Cited by 161Influenza Virus Research StudiesRespiratory viral infections researchinterferon and immune responses

The DOI matches its Crossref record; 51 of the 51 references it cites were found in a registry or an index.

GM-CSF in the Lung Protects against Lethal Influenza Infection

Open access

Huang, Fang-Fang, Barnes, Peter F., Feng, Yan, Donis, Ruben, Chroneos, Zissis C., Idell, Steven, Allen, Timothy, Perez, Daniel R., Whitsett, Jeffrey A., Dunussi-Joannopoulos, Kyri, Shams, Homayoun·2011·American Journal of Respiratory and Critical Care Medicine

DOI 10.1164/rccm.201012-2036ocPMC PMC6938174

Open this paper in CoChat — free account

Abstract

RATIONALE: Alveolar macrophages contribute to host defenses against influenza in animal models. Enhancing alveolar macrophage function may contribute to protection against influenza. OBJECTIVES: To determine if increased expression of granulocyte/macrophage colony-stimulating factor (GM-CSF) in the lung increases resistance to influenza. METHODS: Wild-type mice and transgenic mice that expressed GM-CSF in the lung were infected with influenza virus, and lung pathology, weight loss, and mortality were measured. We also administered GM-CSF to the lungs of wild-type mice that were infected with influenza virus. MEASUREMENTS AND MAIN RESULTS: Wild-type mice all died after infection with different strains of influenza virus, but all transgenic mice expressing GM-CSF in the lungs survived. The latter also had greatly reduced weight loss and lung injury, and showed histologic evidence of a rapid host inflammatory response that controlled infection. The resistance of transgenic mice to influenza was abrogated by elimination of alveolar phagocytes, but not by depletion of T cells, B cells, or neutrophils. Transgenic mice had far more alveolar macrophages than did wild-type mice, and they were more resistant to influenza-induced apoptosis. Delivery of intranasal GM-CSF to wild-type mice also conferred resistance to influenza. CONCLUSIONS: GM-CSF confers resistance to influenza by enhancing innate immune mechanisms that depend on alveolar macrophages. Pulmonary delivery of this cytokine has the potential to reduce the morbidity and mortality due to influenza virus.

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 · 10.1164/rccm.201012-2036oc

Cites

51 of 51 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.

Granulocyte–Macrophage Colony-stimulating Factor to Reverse Sepsis-associated Immunosuppression: A Double-Blind, Randomized, Placebo-controlled Multicenter Trial
Meisel, C., Schefold, J. C., Pschowski, R., Baumann, T., Hetzger, K., Gregor, J. I., Weber‐Carstens, S., Hasper, D., Keh, D., Zuckermann, H., et al. (2009) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200903-0363oc · Cited by 683
Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10
Sun, J., Madan, R., Karp, C. L., & Braciale, T. J. (2009) · Nature Medicine · doi:10.1038/nm.1929 · Cited by 626
GM-CSF Regulates Alveolar Macrophage Differentiation and Innate Immunity in the Lung through PU.1
Shibata, Y., Berclaz, P., Chroneos, Z. C., Yoshida, M., Whitsett, J. A., & Trapnell, B. C. (2001) · Immunity · doi:10.1016/s1074-7613(01)00218-7 · Cited by 623
Self-citation
Granulocyte-macrophage colony-stimulating factor (GM-CSF) and T-cell responses: what we do and don't know
Shi, Y., Liu, C. H., Roberts, A. I., Das, J., Xu, G., Ren, G., Zhang, Y., Zhang, L., Yuan, Z., Tan, H. S., et al. (2006) · Cell Research · doi:10.1038/sj.cr.7310017 · Cited by 550
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
A critical function for CD200 in lung immune homeostasis and the severity of influenza infection
Snelgrove, R. J., Goulding, J., Didierlaurent, A. M., Lyonga, D., Vekaria, S., Edwards, L., Findlay, E. G., Sedgwick, J. D., Barclay, A. N., & Hussell, T. (2008) · Nature Immunology · doi:10.1038/ni.1637 · Cited by 454
Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus
Baskin, C. R., Bielefeldt-Ohmann, H., Tumpey, T. M., Sabourin, P. J., Long, J. P., García-Sastre, A., Tolnay, A.-E., Albrecht, R., Pyles, J. A., Olson, P. H., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813234106 · Cited by 361
Fc Receptor-Mediated Phagocytosis Makes a Significant Contribution to Clearance of Influenza Virus Infections
Huber, V. C., Lynch, J. M., Bucher, D. J., Le, J., & Metzger, D. W. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.12.7381 · Cited by 320
CCL5-CCR5 interaction provides antiapoptotic signals for macrophage survival during viral infection
Tyner, J. W., Uchida, O., Kajiwara, N., Kim, E. Y., Patel, A. C., O’Sullivan, M. P., Walter, M. J., Schwendener, R. A., Cook, D. N., Danoff, T. M., et al. (2005) · Nature Medicine · doi:10.1038/nm1303 · Cited by 299
Type I IFN Modulates Innate and Specific Antiviral Immunity
Durbin, J. E., Fernández-Sesma, A., Lee, C., Rao, T. D., Frey, A. B., Moran, T. M., Vukmanović, S., García‐Sastre, A., & Levy, D. E. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.8.4220 · Cited by 286

