The MGF360-16R ORF of African Swine Fever Virus Strain Georgia Encodes for a Nonessential Gene That Interacts with Host Proteins SERTAD3 and SDCBP
Abstract
African swine fever virus (ASFV) causes a contagious and frequently lethal disease of pigs with significant economic consequences to the swine industry. The ASFV genome encodes for more than 160 genes, but only a few of them have been studied in detail. Here we report the characterization of open reading frame (ORF) MGF360-16R. Kinetic studies of virus RNA transcription demonstrated that the MGF360-16R gene is transcribed as a late virus protein. Analysis of host–protein interactions for the MGF360-16R gene using a yeast two-hybrid screen identified SERTA domain containing 3 (SERTAD3) and syndecan-binding protein (SDCBP) as host protein binding partners. SERTAD3 and SDCBP are both involved in nuclear transcription and SDCBP has been shown to be involved in virus traffic inside the host cell. Interaction between MGF360-16R and SERTAD3 and SDCBP host proteins was confirmed in eukaryotic cells transfected with plasmids expressing MGF360-16R and SERTAD3 or SDCBP fused to fluorescent tags. A recombinant ASFV lacking the MGF360-16R gene (ASFV-G-ΔMGF360-16R) was developed from the highly virulent field isolate Georgia2007 (ASFV-G) and was used to show that MGF360-16R is a nonessential gene. ASFV-G-ΔMGF360-16R had a similar replication ability in primary swine macrophage cell cultures when compared to its parental virus ASFV-G. Experimental infectionmore »
- Authors:
-
[1];
[6];
[6]
- Agricultural Research Service (ARS), Greenport, NY (United States). Plum Island Animal Disease Center; Univ. of Connecticut, Storrs, CT (United States). Dept. of Pathobiology
- Agricultural Research Service (ARS), Greenport, NY (United States). Plum Island Animal Disease Center; Mississippi State Univ., Starkville, MS (United States). Dept. of Pathobiology and Population Medicine
- Agricultural Research Service (ARS), Greenport, NY (United States). Plum Island Animal Disease Center; Kansas State Univ., Manhattan, KS (United States). College of Veterinary Medicine
- Agricultural Research Service (ARS), Greenport, NY (United States). Plum Island Animal Disease Center; Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)
- Agricultural Research Service (ARS), Greenport, NY (United States). Plum Island Animal Disease Center; Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)
- Agricultural Research Service (ARS), Greenport, NY (United States). Plum Island Animal Disease Center
- Agricultural Research Service (ARS), Greenport, NY (United States). Plum Island Animal Disease Center;
- Publication Date:
- Research Org.:
- Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1628591
- Grant/Contract Number:
- SC0014664
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Viruses
- Additional Journal Information:
- Journal Volume: 12; Journal Issue: 1; Journal ID: ISSN 1999-4915
- Publisher:
- MDPI
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; Virology; ASFV; African swine fever virus; ASF; host–viral protein interactions; SDCP1; SERTAD3
Citation Formats
Ramírez-Medina, Elizabeth, Vuono, Elizabeth A., Velazquez-Salinas, Lauro, Silva, Ediane, Rai, Ayushi, Pruitt, Sarah, Berggren, Keith A., Zhu, James, Borca, Manuel V., and Gladue, Douglas P. The MGF360-16R ORF of African Swine Fever Virus Strain Georgia Encodes for a Nonessential Gene That Interacts with Host Proteins SERTAD3 and SDCBP. United States: N. p., 2020.
Web. doi:10.3390/v12010060.
