Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: Nipah Virus-Like Particle Egress Is Modulated by Cytoskeletal and Vesicular Trafficking Pathways: a Validated Particle Proteomics Analysis

Abstract

ABSTRACT Classified as a biosafety level 4 (BSL4) select agent, Nipah virus (NiV) is a deadly henipavirus in theParamyxoviridaefamily, with a nearly 75% mortality rate in humans, underscoring its global and animal health importance. Elucidating the process of viral particle production in host cells is imperative both for targeted drug design and viral particle-based vaccine development. However, little is understood concerning the functions of cellular machinery in paramyxoviral and henipaviral assembly and budding. Recent studies showed evidence for the involvement of multiple NiV proteins in viral particle formation, in contrast to the mechanisms understood for several paramyxoviruses as being reliant on the matrix (M) protein alone. Further, the levels and purposes of cellular factor incorporation into viral particles are largely unexplored for the paramyxoviruses. To better understand the involvement of cellular machinery and the major structural viral fusion (F), attachment (G), and matrix (M) proteins, we performed proteomics analyses on virus-like particles (VLPs) produced from several combinations of these NiV proteins. Our findings indicate that NiV VLPs incorporate vesicular trafficking and actin cytoskeletal factors. The involvement of these biological processes was validated by experiments indicating that the perturbation of key factors in these cellular processes substantially modulated viral particle formation.more » These effects were most impacted for NiV-F-modulated viral particle formation either autonomously or in combination with other NiV proteins, indicating that NiV-F budding relies heavily on these cellular processes. These findings indicate a significant involvement of the NiV fusion protein, vesicular trafficking, and actin cytoskeletal processes in efficient viral particle formation. IMPORTANCENipah virus is a zoonotic biosafety level 4 agent with high mortality rates in humans. The genus to which Nipah virus belongs,Henipavirus, includes five officially recognized pathogens; however, over 20 species have been identified in multiple continents within the last several years. As there are still no vaccines or treatments for NiV infection, elucidating its process of viral particle production is imperative both for targeted drug design as well as for particle-based vaccine development. Developments in high-throughput technologies make proteomic analysis of isolated viral particles a highly insightful approach to understanding the life cycle of pathogens such as Nipah virus.« less

Authors:
 [1];  [2]; ORCiD logo [3]; ORCiD logo [3];  [1];  [1];  [1];  [1];  [1]; ORCiD logo [3];  [3];  [2]; ORCiD logo [3];  [1];  [4]
+ Show Author Affiliations
  1. Cornell Univ., Ithaca, NY (United States)
  2. Washington State Univ., Pullman, WA (United States)
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  4. Harvard Medical School, Boston, MA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1591872
Alternate Identifier(s):
OSTI ID: 1591873
Report Number(s):
PNNL-SA-142825
Journal ID: ISSN 2379-5077
Grant/Contract Number:  
AC05-76RL01830; HSHQPM-14-X-00238
Resource Type:
Accepted Manuscript
Journal Name:
mSystems
Additional Journal Information:
Journal Volume: 4; Journal Issue: 5; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Nipah virus; paramyxovirus; proteomics; vesicular trafficking; endocytosis; cytoskeleton; host-pathogen interaction

