Multiple-clone infections of Mpox: Insights from a single primary lesion

Objectives: The 2022 Mpox epidemic transitioned to human-to-human transmission through primary lesions, showing a higher rate of genomic mutations than typical for a DNA virus. While Orthopoxviruses are traditionally considered to cause monoclonal infections in a single patient, we explored whether...

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Main Authors: Natsuko Kaku, Mayo Yasugi, Evariste Tshibangu-Kabamba, Yoshiyuki Wakabayashi, Yuko Uesaka, Yu Nakagama, Takuto Nogimori, Takuya Yamamoto, Placide Mbala-Kingebeni, Dieudonné Mumba Ngoyi, Eisuke Adachi, Yasutoshi Kido
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:CMI Communications
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Online Access:http://www.sciencedirect.com/science/article/pii/S295059092405042X
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author Natsuko Kaku
Mayo Yasugi
Evariste Tshibangu-Kabamba
Yoshiyuki Wakabayashi
Yuko Uesaka
Yu Nakagama
Takuto Nogimori
Takuya Yamamoto
Placide Mbala-Kingebeni
Dieudonné Mumba Ngoyi
Eisuke Adachi
Yasutoshi Kido
author_facet Natsuko Kaku
Mayo Yasugi
Evariste Tshibangu-Kabamba
Yoshiyuki Wakabayashi
Yuko Uesaka
Yu Nakagama
Takuto Nogimori
Takuya Yamamoto
Placide Mbala-Kingebeni
Dieudonné Mumba Ngoyi
Eisuke Adachi
Yasutoshi Kido
author_sort Natsuko Kaku
collection DOAJ
description Objectives: The 2022 Mpox epidemic transitioned to human-to-human transmission through primary lesions, showing a higher rate of genomic mutations than typical for a DNA virus. While Orthopoxviruses are traditionally considered to cause monoclonal infections in a single patient, we explored whether Mpox virus (MPXV) exhibits genomic plasticity in primary lesions. Methods: Five clones, A3, A4, B3, C2, and C5, were isolated from a primary skin lesion of an adult male patient with Mpox and human immunodeficiency virus on antiretroviral therapy, who was not immunocompromised. Whole-genome sequencing was performed to analyze single nucleotide variations in each clone. The tissue culture infectious dose 50 (TCID50) and cytopathic effects (CPE) were measured at one, three, and six days post-infection as in vitro virus phenotypes. Results: Clones A4, C2, and C5 had dominantly identical sequences, while minor clones A3 and B3 had probably three and certainly one additional unique mutation, respectively. Four mutations in A3 and B3 were located in the viral open reading frames, with A3 causing amino acid substitutions at two sites in B21R and B3 resulting in one amino acid change in I6L. Although there were no significant differences in TCID50 levels among the clones, B3 showed a greater CPE than the others at three and six days post-infection. Conclusions: The coexistence of multiple clones with distinct genotypes and viral characteristics within a primary lesion suggests genomic plasticity in MPXV, indicating that genomic diversity may arise early in infection.
