Pulmonary neuroepithelial bodies are innervated by vagal afferent nerves: An investigation with in vivo anterograde Dil tracing and confocal microscopy

Anatomy and Embryology

Volumn 197, Issue 4, 1998, Pages 325-330

  Van Lommel, A ^b   Lauweryns, J M ^b   Berthoud, H R ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Airways; Chemoreceptors; Lung; Nerve endings; Respiratory system

Indexed keywords

AIRWAY; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; FROZEN SECTION; LUNG; MALE; MITOCHONDRION; NERVE ENDING; NEUROEPITHELIUM; NODOSE GANGLION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE; VAGUS NERVE;

ANIMALIA;

EID: 0031966346     PISSN: 03402061     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004290050142     Document Type: Article

References (47)

1. Adriaensen D, Scheuermann DW, Gomi T, Kimura A, Timmermans JP, De Groodt-Lasseel MHA (1994) The pulmonary neuroepithelial endocrine system in the quail Coturnix coturnix. Light-and electron-microscopical immunocytochemistry and morphology. Anat Rec 239: 65-74
2. Balaguer L, Romano J (1991) Solitary neuroendocrine cells and neuroepithelial bodies in the lower airways of embryonic, fetal, and postnatal sheep. Anat Rec 231: 333-338
3. Beorlegui C, Sesma P, Martinez A (1994) Colocalization of immunoreactivities to serotonin, calcitonin and CGRP in endocrine pulmonary cells of the iberian lizard Podarcis hispanica (Reptilia). Tissue Cell 26: 817-825
4. Berthoud HR, Powley TL (1992) Vagal afferent innervation of the rat fundic stomach: morphological characterization of the gastric tension receptor. J Comp Neurol 319: 261-276
5. Berthoud HR, Kressel M, Neuhuber WL (1992) An anterograde tracing study of the vagal innervation of rat liver, portal vein and biliary system. Anat Embryol 186: 431-442
6. Berthoud HR, Kressel M, Raybould HE, Neuhuber WL (1995) Vagal sensors in the rat duodenal mucosa: distribution and structure as revealed by in vivo Dil-tracing. Anat Embryol 191: 203-212
7. Cervero F (1994) Sensory innervation of the viscera: peripheral basis of visceral pain. Physiol Rev 74: 95-138
8. Coleridge HM, Coleridge JCG (1994) Pulmonary reflexes: neural mechanisms of pulmonary defense. Annu Rev Physiol 56: 69-91
9. Dalsgaard CJ, Lundberg JM (1984) Evidence for a spinal afferent innervation of the guinea pig lower respiratory tract as studied by the horseradish peroxidase technique. Neurosci Lett 45: 117-122
10. Das RM, Jeffery PK, Widdicombe JG (1979) Experimental degeneration of intra-epithelial nerve fibres in cat airways. J Anat 128: 259-267
11. Elftman AG (1943) The afferent and parasympathetic innervation of the lungs and trachea of the dog. Am J Anat 72: 1-27
12. Goniukowska-Witalinska L, Lauweryns JM, Zaccone G, Fasulo S, Tagliafierro G (1992) Ultrastructure and immunocytochemistry of the neuroepithelial bodies in the lung of the tiger salamander, Ambystoma tigrinum (Urodela, Amphibia). Anat Rec 234: 419-431
13. Honjin R (1956a) On the nerve supply of the lung of the mouse, with special reference to the structure of the peripheral vegetative nervous system. J Comp Neurol 105: 587-625
14. Honjin R (1956b) Experimental degeneration of the vagus, and its relation to the nerve supply of the lung of the mouse, with special reference to the crossing innervation of the lung by the vagi. J Comp Neurol 106: 1-19
15. Hoyes AD, Barber P (1980) Innervation of the trachealis muscle in the guinea-pig: a quantitative ultrastructural study. J Anat 130: 789-800
16. Hoyes AD, Barber P (1981) Morphology and response to vagus nerve section of the intra-epithelial axons of the rat trachea. A quantitative ultrastructural study. J Anat 132: 331-339
17. Hoyes AD, Barber P, Jagessar H (1982) Location in the nodose ganglion of the perikarya of neurons whose axons distribute in the epithelium of the rat trachea. J Anat 134: 265-271
18. Hoyt RF, Sorokin SP, McDowell EM, McNelly N (1993) Neuro-epithelial bodies and growth of the airway epithelium in developing hamster lung. Anat Rec 236: 15-22
19. Hung KS (1976) Fine structure of tracheo-bronchial epithelial nerves in the cat. Anat Rec 185: 85-92
20. Hung KS, Loosli CG (1974) Bronchiolar neuro-epithelial bodies in the neonatal mouse lungs. Am J Anat 140: 191-200
21. Hung KS, Hertweck MS, Hardy JD, Loosli CG (1973) Electron microscopic observations of nerve endings in the alveolar walls of mouse lungs. Am Rev Respir Dis 108: 328-333
22. Keith IM, Ekman R (1990) PYY-like material and its spatial relationship with NPY, CGRP and 5-HT in the lung of the Syrian golden hamster. Cell Tissue Res 262: 543-550
23. Krauhs JM (1984) Morphology of presumptive slowly adapting receptors in dog trachea. Anat Rec 210: 73-85
24. Kressel M, Berthoud HR, Neuhuber WL (1994) Vagal innervation of the rat pylorus: an anterograde tracing study using carbo-cyanine dyes and laser scanning confocal microscopy. Cell Tissue Res 275: 109-123
25. Kummer W, Fischer A, Kurkowski R, Heym C (1992) The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labelling immunohistochemistry. Neuroscience 49: 715-737
26. Laitinen A (1985) Ultrastructural organisation of intraepithelial nerves in the human airway tract. Thorax 40: 488-492
27. Larsell O (1921) Nerve terminations in the lung of the rabbit. J Comp Neurol 33: 105-131
28. Larsell O, Dow RS (1921) The innervation of the human lung. Am J Anat 52: 125-146
29. Lauweryns JM, Peuskens JC (1972) Neuro-epithelial bodies (neuroreceptors or secretory organs?) in human infant bronchial and bronchiolar epithelium. Anat Rec 172: 471-482
30. Lauweryns JM, Van Lommel A (1987) Ultrastructure of nerve endings and synaptic junctions in rabbit pulmonary neuroepithelial bodies: a single and serial section analysis. J Anat 151: 65-83
31. Lauweryns JM, Van Ranst L (1987) Calcitonin gene-related peptide immunoreactivity in rat lung: a light and electron microscopic study. Thorax 42: 183-189
32. Lauweryns JM, Cokelaere M, Theunynck P (1972) Neuro-epithelial bodies in the respiratory mucosa of various mammals. A light optical, histochemical and ultrastructural investigation. Z Zellforsch 135: 569-592
33. Lauweryns JM, De Bock V, Guelinckx P, Decramer M (1983) Effects of unilateral hypoxia on neuroepithelial bodies in rabbit lungs. J Appl Physiol 55: 1665-1668
34. Lauweryns JM, Van Lommel AT, Dom RJ (1985) Innervation of rabbit intrapulmonary neuroepithelial bodies. Quantitative and qualitative ultrastructural study after vagotomy. J Neurol Sci 67: 81-92
35. Luts A, Uddman R, Absood A, Hakanson R, Sundler F (1991) Chemical coding of endocrine cells of the airways: presence of helodermin-like peptides. Cell Tissue Res 265: 425-433
36. Martling CR, Sana A, Fischer JA, Hökfelt T, Lundberg JM (1988) Calcitonin gene-related peptide and the lung: neuronal coexistence with substance P, release by capsaicin and vasodilatory effect. Regul Pept 20: 125-139
37. Meyrick B, Reid L (1971) Nerves in rat intra-acinar alveoli: an electron microscopic study. Resp Physiol 11: 367-377
38. Neuhuber WL (1987) Sensory vagal innervation of the rat esophagus and cardia: a light and electron microscopic anterograde study. J Auton Nerv Syst 20: 243-255
39. Quigg M (1991) Distribution of vagal afferent fibers of the guinea pig heart labelled by anterograde transport of conjugated horseradish peroxidase. J Auton Nerv Syst 36: 13-24
40. Sant' Ambrogio G (1987) Nervous receptors of the tracheobronchial tree. Ann Rev Physiol 49: 611-627
41. Scheuermann DW, De Groodt-Lasseel MHA, Stilman C, Meisters ML (1983) A correlative light-, fluorescence-, and electron-microscopic study of neuroepithelial bodies in the lung of the red-eared turtle, Pseudemys scripta elegans. Cell Tissue Res 234: 249-269
42. Scheuermann DW, Adriaensen D, Timmermans JP, De Groodt-Lasseel MHA (1992) Comparative histological overview of the chemical coding of the pulmonary neuroepithelial endocrine system in health and disease. Eur J Morphol 30: 101-112
43. Spencer H, Leof D (1964) The innervation of the human lung. J Anat 98: 599-609
44. Springall DR, Cadieux A, Oliveira H, Su H, Rayston D, Polak JM (1987) Retrograde tracing shows that CGRP-immunoreactive nerves of rat trachea and lung originate from vagal and dorsal root ganglia. J Auton Nerv Syst 20: 155-166
45. Van Lommel A, Lauweryns JM (1993). Neuroepithelial bodies in the Fawn Hooded rat lungs: morphological and neuroanatomical evidence for a sensory innervation. J Anat 183: 553-566
46. Verna A (1979) Ultrastructure of the carotid body in mammals. Int Rev Cytol 60: 271-330
47. Youngson C, Nurse C, Yeger H, Cutz E (1993) Oxygen sensing in airway chemoreceptors. Nature 365: 153-155