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PMID: 30429852 Published · epublish English Journal Article Research Support, Non-U.S. Gov't Review

Protein Tyrosine Phosphatases: Regulators of CD4 T Cells in Inflammatory Bowel Disease.

Frontiers in immunology ·Vol. 9 ·2018-00-00 ·Pages 2504

Pike KA, Tremblay ML

Abstract

Protein tyrosine phosphatases (PTPs) play a critical role in co-ordinating the signaling networks that maintain lymphocyte homeostasis and direct lymphocyte activation. By dephosphorylating tyrosine residues, PTPs have been shown to modulate enzyme activity and both mediate and disrupt protein-protein interactions. Through these molecular mechanisms, PTPs ultimately impact lymphocyte responses to environmental cues such as inflammatory cytokines and chemokines, as well as antigenic stimulation. Mouse models of acute and chronic intestinal inflammation have been shown to be exacerbated in the absence of PTPs such as PTPN2 and PTPN22. This increase in disease severity is due in part to hyper-activation of lymphocytes in the absence of PTP activity. In accordance, human PTPs have been linked to intestinal inflammation. Genome wide association studies (GWAS) identified several PTPs within risk loci for inflammatory bowel disease (IBD). Therapeutically targeting PTP substrates and their associated signaling pathways, such as those implicated in CD4+ T cell responses, has demonstrated clinical efficacy. The current review focuses on the role of PTPs in controlling CD4+ T cell activity in the intestinal mucosa and how disruption of PTP activity in CD4+ T cells can contribute to intestinal inflammation.

Keywords
CD4 T cells JAK-STAT cytokine inflammatory bowel disease protein tyrosine phosphatase
MeSH Terms
Animals CD4-Positive T-Lymphocytes/immunology Disease Models, Animal Genome-Wide Association Study Humans Inflammation/immunology Inflammatory Bowel Diseases/genetics,immunology Intestinal Mucosa/immunology Lymphocyte Activation Mice Protein Tyrosine Phosphatases/genetics,metabolism Risk
Chemicals
Protein Tyrosine Phosphatases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Pike Kelly A
Department of Microbiology and Immunology, McGill University, Montréal, QC, Canada. | Inception Sciences Canada, Montréal, QC, Canada.
Tremblay Michel L
Department of Microbiology and Immunology, McGill University, Montréal, QC, Canada. | Rosalind and Morris Goodman Cancer Centre, McGill University, Montréal, QC, Canada. | Division of Experimental Medicine, Department of Medicine, McGill University, Montréal, QC, Canada. | Department of Biochemistry, McGill University, Montréal, QC, Canada.
References (175)
175 references, click to expand
  1. In Vivo Knockdown of Pathogenic Proteins via Specific and Nongenetic Inhibitor of Apoptosis Protein (IAP)-dependent Protein Erasers (SNIPERs).
    J Biol Chem. 2017 Mar 17;292(11):4556-4570 PMID: 28154167
  2. Purification of the major protein-tyrosine-phosphatases of human placenta.
    J Biol Chem. 1988 May 15;263(14):6722-30 PMID: 2834386
  3. Transcription factor p91 interacts with the epidermal growth factor receptor and mediates activation of the c-fos gene promoter.
    Cell. 1993 Sep 24;74(6):1135-45 PMID: 8402883
  4. A missense single-nucleotide polymorphism in a gene encoding a protein tyrosine phosphatase (PTPN22) is associated with rheumatoid arthritis.
    Am J Hum Genet. 2004 Aug;75(2):330-7 PMID: 15208781
  5. Conditional deletion of Shp2 tyrosine phosphatase in thymocytes suppresses both pre-TCR and TCR signals.
    J Immunol. 2006 Nov 1;177(9):5990-6 PMID: 17056523
  6. Loss of SHP-2 activity in CD4+ T cells promotes melanoma progression and metastasis.
    Sci Rep. 2013 Oct 03;3:2845 PMID: 24088816
  7. Dominant role of antigen dose in CD4+Foxp3+ regulatory T cell induction and expansion.
    J Immunol. 2009 Oct 15;183(8):4895-903 PMID: 19801514
  8. Maintenance infliximab for Crohn's disease: the ACCENT I randomised trial.
    Lancet. 2002 May 4;359(9317):1541-9 PMID: 12047962
  9. Adhesion to target cells is disrupted by the killer cell inhibitory receptor.
    Curr Biol. 2000 Jun 29;10(13):777-80 PMID: 10898979
  10. Isolation of a src homology 2-containing tyrosine phosphatase.
    Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):1123-7 PMID: 1736296
  11. Comprehensive intestinal T helper cell profiling reveals specific accumulation of IFN-γ+IL-17+coproducing CD4+ T cells in active inflammatory bowel disease.
