Mice expressing the ADNFLE valine 287 leucine mutation of the Β2 nicotinic acetylcholine receptor subunit display increased sensitivity to acute nicotine administration and altered presynaptic nicotinic receptor function

Pharmacology Biochemistry and Behavior

Volumn 103, Issue 3, 2013, Pages 603-621

  O'Neill, Heidi C ^a   Laverty, Duncan C ^a   Patzlaff, Natalie E ^a   Cohen, Bruce N ^b   Fonck, Carlos ^b   McKinney, Sheri ^b   McIntosh, J Michael ^c   Lindstrom, Jon M ^d   Lester, Henry A ^b   Grady, Sharon R ^a   Marks, Michael J ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

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

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Autoradiography; Autosomal dominant nocturnal frontal lobe epilepsy; Knock in mouse; Nicotine; Nicotinic acetylcholine receptor; Synaptosomes

Indexed keywords

4 AMINOBUTYRIC ACID; DOPAMINE; LEUCINE; NICOTINE; NICOTINIC RECEPTOR BETA2; PRESYNAPTIC RECEPTOR; RUBIDIUM 86; TRITIUM; VALINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; AUTOSOMAL DOMINANT DISORDER; AUTOSOMAL DOMINANT NOCTURNAL FRONTAL LOBE EPILEPSY; BRAIN CORTEX; CONTROLLED STUDY; DOPAMINE RELEASE; DOSE RESPONSE; DRUG SENSITIVITY; DYSTONIA; ELECTROENCEPHALOGRAPHY; FRONTAL LOBE EPILEPSY; GENE EXPRESSION; GENE MUTATION; HIPPOCAMPUS; HYPOTHERMIA; LIGAND BINDING; LOCOMOTION; MALE; MISSENSE MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SYNAPTOSOME; TONIC CLONIC SEIZURE;

ACETYLCHOLINE; ANIMALS; BODY TEMPERATURE; CENTRAL NERVOUS SYSTEM SENSITIZATION; CEREBRAL CORTEX; DOPAMINE; DYSTONIA; GAMMA-AMINOBUTYRIC ACID; GENE KNOCK-IN TECHNIQUES; HIPPOCAMPUS; MALE; MICE; MOTOR ACTIVITY; MUTATION, MISSENSE; NICOTINE; PRESYNAPTIC TERMINALS; RADIOLIGAND ASSAY; RECEPTORS, NICOTINIC; RUBIDIUM RADIOISOTOPES; SEIZURES; SYNAPTOSOMES;

MUS;

EID: 84869139440     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2012.10.014     Document Type: Article

References (80)

