Protein tyrosine phosphatase with proline-glutamine-serine-threonine-rich motifs negatively regulates TLR-triggered innate responses by selectively inhibiting IκB kinase β/NF-κB activation

Journal of Immunology

Volumn 190, Issue 4, 2013, Pages 1685-1694

  Zhang, Peng ^a   Liu, Xingguang ^a   Li, Yingke ^a   Zhu, Xuhui ^a   Zhan, Zhenzhen ^a   Meng, Jun ^b   Li, Nan ^a   Cao, Xuetao ^a,b,c  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMINE; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 10; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; PROLINE; PROTEIN KINASE; PROTEIN TYROSINE PHOSPHATASE; SERINE; TANK BINDING KINASE 1; THREONINE; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SYNTHESIS; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOGLOBULIN ENHANCER BINDING GENE; IMMUNOREGULATION; INNATE IMMUNITY; INTERFERON GAMMA GENE; MACROPHAGE; MOUSE; MUTANT; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROLINE GLUTAMINE SERINE THREONINE RICH MOTIF; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REPORTER GENE; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; ANIMALS; CELL LINE; CELLS, CULTURED; DOWN-REGULATION; GLUTAMINE; HEK293 CELLS; HUMANS; I-KAPPA B KINASE; IMMUNITY, INNATE; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; NF-KAPPA B; PROLINE; PROTEIN INTERACTION MAPPING; PROTEIN KINASE INHIBITORS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 12; SERINE; THREONINE; TISSUE DISTRIBUTION; TOLL-LIKE RECEPTORS;

EID: 84873552386     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202384     Document Type: Article

References (48)

