Post-translational modification of 14-3-3 isoforms and regulation of cellular function

Seminars in Cell and Developmental Biology

Volumn 22, Issue 7, 2011, Pages 673-680

  Aitken, Alastair ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

14 3 3; Isoforms; Phosphorylation; Post translational modification; Protein protein interaction

Indexed keywords

PROTEIN 14 3 3; SELENOCYSTEINE; SERINE; SPHINGOSINE; TYROSINE;

ACETYLATION; ACYLATION; CELL FUNCTION; HUMAN; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PSEUDOGENE; REVIEW;

EID: 80455174617     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2011.08.003     Document Type: Review

References (103)

1. Moore B.E., Perez V.J. Physiological and biochemical aspects of nervous integration 1967, 343-359. Prentice-Hall, Englewood Cliffs, NJ. F.D. Carlson (Ed.).
2. Ichimura T., Isobe T., Okuyama T., Takahashi N., Araki K., Kuwano R., et al. Molecular cloning of cDNA coding for brain-specific 14-3-3 protein, a protein kinase-dependent activator of tyrosine and tryptophan hydroxylases. Proc Natl Acad Sci U S A 1988, 85:7084-7088.
3. Toker A., Ellis C.A., Sellers L.A., Aitken A. Protein kinase C inhibitor proteins: purification from sheep brain and sequence similarity to lipocortins and 14-3-3 protein. Eur J Biochem 1990, 191:421-429.
4. Toker A., Sellers L.A., Amess B., Patel Y., Harris A., Aitken A. Multiple isoforms of a protein kinase C inhibitor (KCIP-1/14-3-3) from sheep brain. Amino acid sequence of phosphorylated forms. Eur J Biochem 1992, 206:453-461.
5. Martin H., Patel Y., Jones D., Howell S., Robinson K., Aitken A. Antibodies against the major isoforms of 14-3-3 protein. An antibody specific for the N-acetylated amino terminus of a protein. FEBS Lett 1993, 331:296-303.
6. Aitken A., Howell S., Jones D., Madrazo J., Patel Y. 14-3-3 Alpha and delta are the phosphorylated forms of Raf-activating 14-3-3 beta and zeta. In vivo stoichiometric phosphorylation in brain at a Ser-Pro-Glu-Lys MOTIF. J Biol Chem 1995, 270:5706-5709.
7. Leffers H., Madsen P., Rasmussen H.H., Honore B., Andersen A.H., Walbum E., et al. Molecular cloning and expression of the transformation sensitive epithelial marker stratifin. A member of a protein family that has been involved in the protein kinase C signalling pathway. J Mol Biol 1993, 231:982-998.
8. Aitken A. 14-3-3 Proteins: a historic overview. Semin Cancer Biol 2006, 16:162-172.
9. Boston P.F., Jackson P., Thompson R.J. Human 14-3-3 protein: radioimmunoassay, tissue distribution, and cerebrospinal fluid levels in patients with neurological disorders. J Neurochem 1982, 38:1475-1482.
10. Aitken A. Functional specificity in 14-3-3 isoform interactions through dimer formation and phosphorylation. Plant Mol Biol 2002, 50:993-1010.
11. Fuller B., Stevens S.M., Sehnke P.C., Ferl R.J. Proteomic analysis of the 14-3-3 family in Arabidopsis. Proteomics 2006, 6:3050-3059.
12. Todd A., Cossons N., Aitken A., Price G.B., Zannis-Hadjopoulos M. Human cruciform binding protein belongs to the 14-3-3 family. Biochemistry 1998, 37:14317-14325.
13. van Heusden G.P. 14-3-3 Proteins: insights from genome-wide studies in yeast. Genomics 2009, 94:287-293.
14. van Hemert M.J., Steensma H.Y., van Heusden G.P. 14-3-3 Proteins: key regulators of cell division, signalling and apoptosis. Bioessays 2001, 23:936-946.
