38
Views
30
CrossRef citations to date
0
Altmetric
Article

Dual Phosphorylation of Btk by Akt/Protein Kinase B Provides Docking for 14-3-3ζ, Regulates Shuttling, and Attenuates both Tonic and Induced Signaling in B Cells

, , , , &
Pages 3214-3226 | Received 04 Mar 2013, Accepted 05 Jun 2013, Published online: 20 Mar 2023

REFERENCES

  • Smith CI, Islam TC, Mattsson PT, Mohamed AJ, Nore BF, Vihinen M. 2001. The Tec family of cytoplasmic tyrosine kinases: mammalian Btk, Bmx, Itk, Tec, Txk and homologs in other species. Bioessays 23:436–446.
  • Kurosaki T, Hikida M. 2009. Tyrosine kinases and their substrates in B lymphocytes. Immunol. Rev. 228:132–148.
  • Yang WC, Collette Y, Nunes J, Olive D. 2000. Tec kinases: a family with multiple roles in immunity. Immunity 12:373–382.
  • Tsukada S, Saffran DC, Rawlings DJ, Parolini O, Allen RC, Klisak I, Sparkes RS, Kubagawa H, Mohandas T, Quan S, Belmont JW, Cooper MD, Conley ME, Witte ON. 1993. Deficient expression of a B cell cytoplasmic tyrosine kinase in human X-linked agammaglobulinemia. Cell 72:279–290.
  • Vetrie D, Vorechovsky I, Sideras P, Holland J, Davies A, Flinter F, Hammarstrom L, Kinnon C, Levinsky R, Bobrow M, Edvard Smith CI, Bentley DR. 1993. The gene involved in X-linked agammaglobulinaemia is a member of the src family of protein-tyrosine kinases. Nature 361:226–233.
  • Rawlings DJ, Saffran DC, Tsukada S, Largaespada DA, Grimaldi JC, Cohen L, Mohr RN, Bazan JF, Howard M, Copeland NG, Jenkins NA, Witte ON. 1993. Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice. Science 261:358–361.
  • Thomas JD, Sideras P, Smith CI, Vorechovsky I, Chapman V, Paul WE. 1993. Colocalization of X-linked agammaglobulinemia and X-linked immunodeficiency genes. Science 261:355–358.
  • Nore BF, Vargas L, Mohamed AJ, Branden LJ, Backesjo CM, Islam TC, Mattsson PT, Hultenby K, Christensson B, Smith CI. 2000. Redistribution of Bruton's tyrosine kinase by activation of phosphatidylinositol 3-kinase and Rho-family GTPases. Eur. J. Immunol. 30:145–154.
  • Reth M, Brummer T. 2004. Feedback regulation of lymphocyte signalling. Nat. Rev. Immunol. 4:269–277.
  • Mohamed AJ, Yu L, Backesjo CM, Vargas L, Faryal R, Aints A, Christensson B, Berglof A, Vihinen M, Nore BF, Smith CI. 2009. Bruton's tyrosine kinase (Btk): function, regulation, and transformation with special emphasis on the PH domain. Immunol. Rev. 228:58–73.
  • Park H, Wahl MI, Afar DE, Turck CW, Rawlings DJ, Tam C, Scharenberg AM, Kinet JP, Witte ON. 1996. Regulation of Btk function by a major autophosphorylation site within the SH3 domain. Immunity 4:515–525.
  • Kang SW, Wahl MI, Chu J, Kitaura J, Kawakami Y, Kato RM, Tabuchi R, Tarakhovsky A, Kawakami T, Turck CW, Witte ON, Rawlings DJ. 2001. PKCbeta modulates antigen receptor signaling via regulation of Btk membrane localization. EMBO J. 20:5692–5702.
  • Vargas L, Nore BF, Berglof A, Heinonen JE, Mattsson PT, Smith CI, Mohamed AJ. 2002. Functional interaction of caveolin-1 with Bruton's tyrosine kinase and Bmx. J. Biol. Chem. 277:9351–9357.
  • Crosby D, Poole AW. 2002. Interaction of Bruton's tyrosine kinase and protein kinase Ctheta in platelets. Cross-talk between tyrosine and serine/threonine kinases. J. Biol. Chem. 277:9958–9965.
  • Yu L, Mohamed AJ, Vargas L, Berglof A, Finn G, Lu KP, Smith CI. 2006. Regulation of Bruton tyrosine kinase by the peptidylprolyl isomerase Pin1. J. Biol. Chem. 281:18201–18207.
  • Moore BW, Perez VJ. 1967. Specific acidic proteins of the nervous system, p 343–359.InCarlson FD (ed),Physiological and biochemical aspects of nervous integration. Prentice-Hall, Englewood Cliffs, NJ.
  • Muslin AJ, Tanner JW, Allen PM, Shaw AS. 1996. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84:889–897.
  • Morrison DK. 2009. The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol. 19:16–23.
