Abstract
NEMO is the regulatory subunit of the IkappaB kinase (IKK) in NF-kappaB activation, and its CC2-LZ region interacts with Lys63 (K63)-linked polyubiquitin to recruit IKK to receptor signaling complexes. In vitro, CC2-LZ also interacts with tandem diubiquitin. Here we report the crystal structure of CC2-LZ with two dimeric coiled coils representing CC2 and LZ, respectively. Surprisingly, mutagenesis and nuclear magnetic resonance experiments reveal that the binding sites for diubiquitins at LZ are composites of both chains and that each ubiquitin in diubiquitins interacts with symmetrical NEMO asymmetrically. For tandem diubiquitin, the first ubiquitin uses the conserved hydrophobic patch and the C-terminal tail, while the second ubiquitin uses an adjacent surface patch. For K63-linked diubiquitin, the proximal ubiquitin uses its conserved hydrophobic patch, while the distal ubiquitin mostly employs the C-terminal arm including the K63 linkage residue. These studies uncover the energetics and geometry for mutual recognition of NEMO and diubiquitins.
MeSH Terms
Amino Acid Sequence
Binding Sites
Cloning, Molecular
Conserved Sequence
Crystallography, X-Ray
Genetic Predisposition to Disease
Humans
Hydrophobic and Hydrophilic Interactions
I-kappa B Kinase/chemistry,genetics,metabolism
Magnetic Resonance Spectroscopy
Models, Molecular
Molecular Sequence Data
Mutagenesis, Site-Directed
Mutation
NF-kappa B/metabolism
Protein Binding
Protein Conformation
Protein Multimerization
Protein Structure, Tertiary
Recombinant Proteins/chemistry
Structure-Activity Relationship
Ubiquitins/chemistry,metabolism
Chemicals
IKBKG protein, human
NF-kappa B
Recombinant Proteins
UBD protein, human
Ubiquitins
I-kappa B Kinase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Lo Yu-Chih
Department of Biochemistry, Weill Cornell Medical College, New York, NY 10021, USA.
Lin Su-Chang
Rospigliosi Carla C
Conze Dietrich B
Wu Chuan-Jin
Ashwell Jonathan D
Eliezer David
Wu Hao
References (22)
22 references, click to expand
-
NEMO recognition of ubiquitinated Bcl10 is required for T cell receptor-mediated NF-kappaB activation.
Proc Natl Acad Sci U S A. 2008 Feb 26;105(8):3023-8
PMID: 18287044
-
Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains.
Nature. 2008 Sep 18;455(7211):358-62
PMID: 18758443
-
Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO.
Mol Cell. 2006 Apr 21;22(2):245-57
PMID: 16603398
-
Structural determinants for selective recognition of a Lys48-linked polyubiquitin chain by a UBA domain.
Mol Cell. 2005 Jun 10;18(6):687-98
PMID: 15949443
-
IkappaB kinase complexes: gateways to NF-kappaB activation and transcription.
Oncogene. 2006 Oct 30;25(51):6685-705
PMID: 17072322
-
Malt1 ubiquitination triggers NF-kappaB signaling upon T-cell activation.
EMBO J. 2007 Nov 14;26(22):4634-45
PMID: 17948050
-
Ubiquitin binding mediates the NF-kappaB inhibitory potential of ABIN proteins.
Oncogene. 2008 Jun 12;27(26):3739-45
PMID: 18212736
-
Structure of tetraubiquitin shows how multiubiquitin chains can be formed.
J Mol Biol. 1994 Feb 18;236(2):601-9
PMID: 8107144
-
X-linked susceptibility to mycobacteria is caused by mutations in NEMO impairing CD40-dependent IL-12 production.
J Exp Med. 2006 Jul 10;203(7):1745-59
PMID: 16818673
-
Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation.
Nat Cell Biol. 2009 Feb;11(2):123-32
PMID: 19136968
-
Ubiquitin-binding domains.
Biochem J. 2006 Nov 1;399(3):361-72
PMID: 17034365
-
A point mutation in NEMO associated with anhidrotic ectodermal dysplasia with immunodeficiency pathology results in destabilization of the oligomer and reduces lipopolysaccharide- and tumor necrosis factor-mediated NF-kappa B activation.
J Biol Chem. 2006 Mar 10;281(10):6334-48
PMID: 16379012
-
Inhibition of the 26 S proteasome by polyubiquitin chains synthesized to have defined lengths.
J Biol Chem. 1997 Sep 19;272(38):23712-21
PMID: 9295315
-
HADDOCK: a protein-protein docking approach based on biochemical or biophysical information.
J Am Chem Soc. 2003 Feb 19;125(7):1731-7
PMID: 12580598
-
Identification of TRAF6-dependent NEMO polyubiquitination sites through analysis of a new NEMO mutation causing incontinentia pigmenti.
Hum Mol Genet. 2007 Dec 1;16(23):2805-15
PMID: 17728323
-
Ubiquitin signalling in the NF-kappaB pathway.
Nat Cell Biol. 2005 Aug;7(8):758-65
PMID: 16056267
-
NEMO trimerizes through its coiled-coil C-terminal domain.
J Biol Chem. 2002 May 17;277(20):17464-75
PMID: 11877453
-
Introduction to NF-kappaB: players, pathways, perspectives.
Oncogene. 2006 Oct 30;25(51):6680-4
PMID: 17072321
-
Intermolecular disulfide bond formation in the NEMO dimer requires Cys54 and Cys347.
Biochem Biophys Res Commun. 2008 Feb 29;367(1):103-8
PMID: 18164680
-
Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-kappaB activation [corrected].
Nat Cell Biol. 2006 Apr;8(4):398-406
PMID: 16547522
-
Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies.
Cell. 2008 Aug 22;134(4):668-78
PMID: 18724939
-
Mutations in the NF-kappaB signaling pathway: implications for human disease.
Oncogene. 2006 Oct 30;25(51):6831-43
PMID: 17072331