Characterization of projections of longitudinal muscle motor neurons in human colon.
Aged
Cell Size
Choline O-Acetyltransferase
/ metabolism
Colon
/ innervation
Enteric Nervous System
/ cytology
Female
Fluorescent Dyes
Gastrointestinal Motility
Humans
Immunohistochemistry
Male
Middle Aged
Motor Neurons
/ cytology
Muscle, Smooth
/ innervation
Neuroanatomical Tract-Tracing Techniques
Nitric Oxide Synthase
/ metabolism
Smooth muscle
colon
human
motor neuron
tenia
Journal
Neurogastroenterology and motility
ISSN: 1365-2982
Titre abrégé: Neurogastroenterol Motil
Pays: England
ID NLM: 9432572
Informations de publication
Date de publication:
10 2019
10 2019
Historique:
received:
05
05
2019
revised:
07
07
2019
accepted:
08
07
2019
pubmed:
30
7
2019
medline:
26
8
2020
entrez:
30
7
2019
Statut:
ppublish
Résumé
The enteric nervous system contains inhibitory and excitatory motor neurons which modulate smooth muscle contractility. Cell bodies of longitudinal muscle motor neurons have not been identified in human intestine. We used retrograde tracing ex vivo with DiI, with multiple labeling immunohistochemistry, to characterize motor neurons innervating tenial and inter-tenial longitudinal muscle of human colon. The most abundant immunohistochemical markers in the tertiary plexus were vesicular acetylcholine transporter, nitric oxide synthase (NOS), and vasoactive intestinal polypeptide (VIP). Of retrogradely traced motor neurons innervating inter-tenial longitudinal muscle, 95% were located within 6mm oral or anal to the DiI application site. Excitatory motor neuron cell bodies, immunoreactive for choline acetyltransferase (ChAT), were clustered aborally, whereas NOS-immunoreactive cell bodies were distributed either side of the DiI application site. Motor neurons had small cell bodies, averaging 438 + 18µm Tenial and inter-tenial motor neurons innervating the longitudinal muscle have short projections. Inhibitory motor neurons have less polarized projections than cholinergic excitatory motor neurons. Longitudinal and circular muscle layers are innervated by distinct local populations of excitatory and inhibitory motor neurons. A population of human enteric neurons that contribute significantly to colonic motility has been characterized.
Sections du résumé
BACKGROUND
The enteric nervous system contains inhibitory and excitatory motor neurons which modulate smooth muscle contractility. Cell bodies of longitudinal muscle motor neurons have not been identified in human intestine.
METHODS
We used retrograde tracing ex vivo with DiI, with multiple labeling immunohistochemistry, to characterize motor neurons innervating tenial and inter-tenial longitudinal muscle of human colon.
KEY RESULTS
The most abundant immunohistochemical markers in the tertiary plexus were vesicular acetylcholine transporter, nitric oxide synthase (NOS), and vasoactive intestinal polypeptide (VIP). Of retrogradely traced motor neurons innervating inter-tenial longitudinal muscle, 95% were located within 6mm oral or anal to the DiI application site. Excitatory motor neuron cell bodies, immunoreactive for choline acetyltransferase (ChAT), were clustered aborally, whereas NOS-immunoreactive cell bodies were distributed either side of the DiI application site. Motor neurons had small cell bodies, averaging 438 + 18µm
CONCLUSIONS AND INFERENCES
Tenial and inter-tenial motor neurons innervating the longitudinal muscle have short projections. Inhibitory motor neurons have less polarized projections than cholinergic excitatory motor neurons. Longitudinal and circular muscle layers are innervated by distinct local populations of excitatory and inhibitory motor neurons. A population of human enteric neurons that contribute significantly to colonic motility has been characterized.
Substances chimiques
Fluorescent Dyes
0
Nitric Oxide Synthase
EC 1.14.13.39
Choline O-Acetyltransferase
EC 2.3.1.6
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13685Subventions
Organisme : NIH HHS
ID : OT2 OD024899
Pays : United States
Informations de copyright
© 2019 John Wiley & Sons Ltd.
Références
Hennig GW, Costa M, Chen BN, Brookes SJH. Quantitative analysis of peristalsis in the guinea-pig small intestine using spatio-temporal maps. J Physiol. 1999;517(2):575-590.
Smith TK, Robertson WJ. Synchronous movements of the longitudinal and circular muscle during peristalsis in the isolated guinea-pig distal colon. J Physiol. 1998;506(Pt 2):563-577.
Bayliss WM, Starling EH. The movements and innervation of the small intestine. J. Physiol. 1899;24:99-143.
Furness JB. The Enteric Nervous System. Oxford, UK: Blackwell; 2006.
Bayliss WM, Starling EH. The movements and innervation of the small intestine. J. Physiol. 1901;26:125-138.
