NF-κB inducing kinase: A key regulator in the immune system and in cancer

Cytokine and Growth Factor Reviews

Volumn 21, Issue 4, 2010, Pages 213-226

  Thu, Yee Mon ^a   Richmond, A ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Canonical pathway; IKK; NF B; NF B inducing kinase (NIK); Non canonical pathway

Indexed keywords

CHEMOKINE; CYTOKINE; I KAPPA B KINASE; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN INDUCING KINASE; INHIBITOR OF APOPTOSIS PROTEIN 1; INHIBITOR OF APOPTOSIS PROTEIN 2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHOTRANSFERASE; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; BACTERIAL INFECTION; BONE DISEASE; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL DEATH; CELL SURVIVAL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME STABILITY; GENE CONTROL; HEMATOLOGIC MALIGNANCY; HUMAN; IMMUNOPATHOGENESIS; IMMUNOREGULATION; MALIGNANT NEOPLASTIC DISEASE; MELANOMA; MULTIPLE MYELOMA; NONHUMAN; OSTEOCLASTOGENESIS; PANCREAS CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY T LYMPHOCYTE; SOLID TUMOR; TH17 CELL; TRANSCRIPTION REGULATION; VIRUS INFECTION;

ANIMALS; HUMANS; IMMUNE SYSTEM; MICE; NEOPLASMS; NF-KAPPA B; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; SIGNAL TRANSDUCTION;

EID: 77956407149     PISSN: 13596101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2010.06.002     Document Type: Article

References (119)

1. Malinin N.L., Boldin M.P., Kovalenko A.V., Wallach D. MAP3K-related kinase involved in NF-kappaB induction by TNF, CD95 and IL-1. Nature 1997, 385:540-544.
2. Akiba H., Nakano H., Nishinaka S., Shindo M., Kobata T., Atsuta M., 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, 273:13353-13358.
3. Lin X., Mu Y., Cunningham E.T., Marcu K.B., Geleziunas R., Greene W.C. Molecular determinants of NF-kappaB-inducing kinase action. Mol Cell Biol 1998, 18:5899-5907.
4. Smith C., Andreakos E., Crawley J.B., Brennan F.M., Feldmann M., Foxwell B.M. NF-kappaB-inducing kinase is dispensable for activation of NF-kappaB in inflammatory settings but essential for lymphotoxin beta receptor activation of NF-kappaB in primary human fibroblasts. J Immunol 2001, 167:5895-5903.
5. Woronicz J.D., Gao X., Cao Z., Rothe M., Goeddel D.V. IkappaB kinase-beta: NF-kappaB activation and complex formation with IkappaB kinase-alpha and NIK. Science 1997, 278:866-869.
6. Nemoto S., DiDonato J.A., Lin A. Coordinate regulation of IkappaB kinases by mitogen-activated protein kinase kinase kinase 1 and NF-kappaB-inducing kinase. Mol Cell Biol 1998, 18:7336-7343.
7. Nakano H., Shindo M., Sakon S., Nishinaka S., Mihara M., Yagita H., et al. Differential regulation of IkappaB kinase alpha and beta by two upstream kinases, NF-kappaB-inducing kinase and mitogen-activated protein kinase/ERK kinase kinase-1. Proc Natl Acad Sci USA 1998, 95:3537-3542.
8. Sakurai H., Shigemori N., Hasegawa K., Sugita T. TGF-beta-activated kinase 1 stimulates NF-kappa B activation by an NF-kappa B-inducing kinase-independent mechanism. Biochem Biophys Res Commun 1998, 243:545-549.
9. Ninomiya-Tsuji J., Kishimoto K., Hiyama A., Inoue J., Cao Z., Matsumoto K. The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 1999, 398:252-256.