Citation Formats

Johnston, Gunner P., Bradel-Tretheway, Birgit, Piehowski, Paul D., Brewer, Heather M., Lee, Bom Nae Rin, Usher, Nicholas T., Zamora, J. Lizbeth Reyes, Ortega, Victoria, Contreras, Erik M., Teuton, Jeremy R., Wendler, Jason P., Matz, Keesha M., Adkins, Joshua N., Aguilar, Hector C., and Knipe, David M. Nipah Virus-Like Particle Egress Is Modulated by Cytoskeletal and Vesicular Trafficking Pathways: a Validated Particle Proteomics Analysis. United States: N. p., 2019. Web. doi:10.1128/mSystems.00194-19.
Copy to clipboard
Johnston, Gunner P., Bradel-Tretheway, Birgit, Piehowski, Paul D., Brewer, Heather M., Lee, Bom Nae Rin, Usher, Nicholas T., Zamora, J. Lizbeth Reyes, Ortega, Victoria, Contreras, Erik M., Teuton, Jeremy R., Wendler, Jason P., Matz, Keesha M., Adkins, Joshua N., Aguilar, Hector C., & Knipe, David M. Nipah Virus-Like Particle Egress Is Modulated by Cytoskeletal and Vesicular Trafficking Pathways: a Validated Particle Proteomics Analysis. United States. https://doi.org/10.1128/mSystems.00194-19
Copy to clipboard
Johnston, Gunner P., Bradel-Tretheway, Birgit, Piehowski, Paul D., Brewer, Heather M., Lee, Bom Nae Rin, Usher, Nicholas T., Zamora, J. Lizbeth Reyes, Ortega, Victoria, Contreras, Erik M., Teuton, Jeremy R., Wendler, Jason P., Matz, Keesha M., Adkins, Joshua N., Aguilar, Hector C., and Knipe, David M. Tue . "Nipah Virus-Like Particle Egress Is Modulated by Cytoskeletal and Vesicular Trafficking Pathways: a Validated Particle Proteomics Analysis". United States. https://doi.org/10.1128/mSystems.00194-19. https://www.osti.gov/servlets/purl/1591872.
Copy to clipboard
@article{osti_1591872,
title = {Nipah Virus-Like Particle Egress Is Modulated by Cytoskeletal and Vesicular Trafficking Pathways: a Validated Particle Proteomics Analysis},
author = {Johnston, Gunner P. and Bradel-Tretheway, Birgit and Piehowski, Paul D. and Brewer, Heather M. and Lee, Bom Nae Rin and Usher, Nicholas T. and Zamora, J. Lizbeth Reyes and Ortega, Victoria and Contreras, Erik M. and Teuton, Jeremy R. and Wendler, Jason P. and Matz, Keesha M. and Adkins, Joshua N. and Aguilar, Hector C. and Knipe, David M.},
abstractNote = {ABSTRACT Classified as a biosafety level 4 (BSL4) select agent, Nipah virus (NiV) is a deadly henipavirus in theParamyxoviridaefamily, with a nearly 75% mortality rate in humans, underscoring its global and animal health importance. Elucidating the process of viral particle production in host cells is imperative both for targeted drug design and viral particle-based vaccine development. However, little is understood concerning the functions of cellular machinery in paramyxoviral and henipaviral assembly and budding. Recent studies showed evidence for the involvement of multiple NiV proteins in viral particle formation, in contrast to the mechanisms understood for several paramyxoviruses as being reliant on the matrix (M) protein alone. Further, the levels and purposes of cellular factor incorporation into viral particles are largely unexplored for the paramyxoviruses. To better understand the involvement of cellular machinery and the major structural viral fusion (F), attachment (G), and matrix (M) proteins, we performed proteomics analyses on virus-like particles (VLPs) produced from several combinations of these NiV proteins. Our findings indicate that NiV VLPs incorporate vesicular trafficking and actin cytoskeletal factors. The involvement of these biological processes was validated by experiments indicating that the perturbation of key factors in these cellular processes substantially modulated viral particle formation. These effects were most impacted for NiV-F-modulated viral particle formation either autonomously or in combination with other NiV proteins, indicating that NiV-F budding relies heavily on these cellular processes. These findings indicate a significant involvement of the NiV fusion protein, vesicular trafficking, and actin cytoskeletal processes in efficient viral particle formation. IMPORTANCENipah virus is a zoonotic biosafety level 4 agent with high mortality rates in humans. The genus to which Nipah virus belongs,Henipavirus, includes five officially recognized pathogens; however, over 20 species have been identified in multiple continents within the last several years. As there are still no vaccines or treatments for NiV infection, elucidating its process of viral particle production is imperative both for targeted drug design as well as for particle-based vaccine development. Developments in high-throughput technologies make proteomic analysis of isolated viral particles a highly insightful approach to understanding the life cycle of pathogens such as Nipah virus.},
doi = {10.1128/mSystems.00194-19},
journal = {mSystems},
number = 5,
volume = 4,
place = {United States},
year = {Tue Sep 24 00:00:00 EDT 2019},
month = {Tue Sep 24 00:00:00 EDT 2019}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1128/mSystems.00194-19
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Citation Metrics:
Cited by: 8 works
Citation information provided by
Web of Science
Save / Share:
Export Metadata
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:

