Scaffolding adaptor protein Gab1 is required for TLR3/4- and RIG-I-mediated production of proinflammatory cytokines and type I IFN in macrophages

Journal of Immunology

Volumn 184, Issue 11, 2010, Pages 6447-6456

  Zheng, Yuejuan ^a,b   An, Huazhang ^b   Yao, Ming ^a   Hou, Jin ^b   Yu, Yizhi ^b   Feng, Gensheng ^c   Cao, Xuetao ^a,b  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ALPHA INTERFERON; BETA INTERFERON; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P85; RETINOIC ACID INDUCIBLE PROTEIN I; SCAFFOLD PROTEIN; SCAFFOLDING ADAPTOR PROTEIN GAB1; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG; GAB1 PROTEIN, MOUSE; MEMBRANE PROTEIN; NERVE PROTEIN; PHOSPHOPROTEIN; ROBO3 PROTEIN, MOUSE; TLR3 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO; ENZYME ACTIVATION; FEMALE; FIBROBLAST; GENE EXPRESSION; GENE SILENCING; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; VESICULAR STOMATITIS VIRUS; VIRUS INFECTION; VIRUS REPLICATION; ANIMAL; C57BL MOUSE; CELL SEPARATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; IMMUNOLOGY; IMMUNOPRECIPITATION; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BLOTTING, WESTERN; CELL SEPARATION; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IMMUNOPRECIPITATION; INTERFERON TYPE I; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASES; NERVE TISSUE PROTEINS; NF-KAPPA B; PHOSPHOPROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; TRANSFECTION;

EID: 77953397065     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901750     Document Type: Article

References (47)

1. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801.
2. O'Neill, L. A. 2008. The interleukin-1 receptor/Toll-like receptor superfamily: 10 years of progress. Immunol. Rev. 226: 10-18.
3. Kawagoe, T., S. Sato, K. Matsushita, H. Kato, K. Matsui, Y. Kumagai, T. Saitoh, T. Kawai, O. Takeuchi, and S. Akira. 2008. Sequential control of Toll-like receptor-dependent responses by IRAK1 and IRAK2. Nat. Immunol. 9: 684-691.
4. Kawagoe, T., O. Takeuchi, Y. Takabatake, H. Kato, Y. Isaka, T. Tsujimura, and S. Akira. 2009. TANK is a negative regulator of Toll-like receptor signaling and is critical for the prevention of autoimmune nephritis. Nat. Immunol. 10: 965-972.
5. Tamura, T., H. Yanai, D. Savitsky, and T. Taniguchi. 2008. The IRF family transcription factors in immunity and oncogenesis. Annu. Rev. Immunol. 26: 535-584.
6. Tseng, P. H., A. Matsuzawa, W. Zhang, T. Mino, D. A. Vignali, and M. Karin. 2010. Different modes of ubiquitination of the adaptor TRAF3 selectively activate the expression of type I interferons and proinflammatory cytokines. Nat. Immunol. 11: 70-75.
7. 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.
8. Takeuchi, O., and S. Akira. 2009. Innate immunity to virus infection. Immunol. Rev. 227: 75-86.
9. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K. J. Ishii, et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNAviruses. Nature 441: 101-105.
10. Sármay, G., A. Angyal, A. Kertész, M. Maus, and D. Medgyesi. 2006. The multiple function of Grb2 associated binder (Gab) adaptor/scaffolding protein in immune cell signaling. Immunol. Lett. 104: 76-82.
11. Itoh, M., Y. Yoshida, K. Nishida, M. Narimatsu, M. Hibi, and T. Hirano. 2000. Role of Gab1 in heart, placenta, and skin development and growth factor- and cytokine-induced extracellular signal-regulated kinase mitogen-activated protein kinase activation. Mol. Cell. Biol. 20: 3695-3704.
12. Sachs, M., H. Brohmann, D. Zechner, T. Müller, J. Hülsken, I. Walther, U. Schaeper, C. Birchmeier, and W. Birchmeier. 2000. Essential role of Gab1 for signaling by the c-Met receptor in vivo. J. Cell Biol. 150: 1375-1384.
13. Gu, H., and B. G. Neel. 2003. The "Gab" in signal transduction. Trends Cell Biol. 13: 122-130.
14. Basar, T., Y. Shen, and K. Ireton. 2005. Redundant roles for Met docking site tyrosines and the Gab1 pleckstrin homology domain in InlB-mediated entry of Listeria monocytogenes. Infect. Immun. 73: 2061-2074.
15. Fruman, D. A., S. B. Snapper, C. M. Yballe, L. Davidson, J. Y. Yu, F. W. Alt, and L. C. Cantley. 1999. Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85alpha. Science 283: 393-397.
16. Honda, K., A. Takaoka, and T. Taniguchi. 2006. Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25: 349-360. (Pubitemid 44354220)
17. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5: 730-737.
18. You, M., L. M. Flick, D. Yu, and G. S. Feng. 2001. Modulation of the nuclear factor kappa B pathway by Shp-2 tyrosine phosphatase in mediating the induction of interleukin (IL)-6 by IL-1 or tumor necrosis factor. J. Exp. Med. 193: 101-110.
19. 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.
20. Wang, X., N. Li, B. Liu, H. Sun, T. Chen, H. Li, J. Qiu, L. Zhang, T. Wan, and X. Cao. 2004. A novel human phosphatidylethanolamine-binding protein resists tumor necrosis factor α-induced apoptosis by inhibiting mitogen-activated protein kinase pathway activation and phosphatidylethanolamine externalization. J. Biol. Chem. 279: 45855-45864.
21. Shinobu, N., T. Iwamura, M. Yoneyama, K. Yamaguchi, W. Suhara, Y. Fukuhara, F. Amano, and T. Fujita. 2002. Involvement of TIRAP/MAL in signaling for the activation of interferon regulatory factor 3 by lipopolysaccharide. FEBS Lett. 517: 251-256.
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. Xia, S., Z. Guo, X. Xu, H. Yi, Q. Wang, and X. Cao. 2008. Hepatic microenvironment programs hematopoietic progenitor differentiation into regulatory dendritic cells, maintaining liver tolerance. Blood 112: 3175-3185.
25. Ojaniemi, M., V. Glumoff, K. Harju, M. Liljeroos, K. Vuori, and M. Hallman. 2003. Phosphatidylinositol 3-kinase is involved in Toll-like receptor 4-mediated cytokine expression in mouse macrophages. Eur. J. Immunol. 33: 597-605.
