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Robust dengue virus infection in bat cells and limited innate immune responses coupled with positive serology from bats in IndoMalaya and Australasia

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Abstract

Natural reservoir hosts can sustain infection of pathogens without succumbing to overt disease. Multiple bat species host a plethora of viruses, pathogenic to other mammals, without clinical symptoms. Here, we detail infection of bat primary cells, immune cells, and cell lines with Dengue virus. While antibodies and viral RNA were previously detected in wild bats, their ability to sustain infection is not conclusive. Old-world fruitbat cells can be infected, producing high titres of virus with limited cellular responses. In addition, there is minimal interferon (IFN) response in cells infected with MOIs leading to dengue production. The ability to support in vitro replication/production raises the possibility of bats as a transient host in the life cycle of dengue or similar flaviviruses. New antibody serology evidence from Asia/Pacific highlights the previous exposure and raises awareness that bats may be involved in flavivirus dynamics and infection of other hosts.

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Abbreviations

IFN:

Interferon

DENV:

Dengue virus

ZIKV:

Zika virus

JEV:

Japanese encephalitis virus

YFV:

Yellow fever virus

SLEV:

St Louis encephalitis virus

WNV:

West Nile virus

IRG:

Interferon regulated gene

PRR:

Pattern recognition receptor

BMDM:

Bone-marrow-derived macrophage

BMDC:

Bone-marrow-derived dendritic cells

LIPS:

Luciferase immune-precipitation system

SE:

South east

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Acknowledgements

This work was funded by the Singapore National Research Foundation Competitive Research Programme Grant (NRF2012NRF-CRP001-056 to LFW), National Medical Research Council of Singapore New Investigator’s Grant (NMRC/BNIG/2040/2015 to ATI, NMRC/BNIG/2005/2013 to IHM) and a National Medical Research Council Research Grant (ZRRF16006 to LFW and ATI). Many thanks to the following in helping with bat sample processing: NEA/NParks, Crameri Research Consulting, Prof. Joanne Meers of UQ, the Queensland Animal Science Precinct (QASP) team led by Hume Field, and Duke-NUS team members from LEZV/LOVE labs for collection of bat samples. We acknowledge the help from the SingHealth Advanced Bioimaging facility.

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Authors and Affiliations

  1. Duke-NUS Medical School, Singapore, Singapore

    Aaron T. Irving, Pritisha Rozario, Pui-San Kong, Katarina Luko, Wan Ni Chia, Shailendra Mani, Gavin J. D. Smith, Ian H. Mendenhall & Lin-Fa Wang

  2. QIMR Berghofer Medical Research Institute, Herston, QLD, Australia

    Jeffrey J. Gorman & Marcus L. Hastie

  3. Conservation Division, National Parks Board, Singapore, Singapore

    Benjamin PY-H. Lee

  4. Johns Hopkins University, Baltimore, MD, 21205, USA

    H. Benjamin Larman

  5. Harvard University Medical School, Boston, MA, 02115, USA

    Stephen J. Elledge

  6. Howard Hughes Medical Institute, Brigham and Women’s Hospital, Boston, MA, 02115, USA

    Stephen J. Elledge

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  1. Aaron T. Irving
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Contributions

ATI designed the study, performed experiments, analysed the data, and wrote the manuscript under supervision from LFW and with input from all authors. PR, KPS, KL, WNC, and SM performed experiments and analysed data. JLG and MLH performed proteomics studies. BPYHL, JHJN, IHM, and GJDS contributed with wild animal samples in Singapore, processing of bats, and generation of cell lines. BL and SJE designed the ViRScan/PhIP-Seq pipelines and contributed to the manuscript.

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Correspondence to Aaron T. Irving or Lin-Fa Wang.

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Irving, A.T., Rozario, P., Kong, PS. et al. Robust dengue virus infection in bat cells and limited innate immune responses coupled with positive serology from bats in IndoMalaya and Australasia. Cell. Mol. Life Sci. 77, 1607–1622 (2020). https://doi.org/10.1007/s00018-019-03242-x

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  • DOI: https://doi.org/10.1007/s00018-019-03242-x

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