14-3-3 proteins as signaling integration points for cell cycle control and apoptosis

Seminars in Cell and Developmental Biology

Volumn 22, Issue 7, 2011, Pages 688-695

  Gardino, Alexandra K ^a,b   Yaffe, Michael B ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

14 3 3; Apoptosis; Cell cycle checkpoint; DNA damage; Mitosis; Signal transduction

Indexed keywords

PROTEIN 14 3 3; PROTEIN BCL 2; PROTEIN KINASE; TRANSCRIPTION FACTOR;

APOPTOSIS; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; FEEDBACK SYSTEM; LIGAND BINDING; MITOSIS; NONHUMAN; PHENOTYPE; PROTEIN BINDING; REVIEW;

EID: 80455160346     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2011.09.008     Document Type: Review

References (123)

1. Yaffe M.B., Rittinger K., Volinia S., Caron P.R., Aitken A., Leffers H., et al. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 1997, 91:961-971.
2. Johnson C., Crowther S., Stafford M.J., Campbell D.G., Toth R., MacKintosh C. Bioinformatic and experimental survey of 14-3-3-binding sites. Biochem J 2010, 427:69-78.
3. Rittinger K., Budman J., Xu J., Volinia S., Cantley L.C., Smerdon S.J., et al. Structural analysis of 14-3-3 phosphopeptide complexes identifies a dual role for the nuclear export signal of 14-3-3 in ligand binding. Mol Cell 1999, 4:153-166.
4. Coblitz B., Shikano S., Wu M., Gabelli S.B., Cockrell L.M., Spieker M., et al. C-terminal recognition by 14-3-3 proteins for surface expression of membrane receptors. J Biol Chem 2005, 280:36263-36272.
5. Pines J. Four-dimensional control of the cell cycle. Nat Cell Biol 1999, 1:E73-E79.
6. Boutros R., Lobjois V., Ducommun B. CDC25 phosphatases in cancer cells: key players? Good targets?. Nat Rev Cancer 2007, 7:495-507.
7. Donzelli M., Draetta G.F. Regulating mammalian checkpoints through Cdc25 inactivation. EMBO Rep 2003, 4:671-677.
8. Elia A.E., Rellos P., Haire L.F., Chao J.W., Ivins F.J., Hoepker K., et al. The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell 2003, 115:83-95.
9. Karaiskou A., Cayla X., Haccard O., Jessus C., Ozon R. MPF amplification in Xenopus oocyte extracts depends on a two-step activation of cdc25 phosphatase. Exp Cell Res 1998, 244:491-500.
10. Toyoshima-Morimoto F., Taniguchi E., Nishida E. Plk1 promotes nuclear translocation of human Cdc25C during prophase. EMBO Rep 2002, 3:341-348.
11. Gabrielli B.G., De Souza C.P., Tonks I.D., Clark J.M., Hayward N.K., Ellem K.A. Cytoplasmic accumulation of cdc25B phosphatase in mitosis triggers centrosomal microtubule nucleation in HeLa cells. J Cell Sci 1996, 109(Pt 5):1081-1093.
12. Karlsson C., Katich S., Hagting A., Hoffmann I., Pines J. Cdc25B and Cdc25C differ markedly in their properties as initiators of mitosis. J Cell Biol 1999, 146:573-584.
13. Nishijima H., Nishitani H., Seki T., Nishimoto T. A dual-specificity phosphatase Cdc25B is an unstable protein and triggers p34(cdc2)/cyclin B activation in hamster BHK21 cells arrested with hydroxyurea. J Cell Biol 1997, 138:1105-1116.
14. Donzelli M., Squatrito M., Ganoth D., Hershko A., Pagano M., Draetta G.F. Dual mode of degradation of Cdc25 A phosphatase. EMBO J 2002, 21:4875-4884.
15. Molinari M., Mercurio C., Dominguez J., Goubin F., Draetta G.F. Human Cdc25 A inactivation in response to S phase inhibition and its role in preventing premature mitosis. EMBO Rep 2000, 1:71-79.
16. Lee G., White L.S., Hurov K.E., Stappenbeck T.S., Piwnica-Worms H. Response of small intestinal epithelial cells to acute disruption of cell division through CDC25 deletion. Proc Natl Acad Sci U S A 2009, 106:4701-4706.
17. Elia A.E., Cantley L.C., Yaffe M.B. Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 2003, 299:1228-1231.
18. Hoffmann I., Clarke P.R., Marcote M.J., Karsenti E., Draetta G. Phosphorylation and activation of human cdc25-C by cdc2-cyclin B and its involvement in the self-amplification of MPF at mitosis. EMBO J 1993, 12:53-63.
19. Izumi T., Maller J.L. Elimination of cdc2 phosphorylation sites in the cdc25 phosphatase blocks initiation of M-phase. Mol Biol Cell 1993, 4:1337-1350.
20. Wang R., He G., Nelman-Gonzalez M., Ashorn C.L., Gallick G.E., Stukenberg P.T., et al. Regulation of Cdc25C by ERK-MAP kinases during the G2/M transition. Cell 2007, 128:1119-1132.
21. Bartek J., Lukas J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 2003, 3:421-429.
22. Reinhardt H.C., Yaffe M.B. Kinases that control the cell cycle in response to DNA damage: Chk1, Chk2, and MK2. Curr Opin Cell Biol 2009, 21:245-255.
23. Kumagai A., Yakowec P.S., Dunphy W.G. 14-3-3 proteins act as negative regulators of the mitotic inducer Cdc25 in Xenopus egg extracts. Mol Biol Cell 1998, 9:345-354.
24. Peng C.Y., Graves P.R., Thoma R.S., Wu Z., Shaw A.S., Piwnica-Worms H. Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 1997, 277:1501-1505.
25. Giles N., Forrest A., Gabrielli B. 14-3-3 acts as an intramolecular bridge to regulate cdc25B localization and activity. J Biol Chem 2003, 278:28580-28587.
26. Zeng Y., Forbes K.C., Wu Z., Moreno S., Piwnica-Worms H., Enoch T. Replication checkpoint requires phosphorylation of the phosphatase Cdc25 by Cds1 or Chk1. Nature 1998, 395:507-510.
27. Davezac N., Baldin V., Gabrielli B., Forrest A., Theis-Febvre N., Yashida M., et al. Regulation of CDC25B phosphatases subcellular localization. Oncogene 2000, 19:2179-2185.
28. Graves P.R., Lovly C.M., Uy G.L., Piwnica-Worms H. Localization of human Cdc25C is regulated both by nuclear export and 14-3-3 protein binding. Oncogene 2001, 20:1839-1851.
29. Kumagai A., Dunphy W.G. Binding of 14-3-3 proteins and nuclear export control the intracellular localization of the mitotic inducer Cdc25. Genes Dev 1999, 13:1067-1072.
30. Lopez-Girona A., Furnari B., Mondesert O., Russell P. Nuclear localization of Cdc25 is regulated by DNA damage and a 14-3-3 protein. Nature 1999, 397:172-175.
31. Forrest A., Gabrielli B. Cdc25B activity is regulated by 14-3-3. Oncogene 2001, 20:4393-4401.
32. Ogg S., Gabrielli B., Piwnica-Worms H. Purification of a serine kinase that associates with and phosphorylates human Cdc25C on serine 216. J Biol Chem 1994, 269:30461-30469.
33. Yang J., Winkler K., Yoshida M., Kornbluth S. Maintenance of G2 arrest in the Xenopus oocyte: a role for 14-3-3-mediated inhibition of Cdc25 nuclear import. EMBO J 1999, 18:2174-2183.
34. Dalal S.N., Yaffe M.B., DeCaprio J.A. 14-3-3 family members act coordinately to regulate mitotic progression. Cell Cycle 2004, 3:672-677.
35. Wilker E.W., Grant R.A., Artim S.C., Yaffe M.B. A structural basis for 14-3-3sigma functional specificity. J Biol Chem 2005, 280:18891-18898.
36. Mils V., Baldin V., Goubin F., Pinta I., Papin C., Waye M., et al. Specific interaction between 14-3-3 isoforms and the human CDC25B phosphatase. Oncogene 2000, 19:1257-1265.
37. Lee J., Kumagai A., Dunphy W.G. Positive regulation of Wee1 by Chk1 and 14-3-3 proteins. Mol Biol Cell 2001, 12:551-563.
38. Rothblum-Oviatt C.J., Ryan C.E., Piwnica-Worms H. 14-3-3 binding regulates catalytic activity of human Wee1 kinase. Cell Growth Differ 2001, 12:581-589.
39. Benzinger A., Popowicz G.M., Joy J.K., Majumdar S., Holak T.A., Hermeking H. The crystal structure of the non-liganded 14-3-3sigma protein: insights into determinants of isoform specific ligand binding and dimerization. Cell Res 2005, 15:219-227.
40. Chan T.A., Hermeking H., Lengauer C., Kinzler K.W., Vogelstein B. 14-3-3Sigma is required to prevent mitotic catastrophe after DNA damage. Nature 1999, 401:616-620.
41. Chan T.A., Hwang P.M., Hermeking H., Kinzler K.W., Vogelstein B. Cooperative effects of genes controlling the G(2)/M checkpoint. Genes Dev 2000, 14:1584-1588.
42. Hermeking H. The 14-3-3 cancer connection. Nat Rev Cancer 2003, 3:931-943.
43. Hermeking H., Lengauer C., Polyak K., He T.C., Zhang L., Thiagalingam S., et al. 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol Cell 1997, 1:3-11.
44. Laronga C., Yang H.Y., Neal C., Lee M.H. Association of the cyclin-dependent kinases and 14-3-3 sigma negatively regulates cell cycle progression. J Biol Chem 2000, 275:23106-23112.
45. Lee M.H., Lozano G. Regulation of the p53-MDM2 pathway by 14-3-3 sigma and other proteins. Semin Cancer Biol 2006, 16:225-234.
46. Yang H., Zhang Y., Zhao R., Wen Y.Y., Fournier K., Wu H.B., et al. Negative cell cycle regulator 14-3-3sigma stabilizes p27 Kip1 by inhibiting the activity of PKB/Akt. Oncogene 2006, 25:4585-4594.
47. Fujita N., Sato S., Katayama K., Tsuruo T. Akt-dependent phosphorylation of p27Kip1 promotes binding to 14-3-3 and cytoplasmic localization. J Biol Chem 2002, 277:28706-28713.
48. Manke I.A., Nguyen A., Lim D., Stewart M.Q., Elia A.E., Yaffe M.B. 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.
49. Reinhardt H.C., Aslanian A.S., Lees J.A., Yaffe M.B. p53-deficient cells rely on ATM- and ATR-mediated checkpoint signaling through the p38MAPK/MK2 pathway for survival after DNA damage. Cancer Cell 2007, 11:175-189.
50. Walworth N.C. DNA damage: Chk1 and Cdc25, more than meets the eye. Curr Opin Genet Dev 2001, 11:78-82.
51. Wang J.Y. Cellular responses to DNA damage. Curr Opin Cell Biol 1998, 10:240-247.
52. Zhou B.B., Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature 2000, 408:433-439.
53. Jazayeri A., Falck J., Lukas C., Bartek J., Smith G.C., Lukas J., et al. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 2006, 8:37-45.
54. Dunaway S., Liu H.Y., Walworth N.C. Interaction of 14-3-3 protein with Chk1 affects localization and checkpoint function. J Cell Sci 2005, 118:39-50.
55. Reinhardt H.C., Hasskamp P., Schmedding I., Morandell S., van Vugt M.A., 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.
56. Bouche J., Froment C., Dozier C., Esmenjaud-Mailhat C., Lemaire M., Monsarrat B., et al. NanoLC-MS/MS analysis provides new insights into the phosphorylation pattern of Cdc25B in vivo: full overlap with sites of phosphorylation by Chk1 and Cdk1/cycB kinases in vitro. J Proteome Res 2008, 7:1264-1273.
57. Yoo H.Y., Kumagai A., Shevchenko A., Dunphy W.G. Adaptation of a DNA replication checkpoint response depends upon inactivation of Claspin by the Polo-like kinase. Cell 2004, 117:575-588.
58. Mailand N., Bekker-Jensen S., Bartek J., Lukas J. Destruction of Claspin by SCFbetaTrCP restrains Chk1 activation and facilitates recovery from genotoxic stress. Mol Cell 2006, 23:307-318.
59. Mamely I., van Vugt M.A., Smits V.A., Semple J.I., Lemmens B., Perrakis A., et al. Polo-like kinase-1 controls proteasome-dependent degradation of Claspin during checkpoint recovery. Curr Biol 2006, 16:1950-1955.
60. Peschiaroli A., Dorrello N.V., Guardavaccaro D., Venere M., Halazonetis T., Sherman N.E., et al. SCFbetaTrCP-mediated degradation of Claspin regulates recovery from the DNA replication checkpoint response. Mol Cell 2006, 23:319-329.
61. van Vugt M.A., Gardino A.K., Linding R., Ostheimer G.J., Reinhardt H.C., Ong S.E., et al. A mitotic phosphorylation feedback network connects Cdk1, Plk1, 53BP1, and Chk2 to inactivate the G(2)/M DNA damage checkpoint. PLoS Biol 2009, 8:e1000287.
62. Vidanes G.M., Sweeney F.D., Galicia S., Cheung S., Doyle J.P., Durocher D., et al. CDC5 inhibits the hyperphosphorylation of the checkpoint kinase Rad53, leading to checkpoint adaptation. PLoS Biol 2010, 8:e1000286.
63. Takekawa M., Adachi M., Nakahata A., Nakayama I., Itoh F., Tsukuda H., et al. p53-inducible wip1 phosphatase mediates a negative feedback regulation of p38 MAPK-p53 signaling in response to UV radiation. EMBO J 2000, 19:6517-6526.
64. Yamaguchi H., Minopoli G., Demidov O.N., Chatterjee D.K., Anderson C.W., Durell S.R., et al. Substrate specificity of the human protein phosphatase 2Cdelta, Wip1. Biochemistry 2005, 44:5285-5294.
65. Cha H., Lowe J.M., Li H., Lee J.S., Belova G.I., Bulavin D.V., et al. Wip1 directly dephosphorylates gamma-H2AX and attenuates the DNA damage response. Cancer Res 2010, 70:4112-4122.
66. Macurek L., Lindqvist A., Lim D., Lampson M.A., Klompmaker R., Freire R., et al. Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature 2008, 455:119-123.
67. Asano S., Park J.E., Sakchaisri K., Yu L.R., Song S., Supavilai P., et al. Concerted mechanism of Swe1/Wee1 regulation by multiple kinases in budding yeast. EMBO J 2005, 24:2194-2204.
68. Watanabe N., Arai H., Nishihara Y., Taniguchi M., Hunter T., Osada H. M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFbeta-TrCP. Proc Natl Acad Sci U S A 2004, 101:4419-4424.
69. Bartkova J., Horejsi Z., Koed K., Kramer A., Tort F., Zieger K., et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005, 434:864-870.
70. Krempler A., Deckbar D., Jeggo P.A., Lobrich M. An imperfect G2M checkpoint contributes to chromosome instability following irradiation of S and G2 phase cells. Cell Cycle 2007, 6:1682-1686.
71. Margolis S.S., Walsh S., Weiser D.C., Yoshida M., Shenolikar S., Kornbluth S. PP1 control of M phase entry exerted through 14-3-3-regulated Cdc25 dephosphorylation. EMBO J 2003, 22:5734-5745.
72. Margolis S.S., Perry J.A., Weitzel D.H., Freel C.D., Yoshida M., Haystead T.A., et al. A role for PP1 in the Cdc2/Cyclin B-mediated positive feedback activation of Cdc25. Mol Biol Cell 2006, 17:1779-1789.
73. Tzivion G., Luo Z.J., Avruch J. Calyculin A-induced vimentin phosphorylation sequesters 14-3-3 and displaces other 14-3-3 partners in vivo. J Biol Chem 2000, 275:29772-29778.
74. Ku N.O., Michie S., Resurreccion E.Z., Broome R.L., Omary M.B. Keratin binding to 14-3-3 proteins modulates keratin filaments and hepatocyte mitotic progression. Proc Natl Acad Sci U S A 2002, 99:4373-4378.
75. Liao J., Omary M.B. 14-3-3 proteins associate with phosphorylated simple epithelial keratins during cell cycle progression and act as a solubility cofactor. J Cell Biol 1996, 133:345-357.
76. Astuti P., Gabrielli B. Phosphorylation of Cdc25B3 Ser169 regulates 14-3-3 binding to Ser151 and Cdc25B activity. Cell Cycle 2011, 10:1960-1967.
77. Bulavin D.V., Higashimoto Y., Demidenko Z.N., Meek S., Graves P., Phillips C., et al. Dual phosphorylation controls Cdc25 phosphatases and mitotic entry. Nat Cell Biol 2003, 5:545-551.
78. Saurin A.T., Durgan J., Cameron A.J., Faisal A., Marber M.S., Parker P.J. The regulated assembly of a PKCepsilon complex controls the completion of cytokinesis. Nat Cell Biol 2008, 10:891-901.
79. Gorin M.A., Pan Q. Protein kinase C epsilon: an oncogene and emerging tumor biomarker. Mol Cancer 2009, 8:9.
80. Lodygin D., Hermeking H. Epigenetic silencing of 14-3-3sigma in cancer. Semin Cancer Biol 2006, 16:214-224.
81. Wilker E.W., van Vugt M.A., Artim S.A., Huang P.H., Petersen C.P., Reinhardt H.C., et al. 14-3-3sigma controls mitotic translation to facilitate cytokinesis. Nature 2007, 446:329-332.
82. Cornelis S., Bruynooghe Y., Denecker G., Van Huffel S., Tinton S., Beyaert R. Identification and characterization of a novel cell cycle-regulated internal ribosome entry site. Mol Cell 2000, 5:597-605.
83. Hu D., Valentine M., Kidd V.J., Lahti J.M. CDK11(p58) is required for the maintenance of sister chromatid cohesion. J Cell Sci 2007, 120:2424-2434.
84. Petretti C., Savoian M., Montembault E., Glover D.M., Prigent C., Giet R. The PITSLRE/CDK11p58 protein kinase promotes centrosome maturation and bipolar spindle formation. EMBO Rep 2006, 7:418-424.
85. Busino L., Donzelli M., Chiesa M., Guardavaccaro D., Ganoth D., Dorrello N.V., et al. Degradation of Cdc25A by beta-TrCP during S phase and in response to DNA damage. Nature 2003, 426:87-91.
86. Jin J., Shirogane T., Xu L., Nalepa G., Qin J., Elledge S.J., et al. SCFbeta-TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase. Genes Dev 2003, 17:3062-3074.
87. Mailand N., Falck J., Lukas C., Syljuasen R.G., Welcker M., Bartek J., et al. Rapid destruction of human Cdc25A in response to DNA damage. Science 2000, 288:1425-1429.
88. Honaker Y., Piwnica-Worms H. Casein kinase 1 functions as both penultimate and ultimate kinase in regulating Cdc25A destruction. Oncogene 2010, 29:3324-3334.
89. Jin J., Ang X.L., Ye X., Livingstone M., Harper J.W. Differential roles for checkpoint kinases in DNA damage-dependent degradation of the Cdc25A protein phosphatase. J Biol Chem 2008, 283:19322-19328.
90. Kang T., Wei Y., Honaker Y., Yamaguchi H., Appella E., Hung M.C., et al. GSK-3 beta targets Cdc25A for ubiquitin-mediated proteolysis, and GSK-3 beta inactivation correlates with Cdc25A overproduction in human cancers. Cancer Cell 2008, 13:36-47.
91. Mailand N., Podtelejnikov A.V., 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, 21:5911-5920.
92. Chen M.S., Ryan C.E., Piwnica-Worms H. Chk1 kinase negatively regulates mitotic function of Cdc25A phosphatase through 14-3-3 binding. Mol Cell Biol 2003, 23:7488-7497.
93. Wang B., Liu K., Lin H.Y., Bellam N., Ling S., Lin W.C. 14-3-3Tau regulates ubiquitin-independent proteasomal degradation of p21, a novel mechanism of p21 downregulation in breast cancer. Mol Cell Biol 2010, 30:1508-1527.
94. Zha J., Harada H., Yang E., Jockel J., Korsmeyer S.J. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 1996, 87:619-628.
95. Datta S.R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y., et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997, 91:231-241.
96. Tan Y., Ruan H., Demeter M.R., Comb M.J. p90(RSK) blocks bad-mediated cell death via a protein kinase C-dependent pathway. J Biol Chem 1999, 274:34859-34867.
97. Datta S.R., Katsov A., Hu L., Petros A., Fesik S.W., Yaffe M.B., et al. 14-3-3 proteins and survival kinases cooperate to inactivate BAD by BH3 domain phosphorylation. Mol Cell 2000, 6:41-51.
98. Nomura M., Shimizu S., Sugiyama T., Narita M., Ito T., Matsuda H., et al. 14-3-3 Interacts directly with and negatively regulates pro-apoptotic Bax. J Biol Chem 2003, 278:2058-2065.
99. Youle R.J., Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008, 9:47-59.
100. Tsuruta F., Sunayama J., Mori Y., Hattori S., Shimizu S., Tsujimoto Y., et al. JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J 2004, 23:1889-1899.
101. Tobiume K., Matsuzawa A., Takahashi T., Nishitoh H., Morita K., Takeda K., et al. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2001, 2:222-228.
102. Zhang L., Chen J., Fu H. Suppression of apoptosis signal-regulating kinase 1-induced cell death by 14-3-3 proteins. Proc Natl Acad Sci U S A 1999, 96:8511-8515.
103. He K.L., Ting A.T. A20 inhibits tumor necrosis factor (TNF) alpha-induced apoptosis by disrupting recruitment of TRADD and RIP to the TNF receptor 1 complex in Jurkat T cells. Mol Cell Biol 2002, 22:6034-6045.
104. Vincenz C., Dixit V.M. 14-3-3 proteins associate with A20 in an isoform-specific manner and function both as chaperone and adapter molecules. J Biol Chem 1996, 271:20029-20034.
105. Baksh S., Tommasi S., Fenton S., Yu V.C., Martins L.M., Pfeifer G.P., et al. The tumor suppressor RASSF1A and MAP-1 link death receptor signaling to Bax conformational change and cell death. Mol Cell 2005, 18:637-650.
106. Ghazaleh H.A., Chow R.S., Choo S.L., Pham D., Olesen J.D., Wong R.X., et al. 14-3-3 mediated regulation of the tumor suppressor protein, RASSF1A. Apoptosis 2010, 15:117-127.
107. Fu Z., Tindall D.J. FOXOs, cancer and regulation of apoptosis. Oncogene 2008, 27:2312-2319.
108. Brownawell A.M., Kops G.J., Macara I.G., Burgering B.M. Inhibition of nuclear import by protein kinase B (Akt) regulates the subcellular distribution and activity of the forkhead transcription factor AFX. Mol Cell Biol 2001, 21:3534-3546.
109. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P., Hu L.S., et al. Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell 1999, 96:857-868.
110. Brunet A., Kanai F., Stehn J., Xu J., Sarbassova D., Frangioni J.V., et al. 14-3-3 transits to the nucleus and participates in dynamic nucleocytoplasmic transport. J Cell Biol 2002, 156:817-828.
111. Rena G., Prescott A.R., Guo S., Cohen P., Unterman T.G. Roles of the forkhead in rhabdomyosarcoma (FKHR) phosphorylation sites in regulating 14-3-3 binding, transactivation and nuclear targetting. Biochem J 2001, 354:605-612.
112. Dobson M., Ramakrishnan G., Ma S., Kaplun L., Balan V., Fridman R., et al. Bimodal regulation of FoxO3 by AKT and 14-3-3. Biochim Biophys Acta 2011, 1813:1453-1464.
113. Obsil T., Ghirlando R., Anderson D.E., Hickman A.B., Dyda F. Two 14-3-3 binding motifs are required for stable association of forkhead transcription factor FOXO4 with 14-3-3 proteins and inhibition of DNA binding. Biochemistry 2003, 42:15264-15272.
114. Silhan J., Vacha P., Strnadova P., Vecer J., Herman P., Sulc M., et al. 14-3-3 protein masks the DNA binding interface of forkhead transcription factor FOXO4. J Biol Chem 2009, 284:19349-19360.
115. Masters S.C., Fu H. 14-3-3 proteins mediate an essential anti-apoptotic signal. J Biol Chem 2001, 276:45193-45200.
116. Sunayama J., Tsuruta F., Masuyama N., Gotoh Y. JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3. J Cell Biol 2005, 170:295-304.
117. Wang B., Yang H., Liu Y.C., Jelinek T., Zhang L., Ruoslahti E., et al. Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 1999, 38:12499-12504.
118. Nguyen A., Rothman D.M., Stehn J., Imperiali B., Yaffe M.B. Caged phosphopeptides reveal a temporal role for 14-3-3 in G1 arrest and S-phase checkpoint function. Nat Biotechnol 2004, 22:993-1000.
119. Corradi V., Mancini M., Manetti F., Petta S., Santucci M.A., Botta M. Identification of the first non-peptidic small molecule inhibitor of the c-Abl/14-3-3 protein-protein interactions able to drive sensitive and Imatinib-resistant leukemia cells to apoptosis. Bioorg Med Chem Lett 2010, 20:6133-6137.
120. Mancini M., Corradi V., Petta S., Barbieri E., Manetti F., Botta M., et al. A new nonpeptidic inhibitor of 14-3-3 induces apoptotic cell death in chronic myeloid leukemia sensitive or resistant to imatinib. J Pharmacol Exp Ther 2011, 336:596-604.
121. Ottmann C., Weyand M., Sassa T., Inoue T., Kato N., Wittinghofer A., et al. A structural rationale for selective stabilization of anti-tumor interactions of 14-3-3 proteins by cotylenin A. J Mol Biol 2009, 386:913-919.
122. Wurtele M., Jelich-Ottmann C., Wittinghofer A., Oecking C. Structural view of a fungal toxin acting on a 14-3-3 regulatory complex. EMBO J 2003, 22:987-994.
123. Rose R., Erdmann S., Bovens S., Wolf A., Rose M., Hennig S., et al. Identification and structure of small-molecule stabilizers of 14-3-3 protein-protein interactions. Angew Chem Int Ed Engl 2010, 49:4129-4132.