An emerin "proteome": purification of distinct emerin-containing complexes from HeLa cells suggests molecular basis for diverse roles including gene regulation, mRNA splicing, signaling, mechanosensing, and nuclear architecture

Biochemistry. 2007 Jul 31;46(30):8897-908. doi: 10.1021/bi602636m. Epub 2007 Jul 10.

Abstract

Using recombinant bead-conjugated emerin, we affinity-purified seven proteins from HeLa cell nuclear lysates that bind emerin either directly or indirectly. These proteins were identified by mass spectrometry as nuclear alphaII-spectrin, nonmuscle myosin heavy chain alpha, Lmo7 (a predicted transcription regulator; reported separately), nuclear myosin I, beta-actin (reported separately), calponin 3, and SIKE. We now report that emerin binds nuclear myosin I (NMI, a molecular motor) directly in vitro. Furthermore, bead-conjugated emerin bound nuclear alphaII-spectrin and NMI equally well with or without ATP (which stimulates motor activity), whereas ATP decreased actin binding by 65%. Thus alphaII-spectrin and NMI interact stably with emerin. To investigate the physiological relevance of these interactions, we used antibodies against emerin to affinity-purify emerin-associated protein complexes from HeLa cells and then further purified by ion-exchange chromatography to resolve by net charge and by size exclusion chromatography yielding six distinct emerin-containing fractions (0.5-1.6 MDa). Western blotting suggested that each complex had distinct components involved in nuclear architecture (e.g., NMI, alphaII-spectrin, lamins) or gene or chromatin regulation (BAF, transcription regulators, HDACs). Additional constituents were identified by mass spectrometry. One putative gene-regulatory complex (complex 32) included core components of the nuclear corepressor (NCoR) complex, which mediates gene regulation by thyroid hormone and other nuclear receptors. When expressed in HeLa cells, FLAG-tagged NCoR subunits Gps2, HDAC3, TBLR1, and NCoR each co-immunoprecipitated emerin, validating one putative complex. These findings support the hypothesis that emerin scaffolds a variety of functionally distinct multiprotein complexes at the nuclear envelope in vivo. Notably included are nuclear myosin I-containing complexes that might sense and regulate mechanical tension at the nuclear envelope.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Binding Sites / physiology
  • Cell Line, Tumor
  • Chromatin / metabolism
  • Chromatography, Affinity
  • Chromatography, Gel
  • Chromatography, Ion Exchange
  • HeLa Cells
  • Humans
  • Immunoprecipitation
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Membrane Proteins / chemistry
  • Membrane Proteins / isolation & purification
  • Membrane Proteins / physiology*
  • Multiprotein Complexes / metabolism*
  • Nuclear Matrix-Associated Proteins
  • Nuclear Proteins / chemistry
  • Nuclear Proteins / isolation & purification
  • Nuclear Proteins / physiology*
  • Protein Binding / physiology
  • Protein Biosynthesis
  • Proteome / isolation & purification
  • Proteome / metabolism*
  • Recombinant Fusion Proteins / metabolism
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization*
  • Transcription Factors / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Chromatin
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Multiprotein Complexes
  • Nuclear Matrix-Associated Proteins
  • Nuclear Proteins
  • Proteome
  • Recombinant Fusion Proteins
  • Transcription Factors
  • emerin