Exogenous signal-independent nuclear IκB kinase activation triggered by Nkx3.2 enables constitutive nuclear degradation of IκB-α in chondrocytes

Molecular and Cellular Biology

Volumn 31, Issue 14, 2011, Pages 2802-2816

  Yong, Yeryoung ^a   Choi, Seung Won ^a   Choi, Hye Jeong ^a   Nam, Hyung Wook ^a   Kim, Jeong Ah ^a   Jeong, Da Un ^a   Kim, Don Young ^a   Kim, Yu Sam ^a   Kim, Dae Won ^a  

^a Yonsei University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B ALPHA; I KAPPA B KINASE BETA; I KAPPA B KINASE GAMMA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX3.2; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CARTILAGE CELL; CELL NUCLEUS; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BETA-TRANSDUCIN REPEAT-CONTAINING PROTEINS; CELL LINE; CELL NUCLEUS; CHONDROCYTES; HOMEODOMAIN PROTEINS; HUMANS; I-KAPPA B KINASE; I-KAPPA B PROTEINS; MICE; MOLECULAR SEQUENCE DATA; NF-KAPPA B; RNA, SMALL INTERFERING; SERINE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UBIQUITIN;

EID: 79960367011     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00253-10     Document Type: Article

References (48)

1. Adli, M., E. Merkhofer, P. Cogswell, and A. S. Baldwin. 2010. IKKalpha and IKKbeta each function to regulate NF-kappaB activation in the TNF-induced/canonical pathway. PLoS One 5:e9428
2. Beg, A. A., W. C. Sha, R. T. Bronson, S. Ghosh, and D. Baltimore. 1995. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature 376:167-170.
3. Chen, Z., et al. 1995. Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev. 9:1586-1597.
4. Chen, Z. J. 2005. Ubiquitin signalling in the NF-kappaB pathway. Nat. Cell Biol. 7:758-765.
5. Chen, Z. J., L. Parent, and T. Maniatis. 1996. Site-specific phosphorylation of IkappaBalpha by a novel ubiquitination-dependent protein kinase activity. Cell 84:853-862.
6. DiDonato, J. A., M. Hayakawa, D. M. Rothwarf, E. Zandi, and M. Karin. 1997. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature 388:548-554.
7. Doffinger, R., et al. 2001. X-linked anhidrotic ectodermal dysplasia with immunodeficiency is caused by impaired NF-kappaB signaling. Nat. Genet. 27:277-285.
8. Dull, T., et al. 1998. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72:8463-8471.
9. Ea, C. K., L. Deng, Z. P. Xia, G. Pineda, and Z. J. Chen. 2006. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 22:245-257.
10. Gerondakis, S., M. Grossmann, Y. Nakamura, T. Pohl, and R. Grumont. 1999. Genetic approaches in mice to understand Rel/NF-kappaB and IkappaB function: transgenics and knockouts. Oncogene 18:6888-6895.
11. Hacker, H., and M. Karin. 2006. Regulation and function of IKK and IKK-related kinases. Sci. STKE 2006:re13.
12. Hatakeyama, S., et al. 1999. Ubiquitin-dependent degradation of IkappaBalpha is mediated by a ubiquitin ligase Skp1/Cul 1/F-box protein FWD1. Proc. Natl. Acad. Sci. U. S. A. 96:3859-3863.
13. Hayden, M. S., and S. Ghosh. 2004. Signaling to NF-kappaB. Genes Dev. 18:2195-2224.
14. Hu, C. D., Y. Chinenov, and T. K. Kerppola. 2002. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9:789-798.
15. Hu, Y., et al. 1999. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKalpha subunit of IkappaB kinase. Science 284:316-320.
16. Janssen, R., et al. 2004. The same IkappaBalpha mutation in two related individuals leads to completely different clinical syndromes. J. Exp. Med. 200:559-568.
17. Kanegae, Y., A. T. Tavares, J. C. Izpisua Belmonte, and I. M. Verma. 1998. Role of Rel/NF-kappaB transcription factors during the outgrowth of the vertebrate limb. Nature 392:611-614.
18. Karin, M., and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18:621-663.
19. Kim, D. W., H. Kempf, R. E. Chen, and A. B. Lassar. 2003. Characterization of Nkx3.2 DNA binding specificity and its requirement for somitic chondrogenesis. J. Biol. Chem. 278:27532-27539.
20. Kim, D. W., and A. B. Lassar. 2003. Smad-dependent recruitment of a histone deacetylase/Sin3A complex modulates the bone morphogenetic protein-dependent transcriptional repressor activity of Nkx3.2. Mol. Cell. Biol. 23:8704-8717.
21. Li, Q., S. Withoff, and I. M. Verma. 2005. Inflammation-associated cancer: NF-kappaB is the lynchpin. Trends Immunol. 26:318-325.
22. Li, Z. W., et al. 1999. The IKKbeta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis. J. Exp. Med. 189:1839-1845.
