Noncanonical NF-κB activation by the oncoprotein tio occurs through a nonconserved TRAF3-binding motif

Science Signaling

Volumn 6, Issue 272, 2013, Pages

  De Jong, Sarah Jill ^a,c   Albrecht, Jens Christian ^a   Giehler, Fabian ^b   Kieser, Arnd ^b   Sticht, Heinrich ^a   Biesinger, Brigitte ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ONCOPROTEIN; ONCOPROTEIN TIO; PROTEIN P100; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; UBIQUITIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; DNA BINDING MOTIF; GENE EXPRESSION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ALIGNMENT;

AMINO ACID MOTIFS; CELL LINE, TRANSFORMED; GENE EXPRESSION REGULATION; HUMANS; JURKAT CELLS; NF-KAPPA B; ONCOGENE PROTEINS, VIRAL; RHADINOVIRUS; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 3; UBIQUITINATION;

EID: 84876885202     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003309     Document Type: Article

References (47)

1. S. Vallabhapurapu, M. Karin, Regulation and function of NF-κB transcription factors in the immune system. Annu. Rev. Immunol. 27, 693-733 (2009).
2. L. M. Staudt, Oncogenic activation of NF-κB. Cold Spring Harb. Perspect. Biol. 2, a000109 (2010).
3. P. J. Jost, J. Ruland, Aberrant NF-κB signaling in lymphoma: Mechanisms, consequences, and therapeutic implications. Blood 109, 2700-2707 (2007).
4. D. E. de Oliveira, G. Ballon, E. Cesarman, NF-κB signaling modulation by EBV and KSHV. Trends Microbiol. 18, 248-257 (2010).
5. K. T. Jeang, HTLV-1 and adult T-cell leukemia: Insights into viral transformation of cells 30 years after virus discovery. J. Formos. Med. Assoc. 109, 688-693 (2010).
6. A. Kieser, Pursuing different 'TRADDes': TRADD signaling induced by TNF-receptor 1 and the Epstein-Barr virus oncoprotein LMP1. Biol. Chem. 389, 1261-1271 (2008).
7. S. Vallabhapurapu, A. Matsuzawa, W. Zhang, P. H. Tseng, J. J. Keats, H. Wang, D. A. A. Vignali, P. L. Bergsagel, M. Karin, Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-κB signaling. Nat. Immunol. 9, 1364-1370 (2008).
8. B. J. Zarnegar, Y. Wang, D. J. Mahoney, P. W. Dempsey, H. H. Cheung, J. He, T. Shiba, X. Yang, W. C. Yeh, T. W. Mak, R. G. Korneluk, G. Cheng, Noncanonical NF-κB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat. Immunol. 9, 1371-1378 (2008).
9. J. E. Vince, D. Chau, B. Callus, W. W. Wong, C. J. Hawkins, P. Schneider, M. McKinlay, C. A. Benetatos, S. M. Condon, S. K. Chunduru, G. Yeoh, R. Brink, D. L. Vaux, J. Silke, TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFα. J. Cell Biol. 182, 171-184 (2008).
10. E. Varfolomeev, T. Goncharov, H. Maecker, K. Zobel, L. G. Kömüves, K. Deshayes, D. Vucic, Cellular inhibitors of apoptosis are global regulators of NF-κB and MAPK activation by members of the TNF family of receptors. Sci. Signal. 5, ra22 (2012).
11. B. Razani, A. D. Reichardt, G. Cheng, Non-canonical NF-κB signaling activation and regulation: Principles and perspectives. Immunol. Rev. 244, 44-54 (2011).
12. S. C. Sun, Non-canonical NF- κB signaling pathway. Cell Res. 21, 71-85 (2011).
13. Y. M. Thu, A. Richmond, NF-κB inducing kinase: A key regulator in the immune system and in cancer. Cytokine Growth Factor Rev. 21, 213-226 (2010).
14. H. Häcker, P. H. Tseng, M. Karin, Expanding TRAF function: TRAF3 as a tri-faced immune regulator. Nat. Rev. Immunol. 11, 457-468 (2011).
