The HCMV Assembly Compartment Is a Dynamic Golgi-Derived MTOC that Controls Nuclear Rotation and Virus Spread

Dev Cell. 2018 Apr 9;45(1):83-100.e7. doi: 10.1016/j.devcel.2018.03.010.

Abstract

Human cytomegalovirus (HCMV), a leading cause of congenital birth defects, forms an unusual cytoplasmic virion maturation site termed the "assembly compartment" (AC). Here, we show that the AC also acts as a microtubule-organizing center (MTOC) wherein centrosome activity is suppressed and Golgi-based microtubule (MT) nucleation is enhanced. This involved viral manipulation of discrete functions of MT plus-end-binding (EB) proteins. In particular, EB3, but not EB1 or EB2, was recruited to the AC and was required to nucleate MTs that were rapidly acetylated. EB3-regulated acetylated MTs were necessary for nuclear rotation prior to cell migration, maintenance of AC structure, and optimal virus replication. Independently, a myristoylated peptide that blocked EB3-mediated enrichment of MT regulatory proteins at Golgi regions of the AC also suppressed acetylated MT formation, nuclear rotation, and infection. Thus, HCMV offers new insights into the regulation and functions of Golgi-derived MTs and the therapeutic potential of targeting EB3.

Keywords: Golgi; acetylation; cell migration; cytomegalovirus; end-binding protein; microtubule organizing center; nuclear rotation; virus infection.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Cell Movement
  • Cell Nucleus / physiology*
  • Cell Nucleus / virology
  • Cells, Cultured
  • Cytomegalovirus / genetics
  • Cytomegalovirus / isolation & purification
  • Cytomegalovirus / pathogenicity
  • Cytomegalovirus Infections / virology*
  • Golgi Apparatus / physiology
  • Golgi Apparatus / virology*
  • Humans
  • Microtubule-Associated Proteins / genetics
  • Microtubule-Associated Proteins / metabolism*
  • Microtubule-Organizing Center / physiology*
  • Microtubule-Organizing Center / virology
  • Virus Assembly / physiology*

Substances

  • MAPRE1 protein, human
  • MAPRE3 protein, human
  • Microtubule-Associated Proteins