TAPP1 and TAPP2 Are Targets of Phosphatidylinositol 3-Kinase Signaling in B Cells: Sustained Plasma Membrane Recruitment Triggered by the B-Cell Antigen Receptor

REFERENCES

• Aagaard Tillery, K. M., and D. F. Jelinek. 1996. Phosphatidylinositol 3-kinase activation in normal human B lymphocytes: differential sensitivity of growth and differentiation to wortmannin. J. Immunol. 156: 4543–4554.
   PubMedGoogle Scholar
• Aman, M. J., T. D. Lamkin, H. Okada, T. Kurosaki, and K. S. Ravichandran. 1998. The inositol phosphatase SHIP inhibits Akt/PKB activation in B cells. J. Biol. Chem. 273: 33922–33928.
   PubMed Web of Science ®Google Scholar
• Anderson, K. E., P. Lipp, M. Bootman, S. H. Ridley, J. Coadwell, L. Ronnstrand, J. Lennartsson, A. B. Holmes, G. F. Painter, J. Thuring, Z. Lim, H. Erdjument-Bromage, A. Grewal, P. Tempst, L. R. Stephens, and P. T. Hawkins. 2000. DAPP1 undergoes a PI 3-kinase-dependent cycle of plasma-membrane recruitment and endocytosis upon cell stimulation. Curr. Biol. 10: 1403–1412.
   PubMedGoogle Scholar
• Astoul, E., S. Watton, and D. Cantrell. 1999. The dynamics of protein kinase B regulation during B cell antigen receptor engagement. J. Cell Biol. 145: 1511–1520.
   PubMedGoogle Scholar
• Beitz, L. O., D. A. Fruman, T. Kurosaki, L. C. Cantley, and A. M. Scharenberg. 1999. SYK is upstream of phosphoinositide 3-kinase in B cell receptor signaling. J. Biol. Chem. 274: 32662–32666.
   PubMedGoogle Scholar
• Bolland, S., R. N. Pearse, T. Kurosaki, and J. V. Ravetch. 1998. SHIP modulates immune receptor responses by regulating membrane association of Btk. Immunity 8: 509–516.
   PubMed Web of Science ®Google Scholar
• Brauweiler, A. M., I. Tamir, and J. C. Cambier. 2000. Bilevel control of B-cell activation by the inositol 5-phosphatase SHIP. Immunol. Rev. 176: 69–74.
   PubMedGoogle Scholar
• Buhl, A. M., C. M. Pleiman, R. C. Rickert, and J. C. Cambier. 1997. Qualitative regulation of B cell antigen receptor signaling by CD19: selective requirement for PI 3-kinase activation, inositol-1,4,5-trisphosphate production and Ca2+ mobilization. J. Exp. Med. 186: 1897–1910.
   PubMed Web of Science ®Google Scholar
• Choquet, D., M. Partiseti, S. Amigorena, C. Bonnerot, W. H. Fridman, and H. Korn. 1993. Cross-linking of IgG receptors inhibits membrane immunoglobulin-stimulated calcium influx in B lymphocytes. J. Cell Biol. 121: 355–363.
   PubMedGoogle Scholar
• Craxton, A., A. Jiang, T. Kurosaki, and E. A. Clark. 1999. Syk and Bruton's tyrosine kinase are required for B cell antigen receptor-mediated activation of the kinase Akt. J. Biol. Chem. 274: 30644–30650.
   PubMed Web of Science ®Google Scholar
• Damen, J. E., L. Liu, P. Rosten, R. K. Humphries, A. B. Jefferson, P. W. Majerus, and G. Krystal. 1996. The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-triphosphate 5-phosphatase. Proc. Natl. Acad. Sci. USA 93: 1689–1693.
   PubMed Web of Science ®Google Scholar
• Dowler, S., R. A. Currie, D. G. Campbell, M. Deak, G. Kular, C. P. Downes, and D. R. Alessi. 2000. Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities. Biochem. J. 351: 19–31.
