Epinephrine Activation of the β2-Adrenoceptor Is Required for IL-13-Induced Mucin Production in Human Bronchial Epithelial Cells
Mucus hypersecretion by airway epithelium is a hallmark of inflammation in allergic asthma and results in airway narrowing and obstruction. Others have shown that administration a TH2 cytokine, IL-13 is sufficient to cause mucus hypersecretion in vivo and in vitro. Asthma therapy often utilizes β2-a...
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Published in | PloS one Vol. 10; no. 7; p. e0132559 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Public Library of Science
10.07.2015
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Abstract | Mucus hypersecretion by airway epithelium is a hallmark of inflammation in allergic asthma and results in airway narrowing and obstruction. Others have shown that administration a TH2 cytokine, IL-13 is sufficient to cause mucus hypersecretion in vivo and in vitro. Asthma therapy often utilizes β2-adrenoceptor (β2AR) agonists, which are effective acutely as bronchodilators, however chronic use may lead to a worsening of asthma symptoms. In this study, we asked whether β2AR signaling in normal human airway epithelial (NHBE) cells affected mucin production in response to IL-13. This cytokine markedly increased mucin production, but only in the presence of epinephrine. Mucin production was blocked by ICI-118,551, a preferential β2AR antagonist, but not by CGP-20712A, a preferential β1AR antagonist. Constitutive β2AR activity was not sufficient for IL-13 induced mucin production and β-agonist-induced signaling is required. A clinically important long-acting β-agonist, formoterol, was as effective as epinephrine in potentiating IL-13 induced MUC5AC transcription. IL-13 induced mucin production in the presence of epinephrine was significantly reduced by treatment with selective inhibitors of ERK1/2 (FR180204), p38 (SB203580) and JNK (SP600125). Replacement of epinephrine with forskolin + IBMX resulted in a marked increase in mucin production in NHBE cells in response to IL-13, and treatment with the inhibitory cAMP analogue Rp-cAMPS decreased mucin levels induced by epinephrine + IL-13. Our findings suggest that β2AR signaling is required for mucin production in response to IL-13, and that mitogen activated protein kinases and cAMP are necessary for this effect. These data lend support to the notion that β2AR-agonists may contribute to asthma exacerbations by increasing mucin production via activation of β2ARs on epithelial cells. |
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AbstractList | Mucus hypersecretion by airway epithelium is a hallmark of inflammation in allergic asthma and results in airway narrowing and obstruction. Others have shown that administration a TH2 cytokine, IL-13 is sufficient to cause mucus hypersecretion in vivo and in vitro. Asthma therapy often utilizes β2-adrenoceptor (β2AR) agonists, which are effective acutely as bronchodilators, however chronic use may lead to a worsening of asthma symptoms. In this study, we asked whether β2AR signaling in normal human airway epithelial (NHBE) cells affected mucin production in response to IL-13. This cytokine markedly increased mucin production, but only in the presence of epinephrine. Mucin production was blocked by ICI-118,551, a preferential β2AR antagonist, but not by CGP-20712A, a preferential β1AR antagonist. Constitutive β2AR activity was not sufficient for IL-13 induced mucin production and β-agonist-induced signaling is required. A clinically important long-acting β-agonist, formoterol, was as effective as epinephrine in potentiating IL-13 induced MUC5AC transcription. IL-13 induced mucin production in the presence of epinephrine was significantly reduced by treatment with selective inhibitors of ERK1/2 (FR180204), p38 (SB203580) and JNK (SP600125). Replacement of epinephrine with forskolin + IBMX resulted in a marked increase in mucin production in NHBE cells in response to IL-13, and treatment with the inhibitory cAMP analogue Rp-cAMPS decreased mucin levels induced by epinephrine + IL-13. Our findings suggest that β2AR signaling is required for mucin production in response to IL-13, and that mitogen activated protein kinases and cAMP are necessary for this effect. These data lend support to the notion that β2AR-agonists may contribute to asthma exacerbations by increasing mucin production via activation of β2ARs on epithelial cells. Mucus hypersecretion by airway epithelium is a hallmark of inflammation in allergic asthma and results in airway narrowing and obstruction. Others have shown that administration a T H 2 cytokine, IL-13 is sufficient to cause mucus hypersecretion in vivo and in vitro . Asthma therapy often utilizes β 2 -adrenoceptor (β 2 AR) agonists, which are effective acutely as bronchodilators, however chronic use may lead to a worsening of asthma symptoms. In this study, we asked whether β 2 AR signaling in normal human airway epithelial (NHBE) cells affected mucin production in response to IL-13. This cytokine markedly increased mucin production, but only in the presence of epinephrine. Mucin production was blocked by ICI-118,551, a preferential β 2 AR antagonist, but not by CGP-20712A, a preferential β 1 AR antagonist. Constitutive β 2 AR activity was not sufficient for IL-13 induced mucin production and β-agonist-induced signaling is required. A clinically important long-acting β-agonist, formoterol, was as effective as epinephrine in potentiating IL-13 induced MUC5AC transcription. IL-13 induced mucin production in the presence of epinephrine was significantly reduced by treatment with selective inhibitors of ERK1/2 (FR180204), p38 (SB203580) and JNK (SP600125). Replacement of epinephrine with forskolin + IBMX resulted in a marked increase in mucin production in NHBE cells in response to IL-13, and treatment with the inhibitory cAMP analogue Rp-cAMPS decreased mucin levels induced by epinephrine + IL-13. Our findings suggest that β 2 AR signaling is required for mucin production in response to IL-13, and that mitogen activated protein kinases and cAMP are necessary for this effect. These data lend support to the notion that β 2 AR-agonists may contribute to asthma exacerbations by increasing mucin production via activation of β 2 ARs on epithelial cells. |
