Mechanisms underlying tolerance after long-term benzodiazepine use: A future for subtype-selective GABAA receptor modulators?

Advances in Pharmacological Sciences

Volumn 2012, Issue , 2012, Pages

  Vinkers, Christiaan H ^a   Olivier, Berend ^a,b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ACETYLCHOLINE; ANTICONVULSIVE AGENT; ANXIOLYTIC AGENT; BENZODIAZEPINE; DOPAMINE; GLUTAMATE RECEPTOR; GLUTAMIC ACID; HYPNOTIC AGENT; IONOTROPIC RECEPTOR; NEUROSTEROID; NEUROTROPHIC FACTOR; SEDATIVE AGENT; SEROTONIN; TEMAZEPAM;

AMNESIA; DRUG ABUSE; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG METABOLISM; DRUG TOLERANCE; EPILEPSY; GABAERGIC SYSTEM; HUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REINFORCEMENT; REVIEW; SIGNAL TRANSDUCTION;

EID: 84859747943     PISSN: 16876334     EISSN: 16876342     Source Type: Journal    
DOI: 10.1155/2012/416864     Document Type: Review

References (165)

1. Lader M., History of benzodiazepine dependence Journal of Substance Abuse Treatment 1991 8 1-2 53 59
2. Owen R. T., Tyrer P., Benzodiazepine dependence. A review of the evidence Drugs 1983 25 4 385 398 (Pubitemid 13112224)
3. American Psychiatric Association, Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR 2000
4. Petursson H., The benzodiazepine withdrawal syndrome Addiction 1994 89 11 1455 1459 (Pubitemid 24343905)
5. Allison C., Pratt J. A., Neuroadaptive processes in GABAergic and glutamatergic systems in benzodiazepine dependence Pharmacology and Therapeutics 2003 98 2 171 195 (Pubitemid 36513774)
6. Pratt J. A., Brett R. R., Laurie D. J., Benzodiazepine dependence: from neural circuits to gene expression Pharmacology Biochemistry and Behavior 1998 59 4 925 934 (Pubitemid 28237905)
7. Woods J. H., Katz J. L., Winger G., Benzodiazepines: use, abuse, and consequences Pharmacological Reviews 1992 44 2 151 347
8. Ator N. A., Atack J. R., Hargreaves R. J., Burns H. D., Dawson G. R., Reducing abuse liability of GABAA /benzodiazepine ligands via selective partial agonist efficacy at 1 and 2/3 subtypes Journal of Pharmacology and Experimental Therapeutics 2010 332 1 4 16
9. Licata S. C., Rowlett J. K., Abuse and dependence liability of benzodiazepine-type drugs: GABAA receptor modulation and beyond Pharmacology Biochemistry and Behavior 2008 90 1 74 89
10. Tan K. R., Brown M., Labouébe G., Yvon C., Creton C., Fritschy J. M., Rudolph U., Lscher C., Neural bases for addictive properties of benzodiazepines Nature 2010 463 7282 769 774
11. Wafford K. A., GABAA receptor subtypes: any clues to the mechanism of benzodiazepine dependence? Current Opinion in Pharmacology 2005 5 1 47 52 (Pubitemid 40124534)
12. Krystal J. H., Staley J., Mason G., Petrakis I. L., Kaufman J., Harris R. A., Gelernter J., Lappalainen J., -aminobutyric acid type A receptors and alcoholism: intoxication, dependence, vulnerability, and treatment Archives of General Psychiatry 2006 63 9 957 968 (Pubitemid 44330454)
13. Rudolph U., Mohler H., GABA-based therapeutic approaches: GABAA receptor subtype functions Current Opinion in Pharmacology 2006 6 1 18 23 (Pubitemid 43103815)
14. McKernan R. M., Whiting P. J., Which GABAA -receptor subtypes really occur in the brain? Trends in Neurosciences 1996 19 4 139 143
15. Sieghart W., Structure and pharmacology of -aminobutyric acidA receptor subtypes Pharmacological Reviews 1995 47 2 181 234
16. Sieghart W., Sperk G., Subunit composition, distribution and function of GABAA receptor subtypes Current Topics in Medicinal Chemistry 2002 2 8 795 816
17. Cobb S. R., Buhl E. H., Halasy K., Paulsen O., Somogyl P., Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons Nature 1995 378 6552 75 78
18. Lewis D. A., Cho R. Y., Carter C. S., Eklund K., Forster S., Kelly M. A., Montrose D., Subunit-selective modulation of GABA type A receptor neurotransmission and cognition in schizophrenia American Journal of Psychiatry 2008 165 12 1585 1593
19. Mohler H., Fritschy J. M., Rudolph U., A new benzodiazepine pharmacology Journal of Pharmacology and Experimental Therapeutics 2002 300 1 2 8 (Pubitemid 34028501)
20. Belelli D., Harrison N. L., Maguire J., Macdonald R. L., Walker M. C., Cope D. W., Extrasynaptic GABAA receptors: form, pharmacology, and function Journal of Neuroscience 2009 29 41 12757 12763
21. Serwanski D. R., Miralles C. P., Christie S. B., Mehta A. K., Li X., De Blas A. L., Synaptic and nonsynaptic localization of GABAA receptors containing the 5 subunit in the rat brain Journal of Comparative Neurology 2006 499 3 458 470 (Pubitemid 44571940)
