The adaptor CRADD/RAIDD controls activation of endothelial cells by proinflammatory stimuli

Journal of Biological Chemistry

Volumn 289, Issue 32, 2014, Pages 21973-21983

  Qiao, Huan ^a   Liu, Yan ^a   Veach, Ruth A ^a   Wylezinski, Lukasz ^b   Hawiger, Jacek ^a,b  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

BARRIER FUNCTIONS; ENDOTHELIAL BARRIERS; PRO-INFLAMMATORY STIMULI; PROINFLAMMATORY;

ENDOTHELIAL CELLS;

AUTACOID; BCL10 PROTEIN, HUMAN; BCL10 PROTEIN, MOUSE; CARD10 PROTEIN, HUMAN; CARD10 PROTEIN, MOUSE; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; CELL PENETRATING PEPTIDE; CRADD PROTEIN; CRADD PROTEIN, HUMAN; CRADD PROTEIN, MOUSE; RECOMBINANT PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA;

129 MOUSE; ANIMAL; CAPILLARY PERMEABILITY; CELL CULTURE; CYTOLOGY; DEFICIENCY; ENDOTHELIUM CELL; GENETICS; HUMAN; INFLAMMATION; LUNG; METABOLISM; MICROVASCULATURE; MOUSE; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CAPILLARY PERMEABILITY; CARD SIGNALING ADAPTOR PROTEINS; CELL-PENETRATING PEPTIDES; CELLS, CULTURED; CRADD SIGNALING ADAPTOR PROTEIN; ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; LUNG; MICE; MICE, 129 STRAIN; MICROVESSELS; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84905842658     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.588723     Document Type: Article

References (60)

