Detailed Analyses of Zika Virus Tropism in <named-content content-type="genus-species">Culex quinquefasciatus</named-content> Reveal Systemic Refractoriness
ABSTRACT The role of Culex quinquefasciatus in Zika virus transmission has been debated since the epidemic of Zika occurred in the Americas in 2015 to 2016. The majority of studies have found no evidence that C. quinquefasciatus or other Culex species are competent vectors of Zika virus, and the few...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2020-08-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mBio.01765-20 |
| _version_ | 1819203109638897664 |
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| author | Hannah J. MacLeod George Dimopoulos |
| author_facet | Hannah J. MacLeod George Dimopoulos |
| author_sort | Hannah J. MacLeod |
| collection | DOAJ |
| description | ABSTRACT The role of Culex quinquefasciatus in Zika virus transmission has been debated since the epidemic of Zika occurred in the Americas in 2015 to 2016. The majority of studies have found no evidence that C. quinquefasciatus or other Culex species are competent vectors of Zika virus, and the few studies that have proposed Zika vector status for C. quinquefasciatus have relied predominantly on quantitative real-time PCR (qRT-PCR) for viral detection. We assessed the infectious range of pre- and post-epidemic Zika virus isolates in order to classify mosquito samples based on titer infectiousness and demonstrated that two strains of C. quinquefasciatus, including one previously found to be competent, are highly resistant to infection with these Zika isolates compared to Aedes aegypti and are not competent for virus transmission. Further dissection of the dynamics of Zika exposure in both A. aegypti and C. quinquefasciatus revealed that while virus transmission by C. quinquefasciatus is blocked at the levels of the midgut and salivary glands, viral RNA persists in these tissues for prolonged periods post-exposure. We assessed Zika entry dynamics in both Aedes and Culex cells, and our results suggest that Zika virus infection in Culex cells may be blocked downstream of cell entry. These findings strongly suggest that C. quinquefasciatus is not a vector of Zika virus and additionally inform the use of qRT-PCR in vector competence assays as well as our understanding of barriers to arbovirus infection in non-susceptible mosquito species. IMPORTANCE Understanding which mosquito species transmit an emerging arbovirus is critical to effective vector control. During the Zika virus epidemic in 2015 to 2016, Aedes mosquitoes were confirmed as vectors. However, studies addressing the vector status of Culex quinquefasciatus mosquitoes presented conflicting evidence and remain an outstanding source of confusion in the field. Here, we established a robust cell-based assay to identify infectious titers of Zika virus and assessed the virus titers in C. quinquefasciatus by quantitative real-time PCR (qRT-PCR). We found that while low levels of virus were detected in C. quinquefasciatus, these titers did not correspond to infectious virus, and these mosquitoes did not transmit virus in the saliva. We also present evidence that the virus may enter Culex cells before infection is disrupted. Our findings are important for future studies incriminating vector species using qRT-PCR for virus detection and offer new information on how virus transmission is blocked by mosquitoes. |
| first_indexed | 2024-12-23T04:14:41Z |
| format | Article |
| id | doaj.art-9e780adb37ab467eaa4c54e30676c509 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-23T04:14:41Z |
| publishDate | 2020-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-9e780adb37ab467eaa4c54e30676c5092022-12-21T18:00:24ZengAmerican Society for MicrobiologymBio2150-75112020-08-0111410.1128/mBio.01765-20Detailed Analyses of Zika Virus Tropism in <named-content content-type="genus-species">Culex quinquefasciatus</named-content> Reveal Systemic RefractorinessHannah J. MacLeod0George Dimopoulos1W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland, USAW. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland, USAABSTRACT The role of Culex quinquefasciatus in Zika virus transmission has been debated since the epidemic of Zika occurred in the Americas in 2015 to 2016. The majority of studies have found no evidence that C. quinquefasciatus or other Culex species are competent vectors of Zika virus, and the few studies that have proposed Zika vector status for C. quinquefasciatus have relied predominantly on quantitative real-time PCR (qRT-PCR) for viral detection. We assessed the infectious range of pre- and post-epidemic Zika virus isolates in order to classify mosquito samples based on titer infectiousness and demonstrated that two strains of C. quinquefasciatus, including one previously found to be competent, are highly resistant to infection with these Zika isolates compared to Aedes aegypti and are not competent for virus transmission. Further dissection of the dynamics of Zika exposure in both A. aegypti and C. quinquefasciatus revealed that while virus transmission by C. quinquefasciatus is blocked at the levels of the midgut and salivary glands, viral RNA persists in these tissues for prolonged periods post-exposure. We assessed Zika entry dynamics in both Aedes and Culex cells, and our results suggest that Zika virus infection in Culex cells may be blocked downstream of cell entry. These findings strongly suggest that C. quinquefasciatus is not a vector of Zika virus and additionally inform the use of qRT-PCR in vector competence assays as well as our understanding of barriers to arbovirus infection in non-susceptible mosquito species. IMPORTANCE Understanding which mosquito species transmit an emerging arbovirus is critical to effective vector control. During the Zika virus epidemic in 2015 to 2016, Aedes mosquitoes were confirmed as vectors. However, studies addressing the vector status of Culex quinquefasciatus mosquitoes presented conflicting evidence and remain an outstanding source of confusion in the field. Here, we established a robust cell-based assay to identify infectious titers of Zika virus and assessed the virus titers in C. quinquefasciatus by quantitative real-time PCR (qRT-PCR). We found that while low levels of virus were detected in C. quinquefasciatus, these titers did not correspond to infectious virus, and these mosquitoes did not transmit virus in the saliva. We also present evidence that the virus may enter Culex cells before infection is disrupted. Our findings are important for future studies incriminating vector species using qRT-PCR for virus detection and offer new information on how virus transmission is blocked by mosquitoes.https://journals.asm.org/doi/10.1128/mBio.01765-20Aedes aegyptiCulex quinquefasciatusZika virusvector competence |
| spellingShingle | Hannah J. MacLeod George Dimopoulos Detailed Analyses of Zika Virus Tropism in <named-content content-type="genus-species">Culex quinquefasciatus</named-content> Reveal Systemic Refractoriness mBio Aedes aegypti Culex quinquefasciatus Zika virus vector competence |
| title | Detailed Analyses of Zika Virus Tropism in <named-content content-type="genus-species">Culex quinquefasciatus</named-content> Reveal Systemic Refractoriness |
| title_full | Detailed Analyses of Zika Virus Tropism in <named-content content-type="genus-species">Culex quinquefasciatus</named-content> Reveal Systemic Refractoriness |
| title_fullStr | Detailed Analyses of Zika Virus Tropism in <named-content content-type="genus-species">Culex quinquefasciatus</named-content> Reveal Systemic Refractoriness |
| title_full_unstemmed | Detailed Analyses of Zika Virus Tropism in <named-content content-type="genus-species">Culex quinquefasciatus</named-content> Reveal Systemic Refractoriness |
| title_short | Detailed Analyses of Zika Virus Tropism in <named-content content-type="genus-species">Culex quinquefasciatus</named-content> Reveal Systemic Refractoriness |
| title_sort | detailed analyses of zika virus tropism in named content content type genus species culex quinquefasciatus named content reveal systemic refractoriness |
| topic | Aedes aegypti Culex quinquefasciatus Zika virus vector competence |
| url | https://journals.asm.org/doi/10.1128/mBio.01765-20 |
| work_keys_str_mv | AT hannahjmacleod detailedanalysesofzikavirustropisminnamedcontentcontenttypegenusspeciesculexquinquefasciatusnamedcontentrevealsystemicrefractoriness AT georgedimopoulos detailedanalysesofzikavirustropisminnamedcontentcontenttypegenusspeciesculexquinquefasciatusnamedcontentrevealsystemicrefractoriness |