The endoplasmic reticulum acts as a platform for ubiquitylated components of nuclear factor κB signaling

Science Signaling

Volumn 6, Issue 291, 2013, Pages

  Alexia, Catherine ^a,b,c   Poalas, Konstantinos ^a,b,c   Carvalho, Gabrielle ^a,b,c   Zemirli, Naima ^a,b,c   Dwyer, Julie ^d,e,f   Dubois, Sonia M ^a,b,c   Hatchi, Emeline M ^a,b,c   Cordeiro, Nelia ^a,b,c   Smith, Sherri S ^d,e,f   Castanier, Céline ^a,b,c   Le Guelte, Armelle ^d,e,f   Wan, Liling ^g   Kang, Yibin ^g   Vazquez, Aimé ^a,b,c   Gavard, Julie ^d,e,f   Arnoult, Damien ^a,b,c   Bidère, Nicolas ^a,b,c  

^a HÔPITAL PAUL BROUSSE   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c Equipe Labellisée Ligue Nationale Contre le Cancer   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e INSERM   (France)

^f CNRS   (France)

^g PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE PROTEIN; METADHERIN; POLYUBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; CELL FREE SYSTEM; CELL SURFACE; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; INFLAMMATION; INTRACELLULAR SIGNALING; MASS SPECTROMETRY; MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; UBIQUITINATION;

ADAPTIVE IMMUNITY; CELL ADHESION MOLECULES; CYTOKINES; ENDOPLASMIC RETICULUM; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNITY, INNATE; JURKAT CELLS; NF-KAPPA B; POLYUBIQUITIN; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 84884260692     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004496     Document Type: Article

References (36)

