CD25 and CD69 induction by α4β1 outside-in signalling requires TCR early signalling complex proteins

Biochemical Journal

Volumn 454, Issue 1, 2013, Pages 109-121

  Cimo, Ann Marie ^a   Ahmed, Zamal ^a   Mcintyre, Bradley W ^a   Lewis, Dorothy E ^b   Ladbury, John E ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Early signalling complex; Extracellular signal regulated kinase (ERK); Integrin; Outside in signalling; T cell co stimulation

Indexed keywords

ALPHA INTERFERON; B RAF KINASE; CD69 ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE ZAP 70; SMALL INTERFERING RNA; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1; VERY LATE ACTIVATION ANTIGEN 4;

ARTICLE; CELL COMMUNICATION; CONTROLLED STUDY; CROSS LINKING; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; HUMANS; INTEGRIN ALPHA4BETA1; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; JURKAT CELLS; LECTINS, C-TYPE; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84880889645     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130485     Document Type: Article

References (59)

1. Petricoin, E. F., Ito, S., Williams, B. L., Audet, S., Stancato, L. F., Gamero, A., Clouse, K., Grimley, P., Weiss, A., Beeler, J. et al. (1997) Antiproliferative action of interferon-α requires components of T-cell-receptor signaling. Nature 390, 629-632.
2. Micouin, A., Wietzerbin, J., Steunou, V. and Martyŕe, M. C. (2000) p95(vav) associates with type I interferon (IFN) receptor and contributes to the antiproliferative effect of IFN-α in megakaryocytic cell lines. Oncogene 19, 387-394.
3. Ticchioni, M., Charvet, C., Noraz, N., Lamy, L., Steinberg, M., Bernard, A. and Deckert, M. (2002) Signaling through ZAP-70 is required for CXCL12-mediated T-cell transendothelial migration. Blood 99, 3111-3118.
4. Kremer, K. N., Humphreys, T. D., Kumar, A., Qian, N. X. and Hedin, K. E. (2003) Distinct role of ZAP-70 and Src homology 2 domain-containing leukocyte protein of 76 kDa in the prolonged activation of extracellular signal-regulated protein kinase by the stromal cell-derived factor-1 α/CXCL12 chemokine. J. Immunol. 171, 360-367.
5. Ahmed, Z., Beeton, C. A., Williams, M. A., Clements, D., Baldari, C. T. and Ladbury, J. E. (2005) Distinct spatial and temporal distribution of ZAP70 and Lck following stimulation of interferon and T-cell receptors. J. Mol. Biol. 353, 1001-1010.
6. Kumar, A., Humphreys, T. D., Kremer, K. N., Bramati, P. S., Bradfield, L., Edgar, C. E. and Hedin, K. E. (2006) CXCR4 physically associates with the T cell receptor to signal in T cells. Immunity 25, 213-224.
7. Stevens, C. N., Simeone, A. M., John, S., Ahmed, Z., Lucherini, O. M., Baldari, T. and Ladbury, J. E. (2010) T-cell receptor early signaling complex activation in response to interferon-α receptor stimulation. Biochem. J. 428, 429-437.
8. Epler, J. A., Liu, R., Chung, H., Ottoson, N. C. and Shimizu, Y. (2000) Regulation of β1 integrin-mediated adhesion by T cell receptor signaling involves ZAP-70 but differs from signaling events that regulate transcriptional activity. J. Immunol. 165, 4941-4949.
9. Goda, S., Quale, A. C., Woods, M. L., Felthauser, A. and Shimizu, Y. (2004) Control of TCR-mediated activation of β1 integrins by ZAP-70 tyrosine kinase interdomain B region and the linker for activation of T cells adapter protein. J. Immunol. 172, 5379-5387.
10. Horn, J., Wang, X., Reichardt, P., Stradal, T. E., Warnecke, N., Simeoni, L., Gunzer, M., Yablonski, D., Schraven, B. and Kliche, S. (2009) Src homology 2-domain containing leukocyte-specific phosphoprotein of 76 kDa is mandatory for TCR-mediated inside-out signaling, but dispensable for CXCR4-mediated LFA-1 activation, adhesion, and migration of T cells. J. Immunol. 183, 5756-5767.
