The Phosphatase PTP-PEST Promotes Secondary T Cell Responses by Dephosphorylating the Protein Tyrosine Kinase Pyk2

Immunity

Volumn 33, Issue 2, 2010, Pages 167-180

  Davidson, Dominique ^a   Shi, Xiaochu ^a   Zhong, Ming Chao ^a   Rhee, Inmoo ^a,b   Veillette, André ^a,b,c  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Cellimmuno; Molimmuno

Indexed keywords

FOCAL ADHESION KINASE 2; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 12; RAC1 PROTEIN;

ALLELE; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CELL AGGREGATION; CELL MATURATION; CLONAL ANERGY; IMMUNOPATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION;

ANIMALS; CELL AGGREGATION; CELL PROLIFERATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FOCAL ADHESION KINASE 2; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROPEPTIDES; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 12; RAC GTP-BINDING PROTEINS; T-LYMPHOCYTES;

EID: 77955868530     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2010.08.001     Document Type: Article

References (43)

1. Arimura Y., Vang T., Tautz L., Williams S., Mustelin T. TCR-induced downregulation of protein tyrosine phosphatase PEST augments secondary T cell responses. Mol. Immunol. 2008, 45:3074-3084.
2. Avraham H., Park S.Y., Schinkmann K., Avraham S. RAFTK/Pyk2-mediated cellular signalling. Cell. Signal 2000, 12:123-133.
3. Badour K., Zhang J., Shi F., Leng Y., Collins M., Siminovitch K.A. Fyn and PTP-PEST-mediated regulation of Wiskott-Aldrich syndrome protein (WASp) tyrosine phosphorylation is required for coupling T cell antigen receptor engagement to WASp effector function and T cell activation. J. Exp. Med. 2004, 199:99-112.
4. Bagi C.M., Roberts G.W., Andresen C.J. Dual focal adhesion kinase/Pyk2 inhibitor has positive effects on bone tumors: Implications for bone metastases. Cancer 2008, 112:2313-2321.
5. Baker R.G., Hsu C.J., Lee D., Jordan M.S., Maltzman J.S., Hammer D.A., Baumgart T., Koretzky G.A. The adapter protein SLP-76 mediates " outside-in" integrin signaling and function in T cells. Mol. Cell. Biol. 2009, 29:5578-5589.
6. Barnden M.J., Allison J., Heath W.R., Carbone F.R. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 1998, 76:34-40.
7. Bishop A.L., Hall A. Rho GTPases and their effector proteins. Biochem. J. 2000, 348:241-255.
8. Bottini N., Musumeci L., Alonso A., Rahmouni S., Nika K., Rostamkhani M., MacMurray J., Meloni G.F., Lucarelli P., Pellecchia M., et al. A functional variant of lymphoid tyrosine phosphatase is associated with type I diabetes. Nat. Genet. 2004, 36:337-338.
9. Bottini N., Vang T., Cucca F., Mustelin T. Role of PTPN22 in type 1 diabetes and other autoimmune diseases. Semin. Immunol. 2006, 18:207-213.
10. Choi S., Schwartz R.H. Molecular mechanisms for adaptive tolerance and other T cell anergy models. Semin. Immunol. 2007, 19:140-152.
11. Cloutier J.F., Veillette A. Association of inhibitory tyrosine protein kinase p50csk with protein tyrosine phosphatase PEP in T cells and other hemopoietic cells. EMBO J. 1996, 15:4909-4918.
12. Cloutier J.F., Veillette A. Cooperative inhibition of T-cell antigen receptor signaling by a complex between a kinase and a phosphatase. J. Exp. Med. 1999, 189:111-121.
13. Cong F., Spencer S., Coté J.F., Wu Y., Tremblay M.L., Lasky L.A., Goff S.P. Cytoskeletal protein PSTPIP1 directs the PEST-type protein tyrosine phosphatase to the c-Abl kinase to mediate Abl dephosphorylation. Mol. Cell 2000, 6:1413-1423.
14. Coté J.F., Charest A., Wagner J., Tremblay M.L. Combination of gene targeting and substrate trapping to identify substrates of protein tyrosine phosphatases using PTP-PEST as a model. Biochemistry 1998, 37:13128-13137.
15. Davidson D., Veillette A. PTP-PEST, a scaffold protein tyrosine phosphatase, negatively regulates lymphocyte activation by targeting a unique set of substrates. EMBO J. 2001, 20:3414-3426.
16. Davidson D., Schraven B., Veillette A. PAG-associated FynT regulates calcium signaling and promotes anergy in T lymphocytes. Mol. Cell. Biol. 2007, 27:1960-1973.
17. Garton A.J., Tonks N.K. Regulation of fibroblast motility by the protein tyrosine phosphatase PTP-PEST. J. Biol. Chem. 1999, 274:3811-3818.
18. Garton A.J., Flint A.J., Tonks N.K. Identification of p130(cas) as a substrate for the cytosolic protein tyrosine phosphatase PTP-PEST. Mol. Cell. Biol. 1996, 16:6408-6418.
19. Gismondi A., Jacobelli J., Strippoli R., Mainiero F., Soriani A., Cifaldi L., Piccoli M., Frati L., Santoni A. Proline-rich tyrosine kinase 2 and Rac activation by chemokine and integrin receptors controls NK cell transendothelial migration. J. Immunol. 2003, 170:3065-3073.
20. Gjorloff-Wingren A., Saxena M., Williams S., Hammi D., Mustelin T. Characterization of TCR-induced receptor-proximal signaling events negatively regulated by the protein tyrosine phosphatase PEP. Eur. J. Immunol. 1999, 29:3845-3854.
21. Hasegawa K., Martin F., Huang G., Tumas D., Diehl L., Chan A.C. PEST domain-enriched tyrosine phosphatase (PEP) regulation of effector/memory T cells. Science 2004, 303:685-689.
22. Hatton R.D., Harrington L.E., Luther R.J., Wakefield T., Janowski K.M., Oliver J.R., Lallone R.L., Murphy K.M., Weaver C.T. A distal conserved sequence element controls Ifng gene expression by T cells and NK cells. Immunity 2006, 25:717-729.
23. Jamieson J.S., Tumbarello D.A., Halle M., Brown M.C., Tremblay M.L., Turner C.E. Paxillin is essential for PTP-PEST-dependent regulation of cell spreading and motility: A role for paxillin kinase linker. J. Cell Sci. 2005, 118:5835-5847.
24. Jenkins M.K., Chen C.A., Jung G., Mueller D.L., Schwartz R.H. Inhibition of antigen-specific proliferation of type 1 murine T cell clones after stimulation with immobilized anti-CD3 monoclonal antibody. J. Immunol. 1990, 144:16-22.
25. Kaye J., Hsu M.L., Sauron M.E., Jameson S.C., Gascoigne N.R., Hedrick S.M. Selective development of CD4+ T cells in transgenic mice expressing a class II MHC-restricted antigen receptor. Nature 1989, 341:746-749.
26. Kinashi T. Intracellular signalling controlling integrin activation in lymphocytes. Nat. Rev. Immunol. 2005, 5:546-559.
27. Larsen M., Tremblay M.L., Yamada K.M. Phosphatases in cell-matrix adhesion and migration. Nat. Rev. Mol. Cell Biol. 2003, 4:700-711.
28. Lyons P.D., Dunty J.M., Schaefer E.M., Schaller M.D. Inhibition of the catalytic activity of cell adhesion kinase beta by protein-tyrosine phosphatase-PEST-mediated dephosphorylation. J. Biol. Chem. 2001, 276:24422-24431.
29. Macian F., Garcia-Cozar F., Im S.H., Horton H.F., Byrne M.C., Rao A. Transcriptional mechanisms underlying lymphocyte tolerance. Cell 2002, 109:719-731.
30. Mittrucker H.W., Shahinian A., Bouchard D., Kundig T.M., Mak T.W. Induction of unresponsiveness and impaired T cell expansion by staphylococcal enterotoxin B in CD28-deficient mice. J. Exp. Med. 1996, 183:2481-2488.
31. Ostergaard H.L., Lou O., Arendt C.W., Berg N.N. Paxillin phosphorylation and association with Lck and Pyk2 in anti-CD3- or anti-CD45-stimulated T cells. J. Biol. Chem. 1998, 273:5692-5696.
32. Qian D., Lev S., van Oers N.S., Dikic I., Schlessinger J., Weiss A. Tyrosine phosphorylation of Pyk2 is selectively regulated by Fyn during TCR signaling. J. Exp. Med. 1997, 185:1253-1259.
33. Roberts W.G., Ung E., Whalen P., Cooper B., Hulford C., Autry C., Richter D., Emerson E., Lin J., Kath J., et al. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res. 2008, 68:1935-1944.
34. Sabatos C.A., Doh J., Chakravarti S., Friedman R.S., Pandurangi P.G., Tooley A.J., Krummel M.F. A synaptic basis for paracrine interleukin-2 signaling during homotypic T cell interaction. Immunity 2008, 29:238-248.
35. Shen Y., Schneider G., Cloutier J.F., Veillette A., Schaller M.D. Direct association of protein-tyrosine phosphatase PTP-PEST with paxillin. J. Biol. Chem. 1998, 273:6474-6481.
36. Sirois J., Coté J.F., Charest A., Uetani N., Bourdeau A., Duncan S.A., Daniels E., Tremblay M.L. Essential function of PTP-PEST during mouse embryonic vascularization, mesenchyme formation, neurogenesis and early liver development. Mech. Dev. 2006, 123:869-880.
37. Stewart M.P., Cabanas C., Hogg N. T cell adhesion to intercellular adhesion molecule-1 (ICAM-1) is controlled by cell spreading and the activation of integrin LFA-1. J. Immunol. 1996, 156:1810-1817.
38. Utting O., Priatel J.J., Teh S.J., Teh H.S. p59fyn (Fyn) promotes the survival of anergic CD4-CD8- alpha beta TCR+ cells but negatively regulates their proliferative response to antigen stimulation. J. Immunol. 2001, 166:1540-1546.
39. Veillette A., Latour S., Davidson D. Negative regulation of immunoreceptor signaling. Annu. Rev. Immunol. 2002, 20:669-707.
40. Veillette A., Rhee I., Souza C.M., Davidson D. PEST family phosphatases in immunity, autoimmunity, and autoinflammatory disorders. Immunol. Rev. 2009, 228:312-324.
41. Wang L., Gordon R.A., Huynh L., Su X., Park Min K.H., Han J., Arthur J.S., Kalliolias G.D., Ivashkiv L.B. Indirect inhibition of Toll-like receptor and type I interferon responses by ITAM-coupled receptors and integrins. Immunity 2010, 32:518-530.
42. Zhong M.C., Kerlero de Rosbo N., Ben Nun A. Multiantigen/multiepitope-directed immune-specific suppression of " complex autoimmune encephalomyelitis" by a novel protein product of a synthetic gene. J. Clin. Invest. 2002, 110:81-90.
43. Zikherman J., Hermiston M., Steiner D., Hasegawa K., Chan A., Weiss A. PTPN22 deficiency cooperates with the CD45 E613R allele to break tolerance on a non-autoimmune background. J. Immunol. 2009, 182:4093-4106.