Ramírez-Medina, Elizabeth, Vuono, Elizabeth A., Velazquez-Salinas, Lauro, Silva, Ediane, Rai, Ayushi, Pruitt, Sarah, Berggren, Keith A., Zhu, James, Borca, Manuel V., & Gladue, Douglas P. The MGF360-16R ORF of African Swine Fever Virus Strain Georgia Encodes for a Nonessential Gene That Interacts with Host Proteins SERTAD3 and SDCBP. United States. https://doi.org/10.3390/v12010060
Ramírez-Medina, Elizabeth, Vuono, Elizabeth A., Velazquez-Salinas, Lauro, Silva, Ediane, Rai, Ayushi, Pruitt, Sarah, Berggren, Keith A., Zhu, James, Borca, Manuel V., and Gladue, Douglas P. Fri .
"The MGF360-16R ORF of African Swine Fever Virus Strain Georgia Encodes for a Nonessential Gene That Interacts with Host Proteins SERTAD3 and SDCBP". United States. https://doi.org/10.3390/v12010060. https://www.osti.gov/servlets/purl/1628591.
@article{osti_1628591,
title = {The MGF360-16R ORF of African Swine Fever Virus Strain Georgia Encodes for a Nonessential Gene That Interacts with Host Proteins SERTAD3 and SDCBP},
author = {Ramírez-Medina, Elizabeth and Vuono, Elizabeth A. and Velazquez-Salinas, Lauro and Silva, Ediane and Rai, Ayushi and Pruitt, Sarah and Berggren, Keith A. and Zhu, James and Borca, Manuel V. and Gladue, Douglas P.},
abstractNote = {African swine fever virus (ASFV) causes a contagious and frequently lethal disease of pigs with significant economic consequences to the swine industry. The ASFV genome encodes for more than 160 genes, but only a few of them have been studied in detail. Here we report the characterization of open reading frame (ORF) MGF360-16R. Kinetic studies of virus RNA transcription demonstrated that the MGF360-16R gene is transcribed as a late virus protein. Analysis of host–protein interactions for the MGF360-16R gene using a yeast two-hybrid screen identified SERTA domain containing 3 (SERTAD3) and syndecan-binding protein (SDCBP) as host protein binding partners. SERTAD3 and SDCBP are both involved in nuclear transcription and SDCBP has been shown to be involved in virus traffic inside the host cell. Interaction between MGF360-16R and SERTAD3 and SDCBP host proteins was confirmed in eukaryotic cells transfected with plasmids expressing MGF360-16R and SERTAD3 or SDCBP fused to fluorescent tags. A recombinant ASFV lacking the MGF360-16R gene (ASFV-G-ΔMGF360-16R) was developed from the highly virulent field isolate Georgia2007 (ASFV-G) and was used to show that MGF360-16R is a nonessential gene. ASFV-G-ΔMGF360-16R had a similar replication ability in primary swine macrophage cell cultures when compared to its parental virus ASFV-G. Experimental infection of domestic pigs showed that ASFV-G-ΔMGF360-16R is as virulent as the parental virus ASFV-G.},
doi = {10.3390/v12010060},
journal = {Viruses},
number = 1,
volume = 12,
place = {United States},
year = {Fri Jan 03 00:00:00 EST 2020},
month = {Fri Jan 03 00:00:00 EST 2020}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
An IkappaB homolog encoded by African swine fever virus provides a novel mechanism for downregulation of proinflammatory cytokine responses in host macrophages
journal, December 1996
- Powell, P. P.; Dixon, L. K.; Parkhouse, R. M.
- Journal of Virology, Vol. 70, Issue 12
The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest.
journal, November 1991
- Chien, C. T.; Bartel, P. L.; Sternglanz, R.
- Proceedings of the National Academy of Sciences, Vol. 88, Issue 21
African Swine Fever Virus Structural Protein p54 Is Essential for the Recruitment of Envelope Precursors to Assembly Sites
journal, April 2004
- Rodríguez, Javier M.; García-Escudero, Ramón; Salas, María L.
