Summary
The distribution of calcitonin gene-related peptide-like immunoreactive (CGRP-LI) nerves was investigated immunohistochemically in the rectum of normal, capsaicin-treated and congenital aganglionosis rats. The rectum of the normal rat was densely supplied with both extrinsic and intrinsic nerves exhibiting CGRP-like immunoreactivity. Numerous CGRP-LI nerve fibres were seen in both the myenteric and submucous plexuses. Intrinsic CGRP-LI nerve cell bodies were sparsely found in both the ganglionated plexuses, while a large inflow of extrinsic CGRP-LI nerves was characteristically observed in the rat rectum. CGRP-like immunoreactive fibres were abundant in the intramural pelvic nerves which ascend proximally in the intermuscular zone and connect with the myenteric plexus of the rat distal bowel. As compared with CGRP-positive fibres, SP- or SK-positive fibres in the intramural pelvic nerves were far less frequent. The treatment with capsaicin in the neonatal period led to a marked depletion of CGRP-immunoreactivity in these extrinsic nerves as well as in the most terminal varicose fibres seen in the whole layers of the rectal wall. These findings suggest that the vast majority of CGRP-LI fibres in the intramural pelvic nerves are sensory in nature, and that the positive nerve fibres of extrinsic origin directly innervate each layer of the rat rectum. These CGRP-LI sensory fibres associated with the intramural pelvic nerves, may be of importance in the regulation of rectal and colonic function in normal rats. A dense innervation of CGRP-LI nerve fibres, some of which showed the varicose appearance, was also found in the rectum of congenital aganglionosis rats. Thus, it is suggested that there is a large inflow of extrinsic CGRP-LI fibres from the pelvic plexus in the affected rectum. The extrinsic CGRP-LI nerves in the aganglionic segment of the mutant rat might also be related to the regulation of rectal function, providing afferent pathways.
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References
Amara SG, Jonas V, Rosenfeld MG, Ong ES, Evance RM (1982) Alternative RNA processing in calcitonin gene expression generates mRNAs encoding different polypeptide products. Nature 298:240–244
Christensen J, Schulze-Delrieu K (1985) Nerves in the colon: discovery and rediscovery. Gastroenterology 89:222–223
Christensen J, Stiles MJ, Rick GA, Sutherland J (1984) Comparative anatomy of the myenteric plexus of the distal colon in eight mammals. Gastroenterology 86:706–713
Clague JR, Sternini C, Brecha N (1985) Localization of calcitonin gene-related peptide-like immunoreactivity in neurons of the rat gastrointestinal tract. Neurosci Lett 56:63–68
Domoto T, Oki M, Gonda T, Inoue K, Ozaki T (1987) Distribution of nerves containing vascoactive intestinal polypeptide-like immunoreactivity in rats with congenital aganglionosis of the colon. Neurosci Res 4:309–315
Fukai K, Fukuda H (1984) The intramural pelvic nerves in the colon of dogs. J Physiol (Lond) 254:89–98
Gibbins IL, Furness JB, Costa M, MacIntyre I, Hillyard CJ, Girgis S (1985) Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea-pig. Neurosci Lett 57:125–130
Gibson SJ, Polak JM, Bloom SR, Sabate IM, Mulderry PK, Ghatei MA, Morrison JFB, Kelly JS, Evans RM, Rosenfeld MG (1984) Calcitonin gene-related peptide (CGRP) immunoreactivity in the spinal cord of man and eight other spiecies. J Neurosci 4:3101–3111
Hirose R, Nada O, Kawana T, Goto S, Taguchi T, Toyohara T, Ikeda K (1989) An immunohistochemical study of somatostatin-containing nerves in the aganglionic colon of human and rat. Acta Neuropathol 78:372–379
Hua XY, Theodorsson-Norheim E, Lundberg JM, Kinn AC, Hokfelt T, Cuello AC (1987) Co-localization of tachykinins and calcitonin gene-related peptide in capsaicin-sensitive afferents in relation to motility effects on the human ureter in vitro. Neuroscience 23:693–703
Ikadai H, Fujita H, Agematsu Y, Imamichi T (1979) Observation of congenital aganglionosis rat (Hirschsprung's disease) and its genetical analysis (in Japanese). Congenital Anom 19:31–36
Jancso G, Kiraly E (1980) Distribution of chemosensitive primary sensory afferents in the central nervous system of the rat. J Comp Neurol 190:781–792
Jancso G, Kiraly E, Jancso-Gabor A (1977) Pharmacologically induced selective degeneration of chemosensitive primary sensory neurons. Nature 270:741–743
Ju G, Hokfelt T, Brodin E, Fahlrenkrung J, Fischer JA, Frey P, Elde RP, Brown JC (1987) Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-galanin-vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res 247:417–431
