Cdk1-mediated phosphorylation of human ATF7 at Thr-51 and Thr-53 promotes cell-cycle progression into M phase

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Hasegawa, Hitomi ^a   Ishibashi, Kenichi ^a   Kubota, Shoichi ^a   Yamaguchi, Chihiro ^a   Yuki, Ryuzaburo ^a   Nakajo, Haruna ^a   Eckner, Richard ^b   Yamaguchi, Noritaka ^a   Yokoyama, Kazunari K ^c   Yamaguchi, Naoto ^a  

^a CHIBA UNIVERSITY   (Japan)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR; ACTIVATING TRANSCRIPTION FACTOR 2; ACTIVATING TRANSCRIPTION FACTOR 7; AURORA KINASE; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; THREONINE; UNCLASSIFIED DRUG; ATF2 PROTEIN, HUMAN; ATF7 PROTEIN, HUMAN; PHOSPHOTHREONINE;

ANAPHASE; ARTICLE; CELL COUNT; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CELL STRESS; CONTROLLED STUDY; ENZYME ACTIVATION; GENE SILENCING; HUMAN; HUMAN CELL; INHIBITION KINETICS; MITOSIS; PROPHASE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CELL DIVISION; CHEMISTRY; HELA CELL LINE; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION;

ACTIVATING TRANSCRIPTION FACTOR 2; ACTIVATING TRANSCRIPTION FACTORS; AMINO ACID SEQUENCE; ANAPHASE; AURORA KINASES; CDC2 PROTEIN KINASE; CELL DIVISION; G2 PHASE; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PHOSPHOTHREONINE; PROPHASE;

EID: 84919934979     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116048     Document Type: Article

References (64)

