The ζ isoform of diacylglycerol kinase plays a predominant role in regulatory T cell development and TCR-mediated Ras signaling

Science Signaling

Volumn 6, Issue 303, 2013, Pages

  Joshi, Rohan P ^a   Schmidt, Amanda M ^b   Das, Jayajit ^c,f   Pytel, Dariusz ^a   Riese, Matthew J ^a   Lester, Melissa ^a   Diehl, J Alan ^a   Behrens, Edward M ^d   Kambayashi, Taku ^b   Koretzky, Gary A ^a,e  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c NATIONWIDE CHILDREN S HOSPITAL   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

^f OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL; DIACYLGLYCEROL KINASE; DIACYLGLYCEROL KINASE ALPHA; DIACYLGLYCEROL KINASE ZETA; PHOSPHATIDIC ACID; PROTEIN KINASE B; RAS PROTEIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; BINDING AFFINITY; CATALYSIS; CELL MATURATION; COMPUTER MODEL; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME METABOLISM; GENE DELETION; LYMPHOCYTE DIFFERENTIATION; MOLECULAR MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY T LYMPHOCYTE; SECOND MESSENGER; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CLONING, MOLECULAR; DIACYLGLYCEROL KINASE; DNA, COMPLEMENTARY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOPRECIPITATION; MICE; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RAS PROTEINS; RECEPTORS, ANTIGEN, T-CELL; RIBOSOMAL PROTEIN S6 KINASES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY;

EID: 84889254459     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004373     Document Type: Article

References (44)

