Autographa californica Multiple Nucleopolyhedrovirus Ac34 Protein Retains Cellular Actin-Related Protein 2/3 Complex in the Nucleus by Subversion of CRM1-Dependent Nuclear Export

Actin, nucleation-promoting factors (NPFs), and the actin-related protein 2/3 complex (Arp2/3) are key elements of the cellular actin polymerization machinery. With nuclear actin polymerization implicated in ever-expanding biological processes and the discovery of the nuclear import mechanisms of actin and NPFs, determining Arp2/3 nucleo-cytoplasmic shuttling mechanism is important for understanding the function of nuclear actin. A unique feature of alphabaculovirus infection of insect cells is the robust nuclear accumulation of Arp2/3, which induces actin polymerization in the nucleus to assist in virus replication. We found that Ac34, a viral late gene product encoded by the alphabaculovirus Autographa californica multiple nucleopolyhedrovirus (AcMNPV), is involved in Arp2/3 nuclear accumulation during virus infection. Further assays revealed that the subcellular distribution of Arp2/3 under steady-state conditions is controlled by chromosomal maintenance 1 (CRM1)-dependent nuclear export. Upon AcMNPV infection, Ac34 inhibits CRM1 pathway and leads to Arp2/3 retention in the nucleus.

• Publication year

  2016

• Venue

  PLoS Pathogens

• Publication date

  2016-11-01

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1371/journal.ppat.1005994PMID 27802336PMCID 5089780
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• LocNES: a computational tool for locating classical NESs in CRM1 cargo proteins

  2015cited by this paper
• Electron Tomography and Simulation of Baculovirus Actin Comet Tails Support a Tethered Filament Model of Pathogen Propulsion

  2014cited by this paper
• Viral exploitation of actin: force-generation and scaffolding functions in viral infection

  2014cited by this paper
• Mechanisms of nuclear actin in chromatin-remodeling complexes.

  2014cited by this paper
• HIV-1 Triggers WAVE2 Phosphorylation in Primary CD4 T Cells and Macrophages, Mediating Arp2/3-dependent Nuclear Migration*

  2014cited by this paper
• Arp2/3-mediated actin-based motility: a tail of pathogen abuse.

  2013cited by this paper
• Viral Subversion of Nucleocytoplasmic Trafficking

  2013cited by this paper
• Steady‐state nuclear actin levels are determined by export competent actin pool

  2013cited by this paper
• To be or not to be assembled: progressing into nuclear actin filaments

  2013cited by this paper
• A36-dependent Actin Filament Nucleation Promotes Release of Vaccinia Virus

  2013influential reference
• Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%

  2012cited by this paper
• Transcriptional regulation and nuclear reprogramming: roles of nuclear actin and actin-binding proteins

  2012cited by this paper
• Herpes Simplex Virus ICP27 Protein Directly Interacts with the Nuclear Pore Complex through Nup62, Inhibiting Host Nucleocytoplasmic Transport Pathways

  2012cited by this paper
• [Cloning and functional research of Arp2/3-P40/ARPC1 subunit of Sf9 cells].

  2012cited by this paper
• The nucleocapsid protein of measles virus blocks host interferon response.

  2012cited by this paper
• Nuclear localization of actin requires AC102 in Autographa californica multiple nucleopolyhedrovirus-infected cells.

  2012cited by this paper
• Active maintenance of nuclear actin by importin 9 supports transcription

  2012cited by this paper
• An ac34 Deletion Mutant of Autographa californica Nucleopolyhedrovirus Exhibits Delayed Late Gene Expression and a Lack of Virulence In Vivo

  2012cited by this paper
• Baculovirus VP80 Protein and the F-Actin Cytoskeleton Interact and Connect the Viral Replication Factory with the Nuclear Periphery

  2011cited by this paper
• Differential Processing of Nuclear Pore Complex Proteins by Rhinovirus 2A Proteases from Different Species and Serotypes

  2011cited by this paper
• A nucleator arms race: cellular control of actin assembly

  2010cited by this paper
• Recognition of nuclear targeting signals by Karyopherin-β proteins.

