Real Time Analysis of Bovine Viral Diarrhea Virus (BVDV) Infection and Its Dependence on Bovine CD46
Abstract
:1. Introduction
2. Materials and Methods
2.1. Viruses and Cells
2.2. Life Cell Imaging
2.3. Image Processing and Analysis
3. Results
3.1. BVDV Entry Is a Slow Process
3.2. First Detection of BVDV E2-mCherry Signal Is Depending on MOI
3.3. CD46fluo Decreases the Speed of Directed Surface Motion of BVDVE2-mCherry
4. Discussion
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Burckhardt, C.J.; Greber, U.F. Virus movements on the plasma membrane support infection and transmission between cells. PLoS Pathog. 2009, 5, e1000621. [Google Scholar] [CrossRef] [PubMed]
- Lehmann, M.J.; Sherer, N.M.; Marks, C.B.; Pypaert, M.; Mothes, W. Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell Biol. 2005, 170, 317–325. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oh, M.-J.; Akhtar, J.; Desai, P.; Shukla, D. A role for heparan sulfate in viral surfing. Biochem. Biophys. Res. Commun. 2010, 391, 176–181. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schelhaas, M.; Shah, B.; Holzer, M.; Blattmann, P.; Kühling, L.; Day, P.M.; Schiller, J.T.; Helenius, A. Entry of human papillomavirus type 16 by actin-dependent, clathrin- and lipid raft-independent endocytosis. PLoS Pathog. 2012, 8, e1002657. [Google Scholar] [CrossRef] [PubMed]
- Ayala-Nuñez, N.V.; Wilschut, J.; Smit, J.M. Monitoring virus entry into living cells using DiD-labeled dengue virus particles. Methods 2011, 55, 137–143. [Google Scholar] [CrossRef]
- Zhang, S.L.-X.; Tan, H.-C.; Hanson, B.J.; Ooi, E.E. A simple method for Alexa Fluor dye labelling of dengue virus. J. Virol. Methods 2010, 167, 172–177. [Google Scholar] [CrossRef]
- Coller, K.E.; Berger, K.L.; Heaton, N.S.; Cooper, J.D.; Yoon, R.; Randall, G. RNA Interference and Single Particle Tracking Analysis of Hepatitis C Virus Endocytosis. PLoS Pathog. 2009, 5, e1000702. [Google Scholar] [CrossRef] [Green Version]
- van der Schaar, H.M.; Rust, M.J.; Chen, C.; van der Ende-Metselaar, H.; Wilschut, J.; Zhuang, X.; Smit, J.M. Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog. 2008, 4, e1000244. [Google Scholar] [CrossRef] [Green Version]
- Dejarnac, O.; Hafirassou, M.L.; Chazal, M.; Versapuech, M.; Gaillard, J.; Perera-Lecoin, M.; Umana-Diaz, C.; Bonnet-Madin, L.; Carnec, X.; Tinevez, J.Y.; et al. TIM-1 Ubiquitination Mediates Dengue Virus Entry. Cell Rep. 2018, 23, 1779–1793. [Google Scholar] [CrossRef]
- Tamura, T.; Fukuhara, T.; Uchida, T.; Ono, C.; Mori, H.; Sato, A.; Fauzyah, Y.; Okamoto, T.; Kurosu, T.; Setoh, Y.X.; et al. Characterization of Recombinant Flaviviridae Viruses Possessing a Small Reporter Tag. J. Virol. 2018, 92, e01582-17. [Google Scholar] [CrossRef] [Green Version]
- Tamura, T.; Igarashi, M.; Enkhbold, B.; Suzuki, T.; Okamatsu, M.; Ono, C.; Mori, H.; Izumi, T.; Sato, A.; Fauzyah, Y.; et al. In vivo dynamics of reporter Flaviviridae viruses. J. Virol. 2019. [Google Scholar] [CrossRef] [PubMed]
- Merwaiss, F.; Czibener, C.; Alvarez, D.E. Cell-to-Cell Transmission Is the Main Mechanism Supporting Bovine Viral Diarrhea Virus Spread in Cell Culture. J. Virol. 2019, 93. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Riedel, C.; Lamp, B.; Chen, H.-W.; Heimann, M.; Rümenapf, T. Fluorophore labelled BVDV: A novel tool for the analysis of infection dynamics. Sci. Rep. 2019, 9, 5972. [Google Scholar] [CrossRef]
- Iqbal, M.; Flick-Smith, H.; McCauley, J.W. Interactions of bovine viral diarrhoea virus glycoprotein E(rns) with cell surface glycosaminoglycans. J. Gen. Virol. 2000, 81, 451–459. [Google Scholar] [CrossRef] [PubMed]
- Maurer, K.; Krey, T.; Moennig, V.; Thiel, H.-J.; Rümenapf, T. CD46 is a cellular receptor for bovine viral diarrhea virus. J. Virol. 2004, 78, 1792–1799. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Krey, T.; Himmelreich, A.; Heimann, M.; Menge, C.; Thiel, H.-J.; Maurer, K.; Rümenapf, T. Function of bovine CD46 as a cellular receptor for bovine viral diarrhea virus is determined by complement control protein 1. J. Virol. 2006, 80, 3912–3922. [Google Scholar] [CrossRef] [Green Version]
- Grummer, B.; Grotha, S.; Greiser-Wilke, I. Bovine Viral Diarrhoea Virus is Internalized by Clathrin-dependent Receptor-mediated Endocytosis. J. Vet. Med. Ser. B 2004, 51, 427–432. [Google Scholar] [CrossRef]
- Lecot, S.; Belouzard, S.; Dubuisson, J.; Rouillé, Y. Bovine viral diarrhea virus entry is dependent on clathrin-mediated endocytosis. J. Virol. 2005, 79, 10826–10829. [Google Scholar] [CrossRef] [Green Version]
- Krey, T.; Thiel, H.-J.; Rümenapf, T. Acid-resistant bovine pestivirus requires activation for pH-triggered fusion during entry. J. Virol. 2005, 79, 4191–4200. [Google Scholar] [CrossRef] [Green Version]
- Cattaneo, R. Four viruses, two bacteria, and one receptor: Membrane cofactor protein (CD46) as pathogens’ magnet. J. Virol. 2004, 78, 4385–4388. [Google Scholar] [CrossRef] [Green Version]
- Ni Choileain, S.; Astier, A.L. CD46 processing: A means of expression. Immunobiology 2012, 217, 169–175. [Google Scholar] [CrossRef] [Green Version]
- Crimeen-Irwin, B.; Ellis, S.; Christiansen, D.; Ludford-Menting, M.J.; Milland, J.; Lanteri, M.; Loveland, B.E.; Gerlier, D.; Russell, S.M. Ligand binding determines whether CD46 is internalized by clathrin-coated pits or macropinocytosis. J. Biol. Chem. 2003, 278, 46927–46937. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Persson, B.D.; Schmitz, N.B.; Santiago, C.; Zocher, G.; Larvie, M.; Scheu, U.; Casasnovas, J.M.; Stehle, T. Structure of the extracellular portion of CD46 provides insights into its interactions with complement proteins and pathogens. PLoS Pathog. 2010, 6, e1001122. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schneider, C.A.; Rasband, W.S.; Eliceiri, K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9, 671–675. [Google Scholar] [CrossRef] [PubMed]
- Marini, F.; Mazur, J.; Binder, H. flowcatchR: A user-friendly workflow solution for the analysis of time-lapse cell flow imaging data. F1000Research 2015, 4. [Google Scholar] [CrossRef]
- Kohler, F.; Rohrbach, A. Surfing along Filopodia: A Particle Transport Revealed by Molecular-Scale Fluctuation Analyses. Biophys. J. 2015, 108, 2114–2125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schmeiser, S.; Mast, J.; Thiel, H.-J.; König, M. Morphogenesis of pestiviruses: New insights from ultrastructural studies of strain Giraffe-1. J. Virol. 2014, 88, 2717–2724. [Google Scholar] [CrossRef] [Green Version]
- Gray, E.W.; Nettleton, P.F. The Ultrastructure of Cell Cultures Infected with Border Disease and Bovine Virus Diarrhoea Viruses. J. Gen. Virol. 1987, 68, 2339–2346. [Google Scholar] [CrossRef]
- Gerold, G.; Bruening, J.; Weigel, B.; Pietschmann, T. Protein Interactions during the Flavivirus and Hepacivirus Life Cycle. Mol. Cell. Proteomics 2017, 16, S75–S91. [Google Scholar] [CrossRef] [Green Version]
- Zezafoun, H.; Decreux, A.; Desmecht, D. Genetic and splice variations of Bos taurus CD46 shift cell permissivity to BVDV, the bovine pestivirus. Vet. Microbiol. 2011, 152, 315–327. [Google Scholar] [CrossRef] [Green Version]
- Lee, Y.-M.; Tscherne, D.M.; Yun, S.-I.; Frolov, I.; Rice, C.M. Dual Mechanisms of Pestiviral Superinfection Exclusion at Entry and RNA Replication. J. Virol. 2005, 79, 3231–3242. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Romero-Brey, I.; Merz, A.; Chiramel, A.; Lee, J.-Y.; Chlanda, P.; Haselman, U.; Santarella-Mellwig, R.; Habermann, A.; Hoppe, S.; Kallis, S.; et al. Three-Dimensional Architecture and Biogenesis of Membrane Structures Associated with Hepatitis C Virus Replication. PLoS Pathog. 2012, 8, e1003056. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Welsch, S.; Miller, S.; Romero-Brey, I.; Merz, A.; Bleck, C.K.E.; Walther, P.; Fuller, S.D.; Antony, C.; Krijnse-Locker, J.; Bartenschlager, R. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 2009, 5, 365–375. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cortese, M.; Goellner, S.; Acosta, E.G.; Neufeldt, C.J.; Oleksiuk, O.; Lampe, M.; Haselmann, U.; Funaya, C.; Schieber, N.; Ronchi, P.; et al. Ultrastructural Characterization of Zika Virus Replication Factories. Cell Rep. 2017, 18, 2113–2123. [Google Scholar] [CrossRef] [Green Version]
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Riedel, C.; Chen, H.-W.; Reichart, U.; Lamp, B.; Laketa, V.; Rümenapf, T. Real Time Analysis of Bovine Viral Diarrhea Virus (BVDV) Infection and Its Dependence on Bovine CD46. Viruses 2020, 12, 116. https://doi.org/10.3390/v12010116
Riedel C, Chen H-W, Reichart U, Lamp B, Laketa V, Rümenapf T. Real Time Analysis of Bovine Viral Diarrhea Virus (BVDV) Infection and Its Dependence on Bovine CD46. Viruses. 2020; 12(1):116. https://doi.org/10.3390/v12010116
Chicago/Turabian StyleRiedel, Christiane, Hann-Wei Chen, Ursula Reichart, Benjamin Lamp, Vibor Laketa, and Till Rümenapf. 2020. "Real Time Analysis of Bovine Viral Diarrhea Virus (BVDV) Infection and Its Dependence on Bovine CD46" Viruses 12, no. 1: 116. https://doi.org/10.3390/v12010116
APA StyleRiedel, C., Chen, H.-W., Reichart, U., Lamp, B., Laketa, V., & Rümenapf, T. (2020). Real Time Analysis of Bovine Viral Diarrhea Virus (BVDV) Infection and Its Dependence on Bovine CD46. Viruses, 12(1), 116. https://doi.org/10.3390/v12010116