15. H. Ye, Y. C. Park, M. Kreishman, E. Kieff, H. Wu, The structural basis for the recognition of diverse receptor sequences by TRAF2. Mol. Cell 4, 321-330 (1999).
16. K. R. Ely, R. Kodandapani, S. Wu, Protein-protein interactions in TRAF3. Adv. Exp. Med. Biol. 597, 114-121 (2007).
17. B. Zarnegar, S. Yamazaki, J. Q. He, G. Cheng, Control of canonical NF-κB activation through the NIK-IKK complex pathway. Proc. Natl. Acad. Sci. U.S.A. 105, 3503-3508 (2008).
18. Y. Sasaki, D. P. Calado, E. Derudder, B. Zhang, Y. Shimizu, F. Mackay, S. Nishikawa, K. Rajewsky, M. Schmidt-Supprian, NIK overexpression amplifies, whereas ablation of its TRAF3-binding domain replaces BAFF:BAFF-R-mediated survival signals in B cells. Proc. Natl. Acad. Sci. U.S.A. 105, 10883-10888 (2008).
19. S. Basak, H. Kim, J. D. Kearns, V. Tergaonkar, E. O'Dea, S. L. Werner, C. A. Benedict, C. F. Ware, G. Ghosh, I. M. Verma, A. Hoffmann, A fourth IκB protein within the NF-κB signaling module. Cell 128, 369-381 (2007).
20. J. C. Albrecht, U. Friedrich, C. Kardinal, J. Koehn, B. Fleckenstein, S. M. Feller, B. Biesinger, Herpesvirus ateles gene product Tio interacts with nonreceptor protein tyrosine kinases. J. Virol. 73, 4631-4639 (1999).
21. S. Heinemann, B. Biesinger, B. Fleckenstein, J. C. Albrecht, NFκB signaling is induced by the oncoprotein Tio through direct interaction with TRAF6. J. Biol. Chem. 281, 8565-8572 (2006).
22. J. C. Albrecht, I. Müller-Fleckenstein, M. Schmidt, B. Fleckenstein, B. Biesinger, Tyrosine phosphorylation of the Tio oncoprotein is essential for transformation of primary human T cells. J. Virol. 79, 10507-10513 (2005).
23. J. C. Albrecht, B. Biesinger, I. Müller-Fleckenstein, D. Lengenfelder, M. Schmidt, B. Fleckenstein, A. Ensser, Herpesvirus ateles Tio can replace herpesvirus saimiri StpC and Tip oncoproteins in growth transformation of monkey and human T cells. J. Virol. 78, 9814-9819 (2004).
24. S. J. de Jong, J. C. Albrecht, M. Schmidt, I. Müller-Fleckenstein, B. Biesinger, Activation of noncanonical NF-κB signaling by the oncoprotein Tio. J. Biol. Chem. 285, 16495-16503 (2010).
25. S. Wu, P. Xie, K.Welsh, C. Li, C. Z. Ni, X. Zhu, J. C. Reed, A. C. Satterthwait, G. A. Bishop, K. R. Ely, LMP1 protein from the Epstein-Barr virus is a structural CD40 decoy in B lymphocytes for binding to TRAF3. J. Biol. Chem. 280, 33620-33626 (2005).
26. A. Oeckinghaus, M. S. Hayden, S. Ghosh, Crosstalk in NF-κB signaling pathways. Nat. Immunol. 12, 695-708 (2011).
27. S. C. Sun, P. A. Ganchi, C. Béraud, D. W. Ballard, W. C. Greene, Autoregulation of the NF-κB transactivator RelA (p65) by multiple cytoplasmic inhibitors containing ankyrin motifs. Proc. Natl. Acad. Sci. U.S.A. 91, 1346-1350 (1994).
28. Z. B. Yilmaz, D. S. Weih, V. Sivakumar, F. Weih, RelB is required for Peyer's patch development: Differential regulation of p52-RelB by lymphotoxin and TNF. EMBO J. 22, 121-130 (2003).
29. E. Dejardin, N. M. Droin, M. Delhase, E. Haas, Y. Cao, C. Makris, Z. W. Li, M. Karin, C. F. Ware, D. R. Green, The lymphotoxin-β receptor induces different patterns of gene expression via two NF-κB pathways. Immunity 17, 525-535 (2002).
30. Y. N. Demchenko, O. K. Glebov, A. Zingone, J. J. Keats, P. L. Bergsagel, W. M. Kuehl, Classical and/or alternative NF-κB pathway activation in multiple myeloma. Blood 115, 3541-3552 (2010).