1. P. Aridon, C. Marini, C. Di Resta, E. Brilli, M. De Fusco, and F. Politi Increased sensitivity of the neuronal nicotinic receptor alpha 2 subunit causes familial epilepsy with nocturnal wandering and ictal fear Am J Hum Genet 79 2006 342 350 (Pubitemid 44141832)
2. 3H]dopamine release from rat striatal synaptosomes J Pharmacol Exp Ther 312 2005 231 237 (Pubitemid 40096473)
3. C.G. Baddick, and M.J. Marks An autoradiographic survey of mouse brain nicotinic acetylcholine receptors defined by null mutants Biochem Pharmacol 82 2011 828 841
4. D. Bertrand, F. Picard, S. Le Hellard, S. Weiland, I. Favre, and H. Phillips How mutations in the nAChRs can cause ADNFLE epilepsy Epilepsia 43 Suppl. 5 2002 112 122 (Pubitemid 34864217)
5. D. Bertrand, F. Elmslie, E. Hughes, J. Trounce, T. Sander, and S. Bertrand The CHRNB2 mutation I312M is associated with epilepsy and distinct memory deficits Neurobiol Dis 20 2005 799 804 (Pubitemid 41619355)
6. A.L. Carbone, M. Moroni, P.J. Groot-Kormelink, and I. Bermudez Pentameric concatenated (alpha4)(2)(beta2)(3) and (alpha4)(3)(beta2)(2) nicotinic acetylcholine receptors: subunit arrangement determines functional expression Br J Pharmacol 156 2009 970 981
7. G.E. Cartier, D. Yoshikami, W.R. Gray, S. Luo, B.M. Olivera, and J.M. McIntosh A new alpha-conotoxin which targets alpha3beta2 nicotinic acetylcholine receptors J Biol Chem 271 1996 7522 7528 (Pubitemid 26107027)
8. N. Champtiaux, Z.Y. Han, A. Bessis, F.M. Rossi, M. Zoli, and L. Marubio Distribution and pharmacology of alpha 6-containing nicotinic acetylcholine receptors analyzed with mutant mice J Neurosci 22 2002 1208 1217 (Pubitemid 34163722)
9. N. Champtiaux, C. Gotti, M. Cordero-Erausquin, D.J. David, C. Przybylski, and C. Lena Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice J Neurosci 23 2003 7820 7829 (Pubitemid 37055453)
10. A.C. Collins, C.B. Evans, L.L. Miner, and M.J. Marks Mecamylamine blockade of nicotine responses: evidence for two brain nicotinic receptors Pharmacol Biochem Behav 24 1986 1767 1773 (Pubitemid 16066647)
11. R. Combi, L. Dalpra, M.L. Tenchini, and L. Ferini-Strambi Autosomal dominant nocturnal frontal lobe epilepsy - a critical overview J Neurol 251 2004 923 934 (Pubitemid 39119310)
12. M. De Fusco, A. Becchetti, A. Patrignani, G. Annesi, A. Gambardella, and A. Quattrone The nicotinic receptor beta 2 subunit is mutant in nocturnal frontal lobe epilepsy Nat Genet 26 2000 275 276
13. R.M. Drenan, S.R. Grady, P. Whiteaker, T. McClure-Begley, S. McKinney, and J.M. Miwa In vivo activation of midbrain dopamine neurons via sensitized, high-affinity alpha 6 nicotinic acetylcholine receptors Neuron 60 2008 123 136
14. C. Fonck, R. Nashmi, P. Deshpande, M.I. Damaj, M.J. Marks, and A. Riedel Increased sensitivity to agonist-induced seizures, straub tail, and hippocampal theta rhythm in knock-in mice carrying hypersensitive alpha 4 nicotinic receptors J Neurosci 23 2003 2582 2590 (Pubitemid 36418592)
15. C. Fonck, B.N. Cohen, R. Nashmi, P. Whiteaker, D.A. Wagenaar, and N. Rodrigues-Pinguet Novel seizure phenotype and sleep disruptions in knock-in mice with hypersensitive alpha 4* nicotinic receptors J Neurosci 25 2005 11396 11411 (Pubitemid 43083712)
16. B.J. Franklin Keith, and G. Paxinos The mouse brain in stereotaxic coordinates 1997 Acamdemic Press San Diego
17. C.L. Gentry, and R.J. Lukas Regulation of nicotinic acetylcholine receptor numbers and function by chronic nicotine exposure Curr Drug Targets CNS Neurol Disord 1 2002 359 385
