The TRAF3 adaptor protein drives proliferation of anaplastic large cell lymphoma cells by regulating multiple signaling pathways

Cell Cycle

Volumn 13, Issue 12, 2014, Pages 1918-1927

  Muro, Israel ^a   Fang, Gloria ^a   Gardella, KacieA ^a   Mahajan, IndraM ^a   Wright, Casey W ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

JAK STAT; NF B; NIK; PI3K AKT; TRAF3

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3;

ANIMAL CELL; ARTICLE; CELL CYCLE PROGRESSION; CELL DIVISION; CELL GROWTH; CELL MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; G1 PHASE CELL CYCLE CHECKPOINT; IMMUNOBLOTTING; LARGE CELL LYMPHOMA; LYMPHOMA CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; T LYMPHOCYTE; WESTERN BLOTTING; HUMAN; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL PROLIFERATION; HUMANS; LYMPHOMA, LARGE-CELL, ANAPLASTIC; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TNF RECEPTOR-ASSOCIATED FACTOR 3;

EID: 84902438993     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.28895     Document Type: Article

References (50)

1. Sen R, Baltimore D. Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslational mechanism. Cell 1986; 47:921-8; PMID:3096580; http://dx.doi.org/10.1016/0092-8674(86)90807-X
2. Hayden MS, Ghosh S. NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev 2012; 26:203-34; PMID:22302935; http://dx.doi.org/10.1101/gad.183434.111
3. Karin M, Cao Y, Greten FR, Li ZWNF. NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer 2002; 2:301-10; PMID:12001991; http://dx.doi.org/10.1038/nrc780
4. Beg AA, Ruben SM, Scheinman RI, Haskill S, Rosen CA, Baldwin ASJ Jr. I kappa B interacts with the nuclear localization sequences of the subunits of NF-kappa B: a mechanism for cytoplasmic retention. Genes Dev 1992; 6:1899-913; PMID:1340770; http://dx.doi.org/10.1101/gad.6.10.1899
5. Ganchi PA, Sun SC, Greene WC, Ballard DW. I kappa B/MAD-3 masks the nuclear localization signal of NF-kappa B p65 and requires the transactivation domain to inhibit NF-kappa B p65 DNA binding. Mol Biol Cell 1992; 3:1339-52; PMID:1493333; http://dx.doi.org/10.1091/mbc.3.12.1339
6. Basak S, Kim H, Kearns JD, Tergaonkar V, O'Dea E, Werner SL, Benedict CA, Ware CF, Ghosh G, Verma IM, et al. A fourth IkappaB protein within the NF-kappaB signaling module. Cell 2007; 128:369-81; PMID:17254973; http://dx.doi.org/10.1016/j.cell.2006.12.033
7. Oeckinghaus A, Hayden MS, Ghosh S. Crosstalk in NF-κB signaling pathways. Nat Immunol 2011; 12:695-708; PMID:21772278; http://dx.doi.org/10. 1038/ni.2065
8. Sun SC. The noncanonical NF-κB pathway. Immunol Rev 2012; 246:125-40; PMID:22435551; http://dx.doi.org/10.1111/j.1600-065X.2011.01088.x
9. Leung K, Betts JC, Xu L, Nabel GJ. The cytoplasmic domain of the interleukin-1 receptor is required for nuclear factor-kappa B signal transduction. J Biol Chem 1994; 269:1579-82; PMID:8294399
10. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004; 5:730-7; PMID:15208624; http://dx.doi.org/10.1038/ni1087
11. Pfeffer K, Matsuyama T, Kündig TM, Wakeham A, Kishihara K, Shahinian A, Wiegmann K, Ohashi PS, Krönke M, Mak TW. Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell 1993; 73:457-67; PMID:8387893; http://dx.doi.org/10.1016/0092-8674(93)90134-C
12. Ak P, Levine AJ. p53 and NF-κB: different strategies for responding to stress lead to a functional antagonism. FASEB J 2010; 24:3643-52; PMID:20530750; http://dx.doi.org/10.1096/fj.10-160549
13. Wright CW, Rumble JM, Duckett CS. CD30 activates both the canonical and alternative NF-kappaB pathways in anaplastic large cell lymphoma cells. J Biol Chem 2007; 282:10252-62; PMID:17261581; http://dx.doi.org/10.1074/jbc.M608817200
14. Morrison MD, Reiley W, Zhang M, Sun SC. An atypical tumor necrosis factor (TNF) receptor-associated factor-binding motif of B cell-activating factor belonging to the TNF family (BAFF) receptor mediates induction of the noncanonical NF-kappaB signaling pathway. J Biol Chem 2005; 280:10018-24; PMID:15644327; http://dx.doi.org/10.1074/jbc.M413634200
15. Bista P, Zeng W, Ryan S, Bailly V, Browning JL, Lukashev ME. TRAF3 controls activation of the canonical and alternative NFkappaB by the lymphotoxin beta receptor. J Biol Chem 2010; 285:12971-8; PMID:20185819; http://dx.doi.org/10.1074/jbc.M109.076091
16. Uhlik M, Good L, Xiao G, Harhaj EW, Zandi E, Karin M, Sun SC. NF-kappaB-inducing kinase and IkappaB kinase participate in human T-cell leukemia virus I Tax-mediated NF-kappaB activation. J Biol Chem 1998; 273:21132-6; PMID:9694868; http://dx.doi.org/10.1074/jbc.273.33.21132
17. Vallabhapurapu S, Matsuzawa A, Zhang W, Tseng PH, Keats JJ, Wang H, Vignali DA, Bergsagel PL, Karin M. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat Immunol 2008; 9:1364-70; PMID:18997792; http://dx.doi.org/10.1038/ni.1678
18. Liao G, Zhang M, Harhaj EW, Sun SC. Regulation of the NF-kappaB-inducing kinase by tumor necrosis factor receptor-associated factor 3-induced degradation. J Biol Chem 2004; 279:26243-50; PMID:15084608; http://dx.doi.org/ 10.1074/jbc.M403286200
19. Xu Y, Cheng G, Baltimore D. Targeted disruption of TRAF3 leads to postnatal lethality and defective T-dependent immune responses. Immunity 1996; 5:407-15; PMID:8934568; http://dx.doi.org/10.1016/S1074-7613(00)80497-5
20. Xie P, Stunz LL, Larison KD, Yang B, Bishop GA. Tumor necrosis factor receptor-associated factor 3 is a critical regulator of B cell homeostasis in secondary lymphoid organs. Immunity 2007; 27:253-67; PMID:17723217; http://dx.doi.org/10.1016/j.immuni.2007.07.012
21. Gardam S, Sierro F, Basten A, Mackay F, Brink R. TRAF2 and TRAF3 signal adapters act cooperatively to control the maturation and survival signals delivered to B cells by the BAFF receptor. Immunity 2008; 28:391-401; PMID:18313334; http://dx.doi.org/10.1016/j.immuni.2008.01.009
22. Xie P, Kraus ZJ, Stunz LL, Liu Y, Bishop GA. TNF receptor-associated factor 3 is required for T cell-mediated immunity and TCR/CD28 signaling. J Immunol 2011; 186:143-55; PMID:21084666; http://dx.doi.org/10.4049/jimmunol. 1000290
23. Keats JJ, Fonseca R, Chesi M, Schop R, Baker A, Chng WJ, Van Wier S, Tiedemann R, Shi CX, Sebag M, et al. Promiscuous mutations activate the noncanonical NF-kappaB pathway in multiple myeloma. Cancer Cell 2007; 12:131-44; PMID:17692805; http://dx.doi.org/10.1016/j.ccr.2007.07.003
24. Otto C, Giefing M, Massow A, Vater I, Gesk S, Schlesner M, Richter J, Klapper W, Hansmann ML, Siebert R, et al. Genetic lesions of the TRAF3 and MAP3K14 genes in classical Hodgkin lymphoma. Br J Haematol 2012; 157:702-8; PMID:22469134; http://dx.doi.org/10.1111/j.1365-2141.2012.09113.x
25. Rossi D, Deaglio S, Dominguez-Sola D, Rasi S, Vaisitti T, Agostinelli C, Spina V, Bruscaggin A, Monti S, Cerri M, et al. Alteration of BIRC3 and multiple other NF-κB pathway genes in splenic marginal zone lymphoma. Blood 2011; 118:4930-4; PMID:21881048; http://dx.doi.org/10.1182/blood-2011-06-359166
26. Moore CR, Liu Y, Shao C, Covey LR, Morse HC 3rd, Xie P. Specific deletion of TRAF3 in B lymphocytes leads to B-lymphoma development in mice. Leukemia 2012; 26:1122-7; PMID:22033491; http://dx.doi.org/10.1038/leu.2011.309
27. Mercurio F, Didonato J, Rosette C, Karin M. Molecular cloning and characterization of a novel Rel/NF-kappa B family member displaying structural and functional homology to NF-kappa B p50/p105. DNA Cell Biol 1992; 11:523-37; PMID:1388725; http://dx.doi.org/10.1089/dna.1992.11.523
28. Annunziata CM, Davis RE, Demchenko Y, Bellamy W, Gabrea A, Zhan F, Lenz G, Hanamura I, Wright G, Xiao W, et al. Frequent engagement of the classical and alternative NF-kappaB pathways by diverse genetic abnormalities in multiple myeloma. Cancer Cell 2007; 12:115-30; PMID:17692804; http://dx.doi.org/10.1016/ j.ccr.2007.07.004
29. Demchenko YN, Glebov OK, Zingone A, Keats JJ, Bergsagel PL, Kuehl WM. Classical and/or alternative NF-kappaB pathway activation in multiple myeloma. Blood 2010; 115:3541-52; PMID:20053756; http://dx.doi.org/10.1182/blood-2009-09- 243535
30. DiDonato JA, Mercurio F, Karin M. Phosphorylation of I kappa B alpha precedes but is not sufficient for its dissociation from NF-kappa B. Mol Cell Biol 1995; 15:1302-11; PMID:7862124
31. Marienfeld R, May MJ, Berberich I, Serfling E, Ghosh S, Neumann M. RelB forms transcriptionally inactive complexes with RelA/p65. J Biol Chem 2003; 278:19852-60; PMID:12657634; http://dx.doi.org/10.1074/jbc.M301945200
32. Xiao G, Harhaj EW, Sun SCNF. NF-kappaB-inducing kinase regulates the processing of NF-kappaB2 p100. Mol Cell 2001; 7:401-9; PMID:11239468; http://dx.doi.org/10.1016/S1097-2765(01)00187-3
33. Akiba H, Nakano H, Nishinaka S, Shindo M, Kobata T, Atsuta M, Morimoto C, Ware CF, Malinin NL, Wallach D, et al. CD27, a member of the tumor necrosis factor receptor superfamily, activates NF-kappaB and stress-activated protein kinase/c-Jun N-terminal kinase via TRAF2, TRAF5, and NF-kappaB-inducing kinase. J Biol Chem 1998; 273:13353-8; PMID:9582383; http://dx.doi.org/10.1074/jbc.273. 21.13353
34. Dhawan P, Richmond A. A novel NF-kappa B-inducing kinase-MAPK signaling pathway up-regulates NF-kappa B activity in melanoma cells. J Biol Chem 2002; 277:7920-8; PMID:11773061; http://dx.doi.org/10.1074/jbc.M112210200
35. Nadiminty N, Chun JY, Hu Y, Dutt S, Lin X, Gao AC. LIGHT, a member of the TNF superfamily, activates Stat3 mediated by NIK pathway. Biochem Biophys Res Commun 2007; 359:379-84; PMID:17543278; http://dx.doi.org/10.1016/j.bbrc.2007. 05.119
36. Hemmings BA, Restuccia DF. PI3K-PKB/Akt pathway. Cold Spring Harb Perspect Biol 2012; 4:a011189; PMID:22952397; http://dx.doi.org/10.1101/ cshperspect.a011189
37. Franke TF, Kaplan DR, Cantley LC, Toker A. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 1997; 275:665-8; PMID:9005852; http://dx.doi.org/10.1126/science.275.5300.665