    Inflamm Bowel Dis. 2014 Dec;20(12):2321-9 PMID: 25248005
  12. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid.
    J Exp Med. 2007 Aug 6;204(8):1775-85 PMID: 17620362
  13. Structure, inhibitor, and regulatory mechanism of Lyp, a lymphoid-specific tyrosine phosphatase implicated in autoimmune diseases.
    Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):19767-72 PMID: 18056643
  14. Linkage proof for PTPN22, a rheumatoid arthritis susceptibility gene and a human autoimmunity gene.
    Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1649-54 PMID: 17237219
  15. DUSP6 (MKP3) null mice show enhanced ERK1/2 phosphorylation at baseline and increased myocyte proliferation in the heart affecting disease susceptibility.
    J Biol Chem. 2008 Nov 7;283(45):31246-55 PMID: 18753132
  16. Following the fate of one insulin-reactive CD4 T cell: conversion into Teffs and Tregs in the periphery controls diabetes in NOD mice.
    Diabetes. 2012 May;61(5):1169-79 PMID: 22403296
  17. Competitive protein tyrosine phosphatase 1B (PTP1B) inhibitors, prenylated caged xanthones from Garcinia hanburyi and their inhibitory mechanism.
    Bioorg Med Chem. 2017 Apr 15;25(8):2498-2506 PMID: 28318895
  18. TCR ligand density and affinity determine peripheral induction of Foxp3 in vivo.
    J Exp Med. 2010 Aug 2;207(8):1701-11 PMID: 20660617
  19. World Gastroenterology Organization Practice Guidelines for the diagnosis and management of IBD in 2010.
    Inflamm Bowel Dis. 2010 Jan;16(1):112-24 PMID: 19653289
  20. Inflammatory bowel disease: clinical aspects and established and evolving therapies.
    Lancet. 2007 May 12;369(9573):1641-57 PMID: 17499606
  21. A single phosphotyrosine residue of Stat91 required for gene activation by interferon-gamma.
    Science. 1993 Sep 24;261(5129):1744-6 PMID: 7690989
  22. Dual-specificity phosphatase 6 regulates CD4+ T-cell functions and restrains spontaneous colitis in IL-10-deficient mice.
    Mucosal Immunol. 2015 May;8(3):505-15 PMID: 25227984
  23. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene.
    Science. 2006 Dec 1;314(5804):1461-3 PMID: 17068223
  24. Autoimmune-associated PTPN22 R620W variation reduces phosphorylation of lymphoid phosphatase on an inhibitory tyrosine residue.
    J Biol Chem. 2010 Aug 20;285(34):26506-18 PMID: 20538612
  25. TLR4 signaling in effector CD4+ T cells regulates TCR activation and experimental colitis in mice.
    J Clin Invest. 2010 Feb;120(2):570-81 PMID: 20051628
  26. Protein tyrosine phosphatases and the immune response.
    Nat Rev Immunol. 2005 Jan;5(1):43-57 PMID: 15630428
  27. Mechanism of activation of protein kinase JAK2 by the growth hormone receptor.
    Science. 2014 May 16;344(6185):1249783 PMID: 24833397
  28. Lack of SHPTP1 results in src-family kinase hyperactivation and thymocyte hyperresponsiveness.
    Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9624-9 PMID: 8790380
  29. Involvement of the SHP-1 tyrosine phosphatase in regulation of T cell selection.
    J Immunol. 1999 Sep 15;163(6):3012-21 PMID: 10477564
  30. Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria.
    Nat Immunol. 2000 Aug;1(2):113-8 PMID: 11248802
  31. Purified protein derivative of Mycobacterium tuberculosis and excretory-secretory antigen(s) of Toxocara canis expand in vitro human T cells with stable and opposite (type 1 T helper or type 2 T helper) profile of cytokine production.
    J Clin Invest. 1991 Jul;88(1):346-50 PMID: 1829097
  32. Long-term HIV infection with Crohn's disease.
    Am J Gastroenterol. 1995 Jan;90(1):167-8 PMID: 7801934
  33. Mouse Ly-49A interrupts early signaling events in natural killer cell cytotoxicity and functionally associates with the SHP-1 tyrosine phosphatase.