1. Eferl R, Wagner EF (2003) AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 3: 859-868.
2. BreitwieserW, Lyons S, Flenniken AM, Ashton G, Bruder G, et al. (2007) Feedback regulation of p38 activity via ATF2 is essential for survival of embryonic liver cells. Genes Dev 21: 2069-2082.
3. Diring J, Camuzeaux B, Donzeau M, Vigneron M, Rosa-Calatrava M, et al. (2011) A cytoplasmic negative regulator isoform of ATF7 impairs ATF7 and ATF2 phosphorylation and transcriptional activity. PLoS ONE 6: e23351.
4. Walczynski J, Lyons S, Jones N, Breitwieser W (2014) Sensitisation of c-MYC-induced B-lymphoma cells to apoptosis by ATF2. Oncogene 33: 1027-1036.
5. Takeda J, Maekawa T, Sudo T, Seino Y, Imura H, et al. (1991) Expression of the CRE-BP1 transcriptional regulator binding to the cyclic AMP response element in central nervous system, regenerating liver, and human tumors. Oncogene 6: 1009-1014.
6. Goetz J, Chatton B, Mattei MG, Kedinger C (1996) Structure and expression of the ATFa gene. J Biol Chem 271: 29589-29598.
7. Reimold AM, Grusby MJ, Kosaras B, Fries JWU, Mori R, et al. (1996) Chondrodysplasia and neurological abnormalities in ATF-2-deficient mice. Nature 379: 262-265.
8. Maekawa T, Bernier F, Sato M, Nomura S, Singh M, et al. (1999) Mouse ATF-2 null mutants display features of a severe type of meconium aspiration syndrome. J Biol Chem 274: 17813-17819.
9. Gupta S, Campbell D, Derijard B, Davis RJ (1995) Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science 267: 389-393.
10. van Dam H, Wilhelm D, Herr I, Steffen A, Herrlich P, et al. (1995) ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO J 14: 1798-1811.
11. Livingstone C, Patel G, Jones N (1995) ATF-2 contains a phosphorylation-dependent transcriptional activation domain. EMBO J 14: 1785-1797.
12. Ouwens DM, de Ruiter ND, van der Zon GC, Carter AP, Schouten J, et al. (2002) Growth factors can activate ATF2 via a two-step mechanism: phosphorylation of Thr71 through the Ras-MEK-ERK pathway and of Thr69 through RalGDS-Src-p38. EMBO J 21: 3782-3793.
13. Morton S, Davis RJ, Cohen P (2004) Signalling pathways involved in multisite phosphorylation of the transcription factor ATF-2. FEBS Lett 572: 177-183.
14. Lopez-Bergami P, Lau E, Ronai Z (2010) Emerging roles of ATF2 and the dynamic AP1 network in cancer. Nat Rev Cancer 10: 65-76.
15. Yamasaki T, Takahashi A, Pan J, Yamaguchi N, Yokoyama KK (2009) Phosphorylation of activation transcription factor-2 (ATF-2) at serine 121 by protein kinase C controls c-Jun-mediated activation of transcription. J Biol Chem 284: 8567-8581.
16. Camuzeaux B, Diring J, Hamard PJ, Oulad-Abdelghani M, Donzeau M, et al. (2008) p38b2-mediated phosphorylation and sumoylation of ATF7 are mutually exclusive. J Mol Biol 384: 980-991.
17. Gozdecka M, Breitwieser W (2012) The roles of ATF2 (activating transcription factor 2) in tumorigenesis. Biochem Soc Trans 40: 230-234.
18. Lau E, Ronai Z (2012) ATF2- at the crossroad of nuclear and cytosolic functions. J Cell Sci 125: 1-10.
19. Lau E, Kluger H, Varsano T, Lee K, Scheffler I, et al. (2012) PKCe promotes oncogenic functions of ATF2 in the nucleus while blocking its apoptotic function at mitochondria. Cell 148: 543-555.
20. Bhoumik A, Takahashi S, Breitweiser W, Shiloh Y, Jones N, et al. (2005) ATM-dependent phosphorylation of ATF2 is required for the DNA damage response. Mol Cell 18: 577-587.
21. Bhoumik A, Lopez-Bergami P, Ronai Z (2007) ATF2 on the double - activating transcription factor and DNA damage response protein. Pigment Cell Res 20: 498-506.
22. Clute P, Pines J (1999) Temporal and spatial control of cyclin B1 destruction in metaphase. Nat Cell Biol 1: 82-87.
23. Chow JPH, Siu WY, Ho HTB, Ma KHT, Ho CC, et al. (2003) Differential contribution of inhibitory phosphorylation of CDC2 and CDK2 for unperturbed cell cycle control and DNA integrity checkpoints. J Biol Chem 278: 40815-40828.
24. Kuga T, Nakayama Y, Hoshino M, Higashiyama Y, Obata Y, et al. (2007) Differential mitotic activation of endogenous c-Src, c-Yes, and Lyn in HeLa cells. Arch Biochem Biophys 466: 116-124.
25. Aoyama K, Yuki R, Horiike Y, Kubota S, Yamaguchi N, et al. (2013) Formation of long and winding nuclear F-actin bundles by nuclear c-Abl tyrosine kinase. Exp Cell Res 319: 3251-3268.
26. Nakayama Y, Matsui Y, Takeda Y, Okamoto M, Abe K, et al. (2012) c-Src but not Fyn promotes proper spindle orientation in early prometaphase. J Biol Chem 287: 24905-24915.
27. Fukumoto Y, Obata Y, Ishibashi K, Tamura N, Kikuchi I, et al. (2010) Cost-effective gene transfection by DNA compaction at pH 4.0 using acidified, long shelf-life polyethylenimine. Cytotechnology 62: 73-82.
28. Yuan Z, Gong S, Luo J, Zheng Z, Song B, et al. (2009) Opposing roles for ATF2 and c-Fos in c-Junmediated neuronal apoptosis. Mol Cell Biol 29: 2431-2442.
29. Song B, Xie B, Wang C, Li M (2011) Caspase-3 is a target gene of c-Jun: ATF2 heterodimers during apoptosis induced by activity deprivation in cerebellar granule neurons. Neurosci Lett 505: 76-81.
30. Kubota S, Fukumoto Y, Ishibashi K, Soeda S, Kubota S, et al. (2014) Activation of the pre-replication complex is blocked by mimosine through reactive oxygen species-activated Ataxia telangiectasia mutated (ATM) protein without DNA damage. J Biol Chem 289: 5730-5746.
31. Knehr M, Poppe M, Enulescu M, Eickelbaum W, Stoehr M, et al. (1995) A critical appraisal of synchronization methods applied to achieve maximal enrichment of HeLa cells in specific cell cycle phases. Exp Cell Res 217: 546-553.
32. Kasahara K, Nakayama Y, Nakazato Y, Ikeda K, Kuga T, et al. (2007) Src signaling regulates completion of abscission in cytokinesis through ERK/MAPK activation at the midbody. J Biol Chem 282: 5327-5339.
