Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Inflammation
Published in: Inflammation 4/2017

01-08-2017 | ORIGINAL ARTICLE

Inflammatory and Oxidative Stress Markers in Experimental Allergic Asthma

Authors: Renata Tiscoski Nesi, Emanuel Kennedy-Feitosa, Manuella Lanzetti, Mariana Barcellos Ávila, Clarissa Bichara Magalhães, Walter Araújo Zin, Débora Souza Faffe, Luís Cristóvão Porto, Samuel Santos Valença

Published in: Inflammation | Issue 4/2017

Login to get access

Abstract

Ovalbumin-induced allergic lung inflammation (ALI) is a condition believed to be mediated by cytokines, extracellular matrix remodeling, and redox imbalance. In this study, we evaluated pulmonary function together with inflammatory markers as interleukin-4 (IL-4), myeloperoxidase (MPO), eosinophil cells, and redox markers in the lungs of BALB/c mice after ovalbumin (OVA) sensitization and challenge. Our results showed an increase in bronchial hyperresponsiveness stimulated by methacholine (Mch), inflammatory cell influx, especially eosinophils together with an increase of high mobility group box 1 (HMGB1) and altered lipid peroxidation (LP) and antioxidant defenses in the OVA group compared to the control group (p ≤ 0.5). Thus, we demonstrated that OVA-induced ALI altered redox status concomitantly with impaired lung function, which was associated with HMGB1 expression and proteolytic remodeling. Taken together all results found here, we may suggest HMGB1 is an important therapeutic target for asthma, once orchestrates the redox signaling, inflammation, and remodeling that contribute to the disease development.
Literature
1.
Wurst, K.E., et al. 2016. Understanding asthma-chronic obstructive pulmonary disease overlap syndrome. Respiratory Medicine 110: 1–11.PubMedCrossRef
2.
Nielsen, M., C.B. Barnes, and C.S. Ulrik. 2015. Clinical characteristics of the asthma-COPD overlap syndrome—a systematic review. International Journal of Chronic Obstructive Pulmonary Disease 10: 1443–1454.PubMedPubMedCentral
3.
Mims, J.W. 2015. Asthma: definitions and pathophysiology. Int Forum Allergy Rhinol 5 (Suppl 1): S2–S6.PubMedCrossRef
4.
Janson, C. 2010. The importance of airway remodelling in the natural course of asthma. The Clinical Respiratory Journal 4 (Suppl 1): 28–34.PubMedCrossRef
5.
Masoli, M., et al. 2004. The global burden of asthma: executive summary of the GINA Dissemination Committee report. Allergy 59 (5): 469–478.PubMedCrossRef
6.
Al-Harbi, N.O., et al. 2015. Oxidative airway inflammation leads to systemic and vascular oxidative stress in a murine model of allergic asthma. International Immunopharmacology 26 (1): 237–245.PubMedCrossRef
7.
Fatani, S.H. 2014. Biomarkers of oxidative stress in acute and chronic bronchial asthma. The Journal of Asthma 51 (6): 578–584.PubMedCrossRef
8.
9.
Comhair, S.A., and S.C. Erzurum. 2010. Redox control of asthma: molecular mechanisms and therapeutic opportunities. Antioxidants & Redox Signaling 12 (1): 93–124.CrossRef
10.
Abreu, S.C., et al. 2013. Bone marrow mononuclear cell therapy in experimental allergic asthma: intratracheal versus intravenous administration. Respiratory Physiology & Neurobiology 185 (3): 615–624.CrossRef
11.
Antunes, M.A., et al. 2009. Different strains of mice present distinct lung tissue mechanics and extracellular matrix composition in a model of chronic allergic asthma. Respiratory Physiology & Neurobiology 165 (2–3): 202–207.CrossRef
12.
