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Mining the Complex Family of Protein Tyrosine Phosphatases for Checkpoint Regulators in Immunity

  • Claudia Penafuerte
  • Luis Alberto Perez-Quintero
  • Valerie Vinette
  • Teri Hatzihristidis
  • Michel L. TremblayEmail author
Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 410)

Abstract

The family of protein tyrosine phosphatases (PTPs) includes 107 genes in humans that are diverse in their structures and expression profiles. The majority are present in immune cells and play various roles in either inhibiting or promoting the duration and amplitude of signaling cascades. Several PTPs, including TC-PTP (PTPN2) and SHP-1 (PTPN6), have been recognized as being crucial for maintaining proper immune response and self-tolerance, and have gained recognition as true immune system checkpoint modulators. This chapter details the most recent literature on PTPs and immunity by examining their known functions in regulating signaling from either established checkpoint inhibitors or by their intrinsic properties, as modulators of the immune response. Notably, we review PTP regulatory properties in macrophages, antigen-presenting dendritic cells, and T cells. Overall, we present the PTP gene family as a remarkable source of novel checkpoint inhibitors wherein lies a great number of new targets for immunotherapies.

Notes

Acknowledgements

We thank N. Uetani for expert graphical assistance. In addition, we recognize the support of the Canadian Institute of Health Research (grant MOP-62887) and the Aclon-Richard and Edith Strauss Foundation to M.L.T., V.V. is a recipient of the Charlotte and Leo Karassik Family Foundation Fellowship, T.H. is a recipient of a Fonds de Recherche du Quebec—Santé studentships. M.L.T. is a holder of the Jeanne and Jean-Louis Lévesque Chair in Cancer Research.

References

  1. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511. doi: 10.1007/s10753-017-0604-7CrossRefPubMedGoogle Scholar
  2. Alonso A, Pulido R (2016) The extended human PTPome: a growing tyrosine phosphatase family. FEBS J April 283(8):1404–1429Google Scholar
  3. Alonso A, Sasin J, Bottini N, Friedberg I, Friedberg I, Osterman A, Godzik A, Hunter T, Dixon J, Mustelin T (2004) Protein tyrosine phosphatases in the human genome. Cell June 11 117(6):699–711. ReviewGoogle Scholar
  4. An H, Zhao W, Hou J, Zhang Y, Xie Y, Zheng Y et al (2006) SHP-2 phosphatase negatively regulates the TRIF adaptor protein-dependent type I interferon and proinflammatory cytokine production. Immunity 25:919–928. doi: 10.1016/j.immuni.2006.10.014CrossRefPubMedGoogle Scholar
  5. Anderson HA, Maylock CA, Williams JA, Paweletz CP, Shu H, Shacter E (2003) Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat Immunol 4:87–91. doi: 10.1038/ni871CrossRefPubMedGoogle Scholar
  6. Angers-Loustau A, Cote JF, Charest A, Dowbenko D, Spencer S, Lasky LA et al (1999) Protein tyrosine phosphatase-PEST regulates focal adhesion disassembly, migration, and cytokinesis in fibroblasts. J Cell Biol 144:1019–1031CrossRefGoogle Scholar
  7. Anguille S, Smits EL, Lion E, van Tendeloo VF, Berneman ZN (2014) Clinical use of dendritic cells for cancer therapy. Lancet Oncol 15:e257–e267CrossRefGoogle Scholar
  8. Arimura Y, Yagi J (2010) Comprehensive expression profiles of genes for protein tyrosine phosphatases in immune cells. Sci Signal 3(137):1–11CrossRefGoogle Scholar
  9. Arima K, Watanabe N, Hanabuchi S, Chang M, Sun SC, Liu YJ (2010) Distinct signal codes generate dendritic cell functional plasticity. Sci Signal 3:ra4Google Scholar
