61
Views
55
CrossRef citations to date
0
Altmetric
Article

Cross Talk between Phosphatidylinositol 3-Kinase and Cyclic AMP (cAMP)-Protein Kinase A Signaling Pathways at the Level of a Protein Kinase B/β-Arrestin/cAMP Phosphodiesterase 4 Complex

, , , , , , , & show all
Pages 1660-1672 | Received 28 May 2009, Accepted 30 Dec 2009, Published online: 20 Mar 2023

REFERENCES

  • Aandahl, E. M., P. Aukrust, B. S. Skalhegg, F. Muller, S. S. Froland, V. Hansson, and K. Tasken. 1998. Protein kinase A type I antagonist restores immune responses of T cells from HIV-infected patients. FASEB J. 12:855–862.
  • Aandahl, E. M., W. J. Moretto, P. A. Haslett, T. Vang, T. Bryn, K. Tasken, and D. F. Nixon. 2002. Inhibition of antigen-specific T cell proliferation and cytokine production by protein kinase A type I. J. Immunol. 169:802–808.
  • Abrahamsen, H., G. Baillie, J. Ngai, T. Vang, K. Nika, A. Ruppelt, T. Mustelin, M. Zaccolo, M. Houslay, and K. Tasken. 2004. TCR- and CD28-mediated recruitment of phosphodiesterase 4 to lipid rafts potentiates TCR signaling. J. Immunol. 173:4847–4858.
  • Acuto, O., and F. Michel. 2003. CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat. Rev. Immunol. 3:939–951.
  • Acuto, O., S. Mise-Omata, G. Mangino, and F. Michel. 2003. Molecular modifiers of T cell antigen receptor triggering threshold: the mechanism of CD28 costimulatory receptor. Immunol. Rev. 192:21–31.
  • Appleman, L. J., A. A. van Puijenbroek, K. M. Shu, L. M. Nadler, and V. A. Boussiotis. 2002. CD28 costimulation mediates down-regulation of p27kip1 and cell cycle progression by activation of the PI3K/PKB signaling pathway in primary human T cells. J. Immunol. 168:2729–2736.
  • Baillie, G. S., A. Sood, I. McPhee, I. Gall, S. J. Perry, R. J. Lefkowitz, and M. D. Houslay. 2003. Beta-arrestin-mediated PDE4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi. Proc. Natl. Acad. Sci. U. S. A. 100:940–945.
  • Beaulieu, J. M., T. D. Sotnikova, S. Marion, R. J. Lefkowitz, R. R. Gainetdinov, and M. G. Caron. 2005. An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122:261–273.
  • Benovic, J. L., H. Kuhn, I. Weyand, J. Codina, M. G. Caron, and R. J. Lefkowitz. 1987. Functional desensitization of the isolated beta-adrenergic receptor by the beta-adrenergic receptor kinase: potential role of an analog of the retinal protein arrestin (48-kDa protein). Proc. Natl. Acad. Sci. U. S. A. 84:8879–8882.
  • Bolger, G. B., G. S. Baillie, X. Li, M. J. Lynch, P. Herzyk, A. Mohamed, L. H. Mitchell, A. McCahill, C. Hundsrucker, E. Klussmann, D. R. Adams, and M. D. Houslay. 2006. Scanning peptide array analyses identify overlapping binding sites for the signalling scaffold proteins, beta-arrestin and RACK1, in cAMP-specific phosphodiesterase PDE4D5. Biochem. J. 398:23–36.
  • Calleja, V., D. Alcor, M. Laguerre, J. Park, B. Vojnovic, B. A. Hemmings, J. Downward, P. J. Parker, and B. Larijani. 2007. Intramolecular and intermolecular interactions of protein kinase B define its activation in vivo. PLoS. Biol. 5:e95.
  • Conche, C., G. Boulla, A. Trautmann, and C. Randriamampita. 2009. T cell adhesion primes antigen receptor-induced calcium responses through a transient rise in adenosine 3′,5′-cyclic monophosphate. Immunity 30:33–43.
