Kinesin-3 Mediates Axonal Sorting and Directional Transport of Alphaherpesvirus Particles in Neurons
Open accessAbstract
During infection of the nervous system, alphaherpesviruses-including pseudorabies virus (PRV)-use retrograde axonal transport to travel toward the neuronal cell body and anterograde transport to traffic back to the cell periphery upon reactivation from latency. The PRV protein Us9 plays an essential but unknown role in anterograde viral spread. To determine Us9 function, we identified viral and host proteins that interact with Us9 and explored the role of KIF1A, a microtubule-dependent kinesin-3 motor involved in axonal sorting and transport. Viral particles are cotransported with KIF1A in axons of primary rat superior cervical ganglion neurons, and overexpression or disruption of KIF1A function, respectively, increases and reduces anterograde capsid transport. Us9 and KIF1A interact early during infection with the aid of additional viral protein(s) but exhibit diminished binding at later stages, when capsids typically stall in axons. Thus, alphaherpesviruses repurpose the axonal transport and sorting pathway to spread within their hosts.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In PRV-infected neurons, Us9 interacts with KIF1A, and KIF1A is required for viral capsid transport in axons and for infection spread.
“the Enquist research group found that the viral protein Us9 interacts with the cellular kinesin KIF1A.”
From Proteomic approaches to uncovering virus–host protein interactions during the progression of viral infection (2016) · cites this paper as [42]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A protocol for rapid generation of recombinant adenoviruses using the AdEasy system
Luo, J., Deng, Z.-L., Luo, X., Tang, N., Song, W.-X., Chen, J., Sharff, K. A., Luu, H. H., Haydon, R. C., Kinzler, K. W., et al. (2007) · Nature Protocols · doi:10.1038/nprot.2007.135 · Cited by 854 · see citing works
Detergent binding explains anomalous SDS-PAGE migration of membrane proteins
Rath, A., Glibowicka, M., Nadeau, V. G., Chen, G., & Deber, C. M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813167106 · Cited by 816 · see citing works
Klopfenstein, D. R., Tomishige, M., Stuurman, N., & Vale, R. D. (2002) · Cell · doi:10.1016/s0092-8674(02)00708-0 · Cited by 327 · see citing works
Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons
Smith, G. A., Gross, S. P., & Enquist, L. W. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.061029798 · Cited by 270 · see citing works
Self-citationHerpesvirus Transport to the Nervous System and Back Again
Smith, G. A. (2012) · Annual Review of Microbiology · doi:10.1146/annurev-micro-092611-150051 · Cited by 200 · see citing works
Tsai, Y.-C., Greco, T. M., Boonmee, A., Miteva, Y., & Cristea, I. M. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.a111.015156 · Cited by 198 · see citing works
Self-citationA Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport
Pack-Chung, E., Kurshan, P. T., Dickman, D. K., & Schwarz, T. L. (2007) · Nature Neuroscience · doi:10.1038/nn1936 · Cited by 183 · see citing works
A Wide Extent of Inter-Strain Diversity in Virulent and Vaccine Strains of Alphaherpesviruses
SZPARA, M. L., Tafuri, Y. R., Parsons, L. R., Shamim, S. R., Verstrepen, K. J., Legendre, M., & Enquist, L. W. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002282 · Cited by 157 · see citing works
Self-citationLo, K. Y., Kuzmin, A., Unger, S. M., Petersen, J. D., & Silverman, M. A. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.01.018 · Cited by 155 · see citing works
Neuron-to-Cell Spread of Pseudorabies Virus in a Compartmented Neuronal Culture System
Ch’ng, T. H., & Enquist, L. W. (2005) · Journal of Virology · doi:10.1128/jvi.79.17.10875-10889.2005 · Cited by 122 · see citing works
Self-citationSant, C. V., Hagglund, R., Lopez, P., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.161283098 · Cited by 117 · see citing works
Brideau, A. D., Banfield, B. W., & Enquist, L. W. (1998) · Journal of Virology · doi:10.1128/jvi.72.6.4560-4570.1998 · Cited by 108 · see citing works
Self-citationKumar, J., Choudhary, B. C., Metpally, R. P. R., et al. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001200 · Cited by 104 · see citing works
Proteomic Characterization of Pseudorabies Virus Extracellular Virions
Kramer, T., Greco, T. M., Enquist, L. W., & Cristea, I. M. (2011) · Journal of Virology · doi:10.1128/jvi.02253-10 · Cited by 96 · see citing works
Self-citationAlphaherpesvirus Infection Disrupts Mitochondrial Transport in Neurons
Kramer, T., & Enquist, L. W. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.03.005 · Cited by 92 · see citing works
Self-citationPseudorabies Virus Us9 Directs Axonal Sorting of Viral Capsids
Lyman, M. G., Feierbach, B., Curanović, D., et al. (2007) · Journal of Virology · doi:10.1128/jvi.01281-07 · Cited by 81 · see citing works
Resolving the Assembly State of Herpes Simplex Virus during Axon Transport by Live-Cell Imaging
Antinone, S. E., Zaichick, S., & Smith, G. A. (2010) · Journal of Virology · doi:10.1128/jvi.01296-10 · Cited by 78 · see citing works
Brideau, A. D., Eldridge, M. G., & Enquist, L. W. (2000) · Journal of Virology · doi:10.1128/jvi.74.10.4549-4561.2000 · Cited by 67 · see citing works
Self-citationHerpes simplex virus type 2 membrane protein UL56 associates with the kinesin motor protein KIF1A
Koshizuka, T., Kawaguchi, Y., & Nishiyama, Y. (2005) · Journal of General Virology · doi:10.1099/vir.0.80633-0 · Cited by 65 · see citing works
Lyman, M. G., Curanović, D., & Enquist, L. W. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000065 · Cited by 59 · see citing works
Self-citationTaylor, M. P., Kramer, T., Lyman, M. G., Kratchmarov, R., & Enquist, L. W. (2012) · mBio · doi:10.1128/mbio.00063-12 · Cited by 54 · see citing works
Self-citationConjugation of Magnetic Beads for Immunopurification of Protein ComplexesPreprint
Cristea, I. M., & Chait, B. T. (2011) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5610 · Cited by 51 · see citing works
Self-citationCulturing Primary and Transformed Neuronal Cells for Studying Pseudorabies Virus Infection
Ch’ng, T. H., Flood, E. A., & Enquist, L. W. (2004) · Humana Press eBooks · doi:10.1385/1-59259-848-x:299 · Cited by 48 · see citing works
Self-citationUshijima, Y., Koshizuka, T., Goshima, F., Kimura, H., & Nishiyama, Y. (2008) · Journal of Virology · doi:10.1128/jvi.02515-07 · Cited by 46 · see citing works
Affinity Purification of Protein ComplexesPreprint
Cristea, I. M., & Chait, B. T. (2011) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5611 · Cited by 39 · see citing works
Self-citationCompartmented Neuron Cultures for Directional Infection by Alpha Herpesviruses
Curanović, D., Ch’ng, T. H., SZPARA, M. L., & Enquist, L. W. (2009) · Current Protocols in Cell Biology · doi:10.1002/0471143030.cb2604s43 · Cited by 39 · see citing works
Self-citationTsai, Y.-C., Greco, T. M., Boonmee, A., Miteva, Y., & Cristea, I. M. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m111.015156 · Cited by 36 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- Pellett PE Roizman B 2007 The Family: Herpesviridae A Brief Introduction 2 5 Philadelphia, PA Lippincott, Williams, and Wilkins
Cited by
Sorted by citations
Virus Infections in the Nervous System
Koyuncu, O. O., Hogue, I. B., & Enquist, L. W. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.03.010 · Cited by 594 · see citing works
Self-citationLum, K. K., & Cristea, I. M. (2016) · Expert Review of Proteomics · doi:10.1586/14789450.2016.1147353 · Cited by 113 · see citing works
Self-citationThe Impact of Mass Spectrometry–Based Proteomics on Fundamental Discoveries in Virology
Greco, T. M., Diner, B. A., & Cristea, I. M. (2014) · Annual Review of Virology · doi:10.1146/annurev-virology-031413-085527 · Cited by 67 · see citing works
Self-citationHistone Deacetylases in Herpesvirus Replication and Virus-Stimulated Host Defense
Guise, A., Budayeva, H., Diner, B., & Cristea, I. (2013) · Viruses · doi:10.3390/v5071607 · Cited by 43 · see citing works
Self-citationLin, A. E., Greco, T. M., Döhner, K., Sodeik, B., & Cristea, I. M. (2013) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m113.030866 · Cited by 38 · see citing works
Self-citationCell-fusion events induced by α-herpesviruses
Ambrosini, A. E., & Enquist, L. W. (2015) · Future Virology · doi:10.2217/fvl.14.100 · Cited by 15 · see citing works
Self-citation
- Authors
- Kramer, T., Greco, T. M., Taylor, M. P., Ambrosini, A. E., Cristea, I. M., & Enquist, L. W.
- Affiliations
- Princeton University (US)
- Corresponding author
- Enquist, Lynn W.
- Venue
- Cell Host & Microbe
- Publisher
- Elsevier BV
- Published
- 2012-12
- Volume
- 12
- Issue
- 6
- Pages
- 806-814
- ISSN
- 1931-3128 (ISSN-L)
- PMC
- PMC3527838
- OpenAlex
- W2048449303
- Cited by
- 102
- References
- 27
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 4 · 2023: 5 · 2022: 8 · 2021: 8 · 2020: 13 · 2019: 9 · 2018: 5 · 2017: 6 · 2016: 6 · 2015: 12 · 2014: 7 · 2013: 10
- FWCI
- 6.92
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Host & Microbe (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Drug Abuse (DP1DA026192)
- National Cancer Institute (P01CA087661)
- National Institute of Neurological Disorders and Stroke (R01NS060699, R01NS033506, R37 NS33506, R37NS033506)
- National Center for Research Resources (P40RR018604, P40 RR18604)
- Topics
- Health Sciences › Medicine › Epidemiology › Herpesvirus Infections and Treatments
- Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
- Health Sciences › Medicine › Epidemiology › Cytomegalovirus and herpesvirus research
- Keywords
- alphaherpesvirus, pseudorabies virus, KIF1A, kinesin-3, axonal transport, retrograde transport, viral protein-protein interaction, superior cervical ganglion neurons, viral spread, latency reactivation
- MeSH terms
- Animals, Cells, Cultured, Lipoproteins, Neurons, Phosphoproteins, Herpesvirus 1, Suid, Viral Proteins, Kinesins, Protein Interaction Mapping, Intracellular Signaling Peptides and Proteins, Rats, Host-Pathogen Interactions
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review