Phosphatase regulation of macrophage activation

Seminars in Immunology

Volumn 27, Issue 4, 2015, Pages 276-285

  Kozicky, Lisa K ^a   Sly, Laura M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Lipid phosphatase; Macrophage activation; MKP 1; Protein phosphatase; Protein tyrosine phosphatase; PTEN; PTP1B; PTPN22; SHIP; SHP 1; Shp2

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 22; PHOSPHATASE; PHOSPHATIDATE PHOSPHATASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN SH2; PROTEIN TYROSINE PHOSPHATASE 1B; PROTEIN TYROSINE PHOSPHATASE SHP 1; PROTEIN TYROSINE PHOSPHATASE;

CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME REGULATION; MACROPHAGE ACTIVATION; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CYTOLOGY; ENZYMOLOGY; HUMAN; IMMUNOLOGY; MACROPHAGE; METABOLISM;

ANIMALS; HUMANS; MACROPHAGE ACTIVATION; MACROPHAGES; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN TYROSINE PHOSPHATASES;

EID: 84951907181     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2015.07.001     Document Type: Review

References (111)

1. Wynn T.A., Chawla A., Pollard J.W. Macrophage biology in development, homeostasis and disease. Nature 2013, 496:445-455.
2. Jenkins S.J., Ruckerl D., Cook P.C., Jones L.H., Finkelman F.D., van Rooijen N., et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 2011, 332:1284-1288.
3. Martinez F.O., Sica A., Mantovani A., Locati M. Macrophage activation and polarization. Front. Biosci. 2008, 13:453-461.
4. Murray P.J., Wynn T.A. Protective and pathogenic functions of macrophage subsets. Nat. Rev Immunol. 2011, 11:723-737.
5. Martinez F.O., Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000prime Rep. 2014, 6:13.
6. Murray P.J., Allen J.E., Biswas S.K., Fisher E.A., Gilroy D.W., Goerdt S., et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 2014, 41:14-20.
7. Martinez F.O., Helming L., Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Ann. Rev. Immunol. 2009, 27:451-483.
8. Weisser S.B., McLarren K.W., Voglmaier N., van Netten-Thomas C.J., Antov A., Flavell R.A., et al. Alternative activation of macrophages by IL-4 requires SHIP degradation. Eur. J. Immunol. 2011, 41:1742-1753.
9. Bastos K.R., Alvarez J.M., Marinho C.R., Rizzo L.V., Lima M.R. Macrophages from IL-12p40-deficient mice have a bias toward the M2 activation profile. J. Leukoc. Biol. 2002, 71:271-278.
10. Lawrence T., Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat. Rev. Immunol. 2011, 11:750-761.
11. Ramana C.V., Gil M.P., Schreiber R.D., Stark G.R. Stat1-dependent and -independent pathways in IFN-gamma-dependent signaling. Trends Immunol. 2002, 23:96-101.
12. Bhattacharjee A., Shukla M., Yakubenko V.P., Mulya A., Kundu S., Cathcart M.K. IL-4 and IL-13 employ discrete signaling pathways for target gene expression in alternatively activated monocytes/macrophages. Free Radic. Biol. Med. 2013, 54:1-16.
13. Kawasaki T., Kawai T. Toll-like receptor signaling pathways. Front. Immunol. 2014, 5:461.
14. Cantley L.C. The phosphoinositide 3-kinase pathway. Science 2002, 296:1655-1657.
15. Okkenhaug K. Signaling by the phosphoinositide 3-kinase family in immune cells. Annu. Rev. Immunol. 2013, 31:675-704.
16. Whitman M., Downes C.P., Keeler M., Keller T., Cantley L. Type I phosphatidylinositol kinase makes a novel inositol phospholipid, phosphatidylinositol-3-phosphate. Nature 1988, 332:644-646.
17. Wymann M.P., Pirola L. Structure and function of phosphoinositide 3-kinases. Biochim. Biophys. Acta 1998, 1436:127-150.
18. Krystal G. Lipid phosphatases in the immune system. Semin. Immunol. 2000, 12:397-403.
19. Heller N.M., Qi X., Junttila I.S., Shirey K.A., Vogel S.N., Paul W.E., et al. Type I IL-4Rs selectively activate IRS-2 to induce target gene expression in macrophages. Sci. Signal. 2008, 1:ra17.
