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Comprehensive analysis on detection and function of endogenous RNA viruses

Planned

Project AreaNeo-virology: the raison d'etre of viruses
Project/Area Number 16H06430
Research Category

Grant-in-Aid for Scientific Research on Innovative Areas (Research in a proposed research area)

Allocation TypeSingle-year Grants
Review Section Biological Sciences
Research InstitutionKyoto University

Principal Investigator

Tomonaga Keizo  京都大学, ウイルス・再生医科学研究所, 教授 (10301920)

Co-Investigator(Kenkyū-buntansha) 川野 秀一  電気通信大学, 大学院情報理工学研究科, 准教授 (50611448)
Project Period (FY) 2016-06-30 – 2021-03-31
Project Status Completed (Fiscal Year 2020)
Budget Amount *help
¥161,720,000 (Direct Cost: ¥124,400,000、Indirect Cost: ¥37,320,000)
Fiscal Year 2020: ¥30,420,000 (Direct Cost: ¥23,400,000、Indirect Cost: ¥7,020,000)
Fiscal Year 2019: ¥29,510,000 (Direct Cost: ¥22,700,000、Indirect Cost: ¥6,810,000)
Fiscal Year 2018: ¥30,420,000 (Direct Cost: ¥23,400,000、Indirect Cost: ¥7,020,000)
Fiscal Year 2017: ¥29,510,000 (Direct Cost: ¥22,700,000、Indirect Cost: ¥6,810,000)
Fiscal Year 2016: ¥41,860,000 (Direct Cost: ¥32,200,000、Indirect Cost: ¥9,660,000)
Keywords内在性ウイルス / ボルナウイルス / 共進化 / 外適応 / 機械学習 / 内在性RNAウイルス / RNAウイルス / 進化 / ビッグデータ
Outline of Final Research Achievements

In this study, we conducted a comprehensive detection for the existence of endogenous RNA virus sequences in mammalian genomes and elucidated their functions. First, we constructed a program that predicts unknown endogenous RNA virus sequences by using a machine learning method to determine the sequence characteristics of endogenous RNA viruses. We succeeded in identifying unknown endogenous RNA virus-like sequences in the human genome. We also elucidated the functions of endogenous bornavirus-like sequences in the human and bat genomes and revealed that these sequences have been co-opted by host cells as functional proteins, such as RNA-binding protein, during the evolutionary process.

Academic Significance and Societal Importance of the Research Achievements

本研究の遂行により、哺乳動物ゲノムにはいまだ同定されていないウイルスに由来する遺伝子配列が存在する可能性が示された。また、哺乳動物ゲノムに内在化しているRNAウイルス由来配列が機能を持つことが明らかになり、私たちは進化過程で感染したウイルスを自らのゲノムに取り込むことで共存・進化してきた可能性が示された。これらの結果は、生命進化においるウイルス感染の意義についても再構築を迫るものとなった。

Report

(6 results)
  • 2020 Annual Research Report   Final Research Report ( PDF )
  • 2019 Annual Research Report
  • 2018 Annual Research Report
  • 2017 Annual Research Report
  • 2016 Annual Research Report

Research Products

(59 results)

All 2021 2020 2019 2018 2017 2016 Other

All Int'l Joint Research (5 results) Journal Article (18 results) (of which Int'l Joint Research: 6 results,  Peer Reviewed: 18 results,  Open Access: 10 results,  Acknowledgement Compliant: 1 results) Presentation (29 results) (of which Int'l Joint Research: 12 results,  Invited: 10 results) Book (2 results) Remarks (5 results)

  • [Int'l Joint Research] タフツ大学(米国)

    • Related Report
      2018 Annual Research Report
  • [Int'l Joint Research] フライブルク大学(ドイツ)

    • Related Report
      2018 Annual Research Report
  • [Int'l Joint Research] ヴァンダービルト大学/タフツ大学/コーネル大学(米国)

    • Related Report
      2017 Annual Research Report
  • [Int'l Joint Research] フライブルク大学(ドイツ)

    • Related Report
      2017 Annual Research Report
  • [Int'l Joint Research] パスツール研究所(フランス)

    • Related Report
      2017 Annual Research Report
  • [Journal Article] Virus-like insertions with sequence signatures similar to those of endogenous nonretroviral RNA viruses in the human genome2021

    • Author(s)
      Kojima Shohei、Yoshikawa Kohei、Ito Jumpei、Nakagawa So、Parrish Nicholas F.、Horie Masayuki、Kawano Shuichi、Tomonaga Keizo
    • Journal Title

      Proc Natl Acad Sci U S A.