    J Exp Med. 1997 Feb 17;185(4):673-84 PMID: 9034146
  34. JAK inhibition in inflammatory bowel disease.
    Expert Rev Clin Immunol. 2017 Jul;13(7):693-703 PMID: 28164724
  35. Characterization of TCR-induced receptor-proximal signaling events negatively regulated by the protein tyrosine phosphatase PEP.
    Eur J Immunol. 1999 Dec;29(12):3845-54 PMID: 10601992
  36. The autoimmunity-associated gene PTPN22 potentiates toll-like receptor-driven, type 1 interferon-dependent immunity.
    Immunity. 2013 Jul 25;39(1):111-22 PMID: 23871208
  37. Association of ZAP70 and PTPN6, but Not BANK1 or CLEC2D, with inflammatory bowel disease in the Tunisian population.
    Genet Test Mol Biomarkers. 2013 Apr;17(4):321-6 PMID: 23406209
  38. Junctional complexes in various epithelia.
    J Cell Biol. 1963 May;17:375-412 PMID: 13944428
  39. Subcutaneous golimumab induces clinical response and remission in patients with moderate-to-severe ulcerative colitis.
    Gastroenterology. 2014 Jan;146(1):85-95; quiz e14-5 PMID: 23735746
  40. Abnormal mesoderm patterning in mouse embryos mutant for the SH2 tyrosine phosphatase Shp-2.
    EMBO J. 1997 May 1;16(9):2352-64 PMID: 9171349
  41. Adalimumab for maintenance of clinical response and remission in patients with Crohn's disease: the CHARM trial.
    Gastroenterology. 2007 Jan;132(1):52-65 PMID: 17241859
  42. T-cell-receptor-dependent signal intensity dominantly controls CD4(+) T cell polarization In Vivo.
    Immunity. 2014 Jul 17;41(1):63-74 PMID: 24981853
  43. Increased prevalence of circulating novel IL-17 secreting Foxp3 expressing CD4+ T cells and defective suppressive function of circulating Foxp3+ regulatory cells support plasticity between Th17 and regulatory T cells in inflammatory bowel disease patients.
    Inflamm Bowel Dis. 2013 Nov;19(12):2522-34 PMID: 24097227
  44. STAT3 locus in inflammatory bowel disease and multiple sclerosis susceptibility.
    Genes Immun. 2010 Apr;11(3):264-8 PMID: 20200543
  45. T follicular helper cell differentiation, function, and roles in disease.
    Immunity. 2014 Oct 16;41(4):529-42 PMID: 25367570
  46. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria.
    Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15064-9 PMID: 18806221
  47. The protein tyrosine phosphatase SHP-1 regulates integrin-mediated adhesion of macrophages.
    Curr Biol. 1998 Sep 10;8(18):1035-8 PMID: 9740804
  48. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease.
    Nature. 2012 Nov 1;491(7422):119-24 PMID: 23128233
  49. The extended human PTPome: a growing tyrosine phosphatase family.
    FEBS J. 2016 Jun;283(11):2197-201 PMID: 27263510
  50. Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations.
    Nat Genet. 2015 Sep;47(9):979-986 PMID: 26192919
  51. Decline in miR-181a expression with age impairs T cell receptor sensitivity by increasing DUSP6 activity.
    Nat Med. 2012 Oct;18(10):1518-24 PMID: 23023500
  52. The tyrosine phosphatase SHP-1 influences thymocyte selection by setting TCR signaling thresholds.
    Int Immunol. 1999 Dec;11(12):1999-2014 PMID: 10590266
  53. Genetic association of the R620W polymorphism of protein tyrosine phosphatase PTPN22 with human SLE.
    Am J Hum Genet. 2004 Sep;75(3):504-7 PMID: 15273934
  54. The JAK2 variant rs10758669 in Crohn's disease: altering the intestinal barrier as one mechanism of action.
    Int J Colorectal Dis. 2012 May;27(5):565-73 PMID: 22065112
  55. Abnormal tyrosine phosphorylation on T-cell receptor in lymphoproliferative disorders.
    Nature. 1986 Dec 18-31;324(6098):674-6 PMID: 2432431
  56. Cooperative DNA binding and sequence-selective recognition conferred by the STAT amino-terminal domain.
    Science. 1996 Aug 9;273(5276):794-7 PMID: 8670419
  57. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases.
    Science. 1994 Feb 25;263(5150):1136-9 PMID: 7509083
  58. Autoimmune-associated lymphoid tyrosine phosphatase is a gain-of-function variant.
    Nat Genet. 2005 Dec;37(12):1317-9 PMID: 16273109
  59. Polar opposites: Erk direction of CD4 T cell subsets.
    J Immunol. 2012 Jul 15;189(2):721-31 PMID: 22675204
  60. Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor.
