Startseite Lebenswissenschaften Changes in expression of neurotrophins and neurotrophic factors in the model of eosinophilic inflammation of the esophageal mucosa
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Changes in expression of neurotrophins and neurotrophic factors in the model of eosinophilic inflammation of the esophageal mucosa

  • Mariana Brozmanová EMAIL logo , Jozef Hatok , Michal Hennel , Miloš Tatár und Andrea Vážanová
Veröffentlicht/Copyright: 29. Dezember 2017
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Biologia
Aus der Zeitschrift Biologia Band 72 Heft 11

Abstract

Esophageal sensory and motor nerves contribute to the symptoms of eosinophilic esophagitis, however, the mechanisms of this neural dysfunction are essentially unknown. We addressed the hypothesis that eosinophilic inflammation in the esophagus alters production of the key regulators of neural function neurotrophins and neurotrophic factors. We developed and optimized the model of allergic eosinophilic inflammation of esophageal mucosa induced by localized administration of allergen ovalbumin into the esophagus in ovalbumin-sensitized guinea pigs. We evaluated changes in expression of nerve growth factor (NGF), brain-derived neurotrophic factor (BDNF), glial cell-derived neurotrophic factor (GDNF) and artemin in esophageal mucosa by quantitative RT-PCR. We found that the administration of ovalbumin into the esophageal wall of sensitized animals induced a massive eosinophilic infiltration restricted to esophageal mucosa (3 ± 1 vs. 97 ± 23 eosinophils per high power filed). This inflammatory response altered the expression profile of selected neurotrophic factors. The BDNF mRNA was increased (to 200%), artemin mRNA was decreased (to 50%) while NGF and GDNF was not changed. We conclude that a strong eosinophilic inflammation can be induced in guinea pigs and alters the expression of neurotrophins and neurotrophic factors. Our findings will aid mechanistic studies of neural dysfunction in eosinophilic esophagitis.

Acknowledgements

This work was supported by grant Vega 1/0070/15 and by project “Biomedical Center Martin” ITMS code: 26220220 187, co-financed by EU sources.

References

Airaksinen M.S. & Saarma M. 2002. The GDNF family: signalling, biological functions and therapeutic value. Nat. Rev. Neurosci. 3 (2): 383–394. 10.1038/nrn812Suche in Google Scholar PubMed

Bergren D.R. 2001. Enhanced lung C-fiber responsiveness in sensitized adult guinea pigs exposed to chronic tobacco smoke. J. Appl. Physiol.91 (4): 1645–1654. PMID: 1156814610.1152/jappl.2001.91.4.1645Suche in Google Scholar PubMed

Bespalov M.M. & Saarma M. 2007. GDNF family receptor complexes are emerging drug targets. Trends Pharmacol. Sci. 28 (2): 68–74. 10.1016/j.tips.2006.12.0057Suche in Google Scholar PubMed

Brozmanova M., Plevkova J., Tatar M. & Kollarik M. 2008. Cough reflex sensitivity is increased in the guinea pig model of allergic rhinitis. J. Physiol. Pharmacol. 59 (Suppl 6): 153–161. PMID: 19218639Suche in Google Scholar PubMed

Cianferoni A. & Spergel J. 2016. Eosinophilic esophagitis: A comprehensive review. Clin. Rev. Allergy Immunol. 50 (2): 159–174. 10.1007/s12016-015-8501-zSuche in Google Scholar PubMed

Ciobanu C., Reid G. & Babes A. 2009. Acute and chronic effects of neurotrophic factors BDNF and GDNF on responses mediated by thermo-sensitive TRP channels in cultured rat dorsal root ganglion neurons. Brain. Res. 1284: 54–67. 10.1016/j.brainres.2009.06.014Suche in Google Scholar PubMed

de Vries A., Engels F., Henricks P.A., Leusink-Muis T., McGregor G.P., Braun A., Groneberg D.A., Dessing M.C., Nijkamp F.P. & Fischer A. 2006. Airway hyper-responsiveness in allergic asthma in guinea-pigs is mediated by nerve growth factor via the induction of substance P: a potential role for trkA. Clin. Exp. Allergy 36 (9): 1192–1200. 10.1111/j.1365-2222.2006.02549.xSuche in Google Scholar PubMed

Dusenkova S., Ru F., Surdenikova L., Nassenstein C., Hatok J., Dusenka R., Banovcin P. Jr., Kliment J., Tatar M. & Kollarik M. 2014. The expression profile of acid-sensing ion channel (ASIC) subunits ASIC1a, ASIC1b, ASIC2a, ASIC2b, and ASIC3 in the esophageal vagal afferent nerve subtypes. Am. J. Physiol. Gastrointest. Liver Physiol. 307: G922–G930. 10.1152/ajpgi.00129.2014Suche in Google Scholar PubMed PubMed Central

Falempin M., Madhloum A. & Rousseau J.P. 1986. Effects of vagal deafferentation on oesophageal motility and transit in the sheep. J. Physiol. 372: 425–436. 10.1007/978-94-010-9352-l_lSuche in Google Scholar PubMed

Fasanella K.E., Christianson J.A., Chanthaphavong R.S. & Davis B.M. 2008. Distribution and neurochemical identification of pancreatic afferents in the mouse. J. Comp. Neurol. 509 (1): 42–52. 10.1002/cne.21736Suche in Google Scholar PubMed PubMed Central

Hu Y., Liu Z., Yu X., Pasricha P.J., Undem B.J. & Yu S. 2014. Increased acid responsiveness in vagal sensory neurons in a guinea pig model of eosinophilic esophagitis. Am. J. Physiol. Gastrointest. Liver Physiol. 307 (2): G149–G157. 10.1152/ajpgi.00097.2014Suche in Google Scholar PubMed PubMed Central

Hunter D.D. & Undem B.J. 1999. Identification and substance P content of vagal afferent neurons innervating the epithelium of the guinea pig trachea. Am. J. Respir. Crit. Care Med. 159: 1943–1948. 10.1164/ajrccm.159.6.9808078Suche in Google Scholar PubMed

Kashiba H., Uchida Y. & Senba E. 2003. Distribution and colocalization of NGF and GDNF family ligand receptor mRNAs in dorsal root and nodose ganglion neurons of adult rats. Brain. Res. Mol. Brain. Res. 110 (1): 52–62. 10.1016/S0169-328X(02)00584-3Suche in Google Scholar PubMed

Kavitt R.T., Hirano I. & Vaezi M.F. 2016. Diagnosis and treatment of eosinophilic esophagitis in adults. Am. J. Med. 129 (9): 924–934. 10.1016/j.amjmed.2016.04.024Suche in Google Scholar PubMed

Khan N. & Smith M.T. 2015. Neurotrophins and neuropathic pain: Role in pathobiology. molecules. Molecules 20 (6): 10657–10688. 10.3390/molecules200610657Suche in Google Scholar PubMed PubMed Central

Kollarik M., Ru F. & Brozmanova M. 2010. Vagal afferent nerves with the properties of nociceptors. Auton. Neurosci. 153 (1-2): 12–20. 10.1016/j.autneu.2009.08.001Suche in Google Scholar PubMed PubMed Central

Lieu T., Kollarik M., Myers A.C. & Undem B.J. 2011. Neurotrophin- and GDNF family ligand-receptor expression in vagal sensory nerve subtypes innervating the adult guinea pig respiratory tract. Am. J. Physiol. Lung Cell Mol. Physiol. 300: L790–798. 10.1152/ajplung.00449.2010Suche in Google Scholar PubMed PubMed Central

Lieu T.M., Myers A.C., Meeker S. & Undem B.J. 2012. TRPV1 induction in airway vagal low-threshold mechanosensory neurons by allergen challenge and neurotrophic factors. Am. J. Physiol. Lung Cell Mol. Physiol. 302 (9): L941–948. 10.1152/ajplung.00366.2011Suche in Google Scholar PubMed PubMed Central

Mishra A., Hogan S.P., Brandt E.B. & Rothenberg M.E. 2001. An etiological role for aeroallergens and eosinophils in experimental esophagitis. J. Clin. Invest. 107: 83–90. 10.1172/JCI10224Suche in Google Scholar PubMed PubMed Central

Page A.J. & Blackshaw L.A. 2009. Roles of gastro-oesophageal afferents in the mechanisms and symptoms of reflux disease, pp. 227–257. 10.1007/978-3-540-79090-7_7q. In: Canning B. & Spina D. (eds), Sensory Nerves. Handbook of Experimental Pharmacology, vol. 194, Springer, Berlin, Heidelberg, 637 pp. ISBN-13: 978-3662518465, ISBN-10: 3662518465Suche in Google Scholar

Reichardt L.F. 2006. Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 361 (1473): 1545–1564. 10.1098/rstb.2006.1894Suche in Google Scholar PubMed PubMed Central

Rothenberg M.E. 2015. Molecular, genetic, and cellular bases for treating eosinophilic esophagitis. Gastroenterology 148 (6): 1143–1157. 10.1053/j.gastro.2015.02.002Suche in Google Scholar PubMed PubMed Central

Ru F., Surdenikova L., Brozmanova M. & Kollarik M. 2011. Adenosine-induced activation of esophageal nociceptors. Am. J. Physiol. Gastrointest. Liver Physiol. 300 (3): G485–G493. 10.1152/ajpgi.00361.2010Suche in Google Scholar PubMed PubMed Central

Skappak C., Ilarraza R., Wu Y.Q., Drake M.G. & Adamko D.J. 2017. Virus-induced asthma attack: The importance of allergic inflammation in response to viral antigen in an animal model of asthma. PLoS One 12: e0181425. 10.1371/journal.pone.0181425Suche in Google Scholar PubMed PubMed Central

Sengupta J.N. & Shaker R. 2005. Vagal afferent nerve stimulated reflexes in the GI tract, pp. 379–401. In: Undem B.J. & Weinreich D. (eds), Advances in Vagal Afferent Neurobiology, CRC Taylor & Francis, New York, 556 pp. ISBN: 0203492315, 978020349231410.1201/9780203492314.pt6Suche in Google Scholar

Surdenikova L., Ru F., Nassenstein C., Tatar M. & Kollarik M. 2012. The neural crest- and placodes-derived afferent innervation of the mouse esophagus. Neurogastroenterol. Motil. 24: e517-525. 10.1111/nmo.12002Suche in Google Scholar PubMed

Weinkauf B., Rukwied R., Quiding H., Dahllund L., Johansson P. & Schmelz M. 2012. Local gene expression changes after UV-irradiation of human skin. PLoS One 7: e39411. 10.1371/journal.pone.0039411Suche in Google Scholar PubMed PubMed Central

Yu S., Kollarik M., Ouyang A., Myers A.C. & Undem B.J. 2007. Mast cell-mediated long-lasting increases in excitability of vagal C-fibers in guinea pig esophagus. Am. J. Physiol. Gastrointest. Liver. Physiol. 293 (4): G850–G856. 10.1152/ajpgi.00277.2007Suche in Google Scholar PubMed

Yu S., Ru F., Ouyang A. & Kollarik M. 2008. 5-Hydroxytryptamine selectively activates the vagal nodose C-fibre subtype in the guinea-pig oesophagus. Neurogastroenterol. Motil. 20 (9): 1042–1050. 10.1111/j.1365-2982.2008.01136.x.Suche in Google Scholar PubMed

Yu S., Undem B.J. & Kollarik M. 2005. Vagal afferent nerves with nociceptive properties in guinea-pig oesophagus. J. Physiol. 563 (3): 831–842. 10.1113/jphysiol.2004.079574Suche in Google Scholar PubMed PubMed Central

Yu X., Hu Y., Ru F., Kollarik M., Undem B.J. & Yu S. 2015. TRPM8 function and expression in vagal sensory neurons and afferent nerves innervating guinea pig esophagus. Am. J. Physiol. Gastrointest. Liver Physiol. 308 (6): G489–496. 10.1152/ajpgi.00336.2014Suche in Google Scholar PubMed PubMed Central

Received: 2017-6-14
Accepted: 2017-8-3
Published Online: 2017-12-29
Published in Print: 2017-11-27

© 2017 Institute of Zoology, Slovak Academy of Sciences

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