Direct inhibition of NF-κB activation by peptide targeting the NOA ubiquitin binding domain of NEMO

Biochemical Pharmacology

Volumn 82, Issue 9, 2011, Pages 1163-1174

  Chiaravalli, Jeanne ^a   Fontan, Elisabeth ^a   Fsihi, Hafida ^a   Coic, Yves Marie ^a   Baleux, Franoise ^a   Véron, Michel ^a   Agou, Fabrice ^a  

^a CNRS   (France)

Author keywords

IKK complex; NF B; Protein protein interaction inhibitor; Ubiquitin binding domain; Ubiquitin linkage

Indexed keywords

I KAPPA B KINASE; I KAPPA B KINASE GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; POLYUBIQUITIN; PROTEIN INHIBITOR; PROTEIN NEMO OPTINEURIN ABIN; PROTEIN SERINE THREONINE KINASE; UBIQUITIN BINDING INHIBITOR; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BINDING AFFINITY; BINDING SITE; CIRCULAR DICHROISM; DRUG TARGETING; FLUORESCENCE; OLIGOMERIZATION; PRIORITY JOURNAL;

BINDING SITES; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; I-KAPPA B KINASE; MODELS, MOLECULAR; NF-KAPPA B; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; UBIQUITIN;

EID: 80053956525     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2011.07.083     Document Type: Article

References (67)

