Localization of muscarinic receptors M1R, M2R and M3R in the human colon

Neurogastroenterology and Motility

Volumn 22, Issue 9, 2010, Pages

  Harrington, A M ^a,c   Peck, C J ^a   Liu, L ^b   Burcher, E ^b   Hutson, J M ^a,d   Southwell, B R ^a,c  

^a MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d ROYAL CHILDREN'S HOSPITAL   (Australia)

Author keywords

cholinergic; enteric nervous system; human; immunofluorescence; muscarinic receptor

Indexed keywords

BIOLOGICAL MARKER; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; MUSCARINIC M3 RECEPTOR; RECEPTOR SUBTYPE;

ANTIBODY SPECIFICITY; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CELL TYPE; CELLULAR DISTRIBUTION; CHOLINERGIC NERVE CELL; CHOLINERGIC TRANSMISSION; COLON; CONFOCAL MICROSCOPY; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MUSCLE LENGTH; MYENTERIC PLEXUS; NITRERGIC NERVE; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADOLESCENT; BLOTTING, WESTERN; CHILD; CHILD, PRESCHOOL; COLON; ENTERIC NERVOUS SYSTEM; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, CONFOCAL; MUSCLE, SMOOTH; NEURONS; RECEPTOR, MUSCARINIC M1; RECEPTOR, MUSCARINIC M2; RECEPTOR, MUSCARINIC M3; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 77955443345     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2009.01456.x     Document Type: Article

References (71)