Kawai Y, Takami K, Shiosaka S, Emson PC, Hillyard CJ, Girgis S, MacIntyre I, Tohyama M (1985) Topographic localization of calcitonin gene-related peptide in the rat brain: an immuno-histochemical analysis. Neuroscience 15:747–763
Kubota M, Ito Y, Taguchi T, Ikeda K, Ikadai H (1989) Regional differences in the pattern of neurogenic responses in the aganglionic colon from congenitally aganglionosis rats. J Pediatr Surg 24:911–919
Lee Y, Takami K, Kawai Y, Girgis S, Hillyard CJ, MacIntyre I, Emson PC, Tohyama M (1985) Distribution of calcitonin gene-related peptide in the rat peripheral nervous system with reference to its coexistence with substance P. Neuroscience 15:1227–1237
Lee Y, Shiotani N, Hayashi N, Kamada T, Hillyard CJ, Girgis SI, MacIntyre I, Tohyama M (1987) Distribution and origin of calcitonin gene-related peptide in the rat stomach and duodenum: an immunohistochemical analysis. J Neural Transm 68:1–14
Maggi CA, Manzini S, Giuliani S, Santicioli P, Meli A (1986) Extrinsic origin of capsaicin-sensitive innervation of the rat duodenum: possible involvement of calcitonin gene-related peptide (CGRP) in the capsaicin-induced activation of intramural non-adrenergic non-cholinergic neurons. Arch Pharmacol 334:172–180
Maton PN, Sutliff VE, Zhou Z-C, Gardner JD, Jensen RT (1986) Characterization of receptors for calcitonin gene-related peptide (CGRP) on gastric smooth muscle cells. Gastroenterology 90:1573
Mulderry PK, Ghatei MA, Rodrigo J, Allen JM, Rosenfeld MG, Polak JM, Bloom SR (1985) Calcitonin gene-related peptide in cardiovascular tissues of the rat. Neuroscience 14:947–954
Nagahama M, Ozaki T, Hama K (1985) A study of the myenteric plexus of the congenital aganglionosis rat (spotting lethal) Anat Embryol 171:297–304
Ohtani R, Kaneko T, Kline LW, Labedz T, Tang Y, Pang PKT (1989) Localization of calcitonin gene-related peptide in the small intestine of various vertebrate species. Cell Tissue Res 258:35–42
Rodrigo J, Polak JM, Fernandez L, Ghatei MA, Mulderry P, Bloom SR (1985) Calcitonin gene-related peptide immunoreactive sensory and motor nerves of the rat, cat, and monkey esophagus. Gastroenterology 88:444–451
Rosenfeld MG, Mermod J-J, Amara SG, Swanson LW, Sawchenko PE, Rivier J, Vale WW, Ewans RM (1983) Production of novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature 304:129–135
Skofitsch G, Jacobowitz DM (1985) Calcitonin gene-related peptide coexists with substance P in capsaicin-sensitive neurons and sensory ganglia of the rat. Peptides 6:747–754
Stach W (1971) Über die in der Dickdarmwand aszendierenden Nerven des Plexus pelvinus und die Grenze der vagalen und sakralparasympatischen Innervation. Z Mikrosk Anat Forsch 84:65–90
Sternini C, Reeve JR, Brecha N (1987) Distribution and characterization of calcitonin gene-related peptide immunoreactivity in the digestive system of normal and capsaicin-treated rats. Gastroenterology 93:852–862
Su HC, Wharton J, Polak M, Mulderry PK, Ghatei MA, Gibson SJ, Trenghi G, Morrison JFB, Ballesta J, Bloom SR (1986) Calcitonin gene-related peptide immunoreactivity in afferent neurons supplying the urinary tract: combined retrograde tracing and immunohistochemistry. Neuroscience 18:727–747
Su HC, Bishop AE, Power RF, Hamada Y, Polak JM (1987) Dual intrinsic and extrinsic origins of CGRP- and NPY-immunoreactive nerves of rat gut and pancreas. J Neurosci 7:2674–2687
Takano Y, Nagashima A, Masui H, Kuromizu K, Okamiya H (1986) Distribution of substance K (neurokinin A) in the brain and peripheral tissues of rats. Brain Res 400–404
Terenghi G, Polack JM, Ghatei MA, Mulderry PK, Butler JM, Unger WG, Bloom SR (1985) Distribution and origin of calcitonin gene-related peptide (CGRP) immunoreactivity in the sensory innervation of the mammalian eye. J Comp Neurol 233:506–516
Tippins JR, Morris HR, Panico M, Etienne T, Bevis P, Girgis S, MacIntyre I, Azria M, Attinger M (1984) The myotropic and plasma-calcium modulating effects of calcitonin gene-related peptide (CGRP). Neuropeptides 4:425–434
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Hirose, R., Nada, O., Kawana, T. et al. The intramural pelvic nerves immunoreactive for calcitonin gene-related peptide in the rectum of normal and aganglionosis rat. Anat Embryol 187, 37–44 (1993). https://doi.org/10.1007/BF00208195
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DOI: https://doi.org/10.1007/BF00208195