Cited by 217Immune Cell Function and InteractionInfluenza Virus Research StudiesRespiratory viral infections research

The DOI matches its Crossref record; 40 of the 41 references it cites were found in a registry or an index.

Influenza Infection Leads to Increased Susceptibility to Subsequent Bacterial Superinfection by Impairing NK Cell Responses in the Lung

Open access

Small, Cherrie-Lee, Shaler, Christopher R, McCormick, Sarah, Jeyanathan, Mangalakumari, Damjanovic, Daniela, Brown, Earl G, Arck, Petra, Jordana, Manel, Kaushic, Charu, Ashkar, Ali A, Xing, Zhou·2010·The Journal of Immunology

DOI 10.4049/jimmunol.0902772

Open this paper in CoChat — free account Open PDF

Abstract

Influenza viral infection is well-known to predispose to subsequent bacterial superinfection in the lung but the mechanisms have remained poorly defined. We have established a murine model of heterologous infections by an H1N1 influenza virus and Staphylococcus aureus. We found that indeed prior influenza infection markedly increased the susceptibility of mice to secondary S. aureus superinfection. Severe sickness and heightened bacterial infection in flu and S. aureus dual-infected animals were associated with severe immunopathology in the lung. We further found that flu-experienced lungs had an impaired NK cell response in the airway to subsequent S. aureus bacterial infection. Thus, adoptive transfer of naive NK cells to the airway of prior flu-infected mice restored flu-impaired antibacterial host defense. We identified that TNF-alpha production of NK cells played an important role in NK cell-mediated antibacterial host defense as NK cells in flu-experienced lungs had reduced TNF-alpha expression and adoptive transfer of TNF-alpha-deficient NK cells to the airway of flu-infected mice failed to restore flu-impaired antibacterial host defense. Defected NK cell function was found to be an upstream mechanism of depressed antibacterial activities by alveolar macrophages as contrast to naive wild-type NK cells, the NK cells from flu-infected or TNF-alpha-deficient mice failed to enhance S. aureus phagocytosis by alveolar macrophages. Together, our study identifies the weakened NK cell response in the lung to be a novel critical mechanism for flu-mediated susceptibility to bacterial superinfection.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.4049/jimmunol.0902772

Cites

40 of 40 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Staphylococcus aureus: A Well–Armed Pathogen
Archer, G. L. (1998) · Clinical Infectious Diseases · doi:10.1086/520289 · Cited by 653
Inhibition of pulmonary antibacterial defense by interferon-γ during recovery from influenza infection
Sun, K., & Metzger, D. W. (2008) · Nature Medicine · doi:10.1038/nm1765 · Cited by 587
Pathogenicity of Influenza Viruses with Genes from the 1918 Pandemic Virus: Functional Roles of Alveolar Macrophages and Neutrophils in Limiting Virus Replication and Mortality in Mice
Tumpey, T. M., García‐Sastre, A., Taubenberger, J. K., Palese, P., Swayne, D. E., Pantin‐Jackwood, M. J., Schultz‐Cherry, S., Solórzano, A., van Rooijen, N., Katz, J. M., et al. (2005) · Journal of Virology · doi:10.1128/jvi.79.23.14933-14944.2005 · Cited by 504
Staphylococcus aureus : superbug, super genome?
Lindsay, J. A., & Holden, M. T. G. (2004) · Trends in Microbiology · doi:10.1016/j.tim.2004.06.004 · Cited by 479
Natural killer cells as an initial defense against pathogens
Lodoen, M. B., & Lanier, L. L. (2006) · Current Opinion in Immunology · doi:10.1016/j.coi.2006.05.002 · Cited by 473
In vivo evidence for a dependence on interleukin 15 for survival of natural killer cells
Cooper, M. A., Bush, J. E., Fehniger, T. A., VanDeusen, J. B., Waite, R. E., Liu, Y., Aguila, H. L., & Caligiuri, M. A. (2002) · Blood · doi:10.1182/blood-2001-12-0293 · Cited by 456
Lethal Synergism between Influenza Virus and Streptococcus pneumoniae: Characterization of a Mouse Model and the Role of Platelet‐Activating Factor Receptor
McCullers, J. A., & Rehg, J. E. (2002) · The Journal of Infectious Diseases · doi:10.1086/341462 · Cited by 423
Sustained desensitization to bacterial Toll-like receptor ligands after resolutionof respiratory influenza infection
Didierlaurent, A., Goulding, J., Patel, S., Snelgrove, R., Low, L., Bebien, M., Lawrence, T., van Rijt, L. S., Lambrecht, B. N., Sirard, J.-C., et al. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20070891 · Cited by 399
NK cells at the interface between innate and adaptive immunity
Moretta, A., Marcenaro, E., Parolini, S., Ferlazzo, G., & Moretta, L. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402170 · Cited by 387
Interactions between influenza and bacterial respiratory pathogens: implications for pandemic preparedness
Brundage, J. F. (2006) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(06)70466-2 · Cited by 386

