A role for gorilla APOBEC3G in shaping lentivirus evolution including transmission to humans

Yusuke Nakano; Keisuke Yamamoto; Mahoko Takahashi Ueda; Andrew Soper; Yoriyuki Konno; Izumi Kimura; Keiya Uriu; Ryuichi Kumataez; Hirofumi Aso; Naoko Misawa; Shumpei Nagaoka; Soma Shimizu; Keito Mitsumune; Yusuke Kosug; Guillermo Juarez-Fernandez; Jumpei Ito; So Nakagawa; Terumasa Ikeda; Yoshio Koyanagi; Reuben S. Harris; Kei Sato

doi:10.1371/JOURNAL.PPAT.1008812

A role for gorilla APOBEC3G in shaping lentivirus evolution including transmission to humans

Yusuke Nakano, Keisuke Yamamoto, Mahoko Takahashi Ueda, Andrew Soper, Yoriyuki Konno, Izumi Kimura, Keiya Uriu, Ryuichi Kumataez, Hirofumi Aso, Naoko Misawa, Shumpei Nagaoka, Soma Shimizu, Keito Mitsumune, Yusuke Kosug, Guillermo Juarez-Fernandez, Jumpei Ito, So Nakagawa, Terumasa Ikeda, Yoshio Koyanagi, Reuben S. HarrisKei Sato

Molecular Biology (BMBB)

Research output: Contribution to journal › Article › peer-review

12 Scopus citations

Abstract

The APOBEC3 deaminases are potent inhibitors of virus replication and barriers to cross-species transmission. For simian immunodeficiency virus (SIV) to transmit to a new primate host, as happened multiple times to seed the ongoing HIV-1 epidemic, the viral infectivity factor (Vif) must be capable of neutralizing the APOBEC3 enzymes of the new host. Although much is known about current interactions of HIV-1 Vif and human APOBEC3s, the evolutionary changes in SIV Vif required for transmission from chimpanzees to gorillas and ultimately to humans are poorly understood. Here, we demonstrate that gorilla APOBEC3G is a factor with the potential to hamper SIV transmission from chimpanzees to gorillas. Gain-of-function experiments using SIVcpzPtt Vif revealed that this barrier could be overcome by a single Vif acidic amino acid substitution (M16E). Moreover, degradation of gorilla APOBEC3F is induced by Vif through a mechanism that is distinct from that of human APOBEC3F. Thus, our findings identify virus adaptations in gorillas that preceded and may have facilitated transmission to humans.

Original language	English (US)
Article number	e1008812
Journal	PLoS pathogens
Volume	16
Issue number	9
DOIs	https://doi.org/10.1371/JOURNAL.PPAT.1008812
State	Published - Sep 2020

Bibliographical note

Publisher Copyright:
Copyright: © 2020 Nakano et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Nakano, Y., Yamamoto, K., Ueda, M. T., Soper, A., Konno, Y., Kimura, I., Uriu, K., Kumataez, R., Aso, H., Misawa, N., Nagaoka, S., Shimizu, S., Mitsumune, K., Kosug, Y., Juarez-Fernandez, G., Ito, J., Nakagawa, S., Ikeda, T., Koyanagi, Y., ... Sato, K. (2020). A role for gorilla APOBEC3G in shaping lentivirus evolution including transmission to humans. PLoS pathogens, 16(9), Article e1008812. https://doi.org/10.1371/JOURNAL.PPAT.1008812

Nakano, Y, Yamamoto, K, Ueda, MT, Soper, A, Konno, Y, Kimura, I, Uriu, K, Kumataez, R, Aso, H, Misawa, N, Nagaoka, S, Shimizu, S, Mitsumune, K, Kosug, Y, Juarez-Fernandez, G, Ito, J, Nakagawa, S, Ikeda, T, Koyanagi, Y, Harris, RS & Sato, K 2020, 'A role for gorilla APOBEC3G in shaping lentivirus evolution including transmission to humans', PLoS pathogens, vol. 16, no. 9, e1008812. https://doi.org/10.1371/JOURNAL.PPAT.1008812

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abstract = "The APOBEC3 deaminases are potent inhibitors of virus replication and barriers to cross-species transmission. For simian immunodeficiency virus (SIV) to transmit to a new primate host, as happened multiple times to seed the ongoing HIV-1 epidemic, the viral infectivity factor (Vif) must be capable of neutralizing the APOBEC3 enzymes of the new host. Although much is known about current interactions of HIV-1 Vif and human APOBEC3s, the evolutionary changes in SIV Vif required for transmission from chimpanzees to gorillas and ultimately to humans are poorly understood. Here, we demonstrate that gorilla APOBEC3G is a factor with the potential to hamper SIV transmission from chimpanzees to gorillas. Gain-of-function experiments using SIVcpzPtt Vif revealed that this barrier could be overcome by a single Vif acidic amino acid substitution (M16E). Moreover, degradation of gorilla APOBEC3F is induced by Vif through a mechanism that is distinct from that of human APOBEC3F. Thus, our findings identify virus adaptations in gorillas that preceded and may have facilitated transmission to humans.",

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AU - Konno, Yoriyuki

AU - Kimura, Izumi

AU - Uriu, Keiya

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AU - Harris, Reuben S.

AU - Sato, Kei

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A role for gorilla APOBEC3G in shaping lentivirus evolution including transmission to humans

Abstract

Bibliographical note

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