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P2X2 purine receptor immunoreactivity of intraganglionic laminar endings in the mouse gastrointestinal tract

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Abstract

The distribution of P2X2 purine receptor subunit immunoreactivity has been investigated in the mouse gastrointestinal tract. Immunoreactivity occurred in intraganglionic laminar endings (IGLEs) associated with myenteric ganglia throughout the gastrointestinal tract. In the esophagus, IGLEs supplied every myenteric ganglion. The proportion of ganglia supplied decreased from 85% in the stomach to 10% in the ileum, and from 50% in the caecum to 15% in the distal colon. There was substantial loss of IGLEs from myenteric ganglia of all abdominal regions after bilateral subdiaphragmatic section of the vagus nerves. IGLEs in the esophagus consisted of dense clusters of punctate immunoreactive varicosities. In the stomach and duodenum they had prominent lamellar processes and irregular, but smaller, lamellae were found in other regions. Rare immunoreactive IGLEs occurred in the submucosa of the distal colon. P2X2 receptor immunoreactivity was on the surfaces and in the cytoplasm of a minority of nerve cells in myenteric ganglia. It is concluded that P2X2 purine receptor immunoreactivity is a feature of IGLEs in the mouse, and that P2X receptor agonists may modulate sensitivity of the IGLEs.

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References

  • Al Humayyd M, White TD (1985) Adrenergic and possible nonadrenergic sources of adenosine 5'-triphosphate release from nerve varicosities isolated from ileal myenteric plexus. J Pharmacol Exp Ther 233:796–800

    PubMed  Google Scholar 

  • Berthoud H-R, Neuhuber WL (2000) Functional and chemical anatomy of the afferent vagal system. Autonom Neurosci 85:1–17

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Berthoud HR, Jedrzejewska A, Powley TL (1990) Simultaneous labeling of vagal innervation of the gut and afferent projections from the visceral forebrain with diI injected into the dorsal vagal complex in the rat. J Comp Neurol 301:65–79

    CAS  PubMed  Google Scholar 

  • Berthoud HR, Patterson LM, Neumann F, Neuhuber WL (1997) Distribution and structure of vagal afferent intraganglionic laminar ending IGLEs in the rat gastrointestinal tract. Anat Embryol 195:183–191

    CAS  PubMed  Google Scholar 

  • Buéno L, Fioramonti J, Delvaux M, Frexinos J (1997) Mediators and pharmacology of visceral sensitivity: from basic to clinical investigations. Gastroenterology 112:1714–1743

    PubMed  Google Scholar 

  • Castelucci P, Robbins HL, Poole DP, Furness JB (2002) The distribution of purine P2X2 receptors in the guinea pig enteric nervous system. Histochem Cell Biol 117:415–422

    Google Scholar 

  • Dütsch M, Eichhorn U, Wörl J, Wank M, Berthoud HR, Neuhuber WL (1998) Vagal and spinal afferent innervation of the rat esophagus: a combined retrograde tracing and immunocytochemical study with special emphasis on calcium-binding proteins. J Comp Neurol 398:289–307

    Article  PubMed  Google Scholar 

  • Fox EA, Phillips RJ, Martinson FA, Baronowsky EA, Powley TL (2000) Vagal afferent innervation of smooth muscle in the stomach and duodenum of the mouse: morphology and topography. J Comp Neurol 428:558–576

    CAS  PubMed  Google Scholar 

  • Kirkup AJ, Booth CE, Chessell IP, Humphrey PPA, Grundy D (1999) Excitatory effect of P2X receptor activation on mesenteric afferent nerves in the anaesthetised rat. J Physiol (Lond) 520:551–563

    Google Scholar 

  • Lawrentjew BJ (1929) Experimentelle-morphologische Studien über den feineren Bau des autonomen Nervensystems. II. Über den Aufbau der Ganglien der Speiseröhre nebst einigen Bemerkungen über das Vorkommen und die Verteilung zweier Arten von Nervenzellen in dem autonomen Nervensystem. Z Mikrosk Anat Forsch 18:233–262

