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Pseudorabies virus US3-induced tunneling nanotubes contain stabilized microtubules, interact with neighboring cells via cadherins, and allow intercellular molecular communication

Robert Jansens (UGent) , Wim Van Den Broeck (UGent) , Steffi De Pelsmaeker (UGent) , Jochen Lamote (UGent) , Cliff Van Waesberghe (UGent) , Liesbeth Couck (UGent) and Herman Favoreel (UGent)
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Abstract
Tunneling nanotubes (TNTs) are long bridge-like structures that connect eukaryotic cells and mediate intercellular communication. We found earlier that the conserved alphaherpesvirus US3 protein kinase induces long cell projections that contact distant cells and promote intercellular virus spread. In this report, we show that the US3-induced cell projections constitute TNTs. In addition, we report that US3-induced TNTs mediate intercellular transport of information (e.g., green fluorescent protein [GFP]) in the absence of other viral proteins. US3-induced TNTs are remarkably stable compared to most TNTs described in the literature. In line with this, US3-induced TNTs were found to contain stabilized (acetylated and detyrosinated) microtubules. Transmission electron microscopy showed that virus particles are individually transported in membrane-bound vesicles in US3-induced TNTs and are released along the TNT and at the contact area between a TNT and the adjacent cell. Contact between US3-induced TNTs and acceptor cells is very stable, which correlated with a marked enrichment in adherens junction components beta-catenin and E-cadherin at the contact area. These data provide new structural insights into US3-induced TNTs and how they may contribute to intercellular communication and alphaherpesvirus spread. IMPORTANCE: Tunneling nanotubes (TNT) represent an important and yet still poorly understood mode of long-distance intercellular communication. We and others reported earlier that the conserved alphaherpesvirus US3 protein kinase induces long cellular protrusions in infected and transfected cells. Here, we show that US3-induced cell projections constitute TNTs, based on structural properties and transport of biomolecules. In addition, we report on different particular characteristics of US3-induced TNTs that help to explain their remarkable stability compared to physiological TNTs. In addition, transmission electron microscopy assays indicate that, in infected cells, virions travel in the US3-induced TNTs in membranous transport vesicles and leave the TNT via exocytosis. These data generate new fundamental insights into the biology of (US3-induced) TNTs and into how they may contribute to intercellular virus spread and communication.
Keywords
pseudorabies virus, PRV, herpes, US3, tunneling nanotubes, TNT, cadherins, microtubules, pseudorabies, US3 PROTEIN-KINASE, ACTIN CYTOSKELETON, MITOCHONDRIAL TRANSPORT, SINGLE GENES, SPREAD, INFECTION, ALPHAHERPESVIRUS, APOPTOSIS, PHOSPHORYLATION, PENETRATION