Antunes, M.A., et al. 2010. Sex-specific lung remodeling and inflammation changes in experimental allergic asthma. J Appl Physiol (1985) 109 (3): 855–863.CrossRef
13.
Silva, P.L., et al. 2008. Impact of lung remodelling on respiratory mechanics in a model of severe allergic inflammation. Respiratory Physiology & Neurobiology 160 (3): 239–248.CrossRef
14.
Xisto, D.G., et al. 2005. Lung parenchyma remodeling in a murine model of chronic allergic inflammation. American Journal of Respiratory and Critical Care Medicine 171 (8): 829–837.PubMedCrossRef
15.
Lee, C.C., et al. 2013. Inhibition of high-mobility group box 1 in lung reduced airway inflammation and remodeling in a mouse model of chronic asthma. Biochemical Pharmacology 86 (7): 940–949.PubMedCrossRef
16.
Shim, E.J., et al. 2012. The role of high-mobility group box-1 (HMGB1) in the pathogenesis of asthma. Clinical and Experimental Allergy 42 (6): 958–965.PubMedCrossRef
17.
Zhou, Y., et al. 2012. HMGB1 and RAGE levels in induced sputum correlate with asthma severity and neutrophil percentage. Human Immunology 73 (11): 1171–1174.PubMedCrossRef
18.
Lima, C., et al. 2002. Eosinophilic inflammation and airway hyper-responsiveness are profoundly inhibited by a helminth (Ascaris suum) extract in a murine model of asthma. Clinical and Experimental Allergy 32 (11): 1659–1666.PubMedCrossRef
19.
Suzuki, K., et al. 1983. Assay method for myeloperoxidase in human polymorphonuclear leukocytes. Analytical Biochemistry 132 (2): 345–352.PubMedCrossRef
20.
Bannister, J.V., and L. Calabrese. 1987. Assays for superoxide dismutase. Methods of Biochemical Analysis 32: 279–312.PubMedCrossRef
21.
22.
Flohe, L., and W.A. Gunzler. 1984. Assays of glutathione peroxidase. Methods in Enzymology 105: 114–121.PubMedCrossRef
23.
Draper, H.H., and M. Hadley. 1990. Malondialdehyde determination as index of lipid peroxidation. Methods in Enzymology 186: 421–431.PubMedCrossRef
24.
Green, L.C., et al. 1982. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Analytical Biochemistry 126 (1): 131–138.PubMedCrossRef
25.
Niu, R., et al. 2000. Quantitative analysis of matrix metalloproteinases-2 and -9, and their tissue inhibitors-1 and -2 in human placenta throughout gestation. Life Sciences 66 (12): 1127–1137.PubMedCrossRef
26.
Schneider, C.A., W.S. Rasband, and K.W. Eliceiri. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9 (7): 671–675.PubMedCrossRef
27.
Bates, J.H., et al. 1988. Interrupter resistance elucidated by alveolar pressure measurement in open-chest normal dogs. J Appl Physiol (1985) 65 (1): 408–414.
28.
29.
Monteseirin, J. 2009. Neutrophils and asthma. Journal of Investigational Allergology & Clinical Immunology 19 (5): 340–354.
30.
Monteseirin, J., et al. 2001. IgE-dependent release of myeloperoxidase by neutrophils from allergic patients. Clinical and Experimental Allergy 31 (6): 889–892.PubMedCrossRef
31.
Jatakanon, A., et al. 1999. Neutrophilic inflammation in severe persistent asthma. American Journal of Respiratory and Critical Care Medicine 160 (5 Pt 1): 1532–1539.PubMedCrossRef
32.
Lugogo, N.L., et al. 2012. Alveolar macrophages from overweight/obese subjects with asthma demonstrate a proinflammatory phenotype. American Journal of Respiratory and Critical Care Medicine 186 (5): 404–411.PubMedPubMedCentralCrossRef
33.
Molet, S., et al. 2005. Increase in macrophage elastase (MMP-12) in lungs from patients with chronic obstructive pulmonary disease. Inflammation Research 54 (1): 31–36.PubMedCrossRef
34.