      Volume: 118

    • DOI

      10.1073/pnas.2010758118

    • Related Report
      2020 Annual Research Report
    • Peer Reviewed / Open Access
  • [Journal Article] T. Honda. Modeling Borna disease virus in vitro spread reveals the mode of antiviral effect conferred by an endogenous bornavirus-like element2020

    • Author(s)
      K.S. Kim, Y. Yamamoto, S. Nakaoka, K. Tomonaga, S. Iwami,
    • Journal Title

      J Virol.

      Volume: -

    • DOI

      10.1128/jvi.01204-20

    • Related Report
      2020 Annual Research Report
    • Peer Reviewed / Int'l Joint Research
  • [Journal Article] Evolutionary Selection of the Nuclear Localization Signal in the Viral Nucleoprotein Leads to Host Adaptation of the Genus Orthobornavirus2020

    • Author(s)
      Komorizono R, Sassa Y, Horie M, Makino A, Tomonaga K.
    • Journal Title

      Viruses

      Volume: 12 Pages: 1291-1291

    • DOI

      10.3390/v12111291

    • NAID

      120007026452

    • Related Report
      2020 Annual Research Report
    • Peer Reviewed
  • [Journal Article] ADAR2 Is Involved in Self and Nonself Recognition of Borna Disease Virus Genomic RNA in the Nucleus.2020

    • Author(s)
      Yanai M, Kojima S, Sakai M, Komorizono R, Tomonaga K Makino A
    • Journal Title

      J Virol

      Volume: 94 Pages: 01513-01519

    • DOI

      10.1128/jvi.01513-19

    • Related Report
      2019 Annual Research Report
    • Peer Reviewed
  • [Journal Article] Identification of a distinct lineage of aviadenovirus from crane feces.2019

    • Author(s)
      Mukai Y, Tomita Y, Kryukov K, Nakagawa S, Ozawa M, Matsui T, Tomonaga K, Imanishi T, Kawaoka Y, Watanabe T, Horie M
    • Journal Title

      Virus Genes

      Volume: 55 Pages: 815-824

    • DOI

      10.1007/s11262-019-01703-w

    • Related Report
      2019 Annual Research Report
    • Peer Reviewed / Int'l Joint Research
  • [Journal Article] Neo-virology: The raison d'etre of viruses.2019

    • Author(s)
      Watanabe T, Suzuki N, Tomonaga K, Sawa H, Matsuura Y, Kawaguchi Y, Takahashi H, Nagasaki K, Kawaoka Y.
    • Journal Title

      Virus Research

      Volume: 274 Pages: 197751-197751

    • DOI

      10.1016/j.virusres.2019.197751

    • NAID

      130006183770

    • Related Report
      2019 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Intracellular dynamics of actin affects Borna disease virus replication in the nucleus2019

    • Author(s)
      Hirai Yuya、Domae Eisuke、Yoshikawa Yoshihiro、Okamura Hideyuki、Makino Akiko、Tomonaga Keizo
    • Journal Title

      Virus Res

      Volume: 263 Pages: 179-183

    • DOI

      10.1016/j.virusres.2019.02.004

    • Related Report
      2019 Annual Research Report
    • Peer Reviewed / Int'l Joint Research
  • [Journal Article] "Integration of viral sequences into eukaryotic host genomes: legacy of ancient infections".2019

    • Author(s)
      Tomonaga K, Suzuki N, Berkhout B.
    • Journal Title

      Virus Research.

