Impediment of NEMO oligomerization inhibits osteoclastogenesis and osteolysis

Journal of Cellular Biochemistry

Volumn 108, Issue 6, 2009, Pages 1337-1345

  Darwech, Isra ^a   Otero, Jesse ^a   Alhawagri, Muhammad ^a   Dai, Simon ^a   Abu Amer, Yousef ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Coiled coil; Leucine zipper; NEMO IKK ; NF B; Osteoclast; Osteolysis

Indexed keywords

I KAPPA B KINASE GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MONOMER; MUTANT PROTEIN; OSTEOCLAST DIFFERENTIATION FACTOR; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR; UBIQUITIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW DERIVED OSTEOCLAST PRECURSOR; CELL MATURATION; CONTROLLED STUDY; KNOCKOUT GENE; MOUSE; NONHUMAN; OLIGOMERIZATION; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN MOTIF; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; NF-KAPPA B; OSTEOCLASTS; OSTEOLYSIS; RANK LIGAND; RNA, SMALL INTERFERING;

MUS;

EID: 71749083630     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22364     Document Type: Article

References (37)

1. Abu-Amer Y. 2003. Mechanisms of inflammatory mediators in bone loss diseases. In: Rosier RN, Evans CH, editors. Molecular biology in orthopedics. Rosemont, Illinois: AAOS. pp 229-239.
2. Abu-Amer Y, Ross FP, Edwards J, Teitelbaum SL. 1997. Lipopolysaccharide- stimulated osteoclastogenesis is mediated by tumor necrosis factor via its p55 receptor. J Clin Invest 100:1557-1565. (Pubitemid 27425783)
3. Abu-Amer Y, Dowdy S, Ross F, Clohisy J, Teitelbaum S. 2001. TAT fusion proteins containing tyrosine 42-deleted IkBa arrest osteoclastogenesis. J Biol Chem 276:30499-30503. (Pubitemid 37385138)
4. Agou F, Ye F, Goffinont S, Courtois G, Yamaoka S, Israel A, Veron M. 2002. NEMO trimerizes through its coiled-coil C-terminal domain. J Biol Chem 277:17464-17475. (Pubitemid 34967546)
5. Agou F, Courtois G, Chiaravalli J, Baleux F, Coic Y-M, Traincard F, Israel A, Veron M. 2004a. Inhibition of NF-{kappa}B activation by peptides targeting NF-{kappa}B essential modulator (NEMO) oligomerization. J Biol Chem 279:54248-54257. (Pubitemid 40053162)
6. Agou F, Traincard F, Vinolo E, Courtois G, Yamaoka S, Israel A, Veron M. 2004b. The trimerization domain of NEMO is composed of the interacting C-terminal CC2 and LZ coiled-coil subdomains. J Biol Chem 279:27861-27869. (Pubitemid 38900054)
7. Baldwin AS, Jr. 1996. The NF-kB and IkB proteins: New discoveries and insights. [Review] [180 refs]. Annu Rev Immunol 14:649-683.
8. Bloor S, Ryzhakov G, Wagner S, Butler PJG, Smith DL, Krumbach R, Dikic I, Randow F. 2008. Signal processing by its coil zipper domain activates IKK{gamma}. Proc Natl Acad Sci 105:1279-1284.
9. Burns KA, Martinon F. 2004. Inflammatory diseases: Is ubiquitinated NEMO at the hub? Curr Biol 14:R1040-R1042.
10. Chaisson ML, Branstetter DG, Derry JM, Armstrong AP, Tometsko ME, Takeda K, Akira S, Dougall WC. 2004. Osteoclast differentiation is impaired in the absence of IkB kinase-alpha. J Biol Chem 279:54841-54848.
11. Clohisy JC, Roy BC, Biondo C, Frazier E, Willis D, Teitelbaum SL, Abu-Amer Y. 2003. Direct inhibition of NF-kappa B blocks bone erosion associated with inflammatory arthritis. J Immunol 171:5547-5553. (Pubitemid 37432845)
12. Courtois G, Smahi A, Israel A. 2001. NEMO/IKK-gamma: Linking NF-kB to human disease. Trends Mol Med 7:427-430. (Pubitemid 32964151)
13. Dai S, Hirayama T, Abbas S, Abu-Amer Y. 2004. The IkappaB kinase (IKK) inhibitor, NEMO-binding domain peptide, blocks osteoclastogenesis and bone erosion in inflammatory arthritis. J Biol Chem 279:37219-37222. (Pubitemid 39195425)
14. DiDonato J, Hayakawa M, Rothwarf D, Zandi E, Karin M. 1997. A cytokine-responsive I-κB kinase that activates the transcription factor Nf-kB. Nature 388:548-554. (Pubitemid 27339997)
15. Franzoso G, Carlson L, Poljak L, Shores E, Brown K, Leonardi A, Tran T, Boyce B, Siebenlist U. 1997. Requirment for NF-kB in osteoclast and B-cell development. Genes Dev 11:3482-3496. (Pubitemid 28023969)
16. Hirayama T, Dai S, Abbas S, Yamanaka Y, Abu-Amer Y. 2005. Inhibition of inflammatory bone erosion by constitutively active STAT-6 through blockade of JNK and NF-kB activation. Arthritis Rheum 52:2719-2729. (Pubitemid 41369100)
17. Jimi E, Aoki K, Saito H, D'Acquisto F, May MJ, Nakamura I, Sudo T, Kojima T, Okamoto F, Fukushima H, Okabe K, Ohya K, Ghosh S. 2004. Selective inhibition of NF-kappa B blocks osteoclastogenesis and prevents inflammatory bone destruction in vivo. Nat Med 10:617-624. (Pubitemid 38796853)