Show all 51 references

Sorted by citations

The development and function of lung-resident macrophages and dendritic cells
Kopf, M., Schneider, C., & Nobs, S. P. (2015) · Nature Immunology · doi:10.1038/ni.3052 · Cited by 555
The host immune response in respiratory virus infection: balancing virus clearance and immunopathology
Newton, A. H., Cardani, A. N., & Braciale, T. J. (2016) · Seminars in Immunopathology · doi:10.1007/s00281-016-0558-0 · Cited by 493
Pulmonary alveolar proteinosis
Trapnell, B. C., Nakata, K., Bonella, F., Campo, I., Griese, M., Hamilton, J. A., Wang, T. S., Morgan, C., Cottin, V., & McCarthy, C. (2019) · Nature Reviews Disease Primers · doi:10.1038/s41572-019-0066-3 · Cited by 411
Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections
Ghoneim, H. E., Thomas, P. G., & McCullers, J. A. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1300014 · Cited by 394
Influenza-induced monocyte-derived alveolar macrophages confer prolonged antibacterial protection
Aegerter, H., Kulikauskaite, J., Crotta, S., Patel, H., Kelly, G. P., Hessel, E. M., Mack, M., Beinke, S., & Wack, A. (2020) · Nature Immunology · doi:10.1038/s41590-019-0568-x · Cited by 367
Alveolar Macrophages Are Essential for Protection from Respiratory Failure and Associated Morbidity following Influenza Virus Infection
Schneider, C., Nobs, S. P., Heer, A. K., Kurrer, M. O., Klinke, G., van Rooijen, N., Vogel, J., & Köpf, M. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004053 · Cited by 341
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
Human Influenza Virus Infections
Peteranderl, C., Schmoldt, C., & Herold, S. (2016) · Seminars in Respiratory and Critical Care Medicine · doi:10.1055/s-0036-1584801 · Cited by 277
Novel concepts of acute lung injury and alveolar-capillary barrier dysfunction
Herold, S., Gabrielli, N. M., & Vadász, I. (2013) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00232.2013 · Cited by 210
Targeted Prostaglandin E2 Inhibition Enhances Antiviral Immunity through Induction of Type I Interferon and Apoptosis in Macrophages
Coulombe, F., Jaworska, J., Verway, M. J., Tzelepis, F., Massoud, A. H., Gillard, J., Wong, G., Kobinger, G., Xing, Z., Couture, C., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.02.013 · Cited by 207
Identification of a role for TRIM29 in the control of innate immunity in the respiratory tract
Xing, J., Weng, L., Yuan, B., Wang, Z., Li, J., Jin, R., Lu, H., Li, X. C., Liu, Y., & Zhang, Z. (2016) · Nature Immunology · doi:10.1038/ni.3580 · Cited by 205
Alveolar macrophages in tissue homeostasis, inflammation, and infection: evolving concepts of therapeutic targeting
Malainou, C., Abdin, S. M., Lachmann, N., Matt, U., & Herold, S. (2023) · Journal of Clinical Investigation · doi:10.1172/jci170501 · Cited by 215
DAMP Molecule S100A9 Acts as a Molecular Pattern to Enhance Inflammation during Influenza A Virus Infection: Role of DDX21-TRIF-TLR4-MyD88 Pathway
Tsai, S.-Y., Segovia, J. A., Chang, T.-H., Morris, I. R., Berton, M. T., Tessier, P. A., Tardif, M. R., Césaro, A., & Bose, S. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1003848 · Cited by 198
Viral Respiratory Pathogens and Lung Injury
Clementi, N., Ghosh, S., Santis, M. D., Castelli, M., Criscuolo, E., Zanoni, I., Clementi, M., & Mancini, N. (2021) · Clinical Microbiology Reviews · doi:10.1128/cmr.00103-20 · Cited by 202
The lung microenvironment shapes a dysfunctional response of alveolar macrophages in aging
McQuattie-Pimentel, A. C., Ren, Z., Joshi, N., Watanabe, S., Stoeger, T., Chi, M., Lu, Z., Sichizya, L., Aillon, R. P., Chen, C.-I., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci140299 · Cited by 177
GM-CSF: A Promising Target in Inflammation and Autoimmunity
Lee, M.-C., Achuthan, A. A., & Hamilton, J. A. (2020) · ImmunoTargets and Therapy · doi:10.2147/itt.s262566 · Cited by 157
Targeting GM-CSF in COVID-19 Pneumonia: Rationale and Strategies
Bonaventura, A., Vecchié, A., Wang, T. S., Lee, E., Cremer, P. C., Carey, B. C., Rajendram, P., Hudock, K. M., Korbee, L. L., Tassell, B. W. V., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01625 · Cited by 137
The Axl receptor tyrosine kinase is a discriminator of macrophage function in the inflamed lung