20. Arranz A., Doxaki C., Vergadi E., Martinez de la Torre Y., Vaporidi K., Lagoudaki E.D., et al. Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization. Proc. Natl. Acad. Sci. USA 2012, 109:9517-9522.
21. Damen J.E., Liu L., Rosten P., Humphries R.K., Jefferson A.B., Majerus P.W., et al. The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-triphosphate 5-phosphatase. Proc. Natl. Acad. Sci. USA 1996, 93:1689-1693.
22. Lioubin M.N., Algate P.A., Tsai S., Carlberg K., Aebersold A., Rohrschneider L.R. p150Ship, a signal transduction molecule with inositol polyphosphate-5-phosphatase activity. Genes Dev. 1996, 10:1084-1095.
23. Kavanaugh W.M., Pot D.A., Chin S.M., Deuter-Reinhard M., Jefferson A.B., Norris F.A., et al. Multiple forms of an inositol polyphosphate 5-phosphatase form signaling complexes with Shc and Grb2. Curr. Biol. 1996, 6:438-445.
24. Sly L.M., Ho V., Antignano F., Ruschmann J., Hamilton M., Lam V., et al. The role of SHIP in macrophages. Front. Biosci. 2007, 12:2836-2848.
25. Rauh M.J., Ho V., Pereira C., Sham A., Sly L.M., Lam V., et al. SHIP represses the generation of alternatively activated macrophages. Immunity 2005, 23:361-374.
26. Kuroda E., Ho V., Ruschmann J., Antignano F., Hamilton M., Rauh M.J., et al. SHIP represses the generation of IL-3-induced M2 macrophages by inhibiting IL-4 production from basophils. J. Immunol. 2009, 183:3652-3660.
27. Heinsbroek S.E., Gordon S. The role of macrophages in inflammatory bowel diseases. Expert Rev. Mol. Med. 2009, 11:e14.
28. Weisser S.B., Kozicky L.K., Brugger H.K., Ngoh E.N., Cheung B., Jen R., et al. Arginase activity in alternatively activated macrophages protects PI3Kp110delta deficient mice from dextran sodium sulfate induced intestinal inflammation. Eur. J. Immunol. 2014.
29. Uno J.K., Rao K.N., Matsuoka K., Sheikh S.Z., Kobayashi T., Li F., et al. Altered macrophage function contributes to colitis in mice defective in the phosphoinositide-3 kinase subunit p110delta. Gastroenterology 2010, 139. 1642-1653, 1653 e1641-1646.
30. Helgason C.D., Damen J.E., Rosten P., Grewal R., Sorensen P., Chappel S.M., et al. Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev. 1998, 12:1610-1620.
31. Xiao W., Hong H., Kawakami Y., Lowell C.A., Kawakami T. Regulation of myeloproliferation and M2 macrophage programming in mice by Lyn/Hck, SHIP, and Stat5. J. Clin. Invest. 2008, 118:924-934.
32. McLarren K.W., Cole A.E., Weisser S.B., Voglmaier N.S., Conlin V.S., Jacobson K., et al. SHIP-deficient mice develop spontaneous intestinal inflammation and arginase-dependent fibrosis. Am. J. Pathol. 2011, 179:180-188.
33. Kerr W.G., Park M.Y., Maubert M., Engelman R.W. SHIP deficiency causes Crohn's disease-like ileitis. Gut 2011, 60:177-188.
34. Wynn T.A., Barron L. Macrophages: master regulators of inflammation and fibrosis. Semin. Liver Dis. 2010, 30:245-257.
35. Maxwell M.J., Duan M., Armes J.E., Anderson G.P., Tarlinton D.M., Hibbs M.L. Genetic segregation of inflammatory lung disease and autoimmune disease severity in SHIP-1-/- mice. J. Immunol. 2011, 186:7164-7175.
36. Bishop J.L., Sly L.M., Krystal G., Finlay B.B. The inositol phosphatase SHIP controls Salmonella enterica serovar Typhimurium infection in vivo. Infect. Immun. 2008, 76:2913-2922.