- Journal of Virology, Vol. 78, Issue 8
An African swine fever virus ORF with similarity to C-type lectins is non-essential for growth in swine macrophages in vitro and for virus virulence in domestic swine The EMBL/GenBank accession numbers of sequences reported in this paper are AF017027 (Chiredzi/83/1), AF017028 (Crocodile/96/1), AF017029 (Crocodile/96/3), AF017030 (E70), AF017031 (E75) AF017032 (Haiti 811), AF017033 (Fairfield/96/1), AF017034 (Wildebeeslaagte/96/1), AF017035 (Malawi Lil20/1), AF017036 (Pretoriuskop/96/4), AF017037 (Pretoriuskop/96/5), AF017038 (Tengani) and AF017039 (Uganda ’61).
journal, October 1999
- Neilan, J. G.; Borca, M. V.; Lu, Z.
- Journal of General Virology, Vol. 80, Issue 10
Mechanisms of African swine fever virus pathogenesis and immune evasion inferred from gene expression changes in infected swine macrophages
journal, November 2019
- Zhu, James J.; Ramanathan, Palaniappan; Bishop, Elizabeth A.
- PLOS ONE, Vol. 14, Issue 11
The Ep152R ORF of African swine fever virus strain Georgia encodes for an essential gene that interacts with host protein BAG6
journal, September 2016
- Borca, Manuel V.; O’Donnell, Vivian; Holinka, Lauren G.
- Virus Research, Vol. 223
Deletion of the African Swine Fever Virus Gene DP148R Does Not Reduce Virus Replication in Culture but Reduces Virus Virulence in Pigs and Induces High Levels of Protection against Challenge
journal, October 2017
- Reis, Ana L.; Goatley, Lynnette C.; Jabbar, Tamara
- Journal of Virology, Vol. 91, Issue 24
CRISPR-Cas9, a tool to efficiently increase the development of recombinant African swine fever viruses
journal, February 2018
- Borca, Manuel V.; Holinka, Lauren G.; Berggren, Keith A.
- Scientific Reports, Vol. 8, Issue 1
An African swine fever virus virulence-associated gene NL-S with similarity to the herpes simplex virus ICP34.5 gene.
journal, January 1996
- Zsak, L.; Lu, Z.; Kutish, G. F.
- Journal of virology, Vol. 70, Issue 12
A Nonessential African Swine Fever Virus Gene UK Is a Significant Virulence Determinant in Domestic Swine
journal, February 1998
- Zsak, L.; Caler, E.; Lu, Z.
- Journal of Virology, Vol. 72, Issue 2
Effects of the interactions of classical swine fever virus Core protein with proteins of the SUMOylation pathway on virulence in swine
journal, November 2010
- Gladue, D. P.; Holinka, L. G.; Fernandez-Sainz, I. J.
- Virology, Vol. 407, Issue 1
Genomic Analysis of Highly Virulent Georgia 2007/1 Isolate of African Swine Fever Virus
journal, April 2011
- Chapman, David A. G.; Darby, Alistair C.; Da Silva, Melissa
- Emerging Infectious Diseases, Vol. 17, Issue 4
Interaction of CSFV E2 Protein with Swine Host Factors as Detected by Yeast Two-Hybrid System
journal, January 2014
- Gladue, Douglas P.; Baker-Bransetter, Ryan; Holinka, Lauren G.
- PLoS ONE, Vol. 9, Issue 1
The interactome of EBV LMP1 evaluated by proximity-based BioID approach
journal, March 2018
- Rider, Mark A.; Cheerathodi, Mujeeb R.; Hurwitz, Stephanie N.
- Virology, Vol. 516
Development of a fluorescent ASFV strain that retains the ability to cause disease in swine
journal, April 2017
- Borca, Manuel V.; O’Donnell, Vivian; Holinka, Lauren G.
- Scientific Reports, Vol. 7, Issue 1
A Deep-Sequencing Workflow for the Fast and Efficient Generation of High-Quality African Swine Fever Virus Whole-Genome Sequences
journal, September 2019
- Forth, Jan; Forth, Leonie; King, Jacqueline
- Viruses, Vol. 11, Issue 9
Deletion of a CD2-Like Gene, 8-DR, from African Swine Fever Virus Affects Viral Infection in Domestic Swine
journal, April 1998
- Borca, M. V.; Carrillo, C.; Zsak, L.