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spelling doaj-art-b7b60184e6d34bd296ca6f02ed8923b22025-08-20T03:42:45ZengElsevierCMI Communications2950-59092024-12-011310504210.1016/j.cmicom.2024.105042Multiple-clone infections of Mpox: Insights from a single primary lesionNatsuko Kaku0Mayo Yasugi1Evariste Tshibangu-Kabamba2Yoshiyuki Wakabayashi3Yuko Uesaka4Yu Nakagama5Takuto Nogimori6Takuya Yamamoto7Placide Mbala-Kingebeni8Dieudonné Mumba Ngoyi9Eisuke Adachi10Yasutoshi Kido11Graduate School of Medicine, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, Japan; Osaka International Research Center for Infectious Diseases, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, JapanGraduate School of Veterinary Science, Osaka Metropolitan University, 1-58 Rinkuoraikita, Izumisano, Osaka 598-0048, Japan; Asian Health Science Research Institute, Osaka Metropolitan University, 1-58 Rinkuoraikita, Izumisano, Osaka 598-0048, JapanGraduate School of Medicine, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, Japan; Osaka International Research Center for Infectious Diseases, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, Japan; University of Mbujimayi, VJWG+4H7, Avenue Lumumba, Mbuji-Mayi, Democratic Republic of the CongoGraduate School of Medicine, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, Japan; Osaka International Research Center for Infectious Diseases, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, JapanGraduate School of Medicine, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, Japan; Osaka International Research Center for Infectious Diseases, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, JapanGraduate School of Medicine, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, Japan; Osaka International Research Center for Infectious Diseases, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, JapanCenter for Intractable Diseases and ImmunoGenomics, National Institutes of Biomedical Innovation, Health and Nutrition, 7-6-8 Saitoasagi, Ibaraki, Osaka 567-0085, JapanCenter for Intractable Diseases and ImmunoGenomics, National Institutes of Biomedical Innovation, Health and Nutrition, 7-6-8 Saitoasagi, Ibaraki, Osaka 567-0085, JapanInstitut National de Recherche Biomédicale, Ministère de la Santé Publique, M8R2+4WX, Kinshasa, Democratic Republic of the CongoInstitut National de Recherche Biomédicale, Ministère de la Santé Publique, M8R2+4WX, Kinshasa, Democratic Republic of the CongoIMSUT Hospital of The Institute of Medical Science, The University of Tokyo, 4-6-1 Shirokanedai, Minato City, Tokyo 108-8639, JapanGraduate School of Medicine, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, Japan; Osaka International Research Center for Infectious Diseases, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, Japan; Corresponding author at: Department of Virology and Parasitology, Graduate School of Medicine, Osaka Metropolitan University, 1-4-3 Asahimachi, Abeno Ward, Osaka 545-8585, Japan.Objectives: The 2022 Mpox epidemic transitioned to human-to-human transmission through primary lesions, showing a higher rate of genomic mutations than typical for a DNA virus. While Orthopoxviruses are traditionally considered to cause monoclonal infections in a single patient, we explored whether Mpox virus (MPXV) exhibits genomic plasticity in primary lesions. Methods: Five clones, A3, A4, B3, C2, and C5, were isolated from a primary skin lesion of an adult male patient with Mpox and human immunodeficiency virus on antiretroviral therapy, who was not immunocompromised. Whole-genome sequencing was performed to analyze single nucleotide variations in each clone. The tissue culture infectious dose 50 (TCID50) and cytopathic effects (CPE) were measured at one, three, and six days post-infection as in vitro virus phenotypes. Results: Clones A4, C2, and C5 had dominantly identical sequences, while minor clones A3 and B3 had probably three and certainly one additional unique mutation, respectively. Four mutations in A3 and B3 were located in the viral open reading frames, with A3 causing amino acid substitutions at two sites in B21R and B3 resulting in one amino acid change in I6L. Although there were no significant differences in TCID50 levels among the clones, B3 showed a greater CPE than the others at three and six days post-infection. Conclusions: The coexistence of multiple clones with distinct genotypes and viral characteristics within a primary lesion suggests genomic plasticity in MPXV, indicating that genomic diversity may arise early in infection.http://www.sciencedirect.com/science/article/pii/S295059092405042XMpox virusMultiple-clone infectionsGenomic plasticityIntra-host evolutionHuman-to-human transmission
spellingShingle Natsuko Kaku
Mayo Yasugi
Evariste Tshibangu-Kabamba
Yoshiyuki Wakabayashi
Yuko Uesaka
Yu Nakagama
Takuto Nogimori
Takuya Yamamoto
Placide Mbala-Kingebeni
Dieudonné Mumba Ngoyi
Eisuke Adachi
Yasutoshi Kido
Multiple-clone infections of Mpox: Insights from a single primary lesion
CMI Communications
Mpox virus
Multiple-clone infections
Genomic plasticity
Intra-host evolution
Human-to-human transmission
title Multiple-clone infections of Mpox: Insights from a single primary lesion
title_full Multiple-clone infections of Mpox: Insights from a single primary lesion
title_fullStr Multiple-clone infections of Mpox: Insights from a single primary lesion
title_full_unstemmed Multiple-clone infections of Mpox: Insights from a single primary lesion
title_short Multiple-clone infections of Mpox: Insights from a single primary lesion
title_sort multiple clone infections of mpox insights from a single primary lesion
topic Mpox virus
Multiple-clone infections
Genomic plasticity
Intra-host evolution
Human-to-human transmission
url http://www.sciencedirect.com/science/article/pii/S295059092405042X
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