The stress-activated protein kinases p38α/β and JNK1/2 cooperate with Chk1 to inhibit mitotic entry upon DNA replication arrest

Cell Cycle

Volumn 11, Issue 19, 2012, Pages 3627-3637

  Llopis, Alba ^a   Salvador, Noelia ^a   Ercilla, Amaia ^a   Guaita Esteruelas, Sandra ^a   Del Barco Barrantes, Ivan ^b   Gupta, Jalaj ^b   Gaestel, Matthias ^d   Davis, Roger J ^e   Nebreda, Angel R ^b,c   Agell, Neus ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^d HANNOVER MEDICAL SCHOOL   (Germany)

^e UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Chk1; Hydroxyurea; JNK; p38; S M checkpoint; SAPK

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 7 HYDROXYSTAUROSPORINE; APHIDICOLIN; ATR PROTEIN; CAFFEINE; CAMPTOTHECIN; CHECKPOINT KINASE 1; DNA; DOXORUBICIN; ETOPOSIDE; HYDROXYUREA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 14; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FLUORESCENCE ACTIVATED CELL SORTING; MAMMAL CELL; MITOSIS; NONHUMAN; SIGNAL TRANSDUCTION;

EID: 84867242371     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.21917     Document Type: Article

References (48)

1. Bartek J, Lukas C, Lukas J. Checking on DNA damage in S phase. Nat Rev Mol Cell Biol 2004; 5:792-804; PMID:15459660; http://dx.doi.org/10.1038/nrm1493.
2. Nyberg KA, Michelson RJ, Putnam CW, Weinert TA. Toward maintaining the genome: DNA damage and replication checkpoints. Annu Rev Genet 2002; 36:617-56; PMID:12429704; http://dx.doi.org/10.1146/annurev.genet.36.060402.113540.
3. Branzei D, Foiani M. Maintaining genome stability at the replication fork. Nat Rev Mol Cell Biol 2010; 11:208-19; PMID:20177396; http://dx.doi.org/ 10.1038/nrm2852.
4. Tourrière H, Pasero P. Maintenance of fork integrity at damaged DNA and natural pause sites. DNA Repair (Amst) 2007; 6:900-13; PMID:17379579; http://dx.doi.org/10.1016/j.dnarep.2007.02.004.
5. Feijoo C, Hall-Jackson C, Wu R, Jenkins D, Leitch J, Gilbert DM, et al. Activation of mammalian Chk1 during DNA replication arrest: a role for Chk1 in the intra-S phase checkpoint monitoring replication origin firing. J Cell Biol 2001; 154:913-23; PMID:11535615; http://dx.doi.org/10.1083/jcb.200104099.
6. Lindqvist A, Rodríguez-Bravo V, Medema RH. The decision to enter mitosis: feedback and redundancy in the mitotic entry network. J Cell Biol 2009; 185:193-202; PMID:19364923; http://dx.doi.org/10.1083/jcb.200812045.
7. Mailand N, Podtelejnikov AV, Groth A, Mann M, Bartek J, Lukas J. Regulation of G(2)/M events by Cdc25A through phosphorylation-dependent modulation of its stability. EMBO J 2002; 21:5911-20; PMID:12411508; http://dx.doi.org/10.1093/emboj/cdf567.
8. Boutros R, Dozier C, Ducommun B. The when and wheres of CDC25 phosphatases. Curr Opin Cell Biol 2006; 18:185-91; PMID:16488126; http://dx.doi.org/10.1016/j.ceb.2006.02.003.
9. Zachos G, Rainey MD, Gillespie DAF. Chk1-deficient tumour cells are viable but exhibit multiple checkpoint and survival defects. EMBO J 2003; 22:713-23; PMID:12554671; http://dx.doi.org/10.1093/emboj/cdg060.
10. Sancar A, Lindsey-Boltz LA, Unsal-Kaçmaz K, Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004; 73:39-85; PMID:15189136; http://dx.doi.org/10.1146/annurev. biochem.73.011303.073723.
11. Paulsen RD, Cimprich KA. The ATR pathway: fine-tuning the fork. DNA Repair (Amst) 2007; 6:953-66; PMID:17531546; http://dx.doi.org/10.1016/j.dnarep. 2007.02.015.
12. Ge XQ, Blow JJ. Chk1 inhibits replication factory activation but allows dormant origin firing in existing factories. J Cell Biol 2010; 191:1285-97; PMID:21173116; http://dx.doi.org/10.1083/jcb.201007074.
13. Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol Cell 2010; 37:492-502; PMID:20188668; http://dx.doi.org/10.1016/j.molcel.2010.01.021.
14. Trenz K, Errico A, Costanzo V. Plx1 is required for chromosomal DNA replication under stressful conditions.EMBO J 2008; 27:876-85; PMID:18309293; http://dx.doi.org/10.1038/emboj.2008.29.
15. Shiloh Y. The ATM-mediated DNA-damage response: taking shape. Trends Biochem Sci 2006; 31:402-10; PMID:16774833; http://dx.doi.org/10.1016/j.tibs. 2006.05.004.
16. Lafarga V, Cuadrado A, Lopez de Silanes I, Bengoechea R, Fernandez-Capetillo O, Nebreda AR. p38 Mitogen-activated protein kinase- and HuR-dependent stabilization of p21(Cip1) mRNA mediates the G(1)/S checkpoint. Mol Cell Biol 2009; 29:4341-51; PMID:19528229; http://dx.doi.org/10.1128/MCB. 00210-09.
17. Manke IA, Nguyen A, Lim D, Stewart MQ, Elia AEH, Yaffe MB. MAPKAP kinase-2 is a cell cycle checkpoint kinase that regulates the G2/M transition and S phase progression in response to UV irradiation. Mol Cell 2005; 17:37-48; PMID:15629715; http://dx.doi.org/10.1016/j.molcel.2004.11.021.
18. Reinhardt HC, Hasskamp P, Schmedding I, Morandell S, van Vugt MA, Wang X, et al. DNA damage activates a spatially distinct late cytoplasmic cell-cycle checkpoint network controlled by MK2-mediated RNA stabilization. Mol Cell 2010; 40:34-49; PMID:20932473; http://dx.doi.org/10.1016/j.molcel.2010.09.018.
19. Nebreda AR, Porras A. p38 MAP kinases: beyond the stress response. Trends Biochem Sci 2000; 25:257-60; PMID:10838561; http://dx.doi.org/10.1016/S0968- 0004(00)01595-4.
20. Bulavin DV, Higashimoto Y, Popoff IJ, Gaarde WA, Basrur V, Potapova O, et al. Initiation of a G2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature 2001; 411:102-7; PMID:11333986; http://dx.doi.org/10.1038/ 35075107.
21. Lemaire M, Froment C, Boutros R, Mondesert O, Nebreda AR, Monsarrat B, et al. CDC25B phosphorylation by p38 and MK-2. Cell Cycle 2006; 5:1649-53; PMID:16861915; http://dx.doi.org/10.4161/cc.5.15.3006.
22. Gutierrez GJ, Tsuji T, Cross JV, Davis RJ, Templeton DJ, Jiang W, et al. JNK-mediated phosphorylation of Cdc25C regulates cell cycle entry and G(2)/M DNA damage checkpoint. J Biol Chem 2010; 285:14217-28; PMID:20220133; http://dx.doi.org/10.1074/jbc.M110.121848.
23. Goss VL, Cross JV, Ma K, Qian Y, Mola PW, Templeton DJ. SAPK/JNK regulates cdc2/cyclin B kinase through phosphorylation and inhibition of cdc25c. Cell Signal 2003; 15:709-18; PMID:12742231; http://dx.doi.org/10.1016/S0898- 6568(03)00009-3.
24. Uchida S, Yoshioka K, Kizu R, Nakagama H, Matsunaga T, Ishizaka Y, et al. Stress-activated mitogen-activated protein kinases c-Jun NH2-terminal kinase and p38 target Cdc25B for degradation. Cancer Res 2009; 69:6438-44; PMID:19638579; http://dx.doi.org/10.1158/0008-5472.CAN-09-0869.
25. Damrot J, Helbig L, Roos WP, Barrantes SQ, Kaina B, Fritz G. DNA replication arrest in response to genotoxic stress provokes early activation of stress-activated protein kinases (SAPK/JNK). J Mol Biol 2009; 385:1409-21; PMID:19109974; http://dx.doi.org/10.1016/j.jmb.2008.12.015.
26. Lee K, Song K. Basal c-Jun N-terminal kinases promote mitotic progression through histone H3 phosphorylation.Cell Cycle 2008; 7:216-21; PMID:18256527; http://dx.doi.org/10.4161/cc.7.2.5155.
27. Oktay K, Buyuk E, Oktem O, Oktay M, Giancotti FG. The c-Jun N-terminal kinase JNK functions upstream of Aurora B to promote entry into mitosis. Cell Cycle 2008; 7:533-41; PMID:18431843; http://dx.doi.org/10.4161/cc.7.4.5660.
28. Schmitt E, Boutros R, Froment C, Monsarrat B, Ducommun B, Dozier C. CHK1 phosphorylates CDC25B during the cell cycle in the absence of DNA damage. J Cell Sci 2006; 119:4269-75; PMID:17003105; http://dx.doi.org/10.1242/jcs.03200.
29. Gutierrez GJ, Tsuji T, Chen M, Jiang W, Ronai ZA. Interplay between Cdh1 and JNK activity during the cell cycle. Nat Cell Biol 2010; 12:686-95; PMID:20581839; http://dx.doi.org/10.1038/ncb2071.
30. Rodríguez-Bravo V, Guaita-Esteruelas S, Salvador N, Bachs O, Agell N. Different S/M checkpoint responses of tumor and non tumor cell lines to DNA replication inhibition. Cancer Res 2007; 67:11648-56; PMID:18089794; http://dx.doi.org/10.1158/0008-5472.CAN-07-3100.
