TRAF1 Coordinates Polyubiquitin Signaling to Enhance Epstein-Barr Virus LMP1-Mediated Growth and Survival Pathway Activation
The linear ubiquitin assembly complex (LUBAC) plays crucial roles in immune receptor-mediated NF-kB and MAP kinase pathway activation. Comparatively little is known about the extent to which microbial pathogens use LUBAC to activate downstream pathways. We demonstrate that TRAF1 enhances EBV oncoprotein LMP1 TES1/CTAR1 domain mediated MAP kinase and canonical NF-kB activation. LMP1 TES1 signaling induces association between TRAF1 and LUBAC, and triggers M1-polyubiquitin chain attachment to TRAF1 complexes. TRAF1 and LMP1 complexes are decorated by M1-polyubiquitin chains in LCL extracts. TRAF2 plays a key role in LMP1-induced LUBAC recruitment and M1-chain attachment to TRAF1 complexes. TRAF1 and LMP1 complexes are modified by lysine 63-linked polyubiquitin chains in LCL extracts, and TRAF2 is a target of LMP1-induced K63-ubiquitin chain attachment. Thus, the TRAF1:TRAF2 heterotrimer may coordinate ubiquitin signaling downstream of TES1. Depletion of TRAF1 or the LUBAC subunit HOIP impairs LCL growth and survival. Thus, although TRAF1 is the only TRAF without a RING finger ubiquitin ligase domain, TRAF1 nonetheless has important roles in ubiqutin-mediated signal transduction downstream of LMP1. Our work suggests that LUBAC is important for EBV-driven B-cell proliferation, and suggests that LUBAC may be a novel therapeutic target in EBV-associated lymphoproliferative disorders.
Vyšlo v časopise:
TRAF1 Coordinates Polyubiquitin Signaling to Enhance Epstein-Barr Virus LMP1-Mediated Growth and Survival Pathway Activation. PLoS Pathog 11(5): e32767. doi:10.1371/journal.ppat.1004890
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004890
Souhrn
The linear ubiquitin assembly complex (LUBAC) plays crucial roles in immune receptor-mediated NF-kB and MAP kinase pathway activation. Comparatively little is known about the extent to which microbial pathogens use LUBAC to activate downstream pathways. We demonstrate that TRAF1 enhances EBV oncoprotein LMP1 TES1/CTAR1 domain mediated MAP kinase and canonical NF-kB activation. LMP1 TES1 signaling induces association between TRAF1 and LUBAC, and triggers M1-polyubiquitin chain attachment to TRAF1 complexes. TRAF1 and LMP1 complexes are decorated by M1-polyubiquitin chains in LCL extracts. TRAF2 plays a key role in LMP1-induced LUBAC recruitment and M1-chain attachment to TRAF1 complexes. TRAF1 and LMP1 complexes are modified by lysine 63-linked polyubiquitin chains in LCL extracts, and TRAF2 is a target of LMP1-induced K63-ubiquitin chain attachment. Thus, the TRAF1:TRAF2 heterotrimer may coordinate ubiquitin signaling downstream of TES1. Depletion of TRAF1 or the LUBAC subunit HOIP impairs LCL growth and survival. Thus, although TRAF1 is the only TRAF without a RING finger ubiquitin ligase domain, TRAF1 nonetheless has important roles in ubiqutin-mediated signal transduction downstream of LMP1. Our work suggests that LUBAC is important for EBV-driven B-cell proliferation, and suggests that LUBAC may be a novel therapeutic target in EBV-associated lymphoproliferative disorders.
Zdroje
1. Longnecker R, Kieff E and Cohen JI (2013) Epstein-Barr Virus. In: Knipe DMaH, P.M., editor. Fields Virology. 6 ed. Philadelphia: Lippincott, Williams and Wilkins. pp. 1898–1959.