26. Koyasu, S. 2003. The role of PI3K in immune cells. Nat. Immunol. 4: 313-319.
27. Cao, W., S. Manicassamy, H. Tang, S. P. Kasturi, A. Pirani, N. Murthy, and B. Pulendran. 2008. Toll-like receptor-mediated induction of type I interferon in plasmacytoid dendritic cells requires the rapamycin-sensitive PI(3)K-mTOR-p70S6K pathway. Nat. Immunol. 9: 1157-1164.
28. Liu, Y., and L. R. Rohrschneider. 2002. The gift of Gab. FEBS Lett. 515: 1-7.
29. Rodrigues, G. A., M. Falasca, Z. Zhang, S. H. Ong, and J. Schlessinger. 2000. A novel positive feedback loop mediated by the docking protein Gab1 and phosphatidylinositol 3-kinase in epidermal growth factor receptor signaling. Mol. Cell. Biol. 20: 1448-1459.
30. Eulenfeld, R., and F. Schaper. 2009. A new mechanism for the regulation of Gab1 recruitment to the plasma membrane. J. Cell Sci. 122: 55-64.
31. Cunnick, J. M., L. Mei, C. A. Doupnik, and J. Wu. 2001. Phosphotyrosines 627 and 659 of Gab1 constitute a bisphosphoryl tyrosine-based activation motif (BTAM) conferring binding and activation of SHP2. J. Biol. Chem. 276: 24380-24387.
32. Pichlmair, A., and C. Reis e Sousa. 2007. Innate recognition of viruses. Immunity 27: 370-383.
33. Thompson, J. M., and A. Iwasaki. 2008. Toll-like receptors regulation of viral infection and disease. Adv. Drug Deliv. Rev. 60: 786-794.
34. Sarkar, S. N., K. L. Peters, C. P. Elco, S. Sakamoto, S. Pal, and G. C. Sen. 2004. Novel roles of TLR3 tyrosine phosphorylation and PI3 kinase in double-stranded RNA signaling. Nat. Struct. Mol. Biol. 11: 1060-1067.
35. Ruse, M., and U. G. Knaus. 2006. New players in TLR-mediated innate immunity: PI3K and small Rho GTPases. Immunol. Res. 34: 33-48.
36. Eskan, M. A., B. G. Rose, M. R. Benakanakere, M. J. Lee, and D. F. Kinane. 2008. Sphingosine 1-phosphate 1 and TLR4 mediate IFN-β expression in human gingival epithelial cells. J. Immunol. 180: 1818-1825.
37. Zhang, S. Q., W. G. Tsiaras, T. Araki, G. Wen, L. Minichiello, R. Klein, and B. G. Neel. 2002. Receptor-specific regulation of phosphatidylinositol 3′-kinase activation by the protein tyrosine phosphatase Shp2. Mol. Cell. Biol. 22: 4062-4072.
38. Holgado-Madruga, M., D. K. Moscatello, D. R. Emlet, R. Dieterich, and A. J. Wong. 1997. Grb2-associated binder-1 mediates phosphatidylinositol 3-kinase activation and the promotion of cell survival by nerve growth factor. Proc. Natl. Acad. Sci. USA 94: 12419-12424.
39. Garcia-Guzman, M., F. Dolfi, K. Zeh, and K. Vuori. 1999. Met-induced JNK activation is mediated by the adapter protein Crk and correlates with the Gab1 - Crk signaling complex formation. Oncogene 18: 7775-7786.
40. Holgado-Madruga, M., and A. J. Wong. 2003. Gab1 is an integrator of cell death versus cell survival signals in oxidative stress. Mol. Cell. Biol. 23: 4471-4484.
41. Kallin, A., J. B. Demoulin, K. Nishida, T. Hirano, L. Rönnstrand, and C. H. Heldin. 2004. Gab1 contributes to cytoskeletal reorganization and chemotaxis in response to platelet-derived growth factor. J. Biol. Chem. 279: 17897-17904.
42. Kapoor, G. S., Y. Zhan, G. R. Johnson, and D. M. O'Rourke. 2004. Distinct domains in the SHP-2 phosphatase differentially regulate epidermal growth factor receptor/NF-kappaB activation through Gab1 in glioblastoma cells. Mol. Cell. Biol. 24: 823-836.
43. Ehrhardt, C., H. Marjuki, T. Wolff, B. Nürnberg, O. Planz, S. Pleschka, and S. Ludwig. 2006. Bivalent role of the phosphatidylinositol-3- kinase (PI3K) during influenza virus infection and host cell defence. Cell. Microbiol. 8: 1336-1348.
44. Schabbauer, G., J. Luyendyk, K. Crozat, Z. F. Jiang, N. Mackman, S. Bahram, and P. Georgel. 2008. TLR4/CD14-mediated PI3K activation is an essential component of interferon-dependent VSV resistance in macrophages. Mol. Immunol. 45: 2790-2796.
45. Pengal, R. A., L. P. Ganesan, G. Wei, H. Fang, M. C. Ostrowski, and S. Tridandapani. 2006. Lipopolysaccharide-induced production of interleukin-10 is promoted by the serine/threonine kinase Akt. Mol. Immunol. 43: 1557-1564.
46. Bhattacharyya, S., P. Sen, M. Wallet, B. Long, A. S. Baldwin, Jr., and R. Tisch. 2004. Immunoregulation of dendritic cells by IL-10 is mediated through suppression of the PI3K/Akt pathway and of IkappaB kinase activity. Blood 104: 1100-1109.
47. 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.