37. Hunter M.M., Wang A., Parhar K.S., Johnston M.J., Van Rooijen N., Beck P.L., et al. In vitro-derived alternatively activated macrophages reduce colonic inflammation in mice. Gastroenterology 2010, 138:1395-1405.
38. Weisser S.B., Brugger H.K., Voglmaier N.S., McLarren K.W., van Rooijen N., Sly L.M. SHIP-deficient, alternatively activated macrophages protect mice during DSS-induced colitis. J. Leukoc. Biol. 2011, 90:483-492.
39. Leung G., Wang A., Fernando M., Phan V.C., McKay D.M. Bone marrow-derived alternatively activated macrophages reduce colitis without promoting fibrosis: participation of IL-10. Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 304:G781-G792.
40. Li J., Yen C., Liaw D., Podsypanina K., Bose S., Wang S.I., et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 1997, 275:1943-1947.
41. Steck P.A., Pershouse M.A., Jasser S.A., Yung W.K., Lin H., Ligon A.H., et al. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat. Genet. 1997, 15:356-362.
42. Li D.M., Sun H. TEP1, encoded by a candidate tumor suppressor locus, is a novel protein tyrosine phosphatase regulated by transforming growth factor beta. Cancer Res. 1997, 57:2124-2129.
43. Maehama T., Dixon J.E. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 1998, 273:13375-13378.
44. Worby C.A., Dixon J.E. Pten. Ann. Rev. Biochem. 2014, 83:641-669.
45. Wu C., Xue Y., Wang P., Lin L., Liu Q., Li N., et al. IFN-gamma primes macrophage activation by increasing phosphatase and tensin homolog via downregulation of miR-3473b. J. Immunol. 2014, 193:3036-3044.
46. Sly L.M., Rauh M.J., Kalesnikoff J., Song C.H., Krystal G. LPS-induced upregulation of SHIP is essential for endotoxin tolerance. Immunity 2004, 21:227-239.
47. Di Cristofano A., Pesce B., Cordon-Cardo C., Pandolfi P.P. Pten is essential for embryonic development and tumour suppression. Nat. Genet. 1998, 19:348-355.
48. Suzuki A., Yamaguchi M.T., Ohteki T., Sasaki T., Kaisho T., Kimura Y., et al. T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity 2001, 14:523-534.
49. Clausen B.E., Burkhardt C., Reith W., Renkawitz R., Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999, 8:265-277.
50. Sahin E., Haubenwallner S., Kuttke M., Kollmann I., Halfmann A., Dohnal A.M., et al. Macrophage PTEN regulates expression and secretion of arginase I modulating innate and adaptive immune responses. J. Immunol. 2014, 193:1717-1727.
51. Schabbauer G., Matt U., Gunzl P., Warszawska J., Furtner T., Hainzl E., et al. Myeloid PTEN promotes inflammation but impairs bactericidal activities during murine pneumococcal pneumonia. J. Immunol. 2010, 185:468-476.
52. Yue S., Rao J., Zhu J., Busuttil R.W., Kupiec-Weglinski J.W., Lu L., et al. Myeloid PTEN deficiency protects livers from ischemia reperfusion injury by facilitating M2 macrophage differentiation. J. Immunol. 2014, 192:5343-5353.
53. Wang G., Shi Y., Jiang X., Leak R.K., Hu X., Wu Y., et al. HDAC inhibition prevents white matter injury by modulating microglia/macrophage polarization through the GSK3beta/PTEN/Akt axis. Proc. Natl. Acad. Sci. USA 2015, 112:2853-2858.
54. Hunter T. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 1995, 80:225-236.
55. Neel B.G., Tonks N.K. Protein tyrosine phosphatases in signal transduction. Curr. Opin. Cell Biol. 1997, 9:193-204.
56. Brognard J., Hunter T. Protein kinase signaling networks in cancer. Curr. Opin. Gen. Dev. 2011, 21:4-11.
57. Manning G., Whyte D.B., Martinez R., Hunter T., Sudarsanam S. The protein kinase complement of the human genome. Science 2002, 298:1912-1934.
58. Alonso A., Sasin J., Bottini N., Friedberg I., Friedberg I., Osterman A., et al. Protein tyrosine phosphatases in the human genome. Cell 2004, 117:699-711.