    Cell. 1992 Aug 21;70(4):585-93 PMID: 1505025
  61. Protein tyrosine phosphatase containing SH2 domains: characterization, preferential expression in hematopoietic cells, and localization to human chromosome 12p12-p13.
    Mol Cell Biol. 1992 Feb;12(2):836-46 PMID: 1732748
  62. Replication of signals from recent studies of Crohn's disease identifies previously unknown disease loci for ulcerative colitis.
    Nat Genet. 2008 Jun;40(6):713-5 PMID: 18438405
  63. A novel, specific interaction involving the Csk SH3 domain and its natural ligand.
    Nat Struct Biol. 2001 Nov;8(11):998-1004 PMID: 11685249
  64. Receptor-stimulated oxidation of SHP-2 promotes T-cell adhesion through SLP-76-ADAP.
    EMBO J. 2005 Jul 6;24(13):2331-41 PMID: 15933714
  65. SLP-76 is recruited to CD22 and dephosphorylated by SHP-1, thereby regulating B cell receptor-induced c-Jun N-terminal kinase activation.
    Eur J Immunol. 2005 Feb;35(2):644-54 PMID: 15668918
  66. Proteinaceous Regulators and Inhibitors of Protein Tyrosine Phosphatases.
    Molecules. 2018 Feb 12;23(2):null PMID: 29439552
  67. Selective sequestration of STAT1 in the cytoplasm via phosphorylated SHP-2 ameliorates murine experimental colitis.
    J Immunol. 2012 Oct 1;189(7):3497-507 PMID: 22942432
  68. Small molecule targeting of PTPs in cancer.
    Int J Biochem Cell Biol. 2018 Mar;96:171-181 PMID: 28943273
  69. A protein-tyrosine phosphatase with sequence similarity to the SH2 domain of the protein-tyrosine kinases.
    Nature. 1991 Aug 22;352(6337):736-9 PMID: 1652101
  70. Targeting Tyrosine Phosphatases: Time to End the Stigma.
    Trends Pharmacol Sci. 2017 Jun;38(6):524-540 PMID: 28412041
  71. Novel Therapies and Treatment Strategies for Patients with Inflammatory Bowel Disease.
    Curr Treat Options Gastroenterol. 2018 Mar;16(1):129-146 PMID: 29411220
  72. Targeted loss of SHP1 in murine thymocytes dampens TCR signaling late in selection.
    Eur J Immunol. 2016 Sep;46(9):2103-10 PMID: 27354309
  73. Pharmacologic inhibition of MEK-ERK signaling enhances Th17 differentiation.
    J Immunol. 2010 Feb 15;184(4):1849-57 PMID: 20061405
  74. Immunoreceptor tyrosine-based inhibitory motif of the IL-4 receptor associates with SH2-containing phosphatases and regulates IL-4-induced proliferation.
    J Immunol. 2001 Dec 1;167(11):6382-7 PMID: 11714803
  75. Abnormal chemokine-induced responses of immature and mature hematopoietic cells from motheaten mice implicate the protein tyrosine phosphatase SHP-1 in chemokine responses.
    J Exp Med. 1999 Sep 6;190(5):681-90 PMID: 10477552
  76. Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos.
    J Immunol. 2003 Nov 15;171(10):4984-9 PMID: 14607893
  77. Downregulation of PTP1B and TC-PTP phosphatases potentiate dendritic cell-based immunotherapy through IL-12/IFNγ signaling.
    Oncoimmunology. 2017 Apr 28;6(6):e1321185 PMID: 28680757
  78. Tumor suppression by phospholipase C-beta3 via SHP-1-mediated dephosphorylation of Stat5.
    Cancer Cell. 2009 Aug 4;16(2):161-71 PMID: 19647226
  79. Epithelial tyrosine phosphatase SHP-2 protects against intestinal inflammation in mice.
    Mol Cell Biol. 2013 Jun;33(11):2275-84 PMID: 23530062
  80. Commensal host-bacterial relationships in the gut.
    Science. 2001 May 11;292(5519):1115-8 PMID: 11352068
  81. Identification of a human src homology 2-containing protein-tyrosine-phosphatase: a putative homolog of Drosophila corkscrew.
    Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11239-43 PMID: 1280823
  82. In vivo CRISPR screening identifies Ptpn2 as a cancer immunotherapy target.
    Nature. 2017 Jul 27;547(7664):413-418 PMID: 28723893
  83. Multiple treg suppressive modules and their adaptability.
    Front Immunol. 2012 Jun 29;3:178 PMID: 22754556
  84. Allosteric noncompetitive small molecule selective inhibitors of CD45 tyrosine phosphatase suppress T-cell receptor signals and inflammation in vivo.
