Swine Host Protein Coiled-Coil Domain-Containing 115 (CCDC115) Interacts with Classical Swine Fever Virus Structural Glycoprotein E2 during Virus Replication

Vuono, Elizabeth A.; Ramirez-Medina, Elizabeth; Berggren, Keith; Rai, Ayushi; Pruitt, Sarah; Silva, Ediane; Velazquez-Salinas, Lauro; Gladue, Douglas P.; Borca, Manuel V.

doi:10.3390/v12040388

Swine Host Protein Coiled-Coil Domain-Containing 115 (CCDC115) Interacts with Classical Swine Fever Virus Structural Glycoprotein E2 during Virus Replication

Journal Article · Tue Mar 31 00:00:00 EDT 2020 · Viruses

DOI:https://doi.org/10.3390/v12040388· OSTI ID:1816266

Vuono, Elizabeth A. ^[1]; ^[2]; ^[3]; Rai, Ayushi ^[4]; Pruitt, Sarah ^[4]; Silva, Ediane ^[5]; Velazquez-Salinas, Lauro ^[5]; ^[3]; Borca, Manuel V. ^[3]

US Dept. of Homeland Security (DHS), Greenport, NY (United States). Plum Island Animal Disease Center; Mississippi State Univ., Mississippi State, MS (United States). Dept. of Pathobiology and Population Medicine; OSTI
Mississippi State Univ., Mississippi State, MS (United States). Dept. of Pathobiology and Population Medicine; Univ. of Connecticut, Storrs, CT (United States). Dept. of Pathobiology and Veterinary Science
US Dept. of Homeland Security (DHS), Greenport, NY (United States). Plum Island Animal Disease Center
US Dept. of Homeland Security (DHS), Greenport, NY (United States). Plum Island Animal Disease Center; Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)
US Dept. of Homeland Security (DHS), Greenport, NY (United States). Plum Island Animal Disease Center; Kansas State Univ., Manhattan, KS (United States). Dept. of Anatomy and Physiology

Interactions between the major structural glycoprotein E2 of classical swine fever virus (CSFV) with host proteins have been identified as important factors affecting virus replication and virulence. Previously, using the yeast two-hybrid system, we identified swine host proteins specifically interacting with CSFV E2. In this report, we use a proximity ligation assay to demonstrate that swine host protein CCDC115 interacts with E2 in CSFV-infected swine cells. Using a randomly mutated E2 library in the context of a yeast two-hybrid methodology, specific amino acid mutations in the CSFV E2 protein responsible for disrupting the interaction with CCDC115 were identified. A recombinant CSFV mutant (E2ΔCCDC115v) harboring amino acid changes disrupting the E2 protein interaction with CCDC115 was produced and used as a tool to assess the role of the E2–CCDC115 interaction in viral replication and virulence in swine. CSFV E2ΔCCDC115v showed a slightly decreased ability to replicate in the SK6 swine cell line and a greater replication defect in primary swine macrophage cultures. A decreased E2–CCDC115 interaction detected by PLA is observed in cells infected with E2ΔCCDC115v. Importantly, animals intranasally infected with 105 TCID50 of E2ΔCCDC115v experienced a significantly longer survival period when compared with those infected with the parental Brescia strain. This result would indicate that the ability of CSFV E2 to bind host CCDC115 protein during infection plays an important role in virus replication in swine macrophages and in virus virulence during the infection in domestic swine.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge Associated Univ., Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: SC0014664

OSTI ID:: 1816266

Journal Information:: Viruses, Journal Name: Viruses Journal Issue: 4 Vol. 12; ISSN VIRUBR; ISSN 1999-4915

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (29)