Fujimori, T., Grabiec, A. M., Kaur, M., Bell, T. J., Fujino, N., Cook, P. C., Svedberg, F. R., MacDonald, A. S., Maciewicz, R. A., Singh, D., et al. (2015) · Mucosal Immunology · doi:10.1038/mi.2014.129 · Cited by 132
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
A Close Encounter of the Third Kind
Mildner, A., Yona, S., & Jung, S. (2013) · Advances in immunology · doi:10.1016/b978-0-12-417028-5.00003-x · Cited by 136
Interleukin 8 and Acute Lung Injury
Allen, T. C., & Kurdowska, A. (2013) · Archives of Pathology & Laboratory Medicine · doi:10.5858/arpa.2013-0182-ra · Cited by 125
Self-citation
Alveolar epithelial cells orchestrate DC function in murine viral pneumonia
Unkel, B., Högner, K., Clausen, B. E., Lewe-Schlosser, P., Bodner, J., Gattenloehner, S., Janßen, H., Seeger, W., Lohmeyer, J., & Herold, S. (2012) · Journal of Clinical Investigation · doi:10.1172/jci62139 · Cited by 111
Homeostatic Control of Innate Lung Inflammation by Vici Syndrome Gene Epg5 and Additional Autophagy Genes Promotes Influenza Pathogenesis
Lu, Q., Yokoyama, C. C., Williams, J. W., Baldridge, M. T., Jin, X., DesRochers, B. L., Bricker, T. L., Wilen, C. B., Bagaitkar, J., Loginicheva, E., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2015.12.011 · Cited by 103
Type I Interferon Induced Epigenetic Regulation of Macrophages Suppresses Innate and Adaptive Immunity in Acute Respiratory Viral Infection
Kroetz, D. N., Allen, R., Schaller, M. A., Cavallaro, C., Ito, T., & Kunkel, S. L. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005338 · Cited by 94
Effects of Influenza on Alveolar Macrophage Viability Are Dependent on Mouse Genetic Strain
Califano, D., Furuya, Y., & Metzger, D. W. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701406 · Cited by 88
Influenza induces IL-8 and GM-CSF secretion by human alveolar epithelial cells through HGF/c-Met and TGF-α/EGFR signaling
Ito, Y., Correll, K. A., Zemans, R. L., Leslie, C. C., Murphy, R. C., & Mason, R. J. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00290.2014 · Cited by 86
Distinctive features of severe SARS-CoV-2 pneumonia
Budinger, G. R. S., Misharin, A. V., Ridge, K. M., Singer, B. D., & Wunderink, R. G. (2021) · Journal of Clinical Investigation · doi:10.1172/jci149412 · Cited by 87
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
Inhaled Granulocyte/Macrophage Colony–Stimulating Factor as Treatment of Pneumonia-associated Acute Respiratory Distress Syndrome
Herold, S., Högner, K., Vadász, I., Gessler, T., Wilhelm, J., Mayer, K., Morty, R. E., Walmrath, H., Seeger, W., & Lohmeyer, J. (2014) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201311-2041le · Cited by 81
mTORC1 Signaling Regulates Proinflammatory Macrophage Function and Metabolism
Collins, S. L., Oh, M. H., Sun, I., Chan‐Li, Y., Zhao, L., Powell, J. D., & Horton, M. R. (2021) · The Journal of Immunology · doi:10.4049/jimmunol.2100230 · Cited by 82
Legionella-Infected Macrophages Engage the Alveolar Epithelium to Metabolically Reprogram Myeloid Cells and Promote Antibacterial Inflammation
Liu, X., Boyer, M. A., Holmgren, A. M., & Shin, S. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.07.019 · Cited by 78
GM-CSF overexpression after influenza a virus infection prevents mortality and moderates M1-like airway monocyte/macrophage polarization
Halstead, E. S., Umstead, T. M., Davies, M. L., Kawasawa, Y. I., Silveyra, P., Howyrlak, J., Yang, L., Guo, W., Hu, S., Hewage, E. M. K. K., et al. (2018) · Respiratory Research · doi:10.1186/s12931-017-0708-5 · Cited by 76
Self-citation
Activated prostaglandin D2 receptors on macrophages enhance neutrophil recruitment into the lung
Jandl, K., Stacher, E., Bálint, Z., Sturm, E. M., Marić, J., Peinhaupt, M., Luschnig, P., Aringer, I., Fauland, A., Kónya, V., et al. (2016) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2015.11.012 · Cited by 76
Lung epithelial GM-CSF improves host defense function and epithelial repair in influenza virus pneumonia—a new therapeutic strategy?
Rösler, B., & Herold, S. (2016) · Molecular and Cellular Pediatrics · doi:10.1186/s40348-016-0055-5 · Cited by 76
Interleukin-26 in Antibacterial Host Defense of Human Lungs. Effects on Neutrophil Mobilization
