Proinflammatory Activity in Bronchoalveolar Lavage Fluids From Patients With ARDS, a Prominent Role for Interleukin-1
Abstract
Proinflammatory cytokines such as tumor necrosis factor-alpha (TNF) and interleukin-1beta (IL-1) have been found to be elevated in bronchoalveolar lavage (BAL) fluid and in plasma from patients with acute respiratory distress syndrome (ARDS). In order to measure the balance of proinflammatory cytokines and their inhibitors, we quantified the upregulation of intercellular adhesion molecules (ICAM-1) induced by ARDS BAL fluids in human alveolar type II-like (A459) cells, and defined proinflammatory activity as the amount of ICAM-1 induced by the SAL fluids. Proinflammatory activity was detected in 77% of the SAL fluids sampled during the first week of ARDS, was found maximal during the 3 first days after onset of ARDS, and was significantly greater than in BAL specimens from at risk patients. Blocking experiments with specific inhibitors of TNF and IL-1 added to the BAL fluids indicated that the bioactivity measured was mainly due to IL-1. In contrast, proinflammatory activity of conditioned supernates from endotoxin-treated alveolar macrophages was mostly due to TNF. Using a bioassay that measures balance of cytokines with their inhibitors, our results indicate that the net proinflammatory activity in ARDS BAL fluids is attributable to IL-1 and not to TNF.
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IL-1β is a key cytokine driving proinflammatory activity in bronchoalveolar lavage fluid of patients with lung injury.
“IL-1 is a key cytokine driving proinflammatory activity in bronchoalveolar lavage fluid of patients with lung injury (118).”
From Into the Eye of the Cytokine Storm (2012) · cites this paper as [118]
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Nazerian, Y., Ghasemi, M., Yassaghi, Y., Nazerian, A., & Hashemi, S. M. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.109428 · Cited by 82 · see citing works
“ARDS is a notable feature in COVID-19 and is considered the leading cause of mortality [122].”
BackgroundInfluentialA Protective Role of Glibenclamide in Inflammation-Associated Injury
Zhang, G., Lin, X., Zhang, S., Xiu, H., Pan, C., & Cui, W. (2017) · Mediators of Inflammation · doi:10.1155/2017/3578702 · Cited by 88 · see citing works
Soluble MD-2 activity in plasma from patients with severe sepsis and septic shock
Pugin, J., Stern-Voeffray, S., Daubeuf, B., Matthay, M. A., Elson, G., & Dunn-Siegrist, I. (2004) · Blood · doi:10.1182/blood-2003-04-1290 · Cited by 84 · see citing works
Self-citationChang, D., Hayashi, S., Gharib, S. A., Vaisar, T., King, S., Tsuchiya, M., RUZINSKI, J. T., Park, D. R., Matute‐Bello, G., Wurfel, M. M., et al. (2008) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200712-1895oc · Cited by 81 · see citing works
Self-citationPerl, M., Lomas‐Neira, J., Chung, C., & Ayala, A. (2008) · Molecular Medicine · doi:10.2119/2008-00011.perl · Cited by 81 · see citing works
“Levels of Interleukin (IL)-8 and IL-1 have been found increased in the lungs of ALI patients (33,34) and the persistent increase of inflammatory cytokines in the lung correlated with poor outcome in ALI (35–37).”
BackgroundMicroarray-based Analysis of Ventilator-induced Lung Injury
Wurfel, M. M. (2007) · Proceedings of the American Thoracic Society · doi:10.1513/pats.200608-149jg · Cited by 80 · see citing works
“These findings suggest that, in ALI and ARDS, VILI could be exacerbated or sustained by the presence of microbial products that induce innate immune inflammatory responses within the alveolar space.”
BackgroundInfluentialQian, X., Aboushousha, R., van de Wetering, C., Chia, S. B., Amiel, E., Schneider, R. W., van der Velden, J. L. J., Lahue, K. G., Hoagland, D. A., Casey, D. T., et al. (2017) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2017.08.043 · Cited by 81 · see citing works
Cytokines and the acute respiratory distress syndrome (ARDS): A question of balance
Martin, T. R. (1997) · Nature Medicine · doi:10.1038/nm0397-272 · Cited by 79 · see citing works
Self-citationGriffiths, M. J., Ooi, M. H., Wong, S. C., Mohan, A., Podin, Y., Perera, D., Chieng, C. H., Tio, P. H., Cardosa, M. J., & Solomon, T. (2012) · The Journal of Infectious Diseases · doi:10.1093/infdis/jis446 · Cited by 78 · see citing works
“acute respiratory distress syndrome [14].”
Analytic Review: The Pathogenetic and Prognostic Value of Biologic Markers in Acute Lung Injury
Levitt, J. E., Gould, M. K., Ware, L. B., & Matthay, M. A. (2009) · Journal of Intensive Care Medicine · doi:10.1177/0885066609332603 · Cited by 79 · see citing works
Mechanisms of alveolar epithelial repair in acute lung injury - a translational approach
Geiser, T. (2003) · Swiss Medical Weekly · doi:10.4414/smw.2003.10267 · Cited by 77 · see citing works
Meyer, N. J., Feng, R., Li, M., Zhao, Y., Sheu, C., Tejera, P., Gallop, R., Bellamy, S. L., Rushefski, M., Lanken, P. N., et al. (2013) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201208-1501oc · Cited by 77 · see citing works
Abraham, E. H., Kaneko, D., & Shenkar, R. (1999) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1999.276.1.l1 · Cited by 77 · see citing works
MicroRNAs are dynamically regulated and play an important role in LPS-induced lung injury
Cai, Z.-G., Zhang, S.-M., Zhang, Y., Zhou, Y., Wu, H., & Xu, X. (2012) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y11-095 · Cited by 80 · see citing works
“Considering inflammation as a system disorder (Pugin et al. 1996), it would be interesting to see whether miR-16 was also involved in the inflammation, in vivo.”
BackgroundHuman Epidermal Growth Factor Receptor Signaling in Acute Lung Injury
Finigan, J. H., Downey, G. P., & Kern, J. A. (2012) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2012-0100tr · Cited by 75 · see citing works
Induced hypothermia as a new approach to lung rest for the acutely injured lung*
Hong, S., Koh, Y., Lee, I., Kim, M. J., Kim, W. S., Kim, D., Kim, W. D., & Lim, C. (2005) · Critical Care Medicine · doi:10.1097/01.ccm.0000178186.37167.53 · Cited by 75 · see citing works
“In human ARDS, IL-1 is known to be responsible for the majority of proinflammatory activity in the lung and correlates with the severity of disease (38).”
BackgroundPulmonary Inflammation Triggered by Ricin Toxin Requires Macrophages and IL-1 Signaling
Lindauer, M., Wong, J. W., Iwakura, Y., & Magun, B. E. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0901119 · Cited by 74 · see citing works
“Neutrophils responding to cytokine and chemokine gradients accumulate in the airways and contribute to injury and loss of epithelial integrity that characterize ARDS/ALI (35).”
InfluentialSuppression of Acute Lung Injury in Mice by an Inhibitor of Phosphodiesterase Type 4
Miotla, J. M., Teixeira, M. M., & Hellewell, P. G. (1998) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.18.3.2913 · Cited by 72 · see citing works
“Our data on the mouse are consistent with the study of Pugin and coworkers (47), which reported that the proinflammatory activity in BAL fluid from ARDS patients was due to interleukin-1 and not TNFa.”
ResultTonnel, A., Gosset, P., & Tillie‐Leblond, I. (2001) · International Archives of Allergy and Immunology · doi:10.1159/000053729 · Cited by 72 · see citing works
Glycyrrhizic Acid Prevents Sepsis-Induced Acute Lung Injury and Mortality in Rats
Zhao, H., Zhao, M., Wang, Y., Li, F., & Zhang, Z. (2015) · Journal of Histochemistry & Cytochemistry · doi:10.1369/0022155415610168 · Cited by 72 · see citing works
“to fluid transport and subsequent lung edema formation (Pugin et al. 1996; Olman et al. 2002).”
BackgroundRegulation of Lung Epithelial Sodium Channels by Cytokines and Chemokines
Wynne, B. M., Zou, L., Linck, V., Hoover, R. S., Ma, H., & Eaton, D. C. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00766 · Cited by 69 · see citing works
“An earlier study by Pugin and colleagues suggested that of the cytokines present in the BAL fluid, IL-1 β is the most biologically active, and others have suggested that the source may be from early-infiltrating neutrophils (103, 107).”
BackgroundAdult respiratory distress syndrome — an update
Hasleton, & Roberts (1999) · Histopathology · doi:10.1046/j.1365-2559.1999.00700.x · Cited by 67 · see citing works
The Role of Cytokine Responses During Influenza Virus Pathogenesis and Potential Therapeutic Options
Teijaro, J. R. (2014) · Current topics in microbiology and immunology · doi:10.1007/82_2014_411 · Cited by 68 · see citing works
“In fact, elevated levels of IL-1b drive proinflammatory responses in patients with acute respiratory distress syndrome (Pugin et al. 1996).”
Background
- Authors
- Pugin, J., Ricou, B., Steinberg, K. P., Suter, P. M., & Martin, T. R.
- Affiliations
- University Hospital of Geneva (CH)
- Venue
- American journal of respiratory and critical care medicine
- Publisher
- Oxford University Press (OUP)
- Published
- 1996-06-01
- Volume
- 153
- Issue
- 6
- Pages
- 1850-1856
- ISSN
- 1073-449X (ISSN-L)
- 1535-4970
- OpenAlex
- W2015667478
- Cited by
- 323
- References
- 0
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 7 · 2023: 3 · 2022: 12 · 2021: 13 · 2020: 13 · 2019: 8 · 2018: 8 · 2017: 7 · 2016: 7 · 2015: 14 · 2014: 10 · 2013: 16 · 2012: 18
- FWCI
- 15.35
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Respiratory and Critical Care Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (P50HL030542, HL-30542)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Respiratory Support and Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Inflammation biomarkers and pathways
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- acute respiratory distress syndrome, bronchoalveolar lavage fluid, interleukin-1, TNF-α, inflammatory cytokines, ICAM-1, alveolar macrophages, endotoxin, cytokine inhibitors, lung inflammation
- MeSH terms
- Adult, Aged, Bronchoalveolar Lavage Fluid, Humans, Inflammation, Interleukin-1, Lung Neoplasms, Middle Aged, Prospective Studies, Respiratory Distress Syndrome, Time Factors, Tumor Necrosis Factor-alpha, Case-Control Studies, Macrophages, Alveolar
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