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Expression Quantitative Trait Loci for Extreme Host Response to Influenza A in Pre-Collaborative Cross Mice

Daniel Bottomly, Martin T. Ferris, Lauri D. Aicher, Elizabeth Rosenzweig, Alan Whitmore, David L. Aylor, Bart L. Haagmans, Lisa E. Gralinski, Birgit G. Bradel-Tretheway, Janine T. Bryan, David W. Threadgill, Fernando Pardo-Manuel de Villena, Ralph S. Baric, Michael G. Katze, Mark Heise and Shannon K. McWeeney
G3: Genes, Genomes, Genetics February 1, 2012 vol. 2 no. 2 213-221; https://doi.org/10.1534/g3.111.001800
Daniel Bottomly
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Oregon Clinical and Translational Research Institute, Oregon Health & Science University, Portland, Oregon 97239
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Martin T. Ferris
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599
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Lauri D. Aicher
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
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Elizabeth Rosenzweig
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
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Alan Whitmore
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599
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David L. Aylor
Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina, 27514
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Bart L. Haagmans
Erasmus Medical Center, 3000 CA Rotterdam, the Netherlands
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Lisa E. Gralinski
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Epidemiology, University of North Carolina, Chapel Hill, North Carolina, 27599
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Birgit G. Bradel-Tretheway
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
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Janine T. Bryan
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
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David W. Threadgill
Department of Genetics, North Carolina State University, Raleigh, North Carolina, 27695
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Fernando Pardo-Manuel de Villena
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina, 27514
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Ralph S. Baric
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Epidemiology, University of North Carolina, Chapel Hill, North Carolina, 27599Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, North Carolina 27599
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Michael G. Katze
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
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Mark Heise
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, North Carolina 27599
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  • For correspondence: mcweeney@ohsu.eduheisem@med.unc.edu
Shannon K. McWeeney
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Oregon Clinical and Translational Research Institute, Oregon Health & Science University, Portland, Oregon 97239Division of Bioinformatics and Computational Biology, Medical Informatics and Clinical Epidemiology, Oregon Health & Science University, Portland, Oregon 97239Division of Biostatistics, Public Health & Preventative Medicine, Oregon Health & Science University, Portland, Oregon 97239OHSU Knight Cancer Institute, Oregon Health & Science University, Portland, Oregon 97239
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  • For correspondence: mcweeney@ohsu.eduheisem@med.unc.edu
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Abstract

Outbreaks of influenza occur on a yearly basis, causing a wide range of symptoms across the human population. Although evidence exists that the host response to influenza infection is influenced by genetic differences in the host, this has not been studied in a system with genetic diversity mirroring that of the human population. Here we used mice from 44 influenza-infected pre-Collaborative Cross lines determined to have extreme phenotypes with regard to the host response to influenza A virus infection. Global transcriptome profiling identified 2671 transcripts that were significantly differentially expressed between mice that showed a severe (“high”) and mild (“low”) response to infection. Expression quantitative trait loci mapping was performed on those transcripts that were differentially expressed because of differences in host response phenotype to identify putative regulatory regions potentially controlling their expression. Twenty-one significant expression quantitative trait loci were identified, which allowed direct examination of genes associated with regulation of host response to infection. To perform initial validation of our findings, quantitative polymerase chain reaction was performed in the infected founder strains, and we were able to confirm or partially confirm more than 70% of those tested. In addition, we explored putative causal and reactive (downstream) relationships between the significantly regulated genes and others in the high or low response groups using structural equation modeling. By using systems approaches and a genetically diverse population, we were able to develop a novel framework for identifying the underlying biological subnetworks under host genetic control during influenza virus infection.

  • eQTL
  • influenza
  • collaborative cross
  • host response
  • SEM
  • Mouse Collaborative Cross
  • Mouse Genetic Resource
  • Received July 8, 2011.
  • Accepted December 8, 2011.
  • Copyright © 2012 Bottomly et al

This is an open-access article distributed under the terms of the Creative Commons Attribution Unported License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Volume 2 Issue 2, February 2012

G3: Genes|Genomes|Genetics: 2 (2)

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Expression Quantitative Trait Loci for Extreme Host Response to Influenza A in Pre-Collaborative Cross Mice

Daniel Bottomly, Martin T. Ferris, Lauri D. Aicher, Elizabeth Rosenzweig, Alan Whitmore, David L. Aylor, Bart L. Haagmans, Lisa E. Gralinski, Birgit G. Bradel-Tretheway, Janine T. Bryan, David W. Threadgill, Fernando Pardo-Manuel de Villena, Ralph S. Baric, Michael G. Katze, Mark Heise and Shannon K. McWeeney
G3: Genes, Genomes, Genetics February 1, 2012 vol. 2 no. 2 213-221; https://doi.org/10.1534/g3.111.001800
Daniel Bottomly
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Oregon Clinical and Translational Research Institute, Oregon Health & Science University, Portland, Oregon 97239
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Martin T. Ferris
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599
  • Find this author on Google Scholar
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  • Search for this author on this site
Lauri D. Aicher
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
  • Find this author on Google Scholar
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  • Search for this author on this site
Elizabeth Rosenzweig
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
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Alan Whitmore
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599
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David L. Aylor
Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina, 27514
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Bart L. Haagmans
Erasmus Medical Center, 3000 CA Rotterdam, the Netherlands
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Lisa E. Gralinski
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Epidemiology, University of North Carolina, Chapel Hill, North Carolina, 27599
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  • Find this author on PubMed
  • Search for this author on this site
Birgit G. Bradel-Tretheway
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Janine T. Bryan
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
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David W. Threadgill
Department of Genetics, North Carolina State University, Raleigh, North Carolina, 27695
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Fernando Pardo-Manuel de Villena
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina, 27514
  • Find this author on Google Scholar
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  • Search for this author on this site
Ralph S. Baric
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Epidemiology, University of North Carolina, Chapel Hill, North Carolina, 27599Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, North Carolina 27599
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Michael G. Katze
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
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Mark Heise
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, North Carolina 27599
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  • For correspondence: mcweeney@ohsu.eduheisem@med.unc.edu
Shannon K. McWeeney
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Oregon Clinical and Translational Research Institute, Oregon Health & Science University, Portland, Oregon 97239Division of Bioinformatics and Computational Biology, Medical Informatics and Clinical Epidemiology, Oregon Health & Science University, Portland, Oregon 97239Division of Biostatistics, Public Health & Preventative Medicine, Oregon Health & Science University, Portland, Oregon 97239OHSU Knight Cancer Institute, Oregon Health & Science University, Portland, Oregon 97239
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  • For correspondence: mcweeney@ohsu.eduheisem@med.unc.edu
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Citation

Expression Quantitative Trait Loci for Extreme Host Response to Influenza A in Pre-Collaborative Cross Mice

Daniel Bottomly, Martin T. Ferris, Lauri D. Aicher, Elizabeth Rosenzweig, Alan Whitmore, David L. Aylor, Bart L. Haagmans, Lisa E. Gralinski, Birgit G. Bradel-Tretheway, Janine T. Bryan, David W. Threadgill, Fernando Pardo-Manuel de Villena, Ralph S. Baric, Michael G. Katze, Mark Heise and Shannon K. McWeeney
G3: Genes, Genomes, Genetics February 1, 2012 vol. 2 no. 2 213-221; https://doi.org/10.1534/g3.111.001800
Daniel Bottomly
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Oregon Clinical and Translational Research Institute, Oregon Health & Science University, Portland, Oregon 97239
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Martin T. Ferris
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Lauri D. Aicher
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Elizabeth Rosenzweig
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Alan Whitmore
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
David L. Aylor
Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina, 27514
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Bart L. Haagmans
Erasmus Medical Center, 3000 CA Rotterdam, the Netherlands
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Lisa E. Gralinski
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Epidemiology, University of North Carolina, Chapel Hill, North Carolina, 27599
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Birgit G. Bradel-Tretheway
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Janine T. Bryan
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
David W. Threadgill
Department of Genetics, North Carolina State University, Raleigh, North Carolina, 27695
  • Find this author on Google Scholar
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  • Search for this author on this site
Fernando Pardo-Manuel de Villena
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina, 27514
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ralph S. Baric
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Epidemiology, University of North Carolina, Chapel Hill, North Carolina, 27599Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, North Carolina 27599
  • Find this author on Google Scholar
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  • Search for this author on this site
Michael G. Katze
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Microbiology, School of Medicine, University of Washington, Seattle, Washington, 98195
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  • Search for this author on this site
Mark Heise
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, North Carolina 27599
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  • For correspondence: mcweeney@ohsu.eduheisem@med.unc.edu
Shannon K. McWeeney
Pacific Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research, Portland, Oregon 97006Oregon Clinical and Translational Research Institute, Oregon Health & Science University, Portland, Oregon 97239Division of Bioinformatics and Computational Biology, Medical Informatics and Clinical Epidemiology, Oregon Health & Science University, Portland, Oregon 97239Division of Biostatistics, Public Health & Preventative Medicine, Oregon Health & Science University, Portland, Oregon 97239OHSU Knight Cancer Institute, Oregon Health & Science University, Portland, Oregon 97239
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  • For correspondence: mcweeney@ohsu.eduheisem@med.unc.edu

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