Kinetics of Coinfection with Influenza A Virus and Streptococcus pneumoniae
Abstract
Secondary bacterial infections are a leading cause of illness and death during epidemic and pandemic influenza. Experimental studies suggest a lethal synergism between influenza and certain bacteria, particularly Streptococcus pneumoniae, but the precise processes involved are unclear. In this paper, to address the mechanisms and determine the influences of pathogen dose and strain on disease, we infected groups of mice with either the H1N1 subtype influenza A virus A/Puerto Rico/8/34 (PR8) or a version expressing the 1918 PB1-F2 protein (PR8-PB1-F2(1918)), followed seven days later with one of two S. pneumoniae strains, type 2 D39 or type 3 A66.1. We determined that, following bacterial infection, viral titers initially rebound and then decline slowly. Bacterial titers rapidly rise to high levels and remain elevated. We used a kinetic model to explore the coupled interactions and study the dominant controlling mechanisms. We hypothesize that viral titers rebound in the presence of bacteria due to enhanced viral release from infected cells, and that bacterial titers increase due to alveolar macrophage impairment. Dynamics are affected by initial bacterial dose but not by the expression of the influenza 1918 PB1-F2 protein. Finally, our model provides a framework to investigate pathogen interaction during coinfections and to uncovermore »
- Authors:
-
- St. Jude Children's Research Hospital, Memphis, TN (United States). Dept. of Infectious Diseases
- Univ. of Utah, Salt Lake City, UT (United States). Dept. of Mathematics. Dept. of Biology
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Biology and Biophysics; Univ. of Lisbon (Portugal). School of Medicine. Inst. of Molecular Medicine
- Univ. of Arizona, Tucson, AZ (United States). Dept. of Molecular and Cellular Biology
- Univ. of Melbourne (Australia). Dept. of Immunology and Microbiology
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Biology and Biophysics
- Publication Date:
- Research Org.:
- Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
- Sponsoring Org.:
- USDOE; National Inst. of Health (NIH) (United States); National Science Foundation (NSF); James S. McDonnell Foundation (United States); Foundation for Science and Technology (FCT) (Portugal)
- Contributing Org.:
- St. Jude Children's Research Hospital, Memphis, TN (United States); Univ. of Utah, Salt Lake City, UT (United States); Univ. of Arizona, Tucson, AZ (United States); Univ. of Melbourne (Australia)
- OSTI Identifier:
- 1321716
- Report Number(s):
- LA-UR-12-21471
Journal ID: ISSN 1553-7374
- Grant/Contract Number:
- AC52-06NA25396; HHSN272201000055C; OD011095; AI028433; AI100946; P20-GM103452; DMS-0354259; PCOFUND-GA-2009-246542
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Pathogens
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 3; Journal ID: ISSN 1553-7374
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; biological science; influenza; co-infections; pneumococcus; alveolar macrophages; bacterial diseases; influenza A virus; influenza viruses; bacterial pathogens
Citation Formats
Smith, Amber M., Adler, Frederick R., Ribeiro, Ruy M., Gutenkunst, Ryan N., McAuley, Julie L., McCullers, Jonathan A., and Perelson, Alan S. Kinetics of Coinfection with Influenza A Virus and Streptococcus pneumoniae. United States: N. p., 2013.
Web. doi:10.1371/journal.ppat.1003238.
Smith, Amber M., Adler, Frederick R., Ribeiro, Ruy M., Gutenkunst, Ryan N., McAuley, Julie L., McCullers, Jonathan A., & Perelson, Alan S. Kinetics of Coinfection with Influenza A Virus and Streptococcus pneumoniae. United States. https://doi.org/10.1371/journal.ppat.1003238
Smith, Amber M., Adler, Frederick R., Ribeiro, Ruy M., Gutenkunst, Ryan N., McAuley, Julie L., McCullers, Jonathan A., and Perelson, Alan S. Thu .
"Kinetics of Coinfection with Influenza A Virus and Streptococcus pneumoniae". United States. https://doi.org/10.1371/journal.ppat.1003238. https://www.osti.gov/servlets/purl/1321716.
@article{osti_1321716,
title = {Kinetics of Coinfection with Influenza A Virus and Streptococcus pneumoniae},
author = {Smith, Amber M. and Adler, Frederick R. and Ribeiro, Ruy M. and Gutenkunst, Ryan N. and McAuley, Julie L. and McCullers, Jonathan A. and Perelson, Alan S.},
abstractNote = {Secondary bacterial infections are a leading cause of illness and death during epidemic and pandemic influenza. Experimental studies suggest a lethal synergism between influenza and certain bacteria, particularly Streptococcus pneumoniae, but the precise processes involved are unclear. In this paper, to address the mechanisms and determine the influences of pathogen dose and strain on disease, we infected groups of mice with either the H1N1 subtype influenza A virus A/Puerto Rico/8/34 (PR8) or a version expressing the 1918 PB1-F2 protein (PR8-PB1-F2(1918)), followed seven days later with one of two S. pneumoniae strains, type 2 D39 or type 3 A66.1. We determined that, following bacterial infection, viral titers initially rebound and then decline slowly. Bacterial titers rapidly rise to high levels and remain elevated. We used a kinetic model to explore the coupled interactions and study the dominant controlling mechanisms. We hypothesize that viral titers rebound in the presence of bacteria due to enhanced viral release from infected cells, and that bacterial titers increase due to alveolar macrophage impairment. Dynamics are affected by initial bacterial dose but not by the expression of the influenza 1918 PB1-F2 protein. Finally, our model provides a framework to investigate pathogen interaction during coinfections and to uncover dynamical differences based on inoculum size and strain.},
doi = {10.1371/journal.ppat.1003238},
journal = {PLoS Pathogens},
number = 3,
volume = 9,
place = {United States},
year = {Thu Mar 21 00:00:00 EDT 2013},
month = {Thu Mar 21 00:00:00 EDT 2013}
}
Web of Science
Works referenced in this record:
Host Cellular Immune Response to Pneumococcal Lung Infection in Mice
journal, April 2000
- Kadioglu, Aras; Gingles, Neill A.; Grattan, Kate
- Infection and Immunity, Vol. 68, Issue 4
Effect of 1918 PB1-F2 Expression on Influenza A Virus Infection Kinetics
journal, February 2011
- Smith, Amber M.; Adler, Frederick R.; McAuley, Julie L.
