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Ultrastructural characterization of interstitial cells of Cajal associated with the submucosal plexus in the proximal colon of the guinea pig

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Abstract

Interstitial cells of Cajal (ICC) associated with the submucosal (submucous) plexus (ICC-SP) in the proximal colon of the guinea pig were studied by immunohistochemistry and electron microscopy. Whole-mount stretch preparations with c-Kit immunohistochemistry revealed that a number of ICC-SP constituted a dense cellular network around the submucosal plexus. Some of these ICC-SP were observed in the vicinity of the muscularis mucosae in sections immunostained for c-Kit and α-smooth muscle actin. Ultrastructural observation demonstrated, for the first time, that ICC-SP of the proximal colon of the guinea pig retained typical ultrastructural characteristics of ICC repeatedly reported in association with the tunica muscularis of the gastrointestinal tract: a basal lamina, caveolae, many mitochondria, abundant intermediate filaments and the formation of gap junctions with the same type of cells. The most remarkable ultrastructural finding was the presence of thick bundles composed of the processes of ICC-SP connected to each other via large gap junctions. These ICC-SP might be involved in the main mucosal functions of the proximal colon of the guinea pig, namely the transportation of water and electrolytes, possibly via their involvement in the spontaneous contractions of the muscularis mucosae.

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References

  • Araki K, Furuya Y, Kobayashi M, Matsuura K, Ogata T, Isozaki H (1996) Comparison of mucosal microvasculature between the proximal and distal human colon. J Electron Microsc (Tokyo) 45:202–206

    CAS  Google Scholar 

  • Aranishi H, Kunisawa Y, Komuro T (2009) Characterization of interstitial cells of Cajal in the subserosal layer of the guinea-pig colon. Cell Tissue Res 335:323–329

    Article  PubMed  CAS  Google Scholar 

  • Argenzio RA (1985) Digestion, absorption and metabolism. In: Swenson MJ (ed) Duke’s physiology of domestic animals, 10th edn. Cornell University Press, Ithaca, pp 262–277

    Google Scholar 

  • Furness JB (2006) Constituent neurons of the enteric nervous system. In: Furness JB (ed) The enteric nervous system. Blackwell, Oxford, pp 29–79

    Google Scholar 

  • Huizinga JD (1999) Gastrointestinal peristalsis: joint action of enteric nerves, smooth muscle, and interstitial cells of Cajal. Microsc Res Tech 47:239–247

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa K, Ozaki T (1997) Distribution of several gut neuropeptides and their effects on motor activity in muscularis mucosae of guinea-pig proximal colon. J Auton Nerv Syst 64:91–100

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa K, Komuro T (1996) Characterization of the interstitial cells associated with the submuscular plexus of the guinea-pig colon. Anat Embryol 194:49–55

    Article  PubMed  CAS  Google Scholar 

  • Kodama Y, Iino S, Shigemasa Y, Suzuki H (2010) Properties of acetylcholine-induced relaxation of smooth muscle isolated from the proximal colon of the guinea-pig. J Smooth Muscle Res 46:185–200

    Article  PubMed  Google Scholar 

  • Komuro T, Seki K, Horiguchi K (1999) Ultrastructural characterization of the interstitial cells of Cajal. Arch Histol Cytol 62:295–316

    Article  PubMed  CAS  Google Scholar 

  • Kunisawa Y, Komuro T (2008) Interstitial cells of Cajal associated with the submucosal plexus of the guinea-pig stomach. Neurosci Lett 434:273–276

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto-Kikuta S, Ezaki T, Komuro T (2009) Distribution and morphological characteristics of the interstitial cells of Cajal in the ileocaecal junction of the guinea-pig. Cell Tissue Res 338:29–35

    Article  PubMed  Google Scholar 

  • Oltmer S, Engelhardt W von (1994) Absorption of short-chain fatty acids from the in-situ-perfused caecum and colon of the guinea pig. Scand J Gastroenterol 29:1009–1016

    Article  PubMed  CAS  Google Scholar 

  • Percy WH, Rose K, Burton MB (1992) Pharmacologic characterization of the muscularis mucosae in three regions of the rabbit colon. J Pharmacol Exp Ther 261:1136–1142

    PubMed  CAS  Google Scholar 

  • Percy WH, Warren JM, Brunz JT (1999) Characteristics of the muscularis mucosae in the acid-secreting region of the rabbit stomach. Am J Physiol 276:G1213–G1220

    PubMed  CAS  Google Scholar 

  • Percy WH, Kittelsrud JM, Brunz JT (2002) Types of adrenoreceptors mediating responses of rabbit gastric muscularis mucosae. Dig Dis Sci 47:356–364

    Article  PubMed  CAS  Google Scholar 

  • Pieri L, Vannucchi MG, Faussone-Pellegrini MS (2008) Histochemical and ultrastructural characteristics of an interstitial cell type different from ICC and resident in the muscle coat of human gut. J Cell Mol Med 12:1944–1955

    Article  PubMed  Google Scholar 

  • Plujà L, Albertí E, Fernández E, Mikkelsen HB, Thuneberg L, Jiménez M (2001) Evidence supporting presence of two pacemakers in rat colon. Am J Physiol Gastrointest Liver Physiol 281:G255–G266

    PubMed  Google Scholar 

  • Popescu LM, Faussone-Pellegrini MS (2010) Telocytes—a case of serendipity: the winding way from interstitial cells of Cajal (ICC), via interstitial Cajal-like cells (ICLC) to telocytes. J Cell Mol Med 14:729–740

    Article  PubMed  CAS  Google Scholar 

  • Sanders KM (1996) A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology 111:492–515

    Article  PubMed  CAS  Google Scholar 

  • Skinner SA, O'Brien PE (1996) The microvascular structure of the normal colon in rats and humans. J Surg Res 61:482–490

    Article  PubMed  CAS  Google Scholar 

  • Smith TK, Reed JB, Sanders KM (1987) Origin and propagation of electrical slow waves in circular muscle of canine proximal colon. Am J Physiol 252:C215–C224

    PubMed  CAS  Google Scholar 

  • Stevens CE (1977) Comparative physiology of the digestive system. In: Swenson MJ (ed) Duke’s physiology of domestic animals, 9th edn. Cornell University Press, Ithaca, pp 216–232

    Google Scholar 

  • Synnerstad I, Ekblad E, Sundler F, Holm L (1998) Gastric mucosal smooth muscles may explain oscillations in glandular pressure: role of vasoactive intestinal peptide. Gastroenterology 114:284–294

    Article  PubMed  CAS  Google Scholar 

  • Tamada H, Komuro T (2011) Three-dimensional demonstration of the interstitial cells of Cajal associated with the submucosal plexus in guinea-pig caecum. Cell Tissue Res 344:183–188

    Article  PubMed  Google Scholar 

  • Ward SM, Sanders KM (2001) Interstitial cells of Cajal: primary targets of enteric motor innervation. Anat Rec 262:125–135

    Article  PubMed  CAS  Google Scholar 

  • Yoneda S, Fukui H, Takaki M (2004) Pacemaker activity from submucosal interstitial cells of Cajal drives high-frequency and low-amplitude circular muscle contractions in the mouse proximal colon. Neurogastroenterol Motil 16:621–627

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Terumasa Komuro.

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This study was supported by Grant-in-aid for JSPS Fellows from the Ministry of Education, Culture, Sports and Technology, Japan (23•4352 to H.T.).

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Tamada, H., Komuro, T. Ultrastructural characterization of interstitial cells of Cajal associated with the submucosal plexus in the proximal colon of the guinea pig. Cell Tissue Res 347, 319–326 (2012). https://doi.org/10.1007/s00441-011-1312-5

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  • DOI: https://doi.org/10.1007/s00441-011-1312-5

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