15. Rosenquist M., Sehnke P., Ferl R.J., Sommarin M., Larsson C. Evolution of the 14-3-3 protein family: does the large number of isoforms in multicellular organisms reflect functional specificity?. J Mol Evol 2000, 51:446-458.
16. Oecking C., Jaspert N. Plant 14-3-3 proteins catch up with their mammalian orthologs. Curr Opin Plant Biol 2009, 12:760-765.
17. Pietromonaco S.F., Seluja G.A., Aitken A., Elias L. Association of 14-3-3 proteins with centrosomes. Blood Cells Mol Dis 1996, 22:225-237.
18. Han D., Ye G., Liu T., Chen C., Yang X., Wan B., et al. Functional identification of a novel 14-3-3 epsilon splicing variant suggests dimerization is not necessary for 14-3-3 epsilon to inhibit UV-induced apoptosis. Biochem Biophys Res Commun 2010, 396:401-406.
19. Jones D., Martin H., Madrazo J., Robinson K., Nielsen P., Roseboom P., et al. structural analysis of 14-3-3 proteins. J Mol Biol 1995, 245:375-384.
20. Tzivion G., Luo Z., Avruch J. A dimeric 14-3-3 protein is an essential cofactor for Raf kinase activity. Nature 1998, 394:88-92.
21. Yaffe M.B. How do 14-3-3 proteins work? Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett 2002, 513:53-57.
22. Wanna W., Rexroad C.E., Yao J. Identification of a functional splice variant of 14-3-3E1 in rainbow trout. Mar Biotechnol (NY) 2010, 12:70-80.
23. Oowatari Y., Toma K., Ozoe F., Kawamukai M. Identification of sam4 as a rad24 allele in Schizosaccharomyces pombe. Biosci Biotechnol Biochem 2009, 73:1591-1598.
24. Xiao B., Smerdon S.J., Jones D.H., Dodson G.G., Soneji Y., Aitken A., et al. Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature 1995, 376:188-191.
25. Liu D., Bienkowska J., Petosa C., Collier R.J., Fu H., Liddington R. Crystal structure of the zeta isoform of the 14-3-3 protein. Nature 1995, 376:191-194.
26. Schumacher B., Skwarczynska M., Rose R., Ottmann C. Structure of a 14-3-3σ-YAP phosphopeptide complex at 1.15Å resolution. Acta Crystallogr Sect F Struct Biol Cryst Commun 2010, 66:978-984.
27. Telles E., Hosing A.S., Kundu S.T., Venkatraman P., Dalal S.N. A novel pocket in 14-3-3epsilon is required to mediate specific complex formation with cdc25C and to inhibit cell cycle progression upon activation of checkpoint pathways. Exp Cell Res 2009, 315:1448-1457.
28. 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.
29. Messaritou G., Grammenoudi S., Skoulakis E.M. Dimerization is essential for 14-3-3zeta stability and function in vivo. J Biol Chem 2010, 285:1692-1700.
30. Steinacker P., Schwarz P., Reim K., Brechlin P., Jahn O., Kratzin H., et al. Unchanged survival rates of 14-3-3 gamma knockout mice after inoculation with pathological prion protein. Mol Cell Biol 2005, 25:1339-1346.
31. Yang X., Lee W.H., Sobott F., Papagrigoriou E., Robinson C.V., Grossmann J.G., Sundström M., Doyle D.A., Elkins J.M. Structural basis for protein-protein interactions in the 14-3-3 protein family. Proc Natl Acad Sci U S A. 2006, 103:17237-17242.
32. Chaudhri M., Scarabel M., Aitken A. Mammalian and yeast 14-3-3 isoforms form distinct patterns of dimers in vivo. Biochem Biophys Res Commun 2003, 300:679-685.