18. C. Gotti, M. Moretti, F. Clementi, L. Riganti, J.M. McIntosh, and A.C. Collins Expression of nigrostriatal alpha 6-containing nicotinic acetylcholine receptors is selectively reduced, but not eliminated, by beta 3 subunit gene deletion Mol Pharmacol 67 2005 2007 2015 (Pubitemid 41007782)
19. C. Gotti, M. Moretti, N.M. Meinerz, F. Clementi, A. Gaimarri, and A.C. Collins Partial deletion of the nicotinic cholinergic receptor alpha 4 or beta 2 subunit genes changes the acetylcholine sensitivity of receptor-mediated 86Rb + efflux in cortex and thalamus and alters relative expression of alpha 4 and beta 2 subunits Mol Pharmacol 73 2008 1796 1807 (Pubitemid 351724367)
20. 3H]dopamine release from synaptosomes prepared from mouse striatum J Neurochem 59 1992 848 856
21. S.R. Grady, O. Salminen, D.C. Laverty, P. Whiteaker, J.M. McIntosh, and A.C. Collins The subtypes of nicotinic acetylcholine receptors on dopaminergic terminals of mouse striatum Biochem Pharmacol 74 2007 1235 1246 (Pubitemid 47417935)
22. S. Hirose, H. Iwata, H. Akiyoshi, K. Kobayashi, M. Ito, and K. Wada A novel mutation of CHRNA4 responsible for autosomal dominant nocturnal frontal lobe epilepsy Neurology 53 1999 1749 1753 (Pubitemid 29530350)
23. J.C. Hoda, W. Gu, M. Friedli, H.A. Phillips, S. Bertrand, and S.E. Antonarakis Human nocturnal frontal lobe epilepsy: pharmocogenomic profiles of pathogenic nicotinic acetylcholine receptor beta-subunit mutations outside the ion channel pore Mol Pharmacol 74 2008 379 391
24. B.C. Jobst, and P.D. Williamson Frontal lobe seizures Psychiatr Clin North Am 28 3 2005 635 651 (Pubitemid 41191138)
25. B. Katz, and S. Thesleff A study of the desensitization produced by acetylcholine at the motor end-plate J Physiol 138 1957 63 80
26. A. Klaassen, J. Glykys, J. Maguire, C. Labarca, I. Mody, and J. Boulter Seizures and enhanced cortical GABAergic inhibition in two mouse models of human autosomal dominant nocturnal frontal lobe epilepsy Proc Natl Acad Sci U S A 103 2006 19152 19157 (Pubitemid 350002842)
27. A. Kuryatov, W. Berrettini, and J. Lindstrom Acetylcholine receptor (AChR) alpha5 subunit variant associated with risk for nicotine dependence and lung cancer reduces (alpha4beta2)alpha5 AChR function Mol Pharmacol 79 2011 119 125
28. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J Biol Chem 193 1951 265 275
29. Y. Lu, S. Grady, M.J. Marks, M. Picciotto, J.P. Changeux, and A.C. Collins Pharmacological characterization of nicotinic receptor-stimulated GABA release from mouse brain synaptosomes J Pharmacol Exp Ther 287 1998 648 657 (Pubitemid 29133665)
30. I. Manfredi, A.D. Zani, L. Rampoldi, S. Pegorini, I. Bernascone, and M. Moretti Expression of mutant beta2 nicotinic receptors during development is crucial for epileptogenesis Hum Mol Genet 18 2009 1075 1088
31. E.O. Mann, and I. Mody The multifaceted role of inhibition in epilepsy: seizure-genesis through excessive GABAergic inhibition in autosomal dominant nocturnal frontal lobe epilepsy Curr Opin Neurol 21 2008 155 160 (Pubitemid 351644156)
32. M.J. Marks, E. Romm, S.M. Bealer, and A.C. Collins A test battery for measuring nicotine effects in mice Pharmacol Biochem Behav 23 1985 325 330 (Pubitemid 16216461)
33. M.J. Marks, J.R. Pauly, S.D. Gross, E.S. Deneris, I. Hermans-Borgmeyer, and S.F. Heinemann Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment J Neurosci 12 1992 2765 2784
34. M.J. Marks, S.F. Robinson, and A.C. Collins Nicotinic agonists differ in activation and desensitization of 86Rb + efflux from mouse thalamic synaptosomes J Pharmacol Exp Ther 277 1996 1383 1396
35. M.J. Marks, P. Whiteaker, J. Calcaterra, J.A. Stitzel, A.E. Bullock, and S.R. Grady Two pharmacologically distinct components of nicotinic receptor-mediated rubidium efflux in mouse brain require the beta2 subunit J Pharmacol Exp Ther 289 1999 1090 1103 (Pubitemid 29191271)
36. M.J. Marks, J.A. Stitzel, S.R. Grady, M.R. Picciotto, J.P. Changeux, and A.C. Collins Nicotinic-agonist stimulated (86)Rb(+) efflux and [(3)H]epibatidine binding of mice differing in beta2 genotype Neuropharmacology 39 2000 2632 2645
37. 3H]epibatidine binding sites and components of biphasic 86Rb + efflux with high and low sensitivity to stimulation by acetylcholine Neuropharmacology 53 2007 390 405 (Pubitemid 47225090)
38. 86Rb + efflux mediated by alpha4beta2*-nicotinic acetylcholine receptors with high and low-sensitivity to stimulation by acetylcholine display similar agonist-induced desensitization Biochem Pharmacol 80 2010 1238 1251
39. L.M. Marubio, M. del Mar Arroyo-Jimenez, M. Cordero-Erausquin, C. Lena, N. Le Novere, and A. de Kerchove d'Exaerde Reduced antinociception in mice lacking neuronal nicotinic receptor subunits Nature 398 1999 805 810
40. S.E. McCallum, A.C. Collins, R. Paylor, and M.J. Marks Deletion of the beta 2 nicotinic acetylcholine receptor subunit alters development of tolerance to nicotine and eliminates receptor upregulation Psychopharmacology (Berl) 184 2006 314 327 (Pubitemid 43255848)
41. 3H]GABA release from mouse brain synaptosomes is modulated by alpha4beta2 and alpha4alpha5beta2 nicotinic receptor subtypes Mol Pharmacol 75 2009 918 926
42. E.L. Meyer, D. Yoshikami, and J.M. McIntosh The neuronal nicotinic acetylcholine receptors alpha 4* and alpha 6* differentially modulate dopamine release in mouse striatal slices J Neurochem 105 2008 1761 1769 (Pubitemid 351678494)
43. M. Moroni, R. Zwart, E. Sher, B.K. Cassels, and I. Bermudez alpha4beta2 nicotinic receptors with high and low acetylcholine sensitivity: pharmacology, stoichiometry, and sensitivity to long-term exposure to nicotine Mol Pharmacol 70 2006 755 768 (Pubitemid 44092336)
44. M.E. Nelson, A. Kuryatov, C.H. Choi, Y. Zhou, and J. Lindstrom Alternate stoichiometries of alpha4beta2 nicotinic acetylcholine receptors Mol Pharmacol 63 2003 332 341 (Pubitemid 36158368)
45. A. Oldani, M. Zucconi, R. Asselta, M. Modugno, M.T. Bonati, and L. Dalpra Autosomal dominant nocturnal frontal lobe epilepsy. A video-polysomnographic and genetic appraisal of 40 patients and delineation of the epileptic syndrome Brain 121 Pt 2 1998 205 223 (Pubitemid 28075798)
46. H.A. Phillips, I.E. Scheffer, S.F. Berkovic, G.E. Hollway, G.R. Sutherland, and J.C. Mulley Localization of a gene for autosomal dominant nocturnal frontal lobe epilepsy to chromosome 20q 13.2 Nat Genet 10 1995 117 118
47. H.A. Phillips, I. Favre, M. Kirkpatrick, S.M. Zuberi, D. Goudie, and S.E. Heron CHRNB2 is the second acetylcholine receptor subunit associated with autosomal dominant nocturnal frontal lobe epilepsy Am J Hum Genet 68 2001 225 231 (Pubitemid 32048378)
48. M.R. Picciotto, M. Zoli, C. Lena, A. Bessis, Y. Lallemand, and N. Le Novere Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain Nature 374 1995 65 67
49. M.R. Picciotto, M. Zoli, R. Rimondini, C. Lena, L.M. Marubio, and E.M. Pich Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine Nature 391 1998 173 177 (Pubitemid 28092475)
50. M.W. Quick, and R.A. Lester Desensitization of neuronal nicotinic receptors J Neurobiol 53 2002 457 478 (Pubitemid 35375579)
51. M. Quik, X.A. Perez, and S.R. Grady Role of alpha6 nicotinic receptors in CNS dopaminergic function: relevance to addiction and neurological disorders Biochem Pharmacol 82 8 2011 873 882
52. N. Rodrigues-Pinguet, L. Jia, M. Li, A. Figl, A. Klaassen, and A. Truong Five ADNFLE mutations reduce the Ca2 + dependence of the mammalian alpha4beta2 acetylcholine response J Physiol 550 2003 11 26 (Pubitemid 36869266)
53. E.M. Rouiller, V. Moret, and F. Liang Comparison of the connectional properties of the two forelimb areas of the rat sensorimotor cortex: support for the presence of a premotor or supplementary motor cortical area Somatosens Mot Res 10 1993 269 289 (Pubitemid 23285319)
54. A. Rozycka, and W.H. Trzeciak Genetic basis of autosomal dominant nocturnal frontal lobe epilepsy J Appl Genet 44 2003 197 207 (Pubitemid 37123435)
55. O. Salminen, K.L. Murphy, J.M. McIntosh, J. Drago, M.J. Marks, and A.C. Collins Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice Mol Pharmacol 65 2004 1526 1535 (Pubitemid 38668310)
56. O. Salminen, J.A. Drapeau, J.M. McIntosh, A.C. Collins, M.J. Marks, and S.R. Grady Pharmacology of alpha-conotoxin MII-sensitive subtypes of nicotinic acetylcholine receptors isolated by breeding of null mutant mice Mol Pharmacol 71 2007 1563 1571 (Pubitemid 47010909)
57. I.E. Scheffer, K.P. Bhatia, I. Lopes-Cendes, D.R. Fish, C.D. Marsden, and E. Andermann Autosomal dominant nocturnal frontal lobe epilepsy. A distinctive clinical disorder Brain 118 Pt 1 1995 61 73
58. C.D. Son, F.J. Moss, B.N. Cohen, and H.A. Lester Nicotine normalizes intracellular subunit stoichiometry of nicotinic receptors carrying mutations linked to autosomal dominant nocturnal frontal lobe epilepsy Mol Pharmacol 75 2009 1137 1148
59. R. Srinivasan, R. Pantoja, F.J. Moss, E.D. Mackey, C.D. Son, and J. Miwa Nicotine up-regulates alpha4beta2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning J Gen Physiol 137 2011 59 79
60. O.K. Steinlein Animal models for autosomal dominant frontal lobe epilepsy: on the origin of seizures Expert Rev Neurother 10 2010 1859 1867
61. O.K. Steinlein, J.C. Mulley, P. Propping, R.H. Wallace, H.A. Phillips, and G.R. Sutherland A missense mutation in the neuronal nicotinic acetylcholine receptor alpha 4 subunit is associated with autosomal dominant nocturnal frontal lobe epilepsy Nat Genet 11 1995 201 203
62. O.K. Steinlein, A. Magnusson, J. Stoodt, S. Bertrand, S. Weiland, and S.F. Berkovic An insertion mutation of the CHRNA4 gene in a family with autosomal dominant nocturnal frontal lobe epilepsy Hum Mol Genet 6 1997 943 947 (Pubitemid 27239081)
63. L.W. Swanson, D.M. Simmons, P.J. Whiting, and J. Lindstrom Immunohistochemical localization of neuronal nicotinic receptors in the rodent central nervous system J Neurosci 7 1987 3334 3342
64. A.R. Tapper, S.L. McKinney, R. Nashmi, J. Schwarz, P. Deshpande, and C. Labarca Nicotine activation of alpha4* receptors: sufficient for reward, tolerance, and sensitization Science 306 2004 1029 1032 (Pubitemid 39482905)
65. A.R. Tapper, S.L. McKinney, M.J. Marks, and H.A. Lester Nicotine responses in hypersensitive and knockout alpha 4 mice account for tolerance to both hypothermia and locomotor suppression in wild-type mice Physiol Genomics 31 2007 422 428 (Pubitemid 350127782)
66. Y. Teper, D. Whyte, E. Cahir, H.A. Lester, S.R. Grady, and M.J. Marks Nicotine-induced dystonic arousal complex in a mouse line harboring a human autosomal-dominant nocturnal frontal lobe epilepsy mutation J Neurosci 27 2007 10128 10142 (Pubitemid 47450462)
67. J.M. Tepper, and C.R. Lee GABAergic control of substantia nigra dopaminergic neurons Prog Brain Res 160 2007 189 208 (Pubitemid 46702292)
68. T. Tritto, S.E. McCallum, S.A. Waddle, S.R. Hutton, R. Paylor, and A.C. Collins Null mutant analysis of responses to nicotine: deletion of beta2 nicotinic acetylcholine receptor subunit but not alpha7 subunit reduces sensitivity to nicotine-induced locomotor depression and hypothermia Nicotine Tob Res 6 2004 145 158
69. P. Whiteaker, M. Jimenez, J.M. McIntosh, A.C. Collins, and M.J. Marks Identification of a novel nicotinic binding site in mouse brain using [(125)I]-epibatidine Br J Pharmacol 131 2000 729 739
70. 125I-alpha-conotoxin MII identifies a novel nicotinic acetylcholine receptor population in mouse brain Mol Pharmacol 57 2000 913 925 (Pubitemid 30253374)
71. P. Whiteaker, C.G. Peterson, W. Xu, J.M. McIntosh, R. Paylor, and A.L. Beaudet Involvement of the alpha3 subunit in central nicotinic binding populations J Neurosci 22 2002 2522 2529 (Pubitemid 37465801)
72. P. Whiteaker, J.F. Cooper, O. Salminen, M.J. Marks, T.D. McClure-Begley, and R.W. Brown Immunolabeling demonstrates the interdependence of mouse brain alpha4 and beta2 nicotinic acetylcholine receptor subunit expression J Comp Neurol 499 2006 1016 1038 (Pubitemid 44892826)
73. P. Whiting, and J. Lindstrom Purification and characterization of a nicotinic acetylcholine receptor from rat brain Proc Natl Acad Sci USA 84 1987 595 599 (Pubitemid 17006242)
74. J. Xu, B.N. Cohen, Y. Zhu, G. Dziewczapolski, S. Panda, and H.A. Lester Altered activity-rest patterns in mice with a human autosomal-dominant nocturnal frontal lobe epilepsy mutation in the beta2 nicotinic receptor Mol Psychiatry 16 2011 1048 1061
75. C.A. Zambrano, M.J. Marks, B.K. Cassels, and R.B. Maccioni In vivo effects of 3-iodocytisine: pharmacological and genetic analysis of hypothermia and evaluation of chronic treatment on nicotinic binding sites Neuropharmacology 57 2009 332 342
76. M.R. Zarrindast, A. Bayat, and B. Shafaghi Involvement of dopaminergic receptor subtypes in straub tail behaviour in mice Gen Pharmacol 24 1993 127 130 (Pubitemid 23089186)
77. Z.J. Zhang, J. Koifman, D.S. Shin, H. Ye, C.M. Florez, and L. Zhang Transition to seizure: ictal discharge is preceded by exhausted presynaptic GABA release in the hippocampal CA3 region J Neurosci 32 2012 2499 2512
78. Y. Zhou, M.E. Nelson, A. Kuryatov, C. Choi, J. Cooper, and J. Lindstrom Human alpha4beta2 acetylcholine receptors formed from linked subunits J Neurosci 23 2003 9004 9015 (Pubitemid 37243801)
79. M. Zoli, C. Lena, M.R. Picciotto, and J.P. Changeux Identification of four classes of brain nicotinic receptors using beta2 mutant mice J Neurosci 18 1998 4461 4472 (Pubitemid 28280157)
80. R. Zwart, and H.P. Vijverberg Four pharmacologically distinct subtypes of alpha4beta2 nicotinic acetylcholine receptor expressed in Xenopus laevis oocytes Mol Pharmacol 54 1998 1124 1131 (Pubitemid 29002058)