Show all 41 references

Sorted by citations

The co-pathogenesis of influenza viruses with bacteria in the lung.
McCullers, J. A. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3231 · Cited by 722
Viral and Bacterial Interactions in the Upper Respiratory Tract
Bosch, A. A. T. M., Biesbroek, G., Trzcinski, K., Sanders, E. A. M., & Bogaert, D. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003057 · Cited by 651
Regulating the adaptive immune response to respiratory virus infection
Braciale, T. J., Sun, J., & Kim, T. S. (2012) · Nature reviews. Immunology · doi:10.1038/nri3166 · Cited by 374
Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice.
Kudva, A., Scheller, E. V., Robinson, K. M., Crowe, C. R., Choi, S. M., Slight, S. R., Khader, S. A., Dubin, P. J., Enelow, R. I., Kolls, J. K., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1002194 · Cited by 346
Integrative Physiology of Pneumonia
Quinton, L. J., Walkey, A. J., & Mizgerd, J. P. (2018) · Physiological Reviews · doi:10.1152/physrev.00032.2017 · Cited by 330
Influenza and Bacterial Superinfection: Illuminating the Immunologic Mechanisms of Disease
Rynda‐Apple, A., Robinson, K. M., & Alcorn, J. F. (2015) · Infection and Immunity · doi:10.1128/iai.00298-15 · Cited by 294
The role of the local microbial ecosystem in respiratory health and disease
Piters, W. A. A. D. S., Sanders, E. A. M., & Bogaert, D. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0294 · Cited by 300
Bacterial and viral infections associated with influenza
Joseph, C., Togawa, Y., & Shindo, N. (2013) · Influenza and Other Respiratory Viruses · doi:10.1111/irv.12089 · Cited by 250
Immune Dysfunction and Bacterial Coinfections following Influenza
Metzger, D. W., & Sun, K. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1301152 · Cited by 203
Kinetics of Coinfection with Influenza A Virus and Streptococcus pneumoniae
Smith, A. M., Adler, F. R., Ribeiro, R. M., Gutenkunst, R. N., McAuley, J., McCullers, J. A., & Perelson, A. S. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003238 · Cited by 201
Type I Interferon Induction during Influenza Virus Infection Increases Susceptibility to Secondary Streptococcus pneumoniae Infection by Negative Regulation of γδ T Cells
Li, W., Moltedo, B., & Moran, T. M. (2012) · Journal of Virology · doi:10.1128/jvi.01269-12 · Cited by 191
The complement system and human autoimmune diseases
Coss, S. L., Zhou, D., Chua, G. T., Abdul‐Aziz, R., Hoffman, R. P., Wu, Y. L., Ardoin, S. P., Atkinson, J. P., & Yu, C. Y. (2022) · Journal of Autoimmunity · doi:10.1016/j.jaut.2022.102979 · Cited by 189
Influenza virus primes mice for pneumonia from Staphylococcus aureus.
Iverson, A. R., Boyd, K. L., McAuley, J. L., Plano, L. R., Hart, M. E., & McCullers, J. A. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiq113 · Cited by 168
Immunopathogenesis of Staphylococcus aureus pulmonary infection
Parker, D., & Prince, A. S. (2011) · Seminars in Immunopathology · doi:10.1007/s00281-011-0291-7 · Cited by 176
Natural Killer (NK) Cells in Antibacterial Innate Immunity: Angels or Devils?
Souza-Fonseca-Guimarães, F., Adib‐Conquy, M., & Cavaillon, J. (2011) · Molecular Medicine · doi:10.2119/molmed.2011.00201 · Cited by 176
Modeling Influenza Virus Infection: A Roadmap for Influenza Research
Boianelli, A., Nguyễn, V. K., Ebensen, T., Schulze, K., Wilk, E., Sharma, N., Stegemann‐Koniszewski, S., Bruder, D., Toapanta, F. R., Guzmán, C. A., et al. (2015) · Viruses · doi:10.3390/v7102875 · Cited by 158
Innate Immune Function and Mortality in Critically Ill Children With Influenza
Hall, M. W., Geyer, S. M., Guo, C., Panoskaltsis‐Mortari, A., Jouvet, P. A., Ferdinands, J. M., Shay, D. K., Nateri, J., Greathouse, K. C., Sullivan, R., et al. (2012) · Critical Care Medicine · doi:10.1097/ccm.0b013e318267633c · Cited by 154
Pathogenesis of Respiratory Viral and Fungal Coinfections
Salazar, F., Bignell, E., Brown, G. D., Cook, P. C., & Warris, A. (2021) · Clinical Microbiology Reviews · doi:10.1128/cmr.00094-21 · Cited by 164
Failure of Respiratory Defenses in the Pathogenesis of Bacterial Pneumonia of Cattle
Caswell, J. (2013) · Veterinary Pathology · doi:10.1177/0300985813502821 · Cited by 158
Secondary Bacterial Infections in Influenza Virus Infection Pathogenesis
Smith, A. M., & McCullers, J. A. (2014) · Current topics in microbiology and immunology · doi:10.1007/82_2014_394 · Cited by 139
Influenza viral neuraminidase primes bacterial coinfection through TGF-β–mediated expression of host cell receptors
Li, N., Ren, A., Wang, X., Fan, X., Zhao, Y. X., Gao, G. F., Cleary, P. P., & Wang, B. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1414422112 · Cited by 138
Influenza A Virus Impairs Control of Mycobacterium tuberculosis Coinfection Through a Type I Interferon Receptor–Dependent Pathway
Redford, P. S., Mayer-Barber, K. D., McNab, F. W., Stavropoulos, E., Wack, A., Sher, A., & O’Garra, A. (2013) · The Journal of Infectious Diseases · doi:10.1093/infdis/jit424 · Cited by 136
Invasive Aspergillosis Associated With Severe Influenza Infections
Crum‐Cianflone, N. F. (2016) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofw171 · Cited by 134
The immunology of influenza virus-associated bacterial pneumonia.
Robinson, K. M., Kolls, J. K., & Alcorn, J. F. (2015) · Current Opinion in Immunology · doi:10.1016/j.coi.2015.02.002 · Cited by 132
Influenza A Virus Exacerbates Staphylococcus aureus Pneumonia in Mice by Attenuating Antimicrobial Peptide Production
Robinson, K. M., McHugh, K. J., Mandalapu, S., Clay, M. E., Lee, B., Scheller, E. V., Enelow, R. I., Chan, Y. R., Kolls, J. K., & Alcorn, J. F. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jit527 · Cited by 131
Immunopathology in influenza virus infection: Uncoupling the friend from foe
Damjanovic, D., Small, C.-L. N., Jeyananthan, M., McCormick, S. M., & Xing, Z. (2012) · Clinical Immunology · doi:10.1016/j.clim.2012.05.005 · Cited by 134
Self-citation
Outcomes of respiratory viral-bacterial co-infection in adult hospitalized patients
Liu, Y., Ling, L., Wong, S. H., Wang, M. H., Fitzgerald, J. R., Zou, X., Fang, S., Liu, X., Wang, X., Hu, W., et al. (2021) · EClinicalMedicine · doi:10.1016/j.eclinm.2021.100955 · Cited by 133
Critical Role of Natural Killer Cells in Lung Immunopathology During Influenza Infection in Mice
Abdul-Careem, M. F., Mian, M. F., Yue, G., Gillgrass, A. E., Chenoweth, M. J., Barra, N. G., Chew, M. V., Chan, T., Al-Garawi, A. A., Jordana, M., et al. (2012) · The Journal of Infectious Diseases · doi:10.1093/infdis/jis340 · Cited by 127
Self-citation
Signatures of COVID-19 Severity and Immune Response in the Respiratory Tract Microbiome
Merenstein, C., Liang, G., Whiteside, S. A., Güemes, A. G. C., Merlino, M. S., Taylor, L. J., Glascock, A. L., Bittinger, K. L., Tanes, C., Graham-Wooten, J., et al. (2021) · mBio · doi:10.1128/mbio.01777-21 · Cited by 133
Influenza Infection Suppresses NADPH Oxidase–Dependent Phagocytic Bacterial Clearance and Enhances Susceptibility to Secondary Methicillin-Resistant Staphylococcus aureus Infection
Sun, K., & Metzger, D. W. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1303049 · Cited by 125
In vivo and in vitro studies on the roles of neutrophil extracellular traps during secondary pneumococcal pneumonia after primary pulmonary influenza infection
Moorthy, A. N., Narasaraju, T., Rai, P., Perumalsamy, R., Tan, K. B., Wang, S., Engelward, B. P., & Chow, V. T. K. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00056 · Cited by 125
PPAR Gamma: From Definition to Molecular Targets and Therapy of Lung Diseases
de Carvalho, M. V., Gonçalves-de-Albuquerque, C. F., & Silva, A. R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22020805 · Cited by 115
Respiratory Virus Co-infection in Acute Respiratory Infections in Children
Meskill, S. D., & O’Bryant, S. C. (2020) · Current Infectious Disease Reports · doi:10.1007/s11908-020-0711-8 · Cited by 114
Diagnostic Accuracy of the Cepheid 3-gene Host Response Fingerstick Blood Test in a Prospective, Multi-site Study: Interim Results
Sutherland, J. S., van der Spuy, G. D., Gindeh, A., Thương, N. T. T., Namuganga, A., Owolabi, O., Mayanja‐Kizza, H., Nsereko, M., Thwaites, G. E., Winter, J. A., et al. (2021) · Clinical Infectious Diseases · doi:10.1093/cid/ciab839 · Cited by 109
Viral and Bacterial Co-Infections in the Lungs: Dangerous Liaisons