  10. Arregui CO, Balsamo J, Lilien J (1998) Impaired integrin-mediated adhesion and signaling in fibroblasts expressing a dominant-negative mutant PTP1B. J Cell Biol 143:861–873CrossRefGoogle Scholar
  11. Bakdash G, Sittig S, van Dijk T, Figdor C, Jolanda de Vries I (2013) The nature of activatory and tolerogenic dendritic cell-derived signal II. Front Immunol 4:53CrossRefGoogle Scholar
  12. Barron L, Wynn TA (2011) Macrophage activation governs schistosomiasis-induced inflammation and fibrosis. Eur J Immunol 41(9):2509–2514Google Scholar
  13. Bar-Sagi D, Hall A (2000) Ras and Rho GTPases: a family reunion. Cell 103:227–238CrossRefGoogle Scholar
  14. Beatty GL, Chiorean EG, Fishman MP, Saboury B, Teitelbaum UR, Sun W et al (2011) CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 331:612–616CrossRefGoogle Scholar
  15. Berdnikovs S, Pavlov VI, Abdala-Valencia H, McCary CA, Klumpp DJ, Tremblay ML, Cook-Mills JM (2012) PTP1B deficiency exacerbates inflammation and accelerates leukocyte trafficking in vivo. J Immunol 188:874–884CrossRefGoogle Scholar
  16. Bussières-Marmen S, Hutchins AP, Schirbel A, Rebert N, Tiganis T, Fiocchi C, Miranda-Saavedra D, Tremblay ML (2014) Characterization of PTPN2 and its use as a biomarker. Methods January 15 65(2):239–246Google Scholar
  17. Calvo CR, Amsen D, Kruisbeek AM (1997) Cytotoxic T lymphocyte antigen 4 (CTLA-4) interferes with extracellular signal-regulated kinase (ERK) and Jun NH2 terminal kinase (JNK) activation, but does not affect phosphorylation of T cell receptor ζ and ZAP70. J Exp Med 186:1645–1653CrossRefGoogle Scholar
  18. Carmi Y, Prestwood TR, Spitzer MH, Linde IL, Chabon J, Reticker-Flynn NE et al (2016) Akt and SHP-1 are DC-intrinsic checkpoints for tumor immunity. JCI insight 1:e89020CrossRefGoogle Scholar
  19. Chang HH, Miaw SC, Tseng W, Sun YW, Liu CC, Tsao HW et al (2013) PTPN22 modulates macrophage polarization and susceptibility to dextran sulfate sodium-induced colitis. J Immunol 191:2134–2143CrossRefGoogle Scholar
  20. Charbonneau H, Tonks NK, Walsh KA, Fischer EH (1988) The leukocyte common antigen (CD45): A putative receptor-linked protein tyrosine phosphatase. Proc Natl Acad Sci USA 85:7182–7186CrossRefGoogle Scholar
  21. Chemnitz JM, Parry RV, Nichols KE, June CH, Riley JL (2004) SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J Immunol 173:945–954CrossRefGoogle Scholar
  22. Chen YN, LaMarche MJ, Chan HM, Fekkes P, Garcia-Fortanet J, Acker MG, Antonakos B et al (2016) Allosteric inhibition of SHP2 phosphatase inhibits cancers driven by receptor tyrosine kinases. Nature July 7 535(7610):148–152. Epub 2016 Jun 29Google Scholar
  23. Constantino J, Gomes C, Falcao A, Neves BM, Cruz MT (2017) Dendritic cell-based immunotherapy: a basic review and recent advances. Immunol Res. doi: 10.1007/s12026-017-8931-1CrossRefPubMedGoogle Scholar
  24. Covarrubias AJ, Aksoylar HI, Horng T (2015) Control of macrophage metabolism and activation by mTOR and Akt signaling. Semin Immunol 27:286–296CrossRefGoogle Scholar
  25. Croker BA, Krebs DL, Zhang JG, Wormald S, Willson TA, Stanley EG et al (2003) SOCS3 negatively regulates IL-6 signaling in vivo. Nat Immunol 4(6):540–545CrossRefGoogle Scholar
  26. Cromie MJ1, Groisman EA (2010) Promoter and riboswitch control of the Mg2 + transporter MgtA from Salmonella enterica. J Bacteriol January 192(2):604–607Google Scholar
  27. Cunninghame Graham DS, Vyse TJ, Fortin PR, Montpetit A, Cai YC, Lim S, McKenzie T, Farwell L, Rhodes B, Chad L, Hudson TJ, Sharpe A, Terhorst C, Greenwood CM, Wither J, Rioux JD (2008) Association of LY9 in UK and Canadian SLE families. Genes Immun 9:93–102CrossRefGoogle Scholar
