The phosphatase JKAP/DUSP22 inhibits T-cell receptor signalling and autoimmunity by inactivating Lck

Nature Communications

Volumn 5, Issue , 2014, Pages

  Li, Ju Pi ^a   Yang, Chia Yu ^a   Chuang, Huai Chia ^a   Lan, Joung Liang ^b,c,d   Chen, Der Yuan ^b,e   Chen, Yi Ming ^b,e   Wang, Xiaohong ^f   Chen, Alice J ^f   Belmont, John W ^f   Tan, Tse Hua ^a,f  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^e NATIONAL YANG MING UNIVERSITY   (Taiwan)

^f BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DUAL SPECIFICITY PHOSPHATASE; JNK PATHWAY ASSOCIATED PHOSPHATASE; PROTEIN KINASE LCK; T LYMPHOCYTE RECEPTOR; TYROSINE; UNCLASSIFIED DRUG; DUSP22 PROTEIN, MOUSE; JKAP PROTEIN, MOUSE; PHOSPHOPROTEIN PHOSPHATASE;

ENZYME ACTIVITY; IMMUNE RESPONSE; RODENT; SIGNALING;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PROTEIN DEPHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; ANIMAL; C57BL MOUSE; CONFOCAL MICROSCOPY; DENSITOMETRY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYMOLOGY; GENETICS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; AUTOIMMUNITY; CELL LINE, TUMOR; DENSITOMETRY; DUAL-SPECIFICITY PHOSPHATASES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; PHOSPHOPROTEIN PHOSPHATASES; SIGNAL TRANSDUCTION;

EID: 84898427825     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4618     Document Type: Article

References (42)