22. Rudolph U., Crestani F., Benke D., Brnig I., Benson J. A., Fritschy J. M., Martin J. R., Bluethmann H., Mohler H., Benzodiazepine actions mediated by specific -aminobutyric acidA receptor subtypes Nature 1999 401 6755 796 800
23. McKernan R. M., Rosahl T. W., Reynolds D. S., Sur C., Wafford K. A., Atack J. R., Farrar S., Myers J., Cook G., Ferris P., Garrett L., Bristow L., Marshall G., Macaulay A., Brown N., Howell O., Moore K. W., Carling R. W., Street L. J., Castro J. L., Ragan C. I., Dawson G. R., Whiting P. J., Sedative but not anxiolytic properties of benzodiazepines are mediated by the GABAA receptor 1 subtype Nature Neuroscience 2000 3 6 587 592 (Pubitemid 30332078)
24. Atack J. R., GABAA receptor subtype-selective modulators. I. alpha2/alpha3-selective agonists as non-sedating anxiolytics Current Topics in Medicinal Chemistry 2010 2 331 360
25. Collinson N., Kuenzi F. M., Jarolimek W., Maubach K. A., Cothliff R., Sur C., Smith A., Otu F. M., Howell O., Atack J. R., McKernan R. M., Seabrook G. R., Dawson G. R., Whiting P. J., Rosahl T. W., Enhanced learning and memory and altered GABAergic synaptic transmission in mice lacking the 5 subunit of the GABAA receptor Journal of Neuroscience 2002 22 13 5572 5580 (Pubitemid 35386478)
26. Dawson G. R., Maubach K. A., Collinson N., Cobain M., Everitt B. J., MacLeod A. M., Choudhury H. I., McDonald L. M., Pillai G., Rycroft W., Smith A. J., Sternfeld F., Tattersall F. D., Wafford K. A., Reynolds D. S., Seabrook G. R., Atack J. R., An inverse agonist selective for 5 subunit-containing GABAA receptors enhances cognition Journal of Pharmacology and Experimental Therapeutics 2006 316 3 1335 1345 (Pubitemid 43345310)
27. van Rijnsoever C., Tuber M., Choulli M. K., Keist R., Rudolph U., Mohler H., Fritschy J. M., Crestani F., Requirement of 5- GABAA receptors for the development of tolerance to the sedative action of diazepam in mice Journal of Neuroscience 2004 24 30 6785 6790 (Pubitemid 38993900)
28. Ator N. A., Contributions of GABAA receptor subtype selectivity to abuse liability and dependence potential of pharmacological treatments for anxiety and sleep disorders CNS Spectrums 2005 10 1 31 39 (Pubitemid 40139741)
29. Griffiths R. R., Sannerud C. A., Ator N. A., Brady J. V., Zolpidem behavioral pharmacology in baboons: self-injection, discrimination, tolerance and withdrawal Journal of Pharmacology and Experimental Therapeutics 1992 260 3 1199 1208
30. Rowlett J. K., Platt D. M., Lelas S., Atack J. R., Dawson G. R., Different GABAA receptor subtypes mediate the anxiolytic, abuse-related, and motor effects of benzodiazepine-like drugs in primates Proceedings of the National Academy of Sciences of the United States of America 2005 102 3 915 920 (Pubitemid 40282765)
31. Griebel G., Perrault G., Simiand J., SL651498: an anxioselective compound with functional selectivity for alpha2- and alpha3-containing gamma-aminobutyric acidA GABAA receptors Journal of Pharmacology and Experimental Therapeutics 2001 298 2 753 768 (Pubitemid 32673429)
32. Benes F. M., Todtenkopf M. S., Logiotatos P., Williams M., Glutamate decarboxylase(65)-immunoreactive terminals in cingulate and prefrontal cortices of schizophrenic and bipolar brain Journal of Chemical Neuroanatomy 2000 20 3-4 259 269 (Pubitemid 32162885)
33. Schousboe A., Sarup A., Larsson O. M., White H. S., GABA transporters as drug targets for modulation of GABAergic activity Biochemical Pharmacology 2004 68 8 1557 1563 (Pubitemid 39286460)
34. Bateson A. N., Basic pharmacologic mechanisms involved in benzodiazepine tolerance and withdrawal Current Pharmaceutical Design 2002 8 1 5 21 (Pubitemid 34449900)
35. File S. E., Tolerance to the behavioral actions of benzodiazepines Neuroscience and Biobehavioral Reviews 1985 9 1 113 121 (Pubitemid 15136676)
36. File S. E., The history of benzodiazepine dependence: a review of animal studies Neuroscience and Biobehavioral Reviews 1990 14 2 135 146 (Pubitemid 20159550)
37. Schneider-Helmert D., Why low-dose benzodiazepine-dependent insomniacs can't escape their sleeping pills Acta Psychiatrica Scandinavica 1988 78 6 706 711 (Pubitemid 19027339)
38. Lucki I., Rickels K., The behavioral effects of benzodiazepines following long-term use Psychopharmacology Bulletin 1986 22 2 424 433 (Pubitemid 16043815)
