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Structure paper

TitleStructural basis of nucleosome recognition and modification by MLL methyltransferases.
Journal, issue, pagesNature, Vol. 573, Issue 7774, Page 445-449, Year 2019
Publish dateSep 4, 2019
AuthorsHan Xue / Tonghui Yao / Mi Cao / Guanjun Zhu / Yan Li / Guiyong Yuan / Yong Chen / Ming Lei / Jing Huang /
PubMed AbstractMethyltransferases of the mixed-lineage leukaemia (MLL) family-which include MLL1, MLL2, MLL3, MLL4, SET1A and SET1B-implement methylation of histone H3 on lysine 4 (H3K4), and have critical and ...Methyltransferases of the mixed-lineage leukaemia (MLL) family-which include MLL1, MLL2, MLL3, MLL4, SET1A and SET1B-implement methylation of histone H3 on lysine 4 (H3K4), and have critical and distinct roles in the regulation of transcription in haematopoiesis, adipogenesis and development. The C-terminal catalytic SET (Su(var.)3-9, enhancer of zeste and trithorax) domains of MLL proteins are associated with a common set of regulatory factors (WDR5, RBBP5, ASH2L and DPY30) to achieve specific activities. Current knowledge of the regulation of MLL activity is limited to the catalysis of histone H3 peptides, and how H3K4 methyl marks are deposited on nucleosomes is poorly understood. H3K4 methylation is stimulated by mono-ubiquitination of histone H2B on lysine 120 (H2BK120ub1), a prevalent histone H2B mark that disrupts chromatin compaction and favours open chromatin structures, but the underlying mechanism remains unknown. Here we report cryo-electron microscopy structures of human MLL1 and MLL3 catalytic modules associated with nucleosome core particles that contain H2BK120ub1 or unmodified H2BK120. These structures demonstrate that the MLL1 and MLL3 complexes both make extensive contacts with the histone-fold and DNA regions of the nucleosome; this allows ease of access to the histone H3 tail, which is essential for the efficient methylation of H3K4. The H2B-conjugated ubiquitin binds directly to RBBP5, orienting the association between MLL1 or MLL3 and the nucleosome. The MLL1 and MLL3 complexes display different structural organizations at the interface between the WDR5, RBBP5 and MLL1 (or the corresponding MLL3) subunits, which accounts for the opposite roles of WDR5 in regulating the activity of the two enzymes. These findings transform our understanding of the structural basis for the regulation of MLL activity at the nucleosome level, and highlight the pivotal role of nucleosome regulation in histone-tail modification.
External linksNature / PubMed:31485071
MethodsEM (single particle)
Resolution3.2 - 4.5 Å
Structure data

EMDB-0693, PDB-6kiw:
Cryo-EM structure of human MLL3-ubNCP complex (4.0 angstrom)
Method: EM (single particle) / Resolution: 4 Å

EMDB-0694, PDB-6kix:
Cryo-EM structure of human MLL1-NCP complex, binding mode1
Method: EM (single particle) / Resolution: 4.1 Å

EMDB-0695, PDB-6kiz:
Cryo-EM structure of human MLL1-NCP complex, binding mode2
Method: EM (single particle) / Resolution: 4.5 Å

EMDB-9998, PDB-6kiu:
Cryo-EM structure of human MLL1-ubNCP complex (3.2 angstrom)
Method: EM (single particle) / Resolution: 3.2 Å

EMDB-9999, PDB-6kiv:
Cryo-EM structure of human MLL1-ubNCP complex (4.0 angstrom)
Method: EM (single particle) / Resolution: 4 Å

Chemicals

ChemComp-SAH:
S-ADENOSYL-L-HOMOCYSTEINE / S-Adenosyl-L-homocysteine

ChemComp-ZN:
ZINC ION / Zinc

ChemComp-LYS:
LYSINE / Lysine

ChemComp-GLN:
GLUTAMINE / Glutamine

Source
  • homo sapiens (human)
  • xenopus laevis (African clawed frog)
  • synthetic construct (others)
KeywordsCryoelectron Microscopy / DNA-Binding Proteins / Enzyme Activation / Gene Expression Regulation, Enzymologic / Histone-Lysine N-Methyltransferase / Histones / Humans / KMT2A protein, human / KMT2C protein, human / Methylation / Models, Molecular / Myeloid-Lymphoid Leukemia Protein / Nucleosomes / Protein Structure, Quaternary / TRANSCRIPTION/DNA / histone modification / nucleosome / MLL / TRANSCRIPTION / TRANSCRIPTION-DNA complex

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