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Targeted viral adaptation generates a simian-tropic hepatitis B virus that infects marmoset cells

Author

Listed:
  • Yongzhen Liu

    (Princeton University)

  • Thomas R. Cafiero

    (Princeton University)

  • Debby Park

    (Princeton University)

  • Abhishek Biswas

    (Princeton University
    Princeton University)

  • Benjamin Y. Winer

    (Princeton University
    Memorial Sloan-Kettering Cancer Center)

  • Cheul H. Cho

    (Visikol, Inc.)

  • Yaron Bram

    (Weill Cornell Medicine)

  • Vasuretha Chandar

    (Weill Cornell Medicine)

  • Aoife K. O’ Connell

    (Boston University)

  • Hans P. Gertje

    (Boston University)

  • Nicholas Crossland

    (Boston University
    Boston University Chobanian & Avedisian School of Medicine)

  • Robert E. Schwartz

    (Weill Cornell Medicine)

  • Alexander Ploss

    (Princeton University)

Abstract

Hepatitis B virus (HBV) only infects humans and chimpanzees, posing major challenges for modeling HBV infection and chronic viral hepatitis. The major barrier in establishing HBV infection in non-human primates lies at incompatibilities between HBV and simian orthologues of the HBV receptor, sodium taurocholate co-transporting polypeptide (NTCP). Through mutagenesis analysis and screening among NTCP orthologues from Old World monkeys, New World monkeys and prosimians, we determined key residues responsible for viral binding and internalization, respectively and identified marmosets as a suitable candidate for HBV infection. Primary marmoset hepatocytes and induced pluripotent stem cell-derived hepatocyte-like cells support HBV and more efficient woolly monkey HBV (WMHBV) infection. Adapted chimeric HBV genome harboring residues 1–48 of WMHBV preS1 generated here led to a more efficient infection than wild-type HBV in primary and stem cell derived marmoset hepatocytes. Collectively, our data demonstrate that minimal targeted simianization of HBV can break the species barrier in small NHPs, paving the path for an HBV primate model.

Suggested Citation

  • Yongzhen Liu & Thomas R. Cafiero & Debby Park & Abhishek Biswas & Benjamin Y. Winer & Cheul H. Cho & Yaron Bram & Vasuretha Chandar & Aoife K. O’ Connell & Hans P. Gertje & Nicholas Crossland & Robert, 2023. "Targeted viral adaptation generates a simian-tropic hepatitis B virus that infects marmoset cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39148-3
    DOI: 10.1038/s41467-023-39148-3
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    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. Sreya Biswas & Lauren N. Rust & Jochen M. Wettengel & Sofiya Yusova & Miranda Fischer & Julien N. Carson & Josie Johnson & Lei Wei & Trason Thode & Mohan R. Kaadige & Sunil Sharma & Majd Agbaria & Ben, 2022. "Long-term hepatitis B virus infection of rhesus macaques requires suppression of host immunity," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Jae-Hyun Park & Masashi Iwamoto & Ji-Hye Yun & Tomomi Uchikubo-Kamo & Donghwan Son & Zeyu Jin & Hisashi Yoshida & Mio Ohki & Naito Ishimoto & Kenji Mizutani & Mizuki Oshima & Masamichi Muramatsu & Tak, 2022. "Structural insights into the HBV receptor and bile acid transporter NTCP," Nature, Nature, vol. 606(7916), pages 1027-1031, June.
    4. Benjamin Y. Winer & Tiffany S. Huang & Eitan Pludwinski & Brigitte Heller & Felix Wojcik & Gabriel E. Lipkowitz & Amit Parekh & Cheul Cho & Anil Shrirao & Tom W. Muir & Eric Novik & Alexander Ploss, 2017. "Long-term hepatitis B infection in a scalable hepatic co-culture system," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    5. Xiaoming Zhou & Elena J. Levin & Yaping Pan & Jason G. McCoy & Ruchika Sharma & Brian Kloss & Renato Bruni & Matthias Quick & Ming Zhou, 2014. "Structural basis of the alternating-access mechanism in a bile acid transporter," Nature, Nature, vol. 505(7484), pages 569-573, January.
    6. Florian Douam & Carly G. K. Ziegler & Gabriela Hrebikova & Bruno Fant & Robert Leach & Lance Parsons & Wei Wang & Jenna M. Gaska & Benjamin Y. Winer & Brigitte Heller & Alex K. Shalek & Alexander Plos, 2018. "Selective expansion of myeloid and NK cells in humanized mice yields human-like vaccine responses," Nature Communications, Nature, vol. 9(1), pages 1-19, December.
    7. Kapil Goutam & Francesco S. Ielasi & Els Pardon & Jan Steyaert & Nicolas Reyes, 2022. "Structural basis of sodium-dependent bile salt uptake into the liver," Nature, Nature, vol. 606(7916), pages 1015-1020, June.
    8. Benjamin J. Burwitz & Jochen M. Wettengel & Martin A. Mück-Häusl & Marc Ringelhan & Chunkyu Ko & Marvin M. Festag & Katherine B. Hammond & Mina Northrup & Benjamin N. Bimber & Thomas Jacob & Jason S. , 2017. "Hepatocytic expression of human sodium-taurocholate cotransporting polypeptide enables hepatitis B virus infection of macaques," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    9. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
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