elongation of p21CIP1 in response to Aurora B inhibition

Cell Cycle

Volumn 12, Issue 13, 2013, Pages 2051-2060

  Kumari, Geeta ^a   Ulrich, Tanja ^a   Gaubatz, Stefan ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Aurora B; p21; p38; p53; Transcription elongation

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; AURORA B KINASE; BARASERTIB; DORAMAPIMOD; DOXORUBICIN; MITOGEN ACTIVATED PROTEIN KINASE P38; N [4 [6 METHOXY 7 (3 MORPHOLINOPROPOXY) 4 QUINAZOLINYLAMINO]PHENYL]BENZAMIDE; PROTEIN P21; PROTEIN P53;

ARTICLE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA SYNTHESIS; ENDOREDUPLICATION; ENZYME INHIBITION; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION ELONGATION; UPREGULATION;

EID: 84879742114     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.25100     Document Type: Article

References (39)

1. Carmena M, Ruchaud S, Earnshaw WC. Making the Auroras glow: regulation of Aurora A and B kinase function by interacting proteins. Curr Opin Cell Biol 2009; 21:796-805; PMID:19836940; http://dx.doi.org/10.1016/j.ceb.2009.09.008
2. Vader G, Lens SMA. The Aurora kinase family in cell division and cancer. Biochim Biophys Acta 2008; 1786:60-72; PMID:18662747
3. Ruchaud S, Carmena M, Earnshaw WC. Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 2007; 8:798-812; PMID:17848966; http://dx.doi.org/10.1038/nrm2257
4. Marumoto T, Honda S, Hara T, Nitta M, Hirota T, Kohmura E, et al. Aurora-A kinase maintains the fidelity of early and late mitotic events in HeLa cells. J Biol Chem 2003; 278:51786-95; PMID:14523000; http://dx.doi.org/10.1074/ jbc.M306275200
5. Earnshaw WC, Cooke CA. Analysis of the distribution of the INCENPs throughout mitosis reveals the existence of a pathway of structural changes in the chromosomes during metaphase and early events in cleavage furrow formation. J Cell Sci 1991; 98:443-61; PMID:1860899
6. Vader G, Maia AF, Lens SM. The chromosomal passenger complex and the spindle assembly checkpoint: kinetochore-microtubule error correction and beyond. Cell Div 2008; 3:10; PMID:18507820; http://dx.doi.org/10.1186/1747-1028- 3-10
7. Li X, Sakashita G, Matsuzaki H, Sugimoto K, Kimura K, Hanaoka F, et al. Direct association with inner centromere protein (INCENP) activates the novel chromosomal passenger protein, Aurora-C. J Biol Chem 2004; 279:47201-11; PMID:15316025; http://dx.doi.org/10.1074/jbc.M403029200
8. Gautschi O, Heighway J, Mack PC, Purnell PR, Lara PN Jr., Gandara DR. Aurora kinases as anticancer drug targets. Clin Cancer Res 2008; 14:1639-48; PMID:18347165; http://dx.doi.org/10.1158/1078-0432.CCR-07-2179
9. Boss DS, Beijnen JH, Schellens JHM. Clinical experience with aurora kinase inhibitors: a review. Oncologist 2009; 14:780-93; PMID:19684075; http://dx.doi.org/10.1634/theoncologist.2009-0019
10. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, et al. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol 2003; 161:267-80; PMID:12719470; http://dx.doi.org/10.1083/jcb.200208091
11. Dreier MR, Grabovich AZ, Katusin JD, Taylor WR. Short and long-term tumor cell responses to Aurora kinase inhibitors. Exp Cell Res 2009; 315:1085-99; PMID:19233169; http://dx.doi.org/10.1016/j.yexcr.2009.02.008
12. Gizatullin F, Yao Y, Kung V, Harding MW, Loda M, Shapiro GI. The Aurora kinase inhibitor VX-680 induces endoreduplication and apoptosis preferentially in cells with compromised p53-dependent postmitotic checkpoint function. Cancer Res 2006; 66:7668-77; PMID:16885368; http://dx.doi.org/10.1158/0008-5472.CAN-05- 3353
13. Andreassen PR, Lohez OD, Lacroix FB, Margolis RL. Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1. Mol Biol Cell 2001; 12:1315-28; PMID:11359924
14. Senovilla L, Vitale I, Galluzzi L, Vivet S, Joza N, Younes AB, et al. p53 represses the polyploidization of primary mammary epithelial cells by activating apoptosis. Cell Cycle 2009; 8:1380-5; PMID:19342895; http://dx.doi.org/10.4161/cc.8.9.8305
15. Lanni JS, Jacks T. Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol Cell Biol 1998; 18:1055-64; PMID:9448003
16. Minn AJ, Boise LH, Thompson CB. Expression of Bcl-xL and loss of p53 can cooperate to overcome a cell cycle checkpoint induced by mitotic spindle damage. Genes Dev 1996; 10:2621-31; PMID:8895663; http://dx.doi.org/10.1101/gad.10.20. 2621
17. Gully CP, Velazquez-Torres G, Shin JH, Fuentes-Mattei E, Wang E, Carlock C, et al. Aurora B kinase phosphorylates and instigates degradation of p53. Proc Natl Acad Sci USA 2012; 109:E1513-22; PMID:22611192; http://dx.doi.org/10.1073/ pnas.1110287109