11. Bednarczyk, J. L., Szabo, M. C., Wygant, J. N., Lazarovits, A. I. and McIntyre, B. W. (1994) Identification of a combinatorial epitope expressed by the integrin α4β1 heterodimer involved in the regulation of cell adhesion. J. Biol. Chem. 269, 8348-8354.
12. Mege, D., Di Bartolo, V., Germain, V., Tuosto, L., Michel, F. and Acuto, O. (1996) Mutation of tyrosines 492/493 in the kinase domain of ZAP-70 affects multiple T-cell receptor signaling pathways. J. Biol. Chem. 271, 32644-32652.
13. Di Bartolo, V., Mege, D., Germain, V., Pelosi, M., Dufour, E., Michel, F., Magistrelli, G., Isacchi, A. and Acuto, O. (1999) Tyrosine 319, a newly identified phosphorylation site of ZAP-70, plays a critical role in T cell antigen receptor signaling. J. Biol. Chem. 274, 6285-6294.
14. Williams, B. L., Irvin, B. J., Sutor, S. L., Chini, C. C., Yacyshyn, E., Bubeck, W. J., Dalton, M., Chan, A. C. and Abraham, R. T. (1999) Phosphorylation of Tyr319 in ZAP-70 is required for T-cell antigen receptor-dependent phospholipase C-γ 1 and Ras activation. EMBO J. 18, 1832-1844.
15. Wu, J., Motto, D. G., Koretzky, G. A. and Weiss, A. (1996) Vav and SLP-76 interact and functionally cooperate in IL-2 gene activation. Immunity 4, 593-602.
16. Turner, M. and Billadeau, D. D. (2002) VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nat. Rev. Immunol. 2, 476-486.
17. Zhu, M., Janssen, E. and Zhang, W. (2003) Minimal requirement of tyrosine residues of linker for activation of T cells in TCR signaling and thymocyte development. J. Immunol. 170, 325-333.
18. Neumeister, E. N., Zhu, Y., Richard, S., Terhorst, C., Chan, A. C. and Shaw, A. S. (1995) Binding of ZAP-70 to phosphorylated T-cell receptor ζ and η enhances its autophosphorylation and generates specific binding sites for SH2 domain-containing proteins. Mol. Cell. Biol. 15, 3171-3178.
19. Brdicka, T., Kadlecek, T. A., Roose, J. P., Pastuszak, A. W. and Weiss, A. (2005) Intramolecular regulatory switch in ZAP-70: Analogy with receptor tyrosine kinases. Mol. Cell. Biol. 25, 4924-4933.
20. Deindl, S., Kadlecek, T. A., Cao, X., Kuriyan, J. and Weiss, A. (2009) Stability of an autoinhibitory interface in the structure of the tyrosine kinase ZAP-70 impacts T cell receptor response. Proc. Natl. Acad. Sci. U.S.A. 49, 20699-20704.
21. Raab, M., da Silva, A. J., Findell, P. R. and Rudd, C. E. (1997) Regulation of Vav-SLP-76 binding by ZAP-70 and its relevance to TCRζ/CD3 induction of interleukin-2. Immunity 6, 155-164.
22. Kapron-Bras, C., Fitz-Gibbon, L., Jeevaratnam, P., Wilkins, J. and Dedhar, S. (1993) Stimulation of tyrosine phosphorylation and accumulation of GTP-bound p21ras upon antibody-mediated α2β1 integrin activation in T-lymphoblastic cells. J. Biol. Chem. 268, 20701-20704.
23. Illario, M., Cavallo, A. L., Bayer, K. U., Di Matola, T., Fenzi, G., Rossi, G. and Vitale, M. (2003) Calcium/calmodulin-dependent kinase II binds to Raf-1 and modulates integrin-stimulated ERK activation. J. Biol. Chem. 278, 45101-45108.
24. Chetoui, N., Gendron, S., Chamoux, E. and Aoudjit, F. (2006) Collagen type-I-mediated activation of ERK/MAP kinase is dependent on Ras, Raf-1 and protein phosphatase 2A in Jurkat T cells. Mol. Immunol. 43, 1687-1693.
25. Grewal, S. S., Horgan, A. M., York, R. D., Withers, G. S., Banker, G. A. and Stork, P. J. (2000) Neuronal calcium activates a Rap1 and B-Raf signaling pathway via the cyclic adenosine monophosphate-dependent protein kinase. J. Biol. Chem. 275, 3722-3728.
26. Mercer, K. E. and Pritchard, C. A. (2003) Raf proteins and cancer: B-Raf is identified as a mutational target. Biochem. Biophys. Acta 1653, 25-40.
27. Stork, P. J. S. (2003) Does Rap1 deserve a bad Rap? Trends Biochem. Sci. 28, 267-275.