- PLoS Computational Biology, Vol. 7, Issue 2
Expression of the 1918 Influenza A Virus PB1-F2 Enhances the Pathogenesis of Viral and Secondary Bacterial Pneumonia
journal, October 2007
- McAuley, Julie L.; Hornung, Felicita; Boyd, Kelli L.
- Cell Host & Microbe, Vol. 2, Issue 4
Mathematical model of a three-stage innate immune response to a pneumococcal lung infection
journal, May 2011
- Smith, Amber M.; McCullers, Jonathan A.; Adler, Frederick R.
- Journal of Theoretical Biology, Vol. 276, Issue 1
Respiratory viruses predisposing to bacterial infections: role of neuraminidase
journal, January 2004
- Peltola, Ville T.; Mccullers, Jonathan A.
- The Pediatric Infectious Disease Journal, Vol. 23, Issue Supplement
Inhibition of pulmonary antibacterial defense by interferon-γ during recovery from influenza infection
journal, April 2008
- Sun, Keer; Metzger, Dennis W.
- Nature Medicine, Vol. 14, Issue 5
Role of Chemokines and Formyl Peptides in Pneumococcal Pneumonia-Induced Monocyte/Macrophage Recruitment
journal, June 2001
- Fillion, Isabelle; Ouellet, Nathalie; Simard, Marie
- The Journal of Immunology, Vol. 166, Issue 12
Influenza A Inhibits Th17-Mediated Host Defense against Bacterial Pneumonia in Mice
journal, December 2010
- Kudva, Anupa; Scheller, Erich V.; Robinson, Keven M.
- The Journal of Immunology, Vol. 186, Issue 3
Influenza virus neuraminidase inhibitors
journal, March 2000
- Gubareva, Larisa V.; Kaiser, Laurent; Hayden, Frederick G.
- The Lancet, Vol. 355, Issue 9206
Modeling the Viral Dynamics of Influenza A Virus Infection
journal, January 2010
- Smith, Amber M.; Ribeiro, Ruy M.
- Critical Reviews™ in Immunology, Vol. 30, Issue 3
Commensal Bacteria Calibrate the Activation Threshold of Innate Antiviral Immunity
journal, July 2012
- Abt, Michael C.; Osborne, Lisa C.; Monticelli, Laurel A.
- Immunity, Vol. 37, Issue 1
Influenza Infection Leads to Increased Susceptibility to Subsequent Bacterial Superinfection by Impairing NK Cell Responses in the Lung
journal, January 2010
- Small, Cherrie-Lee; Shaler, Christopher R.; McCormick, Sarah
- The Journal of Immunology, Vol. 184, Issue 4
Immunokinetics in severe pneumonia due to influenza virus and bacteria coinfection in mice
journal, July 2004
- Seki, M.; Yanagihara, K.; Higashiyama, Y.
- European Respiratory Journal, Vol. 24, Issue 1
Sustained desensitization to bacterial Toll-like receptor ligands after resolutionof respiratory influenza infection
journal, January 2008
- Didierlaurent, Arnaud; Goulding, John; Patel, Seema
- The Journal of Experimental Medicine, Vol. 205, Issue 2
Statistical mechanical approaches to models with many poorly known parameters
journal, August 2003
- Brown, Kevin S.; Sethna, James P.
- Physical Review E, Vol. 68, Issue 2
Influenza A Virus Protein PB1-F2 Exacerbates IFN-β Expression of Human Respiratory Epithelial Cells
journal, September 2010
- Le Goffic, Ronan; Bouguyon, Edwige; Chevalier, Christophe
- The Journal of Immunology, Vol. 185, Issue 8
Phagocytosis and Killing of Common Bacterial Pathogens of the Lung by Human Alveolar Macrophages
journal, July 1985
- Jonsson, S.; Musher, D. M.; Chapman, A.
- Journal of Infectious Diseases, Vol. 152, Issue 1
Lethal Synergism between Influenza Virus and Streptococcus pneumoniae: Characterization of a Mouse Model and the Role of Platelet‐Activating Factor Receptor
journal, August 2002
- McCullers, Jonathan A.; Rehg, Jerold E.
- The Journal of Infectious Diseases, Vol. 186, Issue 3
Influenza Virus Neuraminidase Contributes to Secondary Bacterial Pneumonia
journal, July 2005
- Peltola, Ville T.; Murti, K. Gopal; McCullers, Jonathan A.
- The Journal of Infectious Diseases, Vol. 192, Issue 2
Kinetics of Influenza A Virus Infection in Humans
journal, July 2006
- Baccam, P.; Beauchemin, C.; Macken, C. A.
- Journal of Virology, Vol. 80, Issue 15
A Single N66S Mutation in the PB1-F2 Protein of Influenza A Virus Increases Virulence by Inhibiting the Early Interferon Response In Vivo
journal, November 2010
- Conenello, G. M.; Tisoncik, J. R.; Rosenzweig, E.
- Journal of Virology, Vol. 85, Issue 2
Influenza A virus infection kinetics: quantitative data and models: Modeling influenza kinetics
journal, December 2010
- Smith, Amber M.; Perelson, Alan S.
- Wiley Interdisciplinary Reviews: Systems Biology and Medicine, Vol. 3, Issue 4
Regression and time series model selection in small samples
journal, January 1989
- Hurvich, Clifford M.; Tsai, Chih-Ling
- Biometrika, Vol. 76, Issue 2
Binding of bacteria to HEp-2 cells infected with influenza A virus
journal, April 1999
- El Ahmer, O.
- FEMS Immunology and Medical Microbiology, Vol. 23, Issue 4
Predominant Role of Bacterial Pneumonia as a Cause of Death in Pandemic Influenza: Implications for Pandemic Influenza Preparedness
journal, October 2008
- Morens, David M.; Taubenberger, Jeffery K.; Fauci, Anthony S.