- Journal of Virology, Vol. 72, Issue 4
Nef interaction with actin compromises human podocyte actin cytoskeletal integrity
journal, February 2013
- Tan, Raymond; Patni, Hitesh; Tandon, Pranai
- Experimental and Molecular Pathology, Vol. 94, Issue 1
The intracellular proteome of African swine fever virus
journal, October 2018
- Keßler, Catharina; Forth, Jan H.; Keil, Günther M.
- Scientific Reports, Vol. 8, Issue 1
Mechanisms of African swine fever virus pathogenesis and immune evasion inferred from gene expression changes in infected swine macrophages
journal, November 2019
- Zhu, James J.; Ramanathan, Palaniappan; Bishop, Elizabeth A.
- PLOS ONE, Vol. 14, Issue 11
Development of a fluorescent ASFV strain that retains the ability to cause disease in swine
journal, April 2017
- Borca, Manuel V.; O’Donnell, Vivian; Holinka, Lauren G.
- Scientific Reports, Vol. 7, Issue 1
An African swine fever virus ORF with similarity to C-type lectins is non-essential for growth in swine macrophages in vitro and for virus virulence in domestic swine The EMBL/GenBank accession numbers of sequences reported in this paper are AF017027 (Chiredzi/83/1), AF017028 (Crocodile/96/1), AF017029 (Crocodile/96/3), AF017030 (E70), AF017031 (E75) AF017032 (Haiti 811), AF017033 (Fairfield/96/1), AF017034 (Wildebeeslaagte/96/1), AF017035 (Malawi Lil20/1), AF017036 (Pretoriuskop/96/4), AF017037 (Pretoriuskop/96/5), AF017038 (Tengani) and AF017039 (Uganda ’61).
journal, October 1999
- Neilan, J. G.; Borca, M. V.; Lu, Z.
- Journal of General Virology, Vol. 80, Issue 10
A novel genetic system to detect protein–protein interactions
journal, July 1989
- Fields, Stanley; Song, Ok-kyu
- Nature, Vol. 340, Issue 6230, p. 245-246
BA71ΔCD2: a New Recombinant Live Attenuated African Swine Fever Virus with Cross-Protective Capabilities
journal, August 2017
- Monteagudo, Paula L.; Lacasta, Anna; López, Elisabeth
- Journal of Virology, Vol. 91, Issue 21
African Swine Fever Virus Multigene Family 360 Genes Affect Virus Replication and Generalization of Infection in Ornithodoros porcinus Ticks
journal, March 2004
- Burrage, T. G.; Lu, Z.; Neilan, J. G.
- Journal of Virology, Vol. 78, Issue 5
Overexpression of SERTAD3, a putative oncogene located within the 19q13 amplicon, induces E2F activity and promotes tumor growth
journal, January 2007
- Darwish, H.; Cho, J. M.; Loignon, M.
- Oncogene, Vol. 26, Issue 29
A novel genetic system to detect protein–protein interactions
journal, July 1989
- Fields, Stanley; Song, Ok-kyu
- Nature, Vol. 340, Issue 6230, p. 245-246
Classical Swine Fever Virus p7 Protein Interacts with Host Protein CAMLG and Regulates Calcium Permeability at the Endoplasmic Reticulum
journal, August 2018
- Gladue, Douglas; Largo, Eneko; Holinka, Lauren
- Viruses, Vol. 10, Issue 9
The L83L ORF of African swine fever virus strain Georgia encodes for a non-essential gene that interacts with the host protein IL-1β
journal, April 2018
- Borca, Manuel V.; O’Donnell, Vivian; Holinka, Lauren G.
