Mutations conferring increased sensitivity to tripartite motif 22 restriction accumulated progressively in the nucleoprotein of seasonal influenza A (H1N1) viruses between 1918 and 2009

I Pagani, Andrea Di Pietro, A Oteiz, M Ghitti, N Mechti, N Naffakh, E Vicenzi

Research output: Contribution to journalArticle

Abstract

Influenza A viruses (IAVs) can cause zoonotic infections with pandemic potential when most of the human population is immunologically naive. After a pandemic, IAVs evolve to become seasonal in the human host by acquiring adaptive mutations. We have previously reported that the interferon (IFN)-inducible tripartite motif 22 (TRIM22) protein restricts the replication of seasonal IAVs by direct interaction with the viral nucleoprotein (NP), leading to its polyubiquitination and proteasomal degradation. Here we show that, in contrast to seasonal H1N1 IAVs, the 2009 pandemic H1N1 strain as well as H1N1 strains from the 1930s are resistant to TRIM22 restriction. We demonstrate that arginine-to-lysine substitutions conferring an increased sensitivity to TRIM22-dependent ubiquitination accumulated progressively in the NP of seasonal influenza A (H1N1) viruses between 1918 and 2009. Our findings suggest that during long-term circulation and evolution of IAVs in humans, adaptive mutations are favored at the expense of an increased sensitivity to some components of the innate immune response. © 2018 Pagani et al.
Original languageEnglish
Article numbere00110-18
JournalmSphere
Volume3
Issue number2
DOIs
Publication statusPublished - 2018

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H1N1 Subtype Influenza A Virus
Nucleoproteins
Influenza A virus
Mutation
Pandemics
Ubiquitination
Zoonoses
Innate Immunity
Interferons
Lysine
Arginine
Population

Cite this

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title = "Mutations conferring increased sensitivity to tripartite motif 22 restriction accumulated progressively in the nucleoprotein of seasonal influenza A (H1N1) viruses between 1918 and 2009",
abstract = "Influenza A viruses (IAVs) can cause zoonotic infections with pandemic potential when most of the human population is immunologically naive. After a pandemic, IAVs evolve to become seasonal in the human host by acquiring adaptive mutations. We have previously reported that the interferon (IFN)-inducible tripartite motif 22 (TRIM22) protein restricts the replication of seasonal IAVs by direct interaction with the viral nucleoprotein (NP), leading to its polyubiquitination and proteasomal degradation. Here we show that, in contrast to seasonal H1N1 IAVs, the 2009 pandemic H1N1 strain as well as H1N1 strains from the 1930s are resistant to TRIM22 restriction. We demonstrate that arginine-to-lysine substitutions conferring an increased sensitivity to TRIM22-dependent ubiquitination accumulated progressively in the NP of seasonal influenza A (H1N1) viruses between 1918 and 2009. Our findings suggest that during long-term circulation and evolution of IAVs in humans, adaptive mutations are favored at the expense of an increased sensitivity to some components of the innate immune response. {\circledC} 2018 Pagani et al.",
author = "I Pagani and {Di Pietro}, Andrea and A Oteiz and M Ghitti and N Mechti and N Naffakh and E Vicenzi",
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language = "English",
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journal = "mSphere",
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publisher = "American Society for Microbiology",
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TY - JOUR

T1 - Mutations conferring increased sensitivity to tripartite motif 22 restriction accumulated progressively in the nucleoprotein of seasonal influenza A (H1N1) viruses between 1918 and 2009

AU - Pagani, I

AU - Di Pietro, Andrea

AU - Oteiz, A

AU - Ghitti, M

AU - Mechti, N

AU - Naffakh, N

AU - Vicenzi, E

PY - 2018

Y1 - 2018

N2 - Influenza A viruses (IAVs) can cause zoonotic infections with pandemic potential when most of the human population is immunologically naive. After a pandemic, IAVs evolve to become seasonal in the human host by acquiring adaptive mutations. We have previously reported that the interferon (IFN)-inducible tripartite motif 22 (TRIM22) protein restricts the replication of seasonal IAVs by direct interaction with the viral nucleoprotein (NP), leading to its polyubiquitination and proteasomal degradation. Here we show that, in contrast to seasonal H1N1 IAVs, the 2009 pandemic H1N1 strain as well as H1N1 strains from the 1930s are resistant to TRIM22 restriction. We demonstrate that arginine-to-lysine substitutions conferring an increased sensitivity to TRIM22-dependent ubiquitination accumulated progressively in the NP of seasonal influenza A (H1N1) viruses between 1918 and 2009. Our findings suggest that during long-term circulation and evolution of IAVs in humans, adaptive mutations are favored at the expense of an increased sensitivity to some components of the innate immune response. © 2018 Pagani et al.

AB - Influenza A viruses (IAVs) can cause zoonotic infections with pandemic potential when most of the human population is immunologically naive. After a pandemic, IAVs evolve to become seasonal in the human host by acquiring adaptive mutations. We have previously reported that the interferon (IFN)-inducible tripartite motif 22 (TRIM22) protein restricts the replication of seasonal IAVs by direct interaction with the viral nucleoprotein (NP), leading to its polyubiquitination and proteasomal degradation. Here we show that, in contrast to seasonal H1N1 IAVs, the 2009 pandemic H1N1 strain as well as H1N1 strains from the 1930s are resistant to TRIM22 restriction. We demonstrate that arginine-to-lysine substitutions conferring an increased sensitivity to TRIM22-dependent ubiquitination accumulated progressively in the NP of seasonal influenza A (H1N1) viruses between 1918 and 2009. Our findings suggest that during long-term circulation and evolution of IAVs in humans, adaptive mutations are favored at the expense of an increased sensitivity to some components of the innate immune response. © 2018 Pagani et al.

U2 - 10.1128/mSphere.00110-18

DO - 10.1128/mSphere.00110-18

M3 - Article

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JO - mSphere

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