Differential intra-host infection kinetics in Aedes aegypti underlie superior transmissibility of African relative to Asian Zika virus
ABSTRACTDespite numerous studies highlighting the higher transmissibility of the African Zika virus (ZIKV) lineage compared to the Asian lineage in mosquito vectors, little is known about how the viruses interact with different tissues during the early steps of mosquito infection. To address this ga...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-12-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msphere.00545-23 |
| _version_ | 1797384677750734848 |
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| author | Rinyaporn Phengchat Phonchanan Pakparnich Chatpong Pethrak Jutharat Pengon Channarong Sartsanga Nunya Chotiwan Kwanchanok Uppakara Kittitat Suksirisawat Louis Lambrechts Natapong Jupatanakul |
| author_facet | Rinyaporn Phengchat Phonchanan Pakparnich Chatpong Pethrak Jutharat Pengon Channarong Sartsanga Nunya Chotiwan Kwanchanok Uppakara Kittitat Suksirisawat Louis Lambrechts Natapong Jupatanakul |
| author_sort | Rinyaporn Phengchat |
| collection | DOAJ |
| description | ABSTRACTDespite numerous studies highlighting the higher transmissibility of the African Zika virus (ZIKV) lineage compared to the Asian lineage in mosquito vectors, little is known about how the viruses interact with different tissues during the early steps of mosquito infection. To address this gap, we aimed to characterize intra-host infection barriers by combining tissue-level monitoring of infection using plaque assays and a novel quantitative analysis of single-cell-level infection kinetics by in situ immunofluorescent staining. Our results revealed that, in Aedes aegypti, an African ZIKV strain exhibited a higher replication rate across various tissues than an Asian ZIKV strain. This difference was potentially due to a higher virus production in individual cells, faster spread within tissues, or a combination of both factors. Furthermore, we observed that higher blood meal titers resulted in a faster viral spread to neighboring cells suggesting that intra-host infection dynamics depend on inoculum size. We also identified a significant bottleneck during midgut infection establishment for both ZIKV lineages, with only a small percentage of the virus population successfully initiating infection. Finally, the in situ immunofluorescent staining technique enabled the examination of virus infection characteristics in different cell types and revealed heterogeneity in viral replication. Together, these findings demonstrate that differences in intra-host infection kinetics underlie differential transmissibility between African and Asian ZIKV lineages. This information could serve as a starting point to further investigate the underlying mechanisms and ultimately inform the development of alternative control strategies.IMPORTANCEThe recent Zika virus (ZIKV) epidemic in the Americas highlights its potential public health threat. While the Asian ZIKV lineage has been identified as the main cause of the epidemic, the African lineage, which has been primarily confined to Africa, has shown evidence of higher transmissibility in Aedes mosquitoes. To gain a deeper understanding of this differential transmissibility, our study employed a combination of tissue-level infection kinetics and single-cell-level infection kinetics using in situ immunofluorescent staining. We discovered that the African ZIKV lineage propagates more rapidly and spreads more efficiently within mosquito cells and tissues than its Asian counterpart. This information lays the groundwork for future exploration of the viral and host determinants driving these variations in propagation efficiency. |
| first_indexed | 2024-03-08T21:40:08Z |
| format | Article |
| id | doaj.art-7290216134694ebc9f013f99866f0ead |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-03-08T21:40:08Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-7290216134694ebc9f013f99866f0ead2023-12-20T14:01:03ZengAmerican Society for MicrobiologymSphere2379-50422023-12-018610.1128/msphere.00545-23Differential intra-host infection kinetics in Aedes aegypti underlie superior transmissibility of African relative to Asian Zika virusRinyaporn Phengchat0Phonchanan Pakparnich1Chatpong Pethrak2Jutharat Pengon3Channarong Sartsanga4Nunya Chotiwan5Kwanchanok Uppakara6Kittitat Suksirisawat7Louis Lambrechts8Natapong Jupatanakul9National Center for Genetic Engineering and Biotechnology (BIOTEC), Khlong Luang, Pathum Thani, ThailandNational Center for Genetic Engineering and Biotechnology (BIOTEC), Khlong Luang, Pathum Thani, ThailandNational Center for Genetic Engineering and Biotechnology (BIOTEC), Khlong Luang, Pathum Thani, ThailandNational Center for Genetic Engineering and Biotechnology (BIOTEC), Khlong Luang, Pathum Thani, ThailandNational Center for Genetic Engineering