A novel role for the histone acetyltransferase Hat1 in the CENP-A/CID assembly pathway in Drosophila melanogaster

Nucleic Acids Res. 2016 Mar 18;44(5):2145-59. doi: 10.1093/nar/gkv1235. Epub 2015 Nov 19.

Abstract

The incorporation of CENP-A into centromeric chromatin is an essential prerequisite for kinetochore formation. Yet, the molecular mechanisms governing this process are surprisingly divergent in different organisms. While CENP-A loading mechanisms have been studied in some detail in mammals, there are still large gaps to our understanding of CENP-A/Cid loading pathways in Drosophila. Here, we report on the characterization and delineation of at least three different CENP-A preloading complexes in Drosophila. Two complexes contain the CENP-A chaperones CAL1, FACT and/or Caf1/Rbap48. Notably, we identified a novel complex consisting of the histone acetyltransferase Hat1, Caf1 and CENP-A/H4. We show that Hat1 is required for proper CENP-A loading into chromatin, since knock-down in S2 cells leads to reduced incorporation of newly synthesized CENP-A. In addition, we demonstrate that CENP-A/Cid interacts with the HAT1 complex via an N-terminal region, which is acetylated in cytoplasmic but not in nuclear CENP-A. Since Hat1 is not responsible for acetylation of CENP-A/Cid, these results suggest a histone acetyltransferase activity-independent escort function for Hat1. Thus, our results point toward intriguing analogies between the complex processing pathways of newly synthesized CENP-A and canonical histones.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Amino Acid Sequence
  • Animals
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Line
  • Cell Nucleus / metabolism
  • Cell Nucleus / ultrastructure
  • Centromere Protein A
  • Chromatin / metabolism*
  • Chromatin / ultrastructure
  • Cytoplasm / metabolism
  • Cytoplasm / ultrastructure
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / metabolism*
  • Gene Expression Regulation
  • Histone Acetyltransferases / genetics*
  • Histone Acetyltransferases / metabolism
  • Histones / genetics*
  • Histones / metabolism
  • Kinetochores / metabolism*
  • Kinetochores / ultrastructure
  • Molecular Sequence Data
  • Plasmids / chemistry
  • Plasmids / metabolism
  • Retinoblastoma-Binding Protein 4 / genetics
  • Retinoblastoma-Binding Protein 4 / metabolism
  • Signal Transduction
  • Transfection

Substances

  • Caf1-55 protein, Drosophila
  • Cal1 protein, Drosophila
  • Carrier Proteins
  • Centromere Protein A
  • Chromatin
  • Cid protein, Drosophila
  • DNA-Binding Proteins
  • Drosophila Proteins
  • FACT protein, Drosophila
  • Histones
  • Retinoblastoma-Binding Protein 4
  • Histone Acetyltransferases
  • histone acetyltransferase type B complex