CSFV proliferation is associated with GBF1 and Rab2 Liang, Wulong; Zheng, Minping; Bao, Changlei Journal of Biosciences, Vol. 42, Issue 1 https://doi.org/10.1007/s12038-016-9659-0	journal	December 2016
The development of an international reference panel of monoclonal antibodies for the differentiation of hog cholera virus from other pestiviruses Edwards, S.; Moennig, V.; Wensvoort, G. Veterinary Microbiology, Vol. 29, Issue 2 https://doi.org/10.1016/0378-1135(91)90118-Y	journal	October 1991
CCDC115 Deficiency Causes a Disorder of Golgi Homeostasis with Abnormal Protein Glycosylation Jansen, Jos C.; Cirak, Sebahattin; van Scherpenzeel, Monique The American Journal of Human Genetics, Vol. 98, Issue 2 https://doi.org/10.1016/j.ajhg.2015.12.010	journal	February 2016
Positive selection pressure on the B/C domains of the E2-gene of classical swine fever virus in endemic areas under C-strain vaccination Pérez, Lester Josué; Díaz de Arce, Heidy; Perera, Carmen Laura Infection, Genetics and Evolution, Vol. 12, Issue 7 https://doi.org/10.1016/j.meegid.2012.04.030	journal	October 2012
Mutation of E1 glycoprotein of classical swine fever virus affects viral virulence in swine Risatti, G. R.; Holinka, L. G.; Lu, Z. Virology, Vol. 343, Issue 1 https://doi.org/10.1016/j.virol.2005.08.015	journal	December 2005
Identification of a novel virulence determinant within the E2 structural glycoprotein of classical swine fever virus Risatti, G. R.; Holinka, L. G.; Carrillo, C. Virology, Vol. 355, Issue 1 https://doi.org/10.1016/j.virol.2006.07.005	journal	November 2006
Mutations in the carboxyl terminal region of E2 glycoprotein of classical swine fever virus are responsible for viral attenuation in swine Risatti, G. R.; Holinka, L. G.; Fernandez Sainz, I. Virology, Vol. 364, Issue 2 https://doi.org/10.1016/j.virol.2007.02.025	journal	August 2007
Effects of the interactions of classical swine fever virus Core protein with proteins of the SUMOylation pathway on virulence in swine Gladue, D. P.; Holinka, L. G.; Fernandez-Sainz, I. J. Virology, Vol. 407, Issue 1 https://doi.org/10.1016/j.virol.2010.07.040	journal	November 2010
Interaction between Core protein of classical swine fever virus with cellular IQGAP1 protein appears essential for virulence in swine Gladue, D. P.; Holinka, L. G.; Fernandez-Sainz, I. J. Virology, Vol. 412, Issue 1 https://doi.org/10.1016/j.virol.2010.12.060	journal	March 2011
Interaction of structural core protein of classical swine fever virus with endoplasmic reticulum-associated degradation pathway protein OS9 Gladue, D. P.; O’Donnell, V.; Fernandez-Sainz, I. J. Virology, Vol. 460-461 https://doi.org/10.1016/j.virol.2014.05.008	journal	July 2014
Beta-actin interacts with the E2 protein and is involved in the early replication of classical swine fever virus He, Fan; Ling, Lijun; Liao, Yajin Virus Research, Vol. 179 https://doi.org/10.1016/j.virusres.2013.10.016	journal	January 2014
Annexin 2 is a host protein binding to classical swine fever virus E2 glycoprotein and promoting viral growth in PK-15 cells Yang, Zhi; Shi, Zixue; Guo, Huancheng Virus Research, Vol. 201 https://doi.org/10.1016/j.virusres.2015.02.013	journal	April 2015
Direct observation of individual endogenous protein complexes in situ by proximity ligation Söderberg, Ola; Gullberg, Mats; Jarvius, Malin Nature Methods, Vol. 3, Issue 12, p. 995-1000 https://doi.org/10.1038/nmeth947	journal	October 2006
The Laminin Receptor Is a Cellular Attachment Receptor for Classical Swine Fever Virus Chen, Jianing; He, Wen-Rui; Shen, Liang Journal of Virology, Vol. 89, Issue 9 https://doi.org/10.1128/JVI.00019-15	journal	February 2015
Thioredoxin 2 Is a Novel E2-Interacting Protein That Inhibits the Replication of Classical Swine Fever Virus Li, Su; Wang, Jinghan; He, Wen-Rui Journal of Virology, Vol. 89, Issue 16 https://doi.org/10.1128/JVI.00429-15	journal	June 2015
