The functional significance of 14-3-3 proteins in cancer: focus on lung cancer

References

[1] Fu H, Subramanian RR, Masters SC. 14-3-3 proteins: structure, function, and regulation. Annu Rev Pharmacol Toxicol. 2000;40:617–47.10.1146/annurev.pharmtox.40.1.617Search in Google Scholar

[2] Mhawech P. 14-3-3 proteins—an update. Cell Res. 2005;15:228–36.10.1038/sj.cr.7290291Search in Google Scholar

[3] Yaffe MB, Rittinger K, Volinia S, Caron PR, Aitken A, Leffers H, et al. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell. 1997;91:961–71.10.1016/S0092-8674(00)80487-0Search in Google Scholar

[4] Aitken A. 14-3-3 and its possible role in co-ordinating multiple signalling pathways. Trends Cell Biol. 1996;6:341–7.10.1016/0962-8924(96)10029-5Search in Google Scholar

[5] Aitken A. 14-3-3 proteins: a historic overview. Seminars in cancer biology: 2006. Amsterdam: Elsevier, 2006:162–72.10.1016/j.semcancer.2006.03.005Search in Google Scholar

[6] Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66:7–30.10.3322/caac.21332Search in Google Scholar PubMed

[7] Youlden DR, Cramb SM, Baade PD. The International Epidemiology of Lung Cancer: geographical distribution and secular trends. J Thorac Oncol. 2008;3:819–31.10.1097/JTO.0b013e31818020ebSearch in Google Scholar PubMed

[8] Siegel R, Naishadham D, Jemal A. Cancer statistics for Hispanics/Latinos, 2012. CA Cancer J Clin. 2012;62:283–98.10.3322/caac.21153Search in Google Scholar PubMed

[9] Saito S, Espinoza-Mercado F, Liu H, Sata N, Cui X, Soukiasian HJ. Current status of research and treatment for non-small cell lung cancer in never-smoking females. Cancer Biol Ther. 2017;1–10. DOI:10.1080/15384047.2017.1323580.Search in Google Scholar PubMed PubMed Central

[10] Spira A, Ettinger DS. Multidisciplinary management of lung cancer. N Engl J Med. 2004;350:379–92.10.1056/NEJMra035536Search in Google Scholar PubMed

[11] Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med. 2008;359:1367–80.10.1056/NEJMra0802714Search in Google Scholar PubMed

[12] Qi W, Liu X, Qiao D, Martinez JD. Isoform-specific expression of 14-3-3 proteins in human lung cancer tissues. Int J Cancer. 2005;113:359–63.10.1002/ijc.20492Search in Google Scholar

[13] Raungrut P, Wongkotsila A, Lirdprapamongkol K, Svasti J, Geater SL, Phukaoloun M, et al. Prognostic significance of 14-3-3gamma overexpression in advanced non-small cell lung cancer. Asian Pac J Cancer Prev. 2014;15:3513–8.10.7314/APJCP.2014.15.8.3513Search in Google Scholar

[14] Radhakrishnan VM, Putnam CW, Qi W, Martinez JD. P53 suppresses expression of the 14-3-3gamma oncogene. BMC Cancer. 2011;11:378.10.1186/1471-2407-11-378Search in Google Scholar

[15] Qi W, Liu X, Chen W, Li Q, Martinez JD. Overexpression of 14-3-3gamma causes polyploidization in H322 lung cancer cells. Mol Carcinog. 2007;46:847–56.10.1002/mc.20314Search in Google Scholar

[16] Petosa C, Masters SC, Bankston LA, Pohl J, Wang B, Fu H, et al. 14-3-3zeta binds a phosphorylated Raf peptide and an unphosphorylated peptide via its conserved amphipathic groove. J Biol Chem. 1998;273:16305–10.10.1074/jbc.273.26.16305Search in Google Scholar

[17] Obsil T, Ghirlando R, Klein DC, Ganguly S, Dyda F. Crystal structure of the 14-3-3zeta:serotonin N-acetyltransferase complex. a role for scaffolding in enzyme regulation. Cell. 2001;105:257–67.10.1016/S0092-8674(01)00316-6Search in Google Scholar

[18] Bridges D, Moorhead GB. 14-3-3 proteins: a number of functions for a numbered protein. Sci STKE. 2005;2005:re10.10.1126/stke.2962005re10Search in Google Scholar PubMed

[19] Veisova D, Rezabkova L, Stepanek M, Novotna P, Herman P, Vecer J, et al. The C-terminal segment of yeast BMH proteins exhibits different structure compared to other 14-3-3 protein isoforms. Biochemistry. 2010;49:3853–61.10.1021/bi100273kSearch in Google Scholar PubMed

[20] Boston PF, Jackson P, Thompson RJ. Human 14-3-3 protein: radioimmunoassay, tissue distribution, and cerebrospinal fluid levels in patients with neurological disorders. J Neurochem. 1982;38:1475–82.10.1111/j.1471-4159.1982.tb07928.xSearch in Google Scholar PubMed

