Abstract
Cholera toxin subunit b was found in vivo and in vitro to label interstitial cells of Cajal in the intestine of rat and mouse. Cholera toxin-labelled interstitial cells were present in the subserosa, the myenteric plexus and the deep muscular plexus of mouse small intestine, and the deep muscular plexus only of the rat small intestine. In the large intestine of the mouse, interstitial cells were present in the subserosa and in a plexus associated with the inner surface of the circular muscle, while in the rat they were only present in the latter location. Macrophages, which were present in many of the same locations as interstitial cells, were also labelled by cholera toxin but could be distinguished from interstitial cells by their ability to take-up fluorescein isothiocyanate-labelled dextran. Labelling with subunit b of cholera toxin is a simple way of labelling interstitial cells of Cajal and which is compatible with a range of physiological and histological procedures.
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Berthoud H-R, Jedrzejewska A, Powley TL (1990) Simultaneous labelling 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
Cassuto J, Jodal M, Tuttle R, Lundgren O (1981) On the role of intramural nerves in the pathogenesis of the cholera toxin-induced intestinal secretion. Scand J Gastroent 16:377–384
Christensen J (1992) A commentary on the morphological identification of the interstitial cells of Cajal in the gut. J Auton Nerv Syst 37:75–88
Christensen J, Rick GA (1987) Intrinsic nerves in the mammalian colon: confirmation of a plexus at the circular muscle-submucosal interface. J Autonom Nerv Syst 21:223–231
Faussone-Pellegrini M-S (1983) Le caratteristiche ultrastrutturali della tunica muscolare dell'ileo e del colon di ratto: A. Porzione interna dello strato circulare. Arch Ital Anat Embriol. 88:25–40
Faussone-Pellegrini M-S (1985) Ultrastructural peculiarities of the inner portion of the circular layer of the colon. Acta Anat 122:187–192
Furness JB, Costa M (1971) Monoamine oxidase histochemistry of enteric neurons in the guinea pig. Histochemie 28:324–336
Fuxe K, Tinner AM, Janson Am, Cintra A, Staines W, Agnati LF (1989) On the cellular localization and distribution of the ganglioside GM1 in the rat brain as revealed by immunofluoresence histochemistry of cholera toxin binding sites. Acta Physiol Scand 137:551–552
Gabella G (1974) Special muscle cells and their innervation in the mammalian small intestine. Cell Tissue Res 153:63–77
Gabella G (1979) Innervation of the gastrointestinal tract. Int Rev Cytol 59:129–193
Holmgren J (1981) Actions of cholera toxin and the prevention of cholera. Nature 292:413–417
Jiang M-M, Kirchgessner A, Gershon MD, Suprenant A (1993) Cholera toxin-sensitive neurons in guinea pig submucosal plexus. Am J Physiol 264:G86-G94
Kobayashi S (1990) The structure of the autonomic end apparatus in the guinea-pig small intestine and the problem of the interstitial cells of Cajal. Acta Med Biol 38:102–127
Kobayashi S, Suzuki M, Endo T, Tsuji S, Daniel EE (1986) Framework of the enteric nerve plexuses: an immunocytochemical study in the guinea pig jejunem using an antiserum to S-100 protein. Arch Histol Jpn 49:159–188
Kobayashi S, Furness JB, Smith TK, Pompolo S (1989) Histological identification of interstitial cells of Cajal in the guinea pig small intestine. Arch Histol Cytol 52:267–286
Laev H, Mahadik SP (1989) Topography of monosialoganglioside (GM1) in rat brain using monoclonal antibodies. Neurosci Lett 102:7–14
Leeden RW (1985) Gangliosides in the neuron. Trends Neurosci 8:169–174
Llewellyn-Smith IJ, Minson JB, Pilowsky PM, (1992) Retrograde tracing with cholera toxin B-gold or with immunocytochemically detected cholera toxin B in central nervous system. Methods Neurosci 8:180–201
Mikkelson HB, Thuneberg L, Rumessen JJ, Thorball N (1985) Macrophage-like cells in the muscularis externa of mouse small intestine. Anat Rec 213:77–86
Mikkelson HB, Thuneberg L, Wittrup IH (1988) Selective double staining of interstitial cells of Cajal and macrophage-like cells in small intestine by an improved supravital methylene blue technique combined with FITC uptake. Anat Embryol 178:191–195
Nambiar MP, Oda T, Chen C, Kuwazuru Y, Wu HC (1993) Involvement of the Golgi region in the intracellular trafficking of cholera toxin. J Cell Physiol 154:222–228
Powley TL, Berthoud HR (1991) A fluorescent labelling strategy for staining the enteric nervous system. J Neurosci Methods 36:9–15
Prosser CL, Holzwarth MA, Barr L (1989) Immunocytochemistry of the interstitial cells of Cajal in the rat intestine. J Auton Nerv Syst 27:17–25
Robertson B, Grant G (1989) Immunocytochemical evidence for the localization of the GM1 ganglioside in carbonic anhydrasecontaining and RT97-immunoreactive rat primary sensory neurons. J Neurocytol 18:77–86
Robertson B, Perry M, Lawson SN (1991) Populations of rat spinal primary afferent neurons with choleragenoid binding compared to those labelled by markers for neurofilament and carbohydrate groups: a quantitative immunocytochemical study. J Neurocytol 20:387–395
Rumessen JJ, Thuneberg L (1982) Plexus muscularis profundus and associated interstitial cells. I. Light microscopic studies on mouse small intestine. Anat Rec 203:115–127
Shuttleworth CW, Xue C, Ward SM, de Vente J, Sanders KM (1993) Immunohistochemical localization of 3′,5′-cyclic guanosine monophosphate in the canine proximal colon: responses to nitric oxide and electrical stimulation of enteric inhibitory neurons. Neuroscience (in press)
Stach W (1972) Der Plexus entericus extremus des Dickdarmes und seine Beziehungen zu den interstitiellen Zellen (Cajal). Z Mikrosk Anat Forsch 85:245–272
Steinman RM, Mellman IS, Muller WA, Cohn ZA (1983) Endocytosis and the recycling of the cell membrane. J Cell Biol 96:1–27
Taxi J (1965) Contribution á l'étude des connexions des neurones moteurs du systeme nerveux autonome. Ann Sci Nat Zool Biol Anim 7:413–674
Thuneberg L (1982) Interstitial cells of Cajal: intestinal pacemaker cells? Adv Anat Embryol Cell Biol 71:1–130
Thuneberg L (1989) Interstitial ccells of Cajal. In: Wood JD, Bethesda MD (eds) Handbook of physiology — the gastrointestinal system, vol 1. American Physiological Society, Washington D.C., USA, pp 349–386
Vaney DI (1984) “Coronate” amacrine cells in the rabbit retina have the “starburst” dendritic morphology. Proc R Soc Lond B 220:501–508
Willison HJ, Kennedy PGE (1993) The fine specificity of anti-GM1 antibodies. Q J Med 86:216–217
Xue C, Ward SM, Shuttleworth CW, Sanders KM (1993) Identification of interstitial cells in canine proximal colon using NADH diaphorase histochemistry. Histochemistry 99:373–384
Young HM, McConalogue K, Furness JB, Vente J de (1993) Nitric oxide targets in the guinea-pig intestine identified by induction of cyclic GMP immunoreactivity. Neuroscience 55:583–596
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Anderson, C.R., Edwards, S.L. Subunit b of cholera toxin labels interstitial cells of Cajal in the gut of rat and mouse. Histochemistry 100, 457–464 (1993). https://doi.org/10.1007/BF00267826
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DOI: https://doi.org/10.1007/BF00267826