  28. David M, Chen HE, Goelz S, Larner AC, Neel BG (1995) Differential regulation of the α/β interferon-stimulated Jak/Stat pathway by the SH2 domain-containing tyrosine phosphatase SHPTP1. Mol Cell Biol 15:7050–7058CrossRefGoogle Scholar
  29. Davies LC, Jenkins SJ, Allen JE, Taylor PR (2013) Tissue-resident macrophages. Nat Immunol 14:986–995CrossRefGoogle Scholar
  30. Dhodapkar MV, Steinman RM, Krasovsky J, Munz C, Bhardwaj N (2001) Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J Exp Med 193:233–238CrossRefGoogle Scholar
  31. Dong Z, Davidson D, Pérez-Quintero LA, Kurosaki T, Swat W, Veillette A (2012) The adaptor SAP controls NK Cell activation by regulating the enzymes Vav-1 and SHIP-1 and by enhancing conjugates with target cells. Immunity 36:974–985CrossRefGoogle Scholar
  32. Dubé N, Bourdeau A, Heinonen KM, Cheng A, Loy AL, Tremblay ML (2005) Genetic ablation of protein tyrosine phosphatase 1B accelerates lymphomagenesis of p53-null mice through the regulation of B-cell development. Cancer Res 65(21):10088–10095. PMID:16267035Google Scholar
  33. Elchebly M, Payette P, Michaliszyn E, Cromlish W, Collins S, Loy AL, Normandin D, Cheng A, Himms-Hagen J, Chan CC, Ramachandran C, Gresser MJ, Tremblay ML, Kennedy BP (1999) Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 283(5407):1544–1548. PMID:10066179Google Scholar
  34. Faure-Andre G, Vargas P, Yuseff MI, Heuze M, Diaz J, Lankar D et al (2008) Regulation of dendritic cell migration by CD74, the MHC class II-associated invariant chain. Science 322:1705–1710CrossRefGoogle Scholar
  35. Feldhammer M, Uetani N, Miranda-Saavedra D, Tremblay ML (2013) PTP1B: a simple enzyme for a complex world. Crit Rev Biochem Mol Biol. Sep-Oct 48(5):430–445CrossRefGoogle Scholar
  36. Fourcade J, Sun Z, Pagliano O, Guillaume P, Luescher IF, Sander C, Kirkwood JM, Olive D, Kuchroo V, Zarour HM (2012) CD8 T cells specific for tumor antigens can be rendered dysfunctional by the tumor microenvironment through upregulation of the inhibitory receptors BTLA and PD-1. Can Res 72:887–896CrossRefGoogle Scholar
  37. Frearson JA, Alexander DA (1998) The phosphotyrosine phosphatase SHP-2 participates in a multimeric signaling complex and regulates T cell receptor (TCR) coupling to the ras/mitogen-activated protein kinase (MAPK) pathway in Jurkat T cells. J Exp Med 187:1417–1426CrossRefGoogle Scholar
  38. Frey AB, Monu N (2008) Signaling defects in anti-tumor T cells. Immunol Rev 222:192–205CrossRefGoogle Scholar
  39. Gabrilovich D (2004) Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat Rev Immunol 4:941–952CrossRefGoogle Scholar
  40. Garg AD, Vara Perez M, Schaaf M, Agostinis P, Zitvogel L, Kroemer G, et al (2017) Trial watch: Dendritic cell-based anticancer immunotherapy. Onco Immunol e1328341Google Scholar
  41. Golubovskaya V, Wu L (2016) Different subsets of T Cells, memory, effector functions, and CAR-T immunotherapy. Cancers 8:36CrossRefGoogle Scholar
  42. Grant L, Shearer K, Czopek A et al (2014) Myeloid-cell protein tyrosine phosphatase-1B deficiency in mice protects against high—fat diet and lipopolysaccharide induced inflammation, hyperinsulinemia and endotoxemia through an IL-10 STAT3-dependent mechanism. Diabetes 63:456–470CrossRefGoogle Scholar
  43. Gungabeesoon J, Tremblay ML, Uetani N (2016) Localizing PRL-2 expression and determining the effects of dietary Mg(2 +) on expression levels. Histochem Cell Biol July 146(1):99–111Google Scholar
  44. Guntermann C, Alexander DR (2002) CTLA-4 suppresses proximal TCR signaling in resting human CD4 T cells by inhibiting ZAP-70 Tyr < sup > 319 </sup > phosphorylation: a potential role for tyrosine phosphatases. J Immunol 168:4420–4429CrossRefGoogle Scholar