Donnelly, L.E., and P.J. Barnes. 2012. Defective phagocytosis in airways disease. Chest 141 (4): 1055–1062.PubMedCrossRef
35.
Marone, G., et al. 1997. Molecular and cellular biology of mast cells and basophils. International Archives of Allergy and Immunology 114 (3): 207–217.PubMedCrossRef
36.
Williams, C.M., and S.J. Galli. 2000. Mast cells can amplify airway reactivity and features of chronic inflammation in an asthma model in mice. The Journal of Experimental Medicine 192 (3): 455–462.PubMedPubMedCentralCrossRef
37.
Haraguchi, M., S. Shimura, and K. Shirato. 1999. Morphometric analysis of bronchial cartilage in chronic obstructive pulmonary disease and bronchial asthma. American Journal of Respiratory and Critical Care Medicine 159 (3): 1005–1013.PubMedCrossRef
38.
Mayr, S.I., et al. 2002. IgE-dependent mast cell activation potentiates airway responses in murine asthma models. Journal of Immunology 169 (4): 2061–2068.CrossRef
39.
KleinJan, A. 2016. Airway inflammation in asthma: key players beyond the Th2 pathway. Current Opinion in Pulmonary Medicine 22 (1): 46–52.PubMedCrossRef
40.
Macedo-Soares, M.F., et al. 2004. Lung eosinophilic inflammation and airway hyperreactivity are enhanced by murine anaphylactic, but not nonanaphylactic, IgG1 antibodies. The Journal of Allergy and Clinical Immunology 114 (1): 97–104.PubMedCrossRef
41.
Olsen, P.C., et al. 2011. Lidocaine-derivative JMF2-1 prevents ovalbumin-induced airway inflammation by regulating the function and survival of T cells. Clinical and Experimental Allergy 41 (2): 250–259.PubMedCrossRef
42.
Silva, P.M., et al. 2001. Modulation of eotaxin formation and eosinophil migration by selective inhibitors of phosphodiesterase type 4 isoenzyme. British Journal of Pharmacology 134 (2): 283–294.PubMedPubMedCentralCrossRef
43.
Neves, J.S., et al. 2008. Eosinophil granules function extracellularly as receptor-mediated secretory organelles. Proceedings of the National Academy of Sciences of the United States of America 105 (47): 18478–18483.PubMedPubMedCentralCrossRef
44.
Neves, J.S., and P.F. Weller. 2009. Functional extracellular eosinophil granules: novel implications in eosinophil immunobiology. Current Opinion in Immunology 21 (6): 694–699.PubMedPubMedCentralCrossRef
45.
Perez, S.A., et al. 1993. Eosinophil granulocyte proliferation induced by an intermediate factor generated in the pleural cavity of rats injected with platelet-activating factor-acether. International Archives of Allergy and Immunology 102 (4): 368–374.PubMedCrossRef
46.
Andersson, U., and H. Erlandsson-Harris. 2004. HMGB1 is a potent trigger of arthritis. Journal of Internal Medicine 255 (3): 344–350.PubMedCrossRef
47.
Inoue, K., et al. 2007. HMGB1 expression by activated vascular smooth muscle cells in advanced human atherosclerosis plaques. Cardiovascular Pathology 16 (3): 136–143.PubMedCrossRef
48.
Andersson, U., and K.J. Tracey. 2003. HMGB1 in sepsis. Scandinavian Journal of Infectious Diseases 35 (9): 577–584.PubMedCrossRef
49.
50.
Hou, C., et al. 2015. HMGB1 contributes to allergen-induced airway remodeling in a murine model of chronic asthma by modulating airway inflammation and activating lung fibroblasts. Cellular & Molecular Immunology 12 (4): 409–423.CrossRef
51.
Ma, L., et al. 2015. High mobility group box 1: a novel mediator of Th2-type response-induced airway inflammation of acute allergic asthma. J Thorac Dis 7 (10): 1732–1741.PubMedPubMedCentral
52.
Henricks, P.A., and F.P. Nijkamp. 2001. Reactive oxygen species as mediators in asthma. Pulmonary Pharmacology & Therapeutics 14 (6): 409–420.CrossRef
53.
Zuo, L., et al. 2013. Molecular mechanisms of reactive oxygen species-related pulmonary inflammation and asthma. Molecular Immunology 56 (1–2): 57–63.PubMedCrossRef
54.
Ma, Y., et al. 2016. Morin attenuates ovalbumin-induced airway inflammation by modulating oxidative stress-responsive MAPK signaling. Oxidative Medicine and Cellular Longevity 2016: 5843672.PubMed
55.
Nadeem, A., et al. 2003. Increased oxidative stress and altered levels of antioxidants in asthma. The Journal of Allergy and Clinical Immunology 111 (1): 72–78.PubMedCrossRef
56.
Rahman, I., et al. 1996. Systemic oxidative stress in asthma, COPD, and smokers. American Journal of Respiratory and Critical Care Medicine 154 (4 Pt 1): 1055–1060.PubMedCrossRef
57.
Smith, L.J., et al. 1997. Reduced superoxide dismutase in lung cells of patients with asthma. Free Radical Biology & Medicine 22 (7): 1301–1307.CrossRef
58.
Comhair, S.A., et al. 2005. Superoxide dismutase inactivation in pathophysiology of asthmatic airway remodeling and reactivity. The American Journal of Pathology 166 (3): 663–674.PubMedPubMedCentralCrossRef
59.
Ahmad, A., M. Shameem, and Q. Husain. 2012. Relation of oxidant-antioxidant imbalance with disease progression in patients with asthma. Ann Thorac Med 7 (4): 226–232.PubMedPubMedCentralCrossRef
60.
Jacobson, G.A., K.C. Yee, and C.H. Ng. 2007. Elevated plasma glutathione peroxidase concentration in acute severe asthma: comparison with plasma glutathione peroxidase activity, selenium and malondialdehyde. Scandinavian Journal of Clinical and Laboratory Investigation 67 (4): 423–430.PubMedCrossRef
61.
Ganas, K., et al. 2001. Total nitrite/nitrate in expired breath condensate of patients with asthma. Respiratory Medicine 95 (8): 649–654.PubMedCrossRef
62.
Nadif, R., et al. 2014. Exhaled nitric oxide, nitrite/nitrate levels, allergy, rhinitis and asthma in the EGEA study. The European Respiratory Journal 44 (2): 351–360.PubMedCrossRef
63.
Rihak, V., et al. 2010. Nitrite in exhaled breath condensate as a marker of nitrossative stress in the airways of patients with asthma, COPD, and idiopathic pulmonary fibrosis. Journal of Clinical Laboratory Analysis 24 (5): 317–322.PubMedCrossRef
64.
Payne, D.N., et al. 2001. Relationship between exhaled nitric oxide and mucosal eosinophilic inflammation in children with difficult asthma, after treatment with oral prednisolone. American Journal of Respiratory and Critical Care Medicine 164 (8 Pt 1): 1376–1381.PubMedCrossRef
65.
Malinovschi, A., et al. 2016. Simultaneously increased fraction of exhaled nitric oxide levels and blood eosinophil counts relate to increased asthma morbidity. The Journal of Allergy and Clinical Immunology 138 (5): 1301–1308.PubMedCrossRef
66.
Watanabe, T., et al. 2011. Increased levels of HMGB-1 and endogenous secretory RAGE in induced sputum from asthmatic patients. Respiratory Medicine 105 (4): 519–525.PubMedCrossRef
67.
Jeffery, P.K. 2001. Remodeling in asthma and chronic obstructive lung disease. American Journal of Respiratory and Critical Care Medicine 164 (10 Pt 2): S28–S38.PubMedCrossRef
68.
Kumagai, K., et al. 1999. Inhibition of matrix metalloproteinases prevents allergen-induced airway inflammation in a murine model of asthma. Journal of Immunology 162 (7): 4212–4219.
69.