Che, K. F., Tengvall, S., Levänen, B., Silverpil, E., Smith, M. E., Awad, M., Vikström, M., Palmberg, L., Qvarfordt, I., Sköld, M. C., et al. (2014) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201404-0689oc · Cited by 73
Boosting efferocytosis in alveolar space using BCG vaccine to protect host against influenza pneumonia
Mukherjee, S., Subramaniam, R., Chen, H., Smith, A. M., Keshava, S., & Shams, H. (2017) · PLoS ONE · doi:10.1371/journal.pone.0180143 · Cited by 69
Self-citation
Sargramostim (rhu GM-CSF) as Cancer Therapy (Systematic Review) and An Immunomodulator. A Drug Before Its Time?
Lazarus, H. M., Ragsdale, C. E., Gale, R. P., & Lyman, G. H. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.706186 · Cited by 72
Polydopamine-based nanomedicines for efficient antiviral and secondary injury protection therapy
Yin, N., Zhang, Z., Ge, Y., Zhao, Y., Gu, Z., Yang, Y., Mao, L., Wei, Z., Liu, J., Shi, J., et al. (2023) · Science Advances · doi:10.1126/sciadv.adf4098 · Cited by 69
Granulocyte macrophage colony-stimulating factor has come of age: From a vaccine adjuvant to antiviral immunotherapy
Petrina, M., Martin, J., & Basta, S. (2021) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2021.01.001 · Cited by 67
High levels of virus-specific CD4+ T cells predict severe pandemic influenza A virus infection.
Zhao, Y., Zhang, Y.-H., Denney, L., Young, D., Powell, T., Peng, Y.-C., Li, N., Yan, H.-P., Wang, D.-Y., Shu, Y., et al. (2012) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201207-1245oc · Cited by 70
Postviral Complications
Prasso, J. E., & Deng, J. C. (2016) · Clinics in Chest Medicine · doi:10.1016/j.ccm.2016.11.006 · Cited by 67
Recruited atypical Ly6G + macrophages license alveolar regeneration after lung injury
Ruscitti, C., Abinet, J., Maréchal, P., Meunier, M., meeûs, C. D., Vanneste, D., Janssen, P., Dourcy, M., Thiry, M., Bureau, F., et al. (2024) · Science Immunology · doi:10.1126/sciimmunol.ado1227 · Cited by 63
Regulation of Host Immune Responses against Influenza A Virus Infection by Mitogen-Activated Protein Kinases (MAPKs)
Yu, J., Sun, X., Goie, J. Y. G., & Zhang, Y. (2020) · Microorganisms · doi:10.3390/microorganisms8071067 · Cited by 59
GM-CSF modulates pulmonary resistance to influenza A infection
Sever-Chroneos, Z., Murthy, A., Davis, J., Florence, J., Kurdowska, A., Krupa, A., Tichelaar, J. W., White, M. R., Hartshorn, K. L., Kobzik, L., et al. (2011) · Antiviral Research · doi:10.1016/j.antiviral.2011.08.022 · Cited by 57
Self-citation
Distinctive Effects of GM-CSF and M-CSF on Proliferation and Polarization of Two Major Pulmonary Macrophage Populations
Draijer, C., Penke, L. R. K., & Peters-Golden, M. L. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1801387 · Cited by 60
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
Self-citation
Cytokine Concentrations in Plasma from Children with Severe and Non-Severe Community Acquired Pneumonia
Haugen, J., Chandyo, R. K., Brokstad, K. A., Mathisen, M., Ulak, M., Basnet, S., Valentiner‐Branth, P., & Strand, T. A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0138978 · Cited by 52
Stable incorporation of GM-CSF into dissolvable microneedle patch improves skin vaccination against influenza
Littauer, E. Q., Mills, L. K., Brock, N., Esser, E. S., Romanyuk, A. V., Pulit-Penaloza, J. A., Vassilieva, E. V., Beaver, J. T., Antao, O. Q., Krammer, F., et al. (2018) · Journal of Controlled Release · doi:10.1016/j.jconrel.2018.02.033 · Cited by 50
Activation of A 1 -Adenosine Receptors Promotes Leukocyte Recruitment to the Lung and Attenuates Acute Lung Injury in Mice Infected with Influenza A/WSN/33 (H1N1) Virus
Aeffner, F., Woods, P. S., & Davis, I. C. (2014) · Journal of Virology · doi:10.1128/jvi.01068-14 · Cited by 49
Innate Immunity and Influenza A Virus Pathogenesis: Lessons for COVID-19
Hartshorn, K. L. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.563850 · Cited by 48
The gene regulatory basis of bystander activation in CD8 + T cells
Watson, N. B., Patel, R. K., Kean, C., Veazey, J., Oyesola, O. O., Laniewski, N., Grenier, J. K., Wang, J., Tabilas, C., Yee Mon, K. J., et al. (2024) · Science Immunology · doi:10.1126/sciimmunol.adf8776 · Cited by 46
The Role and Molecular Mechanism of Action of Surfactant Protein D in Innate Host Defense Against Influenza A Virus