Virus Budding and the ESCRT Pathway
journal, September 2013

STRING v10: protein–protein interaction networks, integrated over the tree of life
journal, October 2014

  • Szklarczyk, Damian; Franceschini, Andrea; Wyder, Stefan
  • Nucleic Acids Research, Vol. 43, Issue D1
  • DOI: 10.1093/nar/gku1003

Late budding domains and host proteins in enveloped virus release
journal, January 2006

Proteomic and Biochemical Analysis of Purified Human Immunodeficiency Virus Type 1 Produced from Infected Monocyte-Derived Macrophages
journal, August 2006

  • Chertova, E.; Chertov, O.; Coren, L. V.
  • Journal of Virology, Vol. 80, Issue 18
  • DOI: 10.1128/JVI.01013-06

Evidence for a New Viral Late-Domain Core Sequence, FPIV, Necessary for Budding of a Paramyxovirus
journal, February 2005

p62/SQSTM1/Sequestosome-1 is an N-recognin of the N-end rule pathway which modulates autophagosome biogenesis
journal, July 2017

Rho GTPases and their role in organizing the actin cytoskeleton
journal, February 2011

  • Sit, S. -T.; Manser, E.
  • Journal of Cell Science, Vol. 124, Issue 5
  • DOI: 10.1242/jcs.064964

Tsg101 and the Vacuolar Protein Sorting Pathway Are Essential for HIV-1 Budding
journal, October 2001

Nipah Virus Matrix Protein Influences Fusogenicity and Is Essential for Particle Infectivity and Stability
journal, December 2015

  • Dietzel, Erik; Kolesnikova, Larissa; Sawatsky, Bevan
  • Journal of Virology, Vol. 90, Issue 5
  • DOI: 10.1128/JVI.02920-15

Viral Late Domains
journal, May 2002

Actin dynamics modulate mechanosensitive immobilization of E-cadherin at adherens junctions
journal, May 2014

  • Engl, W.; Arasi, B.; Yap, L. L.
  • Nature Cell Biology, Vol. 16, Issue 6
  • DOI: 10.1038/ncb2973

Nipah virus fusion protein: Importance of the cytoplasmic tail for endosomal trafficking and bioactivity
journal, July 2015

Structure and assembly of a paramyxovirus matrix protein
journal, August 2012

  • Battisti, A. J.; Meng, G.; Winkler, D. C.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 35
  • DOI: 10.1073/pnas.1210275109

AIP1/ALIX Is a Binding Partner for HIV-1 p6 and EIAV p9 Functioning in Virus Budding
journal, September 2003

The YPLGVG sequence of the Nipah virus matrix protein is required for budding
journal, January 2008

Cell surface dynamics - how Rho GTPases orchestrate the interplay between the plasma membrane and the cortical cytoskeleton
journal, October 2012

  • de Curtis, I.; Meldolesi, J.
  • Journal of Cell Science, Vol. 125, Issue 19
  • DOI: 10.1242/jcs.108266

Control of Vesicular Trafficking by Rho GTPases
journal, May 2003

Paramyxovirus assembly and budding: Building particles that transmit infections
journal, September 2010

  • Harrison, Megan S.; Sakaguchi, Takemasa; Schmitt, Anthony P.
  • The International Journal of Biochemistry & Cell Biology, Vol. 42, Issue 9
  • DOI: 10.1016/j.biocel.2010.04.005

Nipah Virus Entry and Egress from Polarized Epithelial Cells
journal, January 2013

  • Lamp, B.; Dietzel, E.; Kolesnikova, L.
  • Journal of Virology, Vol. 87, Issue 6
  • DOI: 10.1128/JVI.02696-12

InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams
journal, May 2015

  • Heberle, Henry; Meirelles, Gabriela Vaz; da Silva, Felipe R.
  • BMC Bioinformatics, Vol. 16, Issue 1
  • DOI: 10.1186/s12859-015-0611-3