    Mol Pharmacol. 2014 Apr;85(4):553-63 PMID: 24473749
  85. T cell protein tyrosine phosphatase attenuates T cell signaling to maintain tolerance in mice.
    J Clin Invest. 2011 Dec;121(12):4758-74 PMID: 22080863
  86. A novel SHP-1/Grb2-dependent mechanism of negative regulation of cytokine-receptor signaling: contribution of SHP-1 C-terminal tyrosines in cytokine signaling.
    Blood. 2004 Feb 15;103(4):1398-407 PMID: 14551136
  87. Characterization of interleukin-17-producing regulatory T cells in inflamed intestinal mucosa from patients with inflammatory bowel diseases.
    Gastroenterology. 2011 Mar;140(3):957-65 PMID: 21147109
  88. Strong evidence of a combination polymorphism of the tyrosine kinase 2 gene and the signal transducer and activator of transcription 3 gene as a DNA-based biomarker for susceptibility to Crohn's disease in the Japanese population.
    J Clin Immunol. 2009 Nov;29(6):815-25 PMID: 19653082
  89. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria.
    Science. 2004 Mar 12;303(5664):1662-5 PMID: 15016999
  90. PTPN22 deficiency cooperates with the CD45 E613R allele to break tolerance on a non-autoimmune background.
    J Immunol. 2009 Apr 1;182(7):4093-106 PMID: 19299707
  91. Direct association with and dephosphorylation of Jak2 kinase by the SH2-domain-containing protein tyrosine phosphatase SHP-1.
    Mol Cell Biol. 1996 Dec;16(12):6985-92 PMID: 8943354
  92. Recent advances in understanding the role of protein-tyrosine phosphatases in development and disease.
    Dev Biol. 2017 Aug 15;428(2):283-292 PMID: 28728679
  93. Requirement for CD28 co-stimulation is lower in SHP-1-deficient T cells.
    Eur J Immunol. 2001 Dec;31(12):3649-58 PMID: 11745385
  94. Role of protein tyrosine phosphatases in regulating the immune system: implications for chronic intestinal inflammation.
    Inflamm Bowel Dis. 2015 Mar;21(3):645-55 PMID: 25581833
  95. Genetic Variations of PTPN2 and PTPN22: Role in the Pathogenesis of Type 1 Diabetes and Crohn's Disease.
    Front Cell Infect Microbiol. 2015 Dec 24;5:95 PMID: 26734582
  96. CD25- T cells generate CD25+Foxp3+ regulatory T cells by peripheral expansion.
    J Immunol. 2004 Dec 15;173(12):7259-68 PMID: 15585848
  97. T-cell protein tyrosine phosphatase deletion results in progressive systemic inflammatory disease.
    Blood. 2004 May 1;103(9):3457-64 PMID: 14726372
  98. T lymphocyte SHP2-deficiency triggers anti-tumor immunity to inhibit colitis-associated cancer in mice.
    Oncotarget. 2017 Jan 31;8(5):7586-7597 PMID: 27935860
  99. Ustekinumab as Induction and Maintenance Therapy for Crohn's Disease.
    N Engl J Med. 2016 Nov 17;375(20):1946-1960 PMID: 27959607
  100. PTPN2 controls differentiation of CD4⁺ T cells and limits intestinal inflammation and intestinal dysbiosis.
    Mucosal Immunol. 2015 Jul;8(4):918-29 PMID: 25492475
  101. Evidence from cDNA clones that the rat leukocyte-common antigen (T200) spans the lipid bilayer and contains a cytoplasmic domain of 80,000 Mr.
    Cell. 1985 May;41(1):83-93 PMID: 3158393
  102. PEST domain-enriched tyrosine phosphatase (PEP) regulation of effector/memory T cells.
    Science. 2004 Jan 30;303(5658):685-9 PMID: 14752163
  103. Treatment of inflammatory bowel disease with anti-CD4 monoclonal antibody.
    Lancet. 1991 Aug 31;338(8766):570-1 PMID: 1678821
  104. TCR ligand discrimination is enforced by competing ERK positive and SHP-1 negative feedback pathways.
    Nat Immunol. 2003 Mar;4(3):248-54 PMID: 12577055
  105. Carcinoembryonic antigen-related cell adhesion molecule 1 inhibits proximal TCR signaling by targeting ZAP-70.
    J Immunol. 2008 May 1;180(9):6085-93 PMID: 18424730
  106. Targeting Src homology 2 domain-containing tyrosine phosphatase (SHP-1) into lipid rafts inhibits CD3-induced T cell activation.
