The MYC-associated protein CDCA7 is phosphorylated by AKT to regulate MYC-dependent apoptosis and transformation

Molecular and Cellular Biology

Volumn 33, Issue 3, 2013, Pages 498-513

  Montgomery Gill, R ^a   Gabor, Timothy V ^a   Couzens, Amber L ^a   Scheid, Michael P ^a  

^a YORK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DIVISION CONTRON PROTEIN A7; MYC PROTEIN; PROTEIN KINASE B; THREONINE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL TRANSFORMATION; CYTOPLASM; EMBRYO; FIBROBLAST; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION;

14-3-3 PROTEINS; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MYC; RATS; SEQUENCE ALIGNMENT;

EID: 84873035945     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00276-12     Document Type: Article

References (62)

1. Hann SR, Eisenman RN. 1984. Proteins encoded by the human c-myc oncogene: differential expression in neoplastic cells. Mol. Cell. Biol. 4:2486-2497.
2. Meyer N, Kim SS, Penn LZ. 2006. The Oscar-worthy role of Myc in apoptosis. Semin. Cancer Biol. 16:275-287.
3. Meyer N, Penn LZ. 2008. Reflecting on 25 years with MYC. Nat. Rev. Cancer 8:976-990.
4. Oster SK, Ho CSW, Soucie EL, Penn LZ. 2002. The myc oncogene: MarvelouslY Complex. Adv. Cancer Res. 84:81-154.
5. Wolfer A, Ramaswamy S. 2011. MYC and metastasis. Cancer Res. 71: 2034-2037.
6. Wolfer A, Wittner BS, Irimia D, Flavin RJ, Lupien M, Gunawardane RN, Meyer CA, Lightcap ES, Tamayo P, Mesirov JP, Liu XS, Shioda T, Toner M, Loda M, Brown M, Brugge JS, Ramaswamy S. 2010. MYC regulation of a "poor-prognosis" metastatic cancer cell state. Proc. Natl. Acad. Sci. U. S. A. 107:3698-3703.
7. Albihn A, Johnsen JI, Henriksson MA. 2010. MYC in oncogenesis and as a target for cancer therapies. Adv. Cancer Res. 107:163-224.
8. Nilsson JA, Cleveland JL. 2003. Myc pathways provoking cell suicide and cancer. Oncogene 22:9007-9021.
9. Grandori C, Cowley SM, James LP, Eisenman RN. 2000. The Myc/Max/ Mad network and the transcriptional control of cell behavior. Annu. Rev. Cell Dev. Biol. 16:653-699.
10. Soucek L, Evan GI. 2010. The ups and downs of Myc biology. Curr. Opin. Genet. Dev. 20:91-95.
11. Amati B, Littlewood TD, Evan GI, Land H. 1993. The c-Myc protein induces cell cycle progression and apoptosis through dimerization with Max. EMBO J. 12:5083-5087.
12. Born TL, Frost JA, Schonthal A, Prendergast GC, Feramisco JR. 1994. c-Myc cooperates with activated Ras to induce the cdc2 promoter. Mol. Cell. Biol. 14:5710-5718.
13. Coller HA, Grandori C, Tamayo P, Colbert T, Lander ES, Eisenman RN, Golub TR. 2000. Expression analysis with oligonucleotide microar-rays reveals that MYC regulates genes involved in growth, cell cycle, signaling, and adhesion. Proc. Natl. Acad. Sci. U. S. A. 97:3260-3265.
14. Frank SR, Schroeder M, Fernandez P, Taubert S, Amati B. 2001. Binding of c-Myc to chromatin mediates mitogen-induced acetylation of histone H4 and gene activation. Genes Dev. 15:2069-2082.
15. Hanson KD, Shichiri M, Follansbee MR, Sedivy JM. 1994. Effects of c-myc expression on cell cycle progression. Mol. Cell. Biol. 14:5748-5755.
16. Mateyak MK, Obaya AJ, Adachi S, Sedivy JM. 1997. Phenotypes of c-Myc-deficient rat fibroblasts isolated by targeted homologous recombination. Cell Growth Differ. 8:1039-1048.
17. Rudolph B, Saffrich R, Zwicker J, Henglein B, Muller R, Ansorge W, Eilers M. 1996. Activation of cyclin-dependent kinases by Myc mediates induction of cyclin A, but not apoptosis. EMBO J. 15:3065-3076.
18. Askew DS, Ashmun RA, Simmons BC, Cleveland JL. 1991. Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 6:1915-1922.
19. Eischen CM, Roussel MF, Korsmeyer SJ, Cleveland JL. 2001. Bax loss impairs Myc-induced apoptosis and circumvents the selection of p53 mutations during Myc-mediated lymphomagenesis. Mol. Cell. Biol. 21:7653-7662.
20. Evan GI, Wyllie AH, Gilbert CS, Littlewood TD, Land H, Brooks M, Waters CM, Penn LZ, Hancock DC. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69:119-128.
21. Hemann MT, Bric A, Teruya-Feldstein J, Herbst A, Nilsson JA, Cor-don-Cardo C, Cleveland JL, Tansey WP, Lowe SW. 2005. Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature 436:807-811.
22. Hermeking H, Eick D. 1994. Mediation of c-Myc-induced apoptosis by p53. Science 265:2091-2093.
23. Pusapati RV, Rounbehler RJ, Hong S, Powers JT, Yan M, Kiguchi K, McArthur MJ, Wong PK, Johnson DG. 2006. ATM promotes apoptosis and suppresses tumorigenesis in response to Myc. Proc. Natl. Acad. Sci. U. S. A. 103:1446-1451.
24. Qi Y, Gregory MA, Li Z, Brousal JP, West K, Hann SR. 2004. p19ARF directly and differentially controls the functions of c-Myc independently of p53. Nature 431:712-717.
25. Zindy F, Eischen CM, Randle DH, Kamijo T, Cleveland JL, Sherr CJ, Roussel MF. 1998. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 12:2424-2433.
26. Mymryk JS, Shire K, Bayley ST. 1994. Induction of apoptosis by adeno-virus type 5 E1A in rat cells requires a proliferation block. Oncogene 9:1187-1193.
27. Qin XQ, Livingston DM, Kaelin WG, Jr, Adams PD. 1994. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. U. S. A. 91:10918-10922.
28. Rao L, Debbas M, Sabbatini P, Hockenbery D, Korsmeyer S, 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. U. S. A. 89:7742-7746.
29. Wu X, Levine AJ. 1994. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. U. S. A. 91:3602-3606.
30. Bissonnette RP, Echeverri F, Mahboubi A, Green DR. 1992. Apoptotic cell death induced by c-myc is inhibited by bcl-2. Nature 359:552-554.
31. Fanidi A, Harrington EA, Evan GI. 1992. Cooperative interaction betweenc-myc and bcl-2 proto-oncogenes. Nature 359:554-556.
32. Vaux DL, Cory S, Adams JM. 1988. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335:440-442.
33. Kauffmann-Zeh A, Rodriguez-Viciana P, Ulrich E, Gilbert C, Coffer P, Downward J, Evan G. 1997. Suppression of c-Myc-induced apoptosis by Ras signalling through PI(3)K and PKB. Nature 385:544-548.
34. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, Cooper GM, Segal RA, Kaplan DR, Greenberg ME. 1997. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275:661-665.
35. Kennedy SG, Wagner AJ, Conzen SD, Jordan J, Bellacosa A, Tsichlis PN, Hay N. 1997. The PI 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes Dev. 11:701-713.
36. Khwaja A, Rodriguez-Viciana P, Wennstrom S, Warne PH, Downward J. 1997. Matrix adhesion and Ras transformation both activate a phospho-inositide 3-OH kinase and protein kinase B/Akt cellular survival pathway. EMBO J. 16:2783-2793.
37. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241.
38. del Peso L, Gonzalez-Garcia M, Page C, Herrera R, Nunez G. 1997. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278:687-689.
39. She QB, Solit DB, Ye Q, O'Reilly KE, Lobo J, Rosen N. 2005. The BAD protein integrates survival signaling by EGFR/MAPK and PI3K/Akt kinase pathways in PTEN-deficient tumor cells. Cancer Cell 8:287-297.
40. Zundel W, Giaccia A. 1998. Inhibition of the anti-apoptotic PI(3)K/Akt/ Bad pathway by stress. Genes Dev. 12:1941-1946.
41. Bouchard C, Marquardt J, Bras A, Medema RH, Eilers M. 2004. Myc-induced proliferation and transformation require Akt-mediated phosphorylation of FoxO proteins. EMBO J. 23:2830-2840.
42. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868.
43. Brunet A, Kanai F, Stehn J, Xu J, Sarbassova D, Frangioni JV, Dalai SN, DeCaprio JA, Greenberg ME, Yaffe MB. 2002. 14-3-3 transits to the nucleus and participates in dynamic nucleocytoplasmic transport. J. Cell Biol. 156:817-828.
44. Delpuech O, Griffiths B, East P, Essafi A, Lam EW, Burgering B, Downward J, Schulze A. 2007. Induction of Mxi1-SRa by FOXO3a contributes to repression of Myc-dependent gene expression. Mol. Cell. Biol. 27:4917-4930.
45. Singh A, Ye M, Bucur O, Zhu S, Tanya Santos M, Rabinovitz I, Wei W, Gao D, Hahn WC, Khosravi-Far R. 2010. Protein phosphatase 2A reactivates FOXO3a through a dynamic interplay with 14-3-3 and AKT. Mol. Biol. Cell 21:1140-1152.
46. Li J, Simpson L, Takahashi M, Miliaresis C, Myers MP, Tonks N, Parsons R. 1998. The PTEN/MMAC1 tumor suppressor induces cell death that is rescued by the AKT/protein kinase B oncogene. Cancer Res. 58:5667-5672.
47. Stambolic V, Suzuki A, de la Pompa JL, Brothers GM, Mirtsos C, Sasaki T, Ruland J, Penninger JM, Siderovski DP, Mak TW. 1998. Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 95:29-39.
48. Dahia PL, Aguiar RC, Alberta J, Kum JB, Caron S, Sill H, Marsh DJ, Ritz J, Freedman A, Stiles C, Eng C. 1999. PTEN is inversely correlated with the cell survival factor Akt/PKB and is inactivated via multiple mechanisms in haematological malignancies. Hum. Mol. Genet. 8:185-193.
49. Di Cristofano A, Pandolfi PP. 2000. The multiple roles of PTEN in tumor suppression. Cell 100:387-390.
50. Goto Y, Hayashi R, Muramatsu T, Ogawa H, Eguchi I, Oshida Y, Ohtani K, Yoshida K. 2006. JPO1/CDCA7, a novel transcription factor E2F1-induced protein, possesses intrinsic transcriptional regulator activity. Biochim. Biophys. Acta 1759:60-68.
51. Osthus RC, Karim B, Prescott JE, Smith BD, McDevitt M, Huso DL, Dang CV. 2005. The Myc target gene JPO1/CDCA7 is frequently overex-pressed in human tumors and has limited transforming activity in vivo. Cancer Res. 65:5620-5627.
52. Prescott JE, Osthus RC, Lee LA, Lewis BC, Shim H, Barrett JF, Guo Q, Hawkins AL, Griffin CA, Dang CV. 2001. A novel c-Myc-responsive gene, JPO1, participates in neoplastic transformation. J. Biol. Chem. 276: 48276-48284.
53. Huang A, Ho CS, Ponzielli R, Barsyte-Lovejoy D, Bouffet E, Picard D, Hawkins CE, Penn LZ. 2005. Identification of a novel c-Myc protein interactor, JPO2, with transforming activity in medulloblastoma cells. Cancer Res. 65:5607-5619.
54. Skeen JE, Bhaskar PT, Chen CC, Chen WS, Peng XD, Nogueira V, Hahn-Windgassen A, Kiyokawa H, Hay N. 2006. Akt deficiency impairs normal cell proliferation and suppresses oncogenesis in a p53-independent and mTORC1-dependent manner. Cancer Cell 10:269-280.
55. Matitau AE, Scheid MP. 2008. Phosphorylation of MEKK3 at threonine 294 promotes 14-3-3 association to inhibit nuclear factor B activation. J. Biol. Chem. 283:13261-13268.
56. Freeman AK, Morrison DK. 2011. 14-3-3 proteins: diverse functions in cell proliferation and cancer progression. Semin. Cell Dev. Biol. 22:681-687.
57. Wang B, Yang H, Liu YC, Jelinek T, Zhang L, Ruoslahti E, Fu H. 1999. Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 38:12499-12504.
58. Wasylishen AR, Penn LZ. 2010. Myc: the beauty and the beast. Genes Cancer 1:532-541.
59. Efthymiadis A, Shao H, Hubner S, Jans DA. 1997. Kinetic characterization of the human retinoblastoma protein bipartite nuclear localization sequence (NLS) in vivo and in vitro. A comparison with the SV40 large T-antigen NLS. J. Biol. Chem. 272:22134-22139.
60. Moll T, Tebb G, Surana U, Robitsch H, Nasmyth K. 1991. The role of phosphorylation and the CDC28 protein kinase in cell cycleregulated nuclear import of the S. cerevisiae transcription factor SWI5. Cell 66:743-758.
61. Ou XM, Chen K, Shih JC. 2006. Monoamine oxidase A and repressor R1 are involved in apoptotic signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 103:10923-10928.
62. Parisi F, Wirapati P, Naef F. 2007. Identifying synergistic regulation involving c-Myc and sp1 in human tissues. Nucleic Acids Res. 35:1098-1107.