18. Waldman T, Kinzler KW, Vogelstein B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res 1995; 55:5187-90; PMID:7585571
19. Thompson SL, Compton DA. Proliferation of aneuploid human cells is limited by a p53-dependent mechanism. J Cell Biol 2010; 188:369-81; PMID:20123995; http://dx.doi.org/10.1083/jcb.200905057
20. Kuma Y, Sabio G, Bain J, Shpiro N, Márquez R, Cuenda A. BIRB796 inhibits all p38 MAPK isoforms in vitro and in vivo. J Biol Chem 2005; 280:19472-9; PMID:15755732; http://dx.doi.org/10.1074/jbc.M414221200
21. Kim GY, Mercer SE, Ewton DZ, Yan Z, Jin K, Friedman E. The stress-activated protein kinases p38 alpha and JNK1 stabilize p21(Cip1) by phosphorylation. J Biol Chem 2002; 277:29792-802; PMID:12058028; http://dx.doi.org/10.1074/jbc.M201299200
22. Espinosa JM, Verdun RE, Emerson BM. p53 functions through stress- and promoter-specific recruitment of transcription initiation components before and after DNA damage. Mol Cell 2003; 12:1015-27; PMID:14580351; http://dx.doi.org/ 10.1016/S1097-2765(03)00359-9
23. Beckerman R, Donner AJ, Mattia M, Peart MJ, Manley JL, Espinosa JM, et al. A role for Chk1 in blocking transcriptional elongation of p21 RNA during the S-phase checkpoint. Genes Dev 2009; 23:1364-77; PMID:19487575; http://dx.doi.org/10.1101/gad.1795709
24. Gomes NP, Bjerke G, Llorente B, Szostek SA, Emerson BM, Espinosa JM. Gene-specific requirement for P-TEFb activity and RNA polymerase II phosphorylation within the p53 transcriptional program. Genes Dev 2006; 20:601-12; PMID:16510875; http://dx.doi.org/10.1101/gad.1398206
25. Valin A, Ouyang J, Gill G. Transcription factor Sp3 represses expression of p21CIP1 via inhibition of productive elongation by RNA polymerase II. Mol Cell Biol 2013; 33:1582-93; PMID:23401853; http://dx.doi.org/10.1128/MCB.00323- 12
26. Price DH. Poised polymerases: on your mark...get set...go! Mol Cell 2008; 30:7-10; PMID:18406322; http://dx.doi.org/10.1016/j.molcel.2008.03.001
27. Egloff S, Murphy S. Cracking the RNA polymerase II CTD code. Trends Genet 2008; 24:280-8; PMID:18457900; http://dx.doi.org/10.1016/j.tig.2008.03.008
28. Wu L, Ma CA, Zhao Y, Jain A. Aurora B interacts with NIR-p53, leading to p53 phosphorylation in its DNA binding domain and subsequent functional suppression. J Biol Chem 2011; 286:2236-44; PMID:20959462; http://dx.doi.org/10. 1074/jbc.M110.174755
29. Trakala M, Fernández-Miranda G, Pérez de Castro I, Heeschen C, Malumbres M. Aurora B prevents delayed DNA replication and premature mitotic exit by repressing p21 (Cip1). Cell Cycle 2013; 12:1030-41; PMID:23428904; http://dx.doi.org/10.4161/cc.24004
30. Fernández-Miranda G, Trakala M, Martín J, Escobar B, González A, Ghyselinck NB, et al. Genetic disruption of aurora B uncovers an essential role for aurora C during early mammalian development. Development 2011; 138:2661-72; PMID:21613325; http://dx.doi.org/10.1242/dev.066381
31. Proft M, Mas G, de Nadal E, Vendrell A, Noriega N, Struhl K, et al. The stress-activated Hog1 kinase is a selective transcriptional elongation factor for genes responding to osmotic stress. Mol Cell 2006; 23:241-50; PMID:16857590; http://dx.doi.org/10.1016/j.molcel.2006.05.031
32. Simone C, Forcales SV, Hill DA, Imbalzano AN, Latella L, Puri PL. p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nat Genet 2004; 36:738-43; PMID:15208625; http://dx.doi.org/10.1038/ng1378
33. Janssen A, van der Burg M, Szuhai K, Kops GJPL, Medema RH. Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations. Science 2011; 333:1895-8; PMID:21960636; http://dx.doi.org/10.1126/ science.1210214
34. Keen N, Taylor S. Aurora-kinase inhibitors as anticancer agents. Nat Rev Cancer 2004; 4:927-36; PMID:15573114; http://dx.doi.org/10.1038/nrc1502
35. Katayama H, Sen S. Aurora kinase inhibitors as anticancer molecules. Biochim Biophys Acta 2010; 1799:829-39; PMID:20863917; http://dx.doi.org/10. 1016/j.bbagrm.2010.09.004
36. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 1995; 92:9363-7; PMID:7568133; http://dx.doi.org/ 10.1073/pnas.92.20.9363
37. Gagrica S, Hauser S, Kolfschoten I, Osterloh L, Agami R, Gaubatz S. Inhibition of oncogenic transformation by mammalian Lin-9, a pRB-associated protein. EMBO J 2004; 23:4627-38; PMID:15538385; http://dx.doi.org/10.1038/sj. emboj.7600470
38. Lampson MA, Kapoor TM. The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nat Cell Biol 2005; 7:93-8; PMID:15592459; http://dx.doi.org/10.1038/ncb1208
39. Schmit F, Korenjak M, Mannefeld M, Schmitt K, Franke C, von Eyss B, et al. LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 2007; 6:1903-13; PMID:17671431; http://dx.doi.org/10.4161/cc.6.15.4512