Nicotinic acetylcholine receptor (nAChR) dependent chorda tympani taste nerve responses to nicotine, ethanol and acetylcholine

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Ren, Zuo Jun ^a   Mummalaneni, Shobha ^a   Qian, Jie ^a   Baumgarten, Clive M ^a   DeSimone, John A ^a   Lyall, Vijay ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ALCOHOL; G PROTEIN COUPLED RECEPTOR; GUSTDUCIN; NICOTINE; NICOTINIC RECEPTOR; PHOSPHOLIPASE C BETA2; PROTEIN T2R ALPHA; TRANSIENT RECEPTOR POTENTIAL CHANNEL M5; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BITTER TASTE; CELL SUBPOPULATION; CHORDA TYMPANI; CONTROLLED STUDY; FEMALE; MOUSE; NERVE STIMULATION; NONHUMAN; PATCH CLAMP TECHNIQUE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; TASTE ACUITY; TASTE BUD; ANIMAL; CALCIUM SIGNALING; DRUG EFFECTS; KNOCKOUT MOUSE; METABOLISM; TASTE;

CHORDA; MUS; RATTUS;

ACETYLCHOLINE; ANIMALS; CALCIUM SIGNALING; CHORDA TYMPANI NERVE; ETHANOL; FEMALE; MICE; MICE, KNOCKOUT; NICOTINE; RATS; RECEPTORS, NICOTINIC; TASTE;

EID: 84932649897     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0127936     Document Type: Article

References (61)

1. Bobo JK. Nicotine dependence and alcoholism epidemiology and treatment. J Psychoactive Drugs. 1992; 24:123-129.
2. Miller NS, Gold MS. Comorbid cigarette and alcohol addiction: epidemiology and treatment. J Addict Dis. 1998; 17:55-66. PMID: 9549603
3. DiFranza JR, Guerrera MP. Alcoholism and smoking. J Stud Alcohol. 1990; 51: 130-135.
4. Grant BF, Hasin DS, Chou SP, Stinson FS, Dawson DA. Nicotine dependence and psychiatric disorders in the United States: results from the national epidemiologic survey on alcohol and related conditions. Arch Gen Psychiatry. 2004; 61:1107-1115. PMID: 15520358
5. Blomqvist O, Engel JA, Nissbrandt H, Söderpalm B. The mesolimbic dopamine-activating properties of ethanol are antagonized by mecamylamine. Eur J Pharmacol. 1993; 249: 207-213. PMID: 8287902
6. Blomqvist O, Ericson M, Engel JA, Söderpalm B. Accumbal dopamine overflow after ethanol: localization of the antagonizing effect of mecamylamine. Eur J Pharmacol. 1997; 334: 149-156. PMID: 9369343
7. Chatterjee S, Steensland P, Simms JA, Holgate J, Coe JW, Hurst RS et al. Partial agonists of the α3β4∗ neuronal nicotinic acetylcholine receptor reduce ethanol consumption and seeking in rats. Neuropsychopharmacology. 2011; 36:603-615. doi: 10.1038/npp.2010.191 PMID: 21048701
8. Hendrickson LM, Zhao-Shea R, Pang X, Gardner PD, Tapper AR. Activation of alpha4∗ nAChRs is necessary and sufficient for varenicline-induced reduction of alcohol consumption. J Neurosci. 2010; 30:10169-10176.
9. Rezvani AH, Slade S, Wells C, Petro A, Lumeng L, Li T-K et al. Effects of sazetidine-A, a selective α4β2 nicotinic acetylcholine receptor desensitizing agent on alcohol and nicotine self-administration in selectively bred alcohol-preferring (P) rats. Psychopharmacology. 2010; 211:161-174. doi: 10.1007/s00213-010-1878-8 PMID: 20535453
10. Bito-Onon JJ, Simms JA, Chatterjee S, Holgate J, Bartlett SE. Varenicline, a partial agonist at neuronal nicotinic acetylcholine receptors, reduces nicotine-induced increases in 20% ethanol operant self-administration in Sprague-Dawley rats. Addict Biol. 2011; 16:440-449. doi: 10.1111/j.1369-1600.2010.00309.x PMID: 21392178
11. Chi H, de Wit H. Mecamylamine attenuates the subjective stimulant-like effects of alcohol in social drinkers. Alcohol Clin Exp Res. 2003; 27:780-786. PMID: 12766622
12. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW. Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev. 2009; 89:73-120. doi: 10.1152/physrev.00015.2008 PMID: 19126755
13. Schiffman SS. Taste quality and neural coding: Implications from psychophysics and neurophysiology. Physiol Behav. 2000; 69:147-159. PMID: 10854926
14. Simons CT, Boucher Y, Carstens MI, Carstens E. Nicotine suppression of gustatory responses of neurons in the nucleus of the solitary tract. J Neurophysiol. 2006; 96:1877-1886.