- The Journal of Infectious Diseases, Vol. 198, Issue 7
Influenza A Virus Accelerates Neutrophil Apoptosis and Markedly Potentiates Apoptotic Effects of Bacteria
journal, April 1999
- Colamussi, Maria Luisa; White, Mitchell R.; Crouch, Erika
- Blood, Vol. 93, Issue 7
IL-10 Is an Important Mediator of the Enhanced Susceptibility to Pneumococcal Pneumonia after Influenza Infection
journal, June 2004
- van der Sluijs, Koenraad F.; van Elden, Leontine J. R.; Nijhuis, Monique
- The Journal of Immunology, Vol. 172, Issue 12
A novel influenza A virus mitochondrial protein that induces cell death
journal, December 2001
- Chen, Weisan; Calvo, Paul A.; Malide, Daniela
- Nature Medicine, Vol. 7, Issue 12
Influenza Virus-Induced Glucocorticoids Compromise Innate Host Defense against a Secondary Bacterial Infection
journal, February 2010
- Jamieson, Amanda M.; Yu, Shuang; Annicelli, Charles H.
- Cell Host & Microbe, Vol. 7, Issue 2
Successive influenza virus infection and Streptococcus pneumoniae stimulation alter human dendritic cell function
journal, July 2011
- Wu, Yuet; Mao, Huawei; Ling, Man-To
- BMC Infectious Diseases, Vol. 11, Issue 1
The impact of successive infections on the lung microenvironment
journal, December 2007
- Didierlaurent, Arnaud; Goulding, John; Hussell, Tracy
- Immunology, Vol. 122, Issue 4
Combined Infections in mice with Influenza Virus and Diplococcus Pneumoniae
journal, November 1957
- Gerone, Peter J.; Ward, Thomas G.; Chappal, W. Adrian
- American Journal of Epidemiology, Vol. 66, Issue 3
Influenza A virus facilitates Streptococcus pneumoniae transmission and disease
journal, June 2010
- Diavatopoulos, Dimitri A.; Short, Kirsty R.; Price, John T.
- The FASEB Journal, Vol. 24, Issue 6
Impact of the 2009 Influenza Pandemic on Pneumococcal Pneumonia Hospitalizations in the United States
journal, December 2011
- Weinberger, Daniel M.; Simonsen, Lone; Jordan, Richard
- The Journal of Infectious Diseases, Vol. 205, Issue 3
Lethal synergism induced in mice by influenza type A virus and type Ia group B streptococci
journal, August 1983
- Jones, W. T.; Menna, J. H.; Wennerstrom, D. E.
- Infection and Immunity, Vol. 41, Issue 2
Improving therapeutic strategies for secondary bacterial pneumonia following influenza
journal, August 2008
- McCullers, Jonathan A.; English, B. Keith
- Future Microbiology, Vol. 3, Issue 4
Herbaceous perennial plants with short generation time have stronger responses to climate anomalies than those with longer generation time
journal, March 2021
- Compagnoni, Aldo; Levin, Sam; Childs, Dylan Z.
- Nature Communications, Vol. 12, Issue 1
Pulmonary and Systemic Defenses against Challenge with Staphylococcus aureus in Mice with Pneumonia Due to Influenza A Virus
journal, July 1979
- Jakab, G. J.; Warr, G. A.; Knight, M. E.
- Journal of Infectious Diseases, Vol. 140, Issue 1
Influenza Virus Infection Decreases Tracheal Mucociliary Velocity and Clearance of Streptococcus pneumoniae
journal, April 2010
- Pittet, Lynnelle A.; Hall-Stoodley, Luanne; Rutkowski, Melanie R.
- American Journal of Respiratory Cell and Molecular Biology, Vol. 42, Issue 4
Influenza Enhances Susceptibility to Natural Acquisition of and Disease due to Streptococcus pneumoniae in Ferrets
journal, October 2010
- McCullers, Jonathan A.; McAuley, Julie L.; Browall, Sarah
- The Journal of Infectious Diseases, Vol. 202, Issue 8
Microbiota regulates immune defense against respiratory tract influenza A virus infection
journal, March 2011
- Ichinohe, T.; Pang, I. K.; Kumamoto, Y.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 13
Influenza Virus PB1-F2 Protein Induces Cell Death through Mitochondrial ANT3 and VDAC1
journal, January 2005
- Zamarin, Dmitriy; García-Sastre, Adolfo; Xiao, Xiaoyao
- PLoS Pathogens, Vol. 1, Issue 1
Increased susceptibility to bacterial superinfection as a consequence of innate antiviral responses
journal, October 2006
- Navarini, A. A.; Recher, M.; Lang, K. S.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 42
Critically Ill Patients With 2009 Influenza A(H1N1) in Mexico
journal, November 2009
- Domínguez-Cherit, Guillermo
- JAMA, Vol. 302, Issue 17
An accurate two-phase approximate solution to an acute viral infection model
journal, July 2009
- Smith, Amber M.; Adler, Frederick R.; Perelson, Alan S.
- Journal of Mathematical Biology, Vol. 60, Issue 5
Influenza Virus Primes Mice for Pneumonia From Staphylococcus aureus
journal, March 2011
- Iverson, Amy R.; Boyd, Kelli L.; McAuley, Julie L.
- The Journal of Infectious Diseases, Vol. 203, Issue 6
PB1-F2 Proteins from H5N1 and 20th Century Pandemic Influenza Viruses Cause Immunopathology
journal, July 2010
- McAuley, Julie L.; Chipuk, Jerry E.; Boyd, Kelli L.
- PLoS Pathogens, Vol. 6, Issue 7
Bordetella pertussis Infection Exacerbates Influenza Virus Infection through Pertussis Toxin-Mediated Suppression of Innate Immunity
journal, April 2011
- Ayala, Victor I.; Teijaro, John R.; Farber, Donna L.