1. Hawiger, J., and Musser, J. M. (2011) How to approach genome wars in sepsis? Crit. Care 15, 1007
2. Alexander, W. S., and Hilton, D. J. (2004) The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response. Annu. Rev. Immunol. 22, 503-529
3. Liew, F. Y., Xu, D., Brint, E. K., and O'Neill, L. A. (2005) Negative regulation of toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 5, 446-458
4. Rakesh, K., and Agrawal, D. K. (2005) Controlling cytokine signaling by constitutive inhibitors. Biochem. Pharmacol. 70, 649-657
5. Coornaert, B., Carpentier, I., and Beyaert, R. (2009) A20: central gatekeeper in inflammation and immunity. J. Biol. Chem. 284, 8217-8221
6. Lin, Q., Liu, Y., Moore, D. J., Elizer, S. K., Veach, R. A., Hawiger, J., and Ruley, H. E. (2012) Cutting edge: the "death" adaptor CRADD/RAIDD targets BCL10 and suppresses agonist-induced cytokine expression in T lymphocytes. J. Immunol. 188, 2493-2497
7. Paul, S., and Schaefer, B. C. (2013) A new look at T cell receptor signaling to nuclear factor-B. Trends Immunol. 34, 269-281
8. Egawa, T., Albrecht, B., Favier, B., Sunshine, M. J., Mirchandani, K., O'Brien, W., Thome, M., and Littman, D. R. (2003) Requirement for CARMA1 in antigen receptor-induced NF-κB activation and lymphocyte proliferation. Curr. Biol. 13, 1252-1258
9. Gaide, O., Favier, B., Legler, D. F., Bonnet, D., Brissoni, B., Valitutti, S., Bron, C., Tschopp, J., and Thome, M. (2002) CARMA1 is a critical lipid raft-associated regulator of TCR-induced NF-κB activation. Nat. Immunol. 3, 836-843
10. Hara, H., Wada, T., Bakal, C., Kozieradzki, I., Suzuki, S., Suzuki, N., Nghiem, M., Griffiths, E. K., Krawczyk, C., Bauer, B., D'Acquisto, F., Ghosh, S., Yeh, W. C., Baier, G., Rottapel, R., and Penninger, J. M. (2003) The MAGUK family protein CARD11 is essential for lymphocyte activation. Immunity 18, 763-775
11. Jun, J. E., Wilson, L. E., Vinuesa, C. G., Lesage, S., Blery, M., Miosge, L. A., Cook, M. C., Kucharska, E. M., Hara, H., Penninger, J. M., Domashenz, H., Hong, N. A., Glynne, R. J., Nelms, K. A., and Goodnow, C. C. (2003) Identifying the MAGUK protein Carma-1 as a central regulator of humoral immune responses and atopy by genome-wide mouse mutagenesis. Immunity 18, 751-762
12. Newton, K., and Dixit, V. M. (2003) Mice lacking the CARD of CARMA1 exhibit defective B lymphocyte development and impaired proliferation of their B and T lymphocytes. Curr. Biol. 13, 1247-1251
13. Sun, J. (2010) CARMA3: A novel scaffold protein in regulation of NFkappaB activation and diseases. World J. Biol. Chem. 1, 353-361
14. Jiang, C., and Lin, X. (2012) Regulation of NF-κB by the CARD proteins. Immunol. Rev. 246, 141-153
15. McAllister-Lucas, L. M., Jin, X., Gu, S., Siu, K., McDonnell, S., Ruland, J., Delekta, P. C., Van Beek, M., and Lucas, P. C. (2010) The CARMA3-Bcl10-MALT1 signalosome promotes angiotensin II-dependent vascular inflammation and atherogenesis. J. Biol. Chem. 285, 25880-25884
16. Martin, D., Galisteo, R., and Gutkind, J. S. (2009) CXCL8/IL8 stimulates vascular endothelial growth factor (VEGF) expression and the autocrine activation of VEGFR2 in endothelial cells by activating NF-B through the CBM (Carma3/Bcl10/Malt1) complex. J. Biol. Chem. 284, 6038-6042
17. Kenne, E., and Lindbom, L. (2011) Imaging inflammatory plasma leakage in vivo. Thromb. Haemost. 105, 783-789
18. Delekta, P. C., Apel, I. J., Gu, S., Siu, K., Hattori, Y., McAllister-Lucas, L. M., and Lucas, P. C. (2010) Thrombin-dependent NF-κB activation and monocyte/endothelial adhesion are mediated by the CARMA3-Bcl10 MALT1 signalosome. J. Biol. Chem. 285, 41432-41442
19. Blonska, M., and Lin, X. (2009) CARMA1-mediated NF-κB and JNK activation in lymphocytes. Immunol. Rev. 228, 199-211
20. Colgan, O. C., Ferguson, G., Collins, N. T., Murphy, R. P., Meade, G., Cahill, P. A., and Cummins, P. M. (2007) Regulation of bovine brain microvascular endothelial tight junction assembly and barrier function by laminar shear stress. Am. J. Physiol. Heart Circ. Physiol. 292, H3190-H3197
21. Goldenberg, N. M., Steinberg, B. E., Slutsky, A. S., and Lee, W. L. (2011) Broken barriers: a new take on sepsis pathogenesis. Sci. Transl. Med. 3, 88ps25
