Differential regulation of human NK cell-mediated cytotoxicity by the tyrosine kinase Itk

Journal of Immunology

Volumn 178, Issue 6, 2007, Pages 3575-3582

  Khurana, Dianne ^a   Arneson, Laura N ^a   Schoon, Renee A ^a   Dick, Christopher J ^a   Leibson, Paul J ^a,b  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; DNAX ACTIVATING PROTEIN 10; FC RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2D; PROTEIN TYROSINE KINASE; REGULATOR PROTEIN; TYROSINE KINASE INTERLEUKIN 2 INDUCIBLE T CELL KINASE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOIMMUNE DISEASE; CALCIUM MOBILIZATION; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MOLECULAR WEIGHT; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR IMMUNITY; VIRUS INFECTION;

EID: 33947249484     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.6.3575     Document Type: Article

References (53)

1. Billadeau, D. D., J. L. Upshaw, R. A. Schoon, C. J. Dick, and P. J. Leibson. 2003. NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway. Nat. Immunol. 4: 557-564.
2. Upshaw, J. L., L. N. Arneson, R. A. Schoon, C. J. Dick, D. D. Billadeau, and P. J. Leibson. 2006. NKG2D-mediated signaling requires a DAP10-bound Grb2-Vav1 intermediate and phosphatidylinositol-3-kinase in human natural killer cells. Nat. Immunol. 7: 524-532.
3. Meresse, B., Z. Chen, C. Ciszewski, M. Tretiakova, G. Bhagat, T. N. Krausz, D. H. Raulet, L. L. Lanier, V. Groh, T. Spies, et al. 2004. Coordinated induction by IL15 of a TCR-independent NKG2D signaling pathway converts CTL into lymphokine-activated killer cells in celiac disease. Immunity 21: 357-366.
4. Lewis, C. M., C. Broussard, M. J. Czar, and P. L. Schwartzberg. 2001. Tec kinases: modulators of lymphocyte signaling and development. Curr. Opin. Immunol. 13: 317-325.
5. Berg, L. J., L. D. Finkelstein, J. A. Lucas, and P. L. Schwartzberg. 2005. Tec family kinases in T lymphocyte development and function. Annu. Rev. Immunol. 23: 549-600.
6. Kawakami, Y., L. Yao, M. Tashiro, S. Gibson, G. B. Mills, and T. Kawakami. 1995. Activation and interaction with protein kinase C of a cytoplasmic tyrosine kinase, Itk/Tsk/Emt, on FcεRI cross-linking on mast cells. J. Immunol. 155: 3556-3562.
7. Okoh, M. P., and M. Vihinen. 1999. Pleckstrin homology domains of Tec family protein kinases. Biochem. Biophys. Res. Commun. 265: 151-157.
8. August, A., A. Sadra, B. Dupont, and H. Hanafusa. 1997. Src-induced activation of inducible T cell kinase (ITK) requires phosphatidylinositol 3-kinase activity and the Pleckstrin homology domain of inducible T cell kinase. Proc. Natl. Acad. Sci. USA 94: 11227-11232.
9. Heyeck, S. D., H. M. Wilcox, S. C. Bunnell, and L. J. Berg. 1997. Lck phosphorylates the activation loop tyrosine of the Itk kinase domain and activates Itk kinase activity. J. Biol. Chem. 272: 25401-25408.
10. Cheng, G., Z. S. Ye, and D. Baltimore. 1994. Binding of Bruton's tyrosine kinase to Fyn, Lyn, or Hck through a Src homology 3 domain-mediated interaction. Proc. Natl. Acad. Sci. USA 91: 8152-8155.
11. Bunnell, S. C., P. A. Henry, R. Kolluri, T. Kirchhausen, R. J. Rickles, and L. J. Berg. 1996. Identification of Itk/Tsk Src homology 3 domain ligands. J. Biol. Chem. 271: 25646-25656.
12. Marengere, L. E., K. Okkenhaug, A. Clavreul, D. Couez, S. Gibson, G. B. Mills, T. W. Mak, and R. Rottapel. 1997. The SH3 domain of Itk/Emt binds to proline-rich sequences in the cytoplasmic domain of the T cell costimulatory receptor CD28. J. Immunol. 159: 3220-3229.
13. Su, Y. W., Y. Zhang, J. Schweikert, G. A. Koretzky, M. Reth, and J. Wienands. 1999. Interaction of SLP adaptors with the SH2 domain of Tec family kinases. Eur. J. Immunol. 29: 3702-3711.