[21] Shankardas J, Senchyna M, Dimitrijevich SD. Presence and distribution of 14-3-3 proteins in human ocular surface tissues. Mol Vis. 2008;14:2604–15.Search in Google Scholar

[22] Zerr I, Bodemer M, Gefeller O, Otto M, Poser S, Wiltfang J, et al. Detection of 14-3-3 protein in the cerebrospinal fluid supports the diagnosis of Creutzfeldt-Jakob disease. Ann Neurol. 1998;43:32–40.10.1002/ana.410430109Search in Google Scholar PubMed

[23] Jiang K, Pereira E, Maxfield M, Russell B, Goudelock DM, Sanchez Y. Regulation of Chk1 includes chromatin association and 14-3-3 binding following phosphorylation on Ser-345. J Biol Chem. 2003;278:25207–17.10.1074/jbc.M300070200Search in Google Scholar PubMed

[24] Forrest A, Gabrielli B. Cdc25B activity is regulated by 14-3-3. Oncogene. 2001;20:4393.10.1038/sj.onc.1204574Search in Google Scholar PubMed

[25] Samuel T, Weber HO, Rauch P, Verdoodt B, Eppel J-T, McShea A, et al. The G2/M regulator 14-3-3ς prevents apoptosis through sequestration of Bax. J Biol Chem. 2001;276:45201–06.10.1074/jbc.M106427200Search in Google Scholar PubMed

[26] Parker LL, Piwnica-Worms H. Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science. 1992;257:1955–7.10.1126/science.1384126Search in Google Scholar PubMed

[27] Norbury C, Blow J, Nurse P. Regulatory phosphorylation of the p34cdc2 protein kinase in vertebrates. EMBO J. 1991;10:3321–9.10.1002/j.1460-2075.1991.tb04896.xSearch in Google Scholar PubMed PubMed Central

[28] Hermeking H, Benzinger A. 14-3-3 proteins in cell cycle regulation. Semin Cancer Biol. 2006;16:183–92.10.1016/j.semcancer.2006.03.002Search in Google Scholar PubMed

[29] Qi W, Martinez JD. Reduction of 14-3-3 proteins correlates with increased sensitivity to killing of human lung cancer cells by ionizing radiation. Radiat Res. 2003;160:217–23.10.1667/RR3038Search in Google Scholar

[30] Dalal SN, Yaffe MB, DeCaprio JA. 14-3-3 family members act coordinately to regulate mitotic progression. Cell Cycle. 2004;3:672–7.10.4161/cc.3.5.856Search in Google Scholar

[31] Chen MS, Ryan CE, Piwnica-Worms H. Chk1 kinase negatively regulates mitotic function of Cdc25A phosphatase through 14-3-3 binding. Mol Cell Biol. 2003;23:7488–97.10.1128/MCB.23.21.7488-7497.2003Search in Google Scholar PubMed PubMed Central

[32] Wang Y, Jacobs C, Hook KE, Duan H, Booher RN, Sun Y. Binding of 14-3-3beta to the carboxyl terminus of Wee1 increases Wee1 stability, kinase activity, and G2-M cell population. Cell Growth Differ. 2000;11:211–9.Search in Google Scholar

[33] Liu Q, Guntuku S, Cui XS, Matsuoka S, Cortez D, Tamai K, et al. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev. 2000;14:1448–59.10.1101/gad.14.12.1448Search in Google Scholar

[34] Jiang K, Pereira E, Maxfield M, Russell B, Goudelock DM, Sanchez Y. Regulation of Chk1 includes chromatin association and 14-3-3 binding following phosphorylation on Ser-345. J Biol Chem. 2003;278:25207–17.10.1074/jbc.M300070200Search in Google Scholar

[35] Gardino AK, Yaffe MB. 14-3-3 proteins as signaling integration points for cell cycle control and apoptosis. Semin Cell Dev Biol. 2011;22:688–95.10.1016/j.semcdb.2011.09.008Search in Google Scholar

[36] Hermeking H, Lengauer C, Polyak K, He TC, Zhang L, Thiagalingam S, et al. 14-3-3sigma is a p53-regulated inhibitor of G2/M progression. Mol Cell. 1997;1:3–11.10.1016/S1097-2765(00)80002-7Search in Google Scholar

[37] Hermeking H. The 14-3-3 cancer connection. Nat Rev Cancer. 2003;3:931–43.10.1038/nrc1230Search in Google Scholar PubMed

[38] Yang H, Zhang Y, Zhao R, Wen YY, Fournier K, Wu HB, et al. Negative cell cycle regulator 14-3-3sigma stabilizes p27 Kip1 by inhibiting the activity of PKB/Akt. Oncogene. 2006;25:4585–94.10.1038/sj.onc.1209481Search in Google Scholar PubMed

