Mechanism of membranous tunnelling nanotube formation in viral genome delivery.

In internal membrane-containing viruses, a lipid vesicle enclosed by the icosahedral capsid protects the genome. It has been postulated that this internal membrane is the genome delivery device of the virus. Viruses built with this architectural principle infect hosts in all three domains of cellula...

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Autores principales:	Bibiana Peralta, David Gil-Carton, Daniel Castaño-Díez, Aurelie Bertin, Claire Boulogne, Hanna M Oksanen, Dennis H Bamford, Nicola G A Abrescia
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2013
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/8784f7461d924e919a9a34b728deeba3
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spelling	oai:doaj.org-article:8784f7461d924e919a9a34b728deeba32021-11-18T05:37:49ZMechanism of membranous tunnelling nanotube formation in viral genome delivery.1544-91731545-788510.1371/journal.pbio.1001667https://doaj.org/article/8784f7461d924e919a9a34b728deeba32013-09-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24086111/pdf/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885In internal membrane-containing viruses, a lipid vesicle enclosed by the icosahedral capsid protects the genome. It has been postulated that this internal membrane is the genome delivery device of the virus. Viruses built with this architectural principle infect hosts in all three domains of cellular life. Here, using a combination of electron microscopy techniques, we investigate bacteriophage PRD1, the best understood model for such viruses, to unveil the mechanism behind the genome translocation across the cell envelope. To deliver its double-stranded DNA, the icosahedral protein-rich virus membrane transforms into a tubular structure protruding from one of the 12 vertices of the capsid. We suggest that this viral nanotube exits from the same vertex used for DNA packaging, which is biochemically distinct from the other 11. The tube crosses the capsid through an aperture corresponding to the loss of the peripentonal P3 major capsid protein trimers, penton protein P31 and membrane protein P16. The remodeling of the internal viral membrane is nucleated by changes in osmolarity and loss of capsid-membrane interactions as consequence of the de-capping of the vertices. This engages the polymerization of the tail tube, which is structured by membrane-associated proteins. We have observed that the proteo-lipidic tube in vivo can pierce the gram-negative bacterial cell envelope allowing the viral genome to be shuttled to the host cell. The internal diameter of the tube allows one double-stranded DNA chain to be translocated. We conclude that the assembly principles of the viral tunneling nanotube take advantage of proteo-lipid interactions that confer to the tail tube elastic, mechanical and functional properties employed also in other protein-membrane systems.Bibiana PeraltaDavid Gil-CartonDaniel Castaño-DíezAurelie BertinClaire BoulogneHanna M OksanenDennis H BamfordNicola G A AbresciaPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 11, Iss 9, p e1001667 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Bibiana Peralta David Gil-Carton Daniel Castaño-Díez Aurelie Bertin Claire Boulogne Hanna M Oksanen Dennis H Bamford Nicola G A Abrescia Mechanism of membranous tunnelling nanotube formation in viral genome delivery.
description	In internal membrane-containing viruses, a lipid vesicle enclosed by the icosahedral capsid protects the genome. It has been postulated that this internal membrane is the genome delivery device of the virus. Viruses built with this architectural principle infect hosts in all three domains of cellular life. Here, using a combination of electron microscopy techniques, we investigate bacteriophage PRD1, the best understood model for such viruses, to unveil the mechanism behind the genome translocation across the cell envelope. To deliver its double-stranded DNA, the icosahedral protein-rich virus membrane transforms into a tubular structure protruding from one of the 12 vertices of the capsid. We suggest that this viral nanotube exits from the same vertex used for DNA packaging, which is biochemically distinct from the other 11. The tube crosses the capsid through an aperture corresponding to the loss of the peripentonal P3 major capsid protein trimers, penton protein P31 and membrane protein P16. The remodeling of the internal viral membrane is nucleated by changes in osmolarity and loss of capsid-membrane interactions as consequence of the de-capping of the vertices. This engages the polymerization of the tail tube, which is structured by membrane-associated proteins. We have observed that the proteo-lipidic tube in vivo can pierce the gram-negative bacterial cell envelope allowing the viral genome to be shuttled to the host cell. The internal diameter of the tube allows one double-stranded DNA chain to be translocated. We conclude that the assembly principles of the viral tunneling nanotube take advantage of proteo-lipid interactions that confer to the tail tube elastic, mechanical and functional properties employed also in other protein-membrane systems.
format	article
author	Bibiana Peralta David Gil-Carton Daniel Castaño-Díez Aurelie Bertin Claire Boulogne Hanna M Oksanen Dennis H Bamford Nicola G A Abrescia
author_facet	Bibiana Peralta David Gil-Carton Daniel Castaño-Díez Aurelie Bertin Claire Boulogne Hanna M Oksanen Dennis H Bamford Nicola G A Abrescia
author_sort	Bibiana Peralta
title	Mechanism of membranous tunnelling nanotube formation in viral genome delivery.
title_short	Mechanism of membranous tunnelling nanotube formation in viral genome delivery.
title_full	Mechanism of membranous tunnelling nanotube formation in viral genome delivery.
title_fullStr	Mechanism of membranous tunnelling nanotube formation in viral genome delivery.
title_full_unstemmed	Mechanism of membranous tunnelling nanotube formation in viral genome delivery.
title_sort	mechanism of membranous tunnelling nanotube formation in viral genome delivery.
publisher	Public Library of Science (PLoS)
publishDate	2013
url	https://doaj.org/article/8784f7461d924e919a9a34b728deeba3
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Mechanism of membranous tunnelling nanotube formation in viral genome delivery.

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