2. Thorley-Lawson DA, Gross A (2004) Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N Engl J Med 350: 1328–1337. 15044644
3. Cohen JI (2000) Epstein-Barr virus infection. N Engl J Med 343: 481–492. 10944566
4. Cesarman E (2014) Gammaherpesviruses and lymphoproliferative disorders. Annu Rev Pathol 9: 349–372. doi: 10.1146/annurev-pathol-012513-104656 24111911
5. Vereide D, Sugden B (2010) Insights into the evolution of lymphomas induced by Epstein-Barr virus. Adv Cancer Res 108: 1–19. doi: 10.1016/B978-0-12-380888-2.00001-7 21034964
6. Graham JP, Arcipowski KM, Bishop GA (2010) Differential B-lymphocyte regulation by CD40 and its viral mimic, latent membrane protein 1. Immunol Rev 237: 226–248. doi: 10.1111/j.1600-065X.2010.00932.x 20727039
7. Rastelli J, Homig-Holzel C, Seagal J, Muller W, Hermann AC, et al. (2008) LMP1 signaling can replace CD40 signaling in B cells in vivo and has unique features of inducing class-switch recombination to IgG1. Blood 111: 1448–1455. 18006702
8. Uchida J, Yasui T, Takaoka-Shichijo Y, Muraoka M, Kulwichit W, et al. (1999) Mimicry of CD40 signals by Epstein-Barr virus LMP1 in B lymphocyte responses. Science 286: 300–303. 10514374
9. Bishop GA (2009) The many faces of CD40: multiple roles in normal immunity and disease. Semin Immunol 21: 255–256. doi: 10.1016/j.smim.2009.08.002 19713124
10. Clark EA (2014) A Short History of the B-Cell-Associated Surface Molecule CD40. Front Immunol 5: 472. doi: 10.3389/fimmu.2014.00472 25324844
11. Elgueta R, Benson MJ, de Vries VC, Wasiuk A, Guo Y, et al. (2009) Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol Rev 229: 152–172. doi: 10.1111/j.1600-065X.2009.00782.x 19426221
12. Baichwal VR, Sugden B (1988) Transformation of Balb 3T3 cells by the BNLF-1 gene of Epstein-Barr virus. Oncogene 2: 461–467. 2836780
13. Kaye KM, Izumi KM, Kieff E (1993) Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation. Proc Natl Acad Sci U S A 90: 9150–9154. 8415670
14. Wang D, Liebowitz D, Kieff E (1985) An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells. Cell 43: 831–840. 3000618
15. Zhang B, Kracker S, Yasuda T, Casola S, Vanneman M, et al. (2012) Immune surveillance and therapy of lymphomas driven by Epstein-Barr virus protein LMP1 in a mouse model. Cell 148: 739–751. doi: 10.1016/j.cell.2011.12.031 22341446
16. Kulwichit W, Edwards RH, Davenport EM, Baskar JF, Godfrey V, et al. (1998) Expression of the Epstein-Barr virus latent membrane protein 1 induces B cell lymphoma in transgenic mice. Proc Natl Acad Sci U S A 95: 11963–11968. 9751773
17. Dirmeier U, Hoffmann R, Kilger E, Schultheiss U, Briseno C, et al. (2005) Latent membrane protein 1 of Epstein-Barr virus coordinately regulates proliferation with control of apoptosis. Oncogene 24: 1711–1717. 15674340
18. Izumi KM, Kaye KM, Kieff ED (1994) Epstein-Barr virus recombinant molecular genetic analysis of the LMP1 amino-terminal cytoplasmic domain reveals a probable structural role, with no component essential for primary B-lymphocyte growth transformation. J Virol 68: 4369–4376. 8207810
19. Soni V, Yasui T, Cahir-McFarland E, Kieff E (2006) LMP1 transmembrane domain 1 and 2 (TM1-2) FWLY mediates intermolecular interactions with TM3-6 to activate NF-kappaB. J Virol 80: 10787–10793. 16928765
20. Yasui T, Luftig M, Soni V, Kieff E (2004) Latent infection membrane protein transmembrane FWLY is critical for intermolecular interaction, raft localization, and signaling. Proc Natl Acad Sci U S A 101: 278–283. 14695890
