The Germinal Center Kinase TNIK Is Required for Canonical NF-κB and JNK Signaling in B-Cells by the EBV Oncoprotein LMP1 and the CD40 Receptor

PLoS Biology

Volumn 10, Issue 8, 2012, Pages

  Shkoda, Anna ^a   Town, Jennifer A ^a   Griese, Janine ^a   Romio, Michael ^a   Sarioglu, Hakan ^a   Knöfel, Thomas ^a   Giehler, Fabian ^a   Kieser, Arnd ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 RECEPTOR; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LATENT MEMBRANE PROTEIN 1; NCK INTERACTING KINASE; PROTEIN SERINE THREONINE KINASE; RECEPTOR PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; B LYMPHOCYTE; CARBOXY TERMINAL SEQUENCE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; EPSTEIN BARR VIRUS; GENE SILENCING; HUMAN; HUMAN CELL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEOMICS; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANTIGENS, CD40; B-LYMPHOCYTES; CELL PROLIFERATION; CELL TRANSFORMATION, VIRAL; HEK293 CELLS; HERPESVIRUS 4, HUMAN; HUMANS; MAP KINASE SIGNALING SYSTEM; NF-KAPPA B; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS; RNA INTERFERENCE; VIRAL MATRIX PROTEINS;

HUMAN HERPESVIRUS 4;

EID: 84865734196     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001376     Document Type: Article

References (70)

