Differential role for p120-Catenin in regulation of TLR4 signaling in macrophages

Journal of Immunology

Volumn 193, Issue 4, 2014, Pages 1931-1941

  Yang, Zhiyong ^a   Sun, Dong ^a,b   Yan, Zhibo ^a,b   Reynolds, Albert B ^c   Christman, John W ^d   Minshall, Richard D ^a   Malik, Asrar B ^a   Zhang, Yang ^a   Hu, Guochang ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b SHANDONG UNIVERSITY   (China)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CATENIN; CLODRONIC ACID; COFILIN; GUANOSINE TRIPHOSPHATASE; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 6; LIM KINASE; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN P120; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL MEMBRANE; CONTROLLED STUDY; CYTOKINE RELEASE; DIMERIZATION; DOWN REGULATION; ENDOCYTOSIS; ENDOSOME; ENZYME INHIBITION; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; INNATE IMMUNITY; LUNG ALVEOLUS MACROPHAGE; LUNG EDEMA; LUNG INFILTRATE; LUNG LAVAGE; MACROPHAGE; MALE; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

ACUTE LUNG INJURY; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CATENINS; CELLS, CULTURED; ENDOCYTOSIS; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; INTERLEUKIN-6; LEUKOCYTE COUNT; LIPOPOLYSACCHARIDES; MACROPHAGES, ALVEOLAR; MALE; MICE; MICE, INBRED C57BL; MYELOID DIFFERENTIATION FACTOR 88; NEUTROPHILS; NF-KAPPA B; PROTEIN TRANSPORT; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84905969273     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302863     Document Type: Article

References (44)

