PIWI Proteins Play an Antiviral Role in Lepidopteran Cell Lines

Dulce Santos; Thomas-Wolf Verdonckt; Lina Mingels; Stijn Van den Brande; Bart Geens; Filip Van Nieuwerburgh; Anna Kolliopoulou; Luc Swevers; Niels Wynant; Jozef Vanden Broeck

doi:10.3390/v14071442

PIWI Proteins Play an Antiviral Role in Lepidopteran Cell Lines

Viruses. 2022 Jun 30;14(7):1442. doi: 10.3390/v14071442.

Affiliations

¹ Research Group of Molecular Developmental Physiology and Signal Transduction, Division of Animal Physiology and Neurobiology, Department of Biology, KU Leuven, Naamsestraat 59, 3000 Leuven, Belgium.
² Laboratory of Pharmaceutical Biotechnology, Gent University, Ottergemsesteenweg 460, 9000 Gent, Belgium.
³ Insect Molecular Genetics and Biotechnology, Institute of Biosciences and Applications, National Center for Scientific Research "Demokritos", Aghia Paraskevi Attikis, 153 10 Athens, Greece.

Abstract

Insect antiviral immunity primarily relies on RNAi mechanisms. While a key role of small interfering (si)RNAs and AGO proteins has been well established in this regard, the situation for PIWI proteins and PIWI-interacting (pi)RNAs is not as clear. In the present study, we investigate whether PIWI proteins and viral piRNAs are involved in the immunity against single-stranded RNA viruses in lepidopteran cells, where two PIWIs are identified (Siwi and Ago3). Via loss- and gain-of-function studies in Bombyx mori BmN4 cells and in Trichoplusia ni High Five cells, we demonstrated an antiviral role of Siwi and Ago3. However, small RNA analysis suggests that viral piRNAs can be absent in these lepidopteran cells. Together with the current literature, our results support a functional diversification of PIWI proteins in insects.

Keywords: Ago3; Argonaute; Bombyx mori Macula-like Latent Virus (MLV); Cricket Paralysis Virus (CrPV); Flock House Virus (FHV); RNAi; Siwi; Spodoptera frugiperda Rhabdovirus (RV); immunity; insect; piRNA; sRNA; siRNA; virus.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Antiviral Agents* / metabolism
Argonaute Proteins / genetics
Bombyx*
Cell Line
RNA Interference
RNA, Small Interfering / genetics
RNA, Small Interfering / metabolism

Substances

Antiviral Agents
Argonaute Proteins
RNA, Small Interfering

Grants and funding

This study was supported by the Research Foundation of Flanders (FWO), grant number G093119N; the Special Research Fund of KU Leuven, grant number C14/19/069; the Action for the Strategic Development on the Research and Technological Sectors, funded by the Operational Programme “Competitiveness, Entrepreneurship and Innovation” and co-financed by Greece and the European Regional Development Fund; and the project ‘An Open-Access Research Infrastructure of Chemical Biology and Target-Based Screening Technologies for Human and Animal Health, Agriculture and the Environment (OPENSCREEN-GR)’ (MIS 5002691), which is implemented under the Action ‘Reinforcement of the Research and Innovation Infrastructure’, funded by the Operational Programme ‘Competitiveness, Entrepreneurship and Innovation’ (NSRF 2014–2020) and co-financed by Greece and the European Union (European Regional Development Fund). D.S. was a recipient of a Ph.D. fellowship from the Agentschap voor Innovatie door Wetenschap en Technologie (IWT, Agency for Innovation by Science and Technology), and is currently supported by the FWO as a postdoctoral researcher. T.-W.V., L.M., S.V.d.B. and B.G. were/are recipients of Ph.D. fellowships from the FWO.