39. Lucki I., Rickels K., Geller A. M., Chronic use of benzodiazepines and psychomotor and cognitive test performance Psychopharmacology 1986 88 4 426 433 (Pubitemid 16109551)
40. Cowley D. S., Roy-Byrne P. P., Radant A., Ritchie J. C., Greenblatt D. J., Nemeroff C. B., Hommer D. W., Benzodiazepine sensitivity in panic disorder: effects of chronic alprazolam treatment Neuropsychopharmacology 1995 12 2 147 157
41. Allen D., Curran H. V., Lader M., The effects of repeated doses of clomipramine and alprazolam on physiological, psychomotor and cognitive functions in normal subjects European Journal of Clinical Pharmacology 1991 40 4 355 362
42. Kales A., Scharf M. B., Kales J. D., Rebound insomnia: a new clinical syndrome Science 1978 201 4360 1039 1041 (Pubitemid 9035541)
43. Kales A., Soldatos C. R., Bixler E. O., Kales J. D., Early morning insomnia with rapidly eliminated benzodiazepines Science 1983 220 4592 95 97 (Pubitemid 13161722)
44. Pegram V., Hyde P., Linton P., Chronic use of triazolam: the effects on the sleep patterns of insomniacs Journal of International Medical Research 1980 8 3 224 231 (Pubitemid 10114430)
45. Roth T., Kramer M., Lutz T., Intermediate use of triazolam: a sleep laboratory study Journal of International Medical Research 1976 4 1 59 63
46. Mitler M. M., Carskadon M. A., Phillips R. L., Sterling W. R., Zarcone V. P., Spiegel R., Guilleminault C., Dement W. C., Hypnotic efficacy of temazepam: a long-term sleep laboratory evaluation British Journal of Clinical Pharmacology 1979 8 1 63S 68S
47. Kales A., Kales J. D., Sleep laboratory studies of hypnotic drugs: efficacy and withdrawal effects Journal of Clinical Psychopharmacology 1983 3 2 140 150 (Pubitemid 13080265)
48. Soldatos C. R., Dikeos D. G., Whitehead A., Tolerance and rebound insomnia with rapidly eliminated hypnotics: a meta-analysis of sleep laboratory studies International Clinical Psychopharmacology 1999 14 5 287 303
49. Monane M., Glynn R. J., Avorn J., The impact of sedative-hypnotic use on sleep symptoms in elderly nursing home residents Clinical Pharmacology and Therapeutics 1996 59 1 83 92 (Pubitemid 26046773)
50. Curran H. V., Collins R., Fletcher S., Kee S. C. Y., Woods B., Iliffe S., Older adults and withdrawal from benzodiazepine hypnotics in general practice: effects on cognitive function, sleep, mood and quality of life Psychological Medicine 2003 33 7 1223 1237 (Pubitemid 37265211)
51. Poyares D., Guilleminault C., Ohayon M. M., Tufik S., Chronic benzodiazepine usage and withdrawal in insomnia patients Journal of Psychiatric Research 2004 38 3 327 334 (Pubitemid 38299171)
52. Browne T. R., Penry J. K., Benzodiazepines in the treatment of epilepsy: a review Epilepsia 1973 14 3 277 310
53. Loscher W., Rundfeldt C., Honack D., Ebert U., Long-term studies on anticonvulsant tolerance and withdrawal characteristics of benzodiazepine receptor ligands in different seizure models in mice. I. Comparison of diazepam, clonazepam, clobazam and abecarnil Journal of Pharmacology and Experimental Therapeutics 1996 279 2 561 572
54. Rundfeldt C., Wlaz P., Honack D., Loscher W., Anticonvulsant tolerance and withdrawal characteristics of benzodiazepine receptor ligands in different seizure models in mice. Comparison of diazepam, Bretazenil and Abecarnil Journal of Pharmacology and Experimental Therapeutics 1995 275 2 693 702 (Pubitemid 26023614)
55. Gonsalves S. F., Gallager D. W., Time course for development of anticonvulsant tolerance and GABAergic subsensitivity after chronic diazepam Brain Research 1987 405 1 94 99 (Pubitemid 17034936)
56. Ko D., Rho J. M., DeGiorgio C. M., Sato S., Engel J. J., Pedley T. A., Benzodiazpines Epilepsy: A Comprehensive Textbook 1997 Philadelphia, Pa, USA Lippincott-Raven 1475 1489
57. Brodie M. J., Established anticonvulsants and treatment of refractory epilepsy The Lancet 1990 336 8711 350 354 (Pubitemid 20264154)
58. File S. E., Wilks L., Effects of acute and chronic treatment on the pro- and anti-convulsant actions of CL 218, 872, PK 8165 and PK 9084, putative ligands for the benzodiazepine receptor Journal of Pharmacy and Pharmacology 1985 37 4 252 256 (Pubitemid 15149837)
59. Feely M., Boyland P., Picardo A., Cox A., Gent J. P., Lack of anticonvulsant tolerance with RU 32698 and Ro 17-1812 European Journal of Pharmacology 1989 164 2 377 380 (Pubitemid 19138648)