31. Zhao B, Bower MJ, McDevitt PJ, Zhao H, Davis ST, Johanson KO, et al. Structural basis for Chk1 inhibition by UCN-01. J Biol Chem 2002; 277:46609-15; PMID:12244092; http://dx.doi.org/10.1074/jbc.M201233200.
32. Reinhardt HC, Aslanian AS, Lees JA, Yaffe MB. p53-deficient cells rely on ATM- and ATR-mediated checkpoint signaling through the p38MAPK/MK2 pathway for survival after DNA damage. Cancer Cell 2007; 11:175-89; PMID:17292828; http://dx.doi.org/10.1016/j.ccr.2006.11.024.
33. Raman M, Earnest S, Zhang K, Zhao Y, Cobb MH. TAO kinases mediate activation of p38 in response to DNA damage. EMBO J 2007; 26:2005-14; PMID:17396146; http://dx.doi.org/10.1038/sj.emboj.7601668.
34. Brancho D, Tanaka N, Jaeschke A, Ventura JJ, Kelkar N, Tanaka Y, et al. Mechanism of p38 MAP kinase activation in vivo. Genes Dev 2003; 17:1969-78; PMID:12893778; http://dx.doi.org/10.1101/gad.1107303.
35. Ronkina N, Kotlyarov A, Gaestel M. MK2 and MK3 - a pair of isoenzymes? Front Biosci 2008; 13:5511-21; PMID:18508601; http://dx.doi.org/10.2741/3095.
36. Ronkina N, Menon MB, Schwermann J, Arthur JS, Legault H, Telliez JB, et al. Stress induced gene expression: a direct role for MAPKAP kinases in transcriptional activation of immediate early genes. Nucleic Acids Res 2011; 39:2503-18; PMID:21109534; http://dx.doi.org/10.1093/nar/gkq1178.
37. Clifton AD, Young PR, Cohen P. A comparison of the substrate specificity of MAPKAP kinase-2 and MAPKAP kinase-3 and their activation by cytokines and cellular stress. FEBS Lett 1996; 392:209-14; PMID:8774846; http://dx.doi.org/10. 1016/0014-5793(96)00816-2.
38. Borgne A, Meijer L. Sequential dephosphorylation of p34(cdc2) on Thr-14 and Tyr-15 at the prophase/metaphase transition. J Biol Chem 1996; 271:27847-54; PMID:8910383; http://dx.doi.org/10.1074/jbc.271.44.27847.
39. Cuadrado A, Nebreda AR. Mechanisms and functions of p38 MAPK signalling. Biochem J 2010; 429:403-17; PMID:20626350; http://dx.doi.org/10.1042/BJ20100323.
40. Takizawa CG, Morgan DO. Control of mitosis by changes in the subcellular location of cyclin-B1-Cdk1 and Cdc25C. Curr Opin Cell Biol 2000; 12:658-65; PMID:11063929; http://dx.doi.org/10.1016/S0955-0674(00)00149-6.
41. Gavet O, Pines J. Activation of cyclin B1-Cdk1 synchronizes events in the nucleus and the cytoplasm at mitosis.J Cell Biol 2010; 189:247-59; PMID:20404109; http://dx.doi.org/10.1083/jcb.200909144.
42. Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 2009; 9:537-49; PMID:19629069; http://dx.doi.org/10.1038/nrc2694.
43. Tomida T, Takekawa M, O'Grady P, Saito H. Stimulus-specific distinctions in spatial and temporal dynamics of stress-activated protein kinase kinase kinases revealed by a fluorescence resonance energy transfer biosensor. Mol Cell Biol 2009; 29:6117-27; PMID:19737916; http://dx.doi.org/10.1128/MCB.00571-09.
44. Vitale I, Galluzzi L, Castedo M, Kroemer G. Mitotic catastrophe: a mechanism for avoiding genomic instability. Nat Rev Mol Cell Biol 2011; 12:385-92; PMID:21527953; http://dx.doi.org/10.1038/nrm3115.
45. Menon MB, Ronkina N, Schwermann J, Kotlyarov A, Gaestel M. Fluorescence-based quantitative scratch wound healing assay demonstrating the role of MAPKAPK-2/3 in fibroblast migration. Cell Motil Cytoskeleton 2009; 66:1041-7; PMID:19743408; http://dx.doi.org/10.1002/cm.20418.
46. Tournier C, Dong C, Turner TK, Jones SN, Flavell RA, Davis RJ. MKK7 is an essential component of the JNK signal transduction pathway activated by proinflammatory cytokines. Genes Dev 2001; 15:1419-26; PMID:11390361; http://dx.doi.org/10.1101/gad.888501.
47. Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A, et al. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 2000; 288:870-4; PMID:10797012; http://dx.doi.org/10. 1126/science.288.5467.870.
48. Rodríguez-Bravo V, Guaita-Esteruelas S, Florensa R, Bachs O, Agell N. Chk1- and claspin-dependent but ATR/ATM- and Rad17-independent DNA replication checkpoint response in HeLa cells. Cancer Res 2006; 66:8672-9; PMID:16951182; http://dx.doi.org/10.1158/0008-5472.CAN-05-4443.