1. Kawai, T., and S. Akira. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11: 373-384.
2. O'Neill, L. A. 2008. The interleukin-1 receptor/Toll-like receptor superfamily: 10 years of progress. Immunol. Rev. 226: 10-18.
3. Lee, M. S., and Y. J. Kim. 2007. Signaling pathways downstream of patternrecognition receptors and their cross talk. Annu. Rev. Biochem. 76: 447-480.
4. Barton, G. M., and R. Medzhitov. 2003. Toll-like receptor signaling pathways. Science 300: 1524-1525.
5. Blasius, A. L., and B. Beutler. 2010. Intracellular toll-like receptors. Immunity 32: 305-315.
6. Netea, M. G., C. Wijmenga, and L. A. O'Neill. 2012. Genetic variation in Tolllike receptors and disease susceptibility. Nat. Immunol. 13: 535-542.
7. Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell 140: 805-820.
8. Marshak-Rothstein, A., and I. R. Rifkin. 2007. Immunologically active autoantigens: the role of toll-like receptors in the development of chronic inflammatory disease. Annu. Rev. Immunol. 25: 419-441.
9. Liu, J., S. Liu, and X. Cao. 2012. Highlights of the advances in basic immunology in 2011. Cell. Mol. Immunol. 9: 197-207.
10. Liew, F. Y., D. Xu, E. K. Brint, and L. A. O'Neill. 2005. Negative regulation of toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 5: 446-458.
11. Liu, X., M. Yao, N. Li, C. Wang, Y. Zheng, and X. Cao. 2008. CaMKII promotes TLR-triggered proinflammatory cytokine and type I interferon production by directly binding and activating TAK1 and IRF3 in macrophages. Blood 112: 4961-4970.
12. Wang, C., T. Chen, J. Zhang, M. Yang, N. Li, X. Xu, and X. Cao. 2009. The E3 ubiquitin ligase Nrdp1 'preferentially' promotes TLR-mediated production of type I interferon. Nat. Immunol. 10: 744-752.
13. Chang, M., W. Jin, and S. C. Sun. 2009. Peli1 facilitates TRIF-dependent Tolllike receptor signaling and proinflammatory cytokine production. Nat. Immunol. 10: 1089-1095.
14. Liu, X., Z. Zhan, D. Li, L. Xu, F. Ma, P. Zhang, H. Yao, and X. Cao. 2011. Intracellular MHC class II molecules promote TLR-triggered innate immune responses by maintaining activation of the kinase Btk. Nat. Immunol. 12: 416-424.
15. Schneider, M., A. G. Zimmermann, R. A. Roberts, L. Zhang, K. V. Swanson, H. Wen, B. K. Davis, I. C. Allen, E. K. Holl, Z. Ye, et al. 2012. The innate immune sensor NLRC3 attenuates Toll-like receptor signaling via modification of the signaling adaptor TRAF6 and transcription factor NF-kB. Nat. Immunol. 13: 823-831.
16. An, H., H. Xu, M. Zhang, J. Zhou, T. Feng, C. Qian, R. Qi, and X. Cao. 2005. Src homology 2 domain-containing inositol-5-phosphatase 1 (SHIP1) negatively regulates TLR4-mediated LPS response primarily through a phosphatase activity- and PI-3K-independent mechanism. Blood 105: 4685-4692.
17. Han, C., J. Jin, S. Xu, H. Liu, N. Li, and X. Cao. 2010. Integrin CD11b negatively regulates TLR-triggered inflammatory responses by activating Syk and promoting degradation of MyD88 and TRIF via Cbl-b. Nat. Immunol. 11: 734-742.
18. Xu, S., X. Liu, Y. Bao, X. Zhu, C. Han, P. Zhang, X. Zhang, W. Li, and X. Cao. 2012. Constitutive MHC class I molecules negatively regulate TLR-triggered inflammatory responses via the Fps-SHP-2 pathway. Nat. Immunol. 13: 551-559.
19. Tonks, N. K. 2006. Protein tyrosine phosphatases: from genes, to function, to disease. Nat. Rev. Mol. Cell Biol. 7: 833-846.
20. Alonso, A., J. Sasin, N. Bottini, I. Friedberg, I. Friedberg, A. Osterman, A. Godzik, T. Hunter, J. Dixon, and T. Mustelin. 2004. Protein tyrosine phosphatases in the human genome. Cell 117: 699-711.
21. Mustelin, T., T. Vang, and N. Bottini. 2005. Protein tyrosine phosphatases and the immune response. Nat. Rev. Immunol. 5: 43-57.
22. An, H., W. Zhao, J. Hou, Y. Zhang, Y. Xie, Y. Zheng, H. Xu, C. Qian, J. Zhou, Y. Yu, et al. 2006. SHP-2 phosphatase negatively regulates the TRIF adaptor protein-dependent type I interferon and proinflammatory cytokine production. Immunity 25: 919-928.
23. An, H., J. Hou, J. Zhou, W. Zhao, H. Xu, Y. Zheng, Y. Yu, S. Liu, and X. Cao. 2008. Phosphatase SHP-1 promotes TLR- and RIG-I-activated production of type I interferon by inhibiting the kinase IRAK1. Nat. Immunol. 9: 542-550.
24. Yang, Q., D. Co, J. Sommercorn, and N. K. Tonks. 1993. Cloning and expression of PTP-PEST. A novel, human, nontransmembrane protein tyrosine phosphatase. J. Biol. Chem. 268: 6622-6628.
25. Garton, A. J., M. R. Burnham, A. H. Bouton, and N. K. Tonks. 1997. Association of PTP-PEST with the SH3 domain of p130cas; a novel mechanism of protein tyrosine phosphatase substrate recognition. Oncogene 15: 877-885.
26. Spencer, S., D. Dowbenko, J. Cheng, W. Li, J. Brush, S. Utzig, V. Simanis, and L. A. Lasky. 1997. PSTPIP: a tyrosine phosphorylated cleavage furrowassociated protein that is a substrate for a PEST tyrosine phosphatase. J. Cell Biol. 138: 845-860.
27. Shen, Y., G. Schneider, J. F. Cloutier, A. Veillette, and M. D. Schaller. 1998. Direct association of protein-tyrosine phosphatase PTP-PEST with paxillin. J. Biol. Chem. 273: 6474-6481.
28. Lyons, P. D., J. M. Dunty, E. M. Schaefer, and M. D. Schaller. 2001. Inhibition of the catalytic activity of cell adhesion kinase beta by protein-tyrosine phosphatase-PEST-mediated dephosphorylation. J. Biol. Chem. 276: 24422-24431.
29. Davidson, D., and A. Veillette. 2001. PTP-PEST, a scaffold protein tyrosine phosphatase, negatively regulates lymphocyte activation by targeting a unique set of substrates. EMBO J. 20: 3414-3426.
30. Arimura, Y., T. Vang, L. Tautz, S.Williams, and T. Mustelin. 2008. TCR-induced downregulation of protein tyrosine phosphatase PEST augments secondary T cell responses. Mol. Immunol. 45: 3074-3084.
31. Davidson, D., X. Shi, M. C. Zhong, I. Rhee, and A. Veillette. 2010. The phosphatase PTP-PEST promotes secondary T cell responses by dephosphorylating the protein tyrosine kinase Pyk2. Immunity 33: 167-180.
32. Nakamura, K., H. E. Palmer, T. Ozawa, and K. Mashima. 2010. Protein phosphatase 1alpha associates with protein tyrosine phosphatase-PEST inducing dephosphorylation of phospho-serine 39. J. Biochem. 147: 493-500.
33. Mathew, S., S. P. George, Y. Wang, M. R. Siddiqui, K. Srinivasan, L. Tan, and S. Khurana. 2008. Potential molecular mechanism for c-Src kinase-mediated regulation of intestinal cell migration. J. Biol. Chem. 283: 22709-22722.
34. Garton, A. J., A. J. Flint, and N. K. Tonks. 1996. Identification of p130(cas) as a substrate for the cytosolic protein tyrosine phosphatase PTP-PEST. Mol. Cell. Biol. 16: 6408-6418.
35. Zheng, Y., Y. Xia, D. Hawke, M. Halle, M. L. Tremblay, X. Gao, X. Z. Zhou, K. Aldape, M. H. Cobb, K. Xie, et al. 2009. FAK phosphorylation by ERK primes ras-induced tyrosine dephosphorylation of FAK mediated by PIN1 and PTP-PEST. Mol. Cell 35: 11-25.
36. Saraiva, M., and A. O'Garra. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10: 170-181.
37. Liu, F., Y. Xia, A. S. Parker, and I. M. Verma. 2012. IKK biology. Immunol. Rev. 246: 239-253.
38. Schmid, J. A., and A. Birbach. 2008. IkappaB kinase beta (IKKbeta/IKK2/IKBKB)-α key molecule in signaling to the transcription factor NF-kappaB. Cytokine Growth Factor Rev. 19: 157-165.
39. Huang, W. C., J. J. Chen, and C. C. Chen. 2003. c-Src-dependent tyrosine phosphorylation of IKKbeta is involved in tumor necrosis factor-alphainduced intercellular adhesion molecule-1 expression. J. Biol. Chem. 278: 9944-9952.
40. Huang, W. C., J. J. Chen, H. Inoue, and C. C. Chen. 2003. Tyrosine phosphorylation of I-kappa B kinase alpha/beta by protein kinase C-dependent c-Src activation is involved in TNF-alpha-induced cyclooxygenase-2 expression. J. Immunol. 170: 4767-4775.
41. Darwech, I., J. E. Otero, M. A. Alhawagri, and Y. Abu-Amer. 2010. Tyrosine phosphorylation is required for IkappaB kinase-beta (IKKbeta) activation and function in osteoclastogenesis. J. Biol. Chem. 285: 25522-25530.
42. Lenardo, M. J., C. M. Fan, T. Maniatis, and D. Baltimore. 1989. The involvement of NF-kappa B in beta-interferon gene regulation reveals its role as widely inducible mediator of signal transduction. Cell 57: 287-294.
43. Apostolou, E., and D. Thanos. 2008. Virus Infection Induces NF-kappaB dependent interchromosomal associations mediating monoallelic IFN-beta gene expression. Cell 134: 85-96.
44. Wang, J., S. H. Basagoudanavar, X. Wang, E. Hopewell, R. Albrecht, A. García-Sastre, S. Balachandran, and A. A. Beg. 2010. NF-kappa B RelA subunit is crucial for early IFN-beta expression and resistance to RNA virus replication. J. Immunol. 185: 1720-1729.
45. Hayden, M. S., and S. Ghosh. 2008. Shared principles in NF-kappaB signaling. Cell 132: 344-362.
46. Dev, A., S. Iyer, B. Razani, and G. Cheng. 2011. NF-kB and innate immunity. Curr. Top. Microbiol. Immunol. 349: 115-143.
47. Xu, H., H. An, J. Hou, C. Han, P. Wang, Y. Yu, and X. Cao. 2008. Phosphatase PTP1B negatively regulates MyD88- and TRIF-dependent proinflammatory cytokine and type I interferon production in TLR-triggered macrophages. Mol. Immunol. 45: 3545-3552.
48. Sirois, J., J. F. Côté, A. Charest, N. Uetani, A. Bourdeau, S. A. Duncan, E. Daniels, and M. L. Tremblay. 2006. Essential function of PTP-PEST during mouse embryonic vascularization, mesenchyme formation, neurogenesis and early liver development. Mech. Dev. 123: 869-880.