Oliva, J., & Terrier, O. (2021) · Viruses · doi:10.3390/v13091725 · Cited by 113
Postinfluenza bacterial pneumonia: Host defenses gone awry
Ballinger, M. N., & Standiford, T. J. (2010) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2010.0049 · Cited by 103
Negative Regulation of Lung Inflammation and Immunopathology by TNF-α during Acute Influenza Infection
Damjanovic, D., Divangahi, M., Kugathasan, K., Small, C.-L. N., Zganiacz, A., Brown, E. G., Hogaboam, C. M., Gauldie, J., & Xing, Z. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.09.003 · Cited by 104
Self-citation
TRAIL+ monocytes and monocyte‐related cells cause lung damage and thereby increase susceptibility to influenza–Streptococcus pneumoniae coinfection
Ellis, G. T., Davidson, S., Crotta, S., Branzk, N., Papayannopoulos, V., & Wack, A. (2015) · EMBO Reports · doi:10.15252/embr.201540473 · Cited by 102
Tuberculosis and COVID-19: Lessons from the Past Viral Outbreaks and Possible Future Outcomes
Crișan-Dabija, R. A., Grigorescu, C., Pavel, C.-A., Artene, B., Popa, I. V., Cernomaz, A. T., & Burlacu, A. (2020) · Canadian Respiratory Journal · doi:10.1155/2020/1401053 · Cited by 105
Contribution of Dendritic Cell Responses to Sepsis-Induced Immunosuppression and to Susceptibility to Secondary Pneumonia
Bouras, M., Asehnoune, K., & Roquilly, A. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02590 · Cited by 103
Interactions Between Streptococcus Pneumoniae and Influenza Virus: A Mutually Beneficial Relationship?
Short, K. R., Habets, M. N., Hermans, P. W. M., & Diavatopoulos, D. A. (2012) · Future Microbiology · doi:10.2217/fmb.12.29 · Cited by 100
Mechanisms of Bacterial Superinfection Post-influenza: A Role for Unconventional T Cells
Paget, C., & Trottein, F. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00336 · Cited by 91
Host Defense and the Airway Epithelium: Frontline Responses That Protect against Bacterial Invasion and Pneumonia
Eisele, N. A., & Anderson, D. M. (2011) · Journal of Pathogens · doi:10.4061/2011/249802 · Cited by 91
Conventional NK Cells Can Produce IL-22 and Promote Host Defense in Klebsiella pneumoniae Pneumonia
Xu, X., Weiss, I. D., Zhang, H. H., Singh, S. P., Wynn, T. A., Wilson, M. S., & Farber, J. M. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1300039 · Cited by 95
Next generation protein based Streptococcus pneumoniae vaccines
Pichichero, M. E., Khan, M. N., & Xu, Q. (2015) · Human Vaccines & Immunotherapeutics · doi:10.1080/21645515.2015.1052198 · Cited by 92
Innate immune memory of tissue-resident macrophages and trained innate immunity: Re-vamping vaccine concept and strategies
Xing, Z., Afkhami, S., Bavananthasivam, J., Fritz, D. K., D’Agostino, M. R., Vaseghi‐Shanjani, M., Yao, Y., & Jeyanathan, M. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.4mr0220-446r · Cited by 87
Self-citation
The amazing innate immune response to influenza A virus infection
Tripathi, S., White, M. R., & Hartshorn, K. L. (2013) · Innate Immunity · doi:10.1177/1753425913508992 · Cited by 88
Airway immune homeostasis and implications for influenza-induced inflammation
Snelgrove, R. J., Godlee, A., & Hussell, T. (2011) · Trends in Immunology · doi:10.1016/j.it.2011.04.006 · Cited by 80
Pandemic influenza A(H1N1) virus infection in solid organ transplant recipients: impact of viral and non-viral co-infection
Cordero, E., Pérez-Romero, P., Moreno, A., Len, O., Montejo, M., Vidal, E., Martín-Dávila, P., Fariñas, M. C., Fernández-Sabé, N., Giannella, M., et al. (2012) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2011.03537.x · Cited by 77
Pathogenesis ofStaphylococcus aureusnecrotizing pneumonia: the role of PVL and an influenza coinfection
Löffler, B., Niemann, S., Ehrhardt, C., Horn, D., Lanckohr, C., Lina, G., Ludwig, S., & Peters, G. (2013) · Expert Review of Anti-infective Therapy · doi:10.1586/14787210.2013.827891 · Cited by 79
Bacterial and viral infections and related inflammatory responses in chronic obstructive pulmonary disease
D’Anna, S. E., Maniscalco, M., Cappello, F., Carone, M., Motta, A., Balbi, B., Ricciardolo, F. L. M., Caramori, G., & Stefano, A. D. (2020) · Annals of Medicine · doi:10.1080/07853890.2020.1831050 · Cited by 78