10. Pomerantz J.L., Baltimore D. NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO J 1999, 18:6694-6704.
11. Bhattacharyya S, Borthakur A, Tyagi S, Gill R, Chen ML, Dudeja PK, et al. B-cell CLL/lymphoma 10 (BCL10) is required for NF-kappaB production by both canonical and noncanonical pathways and for NF-kappaB-inducing kinase (NIK) phosphorylation. J Biol Chem 2010;285:522-30.
12. Ling L., Cao Z., Goeddel D.V. NF-kappaB-inducing kinase activates IKK-alpha by phosphorylation of Ser-176. Proc Natl Acad Sci USA 1998, 95:3792-3797.
13. Delhase M., Hayakawa M., Chen Y., Karin M. Positive and negative regulation of IkappaB kinase activity through IKKbeta subunit phosphorylation. Science 1999, 284:309-313.
14. O'Mahony A., Lin X., Geleziunas R., Greene W.C. Activation of the heterodimeric IkappaB kinase alpha (IKKalpha)-IKKbeta complex is directional: IKKalpha regulates IKKbeta under both basal and stimulated conditions. Mol Cell Biol 2000, 20:1170-1178.
15. Cohen L., Henzel W.J., Baeuerle P.A. IKAP is a scaffold protein of the IkappaB kinase complex. Nature 1998, 395:292-296.
16. Yin L., Wu L., Wesche H., Arthur C.D., White J.M., Goeddel D.V., et al. Defective lymphotoxin-beta receptor-induced NF-kappaB transcriptional activity in NIK-deficient mice. Science 2001, 291:2162-2165.
17. Shinkura R., Kitada K., Matsuda F., Tashiro K., Ikuta K., Suzuki M., et al. Alymphoplasia is caused by a point mutation in the mouse gene encoding NF-kappa B-inducing kinase. Nat Genet 1999, 22:74-77.
18. Muller J.R., Siebenlist U. Lymphotoxin beta receptor induces sequential activation of distinct NF-kappa B factors via separate signaling pathways. J Biol Chem 2003, 278:12006-12012.
19. Matsumoto M., Iwamasa K., Rennert P.D., Yamada T., Suzuki R., Matsushima A., et al. Involvement of distinct cellular compartments in the abnormal lymphoid organogenesis in lymphotoxin-alpha-deficient mice and alymphoplasia (aly) mice defined by the chimeric analysis. J Immunol 1999, 163:1584-1591.
20. Dejardin E., Droin N.M., Delhase M., Haas E., Cao Y., Makris C., et al. The lymphotoxin-beta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity 2002, 17:525-535.
21. Ramakrishnan P., Wang W., Wallach D. Receptor-specific signaling for both the alternative and the canonical NF-kappaB activation pathways by NF-kappaB-inducing kinase. Immunity 2004, 21:477-489.
22. Garceau N., Kosaka Y., Masters S., Hambor J., Shinkura R., Honjo T., et al. Lineage-restricted function of nuclear factor kappaB-inducing kinase (NIK) in transducing signals via CD40. J Exp Med 2000, 191:381-386.
23. Xiao G., Harhaj E.W., Sun S.C. NF-kappaB-inducing kinase regulates the processing of NF-kappaB2 p100. Mol Cell 2001, 7:401-409.
24. Xiao G., Fong A., Sun S.C. Induction of p100 processing by NF-kappaB-inducing kinase involves docking IkappaB kinase alpha (IKKalpha) to p100 and IKKalpha-mediated phosphorylation. J Biol Chem 2004, 279:30099-30105.
25. Qing G., Xiao G. Essential role of IkappaB kinase alpha in the constitutive processing of NF-kappaB2 p100. J Biol Chem 2005, 280:9765-9768.
26. Qing G., Qu Z., Xiao G. Stabilization of basally translated NF-kappaB-inducing kinase (NIK) protein functions as a molecular switch of processing of NF-kappaB2 p100. J Biol Chem 2005, 280:40578-40582.