1. Fu CA, Shen M, Huang BC, Lasaga J, Payan DG, et al. (1999) TNIK, a novel member of the germinal center kinase family that activates the c-Jun N-terminal kinase pathway and regulates the cytoskeleton. J Biol Chem 274: 30729-30737.
2. Dan I, Watanabe NM, Kusumi A, (2001) The Ste20 group kinases as regulators of MAP kinase cascades. Trends Cell Biol 11: 220-230.
3. Taira K, Umikawa M, Takei K, Myagmar BE, Shinzato M, et al. (2004) The Traf2- and Nck-interacting kinase as a putative effector of Rap2 to regulate actin cytoskeleton. J Biol Chem 279: 49488-49496.
4. Schurch C, Riether C, Matter MS, Tzankov A, Ochsenbein AF, (2012) CD27 signaling on chronic myelogenous leukemia stem cells activates Wnt target genes and promotes disease progression. J Clin Invest 122: 624-638.
5. Mahmoudi T, Li VS, Ng SS, Taouatas N, Vries RG, et al. (2009) The kinase TNIK is an essential activator of Wnt target genes. EMBO J 28: 3329-3340.
6. Shitashige M, Satow R, Jigami T, Aoki K, Honda K, et al. (2010) Traf2- and Nck-interacting kinase is essential for Wnt signaling and colorectal cancer growth. Cancer Res 70: 5024-5033.
7. Kawabe H, Neeb A, Dimova K, Young SM Jr, Takeda M, et al. (2010) Regulation of Rap2A by the ubiquitin ligase Nedd4-1 controls neurite development. Neuron 65: 358-372.
8. Hussain NK, Hsin H, Huganir RL, Sheng M, (2010) MINK and TNIK differentially act on Rap2-mediated signal transduction to regulate neuronal structure and AMPA receptor function. J Neurosci 30: 14786-14794.
9. Young LS, Rickinson AB, (2004) Epstein-Barr virus: 40 years on. Nat Rev Cancer 4: 757-768.
10. 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.
11. Kilger E, Kieser A, Baumann M, Hammerschmidt W, (1998) Epstein-Barr virus-mediated B-cell proliferation is dependent upon latent membrane protein 1, which simulates an activated CD40 receptor. EMBO J 17: 1700-1709.
12. Kaykas A, Worringer K, Sugden B, (2001) CD40 and LMP-1 both signal from lipid rafts but LMP-1 assembles a distinct, more efficient signaling complex. EMBO J 20: 2641-2654.
13. 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.
14. 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.
15. 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.
16. Stunz LL, Busch LK, Munroe ME, Sigmund CD, Tygrett LT, et al. (2004) Expression of the cytoplasmic tail of LMP1 in mice induces hyperactivation of B lymphocytes and disordered lymphoid architecture. Immunity 21: 255-266.
17. 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.
18. Soni V, Cahir-McFarland E, Kieff E, (2007) LMP1 TRAFficking activates growth and survival pathways. Adv Exp Med Biol 597: 173-187.
19. Kieser A, (2008) Pursuing different 'TRADDes': TRADD signaling induced by TNF-receptor 1 and the Epstein-Barr virus oncoprotein LMP1. Biol Chem 389: 1261-1271.
20. Kieser A, (2007) Signal transduction by the Epstein-Barr virus oncogene latent membrane protein 1 (LMP1). Signal Transduction 7: 20-33.
21. 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.
22. Sandberg M, Hammerschmidt W, Sugden B, (1997) Characterization of LMP-1's association with TRAF1, TRAF2, and TRAF3. J Virol 71: 4649-4656.
23. Brodeur SR, Cheng G, Baltimore D, Thorley-Lawson DA, (1997) Localization of the major NF-kappaB-activating site and the sole TRAF3 binding site of LMP-1 defines two distinct signaling motifs. J Biol Chem 272: 19777-19784.
24. Atkinson PG, Coope HJ, Rowe M, Ley SC, (2003) Latent membrane protein 1 of Epstein-Barr virus stimulates processing of NF-kappa B2 p100 to p52. J Biol Chem 278: 51134-51142.
25. Saito N, Courtois G, Chiba A, Yamamoto N, Nitta T, et al. (2003) Two carboxyl-terminal activation regions of Epstein-Barr virus latent membrane protein 1 activate NF-kappaB through distinct signaling pathways in fibroblast cell lines. J Biol Chem 278: 46565-46575.
26. Eliopoulos AG, Caamano JH, Flavell J, Reynolds GM, Murray PG, et al. (2003) Epstein-Barr virus-encoded latent infection membrane protein 1 regulates the processing of p100 NF-kappaB2 to p52 via an IKKgamma/NEMO-independent signalling pathway. Oncogene 22: 7557-7569.
27. 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.
28. Mitchell T, Sugden B, (1995) Stimulation of NF-kappa B-mediated transcription by mutant derivatives of the latent membrane protein of Epstein-Barr virus. J Virol 69: 2968-2976.
29. Huen DS, Henderson SA, Croom-Carter D, Rowe M, (1995) The Epstein-Barr virus latent membrane protein-1 (LMP1) mediates activation of NF-kappa B and cell surface phenotype via two effector regions in its carboxy-terminal cytoplasmic domain. Oncogene 10: 549-560.
30. Kieser A, Kilger E, Gires O, Ueffing M, Kolch W, et al. (1997) Epstein-Barr virus latent membrane protein-1 triggers AP-1 activity via the c-Jun N-terminal kinase cascade. EMBO J 16: 6478-6485.
31. 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.
32. Kutz H, Reisbach G, Schultheiss U, Kieser A, (2008) The c-Jun N-terminal kinase pathway is critical for cell transformation by the latent membrane protein 1 of Epstein-Barr virus. Virology 371: 246-256.
33. Luftig M, Prinarakis E, Yasui T, Tsichritzis T, Cahir-McFarland E, et al. (2003) Epstein-Barr virus latent membrane protein 1 activation of NF-kappaB through IRAK1 and TRAF6. Proc Natl Acad Sci U S A 100: 15595-15600.
34. Kieser A, Kaiser C, Hammerschmidt W, (1999) LMP1 signal transduction differs substantially from TNF receptor 1 signaling in the molecular functions of TRADD and TRAF2. EMBO J 18: 2511-2521.
35. Schneider F, Neugebauer J, Griese J, Liefold N, Kutz H, et al. (2008) The viral oncoprotein LMP1 exploits TRADD for signaling by masking its apoptotic activity. PLoS Biol 6: e8 doi:10.1371/journal.pbio.0060008.
36. 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.