59. Mustelin T. A brief introduction to the protein phosphatase families. Methods Mol. Biol. 2007, 365:9-22.
60. Mustelin T. Are other protein tyrosine phosphatases than PTPN22 associated with autoimmunity?. Semin. Immunol. 2006, 18:254-260.
61. Pouyssegur J., Lenormand P. Fidelity and spatio-temporal control in MAP kinase (ERKs) signalling. Eur. J. Biochem. 2003, 270:3291-3299.
62. Mustelin T., Abraham R.T., Rudd C.E., Alonso A., Merlo J.J. Protein tyrosine phosphorylation in T cell signaling. Front. Biosci. 2002, 7:d918-d969.
63. Freeman R.M., Plutzky J., Neel B.G. Identification of a human src homology 2-containing protein-tyrosine-phosphatase: a putative homolog of Drosophila corkscrew. Proc. Natl. Acad. Sci. USA 1992, 89:11239-11243.
64. Feng G.S., Hui C.C., Pawson T. SH2-containing phosphotyrosine phosphatase as a target of protein-tyrosine kinases. Science 1993, 259:1607-1611.
65. Neel B.G., Gu H., Pao L. The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem. Sci. 2003, 28:284-293.
66. Grossmann K.S., Rosario M., Birchmeier C., Birchmeier W. The tyrosine phosphatase Shp2 in development and cancer. Adv. Cancer Res. 2010, 106:53-89.
67. Roberts A.E., Araki T., Swanson K.D., Montgomery K.T., Schiripo T.A., Joshi V.A., et al. Germline gain-of-function mutations in SOS1 cause Noonan syndrome. Nat. Genet. 2007, 39:70-74.
68. Kontaridis M.I., Swanson K.D., David F.S., Barford D., Neel B.G. PTPN11 (Shp2) mutations in LEOPARD syndrome have dominant negative, not activating, effects. J. Biol. Chem. 2006, 281:6785-6792.
69. Edouard T., Montagner A., Dance M., Conte F., Yart A., Parfait B., et al. How do Shp2 mutations that oppositely influence its biochemical activity result in syndromes with overlapping symptoms?. Cell. Mol. Life Sci. 2007, 64:1585-1590.
70. Li L., Modi H., McDonald T., Rossi J., Yee J.K., Bhatia R. A critical role for SHP2 in STAT5 activation and growth factor-mediated proliferation, survival, and differentiation of human CD34+ cells. Blood 2011, 118:1504-1515.
71. Lehmann U., Schmitz J., Weissenbach M., Sobota R.M., Hortner M., Friederichs K., et al. SHP2 and SOCS3 contribute to Tyr-759-dependent attenuation of interleukin-6 signaling through gp130. J. Biol. Chem. 2003, 278:661-671.
72. Baron M., Davignon J.L. Inhibition of IFN-gamma-induced STAT1 tyrosine phosphorylation by human CMV is mediated by SHP2. J. Immunol. 2008, 181:5530-5536.
73. Ke Y., Lesperance J., Zhang E.E., Bard-Chapeau E.A., Oshima R.G., Muller W.J., et al. Conditional deletion of Shp2 in the mammary gland leads to impaired lobulo-alveolar outgrowth and attenuated Stat5 activation. J. Biol. Chem. 2006, 281:34374-34380.
74. Tao B., Jin W., Xu J., Liang Z., Yao J., Zhang Y., et al. Myeloid-specific disruption of tyrosine phosphatase Shp2 promotes alternative activation of macrophages and predisposes mice to pulmonary fibrosis. J. Immunol. 2014, 193:2801-2811.
75. Barron L., Wynn T.A. Macrophage activation governs schistosomiasis-induced inflammation and fibrosis. Eur. J. Immunol. 2011, 41:2509-2514.
76. Matthews R.J., Bowne D.B., Flores E., Thomas M.L. 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, 12:2396-2405.
77. Cohen S., Dadi H., Shaoul E., Sharfe N., Roifman C.M. Cloning and characterization of a lymphoid-specific, inducible human protein tyrosine phosphatase, Lyp. Blood 1999, 93:2013-2024.
78. Chang H.H., Miaw S.C., Tseng W., Sun Y.W., Liu C.C., Tsao H.W., et al. PTPN22 modulates macrophage polarization and susceptibility to dextran sulfate sodium-induced colitis. J. Immunol. 2013, 191:2134-2143.
