Allergen–Induced Sensory Neuroplasticity in Airways
This study investigates the influence of allergic inflammation in airway sensory innervation. We conclude that allergic inflammation in the guinea pig leads to both an increase in excitability, as manifested by an increase in the mechanical sensitivity of the airway nerve endings, and an induction o...
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| Published in | International archives of allergy and immunology Vol. 118; no. 2-4; pp. 150 - 153 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article Conference Proceeding |
| Language | English |
| Published |
Basel, Switzerland
Karger
01.02.1999
S. Karger AG |
| Subjects | |
| Online Access | Get full text |
| ISBN | 9783805568753 3805568754 |
| ISSN | 1018-2438 1423-0097 |
| DOI | 10.1159/000024053 |
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| Abstract | This study investigates the influence of allergic inflammation in airway sensory innervation. We conclude that allergic inflammation in the guinea pig leads to both an increase in excitability, as manifested by an increase in the mechanical sensitivity of the airway nerve endings, and an induction of substance P production in airway sensory neurons. The data are consistent with the hypothesis that the induction of substance P occurs in fast conducting nodose sensory neurons that were previously devoid of this neuropeptide. Thus, allergen challenge is associated with a phenotypic change in the airway tachykinergic innervation. We also provide evidence that nerve growth factor is a potentially important mediator for these effects, and that it is elevated in the bronchoalveolar lavage of asthmatic subjects. |
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| AbstractList | This study investigates the influence of allergic inflammation in airway sensory innervation. We conclude that allergic inflammation in the guinea pig leads to both an increase in excitability, as manifested by an increase in the mechanical sensitivity of the airway nerve endings, and an induction of substance P production in airway sensory neurons. The data are consistent with the hypothesis that the induction of substance P occurs in fast conducting nodose sensory neurons that were previously devoid of this neuropeptide. Thus, allergen challenge is associated with a phenotypic change in the airway tachykinergic innervation. We also provide evidence that nerve growth factor is a potentially important mediator for these effects, and that it is elevated in the bronchoalveolar lavage of asthmatic subjects. This study investigates the influence of allergic inflammation in airway sensory innervation. We conclude that allergic inflammation in the guinea pig leads to both an increase in excitability, as manifested by an increase in the mechanical sensitivity of the airway nerve endings, and an induction of substance P production in airway sensory neurons. The data are consistent with the hypothesis that the induction of substance P occurs in fast conducting nodose sensory neurons that were previously devoid of this neuropeptide. Thus, allergen challenge is associated with a phenotypic change in the airway tachykinergic innervation. We also provide evidence that nerve growth factor is a potentially important mediator for these effects, and that it is elevated in the bronchoalveolar lavage of asthmatic subjects.This study investigates the influence of allergic inflammation in airway sensory innervation. We conclude that allergic inflammation in the guinea pig leads to both an increase in excitability, as manifested by an increase in the mechanical sensitivity of the airway nerve endings, and an induction of substance P production in airway sensory neurons. The data are consistent with the hypothesis that the induction of substance P occurs in fast conducting nodose sensory neurons that were previously devoid of this neuropeptide. Thus, allergen challenge is associated with a phenotypic change in the airway tachykinergic innervation. We also provide evidence that nerve growth factor is a potentially important mediator for these effects, and that it is elevated in the bronchoalveolar lavage of asthmatic subjects. From Molecular Science to the Treatment of Allergy This study investigates the influence of allergic inflammation in airway sensory innervation. We conclude that allergic inflammation in the guinea pig leads to both an increase in excitability, as manifested by an increase in the mechanical sensitivity of the airway nerve endings, and an induction of substance P production in airway sensory neurons. The data are consistent with the hypothesis that the induction of substance P occurs in fast conducting nodose sensory neurons that were previously devoid of this neuropeptide. Thus, allergen challenge is associated with a phenotypic change in the airway tachykinergic innervation. We also provide evidence that nerve growth factor is a potentially important mediator for these effects, and that it is elevated in the bronchoalveolar lavage of asthmatic subjects. |