[39] 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;277:28706–13.10.1074/jbc.M203668200Search in Google Scholar PubMed

[40] Laronga C, Yang HY, Neal C, Lee MH. Association of the cyclin-dependent kinases and 14-3-3 sigma negatively regulates cell cycle progression. J Biol Chem. 2000;275:23106–12.10.1074/jbc.M905616199Search in Google Scholar PubMed

[41] Dar A, Wu D, Lee N, Shibata E, Dutta A. 14-3-3 proteins play a role in the cell cycle by shielding cdt2 from ubiquitin-mediated degradation. Mol Cell Biol. 2014;34:4049–61.10.1128/MCB.00838-14Search in Google Scholar PubMed PubMed Central

[42] Saurin AT, Durgan J, Cameron AJ, Faisal A, Marber MS, Parker PJ. The regulated assembly of a PKCepsilon complex controls the completion of cytokinesis. Nat Cell Biol. 2008;10:891–901.10.1038/ncb1749Search in Google Scholar PubMed

[43] Duronio RJ, Xiong Y. Signaling pathways that control cell proliferation. Cold Spring Harb Perspect Biol. 2013;5:a008904.10.1101/cshperspect.a008904Search in Google Scholar PubMed PubMed Central

[44] Yeh CK. Cellular senescence and aging. Oral Dis. 2016;22:587–90.10.1111/odi.12483Search in Google Scholar

[45] Morrison D. 14-3-3: modulators of signaling proteins?. Science. 1994;266:56–7.10.1126/science.7939645Search in Google Scholar

[46] Murphy LO, Blenis J. MAPK signal specificity: the right place at the right time. Trends Biochem Sci. 2006;31:268–75.10.1016/j.tibs.2006.03.009Search in Google Scholar

[47] Freeman AK, Morrison DK. 14-3-3 Proteins: diverse functions in cell proliferation and cancer progression. Semin Cell Dev Biol. 2011;22:681–7.10.1016/j.semcdb.2011.08.009Search in Google Scholar

[48] Tartaglia M, Gelb BD. Disorders of dysregulated signal traffic through the RAS‐MAPK pathway: phenotypic spectrum and molecular mechanisms. Ann N Y Acad Sci. 2010;1214:99–121.10.1111/j.1749-6632.2010.05790.xSearch in Google Scholar

[49] Manning BD, Toker A. AKT/PKB signaling: navigating the network. Cell. 2017;169:381–405.10.1016/j.cell.2017.04.001Search in Google Scholar

[50] Staller P, Peukert K, Kiermaier A, Seoane J, Lukas J, Karsunky H, et al. Repression of p15INK4b expression by Myc through association with Miz-1. Nat Cell Biol. 2001;3:392–9.10.1038/35070076Search in Google Scholar

[51] Herold S, Wanzel M, Beuger V, Frohme C, Beul D, Hillukkala T, et al. Negative regulation of the mammalian UV response by Myc through association with Miz-1. Mol Cell. 2002;10:509–21.10.1016/S1097-2765(02)00633-0Search in Google Scholar

[52] Wanzel M, Kleine-Kohlbrecher D, Herold S, Hock A, Berns K, Park J, et al. Akt and 14-3-3eta regulate Miz1 to control cell-cycle arrest after DNA damage. Nat Cell Biol. 2005;7:30–41.10.1038/ncb1202Search in Google Scholar PubMed

[53] Maddika S, Ande SR, Panigrahi S, Paranjothy T, Weglarczyk K, Zuse A, et al. Cell survival, cell death and cell cycle pathways are interconnected: implications for cancer therapy. Drug Resist Updates. 2007;10:13–29.10.1016/j.drup.2007.01.003Search in Google Scholar PubMed

[54] Wang B, Liu K, Lin FT, Lin WC. A role for 14-3-3 tau in E2F1 stabilization and DNA damage-induced apoptosis. J Biol Chem. 2004;279:54140–52.10.1074/jbc.M410493200Search in Google Scholar

[55] Lin WC, Lin FT, Nevins JR. Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes Dev. 2001;15:1833–44.Search in Google Scholar

[56] Milton AH, Khaire N, Ingram L, O’Donnell AJ, La Thangue NB. 14-3-3 proteins integrate E2F activity with the DNA damage response. EMBO J. 2006;25:1046–57.10.1038/sj.emboj.7600999Search in Google Scholar

[57] Dellambra E, Golisano O, Bondanza S, Siviero E, Lacal P, Molinari M, et al. Downregulation of 14-3-3sigma prevents clonal evolution and leads to immortalization of primary human keratinocytes. J Cell Biol. 2000;149:1117–30.10.1083/jcb.149.5.1117Search in Google Scholar

[58] Guo W, Giancotti FG. Integrin signalling during tumour progression. Nat Rev Mol Cell Biol. 2004;5:816–26.10.1038/nrm1490Search in Google Scholar

