Non-conventional functions for NF-κB members: The dark side of NF-κB

Oncogene

Volumn 34, Issue 18, 2015, Pages 2279-2287

  Espinosa, L ^a   Margalef, P ^a   Bigas, A ^a  

^a HOSPITAL DEL MAR   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANIMAL; CELL CYCLE; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; NEOPLASM; SIGNAL TRANSDUCTION;

ANIMALS; CELL CYCLE; GENE EXPRESSION REGULATION; HUMANS; I-KAPPA B PROTEINS; NEOPLASMS; NF-KAPPA B; SIGNAL TRANSDUCTION;

EID: 84936130843     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.188     Document Type: Review

References (96)

1. Sen R, Baltimore D. Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 1986; 46: 705-716.
2. Pahl HL. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 1999; 18: 6853-6866.
3. Hayden MS, Ghosh S. Signaling to NF-kappaB. Genes Dev 2004; 18: 2195-2224.
4. Kucharczak J, Simmons MJ, Fan Y, Gélinas C. To be, or not to be: NF-kappaB is the answer-role of Rel/NF-kappaB in the regulation of apoptosis. Oncogene 2003; 22: 8961-8982.
5. Gerondakis S, Grossmann M, Nakamura Y, Pohl T, Grumont R. Genetic approaches in mice to understand Rel/NF-kappaB and IkappaB function: Transgenics and knockouts. Oncogene 1999; 18: 6888-6895.
6. Staudt LM, Singh H, Sen R, Wirth T, Sharp PA, Baltimore D. A lymphoid-specific protein binding to the octamer motif of immunoglobulin genes. Nature 1986; 323: 640-643.
7. Beg AA, Sha WC, Bronson RT, Ghosh S, Baltimore D. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature 1995; 376: 167-170.
8. Brown K, Park S, Kanno T, Franzoso G, Siebenlist U. Mutual regulation of the transcriptional activator NF-kappa B and its inhibitor, I kappa B-alpha. Proc Natl Acad Sci USA 1993; 90: 2532-2536.
9. Sun SC, Ganchi PA, Ballard DW, Greene WC. NF-kappa B controls expression of inhibitor I kappa B alpha: Evidence for an inducible autoregulatory pathway. Science 1993; 259: 1912-1915.
10. Arenzana-Seisdedos F, Turpin P, Rodriguez M, Thomas D, Hay RTVirelizier JL et al. Nuclear localization of I kappa B alpha promotes active transport of NF-kappa B from the nucleus to the cytoplasm. J Cell Sci 1997; 110(Part 3): 369-378.
11. DiDonato JA, Hayakawa M, Rothwarf DM, Zandi E, Karin M. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature 1997; 388: 548-554.
12. Mercurio F, Zhu H, Murray BW, Shevchenko A, Bennett BL, Li J et al. IKK-1 and IKK-2: Cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 1997; 278: 860-866.
13. Zandi E, Rothwarf DM, Delhase M, Hayakawa M, Karin M. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation. Cell 1997; 91: 243-252.
14. Rothwarf DM, Zandi E, Natoli G, Karin M. IKK-gamma is an essential regulatory subunit of the IkappaB kinase complex. Nature 1998; 395: 297-300.
15. Chen ZJ, Parent L, Maniatis T. Site-specific phosphorylation of IkappaBalpha by a novel ubiquitination-dependent protein kinase activity. Cell 1996; 84: 853-862.
16. Haas TL, Emmerich CH, Gerlach B, Schmukle AC, Cordier SM, Rieser E et al. Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol Cell 2009; 36: 831-844.
17. Tokunaga F, Sakata S, Saeki Y, Satomi Y, Kirisako T, Kamei K et al. Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat Cell Biol 2009; 11: 123-132.
18. Gerlach B, Cordier SM, Schmukle AC, Emmerich CH, Rieser E, Haas TL et al. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 2011; 471: 591-596.
19. Ikeda F, Deribe YL, Skånland SS, Stieglitz B, Grabbe C, Franz-Wachtel M et al. SHARPIN forms a linear ubiquitin ligase complex regulating NF-αB activity and apoptosis. Nature 2011; 471: 637-641.
20. Tokunaga F, Nakagawa T, Nakahara M, Saeki Y, Taniguchi M, Sakata S et al. SHARPIN is a component of the NF-αB-activating linear ubiquitin chain assembly complex. Nature 2011; 471: 633-636.
21. Kovalenko A, Chable-Bessia C, Cantarella G, Israël A, Wallach D, Courtois G. The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 2003; 424: 801-805.
22. Trompouki E, Hatzivassiliou E, Tsichritzis T, Farmer H, Ashworth A, Mosialos G. CYLD is a deubiquitinating enzyme that negatively regulates NF-kappaB activation by TNFR family members. Nature 2003; 424: 793-796.
23. Brummelkamp TR, Nijman SMB, Dirac AMG, Bernards R. Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature 2003; 424: 797-801.
24. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004; 430: 694-699.
25. Boone DL, Turer EE, Lee EG, Ahmad R-C, Wheeler MT, Tsui C et al. The ubiquitinmodifying enzyme A20 is required for termination of Toll-like receptor responses. Nat Immunol 2004; 5: 1052-1060.
26. Wang L, Du F, Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell 2008; 133: 693-703.
27. Dejardin E, Droin NM, Delhase M, Haas E, Cao Y, Makris C et al. The lymphotoxinbeta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity 2002; 17: 525-535.
28. Kayagaki N, Yan M, Seshasayee D, Wang H, Lee W, French DM et al. BAFF/BLyS receptor 3 binds the B cell survival factor BAFF ligand through a discrete surface loop and promotes processing of NF-kappaB2. Immunity 2002; 17: 515-524.
29. 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.
30. Coope HJ, Atkinson PGP, Huhse B, Belich M, Janzen J, Holman MJ et al. CD40 regulates the processing of NF-kappaB2 p100 to p52. EMBO J 2002; 21: 5375-5385.
31. Novack DV, Yin L, Hagen-Stapleton A, Schreiber RD, Goeddel D V, Ross FP et al. The IkappaB function of NF-kappaB2 p100 controls stimulated osteoclastogenesis. J Exp Med 2003; 198: 771-781.
32. Vallabhapurapu S, Matsuzawa A, Zhang W, Tseng P-H, Keats JJ, 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.
33. Senftleben U, Cao Y, Xiao G, Greten FR, Krähn G, Bonizzi G et al. Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science 2001; 293: 1495-1499.
34. Xiao G, Harhaj EW, Sun SC. NF-kappaB-inducing kinase regulates the processing of NF-kappaB2 p100. Mol Cell 2001; 7: 401-409.
35. Amir RE, Haecker H, Karin M, Ciechanover A. Mechanism of processing of the NF-kappa B2 p100 precursor: Identification of the specific polyubiquitin chainanchoring lysine residue and analysis of the role of NEDD8-modification on the SCF(beta-TrCP) ubiquitin ligase. Oncogene 2004; 23: 2540-2547.
36. Betts JC, Nabel GJ. Differential regulation of NF-kappaB2(p100) processing and control by amino-terminal sequences. Mol Cell Biol 1996; 16: 6363-6371.
37. Solan NJ, Miyoshi H, Carmona EM, Bren GD, Paya CV. RelB cellular regulation and transcriptional activity are regulated by p100. J Biol Chem 2002; 277: 1405-1418.
38. Hu Y, Baud V, Delhase M, Zhang P, Deerinck T, Ellisman M et al. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKalpha subunit of IkappaB kinase. Science 1999; 284: 316-320.
39. Takeda K, Takeuchi O, Tsujimura T, Itami S, Adachi O, Kawai T et al. Limb and skin abnormalities in mice lacking IKKalpha. Science 1999; 284: 313-316.
40. Bonizzi G, Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 2004; 25: 280-288.
41. Anest V, Hanson JL, Cogswell PC, Steinbrecher KA, Strahl BD, Baldwin AS. A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression. Nature 2003; 423: 659-663.
42. Yamamoto Y, Verma UN, Prajapati S, Kwak Y-T, Gaynor RB. Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature 2003; 423: 655-659.
43. Park GY, Wang X, Hu N, Pedchenko T V, Blackwell TS, Christman JW. NIK is involved in nucleosomal regulation by enhancing histone H3 phosphorylation by IKKalpha. J Biol Chem 2006; 281: 18684-18690.
44. Temmerman ST, Ma CA, Zhao Y, Keenan J, Aksentijevich I, Fessler M et al. Defective nuclear IKKα Function in patients with ectodermal dysplasia with immune deficiency. J Clin Invest 2012; 122: 315-326.
45. Anest V, Cogswell PC, Baldwin AS. IkappaB kinase alpha and p65/RelA contribute to optimal epidermal growth factor-induced c-fos gene expression independent of IkappaBalpha degradation. J Biol Chem 2004; 279: 31183-31189.
46. Park K-J, Krishnan V, O'Malley BW, Yamamoto Y, Gaynor RB. Formation of an IKKalpha-dependent transcription complex is required for estrogen receptormediated gene activation. Mol Cell 2005; 18: 71-82.
47. Li L, Ruan Q, Hilliard B, Devirgiliis J, Karin M, Chen YH. Transcriptional regulation of the Th17 immune response by IKK(alpha). J Exp Med 2011; 208: 787-796.
48. Hoberg JE, Yeung F, Mayo MW. SMRT derepression by the IkappaB kinase alpha: A prerequisite to NF-kappaB transcription and survival. Mol Cell 2004; 16: 245-255.
49. Fernández-Majada V, Aguilera C, Villanueva A, Vilardell F, Robert-Moreno A, Aytés A et al. Nuclear IKK activity leads to dysregulated notch-dependent gene expression in colorectal cancer. Proc Natl Acad Sci USA 2007; 104: 276-281.
50. Fernández-Majada V, Pujadas J, Vilardell F, Capella G, Mayo MW, Bigas A et al. Aberrant cytoplasmic localization of N-CoR in colorectal tumors. Cell Cycle 2007; 6: 1748-1752.
51. Tu Z, Prajapati S, Park K-J, Kelly NJ, Yamamoto Y, Gaynor RB. IKK alpha regulates estrogen-induced cell cycle progression by modulating E2F1 expression. J Biol Chem 2006; 281: 6699-6706.
52. Prajapati S, Tu Z, Yamamoto Y, Gaynor RB. IKKalpha regulates the mitotic phase of the cell cycle by modulating Aurora A phosphorylation. Cell Cycle 2006; 5: 2371-2380.
53. Barré B, Perkins ND. A cell cycle regulatory network controlling NF-kappaB subunit activity and function. EMBO J 2007; 26: 4841-4855.
54. Criollo A, Senovilla L, Authier H, Maiuri MC, Morselli E, Vitale I et al. The IKK complex contributes to the induction of autophagy. EMBO J 2010; 29: 619-631.
55. Comb WC, Cogswell P, Sitcheran R, Baldwin AS. IKK-dependent, NF-αB-independent control of autophagic gene expression. Oncogene 2011; 30: 1727-1732.
56. Li Q, Pène V, Krishnamurthy S, Cha H, Liang TJ. Hepatitis C virus infection activates an innate pathway involving IKK-α in lipogenesis and viral assembly. Nat Med 2013; 19: 722-729.
57. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 2010; 140: 883-899.
58. Luo J-L, Tan W, Ricono JM, Korchynskyi O, Zhang M, Gonias SL et al. Nuclear cytokine-activated IKKalpha controls prostate cancer metastasis by repressing Maspin. Nature 2007; 446: 690-694.
59. Ammirante M, Luo J-L, Grivennikov S, Nedospasov S, Karin M. B-cell-derived lymphotoxin promotes castration-resistant prostate cancer. Nature 2010; 464: 302-305.
60. Zhang W, Tan W, Wu X, Poustovoitov M, Strasner A, Li W et al. A NIK-IKKα Module expands ErbB2-induced tumor-initiating cells by stimulating nuclear export of p27/Kip1. Cancer Cell 2013; 23: 647-659.
61. Vilimas T, Mascarenhas J, Palomero T, Mandal M, Buonamici S, Meng F et al. Targeting the NF-kappaB signaling pathway in Notch1-induced T-cell leukemia. Nat Med 2007; 13: 70-77.
62. Espinosa L, Cathelin S, D'Altri T, Trimarchi T, Statnikov A, Guiu J et al. The Notch/Hes1 pathway sustains NF-αB activation through CYLD repression in T cell leukemia. Cancer Cell 2010; 18: 268-281.
63. Song LL, Peng Y, Yun J, Rizzo P, Chaturvedi V, Weijzen S et al. Notch-1 associates with IKKalpha and regulates IKK activity in cervical cancer cells. Oncogene 2008; 27: 5833-5844.
64. Hao L, Rizzo P, Osipo C, Pannuti A, Wyatt D, Cheung LW-K et al. Notch-1 activates estrogen receptor-alpha-dependent transcription via IKKalpha in breast cancer cells. Oncogene 2010; 29: 201-213.
65. Margalef P, Fernández-Majada V, Villanueva A, Garcia-Carbonell R, Iglesias M, López L et al. A truncated form of IKKα is responsible for specific nuclear IKK activity in colorectal cancer. Cell Rep 2012; 2: 840-854.
66. Schröfelbauer B, Polley S, Behar M, Ghosh G, Hoffmann A. NEMO ensures signaling specificity of the pleiotropic IKKα by directing its kinase activity toward IαBα. Mol Cell 2012; 47: 111-121.
67. Teo H, Ghosh S, Luesch H, Ghosh A, Wong ET, Malik N et al. Telomereindependent Rap1 is an IKK adaptor and regulates NF-kappaB-dependent gene expression. Nat Cell Biol 2010; 12: 758-767.
68. Tsuchiya Y, Asano T, Nakayama K, Kato T, Karin M, Kamata H. Nuclear IKKbeta is an adaptor protein for IkappaBalpha ubiquitination and degradation in UV-induced NF-kappaB activation. Mol Cell 2010; 39: 570-582.
69. Sakamoto K, Hikiba Y, Nakagawa H, Hirata Y, Hayakawa Y, Kinoshita H et al. Promotion of DNA repair by nuclear IKKα phosphorylation of ATM in response to genotoxic stimuli. Oncogene 2013; 32: 1854-1862.
70. Suzuki K, Verma IM. Phosphorylation of SNAP-23 by IkappaB kinase 2 regulates mast cell degranulation. Cell 2008; 134: 485-495.
71. Hu MC-T, Lee D-F, Xia W, Golfman LS, Ou-Yang F, Yang J-Y et al. IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 2004; 117: 225-237.
72. Aguilera C, Hoya-Arias R, Haegeman G, Espinosa L, Bigas A. Recruitment of IkappaBalpha to the hes1 promoter is associated with transcriptional repression. Proc Natl Acad Sci USA 2004; 101: 16537-16542.
73. Mulero MC, Ferres-Marco D, Islam A, Margalef P, Pecoraro M, Toll A et al. Chromatin-bound IαBα regulates a subset of polycomb target genes in differentiation and cancer. Cancer Cell 2013; 24: 1-16.
74. Rao P, Hayden MS, Long M, Scott ML, West AP, Zhang D et al. IkappaBbeta acts to inhibit and activate gene expression during the inflammatory response. Nature 2010; 466: 1115-1119.
75. Liu L, D'Mello SR. Phosphorylation of IkappaB-beta is necessary for neuronal survival. J Biol Chem 2006; 281: 1506-1515.
76. Hu Y, Baud V, Oga T, Kim KI, Yoshida K, Karin M. IKKalpha controls formation of the epidermis independently of NF-kappaB. Nature 2001; 410: 710-714.
77. Marinari B, Moretti F, Botti E, Giustizieri ML, Descargues P, Giunta A et al. The tumor suppressor activity of IKKalpha in stratified epithelia is exerted in part via the TGF-beta antiproliferative pathway. Proc Natl Acad Sci USA 2008; 105: 17091-17096.
78. Zhu F, Xia X, Liu B, Shen J, Hu Y, Person M et al. IKKalpha shields 14-3-3sigma, a G (2)/M cell cycle checkpoint gene, from hypermethylation, preventing its silencing. Mol Cell 2007; 27: 214-227.
79. Seitz CS, Freiberg RA, Hinata K, Khavari PA. NF-kappaB determines localization and features of cell death in epidermis. J Clin Invest 2000; 105: 253-260.
80. Seitz CS, Lin Q, Deng H, Khavari PA. Alterations in NF-kappaB function in transgenic epithelial tissue demonstrate a growth inhibitory role for NF-kappaB. Proc Natl Acad Sci USA 1998; 95: 2307-2312.
81. Seitz CS, Deng H, Hinata K, Lin Q, Khavari PA. Nuclear factor kappaB subunits induce epithelial cell growth arrest. Cancer Res 2000; 60: 4085-4092.
82. Descargues P, Sil AK, Sano Y, Korchynskyi O, Han G, Owens P et al. IKKalpha is a critical coregulator of a Smad4-independent TGFbeta-Smad2/3 signaling pathway that controls keratinocyte differentiation. Proc Natl Acad Sci USA 2008; 105: 2487-2492.
83. Sil AK, Maeda S, Sano Y, Roop DR, Karin M. IkappaB kinase-alpha acts in the epidermis to control skeletal and craniofacial morphogenesis. Nature 2004; 428: 660-664.
84. Liu B, Park E, Zhu F, Bustos T, Liu J, Shen J et al. A critical role for I kappaB kinase alpha in the development of human and mouse squamous cell carcinomas. Proc Natl Acad Sci USA 2006; 103: 17202-17207.
85. Park E, Zhu F, Liu B, Xia X, Shen J, Bustos T et al. Reduction in IkappaB kinase alpha expression promotes the development of skin papillomas and carcinomas. Cancer Res 2007; 67: 9158-9168.
86. Beg AA, Sha WC, Bronson RT, Baltimore D. Constitutive NF-kappa B activation, enhanced granulopoiesis, and neonatal lethality in I kappa B alpha-deficient mice. Genes Dev 1995; 9: 2736-2746.
87. Klement JF, Rice NR, Car BD, Abbondanzo SJ, Powers GD, Bhatt PH et al. IkappaBalpha deficiency results in a sustained NF-kappaB response and severe widespread dermatitis in mice. Mol Cell Biol 1996; 16: 2341-2349.
88. Rebholz B, Haase I, Eckelt B, Paxian S, Flaig MJ, Ghoreschi K et al. Crosstalk between keratinocytes and adaptive immune cells in an IkappaBalpha proteinmediated inflammatory disease of the skin. Immunity 2007; 27: 296-307.
89. Wuerzberger-Davis SM, Chen Y, Yang DT, Kearns JD, Bates PW, Lynch C et al. Nuclear export of the NF-αB inhibitor IαBα is required for proper B cell and secondary lymphoid tissue formation. Immunity 2011; 34: 188-200.
90. Dajee M, Lazarov M, Zhang JY, Cai T, Green CL, Russell AJ et al. NF-kappaB blockade and oncogenic Ras trigger invasive human epidermal neoplasia. Nature 2003; 421: 639-643.
91. Van Hogerlinden M, Rozell BL, Ahrlund-Richter L, Toftgård R. Squamous cell carcinomas and increased apoptosis in skin with inhibited Rel/nuclear factor-kappaB signaling. Cancer Res 1999; 59: 3299-3303.
92. Shih VF-S, Kearns JD, Basak S, Savinova O V, Ghosh G, Hoffmann A. Kinetic control of negative feedback regulators of NF-kappaB/RelA determines their pathogenand cytokine-receptor signaling specificity. Proc Natl Acad Sci USA 2009; 106: 9619-9624.
93. Bettermann K, Vucur M, Haybaeck J, Koppe C, Janssen J, Heymann F et al. TAK1 suppresses a NEMO-dependent but NF-kappaB-independent pathway to liver cancer. Cancer Cell 2010; 17: 481-496.
94. O'Donnell MA, Hase H, Legarda D, Ting AT. NEMO inhibits programmed necrosis in an NFαB-independent manner by restraining RIP1. PLoS ONE 2012; 7: E41238.
95. Li M, Beg AA. Induction of necrotic-like cell death by tumor necrosis factor alpha and caspase inhibitors: Novel mechanism for killing virus-infected cells. J Virol 2000; 74: 7470-7477.
96. Vercammen D, Beyaert R, Denecker G, Goossens V, Van Loo G, Declercq W et al. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med 1998; 187: 1477-1485.