- PLoS ONE, Vol. 6, Issue 4
Inhibitory effects of aprotinin on influenza A and B viruses in vitro and in vivo
journal, May 2021
- Song, Eun-Jung; Españo, Erica; Shim, Sang-Mu
- Scientific Reports, Vol. 11, Issue 1
A review of mathematical models of influenza A infections within a host or cell culture: lessons learned and challenges ahead
journal, January 2011
- Beauchemin, Catherine AA; Handel, Andreas
- BMC Public Health, Vol. 11, Issue Suppl 1
Naturally Occurring Swine Influenza A Virus PB1-F2 Phenotypes That Contribute to Superinfection with Gram-Positive Respiratory Pathogens
journal, June 2012
- Weeks-Gorospe, J. N.; Hurtig, H. R.; Iverson, A. R.
- Journal of Virology, Vol. 86, Issue 17
Hospitalized Patients with 2009 H1N1 Influenza in the United States, April–June 2009
journal, November 2009
- Jain, Seema; Kamimoto, Laurie; Bramley, Anna M.
- New England Journal of Medicine, Vol. 361, Issue 20
Effect of Neuraminidase on Receptor-mediated Adherence of Streptococcus pneumoniae to Chinchilla Tracheal Epithelium
journal, January 2002
- Tong, Hua Hua; Liu, Xia; Chen, Yiping
- Acta Oto-Laryngologica, Vol. 122, Issue 4
A Simple Method of Estimating Fifty per cent Endpoints12
journal, May 1938
- Reed, L. J.; Muench, H.
- American Journal of Epidemiology, Vol. 27, Issue 3
Effect of Avian Influenza Virus Infection on the Phagocytic Function of Systemic Phagocytes and Pulmonary Macrophages of Turkeys
journal, January 1994
- Kodihalli, S.; Sivanandan, V.; Nagaraja, K. V.
- Avian Diseases, Vol. 38, Issue 1
Alveolar Macrophages Have a Protective Antiinflammatory Role during Murine Pneumococcal Pneumonia
journal, January 2003
- Knapp, Sylvia; Leemans, Jaklien C.; Florquin, Sandrine
- American Journal of Respiratory and Critical Care Medicine, Vol. 167, Issue 2
No apoptotic deaths and different levels of inductions of inflammatory cytokines in alveolar macrophages infected with influenza viruses
journal, November 2004
- Seo, Sang Heui; Webby, Richard; Webster, Robert G.
- Virology, Vol. 329, Issue 2
Influenza Alone and in Sequence with Pneumonia Due to Streptococcus pneumoniae in the Squirrel Monkey
journal, December 1975
- Berendt, R. F.; Long, G. G.; Walker, J. S.
- Journal of Infectious Diseases, Vol. 132, Issue 6
Role of Neuraminidase in Lethal Synergism between Influenza Virus and Streptococcus pneumoniae
journal, March 2003
- McCullers, Jonathan A.; Bartmess, Kimberly C.
- The Journal of Infectious Diseases, Vol. 187, Issue 6
Gram-Positive Pathogens
book, March 2006
- Fischetti, Vincent A.; Novick, Richard P.; Ferretti, Joseph J.
An accurate two-phase approximate solution to an acute viral infection model
journal, July 2009
- Smith, Amber M.; Adler, Frederick R.; Perelson, Alan S.
- Journal of Mathematical Biology, Vol. 60, Issue 5
Influenza A Virus PB1-F2: A Small Protein with a Big Punch
journal, October 2007
- Conenello, Gina M.; Palese, Peter
- Cell Host & Microbe, Vol. 2, Issue 4
Influenza Virus-Induced Glucocorticoids Compromise Innate Host Defense against a Secondary Bacterial Infection
journal, February 2010
- Jamieson, Amanda M.; Yu, Shuang; Annicelli, Charles H.
- Cell Host & Microbe, Vol. 7, Issue 2
Commensal Bacteria Calibrate the Activation Threshold of Innate Antiviral Immunity
journal, July 2012
- Abt, Michael C.; Osborne, Lisa C.; Monticelli, Laurel A.
- Immunity, Vol. 37, Issue 1
Mathematical model of a three-stage innate immune response to a pneumococcal lung infection
journal, May 2011
- Smith, Amber M.; McCullers, Jonathan A.; Adler, Frederick R.
- Journal of Theoretical Biology, Vol. 276, Issue 1
No apoptotic deaths and different levels of inductions of inflammatory cytokines in alveolar macrophages infected with influenza viruses
journal, November 2004
- Seo, Sang Heui; Webby, Richard; Webster, Robert G.
- Virology, Vol. 329, Issue 2
A novel influenza A virus mitochondrial protein that induces cell death
journal, December 2001
- Chen, Weisan; Calvo, Paul A.; Malide, Daniela
- Nature Medicine, Vol. 7, Issue 12
Inhibition of pulmonary antibacterial defense by interferon-γ during recovery from influenza infection
journal, April 2008
- Sun, Keer; Metzger, Dennis W.
- Nature Medicine, Vol. 14, Issue 5
Effect of Neuraminidase on Receptor-mediated Adherence of Streptococcus pneumoniae to Chinchilla Tracheal Epithelium
journal, January 2002
- Tong, Hua Hua; Liu, Xia; Chen, Yiping
- Acta Oto-Laryngologica, Vol. 122, Issue 4
Sustained desensitization to bacterial Toll-like receptor ligands after resolutionof respiratory influenza infection
journal, January 2008
- Didierlaurent, Arnaud; Goulding, John; Patel, Seema
- The Journal of Experimental Medicine, Vol. 205, Issue 2
Influenza Virus Neuraminidase Contributes to Secondary Bacterial Pneumonia
journal, July 2005
- Peltola, Ville T.; Murti, K. Gopal; McCullers, Jonathan A.
- The Journal of Infectious Diseases, Vol. 192, Issue 2
Predominant Role of Bacterial Pneumonia as a Cause of Death in Pandemic Influenza: Implications for Pandemic Influenza Preparedness
journal, October 2008
- Morens, David M.; Taubenberger, Jeffery K.; Fauci, Anthony S.
- The Journal of Infectious Diseases, Vol. 198, Issue 7
Influenza Enhances Susceptibility to Natural Acquisition of and Disease due to Streptococcus pneumoniae in Ferrets
journal, October 2010
- McCullers, Jonathan A.; McAuley, Julie L.; Browall, Sarah
- The Journal of Infectious Diseases, Vol. 202, Issue 8
Regression and time series model selection in small samples
journal, January 1989
- Hurvich, Clifford M.; Tsai, Chih-Ling
- Biometrika, Vol. 76, Issue 2
Pulmonary and Systemic Defenses against Challenge with Staphylococcus aureus in Mice with Pneumonia Due to Influenza A Virus
journal, July 1979
- Jakab, G. J.; Warr, G. A.; Knight, M. E.
- Journal of Infectious Diseases, Vol. 140, Issue 1
Combined Infections in mice with Influenza Virus and Diplococcus Pneumoniae
journal, November 1957
- Gerone, Peter J.; Ward, Thomas G.; Chappal, W. Adrian
- American Journal of Epidemiology, Vol. 66, Issue 3
Python Unleashed on Systems Biology
journal, January 2007
- Myers, Christopher R.; Gutenkunst, Ryan N.; Sethna, James P.
- Computing in Science & Engineering, Vol. 9, Issue 3
The impact of successive infections on the lung microenvironment
journal, December 2007
- Didierlaurent, Arnaud; Goulding, John; Hussell, Tracy
- Immunology, Vol. 122, Issue 4
Binding of bacteria to HEp-2 cells infected with influenza A virus
journal, April 1999
- Ahmer, Omar R.; Raza, Muhammed W.; Ogilvie, Marie M.
- FEMS Immunology & Medical Microbiology, Vol. 23, Issue 4
Insights into the Interaction between Influenza Virus and Pneumococcus
journal, July 2006
- McCullers, J. A.
- Clinical Microbiology Reviews, Vol. 19, Issue 3
Both Influenza-Induced Neutrophil Dysfunction and Neutrophil-Independent Mechanisms Contribute to Increased Susceptibility to a Secondary Streptococcus pneumoniae Infection
journal, September 2006
- McNamee, L. A.; Harmsen, A. G.
- Infection and Immunity, Vol. 74, Issue 12
Filamentous Influenza A Virus Infection Predisposes Mice to Fatal Septicemia following Superinfection with Streptococcus pneumoniae Serotype 3
journal, April 2007
- Speshock, J. L.; Doyon-Reale, N.; Rabah, R.
- Infection and Immunity, Vol. 75, Issue 6
Host Cellular Immune Response to Pneumococcal Lung Infection in Mice
journal, February 2000
- Kadioglu, A.; Gingles, N. A.; Grattan, K.
- Infection and Immunity, Vol. 68, Issue 2
Bacterial Sinusitis and Otitis Media following Influenza Virus Infection in Ferrets
journal, April 2006
- Peltola, V. T.; Boyd, K. L.; McAuley, J. L.
- Infection and Immunity, Vol. 74, Issue 5
Influenza virus neuraminidase activates latent transforming growth factor beta
journal, December 1996
- Schultz-Cherry, S.; Hinshaw, V. S.
- Journal of Virology, Vol. 70, Issue 12
The Influenza A Virus PB1-F2 Protein Targets the Inner Mitochondrial Membrane via a Predicted Basic Amphipathic Helix That Disrupts Mitochondrial Function
journal, July 2003
- Gibbs, J. S.; Malide, D.; Hornung, F.
- Journal of Virology, Vol. 77, Issue 13
Streptococcus pneumoniae: virulence factors, pathogenesis, and vaccines
journal, December 1995
- AlonsoDeVelasco, E.; Verheul, A. F.; Verhoef, J.
- Microbiological Reviews, Vol. 59, Issue 4
Studies on Influenza in the Pandemic of 1957-1958. ii. Pulmonary Complications of Influenza*†
journal, January 1959
- Louria, Donald B.; Blumenfeld, Herbert L.; Ellis, John T.
- Journal of Clinical Investigation, Vol. 38, Issue 1 Pt 1-2
Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice
journal, July 2009
- Shahangian, Arash; Chow, Edward K.; Tian, Xiaoli
- Journal of Clinical Investigation, Vol. 119, Issue 7
Synergistic stimulation of type I interferons during influenza virus coinfection promotes Streptococcus pneumoniae colonization in mice
journal, September 2011
- Nakamura, Shigeki; Davis, Kimberly M.; Weiser, Jeffrey N.
- Journal of Clinical Investigation, Vol. 121, Issue 9
Immunokinetics in severe pneumonia due to influenza virus and bacteria coinfection in mice
journal, July 2004
- Seki, M.; Yanagihara, K.; Higashiyama, Y.
- European Respiratory Journal, Vol. 24, Issue 1
Effect of 1918 PB1-F2 Expression on Influenza A Virus Infection Kinetics
journal, February 2011
- Smith, Amber M.; Adler, Frederick R.; McAuley, Julie L.
- PLoS Computational Biology, Vol. 7, Issue 2
Bordetella pertussis Infection Exacerbates Influenza Virus Infection through Pertussis Toxin-Mediated Suppression of Innate Immunity
journal, April 2011
- Ayala, Victor I.; Teijaro, John R.; Farber, Donna L.
- PLoS ONE, Vol. 6, Issue 4
Influenza Virus PB1-F2 Protein Induces Cell Death through Mitochondrial ANT3 and VDAC1
journal, January 2005
- Zamarin, Dmitriy; García-Sastre, Adolfo; Xiao, Xiaoyao
- PLoS Pathogens, Vol. 1, Issue 1
Improving therapeutic strategies for secondary bacterial pneumonia following influenza
journal, August 2008
- McCullers, Jonathan A.; English, B. Keith
- Future Microbiology, Vol. 3, Issue 4
Influenza Infection Leads to Increased Susceptibility to Subsequent Bacterial Superinfection by Impairing NK Cell Responses in the Lung
journal, January 2010
- Small, Cherrie-Lee; Shaler, Christopher R.; McCormick, Sarah
- The Journal of Immunology, Vol. 184, Issue 4
Influenza A Inhibits Th17-Mediated Host Defense against Bacterial Pneumonia in Mice
journal, December 2010
- Kudva, Anupa; Scheller, Erich V.; Robinson, Keven M.
- The Journal of Immunology, Vol. 186, Issue 3
IL-10 Is an Important Mediator of the Enhanced Susceptibility to Pneumococcal Pneumonia after Influenza Infection
journal, June 2004
- van der Sluijs, Koenraad F.; van Elden, Leontine J. R.; Nijhuis, Monique
- The Journal of Immunology, Vol. 172, Issue 12
Can surveillance of the influenza virus PB1-F2 gene be used to predict the severity of secondary bacterial infections?
journal, October 2012
- Huber, Victor C.
- Virulence, Vol. 3, Issue 6
Works referencing / citing this record:
State-of-the-art in the pneumococcal field: Proceedings of the 11 th International Symposium on Pneumococci and Pneumococcal Diseases (ISPPD-11)
text, January 2020
- Kwambana-Adams, Brenda Anna; Mulholland, E. Kim; Satzke, Catherine
- Griffith University ePress
The role of influenza in the epidemiology of pneumonia
journal, October 2015
- Shrestha, Sourya; Foxman, Betsy; Berus, Joshua
- Scientific Reports, Vol. 5, Issue 1
Contribution of Host Immune Responses Against Influenza D Virus Infection Toward Secondary Bacterial Infection in a Mouse Model
journal, October 2019
- Skelton, Raegan M.; Shepardson, Kelly M.; Hatton, Alexis
- Viruses, Vol. 11, Issue 11
Dynamic Pneumococcal Genetic Adaptations Support Bacterial Growth and Inflammation during Coinfection with Influenza
journal, June 2021
- Smith, Amanda P.; Lane, Lindey C.; van Opijnen, Tim
- Infection and Immunity, Vol. 89, Issue 7
Influenza interaction with cocirculating pathogens and its impact on surveillance, pathogenesis, and epidemic profile: A key role for mathematical modelling
journal, February 2018
- Opatowski, Lulla; Baguelin, Marc; Eggo, Rosalind M.
- PLOS Pathogens, Vol. 14, Issue 2
Back to the Future: Lessons Learned From the 1918 Influenza Pandemic
journal, October 2018
- Short, Kirsty R.; Kedzierska, Katherine; van de Sandt, Carolien E.
- Frontiers in Cellular and Infection Microbiology, Vol. 8
Next generation protein based Streptococcus pneumoniae vaccines
journal, August 2015
- Pichichero, Michael E.; Khan, M. Nadeem; Xu, Qingfu
- Human Vaccines & Immunotherapeutics, Vol. 12, Issue 1
De novo assembly of Sockeye salmon kidney transcriptomes reveal a limited early response to piscine reovirus with or without infectious hematopoietic necrosis virus superinfection
journal, November 2016
- Polinski, Mark P.; Bradshaw, Julia C.; Inkpen, Sabrina M.
- BMC Genomics, Vol. 17, Issue 1
Impact of the H275Y and I223V Mutations in the Neuraminidase of the 2009 Pandemic Influenza Virus In Vitro and Evaluating Experimental Reproducibility
journal, May 2015
- Paradis, Eric G.; Pinilla, Lady Tatiana; Holder, Benjamin P.
- PLOS ONE, Vol. 10, Issue 5
Viral bacterial co-infection of the respiratory tract during early childhood
journal, May 2015
- Brealey, Jaelle C.; Sly, Peter D.; Young, Paul R.
- FEMS Microbiology Letters, Vol. 362, Issue 10
Hierarchical effects of pro-inflammatory cytokines on the post-influenza susceptibility to pneumococcal coinfection
journal, November 2016
- Duvigneau, Stefanie; Sharma-Chawla, Niharika; Boianelli, Alessandro
- Scientific Reports, Vol. 6, Issue 1
Metagenomic biomarker discovery and explanation
journal, January 2011
- Segata, Nicola; Izard, Jacques; Waldron, Levi
- Genome Biology, Vol. 12, Issue 6
Mathematical Models for Immunology: Current State of the Art and Future Research Directions
journal, October 2016
- Eftimie, Raluca; Gillard, Joseph J.; Cantrell, Doreen A.
- Bulletin of Mathematical Biology, Vol. 78, Issue 10
Impact of microbial Aetiology on mortality in severe community-acquired pneumonia
journal, September 2018
- Quah, Jessica; Jiang, Boran; Tan, Poh Choo
- BMC Infectious Diseases, Vol. 18, Issue 1
Influenza Virus Infection Model With Density Dependence Supports Biphasic Viral Decay
journal, July 2018
- Smith, Amanda P.; Moquin, David J.; Bernhauerova, Veronika
- Frontiers in Microbiology, Vol. 9
The co-pathogenesis of influenza viruses with bacteria in the lung
journal, March 2014
- McCullers, Jonathan A.
- Nature Reviews Microbiology, Vol. 12, Issue 4
Influenza Interaction with Cocirculating Pathogens, and Its Impact on Surveillance, Pathogenesis and Epidemic Profile: A Key Role for Mathematical Modeling
posted_content, October 2017
- Opatowski, Lulla; Baguelin, Marc; Eggo, Rosalind M.
- PLOS Pathogens
Allergic inflammation hinders synergistic viral-bacterial co-infection in C57BL/6 mice
posted_content, February 2019
- LeMessurier, Kim S.; Iverson, Amy R.; Chang, Ti-Cheng
- bioRxiv
Secondary Bacterial Infections in Influenza Virus Infection Pathogenesis
book, January 2014
- Smith, Amber M.; McCullers, Jonathan A.
- Influenza Pathogenesis and Control - Volume I
Enhanced IL-1β production is mediated by a TLR2-MYD88-NLRP3 signaling axis during coinfection with influenza A virus and Streptococcus pneumoniae
journal, February 2019
- Rodriguez, Angeline E.; Bogart, Christopher; Gilbert, Christopher M.
- PLOS ONE, Vol. 14, Issue 2
Inhibition of the inflammatory cytokine tumor necrosis factor-alpha with etanercept provides protection against lethal H1N1 influenza infection in mice
journal, January 2013
- Shi, Xunlong; Zhou, Wei; Huang, Hai
- Critical Care, Vol. 17, Issue 6
Respiratory viral infection: a potential “missing link” in the pathogenesis of COPD
journal, February 2019
- Linden, Dermot; Guo-Parke, Hong; Coyle, Peter V.
- European Respiratory Review, Vol. 28, Issue 151
Topological data analysis to uncover the shape of immune responses during co-infection
posted_content, January 2019
- Sasaki, Karin; Bruder, Dunja; Hernandez-Vargas, Esteban
- bioRxiv
Impact of the H275Y and I223V Mutations in the Neuraminidase of the 2009 Pandemic Influenza Virus In Vitro and Evaluating Experimental Reproducibility
posted_content, May 2021
- Beauchemin, Catherine A. A.; Paradis, Eric G.; Pinilla, Lady Tatiana
- PLOS One
Impact of viral upper respiratory tract infection on the concentration of nasopharyngeal pneumococcal carriage among Kenyan children
journal, July 2018
- Morpeth, Susan C.; Munywoki, Patrick; Hammitt, Laura L.
- Scientific Reports, Vol. 8, Issue 1
Canine influenza virus coinfection with Staphylococcus pseudintermedius enhances bacterial colonization, virus load and clinical presentation in mice
journal, June 2016
- Kalhoro, Dildar Hussain; Gao, Shanshan; Xie, Xing
- BMC Veterinary Research, Vol. 12, Issue 1
Mathematical modeling of within-host Zika virus dynamics
journal, August 2018
- Best, Katharine; Perelson, Alan S.
- Immunological Reviews, Vol. 285, Issue 1
Coinfection with Streptococcus pneumoniae Negatively Modulates the Size and Composition of the Ongoing Influenza-Specific CD8 + T Cell Response
journal, October 2014
- Blevins, Lance K.; Wren, John T.; Holbrook, Beth C.
- The Journal of Immunology, Vol. 193, Issue 10
Prevalence and clinical impact of VIral Respiratory tract infections in patients hospitalized for Community-Acquired Pneumonia: the VIRCAP study
journal, November 2019
- Tatarelli, P.; Magnasco, L.; Borghesi, M. L.
- Internal and Emergency Medicine, Vol. 15, Issue 4
Fundamental properties of cooperative contagion processes
journal, October 2017
- Chen, Li; Ghanbarnejad, Fakhteh; Brockmann, Dirk
- New Journal of Physics, Vol. 19, Issue 10
Allergic inflammation alters the lung microbiome and hinders synergistic co-infection with H1N1 influenza virus and Streptococcus pneumoniae in C57BL/6 mice
journal, December 2019
- LeMessurier, Kim S.; Iverson, Amy R.; Chang, Ti-Cheng
- Scientific Reports, Vol. 9, Issue 1
Dynamic Virus-Bacterium Interactions in a Porcine Precision-Cut Lung Slice Coinfection Model: Swine Influenza Virus Paves the Way for Streptococcus suis Infection in a Two-Step Process
journal, April 2015
- Meng, F.; Wu, N. H.; Nerlich, A.
- Infection and Immunity, Vol. 83, Issue 7
IL-1 Signaling Prevents Alveolar Macrophage Depletion during Influenza and Streptococcus pneumoniae Coinfection
journal, January 2018
- Bansal, Shruti; Yajjala, Vijaya Kumar; Bauer, Christopher
- The Journal of Immunology, Vol. 200, Issue 4
Simulation modelling for immunologists
journal, December 2019
- Handel, Andreas; La Gruta, Nicole L.; Thomas, Paul G.
- Nature Reviews Immunology, Vol. 20, Issue 3
Influenza A Virus as a Predisposing Factor for Cryptococcosis
journal, September 2017
- Oliveira, Lorena V. N.; Costa, Marliete C.; Magalhães, Thaís F. F.
- Frontiers in Cellular and Infection Microbiology, Vol. 7
Complex dynamics of synergistic coinfections on realistically clustered networks
journal, July 2015
- Hébert-Dufresne, Laurent; Althouse, Benjamin M.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 33
Modeling Influenza Virus Infection: A Roadmap for Influenza Research
journal, October 2015
- Boianelli, Alessandro; Nguyen, Van; Ebensen, Thomas
- Viruses, Vol. 7, Issue 10
Viral Coinfection Replaces Effects of Suilysin on Streptococcus suis Adherence to and Invasion of Respiratory Epithelial Cells Grown under Air-Liquid Interface Conditions
journal, August 2019
- Meng, Fandan; Tong, Jie; Vötsch, Désirée
- Infection and Immunity, Vol. 87, Issue 8
Host-pathogen kinetics during influenza infection and coinfection: insights from predictive modeling
journal, August 2018
- Smith, Amber M.
- Immunological Reviews, Vol. 285, Issue 1
Multiplicity of Mathematical Modeling Strategies to Search for Molecular and Cellular Insights into Bacteria Lung Infection
journal, August 2017
- Cantone, Martina; Santos, Guido; Wentker, Pia
- Frontiers in Physiology, Vol. 8
Critical Role of HAX-1 in Promoting Avian Influenza Virus Replication in Lung Epithelial Cells
journal, January 2018
- Li, Xue; Qu, Bingqian; He, Ganlin
- Mediators of Inflammation, Vol. 2018
A review of inflammatory mechanism in airway diseases
journal, October 2018
- Aghasafari, Parya; George, Uduak; Pidaparti, Ramana
- Inflammation Research, Vol. 68, Issue 1
Dynamic pneumococcal genetic adaptations support bacterial growth and inflammation during coinfection with influenza
posted_content, January 2019
- Smith, Amanda P.; Lane, Lindey C.; van Opijnen, Tim
Mathematical Models for Immunology: Current State of the Art and Future Research Directions
journal, October 2016
- Eftimie, Raluca; Gillard, Joseph J.; Cantrell, Doreen A.
- Bulletin of Mathematical Biology, Vol. 78, Issue 10
Superinfection and cell regeneration can lead to chronic viral coinfections
journal, April 2019
- Pinky, Lubna; González-Parra, Gilberto; Dobrovolny, Hana M.
- Journal of Theoretical Biology, Vol. 466
Viral–bacterial co-infections in the respiratory tract
journal, February 2017
- Bakaletz, Lauren O.
- Current Opinion in Microbiology, Vol. 35
Metabolic conversion of CI-1040 turns a cellular MEK-inhibitor into an antibacterial compound
journal, June 2018
- Bruchhagen, Christin; Jarick, Marcel; Mewis, Carolin
- Scientific Reports, Vol. 8, Issue 1
Impact of viral upper respiratory tract infection on the concentration of nasopharyngeal pneumococcal carriage among Kenyan children
journal, July 2018
- Morpeth, Susan C.; Munywoki, Patrick; Hammitt, Laura L.
- Scientific Reports, Vol. 8, Issue 1
The role of influenza in the epidemiology of pneumonia
journal, October 2015
- Shrestha, Sourya; Foxman, Betsy; Berus, Joshua
- Scientific Reports, Vol. 5, Issue 1
Hierarchical effects of pro-inflammatory cytokines on the post-influenza susceptibility to pneumococcal coinfection
journal, November 2016
- Duvigneau, Stefanie; Sharma-Chawla, Niharika; Boianelli, Alessandro
- Scientific Reports, Vol. 6, Issue 1
Heterogeneous shedding of influenza by human subjects and its implications for epidemiology and control
journal, December 2016
- Canini, Laetitia; Woolhouse, Mark E. J.; Maines, Taronna R.
- Scientific Reports, Vol. 6, Issue 1
Influenza Interaction with Cocirculating Pathogens, and Its Impact on Surveillance, Pathogenesis and Epidemic Profile: A Key Role for Mathematical Modeling
posted_content, October 2017
- Opatowski, Lulla; Baguelin, Marc; Eggo, Rosalind M.
- PLOS Pathogens
Persistent spatial patterns of interacting contagions
journal, February 2019
- Chen, Li
- Physical Review E, Vol. 99, Issue 2
A Perfect Storm: Increased Colonization and Failure of Vaccination Leads to Severe Secondary Bacterial Infection in Influenza Virus-Infected Obese Mice
journal, November 2017
- Karlsson, Erik A.; Meliopoulos, Victoria A.; van de Velde, Nicholas C.
- mBio, Vol. 8, Issue 5
Application of Optimal Control to Influenza Pneumonia Coinfection with Antiviral Resistance
journal, March 2020
- Kanyiri, Caroline W.; Luboobi, Livingstone; Kimathi, Mark
- Computational and Mathematical Methods in Medicine, Vol. 2020
De novo assembly of Sockeye salmon kidney transcriptomes reveal a limited early response to piscine reovirus with or without infectious hematopoietic necrosis virus superinfection
journal, November 2016
- Polinski, Mark P.; Bradshaw, Julia C.; Inkpen, Sabrina M.
- BMC Genomics, Vol. 17, Issue 1
Impact of microbial Aetiology on mortality in severe community-acquired pneumonia
journal, September 2018
- Quah, Jessica; Jiang, Boran; Tan, Poh Choo
- BMC Infectious Diseases, Vol. 18, Issue 1
Canine influenza virus coinfection with Staphylococcus pseudintermedius enhances bacterial colonization, virus load and clinical presentation in mice
journal, June 2016
- Kalhoro, Dildar Hussain; Gao, Shanshan; Xie, Xing
- BMC Veterinary Research, Vol. 12, Issue 1
Pretreatment of Epithelial Cells with Live Streptococcus pneumoniae Has No Detectable Effect on Influenza A Virus Replication In Vitro
journal, March 2014
- Ouyang, Kang; Woodiga, Shireen A.; Dwivedi, Varun
- PLoS ONE, Vol. 9, Issue 3
Non-Invasive Pneumococcal Pneumonia in Portugal—Serotype Distribution and Antimicrobial Resistance
journal, July 2014
- Horácio, Andreia N.; Lopes, Joana P.; Ramirez, Mário
- PLoS ONE, Vol. 9, Issue 7
An Epithelial Integrin Regulates the Amplitude of Protective Lung Interferon Responses against Multiple Respiratory Pathogens
journal, August 2016
- Meliopoulos, Victoria A.; Van de Velde, Lee-Ann; Van de Velde, Nicholas C.
- PLOS Pathogens, Vol. 12, Issue 8
TRAIL
+
monocytes and monocyte‐related cells cause lung damage and thereby increase susceptibility to influenza–
S
treptococcus pneumoniae
coinfection
journal, August 2015
- Ellis, Gregory T.; Davidson, Sophia; Crotta, Stefania
- EMBO reports, Vol. 16, Issue 9
Capsules of virulent pneumococcal serotypes enhance formation of neutrophil extracellular traps during in vivo pathogenesis of pneumonia
journal, March 2016
- Moorthy, Anandi Narayana; Rai, Prashant; Jiao, Huipeng
- Oncotarget, Vol. 7, Issue 15
Impact of the H275Y and I223V Mutations in the Neuraminidase of the 2009 Pandemic Influenza Virus In Vitro and Evaluating Experimental Reproducibility
posted_content, May 2021
- Beauchemin, Catherine A. A.; Paradis, Eric G.; Pinilla, Lady Tatiana
- PLOS One
Influenza A Virus as a Predisposing Factor for Cryptococcosis
journal, September 2017
- Oliveira, Lorena V. N.; Costa, Marliete C.; Magalhães, Thaís F. F.
- Frontiers in Cellular and Infection Microbiology, Vol. 7
In vivo Neutralization of Pro-inflammatory Cytokines During Secondary Streptococcus pneumoniae Infection Post Influenza A Virus Infection
journal, August 2019
- Sharma-Chawla, Niharika; Stegemann-Koniszewski, Sabine; Christen, Henrike
- Frontiers in Immunology, Vol. 10
Modeling Influenza Virus Infection: A Roadmap for Influenza Research
journal, October 2015
- Boianelli, Alessandro; Nguyen, Van; Ebensen, Thomas
- Viruses, Vol. 7, Issue 10
Combined bacterial and viral treatment: a novel anticancer strategy
journal, January 2015
- Krzykawski, Marcin P.
- Central European Journal of Immunology, Vol. 3