1. Filipp, D., Ballek, O. & Manning, J. Lck, Membrane microdomains, and TCR triggering machinery: defining the new rules of engagement. Front Immunol. 3, 155 (2012)
2. Molina, T. J. et al. Profound block in thymocyte development in mice lacking p56lck. Nature 357, 161-164 (1992)
3. Marth, J. D. et al. Neoplastic transformation induced by an activated lymphocyte-specific protein tyrosine kinase (pp56lck) Mol. Cell. Biol. 8, 540-550 (1988) (Pubitemid 18044870)
4. Abraham, N. & Veillette, A. Activation of p56lck through mutation of a regulatory carboxy-terminal tyrosine residue requires intact sites of autophosphorylation and myristylation. Mol. Cell. Biol. 10, 5197-5206 (1990)
5. Caron, L., Abraham, N., Pawson, T. & Veillette, A. Structural requirements for enhancement of T-cell responsiveness by the lymphocyte-specific tyrosine protein kinase p56lck. Mol. Cell. Biol. 12, 2720-2729 (1992)
6. Hermiston, M. L., Xu, Z. & Weiss, A. CD45: a critical regulator of signaling thresholds in immune cells. Annu. Rev. Immunol. 21, 107-137 (2003) (Pubitemid 37174528)
7. McNeill, L. et al. The differential regulation of Lck kinase phosphorylation sites by CD45 is critical for T cell receptor signaling responses. Immunity 27, 425-437 (2007) (Pubitemid 47418669)
8. Rhee, I. & Veillette, A. Protein tyrosine phosphatases in lymphocyte activation and autoimmunity. Nat. Immunol. 13, 439-447 (2012)
9. Pao, L. I., Badour, K., Siminovitch, K. A. & Neel, B. G. Nonreceptor proteintyrosine phosphatases in immune cell signaling. Annu. Rev. Immunol. 25, 473-523 (2007) (Pubitemid 46697915)
10. Johnson, D. J. et al. Shp1 regulates T cell homeostasis by limiting IL-4 signals. J. Exp. Med. 210, 1419-1431 (2013)
11. Chen, A. J. et al. The dual specificity JKAP specifically activates the c-Jun N-terminal kinase pathway. J. Biol. Chem. 277, 36592-36601 (2002)
12. Huang, C.-Y. & Tan, T.-H. DUSPs, to MAP kinases and beyond. Cell Biosci. 2, 24-33 (2012)
13. Shen, Y. et al. Activation of the Jnk signaling pathway by a dual-specificity phosphatase, JSP-1. Proc. Natl Acad. Sci. USA 98, 13613-13618 (2001) (Pubitemid 33115946)
14. Sekine, Y. et al. Regulation of STAT3-mediated signaling by LMW-DSP2. Oncogene 25, 5801-5806 (2006) (Pubitemid 44435256)
15. Sekine, Y. et al. DUSP22/LMW-DSP2 regulates estrogen receptor-a-mediated signaling through dephosphorylation of Ser-118. Oncogene 26, 6038-6049 (2007) (Pubitemid 47373806)
16. Li, J.-P., Fu, Y.-N., Chen, Y.-R. & Tan, T.-H. JNK pathway-associated phosphatase dephosphorylates focal adhesion kinase and suppresses cell migration. J. Biol. Chem. 285, 5472-5478 (2010)
17. Eglen, R. M. et al. The use of AlphaScreen technology in HTS: current status. Curr. Chem. Genomics 1, 2-10 (2008)
18. Zimmermann, T., Rietdorf, J., Girod, A., Georget, V. & Pepperkok, R. Spectral imaging and linear un-mixing enables improved FRET efficiency with a novel GFP2-YFP FRET pair. FEBS Lett. 531, 245-249 (2002) (Pubitemid 35341202)
19. Jullien, P. et al. Tyr394 and Tyr505 are autophosphorylated in recombinant Lck protein-tyrosine kinase expressed in Escherichia coli. Eur. J. Biochem. 224, 589-596 (1994) (Pubitemid 24282844)
20. Berg, N. N. & Ostergaard, H. L. T cell receptor engagement induces tyrosine phosphorylation of FAK and Pyk2 and their association with Lck. J. Immunol. 159, 1753-1757 (1997) (Pubitemid 127484161)
21. Huang, C.-Y. et al. DUSP4 deficiency enhances CD25 expression and CD4 T-cell proliferation without impeding T-cell development. Eur. J. Immunol. 42, 476-488 (2012)
22. Yang, C.-Y. et al. Dual-specificity phosphatase 14 (DUSP14/MKP6) negatively regulates T-cell receptor signaling by inhibiting TAB1 activation. J. Immunol. 192, 1547-1557 (2014)
23. Salmond, R. J., Huyer, G., Kotsoni, A., Clements, L. & Alexander, D. R. The src homology 2 domain-containing tyrosine phosphatase 2 regulates primary T-dependent immune responses and Th cell differentiation. J. Immunol. 175, 6498-6508 (2005) (Pubitemid 41598892)
24. Hasegawa, K. et al. PEST domain-enriched tyrosine phosphatase (PEP) regulation of effector/memory T cells. Science 303, 685-689 (2004) (Pubitemid 38141637)
25. Wiede, F. et al. T cell protein tyrosine phosphatase attenuates T cell signaling to maintain tolerance in mice. J. Clin. Invest. 121, 4758-4774 (2011)
26. Koretzky, G. A., Picus, J., Thomas, M. L. & Weiss, A. Tyrosine phosphatase CD45 is essential for coupling T-cell antigen receptor to the phosphatidyl inositol pathway. Nature 346, 66-68 (1990)
27. Xiao, Y. Q. et al. Cross-talk between ERK and p38 MAPK mediates selective suppression of pro-inflammatory cytokines by transforming growth factor-b. J. Biol. Chem. 277, 14884-14893 (2002) (Pubitemid 34952562)
28. Tiganis, T. & Bennett, A. M. Protein tyrosine phosphatase function: the substrate perspective. Biochem. J. 402, 1-15 (2007)
29. Tsokos, G. C. Systemic lupus erythematosus. New Engl. J. Med. 365, 2110-2121 (2011)
30. Sanz, I. & Lee, F. E. B cells as therapeutic targets in SLE. Nat. Rev. Rheumatol. 6, 326-337 (2010)
31. Crispin, J. C., Kyttaris, V. C., Terhorst, C. & Tsokos, G. C. T cells as therapeutic targets in SLE. Nat. Rev. Rheumatol. 6, 317-325 (2010)
32. Perl, A. Oxidative stress in the pathology and treatment of systemic lupus erythematosus. Nat. Rev. Rheumatol. 9, 674-686 (2013)
33. Zhang, Y., Zhao, M., Sawalha, A. H., Richardson, B. & Lu, Q. Impaired DNA methylation and its mechanisms in CD4T cells of systemic lupus erythematosus. J. Autoimmun. 41, 92-99 (2013)
34. Crispin, J. C., Hedrich, C. M. & Tsokos, G. C. Gene-function studies in systemic lupus erythematosus. Nat. Rev. Rheumatol. 9, 476-484 (2013)
35. Zhou, G. et al. Protein phosphatase 4 is involved in tumor necrosis factor-a-induced activation of c-Jun N-terminal kinase. J. Biol. Chem. 277, 6391-6398 (2002) (Pubitemid 34968433)
36. Han, J. et al. HIP-55 is important for T-cell proliferation, cytokine production, and immune responses. Mol. Cell. Biol. 25, 6869-6878 (2005) (Pubitemid 41105888)
37. Manders, E. M. M., Verbeek, F. J. & Aten, J. A. Measurement of co-localization of object in dual-color confocal images. J. Microsc. 169, 375-382 (1993) (Pubitemid 23119681)
38. Turner, J. E. et al. CCR5 deficiency aggravates crescentic glomerulonephritis in mice. J. Immunol. 181, 6546-6556 (2008)
39. Shui, J.-W., Hu, M. C. & Tan, T.-H. Conditional knockout mice reveal an essential role of protein phosphatase 4 in thymocyte development and pre-T-cell receptor signaling. Mol. Cell. Biol. 27, 79-91 (2007) (Pubitemid 46013234)
40. Chuang, H.-C. et al. The kinase GLK controls autoimmunity and NF-kB signaling by activating the kinase PKC-y in T cells. Nat. Immunol. 12, 1113-1118 (2011)
41. Miller, S. D. & Karpus, W. J. Experimental autoimmune encephalomyelitis in the mouse. Curr. Protoc. Immunol. Chapter Unit 15-1 (2007)
42. Shui, J. W. et al. Hematopoietic progenitor kinase 1 negatively regulates T cell receptor signaling and T cell-mediated immune responses. Nat. Immunol. 8, 84-91 (2007)