Influenza A virus-induced release of interleukin-10 inhibits the anti-microbial activities of invariant natural killer T cells during invasive pneumococcal superinfection
Barthélémy, A., Ivanov, S., Fontaine, J., Soulard, D., Bouabe, H., Paget, C., Faveeuw, C., & Trottein, F. (2016) · Mucosal Immunology · doi:10.1038/mi.2016.49 · Cited by 75
Viral–bacterial interactions in the respiratory tract
Bellinghausen, C., Rohde, G. G. U., Savelkoul, P. H. M., Wouters, E. F. �., & Stassen, F. R. M. (2016) · Journal of General Virology · doi:10.1099/jgv.0.000627 · Cited by 77
The role of respiratory viruses in the etiology of bacterial pneumonia
Lee, K. H., Gordon, A., & Foxman, B. (2016) · Evolution Medicine and Public Health · doi:10.1093/emph/eow007 · Cited by 73
Post tuberculosis treatment infectious complications
Hsu, D., Irfan, M., Jabeen, K., Iqbal, N., Hasan, R., Migliori, G. B., Zumla, A. I., Visca, D., Centis, R., & Tiberi, S. (2020) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2020.02.032 · Cited by 68
Cellular immune reactions in the lung
Hasenberg, M., Stegemann‐Koniszewski, S., & Gunzer, M. (2012) · Immunological Reviews · doi:10.1111/imr.12020 · Cited by 69
Preventing and Treating Secondary Bacterial Infections with Antiviral Agents
McCullers, J. A. (2011) · Antiviral Therapy · doi:10.3851/imp1730 · Cited by 65
Influenza virus infection is associated with increased risk of death amongst patients hospitalized with confirmed pulmonary tuberculosis in South Africa, 2010–2011
Walaza, S., Tempia, S., Dawood, H., Variava, E., Moyes, J., Cohen, A. L., Wolter, N., Groome, M. J., von Mollendorf, C., Kahn, K., et al. (2015) · BMC Infectious Diseases · doi:10.1186/s12879-015-0746-x · Cited by 63
Clinical Relevance of Natural Killer Cells Following Hematopoietic Stem Cell Transplantation
Palmer, J. M., Rajasekaran, K., Thakar, M. S., & Malarkannan, S. (2013) · Journal of Cancer · doi:10.7150/jca.5049 · Cited by 63
Innate Immune Signaling Activated by MDR Bacteria in the Airway
Parker, D., Ahn, D. S., Cohen, T. S., & Prince, A. S. (2015) · Physiological Reviews · doi:10.1152/physrev.00009.2015 · Cited by 71
PI3K/Akt Signaling Pathway Modulates Influenza Virus Induced Mouse Alveolar Macrophage Polarization to M1/M2b
Zhao, X., Dai, J., Xiao, X., Wu, L., Zeng, J., Sheng, J., Su, J., Chen, X., Wang, G., & Li, K. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104506 · Cited by 63
MicroRNA-155 regulates host immune response to postviral bacterial pneumonia via IL-23/IL-17 pathway
Podsiad, A. B., Standiford, T. J., Ballinger, M. N., Eakin, R., Park, P. K., Kunkel, S. L., Moore, B. B., & Bhan, U. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00224.2015 · Cited by 63
Prevalence, Risk Factors, Clinical Features, and Outcome of Influenza-Associated Pulmonary Aspergillosis in Critically Ill Patients
Lu, L., Lee, H. M., Burke, A., Bassi, G. L., Torres, A., Fraser, J. F., & Fanning, J. P. (2023) · CHEST Journal · doi:10.1016/j.chest.2023.09.019 · Cited by 58
Influenza and tuberculosis co‐infection: A systematic review
Walaza, S., Cohen, C., Tempia, S., Moyes, J., Nguweneza, A., Madhi, S. A., McMorrow, M., & Cohen, A. L. (2019) · Influenza and Other Respiratory Viruses · doi:10.1111/irv.12670 · Cited by 58
Marked Improvement of Severe Lung Immunopathology by Influenza-Associated Pneumococcal Superinfection Requires the Control of Both Bacterial Replication and Host Immune Responses
Damjanovic, D., Lai, R., Jeyanathan, M., Hogaboam, C. M., & Xing, Z. (2013) · American Journal Of Pathology · doi:10.1016/j.ajpath.2013.05.016 · Cited by 60
Self-citation
Protecting Against Post-influenza Bacterial Pneumonia by Increasing Phagocyte Recruitment and ROS Production
Subramaniam, R., Barnes, P. F., Fletcher, K., Boggaram, V., Hillberry, Z., Neuenschwander, P. F., & Shams, H. (2013) · The Journal of Infectious Diseases · doi:10.1093/infdis/jit830 · Cited by 55
Coinfection with Staphylococcus aureus increases risk of severe coagulopathy in critically ill children with influenza A (H1N1) virus infection.
Nguyen, T., Kyle, U. G., Jaimon, N., Tcharmtchi, M. H., Coss-Bu, J. A., Lam, F., Teruya, J., & Loftis, L. (2012) · Critical Care Medicine · doi:10.1097/ccm.0b013e318260c7f8 · Cited by 54
