Sleep deprivation predisposes allergic mice to neutrophilic lung inflammation
Abstract
Background Although different studies associated sleep deprivation (SD) with systemic inflammatory changes, the effect of sleep duration on the pathology of allergic chronic diseases is poorly understood.Objective We sought to evaluate the influence of SD on allergen-induced pulmonary inflammation.Methods Ovalbumin (OVA)-sensitized C57BL/6 mice were exposed to a first set of intranasal OVA challenge under SD or healthy sleep (HS) conditions, followed by a second OVA challenge, 1 week apart. Some groups were subjected to corticosteroid treatment with dexamethasone.Results OVA-sensitized mice with SD had more severe airway inflammation than the allergic group with HS. Analysis of lung parenchyma revealed that the inflammation in allergic mice with SD was marked by an influx of neutrophils (mainly) and eosinophils and secretion of IL-6, TNF-α, and IL-17 in contrast to the eosinophilic inflammation and IL-4 production observed in allergic mice with HS. The same cytokine profile was observed in ex vivo culture of cervical lymph node cells and splenocytes, indicating that in allergic mice SD favors immune responses toward a proinflammatory T H 17 profile. This idea is supported by the fact that disruption of IL-17 signaling (IL-17 receptor A-/-) prevented airway neutrophilia in allergic mice with SD. Furthermore, allergic mice with SD became refractory to corticosteroid treatment in contrast to the allergic group with HS.Conclusion Collectively, our data show that sleep quality participates in the progression of allergen-induced eosinophilic lung inflammation to corticosteroid-refractory neutrophilic manifestation.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
The perception of sleep as poor may play a critical role in WBC upregulation.
“suggesting a critical role of the perception of sleep as poor in WBC upregulation”
From The Sleep-Immune Crosstalk in Health and Disease (2019) · cites this paper as [403]
Increased WBC counts in a sample of over 200 male workers were associated with self-reported poor sleep, but not with sleep duration or shift work patterns.
“increased WBC counts in a sample of over 200 male workers in a manufacturing plant were associated with self-reported poor sleep (assessed by a single question), but not with sleep duration or shift work patterns”
From The Sleep-Immune Crosstalk in Health and Disease (2019) · cites this paper as [403]
Cites
GLOBAL STRATEGY FOR ASTHMA MANAGEMENT AND PREVENTION
PAUWELS, R. A. (1996) · Arerugī/Arerugi · doi:10.15036/arerugi.45.792 · Cited by 9,997 · see citing works
Irwin, M. R., Olmstead, R., & Carroll, J. E. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.05.014 · Cited by 2,085 · see citing works
Why Sleep Is Important for Health: A Psychoneuroimmunology Perspective
Irwin, M. R. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010213-115205 · Cited by 1,325 · see citing works
Besedovsky, L., Lange, T., & Born, J. (2012) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-011-1044-0 · Cited by 1,153 · see citing works
Moore, W. C., Bleecker, E. R., Curran‐Everett, D., ERZURUM, S. C., Ameredes, B. T., Bacharier, L. B., Calhoun, W. J., Castro, M., Chung, K. F., Clark, M. P., et al. (2007) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2006.11.639 · Cited by 923 · see citing works
Neutrophil Recruitment by Human IL-17 Via C-X-C Chemokine Release in the Airways
