Electron tomography and simulation of baculovirus actin comet tails support a tethered filament model of pathogen propulsion.

Several pathogens induce propulsive actin comet tails in cells they invade to disseminate their infection. They achieve this by recruiting factors for actin nucleation, the Arp2/3 complex, and polymerization regulators from the host cytoplasm. Owing to limited information on the structural organizat...

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Autores principales:	Jan Mueller, Julia Pfanzelter, Christoph Winkler, Akihiro Narita, Christophe Le Clainche, Maria Nemethova, Marie-France Carlier, Yuichiro Maeda, Matthew D Welch, Taro Ohkawa, Christian Schmeiser, Guenter P Resch, J Victor Small
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2014
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/a9a2c84bb8f9439888998f9a715b2226
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spelling	oai:doaj.org-article:a9a2c84bb8f9439888998f9a715b22262021-11-18T05:37:37ZElectron tomography and simulation of baculovirus actin comet tails support a tethered filament model of pathogen propulsion.1544-91731545-788510.1371/journal.pbio.1001765https://doaj.org/article/a9a2c84bb8f9439888998f9a715b22262014-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24453943/pdf/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Several pathogens induce propulsive actin comet tails in cells they invade to disseminate their infection. They achieve this by recruiting factors for actin nucleation, the Arp2/3 complex, and polymerization regulators from the host cytoplasm. Owing to limited information on the structural organization of actin comets and in particular the spatial arrangement of filaments engaged in propulsion, the underlying mechanism of pathogen movement is currently speculative and controversial. Using electron tomography we have resolved the three-dimensional architecture of actin comet tails propelling baculovirus, the smallest pathogen yet known to hijack the actin motile machinery. Comet tail geometry was also mimicked in mixtures of virus capsids with purified actin and a minimal inventory of actin regulators. We demonstrate that propulsion is based on the assembly of a fishbone-like array of actin filaments organized in subsets linked by branch junctions, with an average of four filaments pushing the virus at any one time. Using an energy-minimizing function we have simulated the structure of actin comet tails as well as the tracks adopted by baculovirus in infected cells in vivo. The results from the simulations rule out gel squeezing models of propulsion and support those in which actin filaments are continuously tethered during branch nucleation and polymerization. Since Listeria monocytogenes, Shigella flexneri, and Vaccinia virus among other pathogens use the same common toolbox of components as baculovirus to move, we suggest they share the same principles of actin organization and mode of propulsion.Jan MuellerJulia PfanzelterChristoph WinklerAkihiro NaritaChristophe Le ClaincheMaria NemethovaMarie-France CarlierYuichiro MaedaMatthew D WelchTaro OhkawaChristian SchmeiserGuenter P ReschJ Victor SmallPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 12, Iss 1, p e1001765 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Jan Mueller Julia Pfanzelter Christoph Winkler Akihiro Narita Christophe Le Clainche Maria Nemethova Marie-France Carlier Yuichiro Maeda Matthew D Welch Taro Ohkawa Christian Schmeiser Guenter P Resch J Victor Small Electron tomography and simulation of baculovirus actin comet tails support a tethered filament model of pathogen propulsion.
description	Several pathogens induce propulsive actin comet tails in cells they invade to disseminate their infection. They achieve this by recruiting factors for actin nucleation, the Arp2/3 complex, and polymerization regulators from the host cytoplasm. Owing to limited information on the structural organization of actin comets and in particular the spatial arrangement of filaments engaged in propulsion, the underlying mechanism of pathogen movement is currently speculative and controversial. Using electron tomography we have resolved the three-dimensional architecture of actin comet tails propelling baculovirus, the smallest pathogen yet known to hijack the actin motile machinery. Comet tail geometry was also mimicked in mixtures of virus capsids with purified actin and a minimal inventory of actin regulators. We demonstrate that propulsion is based on the assembly of a fishbone-like array of actin filaments organized in subsets linked by branch junctions, with an average of four filaments pushing the virus at any one time. Using an energy-minimizing function we have simulated the structure of actin comet tails as well as the tracks adopted by baculovirus in infected cells in vivo. The results from the simulations rule out gel squeezing models of propulsion and support those in which actin filaments are continuously tethered during branch nucleation and polymerization. Since Listeria monocytogenes, Shigella flexneri, and Vaccinia virus among other pathogens use the same common toolbox of components as baculovirus to move, we suggest they share the same principles of actin organization and mode of propulsion.
format	article
author	Jan Mueller Julia Pfanzelter Christoph Winkler Akihiro Narita Christophe Le Clainche Maria Nemethova Marie-France Carlier Yuichiro Maeda Matthew D Welch Taro Ohkawa Christian Schmeiser Guenter P Resch J Victor Small
author_facet	Jan Mueller Julia Pfanzelter Christoph Winkler Akihiro Narita Christophe Le Clainche Maria Nemethova Marie-France Carlier Yuichiro Maeda Matthew D Welch Taro Ohkawa Christian Schmeiser Guenter P Resch J Victor Small
author_sort	Jan Mueller
title	Electron tomography and simulation of baculovirus actin comet tails support a tethered filament model of pathogen propulsion.
title_short	Electron tomography and simulation of baculovirus actin comet tails support a tethered filament model of pathogen propulsion.
title_full	Electron tomography and simulation of baculovirus actin comet tails support a tethered filament model of pathogen propulsion.
title_fullStr	Electron tomography and simulation of baculovirus actin comet tails support a tethered filament model of pathogen propulsion.
title_full_unstemmed	Electron tomography and simulation of baculovirus actin comet tails support a tethered filament model of pathogen propulsion.
title_sort	electron tomography and simulation of baculovirus actin comet tails support a tethered filament model of pathogen propulsion.
publisher	Public Library of Science (PLoS)
publishDate	2014
url	https://doaj.org/article/a9a2c84bb8f9439888998f9a715b2226
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Electron tomography and simulation of baculovirus actin comet tails support a tethered filament model of pathogen propulsion.

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