Aberrant NF-κB signaling in lymphoma: Mechanisms, consequences, and therapeutic implications

Blood

Volumn 109, Issue 7, 2007, Pages 2700-2707

  Jost, Philipp J ^a   Ruland, Jürgen ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ONCOPROTEIN; VIRUS PROTEIN;

APOPTOSIS; B CELL LYMPHOMA; B LYMPHOCYTE; CANCER GROWTH; CELL CYCLE; CELL MATURATION; CELL SURVIVAL; CHROMOSOME TRANSLOCATION; DOWN REGULATION; DRUG TARGETING; HODGKIN DISEASE; HUMAN; IMMUNE RESPONSE; LARGE CELL LYMPHOMA; LYMPHOCYTE PROLIFERATION; LYMPHOMA CELL; MOLECULAR BIOLOGY; MUCOSA ASSOCIATED LYMPHOID TISSUE LYMPHOMA; OUTCOME ASSESSMENT; PATHOGENESIS; PRIMARY EFFUSION LYMPHOMA; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; T CELL LYMPHOMA; T LYMPHOCYTE; VALIDATION STUDY; BIOLOGICAL MODEL; GENE TRANSLOCATION; GENETICS; LYMPHOCYTE; LYMPHOMA; PATHOPHYSIOLOGY; PHYSIOLOGY; PROGNOSIS;

HODGKIN DISEASE; HUMANS; LEUKEMIA-LYMPHOMA, T-CELL, ACUTE, HTLV-I-ASSOCIATED; LYMPHOCYTES; LYMPHOMA; LYMPHOMA, B-CELL; LYMPHOMA, LARGE-CELL, DIFFUSE; LYMPHOMA, MUCOSA-ASSOCIATED LYMPHOID TISSUE; MODELS, BIOLOGICAL; NF-KAPPA B; ONCOGENE PROTEINS, VIRAL; PROGNOSIS; SIGNAL TRANSDUCTION; TRANSLOCATION, GENETIC;

EID: 33947586159     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-07-025809     Document Type: Review

References (96)

1. Hayden MS, Ghosh S. Signaling to NF-kappaB. Genes Dev. 2004;18:2195-2224.
2. Bonizzi G, Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 2004;25:280-288.
3. Ruland J, Mak TW. From antigen to activation: specific signal transduction pathways linking antigen receptors to NF-kappaB. Semin Immunol. 2003;15:177-183.
4. Li Q, Verma IM. NF-kappaB regulation in the immune system. Nat Rev Immunol. 2002;2:725-734.
5. Hinz M, Krappmann D, Eichten A, Heder A, Scheidereit C, Strauss M. NF-kappaB function in growth control: regulation of cyclin D1 expression and G0/G1-to-S-phase transition. Mol Cell Biol. 1999;19:2690-2698.
6. Toth CR, Hostutler RF, Baldwin AS Jr, Bender TP. Members of the nuclear factor kappa B family transactivate the murine c-myb gene. J Biol Chem. 1995;270:7661-7671.
7. Duyao MP, Kessler DJ, Spicer DB, et al. Transactivation of the c-myc promoter by human T cell leukemia virus type 1 tax is mediated by NF kappa B. J Biol Chem. 1992;267:16288-16291.
8. Romashkova JA, Makarov SS. NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature. 1999;401:86-90.
9. Karin M, Lin A. NF-kappaB at the crossroads of life and death. Nat Immunol. 2002;3:221-227.
10. Thome M, Tschopp J. Regulation of lymphocyte proliferation and death by FLIP. Nat Rev Immunol. 2001;1:50-58.
11. Sasaki Y, Derudder E, Hobeika E, et al. Canonical NF-kappaB activity, dispensable for B cell development, replaces BAFF-receptor signals and promotes B cell proliferation upon activation. Immunity. 2006;24:729-739.
12. Gilmore TD. Multiple mutations contribute to the oncogenicity of the retroviral oncoprotein v-Rel. Oncogene. 1999;18:6925-6937.
13. Kuppers R, Schwering I, Brauninger A, Rajewsky K, Hansmann ML. Biology of Hodgkin's lymphoma. Ann Oncol. 2002;13(suppl 1):11-18.
14. Kanzler H, Kuppers R, Hansmann ML, Rajewsky K. Hodgkin and Reed-Sternberg cells in Hodgkin's disease represent the outgrowth of a dominant tumor clone derived from (crippled) germinal center B cells. J Exp Med. 1996;184:1495-1505.
