The Influenza A Virus Endoribonuclease PA-X Usurps Host mRNA Processing Machinery to Limit Host Gene Expression
Abstract
Often, many viruses shut off host gene expression to inhibit antiviral responses. Viral proteins and host proteins required for viral replication are typically spared in this process, yet the mechanisms of target selectivity during host shutoff remain poorly understood. Using transcriptome-wide and targeted reporter experiments, we demonstrate that the influenza A virus endoribonuclease PA-X usurps RNA splicing to selectively target host RNAs for destruction. Proximity-labeling proteomics reveals that PA-X interacts with cellular RNA processing proteins, some of which are partially required for host shutoff. Thus, PA-X taps into host nuclear pre-mRNA processing mechanisms to destroy nascent mRNAs shortly after their synthesis. This mechanism sets PA-X apart from other viral host shutoff proteins that target actively translating mRNAs in the cytoplasm. Our study reveals a unique mechanism of host shutoff that helps us understand how influenza viruses suppress host gene expression.
- Authors:
-
- Tufts Univ., Boston, MA (United States). Sackler School of Graduate Biomedical Sciences; Tufts Univ. School of Medicine, Boston, MA (United States). Dept. of Molecular Biology and Microbiology
- Dalhousie Univ., Halifax, NS (Canada). Dept. of Microbiology & Immunology
- Tufts Univ. School of Medicine, Boston, MA (United States). Dept. of Molecular Biology and Microbiology
- Harvard Univ., Cambridge, MA (United States). Paulson School of Engineering and Applied Sciences; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Computational Research Division
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Advanced Scientific Computing Research (ASCR); National Institutes of Health (NIH); Canadian Institutes for Health
- OSTI Identifier:
- 1542393
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Cell Reports
- Additional Journal Information:
- Journal Volume: 27; Journal Issue: 3; Journal ID: ISSN 2211-1247
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; influenza; host shutoff; PA-X; splicing; CFIm
Citation Formats
Gaucherand, Lea, Porter, Brittany K., Levene, Rachel E., Price, Emma L., Schmaling, Summer K., Rycroft, Chris H., Kevorkian, Yuzo, McCormick, Craig, Khaperskyy, Denys A., and Gaglia, Marta M. The Influenza A Virus Endoribonuclease PA-X Usurps Host mRNA Processing Machinery to Limit Host Gene Expression. United States: N. p., 2019.
Web. doi:10.1016/j.celrep.2019.03.063.
Gaucherand, Lea, Porter, Brittany K., Levene, Rachel E., Price, Emma L., Schmaling, Summer K., Rycroft, Chris H., Kevorkian, Yuzo, McCormick, Craig, Khaperskyy, Denys A., & Gaglia, Marta M. The Influenza A Virus Endoribonuclease PA-X Usurps Host mRNA Processing Machinery to Limit Host Gene Expression. United States. https://doi.org/10.1016/j.celrep.2019.03.063
Gaucherand, Lea, Porter, Brittany K., Levene, Rachel E., Price, Emma L., Schmaling, Summer K., Rycroft, Chris H., Kevorkian, Yuzo, McCormick, Craig, Khaperskyy, Denys A., and Gaglia, Marta M. Tue .
"The Influenza A Virus Endoribonuclease PA-X Usurps Host mRNA Processing Machinery to Limit Host Gene Expression". United States. https://doi.org/10.1016/j.celrep.2019.03.063. https://www.osti.gov/servlets/purl/1542393.
@article{osti_1542393,
title = {The Influenza A Virus Endoribonuclease PA-X Usurps Host mRNA Processing Machinery to Limit Host Gene Expression},
author = {Gaucherand, Lea and Porter, Brittany K. and Levene, Rachel E. and Price, Emma L. and Schmaling, Summer K. and Rycroft, Chris H. and Kevorkian, Yuzo and McCormick, Craig and Khaperskyy, Denys A. and Gaglia, Marta M.},
abstractNote = {Often, many viruses shut off host gene expression to inhibit antiviral responses. Viral proteins and host proteins required for viral replication are typically spared in this process, yet the mechanisms of target selectivity during host shutoff remain poorly understood. Using transcriptome-wide and targeted reporter experiments, we demonstrate that the influenza A virus endoribonuclease PA-X usurps RNA splicing to selectively target host RNAs for destruction. Proximity-labeling proteomics reveals that PA-X interacts with cellular RNA processing proteins, some of which are partially required for host shutoff. Thus, PA-X taps into host nuclear pre-mRNA processing mechanisms to destroy nascent mRNAs shortly after their synthesis. This mechanism sets PA-X apart from other viral host shutoff proteins that target actively translating mRNAs in the cytoplasm. Our study reveals a unique mechanism of host shutoff that helps us understand how influenza viruses suppress host gene expression.},
doi = {10.1016/j.celrep.2019.03.063},
journal = {Cell Reports},
number = 3,
volume = 27,
place = {United States},
year = {Tue Apr 16 00:00:00 EDT 2019},
month = {Tue Apr 16 00:00:00 EDT 2019}
}
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