Abstract
The development of the canine proximal colon from the completion of organogenesis through 43 days after birth was studied using light microscopy, immunofluorescence and electron microscopy. During this period the tunica muscularis increased in thickness from 42±6 μm in animals midway through the gestation period to 317±29 μm in animals 25–30 days old. This increase in thickness resulted from an increase in the number and size of smooth muscle cells in the circular and longitudinal muscle layers. The cross-sectional thickness of the circular muscle layer increased from 10±2 smooth muscle cells midway through the gestation period to 92±7 cells in animals 25–30 days old. The longitudinal layer increased in thickness from 1.5±1 cells in animals midway through the gestation period to 44±2 cells in animals 25–30 days old. Smooth muscle cells from both layers also increased in diameter and length. Ultrastructural and immunohistochemical studies suggested that many of the smooth muscle cells were undergoing development throughout the fetal period. Midway through the gestation period, the circular layer was positive for desmin-like immunoreactivity (D-LI), while both the circular and longitudinal layers were positive for vimentinlike immunoreactivity (V-LI). By birth, V-LI was suppressed in the circular and longitudinal layers, and both layers expressed D-LI. The enteric nervous system was already established midway through the gestation period, and submucosal and myenteric ganglia could be identified, although the chemical coding and mature morphology of neurons were incomplete. NADPH-diaphorase-positive neurons, indicating the expression of nitric oxide synthase, developed by the time of birth. Interstitial cells of Cajal (IC) could not clearly be identified midway through gestation, however, potential precursors to ICs were observed. Several classes of ICs were identifiable at birth.
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References
Berezin I, Huizinga JD, Daniel EE (1988) Interstitial cells of Cajal in the canine colon: a special communication network at the inner border of the circular muscle. J Comp Neurol 273:42–51
Bredt DS, Hwang MP, Snyder SH (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347:768–770
Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Snyder SH (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci USA 88:7797–7801
El-Sharkawy TY (1983) Electrical activities of the muscle layers of the canine colon. J Physiol [Lond] 342:67–83
Faussone-Pellegrini MS (1984) Morphogenesis of the special circular muscle layer and of the interstitial cells of Cajal related to the plexus muscularis profundus of mouse intestimal muscle coat. Acta Embryol 171:151–158
Faussone-Pellegrini MS (1987) Cytodifferentiation of the interstitial cells of Cajal related to the myenteric plexus of mouse intestinal coat. Anat Embryol 171:163–169
Faussone-Pellegrini MS (1985) Cytodifferentiation of the interstitial cells of Cajal of mouse colonic circular muscle layer. Acta Anat 128:98–109
Gabella G (1989) Development of smooth muscle: study of the chick embryo gizzard. Anat Embryol 180:213–226
Gabella G (1990) Hypertrophy of visceral smooth muscle. Anat Embryol 182:409–424
Hirai SI, Hirabayshi T (1983) Developmental change of protein constituents in chicken gizzards. Dev Biol 97:483–493
Huizinga JD (1991) Action potentials in gastrointestinal smooth muscle. Can J Physiol Pharmacol 69:1133–1142
Langton PD, Burke EP, Sanders KM (1989) Participation of Ca currents in colonic electrical activity. Am J Physiol 257:C451-C460
Mikkelsen HB, Huizinga JD, Thuneberg L, Rumessen JJ (1993) Immunohistochemical localization of a gap junction protein (connexin 43) in the muscularis externa of murine, canine and human intestine. Cell Tissue Res 274:249–256
Pharm TD, Gershon MD, Rothman TP (1991) Time of origin of neurons in the murine enteric nervous system: sequence in relation to phenotype. J Comp Neurol 314:789–798
Phemister RD (1974) Nonneurogenic reproductive failure in the bitch. Vet Clin North Am 4:573–586
Pomeranz HD, Gershon MD (1990) Colonization of the avian hindgut by cells derived from the sacral neural crest. Dev Biol 137:378–394
Rothman TP, Gershon MD (1982) Phenotypic expression in the developing murine enteric nervous system. J Neurosci 2:381–393
Sanders KM (1992) Ionic mechanisms of electrical rhymicity in gastrointestinal smooth muscles. Ann Rev Physiol 54:439–453
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
Timmermans JP, Barbiers M, Scheuermann DW, Bogers JJ, Adriaensen D, Fekete E, Mayer EA, De Groodt-Lasseel MHA (1994) Nitric oxide synthase immunoreactivity in the enteric nervous system of the developing human digestive tract. Cell Tissue Res 275:235–245
Thuneberg L (1982) Interstitial cells of Cajal: intestinal pacemaker cells? Adv Anat Embryol Cell Biol 71:1–130
Torihashi S, Gerthoffer WT, Kobayashi S, Sanders KM (1994) Identification and classification of interstitial cells in the camine proximal colon by ultrastructure and immunocytochemistry. Histochemistry 101:169–183
Torihashi S, Ward SM, Nishikawa SI, Nishi K, Kobayashi S, Sanders KM (1995) c-kit Dependent development of interstitial cells and electrical activity in the murine gastrointestinal tract. Cell Tissue Res 280:97–111
Ward SM, Sanders KM (1990) Pacemaker activity in septal structures of canine colonic circular muscle. Am J Physiol 259:G264-G273
Ward SM, Sanders KM (1992) Upstroke component of electrical slow waves in canine colonic smooth muscle due to nifedipine-resisitant calcium current. J Physiol 455:321–337
Ward SM, Keller RG, Sanders KM (1991) Structure and organization of electrical activity of canine distal colon. Am J Physiol 260:G724-G735
Ward SM, Xue C, Shuttleworth CWR, Bredt DS, Snyder SH, Sanders KM (1992) NADPH diaphorase and nitric oxide synthase colocalization in enteric neurons of canine proximal colon. Am J Physiol 263:G277-G284
Ward SM, Burns AJ, Torihashi S, Sanders KM (1994) Mutation of the proto-oncogene c-kit blocks development of interstitial cells and electrical rhymicity in murine intestine. J Physiol 480.1:91–97
Xue C, Ward SM, Shuttleworth CWR, Sanders KM (1993) Identification of interstitial cells in the canine proximal colon using NADH diaphorase histochemistry. Histochemistry 99:373–384
Young HM, Furness JB, Shuttleworth CWR, Bredt DS, Snyder SH (1992) Co-localization of nitric oxide synthase immunoreactivity and NADPH diaphorase staining in neurons of the guinea-pig intestine. Histochemistry 97:375–378
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Ward, S.M., Torihashi, S. Morphological changes during ontogeny of the canine proximal colon. Cell Tissue Res 282, 93–108 (1995). https://doi.org/10.1007/BF00319136
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DOI: https://doi.org/10.1007/BF00319136