37. Wan J, Sun L, Mendoza JW, Chui YL, Huang DP, et al. (2004) Elucidation of the c-Jun N-terminal kinase pathway mediated by Epstein-Barr virus-encoded latent membrane protein 1. Mol Cell Biol 24: 192-199.
38. Schultheiss U, Puschner S, Kremmer E, Mak TW, Engelmann H, et al. (2001) TRAF6 is a critical mediator of signal transduction by the viral oncogene latent membrane protein 1. EMBO J 20: 5678-5691.
39. Wan J, Zhang W, Wu L, Bai T, Zhang M, et al. (2006) BS69, a specific adaptor in the latent membrane protein 1-mediated c-Jun N-terminal kinase pathway. Mol Cell Biol 26: 448-456.
40. Uemura N, Kajino T, Sanjo H, Sato S, Akira S, et al. (2006) TAK1 is a component of the Epstein-Barr virus LMP1 complex and is essential for activation of JNK but not of NF-kappaB. J Biol Chem 281: 7863-7872.
41. Boehm D, Gewurz BE, Kieff E, Cahir-McFarland E, (2010) Epstein-Barr latent membrane protein 1 transformation site 2 activates NF-kappaB in the absence of NF-kappaB essential modifier residues 133-224 or 373-419. Proc Natl Acad Sci U S A 107: 18103-18108.
42. Wu L, Nakano H, Wu Z, (2006) The C-terminal activating region 2 of the Epstein-Barr virus-encoded latent membrane protein 1 activates NF-kappaB through TRAF6 and TAK1. J Biol Chem 281: 2162-2169.
43. Adhikari A, Xu M, Chen ZJ, (2007) Ubiquitin-mediated activation of TAK1 and IKK. Oncogene 26: 3214-3226.
44. Karin M, Gallagher E, (2009) TNFR signaling: ubiquitin-conjugated TRAFfic signals control stop-and-go for MAPK signaling complexes. Immunol Rev 228: 225-240.
45. Hostager BS, (2007) Roles of TRAF6 in CD40 signaling. Immunol Res 39: 105-114.
46. Xia ZP, Sun L, Chen X, Pineda G, Jiang X, et al. (2009) Direct activation of protein kinases by unanchored polyubiquitin chains. Nature 461: 114-119.
47. 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.
48. Xie P, Hostager BS, Bishop GA, (2004) Requirement for TRAF3 in signaling by LMP1 but not CD40 in B lymphocytes. J Exp Med 199: 661-671.
49. Henriquez NV, Floettmann E, Salmon M, Rowe M, Rickinson AB, (1999) Differential responses to CD40 ligation among Burkitt lymphoma lines that are uniformly responsive to Epstein-Barr virus latent membrane protein 1. J Immunol 162: 3298-3307.
50. Hsing Y, Bishop GA, (1999) Requirement for nuclear factor-kappaB activation by a distinct subset of CD40-mediated effector functions in B lymphocytes. J Immunol 162: 2804-2811.
51. Lomaga MA, Yeh WC, Sarosi I, Duncan GS, Furlonger C, et al. (1999) TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev 13: 1015-1024.
52. Takaesu G, Kishida S, Hiyama A, Yamaguchi K, Shibuya H, et al. (2000) TAB2, a novel adaptor protein, mediates activation of TAK1 MAPKKK by linking TAK1 to TRAF6 in the IL-1 signal transduction pathway. Mol Cell 5: 649-658.
53. Grech AP, Amesbury M, Chan T, Gardam S, Basten A, et al. (2004) TRAF2 differentially regulates the canonical and noncanonical pathways of NF-kappaB activation in mature B cells. Immunity 21: 629-642.
54. Hostager BS, Haxhinasto SA, Rowland SL, Bishop GA, (2003) Tumor necrosis factor receptor-associated factor 2 (TRAF2)-deficient B lymphocytes reveal novel roles for TRAF2 in CD40 signaling. J Biol Chem 278: 45382-45390.
55. Wang C, Deng L, Hong M, Akkaraju GR, Inoue J, et al. (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412: 346-351.
56. Kyriakis JM, (1999) Signaling by the germinal center kinase family of protein kinases. J Biol Chem 274: 5259-5262.
57. Webb N, Connolly G, Tellam J, Yap AS, Khanna R, (2008) Epstein-Barr virus associated modulation of Wnt pathway is not dependent on latent membrane protein-1. PLoS ONE 3: e3254 doi:10.1371/journal.pone.0003254.
58. Satow R, Shitashige M, Jigami T, Honda K, Ono M, et al. (2010) Traf2- and Nck-interacting kinase is essential for canonical Wnt signaling in Xenopus axis formation. J Biol Chem 285: 26289-26294.
59. Siebenlist U, Brown K, Claudio E, (2005) Control of lymphocyte development by nuclear factor-kappaB. Nat Rev Immunol 5: 435-445.
60. Jost PJ, Ruland J, (2007) Aberrant NF-kappaB signaling in lymphoma: mechanisms, consequences, and therapeutic implications. Blood 109: 2700-2707.
61. Platanias LC, (2003) Map kinase signaling pathways and hematologic malignancies. Blood 101: 4667-4679.
62. Eliopoulos AG, Young LS, (2004) The role of the CD40 pathway in the pathogenesis and treatment of cancer. Curr Opin Pharmacol 4: 360-367.
63. Cahir-McFarland ED, Izumi KM, Mosialos G, (1999) Epstein-Barr virus transformation: involvement of latent membrane protein 1-mediated activation of NF-kappaB. Oncogene 18: 6959-6964.
64. Baxendale AJ, Dawson CW, Stewart SE, Mudaliar V, Reynolds G, et al. (2005) Constitutive activation of the CD40 pathway promotes cell transformation and neoplastic growth. Oncogene 24: 7913-7923.
65. Kavathas P, Bach FH, DeMars R, (1980) Gamma ray-induced loss of expression of HLA and glyoxalase I alleles in lymphoblastoid cells. Proc Natl Acad Sci U S A 77: 4251-4255.
66. Kempkes B, Spitkovsky D, Jansen-Durr P, Ellwart JW, Kremmer E, et al. (1995) B-cell proliferation and induction of early G1-regulating proteins by Epstein-Barr virus mutants conditional for EBNA2. EMBO J 14: 88-96.
67. Marchini A, Longnecker R, Kieff E, (1992) Epstein-Barr virus (EBV)-negative B-lymphoma cell lines for clonal isolation and replication of EBV recombinants. J Virol 66: 4972-4981.
68. Dirmeier U, Neuhierl B, Kilger E, Reisbach G, Sandberg ML, et al. (2003) Latent membrane protein 1 is critical for efficient growth transformation of human B cells by Epstein-Barr virus. Cancer Res 63: 2982-2989.
69. Nicholls J, Hahn P, Kremmer E, Frohlich T, Arnold GJ, et al. (2004) Detection of wild type and deleted latent membrane protein 1 (LMP1) of Epstein-Barr virus in clinical biopsy material. J Virol Methods 116: 79-88.
70. Kieser A, (2001) Assaying the activity of kinases regulated by LMP1. Methods Mol Biol 174: 325-336.