1. Hulme EC. Muscarinic acetylcholine receptors: typical G-coupled receptors. Symp Soc Exp Biol 1990 44 : 39 54.
2. Levey AI. Immunological localization of m1-m5 muscarinic acetylcholine receptors in peripheral tissues and brain. Life Sci 1993 6 : 441 448.
3. Caulfield MP, Birdsall NJ. International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 1998 50 : 279 290.
4. Cooke HJ. Neurotransmitters in neuronal reflexes regulating intestinal secretion. Ann N Y Acad Sci 2000 915 : 77 80.
5. Eglen RM. Muscarinic receptors and gastrointestinal tract smooth muscle function. Life Sci 2001 23 : 2573 2578.
6. North RA, Slack BE, Surprenant A. Muscarinic M1 and M2 receptors mediate depolarization and presynaptic inhibition in guinea-pig enteric nervous system. J Physiol 1985 368 : 435 452.
7. North RA, Tokimasa T. Muscarinic synaptic potentials in guinea-pig myenteric plexus neurones. J Physiol 1982 333 : 151 156. (Pubitemid 13221351)
8. Takeuchi T, Tanaka K, Nakajima H, Matsui M, Azuma YT. M2 and M3 muscarinic receptors are involved in enteric nerve-mediated contraction of the mouse ileum: findings obtained with muscarinic-receptor knockout mouse. Am J Physiol Gastrointest Liver Physiol 2007 292 : G154 64.
9. Law NM, Bharucha AE, Undale AS, Zinsmeister AR. Cholinergic stimulation enhances colonic motor activity, transit, and sensation in humans. Am J Physiol Gastrointest Liver Physiol 2001 281 : G1228 37.
10. Giraldo E, Martos F, Gomez A et al. Characterization of muscarinic receptor subtypes in human tissues. Life Sci 1988 43 : 1507 1515.
11. Gomez A, Martos F, Bellido I et al. Muscarinic receptor subtypes in human and rat colon smooth muscle. Biochem Pharmacol 1992 43 : 2413 2419.
12. Mansfield KJ, Mitchelson FJ, Moore KH, Burcher E. Muscarinic receptor subtypes in the human colon: lack of evidence for atypical subtypes. Eur J Pharmacol 2003 3 : 101 109.
13. Oue T, Yoneda A, Shima H, Puri P. Muscarinic acetylcholine receptor expression in aganglionic bowel. Pediatr Surg Int 2000 16 : 267 271.
14. Jonsson M, Norrgard O, Forsgren S. Presence of a marked nonneuronal cholinergic system in human colon: study of normal colon and colon in ulcerative colitis. Inflamm Bowel Dis 2007 13 : 1347 1356.
15. Harrington AM, Hutson JM, Southwell BR. Localisation of muscarinic receptor M1r-M3r immunoreactivity in human colon. Neurogastroenterol Motil 2006 18 : 777.
16. King SK, Sutcliffe JR, Hutson JM. Laparoscopic seromuscular colonic biopsies: a surgeon's experience. J Pediatr Surg 2005 40 : 381 384.
17. Garzon M, Pickel VM. Subcellular distribution of M2 muscarinic receptors in relation to dopaminergic neurons of the rat ventral tegmental area. J Comp Neurol 2006 498 : 821 839.
18. Enriquez de Salamanca A, Siemasko KF, Diebold Y et al. Expression of muscarinic and adrenergic receptors in normal human conjunctival epithelium. Invest Ophthalmol Vis Sci 2005 46 : 504 513.
19. Rybin VO, Xu X, Lisanti MP, Steinberg SF. Differential targeting of beta-adrenergic receptor subtypes and adenylyl cyclase to cardimyocyte caveolae. A mechanism to functionally regulate the cAMP signaling pathway. J Biol Chem 2000 275 : 41447 41457.
20. Fu ML, Gerd W, Ake H, Johan H. Agonist-like activity of anti-peptide antibodies directed against an autoimmune epitope on the heart muscarinic acetylcholine receptor. Receptors Channels 1994 2 : 121 130.
21. Disney AA, Domakonda KV, Aoki C. Differential expression of muscarinic acetylcholine receptors across excitatory and inhibitory cells in visual cortical areas V1 and V2 of the macaque monkey. J Comp Neurol 2006 499 : 49 63.
22. Tong YC, Cheng JT, Hsu CT. Alterations of M(2)-muscarinic receptor protein and mRNA expression in the urothelium and muscle layer of the streptozotocin-induced diabetic rat urinary bladder. Neurosci Lett 2006 406 : 216 221.
23. Wreggett KA, Wells JW. Cooperativity manifest in the binding properties of purified cardiac muscarinic receptors. J Biol Chem 1995 270 : 22488 22499.
24. Kerr PM, Hillier K, Wallis RM, Garland CJ. Characterization of muscarinic receptors mediating contractions of circular and longitudinal muscle of human isolated colon. Br J Pharmacol 1995 115 : 1518 1524.