    J Immunol. 2001 Mar 15;166(6):3975-82 PMID: 11238643
  107. Cutting edge: TGF-beta-induced expression of Foxp3 in T cells is mediated through inactivation of ERK.
    J Immunol. 2008 Mar 1;180(5):2757-61 PMID: 18292494
  108. CD4 antibody treatment in patients with active Crohn's disease: a phase 1 dose finding study.
    Gut. 1997 Mar;40(3):320-7 PMID: 9135519
  109. Association of inhibitory tyrosine protein kinase p50csk with protein tyrosine phosphatase PEP in T cells and other hemopoietic cells.
    EMBO J. 1996 Sep 16;15(18):4909-18 PMID: 8890164
  110. A Toll-like receptor 2 ligand stimulates Th2 responses in vivo, via induction of extracellular signal-regulated kinase mitogen-activated protein kinase and c-Fos in dendritic cells.
    J Immunol. 2004 Apr 15;172(8):4733-43 PMID: 15067049
  111. An RNA aptamer that selectively inhibits the enzymatic activity of protein tyrosine phosphatase 1B in vitro.
    Chembiochem. 2010 Jul 26;11(11):1583-93 PMID: 20572251
  112. Mechanisms and consequences of Jak-STAT signaling in the immune system.
    Nat Immunol. 2017 Mar 22;18(4):374-384 PMID: 28323260
  113. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine.
    Science. 2011 Oct 14;334(6053):255-8 PMID: 21998396
  114. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease.
    Nat Genet. 2008 Aug;40(8):955-62 PMID: 18587394
  115. Pouring fuel on the fire: Th17 cells, the environment, and autoimmunity.
    J Clin Invest. 2015 Jun;125(6):2211-9 PMID: 25961452
  116. Mutations at the murine motheaten locus are within the hematopoietic cell protein-tyrosine phosphatase (Hcph) gene.
    Cell. 1993 Jul 2;73(7):1445-54 PMID: 8324828
  117. Complementation of a mutant cell line: central role of the 91 kDa polypeptide of ISGF3 in the interferon-alpha and -gamma signal transduction pathways.
    EMBO J. 1993 Nov;12(11):4221-8 PMID: 7693454
  118. PTPN22 modulates macrophage polarization and susceptibility to dextran sulfate sodium-induced colitis.
    J Immunol. 2013 Sep 1;191(5):2134-43 PMID: 23913970
  119. Polymorphisms of PTPN11 coding SHP-2 as biomarkers for ulcerative colitis susceptibility in the Japanese population.
    J Clin Immunol. 2009 May;29(3):303-10 PMID: 19160029
  120. Specific recruitment of SH-PTP1 to the erythropoietin receptor causes inactivation of JAK2 and termination of proliferative signals.
    Cell. 1995 Mar 10;80(5):729-38 PMID: 7889566
  121. Lck regulates the tyrosine phosphorylation of the T cell receptor subunits and ZAP-70 in murine thymocytes.
    J Exp Med. 1996 Mar 1;183(3):1053-62 PMID: 8642247
  122. Maintenance therapy with certolizumab pegol for Crohn's disease.
    N Engl J Med. 2007 Jul 19;357(3):239-50 PMID: 17634459
  123. Investigation of JAK2, STAT3 and CCR6 polymorphisms and their gene-gene interactions in inflammatory bowel disease.
    Int J Immunogenet. 2012 Jun;39(3):247-52 PMID: 22269120
  124. Direct regulation of ZAP-70 by SHP-1 in T cell antigen receptor signaling.
    Science. 1996 May 24;272(5265):1173-6 PMID: 8638162
  125. SH2-containing phosphotyrosine phosphatase as a target of protein-tyrosine kinases.
    Science. 1993 Mar 12;259(5101):1607-11 PMID: 8096088
  126. Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis.