   PubMed Web of Science ®Google Scholar
• Dowler, S., R. A. Currie, C. P. Downs, and D. R. Alessi. 1999. DAPP1: a dual adaptor for phosphotyrosine and 3-phosphoinositides. Biochem. J. 342: 7–12.
   PubMedGoogle Scholar
• Floto, R. A., M. P. Mahaut-Smith, B. Somasundaram, and J. M. Allen. 1995. IgG-induced Ca2+ oscillations in differentiated U937 cells; a study using laser scanning confocal microscopy and co-loaded fluo-3 and fura-red fluorescent probes. Cell Calcium 18: 377–389.
   PubMedGoogle Scholar
• Fruman, D. A., S. B. Snapper, C. M. Yballe, L. Davidson, J. Y. Yu, F. W. Alt, and L. C. Cantley. 1999. Impaired B cell development and proliferation in the absence of phosphoinositide 3-kinase p85α. Science 283: 393–397.
   PubMed Web of Science ®Google Scholar
• Garcia, P., R. Gupta, S. Shah, A. J. Morris, S. A. Rudge, S. Scarlata, V. Petrova, S. McLaughlin, and M. J. Rebecchi. 1995. The pleckstrin homology domain of phospholipase C-δ1 binds with high affinity to phosphatidylinositol 4,5-bisphosphate in bilayer membranes. Biochemistry 34: 16228–16234.
   PubMedGoogle Scholar
• Gold, M., and R. Aebersold. 1994. Both phosphatidylinositol 3-kinase and phosphatidylinositol 4-kinase products are increased by antigen receptor signaling in B cells. J. Immunol. 152: 42–50.
   PubMedGoogle Scholar
• Gold, M., V. Chan, C. W. Turck, and A. DeFranco. 1992. Membrane Ig cross-linking regulates phosphatidylinositol 3-kinase in B lymphocytes. J. Immunol. 148: 2012–2022.
   PubMedGoogle Scholar
• Gold, M. R. 2000. Intermediary signaling effectors coupling the B-cell receptor to the nucleus. Curr. Top. Microbiol. Immunol. 245: 77–134.
   PubMedGoogle Scholar
• Gold, M. R., M. P. Scheid, L. Santos, M. Dang-Lawson, R. A. Roth, L. Matsuuchi, V. Duronio, and D. L. Krebs. 1999. The B cell antigen receptor activates the Akt (protein kinase B)/glycogen synthase kinase-3 signaling pathway via phosphatidylinositol 3-kinase. J. Immunol. 163: 1894–1905.
   PubMed Web of Science ®Google Scholar
• Helgason, C. D., C. P. Kalberer, J. E. Damen, S. M. Chappel, N. Pineault, G. Krystal, and R. K. Humphries. 2000. A dual role for Src homology 2 domain-containing inositol-5-phosphatase (SHIP) in immunity: aberrant development and enhanced function of B lymphocytes in SHIP−/− mice. J. Exp. Med. 191: 781–794.
   PubMedGoogle Scholar
• Hirose, K., S. Kadowaki, M. Tanabe, H. Takeshima, and M. Iino. 1999. Spatiotemporal dynamics of inositol 1,4,5-trisphosphate that underlies complex Ca2+ mobilization patterns. Science 284: 1527–1530.
   PubMed Web of Science ®Google Scholar
• Huber, M., C. D. Helgason, M. P. Scheid, V. Duronio, R. K. Humphries, and G. Krystal. 1998. Targeted disruption of SHIP leads to Steel factor-induced degranulation of mast cells. EMBO J. 17: 7311–7319.
   PubMed Web of Science ®Google Scholar
• Isakoff, S. J., T. Cardozo, J. Andreev, Z. Li, K. M. Ferguson, R. Abagyan, M. A. Lemmon, A. Aronheim, and E. Y. Skolnik. 1998. Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast. EMBO J. 17: 5374–5387.
   PubMed Web of Science ®Google Scholar
• Kurosaki, T. 1999. Genetic analysis of B cell antigen receptor signaling. Annu. Rev. Immunol. 17: 555–592.