| Author | Undem, Bradley J. Hunter, Dawn D. Fischer, Axel Liu, Mark Haak-Frendscho, Mary Oakragly, Angela |
| Author_xml | – sequence: 1 givenname: Bradley J. surname: Undem fullname: Undem, Bradley J. – sequence: 2 givenname: Dawn D. surname: Hunter fullname: Hunter, Dawn D. – sequence: 3 givenname: Mark surname: Liu fullname: Liu, Mark – sequence: 4 givenname: Mary surname: Haak-Frendscho fullname: Haak-Frendscho, Mary – sequence: 5 givenname: Angela surname: Oakragly fullname: Oakragly, Angela – sequence: 6 givenname: Axel surname: Fischer fullname: Fischer, Axel |
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| Cites_doi | 10.1016/0166-2236(91)90024-O 10.1016/0165-1838(93)90376-6 10.1016/0165-1838(93)90375-5 10.1016/0306-4522(92)90239-X 10.1146/annurev.neuro.19.1.289 10.1073/pnas.93.20.10955 |
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| Copyright | 1999 S. Karger AG, Basel 1999 INIST-CNRS Copyright (c) 1999 S. Karger AG, Basel |
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| Keywords | Bronchus Sensory nerve Vagus nerve Substance P Neuropeptide Allergy Animal model Innervation Peptide hormone Nerve growth factor Respiratory tract Guinea pig Obstructive pulmonary disease Immunopathology Respiratory disease Mechanoreception Cytokine Rodentia Inflammation Asthma Vertebrata Mammalia Polypeptide Animal Tachykinin Growth factor |
| Language | English |
| License | Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher. https://www.karger.com/Services/SiteLicenses CC BY 4.0 |
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| References | Lewin GR, Barde Y-A: Physiology of the neurotrophins. Annu Rev Neurosci 1996;19: 289-317.883344510.1146/annurev.neuro.19.1.289 Leon A, Buriani A, Toso RD, Fabris M, Romanello S, Aloe L, Levi-Montalcini R: Mast cells synthesize, store, and relase nerve growth factor. Proc Natl Acad Sci USA 1994;91: 3739-3743.8170980 Fujishima H, Takeyama M, Takeuchi T, Saito I, Tsubota K: Elevated levels of substance P in tears of patients with allergic conjunctivitis and vernal keratoconjunctivitis. Clin Exp Allergy 1997;27:372-378.9146929 Woolf CJ, Walter ET: Common patterns of plasticity contributing to nociceptive sensitization in mammals and Aplysia. Trends Neurosci 1991;14:74-78.170854010.1016/0166-2236(91)90024-O Riccio M, Kummer W, Myers AC, Undem BJ: Interganglionic segregation of airway vagal afferent fiber phenotypes. J Physiol 1996;496: 521-530.8910234 Dmitrieva N, Shelton D, Rice ASC, McMahon SB: The role of nerve growth factor in a model of visceral inflammation. Neuroscience 1997; 78:449-459.9145801 Keränen U, Kiviluoto T, Järvinen H, Bäck N, Kivilaakso E, Soinila S: Changes in substance P-immunoreactive innervation of human colon associated with ulcerative colitis. Dig Dis Sci 1995;40:2250-2258.7587798 Levi-Montalcini R, Skaper SD, DalToso R, Petrelli L, Leon A: Nerve growth factor: From neurotrophin to neurokine. Trends Neurosci 1996;19:514-520.8931279 Dmitrieva N, McMahon SB: Sensitisation of visceral afferents by nerve growth factor in the adult rat. Pain 1996;66:87-97.8857635 Fischer A, McGregor GP, Saria A, Philippin B, Kummer W: Induction of tachykinin gene and peptide expression in guinea pig nodose primary afferent neurons by allergic airway inflammation. J Clin Invest 1996;98:2284-2291.8941645 Sharkey KA: Substance P and calcitonin gene-related peptide (CGRP) in gastrointestinal inflammation. Ann NY Acad Sci 1992;664:425- 442.1280934 Undem BJ, Weinreich D: Electrophysiological properties and chemosensitivity of guinea pig nodose ganglion neurons in vitro. J Auton Nerv Syst 1993;44:17-34.810497010.1016/0165-1838(93)90375-5 Galeazza MT, Garry MG, Yost HJ, Strait KA, Hargreves KM, Seybold VS: Plasticity in the synthesis and storage of substance P and calcitonin gene-related peptide in primary afferent neurons during peripheral inflammation. Neuroscience 1995;66:443-458.7477885 Bonini S, Lambiase A, Bonini S, Angelucci F, Magrini L, Manni L, Aloe L: Circulating nerve growth factor levels are increased in humans with allergic diseases and asthma. Proc Natl Acad Sci USA 1996;93:10955-10960.885529010.1073/pnas.93.20.10955 Undem BJ, Hubbard W, Weinreich D: Immunologically induced neuromodulation of guinea pig nodose ganglion neurons. J Auton Nerv Syst 1993;44:35-44.769191810.1016/0165-1838(93)90376-6 Pedersen KE, Meeker SN, Riccio MM, Undem BJ: Selective stimulation of jugular ganglion afferent neurons in guinea pig airways by hypertonic saline. Am Rev Crit Care Med 1998; 84:499-506. Riccio MM, Myers AC, Undem BJ: Immunomodulation of afferent neurons in guinea-pig isolated airway. J Physiol 1996;491:499-509.8866873 Kummer W, Fischer A, Kurkowski R, Heym C: The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labeling immunohistochemistry. Neuroscience 1992; 49:715-737.138014010.1016/0306-4522(92)90239-X ref2 ref1 ref4 ref3 ref6 ref5 |