    Google Scholar 

  • Neuhuber WL (1987) Sensory vagal innervation of the rat esophagus and cardia: a light and electron microscopic anterograde tracing study. J Auton Nerv Syst 20:243–255

    CAS  PubMed  Google Scholar 

  • Neuhuber WL, Kressel M, Stark A, Berthoud HR (1998) 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 70:92–102

    CAS  PubMed  Google Scholar 

  • Nonidez JF (1946) Afferent nerve endings in the ganglia of the intermuscular plexus of the dog's oesophagus. J Comp Neurol 85:177–189

    Google Scholar 

  • Phillips RJ, Baronowsky EA, Powley TL (1997) Afferent innervation of gastrointestinal tract smooth muscle by the hepatic branch of the vagus. J Comp Neurol 384:248–270

    Article  CAS  PubMed  Google Scholar 

  • Powley TL, Holst MC, Boyd DB, Kelly JB (1994) Three-dimensional reconstructions of autonomic projections to the gastrointestinal tract. Microsc Res Tech 29:297–309

    CAS  PubMed  Google Scholar 

  • Rodrigo J, Hernández CJ, Vidal MA, Pedrosa JA (1975) Vegetative innervation of the esophagus. II. Intraganglionic laminar endings. Acta Anat 92:79–100

    CAS  Google Scholar 

  • Rodrigo J, Robles Chillida EM, De Felipe J, Mayo I, Anton JAP, Pedrosa JA, Gomez A (1981) Effects of surgical sympathectomy on laminar nerve endings in myenteric ganglia. Acta Anat 109:34–43

    CAS  Google Scholar 

  • Rodrigo J, De Felipe J, Robles Chillida EM, Pérez Antón JA, Mayo I, Gómez A (1982) Sensory vagal nature and anatomical access paths to esophagus laminar nerve endings in myenteric ganglia. Determination by surgical degeneration methods. Acta Anat 112:47–57

    CAS  Google Scholar 

  • Sengupta JN, Gebhart GF (1994) Gastrointestinal afferent fibers and sensation. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Raven, New York, pp 483–519

  • Tassicker BC, Hennig GW, Costa M, Brookes SJH (1999) Rapid anterograde and retrograde tracing from mesenteric nerve trunks to the guinea-pig small intestine in vitro. Cell Tissue Res 295:437–452

    Article  CAS  PubMed  Google Scholar 

  • Wang FB, Powley TL (2000) Topographic inventories of vagal afferents in gastrointestinal muscle. J Comp Neurol 421:302–324

    Article  CAS  PubMed  Google Scholar 

  • White TD, Leslie RA (1982) Depolarization-induced release of adenosine 5-triphosphate from isolated varicosities derived from the myenteric plexus of the guinea pig small intestine. J Neurosci 2:206–215

    CAS  PubMed  Google Scholar 

  • Williamson S, Pompolo S, Furness JB (1996) GABA and nitric oxide synthase immunoreactivities are colocalized in a subset of inhibitory motor neurons of the guinea-pig small intestine. Cell Tissue Res 284:29–37

    CAS  PubMed  Google Scholar 

  • Zagorodnyuk VP, Brookes SJH (2000) Transduction sites of vagal mechanoreceptors in the guinea pig esophagus. J Neurosci 20:6249–3255

    CAS  PubMed  Google Scholar 

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Acknowledgements

The work was supported by the National Health and Medical Research Council of Australia. Dr. Castelucci was a visiting academic from the Department of Anatomy, University of São Paulo, Brazil. She was supported by a FAPESP Fellowship (Fundação de Amparo a Pesquisa do Estado de São Paulo). We thank Melanie Coffey for assistance with dissection and microscopy.

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Correspondence to John B. Furness.

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Castelucci, P., Robbins, H.L. & Furness, J.B. P2X2 purine receptor immunoreactivity of intraganglionic laminar endings in the mouse gastrointestinal tract. Cell Tissue Res 312, 167–174 (2003). https://doi.org/10.1007/s00441-003-0715-3

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