   PubMed Web of Science ®Google Scholar
• Lander, E. S., L. M. Linton, B. Birren, C. Nusbaum, M. C. Zody, J. Baldwin, K. Devon, K. Dewar, M. Doyle, W. FitzHugh, R. Funke, D. Gage, K. Harris, A. Heaford, J. Howland, L. Kann, J. Lehoczky, R. LeVine, P. McEwan, K. McKernan, J. Meldrim, J. P. Mesirov, C. Miranda, W. Morris, J. Naylor, C. Raymond, M. Rosetti, R. Santos, A. Sheridan, C. Sougnez, N. Stange-Thomann, N. Stojanovic, A. Subramanian, D. Wyman, J. Rogers, J. Sulston, R. Ainscough, S. Beck, D. Bentley, J. Burton, C. Clee, N. Carter, A. Coulson, R. Deadman, P. Deloukas, A. Dunham, I. Dunham, R. Durbin, L. French, D. Grafham, S. Gregory, T. Hubbard, S. Humphray, A. Hunt, M. Jones, C. Lloyd, A. McMurray, L. Matthews, S. Mercer, S. Milne, J. C. Mullikin, A. Mungall, R. Plumb, M. Ross, R. Shownkeen, S. Sims, R. H. Waterston, R. K. Wilson, L. W. Hillier, J. D. McPherson, M. A. Marra, E. R. Mardis, L. A. Fulton, A. T. Chinwalla, K. H. Pepin, W. R. Gish, S. L. Chissoe, M. C. Wendl, K. D. Delehaunty, T. L. Miner, A. Delehaunty, J. B. Kramer, L. L. Cook, R. S. Fulton, D. L. Johnson, P. J. Minx, S. W. Clifton, T. Hawkins, E. Branscomb, P. Predki, P. Richardson, S. Wenning, T. Slezak, N. Doggett, J. F. Cheng, A. Olsen, S. Lucas, C. Elkin, E. Uberbacher, M. Frazier, et al. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860–921.
   PubMed Web of Science ®Google Scholar
• Lemmon, M. A., and K. M. Ferguson. 2000. Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem. J. 350: 1–18.
   PubMed Web of Science ®Google Scholar
• Lemmon, M. A., K. M. Ferguson, R. O'Brien, P. B. Sigler, and J. Schlessinger. 1995. Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain. Proc. Natl. Acad. Sci. USA 92: 10472–10476.
   PubMed Web of Science ®Google Scholar
• Lioubin, M. N., P. A. Algate, S. Tsai, K. Carlberg, A. Aebersold, and L. R. Rohrschneider. 1996. p150Ship, a signal transduction molecule with inositol polyphosphate-5-phosphatase activity. Genes Dev. 10: 1084–1095.
   PubMed Web of Science ®Google Scholar
• Lipp, P., and E. Niggli. 1993. Ratiometric confocal Ca2+ measurements with visible wavelength indicators in isolated cardiac myocytes. Cell Calcium 14: 359–372.
   PubMedGoogle Scholar
• Marshall, A. J., H. Niiro, C. G. Lerner, T. Y. Yun, S. Thomas, C. M. Disteche, and E. A. Clark. 2000. A novel B lymphocyte-associated adaptor protein, Bam32, regulates antigen receptor signaling downstream of phosphatidylinositol 3-kinase. J. Exp. Med. 191: 1319–1332.
   PubMedGoogle Scholar
• Marshall, A. J., H. Niiro, T. J. Yun, and E. A. Clark. 2000. Regulation of B cell activation and differentiation by the phosphatidylinositol 3-kinase and phospholipase Cγ pathways. Immunol. Rev. 176: 30–46.
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay, S., A. S. Ramars, and D. Dash. 2001. Bruton's tyrosine kinase associates with the actin-based cytoskeleton in activated platelets. J. Cell. Biochem. 81: 659–665.
   PubMed Web of Science ®Google Scholar
• Nagel, W., P. Schilcher, L. Zeitlmann, and W. Kolanus. 1998. The PH domain and polybasic domain of cytohesin-1 cooperate specifically in plasma membrane association and cellular function. Mol. Biol. Cell 9: 1981–1994.