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MLA
Jansens, Robert et al. “Pseudorabies Virus US3-induced Tunneling Nanotubes Contain Stabilized Microtubules, Interact with Neighboring Cells via Cadherins, and Allow Intercellular Molecular Communication.” JOURNAL OF VIROLOGY 91.19 (2017): n. pag. Print.
APA
Jansens, R., Van Den Broeck, W., De Pelsmaeker, S., Lamote, J., Van Waesberghe, C., Couck, L., & Favoreel, H. (2017). Pseudorabies virus US3-induced tunneling nanotubes contain stabilized microtubules, interact with neighboring cells via cadherins, and allow intercellular molecular communication. JOURNAL OF VIROLOGY, 91(19).
Chicago author-date
Jansens, Robert, Wim Van Den Broeck, Steffi De Pelsmaeker, Jochen Lamote, Cliff Van Waesberghe, Liesbeth Couck, and Herman Favoreel. 2017. “Pseudorabies Virus US3-induced Tunneling Nanotubes Contain Stabilized Microtubules, Interact with Neighboring Cells via Cadherins, and Allow Intercellular Molecular Communication.” Journal of Virology 91 (19).
Chicago author-date (all authors)
Jansens, Robert, Wim Van Den Broeck, Steffi De Pelsmaeker, Jochen Lamote, Cliff Van Waesberghe, Liesbeth Couck, and Herman Favoreel. 2017. “Pseudorabies Virus US3-induced Tunneling Nanotubes Contain Stabilized Microtubules, Interact with Neighboring Cells via Cadherins, and Allow Intercellular Molecular Communication.” Journal of Virology 91 (19).
Vancouver
1.
Jansens R, Van Den Broeck W, De Pelsmaeker S, Lamote J, Van Waesberghe C, Couck L, et al. Pseudorabies virus US3-induced tunneling nanotubes contain stabilized microtubules, interact with neighboring cells via cadherins, and allow intercellular molecular communication. JOURNAL OF VIROLOGY. 2017;91(19).
IEEE
[1]
R. Jansens et al., “Pseudorabies virus US3-induced tunneling nanotubes contain stabilized microtubules, interact with neighboring cells via cadherins, and allow intercellular molecular communication,” JOURNAL OF VIROLOGY, vol. 91, no. 19, 2017.
@article{8541733,
  abstract     = {Tunneling nanotubes (TNTs) are long bridge-like structures that connect eukaryotic cells and mediate intercellular communication. We found earlier that the conserved alphaherpesvirus US3 protein kinase induces long cell projections that contact distant cells and promote intercellular virus spread. In this report, we show that the US3-induced cell projections constitute TNTs. In addition, we report that US3-induced TNTs mediate intercellular transport of information (e.g., green fluorescent protein [GFP]) in the absence of other viral proteins. US3-induced TNTs are remarkably stable compared to most TNTs described in the literature. In line with this, US3-induced TNTs were found to contain stabilized (acetylated and detyrosinated) microtubules. Transmission electron microscopy showed that virus particles are individually transported in membrane-bound vesicles in US3-induced TNTs and are released along the TNT and at the contact area between a TNT and the adjacent cell. Contact between US3-induced TNTs and acceptor cells is very stable, which correlated with a marked enrichment in adherens junction components beta-catenin and E-cadherin at the contact area. These data provide new structural insights into US3-induced TNTs and how they may contribute to intercellular communication and alphaherpesvirus spread. 
IMPORTANCE: Tunneling nanotubes (TNT) represent an important and yet still poorly understood mode of long-distance intercellular communication. We and others reported earlier that the conserved alphaherpesvirus US3 protein kinase induces long cellular protrusions in infected and transfected cells. Here, we show that US3-induced cell projections constitute TNTs, based on structural properties and transport of biomolecules. In addition, we report on different particular characteristics of US3-induced TNTs that help to explain their remarkable stability compared to physiological TNTs. In addition, transmission electron microscopy assays indicate that, in infected cells, virions travel in the US3-induced TNTs in membranous transport vesicles and leave the TNT via exocytosis. These data generate new fundamental insights into the biology of (US3-induced) TNTs and into how they may contribute to intercellular virus spread and communication.},
  articleno    = {e00749-17},
  author       = {Jansens, Robert and Van Den Broeck, Wim and De Pelsmaeker, Steffi and Lamote, Jochen and Van Waesberghe, Cliff and Couck, Liesbeth and Favoreel, Herman},
  issn         = {0022-538X},
  journal      = {JOURNAL OF VIROLOGY},
  keywords     = {pseudorabies virus,PRV,herpes,US3,tunneling nanotubes,TNT,cadherins,microtubules,pseudorabies,US3 PROTEIN-KINASE,ACTIN CYTOSKELETON,MITOCHONDRIAL TRANSPORT,SINGLE GENES,SPREAD,INFECTION,ALPHAHERPESVIRUS,APOPTOSIS,PHOSPHORYLATION,PENETRATION},
  language     = {eng},
  number       = {19},
  pages        = {13},
  title        = {Pseudorabies virus US3-induced tunneling nanotubes contain stabilized microtubules, interact with neighboring cells via cadherins, and allow intercellular molecular communication},
  url          = {http://dx.doi.org/10.1128/jvi.00749-17},
  volume       = {91},
  year         = {2017},
}

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