15. Kraus M, Alimzhanov MB, Rajewsky N, Rajewsky K. Survival of resting mature B lymphocytes depends on BCR signaling via the Igalpha/beta heterodimer. Cell. 2004;117:787-800.
16. Bargou RC, Leng C, Krappmann D, et al. High-level nuclear NF-kappa B and Oct-2 is a common feature of cultured Hodgkin/Reed-Sternberg cells. Blood. 1996;87:4340-4347.
17. Bargou RC, Emmerich F, Krappmann D, et al. Constitutive nuclear factor-kappaB-RelA activation is required for proliferation and survival of Hodgkin's disease tumor cells. J Clin Invest. 1997;100:2961-2969.
18. Krappmann D, Emmerich F, Kordes U, Scharschmidt E, Dorken B, Scheidereit C. Molecular mechanisms of constitutive NF-kappaB/Rel activation in Hodgkin/Reed-Sternberg cells. Oncogene. 1999;18:943-953.
19. Bishop GA. The multifaceted roles of TRAFs in the regulation of B-cell function. Nat Rev Immunol. 2004;4:775-786.
20. Horie R, Watanabe T, Morishita Y, et al. Ligand-independent signaling by overexpressed CD30 drives NF-kappaB activation in Hodgkin-Reed-Sternberg cells. Oncogene. 2002;21:2493-2503.
21. Horie R, Watanabe T, Ito K, et al. Cytoplasmic aggregation of TRAF2 and TRAF5 proteins in the Hodgkin-Reed-Sternberg cells. Am J Pathol. 2002;160:1647-1654.
22. Hauer J, Puschner S, Ramakrishnan P, et al. TNF receptor (TNFR)-associated factor (TRAF) 3 serves as an inhibitor of TRAF2/5-mediated activation of the noncanonical NF-kappaB pathway by TRAF-binding TNFRs. Proc Natl Acad Sci U S A. 2005;102:2874-2879.
23. Fiumara P, Snell V, Li Y, et al. Functional expression of receptor activator of nuclear factor kappaB in Hodgkin disease cell lines. Blood. 2001;98:2784-2790.
24. Darnay BG, Haridas V, Ni J, Moore PA, Aggarwal BB. Characterization of the intracellular domain of receptor activator of NF-kappaB (RANK). Interaction with tumor necrosis factor receptor-associated factors and activation of NF-kappab and c-Jun N-terminal kinase. J Biol Chem. 1998;273:20551-20555.
25. GrechAP, Amesbury M, Chan T, Gardam S, Basten A, Brink R. TRAF2 differentially regulates the canonical and noncanonical pathways of NF-kappaB activation in mature B cells. Immunity. 2004;21:629-642.
26. Deacon EM, Pallesen G, Niedobitek G, et al. Epstein-Barr virus and Hodgkin's disease: transcriptional analysis of virus latency in the malignant cells. J Exp Med. 1993;177:339-349.
27. Eliopoulos AG, Caamano JH, Flavell J, et al. 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. 2003;22:7557-7569.
28. Cabannes E, Khan G, Aillet F, Jarrett RF, Hay RT. Mutations in the IkBa gene in Hodgkin's disease suggest a tumour suppressor role for IkappaBalpha. Oncogene. 1999;18:3063-3070.
29. Emmerich F, Theurich S, Hummel M, et al. Inactivating I kappa B epsilon mutations in Hodgkin/Reed-Sternberg cells. J Pathol. 2003;201:413-420.
30. Jungnickel B, Staratschek-Jox A, Brauninger A, et al. Clonal deleterious mutations in the IkappaBalpha gene in the malignant cells in Hodgkin's lymphoma. J Exp Med. 2000;191:395-402.
31. Joos S, Menz CK, Wrobel G, et al. Classical Hodgkin lymphoma is characterized by recurrent copy number gains of the short arm of chromosome 2. Blood. 2002;99:1381-1387.
32. Martin-Subero JI, Gesk S, Harder L, et al. Recurrent involvement of the REL and BCL11Aloci in classical Hodgkin lymphoma. Blood. 2002;99:1474-1477.
33. Barth TF, Martin-Subero JI, Joos S, et al. Gains of 2p involving the REL locus correlate with nuclear c-Rel protein accumulation in neoplastic cells of classical Hodgkin lymphoma. Blood. 2003;101:3681-3686.
34. Mathas S, Lietz A, Janz M, et al. Inhibition of NF-kappaB essentially contributes to arsenic-induced apoptosis. Blood. 2003;102:1028-1034.