      Volume: 262 Pages: 1-1

    • DOI

      10.1016/j.virusres.2018.12.012

    • Related Report
      2018 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Paleovirology of bornaviruses: What can be learned from molecular fossils of bornaviruses.2019

    • Author(s)
      Horie M, Tomonaga K.
    • Journal Title

      Virus Research

      Volume: 262 Pages: 002-009

    • DOI

      10.1016/j.virusres.2018.04.006

    • Related Report
      2018 Annual Research Report
    • Peer Reviewed
  • [Journal Article] Degradation of amyloid _ peptide by neprilysin expressed from Borna disease virus vector.2018

    • Author(s)
      Sakai M, Ueda S, Daito T, Asada-Utsugi M, Komatsu Y, Kinoshita A, Maki T, Kuzuya A, Takahashi R, Makino A, Tomonaga K.
    • Journal Title

      Microbiol Immunol.

      Volume: 62 Pages: 467-472

    • DOI

      10.1111/1348-0421.12602

    • Related Report
      2018 Annual Research Report
    • Peer Reviewed
  • [Journal Article] Systematic estimation of insertion dates of endogenous bornavirus-like elements in vesper bats2018

    • Author(s)
      Mukai Y, Horie M, Tomonaga K.
    • Journal Title

      J. Vet. Med. Sci.

      Volume: 80 Issue: 8 Pages: 1356-1363

    • DOI

      10.1292/jvms.18-0211

    • NAID

      130007475243

    • ISSN
      0916-7250, 1347-7439
    • Related Report
      2018 Annual Research Report
    • Peer Reviewed / Open Access
  • [Journal Article] Splicing-Dependent Subcellular Targeting of Borna Disease Virus Nucleoprotein Isoforms.2018

    • Author(s)
      Kojima S, Sato R, Yanai M, Komatsu Y, Horie M, Igarashi M, Tomonaga K.
    • Journal Title

      J Virol.

      Volume: 93

    • DOI

      10.1128/jvi.01621-18

    • Related Report
      2018 Annual Research Report
    • Peer Reviewed
  • [Journal Article] A Viral (Arc)hive for Metazoan Memory.2018

    • Author(s)
      Parrish NF,Tomonaga K.
    • Journal Title

      Cell

      Volume: 172 Pages: 8-10

    • DOI

      10.1016/j.cell.2017.12.029

    • Related Report
      2017 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Antiviral activity of favipiravir (T-705) against mammalian and avian bornaviruses.2017

    • Author(s)
      Tokunaga T, Yamamoto Y, Sakai M, Tomonaga K, Honda T.
    • Journal Title

      Antiviral Research

      Volume: 143 Pages: 237-245

    • DOI

      10.1016/j.antiviral.2017.04.018

    • Related Report
      2017 Annual Research Report
    • Peer Reviewed / Open Access
  • [Journal Article] Dual function of the nuclear export signal of the Borna disease virus nucleoprotein in nuclear export activity and binding to viral phosphoprotein.2017

    • Author(s)
      Yanai M, Sakai M, Makino A, Tomonaga K.
    • Journal Title

      Virology Journal

      Volume: 14 Pages: 126-126

    • DOI

      10.1186/s12985-017-0793-6

    • Related Report
      2017 Annual Research Report
    • Peer Reviewed / Open Access
  • [Journal Article] Linkage between the leader sequence and leader RNA production in Borna disease virus-infected cells.2017

    • Author(s)
      Honda T, Sofuku K, Kojima S, Yamamoto Y, Ohtaki N, Tomonaga K.
    • Journal Title

      Virology

      Volume: 510 Pages: 104-110

    • DOI

      10.1016/j.virol.2017.07.011

    • Related Report
      2017 Annual Research Report
    • Peer Reviewed / Open Access
  • [Journal Article] Generation of a non-transmissive Borna disease virus vector lacking both matrix and glycoprotein genes.2017

    • Author(s)
      Fujino K, Yamamoto Y, Daito T, Makino A, Honda T, Tomonaga K.
    • Journal Title

      Microbiology and Immunology

      Volume: 61 Pages: 380-386

    • DOI

      10.1111/1348-0421.12505

    • NAID

      40021326041

    • Related Report
      2017 Annual Research Report
    • Peer Reviewed / Open Access
  • [Journal Article] Borna Disease Virus Assembles Porous Cage-like Viral Factories in the Nucleus.2016

