Protein kinase D2 is a digital amplifier of T cell receptor-stimulated diacylglycerol signaling in naïve CD8+ T cells

Science Signaling

Volumn 7, Issue 348, 2014, Pages ra99-

  Navarro, María N ^a,b   Feijoo Carnero, Carmen ^a   Arandilla, Alba Gonzalez ^a   Trost, Matthias ^a   Cantrell, Doreen A ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL; LIGAND; PROTEIN KINASE D; PROTEIN KINASE D2; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CD8+ T LYMPHOCYTE; CELL COUNT; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; EFFECTOR CELL; MOUSE; NONHUMAN; ANIMAL; CYTOLOGY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; SIGNAL TRANSDUCTION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; MICE; MICE, KNOCKOUT; PROTEIN KINASES; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION;

EID: 84908461433     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2005477     Document Type: Article

References (29)

1. J. Fielitz, M. S. Kim, J. M. Shelton, X. Qi, J. A. Hill, J. A. Richardson, R. Bassel-Duby, E. N. Olson, Requirement of protein kinase D1 for pathological cardiac remodeling. Proc. Natl. Acad. Sci. U.S.A. 105, 3059-3063 (2008).
2. S. A. Matthews, M. N. Navarro, L. V. Sinclair, E. Emslie, C. Feijoo-Carnero, D. A. Cantrell, Unique functions for protein kinase D1 and protein kinase D2 in mammalian cells. Biochem. J. 432, 153-163 (2010).
3. M. N. Navarro, L. V. Sinclair, C. Feijoo-Carnero, R. Clarke, S. A. Matthews, D. A. Cantrell, Protein kinase D2 has a restricted but critical role in T-cell antigen receptor signalling in mature T-cells. Biochem. J. 442, 649-659 (2012).
4. 748 in protein kinase D are transphosphorylated in vivo. J. Biol. Chem. 276, 32606-32615 (2001).
5. O. Rey, J. R. Reeve, E. Zhukova, J. Sinnett-Smith, E. Rozengurt, G protein-coupled receptor-mediated phosphorylation of the activation loop of protein kinase D: Dependence on plasma membrane translocation and protein kinase Ce. J. Biol. Chem. 279, 34361-34372 (2004).
6. M. Spitaler, E. Emslie, C. D. Wood, D. Cantrell, Diacylglycerol and protein kinase D localization during T lymphocyte activation. Immunity 24, 535-546 (2006).
7. D. Zehn, C. King, M. J. Bevan, E. Palmer, TCR signaling requirements for activating T cells and for generating memory. Cell. Mol. Life Sci. 69, 1565-1575 (2012).
8. M. A. Purbhoo, D. J. Irvine, J. B. Huppa, M. M. Davis, T cell killing does not require the formation of a stable mature immunological synapse. Nat. Immunol. 5, 524-530 (2004).
9. D. J. Irvine, M. A. Purbhoo, M. Krogsgaard, M. M. Davis, Direct observation of ligand recognition by T cells. Nature 419, 845-849 (2002).
10. J. E. Smith-Garvin, G. A. Koretzky, M. S. Jordan, T cell activation. Annu. Rev. Immunol. 27, 591-619 (2009).
11. B. A. Olenchock, R. Guo, J. H. Carpenter, M. Jordan, M. K. Topham, G. A. Koretzky, X. P. Zhong, Disruption of diacylglycerol metabolism impairs the induction of T cell anergy. Nat. Immunol. 7, 1174-1181 (2006).
12. X. P. Zhong, E. A. Hainey, B. A. Olenchock, M. S. Jordan, J. S. Maltzman, K. E. Nichols, H. Shen, G. A. Koretzky, Enhanced T cell responses due to diacylglycerol kinase z deficiency. Nat. Immunol. 4, 882-890 (2003).
13. A. M. Valverde, J. Sinnett-Smith, J. Van Lint, E. Rozengurt, Molecular cloning and characterization of protein kinase D: A target for diacylglycerol and phorbol esters with a distinctive catalytic domain. Proc. Natl. Acad. Sci. U.S.A. 91, 8572-8576 (1994).
14. + T cells. Immunity 39, 846-857 (2013).
15. K. Tkach, G. Altan-Bonnet, T cell responses to antigen: Hasty proposals resolved through long engagements. Curr. Opin. Immunol. 25, 120-125 (2013).
16. G. Altan-Bonnet, R. N. Germain, Modeling T cell antigen discrimination based on feedback control of digital ERK responses. PLOS Biol. 3, e356 (2005).
17. J. Das, M. Ho, J. Zikherman, C. Govern, M. Yang, A. Weiss, A. K. Chakraborty, J. P. Roose, Digital signaling and hysteresis characterize Ras activation in lymphoid cells. Cell 136, 337-351 (2009).
18. M. A. Daniels, E. Teixeiro, J. Gill, B. Hausmann, D. Roubaty, K. Holmberg, G. Werlen, G. A. Holländer, N. R. J. Gascoigne, E. Palmer, Thymic selection threshold defined by compartmentalization of Ras/MAPK signalling. Nature 444, 724-729 (2006).
19. C. G. King, S. Koehli, B. Hausmann, M. Schmaler, D. Zehn, E. Palmer, T cell affinity regulates asymmetric division, effector cell differentiation, and tissue pathology. Immunity 37, 709-720 (2012).
20. D. Zehn, S. Y. Lee, M. J. Bevan, Complete but curtailed T-cell response to very low-affinity antigen. Nature 458, 211-214 (2009).
21. P. Picotti, R. Aebersold, Selected reaction monitoring-based proteomics: Workflows, potential, pitfalls and future directions. Nat. Methods 9, 555-566 (2012).
22. G. M. N. Behrens, M. Li, G. M. Davey, J. Allison, R. A. Flavell, F. R. Carbone, W. R. Heath, Helper requirements for generation of effector CTL to islet beta cell antigens. J. Immunol. 172, 5420-5426 (2004).
23. E. L. Pearce, H. Shen, Generation of CD8 T cell memory is regulated by IL-12. J. Immunol. 179, 2074-2081 (2007).
24. S. Sarkar, V. Kalia, W. N. Haining, B. T. Konieczny, S. Subramaniam, R. Ahmed, Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J. Exp. Med. 205, 625-640 (2008).
25. H. Mukhopadhyay, S. P. Cordoba, P. K. Maini, P. A. van der Merwe, O. Dushek, Systems model of T cell receptor proximal signaling reveals emergent ultrasensitivity. PLOS Comput. Biol. 9, e1003004 (2013).
26. L. M. Kingeter, S. Paul, S. K. Maynard, N. G. Cartwright, B. C. Schaefer, Cutting edge: TCR ligation triggers digital activation of NF-kB. J. Immunol. 185, 4520-4524 (2010).
27. E. Rozengurt, Protein kinase D signaling: Multiple biological functions in health and disease. Physiology 26, 23-33 (2011).
28. S. A. Matthews, E. Rozengurt, D. Cantrell, Characterization of serine 916 as an in vivo autophosphorylation site for protein kinase D/Protein kinase Cm. J. Biol. Chem. 274, 26543-26549 (1999).
29. B. MacLean, D. M. Tomazela, N. Shulman, M. Chambers, G. L. Finney, B. Frewen, R. Kern, D. L. Tabb, D. C. Liebler, M. J. MacCoss, Skyline: An open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966-968 (2010).