15. Oliveira-Maia AJ, Stapleton-Kotloski JR, Lyall V, Phan TH, Mummalaneni S, Melone P et al. Nicotine activates TRPM5-dependent and independent taste pathways. Proc Natl Acad Sci USA. 2009; 1065:1596-1601.
16. Bryant B, Xu J, Audige V, Lischka FW, Rawson NE. Cellular basis for the olfactory response to nicotine ACS Chem Neurosci. 2010; 1: 246-256. doi: 10.1021/cn900042c PMID: 22777075
17. Nashmi R, Xiao C, Deshpande P, McKinney S, Grady SR, Whiteaker P et al. Chronic nicotine cell specifically upregulates functional alpha 4∗ nicotinic receptors: basis for both tolerance in midbrain and enhanced long-term potentiation in perforant path. J Neurosci. 2007; 27:8202-8218. PMID: 17670967
18. Li XC, Karadsheh MS, Jenkins PM, Stitzel JA et al. Genetic correlation between the free-choice oral consumption of nicotine and alcohol in C57BL/6J × C3H/HeJ F2 intercross mice. Behav Brain Res. 2005; 157:79-90. PMID: 15617774
19. Söderpalm B, Ericson M, Olausson P, Blomqvist O, Engel JA. Nicotinic mechanisms involved in the dopamine activating and reinforcing properties of ethanol. Behav Brain Res. 2000; 113:85-96. PMID: 10942035
20. Hendrickson LM, Guildford MJ, Tapper AR. Neuronal nicotinic acetylcholine receptors: common molecular substrates of nicotine and alcohol dependence. Frontiers in Psychiatry. 2013; 4 (Article 29):1-16.
21. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D et al. Coding of sweet, bitter, and umami tastes: Different receptor cells sharing similar signaling pathways. Cell. 2003; 112: 293-301.
22. DeSimone JA, Ren Z, Phan TH, Heck GL, Mummalaneni S, Lyall V. Changes in taste receptor cell [Ca2+]i modulate chorda tympani responses to salty and sour taste stimuli. J Neurophysiol. 2012a; 108:3206-3220. doi: 10.1152/jn.00916.2011 PMID: 22956787
23. DeSimone JA, Phan TH, Ren Z, Mummalaneni S, Lyall V. Changes in taste receptor cell [Ca2+]i modulate chorda tympani responses to bitter, sweet, and umami taste stimuli. J Neurophysiol. 2012b; 108:3221-3232. doi: 10.1152/jn.00129.2012 PMID: 22993258
24. Mummalaneni S, Qian J, Phan TH, Rhyu MR, Heck GL, DeSimone JA et al. Effect of ENaC modulators on rat neural responses to NaCl. PLoS One. 2014; 9: e98049. doi: 10.1371/journal.pone.0098049 PMID: 24839965
25. Vinnikova AK, Alam RI, Malik SA, Ereso GL, Feldman GM, McCarty JM et al.Na+-H+ exchange activity in taste receptor cells. J Neurophysiol. 2004; 91:1297-1313.
26. Béhé P, DeSimone JA, Avenet P, Lindemann B. Membrane currents in taste cells of the rat fungiform papilla. Evidence for two types of Ca currents and inhibition of K currents by saccharin. J Gen Physiol. 1990; 96:1061-1084. PMID: 2280253
27. Ren ZJ and Baumgarten CM. Antagonistic regulation of swelling-activated chloride current in rabbit ventricle by Src and EGFR protein tyrosine kinases. American Journal of Physiology: Heart Circulatory Physiology. 2005; 288: H2628-2636. PMID: 15681694
28. Ren ZJ, Raucci FJ Jr, Browe DM, Baumgarten CM. Regulation of swelling-activated Cl-current by angiotensin II signaling and NADPH oxidase in rabbit ventricle. Cardiovasc Res. 2008; 77:73-80. PMID: 18006461
29. Bancroft A, Levin ED. Ventral hippocampal alpha4beta2 nicotinic receptors and chronic nicotine effects on memory. Neuropharmacology. 2000; 39:2770-2778. PMID: 11044746
30. Lyall V, Heck GL, Phan TH, Mummalaneni S, Malik SA, Vinnikova AK et al. Ethanol modulates the VR-1 variant amiloride-insensitive salt taste receptor. II. Effect on chorda tympani salt responses. J Gen Physiol. 2005; 125:587-600. PMID: 15928404
31. Huganir RL, Greengard P. Regulation of neurotransmitter receptor desensitization by protein phosphorylation. Neuron. 1990; 5: 555-567. PMID: 1699566
32. Wang K, Hackett JT, Cox ME, Van Hoek M, Lindstrom JM, Parsons SJ. Regulation of the neuronal nicotinic acetylcholine receptor by SRC family tyrosine kinases. J Biol Chem. 2004; 279: 8779-8786.
33. Pfaffmann C. The sense of taste. In: Handbook of Physiology: Neurophysiology, eds Field J, Magoun HW, Hall VE ( American Physiological Society, Washington, DC); 1959. Vol 1, pp 507-533.
34. Feyerabend C, Higenbottam T, Russell MA. Nicotine concentrations in urine and saliva of smokers and non-smokers. Br Med J Clin Res Ed. 1982; 284:1002-1004. PMID: 6802384
35. Scinska A, Koros E, Habrat B, Kukwa A, Kostowski W, Bienkowski P. Bitter and sweet components of ethanol taste in humans. Drug and Alcohol Dependence. 2000; 60:199-206. PMID: 10940547
36. Blizard DA. Sweet and bitter taste of ethanol in C57BL/6J and DBA2/J mouse strains. Behav Genet. 2007; 37:146-159. PMID: 17096193
37. Ren Z, Rhyu MR, Phan TH, Mummalaneni S, Murthy KS, Grider JR et al. TRPM5-dependent amilorideand benzamil-insensitive NaCl chorda tympani taste nerve response. Am J Physiol Gastrointest Liver Physiol. 2013; 305:G106-G117. doi: 10.1152/ajpgi.00053.2013 PMID: 23639808
38. Damak S, Rong M, Yasumatsu K, Kokrashvili Z, Pérez CA, Shigemura N et al. Trpm5 null mice respond to bitter, sweet, and umami compounds. Chem Senses. 2006; 31:253-264. PMID: 16436689
39. Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N, Ninomiya Y et al. Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature. 2005; 438:1022-1025. PMID: 16355226
40. Talavera K, Yasumatsu K, Yoshida R, Margolskee RF, Voets T, Ninomiya Y et al. The taste transduction channel TRPM5 is a locus for bitter-sweet taste interactions. FASEB J. 2008; 22:1343-1355. PMID: 18070821
41. Gees M, Alpizar YA, Luyten T, Parys JB, Nilius B, Bultynck G et al. Differential effects of bitter compounds on the taste transduction channels TRPM5 and IP3 receptor type 3. Chem Senses. 2014; 39:295-311. doi: 10.1093/chemse/bjt115 PMID: 24452633
42. Lyall V, Phan TH, Mummalaneni S, Mansouri M, Heck GL, Kobal G et al. Effect of nicotine on chorda tympani responses to salty and sour stimuli. J Neurophysiol. 2007; 98:1662-1674. PMID: 17615133
43. Patra M, Salonen E, Terama E, Vattulainen I, Faller R, Lee BW et al. Under the Influence of Alcohol: The Effect of Ethanol and Methanol on Lipid Bilayers. Biophys J. 2006; 90: 1121-1135. PMID: 16326895
44. Ogura T, Margolskee RF, Tallini YN, Shui B, Kotlikoff MI, Lin W. Immuno-localization of vesicular acetylcholine transporter in mouse taste cells and adjacent nerve fibers: Indication of acetylcholine release. Cell Tissue Res. 2007; 330:17-28. PMID: 17704949
45. Stroud RM, McCarthy MP, Shuster M. Nicotinic acetylcholine receptor superfamily of ligand-gated ion channels. Biochemistry. 1990; 29:11009-11023. PMID: 1703009
46. Lyall V, Alam RI, Phan TH, Phan DQ, Heck GL, DeSimone JA. Excitation and adaptation in the detection of hydrogen ions by taste receptor cells: a role for cAMP and Ca2+. J Neurophysiol. 2002; 87:399-408.
47. Nakayama H, Okuda H, Nakashima T. Phosphorylation of rat brain nicotinic acetylcholine receptor by cAMP-dependent protein kinase in vitro. Brain Res Mol Brain Res. 1993; 20:171-177. PMID: 8255179
48. Nuutinen S, Ekokoski E, Lahdensuo E, Tuominen RK. Nicotine-induced upregulation of human neuronal nicotinic alpha7-receptors is potentiated by modulation of cAMP and PKC in SH-EP1-halpha7 cells. Eur J Pharmacol. 2006; 544:21-30. PMID: 16846598
49. Yoon JY, Jung SR, Hille B, Koh DS. Modulation of nicotinic receptor channels by adrenergic stimulation in rat pinealocytes. Am J Physiol Cell Physiol. 2014; 306:C726-C735. doi: 10.1152/ajpcell.00354.2013 PMID: 24553185
50. Di Angelantonio S, Piccioni A, Moriconi C, Trettel F, Cristalli G, Grassi F et al. Adenosine A2A receptor induces protein kinase A-dependent functional modulation of human α3β4 nicotinic receptor. J Physiol. 2011; 589: 2755-2766. doi: 10.1113/jphysiol.2011.207282 PMID: 21486776
51. Lyall V, Phan TH, Mummalaneni S, Melone P, Mahavadi S, Murthy KS et al. Regulation of the benzamil-insensitive salt taste receptor by intracellular Ca2+, protein kinase C, and calcineurin. J Neurophysiol. 2009; 102:1591-1605.
52. Gu Y. Effects of [Ca2+]i and pH on epithelial Na+ channel activity of cultured mouse cortical collecting ducts. J Exp Biol. 2008; 211: 3167-3173. doi: 10.1242/jeb.019646 PMID: 18805816
53. Guo X, Lester RA. Regulation of nicotinic acetylcholine receptor desensitization by Ca2+. J Neurophysiol. 2007; 97:93-101.
54. Korkosz A, Scinska A, Rogowski A, Mierzejewski P, Kostowski W, Kukwa A et al. Chorda tympani nerve transection does not alter operant oral self-administration of ethanol in the rat. Alcohol. 2003; 30:211-215.
55. Rose JE, Sampson A, Levin ED, Henningfield JE. Mecamylamine increases nicotine preference and attenuates nicotine discrimination. Pharmacol Biochem Behav. 1989; 32: 933-938. PMID: 2798542
56. Coleman J, Williams A, Phan TH, Mummalaneni S, Melone P, Ren Z et al. Strain differences in the neural, behavioral, and molecular correlates of sweet and salty taste in naive, ethanol-and sucrose-exposed P and NP rats. J Neurophysiol. 2011; 106:2606-2621. doi: 10.1152/jn.00196.2010 PMID: 21849614
57. Qian J, Mummalaneni S, Lyall V. Neuronal and behavioral responses to nicotine and ethanol in alcohol preferring (P) and alcohol nonpreferring (NP) rats. AChemS 36th Annual Meeting, April 9-12, 2014; p. 76 (Abstract #115).
58. Carstens E, Kuenzler N, Handwerker HO. Activation of neurons in rat trigeminal subnucleus caudalis by different irritant chemicals applied to oral or ocular mucosa. J Neurophysiol. 1998; 80:465-492.
59. Thuerauf N, Markovic K, Braun G, Bleich S, Reulbach U, Kornhuber J et al. The influence of mecamylamine on trigeminal and olfactory chemoreception of nicotine. Neuropsychopharmacology. 2006; 31:450-461.
60. Talavera K, Gees M, Karashima Y, Meseguer VM, Vanoirbeek JA, Damann N et al. Nicotine activates the chemosensory cation channel TRPA1. Nat Neurosci. 2009; 12:1293-1299. doi: 10.1038/nn.2379 PMID: 19749751
61. Faulkner DC, Growcott JW. Effects of neonatal capsaicin administration on the nociceptive response of the rat to mechanical and chemical stimuli. J Pharm Pharmacol. 1980; 32:656-657.