33. Kligys K., Yao J., Yu D., Jones J.C. 14-3-3zeta/tau heterodimers regulate Slingshot activity in migrating keratinocytes. Biochem Biophys Res Commun 2009, 383:450-454.
34. Fischer A., Baljuls A., Reinders J., Nekhoroshkova E., Sibilski C., Metz R., et al. Regulation of RAF activity by 14-3-3 proteins: RAF kinases associate functionally with both homo- and heterodimeric forms of 14-3-3 proteins. J Biol Chem 2009, 284:3183-3194.
35. Liang X., Butterworth M.B., Peters K.W., Walker W.H., Frizzell R.A. An obligatory heterodimer of 14-3-3beta and 14-3-3epsilon is required for aldosterone regulation of the epithelial sodium channel. J Biol Chem 2008, 283:27418-27425.
36. Jagemann L.R., Pérez-Rivas L.G., Ruiz E.J., Ranea J.A., Sánchez-Jiménez F., Nebreda A.R. The functional interaction of 14-3-3 proteins with the ERK1/2 scaffold KSR1 occurs in an isoform-specific manner. J Biol Chem 2008, 283:17450-17462.
37. Chan T.A., Hermeking H., Lengauer C., Kinzler K.W., Vogelstein B. 14-3-3 Sigma is required to prevent mitotic catastrophe after DNA damage. Nature 1999, 401:616-620.
38. 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.
39. 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.
40. Verdoodt B., Benzinger A., Popowicz G.M., Holak T.A., Hermeking H. Characterization of 14-3-3sigma dimerization determinants: requirement of homodimerization for inhibition of cell proliferation. Cell Cycle 2006, 5:2920-2926.
41. Muslin A.J., Tanner J.W., Allen P.M., Shaw A.S. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 1996, 84:889-897.
42. Yaffe M.B., Rittinger K., Volinia S., Caron P.R., Aitken A., Leffers H., et al. Structural basis for 14-3-3: phosphopeptide binding specificity. Cell 1997, 91:961-971.
43. 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.
44. Ganguly S., Weller J.L., Ho A., Chemineau P., Malpaux B., Klein D.C. Melatonin synthesis: 14-3-3-dependent activation and inhibition of arylalkylamine N-acetyltransferase mediated by phosphoserine-205. Proc Natl Acad Sci U S A 2005, 102:1222-1227.
45. Mackintosh C. Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem J 2004, 381:329-342.
46. Pozuelo-Rubio M., Geraghty K.M., Wong B.H., Wood N.T., Campbell D.G., Morrice N., et al. 14-3-3-Affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation, and trafficking. Biochem J 2004, 379:395-408.
47. Jin J., Smith F.D., Stark C., Wells C.D., Fawcett J.P., Kulkarni S., et al. Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr Biol 2004, 14:1436-1450.
48. Meek S.E., Lane W.S., Piwnica-Worms H. Comprehensive proteomic analysis of interphase and mitotic 14-3-3-binding proteins. J Biol Chem 2004, 279:32046-32054.
49. Waterman M.J., Stavridi E.S., Waterman J.L., Halazonetis T.D. ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nat Genet 1998, 19:175-178.
50. Henriksson M.L., Francis M.S., Peden A., Aili M., Stefansson K., Palmer R., et al. A nonphosphorylated 14-3-3 binding motif on exoenzyme S that is functional in vivo. Eur J Biochem 2002, 269:4921-4929.
51. Wang B., Yang H.S., Liu Y.C., Jelinek T., Zhang L., Ruoslahti E., Fu H. Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 1999, 38:12499-12504.
52. Hamaguchi A., Suzuki E., Murayama K., Fujimura T., Hikita T., Iwabuchi K., et al. Sphingosine-dependent protein kinase-1, directed to 14-3-3, is identified as the kinase domain of protein kinase C delta. J Biol Chem 2003, 278:41557-41565.
53. Jones D.H., Ley S., Aitken A. Isoforms of 14-3-3 protein can form homo- and heterodimers in vivo and in vitro: implications for function as adapter proteins. FEBS Lett 1995, 368:55-58.