22. Vestweber, D. (2008) VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler. Thromb. Vasc. Biol. 28, 223-232
23. Herwig, M. C., Tsokos, M., Hermanns, M. I., Kirkpatrick, C. J., and Müller, A. M. (2013) Vascular endothelial cadherin expression in lung specimens of patients with sepsis-induced acute respiratory distress syndrome and endothelial cell cultures. Pathobiology 80, 245-251
24. Garcia, J. G., Verin, A. D., and Schaphorst, K. L. (1996) Regulation of thrombin-mediated endothelial cell contraction and permeability. Semin. Thromb. Hemost. 22, 309-315
25. Wang, Y., Chen, H., Li, H., Zhang, J., and Gao, Y. (2013) Effect of angiopoietin-like protein 4 on rat pulmonary microvascular endothelial cells exposed to LPS. Int. J. Mol. Med. 32, 568-576
26. Marion, S., Mazzolini, J., Herit, F., Bourdoncle, P., Kambou-Pene, N., Hailfinger, S., Sachse, M., Ruland, J., Benmerah, A., Echard, A., Thome, M., and Niedergang, F. (2012) The NF-κB signaling protein Bcl10 regulates actin dynamics by controlling AP1 and OCRL-bearing vesicles. Dev. Cell 23, 954-967
27. Rueda, D., Gaide, O., Ho, L., Lewkowicz, E., Niedergang, F., Hailfinger, S., Rebeaud, F., Guzzardi, M., Conne, B., Thelen, M., Delon, J., Ferch, U., Mak, T. W., Ruland, J., Schwaller, J., and Thome, M. (2007) Bcl10 controls TCR-and Fc-R-induced actin polymerization. J. Immunol. 178, 4373-4384
28. Unger, R. E., Krump-Konvalinkova, V., Peters, K., and Kirkpatrick, C. J. (2002) In vitro expression of the endothelial phenotype: comparative study of primary isolated cells and cell lines, including the novel cell line HPMEC-ST1.6R. Microvasc. Res. 64, 384-397
29. Schreiber, A. B., Kenney, J., Kowalski, W. J., Friesel, R., Mehlman, T., and Maciag, T. (1985) Interaction of endothelial cell growth factor with heparin: characterization by receptor and antibody recognition. Proc. Natl. Acad. Sci. U.S.A. 82, 6138-6142
30. Fletcher, T. C., DiGiandomenico, A., and Hawiger, J. (2010) Extended anti-inflammatory action of a degradation-resistant mutant of cell-penetrating suppressor of cytokine signaling 3. J. Biol. Chem. 285, 18727-18736
31. Qiao, H., and May, J. M. (2012) Interaction of the transcription start site core region and transcription factor YY1 determine ascorbate transporter SVCT2 exon 1a promoter activity. PloS One 7, e35746
32. Jo, D., Liu, D., Yao, S., Collins, R. D., and Hawiger, J. (2005) Intracellular protein therapy with SOCS3 inhibits inflammation and apoptosis. Nat. Med. 11, 892-898
33. Bhattacharyya, S., Borthakur, A., Dudeja, P. K., and Tobacman, J. K. (2010) Lipopolysaccharide-induced activation of NF-κB non-canonical pathway requires BCL10 serine 138 and NIK phosphorylations. Exp. Cell Res. 316, 3317-3327
34. Dong, W., Liu, Y., Peng, J., Chen, L., Zou, T., Xiao, H., Liu, Z., Li, W., Bu, Y., and Qi, Y. (2006) The IRAK-1-BCL10-MALT1-TRAF6-TAK1 cascade mediates signaling to NF-κB from Toll-like receptor 4. J. Biol. Chem. 281, 26029-26040
35. Desai, T. R., Leeper, N. J., Hynes, K. L., and Gewertz, B. L. (2002) Interleukin-6 causes endothelial barrier dysfunction via the protein kinase C pathway. J. Surg. Res. 104, 118-123
36. DiGiandomenico, A., Wylezinski, L. S., and Hawiger, J. (2009) Intracellular delivery of a cell-penetrating SOCS1 that targets IFN-γ signaling. Sci. Signal. 2, ra37
37. Stamatovic, S. M., Keep, R. F., Kunkel, S. L., and Andjelkovic, A. V. (2003) Potential role of MCP-1 in endothelial cell tight junction "opening": signaling via Rho and Rho kinase. J. Cell Sci. 116, 4615-4628
38. He, F., Peng, J., Deng, X. L., Yang, L. F., Wu, L. W., Zhang, C. L., and Yin, F. (2011) RhoA and NF-κB are involved in lipopolysaccharide-induced brain microvascular cell line hyperpermeability. Neuroscience 188, 35-47
39. Bogatcheva, N. V., Zemskova, M. A., Kovalenkov, Y., Poirier, C., and Verin, A. D. (2009) Molecular mechanisms mediating protective effect of cAMP on lipopolysaccharide (LPS)-induced human lung microvascular endothelial cells (HLMVEC) hyperpermeability. J. Cell Physiol. 221, 750-759
40. van der Heijden, M., van Nieuw Amerongen, G. P., van Bezu, J., Paul, M. A., Groeneveld, A. B., and van Hinsbergh, V. W. (2011) Opposing effects of the angiopoietins on the thrombin-induced permeability of human pulmonary microvascular endothelial cells. PloS One 6, e23448
