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

Summary: 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...

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Main Authors: 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
Format: Article
Language:English
Published: Elsevier 2024-02-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124724000251
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author 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
author_facet 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
author_sort Yoriyuki Konno
collection DOAJ
description Summary: 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.
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spelling doaj.art-41d9fc0df08f49a5bbad067261708bcf2024-02-29T05:18:39ZengElsevierCell Reports2211-12472024-02-01432113697Two-step evolution of HIV-1 budding system leading to pandemic in the human populationYoriyuki Konno0Keiya Uriu1Takayuki Chikata2Toru Takada3Jun-ichi Kurita4Mahoko Takahashi Ueda5Saiful Islam6Benjy Jek Yang Tan7Jumpei Ito8Hirofumi Aso9Ryuichi Kumata10Carolyn Williamson11Shingo Iwami12Masafumi Takiguchi13Yoshifumi Nishimura14Eiji Morita15Yorifumi Satou16So Nakagawa17Yoshio Koyanagi18Kei Sato19Division of Systems Virology, Department of Microbiology and Immunology, The Institute of Medical Science, The University of Tokyo, Tokyo 1088639, JapanDivision 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, JapanJoint Research Center for Human Retrovirus Infection, Kumamoto University, Kumamoto 8608556, JapanDepartment of Biology, Faculty of Sciences, Kyushu University, Fukuoka 8128581, JapanGraduate School of Medical Life Science, Yokohama City University, Kanagawa 2300045, JapanDepartment of Molecular Life Science, Tokai University School of Medicine, Kanagawa 2591193, JapanJoint Research Center for Human Retrovirus Infection, Kumamoto University, Kumamoto 8608556, JapanJoint Research Center for Human Retrovirus Infection, Kumamoto University, Kumamoto 8608556, JapanDivision of Systems Virology, Department of Microbiology and Immunology, The Institute of Medical Science, The University of Tokyo, Tokyo 1088639, JapanDivision 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, JapanDivision of Systems Virology, Department of Microbiology and Immunology, The Institute of Medical Science, The University of Tokyo, Tokyo 1088639, JapanInstitute of Infectious Diseases and Molecular Medicine, University of Cape Town, Cape Town 7925, South AfricaDepartment of Biology, Faculty of Sciences, Kyushu University, Fukuoka 8128581, Japan; MIRAI, Japan Science and Technology Agency, Kawaguchi 3320012, JapanJoint Research Center for Human Retrovirus Infection, Kumamoto University, Kumamoto 8608556, JapanGraduate School of Medical Life Science, Yokohama City University, Kanagawa 2300045, JapanDepartment of Biochemistry and Molecular Biology, Faculty of Agriculture and Life Science, Hirosaki University, Aomori 0368561, JapanJoint Research Center for Human Retrovirus Infection, Kumamoto University, Kumamoto 8608556, JapanDepartment of Molecular Life Science, Tokai University School of Medicine, Kanagawa 2591193, JapanInstitute for Frontier Life and Medical Sciences, Kyoto University, Kyoto 6068507, Japan; Graduate School of Pharmaceutical Sciences, Kyoto University, Kyoto 6068501, JapanDivision 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; Corresponding authorSummary: 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.http://www.sciencedirect.com/science/article/pii/S2211124724000251CP: Microbiology
spellingShingle 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
Two-step evolution of HIV-1 budding system leading to pandemic in the human population
Cell Reports
CP: Microbiology
title Two-step evolution of HIV-1 budding system leading to pandemic in the human population
title_full Two-step evolution of HIV-1 budding system leading to pandemic in the human population
title_fullStr Two-step evolution of HIV-1 budding system leading to pandemic in the human population
title_full_unstemmed Two-step evolution of HIV-1 budding system leading to pandemic in the human population
title_short Two-step evolution of HIV-1 budding system leading to pandemic in the human population
title_sort two step evolution of hiv 1 budding system leading to pandemic in the human population
topic CP: Microbiology
url http://www.sciencedirect.com/science/article/pii/S2211124724000251
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