Emergence and Potential Extinction of Genetic Lineages of Human Metapneumovirus between 2005 and 2021

Groen, Kaz; Nieuwkoop, Stefan van; Meijer, Adam; Veer, Bas van der; Kampen, Jeroen J.A. van; Fraaij, Pieter L. A.; Fouchier, Ron A. M.; Hoogen, Bernadette van den

doi:10.1128/mbio.02280-22

Cited by 10 publications

(14 citation statements)

References 37 publications

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“…HMPV can be categorized in genotypes A and B, which were initially split into four sublineages: A1, A2, B1, and B2 ( 8 ). Viruses from the A1 sublineage have not been detected since 2006, while viruses from the other sublineages have continued to circulate and evolve, resulting in the emergence of newly described sublineages ( 9 ). For instance, in recent years, the circulation of viruses with a duplication in the attachment gene (G) of either 111 or 180 nucleotides (nt) was reported.…”

Section: Introductionmentioning

confidence: 99%

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Human metapneumovirus infection of organoid-derived human bronchial epithelium represents cell tropism and cytopathology as observed in in vivo models

Ribó-Molina,

van Nieuwkoop,

Mykytyn

et al. 2024

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Human metapneumovirus (HMPV), a member of the Pneumoviridae family, causes upper and lower respiratory tract infections in humans. In vitro studies with HMPV have mostly been performed in monolayers of undifferentiated epithelial cells. In vivo studies in cynomolgus macaques and cotton rats have shown that ciliated epithelial cells are the main target of HMPV infection, but these observations cannot be studied in monolayer systems. Here, we established an organoid-derived bronchial culture model that allows physiologically relevant studies on HMPV. Inoculation with multiple prototype HMPV viruses and recent clinical virus isolates led to differences in replication among HMPV isolates. Prolific HMPV replication in this model caused damage to the ciliary layer, including cilia loss at advanced stages post-infection. These cytopathic effects correlated with those observed in previous in vivo studies with cynomolgus macaques. The assessment of the innate immune responses in three donors upon HMPV and RSV inoculation highlighted the importance of incorporating multiple donors to account for donor-dependent variation. In conclusion, these data indicate that the organoid-derived bronchial cell culture model resembles in vivo findings and is therefore a suitable and robust model for future HMPV studies. IMPORTANCE Human metapneumovirus (HMPV) is one of the leading causative agents of respiratory disease in humans, with no treatment or vaccine available yet. The use of primary epithelial cultures that recapitulate the tissue morphology and biochemistry of the human airways could aid in defining more relevant targets to prevent HMPV infection. For this purpose, this study established the first primary organoid-derived bronchial culture model suitable for a broad range of HMPV isolates. These bronchial cultures were assessed for HMPV replication, cellular tropism, cytopathology, and innate immune responses, where the observations were linked to previous in vivo studies with HMPV. This study exposed an important gap in the HMPV field since extensively cell-passaged prototype HMPV B viruses did not replicate in the bronchial cultures, underpinning the need to use recently isolated viruses with a controlled passage history. These results were reproducible in three different donors, supporting this model to be suitable to study HMPV infection.

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Section: Introductionmentioning

confidence: 99%

“…For instance, in recent years, the circulation of viruses with a duplication in the attachment gene (G) of either 111 or 180 nucleotides (nt) was reported. These viruses all belonged to the newly defined lineage A2.2.2 ( 9 – 13 ).…”

Section: Introductionmentioning

confidence: 99%

Human metapneumovirus infection of organoid-derived human bronchial epithelium represents cell tropism and cytopathology as observed in in vivo models

Ribó-Molina,

van Nieuwkoop,

Mykytyn

et al. 2024

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“…The aim of this study was to analyse the hMPV sequences obtained in East Japan in 2018 to 2022, before and after the COVID-19 pandemic, focusing on nearly complete The 180-nt and 111-nt duplications in the G gene of subgroup A2c (also named A2b2) were first reported in Spain and Japan (7)(8)(9)(10). The dominance of these viruses, especially A2c111nt-dup, is a recent global trend (7,11,13,14,27). Although A2c180-dup was not seen after 2018, it was reported that viruses carrying this G gene duplication caused lower respiratory tract infections (LRTI) in adults, possibly due to its immune evasion mechanism (28).…”

Section: Discussionmentioning

confidence: 99%

“…Although A2c180-dup was not seen after 2018, it was reported that viruses carrying this G gene duplication caused lower respiratory tract infections (LRTI) in adults, possibly due to its immune evasion mechanism (28). In Europe, hMPV circulation ebbed in 2020 due to COVID-19, but it re-emerged in and after 2021, and the most frequently detected clade was A2c111nt-dup (11,13). A2c111nt-dup was detected in 2017 to 2019; however, because of COVID-19, hMPV was not seen in 2020 to 2021 in Fukushima, East Japan (15).…”

Section: Discussionmentioning

confidence: 99%

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Molecular Epidemiology of Human Metapneumovirus in East Japan before and after COVID-19, 2017–2022

Shirato,

Suwa,

Nao

et al. 2024

Jpn J Infect Dis

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Human metapneumovirus (hMPV) is genetically classified into two major subgroups, A and B, based on attachment glycoprotein (G) gene sequences, and the A2 subgroup is further separated into three subdivisions A2a, A2b (A2b1), and A2c (A2b2). The appearance of subgroup A2c viruses carrying a 180-or 111-nucleotide duplication in the G gene (A2c180nt-dup or A2c111nt-dup) have been reported in Japan and Spain. The pandemic of coronavirus disease 2019 (COVID-19) disrupted the epidemiological kinetics of other respiratory viruses, including hMPV. In this study, we analysed the sequences of hMPV isolates obtained from 2017 to 2022 in Tokyo and Fukushima, i.e., before and after COVID-19. Subgroup A hMPVs were detected in 2017 to 2019, and most cases were A2c111nt-dup, suggesting there was continuous momentum of this clade, identical to the global situation. Subgroup B, but not subgroup A, viruses were detected in 2022, after the COVID-19 peak. Phylogenetic analysis showed that these resumed subgroup B viruses were closely related to the viruses detected in 2013 to 2016 in Yokohama and in 2019 in Fukushima, suggesting a reappearance of local endemic viruses in East Japan.

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Epidemiological characteristics of human metapneumovirus among children in Nanjing, China

Min,

Wang,

Dong

et al. 2024

Eur J Clin Microbiol Infect Dis

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Emergence and Potential Extinction of Genetic Lineages of Human Metapneumovirus between 2005 and 2021

Abstract: Human metapneumovirus (HMPV) is one of the major causative agents of human respiratory tract infections. Monitoring of virus evolution could aid toward the development of new antiviral treatments or vaccine designs.

Cited by 10 publications

References 37 publications

Human metapneumovirus infection of organoid-derived human bronchial epithelium represents cell tropism and cytopathology as observed in in vivo models

Human metapneumovirus infection of organoid-derived human bronchial epithelium represents cell tropism and cytopathology as observed in in vivo models

Molecular Epidemiology of Human Metapneumovirus in East Japan before and after COVID-19, 2017–2022

Epidemiological characteristics of human metapneumovirus among children in Nanjing, China

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