41. Wegener, E., and Krappmann, D. (2007) CARD-Bcl10-Malt1 Signalosomes: missing link to NF-κB. Sci. STKE 2007, pe21
42. Fraser, C. C. (2008) G protein-coupled receptor connectivity to NF-κB in inflammation and cancer. Int. Rev. Immunol. 27, 320-350
43. Bhattacharyya, S., Borthakur, A., Pant, N., Dudeja, P. K., and Tobacman, J. K. (2007) Bcl10 mediates LPS-induced activation of NF-κB and IL-8 in human intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 293, G429-G437
44. Wang, D., You, Y., Lin, P. C., Xue, L., Morris, S. W., Zeng, H., Wen, R., and Lin, X. (2007) Bcl10 plays a critical role in NF-κB activation induced by G protein-coupled receptors. Proc. Natl. Acad. Sci. U.S.A. 104, 145-150
45. Klemm, S., Zimmermann, S., Peschel, C., Mak, T. W., and Ruland, J. (2007) Bcl10 and Malt1 control lysophosphatidic acid-induced NF-κB activation and cytokine production. Proc. Natl. Acad. Sci. U.S.A. 104, 134-138
46. Coughlin, S. R. (2000) Thrombin signalling and protease-activated receptors. Nature 407, 258-264
47. Minami, T., Sugiyama, A., Wu, S. Q., Abid, R., Kodama, T., and Aird, W. C. (2004) Thrombin and phenotypic modulation of the endothelium. Arterioscler. Thromb. Vasc. Biol. 24, 41-53
48. Major, C. D., Santulli, R. J., Derian, C. K., and Andrade-Gordon, P. (2003) Extracellular mediators in atherosclerosis and thrombosis: lessons from thrombin receptor knockout mice. Arterioscler. Thromb. Vasc. Biol. 23, 931-939
49. Hirano, K. (2007) The roles of proteinase-activated receptors in the vascular physiology and pathophysiology. Arterioscler. Thromb. Vasc. Biol. 27, 27-36
50. Martorell, L., Martínez-González, J., Rodríguez, C., Gentile, M., Calvayrac, O., and Badimon, L. (2008) Thrombin and protease-activated receptors (PARs) in atherothrombosis. Thromb. Haemost. 99, 305-315
51. Chen, Z. J. (2012) Ubiquitination in signaling to and activation of IKK. Immunol. Rev. 246, 95-106
52. Zhou, H., Wertz, I., O'Rourke, K., Ultsch, M., Seshagiri, S., Eby, M., Xiao, W., and Dixit, V. M. (2004) Bcl10 activates the NF-κB pathway through ubiquitination of NEMO. Nature 427, 167-171
53. McAllister-Lucas, L. M., Ruland, J., Siu, K., Jin, X., Gu, S., Kim, D. S., Kuffa, P., Kohrt, D., Mak, T. W., Nuñez, G., and Lucas, P. C. (2007) CARMA3/ Bcl10/MALT1-dependent NF-κB activation mediates angiotensin II-responsive inflammatory signaling in nonimmune cells. Proc. Natl. Acad. Sci. U.S.A. 104, 139-144
54. Aghajanian, A., Wittchen, E. S., Allingham, M. J., Garrett, T. A., and Burridge, K. (2008) Endothelial cell junctions and the regulation of vascular permeability and leukocyte transmigration. J. Thromb. Haemost. 6, 1453-1460
55. Vandenbroucke, E., Mehta, D., Minshall, R., and Malik, A. B. (2008) Regulation of endothelial junctional permeability. Ann. N.Y. Acad. Sci. 1123, 134-145
56. Bannerman, D. D., and Goldblum, S. E. (1999) Direct effects of endotoxin on the endothelium: barrier function and injury. Lab. Investig. 79, 1181-1199
57. Gong, P., Angelini, D. J., Yang, S., Xia, G., Cross, A. S., Mann, D., Bannerman, D. D., Vogel, S. N., and Goldblum, S. E. (2008) TLR4 signaling is coupled to SRC family kinase activation, tyrosine phosphorylation of zonula adherens proteins, and opening of the paracellular pathway in human lung microvascular endothelia. J. Biol. Chem. 283, 13437-13449
58. Liu, A., Gong, P., Hyun, S. W., Wang, K. Z., Cates, E. A., Perkins, D., Bannerman, D. D., Puché, A. C., Toshchakov, V. Y., Fang, S., Auron, P. E., Vogel, S. N., and Goldblum, S. E. (2012) TRAF6 protein couples Toll-like receptor 4 signaling to Src family kinase activation and opening of paracellular pathway in human lung microvascular endothelia. J. Biol. Chem. 287, 16132-16145
59. Yuan, D., and He, P. (2012) Vascular remodeling alters adhesion protein and cytoskeleton reactions to inflammatory stimuli resulting in enhanced permeability increases in rat venules. J. Appl. Physiol. 113, 1110-1120
60. Londoño, D., Carvajal, J., Strle, K., Kim, K. S., and Cadavid, D. (2011) IL-10 Prevents apoptosis of brain endothelium during bacteremia. J. Immunol. 186, 7176-7186