Author | Kim, Hosu Hernandez, Adrian Knoll, Brian J Pokkunuri, Indira Omoluabi, Ozozoma Al-Sawalha, Nour Thanawala, Vaidehi J Bond, Richard A |
AuthorAffiliation | University of Alabama at Birmingham, UNITED STATES 2 Department of Biology and Biochemistry, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America 1 Department of Pharmacological and Pharmaceutical Sciences, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America |
AuthorAffiliation_xml | – name: 1 Department of Pharmacological and Pharmaceutical Sciences, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America – name: 2 Department of Biology and Biochemistry, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America – name: University of Alabama at Birmingham, UNITED STATES |
Author_xml | – sequence: 1 givenname: Nour surname: Al-Sawalha fullname: Al-Sawalha, Nour organization: Department of Pharmacological and Pharmaceutical Sciences, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America – sequence: 2 givenname: Indira surname: Pokkunuri fullname: Pokkunuri, Indira organization: Department of Pharmacological and Pharmaceutical Sciences, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America – sequence: 3 givenname: Ozozoma surname: Omoluabi fullname: Omoluabi, Ozozoma organization: Department of Biology and Biochemistry, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America – sequence: 4 givenname: Hosu surname: Kim fullname: Kim, Hosu organization: Department of Pharmacological and Pharmaceutical Sciences, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America – sequence: 5 givenname: Vaidehi J surname: Thanawala fullname: Thanawala, Vaidehi J organization: Department of Pharmacological and Pharmaceutical Sciences, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America – sequence: 6 givenname: Adrian surname: Hernandez fullname: Hernandez, Adrian organization: Department of Biology and Biochemistry, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America – sequence: 7 givenname: Richard A surname: Bond fullname: Bond, Richard A organization: Department of Pharmacological and Pharmaceutical Sciences, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America; Department of Biology and Biochemistry, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America – sequence: 8 givenname: Brian J surname: Knoll fullname: Knoll, Brian J organization: Department of Pharmacological and Pharmaceutical Sciences, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America; Department of Biology and Biochemistry, University of Houston, 4800 Calhoun Road, Houston, Texas, 77204, United States of America |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26161982$$D View this record in MEDLINE/PubMed |
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Copyright | 2015 Al-Sawalha et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2015 Al-Sawalha et al 2015 Al-Sawalha et al |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Competing Interests: Brian J. Knoll is an Academic Editor for PLOS ONE. RA Bond is a co-inventor on a provisional patent application 2011, joint between MD Anderson and the University of Houston - "The steroid-sparing effects of betaadrenergic inverse agonists." At this point this patent has not been assigned and has no value or license agreement in place or pending issuance. RA Bond is also a minor shareholder in Invion, a company in which he was scientific co-founder. RA Bond sold off almost his entire stock ownership and now owns ~$10,000 worth of stock (as of 12 June 2015). RA Bond has no other role than shareholder with Invion, and is not on any board and has no consulting agreement. This does not alter the authors' adherence to PLOS ONE Editorial policies and criteria. Conceived and designed the experiments: BJK RAB NS. Performed the experiments: NS IP AH OO HK. Analyzed the data: NS IP RAB BJK VT. Wrote the paper: NS VT RAB BJK. Current address: Department of Clinical Pharmacy, College of Pharmacy, Jordan University of Science and Technology, Irbid, Jordan |
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Snippet | Mucus hypersecretion by airway epithelium is a hallmark of inflammation in allergic asthma and results in airway narrowing and obstruction. Others have shown... |
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SubjectTerms | Activation Adenosine Adrenergic beta-2 Receptor Agonists - pharmacology Adrenergic receptors Animals Apoptosis Asthma Binding sites Biochemistry Biology Bronchi - cytology Bronchodilators Cattle Chronic illnesses Cyclic AMP Cyclic AMP - pharmacology Cyclic AMP-Dependent Protein Kinases - metabolism Epinephrine Epinephrine - pharmacology Epithelial cells Epithelial Cells - drug effects Epithelial Cells - enzymology Epithelial Cells - metabolism Epithelium Extracellular signal-regulated kinase Formoterol Forskolin Humans Inflammation Interleukin 13 Interleukin-13 - pharmacology JNK protein Kinases Lymphocytes T MAP Kinase Signaling System - drug effects Mucin Mucin 5AC - metabolism Mucus Pathogenesis Pharmaceutical sciences Pharmacy Physiology Receptors, Adrenergic, beta-2 - metabolism Respiratory tract Rodents Signaling Transcription |
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Title | Epinephrine Activation of the β2-Adrenoceptor Is Required for IL-13-Induced Mucin Production in Human Bronchial Epithelial Cells |
URI | https://www.ncbi.nlm.nih.gov/pubmed/26161982 https://www.proquest.com/docview/1695377935/abstract/ https://search.proquest.com/docview/1696189065 https://pubmed.ncbi.nlm.nih.gov/PMC4498766 https://doaj.org/article/878dd13d12874a7e866e2d60b1e4fa78 http://dx.doi.org/10.1371/journal.pone.0132559 |
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