    • Author(s)
      Hirai Y, Hirano Y, Matsuda A, Hiraoka Y, Honda T, Tomonaga K.
    • Journal Title

      Journal of Biological Chemistry

      Volume: 291 Pages: 25789-25798

    • DOI

      10.1074/jbc.m116.746396

    • Related Report
      2016 Annual Research Report
    • Peer Reviewed / Open Access / Acknowledgement Compliant
  • [Presentation] ゲノムにおけるウイルス配列挿入の歴史: k-mer 出現頻度から読み解く2020

    • Author(s)
      小嶋将平,吉川剛平,伊東潤平,中川草,堀江真行,川野秀一,朝長啓造,Nicholas F. Parrish.
    • Organizer
      日本進化学会第22回オンライン大会
    • Related Report
      2020 Annual Research Report
  • [Presentation] 内在性ボルナウイルス様配列の網羅的解析:中生代から現代にわたるボルナウイルス感染履歴の追跡2020

    • Author(s)
      川崎純菜,小嶋将平,向井八尋,朝長啓造,堀江真行
    • Organizer
      第163回日本獣医学会学術集会
    • Related Report
      2020 Annual Research Report
  • [Presentation] A large-scale metaviromic analysis contributed to a deeper understanding of the evolution viruses: An example of deltaviruses in vertebrates2020

    • Author(s)
      Horie M, Iwamoto M, Shibata Y, Kawasaki J, Kojima S, Wada K, Watashi K, Tomonaga K.
    • Organizer
      第43回日本分子生物学会年会
    • Related Report
      2020 Annual Research Report
  • [Presentation] Evolutionarily Acquired Functions of Endogenous RNA Viral Elements in Mammals2019

    • Author(s)
      朝長啓造
    • Organizer
      第67回日本ウイルス学会学術集会
    • Related Report
      2019 Annual Research Report
    • Invited
  • [Presentation] Endogenous bornavirus-like N element in miniopterid bat genome encodes a potentially multifunctional RNA-binding protein.2019

    • Author(s)
      向井八尋, 堀江真行, 小林由紀, 小嶋将平, 前田健, 朝長啓造
    • Organizer
      第67回日本ウイルス学会学術集会
    • Related Report
      2019 Annual Research Report
  • [Presentation] 機械学習を用いた内在性ウイルス様配列の新規検索手法の開発. 第67回日本ウイルス学会学術集会2019

    • Author(s)
      小嶋将平, 吉川剛平, 伊東潤平, 中川草, 堀江真行, 川野秀一, 朝長啓造.
    • Organizer
      第67回日本ウイルス学会学術集会
    • Related Report
      2019 Annual Research Report
  • [Presentation] 内在性ボルナウイルス様配列の網羅的同定:真核生物とボルナウイルスの共進化過程の追跡2019

    • Author(s)
      川崎純菜, 小嶋将平, 向井八尋, 朝長啓造, 堀江真行
    • Organizer
      第42回日本分子生物学会年会
    • Related Report
      2019 Annual Research Report
  • [Presentation] A one-stage estimation of principal component regression for generalized linear models2018

    • Author(s)
      Shuichi Kawano, Hironori Fujisawa, Toyoyuki Takada, Toshihiko Shiroishi
    • Organizer
      The 2nd International Conference on Econometrics and Statistics
    • Related Report
      2018 Annual Research Report
    • Int'l Joint Research / Invited
  • [Presentation] A one-stage estimation of principal component regression for generalized linear models2018

    • Author(s)
      Shuichi Kawano
    • Organizer
      The 11th International Conference of the ERCIM WG on Computational and Methodological Statistics
    • Related Report
      2018 Annual Research Report
    • Int'l Joint Research / Invited
  • [Presentation] Roles of RNA transcripts from endogenous bornavirus-like elements in host evolution2018

    • Author(s)
      Keizo Tomonaga
    • Organizer
      Evolution
    • Related Report
      2018 Annual Research Report
    • Int'l Joint Research / Invited
  • [Presentation] Roles of non-coding RNAs from endogenous bornavirus-like elements in Borna disease virus infection2018