Etiological analysis and predictive diagnostic model building of community-acquired pneumonia in adult outpatients in Beijing, China
Liu, Y. F., Gao, Y., Chen, M.-F., Cao, B., Yang, X.-H., & Wei, L. (2013) · BMC Infectious Diseases · doi:10.1186/1471-2334-13-309 · Cited by 54
FimH, a TLR4 ligand, induces innate antiviral responses in the lung leading to protection against lethal influenza infection in mice
Abdul-Careem, M. F., Mian, M. F., Gillgrass, A. E., Chenoweth, M. J., Barra, N. G., Chan, T., Al-Garawi, A. A., Chew, M. V., Yue, G., van Roojen, N., et al. (2011) · Antiviral Research · doi:10.1016/j.antiviral.2011.09.004 · Cited by 54
Self-citation
Novel protective mechanism for interleukin-33 at the mucosal barrier during influenza-associated bacterial superinfection
Robinson, K. M., Ramanan, K., Clay, M. E., McHugh, K. J., Rich, H. E. A., & Alcorn, J. F. (2017) · Mucosal Immunology · doi:10.1038/mi.2017.32 · Cited by 51
Mechanisms of Epithelial Immunity Evasion by Respiratory Bacterial Pathogens
Sharma, L., Feng, J., Britto, C. J., & Cruz, C. S. D. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00091 · Cited by 51
The role of influenza in the epidemiology of pneumonia
Shrestha, S., Foxman, B., Berus, J. M., van Panhuis, W. G., Steiner, C., Viboud, C. G., & Rohani, P. (2015) · Scientific Reports · doi:10.1038/srep15314 · Cited by 55
IRF5 regulates lung macrophages M2 polarization during severe acute pancreatitis in vitro
Sun, K., He, S.-B., Qu, J.-G., Dang, S.-C., Chen, J.-X., Gong, A.-H., Xie, R., & Zhang, J.-X. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i42.9368 · Cited by 49
Why is coinfection with influenza virus and bacteria so difficult to control?
Cauley, L. S., & Vella, A. T. (2015) · PubMed · Cited by 49
A Critical, Nonlinear Threshold Dictates Bacterial Invasion and Initial Kinetics During Influenza
Smith, A. M., & Smith, A. P. (2016) · Scientific Reports · doi:10.1038/srep38703 · Cited by 48
Viral strategies predisposing to respiratory bacterial superinfections
Rossi, G. A., Fanous, H., & Colin, A. A. (2020) · Pediatric Pulmonology · doi:10.1002/ppul.24699 · Cited by 54
Nox2-derived oxidative stress results in inefficacy of antibiotics against post-influenza S. aureus pneumonia
Sun, K., Yajjala, V. K., Bauer, C. D., Talmon, G. A., Fischer, K. J., Kielian, T., & Metzger, D. W. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20150514 · Cited by 48
Viruses and bacteria in Th2‐biased allergic airway disease
Lan, F., Zhang, N., Gevaert, E., Zhang, L., & Bachert, C. (2016) · Allergy · doi:10.1111/all.12934 · Cited by 45
Innate Immune Cell Suppression and the Link With Secondary Lung Bacterial Pneumonia
Morgan, D. J., Casulli, J., Chew, C., Connolly, E., Lui, S., Brand, O. J., Rahman, R., Jagger, C. P., & Hussell, T. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02943 · Cited by 45
The prevalence of influenza bacterial co-infection and its role in disease severity: A systematic review and meta-analysis
Qiao, M., Moyes, G., Zhu, F., Li, Y., & Wang, X. (2023) · Journal of Global Health · doi:10.7189/jogh.13.04063 · Cited by 44
Influenza virus infection causes neutrophil dysfunction through reduced G-CSF production and an increased risk of secondary bacteria infection in the lung
Ishikawa, H., Fukui, T., Ino, S., Sasaki, H., Awano, N., Kohda, C., & Tanaka, K. (2016) · Virology · doi:10.1016/j.virol.2016.08.025 · Cited by 43
Influenza (Including Avian Influenza and Swine Influenza)
Treanor, J. J. (2015) · Elsevier eBooks · doi:10.1016/b978-1-4557-4801-3.00167-3 · Cited by 44
A Novel Outbred Mouse Model of 2009 Pandemic Influenza and Bacterial Co-Infection Severity
McHugh, K. J., Mandalapu, S., Kolls, J. K., Ross, T. M., & Alcorn, J. F. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082865 · Cited by 43
A cooperativity between virus and bacteria during respiratory infections
Lalbiaktluangi, C., Yadav, M., Singh, P. K., Singh, A., Iyer, M., Vellingiri, B., Zomuansangi, R., Zothanpuia, Z., & Ram, H. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1279159 · Cited by 43
Super-infection withStaphylococcus aureusinhibits influenza virus-induced type I IFN signalling through impaired STAT1-STAT2 dimerization