14. Windebank, K. P., R. T. Abraham, G. Powis, R. A. Olsen, T. J. Barna, and P. J. Leibson. 1988. Signal transduction during human natural killer cell activation: inositol phosphate generation and regulation by cyclic AMP. J. Immunol. 141: 3951-3957.
15. Billadeau, D. D., S. M. Mackie, R. A. Schoon, and P. J. Leibson. 2000. The Rho family guanine nucleotide exchange factor Vav-2 regulates the development of cell-mediated cytotoxicity. J. Exp. Med. 192: 381-392.
16. Ting, A. T., L. M. Karnitz, R. A. Schoon, R. T. Abraham, and P. J. Leibson. 1992. Fcγ receptor activation induces the tyrosine phosphorylation of both phospholipase C (PLC)-γ1 and PLC-γ2 in natural killer cells. J. Exp. Med. 176: 1751-1755.
17. Binstadt, B. A., K. M. Brumbaugh, C. J. Dick, A. M. Scharenberg, B. L. Williams, M. Colonna, L. L. Lanier, J. P. Kinet, R. T. Abraham, and P. J. Leibson. 1996. Sequential involvement of Lck and SHP-1 with MHC-recognizing receptors on NK cells inhibits FcR-initiated tyrosine kinase activation. Immunity 5: 629-638.
18. Jevremovic, D., D. D. Billadeau, R. A. Schoon, C. J. Dick, and P. J. Leibson. 2001. Regulation of NK cell-mediated cytotoxicity by the adaptor protein 3BP2. J. Immunol. 166: 7219-7228.
19. Billadeau, D. D., K. M. Brumbaugh, C. J. Dick, R. A. Schoon, X. R. Bustelo, and P. J. Leibson. 1998. The Vav-Rac1 pathway in cytotoxic lymphocytes regulates the generation of cell-mediated killing. J. Exp. Med. 188: 549-559.
20. Ting, A. T., C. J. Dick, R. A. Schoon, L. M. Karnitz, R. T. Abraham, and P. J. Leibson. 1995. Interaction between Lck and Syk family tyrosine kinases in Fcγ receptor-initiated activation of natural killer cells. J. Biol. Chem. 270: 16415-16421.
21. Upshaw, J. L., R. A. Schoon, C. J. Dick, D. D. Billadeau, and P. J. Leibson. 2005. The isoforms of phospholipase C-γ are differentially used by distinct human NK activating receptors. J. Immunol. 175: 213-218.
22. Bryant, J., R. Day, T. L. Whiteside, and R. B. Herberman. 1992. Calculation of lytic units for the expression of cell-mediated cytotoxicity. J. Immunol. Methods 146: 91-103.
23. Takayama, H., G. Trenn, and M. V. Sitkovsky. 1987. A novel cytotoxic T lymphocyte activation assay: optimized conditions for antigen receptor triggered granule enzyme secretion. J. Immunol. Methods 104: 183-190.
24. Rubin, P., H. F. Pross, and J. C. Roder. 1982. Studies of human natural killer cells. II. Analysis at the single cell level. J. Immunol. 128: 2553-2558.
25. Vivier, E., J. A. Nunes, and F. Vely. 2004. Natural killer cell signaling pathways. Science 306: 1517-1519.
26. Houtman, J. C., R. A. Houghtling, M. Barda-Saad, Y. Toda, and L. E. Samelson. 2005. Early phosphorylation kinetics of proteins involved in proximal TCR-mediated signaling pathways. J. Immunol. 175: 2449-2458.
27. Humphries, L. A., C. Dangelmaier, K. Sommer, K. Kipp, R. M. Kato, N. Griffith, I. Bakman, C. W. Turk, J. L. Daniel, and D. J. Rawlings. 2004. Tec kinases mediate sustained calcium influx via site-specific tyrosine phosphorylation of the phospholipase Cγ Src homology 2-Src homology 3 linker. J. Biol. Chem. 279: 37651-37661.
28. Nishibe, S., M. I. Wahl, S. M. Hernandez-Sotomayor, N. K. Tonks, S. G. Rhee, and G. Carpenter. 1990. Increase of the catalytic activity of phospholipase C-γ1 by tyrosine phosphorylation. Science 250: 1253-1256.
29. Schaeffer, E. M., J. Debnath, G. Yap, D. McVicar, X. C. Liao, D. R. Littman, A. Sher, H. E. Varmus, M. J. Lenardo, and P. L. Schwartzberg. 1999. Requirement for Tec kinases Rlk and Itk in T cell receptor signaling and immunity. Science 284: 638-641.
30. Bachmann, M. F., D. R. Littman, and X. C. Liao. 1997. Antiviral immune responses in Itk-deficient mice. J. Virol. 71: 7253-7257.
