Am. J. Respir. Crit. Care Med., Volume 159, Number 6, June 1999, 1943-1948

Identification and Substance P Content of Vagal Afferent Neurons Innervating the Epithelium of the Guinea Pig Trachea

DAWN D. HUNTER and BRADLEY J. UNDEM

The Johns Hopkins Medical Institution, Department of Medicine, Division of Clinical Immunology, The Asthma and Allergy Center, Baltimore, Maryland

Both the nodose and jugular vagal ganglia provide sensory innervation to the airways. The purpose of this study was to localize and characterize the substance P (SP) content of vagal afferent neurons that project specifically to the tracheal epithelium. A retrograde neuronal tracer, fast blue dye or rhodamine-labeled latex microspheres, was instilled into the guinea pig trachea. After 7 d, the nodose and jugular ganglia were removed, sectioned, and prepared for immunocytochemistry. Sections of tracheal mucosa demonstrated that fast blue dye diffused throughout the airway wall, whereas the rhodamine-labeled microspheres, as expected, did not penetrate the basement membrane and were thus localized to the epithelium. When the diffusible fast blue dye was used, approximately 60% of the labeled neurons were found in the nodose ganglia and 40% in the jugular ganglia. By contrast, when the beads were used to label only epithelial nerve fibers, 97 ± 1% of the tracheal neurons taking up the dye were derived from jugular neurons, 60 ± 6% of which contained SP immunoreactivity. These studies demonstrate that, in contrast to the submucosa, nerve fibers innervating the epithelium of the trachea are derived nearly exclusively from neurons with cell bodies in the jugular ganglia.

This article has been cited by other articles:

				J. P. Ianowski, J. Y. Choi, J. J. Wine, and J. W. Hanrahan Mucus secretion by single tracheal submucosal glands from normal and cystic fibrosis transmembrane conductance regulator knockout mice J. Physiol., April 1, 2007; 580(1): 301 - 314. [Abstract] [Full Text] [PDF]

				B. J. Canning, D. G. Farmer, and N. Mori Mechanistic studies of acid-evoked coughing in anesthetized guinea pigs Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2006; 291(2): R454 - R463. [Abstract] [Full Text] [PDF]

				Z.-X. Wu and R. D. Dey Nerve growth factor-enhanced airway responsiveness involves substance P in ferret intrinsic airway neurons Am J Physiol Lung Cell Mol Physiol, July 1, 2006; 291(1): L111 - L118. [Abstract] [Full Text] [PDF]

				B. J. Canning Anatomy and Neurophysiology of the Cough Reflex: ACCP Evidence-Based Clinical Practice Guidelines Chest, January 1, 2006; 129(1_suppl): 33S - 47S. [Abstract] [Full Text] [PDF]

				B. J. Canning, S. B. Mazzone, S. N. Meeker, N. Mori, S. M. Reynolds, and B. J. Undem Identification of the tracheal and laryngeal afferent neurones mediating cough in anaesthetized guinea-pigs J. Physiol., June 1, 2004; 557(2): 543 - 558. [Abstract] [Full Text] [PDF]

				B. J. Undem, B. Chuaychoo, M.-G. Lee, D. Weinreich, A. C. Myers, and M. Kollarik Subtypes of vagal afferent C-fibres in guinea-pig lungs J. Physiol., May 1, 2004; 556(3): 905 - 917. [Abstract] [Full Text] [PDF]

				Z.-X. Wu, B. E. Satterfield, and R. D. Dey Substance P released from intrinsic airway neurons contributes to ozone-enhanced airway hyperresponsiveness in ferret trachea J Appl Physiol, August 1, 2003; 95(2): 742 - 750. [Abstract] [Full Text] [PDF]

				J. B. Morris, P. T. Symanowicz, J. E. Olsen, R. S. Thrall, M. M. Cloutier, and A. K. Hubbard Immediate sensory nerve-mediated respiratory responses to irritants in healthy and allergic airway-diseased mice J Appl Physiol, April 1, 2003; 94(4): 1563 - 1571. [Abstract] [Full Text] [PDF]

				B. J. Undem, E. J. Oh, E. Lancaster, and D. Weinreich Effect of Extracellular Calcium on Excitability of Guinea Pig Airway Vagal Afferent Nerves J Neurophysiol, March 1, 2003; 89(3): 1196 - 1204. [Abstract] [Full Text] [PDF]

				J. P. Lamb and M. P. Sparrow Three-Dimensional Mapping of Sensory Innervation with Substance P in Porcine Bronchial Mucosa: Comparison with Human Airways Am. J. Respir. Crit. Care Med., November 1, 2002; 166(9): 1269 - 1281. [Abstract] [Full Text] [PDF]

				Z.-X. Wu, B. E. Satterfield, J. S. Fedan, and R. D. Dey Interleukin-1beta -induced airway hyperresponsiveness enhances substance P in intrinsic neurons of ferret airway Am J Physiol Lung Cell Mol Physiol, November 1, 2002; 283(5): L909 - L917. [Abstract] [Full Text] [PDF]

				K. Kwong and L.-Y. Lee PGE2 sensitizes cultured pulmonary vagal sensory neurons to chemical and electrical stimuli J Appl Physiol, October 1, 2002; 93(4): 1419 - 1428. [Abstract] [Full Text] [PDF]

				M. J. Carr, D. D. Hunter, D. B. Jacoby, and B. J. Undem Expression of Tachykinins in Nonnociceptive Vagal Afferent Neurons during Respiratory Viral Infection in Guinea Pigs Am. J. Respir. Crit. Care Med., April 15, 2002; 165(8): 1071 - 1075. [Abstract] [Full Text] [PDF]

				K. Kwong, Z.-X. Wu, M. L. Kashon, K. M. Krajnak, P. M. Wise, and L.-Y. Lee Chronic Smoking Enhances Tachykinin Synthesis and Airway Responsiveness in Guinea Pigs Am. J. Respir. Cell Mol. Biol., September 1, 2001; 25(3): 299 - 305. [Abstract] [Full Text] [PDF]

				Z.-X. Wu, D. F. Maize Jr., B. E. Satterfield, D. G. Frazer, J. S. Fedan, and R. D. Dey Role of intrinsic airway neurons in ozone-induced airway hyperresponsiveness in ferret trachea J Appl Physiol, July 1, 2001; 91(1): 371 - 378. [Abstract] [Full Text] [PDF]

				M. J. CARR, N. M. SCHECHTER, and B. J. UNDEM Trypsin-induced, Neurokinin-mediated Contraction of Guinea Pig Bronchus Am. J. Respir. Crit. Care Med., November 1, 2000; 162(5): 1662 - 1667. [Abstract] [Full Text]