28. Jin, A., Kurosu, T., Tsuji, K., Mizuchi, D., Arai, A., Fujita, H., Hattori, M., Minato, N. and Miura, O. (2006) BCR/ABL and IL-3 activate Rap1 to stimulate the B-Raf/MEK/Erk and Akt signaling pathways and to regulate proliferation, apoptosis, and adhesion. Oncogene 25, 4332-4340.
29. Udagawa, T. and McIntyre, B. W. (1992) A VLA-4 α-chain specific monoclonal antibody enhances CD3-induced IL-2/IL-2 receptor-dependent T-cell proliferation. Lymphokine Cytokine Res. 11, 193-199.
30. Soto, T., Tachibana, K., Nojima, Y., D'Avirro, N. and Morimoto, C. (1995) Role of the VLA-4 molecule in T cell costimulation. J. Immunol. 155, 2938-2947.
31. Udagawa, T., Woodside, D. G. and McIntyre, B. W. (1996) α4β1 (CD49d/CD29) integrin costimulation of human T cells enhances transcription factor and cytokine induction in the absence of altered sensitivity to anti-CD3 stimulation. J. Immunol. 157, 1965-1972.
32. Nguyen, K., Sylvain, N. R. and Bunnell, S. C. (2008) T cell costimulation via the integrin VLA-4 inhibits the actin-dependent centralization of signaling microclusters containing the adaptor SLP-76. Immunity 28, 810-821.
33. Fernandez-Riejos, P., Goberna, R. and Sanchez-Margalet, V. (2008) Leptin promotes cell survival and activates Jurkat T lymphocytes by stimulation of mitogen-Activated protein kinase. Clin. Exp. Immunol. 151, 505-518.
34. Houben, R., Voight, H., Noelke, C., Hofmeister, V., Becker, J. C. and Schrama, D. (2009) MAPK-independent impairment of T-cell responses by the multikinase inhibitor sorafenib. Mol. Cancer Ther. 8, 433-440.
35. Wang, X., Hao, J., Metzger, D. L., Ao, Z., Chen, L., Ou, D., Verchere, B., Mui, A. and Warnock, G. L. (2012) B7-H4 treatment of T cells inhibits ERK, JNK, p38, and AKT activation. PLoS ONE 7, e28232.
36. Kim, G., Jang, M., Son, Y., Seo, M., Ji, S., Han, S., Jung, I., Park, Y., Jung, H. and Yun, C. (2013) Curcumin inhibits CD4+ T cell activation, but augments Cd69 expression and TGF-β1-mediated generation of regulatory T cells at late phase. PLoS ONE 8, e62300.
37. Evans, R., Lellouch, A. C., Svensson, L., McDowall, A. and Hogg, N. (2011) The integrin LFA-1 signals through ZAP-70 to regulate expression of high affinity LFA-1 on T lymphocytes. Blood 117, 3331-3342.
38. Katzav, S., Sutherland, M., Packham, G., Yi, T. and Weiss, A. (1994) The protein tyrosine kinase ZAP-70 can associated with the SH2 domain of proto-Vav. J. Biol. Chem. 269, 32579-32585.
39. Sylvain, N. R., Nguyen, K. and Bunnell, S. C. (2011) Vav1-mediated scaffolding interactions stabilize SLP-76 microclusters and contribute to antigen-dependent T cell responses. Sci. Signaling 4, ra14.
40. Bezman, N. A., Liam, L., Abrams, C. S., Brass, L. F., Kahn, M. L., Jordan, M. S. and Koretzky, G. A. (2008) Requirements of SLP76 tyrosines in ITAM and integrin receptor signaling and in platelet function in vivo. J. Exp. Med. 205, 1775-1788.
41. Newbrough, S. A., Mocsai, A., Clemens, R. A., Wu, J. N., Silverman, M. A., Singer, A. L., Lowell, C. A. and Koretzky, G. A. (2003) SLP-76 regulates Fcγ receptor and integrin signaling in neutrophils. Immunity 19, 759-769.
42. Baker, R. G., Hsu, C. J., Lee, D., Jordan, M. S., Maltzman, J. S., Hammer, D. A., Baumgart, T. and Koretzsky, G. A. (2009) The adapter protein SLP-76 mediates "outside-in" integrin signaling and function in T cells. Mol. Cell. Biol. 29, 5578-5589.
43. Das, S., Banerji, A., Frei, E. and Chatterjee, A. (2008) Rapid expression and activation of MMP-2 and MMP-9 upon exposure of human breast cancer cells (MCF-7) to fibronectin in serum free medium. Life Sci. 82, 467-476.
44. Saleem, S., Li, J., Yee, S.-P., Fellows, G. F., Goodyer, C. G. and Wang, R. (2009) β1 integrin/FAK/ERK signaling pathway is essential for human fetal islet cell differentiation and survival. J. Pathol. 219, 182-192.