35. Farber EM. History of the treatment of psoriasis. J AmAcad Dermatol. 1992;27:640-645.
36. Zucca E, Bertoni F, Roggero E, Cavalli F. The gastric marginal zone B-cell lymphoma of MALT type. Blood. 2000;96:410-419.
37. Wotherspoon AC, Doglioni C, Diss TC, et al. Regression of primary low-grade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet. 1993;342:575-577.
38. Liu H, Ruskon-Fourmestraux A, Lavergne-Slove A, et al. Resistance of t(11;18) positive gastric mucosa-associated lymphoid tissue lymphoma to Helicobacter pylori eradication therapy. Lancet. 2001;357:39-40.
39. Willis TG, Jadayel DM, Du MQ, et al. Bcl10 is involved in t(1;14)(p22;q32) of MALT B cell lymphoma and mutated in multiple tumor types [see comments]. Cell. 1999;96:35-45.
40. Dierlamm J, Baens M, Wlodarska I, et al. The apoptosis inhibitor gene API2 and a novel 18q gene, MLT, are recurrently rearranged in the t(11;18)(q21;q21)p6ssociated with mucosa-associated lymphoid tissue lymphomas. Blood. 1999;93:3601-3609.
41. Akagi T, Motegi M, Tamura A, et al. A novel gene, MALT1 at 18q21, is involved in t(11;18) (q21;q21) found in low-grade B-cell lymphoma of mucosa-associated lymphoid tissue. Oncogene. 1999;18:5785-5794.
42. Lucas PC, Yonezumi M, Inohara N, et al. Bcl10 and MALT1, independent targets of chromosomal translocation in malt lymphoma, cooperate in a novel NF-kappa B signaling pathway. J Biol Chem. 2001;276:19012-19019.
43. Ruefli-Brasse AA, French DM, Dixit VM. Regulation of NF-kappaB-dependent lymphocyte activation and development by paracaspase. Science. 2003;302:1581-1584.
44. Ruland J, Duncan GS, Elia A, et al. Bcl10 is a positive regulator of antigen receptor-induced activation of NF-kappaB and neural tube closure. Cell. 2001;104:33-42.
45. Ruland J, Duncan GS,Wakeham A, MakTW. Differential requirement for Malt1 in T and B cell antigen receptor signaling. Immunity. 2003;19:749-758.
46. Zhou H, Wertz I, O'Rourke K, et al. Bcl10 activates the NF-kappaB pathway through ubiquitination of NEMO. Nature. 2004;427:167-171.
47. Zhou H, Du MQ, Dixit VM. Constitutive NF-kappaB activation by the t(11;18)(q21;q21) product in MALT lymphoma is linked to deregulated ubiquitin ligase activity. Cancer Cell. 2005;7:425-431.
48. Varfolomeev E, Wayson SM, Dixit VM, Fairbrother WJ, Vucic D. The inhibitor of apoptosis protein fusion c-IAP2.MALT1 stimulates NF-kappaB activation independently of TRAF1 AND TRAF2. J Biol Chem. 2006;281:29022-29029.
49. Streubel B, Vinatzer U, Lamprecht A, Raderer M, Chott A. T(3;14)(p14.1;q32) involving IGH and FOXP1 is a novel recurrent chromosomal aberration in MALT lymphoma. Leukemia. 2005;19:652-658.
50. Vargha-Khadem F, Gadian DG, Copp A, Mishkin M. FOXP2 and the neuroanatomy of speech and language. Nat Rev Neurosci. 2005;6:131-138.
51. Wu Y, Borde M, Heissmeyer V, et al. FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell. 2006;126:375-387.
52. Bettelli E, Dastrange M, Oukka M. Foxp3 interacts with nuclear factor of activated T cells and NF-kappa B to repress cytokine gene expression and effector functions of T helper cells. Proc Natl Acad Sci U S A. 2005;102:5138-5143.
53. Bernal-Mizrachi L, Lovly CM, Ratner L. The role of NF-{kappa}B-1 and NF-{kappa}B-2-mediated resistance to apoptosis in lymphomas. Proc Natl Acad Sci U S A. 2006;103:9220-9225.
54. Wright G, Tan B, Rosenwald A, Hurt EH, Wiestner A, Staudt LM. A gene expression-based method to diagnose clinically distinct subgroups of diffuse large B cell lymphoma. Proc Natl Acad Sci U S A. 2003;100:9991-9996.
55. Alizadeh AA, Eisen MB, Davis RE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000;403:503-511.
56. Rosenwald A, Wright G, Chan WC, et al. The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N Engl J Med. 2002;346:1937-1947.
57. Davis RE, Brown KD, Siebenlist U, Staudt LM. Constitutive nuclear factor kappaB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J Exp Med. 2001;194:1861-1874.