27. Park G.Y., Wang X., Hu N., Pedchenko T.V., Blackwell T.S., Christman J.W. NIK is involved in nucleosomal regulation by enhancing histone H3 phosphorylation by IKKalpha. J Biol Chem 2006, 281:18684-18690.
28. Zarnegar B., Yamazaki S., He J.Q., Cheng G. Control of canonical NF-kappaB activation through the NIK-IKK complex pathway. Proc Natl Acad Sci USA 2008, 105:3503-3508.
29. Basak S., Kim H., Kearns J.D., Tergaonkar V., O'Dea E., Werner S.L., et al. A fourth IkappaB protein within the NF-kappaB signaling module. Cell 2007, 128:369-381.
30. Vallabhapurapu S., Matsuzawa A., Zhang W., Tseng P.H., Keats J.J., Wang H., et al. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat Immunol 2008, 9:1364-1370.
31. Zarnegar B.J., Wang Y., Mahoney D.J., Dempsey P.W., Cheung H.H., He J., et al. Noncanonical NF-kappaB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat Immunol 2008, 9:1371-1378.
32. Yamada T., Mitani T., Yorita K., Uchida D., Matsushima A., Iwamasa K., et al. Abnormal immune function of hemopoietic cells from alymphoplasia (aly) mice, a natural strain with mutant NF-kappa B-inducing kinase. J Immunol 2000, 165:804-812.
33. Sanchez-Valdepenas C., Martin A.G., Ramakrishnan P., Wallach D., Fresno M. NF-kappaB-inducing kinase is involved in the activation of the CD28 responsive element through phosphorylation of c-Rel and regulation of its transactivating activity. J Immunol 2006, 176:4666-4674.
34. Wang C.Y., Mayo M.W., Korneluk R.G., Goeddel D.V., Baldwin A.S. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 1998, 281:1680-1683.
35. Sasaki Y., Calado D.P., Derudder E., Zhang B., Shimizu Y., Mackay F., et al. NIK overexpression amplifies, whereas ablation of its TRAF3-binding domain replaces BAFF:BAFF-R-mediated survival signals in B cells. Proc Natl Acad Sci USA 2008, 105:10883-10888.
36. Bista P., Zeng W., Ryan S., Bailly V., Browning J., Lukashev M.E. TRAF3 controls activation of the canonical and alternative NF{kappa}B by the lymphotoxin beta receptor. J Biol Chem 2010, 285:12971-12978.
37. Xiao G., Sun S.C. Negative regulation of the nuclear factor kappa B-inducing kinase by a cis-acting domain. J Biol Chem 2000, 275:21081-21085.
38. Liao G., Zhang M., Harhaj E.W., Sun S.C. Regulation of the NF-kappaB-inducing kinase by tumor necrosis factor receptor-associated factor 3-induced degradation. J Biol Chem 2004, 279:26243-26250.
39. Birbach A., Gold P., Binder B.R., Hofer E., de Martin R., Schmid J.A. Signaling molecules of the NF-kappa B pathway shuttle constitutively between cytoplasm and nucleus. J Biol Chem 2002, 277:10842-10851.
40. Birbach A., Bailey S.T., Ghosh S., Schmid J.A. Cytosolic, nuclear and nucleolar localization signals determine subcellular distribution and activity of the NF-kappaB inducing kinase NIK. J Cell Sci 2004, 117:3615-3624.
41. Miyawaki S., Nakamura Y., Suzuka H., Koba M., Yasumizu R., Ikehara S., et al. A new mutation, aly, that induces a generalized lack of lymph nodes accompanied by immunodeficiency in mice. Eur J Immunol 1994, 24:429-434.
42. Luftig M.A., Cahir-McFarland E., Mosialos G., Kieff E. Effects of the NIK aly mutation on NF-kappaB activation by the Epstein-Barr virus latent infection membrane protein, lymphotoxin beta receptor, and CD40. J Biol Chem 2001, 276:14602-14606.