1. B. Skaug, X. Jiang, Z. J. Chen, The role of ubiquitin in NF-kB regulatory pathways. Annu. Rev. Biochem. 78, 769-796 (2009).
2. A. P. West, G. S. Shadel, S. Ghosh, Mitochondria in innate immune responses. Nat. Rev. Immunol. 11, 389-402 (2011).
3. M. S. Hayden, S. Ghosh, Shared principles in NF-kB signaling. Cell 132, 344-362 (2008).
4. M. J. Bertrand, S. Milutinovic, K. M. Dickson, W. C. Ho, A. Boudreault, J. Durkin, J. W. Gillard, J. B. Jaquith, S. J. Morris, P. A. Barker, cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 30, 689-700 (2008).
5. C. K. Ea, L. Deng, Z. P. Xia, G. Pineda, Z. J. Chen, Activation of IKK by TNFa requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 22, 245-257 (2006).
6. E. Varfolomeev, T. Goncharov, A. V. Fedorova, J. N. Dynek, K. Zobel, K. Deshayes, W. J. Fairbrother, D. Vucic, c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor a (TNFa)-induced NF-kB activation. J. Biol. Chem. 283, 24295-24299 (2008).
7. A. Matsuzawa, P. H. Tseng, S. Vallabhapurapu, J. L. Luo,W. Zhang, H. Wang, D. A. Vignali, E. Gallagher, M. Karin, Essential cytoplasmic translocation of a cytokine receptor-Assembled signaling complex. Science 321, 663-668 (2008).
8. L. Sun, L. Deng, C. K. Ea, Z. P. Xia, Z. J. Chen, The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol. Cell 14, 289-301 (2004).
9. C. J. Wu, J. D. Ashwell, NEMO recognition of ubiquitinated Bcl10 is required for T cell receptor-mediated NF-kB activation. Proc. Natl. Acad. Sci. U.S.A. 105, 3023-3028 (2008).
10. H. Schmidt, C. Gelhaus, R. Lucius, M. Nebendahl, M. Leippe, O. Janssen, Enrichment and analysis of secretory lysosomes from lymphocyte populations. BMC Immunol. 10, 41 (2009).
11. L. Deng, C. Wang, E. Spencer, L. Yang, A. Braun, J. You, C. Slaughter, C. Pickart, Z. J. Chen, Activation of the IkB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103, 351-361 (2000).
12. G. Hu, Y. Wei, Y. Kang, The multifaceted role of MTDH/AEG-1 in cancer progression. Clin. Cancer Res. 15, 5615-5620 (2009).
13. D. M. Brown, E. Ruoslahti, Metadherin, a cell surface protein in breast tumors that mediates lung metastasis. Cancer Cell 5, 365-374 (2004).
14. H. G. Sutherland, Y. W. Lam, S. Briers, A. I. Lamond, W. A. Bickmore, 3D3/lyric: A novel transmembrane protein of the endoplasmic reticulum and nuclear envelope, which is also present in the nucleolus. Exp. Cell Res. 294, 94-105 (2004).
15. D. C. Kang, Z. Z. Su, D. Sarkar, L. Emdad, D. J. Volsky, P. B. Fisher, Cloning and characterization of HIV-1-inducible astrocyte elevated gene-1, AEG-1. Gene 353, 8-15 (2005).
16. L. Emdad, D. Sarkar, Z. Z. Su, A. Randolph, H. Boukerche, K. Valerie, P. B. Fisher, Activation of the nuclear factor kB pathway by astrocyte elevated gene-1: Implications for tumor progression and metastasis. Cancer Res. 66, 1509-1516 (2006).
17. H. Häcker, P. H. Tseng, M. Karin, Expanding TRAF function: TRAF3 as a tri-faced immune regulator. Nat. Rev. Immunol. 11, 457-468 (2011).
18. G. S. Hotamisligil, Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140, 900-917 (2010).
19. O. Takeuchi, S. Akira, Pattern recognition receptors and inflammation. Cell 140, 805-820 (2010).
20. A. M. Mabb, S. M. Wuerzberger-Davis, S. Miyamoto, PIASy mediates NEMO sumoylation and NF-kB activation in response to genotoxic stress. Nat. Cell Biol. 8, 986-993 (2006).
21. B. K. Yoo, L. Emdad, Z. Z. Su, A. Villanueva, D. Y. Chiang, N. D. Mukhopadhyay, A. S. Mills, S. Waxman, R. A. Fisher, J. M. Llovet, P. B. Fisher, D. Sarkar, Astrocyte elevated gene-1 regulates hepatocellular carcinoma development and progression. J. Clin. Invest. 119, 465-477 (2009).
22. L. Song, W. Li, H. Zhang, W. Liao, T. Dai, C. Yu, X. Ding, L. Zhang, J. Li, Overexpression of AEG-1 significantly associates with tumour aggressiveness and poor prognosis in human non-small cell lung cancer. J. Pathol. 219, 317-326 (2009).
23. L. Emdad, D. Sarkar, S. G. Lee, Z. Z. Su, B. K. Yoo, R. Dash, A. Yacoub, C. E. Fuller, K. Shah, P. Dent, J. N. Bruce, P. B. Fisher, Astrocyte elevated gene-1: A novel target for human glioma therapy. Mol. Cancer Ther. 9, 79-88 (2010).
24. G. Hu, R. A. Chong, Q. Yang, Y. Wei, M. A. Blanco, F. Li, M. Reiss, J. L. Au, B. G. Haffty, Y. Kang, MTDH activation by 8q22 genomic gain promotes chemoresistance and metastasis of poor-prognosis breast cancer. Cancer Cell 15, 9-20 (2009).
25. X. Li, X. Kong, Q. Huo, H. Guo, S. Yan, C. Yuan, M. S. Moran, C. Shao, Q. Yang, Metadherin enhances the invasiveness of breast cancer cells by inducing epithelial to mesenchymal transition. Cancer Sci. 102, 1151-1157 (2011).
26. S. K. Bhutia, T. P. Kegelman, S. K. Das, B. Azab, Z. Z. Su, S. G. Lee, D. Sarkar, P. B. Fisher, Astrocyte elevated gene-1 induces protective autophagy. Proc. Natl. Acad. Sci. U.S.A. 107, 22243-22248 (2010).
27. L. Emdad, S. G. Lee, Z. Z. Su, H. Y. Jeon, H. Boukerche, D. Sarkar, P. B. Fisher, Astrocyte elevated gene-1 (AEG-1) functions as an oncogene and regulates angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 106, 21300-21305 (2009).
28. S. Carrasco, T. Meyer, STIM proteins and the endoplasmic reticulum-plasma membrane junctions. Annu. Rev. Biochem. 80, 973-1000 (2011).
29. R. M. Luik, B. Wang, M. Prakriya, M. M. Wu, R. S. Lewis, Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 454, 538-542 (2008).
30. K. Husnjak, I. Dikic, Ubiquitin-binding proteins: Decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 81, 291-322 (2012).
31. D. L. Burdette, R. E. Vance, STING and the innate immune response to nucleic acids in the cytosol. Nat. Immunol. 14, 19-26 (2013).
32. S. S. Vembar, J. L. Brodsky, One step at a time: Endoplasmic reticulum-Associated degradation. Nat. Rev. Mol. Cell Biol. 9, 944-957 (2008).
33. N. Bidère, V. N. Ngo, J. Lee, C. Collins, L. Zheng, F. Wan, R. E. Davis, G. Lenz, D. E. Anderson, D. Arnoult, A. Vazquez, K. Sakai, J. Zhang, Z. Meng, T. D. Veenstra, L. M. Staudt, M. J. Lenardo, Casein kinase 1a governs antigen-receptor-induced NF-kB activation and human lymphoma cell survival. Nature 458, 92-96 (2009).
34. G. Carvalho, A. Le Guelte, C. Demian, A. Vazquez, J. Gavard, N. Bidère, Interplay between BCL10, MALT1 and IkBa during T-cell-receptor-mediated NFkB activation. J. Cell Sci. 123, 2375-2380 (2010).
35. D. Arnoult, F. Soares, I. Tattoli, C. Castanier, D. J. Philpott, S. E. Girardin, An N-Terminal addressing sequence targets NLRX1 to the mitochondrial matrix. J. Cell Sci. 122, 3161-3168 (2009).
36. A. Oeckinghaus, E.Wegener, V.Welteke, U. Ferch, S. C. Arslan, J. Ruland, C. Scheidereit, D. Krappmann, Malt1 ubiquitination triggers NF-kB signaling upon T-cell activation. EMBO J. 26, 4634-4645 (2007).