Warnking, K., Klemm, C., Löffler, B., Niemann, S., van Krüchten, A., Peters, G., Ludwig, S., & Ehrhardt, C. (2014) · Cellular Microbiology · doi:10.1111/cmi.12375 · Cited by 40
IL-1 Signaling Prevents Alveolar Macrophage Depletion during Influenza and Streptococcus pneumoniae Coinfection
Bansal, S., Yajjala, V. K., Bauer, C. D., & Sun, K. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1700210 · Cited by 41
Type I interferon signaling regulates the composition of inflammatory infiltrates upon infection with Listeria monocytogenes
Brzoza‐Lewis, K. L., Hoth, J. J., & Hiltbold, E. M. (2011) · Cellular Immunology · doi:10.1016/j.cellimm.2011.11.008 · Cited by 40
Patterns in Bacterial- and Viral-Induced Immunosuppression and Secondary Infections in the ICU
Koch, R. M., Kox, M., de Jonge, M. I., van der Hoeven, J. G., Ferwerda, G., & Pickkers, P. (2016) · Shock · doi:10.1097/shk.0000000000000731 · Cited by 42
Viral coinfection promotes tuberculosis immunopathogenesis by type I IFN signaling-dependent impediment of Th1 cell pulmonary influx
Kang, T. G., Kwon, K. W., Kim, K. S., Lee, I., Kim, M. J., Ha, S., & Shin, S. J. (2022) · Nature Communications · doi:10.1038/s41467-022-30914-3 · Cited by 40
Influenza and Pneumonia Mortality in 66 Large Cities in the United States in Years Surrounding the 1918 Pandemic
Acuña-Soto, R., Viboud, C. G., & Chowell, G. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023467 · Cited by 38
Bacterial–viral load and the immune response in stable and exacerbated COPD: significance and therapeutic prospects
D’Anna, S. E., Balbi, B., Cappello, F., Carone, M., & Stefano, A. D. (2016) · International Journal of COPD · doi:10.2147/copd.s93398 · Cited by 38
A review of guidance on immunization in persons with defective or deficient splenic function
Kuchar, E. P., Miśkiewicz, K., & Karlikowska‐Skwarnik, M. (2015) · British Journal of Haematology · doi:10.1111/bjh.13660 · Cited by 37
Lethal Coinfection of Influenza Virus and Streptococcus pneumoniae Lowers Antibody Response to Influenza Virus in Lung and Reduces Numbers of Germinal Center B Cells, T Follicular Helper Cells, and Plasma Cells in Mediastinal Lymph Node
Wu, Y., Tu, W., Lam, K.-T., Chow, K., Ho, P., Guan, Y., Peiris, J. S. M., & Lau, Y. (2014) · Journal of Virology · doi:10.1128/jvi.02455-14 · Cited by 37
RIG-I Activation Protects and Rescues from Lethal Influenza Virus Infection and Bacterial Superinfection
Coch, C., Stümpel, J. P., Waldau, V. V. L., Wohlleber, D., Kümmerer, B. M., Bekeredjian‐Ding, I., Kochs, G., Garbi, N., Herberhold, S., Schuberth-Wagner, C., et al. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2017.07.003 · Cited by 37
The host immune dynamics of pneumococcal colonization: Implications for novel vaccine development
Khan, M. N., & Pichichero, M. E. (2014) · Human Vaccines & Immunotherapeutics · doi:10.4161/21645515.2014.979631 · Cited by 38
Oseltamivir PK/PD Modeling and Simulation to Evaluate Treatment Strategies against Influenza-Pneumococcus Coinfection
Boianelli, A., Sharma-Chawla, N., Bruder, D., & Hernandez-Vargas, E. A. (2016) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2016.00060 · Cited by 37
The Unexpected Impact of Vaccines on Secondary Bacterial Infections Following Influenza
Smith, A. M., & Huber, V. C. (2017) · Viral Immunology · doi:10.1089/vim.2017.0138 · Cited by 36
The Role of Virus Infection in Deregulating the Cytokine Response to Secondary Bacterial Infection
Mehta, D., Petes, C., Gee, K., & Basta, S. (2015) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2015.0072 · Cited by 36
Port d’Entrée for Respiratory Infections – Does the Influenza A Virus Pave the Way for Bacteria?
Siemens, N., Oehmcke-Hecht, S., Mettenleiter, T. C., Kreikemeyer, B., Valentin‐Weigand, P., & Hammerschmidt, S. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.02602 · Cited by 34
Antibody Treatment against Angiopoietin-Like 4 Reduces Pulmonary Edema and Injury in Secondary Pneumococcal Pneumonia
Li, L., Foo, B. J. W., Kwok, K. W., Sakamoto, N., Mukae, H., Izumikawa, K., Mandard, S., Quenot, J., Lagrost, L., Teh, W. K., et al. (2019) · mBio · doi:10.1128/mbio.02469-18 · Cited by 36