  45. Hardy S, Uetani N, Wong N, Kostantin E, Labbé DP, Bégin LR, Mes-Masson A, Miranda-Saavedra D, Tremblay ML (2015) The protein tyrosine phosphatase PRL-2 interacts with the magnesium transporter CNNM3 to promote oncogenesis. Oncogene February 19 34(8):986–995Google Scholar
  46. Haymaker CL, Wu RC, Ritthipichai K, Bernatchez C, Forget MA, Chen JQ, Liu H, Wang E, Marincola F, Hwu P, Radvanyi LG (2015) BTLA marks a less-differentiated tumor-infiltrating lymphocyte subset in melanoma with enhanced survival properties. Oncoimmunology 4:e1014246CrossRefGoogle Scholar
  47. Heinonen KM, Bourdeau A, Doody KM, Tremblay ML (2009) Protein tyrosine phosphatases PTP-1B and TC-PTP play nonredundant roles in macrophage development and IFN-γ signaling. Proc Natl Acad Sci 106:9368–9372CrossRefGoogle Scholar
  48. Hoentjen F, Sartor RB, Ozaki M, Jobin C (2005) STAT3 regulates NF-kappaB recruitment to the IL-12p40 promoter in dendritic cells. Blood 105:689–696CrossRefGoogle Scholar
  49. Irie-Sasake J, Sasaki T, Matsumoto W, Opavsky A, Cheng M, Welstead G et al (2000) CD45 is a JAK phosphatase and negatively regulated cytokine receptor signaling. Nature 409:349–354CrossRefGoogle Scholar
  50. Julien SG, Dubé N, Hardy S, Tremblay ML (2011) Inside the human cancer tyrosine phosphatome. Nat Rev Cancer January 11(1):35–49Google Scholar
  51. Kitamura H, Kamon H, Sawa S, Park SJ, Katunuma N, Ishihara K et al (2005) IL-6-STAT3 controls intracellular MHC class II alphabeta dimer level through cathepsin S activity in dendritic cells. Immunity 23:491–502CrossRefGoogle Scholar
  52. Kozicky LK, Sly LM (2015) Phosphatase regulation of macrophage activation. Semin Immunol 27:276–285CrossRefGoogle Scholar
  53. Lang R, Pauleau AL, Parganas E, Takahashi Y, Mages J, Ihle JN et al (2003) SOCS3 regulates the plasticity of gp130 signaling. Nat Immunol 4(6):546–550CrossRefGoogle Scholar
  54. Laouar Y, Welte T, Fu XY, Flavell RA (2003) STAT3 is required for Flt3L-dependent dendritic cell differentiation. Immunity 19:903–912CrossRefGoogle Scholar
  55. Latchman Y1, Wood CR, Chernova T, Chaudhary D, Borde M, Chernova I, Iwai Y, Long AJ, Brown JA, Nunes R, Greenfield EA, Bourque K, Boussiotis VA, Carter LL, Carreno BM, Malenkovich N, Nishimura H, Okazaki T, Honjo T, Sharpe AH, Freeman GJ (2001) PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol 2:261–268Google Scholar
  56. Latour S, Gish G, Helgason CD, Humphries RK, Pawson T, Veillette A (2001) Regulation of SLAM-mediated signal transduction by SAP, the X-linked lymphoproliferative gene product. Nat Immunol 2:681–690CrossRefGoogle Scholar
  57. Ledbetter JA, Tonks NK, Fischer EH, Clark EA (1988) CD45 regulates signal transduction and lymphocyte activation by specific association with receptor molecules on T or B cells. Proc Natl Acad Sci USA 85:8628–8632Google Scholar
  58. Lee KM, Chuang E, Griffin M, Khattri R, Hong DK, Zhang W, Straus D, Samelson LE, Thompson CB, Bluestone JA (1998) Molecular basis of T cell inactivation by CTLA-4. Science 282:2263–2266CrossRefGoogle Scholar
  59. Li HS, Watowich SS (2013) Diversification of dendritic cell subsets: emerging roles for STAT proteins. Jak-Stat 2:e25112CrossRefGoogle Scholar
  60. Lim WA1, Pawson T (2010) Phosphotyrosine signaling: evolving a new cellular communication system. Cell September 3 142(5):661–667Google Scholar
  61. Lissandrini D, Vermi W, Vezzalini M, Sozzani S, Facchetti F, Bellone G et al (2006) Receptor-type protein tyrosine phosphatase gamma (PTPgamma), a new identifier for myeloid dendritic cells and specialized macrophages. Blood 108:4223–4231CrossRefGoogle Scholar
  62. Li M, Xia P, Du Y et al (2014) T-cell immunoglobulin and ITIM Domain (TIGIT) receptor/poliovirus receptor (PVR) ligand engagement suppresses interferon-γ Production of natural killer cells via β-arrest in 2-mediated negative signaling. J Biol Chem 289:17647–17657CrossRefGoogle Scholar
  63. Liu X-G, Hou M, Liu Y (2017) TIGIT: a novel therapeutic target for tumor immunotherapy. Immunological Investigations 46:172–182CrossRefGoogle Scholar
  64. Lozano E, Dominguez-Villar M, Kuchroo V, Hafler DA (2012) The TIGIT/CD226 axis regulates human T cell function. J Immunol 188:3869–3875CrossRefGoogle Scholar
  65. Lu X, Malumbres R, Shields B, Jiang X, Sarosiek KA, Natkunam Y, Tiganis T, Lossos IS (2008) PTP1B is a negative regulator of interleukin 4–induced STAT6 signaling, Blood 112:4098–108Google Scholar
  66. Lugo-Villarino G, Maldonado-Lopez R, Possemato R, Penaranda C, Glimcher LH (2003) T-bet is required for optimal production of IFN-gamma and antigen-specific T cell activation by dendritic cells. PNAS 100:7749–7754CrossRefGoogle Scholar
  67. Mantovani A, Marchesi D, Malesci A, Laghi L, Allavena P (2017) Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol 14(7):399–416CrossRefGoogle Scholar
  68. Marengère LE, Waterhouse P, Duncan GS, Mittrücker HW, Feng GS, Mak TW (1996) Regulation of T cell receptor signaling by tyrosine phosphatase SYP association with CTLA-4. Science 272:1170–1173CrossRefGoogle Scholar
  69. Medgyesi D, Hobeika E, Biesen R, Kollert F, Taddeo A, Voll RE, Hiepe F, Reth M (2014) The protein tyrosine phosphatase PTP1B is a negative regulator of CD40 and BAFF-R signaling and controls B cell autoimmunity. J Exp Med 211:427–440CrossRefGoogle Scholar
  70. Mills CD, Shearer J, Evans R, Caldwell MD (1992) Macrophage arginine metabolism and the inhibition or stimulation of cancer. J Immunol 149:2709–2714PubMedGoogle Scholar
  71. Mills CD, Lenz LL, Harris RA (2016) A breakthrough: macrophage-directed cancer immunotherapy. Can Res 76(3):513–516CrossRefGoogle Scholar
  72. Murphy K, Weaver C (2017) Janeway’s immunobiology, 9th edn. Garland Science, Taylor & Francis Group, pp 7, 78–79, 839, 841Google Scholar
  73. Murphy K, Travers P, M. Walport M (2008) Janeway’s Immunobiology. 7th edn. Garland Science, Taylor & Francis Group. 888ppGoogle Scholar
  74. Murray PJ, Wynn TA (2011) Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 11:723–737CrossRefGoogle Scholar
  75. Myers Michael P, Andersen Jannik N, Cheng Alan, Tremblay Michel L, Horvath Curt M, Parisien Jean-Patrick, Salmeen Annette, Barford David, Tonks Nicholas K (2001) TYK2 and JAK2 are substrates of protein-tyrosine phosphatase 1B. J Biol Chem 276:47771–47774CrossRefGoogle Scholar
  76. Nicolette CA, Healey D, Tcherepanova I, Whelton P, Monesmith T, Coombs L et al (2007) Dendritic cells for active immunotherapy: optimizing design and manufacture in order to develop commercially and clinically viable products. Vaccine 25(Suppl 2):B47–B60CrossRefGoogle Scholar
  77. Okazaki T, Maeda A, Nishimura H, Kurosaki T, Honjo T (2001) PD-1 immunoreceptor inhibits B cell receptor-mediated signaling by recruiting src homology 2-domain-containing tyrosine phosphatase 2 to phosphotyrosine. Proc Natl Acad Sci 98:13866–13871CrossRefGoogle Scholar
  78. Pandey R, Saxena M, Kapur R (2017) Role of SHP2 in hematopoiesis and leukemogenesis. Curr Opin Hematol July 24(4):307–313Google Scholar
  79. Paulos CM, June CH (2010) Putting the brakes on BTLA in T cell–mediated cancer immunotherapy. J Clin Investig 120:76–80CrossRefGoogle Scholar
  80. Pawson T (2004) Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116:191–203CrossRefGoogle Scholar
  81. Penafuerte C, Feldhammer M, Mills JR, Vinette V, Pike KA, Hall A et al (2017) Downregulation of PTP1B and TC-PTP phosphatases potentiate dendritic cell-based immunotherapy through IL-12/IFNγ signaling. OncoImmunology 6:e1321185CrossRefGoogle Scholar
  82. Pérez-Quintero LA, Roncagalli R, Guo H, Latour S, Davidson D, Veillette A (2014) EAT-2, a SAP-like adaptor, controls NK cell activation through phospholipase Cγ, Ca ++, and Erk, leading to granule polarization. J Exp Med 211:727–742CrossRefGoogle Scholar
  83. Pike KA, Hutchins AP, Vinette V, Théberge JF, Sabbagh L, Tremblay ML, et al (2014). Protein tyrosine phosphatase 1B is a regulator of the IL-10-induced transcriptional program in macrophages. Sci Signal 7(324): ra43Google Scholar
  84. Pike KA, Tremblay ML (2016) TC-PTP and PTP1B: regulating JAK-STAT signaling, controlling lymphoid malignancies. Cytokine 82:52–57CrossRefGoogle Scholar
  85. Ramachandran IR, Song W, Lapteva N, Seethammagari M, Slawin KM, Spencer DM, Levitt JM (2011) The phosphatase SRC homology region 2 domain-containing phosphatase-1 is an intrinsic central regulator of dendritic cell function. J Immunol 186(7):3934–3945. PMID:21357539. doi: 10.4049/jimmunol.1001675
  86. Rothlin CV, Ghosh S, Zuniga EI, Oldstone MB, Lemke G (2007) TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 131:1124–1136CrossRefGoogle Scholar
  87. Ruffell B, Coussens LM (2015) Macrophages and therapeutic resistance in cancer. Cancer Cell 13:462–472CrossRefGoogle Scholar
  88. Sathish JG1, Johnson KG, Fuller KJ, LeRoy FG, Meyaard L, Sims MJ, Matthews RJ (2001) Constitutive association of SHP-1 with Leukocyte-associated Ig-Like receptor-1 in human T cells. J Immunol 166:1763–1770Google Scholar
  89. Schneider H, Smith X, Liu H, Bismuth G, Rudd CE (2008) CTLA-4 disrupts ZAP70 microcluster formation with reduced T cell/APC dwell times and calcium mobilization. Eur J Immunol 38:40–47CrossRefGoogle Scholar
  90. Shlapatska LM, Mikhalap SV, Berdova AG, Zelensky OM, Yun TJ, Nichols KE, Clark EA, Sidorenko SP (2001) CD150 Association with either the SH2-containing inositol phosphatase or the SH2-containing protein tyrosine phosphatase is regulated by the adaptor protein SH2D1A. J Immunol 166:5480–5487CrossRefGoogle Scholar
  91. Stitt TN, Conn G, Gore M, Lai C, Bruno J, Radziejewski C et al (1995) The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro 3/Axl family of receptor tyrosine kinases. Cell 80:661–670CrossRefGoogle Scholar
  92. St-Pierre J, Tremblay ML (2012) Modulation of leptin resistance by protein tyrosine phosphatases. Cell Metab March 7 15(3):292–297Google Scholar
  93. Stuible M, Dubé N, Tremblay ML (2008) PTP1B regulates cortactin tyrosine phosphorylation by targeting Tyr446. J Biol Chem June 6 283(23):15740–15746Google Scholar
  94. Tao B, Jin W, Xu J, Liang Z, Yao J, Zhang Y et al (2014) Myeloid-specific disruption of tyrosine phosphatase Shp2 promotes alternative activation of macrophages and predisposes mice to pulmonary fibrosis. J Immunol 193(6):2801–2811CrossRefGoogle Scholar
  95. Tonks NK (2006) Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol November 7(11):833–846Google Scholar
  96. Tonks NK (2013) Protein tyrosine phosphatases–from housekeeping enzymes to master regulators of signal transduction. FEBS J January 280(2):346–378Google Scholar
  97. Tonks NK, Charbonneau H, Diltz CD, Fischer EH, Walsh KA (1984) Demonstration that the leukocyte common antigen CD45 is a protein tyrosine phosphatase. Biochemistry 27:8695–8701CrossRefGoogle Scholar