| References_xml | – reference: Riccio MM, Myers AC, Undem BJ: Immunomodulation of afferent neurons in guinea-pig isolated airway. J Physiol 1996;491:499-509.8866873 – reference: Undem BJ, Weinreich D: Electrophysiological properties and chemosensitivity of guinea pig nodose ganglion neurons in vitro. J Auton Nerv Syst 1993;44:17-34.810497010.1016/0165-1838(93)90375-5 – reference: Keränen U, Kiviluoto T, Järvinen H, Bäck N, Kivilaakso E, Soinila S: Changes in substance P-immunoreactive innervation of human colon associated with ulcerative colitis. Dig Dis Sci 1995;40:2250-2258.7587798 – reference: Leon A, Buriani A, Toso RD, Fabris M, Romanello S, Aloe L, Levi-Montalcini R: Mast cells synthesize, store, and relase nerve growth factor. Proc Natl Acad Sci USA 1994;91: 3739-3743.8170980 – reference: Kummer W, Fischer A, Kurkowski R, Heym C: The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labeling immunohistochemistry. Neuroscience 1992; 49:715-737.138014010.1016/0306-4522(92)90239-X – reference: Riccio M, Kummer W, Myers AC, Undem BJ: Interganglionic segregation of airway vagal afferent fiber phenotypes. J Physiol 1996;496: 521-530.8910234 – reference: Levi-Montalcini R, Skaper SD, DalToso R, Petrelli L, Leon A: Nerve growth factor: From neurotrophin to neurokine. Trends Neurosci 1996;19:514-520.8931279 – reference: Dmitrieva N, Shelton D, Rice ASC, McMahon SB: The role of nerve growth factor in a model of visceral inflammation. Neuroscience 1997; 78:449-459.9145801 – reference: Dmitrieva N, McMahon SB: Sensitisation of visceral afferents by nerve growth factor in the adult rat. Pain 1996;66:87-97.8857635 – reference: Sharkey KA: Substance P and calcitonin gene-related peptide (CGRP) in gastrointestinal inflammation. Ann NY Acad Sci 1992;664:425- 442.1280934 – reference: Galeazza MT, Garry MG, Yost HJ, Strait KA, Hargreves KM, Seybold VS: Plasticity in the synthesis and storage of substance P and calcitonin gene-related peptide in primary afferent neurons during peripheral inflammation. Neuroscience 1995;66:443-458.7477885 – reference: Woolf CJ, Walter ET: Common patterns of plasticity contributing to nociceptive sensitization in mammals and Aplysia. Trends Neurosci 1991;14:74-78.170854010.1016/0166-2236(91)90024-O – reference: Fischer A, McGregor GP, Saria A, Philippin B, Kummer W: Induction of tachykinin gene and peptide expression in guinea pig nodose primary afferent neurons by allergic airway inflammation. J Clin Invest 1996;98:2284-2291.8941645 – reference: Fujishima H, Takeyama M, Takeuchi T, Saito I, Tsubota K: Elevated levels of substance P in tears of patients with allergic conjunctivitis and vernal keratoconjunctivitis. Clin Exp Allergy 1997;27:372-378.9146929 – reference: Undem BJ, Hubbard W, Weinreich D: Immunologically induced neuromodulation of guinea pig nodose ganglion neurons. J Auton Nerv Syst 1993;44:35-44.769191810.1016/0165-1838(93)90376-6 – reference: Bonini S, Lambiase A, Bonini S, Angelucci F, Magrini L, Manni L, Aloe L: Circulating nerve growth factor levels are increased in humans with allergic diseases and asthma. Proc Natl Acad Sci USA 1996;93:10955-10960.885529010.1073/pnas.93.20.10955 – reference: Lewin GR, Barde Y-A: Physiology of the neurotrophins. Annu Rev Neurosci 1996;19: 289-317.883344510.1146/annurev.neuro.19.1.289 – reference: Pedersen KE, Meeker SN, Riccio MM, Undem BJ: Selective stimulation of jugular ganglion afferent neurons in guinea pig airways by hypertonic saline. Am Rev Crit Care Med 1998; 84:499-506. – ident: ref4 doi: 10.1016/0166-2236(91)90024-O – ident: ref2 doi: 10.1016/0165-1838(93)90376-6 – ident: ref1 doi: 10.1016/0165-1838(93)90375-5 – ident: ref3 doi: 10.1016/0306-4522(92)90239-X – ident: ref5 doi: 10.1146/annurev.neuro.19.1.289 – ident: ref6 doi: 10.1073/pnas.93.20.10955 |
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| SubjectTerms | Allergens - immunology Allergic diseases Animals Biological and medical sciences Guinea Pigs Immunopathology Medical sciences Neuronal Plasticity - immunology Neurons, Afferent - immunology Neuro–Immune Interactions Respiratory and ent allergic diseases Respiratory System - immunology Respiratory System - innervation Substance P - immunology |
| Title | Allergen–Induced Sensory Neuroplasticity in Airways |
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