Authors: Small, C.-L., Shaler, C. R., McCormick, S., Jeyanathan, M., Damjanovic, D., Brown, E. G., Arck, P., Jordana, M., Kaushic, C., Ashkar, A. A., & Xing, Z.
Affiliations: Michael G. DeGroote Institute for Infectious Disease Research (CA)
University of Ottawa (CA)
McMaster University (CA)
Corresponding author: McCormick, Sarah
Jeyanathan, Mangalakumari
Damjanovic, Daniela
Jordana, Manel
Kaushic, Charu
Xing, Zhou
ORCID: Shaler, Christopher R
McCormick, Sarah
Brown, Earl G
Arck, Petra
Jordana, Manel
Kaushic, Charu
Ashkar, Ali A
Xing, Zhou
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2010-01-18
Volume: 184
Issue: 4
Pages: 2048-2056
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.0902772
OpenAlex: W2122758441
Cited by: 216
References: 41
Citations by year: 2026: 2 · 2025: 10 · 2024: 8 · 2023: 11 · 2022: 12 · 2021: 17 · 2020: 14 · 2019: 12 · 2018: 10 · 2017: 14 · 2016: 17 · 2015: 17 · 2014: 18 · 2013: 25 · 2012: 10
FWCI: 7.42
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: Canadian Institutes of Health Research
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immune Cell Function and Interaction
Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
Keywords: influenza virus, secondary bacterial infection, Staphylococcus aureus, natural killer cells, TNF-α, alveolar macrophages, secondary infection susceptibility, heterologous infection, lung immunopathology, phagocytosis, adoptive transfer, H1N1 influenza
MeSH terms: Animals, Disease Susceptibility, Female, Killer Cells, Natural, Mice, Inbred C57BL, Orthomyxoviridae Infections, Pneumonia, Viral, Staphylococcal Infections, Superinfection, Macrophages, Alveolar, Pneumonia, Bacterial, Mice, Influenza A Virus, H1N1 Subtype

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Influenza Infection Leads to Increased Susceptibility to Subsequent Bacterial Superinfection by Impairing NK Cell Responses in the Lung

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks