Functional Expression of Human α9* Nicotinic Acetylcholine Receptors in X. laevis Oocytes Is Dependent on the α9 Subunit 5′ UTR

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Filchakova, Olena ^a   McIntosh, J Michael ^a,b,c  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA10; NICOTINIC RECEPTOR ALPHA9; RNA; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FEMALE; GENETIC COMPLEMENTATION; HETEROLOGOUS EXPRESSION; HUMAN; MOSAIC VIRUS; NONHUMAN; OOCYTE; PROTEIN EXPRESSION; RAT; RNA SEQUENCE; XENOPUS LAEVIS;

5' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; DNA PRIMERS; HUMANS; OOCYTES; PATCH-CLAMP TECHNIQUES; RECEPTORS, NICOTINIC; XENOPUS LAEVIS;

EID: 84878092285     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064655     Document Type: Article

References (102)

1. Skok VI, (2002) Nicotinic acetylcholine receptors in autonomic ganglia. Auton Neurosci 97: 1-11.
2. Wang N, Orr-Urtreger A, Korczyn AD, (2002) The role of neuronal nicotinic acetylcholine receptor subunits in autonomic ganglia: lessons from knockout mice. Prog Neurobiol 68: 341-360.
3. Kuffler SW, Yoshikami D, (1975) The number of transmitter molecules in a quantum: an estimate from iontophoretic application of acetylcholine at the neuromuscular synapse. J Physiol 251: 465-482.
4. Kuffler SW, Yoshikami D, (1975) The distribution of acetylcholine sensitivity at the post-synaptic membrane of vertebrate skeletal twitch muscles: iontophoretic mapping in the micron range. J Physiol 244: 703-730.
5. Marchi M, Grilli M, (2010) Presynaptic nicotinic receptors modulating neurotransmitter release in the central nervous system: functional interactions with other coexisting receptors. Prog Neurobiol 92: 105-111.
6. Robinson L, Platt B, Riedel G, (2011) Involvement of the cholinergic system in conditioning and perceptual memory. Behav Brain Res 221: 443-465.
7. Levin ED, (2012) alpha7-Nicotinic receptors and cognition. Curr Drug Targets 13: 602-606.
8. Quik M, McIntosh JM, (2006) Striatal alpha6* nicotinic acetylcholine receptors: potential targets for Parkinson's disease therapy. J Pharmacol Exp Ther 316: 481-489.
9. Parri HR, Hernandez CM, Dineley KT, (2011) Research update: Alpha7 nicotinic acetylcholine receptor mechanisms in Alzheimer's disease. Biochem Pharmacol 82: 931-942.
10. Dani JA, Jenson D, Broussard JI, De Biasi M, (2011) Neurophysiology of Nicotine Addiction. J Addict Res Ther S1.
11. De Biasi M, Dani JA, (2011) Reward, addiction, withdrawal to nicotine. Annu Rev Neurosci 34: 105-130.
12. Leonard S, Gault J, Hopkins J, Logel J, Vianzon R, et al. (2002) Association of promoter variants in the alpha7 nicotinic acetylcholine receptor subunit gene with an inhibitory deficit found in schizophrenia. Arch Gen Psychiatry 59: 1085-1096.
13. Leonard S, Freedman R, (2006) Genetics of chromosome 15q13-q14 in schizophrenia. Biol Psychiatry 60: 115-122.
14. Millar NS, Gotti C, (2009) Diversity of vertebrate nicotinic acetylcholine receptors. Neuropharmacology 56: 237-246.
15. Elgoyhen AB, Johnson DS, Boulter J, Vetter DE, Heinemann S, (1994) Alpha 9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell 79: 705-715.
16. Lips KS, Pfeil U, Kummer W, (2002) Coexpression of alpha 9 and alpha 10 nicotinic acetylcholine receptors in rat dorsal root ganglion neurons. Neuroscience 115: 1-5.