1. J. E. Smith-Garvin, G. A. Koretzky, M. S. Jordan, T cell activation. Annu. Rev. Immunol. 27, 591-619 (2009).
2. D. G. Motto, S. E. Ross, J. Wu, L. R. Hendricks-Taylor, G. A. Koretzky, Implication of the GRB2-associated phosphoprotein SLP-76 in T cell receptor-mediated interleukin 2 production. J. Exp. Med. 183, 1937-1943 (1996).
3. J. B. Imboden, J. D. Stobo, Transmembrane signalling by the T cell antigen receptor. Perturbation of the T3-antigen receptor complex generates inositol phosphates and releases calcium ions from intracellular stores. J. Exp. Med. 161, 446-456 (1985).
4. C. E. Tognon, H. E. Kirk, L. A. Passmore, I. P. Whitehead, C. J. Der, R. J. Kay, Regulation of RasGRP via a phorbol ester-responsive C1 domain. Mol. Cell. Biol. 18, 6995-7008 (1998).
5. N. Coudronniere, M. Villalba, N. Englund, A. Altman, NF-kB activation induced by T cell receptor/CD28 costimulation is mediated by protein kinase C-q. Proc. Natl. Acad. Sci. U.S.A. 97, 3394-3399 (2000).
6. E. J. Quann, E. Merino, T. Furuta, M. Huse, Localized diacylglycerol drives the polarization of the microtubule-organizing center in T cells. Nat. Immunol. 10, 627-635 (2009).
7. B. K. Gorentla, C. K. Wan, X. P. Zhong, Negative regulation of mTOR activation by diacylglycerol kinases. Blood 117, 4022-4031 (2011).
8. 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 ζ deficiency. Nat. Immunol. 4, 882-890 (2003).
9. 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).
10. X. P. Zhong, E. A. Hainey, B. A. Olenchock, H. Zhao, M. K. Topham, G. A. Koretzky, Regulation of T cell receptor-induced activation of the Ras-ERK pathway by diacylglycerol kinase ζ. J. Biol. Chem. 277, 31089-31098 (2002).
11. J. Shin, T. F. O'Brien, J. M. Grayson, X. P. Zhong, Differential regulation of primary and memory CD8 T cell immune responses by diacylglycerol kinases. J. Immunol. 188, 2111-2117 (2012).
12. M. Takahashi, T. Yamamoto, H. Sakai, F. Sakane, Calcium negatively regulates an intramolecular interaction between the N-terminal recoverin homology and EF-hand motif domains and the C-terminal C1 and catalytic domains of diacylglycerol kinase a. Biochem. Biophys. Res. Commun. 423, 571-576 (2012).
13. K. Yamada, F. Sakane, N. Matsushima, H. Kanoh, EF-hand motifs of a, b and g isoforms of diacylglycerol kinase bind calcium with different affinities and conformational changes. Biochem. J. 321, 59-64 (1997).
14. F. Sakane, K. Yamada, S. Imai, H. Kanoh, Porcine 80-kDa diacylglycerol kinase is a calcium-binding and calcium/phospholipid-dependent enzyme and undergoes calciumdependent translocation. J. Biol. Chem. 266, 7096-7100 (1991).
15. Y. Jiang, W. Qian, J. W. Hawes, J. P. Walsh, A domain with homology to neuronal calcium sensors is required for calcium-dependent activation of diacylglycerol kinase α. J. Biol. Chem. 275, 34092-34099 (2000).
16. M. A.Sanjuan, B. Pradet-Balade, D. R. Jones, C.Martínez-A, J.C.Stone, J. A. Garcia-Sanz, I. Merida, T cell activation in vivo targets diacylglycerol kinase a to the membrane: A novel mechanism for Ras attenuation. J. Immunol. 170, 2877-2883 (2003).
17. T. Santos, S. Carrasco, D. R. Jones, I. Mérida, A. Eguinoa, Dynamics of diacylglycerol kinase ζ translocation in living T-cells. Study of the structural domain requirements for translocation and activity. J. Biol. Chem. 277, 30300-30309 (2002).
18. S. I. Gharbi, E. Rincón, A. Avila-Flores, P. Torres-Ayuso, M. Almena, M. A. Cobos, J. P. Albar, I. Mérida, Diacylglycerol kinase ζ controls diacylglycerol metabolism at the immune synapse. Mol. Biol. Cell 22, 4406-4414 (2011).
19. B. Luo, S. M. Prescott, M. K. Topham, Protein kinase C a phosphorylates and negatively regulates diacylglycerol kinase ζ. J. Biol. Chem. 278, 39542-39547 (2003).
20. A. M. Schmidt, T. Zou, R. P. Joshi, T. M. Leichner, M. A. Pimentel, C. L. Sommers, T. Kambayashi, Diacylglycerol kinase ζ limits the generation of natural regulatory T cells. Sci. Signal. 6, ra101 (2013).
21. + T cell functional responses. J. Biol. Chem. 286, 5254-5265 (2011).
22. R. Guo, C. K. Wan, J. H. Carpenter, T. Mousallem, R. M. N. Boustany, C. T. Kuan, A. W. Burks, X. P. Zhong, Synergistic control of T cell development and tumor suppression by diacylglycerol kinase α and ζ. Proc. Natl. Acad. Sci. U.S.A. 105, 11909-11914 (2008).
23. Y. Zha, R. Marks, A. W. Ho, A. C. Peterson, S. Janardhan, I. Brown, K. Praveen, S. Stang, J. C. Stone, T. F. Gajewski, T cell anergy is reversed by active Ras and is regulated by diacylglycerol kinase-α. Nat. Immunol. 7, 1166-1173 (2006).
24. M. Spitaler, E. Emslie, C. D. Wood, D. Cantrell, Diacylglycerol and protein kinase D localization during T lymphocyte activation. Immunity 24, 535-546 (2006).
25. D. S. Regier, J. Higbee, K. M. Lund, F. Sakane, S. M. Prescott, M. K. Topham, Diacylglycerol kinase i regulates Ras guanyl-releasing protein 3 and inhibits Rap1 signaling. Proc. Natl. Acad. Sci. U.S.A. 102, 7595-7600 (2005).
26. M. K. Topham, S. M. Prescott, Diacylglycerol kinase z regulates Ras activation by a novel mechanism. J. Cell Biol. 152, 1135-1143 (2001).
27. 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).
28. R. Ard, K. Mulatz, H. Abramovici, J. C. Maillet, A. Fottinger, T. Foley, M. R. Byham, T. A. Iqbal, A. Yoneda, J. R. Couchman, R. J. Parks, S. H. Gee, Diacylglycerol kinase z regulates RhoA activation via a kinase-independent scaffolding mechanism. Mol. Biol. Cell 23, 4008-4019 (2012).
29. M. S. Jordan, A. Boesteanu, A. J. Reed, A. L. Petrone, A. E. Holenbeck, M. A. Lerman, A. Naji, A. J. Caton, Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat. Immunol. 2, 301-306 (2001).
30. G. Baldanzi, A. Pighini, V. Bettio, E. Rainero, S. Traini, F. Chianale, P. E. Porporato, N. Filigheddu, R. Mesturini, S. Song, T. Schweighoffer, L. Patrussi, C. T. Baldari, X. P. Zhong, W. J. van Blitterswijk, F. Sinigaglia, K. E. Nichols, I. Rubio, O. Parolini, A. Graziani, SAP-mediated inhibition of diacylglycerol kinase α regulates TCR-induced diacylglycerol signaling. J. Immunol. 187, 5941-5951 (2011).
31. F. Sakane, M. Kai, I. Wada, S. Imai, H. Kanoh, The C-terminal part of diacylglycerol kinase a lacking zinc fingers serves as a catalytic domain. Biochem. J. 318 (Pt. 2), 583-590 (1996).
32. R. M. Epand, A. Kam, N. Bridgelal, A. Saiga, M. K. Topham, The a isoform of diacylglycerol kinase exhibits arachidonoyl specificity with alkylacylglycerol. Biochemistry 43, 14778-14783 (2004).
33. M. L. Fanani, M. K. Topham, J. P. Walsh, R. M. Epand, Lipid modulation of the activity of diacylglycerol kinase α- and ζ-isoforms: Activation by phosphatidylethanolamine and cholesterol. Biochemistry 43, 14767-14777 (2004).
34. P. Sánchez-Piñera, V. Micol, S. Corbalán- García, J. C. Gómez-Fernández, A comparative study of the activation of protein kinase C a by different diacylglycerol isomers. Biochem. J. 337 (Pt. 3), 387-395 (1999).
35. A. K. Hinderliter, A. R. Dibble, R. L. Biltonen, J. J. Sando, Activation of protein kinase C by coexisting diacylglycerol-enriched and diacylglycerol-poor lipid domains. Biochemistry 36, 6141-6148 (1997).
36. + T cells deficient in diacylglycerol kinases. Cancer Res. 73, 3566-3577 (2013).
37. C. Lo Celso, D. Scadden, Isolation and transplantation of hematopoietic stem cells (HSCs). J. Vis. Exp. 2, 157 (2007).
38. J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J.White, V. Hartenstein, K. Eliceiri, P. Tomancak, A. Cardona, Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).
39. E. Bobrovnikova-Marjon, D. Pytel, M. J. Riese, L. P. Vaites, N. Singh, G. A. Koretzky, E. S. Witze, J. A. Diehl, PERK utilizes intrinsic lipid kinase activity to generate phosphatidic acid, mediate Akt activation, and promote adipocyte differentiation. Mol. Cell. Biol. 32, 2268-2278 (2012).
40. D. T. Gillespie, Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81, 2340-2361 (1977).
41. P. S. Swain, M. B. Elowitz, E. D. Siggia, Intrinsic and extrinsic contributions to stochasticity in gene expression. Proc. Natl. Acad. Sci. U.S.A. 99, 12795-12800 (2002).
42. D. Volfson, J. Marciniak, W. J. Blake, N. Ostroff, L. S. Tsimring, J. Hasty, Origins of extrinsic variability in eukaryotic gene expression. Nature 439, 861-864 (2006).
43. M. Lis, M. N. Artyomov, S. Devadas, A. K. Chakraborty, Efficient stochastic simulation of reaction-diffusion processes via direct compilation. Bioinformatics 25, 2289-2291 (2009).
44. L. R. Stephens, T. R. Jackson, P. T. Hawkins, Agonist-stimulated synthesis of phosphatidylinositol(3,4,5)-trisphosphate: A new intracellular signalling system? Biochim. Biophys. Acta 1179, 27-75 (1993).