The ESCRT Machinery Is Recruited by the Viral BFRF1 Protein to the Nucleus-Associated Membrane for the Maturation of Epstein-Barr Virus

Chung Pei Lee, Po Ting Liu, Hsiu Ni Kung, Mei Tzu Su, Huey Huey Chua, Yu Hsin Chang, Chou Wei Chang, Ching Hwa Tsai, Fu-Tong Liu, Mei Ru Chen

Research output: Contribution to journalArticle

57 Citations (Scopus)

Abstract

The cellular endosomal sorting complex required for transport (ESCRT) machinery participates in membrane scission and cytoplasmic budding of many RNA viruses. Here, we found that expression of dominant negative ESCRT proteins caused a blockade of Epstein-Barr virus (EBV) release and retention of viral BFRF1 at the nuclear envelope. The ESCRT adaptor protein Alix was redistributed and partially colocalized with BFRF1 at the nuclear rim of virus replicating cells. Following transient transfection, BFRF1 associated with ESCRT proteins, reorganized the nuclear membrane and induced perinuclear vesicle formation. Multiple domains within BFRF1 mediated vesicle formation and Alix recruitment, whereas both Bro and PRR domains of Alix interacted with BFRF1. Inhibition of ESCRT machinery abolished BFRF1-induced vesicle formation, leading to the accumulation of viral DNA and capsid proteins in the nucleus of EBV-replicating cells. Overall, data here suggest that BFRF1 recruits the ESCRT components to modulate nuclear envelope for the nuclear egress of EBV.

Original languageEnglish (US)
Article numbere1002904
JournalPLoS Pathogens
Volume8
Issue number9
DOIs
StatePublished - Sep 2012

Fingerprint

Endosomal Sorting Complexes Required for Transport
Viral Proteins
Human Herpesvirus 4
Membranes
Nuclear Envelope
Carrier Proteins
Virus Release
RNA Viruses
Viral DNA
Capsid Proteins
Transfection
Cell Membrane
Viruses

ASJC Scopus subject areas

  • Microbiology
  • Parasitology
  • Virology
  • Immunology
  • Genetics
  • Molecular Biology

Cite this

The ESCRT Machinery Is Recruited by the Viral BFRF1 Protein to the Nucleus-Associated Membrane for the Maturation of Epstein-Barr Virus. / Lee, Chung Pei; Liu, Po Ting; Kung, Hsiu Ni; Su, Mei Tzu; Chua, Huey Huey; Chang, Yu Hsin; Chang, Chou Wei; Tsai, Ching Hwa; Liu, Fu-Tong; Chen, Mei Ru.

In: PLoS Pathogens, Vol. 8, No. 9, e1002904, 09.2012.

Research output: Contribution to journalArticle

Lee, CP, Liu, PT, Kung, HN, Su, MT, Chua, HH, Chang, YH, Chang, CW, Tsai, CH, Liu, F-T & Chen, MR 2012, 'The ESCRT Machinery Is Recruited by the Viral BFRF1 Protein to the Nucleus-Associated Membrane for the Maturation of Epstein-Barr Virus', PLoS Pathogens, vol. 8, no. 9, e1002904. https://doi.org/10.1371/journal.ppat.1002904
Lee, Chung Pei ; Liu, Po Ting ; Kung, Hsiu Ni ; Su, Mei Tzu ; Chua, Huey Huey ; Chang, Yu Hsin ; Chang, Chou Wei ; Tsai, Ching Hwa ; Liu, Fu-Tong ; Chen, Mei Ru. / The ESCRT Machinery Is Recruited by the Viral BFRF1 Protein to the Nucleus-Associated Membrane for the Maturation of Epstein-Barr Virus. In: PLoS Pathogens. 2012 ; Vol. 8, No. 9.
@article{fda3be31dfe543628c6aafed463b249c,
title = "The ESCRT Machinery Is Recruited by the Viral BFRF1 Protein to the Nucleus-Associated Membrane for the Maturation of Epstein-Barr Virus",
abstract = "The cellular endosomal sorting complex required for transport (ESCRT) machinery participates in membrane scission and cytoplasmic budding of many RNA viruses. Here, we found that expression of dominant negative ESCRT proteins caused a blockade of Epstein-Barr virus (EBV) release and retention of viral BFRF1 at the nuclear envelope. The ESCRT adaptor protein Alix was redistributed and partially colocalized with BFRF1 at the nuclear rim of virus replicating cells. Following transient transfection, BFRF1 associated with ESCRT proteins, reorganized the nuclear membrane and induced perinuclear vesicle formation. Multiple domains within BFRF1 mediated vesicle formation and Alix recruitment, whereas both Bro and PRR domains of Alix interacted with BFRF1. Inhibition of ESCRT machinery abolished BFRF1-induced vesicle formation, leading to the accumulation of viral DNA and capsid proteins in the nucleus of EBV-replicating cells. Overall, data here suggest that BFRF1 recruits the ESCRT components to modulate nuclear envelope for the nuclear egress of EBV.",
author = "Lee, {Chung Pei} and Liu, {Po Ting} and Kung, {Hsiu Ni} and Su, {Mei Tzu} and Chua, {Huey Huey} and Chang, {Yu Hsin} and Chang, {Chou Wei} and Tsai, {Ching Hwa} and Fu-Tong Liu and Chen, {Mei Ru}",
year = "2012",
month = "9",
doi = "10.1371/journal.ppat.1002904",
language = "English (US)",
volume = "8",
journal = "PLoS Pathogens",
issn = "1553-7366",
publisher = "Public Library of Science",
number = "9",