Activation of the Nipah Virus Fusion Protein in MDCK Cells Is Mediated by Cathepsin B within the Endosome-Recycling Compartment
journal, January 2012

  • Diederich, S.; Sauerhering, L.; Weis, M.
  • Journal of Virology, Vol. 86, Issue 7
  • DOI: 10.1128/JVI.06628-11

Virus-like particles: Passport to immune recognition
journal, September 2006

Actin Dynamics, Architecture, and Mechanics in Cell Motility
journal, January 2014

  • Blanchoin, Laurent; Boujemaa-Paterski, Rajaa; Sykes, Cécile
  • Physiological Reviews, Vol. 94, Issue 1
  • DOI: 10.1152/physrev.00018.2013

Co-assembly of Viral Envelope Glycoproteins Regulates Their Polarized Sorting in Neurons
journal, May 2014

Chemically Etched Open Tubular and Monolithic Emitters for Nanoelectrospray Ionization Mass Spectrometry
journal, November 2006

  • Kelly, Ryan T.; Page, Jason S.; Luo, Quanzhou
  • Analytical Chemistry, Vol. 78, Issue 22, p. 7796-7801
  • DOI: 10.1021/ac061133r

Dynamics of the Rho-family small GTPases in actin regulation and motility
journal, March 2011

  • Spiering, Désirée; Hodgson, Louis
  • Cell Adhesion & Migration, Vol. 5, Issue 2
  • DOI: 10.4161/cam.5.2.14403

Mutations in the Transmembrane Domain and Cytoplasmic Tail of Hendra Virus Fusion Protein Disrupt Virus-Like-Particle Assembly
journal, May 2017

  • Cifuentes-Muñoz, Nicolás; Sun, Weina; Ray, Greeshma
  • Journal of Virology, Vol. 91, Issue 14
  • DOI: 10.1128/JVI.00152-17

Requirements for the Assembly and Release of Newcastle Disease Virus-Like Particles
journal, September 2006

  • Pantua, H. D.; McGinnes, L. W.; Peeples, M. E.
  • Journal of Virology, Vol. 80, Issue 22
  • DOI: 10.1128/JVI.00726-06

Endocytosis of the Nipah Virus Glycoproteins
journal, February 2005

Proteomic analysis of purified Newcastle disease virus particles
journal, January 2012

Unraveling a Three-Step Spatiotemporal Mechanism of Triggering of Receptor-Induced Nipah Virus Fusion and Cell Entry
journal, November 2013

Cytoplasmic Motifs in the Nipah Virus Fusion Protein Modulate Virus Particle Assembly and Egress
journal, March 2017

  • Johnston, Gunner P.; Contreras, Erik M.; Dabundo, Jeffrey
  • Journal of Virology, Vol. 91, Issue 10
  • DOI: 10.1128/JVI.02150-16

Tsg101 Is Recruited by a Late Domain of the Nucleocapsid Protein To Support Budding of Marburg Virus-Like Particles
journal, May 2010

  • Dolnik, O.; Kolesnikova, L.; Stevermann, L.
  • Journal of Virology, Vol. 84, Issue 15
  • DOI: 10.1128/JVI.00476-10

Promotion of virus assembly and organization by the measles virus matrix protein
journal, April 2018

Actin filaments disruption and stabilization affect measles virus maturation by different mechanisms
journal, January 2013

Interactions of human retroviruses with the host cell cytoskeleton
journal, August 2006

  • Fackler, Oliver T.; Kräusslich, Hans-Georg
  • Current Opinion in Microbiology, Vol. 9, Issue 4
  • DOI: 10.1016/j.mib.2006.06.010

AIP1/Alix Is a Binding Partner of Sendai Virus C Protein and Facilitates Virus Budding
journal, June 2005

Paramyxovirus Sendai virus-like particle formation by expression of multiple viral proteins and acceleration of its release by C protein
journal, July 2004