  2010cited by this paper
• Actin-based motility drives baculovirus transit to the nucleus and cell surface

  2010cited by this paper
• The Putative Pocket Protein Binding Site of Autographa californica Nucleopolyhedrovirus BV/ODV-C42 Is Required for Virus-Induced Nuclear Actin Polymerization

  2010cited by this paper
• Rhinovirus 3C Protease Can Localize in the Nucleus and Alter Active and Passive Nucleocytoplasmic Transport

  2009cited by this paper
• Identification of a Hydrophobic Domain of HA2 Essential to Morphogenesis of Helicoverpa armigera Nucleopolyhedrovirus

  2008cited by this paper
• Leader-Induced Phosphorylation of Nucleoporins Correlates with Nuclear Trafficking Inhibition by Cardioviruses

  2008cited by this paper
• Autographa californica Multiple Nucleopolyhedrovirus Nucleocapsid Protein BV/ODV-C42 Mediates the Nuclear Entry of P78/83

  2008influential reference
• HA2 from the Helicoverpa armigera nucleopolyhedrovirus: a WASP-related protein that activates Arp2/3-induced actin filament formation.

  2007cited by this paper
• Ebola virus VP24 binds karyopherin alpha1 and blocks STAT1 nuclear accumulation.

  2006cited by this paper
• A picornavirus protein interacts with Ran-GTPase and disrupts nucleocytoplasmic transport

  2006cited by this paper
• Severe Acute Respiratory Syndrome Coronavirus Open Reading Frame (ORF) 3b, ORF 6, and Nucleocapsid Proteins Function as Interferon Antagonists

  2006cited by this paper
• Alpha-Herpesvirus Infection Induces the Formation of Nuclear Actin Filaments

  2006cited by this paper
• The ARP2/3 complex: an actin nucleator comes of age

  2006cited by this paper
• Ebola Virus VP24 Binds Karyopherin α1 and Blocks STAT1 Nuclear Accumulation

  2006cited by this paper
• Dynamic Nuclear Actin Assembly by Arp2/3 Complex and a Baculovirus WASP-Like Protein

  2006cited by this paper
• Actin-based motility of intracellular pathogens.

  2005cited by this paper
• Identification of a bacterial factor required for actin‐based motility of Burkholderia pseudomallei

  2005cited by this paper
• * These authors contributed equally to this work. Corresponding author:

  2004cited by this paper
• Nuclear actin and myosin I are required for RNA polymerase I transcription

  2004cited by this paper
• Exportin 7 defines a novel general nuclear export pathway

  2004cited by this paper
• The RickA protein of Rickettsia conorii activates the Arp2/3 complex

  2004cited by this paper
• A role for beta-actin in RNA polymerase III transcription.

  2004cited by this paper
• Actin is part of pre-initiation complexes and is necessary for transcription by RNA polymerase II

  2004cited by this paper
• The L2 Minor Capsid Protein of Human Papillomavirus Type 16 Interacts with a Network of Nuclear Import Receptors

  2004cited by this paper
• Autographa californica nucleopolyhedrovirus infection of Spodoptera frugiperda cells: a global analysis of host gene regulation during infection, using a differential display approach.

  2003cited by this paper
• Exportin 6: a novel nuclear export receptor that is specific for profilin·actin complexes

  2003cited by this paper
• The L1 major capsid protein of human papillomavirus type 11 interacts with Kap beta2 and Kap beta3 nuclear import receptors.

  2003cited by this paper
• Translocation of N-WASP by Nuclear Localization and Export Signals into the Nucleus Modulates Expression of HSP90*

  2003cited by this paper
• The L1 major capsid protein of human papillomavirus type 11 interacts with kap β2 and kap β3 nuclear import receptors

  2003cited by this paper
• Exp5 exports eEF1A via tRNA from nuclei and synergizes with other transport pathways to confine translation to the cytoplasm

  2002cited by this paper
• Identification of Six Autographa californica Multicapsid Nucleopolyhedrovirus Early Genes That Mediate Nuclear Localization of G-Actin

  2002cited by this paper
• Effects of poliovirus infection on nucleo‐cytoplasmic trafficking and nuclear pore complex composition

  2001cited by this paper
• Exportin 4: a mediator of a novel nuclear export pathway in higher eukaryotes

  2000cited by this paper
• The nuclear pore complex: a protein machine bridging the nucleus and cytoplasm.