Foot-and-Mouth Disease Virus Modulates Cellular Vimentin for Virus Survival Gladue, D. P.; O'Donnell, V.; Baker-Branstetter, R. Journal of Virology, Vol. 87, Issue 12 https://doi.org/10.1128/JVI.00448-13	journal	April 2013
Classical Swine Fever Virus p7 Protein Is a Viroporin Involved in Virulence in Swine Gladue, D. P.; Holinka, L. G.; Largo, E. Journal of Virology, Vol. 86, Issue 12 https://doi.org/10.1128/JVI.00560-12	journal	April 2012
Mitogen-Activated Protein Kinase Kinase 2, a Novel E2-Interacting Protein, Promotes the Growth of Classical Swine Fever Virus via Attenuation of the JAK-STAT Signaling Pathway Wang, Jinghan; Chen, Shucheng; Liao, Yajin Journal of Virology, Vol. 90, Issue 22 https://doi.org/10.1128/JVI.01407-16	journal	September 2016
Structural Glycoprotein E2 of Classical Swine Fever Virus Interacts with Host Protein Dynactin Subunit 6 (DCTN6) during the Virus Infectious Cycle Borca, M. V.; Vuono, E. A.; Ramirez-Medina, E. Journal of Virology, Vol. 94, Issue 1 https://doi.org/10.1128/JVI.01642-19	journal	October 2019
N-Linked Glycosylation Status of Classical Swine Fever Virus Strain Brescia E2 Glycoprotein Influences Virulence in Swine Risatti, G. R.; Holinka, L. G.; Fernandez Sainz, I. Journal of Virology, Vol. 81, Issue 2 https://doi.org/10.1128/JVI.01824-06	journal	November 2006
Interaction of Foot-and-Mouth Disease Virus Nonstructural Protein 3A with Host Protein DCTN3 Is Important for Viral Virulence in Cattle Gladue, D. P.; O'Donnell, V.; Baker-Bransetter, R. Journal of Virology, Vol. 88, Issue 5 https://doi.org/10.1128/JVI.03059-13	journal	December 2013
Hemoglobin Subunit Beta Interacts with the Capsid Protein and Antagonizes the Growth of Classical Swine Fever Virus Li, D.; Dong, H.; Li, S. Journal of Virology, Vol. 87, Issue 10 https://doi.org/10.1128/JVI.03130-12	journal	March 2013
Antigenic structure of envelope glycoprotein E1 of hog cholera virus van Rijn, P. A.; Miedema, G. K.; Wensvoort, G. Journal of Virology, Vol. 68, Issue 6 https://doi.org/10.1128/JVI.68.6.3934-3942.1994	journal	June 1994
Mutations Abrogating the RNase Activity in Glycoprotein E ^rns of the Pestivirus Classical Swine Fever Virus Lead to Virus Attenuation Meyers, Gregor; Saalmüller, Armin; Büttner, Mathias Journal of Virology, Vol. 73, Issue 12 https://doi.org/10.1128/JVI.73.12.10224-10235.1999	journal	December 1999
The E2 Glycoprotein of Classical Swine Fever Virus Is a Virulence Determinant in Swine Risatti, G. R.; Borca, M. V.; Kutish, G. F. Journal of Virology, Vol. 79, Issue 6 https://doi.org/10.1128/JVI.79.6.3787-3796.2005	journal	February 2005
Interaction of CSFV E2 Protein with Swine Host Factors as Detected by Yeast Two-Hybrid System Gladue, Douglas P.; Baker-Bransetter, Ryan; Holinka, Lauren G. PLoS ONE, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pone.0085324	journal	January 2014
Reemergence of Classical Swine Fever, Japan, 2018 Postel, Alexander; Nishi, Tatsuya; Kameyama, Ken-ichiro Emerging Infectious Diseases, Vol. 25, Issue 6 https://doi.org/10.3201/eid2506.181578	journal	June 2019
Classical Swine Fever Virus p7 Protein Interacts with Host Protein CAMLG and Regulates Calcium Permeability at the Endoplasmic Reticulum Gladue, Douglas; Largo, Eneko; Holinka, Lauren Viruses, Vol. 10, Issue 9 https://doi.org/10.3390/v10090460	journal	August 2018
Interaction of Structural Glycoprotein E2 of Classical Swine Fever Virus with Protein Phosphatase 1 Catalytic Subunit Beta (PPP1CB) Vuono, Elizabeth; Ramirez-Medina, Elizabeth; Holinka, Lauren Viruses, Vol. 11, Issue 4 https://doi.org/10.3390/v11040307	journal	March 2019

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59 BASIC BIOLOGICAL SCIENCES
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Swine Host Protein Coiled-Coil Domain-Containing 115 (CCDC115) Interacts with Classical Swine Fever Virus Structural Glycoprotein E2 during Virus Replication

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