31. L. V. Pham, L. Fu, A. T. Tamayo, C. Bueso-Ramos, E. Drakos, F. Vega, L. J. Medeiros, R. J. Ford, Constitutive BR3 receptor signaling in diffuse, large B-cell lymphomas stabilizes nuclear factor-κB-inducing kinase while activating both canonical and alternative nuclear factor-κB pathways. Blood 117, 200-210 (2011).
32. P. S. Norris, C. F. Ware, The LTßR signaling pathway. Adv. Exp. Med. Biol. 597, 160-172 (2007).
33. V. Soni, E. Cahir-McFarland, E. Kieff, LMP1 TRAFficking activates growth and survival pathways. Adv. Exp. Med. Biol. 597, 173-187 (2007).
34. J. M. Zapata, V. Martínez-García, S. Lefebvre, Phylogeny of the TRAF/MATH domain. Adv. Exp. Med. Biol. 597, 1-24 (2007).
35. C. Z. Ni, G. Oganesyan, K. Welsh, X. Zhu, J. C. Reed, A. C. Satterthwait, G. Cheng, K. R. Ely, Key molecular contacts promote recognition of the BAFF receptor by TNF receptor-associated factor 3: Implications for intracellular signaling regulation. J. Immunol. 173, 7394-7400 (2004).
36. S. C. Sun, Controlling the fate of NIK: A central stage in noncanonical NF-κB signaling. Sci. Signal. 3, pe18 (2010).
37. G. Liao, M. Zhang, E. W. Harhaj, S. C. Sun, Regulation of the NF-κB-inducing kinase by tumor necrosis factor receptor-associated factor 3-induced degradation. J. Biol. Chem. 279, 26243-26250 (2004).
38. H. Sanjo, D. M. Zajonc, R. Braden, P. S. Norris, C. F. Ware, Allosteric regulation of the ubiquitin:NIK and ubiquitin:TRAF3 E3 ligases by the lymphotoxin-β receptor. J. Biol. Chem. 285, 17148-17155 (2010).
39. A. Kieser, C. Kaiser, W. Hammerschmidt, LMP1 signal transduction differs substantially from TNF receptor 1 signaling in the molecular functions of TRADD and TRAF2. EMBO J. 18, 2511-2521 (1999).
40. K. Katsch, S. J. de Jong, M. Schmidt, I. Müller-Fleckenstein, B. Fleckenstein, J. C. Albrecht, B. Biesinger, Species restriction of Herpesvirus saimiri and Herpesvirus ateles: Human lymphocyte transformation correlates with distinct signaling properties of viral oncoproteins. Virus Res. 165, 179-189 (2012).
41. J. S. Bonifacino, Metabolic labeling with amino acids. Curr. Protoc. Cell Biol. Chapter 7, Unit 7.1 (2001).
42. K. Heinzelmann, B. A. Scholz, A. Nowak, E. Fossum, E. Kremmer, J. Haas, R. Frank, B. Kempkes, Kaposi 's sarcoma-associated herpesvirus viral interferon regulatory factor 4 (vIRF4/K10) is a novel interaction partner of CSL/CBF1, the major downstream effector of Notch signaling. J. Virol. 84, 12255-12264 (2010).
43. H. R. Lee, W. C. Choi, S. Lee, J. Hwang, E. Hwang, K. Guchhait, J. Haas, Z. Toth, Y. H. Jeon, T. K. Oh, M. H. Kim, J. U. Jung, Bilateral inhibition of HAUSP deubiquitinase by a viral interferon regulatory factor protein. Nat. Struct. Mol. Biol. 18, 1336-1344 (2011).
44. N. Eswar, D. Eramian, B. Webb, M. Y. Shen, A. Sali, Protein structure modeling with MODELLER. Methods Mol. Biol. 426, 145-159 (2008).
45. A. C. Wallace, R. A. Laskowski, J. M. Thornton, LIGPLOT: A program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8, 127-134 (1995).
46. R. A. Sayle, E. J. Milner-White, RASMOL: Biomolecular graphics for all. Trends Biochem. Sci. 20, 374 (1995).
47. J. D. Thompson, T. J. Gibson, D. G. Higgins, Multiple sequence alignment using ClustalW and ClustalX. Curr. Protoc. Bioinformatics Chapter 2, Unit 2.3 (2002).