    PLoS Med. 2008 Mar 4;5(3):e54 PMID: 18318598
  127. Recruitment of tyrosine phosphatase HCP by the killer cell inhibitor receptor.
    Immunity. 1996 Jan;4(1):77-85 PMID: 8574854
  128. Crystal structure of the MAPK phosphatase Pyst1 catalytic domain and implications for regulated activation.
    Nat Struct Biol. 1999 Feb;6(2):174-81 PMID: 10048930
  129. ZAP-70: a 70 kd protein-tyrosine kinase that associates with the TCR zeta chain.
    Cell. 1992 Nov 13;71(4):649-62 PMID: 1423621
  130. Impaired bone marrow microenvironment and immune function in T cell protein tyrosine phosphatase-deficient mice.
    J Exp Med. 1997 Aug 29;186(5):683-93 PMID: 9271584
  131. Allosteric inhibition of SHP2 phosphatase inhibits cancers driven by receptor tyrosine kinases.
    Nature. 2016 Jul 7;535(7610):148-52 PMID: 27362227
  132. Targeting the disordered C terminus of PTP1B with an allosteric inhibitor.
    Nat Chem Biol. 2014 Jul;10(7):558-66 PMID: 24845231
  133. Role of the protein tyrosine phosphatase Shp2 in homeostasis of the intestinal epithelium.
    PLoS One. 2014 Mar 27;9(3):e92904 PMID: 24675817
  134. Identification of the tyrosine phosphatase PTP1C as a B cell antigen receptor-associated protein involved in the regulation of B cell signaling.
    J Exp Med. 1995 Jun 1;181(6):2077-84 PMID: 7539038
  135. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene.
    Science. 1999 Mar 5;283(5407):1544-8 PMID: 10066179
  136. T Cells Deficient in the Tyrosine Phosphatase SHP-1 Resist Suppression by Regulatory T Cells.
    J Immunol. 2017 Jul 1;199(1):129-137 PMID: 28550200
  137. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins.
    J Immunol. 1986 Apr 1;136(7):2348-57 PMID: 2419430
  138. Conformation-sensing antibodies stabilize the oxidized form of PTP1B and inhibit its phosphatase activity.
    Cell. 2011 Sep 30;147(1):185-98 PMID: 21962515
  139. Characterization of candidate genes in inflammatory bowel disease-associated risk loci.
    JCI Insight. 2016 Aug 18;1(13):e87899 PMID: 27668286
  140. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism.
    Science. 2009 Jul 31;325(5940):617-20 PMID: 19644121
  141. Lack of the phosphatase PTPN22 increases adhesion of murine regulatory T cells to improve their immunosuppressive function.
    Sci Signal. 2012 Nov 27;5(252):ra87 PMID: 23193160
  142. Identification of substrates of human protein-tyrosine phosphatase PTPN22.
    J Biol Chem. 2006 Apr 21;281(16):11002-10 PMID: 16461343
  143. The autoimmune disease-associated PTPN22 variant promotes calpain-mediated Lyp/Pep degradation associated with lymphocyte and dendritic cell hyperresponsiveness.
    Nat Genet. 2011 Aug 14;43(9):902-7 PMID: 21841778
  144. Characterization of the major protein-tyrosine-phosphatases of human placenta.
    J Biol Chem. 1988 May 15;263(14):6731-7 PMID: 2834387
  145. Harnessing the plasticity of CD4(+) T cells to treat immune-mediated disease.
    Nat Rev Immunol. 2016 Mar;16(3):149-63 PMID: 26875830
  146. Functions of Shp2 in cancer.
    J Cell Mol Med. 2015 Sep;19(9):2075-83 PMID: 26088100
  147. Modeling T cell antigen discrimination based on feedback control of digital ERK responses.
    PLoS Biol. 2005 Nov;3(11):e356 PMID: 16231973
  148. Comprehensive expression profiles of genes for protein tyrosine phosphatases in immune cells.
    Sci Signal. 2010 Aug 31;3(137):rs1 PMID: 20807954
  149. In vivo instruction of suppressor commitment in naive T cells.
    J Exp Med. 2004 May 17;199(10):1401-8 PMID: 15148338
  150. Characterization of hematopoietic intracellular protein tyrosine phosphatases: description of a phosphatase containing an SH2 domain and another enriched in proline-, glutamic acid-, serine-, and threonine-rich sequences.
    Mol Cell Biol. 1992 May;12(5):2396-405 PMID: 1373816
  151. The phosphatase DUSP2 controls the activity of the transcription activator STAT3 and regulates TH17 differentiation.
    Nat Immunol. 2015 Dec;16(12):1263-73 PMID: 26479789
  152. CD4 count remission hypothesis in patients with inflammatory bowel disease and human immunodeficiency virus infection: a systematic review of the literature.
    Ann Gastroenterol. 2015 Jul-Sep;28(3):337-346 PMID: 26126511
  153. Tofacitinib as Induction and Maintenance Therapy for Ulcerative Colitis.
    N Engl J Med. 2017 Aug 3;377(5):496-7 PMID: 28767341
  154. The src homology 2 domain-containing tyrosine phosphatase 2 regulates primary T-dependent immune responses and Th cell differentiation.