    • Author(s)
      Keizo Tomonaga
    • Organizer
      2nd International Symposium on RNA virus persistence
    • Related Report
      2018 Annual Research Report
    • Int'l Joint Research / Invited
  • [Presentation] Intranuclear persistent infection of bornavirus as an evolutionary strategy determining the survival and fitness2018

    • Author(s)
      Keizo Tomonaga
    • Organizer
      Virus Dynamics Workshop in Japan
    • Related Report
      2018 Annual Research Report
    • Int'l Joint Research / Invited
  • [Presentation] Systematic investigation of novel lineages of endogenous bornavirus-like elements in vertebrate genomes.2018

    • Author(s)
      Masayuki Horie, Shohei Kojima, Bea Clarise B.Garcia, Dong-Yun Kim, Yahiro Mukai, Nicholas F. Parrish, Keizo Tomonaga.
    • Organizer
      17th Negative Strand RNA Virus
    • Related Report
      2018 Annual Research Report
    • Int'l Joint Research
  • [Presentation] Alternative splicing unmasks an endoplasmic reticulum targeting signal of Borna disease virus nucleoprotein2018

    • Author(s)
      Shohei Kojima, Ryo Sato, Mako Yanai, Yumiko Komatsu, Manabu Igarashi, Masayuki Horie, Keizo Tomonaga.
    • Organizer
      17th Negative Strand RNA Virus
    • Related Report
      2018 Annual Research Report
    • Int'l Joint Research
  • [Presentation] Translational regulation of Borna disease  virus.2018

    • Author(s)
      Akiko Makino, Yutaro Yamamoto, Yuya Hirai, Keizo Tomonaga.
    • Organizer
      17th Negative Strand RNA Virus
    • Related Report
      2018 Annual Research Report
    • Int'l Joint Research
  • [Presentation] Investigation of the biological role of an endogenous bornavirus-like element in miniopterid bat genomes.2018

    • Author(s)
      Yahiro Mukai, Masayuki Horie, Yuki Kobayashi, Shohei Kojima, Ken Maeda, Keizo Tomonaga.
    • Organizer
      17th Negative Strand RNA Virus
    • Related Report
      2018 Annual Research Report
    • Int'l Joint Research
  • [Presentation] 内在性ボルナウイルス様エレメント由来非コードRNAはボルナウイルスの感染を抑制する.2018

    • Author(s)
      小嶋 将平, 本田 知之, 朝長 啓造.
    • Organizer
      第20回日本RNA学会年会
    • Related Report
      2018 Annual Research Report
  • [Presentation] Determination of interacting host factors of an endogenous bornavirus-like element-derived protein in miniopterid bat cells.2018

    • Author(s)
      向井八尋, 堀江真行, 小林由紀, 小嶋将平, 前田健, 朝長啓造
    • Organizer
      第66回日 本ウイルス学会学術集会
    • Related Report
      2018 Annual Research Report
  • [Presentation] Characterization of newly discovered endogenous bornavirus-like elements in the human genome.2018

    • Author(s)
      Dong-Yun Kim, Yahiro Mukai, Shohei Kojima, Yumiko Komatsu, Masayuki Horie, Keizo Tomonaga.
    • Organizer
      第66回日 本ウイルス学会学術集会
    • Related Report
      2018 Annual Research Report
  • [Presentation] 内在性RNAウイルス様配列の新規   検索手法の開発と新たなウイルス様配列の同定.2018

    • Author(s)
      小嶋将平, 川野秀一, 伊藤潤平, 中川草, 堀江真行, 朝長啓造.
    • Organizer
      第41回日本分子生物学会年会.
    • Related Report
      2018 Annual Research Report
  • [Presentation] Bornavirus: a new model of coevolution between RNA virus and host.2018

    • Author(s)
      Tomonaga K
    • Organizer
      The 91st Annual Meeting of Japanese Society for Bacteriology.
    • Related Report
      2017 Annual Research Report
    • Invited
  • [Presentation] Loading of small RNAs derived from an endogenous bornaviruses element on the MIWI protein in GC2 Cells.2017