17. Lips KS, Bruggmann D, Pfeil U, Vollerthun R, Grando SA, et al. (2005) Nicotinic acetylcholine receptors in rat and human placenta. Placenta 26: 735-746.
18. Kummer W, Lips KS, Pfeil U, (2008) The epithelial cholinergic system of the airways. Histochem Cell Biol 130: 219-234.
19. Colomer C, Olivos-Ore LA, Vincent A, McIntosh JM, Artalejo AR, et al. (2010) Functional characterization of alpha9-containing cholinergic nicotinic receptors in the rat adrenal medulla: implication in stress-induced functional plasticity. J Neurosci 30: 6732-6742.
20. Verbitsky M, Rothlin CV, Katz E, Elgoyhen AB, (2000) Mixed nicotinic-muscarinic properties of the alpha9 nicotinic cholinergic receptor. Neuropharmacology 39: 2515-2524.
21. Sgard F, Charpantier E, Bertrand S, Walker N, Caput D, et al. (2002) A novel human nicotinic receptor subunit, alpha10, that confers functionality to the alpha9-subunit. Mol Pharmacol 61: 150-159.
22. Vincler M, (2005) Neuronal nicotinic receptors as targets for novel analgesics. Expert Opin Investig Drugs 14: 1191-1198.
23. Vincler M, Wittenauer S, Parker R, Ellison M, Olivera BM, et al. (2006) Molecular mechanism for analgesia involving specific antagonism of alpha9alpha10 nicotinic acetylcholine receptors. Proc Natl Acad Sci U S A 103: 17880-17884.
24. Vincler M, McIntosh JM, (2007) Targeting the alpha9alpha10 nicotinic acetylcholine receptor to treat severe pain. Expert Opin Ther Targets 11: 891-897.
25. McIntosh JM, Absalom N, Chebib M, Elgoyhen AB, Vincler M, (2009) Alpha9 nicotinic acetylcholine receptors and the treatment of pain. Biochem Pharmacol 78: 693-702.
26. Holtman JR, Dwoskin LP, Dowell C, Wala EP, Zhang Z, et al. (2011) The novel small molecule alpha9alpha10 nicotinic acetylcholine receptor antagonist ZZ-204G is analgesic. Eur J Pharmacol 670: 500-508.
27. Wala EP, Crooks PA, McIntosh JM, Holtman JR Jr, (2012) Novel Small Molecule alpha9alpha10 Nicotinic Receptor Antagonist Prevents and Reverses Chemotherapy-Evoked Neuropathic Pain in Rats. Anesth Analg 115: 713-720.
28. Nguyen VT, Ndoye A, Grando SA, (2000) Novel human alpha9 acetylcholine receptor regulating keratinocyte adhesion is targeted by Pemphigus vulgaris autoimmunity. Am J Pathol 157: 1377-1391.
29. Vetter DE, Liberman MC, Mann J, Barhanin J, Boulter J, et al. (1999) Role of alpha9 nicotinic ACh receptor subunits in the development and function of cochlear efferent innervation. Neuron 23: 93-103.
30. Maison SF, Luebke AE, Liberman MC, Zuo J, (2002) Efferent protection from acoustic injury is mediated via alpha9 nicotinic acetylcholine receptors on outer hair cells. J Neurosci 22: 10838-10846.
31. Elgoyhen AB, Vetter DE, Katz E, Rothlin CV, Heinemann SF, et al. (2001) alpha10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Proc Natl Acad Sci U S A 98: 3501-3506.
32. Lustig LR, Peng H, Hiel H, Yamamoto T, Fuchs PA, (2001) Molecular cloning and mapping of the human nicotinic acetylcholine receptor alpha10 (CHRNA10). Genomics 73: 272-283.