[59] Hood JD, Cheresh DA. Role of integrins in cell invasion and migration. Nat Rev Cancer. 2002;2:91–100.10.1038/nrc727Search in Google Scholar

[60] Han DC, Rodriguez LG, Guan JL. Identification of a novel interaction between integrin beta1 and 14-3-3beta. Oncogene. 2001;20:346–57.10.1038/sj.onc.1204068Search in Google Scholar

[61] Fagerholm S, Morrice N, Gahmberg CG, Cohen P. Phosphorylation of the cytoplasmic domain of the integrin CD18 chain by protein kinase C isoforms in leukocytes. J Biol Chem. 2002;277:1728–38.10.1074/jbc.M106856200Search in Google Scholar

[62] Santoro MM, Gaudino G, Marchisio PC. The MSP receptor regulates alpha6beta4 and alpha3beta1 integrins via 14-3-3 proteins in keratinocyte migration. Dev Cell. 2003;5:257–71.10.1016/S1534-5807(03)00201-6Search in Google Scholar

[63] Deakin NO, Bass MD, Warwood S, Schoelermann J, Mostafavi-Pour Z, Knight D, et al. An integrin-alpha4-14-3-3zeta-paxillin ternary complex mediates localised Cdc42 activity and accelerates cell migration. J Cell Sci. 2009;122:1654–64.10.1242/jcs.049130Search in Google Scholar PubMed PubMed Central

[64] Eiseler T, Hausser A, De Kimpe L, Van Lint J, Pfizenmaier K. Protein kinase D controls actin polymerization and cell motility through phosphorylation of cortactin. J Biol Chem. 2010;285:18672–83.10.1074/jbc.M109.093880Search in Google Scholar PubMed PubMed Central

[65] Weaver AM. Cortactin in tumor invasiveness. Cancer Lett. 2008;265:157–66.10.1016/j.canlet.2008.02.066Search in Google Scholar

[66] Huang TY, DerMardirossian C, Bokoch GM. Cofilin phosphatases and regulation of actin dynamics. Curr Opin Cell Biol. 2006;18:26–31.10.1016/j.ceb.2005.11.005Search in Google Scholar

[67] Peterburs P, Heering J, Link G, Pfizenmaier K, Olayioye MA, Hausser A. Protein kinase D regulates cell migration by direct phosphorylation of the cofilin phosphatase slingshot 1 like. Cancer Res. 2009;69:5634–8.10.1158/0008-5472.CAN-09-0718Search in Google Scholar

[68] Ohashi K, Nagata K, Maekawa M, Ishizaki T, Narumiya S, Mizuno K. Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J Biol Chem. 2000;275:3577–82.10.1074/jbc.275.5.3577Search in Google Scholar

[69] Nagata-Ohashi K, Ohta Y, Goto K, Chiba S, Mori R, Nishita M, et al. A pathway of neuregulin-induced activation of cofilin-phosphatase Slingshot and cofilin in lamellipodia. J Cell Biol. 2004;165:465–71.10.1083/jcb.200401136Search in Google Scholar

[70] Eiseler T, Döppler H, Yan IK, Kitatani K, Mizuno K, Storz P. Protein kinase D1 regulates cofilin-mediated F-actin reorganization and cell motility through slingshot. Nat Cell Biol. 2009;11:545–56.10.1038/ncb1861Search in Google Scholar

[71] Masters SC, Subramanian RR, Truong A, Yang H, Fujii K, Zhang H, et al. Survival-promoting functions of 14-3-3 proteins. Biochem Soc Trans. 2002;30:360–5.10.1042/bst0300360Search in Google Scholar

[72] Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell. 1996;87:619–28.10.1016/S0092-8674(00)81382-3Search in Google Scholar

[73] Neal CL, Xu J, Li P, Mori S, Yang J, Neal NN, et al. Overexpression of 14-3-3zeta in cancer cells activates PI3K via binding the p85 regulatory subunit. Oncogene. 2012;31:897–906.10.1038/onc.2011.284Search in Google Scholar

[74] Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 1999;96:857–68.10.1016/S0092-8674(00)80595-4Search in Google Scholar

[75] Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer. 2009;9:537–49.10.1038/nrc2694Search in Google Scholar

[76] Weston CR, Davis RJ. The JNK signal transduction pathway. Curr Opin Cell Biol. 2007;19:142–9.10.1016/j.ceb.2007.02.001Search in Google Scholar

[77] 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 USA. 1999;96:8511–5.10.1073/pnas.96.15.8511Search in Google Scholar

[78] Cao W, Yang X, Zhou J, Teng Z, Cao L, Zhang X, et al. Targeting 14-3-3 protein, difopein induces apoptosis of human glioma cells and suppresses tumor growth in mice. Apoptosis. 2010;15:230–41.10.1007/s10495-009-0437-4Search in Google Scholar