Hsieh, I.-N., Luna, X. D., White, M. R., & Hartshorn, K. L. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01368 · Cited by 45
Plasminogen Activator Inhibitor-1 in Cigarette Smoke Exposure and Influenza A Virus Infection-Induced Lung Injury
Bhandary, Y. P., Shetty, S. K., Marudamuthu, A. S., Midde, K., Ji, H.-L., Shams, H., Subramaniam, R., Fu, J., Idell, S., & Shetty, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123187 · Cited by 43
Self-citation
BATF promotes group 2 innate lymphoid cell–mediated lung tissue protection during acute respiratory virus infection
Wu, X., Kasmani, M. Y., Zheng, S., Khatun, A., Yao, C., Winkler, W., Zander, R., Burns, R., Taparowsky, E. J., Sun, J., et al. (2022) · Science Immunology · doi:10.1126/sciimmunol.abc9934 · Cited by 43
Tyk2 as a target for immune regulation in human viral/bacterial pneumonia
Berg, J., Zscheppang, K., Fatykhova, D., Tönnies, M., Bauer, T. T., Schneider, P., Neudecker, J., Rückert, J. C., Eggeling, S., Schimek, M., et al. (2017) · European Respiratory Journal · doi:10.1183/13993003.01953-2016 · Cited by 43
Respiratory Viruses and Asthma
Ramsahai, J. M., Pathinayake, P. S., Malik, B., Bartlett, N. W., & Wark, P. A. B. (2018) · Seminars in Respiratory and Critical Care Medicine · doi:10.1055/s-0037-1617412 · Cited by 39
Recombinant Human Granulocyte-Macrophage Colony-Stimulating Factor (rhu GM-CSF) as Adjuvant Therapy for Invasive Fungal Diseases
Chen, T. K., Batra, J. S., Michalik, D. E., Casillas, J., Patel, R., Ruiz, M. E., Hara, H., Patel, B., Kadapakkam, M., Ch’ng, J., et al. (2022) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofac535 · Cited by 41
Loss of GM-CSF-dependent instruction of alveolar macrophages in COVID-19 provides a rationale for inhaled GM-CSF treatment
Bosteels, C., Damme, K. F. A. V., Leeuw, E. D., Declercq, J., Maes, B., Bosteels, V., Hoste, L., Naesens, L., Debeuf, N., Deckers, J., et al. (2022) · Cell Reports Medicine · doi:10.1016/j.xcrm.2022.100833 · Cited by 43
Delivery of GM-CSF to Protect against Influenza Pneumonia
Subramaniam, R., Hillberry, Z., Chen, H., Feng, Y., Fletcher, K., Neuenschwander, P. F., & Shams, H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0124593 · Cited by 37
Self-citation
Lethal synergy between SARS-CoV-2 and Streptococcus pneumoniae in hACE2 mice and protective efficacy of vaccination
Barman, T. K., Singh, A. K., Bonin, J. L., Nafiz, T. N., Salmon, S. L., & Metzger, D. W. (2022) · JCI Insight · doi:10.1172/jci.insight.159422 · Cited by 34
Targeting alveolar macrophages: a promising intervention for pulmonary infection and acute lung injury
Hou, F., Shi, N., Yuan, H., LI, B. C., Xiao, J., Xiao, K., & Xie, L. (2025) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-025-00750-6 · Cited by 40
Contribution of innate immune cells to pathogenesis of severe influenza virus infection
Cole, S., & Ho, L. (2017) · Clinical Science · doi:10.1042/cs20160484 · Cited by 38
Alveolar macrophages: novel therapeutic targets for respiratory diseases
Lim, P. N., Cervantes, M. M., Pham, L. K., & Rothchild, A. C. (2021) · Expert Reviews in Molecular Medicine · doi:10.1017/erm.2021.21 · Cited by 35
The Role of Macrophages in Influenza a Virus Infection
Nicol, M. Q., & Dutia, B. M. (2014) · Future Virology · doi:10.2217/fvl.14.65 · Cited by 38
Therapeutic strategies in pneumonia: going beyond antibiotics
Müller-Redetzky, H., Lienau, J., Suttorp, N., & Witzenrath, M. (2015) · European Respiratory Review · doi:10.1183/16000617.0034-2015 · Cited by 37
Pulmonary Alveolar Proteinosis Syndrome
Kelly, A. K., & McCarthy, C. (2020) · Seminars in Respiratory and Critical Care Medicine · doi:10.1055/s-0039-3402727 · Cited by 34
Greater Efficacy of Black Ginseng (CJ EnerG) over Red Ginseng against Lethal Influenza A Virus Infection
Kim, E.-H., Kim, S.-W., Park, S., Kim, S., Yu, K.-M., Kim, S. G., Lee, S., Seo, Y.-K., Cho, N.-H., Kang, K., et al. (2019) · Nutrients · doi:10.3390/nu11081879 · Cited by 33
Key Role of MicroRNA in the Regulation of Granulocyte Macrophage Colony-stimulating Factor Expression in Murine Alveolar Epithelial Cells during Oxidative Stress
Sturrock, A., Mir-Kasimov, M., Baker, J., Rowley, J. W., & Paine, R. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.535922 · Cited by 32