31. + T cell help. J. Immunol. 176: 1571-1581.
32. + T cell lineages in mice deficient for the Tec kinases Itk and Rlk. Immunity 25: 93-104.
33. + T cells. Immunity 25: 79-91.
34. August, A., S. Gibson, Y. Kawakami, T. Kawakami, G. B. Mills, and B. Dupont. 1994. CD28 is associated with and induces the immediate tyrosine phosphorylation and activation of the Tec family kinase ITK/EMT in the human Jurkat leukemic T cell line. Proc. Natl. Acad. Sci. USA 91: 9347-9351.
35. 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. USA 92: 8891-8895.
36. Liao, X. C., and D. R. Littman. 1995. Altered T cell receptor signaling and disrupted T cell development in mice lacking Itk. Immunity 3: 757-769.
37. Liao, X. C., S. Fournier, N. Killeen, A. Weiss, J. P. Allison, and D. R. Littman. 1997. Itk negatively regulates induction of T cell proliferation by CD28 costimulation. J. Exp. Med. 186: 221-228.
38. Li, C. R., and L. J. Berg. 2005. Itk is not essential for CD28 signaling in naive T cells. J. Immunol. 174: 4475-4479.
39. Shan, X., and R. L. Wange. 1999. Itk/Emt/Tsk activation in response to CD3 cross-linking in Jurkat T cells requires ZAP-70 and Lat and is independent of membrane recruitment. J. Biol. Chem. 274: 29323-29330.
40. Dombroski, D., R. A. Houghtling, C. M. Labno, P. Precht, A. Takesono, N. J. Caplen, D. D. Billadeau, R. L. Wange, J. K. Burkhardt, and P. L. Schwartzberg. 2005. Kinase-independent functions for Itk in TCR-induced regulation of Vav and the actin cytoskeleton. J. Immunol. 174: 1385-1392.
41. Takesono, A., R. Horai, M. Mandai, D. Dombroski, and P. L. Schwartzberg. 2004. Requirement for Tec kinases in chemokine-induced migration and activation of Cdc42 and Rac. Curr. Biol. 14: 917-922.
42. 1 integrins by the T cell receptor. EMBO J. 20: 1232-1244.
43. Liu, Q. H., X. Liu, Z. Wen, B. Hondowicz, L. King, J. Monroe, and B. D. Freedman. 2005. Distinct calcium channels regulate responses of primary B lymphocytes to B cell receptor engagement and mechanical stimuli. J. Immunol. 174: 68-79.
44. 2+ response amplitude and duration. Nature 386: 855-858.
45. Dolmetsch, R. E., K. Xu, and R. S. Lewis. 1998. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392: 933-936.
46. Saito, K., K. F. Tolias, A. Saci, H. B. Koon, L. A. Humphries, A. Scharenberg, D. J. Rawlings, J. P. Kinet, and C. L. Carpenter. 2003. BTK regulates PtdIns-4,5-P2 synthesis: importance for calcium signaling and PI3K activity. Immunity 19: 669-678.
47. 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.
48. Gomez, J., A. Martinez de Aragon, P. Bonay, C. Pitton, A. Garcia, A. Silva, M. Fresno, F. Alvarez, and A. Rebollo. 1995. Physical association and functional relationship between protein kinase Cζ and the actin cytoskeleton. Eur. J. Immunol. 25: 2673-2678.
49. Fronhofer, V., M. R. Lennartz, and D. J. Loegering. 2006. Role of PKC isoforms in the FcγR-mediated inhibition of LPS-stimulated IL-12 secretion by macrophages. J. Leukocyte Biol. 79: 408-415.
50. Leitges, M., K. Gimborn, W. Elis, J. Kalesnikoff, M. R. Hughes, G. Krystal, and M. Huber. 2002. Protein kinase C-6 is a negative regulator of antigen-induced mast cell degranulation. Mol. Cell. Biol. 22: 3970-3980.
51. Uckun, F. M. 1998. Bruton's tyrosine kinase (BTK) as a dual-function regulator of apoptosis. Biochem. Pharmacol. 56: 683-691.
52. Nishizumi, H., K. Horikawa, I. Mlinaric-Rascan, and T. Yamamoto. 1998. A double-edged kinase Lyn: a positive and negative regulator for antigen receptor-mediated signals. J. Exp. Med. 187: 1343-1348.
53. Groh, V., A. Bruhl, H. El-Gabalawy, J. L. Nelson, and T. Spies. 2003. Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis. Proc. Natl. Acad. Sci. USA 100: 9452-9457.