23. Meffert, M. K., and D. Baltimore. 2005. Physiological functions for brain NF-kappaB. Trends Neurosci. 28:37-43.
24. Mercurio, F., et al. 1997. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 278:860-866.
25. Murtaugh, L. C., L. Zeng, J. H. Chyung, and A. B. Lassar. 2001. The chick transcriptional repressor Nkx3.2 acts downstream of Shh to promote BMPdependent axial chondrogenesis. Dev. Cell 1:411-422.
26. Oeckinghaus, A., and S. Ghosh. 2009. The NF-kappaB family of transcription factors and its regulation. Cold Spring Harb. Perspect. Biol. 1:a000034.
27. Oshima, S., et al. 2009. ABIN-1 is a ubiquitin sensor that restricts cell death and sustains embryonic development. Nature 457:906-909.
28. Park, M., et al. 2007. Constitutive RelA activation mediated by Nkx3.2 controls chondrocyte viability. Nat. Cell Biol. 9:287-298.
29. Provot, S., et al. 2006. Nkx3.2/Bapx1 acts as a negative regulator of chondrocyte maturation. Development 133:651-662.
30. Rothwarf, D. M., and M. Karin. 1999. The NF-kappa B activation pathway: a paradigm in information transfer from membrane to nucleus. Sci. STKE 1999:RE1.
31. Rothwarf, D. M., E. Zandi, G. Natoli, and M. Karin. 1998. IKK-gamma is an essential regulatory subunit of the IkappaB kinase complex. Nature 395:297-300.
32. Scherer, D. C., J. A. Brockman, Z. Chen, T. Maniatis, and D. W. Ballard. 1995. Signal-induced degradation of I kappa B alpha requires site-specific ubiquitination. Proc. Natl. Acad. Sci. U. S. A. 92:11259-11263.
33. Skowyra, D., K. L. Craig, M. Tyers, S. J. Elledge, and J. W. Harper. 1997. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209-219.
34. Tang, E. D., C. Y. Wang, Y. Xiong, and K. L. Guan. 2003. A role for NF-kappaB essential modifier/IkappaB kinase-gamma (NEMO/IKKgamma) ubiquitination in the activation of the IkappaB kinase complex by tumor necrosis factor-alpha. J. Biol. Chem. 278:37297-37305.
35. Tokunaga, F., et al. 2009. Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat. Cell Biol. 11:123-132.
36. Traenckner, E. B., et al. 1995. Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha proteolysis and NF-kappa B activation in response to diverse stimuli. EMBO J. 14:2876-2883.
37. Tribioli, C., and T. Lufkin. 1997. Molecular cloning, chromosomal mapping and developmental expression of BAPX1, a novel human homeobox-containing gene homologous to Drosophila bagpipe. Gene 203:225-233.
38. Tsukahara, T., et al. 1999. Induction of Bcl-x(L) expression by human T-cell leukemia virus type 1 Tax through NF-kappaB in apoptosis-resistant T-cell transfectants with Tax. J. Virol. 73:7981-7987.
39. Vallabhapurapu, S., and M. Karin. 2009. Regulation and function of NFkappaB transcription factors in the immune system. Annu. Rev. Immunol. 27:693-733.
40. Windheim, M., M. Stafford, M. Peggie, and P. Cohen. 2008. Interleukin-1 (IL-1) induces the Lys63-linked polyubiquitination of IL-1 receptor-associated kinase 1 to facilitate NEMO binding and the activation of IkappaBalpha kinase. Mol. Cell. Biol. 28:1783-1791.
41. Wu, C. J., D. B. Conze, T. Li, S. M. Srinivasula, and J. D. Ashwell. 2006. Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-kappaB activation [corrected]. Nat. Cell Biol. 8:398-406.
42. Wu, G., et al. 2003. Structure of a beta-TrCP1-Skp1-beta-catenin complex: destruction motif binding and lysine specificity of the SCF(beta-TrCP1) ubiquitin ligase. Mol. Cell 11:1445-1456.
43. Wu, S., J. K. Flint, G. Rezvani, and F. De Luca. 2007. Nuclear factor-kappaB p65 facilitates longitudinal bone growth by inducing growth plate chondrocyte proliferation and differentiation and by preventing apoptosis. J. Biol. Chem. 282:33698-33706.
44. Yamaoka, S., et al. 1998. Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation. Cell 93:1231-1240.
45. Zaffran, S., and M. Frasch. 2005. The homeodomain of Tinman mediates homo- and heterodimerization of NK proteins. Biochem. Biophys. Res. Commun. 334:361-369.
46. Zandi, E., D. M. Rothwarf, M. Delhase, M. Hayakawa, and M. Karin. 1997. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation. Cell 91:243-252.
47. Zeng, L., H. Kempf, L. C. Murtaugh, M. E. Sato, and A. B. Lassar. 2002. Shh establishes an Nkx3.2/Sox9 autoregulatory loop that is maintained by BMP signals to induce somitic chondrogenesis. Genes Dev. 16:1990-2005.
48. Zhou, H., et al. 2004. Bcl10 activates the NF-kappaB pathway through ubiquitination of NEMO. Nature 427:167-171.