[79] Xing H, Zhang S, Weinheimer C, Kovacs A, Muslin AJ. 14-3-3 proteins block apoptosis and differentially regulate MAPK cascades. EMBO J. 2000;19:349–58.10.1093/emboj/19.3.349Search in Google Scholar

[80] Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell. 2004;6:463–77.10.1016/S1534-5807(04)00099-1Search in Google Scholar

[81] Boya P, Reggiori F, Codogno P. Emerging regulation and functions of autophagy. Nat Cell Biol. 2013;15:713–20.10.1038/ncb2788Search in Google Scholar PubMed PubMed Central

[82] Shintani T, Klionsky DJ. Autophagy in health and disease: a double-edged sword. Science. 2004;306:990–5.10.1126/science.1099993Search in Google Scholar PubMed PubMed Central

[83] Alva AS, Gultekin SH, Baehrecke EH. Autophagy in human tumors: cell survival or death?. Cell Death Differ. 2004;11:1046–8.10.1038/sj.cdd.4401445Search in Google Scholar PubMed

[84] Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science. 2011;331:456–61.10.1126/science.1196371Search in Google Scholar PubMed PubMed Central

[85] Mendoza MC, Er EE, Blenis J. The Ras-ERK and PI3K-mTOR pathways: cross-talk and compensation. Trends Biochem Sci. 2011;36:320–8.10.1016/j.tibs.2011.03.006Search in Google Scholar PubMed PubMed Central

[86] Hardie DG. Sensing of energy and nutrients by AMP-activated protein kinase. Am J Clin Nutr. 2011;93:891S–6.10.3945/ajcn.110.001925Search in Google Scholar PubMed

[87] Hardie DG, Ross FA, Hawley SA. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol. 2012;13:251–62.10.1038/nrm3311Search in Google Scholar PubMed PubMed Central

[88] Faubert B, Vincent EE, Poffenberger MC, Jones RG. The AMP-activated protein kinase (AMPK) and cancer: many faces of a metabolic regulator. Cancer Lett. 2015;356:165–70.10.1016/j.canlet.2014.01.018Search in Google Scholar PubMed

[89] Shaw RJ. LKB1 and AMP-activated protein kinase control of mTOR signalling and growth. Acta Physiol (Oxf). 2009;196:65–80.10.1111/j.1748-1716.2009.01972.xSearch in Google Scholar PubMed PubMed Central

[90] Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell. 2008;30:214–26.10.1016/j.molcel.2008.03.003Search in Google Scholar PubMed PubMed Central

[91] Brugarolas J, Lei K, Hurley RL, Manning BD, Reiling JH, Hafen E, et al. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 2004;18:2893–904.10.1101/gad.1256804Search in Google Scholar PubMed PubMed Central

[92] DeYoung MP, Horak P, Sofer A, Sgroi D, Ellisen LW. Hypoxia regulates TSC1/2–mTOR signaling and tumor suppression through REDD1-mediated 14-3-3 shuttling. Genes Dev. 2008;22:239–51.10.1101/gad.1617608Search in Google Scholar PubMed PubMed Central

[93] Sofer A, Lei K, Johannessen CM, Ellisen LW. Regulation of mTOR and cell growth in response to energy stress by REDD1. Mol Cell Biol. 2005;25:5834–45.10.1128/MCB.25.14.5834-5845.2005Search in Google Scholar PubMed PubMed Central

[94] Cai S-L, Tee AR, Short JD, Bergeron JM, Kim J, Shen J, et al. Activity of TSC2 is inhibited by AKT-mediated phosphorylation and membrane partitioning. J Cell Biol. 2006;173:279–89.10.1083/jcb.200507119Search in Google Scholar PubMed PubMed Central

[95] Huang J, Manning BD. A complex interplay between Akt, TSC2 and the two mTOR complexes. Biochem Soc Trans. 2009;37:217–22.10.1042/BST0370217Search in Google Scholar PubMed PubMed Central

[96] Oshiro N, Takahashi R, Yoshino K, Tanimura K, Nakashima A, Eguchi S, et al. The proline-rich Akt substrate of 40 kDa (PRAS40) is a physiological substrate of mammalian target of rapamycin complex 1. J Biol Chem. 2007;282:20329–39.10.1074/jbc.M702636200Search in Google Scholar PubMed PubMed Central

[97] McKay MM, Morrison DK. Integrating signals from RTKs to ERK/MAPK. Oncogene. 2007;26:3113–21.10.1038/sj.onc.1210394Search in Google Scholar PubMed

[98] Rozengurt E. Mitogenic signaling pathways induced by G protein-coupled receptors. J Cell Physiol. 2007;213:589–602.10.1002/jcp.21246Search in Google Scholar PubMed

[99] Wang J, Whiteman MW, Lian H, Wang G, Singh A, Huang D, et al. A non-canonical MEK/ERK signaling pathway regulates autophagy via regulating Beclin 1. J Biol Chem. 2009;284:21412–24.10.1074/jbc.M109.026013Search in Google Scholar PubMed PubMed Central

[100] Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 1999;402:672–6.10.1038/45257Search in Google Scholar PubMed

[101] Dumaz N, Marais R. Protein kinase A blocks Raf-1 activity by stimulating 14-3-3 binding and blocking Raf-1 interaction with Ras. J Biol Chem. 2003;278:29819–23.10.1074/jbc.C300182200Search in Google Scholar PubMed

[102] Dhillon AS, Meikle S, Peyssonnaux C, Grindlay J, Kaiser C, Steen H, et al. A Raf-1 mutant that dissociates MEK/extracellular signal-regulated kinase activation from malignant transformation and differentiation but not proliferation. Mol Cell Biol. 2003;23:1983–93.10.1128/MCB.23.6.1983-1993.2003Search in Google Scholar PubMed PubMed Central

[103] Grozinger CM, Schreiber SL. Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc Natl Acad Sci USA. 2000;97:7835–40.10.1073/pnas.140199597Search in Google Scholar PubMed PubMed Central

[104] Kanai F, Marignani PA, Sarbassova D, Yagi R, Hall RA, Donowitz M, et al. TAZ: a novel transcriptional co-activator regulated by interactions with 14-3-3 and PDZ domain proteins. EMBO J. 2000;19:6778–91.10.1093/emboj/19.24.6778Search in Google Scholar PubMed PubMed Central

[105] 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;27:88–99.10.1038/sj.emboj.7601954Search in Google Scholar PubMed PubMed Central

[106] McKinsey TA, Zhang CL, Olson EN. Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. Proc Natl Acad Sci U S A. 2000;97:14400–5.10.1073/pnas.260501497Search in Google Scholar PubMed PubMed Central

[107] Greer EL, Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene. 2005;24:7410–25.10.1038/sj.onc.1209086Search in Google Scholar PubMed

[108] Webb AE, Brunet A. FOXO transcription factors: key regulators of cellular quality control. Trends Biochem Sci. 2014;39:159–69.10.1016/j.tibs.2014.02.003Search in Google Scholar PubMed PubMed Central

[109] Medema RH, Kops GJ, Bos JL, Burgering BM. AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature. 2000;404:782–7.10.1038/35008115Search in Google Scholar PubMed

[110] Brunet A, Kanai F, Stehn J, Xu J, Sarbassova D, Frangioni JV, et al. 14-3-3 transits to the nucleus and participates in dynamic nucleocytoplasmic transport. J Cell Biol. 2002;156:817–28.10.1083/jcb.200112059Search in Google Scholar PubMed PubMed Central

[111] Stavridi ES, Chehab NH, Malikzay A, Halazonetis TD. Substitutions that compromise the ionizing radiation-induced association of p53 with 14-3-3 proteins also compromise the ability of p53 to induce cell cycle arrest. Cancer Res. 2001;61:7030–3.Search in Google Scholar

[112] Waterman MJ, Stavridi ES, Waterman JL, Halazonetis TD. ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nat Genet. 1998;19:175–8.10.1038/542Search in Google Scholar PubMed

[113] Beck T, Hall MN. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature. 1999;402:689–92.10.1038/45287Search in Google Scholar PubMed

[114] Kakiuchi K, Yamauchi Y, Taoka M, Iwago M, Fujita T, Ito T, et al. Proteomic analysis of in vivo 14-3-3 interactions in the yeast Saccharomyces cerevisiae. Biochemistry. 2007;46:7781–92.10.1021/bi700501tSearch in Google Scholar PubMed

[115] Parua PK, Dombek KM, Young ET. Yeast 14-3-3 protein functions as a comodulator of transcription by inhibiting coactivator functions. J Biol Chem. 2014;289:35542–60.10.1074/jbc.M114.592287Search in Google Scholar PubMed PubMed Central

[116] Morrison DK. The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol. 2009;19:16–23.10.1016/j.tcb.2008.10.003Search in Google Scholar PubMed PubMed Central

[117] Tzivion G, Gupta VS, Kaplun L, Balan V. 14-3-3 proteins as potential oncogenes. Semin Cancer Biol. 2006;16:203–13.10.1016/j.semcancer.2006.03.004Search in Google Scholar PubMed

[118] Luo J, Feng J, Lu J, Wang Y, Tang X, Xie F, et al. Aberrant methylation profile of 14-3-3 sigma and its reduced transcription/expression levels in Chinese sporadic female breast carcinogenesis. Med Oncol. 2010;27:791–7.10.1007/s12032-009-9287-8Search in Google Scholar PubMed

[119] Zurita M, Lara PC, del Moral R, Torres B, Linares-Fernandez JL, Arrabal SR, et al. Hypermethylated 14-3-3-sigma and ESR1 gene promoters in serum as candidate biomarkers for the diagnosis and treatment efficacy of breast cancer metastasis. BMC Cancer. 2010;10:217.10.1186/1471-2407-10-217Search in Google Scholar PubMed PubMed Central

[120] Lodygin D, Diebold J, Hermeking H. Prostate cancer is characterized by epigenetic silencing of 14-3-3sigma expression. Oncogene. 2004;23:9034–41.10.1038/sj.onc.1208004Search in Google Scholar PubMed

[121] Moreira JM, Gromov P, Celis JE. Expression of the tumor suppressor protein 14-3-3 sigma is down-regulated in invasive transitional cell carcinomas of the urinary bladder undergoing epithelial-to-mesenchymal transition. Mol Cell Proteomics. 2004;3:410–9.10.1074/mcp.M300134-MCP200Search in Google Scholar PubMed

[122] Iwata N, Yamamoto H, Sasaki S, Itoh F, Suzuki H, Kikuchi T, et al. Frequent hypermethylation of CpG islands and loss of expression of the 14-3-3 sigma gene in human hepatocellular carcinoma. Oncogene. 2000;19:5298–302.10.1038/sj.onc.1203898Search in Google Scholar PubMed

[123] Ye M, Huang T, Ying Y, Li J, Yang P, Ni C, et al. Detection of 14-3-3 sigma (sigma) promoter methylation as a noninvasive biomarker using blood samples for breast cancer diagnosis. Oncotarget. 2017;8:9230–42.10.18632/oncotarget.13992Search in Google Scholar PubMed PubMed Central

[124] Yang H, Wen YY, Zhao R, Lin YL, Fournier K, Yang HY, et al. DNA damage-induced protein 14-3-3 sigma inhibits protein kinase B/Akt activation and suppresses Akt-activated cancer. Cancer Res. 2006;66:3096–105.10.1158/0008-5472.CAN-05-3620Search in Google Scholar PubMed

[125] Ling C, Zuo D, Xue B, Muthuswamy S, Muller WJ. A novel role for 14-3-3sigma in regulating epithelial cell polarity. Genes Dev. 2010;24:947–56.10.1101/gad.1896810Search in Google Scholar PubMed PubMed Central

[126] Tsai JH, Yang J. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev. 2013;27:2192–206.10.1101/gad.225334.113Search in Google Scholar

[127] Raychaudhuri K, Chaudhary N, Gurjar M, D’Souza R, Limzerwala J, Maddika S, et al. 14-3-3sigma gene loss leads to activation of the epithelial to mesenchymal transition due to the stabilization of c-Jun protein. J Biol Chem. 2016;291:16068–81.10.1074/jbc.M116.723767Search in Google Scholar

[128] Danes CG, Wyszomierski SL, Lu J, Neal CL, Yang W, Yu D. 14-3-3 zeta down-regulates p53 in mammary epithelial cells and confers luminal filling. Cancer Res. 2008;68:1760–7.10.1158/0008-5472.CAN-07-3177Search in Google Scholar

[129] Rehman SK, Li SH, Wyszomierski SL, Wang Q, Li P, Sahin O, et al. 14-3-3zeta orchestrates mammary tumor onset and progression via miR-221-mediated cell proliferation. Cancer Res. 2014;74:363–73.10.1158/0008-5472.CAN-13-2016Search in Google Scholar

[130] Jin LM, Han XH, Jie YQ, Meng SS. 14-3-3zeta silencing retards tongue squamous cell carcinoma progression by inhibiting cell survival and migration. Cancer Gene Ther. 2016;23:206–13.10.1038/cgt.2016.15Search in Google Scholar

[131] Xu J, Acharya S, Sahin O, Zhang Q, Saito Y, Yao J, et al. 14-3-3zeta turns TGF-beta’s function from tumor suppressor to metastasis promoter in breast cancer by contextual changes of Smad partners from p53 to Gli2. Cancer Cell. 2015;27:177–92.10.1016/j.ccell.2014.11.025Search in Google Scholar

[132] Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell. 2003;3:537–49.10.1016/S1535-6108(03)00132-6Search in Google Scholar

[133] Waning DL, Guise TA. Molecular mechanisms of bone metastasis and associated muscle weakness. Clin Cancer Res. 2014;20:3071–7.10.1158/1078-0432.CCR-13-1590Search in Google Scholar PubMed PubMed Central

[134] Bergamaschi A, Katzenellenbogen BS. Tamoxifen downregulation of miR-451 increases 14-3-3zeta and promotes breast cancer cell survival and endocrine resistance. Oncogene. 2012;31:39–47.10.1038/onc.2011.223Search in Google Scholar PubMed PubMed Central

[135] Matta A, DeSouza LV, Ralhan R, Siu KW. Small interfering RNA targeting 14-3-3zeta increases efficacy of chemotherapeutic agents in head and neck cancer cells. Mol Cancer Ther. 2010;9:2676–88.10.1158/1535-7163.MCT-10-0312Search in Google Scholar PubMed

[136] Maxwell SA, Li Z, Jaye D, Ballard S, Ferrell J, Fu H. 14-3-3zeta mediates resistance of diffuse large B cell lymphoma to an anthracycline-based chemotherapeutic regimen. J Biol Chem. 2009;284:22379–89.10.1074/jbc.M109.022418Search in Google Scholar PubMed PubMed Central

[137] Phan LM, Yeung SC, Lee MH. Cancer metabolic reprogramming: importance, main features, and potentials for precise targeted anti-cancer therapies. Cancer Biol Med. 2014;11:1–19.Search in Google Scholar

[138] Phan L, Chou PC, Velazquez-Torres G, Samudio I, Parreno K, Huang Y, et al. The cell cycle regulator 14-3-3sigma opposes and reverses cancer metabolic reprogramming. Nat Commun. 2015;6:7530.10.1038/ncomms8530Search in Google Scholar PubMed PubMed Central

[139] Chang CC, Zhang C, Zhang Q, Sahin O, Wang H, Xu J, et al. Upregulation of lactate dehydrogenase a by 14-3-3zeta leads to increased glycolysis critical for breast cancer initiation and progression. Oncotarget. 2016;7:35270–83.10.18632/oncotarget.9136Search in Google Scholar PubMed PubMed Central

[140] Mukhopadhyay A, Sehgal L, Bose A, Gulvady A, Senapati P, Thorat R, et al. 14-3-3gamma prevents centrosome amplification and neoplastic progression. Sci Rep. 2016;6:26580.10.1038/srep26580Search in Google Scholar PubMed PubMed Central

[141] Xiao Y, Lin VY, Ke S, Lin GE, Lin FT, Lin WC. 14-3-3tau promotes breast cancer invasion and metastasis by inhibiting RhoGDIalpha. Mol Cell Biol. 2014;34:2635–49.10.1128/MCB.00076-14Search in Google Scholar PubMed PubMed Central

[142] Sun N, Wu Y, Huang B, Liu Q, Dong Y, Ding J, et al. Decreased expression of 14-3-3 sigma, an early event of malignant transformation of respiratory epithelium, also facilitates progression of squamous cell lung cancer. Thorac Cancer. 2015;6:715–21.10.1111/1759-7714.12246Search in Google Scholar PubMed PubMed Central

[143] Pereira-Faca SR, Kuick R, Puravs E, Zhang Q, Krasnoselsky AL, Phanstiel D, et al. Identification of 14-3-3 theta as an antigen that induces a humoral response in lung cancer. Cancer Res. 2007;67:12000–6.10.1158/0008-5472.CAN-07-2913Search in Google Scholar PubMed

[144] Niemantsverdriet M, Wagner K, Visser M, Backendorf C. Cellular functions of 14-3-3 zeta in apoptosis and cell adhesion emphasize its oncogenic character. Oncogene. 2008;27:1315–9.10.1038/sj.onc.1210742Search in Google Scholar PubMed

[145] Li Z, Zhao J, Du Y, Park HR, Sun SY, Bernal-Mizrachi L, et al. Down-regulation of 14-3-3zeta suppresses anchorage-independent growth of lung cancer cells through anoikis activation. Proc Natl Acad Sci USA. 2008;105:162–7.10.1073/pnas.0710905105Search in Google Scholar PubMed PubMed Central

[146] Fan T, Li R, Todd NW, Qiu Q, Fang HB, Wang H, et al. Up-regulation of 14-3-3zeta in lung cancer and its implication as prognostic and therapeutic target. Cancer Res. 2007;67:7901–6.10.1158/0008-5472.CAN-07-0090Search in Google Scholar PubMed

[147] Zhao G-Y, Ding J-Y, Gu J, Lu C-L, Lin Z-W, Guo J, et al. The overexpression of 14-3-3ζ and Hsp27 promotes non–small cell lung cancer progression. Cancer. 2014;120:652–63.10.1002/cncr.28452Search in Google Scholar PubMed

[148] Tong S, Xia T, Fan K, Jiang K, Zhai W, Li JS, et al. 14-3-3zeta promotes lung cancer cell invasion by increasing the Snail protein expression through atypical protein kinase C (aPKC)/NF-kappaB signaling. Exp Cell Res. 2016;348:1–9.10.1016/j.yexcr.2016.08.014Search in Google Scholar PubMed

[149] Song T, Tian X, Kai F, Ke J, Wei Z, Jing-Song L, et al. Loss of Par3 promotes lung adenocarcinoma metastasis through 14-3-3zeta protein. Oncotarget. 2016;7:64260–73.10.18632/oncotarget.11728Search in Google Scholar PubMed PubMed Central