79. 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.
80. Gregorieff A., Cloutier J.F., Veillette A. Sequence requirements for association of protein-tyrosine phosphatase PEP with the Src homology 3 domain of inhibitory tyrosine protein kinase p50(csk). J. Biol. Chem. 1998, 273:13217-13222.
81. Ghose R., Shekhtman A., Goger M.J., Ji H., Cowburn D. A novel, specific interaction involving the Csk SH3 domain and its natural ligand. Nat. Struct. Biol. 2001, 8:998-1004.
82. Spalinger M.R., Lang S., Weber A., Frei P., Fried M., Rogler G., et al. Loss of protein tyrosine phosphatase nonreceptor type 22 regulates interferon-gamma-induced signaling in human monocytes. Gastroenterology 2013, 144(978-988):e910.
83. Keyse S.M., Emslie E.A. Oxidative stress and heat shock induce a human gene encoding a protein-tyrosine phosphatase. Nature 1992, 359:644-647.
84. Comalada M., Lloberas J., Celada A. MKP-1: a critical phosphatase in the biology of macrophages controlling the switch between proliferation and activation. Eur. J Immunol. 2012, 42:1938-1948.
85. Farooq A., Zhou M.M. Structure and regulation of MAPK phosphatases. Cell. Signal. 2004, 16:769-779.
86. Valledor A.F., Arpa L., Sanchez-Tillo E., Comalada M., Casals C., Xaus J., et al. IFN-{gamma}-mediated inhibition of MAPK phosphatase expression results in prolonged MAPK activity in response to M-CSF and inhibition of proliferation. Blood 2008, 112:3274-3282.
87. Lomonaco S.L., Kahana S., Blass M., Brody Y., Okhrimenko H., Xiang C., et al. Phosphorylation of protein kinase Cdelta on distinct tyrosine residues induces sustained activation of Erk1/2 via down-regulation of MKP-1: role in the apoptotic effect of etoposide. J. Biol. Chem. 2008, 283:17731-17739.
88. Zhao Q., Wang X., Nelin L.D., Yao Y., Matta R., Manson M.E., et al. MAP kinase phosphatase 1 controls innate immune responses and suppresses endotoxic shock. J. Exp. Med. 2006, 203:131-140.
89. Hammer M., Mages J., Dietrich H., Servatius A., Howells N., Cato A.C., et al. Dual specificity phosphatase 1 (DUSP1) regulates a subset of LPS-induced genes and protects mice from lethal endotoxin shock. J. Exp. Med. 2006, 203:15-20.
90. Chi H., Barry S.P., Roth R.J., Wu J.J., Jones E.A., Bennett A.M., et al. Dynamic regulation of pro- and anti-inflammatory cytokines by MAPK phosphatase 1 (MKP-1) in innate immune responses. Proc. Natl. Acad. Sci. USA 2006, 103:2274-2279.
91. Rodriguez N., Dietrich H., Mossbrugger I., Weintz G., Scheller J., Hammer M., et al. Increased inflammation and impaired resistance to Chlamydophila pneumoniae infection in Dusp1(-/-) mice: critical role of IL-6. J. Leukoc. Biol. 2010, 88:579-587.
92. Frazier W.J., Wang X., Wancket L.M., Li X.A., Meng X., Nelin L.D., et al. Increased inflammation, impaired bacterial clearance, and metabolic disruption after gram-negative sepsis in Mkp-1-deficient mice. J. Immunol. 2009, 183:7411-7419.
93. Valledor A.F., Xaus J., Comalada M., Soler C., Celada A. Protein kinase C epsilon is required for the induction of mitogen-activated protein kinase phosphatase-1 in lipopolysaccharide-stimulated macrophages. J. Immunol. 2000, 164:29-37.
94. Yu H., Sun Y., Haycraft C., Palanisamy V., Kirkwood K.L. MKP-1 regulates cytokine mRNA stability through selectively modulation subcellular translocation of AUF1. Cytokine 2011, 56:245-255.
95. Perdiguero E., Kharraz Y., Serrano A.L., Munoz-Canoves P. MKP-1 coordinates ordered macrophage-phenotype transitions essential for stem cell-dependent tissue repair. Cell Cycle 2012, 11:877-886.