and Biotechnology (BIOTEC), Khlong Luang, Pathum Thani, ThailandChakri Naruebodindra Medical Institute, Faculty of Medicine Ramathibodi Hospital, Mahidol University, Samut Prakan, ThailandChakri Naruebodindra Medical Institute, Faculty of Medicine Ramathibodi Hospital, Mahidol University, Samut Prakan, ThailandNational Center for Genetic Engineering and Biotechnology (BIOTEC), Khlong Luang, Pathum Thani, ThailandInstitut Pasteur, Université Paris Cité, CNRS UMR2000, Insect-Virus Interactions Unit, Paris, FranceNational Center for Genetic Engineering and Biotechnology (BIOTEC), Khlong Luang, Pathum Thani, ThailandABSTRACTDespite numerous studies highlighting the higher transmissibility of the African Zika virus (ZIKV) lineage compared to the Asian lineage in mosquito vectors, little is known about how the viruses interact with different tissues during the early steps of mosquito infection. To address this gap, we aimed to characterize intra-host infection barriers by combining tissue-level monitoring of infection using plaque assays and a novel quantitative analysis of single-cell-level infection kinetics by in situ immunofluorescent staining. Our results revealed that, in Aedes aegypti, an African ZIKV strain exhibited a higher replication rate across various tissues than an Asian ZIKV strain. This difference was potentially due to a higher virus production in individual cells, faster spread within tissues, or a combination of both factors. Furthermore, we observed that higher blood meal titers resulted in a faster viral spread to neighboring cells suggesting that intra-host infection dynamics depend on inoculum size. We also identified a significant bottleneck during midgut infection establishment for both ZIKV lineages, with only a small percentage of the virus population successfully initiating infection. Finally, the in situ immunofluorescent staining technique enabled the examination of virus infection characteristics in different cell types and revealed heterogeneity in viral replication. Together, these findings demonstrate that differences in intra-host infection kinetics underlie differential transmissibility between African and Asian ZIKV lineages. This information could serve as a starting point to further investigate the underlying mechanisms and ultimately inform the development of alternative control strategies.IMPORTANCEThe recent Zika virus (ZIKV) epidemic in the Americas highlights its potential public health threat. While the Asian ZIKV lineage has been identified as the main cause of the epidemic, the African lineage, which has been primarily confined to Africa, has shown evidence of higher transmissibility in Aedes mosquitoes. To gain a deeper understanding of this differential transmissibility, our study employed a combination of tissue-level infection kinetics and single-cell-level infection kinetics using in situ immunofluorescent staining. We discovered that the African ZIKV lineage propagates more rapidly and spreads more efficiently within mosquito cells and tissues than its Asian counterpart. This information lays the groundwork for future exploration of the viral and host determinants driving these variations in propagation efficiency.https://journals.asm.org/doi/10.1128/msphere.00545-23arbovirusZikamidgut infection barriertransmissioninfection kinetics |
| spellingShingle | Rinyaporn Phengchat Phonchanan Pakparnich Chatpong Pethrak Jutharat Pengon Channarong Sartsanga Nunya Chotiwan Kwanchanok Uppakara Kittitat Suksirisawat Louis Lambrechts Natapong Jupatanakul Differential intra-host infection kinetics in Aedes aegypti underlie superior transmissibility of African relative to Asian Zika virus mSphere arbovirus Zika midgut infection barrier transmission infection kinetics |
| title | Differential intra-host infection kinetics in Aedes aegypti underlie superior transmissibility of African relative to Asian Zika virus |
| title_full | Differential intra-host infection kinetics in Aedes aegypti underlie superior transmissibility of African relative to Asian Zika virus |
| title_fullStr | Differential intra-host infection kinetics in Aedes aegypti underlie superior transmissibility of African relative to Asian Zika virus |
| title_full_unstemmed | Differential intra-host infection kinetics in Aedes aegypti underlie superior transmissibility of African relative to Asian Zika virus |
| title_short | Differential intra-host infection kinetics in Aedes aegypti underlie superior transmissibility of African relative to Asian Zika virus |
| title_sort | differential intra host infection kinetics in aedes aegypti underlie superior transmissibility of african relative to asian zika virus |
| topic | arbovirus Zika midgut infection barrier transmission infection kinetics |
| url | https://journals.asm.org/doi/10.1128/msphere.00545-23 |
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