Lammers WJ. Spatial and temporal coupling between slow waves and pendular contractions. Am J Physiol Gastrointest Liver Physiol. 2005;289(5):G898-903.
Lentle RG, De Loubens C, Hulls C, Janssen PWM, Golding MD, Chambers JP. A comparison of the organization of longitudinal and circular contractions during pendular and segmental activity in the duodenum of the rat and guinea pig. Neurogastroenterol Motil. 2012;24(7):686-e298.
Trendelenburg P. Physiologische und pharmakologische Versuche Uber die Dunndarmperistaltik. Naunyn-Schmiedeberg Arch. Exp.Pathol. Pharmakol, 1917. 81: p. 55-129.
Brookes S, Song Z-M, Steele PA, Costa M. Identification of motor neurons to the longitudinal muscle of the guinea pig ileum. Gastroenterology. 1992;103(3):961-973.
Brookes S, Steele PA, Costa M. Identification and immunohistochemistry of cholinergic and non-cholinergic circular muscle motor neurons in the guinea-pig small intestine. Neuroscience. 1991;42(3):863-878.
Brookes S, Steele PA, Costa M. Calretinin immunoreactivity in cholinergic motor neurones, interneurones and vasomotor neurones in the guinea-pig small intestine. Cell Tissue Res. 1991;263(3):471-481.
Neunlist M, Michel K, Aubé A-C, Galmiche J, Schemann M. Projections of excitatory and inhibitory motor neurones to the circular and longitudinal muscle of the guinea pig colon. Cell Tissue Research. 2001;305(3):325-330.
Porter AJ, Wattchow DA, Brookes SJ, Costa M. The neurochemical coding and projections of circular muscle motor neurons in the human colon. Gastroenterology. 1997;113(6):1916-1923.
Porter AJ, Wattchow DA, Brookes SJ, Costa M. Projections of nitric oxide synthase and vasoactive intestinal polypeptide-reactive submucosal neurons in the human colon. J Gastroenterol Hepatol. 1999;14(12):1180-1187.
Porter AJ, Wattchow DA, Brookes SJH, Costa M. Cholinergic and nitrergic interneurones in the myenteric plexus of the human colon. Gut. 2002;51(1):70-75.
Wattchow DA, Brookes SJ, Costa M. The morphology and projections of retrogradely labeled myenteric neurons in the human intestine. Gastroenterology. 1995;109(3):866-875.
Richardson KC. Electronmicroscopic observations on Auerbach's plexus in the rabbit, with special reference to the problem of smooth muscle innervation. Am J Anat. 1958;103(1):99-135.
Llewellyn-Smith IJ, Costa M, Furness JB, Bornstein JC. Structure of the tertiary component of the myenteric plexus in the guinea-pig small intestine. Cell Tissue Res. 1993;272(3):509-516.
Gabella G. Development and ageing of intestinal musculature and nerves: the guinea-pig taenia coli. J Neurocytol. 2001;30(9-10):733-766.
Bennett MR, Rogers DC. A study of the innervation of the taenia coli. J Cell Biol. 1967;33(3):573-596.
Kuriyama T, Osa T, Toida N. Electrophysiological study of the intestinal smooth muscle of the guinea-pig. J-Physiol. 1967;191:239-255.
Carbone SE, Wattchow DA, Spencer NJ, Brookes SJH. Loss of responsiveness of circular smooth muscle cells from the guinea pig ileum is associated with changes in gap junction coupling. Am J Physiol Gastrointest Liver Physiol. 2012;302(12):G1434-G1444.
Furness JB, Clerc N, Lomax AEG, Bornstein JC, Kunze WAA. Shapes and projections of tertiary plexus neurons of the guinea-pig small intestine. Cell Tissue Res. 2000;300(3):383-387.
Burnstock G, Campbell G, Rand MJ. The inhibitory innervation of the taenia of the guinea-pig caecum. J Physiol. 1966;182(3):504-526.
Bennett MR. Transmission from intramural excitatory nerves to the smooth muscle cells of the guinea-pig taenia coli. J Physiol. 1966;185(1):132-147.
Burnstock G, Campbell G, Satchell D, Smythe A. Evidence that adenosine triphosphate or a related nucleotide is the transmitter substance released by non-adrenergic inhibitory nerves in the gut. Br J Pharmacol. 1970;40(4):668-688.
Campbell G. Nerve-mediated excitation of the taenia of the guinea-pig caecum. J Physiol. 1966;185(1):148-159.
Zhang Y, Paterson WG. Excitatory purinergic neurotransmission in smooth muscle of guinea-pig [corrected] taenia caeci. J Physiol. 2005;563(Pt 3):855-865. [Erratum appears in J Physiol. 2005 May 1;564(Pt 3):953].