58. Takahashi H, Feuerhake F, Monti S, Kutok JL, Aster JC, Shipp MA. Lack of IKBA coding region mutations in primary mediastinal large B-cell lymphoma and the host response subtype of diffuse large B-cell lymphoma. Blood. 2006;107:844-845.
59. Thomas RK, Wickenhauser C, Tawadros S, et al. Mutational analysis of the IkappaBalpha gene in activated B cell-like diffuse large B-cell lymphoma. Br J Haematol. 2004;126:50-54.
60. Lam LT, Davis RE, Pierce J, et al. Small molecule inhibitors of IkappaB kinase are selectively toxic for subgroups of diffuse large B-cell lymphoma defined by gene expression profiling. Clin Cancer Res. 2005;11:28-40.
61. Ngo VN, Davis RE, Lamy L, et al. A loss-of-function RNA interference screen for molecular targets in cancer. Nature. 2006;441:106-10.
62. Staudt LM. Molecular diagnosis of the hematologic cancers. N Engl J Med. 2003;348:1777-1785.
63. Rosenwald A, Wright G, Leroy K, et al. Molecular diagnosis of primary mediastinal B cell lymphoma identifies a clinically favorable subgroup of diffuse large B cell lymphoma related to Hodgkin lymphoma. J Exp Med. 2003;198:851-862.
64. Neri A, Chang CC, Lombardi L, et al. B cell lymphoma-associated chromosomal translocation involves candidate oncogene lyt-10, homologous to NF-kappa B p50. Cell. 1991;67:1075-1087.
65. Ishikawa H, Carrasco D, Claudio E, Ryseck RP, Bravo R. Gastric hyperplasia and increased proliferative responses of lymphocytes in mice lacking the COOH-terminal ankyrin domain of NFkappaB2. J Exp Med. 1997;186:999-1014.
66. Rao PH, Houldsworth J, Dyomina K, et al. Chromosomal and gene amplification in diffuse large B-cell lymphoma. Blood. 1998;92:234-240.
67. Palanisamy N, Abou-Elella AA, Chaganti SR, et al. Similar patterns of genomic alterations characterize primary mediastinal large-B-cell lymphoma and diffuse large-B-cell lymphoma. Genes Chromosomes Cancer. 2002;33:114-122.
68. Cesarman E, Chang Y, Moore PS, Said JW, Knowles DM. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med. 1995;332:1186-1191.
69. Horenstein MG, Nador RG, Chadburn A, et al. Epstein-Barr virus latent gene expression in primary effusion lymphomas containing Kaposi's sarcoma-associated herpesvirus/human herpesvirus-8. Blood. 1997;90:1186-1191.
70. Chaudhary PM, Jasmin A, Eby MT, Hood L. Modulation of the NF-kappa B pathway by virally encoded death effector domains-containing proteins. Oncogene. 1999;18:5738-5746.
71. Guasparri I, Keller SA, Cesarman E. KSHV vFLIP is essential for the survival of infected lymphoma cells. J Exp Med. 2004;199:993-1003.
72. Djerbi M, Screpanti V, Catrina AI, Bogen B, Biberfeld P, Grandien A. The inhibitor of death receptor signaling, FLICE-inhibitory protein defines a new class of tumor progression factors. J Exp Med. 1999;190:1025-1032.
73. Liu L, Eby MT, Rathore N, Sinha SK, Kumar A, Chaudhary PM. The human herpes virus 8-encoded viral FLICE inhibitory protein physically associates with and persistently activates the Ikappa B kinase complex. J Biol Chem. 2002;277:13745-13751.
74. Keller SA, Schattner EJ, Cesarman E. Inhibition of NF-kappaB induces apoptosis of KSHV-infected primary effusion lymphoma cells. Blood. 2000;96:2537-2542.
75. Poiesz BJ, Ruscetti FW, Reitz MS, Kalyanaraman VS, Gallo RC. Isolation of a new type C retrovirus (HTLV) in primary uncultured cells of a patient with Sezary T-cell leukaemia. Nature. 1981;294:268-271.
76. Cann AJ, Rosenblatt JD, Wachsman W, Shah NP, Chen IS. Identification of the gene responsible for human T-cell leukaemia virus transcriptional regulation. Nature. 1985;318:571-574.
77. Ross TM, Pettiford SM, Green PL. The tax gene of human T-cell leukemia virus type 2 is essential for transformation of human T lymphocytes. J Virol. 1996;70:5194-5202.