33. Gopalakrishnan M, Monteggia LM, Anderson DJ, Molinari EJ, Piattoni-Kaplan M, et al. (1996) Stable expression, pharmacologic properties and regulation of the human neuronal nicotinic acetylcholine alpha 4 beta 2 receptor. J Pharmacol Exp Ther 276: 289-297.
34. Eaton JB, Peng JH, Schroeder KM, George AA, Fryer JD, et al. (2003) Characterization of human alpha 4 beta 2-nicotinic acetylcholine receptors stably and heterologously expressed in native nicotinic receptor-null SH-EP1 human epithelial cells. Mol Pharmacol 64: 1283-1294.
35. Deneris ES, Connolly J, Boulter J, Wada E, Wada K, et al. (1988) Primary structure and expression of beta 2: a novel subunit of neuronal nicotinic acetylcholine receptors. Neuron 1: 45-54.
36. Couturier S, Bertrand D, Matter JM, Hernandez MC, Bertrand S, et al. (1990) A neuronal nicotinic acetylcholine receptor subunit (alpha 7) is developmentally regulated and forms a homo-oligomeric channel blocked by alpha-BTX. Neuron 5: 847-856.
37. Gotti C, Hanke W, Maury K, Moretti M, Ballivet M, et al. (1994) Pharmacology and biophysical properties of alpha 7 and alpha 7-alpha 8 alpha-bungarotoxin receptor subtypes immunopurified from the chick optic lobe. Eur J Neurosci 6: 1281-1291.
38. van Kleef RG, Vijverberg HP, Westerink RH, (2008) Selective inhibition of human heteromeric alpha9alpha10 nicotinic acetylcholine receptors at a low agonist concentration by low concentrations of ototoxic organic solvents. Toxicol In Vitro 22: 1568-1572.
39. Halai R, Clark RJ, Nevin ST, Jensen JE, Adams DJ, et al. (2009) Scanning mutagenesis of alpha-conotoxin Vc1.1 reveals residues crucial for activity at the alpha9alpha10 nicotinic acetylcholine receptor. J Biol Chem 284: 20275-20284.
40. Lansdell SJ, Gee VJ, Harkness PC, Doward AI, Baker ER, et al. (2005) RIC-3 enhances functional expression of multiple nicotinic acetylcholine receptor subtypes in mammalian cells. Mol Pharmacol 68: 1431-1438.
41. Fucile S, Sucapane A, Eusebi F, (2006) Ca2+ permeability through rat cloned alpha9-containing nicotinic acetylcholine receptors. Cell Calcium 39: 349-355.
42. Gray NK, Hentze MW, (1994) Regulation of protein synthesis by mRNA structure. Mol Biol Rep 19: 195-200.
43. Jacobs E, Mills JD, Janitz M, (2012) The role of RNA structure in posttranscriptional regulation of gene expression. J Genet Genomics 39: 535-543.
44. Kozak M, (2005) Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 361: 13-37.
45. Nomura M, Ohsuye K, Mizuno A, Sakuragawa Y, Tanaka S, (1984) Influence of messenger RNA secondary structure on translation efficiency. Nucleic Acids Symp Ser pp. 173-176.
46. Kozak M, (1990) Downstream secondary structure facilitates recognition of initiator codons by eukaryotic ribosomes. Proc Natl Acad Sci U S A 87: 8301-8305.
47. Pesole G, Grillo G, Larizza A, Liuni S, (2000) The untranslated regions of eukaryotic mRNAs: structure, function, evolution and bioinformatic tools for their analysis. Brief Bioinform 1: 236-249.
48. Araujo PR, Yoon K, Ko D, Smith AD, Qiao M, et al. (2012) Before It Gets Started: Regulating Translation at the 5′ UTR. Comp Funct Genomics 2012: 475731.
49. Wilkie GS, Dickson KS, Gray NK, (2003) Regulation of mRNA translation by 5′- and 3′-UTR-binding factors. Trends Biochem Sci 28: 182-188.
50. Falcone D, Andrews DW, (1991) Both the 5′ untranslated region and the sequences surrounding the start site contribute to efficient initiation of translation in vitro. Mol Cell Biol 11: 2656-2664.
51. Liman ER, Tytgat J, Hess P, (1992) Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs. Neuron 9: 861-871.
52. Kruys V, Wathelet M, Poupart P, Contreras R, Fiers W, et al. (1987) The 3′ untranslated region of the human interferon-beta mRNA has an inhibitory effect on translation. Proc Natl Acad Sci U S A 84: 6030-6034.
53. Cartier GE, Yoshikami D, Gray WR, Luo S, Olivera BM, et al. (1996) A new alpha-conotoxin which targets alpha3beta2 nicotinic acetylcholine receptors. J Biol Chem 271: 7522-7528.
54. Kariko K, Kuo A, Barnathan E, (1999) Overexpression of urokinase receptor in mammalian cells following administration of the in vitro transcribed encoding mRNA. Gene Ther 6: 1092-1100.
55. Fan Q, Treder K, Miller WA, (2012) Untranslated regions of diverse plant viral RNAs vary greatly in translation enhancement efficiency. BMC Biotechnol 12: 22.
56. Gallie DR, Sleat DE, Watts JW, Turner PC, Wilson TM, (1987) The 5′-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo. Nucleic Acids Res 15: 3257-3273.
57. Gallie DR, Walbot V, (1992) Identification of the motifs within the tobacco mosaic virus 5′-leader responsible for enhancing translation. Nucleic Acids Res 20: 4631-4638.
58. Gallie DR, Sleat DE, Watts JW, Turner PC, Wilson TM, (1987) A comparison of eukaryotic viral 5′-leader sequences as enhancers of mRNA expression in vivo. Nucleic Acids Res 15: 8693-8711.
59. Jobling SA, Gehrke L, (1987) Enhanced translation of chimaeric messenger RNAs containing a plant viral untranslated leader sequence. Nature 325: 622-625.
60. Sleat DE, Gallie DR, Jefferson RA, Bevan MW, Turner PC, et al. (1987) Characterisation of the 5′-leader sequence of tobacco mosaic virus RNA as a general enhancer of translation in vitro. Gene 60: 217-225.
61. Sumikawa K, Houghton M, Emtage JS, Richards BM, Barnard EA, (1981) Active multi-subunit ACh receptor assembled by translation of heterologous mRNA in Xenopus oocytes. Nature 292: 862-864.
62. Barnard EA, Miledi R, Sumikawa K, (1982) Translation of exogenous messenger RNA coding for nicotinic acetylcholine receptors produces functional receptors in Xenopus oocytes. Proc R Soc Lond B Biol Sci 215: 241-246.
63. Papke RL, Boulter J, Patrick J, Heinemann S, (1989) Single-channel currents of rat neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes. Neuron 3: 589-596.
64. Duvoisin RM, Deneris ES, Patrick J, Heinemann S, (1989) The functional diversity of the neuronal nicotinic acetylcholine receptors is increased by a novel subunit: beta 4. Neuron 3: 487-496.
65. Kuryatov A, Olale F, Cooper J, Choi C, Lindstrom J, (2000) Human alpha6 AChR subtypes: subunit composition, assembly, and pharmacological responses. Neuropharmacology 39: 2570-2590.
66. Kozak M, (1986) Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44: 283-292.
67. Soreq H, Ben-Aziz R, Prody CA, Seidman S, Gnatt A, et al. (1990) Molecular cloning and construction of the coding region for human acetylcholinesterase reveals a G + C-rich attenuating structure. Proc Natl Acad Sci U S A 87: 9688-9692.
68. Morel N, Massoulie J, (2000) Comparative expression of homologous proteins. A novel mode of transcriptional regulation by the coding sequence folding compatibility of chimeras. J Biol Chem 275: 7304-7312.
69. Lammich S, Schobel S, Zimmer AK, Lichtenthaler SF, Haass C, (2004) Expression of the Alzheimer protease BACE1 is suppressed via its 5′-untranslated region. EMBO Rep 5: 620-625.
70. Niesler B, Flohr T, Nothen MM, Fischer C, Rietschel M, et al. (2001) Association between the 5′ UTR variant C178T of the serotonin receptor gene HTR3A and bipolar affective disorder. Pharmacogenetics 11: 471-475.
71. Mihailovich M, Thermann R, Grohovaz F, Hentze MW, Zacchetti D, (2007) Complex translational regulation of BACE1 involves upstream AUGs and stimulatory elements within the 5′ untranslated region. Nucleic Acids Res 35: 2975-2985.
72. Venkatachalan SP, Bushman JD, Mercado JL, Sancar F, Christopherson KR, et al. (2007) Optimized expression vector for ion channel studies in Xenopus oocytes and mammalian cells using alfalfa mosaic virus. Pflugers Arch 454: 155-163.
73. Gallie DR, (2002) The 5′-leader of tobacco mosaic virus promotes translation through enhanced recruitment of eIF4F. Nucleic Acids Res 30: 3401-3411.
74. Brederode FT, Koper-Zwarthoff EC, Bol JF, (1980) Complete nucleotide sequence of alfalfa mosaic virus RNA 4. Nucleic Acids Res 8: 2213-2223.
75. Gehrke L, Auron PE, Quigley GJ, Rich A, Sonenberg N, (1983) 5′-Conformation of capped alfalfa mosaic virus ribonucleic acid 4 may reflect its independence of the cap structure or of cap-binding protein for efficient translation. Biochemistry 22: 5157-5164.
76. Chatterjee S, Pal JK, (2009) Role of 5′- and 3′-untranslated regions of mRNAs in human diseases. Biol Cell 101: 251-262.
77. Hudder A, Werner R, (2000) Analysis of a Charcot-Marie-Tooth disease mutation reveals an essential internal ribosome entry site element in the connexin-32 gene. J Biol Chem 275: 34586-34591.
78. Brown CY, Mize GJ, Pineda M, George DL, Morris DR, (1999) Role of two upstream open reading frames in the translational control of oncogene mdm2. Oncogene 18: 5631-5637.
79. Jin X, Turcott E, Englehardt S, Mize GJ, Morris DR, (2003) The two upstream open reading frames of oncogene mdm2 have different translational regulatory properties. J Biol Chem 278: 25716-25721.
80. Morris DR, Geballe AP, (2000) Upstream open reading frames as regulators of mRNA translation. Mol Cell Biol 20: 8635-8642.
81. Soreq H, Nudel U, Salomon R, Revel M, Littauer UZ, (1974) In vitro translation of polyadenylic acid-free rabbit globin messenger RNA. J Mol Biol 88: 233-245.
82. Huez G, Marbaix G, Hubert E, Leclercq M, Nudel U, et al. (1974) Role of the polyadenylate segment in the translation of globin messenger RNA in Xenopus oocytes. Proc Natl Acad Sci U S A 71: 3143-3146.
83. Pascale A, Govoni S, (2012) The complex world of post-transcriptional mechanisms: is their deregulation a common link for diseases? Focus on ELAV-like RNA-binding proteins. Cell Mol Life Sci 69: 501-517.
84. Alexander JK, Govind AP, Drisdel RC, Blanton MP, Vallejo Y, et al. (2010) Palmitoylation of nicotinic acetylcholine receptors. J Mol Neurosci 40: 12-20.
85. Swope SL, Moss SJ, Raymond LA, Huganir RL, (1999) Regulation of ligand-gated ion channels by protein phosphorylation. Adv Second Messenger Phosphoprotein Res 33: 49-78.
86. daCosta CJ, Kaiser DE, Baenziger JE, (2005) Role of glycosylation and membrane environment in nicotinic acetylcholine receptor stability. Biophys J 88: 1755-1764.
87. Nishizaki T, (2003) N-glycosylation sites on the nicotinic ACh receptor subunits regulate receptor channel desensitization and conductance. Brain Res Mol Brain Res 114: 172-176.
88. Chang W, Gelman MS, Prives JM, (1997) Calnexin-dependent enhancement of nicotinic acetylcholine receptor assembly and surface expression. J Biol Chem 272: 28925-28932.
89. Wanamaker CP, Green WN, (2007) Endoplasmic reticulum chaperones stabilize nicotinic receptor subunits and regulate receptor assembly. J Biol Chem 282: 31113-31123.
90. Srinivasan R, Pantoja R, Moss FJ, Mackey ED, Son CD, et al. (2011) Nicotine up-regulates alpha4beta2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning. J Gen Physiol 137: 59-79.
91. Lester HA, Xiao C, Srinivasan R, Son CD, Miwa J, et al. (2009) Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery. AAPS J 11: 167-177.
92. Kuryatov A, Luo J, Cooper J, Lindstrom J, (2005) Nicotine acts as a pharmacological chaperone to up-regulate human alpha4beta2 acetylcholine receptors. Mol Pharmacol 68: 1839-1851.
93. Valles AS, Barrantes FJ, (2012) Chaperoning alpha7 neuronal nicotinic acetylcholine receptors. Biochim Biophys Acta 1818: 718-729.
94. Valles AS, Roccamo AM, Barrantes FJ, (2009) Ric-3 chaperone-mediated stable cell-surface expression of the neuronal alpha7 nicotinic acetylcholine receptor in mammalian cells. Acta Pharmacol Sin 30: 818-827.
95. Williams ME, Burton B, Urrutia A, Shcherbatko A, Chavez-Noriega LE, et al. (2005) Ric-3 promotes functional expression of the nicotinic acetylcholine receptor alpha7 subunit in mammalian cells. J Biol Chem 280: 1257-1263.
96. Roncarati R, Seredenina T, Jow B, Jow F, Papini S, et al. (2008) Functional properties of alpha7 nicotinic acetylcholine receptors co-expressed with RIC-3 in a stable recombinant CHO-K1 cell line. Assay Drug Dev Technol 6: 181-193.
97. Cheng A, McDonald NA, Connolly CN, (2005) Cell surface expression of 5-hydroxytryptamine type 3 receptors is promoted by RIC-3. J Biol Chem 280: 22502-22507.
98. Nie L, Song H, Chen MF, Chiamvimonvat N, Beisel KW, et al. (2004) Cloning and expression of a small-conductance Ca(2+)-activated K+ channel from the mouse cochlea: coexpression with alpha9/alpha10 acetylcholine receptors. J Neurophysiol 91: 1536-1544.
99. Baker ER, Zwart R, Sher E, Millar NS, (2004) Pharmacological properties of alpha 9 alpha 10 nicotinic acetylcholine receptors revealed by heterologous expression of subunit chimeras. Mol Pharmacol 65: 453-460.
100. Osman AA, Schrader AD, Hawkes AJ, Akil O, Bergeron A, et al. (2008) Muscle-like nicotinic receptor accessory molecules in sensory hair cells of the inner ear. Mol Cell Neurosci 38: 153-169.
101. Flores CM, Rogers SW, Pabreza LA, Wolfe BB, Kellar KJ, (1992) A subtype of nicotinic cholinergic receptor in rat brain is composed of alpha 4 and beta 2 subunits and is up-regulated by chronic nicotine treatment. Mol Pharmacol 41: 31-37.
102. Lee CH, Huang CS, Chen CS, Tu SH, Wang YJ, et al. (2010) Overexpression and activation of the alpha9-nicotinic receptor during tumorigenesis in human breast epithelial cells. J Natl Cancer Inst 102: 1322-1335.