25. Schemann M, Michel K, Peters S, Bischoff SC, Neunlist M. Cutting-edge technology. III. Imaging and the gastrointestinal tract: mapping the human enteric nervous system. Am J Physiol Gastrointest Liver Physiol 2002 282 : G919 25.
26. Harrington AM, Hutson JM, Southwell BR. Immunohistochemical localisation of cholinergic muscarinic receptor subtype 1 (M1r) in the guinea pig and human enteric nervous system. J Chem Neuroanat 2007 33 : 193 201.
27. Uchiyama T, Chess-Williams R. Muscarinic receptor subtypes of the bladder and gastrointestinal tract. J Smooth Muscle Res 2004 40 : 237 247.
28. Al-Saffar A, Hellstrom PM. Contractile responses to natural tachykinins and selective tachykinin analogs in normal and inflamed ileal and colonic muscle. Scand J Gastroenterol 2001 36 : 485 493.
29. Tobin G, Giglio D, Lundgren O. Muscarinic receptor subtypes in the alimentary tract. J Physiol Pharmacol 2009 60 : 3 21.
30. Giglio D, Tobin G. Muscarinic receptor subtypes in the lower urinary tract. Pharmacology 2009 83 : 259 269.
31. Vizi ES, Kobayashi O, Torocsik A et al. Heterogeneity of presynaptic muscarinic receptors involved in modulation of transmitter release. Neuroscience 1989 31 : 259 267.
32. Ward SM, Dalziel HH, Khoyi MA, Westfall AS, Sanders KM, Westfall DP. Hyperpolarization and inhibition of contraction mediated by nitric oxide released from enteric inhibitory neurones in guinea-pig taenia coli. Br J Pharm 1996 118 : 49 56.
33. Dietrich C, Kilbinger H. Prejunctional M1 and postjunctional M3 muscarinic receptors in the circular muscle of the guinea-pig ileum. Naunyn Schmiedebergs Arch Pharmacol 1995 351 : 237 243.
34. Eglen RM, Choppin A, Watson N. Therapeutic opportunities from muscarinic receptor research. Trends Pharmacol Sci 2001 22 : 409 414.
35. Schemann M. Control of gastrointestinal motility by the "gut brain"- the enteric nervous system. J Pediatr Gastroenterol Nutr 2005 41 (Suppl. 1 S4 6.
36. Porter AJ, Wattchow DA, Brookes SJ, Costa M. Cholinergic and nitrergic interneurones in the myenteric plexus of the human colon. Gut 2002 51 : 70 5.
37. 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 : 1916 1923.
38. Quinson N, Robbins HL, Clark MJ, Furness JB. Calbindin immunoreactivity of enteric neurons in the guinea-pig ileum. Cell Tissue Res 2001 305 : 3 9.
39. Brehmer A, Croner R, Dimmler A, Papadopoulos T, Schrodl F, Neuhuber W. Immunohistochemical characterization of putative primary afferent (sensory) myenteric neurons in human small intestine. Auton Neurosci 2004 2 : 49 59.
40. Johnson PJ, Bornstein JC, Yuan SY, Furness JB. Analysis of contributions of acetylcholine and tachykinins to neuro-neuronal transmission in motility reflexes in the guinea-pig ileum. Br J Pharmacol 1996 118 : 973 983.
41. Izzo AA, Mascolo N, Di Carlo G, Capasso F. Ascending neural pathways in the isolated guinea-pig ileum: effect of muscarinic M1, M2 and M3 cholinergic antagonists. Neuroscience 1999 91 : 1575 1580.
42. Olgart C, Iversen HH. Nitric oxide-dependent relaxation induced by M1 muscarinic receptor activation in the rat small intestine. Br J Pharmacol 1999 127 : 309 313.
43. Iverson H, Wiklund NP, Olgart C, Gustafsson LE. Nerve stimulation-induced nitric oxide release as a consequence of muscarinic M1 receptor activation. Eur J Pharmacol 1997 331 : 213 219.
44. Wiklund CU, Wiklund NP, Gustafsson LE. Modulation of neuroeffector transmission by endogenous nitric oxide: a role for acetylcholine receptor-activated nitric oxide formation, as indicated by measurements of nitric oxide/nitrite release. Eur J Pharmacol 1993 3 : 235 242.
45. Andriantsitohaina R, Surprenant A. Acetylcholine released from guinea-pig submucosal neurones dilates arterioles by releasing nitric oxide from endothelium. J Physiol 1992 453 : 493 502.
46. Neild TO, Shen KZ, Surprenant A. Vasodilatation of arterioles by acetylcholine released from single neurones in the guinea-pig submucosal plexus. J Physiol 1990 420 : 247 265.
47. Surprenant A. Control of the gastrointestinal tract by enteric neurons. Annu Rev Physiol 1994 56 : 117 140.
48. Kotecha N. Mechanisms underlying ACh induced modulation of neurogenic and applied ATP constrictions in the submucosal arterioles of the guinea-pig small intestine. Br J Pharmacol 1999 126 : 1625 1633.
49. Kotecha N, Coffa FP. NO mediates postjunctional inhibitory effect of neurogenic ACh in guinea pig small intestinal microcirculation. Am J Physiol 1999 2 : H1441 6.
50. Kotecha N, Neild TO. Vasodilatation and smooth muscle membrane potential changes in arterioles from the guinea-pig small intestine. J Physiol 1995 3 : 661 667.
51. Bungardt E, Vockert E, Feifel R et al. Characterization of muscarinic receptors mediating vasodilation in guinea-pig ileum submucosal arterioles by the use of computer-assisted videomicroscopy. Eur J Pharmacol 1992 213 : 53 61.
52. Hatoum OA, Binion DG, Miura H, Telford G, Otterson MF, Gutterman DD. Role of hydrogen peroxide in ACh-induced dilation of human submucosal intestinal microvessels. Am J Physiol Heart Circ Physiol 2005 288 : H48 54.
53. Hatoum OA, Binion DG, Otterson MF, Gutterman DD. Acquired microvascular dysfunction in inflammatory bowel disease: loss of nitric oxide-mediated vasodilation. Gastroenterology 2003 125 : 58 69.
54. Carey HV, Tien XY, Wallace LJ, Cooke HJ. Muscarinic receptor subtypes mediating the mucosal response to neural stimulation of guinea pig ileum. Am J Physiol 1987 253 : G323 9.
55. O'Malley KE, Farrell CB, O'Boyle KM, Baird AW. Cholinergic activation of Cl-secretion in rat colonic epithelia. Eur J Pharmacol 1995 275 : 83 9.
56. Kuwahara A, Tien XY, Wallace LJ, Cooke HJ. Cholinergic receptors mediating secretion in guinea pig colon. J Pharmacol Exp Ther 1987 242 : 600 606. (Pubitemid 17143495)
57. Haberberger R, Schultheiss G, Diener M. Epithelial muscarinic M1 receptors contribute to carbachol-induced ion secretion in mouse colon. Eur J Pharmacol 2006 530 : 229 233.
58. Pradidarcheep W, Stallen J, Labruyere WT, Dabhoiwala NF, Michel MC, Lamers WH. Lack of specificity of commercially available antisera against muscarinergic and adrenergic receptors. Naunyn Schmiedebergs Arch Pharmacol 2009 379 : 397 402.
59. Zeng F, Wess J. Molecular aspects of muscarinic receptor dimerization. Neuropsychopharmacology 2000 4 (Suppl. S19 31.
60. Colozo AT, Park PS, Sum CS, Pisterzi LF, Wells JW. Cholesterol as a determinant of cooperativity in the M2 muscarinic cholinergic receptor. Biochem Pharmacol 2007 74 : 236 255.
61. Jadcheral S. Inflammation inhibits muscarinic signaling in in vivo canine colonic circular smooth muscle cells. Pediatr Res 2002 52 : 756 762.
62. Goldblatt F, Gordon TP, Waterman SA. Antibody-mediated gastrointestinal dysmotility in scleroderma erratum appears in Gastroenterology 2002 Dec;123(6):2164 Gastroenterology 2002 123 : 1144 1150.
63. Anini Y, Brubaker PL. Muscarinic receptors control glucagon-like peptide 1 secretion by human endocrine L cells. Endocrinology 2003 144 : 3244 3250.
64. Balks HJ, Holst JJ, von zur Muhlen A, Brabant G. Rapid oscillations in plasma glucagon-like peptide-1 (GLP-1) in humans: cholinergic control of GLP-1 secretion via muscarinic receptors. J Clin Endocrinol Metab 1997 82 : 786 790.
65. Zhang Z, Koch TR, Mustin E, Walgenbach-Telford S, Telford GL. Muscarinic cholinergic receptor density following small intestinal transplantation in rats. Am J Physiol 1993 265 : G1057 63.
66. Matsui M, Griffin MT, Shehnaz D, Taketo MM, Ehlert FJ. Increased relaxant action of forskolin and isoproterenol against muscarinic agonist-induced contractions in smooth muscle from M2 receptor knockout mice. J Pharmacol Exp Ther 2003 305 : 106 113.
67. Coulson FR, Jacoby DB, Fryer AD. Increased function of inhibitory neuronal M2 muscarinic receptors in trachea and ileum of diabetic rats. Br J Pharmacol 2002 135 : 1355 1362.
68. Borody TJ, Quigley EM, Phillips SF et al. Effects of morphine and atropine on motility and transit in the human ileum. Gastroenterology 1985 89 : 562 570.
69. Lecci A, Santicioli P, Maggi CA. Pharmacology of transmission to gastrointestinal muscle. Curr Opin Pharmacol 2002 2 : 630 641.
70. Zinner N. Darifenacin: a muscarinic M3-selective receptor antagonist for the treatment of overactive bladder. Expert Opin Pharmacother 2007 8 : 511 523.
71. Tytgat GN. Hyoscine butylbromide: a review of its use in the treatment of abdominal cramping and pain. Drugs 2007 67 : 1343 1357.