An Immature Myeloid/Myeloid-Suppressor Cell Response Associated with Necrotizing Inflammation Mediates Lethal Pulmonary Tularemia
Periasamy, S., Avram, D., McCabe, A. F., MacNamara, K. C., Sellati, T. J., & Harton, J. A. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005517 · Cited by 31
Memory CD4 T Cell-Mediated Immunity against Influenza A Virus: More than a Little Helpful
McKinstry, K. K., Dutton, R. W., Swain, S. L., & Strutt, T. M. (2013) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-013-0236-z · Cited by 31
Dissecting host cell death programs in the pathogenesis of influenza
Downey, J., Pernet, E., Coulombe, F., & Divangahi, M. (2018) · Microbes and Infection · doi:10.1016/j.micinf.2018.03.005 · Cited by 33
GM-CSF: Orchestrating the Pulmonary Response to Infection
McCormick, T. S., Hejal, R. B., Leal, L. O., & Ghannoum, M. A. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.735443 · Cited by 31
TGF-β-induced IL-6 prevents development of acute lung injury in influenza A virus-infected F508del CFTR-heterozygous mice
Woods, P. S., Tazi, M., Chesarino, N. M., Amer, A. O., & Davis, I. C. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00078.2015 · Cited by 30
Lower respiratory tract delivery, airway clearance, and preclinical efficacy of inhaled GM-CSF in a postinfluenza pneumococcal pneumonia model
Umstead, T. M., Hewage, E. M. K. K., Mathewson, M., Beaudoin, S. R., Chroneos, Z. C., Wang, M., & Halstead, E. S. (2020) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00296.2019 · Cited by 30
Self-citation
Influenza, a One Health paradigm—Novel therapeutic strategies to fight a zoonotic pathogen with pandemic potential
Ludwig, S., Zell, R., Schwemmle, M., & Herold, S. (2014) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2014.08.016 · Cited by 29
Matrix MTMadjuvanted virosomal H5N1 vaccine induces balanced Th1/Th2 CD4+T cell responses in man
Pedersen, G. K., Sjursen, H., Nøstbakken, J. K., Jul‐Larsen, Å., Höschler, K., & Cox, R. J. (2014) · Human Vaccines & Immunotherapeutics · doi:10.4161/hv.29583 · Cited by 28
Respiratory Epithelial Cells as Master Communicators during Viral Infections
Miura, T. A. (2019) · Current Clinical Microbiology Reports · doi:10.1007/s40588-019-0111-8 · Cited by 30
Osteopontin aggravates acute lung injury in influenza virus infection by promoting macrophages necroptosis
Wang, J., Li, X., Wang, Y., Li, Y., Shi, F., & Diao, H. (2022) · Cell Death Discovery · doi:10.1038/s41420-022-00904-x · Cited by 27
Journey of monocytes and macrophages upon influenza A virus infection
Ruscitti, C., Radermecker, C., & Marichal, T. (2024) · Current Opinion in Virology · doi:10.1016/j.coviro.2024.101409 · Cited by 27
B cells modulate lung antiviral inflammatory responses via the neurotransmitter acetylcholine
Prieto, A. C., Luo, Z. L., Kulaga, H. M., & Baumgarth, N. (2025) · Nature Immunology · doi:10.1038/s41590-025-02124-8 · Cited by 27
Recombinant human granulocyte macrophage-colony stimulating factor expressed in yeast (sargramostim): A potential ally to combat serious infections
Damiani, G. B., McCormick, T. S., Leal, L. O., & Ghannoum, M. A. (2019) · Clinical Immunology · doi:10.1016/j.clim.2019.108292 · Cited by 26
Recombinant GM-CSF for diseases of GM-CSF insufficiency: Correcting dysfunctional mononuclear phagocyte disorders
Lazarus, H. M., Pitts, K., Wang, T. S., Lee, E., Buchbinder, E. L., Dougan, M. L., Armstrong, D. G., Paine, R., Ragsdale, C. E., Boyd, T. D., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1069444 · Cited by 29
Innate Immune Induction and Influenza Protection Elicited by a Response-Selective Agonist of Human C5a
Sanderson, S. D., Thoman, M. L., Kis, K., Virts, E. L., Herrera, E. B., Widmann, S., Sepulveda, H., & Phillips, J. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040303 · Cited by 25
Interplay between pulmonary epithelial stem cells and innate immune cells contribute to the repair and regeneration of ALI/ARDS
Wang, J., Peng, X., Yuan, N., Wang, B., Chen, S., Wang, B., & Xie, L. (2024) · Translational research · doi:10.1016/j.trsl.2024.05.012 · Cited by 28
Shaping of the alveolar landscape by respiratory infections and long-term consequences for lung immunity