Costa M, Furness JB, Humphreys CM. Apamin distinguishes two types of relaxation mediated by enteric nerves in the guinea-pig gastrointestinal tract. Naunyn-Schmiedebergs Archives of Pharmacology. 1986;332(1):79-88.
Grider JR, Cable MB, Bitar KN, Said SI, Makhlouf GM. Vasoactive intestinal peptide. Relaxant neurotransmitter in tenia coli of the guinea pig. Gastroenterology. 1985;89(1):36-42.
Schemann M, Sann H, Schaaf C, Mader M. Identification of cholinergic neurons in enteric nervous system by antibodies against choline acetyltransferase. Am J Physiol. 1993;265(5 Pt 1):G1005-G1009.
Porter AJ, Wattchow DA, Brookes SJ, Schemann M, Costa M. Choline acetyltransferase immunoreactivity in the human small and large intestine. Gastroenterology. 1996;111(2):401-408.
Murphy EMA, Defontgalland D, costa M, brookes SJH, wattchow DA. Quantification of subclasses of human colonic myenteric neurons by immunoreactivity to Hu, choline acetyltransferase and nitric oxide synthase. Neurogastroenterol Motil. 2007;19(2):126-134.
Ng K-S, Montes-Adrian NA, Mahns DA, Gladman MA. Quantification and neurochemical coding of the myenteric plexus in humans: No regional variation between the distal colon and rectum. Neurogastroenterol Motil. 2018;30(3):e13193.
Brookes S. Retrograde tracing of enteric neuronal pathways. Neurogastroenterol Motil. 2001;13(1):1-18.
Tam FS, Hillier K. The role of nitric oxide in mediating non-adrenergic non-cholinergic relaxation in longitudinal muscle of human taenia coli. Life Sci. 1992;51(16):1277-1284.
Jabari S, da Silveira ABM, de Oliveira EC, Quint K, Neuhuber W, Brehmer A. Preponderance of inhibitory versus excitatory intramuscular nerve fibres in human chagasic megacolon. Int J Colorectal Dis. 2012;27(9):1181-1189.
Lentle RG, Janssen PWM, Asvarujanon P, Chambers P, Stafford KJ, Hemar Y. High-definition spatiotemporal mapping of contractile activity in the isolated proximal colon of the rabbit. J Comp Physiol B. 2008;178(3):257-268.
Chen J-H, Yang Z, Yu Y, Huizinga JD. Haustral boundary contractions in the proximal 3-taeniated rabbit colon. Am J Physiol Gastrointest Liver Physiol. 2016;310(3):G181-G192.
Ritchie JA. Colonic motor activity and bowel function. I. Normal movement of contents. Gut. 1968;9(4):442-456.
Schulze-delrieu K, Brown BP, Lange W, et al. Volume shifts, unfolding and rolling of haustra in the isolated guinea pig caecum. Neurogastroenterol Motil. 1996;8(3):217-225.
Rosin DL, Chang DA, Guyenet PG. Afferent and efferent connections of the rat retrotrapezoid nucleus. J Comp Neurol. 2006;499(1):64-89.
Reiche D, Pfannkuche H, Michel K, Hoppe S, Schemann M. Immunohistochemical evidence for the presence of calbindin containing neurones in the myenteric plexus of the guinea-pig stomach. Neurosci Lett. 1999;270(2):71-74.
Bell CC, Meek J, Yang JY. Immunocytochemical identification of cell types in the mormyrid electrosensory lobe. J Comp Neurol. 2005;483(1):124-142.
Gnanamanickam GJ, Llewellyn-Smith IJ. Innervation of the rat uterus at estrus: a study in full-thickness, immunoperoxidase-stained whole-mount preparations. J Comp Neurol. 2011;519(4):621-643.
Heinicke EA, Kiernan JA. An immunohistochemical study of the myenteric plexus of the colon in the rat and mouse. J Anat. 1990;170:51-62.
Olsson C, Chen BN, Jones S, Chataway TK, Costa M, Brookes SJH. Comparison of extrinsic efferent innervation of guinea pig distal colon and rectum. J Comp Neurol. 2006;496(6):787-801.
Morris JL, Zhu B-S, Gibbins IL, Blessing WW. Subpopulations of sympathetic neurons project to specific vascular targets in the pinna of the rabbit ear. J Comp Neurol. 1999;412(1):147-160.
Kim YS, Paik SK, Cho YS, et al. Expression of P2X3 receptor in the trigeminal sensory nuclei of the rat. J Comp Neurol. 2008;506(4):627-639.
Quraishi S, Gayet J, Morgans CW, Duvoisin RM. Distribution of group-III metabotropic glutamate receptors in the retina. J Comp Neurol. 2007;501(6):931-943.
Furness JB, Costa M, Walsh JH. Evidence for and significance of the projection of VIP neurons from the myenteric plexus to the taenia coli in the guinea pig. Gastroenterology. 1981;80(6):1557-1561.