}

TY - JOUR

T1 - The ESCRT Machinery Is Recruited by the Viral BFRF1 Protein to the Nucleus-Associated Membrane for the Maturation of Epstein-Barr Virus

AU - Lee, Chung Pei

AU - Liu, Po Ting

AU - Kung, Hsiu Ni

AU - Su, Mei Tzu

AU - Chua, Huey Huey

AU - Chang, Yu Hsin

AU - Chang, Chou Wei

AU - Tsai, Ching Hwa

AU - Liu, Fu-Tong

AU - Chen, Mei Ru

PY - 2012/9

Y1 - 2012/9

N2 - The cellular endosomal sorting complex required for transport (ESCRT) machinery participates in membrane scission and cytoplasmic budding of many RNA viruses. Here, we found that expression of dominant negative ESCRT proteins caused a blockade of Epstein-Barr virus (EBV) release and retention of viral BFRF1 at the nuclear envelope. The ESCRT adaptor protein Alix was redistributed and partially colocalized with BFRF1 at the nuclear rim of virus replicating cells. Following transient transfection, BFRF1 associated with ESCRT proteins, reorganized the nuclear membrane and induced perinuclear vesicle formation. Multiple domains within BFRF1 mediated vesicle formation and Alix recruitment, whereas both Bro and PRR domains of Alix interacted with BFRF1. Inhibition of ESCRT machinery abolished BFRF1-induced vesicle formation, leading to the accumulation of viral DNA and capsid proteins in the nucleus of EBV-replicating cells. Overall, data here suggest that BFRF1 recruits the ESCRT components to modulate nuclear envelope for the nuclear egress of EBV.

AB - The cellular endosomal sorting complex required for transport (ESCRT) machinery participates in membrane scission and cytoplasmic budding of many RNA viruses. Here, we found that expression of dominant negative ESCRT proteins caused a blockade of Epstein-Barr virus (EBV) release and retention of viral BFRF1 at the nuclear envelope. The ESCRT adaptor protein Alix was redistributed and partially colocalized with BFRF1 at the nuclear rim of virus replicating cells. Following transient transfection, BFRF1 associated with ESCRT proteins, reorganized the nuclear membrane and induced perinuclear vesicle formation. Multiple domains within BFRF1 mediated vesicle formation and Alix recruitment, whereas both Bro and PRR domains of Alix interacted with BFRF1. Inhibition of ESCRT machinery abolished BFRF1-induced vesicle formation, leading to the accumulation of viral DNA and capsid proteins in the nucleus of EBV-replicating cells. Overall, data here suggest that BFRF1 recruits the ESCRT components to modulate nuclear envelope for the nuclear egress of EBV.

UR - http://www.scopus.com/inward/record.url?scp=84866920100&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84866920100&partnerID=8YFLogxK

U2 - 10.1371/journal.ppat.1002904

DO - 10.1371/journal.ppat.1002904

M3 - Article

C2 - 22969426

AN - SCOPUS:84866920100

VL - 8

JO - PLoS Pathogens

JF - PLoS Pathogens

SN - 1553-7366

IS - 9

M1 - e1002904

ER -