18. Karin M. 2008. The IkappaB kinase-A bridge between inflammation and cancer. Cell Res 18:334-342. (Pubitemid 351333897)
19. Karin M, Yamamoto Y, Wang M. 2004. The IKK NF-kB system: A treasure trove for drug development. Nat Rev 3:17-26. (Pubitemid 38088695)
20. Ku CL, Dupuis-Girod S, Dittrich AM, Bustamante J, Santos OF, Schulze I, Bertrand Y, Couly G, Bodemer C, Bossuyt X, Picard C, Casanova JL. 2005. NEMO mutations in 2 unrelated boys with severe infections and conical teeth. Pediatrics 115:e615-e619. (Pubitemid 43843220)
21. Lawrence T, Bebien M, Liu GY, Nizet V, Karin M. 2005. IKK-alpha-limits macrophage NF-kB activation and contributes to the resolution of inflammation. Nature 434:1138-1143. (Pubitemid 40663493)
22. Li Q, Lu Q, Bottero V, Estepa G, Morrison L, Mercurio F, Verma IM. 2005. Enhanced NF-kB activation and cellular function in macrophages lacking IkB kinase 1 (IKK1). Proc Natl Acad Sci 102(35):12425-12430. (Pubitemid 41266375)
23. May MJ, D'Acquisto F, Madge LA, Glockner J, Pober JS, Ghosh S. 2000. Selective inhibition of NF-kappa B activation by a peptide that blocks the interaction of NEMO with the Ikappa B kinase complex. Science 289:1550-1554. (Pubitemid 30677473)
24. May MJ, Marienfeld RB, Ghosh S. 2002. Characterization of the Ikappa B-kinase NEMO binding domain. J Biol Chem 277:45992-46000. (Pubitemid 35417584)
25. Mercurio F, Zhu H, Murray BW, Shevchenko A, Bennett BL, Li J, Young DB, Barbosa M, Mann M, Manning A, Rao A. 1997. IKK-1 and IKK-2: Cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science (New York, NY) 278:860-866. (Pubitemid 27467923)
26. Ni C-Y, Wu Z-H, Florence WC, Parekh VV, Arrate MP, Pierce S, Schweitzer B, Van Kaer L, Joyce S, Miyamoto S, Ballard DW, Oltz EM. 2008. Cutting edge: K63-linked polyubiquitination of NEMO modulates TLR signaling and inflammation in vivo. J Immunol 180:7107-7111.
27. Novack DV, Yin L, Hagen-Stapleton A, Schreiber RD, Goeddel DV, Ross FP, Teitelbaum SL. 2003. The I-kappaB function of NF-kappaB2 p100 controls stimulated osteoclastogenesis. J Exp Med 198:771-781. (Pubitemid 37087776)
28. Otero JE, Dai S, Foglia D, Alhawagri M, Vacher J, Pasparakis M, Abu-Amer Y. 2008. Defective osteoclastogenesis by IKKbeta-null precursors is a result of receptor activator of NF-kappaB ligand (RANKL)-induced JNK-dependent apoptosis and impaired differentiation. J Biol Chem 283: 24546-24553.
29. Regnier C, Song H, Gao X, Goeddel D, Cao Z, Rothe M. 1997. Identification and characterization of an I-κB kinase. Cell 90:373-383.
30. Ruocco MG, Maeda S, Park JM, Lawrence T, Hsu L-C, Cao Y, Schett G, Wagner EF, Karin M. 2005. IkB kinase-beta, but not IKK-alpha, is a critical mediator of osteoclast survival and is required for inflammation-induced bone loss. J Exp Med 201:1677-1687. (Pubitemid 40721011)
31. Shibata W, Maeda S, Hikiba Y, Yanai A, Ohmae T, Sakamoto K, Nakagawa H, Ogura K, Omata M. 2007. Cutting edge: The I{kappa}B kinase (IKK) inhibitor, NEMO-binding domain peptide, blocks inflammatory injury in murine colitis. J Immunol 179:2681-2685.
32. Stancovski I, Baltimore D. 1997. NF-kB activation: The IkB kinase revealed? Cell 91:299-302.
33. Tegethoff S, Behlke J, Scheidereit C. 2003. Tetrameric oligomerization of IkappaB kinase gamma (IKKgamma) is obligatory for IKK complex activity and NF-kappaB activation. Mol Cell Biol 23:2029-2041. (Pubitemid 36278814)
34. Tokunaga F, Sakata S-I, Saeki Y, Satomi Y, Kirisako T, Kamei K, Nakagawa T, Kato M, Murata S, Yamaoka S, Yamamoto M, Akira S, Takao T, Tanaka K, Iwai K. 2009. Involvement of linear polyubiquitylation of NEMO in NF-[kappa]B activation. Nat Cell Biol 11:123-132.
35. Vaira S, Alhawagri M, Anwisye I, Kitaura H, Faccio R, Novack DV. 2008a. RelA/p65 promotes osteoclast differentiation by blocking a RANKL-induced apoptotic JNK pathway in mice. J Clin Invest 118:2088-2097. (Pubitemid 351872328)
36. Vaira S, Johnson T, Hirbe AC, Alhawagri M, Anwisye I, Sammut B, O'Neal J, Zou W, Weilbaecher KN, Faccio R, Novack DV. 2008b. RelB is the NF-kappaB subunit downstream of NIK responsible for osteoclast differentiation. Proc Natl Acad Sci USA 105:3897-3902. (Pubitemid 351723496)
37. Wu CJ, Conze DB, Li T, Srinivasula SM, Ashwell JD. 2006. Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-kappaB activation [corrected]. Nat Cell Biol 8:398-406.