54. Robinson K., Jones D.H., Patel Y., Martin H., Madrazo J., Martin S., et al. Mechanism of inhibition of protein kinase C by 14-3-3 isoforms. 14-3-3 Isoforms do not have PLA2 activity. Biochem J 1994, 299:853-861.
55. Ma Y., Pitson S., Hercus T., Murphy J., Lopez A., Woodcock J. Sphingosine activates protein kinase A type II by a novel cAMP-independent mechanism. J Biol Chem 2005, 280:26011-26017.
56. Woodcock J.M., Murphy J., Stomski F.C., Berndt M.C., Lopez A.F. The dimeric versus monomeric status of 14-3-3zeta is controlled by phosphorylation of Ser58 at the dimer interface. J Biol Chem 2003, 278:36323-36327.
57. Woodcock J.M., Ma Y., Coolen C., Pham D., Jones C., Lopez A.F., et al. FTY720 directly bind pro-survival 14-3-3 proteins to regulate their function. Cell Signal 2010, 22:1291-1299.
58. Kanno T., Nishizaki T. Sphingosine induces apoptosis in hippocampal neurons and astrocytes by activating caspase-3/-9 via a mitochondrial pathway linked to SDK/14-3-3 Protein/Bax/Cytochrome c. J Cell Physiol December 7, 2010, [Epub ahead of print].
59. Kim Y.S., Choi M.Y., Kim Y.H., Jeon B.T., Lee D.H., Roh G.S., et al. Protein kinase Cdelta is associated with 14-3-3 phosphorylation in seizure-induced neuronal death. Epilepsy Res 2010, 92:30-40.
60. Powell D.W., Rane M.J., Chen Q., Singh S., McLeish K.R. Identification of 14-3-3zeta as a protein kinase B/Akt substrate. J Biol Chem 2002, 277:21639-21642.
61. Ellis J.J., Valencia T.G., Zeng H., Roberts L.D., Deaton R.A., Grant S.R. CaM kinase IIdeltaC phosphorylation of 14-3-3beta in vascular smooth muscle cells: activation of class II HDAC repression. Mol Cell Biochem 2003, 242:153-161.
62. 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.
63. 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.
64. Yoshida K., Yamaguchi T., Natsume T., Kufe D., Miki Y. JNK phosphorylation of 14-3-3 proteins regulates nuclear targeting of c-Abl in the apoptotic response to DNA damage. Nat Cell Biol 2005, 7:278-285.
65. Kim Y.S., Jung M.H., Choi M.Y., Kim Y.H., Sheverdin V., Kim J.H., et al. Glutamine attenuates tubular cell apoptosis in acute kidney injury via inhibition of the c-Jun N-terminal kinase phosphorylation of 14-3-3. Crit Care Med 2009, 37:2033-2044.
66. Dubois T., Rommel C., Howell S., Steinhusen U., Soneji Y., Moelling K., et al. 14-3-3 is phosphorylated by casein kinase I on residue 233. Phosphorylation at this site in vivo regulates Raf/14-3-3 interaction. J Biol Chem 1997, 272:28882-28888.
67. Clokie S.J., Cheung K.Y., Mackie S., Marquez R., Peden A.H., Aitken A. BCR kinase phosphorylates 14-3-3 tau on residue 233. FEBS J 2005, 272:3767-3776.
68. Rommel C., Radziwill G., Lovric J., Noeldeke J., Heinicke T., Jones D., et al. Activated Ras displaces 14-3-3 from the amino terminus of c-Raf-1. Oncogene 1996, 12:609-619.
69. Ren R. Mechanisms of BCR-ABL in the pathogenesis of chronic myelogenous leukaemia. Nat Rev Cancer 2005, 5:172-183.
70. Reuther G.W., Fu H., Cripe L.D., Collier R.J., Pendergast A.M. Association of the protein kinases c-Bcr and Bcr-Abl with proteins of the 14-3-3 family. Science 1994, 266:129-133.
