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A Heritable Antiviral RNAi Response Limits Orsay Virus Infection in Caenorhabditis elegans N2

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  • Mark G Sterken
  • L Basten Snoek
  • Kobus J Bosman
  • Jikke Daamen
  • Joost A G Riksen
  • Jaap Bakker
  • Gorben P Pijlman
  • Jan E Kammenga

Abstract

Orsay virus (OrV) is the first virus known to be able to complete a full infection cycle in the model nematode species Caenorhabditis elegans. OrV is transmitted horizontally and its infection is limited by antiviral RNA interference (RNAi). However, we have no insight into the kinetics of OrV replication in C. elegans. We developed an assay that infects worms in liquid, allowing precise monitoring of the infection. The assay revealed a dual role for the RNAi response in limiting Orsay virus infection in C. elegans. Firstly, it limits the progression of the initial infection at the step of recognition of dsRNA. Secondly, it provides an inherited protection against infection in the offspring. This establishes the heritable RNAi response as anti-viral mechanism during OrV infections in C. elegans. Our results further illustrate that the inheritance of the anti-viral response is important in controlling the infection in the canonical wild type Bristol N2. The OrV replication kinetics were established throughout the worm life-cycle, setting a standard for further quantitative assays with the OrV-C. elegans infection model.

Suggested Citation

  • Mark G Sterken & L Basten Snoek & Kobus J Bosman & Jikke Daamen & Joost A G Riksen & Jaap Bakker & Gorben P Pijlman & Jan E Kammenga, 2014. "A Heritable Antiviral RNAi Response Limits Orsay Virus Infection in Caenorhabditis elegans N2," PLOS ONE, Public Library of Science, vol. 9(2), pages 1-8, February.
    • Handle: RePEc:plo:pone00:0089760
    DOI: 10.1371/journal.pone.0089760
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    References listed on IDEAS

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    1. Cynthia J. Kenyon, 2010. "The genetics of ageing," Nature, Nature, vol. 464(7288), pages 504-512, March.
    2. Andrew Fire & SiQun Xu & Mary K. Montgomery & Steven A. Kostas & Samuel E. Driver & Craig C. Mello, 1998. "Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans," Nature, Nature, vol. 391(6669), pages 806-811, February.
    3. R. Lu & M. Maduro & F. Li & H. W. Li & G. Broitman-Maduro & W. X. Li & S. W. Ding, 2005. "Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans," Nature, Nature, vol. 436(7053), pages 1040-1043, August.
    4. Courtney Wilkins & Ryan Dishongh & Steve C. Moore & Michael A. Whitt & Marie Chow & Khaled Machaca, 2005. "RNA interference is an antiviral defence mechanism in Caenorhabditis elegans," Nature, Nature, vol. 436(7053), pages 1044-1047, August.
    5. Nadine L. Vastenhouw & Karin Brunschwig & Kristy L. Okihara & Fritz Müller & Marcel Tijsterman & Ronald H. A. Plasterk, 2006. "Long-term gene silencing by RNAi," Nature, Nature, vol. 442(7105), pages 882-882, August.
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