43. Moore C.R., Bishop G.A. Differential regulation of CD40-mediated TNF receptor-associated factor degradation in B lymphocytes. J Immunol 2005, 175:3780-3789.
44. Morrison M.D., Reiley W., Zhang M., Sun S.C. 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, 280:10018-10024.
45. He J.Q., Zarnegar B., Oganesyan G., Saha S.K., Yamazaki S., Doyle S.E., et al. Rescue of TRAF3-null mice by p100 NF-kappa B deficiency. J Exp Med 2006, 203:2413-2418.
46. Grech A.P., 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.
47. Varfolomeev E., Blankenship J.W., Wayson S.M., Fedorova A.V., Kayagaki N., Garg P., et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 2007, 131:669-681.
48. Demchenko Y.N., Glebov O.K., Zingone A., Keats J.J., Bergsagel P.L., Kuehl W.M. Classical and/or alternative NF{kappa}B pathway activation in multiple myeloma. Blood 2010, 115:3541-3552.
49. Feltham R.L., Moulin M., Vince J.E., Mace P.D., Wong W.W., Anderton H., et al. TNF signaling, but not TWEAK triggered cellular Inhibitor of APoptosis protein 1 (cIAP1) degradation, requires cIAP1 RING dimerization and E2 binding. J Biol Chem 2010, 285:17525-17536.
50. Sanjo H., Zajonc D.M., Braden R., Norris P.S., Ware C.F. Allosteric regulation of the ubiquitin:NIK and TRAF3 E3 ligases by the lymphotoxin-{beta} receptor. J Biol Chem 2010, 285:17148-17155.
51. Song H.Y., Regnier C.H., Kirschning C.J., Goeddel D.V., Rothe M. Tumor necrosis factor (TNF)-mediated kinase cascades: bifurcation of nuclear factor-kappaB and c-jun N-terminal kinase (JNK/SAPK) pathways at TNF receptor-associated factor 2. Proc Natl Acad Sci USA 1997, 94:9792-9796.
52. Li Y., Kang J., Friedman J., Tarassishin L., Ye J., Kovalenko A., et al. Identification of a cell protein (FIP-3) as a modulator of NF-kappaB activity and as a target of an adenovirus inhibitor of tumor necrosis factor alpha-induced apoptosis. Proc Natl Acad Sci USA 1999, 96:1042-1047.
53. Bouwmeester T., Bauch A., Ruffner H., Angrand P.O., Bergamini G., Croughton K., et al. A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat Cell Biol 2004, 6:97-105.
54. Lich J.D., Williams K.L., Moore C.B., Arthur J.C., Davis B.K., Taxman D.J., et al. Monarch-1 suppresses non-canonical NF-kappaB activation and p52-dependent chemokine expression in monocytes. J Immunol 2007, 178:1256-1260.
55. Qing G., Yan P., Qu Z., Liu H., Xiao G. Hsp90 regulates processing of NF-kappa B2 p100 involving protection of NF-kappa B-inducing kinase (NIK) from autophagy-mediated degradation. Cell Res 2007, 17:520-530.
56. Hu W.H., Mo X.M., Walters W.M., Brambilla R., Bethea J.R. TNAP, a novel repressor of NF-kappaB-inducing kinase, suppresses NF-kappaB activation. J Biol Chem 2004, 279:35975-35983.
57. Hu W.H., Pendergast J.S., Mo X.M., Brambilla R., Bracchi-Ricard V., Li F., et al. NIBP, a novel NIK and IKK(beta)-binding protein that enhances NF-(kappa)B activation. J Biol Chem 2005, 280:29233-29241.
58. Yeung K.C., Rose D.W., Dhillon A.S., Yaros D., Gustafsson M., Chatterjee D., et al. Raf kinase inhibitor protein interacts with NF-kappaB-inducing kinase and TAK1 and inhibits NF-kappaB activation. Mol Cell Biol 2001, 21:7207-7217.