78. Rosin O, Koch C, Schmitt I, Semmes OJ, Jeang KT, Grassmann R. A human T-cell leukemia virus Tax variant incapable of activating NF-kappaB retains its immortalizing potential for primary Tlymphocytes. J Biol Chem. 1998;273:6698-6703.
79. Tanaka A, Takahashi C, Yamaoka S, Nosaka T, Maki M, Hatanaka M. Oncogenic transformation by the tax gene of human T-cell leukemia virus type I in vitro. Proc Natl Acad Sci U SA. 1990;87:1071-1075.
80. Grossman WJ, Kimata JT, Wong FH, Zutter M, Ley TJ, Ratner L. Development of leukemia in mice transgenic for the tax gene of human T-cell leukemia virus type I. Proc Natl Acad Sci U S A. 1995;92:1057-1061.
81. Hasegawa H, Sawa H, Lewis MJ, et al. Thymus-derived leukemia-lymphoma in mice transgenic for the Tax gene of human T-lymphotropic virus type I. Nat Med. 2006;12:466-472.
82. Carter RS, Geyer BC, Xie M, Acevedo-Suarez CA, Ballard DW. Persistent activation of NF-kappa B by the tax transforming protein involves chronic phosphorylation of IkappaB kinase subunits IKKbeta and IKKgamma. J Biol Chem. 2001;276:24445-24448.
83. Sun SC, Ballard DW. Persistent activation of NF-kappaB by the tax transforming protein of HTLV-1: hijacking cellular IkappaB kinases. Oncogene. 1999;18:6948-6958.
84. Xiao G, Cvijic ME, Fong A, et al. Retroviral oncoprotein Tax induces processing of NF-kappaB2/p100 in T cells: evidence for the involvement of IKKalpha. EMBO J. 2001;20:6805-6815.
85. Beraud C, Sun SC, Ganchi P, BallardDW, Greene WC. Human T-cell leukemia virus type I Tax associates with and is negatively regulated by the NF-kappa B2 p100 gene product: implications for viral latency. Mol Cell Biol. 1994;14:1374-1382.
86. Yin MJ, Christerson LB, Yamamoto Y, et al. HTLV-I Tax protein binds to MEKK1 to stimulate IkappaB kinase activity and NF-kappaB activation. Cell. 1998;93:875-884.
87. Ballard DW, Bohnlein E, Lowenthal JW, Wano Y, Franza BR, Greene WC. HTLV-I tax induces cellular proteins that activate the kappa B element in the IL-2 receptor alpha gene. Science. 1988;241:1652-1655.
88. Siekevitz M, Feinberg MB, Holbrook N, Wong-Staal F, Greene WC. Activation of interleukin 2 and interleukin 2 receptor (Tac) promoter expression by the trans-activator (tat) gene product of human T-cell leukemia virus, type I. Proc Natl Acad Sci U S A. 1987;84:5389-5393.
89. Cross SL, Feinberg MB,Wolf JB, Holbrook NJ, Wong-Staal F, Leonard WJ. Regulation of the human interleukin-2 receptor alpha chain promoter: activation of a nonfunctional promoter by the transactivator gene of HTLV-I. Cell. 1987;49:47-56.
90. Mori N, Yamada Y, Ikeda S, et al. Bay 11-7082 inhibits transcription factor NF-kappaB and induces apoptosis of HTLV-I-infected T-cell lines and primary adult T-cell leukemia cells. Blood. 2002;100:1828-1834.
91. Hideshima T, Anderson KC. Molecular mechanisms of novel therapeutic approaches for multiple myeloma. Nat Rev Cancer. 2002;2:927-937.
92. Hideshima T, Chauhan D, Hayashi T, et al. Proteasome inhibitor PS-341 abrogates IL-6 triggered signaling cascades via caspase-dependent downregulation of gp130 in multiple myeloma. Oncogene. 2003;22:8386-8393.
93. Richardson PG, Sonneveld P, SchusterMW, et al. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N Engl J Med. 2005;352:2487-2498.
94. Mitsiades CS, Mitsiades N, Hideshima T, Richardson PG, Anderson KC. Proteasome inhibition as a new therapeutic principle in hematological malignancies. Curr Drug Targets. 2006;7:1341-1347.
95. Wang M, Zhou Y, Zhang L, Nguyen CA, Romaguera J. Use of bortezomib in B-cell non-Hodgkin's lymphoma. Expert Rev Anticancer Ther. 2006;6:983-991.
96. Janssens S, Tschopp J. Signals from within: the DNA-damage-induced NF-kappaB response. Cell Death Differ. 2006;13:773-784.