Rodriguez-Rodriguez, L., Gillet, L., & Machiels, B. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1149015 · Cited by 23
A new factor influencing pathogen detection by molecular assay in children with both mild and severe hand, foot, and mouth disease
Zhu, D., Zhao, X.-Y., Yao, Y., Dai, F.-F., Han, H., Li, R., Jin, R.-H., Liang, L.-C., & Li, N. (2013) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2013.02.011 · Cited by 20
Alveolar Macrophages in Viral Respiratory Infections: Sentinels and Saboteurs of Lung Defense
Pöpperl, P., Stoff, M., & Beineke, A. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26010407 · Cited by 21
Exploring the mechanism of action of Xuanfei Baidu granule (XFBD) in the treatment of COVID-19 based on molecular docking and molecular dynamics
Xiong, L., Cao, J., Yang, X., Chen, S., Wu, M., Wang, C., Xu, H., Chen, Y., Zhang, R., Hu, X., et al. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.965273 · Cited by 18
The role of alveolar macrophages in viral respiratory infections and their therapeutic implications
Javaherdehi, A. P., Ghanbari, S., Mahdavi, P., Zafarani, A., & Razizadeh, M. H. (2024) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2024.101826 · Cited by 18
IFN-γ primes bone marrow neutrophils to acquire regulatory functions in severe viral respiratory infections
Creusat, F., Jouan, Y., Gonzalez, L., Barsac, E., Ilango, G., Lemoine, R., Soulard, D., Hankard, A., Boisseau, C., Guillon, A., et al. (2024) · Science Advances · doi:10.1126/sciadv.adn3257 · Cited by 19
Inhaled Sargramostim (Recombinant Human Granulocyte-Macrophage Colony-Stimulating Factor) for COVID-19-Associated Acute Hypoxemia: Results of the Phase 2, Randomized, Open-Label Trial (iLeukPulm)
Paine, R., Chasse, R., Halstead, E. S., Nfonoyim, J. M., Park, D. J., Byun, T., Patel, B., Molina-Pallete, G., Harris, E. S., Garner, F., et al. (2022) · Military Medicine · doi:10.1093/milmed/usac362 · Cited by 19
Pro-inflammatory cytokine dysregulation is associated with novel avian influenza A (H7N9) virus in primary human macrophages
Zhao, C., Qi, X., Ding, M., Sun, X., Zhou, Z., Zhang, S., Zen, K., & Li, X. (2015) · Journal of General Virology · doi:10.1099/jgv.0.000357 · Cited by 17
Sargramostim and Immune Checkpoint Inhibitors: Combinatorial Therapeutic Studies in Metastatic Melanoma
Tarhini, A. A., Joshi, I., & Garner, F. (2021) · Immunotherapy · doi:10.2217/imt-2021-0119 · Cited by 17
Managing COVID-19 infection in a Young Acute Myeloid Leukemia Patient Successfully With Antiviral and Granulocyte Colony Stimulating Factor: Playing on a Sticky Wicket
Talwar, D., Kumar, S., Acharya, S., Khanna, S., & Hulkoti, V. S. (2021) · Cureus · doi:10.7759/cureus.16589 · Cited by 16
FBXO6 regulates the antiviral immune responses via mediating alveolar macrophages survival
Cen, M., Ouyang, W., Lin, X., Du, X., Hu, H., Lu, H., Zhang, W., Xia, J., Qin, F. X.-F., & Xu, F. (2022) · Journal of Medical Virology · doi:10.1002/jmv.28203 · Cited by 16
Tissue kallikrein regulates alveolar macrophage apoptosis early in influenza virus infection
Magnen, M., Gueugnon, F., Petit‐Courty, A., Baranek, T., Sizaret, D., Brewah, Y. A., Humbles, A. A., Si‐Tahar, M., & Courty, Y. (2019) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00379.2018 · Cited by 16
Lethal influenza infection: Is a macrophage to blame?
Halstead, E. S., & Chroneos, Z. C. (2015) · Expert Review of Anti-infective Therapy · doi:10.1586/14787210.2015.1094375 · Cited by 16
Self-citation
Immunometabolic Signature during Respiratory Viral Infection: A Potential Target for Host-Directed Therapies
dos Reis, L. M., Berçot, M. R., Castelucci, B. G., Martins, A. J. E., Castro, G., & Moraes‐Vieira, P. M. (2023) · Viruses · doi:10.3390/v15020525 · Cited by 17
Surfactant protein A alters endosomal trafficking of influenza A virus in macrophages
Yau, E., Yang, L., Chen, Y., Umstead, T. M., Atkins, H., Katz, Z. E., Yewdell, J. W., Gandhi, C. K., Halstead, E. S., & Chroneos, Z. C. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.919800 · Cited by 15
Self-citation
Viral pneumonia and pulmonary alveolar proteinosis: the cause and the effect, case report
Albogami, S. M., & Touman, A. (2019) · AME Case Reports · doi:10.21037/acr.2019.09.04 · Cited by 14