1. M.S. Hayden, and S. Ghosh Shared principles in NF-kappaB signaling Cell 132 2008 344 362
2. N.D. Perkins Integrating cell-signalling pathways with NF-kappaB and IKK function Nat Rev Mol Cell Biol 8 2007 49 62 (Pubitemid 46012014)
3. C. Scheidereit IkappaB kinase complexes: gateways to NF-kappaB activation and transcription Oncogene 25 2006 6685 6705 (Pubitemid 44657846)
4. S. Vallabhapurapu, and M. Karin Regulation and function of NF-kappaB transcription factors in the immune system Annu Rev Immunol 27 2009 693 733
5. S. Sato, H. Sanjo, K. Takeda, J. Ninomiya-Tsuji, M. Yamamoto, and T. Kawai Essential function for the kinase TAK1 in innate and adaptive immune responses Nat Immunol 6 2005 1087 1095 (Pubitemid 41541786)
6. J.H. Shim, C. Xiao, A.E. Paschal, S.T. Bailey, P. Rao, and M.S. Hayden TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo Genes Dev 19 2005 2668 2681 (Pubitemid 41627934)
7. Y. Kulathu, M. Akutsu, A. Bremm, K. Hofmann, and D. Komander Two-sided ubiquitin binding explains specificity of the TAB2 NZF domain Nat Struct Mol Biol 16 2009 1328 1330
8. Y. Sato, A. Yoshikawa, H. Mimura, M. Yamashita, A. Yamagata, and S. Fukai Structural basis for specific recognition of Lys 63-linked polyubiquitin chains by tandem UIMs of RAP80 EMBO J 28 2009 2461 2468
9. F. Tokunaga, S. Sakata, Y. Saeki, Y. Satomi, T. Kirisako, and K. Kamei Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation Nat Cell Biol 11 2009 123 132
10. B. Gerlach, S.M. Cordier, A.C. Schmukle, C.H. Emmerich, E. Rieser, and T.L. Haas Linear ubiquitination prevents inflammation and regulates immune signalling Nature 471 2011 591 596
11. F. Ikeda, Y.L. Deribe, S.S. Skanland, B. Stieglitz, C. Grabbe, and M. Franz-Wachtel SHARPIN forms a linear ubiquitin ligase complex regulating NF-kappaB activity and apoptosis Nature 471 2011 637 641
12. F. Tokunaga, T. Nakagawa, M. Nakahara, Y. Saeki, M. Taniguchi, and S. Sakata SHARPIN is a component of the NF-kappaB-activating linear ubiquitin chain assembly complex Nature 471 2011 633 636
13. T.L. Haas, C.H. Emmerich, B. Gerlach, A.C. Schmukle, S.M. Cordier, and E. Rieser Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction Mol Cell 36 2009 831 844
14. M. Xu, B. Skaug, W. Zeng, and Z.J. Chen A ubiquitin replacement strategy in human cells reveals distinct mechanisms of IKK activation by TNFalpha and IL-1beta Mol Cell 36 2009 302 314
15. Z.P. Xia, L. Sun, X. Chen, G. Pineda, X. Jiang, and A. Adhikari Direct activation of protein kinases by unanchored polyubiquitin chains Nature 461 2009 114 119
16. R.B. Marienfeld, L. Palkowitsch, and S. Ghosh Dimerization of the I kappa B kinase-binding domain of NEMO is required for tumor necrosis factor alpha-induced NF-kappa B activity Mol Cell Biol 26 2006 9209 9219 (Pubitemid 44904417)
17. M. Rushe, L. Silvian, S. Bixler, L.L. Chen, A. Cheung, and S. Bowes Structure of a NEMO/IKK-associating domain reveals architecture of the interaction site Structure 16 2008 798 808 (Pubitemid 351615013)
18. C. Bagneris, A.V. Ageichik, N. Cronin, B. Wallace, M. Collins, and C. Boshoff Crystal structure of a vFlip-IKKgamma complex: insights into viral activation of the IKK signalosome Mol Cell 30 2008 620 631 (Pubitemid 351755065)
19. O. Grubisha, M. Kaminska, S. Duquerroy, E. Fontan, F. Cordier, and A. Haouz DARPin-assisted crystallography of the CC2-LZ domain of NEMO reveals a coupling between dimerization and ubiquitin binding J Mol Biol 395 2010 89 104
20. F. Agou, G. Courtois, J. Chiaravalli, F. Baleux, Y.M. Coic, and F. Traincard Inhibition of NF-kappa B activation by peptides targeting NF-kappa B essential modulator (nemo) oligomerization J Biol Chem 279 2004 54248 54257 (Pubitemid 40053162)
21. K. Heyninck, M.M. Kreike, and R. Beyaert Structure-function analysis of the A20-binding inhibitor of NF-kappa B activation, ABIN-1 FEBS Lett 536 2003 135 140 (Pubitemid 36206420)
22. H. Sebban, S. Yamaoka, and G. Courtois Posttranslational modifications of NEMO and its partners in NF-kappaB signaling Trends Cell Biol 16 2006 569 577 (Pubitemid 44636218)
23. S. Wagner, I. Carpentier, V. Rogov, M. Kreike, F. Ikeda, and F. Lohr Ubiquitin binding mediates the NF-kappaB inhibitory potential of ABIN proteins Oncogene 27 2008 3739 3745 (Pubitemid 351912974)
24. C.K. Ea, L. Deng, Z.P. Xia, G. Pineda, and Z.J. Chen Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO Mol Cell 22 2006 245 257
25. C.J. Wu, D.B. Conze, T. Li, S.M. Srinivasula, and J.D. Ashwell Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-kappaB activation Nat Cell Biol 8 2006 398 406
26. Y.C. Lo, S.C. Lin, C.C. Rospigliosi, D.B. Conze, C.J. Wu, and J.D. Ashwell Structural basis for recognition of diubiquitins by NEMO Mol Cell 33 2009 602 615
27. S. Rahighi, F. Ikeda, M. Kawasaki, M. Akutsu, N. Suzuki, and R. Kato Specific recognition of linear ubiquitin chains by NEMO is important for NF-kappaB activation Cell 136 2009 1098 1109
28. A. Yoshikawa, Y. Sato, M. Yamashita, H. Mimura, A. Yamagata, and S. Fukai Crystal structure of the NEMO ubiquitin-binding domain in complex with Lys 63-linked di-ubiquitin FEBS Lett 583 2009 3317 3322
29. F. Cordier, E. Vinolo, M. Veron, M. Delepierre, and F. Agou Solution structure of NEMO zinc-finger and impact of an anhidrotic ectodermal dysplasia with immunodeficiency-related point mutation J Mol Biol 377 2008 1419 1432
30. F. Cordier, O. Grubisha, F. Traincard, M. Veron, M. Delepierre, and F. Agou The zinc finger of NEMO is a functional ubiquitin-binding domain J Biol Chem 284 2009 2902 2907
31. E. Laplantine, E. Fontan, J. Chiaravalli, T. Lopez, G. Lakisic, and M. Veron NEMO specifically recognizes K63-linked poly-ubiquitin chains through a new bipartite ubiquitin-binding domain EMBO J 28 2009 2885 2895
32. V. Baud, and M. Karin Is, NF-kappaB a good target for cancer therapy? Hopes and pitfalls Nat Rev Drug Discov 8 2009 33 40
33. M. Karin, and F.R. Greten NF-kappaB: linking inflammation and immunity to cancer development and progression Nat Rev Immunol 5 2005 749 759 (Pubitemid 41400849)
34. H.J. Kim, N. Hawke, A.S. Baldwin, and NF-kappaB IKK as therapeutic targets in cancer Cell Death Differ 13 2006 738 747
35. D. Legarda-Addison, H. Hase, M.A. O'Donnell, and A.T. Ting NEMO/IKKgamma regulates an early NF-kappaB-independent cell-death checkpoint during TNF signaling Cell Death Differ 16 2009 1279 1288
36. K. Nagashima, V.G. Sasseville, D. Wen, A. Bielecki, H. Yang, and C. Simpson Rapid TNFR1-dependent lymphocyte depletion in vivo with a selective chemical inhibitor of IKKbeta Blood 107 2006 4266 4273 (Pubitemid 43801350)
37. R. Doffinger, A. Smahi, C. Bessia, F. Geissmann, J. Feinberg, and A. Durandy X-linked anhidrotic ectodermal dysplasia with immunodeficiency is caused by impaired NF-kappaB signaling Nat Genet 27 2001 277 285 (Pubitemid 32201848)
38. S. Bloor, G. Ryzhakov, S. Wagner, P.J. Butler, D.L. Smith, and R. Krumbach Signal processing by its coil zipper domain activates IKK gamma Proc Natl Acad Sci USA 105 2008 1279 1284 (Pubitemid 351397044)
39. E.W. Harhaj, L. Good, G. Xiao, M. Uhlik, M.E. Cvijic, and I. Rivera-Walsh Somatic mutagenesis studies of NF-kappa B signaling in human T cells: evidence for an essential role of IKK gamma in NF-kappa B activation by T-cell costimulatory signals and HTLV-I Tax protein Oncogene 19 2000 1448 1456 (Pubitemid 30171176)
40. E. Fontan, F. Traincard, S.G. Levy, S. Yamaoka, M. Veron, and F. Agou NEMO oligomerization in the dynamic assembly of the IkappaB kinase core complex FEBS J 274 2007 2540 2551 (Pubitemid 46669339)
41. F. Mousson, Y.M. Coic, F. Baleux, V. Beswick, A. Sanson, and J.M. Neumann Deciphering the role of individual acyl chains in the interaction network between phosphatidylserines and a single-spanning membrane protein Biochemistry 41 2002 13611 13616 (Pubitemid 35332697)
42. G. Courtois, S.T. Whiteside, C.H. Sibley, and A. Israel Characterization of a mutant cell line that does not activate NF-kappaB in response to multiple stimuli Mol Cell Biol 17 1997 1441 1449 (Pubitemid 27097373)
43. F. Agou, F. Traincard, E. Vinolo, G. Courtois, S. Yamaoka, and A. Israel The trimerization domain of NEMO is composed of the interacting C-terminal CC2 and LZ coiled-coil subdomains J Biol Chem 279 2004 27861 27869 (Pubitemid 38900054)
44. E. Wyler, M. Kaminska, Y.M. Coic, F. Baleux, M. Veron, and F. Agou Inhibition of NF-kappaB activation with designed ankyrin-repeat proteins targeting the ubiquitin-binding/oligomerization domain of NEMO Protein Sci 16 2007 2013 2022 (Pubitemid 47367124)
45. S.W. Jones, R. Christison, K. Bundell, C.J. Voyce, S.M. Brockbank, and P. Newham Characterisation of cell-penetrating peptide-mediated peptide delivery Br J Pharmacol 145 2005 1093 1102 (Pubitemid 43079982)
46. J.S. Wadia, and S.F. Dowdy Transmembrane delivery of protein and peptide drugs by TAT-mediated transduction in the treatment of cancer Adv Drug Deliv Rev 57 2005 579 596 (Pubitemid 40255562)
47. A.D. Sharrocks The ETS-domain transcription factor family Nat Rev Mol Cell Biol 2 2001 827 837 (Pubitemid 33674083)
48. F. Mechta-Grigoriou, D. Gerald, and M. Yaniv The mammalian Jun proteins: redundancy and specificity Oncogene 20 2001 2378 2389 (Pubitemid 32531296)
49. G.R. Crabtree, and E.N. Olson NFAT signaling: choreographing the social lives of cells Cell 109 Suppl. 2002 S67 S79
50. S. Papa, C. Bubici, F. Zazzeroni, C.G. Pham, C. Kuntzen, and J.R. Knabb The NF-kappaB-mediated control of the JNK cascade in the antagonism of programmed cell death in health and disease Cell Death Differ 13 2006 712 729
51. G.L. Bidwell 3rd, and D. Raucher Therapeutic peptides for cancer therapy. Part I - peptide inhibitors of signal transduction cascades Expert Opin Drug Deliv 6 2009 1033 1047
52. R.E. Moellering, M. Cornejo, T.N. Davis, C. Del Bianco, J.C. Aster, and S.C. Blacklow Direct inhibition of the NOTCH transcription factor complex Nature 462 2009 182 188
53. G.G. Prive, and A. Melnick Specific peptides for the therapeutic targeting of oncogenes Curr Opin Genet Dev 16 2006 71 77 (Pubitemid 43089615)
54. D. Raucher, S. Moktan, I. Massodi, and G.L. Bidwell 3rd Therapeutic peptides for cancer therapy. Part II - cell cycle inhibitory peptides and apoptosis-inducing peptides Expert Opin Drug Deliv 6 2009 1049 1064
55. Y. Sato, A. Yoshikawa, M. Yamashita, A. Yamagata, and S. Fukai Structural basis for specific recognition of Lys 63-linked polyubiquitin chains by NZF domains of TAB2 and TAB3 EMBO J 28 2009 3903 3909
56. A. Acharya, V. Rishi, and C. Vinson Stability of 100 homo and heterotypic coiled-coil a-a' pairs for ten amino acids (A, L, I, V, N, K, S, T, E, and R) Biochemistry 45 2006 11324 11332 (Pubitemid 44453980)
57. G. Grigoryan, and A.E. Keating Structural specificity in coiled-coil interactions Curr Opin Struct Biol 18 2008 477 483
58. R.A. Kammerer, T. Schulthess, R. Landwehr, A. Lustig, J. Engel, and U. Aebi An autonomous folding unit mediates the assembly of two-stranded coiled coils Proc Natl Acad Sci USA 95 1998 13419 13424 (Pubitemid 128616256)
59. J.K. Myers, and T.G. Oas Reinterpretation of GCN4-p1 folding kinetics: partial helix formation precedes dimerization in coiled coil folding J Mol Biol 289 1999 205 210
60. M.O. Steinmetz, I. Jelesarov, W.M. Matousek, S. Honnappa, W. Jahnke, and J.H. Missimer Molecular basis of coiled-coil formation Proc Natl Acad Sci USA 104 2007 7062 7067 (Pubitemid 47186009)
61. M.J. Bertrand, S. Milutinovic, K.M. Dickson, W.C. Ho, A. Boudreault, and J. Durkin cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination Mol Cell 30 2008 689 700 (Pubitemid 351818251)
62. E. Varfolomeev, T. Goncharov, A.V. Fedorova, J.N. Dynek, K. Zobel, and K. Deshayes c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor alpha (TNFalpha)-induced NF-kappaB activation J Biol Chem 283 2008 24295 24299
63. L. Deng, C. Wang, E. Spencer, L. Yang, A. Braun, and J. You Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain Cell 103 2000 351 361
64. Q. Yin, B. Lamothe, B.G. Darnay, and H. Wu Structural basis for the lack of E2 interaction in the RING domain of TRAF2 Biochemistry 48 2009 10558 10567
65. Q. Yin, S.C. Lin, B. Lamothe, M. Lu, Y.C. Lo, and G. Hura E2 interaction and dimerization in the crystal structure of TRAF6 Nat Struct Mol Biol 16 2009 658 666
66. S.M. Park, J.B. Yoon, and T.H. Lee Receptor interacting protein is ubiquitinated by cellular inhibitor of apoptosis proteins (c-IAP1 and c-IAP2) in vitro FEBS Lett 566 2004 151 156 (Pubitemid 38625950)
67. M.J. May, F. D'Acquisto, L.A. Madge, J. Glockner, J.S. Pober, and S. Ghosh Selective inhibition of NF-kappaB activation by a peptide that blocks the interaction of NEMO with the IkappaB kinase complex Science 289 2000 1550 1554