21. Lee J, Sugden B (2007) A membrane leucine heptad contributes to trafficking, signaling, and transformation by latent membrane protein 1. J Virol 81: 9121–9130. 17581993
22. Gires O, Zimber-Strobl U, Gonnella R, Ueffing M, Marschall G, et al. (1997) Latent membrane protein 1 of Epstein-Barr virus mimics a constitutively active receptor molecule. EMBO J 16: 6131–6140. 9359753
23. Martin J, Sugden B (1991) The latent membrane protein oncoprotein resembles growth factor receptors in the properties of its turnover. Cell Growth Differ 2: 653–600. 1667088
24. Ye H, Park YC, Kreishman M, Kieff E, Wu H (1999) The structural basis for the recognition of diverse receptor sequences by TRAF2. Mol Cell 4: 321–330. 10518213
25. Izumi KM, Kaye KM, Kieff ED (1997) The Epstein-Barr virus LMP1 amino acid sequence that engages tumor necrosis factor receptor associated factors is critical for primary B lymphocyte growth transformation. Proc Natl Acad Sci U S A 94: 1447–1452. 9037073
26. Luftig M, Yasui T, Soni V, Kang MS, Jacobson N, et al. (2004) Epstein-Barr virus latent infection membrane protein 1 TRAF-binding site induces NIK/IKK alpha-dependent noncanonical NF-kappaB activation. Proc Natl Acad Sci U S A 101: 141–146. 14691250
27. Floettmann JE, Eliopoulos AG, Jones M, Young LS, Rowe M (1998) Epstein-Barr virus latent membrane protein-1 (LMP1) signalling is distinct from CD40 and involves physical cooperation of its two C-terminus functional regions. Oncogene 17: 2383–2392. 9811470
28. Busch LK, Bishop GA (2001) Multiple carboxyl-terminal regions of the EBV oncoprotein, latent membrane protein 1, cooperatively regulate signaling to B lymphocytes via TNF receptor-associated factor (TRAF)-dependent and TRAF-independent mechanisms. J Immunol 167: 5805–5813. 11698454
29. Devergne O, Hatzivassiliou E, Izumi KM, Kaye KM, Kleijnen MF, et al. (1996) Association of TRAF1, TRAF2, and TRAF3 with an Epstein-Barr virus LMP1 domain important for B-lymphocyte transformation: role in NF-kappaB activation. Mol Cell Biol 16: 7098–7108. 8943365
30. Sandberg M, Hammerschmidt W, Sugden B (1997) Characterization of LMP-1's association with TRAF1, TRAF2, and TRAF3. J Virol 71: 4649–4656. 9151858
31. Mainou BA, Everly DN Jr., Raab-Traub N (2007) Unique signaling properties of CTAR1 in LMP1-mediated transformation. J Virol 81: 9680–9692. 17626074
32. Huye LE, Ning S, Kelliher M, Pagano JS (2007) Interferon regulatory factor 7 is activated by a viral oncoprotein through RIP-dependent ubiquitination. Mol Cell Biol 27: 2910–2918. 17296724
33. Zhang L, Wu L, Hong K, Pagano JS (2001) Intracellular signaling molecules activated by Epstein-Barr virus for induction of interferon regulatory factor 7. J Virol 75: 12393–12401. 11711629
34. Song YJ, Izumi KM, Shinners NP, Gewurz BE, Kieff E (2008) IRF7 activation by Epstein-Barr virus latent membrane protein 1 requires localization at activation sites and TRAF6, but not TRAF2 or TRAF3. Proc Natl Acad Sci U S A 105: 18448–18453. doi: 10.1073/pnas.0809933105 19017798
35. Bentz GL, Whitehurst CB, Pagano JS (2011) Epstein-Barr virus latent membrane protein 1 (LMP1) C-terminal-activating region 3 contributes to LMP1-mediated cellular migration via its interaction with Ubc9. J Virol 85: 10144–10153. doi: 10.1128/JVI.05035-11 21795333
36. Meckes DG Jr., Menaker NF, Raab-Traub N (2013) Epstein-Barr virus LMP1 modulates lipid raft microdomains and the vimentin cytoskeleton for signal transduction and transformation. J Virol 87: 1301–1311. doi: 10.1128/JVI.02519-12 23152522
