Glycoproteins gE and gI Are Required for Efficient KIF1A-Dependent Anterograde Axonal Transport of Alphaherpesvirus Particles in Neurons
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| Published in | Journal of Virology Vol. 87; no. 17; pp. 9431 - 9440 |
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| Main Authors | , , , , , , |
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| Language | English |
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American Society for Microbiology
01.09.2013
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| ISSN | 0022-538X 1098-5514 1098-5514 |
| DOI | 10.1128/JVI.01317-13 |
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Alphaherpesviruses, including pseudorabies virus (PRV), spread directionally within the nervous systems of their mammalian hosts. Three viral membrane proteins are required for efficient anterograde-directed spread of infection in neurons, including Us9 and a heterodimer composed of the glycoproteins gE and gI. We previously demonstrated that the kinesin-3 motor KIF1A mediates anterograde-directed transport of viral particles in axons of cultured peripheral nervous system (PNS) neurons. The PRV Us9 protein copurifies with KIF1A, recruiting the motor to transport vesicles, but at least one unidentified additional viral protein is necessary for this interaction. Here we show that gE/gI are required for efficient anterograde transport of viral particles in axons by mediating the interaction between Us9 and KIF1A. In the absence of gE/gI, viral particles containing green fluorescent protein (GFP)-tagged Us9 are assembled in the cell body but are not sorted efficiently into axons. Importantly, we found that gE/gI are necessary for efficient copurification of KIF1A with Us9, especially at early times after infection. We also constructed a PRV recombinant that expresses a functional gE-GFP fusion protein and used affinity purification coupled with mass spectrometry to identify gE-interacting proteins. Several viral and host proteins were found to associate with gE-GFP. Importantly, both gI and Us9, but not KIF1A, copurified with gE-GFP. We propose that gE/gI are required for efficient KIF1A-mediated anterograde transport of viral particles because they indirectly facilitate or stabilize the interaction between Us9 and KIF1A. Alphaherpesviruses, including pseudorabies virus (PRV), spread directionally within the nervous systems of their mammalian hosts. Three viral membrane proteins are required for efficient anterograde-directed spread of infection in neurons, including Us9 and a heterodimer composed of the glycoproteins gE and gI. We previously demonstrated that the kinesin-3 motor KIF1A mediates anterograde-directed transport of viral particles in axons of cultured peripheral nervous system (PNS) neurons. The PRV Us9 protein copurifies with KIF1A, recruiting the motor to transport vesicles, but at least one unidentified additional viral protein is necessary for this interaction. Here we show that gE/gI are required for efficient anterograde transport of viral particles in axons by mediating the interaction between Us9 and KIF1A. In the absence of gE/gI, viral particles containing green fluorescent protein (GFP)-tagged Us9 are assembled in the cell body but are not sorted efficiently into axons. Importantly, we found that gE/gI are necessary for efficient copurification of KIF1A with Us9, especially at early times after infection. We also constructed a PRV recombinant that expresses a functional gE-GFP fusion protein and used affinity purification coupled with mass spectrometry to identify gE-interacting proteins. Several viral and host proteins were found to associate with gE-GFP. Importantly, both gI and Us9, but not KIF1A, copurified with gE-GFP. We propose that gE/gI are required for efficient KIF1A-mediated anterograde transport of viral particles because they indirectly facilitate or stabilize the interaction between Us9 and KIF1A.Alphaherpesviruses, including pseudorabies virus (PRV), spread directionally within the nervous systems of their mammalian hosts. Three viral membrane proteins are required for efficient anterograde-directed spread of infection in neurons, including Us9 and a heterodimer composed of the glycoproteins gE and gI. We previously demonstrated that the kinesin-3 motor KIF1A mediates anterograde-directed transport of viral particles in axons of cultured peripheral nervous system (PNS) neurons. The PRV Us9 protein copurifies with KIF1A, recruiting the motor to transport vesicles, but at least one unidentified additional viral protein is necessary for this interaction. Here we show that gE/gI are required for efficient anterograde transport of viral particles in axons by mediating the interaction between Us9 and KIF1A. In the absence of gE/gI, viral particles containing green fluorescent protein (GFP)-tagged Us9 are assembled in the cell body but are not sorted efficiently into axons. Importantly, we found that gE/gI are necessary for efficient copurification of KIF1A with Us9, especially at early times after infection. We also constructed a PRV recombinant that expresses a functional gE-GFP fusion protein and used affinity purification coupled with mass spectrometry to identify gE-interacting proteins. Several viral and host proteins were found to associate with gE-GFP. Importantly, both gI and Us9, but not KIF1A, copurified with gE-GFP. We propose that gE/gI are required for efficient KIF1A-mediated anterograde transport of viral particles because they indirectly facilitate or stabilize the interaction between Us9 and KIF1A. |
| Author | Toh Hean Ch'ng Ileana M. Cristea Todd M. Greco Matthew P. Taylor Tal Kramer Radomir Kratchmarov Lynn W. Enquist |
| Author_xml | – sequence: 1 givenname: Radomir surname: Kratchmarov fullname: Kratchmarov, Radomir organization: Department of Molecular Biology, Princeton University, Princeton, New Jersey, USA – sequence: 2 givenname: Tal surname: Kramer fullname: Kramer, Tal organization: Department of Molecular Biology, Princeton University, Princeton, New Jersey, USA – sequence: 3 givenname: Todd M. surname: Greco fullname: Greco, Todd M. organization: Department of Molecular Biology, Princeton University, Princeton, New Jersey, USA – sequence: 4 givenname: Matthew P. surname: Taylor fullname: Taylor, Matthew P. organization: Department of Molecular Biology, Princeton University, Princeton, New Jersey, USA – sequence: 5 givenname: Toh Hean surname: Ch'ng fullname: Ch'ng, Toh Hean organization: Department of Molecular Biology, Princeton University, Princeton, New Jersey, USA – sequence: 6 givenname: Ileana M. surname: Cristea fullname: Cristea, Ileana M. organization: Department of Molecular Biology, Princeton University, Princeton, New Jersey, USA – sequence: 7 givenname: Lynn W. surname: Enquist fullname: Enquist, Lynn W. organization: Department of Molecular Biology, Princeton University, Princeton, New Jersey, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23804637$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Present address: Tal Kramer, F.M. Kirby Neurobiology Center, Children's Hospital Boston and Harvard Medical School, Boston, Massachusetts, USA; Toh Hean Ch'ng, Department of Biological Chemistry, University of California, Los Angeles, Los Angeles, California, USA. R.K. and T.K. contributed equally to this article. |
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Mendeley... Alphaherpesviruses, including pseudorabies virus (PRV), spread directionally within the nervous systems of their mammalian hosts. Three viral membrane proteins... |
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| StartPage | 9431 |
| SubjectTerms | Alphaherpesvirinae - genetics Alphaherpesvirinae - pathogenicity Alphaherpesvirinae - physiology Alphaherpesvirus Animals Axonal Transport - physiology Cell Line Cells, Cultured Herpesvirus 1, Suid - genetics Herpesvirus 1, Suid - pathogenicity Herpesvirus 1, Suid - physiology Host-Pathogen Interactions Kinesin - physiology Lipoproteins - genetics Lipoproteins - physiology Neurons - physiology Neurons - virology PC12 Cells Phosphoproteins - genetics Phosphoproteins - physiology Pseudorabies virus Rats Recombinant Fusion Proteins - genetics Recombinant Fusion Proteins - physiology Swine Viral Envelope Proteins - genetics Viral Envelope Proteins - physiology Viral Proteins - genetics Viral Proteins - physiology Virion - physiology Virus-Cell Interactions |
| Title | Glycoproteins gE and gI Are Required for Efficient KIF1A-Dependent Anterograde Axonal Transport of Alphaherpesvirus Particles in Neurons |
| URI | http://jvi.asm.org/content/87/17/9431.abstract https://www.ncbi.nlm.nih.gov/pubmed/23804637 https://www.proquest.com/docview/1424326078 https://www.proquest.com/docview/1434020166 https://pubmed.ncbi.nlm.nih.gov/PMC3754139 |
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