1. Barton, G. M. , and R. Medzhitov. 2003. Toll-like receptor signaling pathways. Science 300: 1524-1525.
2. Beutler, B. 2000. Tlr4: central component of the sole mammalian LPS sensor. Curr. Opin. Immunol. 12: 20-26.
3. Biswas, S. K. , L. Gangi, S. Paul, T. Schioppa, A. Saccani, M. Sironi, B. Bottazzi, A. Doni, B. Vincenzo, F. Pasqualini, et al. 2006. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NFkappaB and enhanced IRF-3/STAT1 activation). Blood 107: 2112-2122.
4. Biswas, S. K. , P. Bist, M. K. Dhillon, T. Kajiji, C. Del Fresno, M. Yamamoto, E. Lopez-Collazo, S. Akira, and V. Tergaonkar. 2007. Role for MyD88-independent, TRIF pathway in lipid A/TLR4-induced endotoxin tolerance. J. Immunol. 179: 4083-4092.
5. Husebye, H. , Ø. Halaas, H. Stenmark, G. Tunheim, Ø. Sandanger, B. Bogen, A. Brech, E. Latz, and T. Espevik. 2006. Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J. 25: 683-692.
6. Kagan, J. C. , T. Su, T. Horng, A. Chow, S. Akira, and R. Medzhitov. 2008. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferonb. Nat. Immunol. 9: 361-368.
7. Latz, E. , A. Visintin, E. Lien, K. A. Fitzgerald, T. Espevik, and D. T. Golenbock. 2003. The LPS receptor generates inflammatory signals from the cell surface. J. Endotoxin Res. 9: 375-380.
8. Tanimura, N. , S. Saitoh, F. Matsumoto, S. Akashi-Takamura, and K. Miyake. 2008. Roles for LPS-dependent interaction and relocation of TLR4 and TRAM in TRIF-signaling. Biochem. Biophys. Res. Commun. 368: 94-99.
9. Chiasson, C. M. , K. B. Wittich, P. A. Vincent, V. Faundez, and A. P. Kowalczyk. 2009. p120-catenin inhibits VE-cadherin internalization through a Rhoindependent mechanism. Mol. Biol. Cell. 20: 1970-1980.
10. Hu, G. 2012. p120-Catenin: a novel regulator of innate immunity and inflammation. Crit. Rev. Immunol. 32: 127-138.
11. Wang, Y. L. , A. B. Malik, Y. Sun, S. Hu, A. B. Reynolds, R. D. Minshall, and G. Hu. 2011. Innate immune function of the adherens junction protein p120-catenin in endothelial response to endotoxin. J. Immunol. 186: 3180-3187.
12. Zhang, X. , R. Goncalves, D. M. Mosser. 2008. The isolation and characterization of murine macrophages. Curr. Protoc. Immunol. Chapter 14: Unit 14. 1.
13. Sun, Y. , G. Hu, X. Zhang, and R. D. Minshall. 2009. Phosphorylation of caveolin-1 regulates oxidant-induced pulmonary vascular permeability via paracellular and transcellular pathways. Circ. Res. 105: 676-685, 15 p following 685.
14. Nishimura, N. , and T. Sasaki. 2008. Exocytosis and endocytosis. Methods Mol. Biol. 440: 89-96.
15. Wu, J. , Z. Yan, D. E. Schwartz, J. Yu, A. B. Malik, and G. Hu. 2013. Activation of NLRP3 inflammasome in alveolar macrophages contributes to mechanical stretch-induced lung inflammation and injury. J. Immunol. 190: 3590-3599.
16. Zanoni, I. , R. Ostuni, G. Capuano, M. Collini, M. Caccia, A. E. Ronchi, M. Rocchetti, F. Mingozzi, M. Foti, G. Chirico, et al. 2009. CD14 regulates the dendritic cell life cycle after LPS exposure through NFAT activation. Nature 460: 264-268.
17. Liu, D. , Z. Yan, R. D. Minshall, D. E. Schwartz, Y. Chen, and G. Hu. 2012. Activation of calpains mediates early lung neutrophilic inflammation in ventilator-induced lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 302: L370-L379.
18. Walsh, D. E. , C. M. Greene, T. P. Carroll, C. C. Taggart, P. M. Gallagher, S. J. O'Neill, and N. G. McElvaney. 2001. Interleukin-8 up-regulation by neutrophil elastase is mediated by MyD88/IRAK/TRAF-6 in human bronchial epithelium. J. Biol. Chem. 276: 35494-35499.
19. Hoshino, K. , O. Takeuchi, T. Kawai, H. Sanjo, T. Ogawa, Y. Takeda, K. Takeda, and S. Akira. 1999. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162: 3749-3752.
20. Chang, J. , S. L. Kunkel, and C. H. Chang. 2009. Negative regulation of MyD88-dependent signaling by IL-10 in dendritic cells. Proc. Natl. Acad. Sci. USA 106: 18327-18332.
21. Fitzgerald, K. A. , D. C. Rowe, B. J. Barnes, D. R. Caffrey, A. Visintin, E. Latz, B. Monks, P. M. Pitha, and D. T. Golenbock. 2003. LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J. Exp. Med. 198: 1043-1055.
22. Yamamoto, M. , S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira. 2003. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301: 640-643.
23. Pedchenko, T. V. , G. Y. Park, M. Joo, T. S. Blackwell, and J. W. Christman. 2005. Inducible binding of PU. 1 and interacting proteins to the Toll-like receptor 4 promoter during endotoxemia. Am. J. Physiol. Lung Cell. Mol. Physiol. 289: L429-L437.
24. Kaksonen, M. , C. P. Toret, and D. G. Drubin. 2006. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 7: 404-414.
25. Smythe, E. , and K. R. Ayscough. 2006. Actin regulation in endocytosis. J. Cell Sci. 119: 4589-4598.
26. Lamaze, C. , T. H. Chuang, L. J. Terlecky, G. M. Bokoch, and S. L. Schmid. 1996. Regulation of receptor-mediated endocytosis by Rho and Rac. Nature 382: 177-179.
27. Anastasiadis, P. Z. 2007. p120-ctn: a nexus for contextual signaling via Rho GTPases. Biochim. Biophys. Acta 1773: 34-46.
28. Anastasiadis, P. Z. , S. Y. Moon, M. A. Thoreson, D. J. Mariner, H. C. Crawford, Y. Zheng, and A. B. Reynolds. 2000. Inhibition of RhoA by p120 catenin. Nat. Cell Biol. 2: 637-644.
29. Imai, Y. , K. Kuba, G. G. Neely, R. Yaghubian-Malhami, T. Perkmann, G. van Loo, M. Ermolaeva, R. Veldhuizen, Y. H. Leung, H. Wang, et al. 2008. Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 133: 235-249.
30. 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.
31. Kondo, T. , T. Kawai, and S. Akira. 2012. Dissecting negative regulation of Tolllike receptor signaling. Trends Immunol. 33: 449-458.
32. Kawai, T. , O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11: 115-122.
33. Fitzgerald, K. A. , E. M. Palsson-McDermott, A. G. Bowie, C. A. Jefferies, A. S. Mansell, G. Brady, E. Brint, A. Dunne, P. Gray, M. T. Harte, et al. 2001. Mal (MyD88-adapter-like) is required for Toll-like receptor-4 signal transduction. Nature 413: 78-83.
34. Zanoni, I. , R. Ostuni, L. R. Marek, S. Barresi, R. Barbalat, G. M. Barton, F. Granucci, and J. C. Kagan. 2011. CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147: 868-880.
35. Thieblemont, N. , and S. D. Wright. 1999. Transport of bacterial lipopolysaccharide to the golgi apparatus. J. Exp. Med. 190: 523-534.
36. Latz, E. , A. Visintin, E. Lien, K. A. Fitzgerald, B. G. Monks, E. A. Kurt-Jones, D. T. Golenbock, and T. Espevik. 2002. Lipopolysaccharide rapidly traffics to and from the Golgi apparatus with the toll-like receptor 4-MD-2-CD14 complex in a process that is distinct from the initiation of signal transduction. J. Biol. Chem. 277: 47834-47843.
37. Hornef, M. W. , T. Frisan, A. Vandewalle, S. Normark, and A. Richter-Dahlfors. 2002. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J. Exp. Med. 195: 559-570.
38. Qualmann, B. , and H. Mellor. 2003. Regulation of endocytic traffic by Rho GTPases. Biochem. J. 371: 233-241.
39. Wildenberg, G. A. , M. R. Dohn, R. H. Carnahan, M. A. Davis, N. A. Lobdell, J. Settleman, and A. B. Reynolds. 2006. p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 127: 1027-1039.
40. Manukyan, M. , P. Nalbant, S. Luxen, K. M. Hahn, and U. G. Knaus. 2009. RhoA GTPase activation by TLR2 and TLR3 ligands: connecting via Src to NF-k B. J. Immunol. 182: 3522-3529.
41. Raftopoulou, M. , and A. Hall. 2004. Cell migration: Rho GTPases lead the way. Dev. Biol. 265: 23-32.
42. Wang, D. , J. Lou, C. Ouyang, W. Chen, Y. Liu, X. Liu, X. Cao, J. Wang, and L. Lu. 2010. Ras-related protein Rab10 facilitates TLR4 signaling by promoting replenishment of TLR4 onto the plasma membrane. Proc. Natl. Acad. Sci. USA 107: 13806-13811.
43. Kawai, T. , and S. Akira. 2006. TLR signaling. Cell Death Differ. 13: 816-825.
44. Triantafilou, M. , M. Manukyan, A. Mackie, S. Morath, T. Hartung, H. Heine, and K. Triantafilou. 2004. Lipoteichoic acid and toll-like receptor 2 internalization and targeting to the Golgi are lipid raft-dependent. J. Biol. Chem. 279: 40882-40889.