    J Immunol. 2005 Nov 15;175(10):6498-508 PMID: 16272304
  155. Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis.
    Immunity. 2010 May 28;32(5):605-15 PMID: 20493732
  156. The dual specificity phosphatases M3/6 and MKP-3 are highly selective for inactivation of distinct mitogen-activated protein kinases.
    J Biol Chem. 1996 Nov 1;271(44):27205-8 PMID: 8910287
  157. Differential association of two PTPN22 coding variants with Crohn's disease and ulcerative colitis.
    Inflamm Bowel Dis. 2011 Nov;17(11):2287-94 PMID: 21287672
  158. Interferon activation of the transcription factor Stat91 involves dimerization through SH2-phosphotyrosyl peptide interactions.
    Cell. 1994 Mar 11;76(5):821-8 PMID: 7510216
  159. Evaluation of 22 genetic variants with Crohn's disease risk in the Ashkenazi Jewish population: a case-control study.
    BMC Med Genet. 2011 May 06;12:63 PMID: 21548950
  160. Immune markers and differential signaling networks in ulcerative colitis and Crohn's disease.
    Inflamm Bowel Dis. 2012 Dec;18(12):2342-56 PMID: 22467146
  161. A functional variant of lymphoid tyrosine phosphatase is associated with type I diabetes.
    Nat Genet. 2004 Apr;36(4):337-8 PMID: 15004560
  162. Protein tyrosine phosphatases as potential therapeutic targets.
    Acta Pharmacol Sin. 2014 Oct;35(10):1227-46 PMID: 25220640
  163. Increased energy expenditure, decreased adiposity, and tissue-specific insulin sensitivity in protein-tyrosine phosphatase 1B-deficient mice.
    Mol Cell Biol. 2000 Aug;20(15):5479-89 PMID: 10891488
  164. Th9 cells, new players in adaptive immunity.
    Trends Immunol. 2014 Feb;35(2):61-8 PMID: 24215739
  165. Motheaten and viable motheaten mice have mutations in the haematopoietic cell phosphatase gene.
    Nat Genet. 1993 Jun;4(2):124-9 PMID: 8348149
  166. ERK differentially regulates Th17- and Treg-cell development and contributes to the pathogenesis of colitis.
    Eur J Immunol. 2013 Jul;43(7):1716-26 PMID: 23620016
  167. A STAT protein domain that determines DNA sequence recognition suggests a novel DNA-binding domain.
    Genes Dev. 1995 Apr 15;9(8):984-94 PMID: 7774815
  168. Identification of function-regulating antibodies targeting the receptor protein tyrosine phosphatase sigma ectodomain.
    PLoS One. 2017 May 30;12(5):e0178489 PMID: 28558026
  169. Shp1 regulates T cell homeostasis by limiting IL-4 signals.
    J Exp Med. 2013 Jul 1;210(7):1419-31 PMID: 23797092
  170. The lymphoid protein tyrosine phosphatase Lyp interacts with the adaptor molecule Grb2 and functions as a negative regulator of T-cell activation.
    Exp Hematol. 2002 Mar;30(3):237-44 PMID: 11882361
  171. Ptpn11 Deletion in CD4+ Cells Does Not Affect T Cell Development and Functions but Causes Cartilage Tumors in a T Cell-Independent Manner.
    Front Immunol. 2017 Oct 16;8:1326 PMID: 29085371
  172. Inflammatory bowel disease.
    N Engl J Med. 2009 Nov 19;361(21):2066-78 PMID: 19923578
  173. T cell activation is reduced by the catalytically inactive form of protein tyrosine phosphatase SHP-2.
    Int J Clin Exp Med. 2015 Apr 15;8(4):6568-77 PMID: 26131287
  174. Identification and Characterization of Von Hippel-Lindau-Recruiting Proteolysis Targeting Chimeras (PROTACs) of TANK-Binding Kinase 1.
    J Med Chem. 2018 Jan 25;61(2):583-598 PMID: 28692295
  175. Protein tyrosine phosphatase non-receptor type 2 and inflammatory bowel disease.
    World J Gastroenterol. 2016 Jan 21;22(3):1034-44 PMID: 26811645
Article Info
Journal
Frontiers in immunology
Abbr.
Front Immunol
ISSN
1664-3224
Published
2018-00-00
Epub
2018-00-31
Pages
2504
Language
English
Region
Switzerland
NLM ID
101560960
PMCID
PMC6220082
Subset
IM
Grants
CIHR · MOP 142497 · Canada
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