38. Song MS, Salmena L, Pandolfi PP. The functions and regulation of the PTEN tumour suppressor. Nat Rev Mol Cell Biol 2012; 13:283-96; PMID:22473468
39. Stambolic V, Suzuki A, de la Pompa JL, Brothers GM, Mirtsos C, Sasaki T, Ruland J, Penninger JM, Siderovski DP, Mak TW. Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 1998; 95:29-39; PMID:9778245; http://dx.doi.org/10.1016/S0092-8674(00)81780-8
40. Tamura M, Gu J, Danen EH, Takino T, Miyamoto S, Yamada KM. PTEN interactions with focal adhesion kinase and suppression of the extracellular matrix-dependent phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem 1999; 274:20693-703; PMID:10400703; http://dx.doi.org/10.1074/jbc.274.29. 20693
41. Lee JO, Yang H, Georgescu MM, Di Cristofano A, Maehama T, Shi Y, Dixon JE, Pandolfi P, Pavletich NP. Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 1999; 99:323-34; PMID:10555148; http://dx.doi.org/10.1016/ S0092-8674(00)81663-3
42. Wang X, Huang Y, Li L, Wei Q. TRAF3 negatively regulates calcineurin-NFAT pathway by targeting calcineurin B subunit for degradation. IUBMB Life 2012; 64:748-56; PMID:22715070; http://dx.doi.org/10.1002/iub.1060
43. Lu LF, Gondek DC, Scott ZA, Noelle RJNF. NF kappa B-inducing kinase deficiency results in the development of a subset of regulatory T cells, which shows a hyperproliferative activity upon glucocorticoid-induced TNF receptor family-related gene stimulation. J Immunol 2005; 175:1651-7; PMID:16034105
44. Casares N, Rudilla F, Arribillaga L, Llopiz D, Riezu- Boj JI, Lozano T, López-Sagaseta J, Guembe L, Sarobe P, Prieto J, et al. A peptide inhibitor of FOXP3 impairs regulatory T cell activity and improves vaccine efficacy in mice. J Immunol 2010; 185:5150-9; PMID:20870946; http://dx.doi.org/10.4049/jimmunol.1001114
45. Kasprzycka M, Marzec M, Liu X, Zhang Q, Wasik MA. Nucleophosmin/ anaplastic lymphoma kinase (NPM/ALK) oncoprotein induces the T regulatory cell phenotype by activating STAT3. Proc Natl Acad Sci U S A 2006; 103:9964-9; PMID:16766651; http://dx.doi.org/10.1073/pnas.0603507103
46. Wolke C, Tadje J, Bukowska A, Täger M, Bank U, Ittenson A, Ansorge S, Lendeckel U. Assigning the phenotype of a natural regulatory T-cell to the human T-cell line, KARPAS-299. Int J Mol Med 2006; 17:275-8; PMID:16391826
47. Leventaki V, Drakos E, Medeiros LJ, Lim MS, Elenitoba-Johnson KS, Claret FX, Rassidakis GZ. NPM-ALK oncogenic kinase promotes cell-cycle progression through activation of JNK/cJun signaling in anaplastic large-cell lymphoma. Blood 2007; 110:1621-30; PMID:17416736; http://dx.doi.org/10.1182/blood-2006-11- 059451
48. Chetoui N, Boisvert M, Gendron S, Aoudjit F. Interleukin-7 promotes the survival of human CD4+ effector/memory T cells by up-regulating Bcl-2 proteins and activating the JAK/STAT signalling pathway. Immunology 2010; 130:418-26; PMID:20465565; http://dx.doi.org/10.1111/j.1365-2567.2009.03244.x
49. Patel ES, Chang LJ. Synergistic effects of interleukin-7 and pre-T cell receptor signaling in human T cell development. J Biol Chem 2012; 287:33826-35; PMID:22859301; http://dx.doi.org/10.1074/jbc.M112.380113
50. Johnson SE, Shah N, Bajer AA, LeBien TW. IL-7 activates the phosphatidylinositol 3-kinase/AKT pathway in normal human thymocytes but not normal human B cell precursors. J Immunol 2008; 180:8109-17; PMID:18523275