Laan, M., Cui, Z.-H., Hoshino, H., Lötvall, J. O., Sjöstrand, M., Gruenert, D. C., Skoogh, B., & Lindén, A. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.4.2347 · Cited by 880 · see citing works
TH17 Cells Mediate Steroid-Resistant Airway Inflammation and Airway Hyperresponsiveness in Mice
McKinley, L., Alcorn, J. F., Peterson, A., DuPont, R., Kapadia, S. B., Logar, A., Henry, A. C., Irvin, C. G., Piganelli, J. D., Ray, A., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.6.4089 · Cited by 773 · see citing works
Corticosteroid resistance in patients with asthma and chronic obstructive pulmonary disease
Barnes, P. J. (2013) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2012.12.1564 · Cited by 698 · see citing works
Busse, W. W., Holgate, S. T., Kerwin, E., Chon, Y., Feng, J., Lin, J., & Lin, S. (2013) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201212-2318oc · Cited by 667 · see citing works
Interleukin-17 is a negative regulator of established allergic asthma
Schnyder‐Candrian, S., Togbe, D., Couillin, I., Mercier, I., Brombacher, F., Quesniaux, V. F. J., Fossiez, F., Ryffel, B., & Schnyder, B. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20061401 · Cited by 564 · see citing works
van Leeuwen, W. M. A., Lehto, M., Karisola, P., Lindholm, H., Luukkonen, R., Sallinen, M., Härmä, M., Porkka-Heiskanen, T., & Alenius, H. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004589 · Cited by 483 · see citing works
An epithelial circadian clock controls pulmonary inflammation and glucocorticoid action
Gibbs, J. E., Ince, L. M., Matthews, L. C., Mei, J., Bell, T., Yang, N., Saer, B., Begley, N., Poolman, T. M., Pariollaud, M., et al. (2014) · Nature Medicine · doi:10.1038/nm.3599 · Cited by 456 · see citing works
T H 17 Cell Differentiation Is Regulated by the Circadian Clock
Yu, X., Rollins, D., Ruhn, K. A., Stubblefield, J. J., Green, C. B., Kashiwada, M., Rothman, P. B., Takahashi, J. S., & Hooper, L. V. (2013) · Science · doi:10.1126/science.1243884 · Cited by 445 · see citing works
Irvin, C., Zafar, I., Good, J. T., Rollins, D. R., Christianson, C. A., Gorska, M. M., Martin, R. J., & Alam, R. (2014) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2014.05.038 · Cited by 318 · see citing works
Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice
Silva, R. H., Abílio, V. C., Takatsu, A. L., Kameda, S. R., Grassl, C., Chehin, A. B., Medrano, W. A., Calzavara, M. B., Registro, S., Andersen, M. L., et al. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2003.11.032 · Cited by 307 · see citing works
Self-citationMiyamoto, M., Prause, O., Sjöstrand, M., Laan, M., Lötvall, J. O., & Lindén, A. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.9.4665 · Cited by 281 · see citing works
Diesel exhaust particle induction of IL-17A contributes to severe asthma
Brandt, E. B., Kovacic, M. B., Lee, G. B., Gibson, A. M., Acciani, T. H., Cras, T. D. L., Ryan, P., Budelsky, A., & Hershey, G. K. K. (2013) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2013.06.048 · Cited by 265 · see citing works
The Bidirectional Relationship between Sleep and Immunity against Infections
Ibarra‐Coronado, E., Pantaleón-Martínez, A. M., Velázquez‐Moctezuma, J., Prospero-Garcia, O. E., Méndez‐Díaz, M., Pérez-Tapia, M., Pavón, L., & Morales‐Montor, J. (2015) · Journal of Immunology Research · doi:10.1155/2015/678164 · Cited by 228 · see citing works
Sleep after Vaccination Boosts Immunological Memory
Lange, T., Dimitrov, S., Bollinger, T., Diekelmann, S., & Born, J. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1100015 · Cited by 201 · see citing works
Rodriguez, D., Keller, A. C., Faquim-Mauro, E. L., de Macedo, M. S., Cunha, F. Q., Lefort, J., Vargaftig, B. B., & Russo, M. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.2.1001 · Cited by 169 · see citing works
Self-citationIrwin, M. R., Witarama, T., Caudill, M. M., Olmstead, R., & Breen, E. C. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.09.017 · Cited by 163 · see citing works
REM Sleep Deprivation in Rats Results in Inflammation and Interleukin-17 Elevation
Yehuda, S., Sredni, B., Carasso, R. L., & Kenigsbuch-Sredni, D. (2009) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2008.0080 · Cited by 158 · see citing works
Everson, C. A. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00021.2005 · Cited by 141 · see citing works
Refractory asthma: mechanisms, targets, and therapy
Trevor, J. L., & Deshane, J. S. (2014) · Allergy · doi:10.1111/all.12412 · Cited by 130 · see citing works
The Sleep-Immunity Relationship
Gamaldo, C. E., Shaikh, A. K., & McArthur, J. C. (2012) · Neurologic Clinics · doi:10.1016/j.ncl.2012.08.007 · Cited by 124 · see citing works
Ulich, T., del Castillo, J., & Souza, L. (1988) · PubMed · Cited by 104 · see citing works
Axelsson, J., Rehman, J.-U., Akerstedt, T., Ekman, R., Miller, G. E., Höglund, C. O., & Lekander, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082291 · Cited by 103 · see citing works
Asthma heterogeneity and severity
Carr, T. F., & Bleecker, E. R. (2016) · World Allergy Organization Journal · doi:10.1186/s40413-016-0131-2 · Cited by 102 · see citing works
T Helper 17 Cells in Airway Diseases
Halwani, R., Al‐Muhsen, S., & Hamid, Q. A. (2013) · CHEST Journal · doi:10.1378/chest.12-0598 · Cited by 83 · see citing works
BCL-2 protects human and mouse Th17 cells from glucocorticoid-induced apoptosis
Banuelos, J., Shin, S. C., Cao, Y., Bochner, B. S., Morales‐Nebreda, L., Budinger, G. R. S., Zhou, L., Li, S., Xin, J. J., Lingen, M. W., et al. (2016) · Allergy · doi:10.1111/all.12840 · Cited by 83 · see citing works
A gradient of glucocorticoid sensitivity among helper T cell cytokines
Banuelos, J., & Lu, N. (2016) · Cytokine & growth factor reviews · doi:10.1016/j.cytogfr.2016.05.002 · Cited by 70 · see citing works
Th17 regulating lower airway disease
Cosmi, L., Liotta, F., & Annunziato, F. (2015) · Current Opinion in Allergy and Clinical Immunology · doi:10.1097/aci.0000000000000227 · Cited by 65 · see citing works
Zager, A., Andersen, M. L., Lima, M. M. S., Reksidler, A. B., Machado, R. B., & Tufik, S. (2009) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.03.005 · Cited by 63 · see citing works
Self-citationMissed sleep and asthma morbidity in urban children
Daniel, L. C., Boergers, J., Kopel, S. J., et al. (2012) · Annals of Allergy Asthma & Immunology · doi:10.1016/j.anai.2012.05.015 · Cited by 62 · see citing works
Andersen, M. L., Martins, P. J. F., D’Almeida, V., Santos, R. F., Bignotto, M., & Tufik, S. (2004) · Experimental Gerontology · doi:10.1016/j.exger.2004.02.007 · Cited by 61 · see citing works
Self-citationGlucocorticoid-resistant Th17 cells are selectively attenuated by cyclosporine A
Schewitz‐Bowers, L. P., Lait, P. J. P., Copland, D. A., Chen, P., Wu, W., Dhanda, A., Vistica, B. P., Williams, E. L., Liu, B., Jawad, S., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1418316112 · Cited by 58 · see citing works
Sleep disturbances and asthma control: a real life study.
Braido, F., Baiardini, I., Ghiglione, V., Fassio, O., Bordo, A., Cauglia, S., & Canonica, G. W. (2009) · PubMed · Cited by 47 · see citing works
Severe Asthma: An Expanding and Mounting Clinical Challenge
Bell, M. C., & Busse, W. W. (2013) · The Journal of Allergy and Clinical Immunology In Practice · doi:10.1016/j.jaip.2013.01.005 · Cited by 46 · see citing works
Inhibition of murine granulopoiesis in vitro by dexamethasone
Golde, D. W., Bersch, N., Quan, S. G., et al. (1976) · American Journal of Hematology · doi:10.1002/ajh.2830010402 · Cited by 40 · see citing works
Lange, T., Dimitrov, S., Fehm, H., & Born, J. (2006) · International Immunopharmacology · doi:10.1016/j.intimp.2005.08.006 · Cited by 38 · see citing works
Schramm, R., & Thorlacius, H. (2003) · Infection and Immunity · doi:10.1128/iai.71.5.2542-2547.2003 · Cited by 35 · see citing works
Frequent nocturnal awakening in early life is associated with nonatopic asthma in children
Kozyrskyj, A. L., Kendall, G. E., Zubrick, S. R., Newnham, J. P., & Sly, P. D. (2009) · European Respiratory Journal · doi:10.1183/09031936.00040509 · Cited by 33 · see citing works
Ruiz, F. S., Andersen, M. L., Guindalini, C., Araújo, L. P., Lopes, J. D., & Tufik, S. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.12.027 · Cited by 31 · see citing works
Self-citationThe immune recovery function of sleep – Tracked by neutrophil counts
Lange, T., & Born, J. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.08.008 · Cited by 30 · see citing works
Health-related quality of life predicts onset of asthma in a longitudinal population study
Leander, M., Cronqvist, A., Janson, C., Uddenfeldt, M., & Rask‐Andersen, A. (2008) · Respiratory Medicine · doi:10.1016/j.rmed.2008.09.015 · Cited by 29 · see citing works
Day, C. E., Zhang, S., Riley, J., et al. (2009) · Journal of Immunological Methods · doi:10.1016/j.jim.2008.12.001 · Cited by 19 · see citing works
Li, H., Liu, X., Poh, Y., Wu, L., Zhou, Q., & Cai, B. (2014) · Biomedical Chromatography · doi:10.1002/bmc.3232 · Cited by 16 · see citing works
Brandt, E. B., & Hershey, G. K. K. (2016) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2016.03.037 · Cited by 16 · see citing works
Borges, M. D. C., Marchica, C. L., Narayanan, V., et al. (2013) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2013.07.005 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Sleep-Immune Crosstalk in Health and Disease
Besedovsky, L., Lange, T., & Haack, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00010.2018 · Cited by 1,479 · see citing works
- Authors
- Nunes, J. O. F., Apostolico, J. D. S., Andrade, D. A. G., Ruiz, F. S., Fernandes, E. R., Andersen, M. L., Keller, A. C., & Rosa, D. S.
- Affiliations
- Universidade Federal de São Paulo (BR)
- Corresponding author
- Keller, Alexandre C.
- Rosa, Daniela S.
- Venue
- Journal of Allergy and Clinical Immunology
- Publisher
- Elsevier BV
- Published
- 2018-03
- Volume
- 141
- Issue
- 3
- Pages
- 1018-1027.e4
- ISSN
- 0091-6749 (ISSN-L)
- OpenAlex
- W2738221152
- Cited by
- 43
- References
- 49
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 1 · 2023: 11 · 2022: 4 · 2021: 4 · 2020: 11 · 2019: 4
- FWCI
- 3.03
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Allergy and Clinical Immunology (publishedVersion)
- PubMed (publishedVersion)
- UNIFESP Institutional Repository (Universidade Federal de São Paulo) (submittedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Asthma and respiratory diseases
- Health Sciences › Medicine › Immunology and Allergy › Allergic Rhinitis and Sensitization
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- sleep deprivation, allergic airway inflammation, neutrophilic inflammation, eosinophilic inflammation, ovalbumin sensitization, IL-17, Th17 cells, IL-17 receptor A, steroid resistance, dexamethasone, cytokine profile, sleep quality
- MeSH terms
- Animals, Disease Susceptibility, Female, Humans, Hypersensitivity, Inflammation, Pneumonia, Sleep Deprivation, Cytokines, Mice, Knockout, Mice, Th17 Cells
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