M5 receptor activation produces opposing physiological outcomes in dopamine neurons depending on the receptor's location

Journal of Neuroscience

Volumn 34, Issue 9, 2014, Pages 3253-3262

  Foster, Daniel J ^a   Gentry, Patrick R ^a   Lizardi Ortiz, Jose E ^b   Bridges, Thomas M ^a,c   Wood, Michael R ^a,c,d   Niswender, Colleen M ^a,c   Sulzer, David ^b   Lindsley, Craig W ^a,c,d   Xiang, Zixiu ^a   Conn, P Jeffrey ^a,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

Acetylcholine; Allosteric; Dopamine; MAChR; Muscarinic

Indexed keywords

MUSCARINIC AGENT; MUSCARINIC M5 RECEPTOR; OXOTREMORINE M; SCOPOLAMINE; UNCLASSIFIED DRUG; VU 0238429; 1 (4 METHOXYBENZYL) 5 (TRIFLUOROMETHOXY)INDOLINE 2,3 DIONE; 1-(4-METHOXYBENZYL)-5-(TRIFLUOROMETHOXY)INDOLINE-2,3-DIONE; ACETYLCHOLINE; CALCIUM; DOPAMINE; INDOLE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; LONG TERM POTENTIATION; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; SPIKE WAVE; SUBSTANTIA NIGRA PARS COMPACTA; ALLOSTERIC; ANIMAL; BRAIN; C57BL MOUSE; CHO CELL; CRICETULUS; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; IN VITRO STUDY; KNOCKOUT MOUSE; MACHR; MEMBRANE POTENTIAL; METABOLISM; MUSCARINIC; NEWBORN; PHYSIOLOGY; PROTEIN BINDING; SPRAGUE DAWLEY RAT;

ACETYLCHOLINE; ALLOSTERIC; DOPAMINE; MACHR; MUSCARINIC;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CALCIUM; CHO CELLS; CRICETULUS; DOPAMINE; DOPAMINERGIC NEURONS; DOSE-RESPONSE RELATIONSHIP, DRUG; INDOLES; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, MUSCARINIC M5; TRANSFECTION;

EID: 84894435993     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4896-13.2014     Document Type: Article

References (39)

1. Basile AS, Fedorova I, Zapata A, Liu X, Shippenberg T, Duttaroy A, Yamada M, Wess J (2002) Deletion of the M5 muscarinic acetylcholine receptor attenuates morphine reinforcement and withdrawal but not morphine analgesia. Proc Natl Acad Sci U S A 99:11452-11457. CrossRef Medline
2. Bendor J, Lizardi-Ortiz JE, Westphalen RI, Brandstetter M, HemmingsHCJr, Sulzer D, Flajolet M, Greengard P (2010) AGAP1/AP-3-dependent endocytic recycling ofM5muscarinic receptors promotes dopamine release. EMBO J 29:2813-2826. CrossRef Medline
3. Bonner TI, Young AC, Brann MR, Buckley NJ (1988) Cloning and expression of the human and rat m5 muscarinic acetylcholine receptor genes. Neuron 1:403-410. CrossRef Medline
4. Bridges TM, Marlo JE, NiswenderCM, Jones CK, Jadhav SB, Gentry PR, Plumley HC, Weaver CD, Conn PJ, LindsleyCW (2009) Discovery of the first highly M5-preferring muscarinic acetylcholine receptor ligand, anM5positive allosteric modulator derived from a series of 5-trifluoromethoxy N-benzyl isatins. J Med Chem 52:3445-3448. CrossRef Medline
5. Bridges TM, Kennedy JP, Cho HP, Breininger ML, Gentry PR, Hopkins CR, Conn PJ, Lindsley CW (2010) Chemical lead optimization of a pan Gq mAChR M1, M3, M5 positive allosteric modulator (PAM) lead. Part I: development of the first highly selective M5 PAM. Bioorg Med Chem Lett 20:558-562. CrossRef Medline
6. Bymaster FP, Carter PA, Yamada M, Gomeza J, Wess J, Hamilton SE, Nathanson NM, McKinzie DL, Felder CC (2003) Role of specific muscarinic receptor subtypes in cholinergic parasympathomimetic responses, in vivo phosphoinositide hydrolysis, and pilocarpine-induced seizure activity. Eur J Neurosci 17:1403-1410. CrossRef Medline
7. Chan WY, McKinzie DL, Bose S, Mitchell SN, Witkin JM, Thompson RC, Christopoulos A, Lazareno S, Birdsall NJ, Bymaster FP, Felder CC (2008) Allosteric modulation of the muscarinic M4 receptor as an approach to treating schizophrenia. Proc Natl Acad Sci U S A 105:10978-10983. CrossRef Medline
8. De Luca V, Wang H, Squassina A, Wong GW, Yeomans J, Kennedy JL (2004) Linkage of M5 muscarinic and alpha7-nicotinic receptor genes on 15q13 to schizophrenia. Neuropsychobiology 50:124-127. CrossRef Medline
9. Eglen RM, Choppin A, Dillon MP, Hegde S (1999) Muscarinic receptor ligands and their therapeutic potential. Curr Opin Chem Biol 3:426-432. CrossRef Medline
10. Forster GL, Yeomans JS, Takeuchi J, BlahaCD (2002) M5muscarinic receptors are required for prolonged accumbal dopamine release after electrical stimulation of the pons in mice. J Neurosci 22:RC190. Medline
11. Foster DJ, Jones CK, Conn PJ (2012) Emerging approaches for treatment of schizophrenia: modulation of cholinergic signaling. Discov Med 14:413-420. Medline
12. Guzman JN, Sánchez-Padilla J, Chan CS, Surmeier DJ (2009) Robust pacemaking in substantia nigra dopaminergic neurons. J Neurosci 29:11011-11019. CrossRef Medline
13. Katzenschlager R, Sampaio C, Costa J, Lees A (2003) Anticholinergics for symptomatic management of Parkinson's disease. Cochrane Database Syst Rev 2:CD003735. Medline
14. Lacey MG, Calabresi P, North RA (1990) Muscarine depolarizes rat substantia nigra zona compacta and ventral tegmental neurons in vitro through M1-like receptors. J Pharmacol Exp Ther 253:395-400. Medline
15. Lester DB, Rogers TD, Blaha CD (2010) Acetylcholine-dopamine interactions in the pathophysiology and treatment of CNS disorders. CNS Neurosci Ther 16:137-162. CrossRef Medline
16. Liao CF, Themmen AP, Joho R, Barberis C, Birnbaumer M, Birnbaumer L (1989) Molecular cloning and expression of a fifth muscarinic acetylcholine receptor. J Biol Chem 264:7328-7337. Medline
17. 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 (2009) Selective activation of the M1 muscarinic acetylcholine receptor achieved by allosteric potentiation. Proc Natl Acad SciU S A 106:15950-15955. CrossRef Medline
18. Marlo JE, Niswender CM, Days EL, Bridges TM, Xiang Y, Rodriguez AL, Shirey JK, Brady AE, Nalywajko T, Luo Q, Austin CA, Williams MB, Kim K, Williams R, Orton D, Brown HA, Lindsley CW, Weaver CD, Conn PJ (2009) Discovery and characterization of novel allosteric potentiators of M1muscarinic receptors reveals multiple modes of activity. Mol Pharmacol 75:577-588. CrossRef Medline
19. Mena-Segovia J, Winn P, Bolam JP (2008) Cholinergic modulation of midbrain dopaminergic systems. Brain Res Rev 58:265-271. CrossRef Medline
20. Möhler H, Fritschy JM, Rudolph U (2002) A new benzodiazepine pharmacology. J Pharmacol Exp Ther 300:2-8. CrossRef Medline
21. Oldenburg IA, Ding JB (2011) Cholinergic modulation of synaptic integration and dendritic excitability in the striatum. Curr Opin Neurobiol 21: 425-432. CrossRef Medline
22. Patel JC, Rossignol E, Rice ME, Machold RP (2012) Opposing regulation of dopaminergic activity and exploratory motor behavior by forebrain and brainstem cholinergic circuits. Nat Commun 3:1172. CrossRef Medline
23. Purves D (2012) Neuroscience, Ed 5. Sunderland, MA: Sinauer Associates.
24. Rice ME, Patel JC, Cragg SJ (2011) Dopamine release in the basal ganglia. Neuroscience 198:112-137. CrossRef Medline
25. Schmitz Y, Schmauss C, Sulzer D (2002) Altered dopamine release and uptake kinetics in mice lacking D2 receptors. J Neurosci 22:8002-8009. Medline
26. Shekhar A, Potter WZ, Lightfoot J, Lienemann J, Dubé S, Mallinckrodt C, Bymaster FP, McKinzie DL, Felder CC (2008) Selective muscarinic receptor agonist xanomeline as a novel treatment approach for schizophrenia. Am J Psychiatry 165:1033-1039. CrossRef Medline
27. Shirey JK, Xiang Z, Orton D, Brady AE, Johnson KA, Williams R, Ayala JE, Rodriguez AL, Wess J, Weaver D, Niswender CM, Conn PJ (2008) An allosteric potentiator of M4 mAChR modulates hippocampal synaptic transmission. Nat Chem Biol 4:42-50. CrossRef Medline
28. Shirey JK, Brady AE, Jones PJ, Davis AA, Bridges TM, Kennedy JP, Jadhav SB, Menon UN, Xiang Z, Watson ML, Christian EP, Doherty JJ, Quirk MC, Snyder DH, Lah JJ, Levey AI, Nicolle MM, Lindsley CW, Conn PJ (2009) A selective allosteric potentiator of the M1 muscarinic acetylcholine receptor increases activity of medial prefrontal cortical neurons and restores impairments in reversal learning. J Neurosci 29:14271-14286. CrossRef Medline
29. Steidl S, Miller AD, Blaha CD, Yeomans JS (2011) M(5) muscarinic receptors mediate striatal dopamine activation by ventral tegmental morphine and pedunculopontine stimulation in mice. PLoS One 6:e27538. CrossRef Medline
30. Suratman S, Leach K, Sexton P, Felder C, Loiacono R, Christopoulos A (2011) Impact of species variability and 'probe-dependence' on the detection and in vivo validation of allosteric modulation at the M4 muscarinic acetylcholine receptor. Br J Pharmacol 162:1659-1670. CrossRef Medline
31. ThomsenM, Woldbye DP, Wörtwein G, Fink-Jensen A, Wess J, CaineSB (2005) Reduced cocaine self-administration in muscarinic M5 acetylcholine receptor-deficient mice. J Neurosci 25:8141-8149. CrossRef Medline
32. ThomsenM, Wörtwein G, Fink-Jensen A, Woldbye DP, Wess J, CaineSB (2007) Decreased prepulse inhibition and increased sensitivity to muscarinic, but not dopaminergic drugs in M5 muscarinic acetylcholine receptor knock-out mice. Psychopharmacology 192:97-110. CrossRef Medline
33. Threlfell S, Clements MA, Khodai T, Pienaar IS, Exley R, Wess J, Cragg SJ (2010) Striatal muscarinic receptors promote activity dependence of dopamine transmission via distinct receptor subtypes on cholinergic interneurons in ventral versus dorsal striatum. J Neurosci 30:3398-3408. CrossRef Medline
34. Valant C, Felder CC, Sexton PM, Christopoulos A (2012) Probe dependence in the allosteric modulation of a G protein-coupled receptor: implications for detection and validation of allosteric ligand effects. Mol Pharmacol 81:41-52. CrossRef Medline
35. Wang H, Ng K, Hayes D, Gao X, Forster G, Blaha C, Yeomans J (2004) Decreased amphetamine-induced locomotion and improved latent inhibition in mice mutant for the M5 muscarinic receptor gene found in the human 15q schizophrenia region. Neuropsychopharmacology 29:2126-2139. CrossRef Medline
36. Weiner DM, Levey AI, Brann MR (1990) Expression of muscarinic acetylcholine and dopamine receptor mRNAs in rat basal ganglia. Proc Natl Acad Sci U S A 87:7050-7054. CrossRef Medline
37. Yamada M, Lamping KG, Duttaroy A, Zhang W, Cui Y, Bymaster FP, McKinzie DL, Felder CC, Deng CX, Faraci FM, Wess J (2001) Cholinergic dilation of cerebral blood vessels is abolished in M(5) muscarinic acetylcholine receptor knockout mice. Proc Natl Acad Sci U S A 98:14096-14101. CrossRef Medline
38. Yasuda RP, Ciesla W, Flores LR, Wall SJ, Li M, Satkus SA, Weisstein JS, Spagnola BV, Wolfe BB (1993) Development of antisera selective for m4 and m5 muscarinic cholinergic receptors: distribution of m4 and m5 receptors in rat brain. Mol Pharmacol 43:149-157. Medline
39. Zhao S, Ting JT, Atallah HE, Qiu L, Tan J, Gloss B, Augustine GJ, Deisseroth K, Luo M, GraybielAM, FengG (2011) Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nat Methods 8:745-752. CrossRef Medline