Influenza C and D Viruses Package Eight Organized Ribonucleoprotein Complexes

Author:

Nakatsu Sumiho1,Murakami Shin2,Shindo Keiko3,Horimoto Taisuke2,Sagara Hiroshi4,Noda Takeshi53,Kawaoka Yoshihiro167

Affiliation:

1. Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Tokyo, Japan

2. Department of Veterinary Microbiology, Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, Japan

3. Laboratory of Ultrastructural Virology, Institute for Frontier Life and Medical Sciences, Kyoto University, Kyoto, Japan

4. Medical Proteomics Laboratory, Institute of Medical Science, University of Tokyo, Tokyo, Japan

5. PRESTO, Japan Science and Technology Agency, Saitama, Japan

6. Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin—Madison, Wisconsin, USA

7. International Research Center for Infectious Diseases, Institute of Medical Science, University of Tokyo, Tokyo, Japan

Abstract

ABSTRACT Influenza A and B viruses have eight-segmented, single-stranded, negative-sense RNA genomes, whereas influenza C and D viruses have seven-segmented genomes. Each genomic RNA segment exists in the form of a ribonucleoprotein complex (RNP) in association with nucleoproteins and an RNA-dependent RNA polymerase in virions. Influenza D virus was recently isolated from swine and cattle, but its morphology is not fully studied. Here, we examined the morphological characteristics of D/bovine/Yamagata/10710/2016 (D/Yamagata) and C/Ann Arbor/50 (C/AA), focusing on RNPs packaged within the virions. By scanning transmission electron microscopic tomography, we found that more than 70% of D/Yamagata and C/AA virions packaged eight RNPs arranged in the “1+7” pattern as observed in influenza A and B viruses, even though type C and D virus genomes are segmented into only seven segments. These results imply that influenza viruses generally package eight RNPs arranged in the “1+7” pattern regardless of the number of RNA segments in their genome. IMPORTANCE The genomes of influenza A and B viruses are segmented into eight segments of negative-sense RNA, and those of influenza C and D viruses are segmented into seven segments. For progeny virions to be infectious, each virion needs to package all of their genomic segments. Several studies support the conclusion that influenza A and B viruses selectively package eight distinct genomic RNA segments; however, the packaging of influenza C and D viruses, which possess seven segmented genomes, is less understood. By using electron microscopy, we showed that influenza C and D viruses package eight RNA segments just as influenza A and B viruses do. These results suggest that influenza viruses prefer to package eight RNA segments within virions independent of the number of genome segments.

Funder

HHS | NIH | National Institute of Allergy and Infectious Diseases

Daiichi Sankyo Foundation of Life Science

Japan Agency for Medical Research and Development

Takeda Medical Research Foundation

Ministry of Education, Culture, Sports, Science and Technology

MEXT | Japan Society for the Promotion of Science

MEXT | Japan Science and Technology Agency

Publisher

American Society for Microbiology

Subject

Virology,Insect Science,Immunology,Microbiology

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