- Virus Research, Vol. 249
African swine fever virus-induced polypeptides in vero cells
journal, September 1986
- Santarén, Juan F.; Viñuela, Eladio
- Virus Research, Vol. 5, Issue 4
A BIR Motif Containing Gene of African Swine Fever Virus,4CL,Is Nonessential for Growthin Vitroand Viral Virulence
journal, April 1997
- Neilan, J. G.; Lu, Z.; Kutish, G. F.
- Virology, Vol. 230, Issue 2
African swine fever virus Georgia isolate harboring deletions of 9GL and MGF360/505 genes is highly attenuated in swine but does not confer protection against parental virus challenge
journal, August 2016
- O’Donnell, Vivian; Holinka, Lauren G.; Sanford, Brenton
- Virus Research, Vol. 221
The CD63-syntenin-1 complex controls post-endocytic trafficking of oncogenic human papillomaviruses
text, January 2016
- Gräßel, Linda; Fast, Laura Aline; Scheffer, Konstanze D.
- Nature Publishing Group
Characterization of P30, a highly antigenic membrane and secreted protein of African Swine Fever Virus
journal, July 1992
- Afonso, Claudio L.; Alcaraz, Carlos; Brun, Alejandro
- Virology, Vol. 189, Issue 1
African Swine Fever Virus Protein p54 Interacts with the Microtubular Motor Complex through Direct Binding to Light-Chain Dynein
journal, October 2001
- Alonso, C.; Miskin, J.; Hernaez, B.
- Journal of Virology, Vol. 75, Issue 20
Sensitivity of African swine fever virus to type I interferon is linked to genes within multigene families 360 and 505
journal, June 2016
- Golding, Josephine P.; Goatley, Lynnette; Goodbourn, Steve
- Virology, Vol. 493
African swine fever virus-induced proteins on the plasma membranes of infected cells
journal, February 1989
- Alcaraz, C.; Pasamontes, B.; Ruiz Gonzalvo, F.
- Virology, Vol. 168, Issue 2
The L83L ORF of African swine fever virus strain Georgia encodes for a non-essential gene that interacts with the host protein IL-1β
journal, April 2018
- Borca, Manuel V.; O’Donnell, Vivian; Holinka, Lauren G.
- Virus Research, Vol. 249
Two-dimensional analysis of african swine fever virus proteins and proteins induced in infected cells
journal, July 1986
- Esteves, Aida; Marques, Maria Isabel; Costa, João V.
- Virology, Vol. 152, Issue 1
Identification of genes that are associated with DNA repeats in prokaryotes
journal, March 2002
- Jansen, Ruud.; Embden, Jan. D. A. van; Gaastra, Wim.
- Molecular Microbiology, Vol. 43, Issue 6
SMART: recent updates, new developments and status in 2015
journal, October 2014
- Letunic, Ivica; Doerks, Tobias; Bork, Peer
- Nucleic Acids Research, Vol. 43, Issue D1
Effects of the interactions of classical swine fever virus Core protein with proteins of the SUMOylation pathway on virulence in swine
journal, November 2010
- Gladue, D. P.; Holinka, L. G.; Fernandez-Sainz, I. J.
- Virology, Vol. 407, Issue 1
Genomic Analysis of Highly Virulent Georgia 2007/1 Isolate of African Swine Fever Virus
journal, April 2011
- Chapman, David A. G.; Darby, Alistair C.; Da Silva, Melissa
- Emerging Infectious Diseases, Vol. 17, Issue 4
Interaction of CSFV E2 Protein with Swine Host Factors as Detected by Yeast Two-Hybrid System
journal, January 2014
- Gladue, Douglas P.; Baker-Bransetter, Ryan; Holinka, Lauren G.
- PLoS ONE, Vol. 9, Issue 1
The intracellular proteome of African swine fever virus
journal, October 2018
- Keßler, Catharina; Forth, Jan H.; Keil, Günther M.
- Scientific Reports, Vol. 8, Issue 1
CRISPR-Cas9, a tool to efficiently increase the development of recombinant African swine fever viruses
journal, February 2018
- Borca, Manuel V.; Holinka, Lauren G.; Berggren, Keith A.
- Scientific Reports, Vol. 8, Issue 1
An African Swine Fever Virus ERV1-ALRHomologue, 9GL, Affects Virion Maturation and Viral Growth in Macrophages and Viral Virulence in Swine
journal, February 2000
- Lewis, T.; Zsak, L.; Burrage, T. G.
- Journal of Virology, Vol. 74, Issue 3
A Deep-Sequencing Workflow for the Fast and Efficient Generation of High-Quality African Swine Fever Virus Whole-Genome Sequences
journal, September 2019
- Forth, Jan; Forth, Leonie; King, Jacqueline
- Viruses, Vol. 11, Issue 9
African Swine Fever Virus Georgia 2007 with a Deletion of Virulence-Associated Gene 9GL (B119L), when Administered at Low Doses, Leads to Virus Attenuation in Swine and Induces an Effective Protection against Homologous Challenge
journal, June 2015
- O'Donnell, Vivian; Holinka, Lauren G.; Krug, Peter W.
- Journal of Virology, Vol. 89, Issue 16
Characterization of P30, a highly antigenic membrane and secreted protein of African Swine Fever Virus
journal, July 1992
- Afonso, Claudio L.; Alcaraz, Carlos; Brun, Alejandro
- Virology, Vol. 189, Issue 1
A Conserved African Swine Fever Virus IκB Homolog, 5EL, Is Nonessential for Growthin Vitroand Virulence in Domestic Swine
journal, September 1997
- Neilan, J. G.; Lu, Z.; Kutish, G. F.
- Virology, Vol. 235, Issue 2
Multigene families in African swine fever virus: family 360.
journal, January 1990
- González, A.; Calvo, V.; Almazán, F.
- Journal of Virology, Vol. 64, Issue 5
The CD63-Syntenin-1 Complex Controls Post-Endocytic Trafficking of Oncogenic Human Papillomaviruses
journal, August 2016
- Gräßel, Linda; Fast, Laura Aline; Scheffer, Konstanze D.
- Scientific Reports, Vol. 6, Issue 1
SMART: recent updates, new developments and status in 2015
journal, October 2014
- Letunic, Ivica; Doerks, Tobias; Bork, Peer
- Nucleic Acids Research, Vol. 43, Issue D1
African swine fever virus Georgia isolate harboring deletions of 9GL and MGF360/505 genes is highly attenuated in swine but does not confer protection against parental virus challenge
journal, August 2016
- O’Donnell, Vivian; Holinka, Lauren G.; Sanford, Brenton
- Virus Research, Vol. 221
Proteins specified by African Swine Fever virus: V.-Identification of immediate early, early and late proteins
journal, September 1987
- Escribano, J. M.; Tabar�s, E.
- Archives of Virology, Vol. 92, Issue 3-4
Nef interaction with actin compromises human podocyte actin cytoskeletal integrity
journal, February 2013
- Tan, Raymond; Patni, Hitesh; Tandon, Pranai
- Experimental and Molecular Pathology, Vol. 94, Issue 1
African swine fever virus-induced proteins on the plasma membranes of infected cells
journal, February 1989
- Alcaraz, C.; Pasamontes, B.; Ruiz Gonzalvo, F.
- Virology, Vol. 168, Issue 2
Sensitivity of African swine fever virus to type I interferon is linked to genes within multigene families 360 and 505
journal, June 2016
- Golding, Josephine P.; Goatley, Lynnette; Goodbourn, Steve
- Virology, Vol. 493
Two-dimensional analysis of african swine fever virus proteins and proteins induced in infected cells
journal, July 1986
- Esteves, Aida; Marques, Maria Isabel; Costa, João V.
- Virology, Vol. 152, Issue 1