Role of m1, m3, and m5 muscarinic acetylcholine receptors in cholinergic dilation of small arteries studied with gene-targeted mice

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 300, Issue 5, 2011, Pages

  Gericke, Adrian ^a   Sniatecki, Jan J ^a   Mayer, Veronique G A ^a   Goloborodko, Evgeny ^a   Patzak, Andreas ^b   Wess, Jürgen ^c   Pfeiffer, Norbert ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Genetically altered mice; Muscarinic receptors; Vasodilation

Indexed keywords

ACETYLCHOLINE; ATROPINE; CARBACHOL; MESSENGER RNA; MUSCARINIC M1 RECEPTOR; MUSCARINIC M3 RECEPTOR; MUSCARINIC M5 RECEPTOR; NITROPRUSSIDE SODIUM; SUBSTANCE P; VASODILATOR AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL REACTIVITY; CANNULATION; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; EMBRYO; GENE TARGETING; MICROPIPETTE; MICROSCOPY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RENAL ARTERY; SKELETAL MUSCLE; SKIN BLOOD VESSEL; VASODILATATION; ANIMAL; ANIMAL MODEL; ARTERY; DOSE RESPONSE; DRUG EFFECT; GENETICS; KIDNEY; MALE; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; SKIN; VASCULARIZATION;

ACETYLCHOLINE; ANIMALS; ARTERIES; DOSE-RESPONSE RELATIONSHIP, DRUG; KIDNEY; MALE; MICE; MICE, KNOCKOUT; MODELS, ANIMAL; MUSCLE, SKELETAL; NITROPRUSSIDE; RECEPTOR, MUSCARINIC M1; RECEPTOR, MUSCARINIC M3; RECEPTOR, MUSCARINIC M5; RNA, MESSENGER; SKIN; SUBSTANCE P; VASODILATION; VASODILATOR AGENTS;

EID: 79955767962     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00982.2010     Document Type: Article

References (49)

1. Altiere RJ, Travis DC, Roberts J, Thompson DC. Pharmacological characterization of muscarinic receptors mediating acetylcholine-induced contraction and relaxation in rabbit intrapulmonary arteries. J Pharmacol Exp Ther 270: 269-276, 1994.
2. Beny JL, Nguyen MN, Marino M, Matsui M. Muscarinic receptor knockout mice confirm involvement of M3 receptor in endotheliumdependent vasodilatation in mouse arteries. J Cardiovasc Pharmacol 51: 505-512, 2008.
3. Boulanger CM, Morrison KJ, Vanhoutte PM. Mediation by M3- muscarinic receptors of both endothelium-dependent contraction and relaxation to acetylcholine in the aorta of the spontaneously hypertensive rat. Br J Pharmacol 112: 519-524, 1994.
4. Bridges TM, Marlo JE, Niswender CM, Jones CK, Jadhav SB, Gentry PR, Plumley HC, Weaver CD, Conn PJ, Lindsley CW. Discovery of the first highly M5-preferring muscarinic acetylcholine receptor ligand, an M5 positive allosteric modulator derived from a series of 5-trifluoromethoxy N-benzyl isatins. J Med Chem 52: 3445-3448, 2009.
5. Bruning TA, Chang PC, Hendriks MG, Vermeij P, Pfaffendorf M, van Zwieten PA. In vivo characterization of muscarinic receptor subtypes that mediate vasodilatation in patients with essential hypertension. Hypertension 26: 70-77, 1995.
6. Bruning TA, Hendriks MG, Chang PC, Kuypers EA, van Zwieten PA. In vivo characterization of vasodilating muscarinic-receptor subtypes in humans. Circ Res 74: 912-919, 1994.
7. Brunner F, Kuhberger E, Groschner K, Poch G, Kukovetz WR. Characterization of muscarinic receptors mediating endothelium-dependent relaxation of bovine coronary artery. Eur J Pharmacol 200: 25-33, 1991.
8. Budzik B, Garzya V, Shi D, Foley JJ, Rivero RA, Langmead CJ, Watson J, Wu Z, Forbes IT, Jin J. 2' Biaryl amides as novel and subtype selective M1 agonists. Part I. Identification, synthesis, and initial SAR. Bioorg Med Chem Lett 20: 3540-3544, 2010.
9. Caulfield MP, Birdsall NJ. International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 50: 279-290, 1998.
10. Chiba S, Tsukada M. Possible involvement of muscarinic M1 and M3 receptor subtypes mediating vasodilation in isolated, perfused canine lingual arteries. Clin Exp Pharmacol Physiol 23: 839-843, 1996.
11. Dauphin F, Hamel E. Muscarinic receptor subtype mediating vasodilation feline middle cerebral artery exhibits M3 pharmacology. Eur J Pharmacol 178: 203-213, 1990.
12. Eglen RM, Nahorski SR. The muscarinic M5 receptor: a silent or emerging subtype? Br J Pharmacol 130: 13-21, 2000.
13. Elhusseiny A, Hamel E. Muscarinic- but not nicotinic-acetylcholine receptors mediate a nitric oxide-dependent dilation in brain cortical arterioles: a possible role for the M5 receptor subtype. J Cereb Blood Flow Metab 20: 298-305, 2000.
14. Eltze M, Ullrich B, Mutschler E, Moser U, Bungardt E, Friebe T, Gubitz C, Tacke R, Lambrecht G. Characterization of muscarinic receptors mediating vasodilation in rat perfused kidney. Eur J Pharmacol 238: 343-355, 1993.
15. Faraci FM, Sigmund CD. Vascular biology in genetically altered mice: smaller vessels, bigger insight. Circ Res 85: 1214-1225, 1999.
16. Fernandes FA, Alonso MJ, Marin J, Salaices M. M3-muscarinic receptor mediates prejunctional inhibition of noradrenaline release and the relaxation in cat femoral artery. J Pharm Pharmacol 43: 644-649, 1991.
17. Fisahn A, Yamada M, Duttaroy A, Gan JW, Deng CX, McBain CJ, Wess J. Muscarinic induction of hippocampal gamma oscillations requires coupling of the M1 receptor to two mixed cation currents. Neuron 33: 615-624, 2002.
18. Flaim SF, Weitzel RL, Zelis R. Mechanism of action of nitroglycerin during exercise in a rat model of heart failure. Improvement of blood flow to the renal, splanchnic, and cutaneous beds. Circ Res 49: 458-468, 1981.
19. Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288: 373-376, 1980.
20. Gericke A, Mayer VG, Steege A, Patzak A, Neumann U, Grus FH, Joachim SC, Choritz L, Wess J, Pfeiffer N. Cholinergic responses of ophthalmic arteries in M3 and M5 muscarinic acetylcholine receptor knockout mice. Invest Ophthalmol Vis Sci 50: 4822-4827, 2009.
21. Hendriks MG, Pfaffendorf M, Van Zwieten PA. Characterization of the muscarinic receptor subtype mediating vasodilation in the rat perfused mesenteric vascular bed preparation. J Auton Pharmacol 12: 411-420, 1992.
22. Hendriks MG, Pfaffendorf M, van Zwieten PA. Characterization of the muscarinic receptors in the mesenteric vascular bed of spontaneously hypertensive rats. J Hypertens 11: 1329-1335, 1993.
23. Hsu HH, Duning K, Meyer HH, Stolting M, Weide T, Kreusser S, van Le T, Gerard C, Telgmann R, Brand-Herrmann SM, Pavenstadt H, Bek MJ. Hypertension in mice lacking the CXCR3 chemokine receptor. Am J Physiol Renal Physiol 296: F780-F789, 2009.
24. Klonizakis M, Tew G, Michaels J, Saxton J. Impaired microvascular endothelial function is restored by acute lower-limb exercise in postsurgical varicose vein patients. Microvasc Res 77: 158-162, 2009.
25. Lamping KG, Wess J, Cui Y, Nuno DW, Faraci FM. Muscarinic (M) receptors in coronary circulation: gene-targeted mice define the role of M2 and M3 receptors in response to acetylcholine. Arterioscler Thromb Vasc Biol 24: 1253-1258, 2004.
26. Leung HS, Leung FP, Yao X, Ko WH, Chen ZY, Vanhoutte PM, Huang Y. Endothelial mediators of the acetylcholine-induced relaxation of the rat femoral artery. Vascul Pharmacol 44: 299-308, 2006.
27. Ma L, Seager MA, Wittmann M, Jacobson M, Bickel D, Burno M, Jones K, Graufelds VK, Xu G, Pearson M, McCampbell A, Gaspar R, Shughrue P, Danziger A, Regan C, Flick R, Pascarella D, Garson S, Doran S, Kreatsoulas C, Veng L, Lindsley CW, Shipe W, Kuduk S, Sur C, Kinney G, Seabrook GR, Ray WJ. Selective activation of the M1 muscarinic acetylcholine receptor achieved by allosteric potentiation. Proc Natl Acad Sci USA 106: 15950-15955, 2009.
28. McCormack DG, Mak JC, Minette P, Barnes PJ. Muscarinic receptor subtypes mediating vasodilation in the pulmonary artery. Eur J Pharmacol 158: 293-297, 1988.
29. Norel X, Walch L, Costantino M, Labat C, Gorenne I, Dulmet E, Rossi F, Brink C. M1 and M3 muscarinic receptors in human pulmonary arteries. Br J Pharmacol 119: 149-157, 1996.
30. Obi T, Kabeyama A, Nishio A. Characterization of muscarinic receptor subtype mediating contraction and relaxation in equine coronary artery in vitro. J Vet Pharmacol Ther 17: 226-231, 1994.
31. Pelc LR, Daemmgen JW, Gross GJ, Warltier DC. Muscarinic receptor subtypes mediating myocardial blood flow redistribution. J Cardiovasc Pharmacol 11: 424-431, 1988.
32. Pesic S, Jovanovic A, Grbovic L. Muscarinic receptor subtypes mediating vasorelaxation of the perforating branch of the human internal mammary artery. Pharmacology 63: 185-190, 2001.
33. Peyter AC, Muehlethaler V, Liaudet L, Marino M, Di Bernardo S, Diaceri G, Tolsa JF. Muscarinic receptor M1 and phosphodiesterase 1 are key determinants in pulmonary vascular dysfunction following perinatal hypoxia in mice. Am J Physiol Lung Cell Mol Physiol 295: L201-L213, 2008.
34. Phillips JK, Vidovic M, Hill CE. Variation in mRNA expression of alpha-adrenergic, neurokinin and muscarinic receptors amongst four arteries of the rat. J Auton Nerv Syst 62: 85-93, 1997.
35. Ren LM, Nakane T, Chiba S. Muscarinic receptor subtypes mediating vasodilation and vasoconstriction in isolated, perfused simian coronary arteries. J Cardiovasc Pharmacol 22: 841-846, 1993.
36. Ryberg AT, Selberg H, Soukup O, Gradin K, Tobin G. Cholinergic submandibular effects and muscarinic receptor expression in blood vessels of the rat. Arch Oral Biol 53: 605-616, 2008.
37. Scremin OU, Jenden DJ. Cholinergic control of cerebral blood flow in stroke, trauma and aging. Life Sci 58: 2011-2018, 1996.
38. Shimizu T, Rosenblum WI, Nelson GH. M3 and M1 receptors in cerebral arterioles in vivo: evidence for downregulated or ineffective M1 when endothelium is intact. Am J Physiol Heart Circ Physiol 264: H665-H669, 1993.
39. Simonsen U, Prieto D, Rivera L, Hernandez M, Mulvany MJ, Garcia- Sacristan A. Heterogeneity of muscarinic receptors in lamb isolated coronary resistance arteries. Br J Pharmacol 109: 998-1007, 1993.
40. Stahl E, Ellis J. Novel allosteric effects of amiodarone at the muscarinic M5 receptor. J Pharmacol Exp Ther 334: 214-222, 2010.
41. Tong XK, Hamel E. Regional cholinergic denervation of cortical microvessels and nitric oxide synthase-containing neurons in Alzheimer's disease. Neuroscience 92: 163-175, 1999.
42. Vita JA, Treasure CB, Nabel EG, McLenachan JM, Fish RD, Yeung AC, Vekshtein VI, Selwyn AP, Ganz P. Coronary vasomotor response to acetylcholine relates to risk factors for coronary artery disease. Circulation 81: 491-497, 1990.
43. Wess J. Molecular biology of muscarinic acetylcholine receptors. Crit Rev Neurobiol 10: 69-99, 1996.
44. Wess J. Muscarinic acetylcholine receptor knockout mice: novel phenotypes and clinical implications. Annu Rev Pharmacol Toxicol 44: 423-450, 2004.
45. Wess J, Eglen RM, Gautam D. Muscarinic acetylcholine receptors: mutant mice provide new insights for drug development. Nat Rev Drug Discov 6: 721-733, 2007.
46. Yamada M, Lamping KG, Duttaroy A, Zhang W, Cui Y, Bymaster FP, McKinzie DL, Felder CC, Deng CX, Faraci FM, Wess J. Cholinergic dilation of cerebral blood vessels is abolished in M5 muscarinic acetylcholine receptor knockout mice. Proc Natl Acad Sci USA 98: 14096-14101, 2001.
47. Yamada M, Miyakawa T, Duttaroy A, Yamanaka A, Moriguchi T, Makita R, Ogawa M, Chou CJ, Xia B, Crawley JN, Felder CC, Deng CX, Wess J. Mice lacking the M3 muscarinic acetylcholine receptor are hypophagic and lean. Nature 410: 207-212, 2001.
48. Zagvazdin Y, Fitzgerald ME, Reiner A. Role of muscarinic cholinergic transmission in Edinger-Westphal nucleus-induced choroidal vasodilation in pigeon. Exp Eye Res 70: 315-327, 2000.
49. Zapata-Sudo G, Pereira SL, Beiral HJ, Kummerle AE, Raimundo JM, Antunes F, Sudo RT, Barreiro EJ, Fraga CA. Pharmacological characterization of (3-thienylidene)-3,4-methylenedioxybenzoylhydrazide: a novel muscarinic agonist with antihypertensive profile. Am J Hypertens 23: 135-141, 2010.