Intracellular Ebola virus nucleocapsid assembly revealed by in situ cryo-electron tomography

Cell. 2024 Oct 3;187(20):5587-5603.e19. doi: 10.1016/j.cell.2024.08.044. Epub 2024 Sep 17.

Abstract

Filoviruses, including the Ebola and Marburg viruses, cause hemorrhagic fevers with up to 90% lethality. The viral nucleocapsid is assembled by polymerization of the nucleoprotein (NP) along the viral genome, together with the viral proteins VP24 and VP35. We employed cryo-electron tomography of cells transfected with viral proteins and infected with model Ebola virus to illuminate assembly intermediates, as well as a 9 Å map of the complete intracellular assembly. This structure reveals a previously unresolved third and outer layer of NP complexed with VP35. The intrinsically disordered region, together with the C-terminal domain of this outer layer of NP, provides the constant width between intracellular nucleocapsid bundles and likely functions as a flexible tether to the viral matrix protein in the virion. A comparison of intracellular nucleocapsids with prior in-virion nucleocapsid structures reveals that the nucleocapsid further condenses vertically in the virion. The interfaces responsible for nucleocapsid assembly are highly conserved and offer targets for broadly effective antivirals.

Keywords: Ebola virus; Mononegavirales; antiviral; correlative light and electron microscopy; cryo-electron tomography; filovirus; focused-ion beam milling; immune suppressor; in situ structural biology; integrative modeling; nucleocapsid; nucleoprotein; phosphoprotein; subtomogram averaging; virus assembly; virus pathogenesis; virus structure.

MeSH terms

  • Animals
  • Chlorocebus aethiops
  • Cryoelectron Microscopy / methods
  • Ebolavirus* / chemistry
  • Ebolavirus* / metabolism
  • Ebolavirus* / physiology
  • Ebolavirus* / ultrastructure
  • Electron Microscope Tomography*
  • Hemorrhagic Fever, Ebola / virology
  • Humans
  • Models, Molecular
  • Nucleocapsid Proteins / chemistry
  • Nucleocapsid Proteins / metabolism
  • Nucleocapsid Proteins / ultrastructure
  • Nucleocapsid* / chemistry
  • Nucleocapsid* / metabolism
  • Nucleocapsid* / ultrastructure
  • Nucleoproteins / chemistry
  • Nucleoproteins / metabolism
  • Nucleoproteins / ultrastructure
  • Viral Proteins / chemistry
  • Viral Proteins / metabolism
  • Viral Proteins / ultrastructure
  • Virion / metabolism
  • Virion / ultrastructure
  • Virus Assembly*

Substances

  • Nucleocapsid Proteins
  • Nucleoproteins
  • Viral Proteins
  • VP24 protein, Ebola virus