  • Fu H, Subramanian RR, Masters SC. 2000. 14-3-3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 40:617–647.
  • Yaffe MB, Rittinger K, Volinia S, Caron PR, Aitken A, Leffers H, Gamblin SJ, Smerdon SJ, Cantley LC. 1997. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91:961–971.
  • 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.
  • Kovacina KS, Park GY, Bae SS, Guzzetta AW, Schaefer E, Birnbaum MJ, Roth RA. 2003. Identification of a proline-rich Akt substrate as a 14-3-3 binding partner. J. Biol. Chem. 278:10189–10194.
  • Lindvall JM, Blomberg KE, Berglof A, Yang Q, Smith CI, Islam TC. 2004. Gene expression profile of B cells from Xid mice and Btk knockout mice. Eur. J. Immunol. 34:1981–1991.
  • Gustafsson MO, Hussain A, Mohammad DK, Mohamed AJ, Nguyen V, Metalnikov P, Colwill K, Pawson T, Smith CI, Nore BF. 2012. Regulation of nucleocytoplasmic shuttling of Bruton's tyrosine kinase (Btk) through a novel SH3-dependent interaction with ankyrin repeat domain 54 (ANKRD54). Mol. Cell. Biol. 32:2440–2453.
  • Mohamed AJ, Vargas L, Nore BF, Backesjo CM, Christensson B, Smith CI. 2000. Nucleocytoplasmic shuttling of Bruton's tyrosine kinase. J. Biol. Chem. 275:40614–40619.
  • Heinonen JE, Smith CI, Nore BF. 2002. Silencing of Bruton's tyrosine kinase (Btk) using short interfering RNA duplexes (siRNA). FEBS Lett. 527:274–278.
  • Lindvall J, Islam TC. 2002. Interaction of Btk and Akt in B cell signaling. Biochem. Biophys. Res. Commun. 293:1319–1326.
  • Honigberg LA, Smith AM, Sirisawad M, Verner E, Loury D, Chang B, Li S, Pan Z, Thamm DH, Miller RA, Buggy JJ. 2010. The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proc. Natl. Acad. Sci. U. S. A. 107:13075–13080.
  • Mancini M, Corradi V, Petta S, Barbieri E, Manetti F, Botta M, Santucci MA. 2011. 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. 336:596–604.
  • Gu M, Du X. 1998. A novel ligand-binding site in the zeta-form 14-3-3 protein recognizing the platelet glycoprotein Ibalpha and distinct from the c-Raf-binding site. J. Biol. Chem. 273:33465–33471.
  • Tzivion G, Shen YH, Zhu J. 2001. 14-3-3 proteins; bringing new definitions to scaffolding. Oncogene 20:6331–6338.
  • Dubois T, Howell S, Amess B, Kerai P, Learmonth M, Madrazo J, Chaudhri M, Rittinger K, Scarabel M, Soneji Y, Aitken A. 1997. Structure and sites of phosphorylation of 14-3-3 protein: role in coordinating signal transduction pathways. J. Protein Chem. 16:513–522.
  • Liu YC, Liu Y, Elly C, Yoshida H, Lipkowitz S, Altman A. 1997. Serine phosphorylation of Cbl induced by phorbol ester enhances its association with 14-3-3 proteins in T cells via a novel serine-rich 14-3-3-binding motif. J. Biol. Chem. 272:9979–9985.
  • Obata T, Yaffe MB, Leparc GG, Piro ET, Maegawa H, Kashiwagi A, Kikkawa R, Cantley LC. 2000. Peptide and protein library screening defines optimal substrate motifs for AKT/PKB. J. Biol. Chem. 275:36108–36115.
  • Fayard E, Xue G, Parcellier A, Bozulic L, Hemmings BA. 2010. Protein kinase B (PKB/Akt), a key mediator of the PI3K signaling pathway. Curr. Top. Microbiol. Immunol. 346:31–56.
  • Manning BD, Cantley LC. 2007. AKT/PKB signaling: navigating downstream. Cell 129:1261–1274.
  • Yoeli-Lerner M, Toker A. 2006. Akt/PKB signaling in cancer: a function in cell motility and invasion. Cell Cycle 5:603–605.
  • Barnett SF, Bilodeau MT, Lindsley CW. 2005. The Akt/PKB family of protein kinases: a review of small molecule inhibitors and progress towards target validation. Curr. Top. Med. Chem. 5:109–125.
  • Song G, Ouyang G, Bao S. 2005. The activation of Akt/PKB signaling pathway and cell survival. J. Cell. Mol. Med. 9:59–71.
  • St-Germain ME, Gagnon V, Parent S, Asselin E. 2004. Regulation of COX-2 protein expression by Akt in endometrial cancer cells is mediated through NF-kappaB/IkappaB pathway. Mol. Cancer 3:7.
  • Lam KP, Kuhn R, Rajewsky K. 1997. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 90:1073–1083.
  • Monroe JG. 2006. ITAM-mediated tonic signalling through pre-BCR and BCR complexes. Nat. Rev. Immunol. 6:283–294.
  • Deane JA, Fruman DA. 2004. Phosphoinositide 3-kinase: diverse roles in immune cell activation. Annu. Rev. Immunol. 22:563–598.
  • Yusuf I, Zhu X, Kharas MG, Chen J, Fruman DA. 2004. Optimal B-cell proliferation requires phosphoinositide 3-kinase-dependent inactivation of FOXO transcription factors. Blood 104:784–787.
  • Hinman RM, Bushanam JN, Nichols WA, Satterthwaite AB. 2007. B cell receptor signaling down-regulates forkhead box transcription factor class O 1 mRNA expression via phosphatidylinositol 3-kinase and Bruton's tyrosine kinase. J. Immunol. 178:740–747.
  • Huang H, Regan KM, Lou Z, Chen J, Tindall DJ. 2006. CDK2-dependent phosphorylation of FOXO1 as an apoptotic response to DNA damage. Science 314:294–297.
  • Kops GJ, de Ruiter ND, De Vries-Smits AM, Powell DR, Bos JL, Burgering BM. 1999. Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 398:630–634.
  • Webb CF, Yamashita Y, Ayers N, Evetts S, Paulin Y, Conley ME, Smith EA. 2000. The transcription factor Bright associates with Bruton's tyrosine kinase, the defective protein in immunodeficiency disease. J. Immunol. 165:6956–6965.
  • Lai S, O'Callaghan B, Zoghbi HY, Orr HT. 2011. 14-3-3 binding to ataxin-1(ATXN1) regulates its dephosphorylation at Ser-776 and transport to the nucleus. J. Biol. Chem. 286:34606–34616.
  • Mancini M, Veljkovic N, Corradi V, Zuffa E, Corrado P, Pagnotta E, Martinelli G, Barbieri E, Santucci MA. 2009. 14-3-3 ligand prevents nuclear import of c-ABL protein in chronic myeloid leukemia. Traffic 10:637–647.
  • 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.
  • McKinsey TA, Zhang CL, Lu J, Olson EN. 2000. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408:106–111.
  • Wang AH, Kruhlak MJ, Wu J, Bertos NR, Vezmar M, Posner BI, Bazett-Jones DP, Yang XJ. 2000. Regulation of histone deacetylase 4 by binding of 14-3-3 proteins. Mol. Cell. Biol. 20:6904–6912.
  • Ha CH, Kim JY, Zhao J, Wang W, Jhun BS, Wong C, Jin ZG. 2010. PKA phosphorylates histone deacetylase 5 and prevents its nuclear export, leading to the inhibition of gene transcription and cardiomyocyte hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 107:15467–15472.
  • Ciechanover A, Orian A, Schwartz AL. 2000. Ubiquitin-mediated proteolysis: biological regulation via destruction. Bioessays 22:442–451.
  • Yu L, Mohamed AJ, Simonson OE, Vargas L, Blomberg KE, Bjorkstrand B, Arteaga HJ, Nore BF, Smith CI. 2008. Proteasome-dependent autoregulation of Bruton tyrosine kinase (Btk) promoter via NF-kappaB. Blood 111:4617–4626.
  • LeBron C, Chen L, Gilkes DM, Chen J. 2006. Regulation of MDMX nuclear import and degradation by Chk2 and 14-3-3. EMBO J. 25:1196–1206.
  • Wang X, Li JP, Chiu LL, Lan JL, Chen DY, Boomer J, Tan TH. 2012. Attenuation of T cell receptor signaling by serine phosphorylation-mediated lysine-30 ubiquitination of SLP-76. J. Biol. Chem. 287:34091–34100.
  • Wang X, Li JP, Kuo HK, Chiu LL, Dement GA, Lan JL, Chen DY, Yang CY, Hu H, Tan TH. 2012. Down-regulation of B cell receptor signaling by hematopoietic progenitor kinase 1 (HPK1)-mediated phosphorylation and ubiquitination of activated B cell linker protein (BLNK). J. Biol. Chem. 287:11037–11048.
  • Porter GW, Khuri FR, Fu H. 2006. Dynamic 14-3-3/client protein interactions integrate survival and apoptotic pathways. Semin. Cancer Biol. 16:193–202.
  • Pozuelo Rubio M, Geraghty KM, Wong BH, Wood NT, Campbell DG, Morrice N, Mackintosh C. 2004. 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem. J. 379:395–408.
  • van Heusden GP. 2005. 14-3-3 proteins: regulators of numerous eukaryotic proteins. IUBMB Life 57:623–629.
  • Johnson C, Crowther S, Stafford MJ, Campbell DG, Toth R, MacKintosh C. 2010. Bioinformatic and experimental survey of 14-3-3-binding sites. Biochem. J. 427:69–78.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.