  98. Uetani N, Hardy S, Gravel SP, Kiessling S, Pietrobon A, Wong NN, Chénard V, Cermakian N, St-Pierre J, Tremblay ML (2017) PRL2 links magnesium flux and sex-dependent circadian metabolic rhythms. JCI Insight July 6 2(13)Google Scholar
  99. van Beek JJ, Wimmers F, Hato SV, de Vries IJ, Skold AE (2014) Dendritic cell cross talk with innate and innate-like effector cells in antitumor immunity: implications for DC vaccination. Crit Rev Immunol 34:517–536CrossRefGoogle Scholar
  100. Veillette A, Dong Z, Pérez-Quintero LA, Zhong MC, Cruz-Munoz ME (2009) Importance and mechanism of ‘switch’ function of SAP family adapters. Immunol Rev 232:229–239CrossRefGoogle Scholar
  101. Veillette A, Pérez-Quintero LA, Latour S (2013) X-linked lymphoproliferative syndromes and related autosomal recessive disorders. Curr Opin Allergy Clin Immunol 13:614–622CrossRefGoogle Scholar
  102. Wakamatsu E Mathis D, Benoist C (2013) Convergent and divergent effects of costimulatory molecules in conventional and regulatory CD4 + T cells. Proc Natl Acad Sci 110:1023–1028Google Scholar
  103. Watanabe N, Gavrieli M et al (2003) BTLA is a lymphocyte inhibitory receptor with similarities to CTLA-4 and PD-1. Nat Immunol 4:670–679CrossRefGoogle Scholar
  104. Watson HA, Wehenkel S, Matthews J, Ager A (2016) SHP-1: the next checkpoint target for cancer immunotherapy? Biochem Soc Trans 44:356–362CrossRefGoogle Scholar
  105. Wherry EJ, Kurachi M (2015) Molecular and cellular insights into T cell exhaustion. Nat Rev Immunol 15:486–499CrossRefGoogle Scholar
  106. Wiede F, Shields BJ, Chew SH et al (2011) T cell protein tyrosine phosphatase attenuates T cell signaling to maintain tolerance in mice. J Clin Invest 121:4758–474Google Scholar
  107. Wiede F, Sacirbegovic F, Leong YA, Yu D, Tiganis T (2017) PTPN2-deficiency exacerbates T follicular helper cell and B cell responses and promotes the development of autoimmunity. J Autoimmun 76:85–100CrossRefGoogle Scholar
  108. Wu, TH, Zhen Y, et al (2007) B and T lymphocyte attenuator interacts with CD3[zeta] and inhibits tyrosine phosphorylation of TCR[zeta] complex during T-cell activation. Immunol Cell Biol 85:590–595Google Scholar
  109. Yokosuka T, Takamatsu M, et al (2012) Programmed cell death 1 forms negative costimulatory microclusters that directly inhibit T cell receptor signaling by recruiting phosphatase SHP2. J Exp Med 209:1201–1217Google Scholar
  110. Xu D1, Qu CK (2008) Protein tyrosine phosphatases in the JAK/STAT pathway Front Biosci May 1 13:4925–4932Google Scholar
  111. You-Ten KE1, Muise ES, Itié A, Michaliszyn E, Wagner J, Jothy S, Lapp WS, Tremblay ML (1997) Impaired bone marrow microenvironment and immune function in T cell protein tyrosine phosphatase–deficient mice. J Exper Med 186:683–693Google Scholar
  112. Yu DH, Qu CK, Henegariu O, Lu X, Feng GS (1998) Protein-tyrosine phosphatase Shp-2 regulates cell spreading, migration, and focal adhesion. J Biol Chem 273:21125–21131Google Scholar
  113. Zikherman J, Weiss A (2008) Alternative splicing of CD45: the tip of the iceberg. Immunity December 19 29(6):839–841Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Claudia Penafuerte
    • 1
    • 2
  • Luis Alberto Perez-Quintero
    • 1
  • Valerie Vinette
    • 1
  • Teri Hatzihristidis
    • 1
  • Michel L. Tremblay
    • 1
    Email author
  1. 1.Rosalind and Morris Goodman Cancer Research Centre and Department of BiochemistryMcGill UniversityMontrealCanada
  2. 2.Biotechnology Research Institute-NRCMontrealCanada

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