59. Chaudhary P.M., Eby M.T., Jasmin A., Kumar A., Liu L., Hood L. Activation of the NF-kappaB pathway by caspase 8 and its homologs. Oncogene 2000, 19:4451-4460.
60. Chaudhary P.M., Jasmin A., Eby M.T., Hood L. Modulation of the NF-kappa B pathway by virally encoded death effector domains-containing proteins. Oncogene 1999, 18:5738-5746.
61. Habib A.A., Chatterjee S., Park S.K., Ratan R.R., Lefebvre S., Vartanian T. The epidermal growth factor receptor engages receptor interacting protein and nuclear factor-kappa B (NF-kappa B)-inducing kinase to activate NF-kappa B. Identification of a novel receptor-tyrosine kinase signalosome. J Biol Chem 2001, 276:8865-8874.
62. Chen D., Xu L.G., Chen L., Li L., Zhai Z., Shu H.B. NIK is a component of the EGF/heregulin receptor signaling complexes. Oncogene 2003, 22:4348-4355.
63. Lin X., Cunningham E.T., Mu Y., Geleziunas R., Greene W.C. The proto-oncogene Cot kinase participates in CD3/CD28 induction of NF-kappaB acting through the NF-kappaB-inducing kinase and IkappaB kinases. Immunity 1999, 10:271-280.
64. Nadiminty N., Chun J.Y., Hu Y., Dutt S., Lin X., Gao A.C., et al. a member of the TNF superfamily, activates Stat3 mediated by NIK pathway. Biochem Biophys Res Commun 2007, 359:379-384.
65. Yang C.H., Murti A., Pfeffer L.M. Interferon induces NF-kappa B-inducing kinase/tumor necrosis factor receptor-associated factor-dependent NF-kappa B activation to promote cell survival. J Biol Chem 2005, 280:31530-31536.
66. Pan Q., Kravchenko V., Katz A., Huang S., Ii M., Mathison J.C., et al. NF-kappa B-inducing kinase regulates selected gene expression in the Nod2 signaling pathway. Infect Immun 2006, 74:2121-2127.
67. Foehr E.D., Bohuslav J., Chen L.F., DeNoronha C., Geleziunas R., Lin X., et al. The NF-kappa B-inducing kinase induces PC12 cell differentiation and prevents apoptosis. J Biol Chem 2000, 275:34021-34024.
68. Rangaswami H., Bulbule A., Kundu G.C. Nuclear factor-inducing kinase plays a crucial role in osteopontin-induced MAPK/IkappaBalpha kinase-dependent nuclear factor kappaB-mediated promatrix metalloproteinase-9 activation. J Biol Chem 2004, 279:38921-38935.
69. Shinkura R., Matsuda F., Sakiyama T., Tsubata T., Hiai H., Paumen M., et al. Defects of somatic hypermutation and class switching in alymphoplasia (aly) mutant mice. Int Immunol 1996, 8:1067-1075.
70. Kunisawa J., Gohda M., Kurashima Y., Ishikawa I., Higuchi M., Kiyono H. Sphingosine 1-phosphate-dependent trafficking of peritoneal B cells requires functional NFkappaB-inducing kinase in stromal cells. Blood 2008, 111:4646-4652.
71. Mills D.M., Bonizzi G., Karin M., Rickert R.C. Regulation of late B cell differentiation by intrinsic IKKalpha-dependent signals. Proc Natl Acad Sci USA 2007, 104:6359-6364.
72. Claudio E., Brown K., Park S., Wang H., Siebenlist U. BAFF-induced NEMO-independent processing of NF-kappa B2 in maturing B cells. Nat Immunol 2002, 3:958-965.
73. Siebenlist U., Brown K., Claudio E. Control of lymphocyte development by nuclear factor-kappaB. Nat Rev Immunol 2005, 5:435-445.