    • Author(s)
      Honda T, Liu X, Garcia BC, Parrish NF, Tomonaga K.
    • Organizer
      The 16th Awaji International Forum on Infection and Immunity.
    • Related Report
      2017 Annual Research Report
    • Int'l Joint Research
  • [Presentation] ユビナガコウモリゲノムに内在する内在性ボルナウイルス様エレメントの基本的な性状解析と内在化年代の推定2017

    • Author(s)
      向井八尋,堀江真行,小嶋将平,長田奈緒,前田 健,朝長啓造
    • Organizer
      第160回日本獣医学会学術集会
    • Related Report
      2017 Annual Research Report
  • [Presentation] Molecular biological and evolutionary analysis of an endogenous bornavirus-like nucleoprotein element in miniopterid bat genomes.2017

    • Author(s)
      Mukai Y, Horie M, Kobayashi K, Kojima S, Nagata N, Maeda K and Tomonaga K.
    • Organizer
      第65回日本ウイルス学会学術集会
    • Related Report
      2017 Annual Research Report
  • [Presentation] Bornavirus infection: a new model of evolution and coexistence of RNA viruses.2017

    • Author(s)
      Tomonaga K
    • Organizer
      The National Symposium on Zoonoses Research 2017
    • Related Report
      2017 Annual Research Report
    • Int'l Joint Research / Invited
  • [Presentation] 哺乳動物ゲノムに内在化しているボルナウイルス由来因子の機能解析2016

    • Author(s)
      朝長啓造
    • Organizer
      第39回分子生物学会
    • Place of Presentation
      横浜
    • Year and Date
      2016-11-30
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] Transcription profile and prospective function of non-retroviral RNA virus-derived elements in mammalian genomes.2016

    • Author(s)
      Keizo Tomonaga
    • Organizer
      International Conference of the Genetics Society of Korea 2016
    • Place of Presentation
      Jeju Island, Korea
    • Year and Date
      2016-11-09
    • Related Report
      2016 Annual Research Report
    • Int'l Joint Research / Invited
  • [Presentation] カワリリスボルナウイルスの特性評価.2016

    • Author(s)
      389.牧野晶子, 小森園 亮, Bea Clarise Garcia, 朝長啓造.
    • Organizer
      第64回日本ウイルス学会学術集会.
    • Place of Presentation
      札幌
    • Year and Date
      2016-10-23
    • Related Report
      2016 Annual Research Report
  • [Presentation] ウイルス感染を抑制する内在性ボルナウイルス由来RNAエレメントの進化.2016

    • Author(s)
      小嶋将平, 本田知之, 朝長啓造.
    • Organizer
      第64回日本ウイルス学会学術集会.
    • Place of Presentation
      札幌,
    • Year and Date
      2016-10-23
    • Related Report
      2016 Annual Research Report
  • [Book] ネオウイルス学2021

    • Author(s)
      河岡義裕
    • Total Pages
      315
    • Publisher
      集英社
    • Related Report
      2020 Annual Research Report
  • [Book] グローバル時代のウイルス感染症2019

    • Author(s)
      西條 政幸
    • Total Pages
      296
    • Publisher
      日本医事新報社
    • ISBN
      9784784921508
    • Related Report
      2019 Annual Research Report
  • [Remarks] 京都大学ウイルス・再生医科学研究所

    • URL

      https://www.infront.kyoto-u.ac.jp/

    • Related Report
      2020 Annual Research Report
  • [Remarks] 京都大学ウイルス・再生医科学研究所 朝長研究室

    • URL

      https://t.rnavirus.virus.kyoto-u.ac.jp/

    • Related Report
      2018 Annual Research Report
  • [Remarks] 京都大学ウイルス・再生医科学研究所RNAウイルス分野

    • URL

      https://t.rnavirus.virus.kyoto-u.ac.jp/

    • Related Report
      2017 Annual Research Report
  • [Remarks] 京都大学ウイルス・再生医科学研究所朝長研究室HP

    • URL

      https://t.rnavirus.virus.kyoto-u.ac.jp/

    • Related Report
      2016 Annual Research Report
  • [Remarks] ネオウイルス学領域HP

    • URL

      http://neo-virology.org/

    • Related Report
      2016 Annual Research Report

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Published: 2016-07-04   Modified: 2022-02-28  

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