96. Haj F.G., Markova B., Klaman L.D., Bohmer F.D., Neel B.G. Regulation of receptor tyrosine kinase signaling by protein tyrosine phosphatase-1B. J. Biol. Chem. 2003, 278:739-744.
97. Chernoff J., Schievella A.R., Jost C.A., Erikson R.L., Neel B.G. Cloning of a cDNA for a major human protein-tyrosine-phosphatase. Proc. Natl. Acad. Sci. USA 1990, 87:2735-2739.
98. Frangioni J.V., Beahm P.H., Shifrin V., Jost C.A., Neel B.G. The nontransmembrane tyrosine phosphatase PTP-1B localizes to the endoplasmic reticulum via its 35 amino acid C-terminal sequence. Cell 1992, 68:545-560.
99. Traves P.G., Pardo V., Pimentel-Santillana M., Gonzalez-Rodriguez A., Mojena M., Rico D., et al. Pivotal role of protein tyrosine phosphatase 1B (PTP1B) in the macrophage response to pro-inflammatory and anti-inflammatory challenge. Cell Death Dis. 2014, 5:e1125.
100. Xu H., An H., Hou J., Han C., Wang P., Yu Y., et al. Phosphatase PTP1B negatively regulates MyD88- and TRIF-dependent proinflammatory cytokine and type I interferon production in TLR-triggered macrophages. Mol. Immunol. 2008, 45:3545-3552.
101. Lu X., Malumbres R., Shields B., Jiang X., Sarosiek K.A., Natkunam Y., et al. PTP1B is a negative regulator of interleukin 4-induced STAT6 signaling. Blood 2008, 112:4098-4108.
102. Pike K.A., Hutchins A.P., Vinette V., Theberge J.F., Sabbagh L., Tremblay M.L., et al. Protein tyrosine phosphatase 1B is a regulator of the interleukin-10-induced transcriptional program in macrophages. Sci. Signal. 2014, 7:ra43.
103. Plutzky J., Neel B.G., Rosenberg R.D., Eddy R.L., Byers M.G., Jani-Sait S., et al. Chromosomal localization of an SH2-containing tyrosine phosphatase (PTPN6). Genomics 1992, 13:869-872.
104. Tsui F.W., Martin A., Wang J., Tsui H.W. Investigations into the regulation and function of the SH2 domain-containing protein-tyrosine phosphatase SHP-1. Immunol. Res. 2006, 35:127-136.
105. Amin S., Kumar A., Nilchi L., Wright K., Kozlowski M. Breast cancer cells proliferation is regulated by tyrosine phosphatase SHP1 through c-jun N-terminal kinase and cooperative induction of RFX-1 and AP-4 transcription factors. Mol. Cancer Res. 2011, 9:1112-1125.
106. Kon-Kozlowski M., Pani G., Pawson T., Siminovitch K.A. The tyrosine phosphatase PTP1C associates with Vav, Grb2, and mSos1 in hematopoietic cells. J. Biol. Chem. 1996, 271:3856-3862.
107. Minton K. Animal models: unravelling the motheaten phenotype. Nat. Rev. Immunol. 2013, 13:306.
108. Tsui F.W., Tsui H.W. Molecular basis of the motheaten phenotype. Immunol. Rev. 1994, 138:185-206.
109. Christophi G.P., Massa P.T. Central neuroinvasion and demyelination by inflammatory macrophages after peripheral virus infection is controlled by SHP-1. Viral Immunol. 2009, 22:371-387.
110. Hardin A.O., Meals E.A., Yi T., Knapp K.M., English B.K. SHP-1 inhibits LPS-mediated TNF and iNOS production in murine macrophages. Biochem. Biophys. Res. Commun. 2006, 342:547-555.
111. Rego D., Kumar A., Nilchi L., Wright K., Huang S., Kozlowski M. IL-6 production is positively regulated by two distinct Src homology domain 2-containing tyrosine phosphatase-1 (SHP-1)-dependent CCAAT/enhancer-binding protein beta and NF-kappaB pathways and an SHP-1-independent NF-kappaB pathway in lipopolysaccharide-stimulated bone marrow-derived macrophages. J. Immunol. 2011, 186:5443-5456.