Matsuse, T., et al. 1991. Capsaicin inhibits airway hyperresponsiveness but not lipoxygenase activity or eosinophilia after repeated aerosolized antigen in guinea pigs. The American Review of Respiratory Disease 144 (2): 368–372.PubMedCrossRef
70.
Prikk, K., et al. 2002. Airway obstruction correlates with collagenase-2 (MMP-8) expression and activation in bronchial asthma. Laboratory Investigation 82 (11): 1535–1545.PubMedCrossRef
71.
Cook-Mills, J.M. 2006. Hydrogen peroxide activation of endothelial cell-associated MMPs during VCAM-1-dependent leukocyte migration. Cellular and Molecular Biology (Noisy-le-Grand, France) 52 (4): 8–16.
72.
Trifilieff, A., et al. 2002. Pharmacological profile of PKF242-484 and PKF241-466, novel dual inhibitors of TNF-alpha converting enzyme and matrix metalloproteinases, in models of airway inflammation. British Journal of Pharmacology 135 (7): 1655–1664.PubMedPubMedCentralCrossRef
73.
Gordon, J.R., et al. 2005. CD8 alpha+, but not CD8 alpha-, dendritic cells tolerize Th2 responses via contact-dependent and -independent mechanisms, and reverse airway hyperresponsiveness, Th2, and eosinophil responses in a mouse model of asthma. Journal of Immunology 175 (3): 1516–1522.CrossRef
74.
Ferguson, A.C., M. Whitelaw, and H. Brown. 1992. Correlation of bronchial eosinophil and mast cell activation with bronchial hyperresponsiveness in children with asthma. The Journal of Allergy and Clinical Immunology 90 (4 Pt 1): 609–613.PubMedCrossRef
75.
Ok, I.S., et al. 2009. Pinellia ternata, Citrus reticulata, and their combinational prescription inhibit eosinophil infiltration and airway hyperresponsiveness by suppressing CCR3+ and Th2 cytokines production in the ovalbumin-induced asthma model. Mediators of Inflammation 2009: 413270.PubMedPubMedCentralCrossRef
76.
Iwashita, H., et al. 2006. Role of eosinophil chemotactic factor by T lymphocytes on airway hyperresponsiveness in a murine model of allergic asthma. American Journal of Respiratory Cell and Molecular Biology 35 (1): 103–109.PubMedCrossRef
77.
Martin, L.B., et al. 1996. Eosinophils in allergy: role in disease, degranulation, and cytokines. International Archives of Allergy and Immunology 109 (3): 207–215.PubMedCrossRef
Metadata
Title
Inflammatory and Oxidative Stress Markers in Experimental Allergic Asthma
Authors
Renata Tiscoski Nesi
Emanuel Kennedy-Feitosa
Manuella Lanzetti
Mariana Barcellos Ávila
Clarissa Bichara Magalhães
Walter Araújo Zin
Débora Souza Faffe
Luís Cristóvão Porto
Samuel Santos Valença
Publication date
01-08-2017
Publisher
Springer US
Published in
Inflammation / Issue 4/2017
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-017-0560-2

Other articles of this Issue 4/2017

Inflammation 4/2017 Go to the issue

ORIGINAL ARTICLE

An Active Drimane-Type Lactone from Polygonum jucundum Attenuates Lipopolysaccharide-Induced Acute Lung Injury in Mice Through TLR4-MAPKs Signaling Pathway

Erratum

Erratum to: The Natural Course of Atopic Dermatitis and the Association with Asthma

ORIGINAL ARTICLE

Involvements of γδT Lymphocytes in Acute and Chronic Skin Wound Repair

ORIGINAL ARTICLE

Salidroside Inhibits Inflammation Through PI3K/Akt/HIF Signaling After Focal Cerebral Ischemia in Rats

ORIGINAL ARTICLE

Protective Effect of Gentianine, a compound from Du Huo Ji Sheng Tang, against Freund’s Complete Adjuvant-Induced Arthritis in Rats

ORIGINAL ARTICLE

Age-Related Changes in Inflammatory Response after Experimental Envenomation: Impact on the Susceptibility to Androctonus australis hector Venom

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits