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Journal of Virology, March 2005, p. 2847-2858, Vol. 79, No. 5
0022-538X/05/$08.00+0     doi:10.1128/JVI.79.5.2847-2858.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Involvement of the Toll-Like Receptor 9 Signaling Pathway in the Induction of Innate Immunity by Baculovirus{dagger}

Takayuki Abe,1 Hiroaki Hemmi,2 Hironobu Miyamoto,1 Kohji Moriishi,1 Shinichi Tamura,3 Hiroshi Takaku,4 Shizuo Akira,2 and Yoshiharu Matsuura1*

Research Center for Emerging Infectious Diseases,1 Department of Host Defense,2 Laboratory of Prevention of Viral Diseases, Research Institute for Microbial Diseases, Osaka University, Osaka,3 Department of Industrial Chemistry and High Technology Research Center, Chiba Institute of Technology, Chiba, Japan4

Received 11 July 2004/ Accepted 6 October 2004

We have previously shown that mice inoculated intranasally with a wild-type baculovirus (Autographa californica nuclear polyhedrosis virus [AcNPV]) are protected from a lethal challenge by influenza virus. However, the precise mechanism of induction of this protective immune response by the AcNPV treatment remained unclear. Here we show that AcNPV activates immune cells via the Toll-like receptor 9 (TLR9)/MyD88-dependent signaling pathway. The production of inflammatory cytokines was severely reduced in peritoneal macrophages (PECs) and splenic CD11c+ dendritic cells (DCs) derived from mice deficient in MyD88 or TLR9 after cultivation with AcNPV. In contrast, a significant amount of alpha interferon (IFN-{alpha}) was still detectable in the PECs and DCs of these mice after stimulation with AcNPV, suggesting that a TLR9/MyD88-independent signaling pathway might also participate in the production of IFN-{alpha} by AcNPV. Since previous work showed that TLR9 ligands include bacterial DNA and certain oligonucleotides containing unmethylated CpG dinucleotides, we also examined the effect of baculoviral DNA on the induction of innate immunity. Transfection of the murine macrophage cell line RAW264.7 with baculoviral DNA resulted in the production of the inflammatory cytokine, while the removal of envelope glycoproteins from viral particles, UV irradiation of the virus, and pretreatment with purified baculovirus envelope proteins or endosomal maturation inhibitors diminished the induction of the immune response by AcNPV. Together, these results indicate that the internalization of viral DNA via membrane fusion mediated by the viral envelope glycoprotein, as well as endosomal maturation, which releases the viral genome into TLR9-expressing cellular compartments, is necessary for the induction of the innate immune response by AcNPV.

* Corresponding author. Mailing address: Research Center for Emerging Infectious Diseases, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamada-oka, Suita, Osaka 565-0871, Japan. Phone: 81-6-6879-8340. Fax: 81-6-6879-8269. E-mail: matsuura{at}biken.osaka-u.ac.jp.

{dagger} This study is dedicated to the memory of Ikuko Yanase.

Journal of Virology, March 2005, p. 2847-2858, Vol. 79, No. 5
0022-538X/05/$08.00+0     doi:10.1128/JVI.79.5.2847-2858.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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