74. Xie P., Stunz L.L., Larison K.D., Yang B., Bishop G.A. Tumor necrosis factor receptor-associated factor 3 is a critical regulator of B cell homeostasis in secondary lymphoid organs. Immunity 2007, 27:253-267.
75. Gardam S., Sierro F., Basten A., Mackay F., Brink R., TRAF2 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.
76. Zapata J.M., Llobet D., Krajewska M., Lefebvre S., Kress C.L., Reed J.C. Lymphocyte-specific TRAF3 transgenic mice have enhanced humoral responses and develop plasmacytosis, autoimmunity, inflammation, and cancer. Blood 2009, 113:4595-4603.
77. Kajiura F., Sun S., Nomura T., Izumi K., Ueno T., Bando Y., et al. NF-kappa B-inducing kinase establishes self-tolerance in a thymic stroma-dependent manner. J Immunol 2004, 172:2067-2075.
78. Lu L.F., Gondek D.C., Scott Z.A., Noelle R.J. 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, 175:1651-1657.
79. Akiyama T., Shimo Y., Yanai H., Qin J., Ohshima D., Maruyama Y., et al. The tumor necrosis factor family receptors RANK and CD40 cooperatively establish the thymic medullary microenvironment and self-tolerance. Immunity 2008, 29:423-437.
80. Jin W., Zhou X.F., Yu J., Cheng X., Sun S.C. Regulation of Th17 cell differentiation and EAE induction by MAP3K NIK. Blood 2009, 113:6603-6610.
81. Mathur A.N., Chang H.C., Zisoulis D.G., Stritesky G.L., Yu Q., O'Malley J.T., et al. Stat3 and Stat4 direct development of IL-17-secreting Th cells. J Immunol 2007, 178:4901-4907.
82. Elewaut D., Shaikh R.B., Hammond K.J., De Winter H., Leishman A.J., Sidobre S., et al. NIK-dependent RelB activation defines a unique signaling pathway for the development of V alpha 14i NKT cells. J Exp Med 2003, 197:1623-1633.
83. Acuto O., Michel F. CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat Rev Immunol 2003, 3:939-951.
84. Matsumoto M., Yamada T., Yoshinaga S.K., Boone T., Horan T., Fujita S., et al. Essential role of NF-kappa B-inducing kinase in T cell activation through the TCR/CD3 pathway. J Immunol 2002, 169:1151-1158.
85. Fagarasan S., Shinkura R., Kamata T., Nogaki F., Ikuta K., Tashiro K., et al. Alymphoplasia (aly)-type nuclear factor kappaB-inducing kinase (NIK) causes defects in secondary lymphoid tissue chemokine receptor signaling and homing of peritoneal cells to the gut-associated lymphatic tissue system. J Exp Med 2000, 191:1477-1486.
86. Lind E.F., Ahonen C.L., Wasiuk A., Kosaka Y., Becher B., Bennett K.A., et al. Dendritic cells require the NF-kappaB2 pathway for cross-presentation of soluble antigens. J Immunol 2008, 181:354-363.
87. Andreakos E., Williams R.O., Wales J., Foxwell B.M., Feldmann M. Activation of NF-kappaB by the intracellular expression of NF-kappaB-inducing kinase acts as a powerful vaccine adjuvant. Proc Natl Acad Sci USA 2006, 103:14459-14464.
88. Azim A.C., Wang X., Park G.Y., Sadikot R.T., Cao H., Mathew B., et al. NF-kappaB-inducing kinase regulates cyclooxygenase 2 gene expression in macrophages by phosphorylation of PU.1. J Immunol 2007, 179:7868-7875.
89. Ye Z., Lich J.D., Moore C.B., Duncan J.A., Williams K.L., Ting J.P. ATP binding by monarch-1/NLRP12 is critical for its inhibitory function. Mol Cell Biol 2008, 28:1841-1850.