Virus-like particles as immunogens
journal, September 2003

Regulating Rho GTPases and their regulators
journal, June 2016

  • Hodge, Richard G.; Ridley, Anne J.
  • Nature Reviews Molecular Cell Biology, Vol. 17, Issue 8
  • DOI: 10.1038/nrm.2016.67

Regulation of endocytic traffic by Rho GTPases
journal, April 2003

  • Qualmann, Britta; Mellor, Harry
  • Biochemical Journal, Vol. 371, Issue 2
  • DOI: 10.1042/BJ20030139

Novel Henipa-like Virus, Mojiang Paramyxovirus, in Rats, China, 2012
journal, June 2014

  • Wu, Zhiqiang; Yang, Li; Yang, Fan
  • Emerging Infectious Diseases, Vol. 20, Issue 6
  • DOI: 10.3201/eid2006.131022

Cedar Virus: A Novel Henipavirus Isolated from Australian Bats
journal, August 2012

The targeting of Lamp1 to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane.
journal, February 1996

  • Rohrer, J.; Schweizer, A.; Russell, D.
  • The Journal of Cell Biology, Vol. 132, Issue 4
  • DOI: 10.1083/jcb.132.4.565

N-Glycans on the Nipah Virus Attachment Glycoprotein Modulate Fusion and Viral Entry as They Protect against Antibody Neutralization
journal, August 2012

  • Biering, S. B.; Huang, A.; Vu, A. T.
  • Journal of Virology, Vol. 86, Issue 22
  • DOI: 10.1128/JVI.01304-12

SNaPP: Simplified Nanoproteomics Platform for Reproducible Global Proteomic Analysis of Nanogram Protein Quantities
journal, March 2016

  • Huang, Eric L.; Piehowski, Paul D.; Orton, Daniel J.
  • Endocrinology, Vol. 157, Issue 3
  • DOI: 10.1210/en.2015-1821

Recruitment of Alix/AIP1 to the plasma membrane by Sendai virus C protein facilitates budding of virus-like particles
journal, February 2008

Influenza Virus M2 Protein Mediates ESCRT-Independent Membrane Scission
journal, September 2010

Role of Matrix and Fusion Proteins in Budding of Sendai Virus
journal, December 2001

Rho GTPase activity modulates paramyxovirus fusion protein-mediated cell–cell fusion
journal, July 2006

Subversion of the actin cytoskeleton during viral infection
journal, April 2011

  • Taylor, Matthew P.; Koyuncu, Orkide O.; Enquist, Lynn W.
  • Nature Reviews Microbiology, Vol. 9, Issue 6
  • DOI: 10.1038/nrmicro2574

Involvement of Clathrin-Mediated Endocytosis in Human Immunodeficiency Virus Type 1 Entry
journal, January 2005

Proteomic composition of Nipah virus-like particles
journal, February 2018

  • Vera-Velasco, Natalia Mara; García-Murria, Maria Jesús; Sánchez del Pino, Manuel M.
  • Journal of Proteomics, Vol. 172
  • DOI: 10.1016/j.jprot.2017.10.012

Virus-like particles: flexible platforms for vaccine development
journal, June 2007

Spatially-Resolved Proteomics: Rapid Quantitative Analysis of Laser Capture Microdissected Alveolar Tissue Samples
journal, December 2016

  • Clair, Geremy; Piehowski, Paul D.; Nicola, Teodora
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep39223

Late Assembly Motifs of Human T-Cell Leukemia Virus Type 1 and Their Relative Roles in Particle Release
journal, May 2004

Protein Analysis of Purified Respiratory Syncytial Virus Particles Reveals an Important Role for Heat Shock Protein 90 in Virus Particle Assembly
journal, June 2010

  • Radhakrishnan, Anuradha; Yeo, Dawn; Brown, Gaie
  • Molecular & Cellular Proteomics, Vol. 9, Issue 9
  • DOI: 10.1074/mcp.M110.001651

An LYPSL Late Domain in the Gag Protein Contributes to the Efficient Release and Replication of Rous Sarcoma Virus
journal, April 2010

  • Dilley, K. A.; Gregory, D.; Johnson, M. C.
  • Journal of Virology, Vol. 84, Issue 13
  • DOI: 10.1128/JVI.00238-10

Bats host major mammalian paramyxoviruses
journal, January 2012

  • Drexler, Jan Felix; Corman, Victor Max; Müller, Marcel Alexander
  • Nature Communications, Vol. 3, Issue 1
  • DOI: 10.1038/ncomms1796

The PTAP sequence duplication in HIV-1 subtype C Gag p6 in drug-naive subjects of India and South Africa
journal, January 2017

  • Sharma, Shilpee; Aralaguppe, Shambhu G.; Abrahams, Melissa-Rose
  • BMC Infectious Diseases, Vol. 17, Issue 1
  • DOI: 10.1186/s12879-017-2184-4

Novel Functions of Hendra Virus G N-Glycans and Comparisons to Nipah Virus
journal, May 2015

  • Bradel-Tretheway, Birgit G.; Liu, Qian; Stone, Jacquelyn A.
  • Journal of Virology, Vol. 89, Issue 14
  • DOI: 10.1128/JVI.00773-15

Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003

Mutations in human dynamin block an intermediate stage in coated vesicle formation
journal, August 1993

  • van der Bliek, Am; Redelmeier, Te; Damke, H.
  • The Journal of Cell Biology, Vol. 122, Issue 3
  • DOI: 10.1083/jcb.122.3.553

N-Glycans on Nipah Virus Fusion Protein Protect against Neutralization but Reduce Membrane Fusion and Viral Entry
journal, April 2006

Angiomotin functions in HIV-1 assembly and budding
journal, January 2015

Nipah Virus C Protein Recruits Tsg101 to Promote the Efficient Release of Virus in an ESCRT-Dependent Pathway
journal, May 2016

Rho Regulates Membrane Transport in the Endocytic Pathway to Control Plasma Membrane Specialization in Oligodendroglial Cells
journal, March 2007

Mechanisms for enveloped virus budding: Can some viruses do without an ESCRT?
journal, March 2008

Requirements for Budding of Paramyxovirus Simian Virus 5 Virus-Like Particles
journal, April 2002

Retroviral Assembly and Budding Occur through an Actin-Driven Mechanism
journal, November 2009

Respiratory syncytial virus uses a Vps4-independent budding mechanism controlled by Rab11-FIP2
journal, July 2008

  • Utley, T. J.; Ducharme, N. A.; Varthakavi, V.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 29
  • DOI: 10.1073/pnas.0712144105

Rho GTPases in cell biology
journal, December 2002

  • Etienne-Manneville, Sandrine; Hall, Alan
  • Nature, Vol. 420, Issue 6916
  • DOI: 10.1038/nature01148

Specific Activation of mTORC1 by Rheb G-protein in Vitro Involves Enhanced Recruitment of Its Substrate Protein
journal, March 2009

  • Sato, Tatsuhiro; Nakashima, Akio; Guo, Lea
  • Journal of Biological Chemistry, Vol. 284, Issue 19
  • DOI: 10.1074/jbc.M809207200

Polybasic KKR Motif in the Cytoplasmic Tail of Nipah Virus Fusion Protein Modulates Membrane Fusion by Inside-Out Signaling
journal, February 2007

  • Aguilar, H. C.; Matreyek, K. A.; Choi, D. Y.
  • Journal of Virology, Vol. 81, Issue 9
  • DOI: 10.1128/JVI.02205-06

Sendai virus induced cytoplasmic actin remodeling correlates with efficient virus particle production
journal, February 2011

Mumps Virus Matrix, Fusion, and Nucleocapsid Proteins Cooperate for Efficient Production of Virus-Like Particles
journal, May 2009

Electrostatic Interactions between Hendra Virus Matrix Proteins Are Required for Efficient Virus-Like-Particle Assembly
journal, April 2018

  • Liu, Yu Chih; Grusovin, Julian; Adams, Timothy E.
  • Journal of Virology, Vol. 92, Issue 13
  • DOI: 10.1128/JVI.00143-18
    Sort by:
    [ × clear filter / sort ]

    Similar Records in DOE PAGES and OSTI.GOV collections: