Encapsidated Host Factors in Alphavirus Particles Influence Midgut Infection of Aedes aegypti

Transmission of mosquito-borne viruses requires the efficient infection of both a permissive vertebrate host and a competent mosquito vector. The infectivity of Sindbis virus (SINV), the type species of the Alphavirus genus, is influenced by both the original and new host cell. We have shown that in...

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Main Authors: David Mackenzie-Liu, Kevin J. Sokoloski, Sarah Purdy, Richard W. Hardy
Format: Article
Language:English
Published: MDPI AG 2018-05-01
Series:Viruses
Subjects:
Online Access:http://www.mdpi.com/1999-4915/10/5/263
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author David Mackenzie-Liu
Kevin J. Sokoloski
Sarah Purdy
Richard W. Hardy
author_facet David Mackenzie-Liu
Kevin J. Sokoloski
Sarah Purdy
Richard W. Hardy
author_sort David Mackenzie-Liu
collection DOAJ
description Transmission of mosquito-borne viruses requires the efficient infection of both a permissive vertebrate host and a competent mosquito vector. The infectivity of Sindbis virus (SINV), the type species of the Alphavirus genus, is influenced by both the original and new host cell. We have shown that infection of vertebrate cells by SINV, chikungunya virus (CHIKV), and Ross River virus (RRV) produces two subpopulations of virus particles separable based on density. In contrast, a single population of viral particles is produced by mosquito cells. Previous studies demonstrated that the denser vertebrate-derived particles and the mosquito-derived particles contain components of the small subunit of the host cell ribosome, whereas the less dense vertebrate-derived particles do not. Infection of mice with RRV showed that both particle subpopulations are produced in an infected vertebrate, but in a tissue specific manner with serum containing only the less dense version of the virus particles. Previous infectivity studies using SINV particles have shown that the denser particles (SINVHeavy) and mosquito derived particles SINVC6/36 are significantly more infectious in vertebrate cells than the less dense vertebrate derived particles (SINVLight). The current study shows that SINVLight particles, initiate the infection of the mosquito midgut more efficiently than SINVHeavy particles and that this enhanced infectivity is associated with an exacerbated immune response to SINVLight infection in midgut tissues. The enhanced infection of SINVLight is specific to the midgut as intrathoracically injected virus do not exhibit the same fitness advantage. Together, our data indicate a biologically significant role for the SINVLight subpopulation in the efficient transmission from infected vertebrates to the mosquito vector.
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spelling doaj.art-c9ca3716c9f44acf8d0df4bd76a5355c2022-12-22T00:54:05ZengMDPI AGViruses1999-49152018-05-0110526310.3390/v10050263v10050263Encapsidated Host Factors in Alphavirus Particles Influence Midgut Infection of Aedes aegyptiDavid Mackenzie-Liu0Kevin J. Sokoloski1Sarah Purdy2Richard W. Hardy3Department of Biology, Indiana University, Bloomington, IN 47405, USADepartment of Microbiology and Immunology, and the Center for Predictive Medicine for Biodefense and Emerging Infectious Diseases, University of Louisville School of Medicine, Louisville, KY 40202, USADepartment of Biology, Indiana University, Bloomington, IN 47405, USADepartment of Biology, Indiana University, Bloomington, IN 47405, USATransmission of mosquito-borne viruses requires the efficient infection of both a permissive vertebrate host and a competent mosquito vector. The infectivity of Sindbis virus (SINV), the type species of the Alphavirus genus, is influenced by both the original and new host cell. We have shown that infection of vertebrate cells by SINV, chikungunya virus (CHIKV), and Ross River virus (RRV) produces two subpopulations of virus particles separable based on density. In contrast, a single population of viral particles is produced by mosquito cells. Previous studies demonstrated that the denser vertebrate-derived particles and the mosquito-derived particles contain components of the small subunit of the host cell ribosome, whereas the less dense vertebrate-derived particles do not. Infection of mice with RRV showed that both particle subpopulations are produced in an infected vertebrate, but in a tissue specific manner with serum containing only the less dense version of the virus particles. Previous infectivity studies using SINV particles have shown that the denser particles (SINVHeavy) and mosquito derived particles SINVC6/36 are significantly more infectious in vertebrate cells than the less dense vertebrate derived particles (SINVLight). The current study shows that SINVLight particles, initiate the infection of the mosquito midgut more efficiently than SINVHeavy particles and that this enhanced infectivity is associated with an exacerbated immune response to SINVLight infection in midgut tissues. The enhanced infection of SINVLight is specific to the midgut as intrathoracically injected virus do not exhibit the same fitness advantage. Together, our data indicate a biologically significant role for the SINVLight subpopulation in the efficient transmission from infected vertebrates to the mosquito vector.http://www.mdpi.com/1999-4915/10/5/263alphavirusmosquitotransmission
spellingShingle David Mackenzie-Liu
Kevin J. Sokoloski
Sarah Purdy
Richard W. Hardy
Encapsidated Host Factors in Alphavirus Particles Influence Midgut Infection of Aedes aegypti
Viruses
alphavirus
mosquito
transmission
title Encapsidated Host Factors in Alphavirus Particles Influence Midgut Infection of Aedes aegypti
title_full Encapsidated Host Factors in Alphavirus Particles Influence Midgut Infection of Aedes aegypti
title_fullStr Encapsidated Host Factors in Alphavirus Particles Influence Midgut Infection of Aedes aegypti
title_full_unstemmed Encapsidated Host Factors in Alphavirus Particles Influence Midgut Infection of Aedes aegypti
title_short Encapsidated Host Factors in Alphavirus Particles Influence Midgut Infection of Aedes aegypti
title_sort encapsidated host factors in alphavirus particles influence midgut infection of aedes aegypti
topic alphavirus
mosquito
transmission
url http://www.mdpi.com/1999-4915/10/5/263
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