   PubMedGoogle Scholar
• Nore, B. F., L. Vargas, A. J. Mohamed, L. J. Branden, C. M. Backesjo, T. C. Islam, P. T. Mattsson, K. Hultenby, B. Christensson, and C. I. Smith. 2000. Redistribution of Bruton's tyrosine kinase by activation of phosphatidylinositol 3-kinase and Rho-family GTPases. Eur. J. Immunol. 30: 145–154.
   PubMed Web of Science ®Google Scholar
• Ono, M., H. Okada, S. Bolland, S. Yanagi, T. Kurosaki, and J. V. Ravetch. 1997. Deletion of SHIP or SHP-1 reveals two distinct pathways for inhibitory signaling. Cell 90: 293–301.
   PubMed Web of Science ®Google Scholar
• Phillips, N. E., and D. C. Parker. 1983. Fc-dependent inhibition of mouse B cell activation by whole anti-mu antibodies. J. Immunol. 130: 602–606.
   PubMed Web of Science ®Google Scholar
• Rameh, L. E., A. K. Arvidsson, K. L. Carraway III, A. D. Couvillon, G. Rathbun, A. Crompton, B. VanRenterghem, M. P. Czech, K. S. Ravichandran, S. J. Burakoff, D. S. Wang, C. S. Chen, and L. C. Cantley. 1997. A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J. Biol. Chem. 272: 22059–22066.
   PubMed Web of Science ®Google Scholar
• Rameh, L. E., and L. C. Cantley. 1999. The role of phosphoinositide 3-kinase lipid products in cell function. J. Biol. Chem. 274: 8347–8350.
   PubMed Web of Science ®Google Scholar
• Rao, V. R., M. N. Corradetti, J. Chen, J. Peng, J. Yuan, G. D. Prestwich, and J. S. Brugge. 1999. Expression cloning of protein targets for 3-phosphorylated phosphoinositides. J. Biol. Chem. 274: 37893–37900.
   PubMedGoogle Scholar
• Rawlings, D. J. 1999. Bruton's tyrosine kinase controls a sustained calcium signal essential for B lineage development and function. Clin. Immunol. 91: 243–253.
   PubMedGoogle Scholar
• Rawlings, D. J., A. M. Scharenberg, H. Park, M. I. Wahl, S. Lin, R. M. Kato, A. C. Fluckiger, O. N. Witte, and J. P. Kinet. 1996. Activation of BTK by a phosphorylation mechanism initiated by SRC family kinases. Science 271: 822–825.
   PubMed Web of Science ®Google Scholar
• Reif, K., C. D. Nobes, G. Thomas, A. Hall, and D. A. Cantrell. 1996. Phosphatidylinositol 3-kinase signals activate a selective subset of Rac/Rho-dependent effector pathways. Curr. Biol. 6: 1445–1455.
   PubMedGoogle Scholar
• Salim, K., M. J. Bottomley, E. Querfurth, M. J. Zvelebil, I. Gout, R. Scaif, R. L. Margolis, R. Gigg, C. I. E. Smith, P. C. Driscoll, M. D. Waterfield, and G. Panayotou. 1996. Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and the Bruton's tyrosine kinase. EMBO J. 15: 6241–6250.
   PubMed Web of Science ®Google Scholar
• Scharenberg, A. M., and J. P. Kinet. 1998. PtdIns-3,4,5-P3: a regulatory nexus between tyrosine kinases and sustained calcium signals. Cell 94: 5–8.
   PubMed Web of Science ®Google Scholar
• Scheid, M. P., M. Huber, J. E. Damen, M. Hughes, V. Kang, P. Neilsen, G. D. Prestwich, G. Krystal, and V. Duronio. 2002. Phosphatidylinositol (3,4,5)P3 is essential but not sufficient for protein kinase B (PKB) activation; phosphatidylinositol (3,4)P2 is required for PKB phosphorylation at Ser-473: studies using cells from SH2-containing inositol-5-phosphatase knockout mice. J. Biol. Chem. 277: 9027–9035.
   PubMed Web of Science ®Google Scholar
• Stauffer, T. P., S. Ahn, and T. Meyer. 1998. Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Curr. Biol. 8: 343–346.
   PubMed Web of Science ®Google Scholar
• Suzuki, H., Y. Terauchi, M. Fujiwara, S. Aizawa, Y. Yazaki, T. Kadowaki, and S. Koyasu. 1999. Xid-like immunodeficiency in mice with disruption of the p85α subunit of phosphoinositide 3-kinase. Science 283: 390–392.
   PubMed Web of Science ®Google Scholar
• Takai, T., M. Ono, M. Hikida, H. Ohmori, and J. V. Ravetch. 1996. Augmented humoral and anaphylactic responses in FcγRII-deficient mice. Nature 379: 346–349.
   PubMed Web of Science ®Google Scholar
• Takata, M., and T. Kurosaki. 1996. A role for Bruton's tyrosine kinase in B cell antigen receptor-mediated activation of phospholipase C-γ2. J. Exp. Med. 184: 31–40.
   PubMed Web of Science ®Google Scholar
• Tall, E. G., I. Spector, S. N. Pentyala, I. Bitter, and M. J. Rebecchi. 2000. Dynamics of phosphatidylinositol 4,5-bisphosphate in actin-rich structures. Curr. Biol. 10: 743–746.
   PubMedGoogle Scholar
• Toker, A., and L. C. Cantley. 1997. Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 387: 673–676.
   PubMed Web of Science ®Google Scholar
• Touhara, K., J. Inglese, J. A. Pitcher, G. Shaw, and R. J. Lefkowitz. 1994. Binding of G protein β γ-subunits to pleckstrin homology domains. J. Biol. Chem. 269: 10217–10220.
   PubMedGoogle Scholar
• van der Wal, J., R. Habets, P. Varnai, T. Balla, and K. Jalink. 2001. Monitoring agonist-induced phospholipase C activation in live cells by fluorescence resonance energy transfer. J. Biol. Chem. 276: 15337–15344.
   PubMed Web of Science ®Google Scholar
• Varnai, P., and T. Balla. 1998. Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J. Cell Biol. 143: 501–510.
   PubMed Web of Science ®Google Scholar
• Varnai, P., K. L. Rother, and T. Balla. 1999. Phosphatidylinositol 3-kinase-dependent membrane association of the Bruton's tyrosine kinase pleckstrin homology domain visualized in single living cells. J. Biol. Chem. 274: 10983–10989.
   PubMed Web of Science ®Google Scholar
• Venkataraman, C., G. Shankar, G. Sen, and S. Bondada. 1999. Bacterial lipopolysaccharide induced B cell activation is mediated via a phosphatidylinositol 3-kinase dependent signaling pathway. Immunol. Lett. 69: 233–238.
   PubMedGoogle Scholar
• Venkateswarlu, K., F. Gunn-Moore, P. B. Oatey, J. M. Tavare, and P. J. Cullen. 1998. Nerve growth factor- and epidermal growth factor-stimulated translocation of the ADP-ribosylation factor-exchange factor GRP1 to the plasma membrane of PC12 cells requires activation of phosphatidylinositol 3-kinase and the GRP1 pleckstrin homology domain. J. Biochem. 335: 139–146.
   Google Scholar
• Yao, L., P. Janmey, L. G. Frigeri, W. Han, J. Fujita, Y. Kawakami, J. R. Apgar, and T. Kawakami. 1999. Pleckstrin homology domains interact with filamentous actin. J. Biol. Chem. 274: 19752–19761.
   PubMed Web of Science ®Google Scholar
• Yao, L., Y. Kawakami, and T. Kawakami. 1994. The pleckstrin homology domain of Bruton tyrosine kinase interacts with protein kinase C. Proc. Natl. Acad. Sci. USA 91: 9175–9179.
   PubMed Web of Science ®Google Scholar