Innervation of tracheal parasympathetic ganglia by esophageal cholinergic neurons: evidence from anatomic and functional studies in guinea pigs - PubMed

Affiliations

• PMID: 20061441
• DOI: 10.1152/ajplung.00166.2009

Free article

Innervation of tracheal parasympathetic ganglia by esophageal cholinergic neurons: evidence from anatomic and functional studies in guinea pigs

Stuart B Mazzone et al. Am J Physiol Lung Cell Mol Physiol. 2010 Mar.

Free article

Abstract

In the present study, we describe a subset of nerve fibers, characterized by their immunoreactivity for the calcium-binding protein calretinin, that are densely and selectively associated with cholinergic postganglionic neurons in the guinea pig tracheal ganglia. Retrograde neuronal tracing with cholera toxin B, combined with immunohistochemical analyses, showed that these nerve fibers do not originate from sensory neurons in the nodose, jugular, or dorsal root ganglia or from motor neurons in the nucleus ambiguus, dorsal motor nucleus of the vagus nerve, spinal cord, stellate ganglia, or superior cervical ganglia. Calretinin-immunoreactive nerve fibers disappeared from tracheal segments after 48 h in organotypic culture, indicating that the fibers were of extrinsic origin. However, calretinin-positive nerve fibers persisted in tracheal ganglia when tracheae were cocultured with the adjacent esophagus intact. Immunohistochemical analysis of the esophagus revealed a population of cholinergic neurons in the esophageal myenteric plexus that coexpressed calretinin. In functional studies, electrical stimulation of the esophagus in vitro evoked measurable contractions of the trachea. These contractions were not altered by prior organotypic culture of the trachea and esophagus to remove the extrinsic innervation to the airways but were significantly (P < 0.05) inhibited by the ganglionic blocker hexamethonium or by physical disruption of the tissue connecting the trachea and esophagus. These data suggest that a subset of esophageal neurons, characterized by the expression of calretinin and acetylcholine, provide a previously unrecognized excitatory input to tracheal cholinergic ganglia in guinea pigs.

Similar articles

• Evidence that distinct neural pathways mediate parasympathetic contractions and relaxations of guinea-pig trachealis.

  Canning BJ, Undem BJ. Canning BJ, et al. J Physiol. 1993 Nov;471:25-40. doi: 10.1113/jphysiol.1993.sp019889. J Physiol. 1993. PMID: 7907144 Free PMC article.

• The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labelling immunohistochemistry.

  Kummer W, Fischer A, Kurkowski R, Heym C. Kummer W, et al. Neuroscience. 1992 Aug;49(3):715-37. doi: 10.1016/0306-4522(92)90239-x. Neuroscience. 1992. PMID: 1380140

• Origin of neuronal nitric oxide synthase (NOS)-immunoreactive fibers in guinea pig parasympathetic cardiac ganglia.

  Calupca MA, Vizzard MA, Parsons RL. Calupca MA, et al. J Comp Neurol. 2000 Oct 23;426(3):493-504. J Comp Neurol. 2000. PMID: 10992251

• Innervation of the carotid body: Immunohistochemical, denervation, and retrograde tracing studies.

  Ichikawa H. Ichikawa H. Microsc Res Tech. 2002 Nov 1;59(3):188-95. doi: 10.1002/jemt.10193. Microsc Res Tech. 2002. PMID: 12384963 Review.

Cited by

• Histological, immunohistochemical and transcriptomic characterization of human tracheoesophageal fistulas.

  Brosens E, Felix JF, Boerema-de Munck A, de Jong EM, Lodder EM, Swagemakers S, Buscop-van Kempen M, de Krijger RR, Wijnen RMH, van IJcken WFJ, van der Spek P, de Klein A, Tibboel D, Rottier RJ. Brosens E, et al. PLoS One. 2020 Nov 17;15(11):e0242167. doi: 10.1371/journal.pone.0242167. eCollection 2020. PLoS One. 2020. PMID: 33201890 Free PMC article.

• The effect of hyperpolarization-activated cyclic nucleotide-gated ion channel inhibitors on the vagal control of guinea pig airway smooth muscle tone.

  McGovern AE, Robusto J, Rakoczy J, Simmons DG, Phipps S, Mazzone SB. McGovern AE, et al. Br J Pharmacol. 2014 Aug;171(15):3633-50. doi: 10.1111/bph.12745. Br J Pharmacol. 2014. PMID: 24762027 Free PMC article.

• Expression of Sex Steroid Hormone Receptors in Vagal Motor Neurons Innervating the Trachea and Esophagus in Mouse.

  Mukudai S, Ichi Matsuda K, Bando H, Takanami K, Nishio T, Sugiyama Y, Hisa Y, Kawata M. Mukudai S, et al. Acta Histochem Cytochem. 2016 Feb 27;49(1):37-46. doi: 10.1267/ahc.15037. Epub 2016 Feb 24. Acta Histochem Cytochem. 2016. PMID: 27006520 Free PMC article.

• Mechanisms of airway responses to esophageal acidification in cats.

  Lang IM, Haworth ST, Medda BK, Forster H, Shaker R. Lang IM, et al. J Appl Physiol (1985). 2016 Apr 1;120(7):774-83. doi: 10.1152/japplphysiol.00758.2015. Epub 2016 Feb 4. J Appl Physiol (1985). 2016. PMID: 26846551 Free PMC article.

• Airway smooth muscle in airway reactivity and remodeling: what have we learned?

  Prakash YS. Prakash YS. Am J Physiol Lung Cell Mol Physiol. 2013 Dec;305(12):L912-33. doi: 10.1152/ajplung.00259.2013. Epub 2013 Oct 18. Am J Physiol Lung Cell Mol Physiol. 2013. PMID: 24142517 Free PMC article. Review.

Publication types

MeSH terms

Substances

LinkOut - more resources

• Full Text Sources

  • Atypon