  • Defea, K. 2008. Beta-arrestins and heterotrimeric G-proteins: collaborators and competitors in signal transduction. Br. J. Pharmacol. 153 (Suppl. 1):S298–S309.
  • DeWire, S. M., S. Ahn, R. J. Lefkowitz, and S. K. Shenoy. 2007. Beta-arrestins and cell signaling. Annu. Rev. Physiol. 69:483–510.
  • Diehn, M., A. A. Alizadeh, O. J. Rando, C. L. Liu, K. Stankunas, D. Botstein, G. R. Crabtree, and P. O. Brown. 2002. Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation. Proc. Natl. Acad. Sci. U. S. A. 99:11796–11801.
  • Dodson, L. F., J. S. Boomer, C. M. Deppong, D. D. Shah, J. Sim, T. L. Bricker, J. H. Russell, and J. M. Green. 2009. Targeted knock-in mice expressing mutations of CD28 reveal an essential pathway for costimulation. Mol. Cell. Biol. 29:3710–3721.
  • Gaidarov, I., J. G. Krupnick, J. R. Falck, J. L. Benovic, and J. H. Keen. 1999. Arrestin function in G protein-coupled receptor endocytosis requires phosphoinositide binding. EMBO J. 18:871–881.
  • Garcon, F., D. T. Patton, J. L. Emery, E. Hirsch, R. Rottapel, T. Sasaki, and K. Okkenhaug. 2008. CD28 provides T-cell costimulation and enhances PI3K activity at the immune synapse independently of its capacity to interact with the p85/p110 heterodimer. Blood 111:1464–1471.
  • Goodman, O. B., Jr., J. G. Krupnick, F. Santini, V. V. Gurevich, R. B. Penn, A. W. Gagnon, J. H. Keen, and J. L. Benovic. 1996. Beta-arrestin acts as a clathrin adaptor in endocytosis of the beta2-adrenergic receptor. Nature 383:447–450.
  • Gurevich, V. V., E. V. Gurevich, and W. M. Cleghorn. 2008. Arrestins as multi-functional signaling adaptors. Handb. Exp. Pharmacol. 2008:15–37.
  • Holdorf, A. D., J. M. Green, S. D. Levin, M. F. Denny, D. B. Straus, V. Link, P. S. Changelian, P. M. Allen, and A. S. Shaw. 1999. Proline residues in CD28 and the Src homology (SH)3 domain of Lck are required for T cell costimulation. J. Exp. Med. 190:375–384.
  • Kim, H. H., M. Tharayil, and C. E. Rudd. 1998. Growth factor receptor-bound protein 2 SH2/SH3 domain binding to CD28 and its role in co-signaling. J. Biol. Chem. 273:296–301.
  • Kim, Y. M., and J. L. Benovic. 2002. Differential roles of arrestin-2 interaction with clathrin and adaptor protein 2 in G protein-coupled receptor trafficking. J. Biol. Chem. 277:30760–30768.
  • Kramer, A., and J. Schneider-Mergener. 1998. Synthesis and screening of peptide libraries on continuous cellulose membrane supports. Methods Mol. Biol. 87:25–39.
  • Laporte, S. A., W. E. Miller, K. M. Kim, and M. G. Caron. 2002. Beta-arrestin/AP-2 interaction in G protein-coupled receptor internalization: identification of a beta-arrestin binging site in beta 2-adaptin. J. Biol. Chem. 277:9247–9254.
  • Laporte, S. A., R. H. Oakley, J. Zhang, J. A. Holt, S. S. Ferguson, M. G. Caron, and L. S. Barak. 1999. The beta2-adrenergic receptor/betaarrestin complex recruits the clathrin adaptor AP-2 during endocytosis. Proc. Natl. Acad. Sci. U. S. A. 96:3712–3717.
  • Ledbetter, J. A., M. Parsons, P. J. Martin, J. A. Hansen, P. S. Rabinovitch, and C. H. June. 1986. Antibody binding to CD5 (Tp67) and Tp44 T cell surface molecules: effects on cyclic nucleotides, cytoplasmic free calcium, and cAMP-mediated suppression. J. Immunol. 137:3299–3305.
  • Lobban, M., Y. Shakur, J. Beattie, and M. D. Houslay. 1994. Identification of two splice variant forms of type-IVB cyclic AMP phosphodiesterase, DPD (rPDE-IVB1) and PDE-4 (rPDE-IVB2) in brain: selective localization in membrane and cytosolic compartments and differential expression in various brain regions. Biochem. J. 304:399–406.
  • Luan, B., J. Zhao, H. Wu, B. Duan, G. Shu, X. Wang, D. Li, W. Jia, J. Kang, and G. Pei. 2009. Deficiency of a beta-arrestin-2 signal complex contributes to insulin resistance. Nature 457:1146–1149.
  • Lynch, M. J., G. S. Baillie, A. Mohamed, X. Li, C. Maisonneuve, E. Klussmann, G. van Heeke, and M. D. Houslay. 2005. RNA silencing identifies PDE4D5 as the functionally relevant cAMP phosphodiesterase interacting with beta arrestin to control the protein kinase A/AKAP79-mediated switching of the beta2-adrenergic receptor to activation of ERK in HEK293B2 cells. J. Biol. Chem. 280:33178–33189.
  • Marchmont, R. J., and M. D. Houslay. 1980. A peripheral and an intrinsic enzyme constitute the cyclic AMP phosphodiesterase activity of rat liver plasma membranes. Biochem. J. 187:381–392.
  • Michel, F., G. Attal-Bonnefoy, G. Mangino, S. Mise-Omata, and O. Acuto. 2001. CD28 as a molecular amplifier extending TCR ligation and signaling capabilities. Immunity 15:935–945.
  • Milburn, C. C., M. Deak, S. M. Kelly, N. C. Price, D. R. Alessi, and D. M. Van Aalten. 2003. Binding of phosphatidylinositol 3,4,5-trisphosphate to the pleckstrin homology domain of protein kinase B induces a conformational change. Biochem. J. 375:531–538.
  • Nelson, C. D., S. J. Perry, D. S. Regier, S. M. Prescott, M. K. Topham, and R. J. Lefkowitz. 2007. Targeting of diacylglycerol degradation to M1 muscarinic receptors by beta-arrestins. Science 315:663–666.
  • Okkenhaug, K., and R. Rottapel. 1998. Grb2 forms an inducible protein complex with CD28 through a Src homology 3 domain-proline interaction. J. Biol. Chem. 273:21194–21202.
  • Okkenhaug, K., L. Wu, K. M. Garza, R. J. La, W. Khoo, B. Odermatt, T. W. Mak, P. S. Ohashi, and R. Rottapel. 2001. A point mutation in CD28 distinguishes proliferative signals from survival signals. Nat. Immunol. 2:325–332.
  • Pages, F., M. Ragueneau, R. Rottapel, A. Truneh, J. Nunes, J. Imbert, and D. Olive. 1994. Binding of phosphatidylinositol-3-OH kinase to CD28 is required for T-cell signalling. Nature 369:327–329.
  • Perry, S. J., G. S. Baillie, T. A. Kohout, I. McPhee, M. M. Magiera, K. L. Ang, W. E. Miller, A. J. McLean, M. Conti, M. D. Houslay, and R. J. Lefkowitz. 2002. Targeting of cyclic AMP degradation to beta 2-adrenergic receptors by beta-arrestins. Science 298:834–836.
  • Povsic, T. J., T. A. Kohout, and R. J. Lefkowitz. 2003. Beta-arrestin1 mediates insulin-like growth factor 1 (IGF-1) activation of phosphatidylinositol 3-kinase (PI3K) and anti-apoptosis. J. Biol. Chem. 278:51334–51339.
  • Prasad, K. V., Y. C. Cai, M. Raab, B. Duckworth, L. Cantley, S. E. Shoelson, and C. E. Rudd. 1994. T-cell antigen CD28 interacts with the lipid kinase phosphatidylinositol 3-kinase by a cytoplasmic Tyr(P)-Met-Xaa-Met motif. Proc. Natl. Acad. Sci. U. S. A. 91:2834–2838.
  • Raab, M., Y. C. Cai, S. C. Bunnell, S. D. Heyeck, L. J. Berg, and C. E. Rudd. 1995. p56Lck and p59Fyn regulate CD28 binding to phosphatidylinositol 3-kinase, growth factor receptor-bound protein GRB-2, and T cell-specific protein-tyrosine kinase ITK: implications for T-cell costimulation. Proc. Natl. Acad. Sci. U. S. A. 92:8891–8895.
  • 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.
  • Rudd, C. E., and M. Raab. 2003. Independent CD28 signaling via VAV and SLP-76: a model for in trans costimulation. Immunol. Rev. 192:32–41.
  • Ruppelt, A., R. Mosenden, M. Gronholm, E. M. Aandahl, D. Tobin, C. R. Carlson, H. Abrahamsen, F. W. Herberg, O. Carpen, and K. Tasken. 2007. Inhibition of T cell activation by cyclic adenosine 5′-monophosphate requires lipid raft targeting of protein kinase A type I by the A-kinase anchoring protein ezrin. J. Immunol. 179:5159–5168.
  • Skalhegg, B. S., B. F. Landmark, S. O. Doskeland, V. Hansson, T. Lea, and T. Jahnsen. 1992. Cyclic AMP-dependent protein kinase type I mediates the inhibitory effects of 3′,5′-cyclic adenosine monophosphate on cell replication in human T lymphocytes. J. Biol. Chem. 267:15707–15714.
  • Skalhegg, B. S., K. Tasken, V. Hansson, H. S. Huitfeldt, T. Jahnsen, and T. Lea. 1994. Location of cAMP-dependent protein kinase type I with the TCR-CD3 complex. Science 263:84–87.
  • Tavano, R., G. Gri, B. Molon, B. Marinari, C. E. Rudd, L. Tuosto, and A. Viola. 2004. CD28 and lipid rafts coordinate recruitment of Lck to the immunological synapse of human T lymphocytes. J. Immunol. 173:5392–5397.
  • Torgersen, K. M., T. Vang, H. Abrahamsen, S. Yaqub, V. Horejsi, B. Schraven, B. Rolstad, T. Mustelin, and K. Tasken. 2001. Release from tonic inhibition of T cell activation through transient displacement of C-terminal Src kinase (Csk) from lipid rafts. J. Biol. Chem. 276:29313–29318.
  • Vang, T., K. Tasken, B. S. Skalhegg, V. Hansson, and F. O. Levy. 1998. Kinetic properties of the C-terminal Src kinase, p50csk. Biochim. Biophys. Acta 1384:285–293.
  • Vang, T., K. M. Torgersen, V. Sundvold, M. Saxena, F. O. Levy, B. S. Skalhegg, V. Hansson, T. Mustelin, and K. Tasken. 2001. Activation of the COOH-terminal Src kinase (Csk) by cAMP-dependent protein kinase inhibits signaling through the T cell receptor. J. Exp. Med. 193:497–507.
  • Waugh, C., L. Sinclair, D. Finlay, J. R. Bayascas, and D. Cantrell. 2009. Phosphoinositide (3,4,5)-triphosphate binding to phosphoinositide-dependent kinase 1 regulates a protein kinase B/Akt signaling threshold that dictates T-cell migration, not proliferation. Mol. Cell. Biol. 29:5952–5962.
  • Zhang, W., J. Sloan-Lancaster, J. Kitchen, R. P. Trible, and L. E. Samelson. 1998. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92:83–92.

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.