  2000cited by this paper
• Actin‐based motility of pathogens: the Arp2/3 complex is a central player

  2000cited by this paper
• Virus taxonomy: classification and nomenclature of viruses. Seventh report of the International Committee on Taxonomy of Viruses.

  2000cited by this paper
• The Arp2/3 complex: a multifunctional actin organizer.

  1999cited by this paper
• Nuclear F-actin is required for AcMNPV nucleocapsid morphogenesis.

  1999cited by this paper
• The role of exportin‐t in selective nuclear export of mature tRNAs

  1998cited by this paper
• Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1.

  1998cited by this paper
• Actin polymerization is induced by Arp 2/3 protein complex at the surface of Listeria monocytogenes

  1997cited by this paper
• CRM1 is responsible for intracellular transport mediated by the nuclear export signal

  1997cited by this paper
• Export of importin alpha from the nucleus is mediated by a specific nuclear transport factor.

  1997cited by this paper
• CRM1 is an export receptor for leucine-rich nuclear export signals.

  1997cited by this paper
• Evidence for a role of CRM1 in signal-mediated nuclear protein export.

  1997cited by this paper
• Actin-based motility of vaccinia virus

  1995cited by this paper
• Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose

  1994cited by this paper
• Autographa californica M nuclear polyhedrosis virus and cytochalasin D: antagonists in the regulation of protein synthesis.

  1991cited by this paper
• Identification, sequence, and transcriptional mapping of the major capsid protein gene of the baculovirus Autographa californica nuclear polyhedrosis virus

  1989cited by this paper
• Regulation of host RNA levels during baculovirus infection.

  1988cited by this paper

• Multifaceted interactions between host ESCRT-III and budded virus-related proteins involved in entry and egress of the baculovirus Autographa californica multiple nucleopolyhedrovirus

  2024cites this paper
• A CRM1-dependent nuclear export signal in Autographa californica multiple nucleopolyhedrovirus Ac93 is important for the formation of intranuclear microvesicles

  2024influential citation
• Enhanced virulence of genetically engineered Autographa californica nucleopolyhedrovirus owing to accelerated viral DNA replication aided by inserted ascovirus genes.

  2023cites this paper
• Transcriptomics and interactomics during the primary infection of an SfNPV baculovirus on Spodoptera frugiperda larvae

  2023cites this paper
• Nuclear Cytoskeleton in Virus Infection

  2022cites this paper
• Spodoptera frugiperda mRNA export factor interacts with and mediates the nuclear import of Autographa californica multiple nucleopolyhedrovirus ORF34 (Ac34).

  2021cites this paper
• Effects of CRM1-dependent nuclear export inhibition on viral structural protein nuclear accumulation during Autographa californica Multiple Nucleopolyhedrovirus Infection.

  2021cites this paper
• A Tale of Two Transcriptomic Responses in Agricultural Pests via Host Defenses and Viral Replication

  2020cites this paper
• Knockdown of BmTCP-1β Delays BmNPV Infection in vitro

  2019cites this paper
• Dissecting the Cell Entry Pathway of Baculovirus by Single-Particle Tracking and Quantitative Electron Microscopic Analysis

  2019cites this paper
• Ac102 Participates in Nuclear Actin Polymerization by Modulating BV/ODV-C42 Ubiquitination during Autographa californica Multiple Nucleopolyhedrovirus Infection

  2018cites this paper
• Autographa Californica Multiple Nucleopolyhedrovirus Enters Host Cells via Clathrin-Mediated Endocytosis and Direct Fusion with the Plasma Membrane

  2018cites this paper
• Ac34 protein of AcMNPV promoted progeny virus production and induced the apoptosis in host Sf9 cells

  2018cites this paper
• A structured review of baculovirus infection process: integration of mathematical models and biomolecular information on cell-virus interaction.

  2018cites this paper
• Comprehensive analysis of single molecule sequencing-derived complete genome and whole transcriptome of Hyposidra talaca nuclear polyhedrosis virus

  2018cites this paper
• The 91-205 amino acid region of AcMNPV ORF34 (Ac34), which comprises a potential C3H zinc finger, is required for its nuclear localization and optimal virus multiplication.

  2017cites this paper
• The role of viral protein Ac34 in nuclear relocation of subunits of the actin-related protein 2/3 complex

  2016cites this paper