Mitochondrion-Dependent Apoptosis Is Essential for <named-content content-type="genus-species">Rickettsia parkeri</named-content> Infection and Replication in Vector Cells

ABSTRACT Apoptosis is an innate immune response induced by infection in eukaryotes that contributes significantly to protection from pathogens. However, little is known about the role of apoptosis in the interactions of arthropod vectors with the rickettsiae that they transmit. Rickettsia spp. are v...

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Autores principales:	Xin-Ru Wang, Nicole Y. Burkhardt, Timothy J. Kurtti, Jonathan D. Oliver, Lisa D. Price, Benjamin Cull, Cody J. Thorpe, Michalina Silva Thiel, Ulrike G. Munderloh
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	tick apoptosis mitochondria Rickettsia pathogenesis Rickettsia tick-borne pathogens Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f1c0b86748664ffb91c1b01d70d14734
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spelling	oai:doaj.org-article:f1c0b86748664ffb91c1b01d70d147342021-12-02T18:21:19ZMitochondrion-Dependent Apoptosis Is Essential for <named-content content-type="genus-species">Rickettsia parkeri</named-content> Infection and Replication in Vector Cells10.1128/mSystems.01209-202379-5077https://doaj.org/article/f1c0b86748664ffb91c1b01d70d147342021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01209-20https://doaj.org/toc/2379-5077ABSTRACT Apoptosis is an innate immune response induced by infection in eukaryotes that contributes significantly to protection from pathogens. However, little is known about the role of apoptosis in the interactions of arthropod vectors with the rickettsiae that they transmit. Rickettsia spp. are vector-borne obligately intracellular bacteria and display different degrees of virulence in their eukaryotic hosts. In this study, we found that infection with Rickettsia parkeri (Rp) activated the apoptosis pathway in an Amblyomma americanum tick cell line (AAE2), as evidenced by the loss of phospholipid membrane asymmetry and DNA fragmentations. Additionally, infection with Rp also led to apoptosis activation in cell lines of different tick species. Interestingly, suppressing apoptosis decreased Rp infection and replication, while the activation of apoptosis increased Rp accumulation at the early stage of infection. Moreover, mitochondrion-dependent apoptosis was essential for Rp infection and replication in vector cells, and apoptosis induction required intracellular rickettsia replication. We further showed that Rp utilizes two different survival strategies to modulate apoptosis in the arthropod vectors and mammalian host cells. There was no direct correlation between apoptosis activation in vector cells and rickettsial pathogenicity. These novel findings indicate a possible mechanism whereby apoptosis facilitates infection and replication of a Rickettsia sp. in an arthropod vector. These results contribute to our understanding of how the vector's responses to pathogen infection affect pathogen replication and therefore transmission. IMPORTANCE Rickettsioses, infections caused by the genus Rickettsia, are among the oldest known infectious diseases. Ticks are essential arthropod vectors for rickettsiae, and knowledge about the interactions between ticks, their hosts, and pathogens is fundamental for identifying drivers of tick-borne rickettsioses. Despite the rapid development in apoptosis research with rickettsiae, little is known regarding the role of apoptosis in the interactions between Rickettsia spp., vertebrate hosts, and arthropod vectors. Here, we demonstrated that mitochondrion-dependent apoptosis is essential for rickettsial infection and replication in vector cells and that apoptosis induction requires intracellular rickettsial replication. However, rickettsial pathogenicity is not linked with apoptosis activation in tick cells. Our findings improve understanding of the apoptosis mechanism in arthropods exploited by rickettsiae and also the potential to discover specific targets for new vaccines and drugs to prevent or treat rickettsial infections.Xin-Ru WangNicole Y. BurkhardtTimothy J. KurttiJonathan D. OliverLisa D. PriceBenjamin CullCody J. ThorpeMichalina Silva ThielUlrike G. MunderlohAmerican Society for MicrobiologyarticletickapoptosismitochondriaRickettsia pathogenesisRickettsiatick-borne pathogensMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	tick apoptosis mitochondria Rickettsia pathogenesis Rickettsia tick-borne pathogens Microbiology QR1-502
spellingShingle	tick apoptosis mitochondria Rickettsia pathogenesis Rickettsia tick-borne pathogens Microbiology QR1-502 Xin-Ru Wang Nicole Y. Burkhardt Timothy J. Kurtti Jonathan D. Oliver Lisa D. Price Benjamin Cull Cody J. Thorpe Michalina Silva Thiel Ulrike G. Munderloh Mitochondrion-Dependent Apoptosis Is Essential for <named-content content-type="genus-species">Rickettsia parkeri</named-content> Infection and Replication in Vector Cells
description	ABSTRACT Apoptosis is an innate immune response induced by infection in eukaryotes that contributes significantly to protection from pathogens. However, little is known about the role of apoptosis in the interactions of arthropod vectors with the rickettsiae that they transmit. Rickettsia spp. are vector-borne obligately intracellular bacteria and display different degrees of virulence in their eukaryotic hosts. In this study, we found that infection with Rickettsia parkeri (Rp) activated the apoptosis pathway in an Amblyomma americanum tick cell line (AAE2), as evidenced by the loss of phospholipid membrane asymmetry and DNA fragmentations. Additionally, infection with Rp also led to apoptosis activation in cell lines of different tick species. Interestingly, suppressing apoptosis decreased Rp infection and replication, while the activation of apoptosis increased Rp accumulation at the early stage of infection. Moreover, mitochondrion-dependent apoptosis was essential for Rp infection and replication in vector cells, and apoptosis induction required intracellular rickettsia replication. We further showed that Rp utilizes two different survival strategies to modulate apoptosis in the arthropod vectors and mammalian host cells. There was no direct correlation between apoptosis activation in vector cells and rickettsial pathogenicity. These novel findings indicate a possible mechanism whereby apoptosis facilitates infection and replication of a Rickettsia sp. in an arthropod vector. These results contribute to our understanding of how the vector's responses to pathogen infection affect pathogen replication and therefore transmission. IMPORTANCE Rickettsioses, infections caused by the genus Rickettsia, are among the oldest known infectious diseases. Ticks are essential arthropod vectors for rickettsiae, and knowledge about the interactions between ticks, their hosts, and pathogens is fundamental for identifying drivers of tick-borne rickettsioses. Despite the rapid development in apoptosis research with rickettsiae, little is known regarding the role of apoptosis in the interactions between Rickettsia spp., vertebrate hosts, and arthropod vectors. Here, we demonstrated that mitochondrion-dependent apoptosis is essential for rickettsial infection and replication in vector cells and that apoptosis induction requires intracellular rickettsial replication. However, rickettsial pathogenicity is not linked with apoptosis activation in tick cells. Our findings improve understanding of the apoptosis mechanism in arthropods exploited by rickettsiae and also the potential to discover specific targets for new vaccines and drugs to prevent or treat rickettsial infections.
format	article
author	Xin-Ru Wang Nicole Y. Burkhardt Timothy J. Kurtti Jonathan D. Oliver Lisa D. Price Benjamin Cull Cody J. Thorpe Michalina Silva Thiel Ulrike G. Munderloh
author_facet	Xin-Ru Wang Nicole Y. Burkhardt Timothy J. Kurtti Jonathan D. Oliver Lisa D. Price Benjamin Cull Cody J. Thorpe Michalina Silva Thiel Ulrike G. Munderloh
author_sort	Xin-Ru Wang
title	Mitochondrion-Dependent Apoptosis Is Essential for <named-content content-type="genus-species">Rickettsia parkeri</named-content> Infection and Replication in Vector Cells
title_short	Mitochondrion-Dependent Apoptosis Is Essential for <named-content content-type="genus-species">Rickettsia parkeri</named-content> Infection and Replication in Vector Cells
title_full	Mitochondrion-Dependent Apoptosis Is Essential for <named-content content-type="genus-species">Rickettsia parkeri</named-content> Infection and Replication in Vector Cells
title_fullStr	Mitochondrion-Dependent Apoptosis Is Essential for <named-content content-type="genus-species">Rickettsia parkeri</named-content> Infection and Replication in Vector Cells
title_full_unstemmed	Mitochondrion-Dependent Apoptosis Is Essential for <named-content content-type="genus-species">Rickettsia parkeri</named-content> Infection and Replication in Vector Cells
title_sort	mitochondrion-dependent apoptosis is essential for <named-content content-type="genus-species">rickettsia parkeri</named-content> infection and replication in vector cells
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/f1c0b86748664ffb91c1b01d70d14734
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Mitochondrion-Dependent Apoptosis Is Essential for <named-content content-type="genus-species">Rickettsia parkeri</named-content> Infection and Replication in Vector Cells

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