Authors: Huang, F.-F., Barnes, P. F., Feng, Y., Donis, R., Chroneos, Z. C., Idell, S., Allen, T., Perez, D. R., Whitsett, J. A., Dunussi-Joannopoulos, K., & Shams, H.
Affiliations: Center for Pulmonary and Infectious Disease Control
Centers for Disease Control and Prevention, Atlanta, Georgia
The University of Texas Health Science Center at Tyler (US)
University of Maryland, College Park (US)
Cincinnati Children's Hospital Medical Center (US)
Pfizer Research, Cambridge, Massachusetts
Corresponding author: Shams, Homayoun
ORCID: Feng, Yan
Chroneos, Zissis C.
Idell, Steven
Perez, Daniel R.
Whitsett, Jeffrey A.
Shams, Homayoun
Venue: American Journal of Respiratory and Critical Care Medicine
Publisher: Oxford University Press (OUP)
Published: 2011-07
Volume: 184
Issue: 2
Pages: 259-268
ISSN: 1073-449X (ISSN-L)
1535-4970
DOI: 10.1164/rccm.201012-2036oc
PMC: PMC6938174
OpenAlex: W2100796791
Cited by: 161
References: 51
Citations by year: 2026: 3 · 2025: 9 · 2024: 11 · 2023: 9 · 2022: 14 · 2021: 18 · 2020: 15 · 2019: 10 · 2018: 6 · 2017: 4 · 2016: 10 · 2015: 16 · 2014: 14 · 2013: 11 · 2012: 9
FWCI: 8.64
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: American Journal of Respiratory and Critical Care Medicine (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: American Heart Association
Flight Attendant Medical Research Institute
Cain Foundation
National Heart, Lung, and Blood Institute (R01HL068127)
Topics: Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
Keywords: GM-CSF, influenza virus, alveolar macrophages, innate immunity, lung protection, transgenic mice, lung injury, apoptosis, host defense
MeSH terms: Administration, Intranasal, Animals, Disease Models, Animal, Flow Cytometry, Lung, Mice, Inbred C57BL, Mice, Transgenic, Orthomyxoviridae Infections, Weight Loss, Granulocyte-Macrophage Colony-Stimulating Factor, Macrophages, Alveolar, Apoptosis, Mice

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

GM-CSF in the Lung Protects against Lethal Influenza Infection

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