71. Obsilova V., Herman P., Vecer J., Sulc M., Teisinger J., Obsil T. 14-3-3{zeta} C-terminal stretch changes its conformation upon ligand binding and phosphorylation at Thr232. J Biol Chem 2004, 279:4531-4540.
72. Sluchanko N.N., Sudnitsyna M.V., Chernik I.S., Seit-Nebi A.S., Gusev N.B. Phosphomimicking mutations of human 14-3-3ζ affect its interaction with tau protein and small heat shock protein HspB6. Arch Biochem Biophys 2011, 506:24-34.
73. Barry E.F., Felquer F.A., Powell J.A., Biggs L., Stomski F.C., Urbani A., et al. 14-3-3:Shc scaffolds integrate phosphoserine and phosphotyrosine signaling to regulate phosphatidylinositol 3-kinase activation and cell survival. J Biol Chem 2009, 284:12080-12090.
74. Giacometti S., Camoni L., Albumi C., Visconti S., De Michelis M.I., Aducci P. Tyrosine phosphorylation inhibits the interaction of 14-3-3 proteins with the plant plasma membrane H+-ATPase. Plant Biol (Stuttg) 2004, 6:422-431.
75. Liu Y., Ross J.F., Bodine P.V., Billiard J. Homodimerization of Ror2 tyrosine kinase receptor induces 14-3-3(beta) phosphorylation and promotes osteoblast differentiation and bone formation. Mol Endocrinol 2007, 21:3050-3061.
76. Furlanetto R.W., Dey B.R., Lopaczynski W., Nissley S.P. 14-3-3 Proteins interact with the insulin-like growth factor receptor but not the insulin receptor. Biochem J 1997, 327:765-771.
77. Bonnefoy-Berard N., Liu Y.C., von Willebrand M., Sung A., Elly C., Mustelin T., et al. Inhibition of phosphatidylinositol 3-kinase activity by association with 14-3-3 proteins in T cells. Proc Natl Acad Sci U S A 1995, 92:10142-10146.
78. Daub H., Olsen J.V., Bairlein M., Gnad F., Oppermann F.S., Korner R., et al. Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol Cell 2008, 31:438-448.
79. Beausoleil S.A., Villen J., Gerber S.A., Rush J., Gygi S.P. A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol 2006, 24:1285-1292.
80. Dephoure N., Zhou C., Villen J., Beausoleil S.A., Bakalarski C.E., Elledge S.J., et al. A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci U S A 2008, 105:10762-10767.
81. Oppermann F.S., Gnad F., Olsen J.V., Hornberger R., Greff Z., Kéri G., et al. Large-scale proteomics analysis of the human kinome. Mol Cell Proteomics 2009, 8:1751-1764.
82. Mayya V., Lundgren D.H., Hwang S.-I., Rezaul K., Wu L., Eng J.K., et al. Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions. Sci Signal 2009, 2:RA46.
83. Oppermann F.S., Gnad F., Olsen J.V., Hornberger R., Greff Z., Keri G., et al. Large-scale proteomics analysis of the human kinome. Nat Biotechnol 2009, 24:1285-1292.
84. Aitken A. Structure determination of acylated proteins. Lipid modification of proteins, a practical approach 1992, 63-88. IRL Press, Oxford, [chapter 4]. N.M. Hooper, A.J. Turner (Eds.).
85. Clark K.L., Oelke A., Johnson M.E., Eilert K.D., Simpson P.C., Todd S.C. CD81 associates with 14-3-3 in a redox-regulated palmitoylation-dependent manner. J Biol Chem 2004, 279:19401-19406.
86. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
87. Winter S., Fischle W., Seiser C. Modulation of 14-3-3 interaction with phosphorylated histone H3 by combinatorial modification patterns. Cell Cycle 2008, 7:1336-1342.
88. Winter S., Simboeck E., Fischle W., Zupkovitz G., Dohnal I., Mechtler K., et al. 14-3-3 Proteins recognize a histone code at histone H3 and are required for transcriptional activation. EMBO J 2008, 27:88-99.
89. Walter W., Clynes D., Tang Y., Marmorstein R., Mellor J., Berger S.L. 14-3-3 Interaction with histone H3 involves a dual modification pattern of phosphoacetylation. Mol Cell Biol 2008, 28:2840-2849.
90. Macdonald N., Welburn J.P., Noble M.E., Nguyen A., Yaffe M.B., Clynes D., et al. Molecular basis for the recognition of phosphorylated and phosphoacetylated histone H3 by 14-3-3. Mol Cell 2005, 20:199-211.
91. Lalle M., Bavassano C., Fratini F., Cecchetti S., Boisguerin P., Crescenzi M., et al. Involvement of 14-3-3 protein post-translational modifications in Giardia duodenalis encystation. Int J Parasitol 2010, 40:201-213.
92. Lalle M., Camerini S., Cecchetti S., Fantauzzi C.B., Crescenzi M., Pozio E. Giardia duodenalis 14-3-3 protein is polyglycylated by a tubulin tyrosine ligase-like member and deglycylated by two metallocarboxypeptidases. J Biol Chem 2011, 286:4471-4484.
93. Dikiy A., Novoselov S.V., Fomenko D.E., Sengupta A., Carlson B.A., Cerny R.L., et al. SelT, SelW, SelH, and Rdx12: genomics and molecular insights into the functions of selenoproteins of a novel thioredoxin-like family. Biochemistry 2007, 46:6871-6882.
94. Musiani F., Ciurli S., Dikiy A. Interaction of selenoprotein W with 14-3-3 proteins: a computational approach. J Proteome Res 2011, 10:968-976.
95. Santpere G., Puig B., Ferrer I. Oxidative damage of 14-3-3 zeta and gamma isoforms in Alzheimer's disease and cerebral amyloid angiopathy. Neuroscience 2007, 146:1640-1651.
96. Santpere G., Puig B., Ferrer I., Retracted Oxidative damage of 14-3-3 zeta and gamma isoforms in Alzheimer's disease and cerebral amyloid angiopathy. Neuroscience 2009, 161:663.
97. Savitsky P.A., Finkel T. Redox regulation of Cdc25C. J Biol Chem 2002, 277:20535-20540.
98. Kasahara K., Goto H., Enomoto M., Tomono Y., Kiyono T., Inagaki M. 14-3-3gamma Mediates Cdc25A proteolysis to block premature mitotic entry after DNA damage. EMBO J 2010, 29:2802-2812.
99. Klein D.C. Arylalkylamine N-acetyltransferase: "the Timezyme". J Biol Chem 2007, 282:4233-4237.
100. Won J., Kim D.Y., La M., Kim D., Meadows G.G., Joe C.O. Cleavage of 14-3-3 protein by caspase-3 facilitates bad interaction with Bcl-x(L) during apoptosis. J Biol Chem 2003, 278:19347-19351.
101. Ferguson A.T., Evron E., Umbricht C.B., Pandita T.K., Chan T.A., Hermeking H., et al. High frequency of hypermethylation at the 14-3-3 sigma locus leads to gene silencing in breast cancer. Proc Natl Acad Sci U S A 2000, 97:6049-6054.
102. Horie-Inoue K., Inoue S. Epigenetic and proteolytic inactivation of 14-3-3sigma in breast and prostate cancers. Semin Cancer Biol 2006, 16:235-239.
103. Urano T., Saito T., Tsukui T., Fujita M., Hosoi T., Muramatsu M., et al. Efp targets 14-3-3 sigma for proteolysis and promotes breast tumour growth. Nature 2002, 417:871-875.