90. Luftig M., Yasui T., Soni V., Kang M.S., Jacobson N., Cahir-McFarland E., et al. Epstein-Barr virus latent infection membrane protein 1 TRAF-binding site induces NIK/IKK alpha-dependent noncanonical NF-kappaB activation. Proc Natl Acad Sci USA 2004, 101:141-146.
91. Albrecht J.C., Biesinger B., Muller-Fleckenstein I., Lengenfelder D., Schmidt M., Fleckenstein B., et al. Herpesvirus ateles Tio can replace herpesvirus saimiri StpC and Tip oncoproteins in growth transformation of monkey and human T cells. J Virol 2004, 78:9814-9819.
92. de Jong S.J., Albrecht J.C., Schmidt M., Mueller-Fleckenstein I., Biesinger B. Activation of non-canonical NF-{kappa}B signaling by the oncoprotein TIO. J Biol Chem 2010, 285:16495-16503.
93. Sorokina E.M., Merlo J.J., Tsygankov A.Y. Molecular mechanisms of the effect of herpesvirus saimiri protein StpC on the signaling pathway leading to NF-kappaB activation. J Biol Chem 2004, 279:13469-13477.
94. Liu P., Li K., Garofalo R.P., Brasier A.R. Respiratory syncytial virus induces RelA release from cytoplasmic 100-kDa NF-kappa B2 complexes via a novel retinoic acid-inducible gene-I{middle dot}NF-kappa B-inducing kinase signaling pathway. J Biol Chem 2008, 283:23169-23178.
95. Karrer U., Althage A., Odermatt B., Roberts C.W., Korsmeyer S.J., Miyawaki S., et al. On the key role of secondary lymphoid organs in antiviral immune responses studied in alymphoplastic (aly/aly) and spleenless (Hox11(-)/-) mutant mice. J Exp Med 1997, 185:2157-2170.
96. Shuto T., Xu H., Wang B., Han J., Kai H., Gu X.X., et al. Activation of NF-kappa B by nontypeable Hemophilus influenzae is mediated by toll-like receptor 2-TAK1-dependent NIK-IKK alpha/beta-I kappa B alpha and MKK3/6-p38 MAP kinase signaling pathways in epithelial cells. Proc Natl Acad Sci USA 2001, 98:8774-8779.
97. Novack D.V., Yin L., Hagen-Stapleton A., Schreiber R.D., Goeddel D.V., Ross F.P., et al. The IkappaB function of NF-kappaB2 p100 controls stimulated osteoclastogenesis. J Exp Med 2003, 198:771-781.
98. Vaira S., Johnson T., Hirbe A.C., Alhawagri M., Anwisye I., Sammut B., et al. RelB is the NF-kappaB subunit downstream of NIK responsible for osteoclast differentiation. Proc Natl Acad Sci USA 2008, 105:3897-3902.
99. Yao Z., Xing L., Boyce B.F. NF-kappaB p100 limits TNF-induced bone resorption in mice by a TRAF3-dependent mechanism. J Clin Invest 2009, 119:3024-3034.
100. Tanaka S., Nakano H. NF-kappaB2 (p100) limits TNF-alpha-induced osteoclastogenesis. J Clin Invest 2009, 119:2879-2881.
101. Kong Y.Y., Feige U., Sarosi I., Bolon B., Tafuri A., Morony S., et al. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 1999, 402:304-309.
102. Pettit A.R., Ji H., von Stechow D., Muller R., Goldring S.R., Choi Y., et al. TRANCE/RANKL knockout mice are protected from bone erosion in a serum transfer model of arthritis. Am J Pathol 2001, 159:1689-1699.
103. Aya K., Alhawagri M., Hagen-Stapleton A., Kitaura H., Kanagawa O., Novack D.V. NF-(kappa)B-inducing kinase controls lymphocyte and osteoclast activities in inflammatory arthritis. J Clin Invest 2005, 115:1848-1854.
104. Kubota N., Terauchi Y., Miki H., Tamemoto H., Yamauchi T., Komeda K., et al. PPAR gamma mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell 1999, 4:597-609.
105. Suzawa M., Takada I., Yanagisawa J., Ohtake F., Ogawa S., Yamauchi T., et al. Cytokines suppress adipogenesis and PPAR-gamma function through the TAK1/TAB1/NIK cascade. Nat Cell Biol 2003, 5:224-230.
106. Takada I., Suzawa M., Matsumoto K., Kato S. Suppression of PPAR transactivation switches cell fate of bone marrow stem cells from adipocytes into osteoblasts. Ann NY Acad Sci 2007, 1116:182-195.
107. Vince J.E., Wong W.W., Khan N., Feltham R., Chau D., Ahmed A.U., et al. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 2007, 131:682-693.
108. Petersen S.L., Wang L., Yalcin-Chin A., Li L., Peyton M., Minna J., et al. Autocrine TNFalpha signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 2007, 12:445-456.
109. Annunziata C.M., Davis R.E., Demchenko Y., Bellamy W., Gabrea A., Zhan F., et al. Frequent engagement of the classical and alternative NF-kappaB pathways by diverse genetic abnormalities in multiple myeloma. Cancer Cell 2007, 12:115-130.
110. Keats J.J., Fonseca R., Chesi M., Schop R., Baker A., Chng W.J., et al. Promiscuous mutations activate the noncanonical NF-kappaB pathway in multiple myeloma. Cancer Cell 2007, 12:131-144.
111. Zapata J.M., Krajewska M., Krajewski S., Kitada S., Welsh K., Monks A., et al. TNFR-associated factor family protein expression in normal tissues and lymphoid malignancies. J Immunol 2000, 165:5084-5096.
112. Bellavia D., Campese A.F., Alesse E., Vacca A., Felli M.P., Balestri A., et al. Constitutive activation of NF-kappaB and T-cell leukemia/lymphoma in Notch3 transgenic mice. EMBO J 2000, 19:3337-3348.
113. Vacca A., Felli M.P., Palermo R., Di Mario G., Calce A., Di Giovine M., et al. Notch3 and pre-TCR interaction unveils distinct NF-kappaB pathways in T-cell development and leukemia. EMBO J 2006, 25:1000-1008.
114. Saitoh Y., Yamamoto N., Dewan M.Z., Sugimoto H., Martinez Bruyn V.J., Iwasaki Y., et al. Overexpressed NF-kappaB-inducing kinase contributes to the tumorigenesis of adult T-cell leukemia and Hodgkin Reed-Sternberg cells. Blood 2008, 111:5118-5129.
115. Nishina T., Yamaguchi N., Gohda J., Semba K., Inoue J. NIK is involved in constitutive activation of the alternative NF-kappaB pathway and proliferation of pancreatic cancer cells. Biochem Biophys Res Commun 2009, 388:96-101.
116. Saitoh Y, Martinez Bruyn VJ, Uota S, Hasegawa A, Yamamoto N, Imoto I, et al. Overexpression of NF-kappaB inducing kinase underlies constitutive NF-kappaB activation in lung cancer cells. Lung Cancer 2010; doi:10.1016/j.lungcan.2010.03.001.
117. Yamaguchi N., Ito T., Azuma S., Ito E., Honma R., Yanagisawa Y., et al. Constitutive activation of nuclear factor-kappaB is preferentially involved in the proliferation of basal-like subtype breast cancer cell lines. Cancer Sci 2009, 100:1668-1674.
118. 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, 277:7920-7928.
119. Dhawan P., Su Y., Thu Y.M., Yu Y., Baugher P., Ellis D.L., et al. The lymphotoxin-beta receptor is an upstream activator of NF-kappaB-mediated transcription in melanoma cells. J Biol Chem 2008, 283:15399-15408.