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J. Biol. Chem., Vol. 281, Issue 35, 25315-25325, September 1, 2006

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Caliciviruses Differ in Their Functional Requirements for eIF4F Components^*

Yasmin Chaudhry, Arabinda Nayak¹, Marie-Eve Bordeleau^¶, Junichi Tanaka^||, Jerry Pelletier^¶2, Graham J. Belsham³⁴, Lisa O. Roberts^**3, and Ian G. Goodfellow⁵

From the Department of Virology, Faculty of Medicine, Imperial College London, St. Mary's Campus, Norfolk Place, London W2 1PG, United Kingdom, the Biotechnology and Biological Sciences Research Council Institute for Animal Health, Pirbright, Woking, Surrey GU24 0NF, United Kingdom, the ^¶Department of Biochemistry, McIntyre Medical Sciences Building, McGill University, Montreal, Quebec H3G 1Y6, Canada, the ^||Department of Chemistry, Biology, and Marine Sciences, University of the Ryukyus, Nishihara, Okinawa 903-0213, Japan, and the ^**School of Biomedical and Molecular Sciences, University of Surrey, Guildford, Surrey GU2 7XH, United Kingdom

Two classes of viruses, namely members of the Potyviridae and Caliciviridae, use a novel mechanism for the initiation of protein synthesis that involves the interaction of translation initiation factors with a viral protein covalently linked to the viral RNA, known as VPg. The calicivirus VPg proteins can interact directly with the initiation factors eIF4E and eIF3. Translation initiation on feline calicivirus (FCV) RNA requires eIF4E because it is inhibited by recombinant 4E-BP1. However, to date, there have been no functional studies carried out with respect to norovirus translation initiation, because of a lack of a suitable source of VPg-linked viral RNA. We have now used the recently identified murine norovirus (MNV) as a model system for norovirus translation and have extended our previous studies with FCV RNA to examine the role of the other eIF4F components in translation initiation. We now demonstrate that, as with FCV, MNV VPg interacts directly with eIF4E, although, unlike FCV RNA, translation of MNV RNA is not sensitive to 4E-BP1, eIF4E depletion, or foot-and-mouth disease virus Lb protease-mediated cleavage of eIF4G. We also demonstrate that both FCV and MNV RNA translation require the RNA helicase component of the eIF4F complex, namely eIF4A, because translation was sensitive (albeit to different degrees) to a dominant negative form and to a small molecule inhibitor of eIF4A (hippuristanol). These results suggest that calicivirus RNAs differ with respect to their requirements for the components of the eIF4F translation initiation complex.

Received for publication, March 9, 2006 , and in revised form, June 7, 2006.

^* The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ Present address: Dept. of Microbiology and Immunology, University of California, San Francisco, CA 94143-2280.

² Supported by National Cancer Institute of Canada Grant 014313.

³ Supported by the Biotechnology and Biological Sciences Research Council (BBSRC).

⁴ Present address: Danish Institute for Food and Veterinary Research, Dept of Virology, Lindholm, DK-4771 Kalvehave, Denmark.

⁵ Supported by the Wellcome Trust and the Biotechnology and Biological Sciences Research Council (BBSRC). To whom correspondence should be addressed. Tel.: 44-20-7594-2002; Fax: 44-20-7594-3973; E-mail: I.Goodfellow{at}imperial.ac.uk.

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