37. Shkoda A, Town JA, Griese J, Romio M, Sarioglu H, et al. (2012) The germinal center kinase TNIK is required for canonical NF-kappaB and JNK signaling in B-cells by the EBV oncoprotein LMP1 and the CD40 receptor. PLoS Biol 10: e1001376. doi: 10.1371/journal.pbio.1001376 22904686
38. Gewurz BE, Towfic F, Mar JC, Shinners NP, Takasaki K, et al. (2012) Genome-wide siRNA screen for mediators of NF-kappaB activation. Proc Natl Acad Sci U S A 109: 2467–2472. doi: 10.1073/pnas.1120542109 22308454
39. Talaty P, Emery A, Holthusen K, Everly DN Jr. (2012) Identification of transmembrane protein 134 as a novel LMP1-binding protein by using bimolecular fluorescence complementation and an enhanced retroviral mutagen. J Virol 86: 11345–11355. 22855487
40. Kaye KM, Izumi KM, Mosialos G, Kieff E (1995) The Epstein-Barr virus LMP1 cytoplasmic carboxy terminus is essential for B-lymphocyte transformation; fibroblast cocultivation complements a critical function within the terminal 155 residues. J Virol 69: 675–683. 7815530
41. Kaye KM, Izumi KM, Li H, Johannsen E, Davidson D, et al. (1999) An Epstein-Barr virus that expresses only the first 231 LMP1 amino acids efficiently initiates primary B-lymphocyte growth transformation. J Virol 73: 10525–10530. 10559372
42. Cahir-McFarland ED, Carter K, Rosenwald A, Giltnane JM, Henrickson SE, et al. (2004) Role of NF-kappa B in cell survival and transcription of latent membrane protein 1-expressing or Epstein-Barr virus latency III-infected cells. J Virol 78: 4108–4119. 15047827
43. Gewurz BE, Mar JC, Padi M, Zhao B, Shinners NP, et al. (2011) Canonical NF-kappaB activation is essential for Epstein-Barr virus latent membrane protein 1 TES2/CTAR2 gene regulation. J Virol 85: 6764–6773. doi: 10.1128/JVI.00422-11 21543491
44. Morris MA, Dawson CW, Wei W, O'Neil JD, Stewart SE, et al. (2008) Epstein-Barr virus-encoded LMP1 induces a hyperproliferative and inflammatory gene expression programme in cultured keratinocytes. J Gen Virol 89: 2806–2820. doi: 10.1099/vir.0.2008/003970-0 18931079
45. Vockerodt M, Morgan SL, Kuo M, Wei W, Chukwuma MB, et al. (2008) The Epstein-Barr virus oncoprotein, latent membrane protein-1, reprograms germinal centre B cells towards a Hodgkin's Reed-Sternberg-like phenotype. J Pathol 216: 83–92. doi: 10.1002/path.2384 18566961
46. Mosialos G, Birkenbach M, Yalamanchili R, VanArsdale T, Ware C, et al. (1995) The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell 80: 389–399. 7859281
47. Durkop H, Foss HD, Demel G, Klotzbach H, Hahn C, et al. (1999) Tumor necrosis factor receptor-associated factor 1 is overexpressed in Reed-Sternberg cells of Hodgkin's disease and Epstein-Barr virus-transformed lymphoid cells. Blood 93: 617–623. 9885224
48. Rodig SJ, Savage KJ, Nguyen V, Pinkus GS, Shipp MA, et al. (2005) TRAF1 expression and c-Rel activation are useful adjuncts in distinguishing classical Hodgkin lymphoma from a subset of morphologically or immunophenotypically similar lymphomas. Am J Surg Pathol 29: 196–203. 15644776
49. Murray PG, Flavell JR, Baumforth KR, Toomey SM, Lowe D, et al. (2001) Expression of the tumour necrosis factor receptor-associated factors 1 and 2 in Hodgkin's disease. J Pathol 194: 158–164. 11400143
50. Siegler G, Meyer B, Dawson C, Brachtel E, Lennerz J, et al. (2004) Expression of tumor necrosis factor receptor-associated factor 1 in nasopharyngeal carcinoma: possible upregulation by Epstein-Barr virus latent membrane protein 1. Int J Cancer 112: 265–272. 15352039
51. Liebowitz D (1998) Epstein-Barr virus and a cellular signaling pathway in lymphomas from immunosuppressed patients. N Engl J Med 338: 1413–1421. 9580648
52. Eliopoulos AG, Waites ER, Blake SM, Davies C, Murray P, et al. (2003) TRAF1 is a critical regulator of JNK signaling by the TRAF-binding domain of the Epstein-Barr virus-encoded latent infection membrane protein 1 but not CD40. J Virol 77: 1316–1328. 12502848
53. McPherson AJ, Snell LM, Mak TW, Watts TH (2012) Opposing roles for TRAF1 in the alternative versus classical NF-kappaB pathway in T cells. J Biol Chem 287: 23010–23019. doi: 10.1074/jbc.M112.350538 22570473
54. Wang C, McPherson AJ, Jones RB, Kawamura KS, Lin GH, et al. (2012) Loss of the signaling adaptor TRAF1 causes CD8+ T cell dysregulation during human and murine chronic infection. J Exp Med 209: 77–91. doi: 10.1084/jem.20110675 22184633
55. Gerlach B, Cordier SM, Schmukle AC, Emmerich CH, Rieser E, et al. (2011) Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 471: 591–596. doi: 10.1038/nature09816 21455173
56. Iwai K (2014) Diverse roles of the ubiquitin system in NF-kappaB activation. Biochim Biophys Acta 1843: 129–136. doi: 10.1016/j.bbamcr.2013.03.011 23523932
57. Haas TL, Emmerich CH, Gerlach B, Schmukle AC, Cordier SM, et al. (2009) Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol Cell 36: 831–844. doi: 10.1016/j.molcel.2009.10.013 20005846
58. Ikeda F, Deribe YL, Skanland SS, Stieglitz B, Grabbe C, et al. (2011) SHARPIN forms a linear ubiquitin ligase complex regulating NF-kappaB activity and apoptosis. Nature 471: 637–641. doi: 10.1038/nature09814 21455181
59. Tokunaga F, Nakagawa T, Nakahara M, Saeki Y, Taniguchi M, et al. (2011) SHARPIN is a component of the NF-kappaB-activating linear ubiquitin chain assembly complex. Nature 471: 633–636. doi: 10.1038/nature09815 21455180
60. Hostager BS, Fox DK, Whitten D, Wilkerson CG, Eipper BA, et al. (2010) HOIL-1L interacting protein (HOIP) as an NF-kappaB regulating component of the CD40 signaling complex. PLoS One 5: e11380. doi: 10.1371/journal.pone.0011380 20614026
61. Rahighi S, Ikeda F, Kawasaki M, Akutsu M, Suzuki N, et al. (2009) Specific recognition of linear ubiquitin chains by NEMO is important for NF-kappaB activation. Cell 136: 1098–1109. doi: 10.1016/j.cell.2009.03.007 19303852
62. Lo YC, Lin SC, Rospigliosi CC, Conze DB, Wu CJ, et al. (2009) Structural basis for recognition of diubiquitins by NEMO. Mol Cell 33: 602–615. doi: 10.1016/j.molcel.2009.01.012 19185524
63. Clark K, Nanda S, Cohen P (2013) Molecular control of the NEMO family of ubiquitin-binding proteins. Nat Rev Mol Cell Biol 14: 673–685. doi: 10.1038/nrm3644 23989959
64. Sowa ME, Bennett EJ, Gygi SP, Harper JW (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138: 389–403. doi: 10.1016/j.cell.2009.04.042 19615732
65. Rozenblatt-Rosen O, Deo RC, Padi M, Adelmant G, Calderwood MA, et al. (2012) Interpreting cancer genomes using systematic host network perturbations by tumour virus proteins. Nature 487: 491–495. doi: 10.1038/nature11288 22810586
66. Izumi KM, Kieff ED (1997) The Epstein-Barr virus oncogene product latent membrane protein 1 engages the tumor necrosis factor receptor-associated death domain protein to mediate B lymphocyte growth transformation and activate NF-kappaB. Proc Natl Acad Sci U S A 94: 12592–12597. 9356494
67. Devergne O, Cahir McFarland ED, Mosialos G, Izumi KM, Ware CF, et al. (1998) Role of the TRAF binding site and NF-kappaB activation in Epstein-Barr virus latent membrane protein 1-induced cell gene expression. J Virol 72: 7900–7908. 9733827
68. Doench JG, Hartenian E, Graham DB, Tothova Z, Hegde M, et al. (2014) Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat Biotechnol 32: 1262–1267. doi: 10.1038/nbt.3026 25184501
69. Naito Y, Hino K, Bono H, Ui-Tei K (2015) CRISPRdirect: software for designing CRISPR/Cas guide RNA with reduced off-target sites. Bioinformatics 31: 1120–1123. doi: 10.1093/bioinformatics/btu743 25414360
70. Sanjana NE, Shalem O, Zhang F (2014) Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods 11: 783–784. doi: 10.1038/nmeth.3047 25075903
71. van Wijk SJ, Fiskin E, Dikic I (2013) Selective monitoring of ubiquitin signals with genetically encoded ubiquitin chain-specific sensors. Nat Protoc 8: 1449–1458. doi: 10.1038/nprot.2013.089 23807287
72. van Wijk SJ, Fiskin E, Putyrski M, Pampaloni F, Hou J, et al. (2012) Fluorescence-based sensors to monitor localization and functions of linear and K63-linked ubiquitin chains in cells. Mol Cell 47: 797–809. doi: 10.1016/j.molcel.2012.06.017 22819327
73. Fu B, Li S, Wang L, Berman MA, Dorf ME (2014) The ubiquitin conjugating enzyme UBE2L3 regulates TNFalpha-induced linear ubiquitination. Cell Res 24: 376–379. doi: 10.1038/cr.2013.133 24060851
74. Li S, Wang L, Berman M, Kong YY, Dorf ME (2011) Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity 35: 426–440. doi: 10.1016/j.immuni.2011.06.014 21903422
75. Mellacheruvu D, Wright Z, Couzens AL, Lambert JP, St-Denis NA, et al. (2013) The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat Methods 10: 730–736. doi: 10.1038/nmeth.2557 23921808
76. Choi H, Larsen B, Lin ZY, Breitkreutz A, Mellacheruvu D, et al. (2011) SAINT: probabilistic scoring of affinity purification-mass spectrometry data. Nat Methods 8: 70–73. doi: 10.1038/nmeth.1541 21131968
77. Choi H, Liu G, Mellacheruvu D, Tyers M, Gingras AC, et al. (2012) Analyzing protein-protein interactions from affinity purification-mass spectrometry data with SAINT. Curr Protoc Bioinformatics Chapter 8: Unit8 15.
78. Kwon Y, Vinayagam A, Sun X, Dephoure N, Gygi SP, et al. (2013) The Hippo signaling pathway interactome. Science 342: 737–740. doi: 10.1126/science.1243971 24114784
79. Breitkreutz A, Choi H, Sharom JR, Boucher L, Neduva V, et al. (2010) A global protein kinase and phosphatase interaction network in yeast. Science 328: 1043–1046. doi: 10.1126/science.1176495 20489023
80. Choi H, Glatter T, Gstaiger M, Nesvizhskii AI (2012) SAINT-MS1: protein-protein interaction scoring using label-free intensity data in affinity purification-mass spectrometry experiments. J Proteome Res 11: 2619–2624. doi: 10.1021/pr201185r 22352807
81. Matsumoto ML, Dong KC, Yu C, Phu L, Gao X, et al. (2012) Engineering and structural characterization of a linear polyubiquitin-specific antibody. J Mol Biol 418: 134–144. doi: 10.1016/j.jmb.2011.12.053 22227388
82. Fries KL, Miller WE, Raab-Traub N (1999) The A20 protein interacts with the Epstein-Barr virus latent membrane protein 1 (LMP1) and alters the LMP1/TRAF1/TRADD complex. Virology 264: 159–166. 10544141
83. Zheng C, Kabaleeswaran V, Wang Y, Cheng G, Wu H (2010) Crystal structures of the TRAF2: cIAP2 and the TRAF1: TRAF2: cIAP2 complexes: affinity, specificity, and regulation. Mol Cell 38: 101–113. doi: 10.1016/j.molcel.2010.03.009 20385093
84. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, et al. (2007) IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 131: 669–681. 18022362
85. Aviel S, Winberg G, Massucci M, Ciechanover A (2000) Degradation of the epstein-barr virus latent membrane protein 1 (LMP1) by the ubiquitin-proteasome pathway. Targeting via ubiquitination of the N-terminal residue. J Biol Chem 275: 23491–23499. 10807912
86. Cadwell K, Coscoy L (2005) Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 309: 127–130. 15994556
87. Dubois SM, Alexia C, Wu Y, Leclair HM, Leveau C, et al. (2014) A catalytic-independent role for the LUBAC in NF-kappaB activation upon antigen receptor engagement and in lymphoma cells. Blood 123: 2199–2203. doi: 10.1182/blood-2013-05-504019 24497531
88. Yang Y, Schmitz R, Mitala J, Whiting A, Xiao W, et al. (2014) Essential role of the linear ubiquitin chain assembly complex in lymphoma revealed by rare germline polymorphisms. Cancer Discov 4: 480–493. doi: 10.1158/2159-8290.CD-13-0915 24491438
89. Newton K, Matsumoto ML, Wertz IE, Kirkpatrick DS, Lill JR, et al. (2008) Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 134: 668–678. doi: 10.1016/j.cell.2008.07.039 18724939
90. Price AM, Tourigny JP, Forte E, Salinas RE, Dave SS, et al. (2012) Analysis of Epstein-Barr virus-regulated host gene expression changes through primary B-cell outgrowth reveals delayed kinetics of latent membrane protein 1-mediated NF-kappaB activation. J Virol 86: 11096–11106. 22855490
91. Guo F, Sun A, Wang W, He J, Hou J, et al. (2009) TRAF1 is involved in the classical NF-kappaB activation and CD30-induced alternative activity in Hodgkin's lymphoma cells. Mol Immunol 46: 2441–2448. doi: 10.1016/j.molimm.2009.05.178 19540595
92. Eliopoulos AG, Blake SM, Floettmann JE, Rowe M, Young LS (1999) Epstein-Barr virus-encoded latent membrane protein 1 activates the JNK pathway through its extreme C terminus via a mechanism involving TRADD and TRAF2. J Virol 73: 1023–1035. 9882303
93. Rieser E, Cordier SM, Walczak H (2013) Linear ubiquitination: a newly discovered regulator of cell signalling. Trends Biochem Sci 38: 94–102. doi: 10.1016/j.tibs.2012.11.007 23333406
94. Rahighi S, Dikic I (2012) Selectivity of the ubiquitin-binding modules. FEBS Lett 586: 2705–2710. doi: 10.1016/j.febslet.2012.04.053 22569095
95. Chen J, Chen ZJ (2013) Regulation of NF-kappaB by ubiquitination. Curr Opin Immunol 25: 4–12. doi: 10.1016/j.coi.2012.12.005 23312890
96. Emmerich CH, Ordureau A, Strickson S, Arthur JS, Pedrioli PG, et al. (2013) Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc Natl Acad Sci U S A 110: 15247–15252. doi: 10.1073/pnas.1314715110 23986494
97. Damgaard RB, Nachbur U, Yabal M, Wong WW, Fiil BK, et al. (2012) The ubiquitin ligase XIAP recruits LUBAC for NOD2 signaling in inflammation and innate immunity. Mol Cell 46: 746–758. doi: 10.1016/j.molcel.2012.04.014 22607974
98. Warner N, Burberry A, Franchi L, Kim YG, McDonald C, et al. (2013) A genome-wide siRNA screen reveals positive and negative regulators of the NOD2 and NF-kappaB signaling pathways. Sci Signal 6: rs3.
99. Li S, Wang L, Dorf ME (2009) PKC phosphorylation of TRAF2 mediates IKKalpha/beta recruitment and K63-linked polyubiquitination. Mol Cell 33: 30–42. doi: 10.1016/j.molcel.2008.11.023 19150425
100. Schmukle AC, Walczak H (2012) No one can whistle a symphony alone—how different ubiquitin linkages cooperate to orchestrate NF-kappaB activity. J Cell Sci 125: 549–559. doi: 10.1242/jcs.091793 22389394
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2015 Číslo 5
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Human Cytomegalovirus miR-UL112-3p Targets TLR2 and Modulates the TLR2/IRAK1/NFκB Signaling Pathway
- Paradoxical Immune Responses in Non-HIV Cryptococcal Meningitis
- Survives with a Minimal Peptidoglycan Synthesis Machine but Sacrifices Virulence and Antibiotic Resistance
- Fob1 and Fob2 Proteins Are Virulence Determinants of via Facilitating Iron Uptake from Ferrioxamine