Two-step evolution of HIV-1 budding system leading to pandemic in the human population

Yoriyuki Konno; Keiya Uriu; Takayuki Chikata; Toru Takada; Jun-Ichi Kurita; Mahoko Takahashi Ueda; Saiful Islam; Benjy Jek Yang Tan; Jumpei Ito; Hirofumi Aso; Ryuichi Kumata; Carolyn Williamson; Shingo Iwami; Masafumi Takiguchi; Yoshifumi Nishimura; Eiji Morita; Yorifumi Satou; So Nakagawa; Yoshio Koyanagi; Kei Sato

doi:10.1016/j.celrep.2024.113697

Two-step evolution of HIV-1 budding system leading to pandemic in the human population

Cell Rep. 2024 Feb 27;43(2):113697. doi: 10.1016/j.celrep.2024.113697. Epub 2024 Jan 30.

Authors

Yoriyuki Konno¹, Keiya Uriu², Takayuki Chikata³, Toru Takada⁴, Jun-Ichi Kurita⁵, Mahoko Takahashi Ueda⁶, Saiful Islam³, Benjy Jek Yang Tan³, Jumpei Ito¹, Hirofumi Aso⁷, Ryuichi Kumata¹, Carolyn Williamson⁸, Shingo Iwami⁹, Masafumi Takiguchi³, Yoshifumi Nishimura⁵, Eiji Morita¹⁰, Yorifumi Satou³, So Nakagawa⁶, Yoshio Koyanagi¹¹, Kei Sato¹²

Affiliations

¹ Division of Systems Virology, Department of Microbiology and Immunology, The Institute of Medical Science, The University of Tokyo, Tokyo 1088639, Japan.
² Division of Systems Virology, Department of Microbiology and Immunology, The Institute of Medical Science, The University of Tokyo, Tokyo 1088639, Japan; Graduate School of Medicine, the University of Tokyo, Tokyo 1130033, Japan; Department of Biochemistry and Molecular Biology, Faculty of Agriculture and Life Science, Hirosaki University, Aomori 0368561, Japan.
³ Joint Research Center for Human Retrovirus Infection, Kumamoto University, Kumamoto 8608556, Japan.
⁴ Department of Biology, Faculty of Sciences, Kyushu University, Fukuoka 8128581, Japan.
⁵ Graduate School of Medical Life Science, Yokohama City University, Kanagawa 2300045, Japan.
⁶ Department of Molecular Life Science, Tokai University School of Medicine, Kanagawa 2591193, Japan.
⁷ Division of Systems Virology, Department of Microbiology and Immunology, The Institute of Medical Science, The University of Tokyo, Tokyo 1088639, Japan; Institute for Frontier Life and Medical Sciences, Kyoto University, Kyoto 6068507, Japan; Graduate School of Pharmaceutical Sciences, Kyoto University, Kyoto 6068501, Japan.
⁸ Institute of Infectious Diseases and Molecular Medicine, University of Cape Town, Cape Town 7925, South Africa.
⁹ Department of Biology, Faculty of Sciences, Kyushu University, Fukuoka 8128581, Japan; MIRAI, Japan Science and Technology Agency, Kawaguchi 3320012, Japan.
¹⁰ Department of Biochemistry and Molecular Biology, Faculty of Agriculture and Life Science, Hirosaki University, Aomori 0368561, Japan.
¹¹ Institute for Frontier Life and Medical Sciences, Kyoto University, Kyoto 6068507, Japan; Graduate School of Pharmaceutical Sciences, Kyoto University, Kyoto 6068501, Japan.
¹² Division of Systems Virology, Department of Microbiology and Immunology, The Institute of Medical Science, The University of Tokyo, Tokyo 1088639, Japan; Graduate School of Medicine, the University of Tokyo, Tokyo 1130033, Japan; International Research Center for Infectious Diseases, The Institute of Medical Science, The University of Tokyo, Tokyo 1088639, Japan; International Vaccine Design Center, The Institute of Medical Science, The University of Tokyo, Tokyo 1088639, Japan; Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa 2778561, Japan; CREST, Japan Science and Technology Agency, Kawaguchi 3320012, Japan. Electronic address: keisato@g.ecc.u-tokyo.ac.jp.

PMID: 38294901
DOI: 10.1016/j.celrep.2024.113697

Abstract

The pandemic HIV-1, HIV-1 group M, emerged from a single spillover event of its ancestral lentivirus from a chimpanzee. During human-to-human spread worldwide, HIV-1 diversified into multiple subtypes. Here, our interdisciplinary investigation mainly sheds light on the evolutionary scenario of the viral budding system of HIV-1 subtype C (HIV-1C), a most successfully spread subtype. Of the two amino acid motifs for HIV-1 budding, the P(T/S)AP and YPxL motifs, HIV-1C loses the YPxL motif. Our data imply that HIV-1C might lose this motif to evade immune pressure. Additionally, the P(T/S)AP motif is duplicated dependently of the level of HIV-1 spread in the human population, and >20% of HIV-1C harbored the duplicated P(T/S)AP motif. We further show that the duplication of the P(T/S)AP motif is caused by the expansion of the CTG triplet repeat. Altogether, our results suggest that HIV-1 has experienced a two-step evolution of the viral budding process during human-to-human spread worldwide.

Keywords: CP: Microbiology; HIV-1; budding; evolution; systems virology.

MeSH terms

Animals
Cell Division
HIV Seropositivity*
HIV-1* / genetics
Humans
Lentivirus
Pan troglodytes
Pandemics