Enteric co-innervation of striated muscle fibres in human oesophagus

Neurogastroenterology and Motility

Volumn 20, Issue 6, 2008, Pages 597-610

  Kallmunzer B ^a   Sorensen B ^a   Neuhuber, W L ^a   Worl J ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Enteric nervous system; Local reflex circuit; Neuromuscular junction; Neuronal nitric oxide synthase; Oesophageal motility; Skeletal muscle

Indexed keywords

GALANIN; NEUROPEPTIDE Y; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; VASOACTIVE INTESTINAL POLYPEPTIDE;

ARTICLE; CHOLINERGIC NERVE; CONFOCAL LASER MICROSCOPY; ESOPHAGUS MOTILITY; ESOPHAGUS MUSCLE; HUMAN; IMMUNOHISTOCHEMISTRY; INTESTINE INNERVATION; MUSCLE CELL; ORGAN DONOR; PRIORITY JOURNAL; SKELETAL MUSCLE; VAGUS NERVE;

AGED; AGED, 80 AND OVER; ENTERIC NERVOUS SYSTEM; ESOPHAGUS; FEMALE; HUMANS; MALE; MIDDLE AGED; MUSCLE FIBERS; MUSCLE, SKELETAL; MUSCLE, SMOOTH;

EID: 43549102847     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2007.01075.x     Document Type: Article

References (43)

1. Wörl J, Neuhuber WL. Enteric co-innervation of motor endplates in the esophagus: state of the art ten years after. Histochem Cell Biol 2005 123 : 117 30.
2. Bieger D, Hopkins DA. Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: the nucleus ambiguus. J Comp Neurol 1987 262 : 546 62.
3. Cunningham ETJ, Sawchenko PE. Central neural control of esophageal motility: a review. Dysphagia 1990 5 : 35 51.
4. Neuhuber WL, Kressel M, Stark A, Berthoud HR. Vagal efferent and afferent innervation of the rat esophagus as demonstrated by anterograde DiI and DiA tracing: focus on myenteric ganglia. J Auton Nerv Syst 1998 70 : 92 102.
5. Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev 2001 81 : 929 69.
6. Park H, Conklin JL. Neuromuscular control of esophageal peristalsis. Curr Gastroenterol Rep 1999 1 : 186 97.
7. Bieger D, Neuhuber WL. Neural circuits and mediators regulating swallowing in the brainstem. Gastrointestinal Motil Online 2006 doi:.
8. Neuhuber WL, Wörl J, Berthoud H-R, Conte B. NADPH-diaphorase- positive nerve fibers associated with motor endplates in the rat esophagus: new evidence for co-innervation of striated muscle by enteric neurons. Cell Tissue Res 1994 276 : 23 30.
9. Wörl J, Mayer B, Neuhuber WL. Nitrergic innervation of the rat esophagus: focus on motor endplates. J Auton Nerv Syst 1994 49 : 227 33.
10. Wörl J, Mayer B, Neuhuber WL. Spatial relationships of enteric nerve fibers to vagal motor terminals and the sarcolemma in motor endplates of the rat esophagus. A confocal laser scanning and electron-microscopic study. Cell Tissue Res 1997 287 : 113 8.
11. Boudaka A, Wörl J, Shiina T et al. Involvement of TRPV1-dependent and -independent components in the regulation of vagally induced contractions in the mouse esophagus. Eur J Pharmacol 2007 556 : 157 65.
12. Izumi N, Matsuyama H, Ko M, Shimizu Y, Takewaki T. Role of intrinsic nitrergic neurones on vagally mediated striated muscle contractions in the hamster oesophagus. J Physiol 2003 551 : 287 94.
13. Shiina T, Shimizu Y, Boudaka A, Wörl J, Takewaki T. Tachykinins are involved in local reflex modulation of vagally mediated striated muscle contractions in the rat esophagus via tachykinin NK1 receptors. Neuroscience 2006 139 : 495 503.
14. Goetsch E. The structure of the mammalian oesophagus. Am J Anat 1910 10 : 1 40.
15. Meyer GW, Austin RM, Brady CE, Castell DO. Muscle anatomy of the human esophagus. J Clin Gastroenterol 1986 8 : 131 4.
16. Kallmünzer B, Sörensen B, Neuhuber WL, Wörl J. Heterogeneity of neuromuscular junctions in striated muscle of human esophagus demonstrated by triple staining for the vesicular acetylcholine transporter, alpha-bungarotoxin, and acetylcholinesterase. Cell Tissue Res 2006 324 : 181 8.
17. Floyd K. Cholinesterase activity in sheep oesophageal muscle. J Anat 1973 116 : 357 73.
18. Mayr R, Zenker W, Gruber H. Zwischensehnenfreie Skeletmuskelfaser- Verbindungen. Z Zellforsch 1967 79 : 319 25.
19. Standring S, ed. Gray's Anatomy, 39th edn. Edinburgh : Elsevier, 2004.
20. Benninghoff A, Drenckhahn D, eds. Anatomie, 16th edn. München : Urban&Fischer, 2003.
21. Kaufmann P, Lierse W, Stark J, Stelzner F. Die Muskelanordnung in der Speiseröhre. Ergeb Anat Entwicklungsgesch 1968 40 : 5 34.
22. Périé S, St Guily JL, Callard P, Sebille A. Innervation of adult human laryngeal muscle fibers. J Neurol Sci 1997 149 : 81 6.
23. Breuer C, Neuhuber WL, Wörl J. Development of neuromuscular junctions in the mouse esophagus: morphology suggests a role for enteric co-innervation during maturation of vagal myoneural contacts. J Comp Neurol 2004 475 : 47 69.
24. Grozdanovic Z, Nakos G, Dahrmann G, Mayer B, Gossrau R. Species-independent expression of nitric oxide synthase in the sarcolemma region of visceral and somatic striated muscle fibers. Cell Tissue Res 1995 281 : 493 9.
25. Grozdanovic Z, Christova T, Gossrau R. Differences in the localization of the postsynaptic nitric oxide synthase I and acetylcholinesterase suggest a heterogeneity of neuromuscular junctions in rat and mouse skeletal muscles. Acta Histochem 1997 99 : 47 53.
26. Silvagno F, Xia H, Bredt DS. Neuronal nitric-oxide synthase-μ, an alternatively spliced isoform expressed in differentiated skeletal muscle. J Biol Chem 1996 271 : 11 204 8.
27. Brenman JE, Xia H, Chao DS, Black SM, Bredt DS. Regulation of neuronal nitric oxide synthase through alternative transcripts. Dev Neurosci 1997 19 : 224 31.
28. Wörl J, Dütsch F, Neuhuber WL. Development of neuromuscular junctions in the mouse esophagus: focus on establishment and reduction of enteric co-innervation. Anat Embryol 2002 205 : 141 52.
29. Wörl J, Fischer J, Neuhuber WL. Nonvagal origin of galanin-containing nerve terminals innervating striated muscle fibers of the rat esophagus. Cell Tissue Res 1998 292 : 453 61.
30. Neuhuber WL, Eichhorn U, Wörl J. Enteric co-innervation of striated muscle fibers in the esophagus: just a 'hangover'? Anat Rec 2001 262 : 41 6.
31. Gruber H. Motor innervation of the striated oesophagus muscle. Part 1. Intramural distribution of the right and left vagus nerve in the rat oesophagus as revealed by the glycogen depletion technique. J Neurol Sci 1978 36 : 41 53.
32. Kuramoto H, Endo Y. Galanin-immunoreactive nerve terminals innervating the striated muscle fibers of the rat esophagus. Neurosci Lett 1995 188 : 171 4.
33. Whitmore I. Oesophageal striated muscle arrangement and histochemical fibre types in guinea-pig, marmoset, macaque and man. J Anat 1982 134 : 685 95.
34. Leese G, Hopwood D. Muscle fibre typing in the human pharyngeal constrictors and oesophagus: the effect of ageing. Acta Anat 1986 127 : 77 80.
35. Peghini PL, Pursnani KG, Gideon MR, Castell JA, Nierman J, Castell DO. Proximal and distal esophageal contractions have similar manometric features. Am J Physiol 1998 274 : G325 30.
36. Mittal RK, Padda B, Bhalla V, Bhargava V, Liu J. Synchrony between circular and longitudinal muscle contractions during peristalsis in normal subjects. Am J Physiol Gastrointest Liver Physiol 2006 290 : G431 8.
37. Dunaway PM, Maydonovitch CL, Wong RKH. Characterization of esophageal striated muscle in patients with achalasia. Dig Dis Sci 2000 45 : 285 8.
38. Zhang ZG, Diamant NE. Repetitive contractions of the upper esophageal body and sphincter in achalasia. Dysphagia 1994 9 : 12 9.
39. Dantas RO, Aprile LRO, Aben-Athar CG, Miranda ALM. Esophageal striated muscle contractions in patients with Chagas' disease and idiopathic achalasia. Braz J Med Biol Res 2002 35 : 677 83.
40. Jung H-Y, Puckett JL, Bhalla V et al. Asynchrony between the circular and the longitudinal muscle contraction in patients with nutcracker esophagus. Gastroenterology 2005 128 : 1179 86.
41. Rao SSC, Hayek B, Mudipalli R, Gregersen H. Does esophageal function vary at the striated and smooth muscle segments in functional chest pain? Am J Gastroenterol 2002 97 : 2201 7.
42. Mayer B, John M, Heinzel B et al. Brain nitric oxide synthase is a biopterin- and flavin-containing multi-functional oxide-reductase. FEBS Lett 1991 288 : 187 91.
43. Schäfer MK-H, Weihe E, Erickson JD, Eiden LE. Human and monkey cholinergic neurons visualized in paraffin-embedded tissues by immunoreactivity for VAChT, the vesicular acetylcholine transporter. J Mol Neurosci 1995 6 : 225 35.