33. Matsui Y, Nakayama Y, Okamoto M, Fukumoto Y, Yamaguchi N (2012) Enrichment of cell populations in metaphase, anaphase, and telophase by synchronization using nocodazole and blebbistatin: a novel method suitable for examining dynamic changes in proteins during mitotic progression. Eur J Cell Biol 91: 413-419.
34. Takahashi A, Obata Y, Fukumoto Y, Nakayama Y, Kasahara K, et al. (2009) Nuclear localization of Src-family tyrosine kinases is required for growth factor-induced euchromatinization. Exp Cell Res 315: 1117-1141.
35. Pan J, Nakade K, Huang YC, Zhu ZW, Masuzaki S, et al. (2010) Suppression of cell-cycle progression by Jun dimerization protein-2 (JDP2) involves downregulation of cyclin-A2. Oncogene 29: 6245-6256.
36. Tanigawa S, Lee CH, Lin CS, Ku CC, Hasegawa H, et al. (2013) Jun dimerization protein 2 is a critical component of the Nrf2/MafK complex regulating the response to ROS homeostasis. Cell Death Dis 4: e921.
37. Kasahara K, Nakayama Y, Ikeda K, Fukushima Y, Matsuda D, et al. (2004) Trafficking of Lyn through the Golgi caveolin involves the charged residues on aE and aI helices in the kinase domain. J Cell Biol 165: 641-652.
38. Sato I, Obata Y, Kasahara K, Nakayama Y, Fukumoto Y, et al. (2009) Differential trafficking of Src, Lyn, Yes and Fyn is specified by the state of palmitoylation in the SH4 domain. J Cell Sci 122: 965-975.
39. Ishibashi K, Fukumoto Y, Hasegawa H, Abe K, Kubota S, et al. (2013) Nuclear ErbB4 signaling through H3K9me3 is antagonized by EGFR-activated c-Src. J Cell Sci 126: 625-637.
40. Kubota S, Fukumoto Y, Aoyama K, Ishibashi K, Yuki R, et al. (2013) Phosphorylation of KRABassociated protein 1 (KAP1) at Tyr-449, Tyr-458, and Tyr-517 by nuclear tyrosine kinases inhibits the association of KAP1 and heterochromatin protein 1α (HP1α) with heterochromatin. J Biol Chem 288: 17871-17883.
41. Maekawa T, Kim S, Nakai D, Makino C, Takagi T, et al. (2010) Social isolation stress induces ATF-7 phosphorylation and impairs silencing of the 5-HT 5B receptor gene. EMBO J 29: 196-208.
42. Hsu JY, Sun ZW, Li X, Reuben M, Tatchell K, et al. (2000) Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102: 279-291.
43. Giet R, Glover DM (2001) Drosophila Aurora B kinase is required for histone H3 phosphorylation and condensing recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J Cell Biol 152: 669-682.
44. Crosio C, Fimia GM, Loury R, Kimura M, Okano Y, et al. (2002) Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian aurora kinases. Mol Cell Biol 22: 874-885.
45. Ruchaud S, Carmena M, Earnshaw WC (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8: 798-812.
46. Li XY, Green MR (1996) Intramolecular inhibition of activating transcription factor-2 function by its DNAbinding domain. Genes Dev 10: 517-527.
47. Benbrook DM, Jones NC (1990) Heterodimer formation between CREB and JUN proteins. Oncogene 5: 295-302.
48. Chatton B, Bocco JL, Gaire M, Hauss C, Reimund B, et al. (1993) Transcriptional activation by the adenovirus larger E1a product is mediated by members of the cellular transcription factor ATF family which can directly associate with E1a. Mol Cell Biol 13: 561-570.
49. Kawasaki H, Song J, Eckner R, Ugai H, Chiu R, et al. (1998) p300 and ATF-2 are components of the DRF complex, which regulates retinoic acid- and E1A-mediated transcription of the c-jun gene in F9 cells. Genes Dev 12: 233-245.
50. de Graeve F, Bahr A, Sabapathy KT, Hauss C, Wagner EF, et al. (1999) Role of the ATFa/JNK2 complex in Jun activation. Oncogene 18: 3491-3500.
51. Jin C, Ugai H, Song J, Murata T, Nili F, et al. (2001) Identification of mouse Jun dimerization protein 2 as a novel repressor of ATF-2. FEBS Lett 489: 34-41.
52. Hamard PJ, Dalbies-Tran R, Hauss C, Davidson I, Kedinger C, et al. (2005) A functional interaction between ATF7 and TAF12 that is modulated by TAF4. Oncogene 24: 3472-3483.
53. Nigg EA (2001) Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2: 21-32.
54. Pines J, Rieder CL (2001) Re-staging mitosis: a contemporary view of mitotic progression. Nat Cell Biol 3: E3-E6.
55. Newman JRS, Keating AE (2003) Comprehensive identification of human bZIP interactions with coiledcoil arrays. Science 300: 2097-2101.
56. Fuchs SY, Ronai Z (1999) Ubiquitination and degradation of ATF2 are dimerization dependent. Mol Cell Biol 19: 3289-3298.
57. Fuchs SY, Tappin I, Ronai Z (2000) Stability of the ATF2 transcription factor is regulated by phosphorylation and dephosphorylation. J Biol Chem 275: 12560-12564.
58. Barr AR, Gergely F (2007) Aurora-A: the maker and breaker of spindle poles. J Cell Sci 120: 2987-2996.
59. Marumoto T, Honda S, Hara T, Nitta M, Hirota T, et al. (2003) Aurora-A kinase maintains the fidelity of early and late mitotic events in HeLa cells. J Biol Chem 278: 51786-51795.
60. Hirota T, Kunitoku N, Sasayama T, Marumoto T, Zhang D, et al. (2003) Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell 114: 585-598.
61. de Castro IP, de Cárcer G, Montoya G, Malumbres M (2008) Emerging cancer therapeutic opportunities by inhibiting mitotic kinases. Curr Opin Pharmacol 8: 375-383.
62. Marumoto T, Hirota T, Morisaki T, Kunitoku N, Zhang D, et al. (2002) Roles of aurora-A kinase in mitotic entry and G2 checkpoint in mammalian cells. Genes Cells 7: 1173-1182.
63. Acquaviva C, Pines J (2006) The anaphase-promoting complex/cyclosome: APC/C. J Cell Sci 119: 2401-2404.
64. Bassermann F, Eichner R, Pagano M (2014) The ubiquitin proteasome system-implications for cell cycle control and the targeted treatment of cancer. Biochim Biophys Acta 1843: 150-162.