45. Maity, G., Fahreen, S., Banerji, A., Choudhury, P. R., Sen, T., Dutta, A. and Chatterjee, A. (2010) Fibronectin-integrin mediated signaling in human cervical cancer cells (SiHa). Mol. Cell. Biochem. 336, 65-74.
46. Barberis, L., Wary, K. K., Fiucci, G., Liu, F., Hirsch, E., Brancaccio, M., Altruda, F., Tarone, G. and Giancotti, F. G. (2000) Distinct roles of the adaptor protein Shc and focal adhesion kinase in integrin signaling to ERK. J. Biol. Chem. 275, 36532-36540.
47. Calipel, A., Mouriaux, F., Glotin, A.-L., Malecaze, F., Faussat, A.-M. and Mascarelli, F. (2006) Extracellular signal-regulated kinase-dependent proliferation is mediated through protein kinase A/B-Raf pathway in human uveal melanoma cells. J. Biol. Chem. 281, 9238-9250.
48. Carey, K. D., Dillon, T. J., Schmitt, J. M., Baird, A. M., Holdorf, A. D., Straus, D. B., Shaw, A. S. and Stork, P. J. (2000) CD28 and the tyrosine kinase lck stimulate mitogen-Activated protein kinase activity in T cells via inhibition of the small G protein Rap1. Mol. Cell. Biol. 20, 8409-8419.
49. Tsukamoto, H., Irie, A. and Nishimura, Y. (2004) B-Raf contributes to sustained extracellular signal-regulated kinase activation associated with interleukin-2 production stimulated through the T cell receptor. J. Biol. Chem. 279, 48457-48465.
50. Dillon, T. J., Karpitski, V., Wetzel, S. A., Parker, D. C., Shaw, A. S. and Stork, P. J. S. (2003) Ectopic B-Raf expression enhances extracellular signal-regulated kinase (ERK) signaling in T cells and prevents antigen-presenting cell-induced anergy. J. Biol. Chem. 278, 35940-35949.
51. Holleran, B. J., Barbar, E., Payet, M. D. and Dupuis, G. (2003) Differential recruitment of α2β1 and α4β1 integrins to lipid rafts in Jurkat T lymphocytes exposed to collagen type IV and fibronectin. J. Leukoc. Biol. 73, 243-252.
52. Li, D., Molldrem, J. J. and Ma, Q. (2009) LFA-1 regulates CD8+ T cell activation via T cell receptor-mediated and LFA-1-mediated Erk1/2 signal pathways. J. Biol. Chem. 284, 21001-21010.
53. Fiegelson, S. W., Grabovsky, V., Winter, E., Chen, L. L., Pepinsky, R. B., Yednock, T., Yablonski, D., Lobb, R. and Alon, R. (2001) The Src kinase p56(lck) up-regulates VLA-4 integrin affinity. Implications for rapid spontaneous and chemokine-triggered T cell adhesion to VCAM-1 and fibronectin. J. Biol. Chem. 276, 13891-13901.
54. Billard, M. J. and McIntyre, B. W. (2008) CD45RA T-cell activation without proliferation by a partial agonist monoclonal antibody to β1 integrin. Immunol. Cell Biol. 86, 381-384.
55. Wang, H., Wei, B., Bismuth, G. and Rudd, C. E. (2009) SLP-76-ADAP adaptor module regulates LFA-1 mediated costimulation and T cell motility. Proc. Natl. Acad. Sci. U.S.A. 106, 12436-12441.
56. Woodside, D. G., Long, D. A. and McIntyre, B. W. (1999) Intracellular analysis of interleukin-2 induction provides direct evidence at the single cell level of differential coactivation requirements for CD45RA+ and CD45RO+ T cell subsets. J. Interferon Cytokine Res. 19, 769-779.
57. Sagi, Y., Landrigan, A., Levy, R. and Levy, S. (2012) Complementary costimulation of human T-cell subpopulations by cluster of differentiation 28 (CD28) and CD81. Proc. Natl. Acad. Sci. U.S.A. 109, 1613-1618.
58. Deeths, M. J. and Mescher, M. F. (1999) ICAM-1 and B7-1 provide similar but distinct costimulation for CD8+ T cells, while CD4+ T cells are poorly costimulated by ICAM-1. Eur. J. Immunol. 29, 45-53.
59. Laux, I., Khoshnan, A., Tindell, C., Bae, D., Zhu, X., June, C. H., Effros, R. B. and Nel, A. (2000) Response differences between human CD4+ and CD8+ T-cells during CD28 costimulation: implications for immune cell-based therapies and studies related to the expansion of double-positive T-cells during aging. Clin. Immunol. 96, 187-197.