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The dynamic proteome of influenza A virus infection identifies M segment splicing as a host range determinant

Boris Bogdanow, Katrin Eichelbaum, Anne Sadewasser, Xi Wang, Immanuel Husic, Katharina Paki, Martha Hergeselle, Barbara Vetter, Jingyi Hou, Wei Chen, Lüder Wiebusch, Irmtraud M. Meyer, Thorsten Wolff, Matthias Selbach
doi: https://doi.org/10.1101/438176
Boris Bogdanow
Max Delbrück Center for Molecular Medicine, Robert-Rössle-Str. 10, 13125 BerlinUnit 17 “Influenza and other Respiratory Viruses”, Robert Koch Institut, Seestr. 10, 13353 Berlin, Germany
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Katrin Eichelbaum
Max Delbrück Center for Molecular Medicine, Robert-Rössle-Str. 10, 13125 Berlin
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Anne Sadewasser
Unit 17 “Influenza and other Respiratory Viruses”, Robert Koch Institut, Seestr. 10, 13353 Berlin, Germany
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Xi Wang
Max Delbrück Center for Molecular Medicine, Robert-Rössle-Str. 10, 13125 BerlinDivision of Theoretical Systems Biology, German Cancer Research Center, 69120 Heidelberg, Germany
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Immanuel Husic
Max Delbrück Center for Molecular Medicine, Robert-Rössle-Str. 10, 13125 Berlin
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Katharina Paki
Unit 17 “Influenza and other Respiratory Viruses”, Robert Koch Institut, Seestr. 10, 13353 Berlin, Germany
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Martha Hergeselle
Max Delbrück Center for Molecular Medicine, Robert-Rössle-Str. 10, 13125 Berlin
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Barbara Vetter
Labor für Pädiatrische Molekularbiologie, Charité Universitätsmedizin Berlin, Augustenburger Platz 1, 13353 Berlin, Germany
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Jingyi Hou
Max Delbrück Center for Molecular Medicine, Robert-Rössle-Str. 10, 13125 Berlin
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Wei Chen
Max Delbrück Center for Molecular Medicine, Robert-Rössle-Str. 10, 13125 BerlinDepartment of Biology, Southern University of Science and Technology, Xuanyuan Rd. 1088, 518055 Shenzhen, China
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Lüder Wiebusch
Labor für Pädiatrische Molekularbiologie, Charité Universitätsmedizin Berlin, Augustenburger Platz 1, 13353 Berlin, Germany
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Irmtraud M. Meyer
Max Delbrück Center for Molecular Medicine, Robert-Rössle-Str. 10, 13125 Berlin
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Thorsten Wolff
Unit 17 “Influenza and other Respiratory Viruses”, Robert Koch Institut, Seestr. 10, 13353 Berlin, Germany
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Matthias Selbach
Max Delbrück Center for Molecular Medicine, Robert-Rössle-Str. 10, 13125 BerlinCharité Universitätsmedizin Berlin, 10117 Berlin, Germany
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SUMMARY

A century ago, influenza A virus (IAV) infection caused the 1918 flu pandemic and killed an estimated 20-40 million people. Pandemic IAV outbreaks occur when strains from animal reservoirs acquire the ability to infect and spread among humans. The molecular details of this species barrier are incompletely understood. We combined metabolic pulse labeling and quantitative shotgun proteomics to globally monitor protein synthesis upon infection of human cells with a human-and a bird-adapted IAV strain. While production of host proteins was remarkably similar, we observed striking differences in the kinetics of viral protein synthesis over the course of infection. Most importantly, the matrix protein M1 was inefficiently produced by the bird-adapted strain at later stages. We show that impaired production of M1 from bird-adapted strains is caused by increased splicing of the M segment RNA to alternative isoforms. Experiments with reporter constructs and recombinant influenza viruses revealed that strain-specific M segment splicing is controlled by the 3’ splice site and functionally important for permissive infection. Independent in silico evidence shows that avian-adapted M segments have evolved different conserved RNA structure features than human-adapted sequences. Thus, our data identifies M segment RNA splicing as a viral determinant of host range.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted October 08, 2018.
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The dynamic proteome of influenza A virus infection identifies M segment splicing as a host range determinant
Boris Bogdanow, Katrin Eichelbaum, Anne Sadewasser, Xi Wang, Immanuel Husic, Katharina Paki, Martha Hergeselle, Barbara Vetter, Jingyi Hou, Wei Chen, Lüder Wiebusch, Irmtraud M. Meyer, Thorsten Wolff, Matthias Selbach
bioRxiv 438176; doi: https://doi.org/10.1101/438176
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The dynamic proteome of influenza A virus infection identifies M segment splicing as a host range determinant
Boris Bogdanow, Katrin Eichelbaum, Anne Sadewasser, Xi Wang, Immanuel Husic, Katharina Paki, Martha Hergeselle, Barbara Vetter, Jingyi Hou, Wei Chen, Lüder Wiebusch, Irmtraud M. Meyer, Thorsten Wolff, Matthias Selbach
bioRxiv 438176; doi: https://doi.org/10.1101/438176

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