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Zika virus infection in chemosensory cells

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Abstract

Zika virus (ZIKV) is an emerging virus belonging to the genus Flavivirus. ZIKV infection is a significant health concern, with increasing numbers of reports of microcephaly cases in fetuses and Guillain–Barré syndrome (GBS) in adults. Interestingly, chemosensory disturbances are also reported as one of the manifestations of GBS. ZIKV infects several human tissues and cell types in vitro and in vivo. However, there is no study demonstrating ZIKV infection and replication in chemosensory cells, including olfactory and taste cells. Taste papilla and olfactory cells are chemosensory receptor cells with unique histological, molecular, and physiological characteristics. Here we examined ZIKV infection (PRVABC59) in cultured human olfactory epithelial cells (hOECs) and fungiform taste papilla (HBO) cells in vitro, as well as in vivo mouse taste and olfactory epithelial and olfactory bulb tissues. Interestingly, while HBO cells showed resistance to ZIKV replication, hOECs were highly susceptible for ZIKV infection and replication. Further, we demonstrated the presence of ZIKV particles and expression of viral proteins in olfactory epithelium, as well as in olfactory bulb, but not in taste papillae, of immunocompromised mice (ifnar/−) infected with the PRVABC59 strain of ZIKV. These observations suggest that chemosensory cells in the olfactory neuroepithelium and olfactory bulb may be important tissues for ZIKV replication and dissemination.

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Data availability

The data sets used and/or analyzed during the current study are available from the authors on reasonable request.

Abbreviations

CNS:

central nervous system

DAPI:

4′,6-diamidino-2-phenylindole

DMEM:

Dulbecco’s modified Eagle’s medium

FBS:

fetal bovine serum

GBS:

Guillain–Barré syndrome

H&E:

hematoxylin and eosin

HBO cells:

human fungiform taste papilla cells

hOECs:

human olfactory epithelial cells

MOI:

multiplicity of infection

OMP:

olfactory marker protein

PBS:

phosphate-buffered saline

PFU:

plaque-forming unit

PLC:

phospholipase C

qRT-PCR:

quantitative reverse-transcription polymerase chain reaction

ZIKV:

Zika virus

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Acknowledgments

The authors acknowledge Patricia Watson for editorial assistance. Human olfactory cells were kindly provided by Chang-Gyu Hahn of University of Pennsylvania.

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Authors and Affiliations

Authors

Contributions

MHO and IKS conceived and designed the research, analyzed the experiments, coordinated collaborations, and wrote the manuscript. JG and AIS contributed reagents and participated in the design of the experiments. MD, SC, and AG-B performed the experiments and helped in the acquisition of the data.

Corresponding authors

Correspondence to Mehmet Hakan Ozdener or Ilker Kudret Sariyer.

Ethics declarations

This study was carried out in accordance with recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All mouse procedures were approved by Institutional Animal Care and Use Committee (IACUC) of the Lewis Katz School of Medicine at Temple University and performed in accordance with the IACUC guidelines (protocol no. IACUC-2017-4624).

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Not applicable.

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Not applicable.

Competing interests

A patent portfolio covering methods for culturing mammalian taste cells has been filed by Monell Chemical Senses Center, and M.H.O. is named as one of the inventors. M.H.O. receives research support and royalties. The other authors declare no competing interests.

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Ozdener, M.H., Donadoni, M., Cicalese, S. et al. Zika virus infection in chemosensory cells. J. Neurovirol. 26, 371–381 (2020). https://doi.org/10.1007/s13365-020-00835-2

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  • DOI: https://doi.org/10.1007/s13365-020-00835-2

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