60. Loscher W., Rundfeldt C., Honack D., Ebert U., Long-term studies on anticonvulsant tolerance and withdrawal characteristics of benzodiazepine receptor ligands in different seizure models in mice. II. The novel imidazoquinazolines NNC 14-0185 and NNC 14-0189 Journal of Pharmacology and Experimental Therapeutics 1996 279 2 573 581
61. Curran H. V., Bond A., O'Sullivan G., Bruce M., Marks I., Lelliot P., Shine P., Lader M., Memory functions, alprazolam and exposure therapy: a controlled longitudinal study of agoraphobia with panic disorder Psychological Medicine 1994 24 4 969 976
62. Tata P. R., Rollings J., Collins M., Pickering A., Jacobson R. R., Lack of cognitive recovery following withdrawal from long-term benzodiazepine use Psychological Medicine 1994 24 1 203 213 (Pubitemid 24083695)
63. Barker M. J., Greenwood K. M., Jackson M., Crowe S. F., Persistence of cognitive effects after withdrawal from long-term benzodiazepine use: a meta-analysis Archives of Clinical Neuropsychology 2004 19 3 437 454 (Pubitemid 38373546)
64. Tsunoda K., Uchida H., Suzuki T., Watanabe K., Yamashima T., Kashima H., Effects of discontinuing benzodiazepine-derivative hypnotics on postural sway and cognitive functions in the elderly International Journal of Geriatric Psychiatry 2010 25 12 1259 1265
65. Tonne U., Hiltunen A. J., Vikander B., Engelbrektsson K., Bergman H., Berman I., Leifman H., Borg S., Neuropsychological changes during steady-state drug use, withdrawal and abstinence in primary benzodiazepine-dependent patients Acta Psychiatrica Scandinavica 1995 91 5 299 304
66. Rickels K., Lucki I., Schweizer E., Garca-Espaa F., Case W. G., Psychomotor performance of long-term benzodiazepine users before, during, and after benzodiazepine discontinuation Journal of Clinical Psychopharmacology 1999 19 2 107 113 (Pubitemid 29161955)
67. Schweizer E., Rickels K., Weiss S., Zavodnick S., Maintenance drug treatment of panic disorder: I. Results of a prospective, placebo-controlled comparison of alprazolam and imipramine Archives of General Psychiatry 1993 50 1 51 60 (Pubitemid 23026989)
68. Rickels K., Case G., Downing R. W., Winokur A., Long-term diazepam therapy and clinical outcome The Journal of the American Medical Association 1983 250 6 767 771 (Pubitemid 13039567)
69. Charney D. S., Woods S. W., Benzodiazepine treatment of panic disorder: a comparison of alprazolam and lorazepam Journal of Clinical Psychiatry 1989 50 11 418 423 (Pubitemid 19282226)
70. Ballenger J. C., Long-term pharmacologic treatment of panic disorder Journal of Clinical Psychiatry 1991 52 2, supplement 18 23
71. Burrows G. D., Judd F. K., Norman T. R., Long-term drug treatment of panic disorder Journal of Psychiatric Research 1993 27 supplement 1 111 125 (Pubitemid 24036527)
72. Pollack M. H., Tesar G. E., Rosenbaum J. F., Spier S. A., Clonazepam in the treatment of panic disorder and agoraphobia: a one-year follow-up Journal of Clinical Psychopharmacology 1986 6 5 302 304 (Pubitemid 17206875)
73. Cohn J. B., Wilcox C. S., Long-term comparison of alprazolam, lorazepam and placebo in patients with an anxiety disorder Pharmacotherapy 1984 4 2 93 98 (Pubitemid 14148711)
74. Sutherland S. M., Tupler L. A., Colket J. T., Davidson J. R. T., A 2-year follow-up of social phobia: status after a brief medication trial Journal of Nervous and Mental Disease 1996 184 12 731 738
75. Davidson J. R. T., Ford S. M., Smith R. D., Potts N. L. S., Long-term treatment of social phobia with clonazepam Journal of Clinical Psychiatry 1991 52 11, supplement 16 20
76. Otto M. W., Pollack M. H., Gould R. A., Worthington J. J., McArdle E. T., Rosenbaum J. F., Heimberg R. G., A comparison of the efficacy of clonazepam and cognitive-behavioral group therapy for the treatment of social phobia Journal of Anxiety Disorders 2000 14 4 345 358 (Pubitemid 30665663)
77. Griffiths R. R., Weerts E. M., Benzodiazepine self-administration in humans and laboratory animalsimplications for problems of long-term use and abuse Psychopharmacology 1997 134 1 1 37 (Pubitemid 27485546)
78. Weerts E. M., Griffiths R. R., Zolpidem self-injection with concurrent physical dependence under conditions of long-term continuous availability in baboons Behavioural Pharmacology 1998 9 3 285 297 (Pubitemid 28273114)
79. Weerts E. M., Kaminski B. J., Griffiths R. R., Stable low-rate midazolam self-injection with concurrent physical dependence under conditions of long-term continuous availability in baboons Psychopharmacology 1998 135 1 70 81 (Pubitemid 28055452)
80. Soumerai S. B., Simoni-Wastila L., Singer C., Mah C., Gao X., Salzman C., Ross-Degnan D., Lack of relationship between long-term use of benzodiazepines and escalation to high dosages Psychiatric Services 2003 54 7 1006 1011 (Pubitemid 36793455)
81. Fernandes C., File S. E., Berry D., Evidence against oppositional and pharmacokinetic mechanisms of tolerance to diazepam's sedative effects Brain Research 1996 734 1-2 236 242 (Pubitemid 26334051)
82. Friedman L. K., Gibbs T. T., Farb D. H., -aminobutyric acidA receptor regulation: heterologous uncoupling of modulatory site interactions induced by chronic steroid, barbiturate, benzodiazepine, or GABA treatment in culture Brain Research 1996 707 1 100 109
83. Gallager D. W., Lakoski J. M., Gonsalves Rauch S. F. S. L., Chronic benzodiazepine treatment decreases postsynaptic GABA sensitivity Nature 1984 308 5954 74 77 (Pubitemid 14130936)
84. Wong G., Lyon T., Skolnick P., Chronic exposure to benzodiazepine receptor ligands uncouples the aminobutyric acid type A receptor in WSS-1 cells Molecular Pharmacology 1994 46 6 1056 1062
85. Tietz E. I., Chiu T. H., Rosenberg H. C., Regional GABA/benzodiazepine receptor/chloride channel coupling after acute and chronic benzodiazepine treatment European Journal of Pharmacology 1989 167 1 57 65 (Pubitemid 19213706)
86. Primus R. J., Yu J., Xu J., Hartnett C., Meyyappan M., Kostas C., Ramabhadran T. V., Gallager D. W., Allosteric uncoupling after chronic benzodiazepine exposure of recombinant -aminobutyric acidA receptors expressed in Sf9 cells: ligand efficacy and subtype selectivity Journal of Pharmacology and Experimental Therapeutics 1996 276 3 882 890
87. Pericic D., Strac D. S., Jembrek M. J., Vlainic J., Allosteric uncoupling and up-regulation of benzodiazepine and GABA recognition sites following chronic diazepam treatment of HEK 293 cells stably transfected with 1 2 2S subunits of GABAA receptors Naunyn-Schmiedeberg's Archives of Pharmacology 2007 375 3 177 187 (Pubitemid 46525450)
88. Klein R. L., Harris R. A., Regulation of GABAA receptor structure and function by chronic drug treatments in vivo and with stably transfected cells Japanese Journal of Pharmacology 1996 70 1 1 15
89. Klein R. L., Mascia M. P., Harkness P. C., Hadingham K. L., Whiting P. J., Harris R. A., Regulation of allosteric coupling and function of stably expressed -aminobutyric acid GABAA receptors by chronic treatment with GABAA and benzodiazepine agonists Journal of Pharmacology and Experimental Therapeutics 1995 274 3 1484 1492
90. Ali N. J., Olsen R. W., Chronic benzodiazepine treatment of cells expressing recombinant GABAA receptors uncouples allosteric binding: studies on possible mechanisms Journal of Neurochemistry 2001 79 5 1100 1108 (Pubitemid 33117091)
91. Itier V., Granger P., Perrault G., Depoortere H., Scatton B., Avenet P., Protracted treatment with diazepam reduces benzodiazepine1 receptor-mediated potentiation of gamma-aminobutyric acid-induced currents in dissociated rat hippocampal neurons Journal of Pharmacology and Experimental Therapeutics 1996 279 3 1092 1099
92. Heninger C., Gallager D. W., Altered -aminobutyric acid/benzodiazepine interaction after chronic diazepam exposure Neuropharmacology 1988 27 10 1073 1076
93. Brett R. R., Pratt J. A., Changes in benzodiazepine-GABA receptor coupling in an accumbens-habenula circuit after chronic diazepam treatment British Journal of Pharmacology 1995 116 5 2375 2384
94. Roca D. J., Rozenberg I., Farrant M., Farb D. H., Chronic agonist exposure induces down-regulation and allosteric uncoupling of the -aminobutyric acid/benzodiazepine receptor complex Molecular Pharmacology 1990 37 1 37 43 (Pubitemid 20038447)
95. Kittler J. T., Moss S. J., Modulation of GABAA receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition Current Opinion in Neurobiology 2003 13 3 341 347 (Pubitemid 36792247)
96. Poisbeau P., Cheney M. C., Browning M. D., Mody I., Modulation of synaptic GABAA receptor function by PKA and PKC in adult hippocampal neurons Journal of Neuroscience 1999 19 2 674 683 (Pubitemid 29036019)
97. Lilly S. M., Zeng X. J., Tietz E. I., Role of protein kinase A in GABAA receptor dysfunction in CA1 pyramidal cells following chronic benzodiazepine treatment Journal of Neurochemistry 2003 85 4 988 998 (Pubitemid 36578630)
98. Huopaniemi, L., Keist R., Randolph A., Certa U., Rudolph U., Diazepam-induced adaptive plasticity revealed by alpha1 GABAA receptor-specific expression profiling Journal of Neurochemistry 2004 88 5 1059 1067 (Pubitemid 38280674)
99. Mierlak D., Farb D. H., Modulation of neurotransmitter receptor desensitization chlordiazepoxide stimulates fading of the GABA response Journal of Neuroscience 1988 8 3 814 820 (Pubitemid 18085153)
100. Jacob T. C., Moss S. J., Jurd R., GABAA receptor trafficking and its role in the dynamic modulation of neuronal inhibition Nature Reviews Neuroscience 2008 9 5 331 343 (Pubitemid 351556042)
101. Arancibia-Crcamo I. L., Kittler J. T., Regulation of GABAA receptor membrane trafficking and synaptic localization Pharmacology and Therapeutics 2009 123 1 17 31
102. Uusi-Oukari M., Korpi E. R., Regulation of GABAA receptor subunit expression by pharmacological agents Pharmacological Reviews 2010 62 1 97 135
103. Arnot M. I., Davies M., Martin I. L., Bateson A. N., GABAA receptor gene expression in rat cortex: differential effects of two chronic diazepam treatment regimes Journal of Neuroscience Research 2001 64 6 617 625 (Pubitemid 32520684)
104. Little H. J., Nutt D. J., Taylor S. C., Bidirectional effects of chronic treatment with agonists and inverse agonists at the benzodiazepine receptor Brain Research Bulletin 1987 19 3 371 378 (Pubitemid 18014958)
105. Tehrani M. H., Barnes E. M. Jr., Sequestration of gamma-aminobutyric acidA receptors on clathrin-coated vesicles during chronic benzodiazepine administration in vivo Journal of Pharmacology and Experimental Therapeutics 1997 283 1 384 390 (Pubitemid 27438985)
106. Barnes E. M. Jr., Intracellular trafficking of GABAA receptors Life Sciences 2000 66 12 1063 1070
107. Liang J., Zhang N., Cagetti E., Houser C. R., Olsen R. W., Spigelman I., Chronic intermittent ethanol-induced switch of ethanol actions from extrasynaptic to synaptic hippocampal GABAA receptors Journal of Neuroscience 2006 26 6 1749 1758 (Pubitemid 43236987)
108. Herman J. P., Mueller N. K., Figueiredo H., Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration Annals of the New York Academy of Sciences 2004 1018 35 45 (Pubitemid 38951388)
109. Homayoun H., Moghaddam B., NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons Journal of Neuroscience 2007 27 43 11496 11500 (Pubitemid 350006886)
110. Stephens D. N., A glutamatergic hypothesis of drug dependence: extrapolations from benzodiazepine receptor ligands Behavioural Pharmacology 1995 6 5-6 425 446
111. Marley R. J., Heninger C., Hernandez T. D., Gallager D. W., Chronic administration of -carboline-3-carboxylic acid methylamide by continuous intraventricular infusion increases GABAergic function Neuropharmacology 1991 30 3 245 251
112. Izzo E., Auta J., Impagnatiello F., Pesold C., Guidotti A., Costa E., Glutamic acid decarboxylase and glutamate receptor changes during tolerance and dependence to benzodiazepines Proceedings of the National Academy of Sciences of the United States of America 2001 98 6 3483 3488 (Pubitemid 32220871)
113. Traynelis S. F., Wollmuth L. P., McBain C. J., Menniti F. S., Vance K. M., Ogden K. K., Hansen K. B., Yuan H., Myers S. J., Dingledine R., Glutamate receptor ion channels: structure, regulation, and function Pharmacological Reviews 2010 62 3 405 496
114. Bard L., Groc L., Glutamate receptor dynamics and protein interaction: lessons from the NMDA receptor Molecular and Cellular Neuroscience 2011 48 4 298 307
115. Paoletti P., Neyton J., NMDA receptor subunits: function and pharmacology Current Opinion in Pharmacology 2007 7 1 39 47 (Pubitemid 46238036)
116. Nakagawa T., The biochemistry, ultrastructure, and subunit assembly mechanism of AMPA receptors Molecular Neurobiology 2010 42 3 161 184
117. Armstrong N., Jasti J., Beich-Frandsen M., Gouaux E., Measurement of conformational changes accompanying desensitization in an Ionotropic glutamate receptor Cell 2006 127 1 85 97 (Pubitemid 44466635)
118. Lerma J., Kainate receptor physiology Current Opinion in Pharmacology 2006 6 1 89 97 (Pubitemid 43103824)
119. Khanna J. M., Chau A., Shah G., Effect of NMDA antagonists on rapid tolerance to benzodiazepines Brain Research Bulletin 1997 42 2 99 103
120. File S. E., Fernandes C., Dizocilpine prevents the development of tolerance to the sedative effects of diazepam in rats Pharmacology Biochemistry and Behavior 1994 47 4 823 826 (Pubitemid 24119887)
121. Steppuhn K. G., Turski L., Diazepam dependence prevented by glutamate antagonists Proceedings of the National Academy of Sciences of the United States of America 1993 90 14 6889 6893 (Pubitemid 23207319)
122. Koff J. M., Pritchard G. A., Greenblatt D. J., Miller L. G., The NMDA receptor competitive antagonist CPP modulates benzodiazepine tolerance and discontinuation Pharmacology 1997 55 5 217 227 (Pubitemid 27472693)
123. Fernandes C., File S. E., Dizocilpine does not prevent the development of tolerance to the anxiolytic effects of diazepam in rats Brain Research 1999 815 2 431 434 (Pubitemid 29225293)
124. Tsuda M., Shimizu N., Yajima Y., Suzuki T., Misawa M., Hypersusceptibility to DMCM-induced seizures during diazepam withdrawal in mice: evidence for upregulation of NMDA receptors Naunyn-Schmiedeberg's Archives of Pharmacology 1998 357 3 309 315 (Pubitemid 28112581)
125. Perez M. F., Salmiron R., Ramirez O. A., NMDA-NR1 and -NR2B subunits mRNA expression in the hippocampus of rats tolerant to diazepam Behavioural Brain Research 2003 144 1-2 119 124 (Pubitemid 37011173)
126. Almiron R. S., Perez M. F., Ramirez O. A., MK-801 prevents the increased NMDA-NR1 and NR2B subunits mRNA expression observed in the hippocampus of rats tolerant to diazepam Brain Research 2004 1008 1 54 60 (Pubitemid 38469976)
127. Van Sickle B. J., Cox A. S., Schak K., Greenfield L. J., Tietz E. I., Chronic benzodiazepine administration alters hippocampal CA1 neuron excitability: NMDA receptor function and expression Neuropharmacology 2002 43 4 595 606 (Pubitemid 35279570)
128. Bonavita C., Ferrero A., Cereseto M., Velardez M., Rubio M., Wikinski S., Adaptive changes in the rat hippocampal glutamatergic neurotransmission are observed during long-term treatment with lorazepam Psychopharmacology 2003 166 2 163 167 (Pubitemid 36313123)
129. Bonavita C. D., Bisagno V., Bonelli C. G., Acosta G. B., Rubio M. C., Wikinski S. I., Tolerance to the sedative effect of lorazepam correlates with a diminution in cortical release and affinity for glutamate Neuropharmacology 2002 42 5 619 625 (Pubitemid 34457742)
130. Allison C., Pratt J. A., Differential effects of two chronic diazepam treatment regimes on withdrawal anxiety and AMPA receptor characteristics Neuropsychopharmacology 2006 31 3 602 619 (Pubitemid 43276976)
131. Van Sickle B. J., Tietz E. I., Selective enhancement of AMPA receptor-mediated function in hippocampal CA1 neurons from chronic benzodiazepine-treated rats Neuropharmacology 2002 43 1 11 27 (Pubitemid 35245670)
132. Aitta-aho T., Vekovischeva O. Y., Neuvonen P. J., Korpi E. R., Reduced benzodiazepine tolerance, but increased flumazenil-precipitated withdrawal in AMPA-receptor GluR-A subunit-deficient mice Pharmacology Biochemistry and Behavior 2009 92 2 283 290
133. Lyons H. R., Land M. B., Gibbs T. T., Farb D. H., Distinct signal transduction pathways for GABA-induced GABAA receptor down-regulation and uncoupling in neuronal culture: a role for voltage-gated calcium channels Journal of Neurochemistry 2001 78 5 1114 1125 (Pubitemid 32823160)
134. Lu B., Pang P. T., Woo N. H., The yin and yang of neurotrophin action Nature Reviews Neuroscience 2005 6 8 603 614 (Pubitemid 41059335)
135. Brunig I., Penschuck S., Berninger B., Benson J., Fritschy J. M., BDNF reduces miniature inhibitory postsynaptic currents by rapid downregulation of GABAA receptor surface expression European Journal of Neuroscience 2001 13 7 1320 1328 (Pubitemid 32328486)
136. Jovanovic J. N., Thomas P., Kittler J. T., Smart T. G., Moss S. J., Brain-derived neurotrophic factor modulates fast synaptic inhibition by regulating GABAA receptor phosphorylation, activity, and cell-surface stability Journal of Neuroscience 2004 24 2 522 530 (Pubitemid 38112385)
137. Tanaka T., Saito H., Matsuki N., Inhibition of GABAA synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus Journal of Neuroscience 1997 17 9 2959 2966 (Pubitemid 27175810)
138. Cheng Q., Yeh H. H., Brain-derived neurotrophic factor attenuates mouse cerebellar granule cell GABAA receptor-mediated responses via postsynaptic mechanisms Journal of Physiology 2003 548 3 711 721 (Pubitemid 36592767)
139. Henneberger C., Jttner R., Rothe T., Grantyn R., Postsynaptic action of BDNF on GABAergic synaptic transmission in the superficial layers of the mouse superior colliculus Journal of Neurophysiology 2002 88 2 595 603 (Pubitemid 34874393)
140. Mizoguchi Y., Kanematsu T., Hirata M., Nabekura J., A rapid increase in the total number of cell surface functional GABAA receptors induced by brain-derived neurotrophic factor in rat visual cortex Journal of Biological Chemistry 2003 278 45 44097 44102 (Pubitemid 37377151)
141. Bolton M. M., Pittman A. J., Lo D. C., Lo, Brain-derived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippocampal cultures Journal of Neuroscience 2000 20 9 3221 3232 (Pubitemid 30263140)
142. Hewitt S. A., Bains J. S., Brain-derived neurotrophic factor silences GABA synapses onto hypothalamic neuroendocrine cells through a postsynaptic dynamin-mediated mechanism Journal of Neurophysiology 2006 95 4 2193 2198
143. Yan Z., Regulation of GABAergic inhibition by serotonin signaling in prefrontal cortex: molecular mechanisms and functional implications Molecular Neurobiology 2002 26 2-3 203 216 (Pubitemid 35239800)
144. Feng J., Cai X., Zhao J., Yan Z., Serotonin receptors modulate GABAA receptor channels through activation of anchored protein kinase C in prefrontal cortical neurons Journal of Neuroscience 2001 21 17 6502 6511 (Pubitemid 32781094)
145. Brandon N. J., Jovanovic J. N., Smart T. G., Moss S. J., Receptor for activated C kinase-1 facilitates protein kinase C-dependent phosphorylation and functional modulation of GABAA receptors with the activation of G-protein-coupled receptors Journal of Neuroscience 2002 22 15 6353 6361 (Pubitemid 35386390)
146. Wang X., Zhong P., Yan Z., Dopamine D4 receptors modulate GABAergic signaling in pyramidal neurons of prefrontal cortex Journal of Neuroscience 2002 22 21 9185 9193 (Pubitemid 35356161)
147. Nutt D. J., Cowen P. J., Franklin M., The effect of diazepam on indices
148. Khan A., Haleem D. J., Tolerance in the anxiolytic profile following repeated administration of diazepam but not buspirone is associated with a decrease in the responsiveness of postsynaptic 5-HT-1A receptors Acta Biologica Hungarica 2007 58 4 345 357 (Pubitemid 351160509)
149. Hegarty A. A., Vogel W. H., The effect of acute and chronic diazepam treatment on stress-induced changes in cortical dopamine in the rat Pharmacology Biochemistry and Behavior 1995 52 4 771 778
150. Lambert J. J., Cooper M. A., Simmons R. D. J., Weir C. J., Belelli D., Neurosteroids: endogenous allosteric modulators of GABAA receptors Psychoneuroendocrinology 2009 34 supplement 1 S48 S58
151. Herd M. B., Belelli D., Lambert J. J., Neurosteroid modulation of synaptic and extrasynaptic GABAA receptors Pharmacology and Therapeutics 2007 116 1 20 34 (Pubitemid 47391030)
152. Usami N., Yamamoto T., Shintani S., Higaki Y., Ishikura S., Katagiri Y., Hara A., Substrate specificity of human 3(20) -hydroxysteroid dehydrogenase for neurosteroids and its inhibition by benzodiazepines Biological and Pharmaceutical Bulletin 2002 25 4 441 445 (Pubitemid 40044660)
153. Wilson M. A., Biscardi R., Effects of gender and gonadectomy on responses to chronic benzodiazepine receptor agonist exposure in rats European Journal of Pharmacology 1992 215 1 99 107
154. Reddy D. S., Kulkarni S. K., Neurosteroid coadministration prevents development of tolerance and augments recovery from benzodiazepine withdrawal anxiety and hyperactivity in mice Methods and Findings in Experimental and Clinical Pharmacology 1997 19 6 395 405 (Pubitemid 27469550)
155. Mirza N. R., Nielsen E. O., Do subtype-selective gamma-aminobutyric acid A receptor modulators have a reduced propensity to induce physical dependence in mice? Journal of Pharmacology and Experimental Therapeutics 2006 316 3 1378 1385 (Pubitemid 43348698)
156. Atack J. R., Wafford K. A., Tye S. J., TPA023 [7-(1, 1-dimethylethyl)-6- (2-ethyl-2H-1, 2, 4-triazol-3-ylmethoxy)-3-(2-fluor ophenyl)-1, 2, 4-triazolo[4, 3-b]pyridazine], an agonist selective for alpha2- and alpha3-containing GABAA receptors, is a nonsedating anxiolytic in rodents and primates Journal of Pharmacology and Experimental Therapeutics 2006 316 1 410 422
157. Knabl J., Witschi R., Hosl K., Reinold H., Zeilhofer U. B., Ahmadi S., Brockhaus J., Sergejeva M., Hess A., Brune K., Fritschy J. M., Rudolph U., Mohler H., Zeilhofer H. U., Reversal of pathological pain through specific spinal GABAA receptor subtypes Nature 2008 451 7176 330 334
158. Zammit G., Comparative tolerability of newer agents for insomnia Drug Safety 2009 32 9 735 748
159. Ravishankar A., Carnwath T., Zolpidem tolerance and dependencetwo case reports Journal of Psychopharmacology 1998 12 1 103 104 (Pubitemid 28143012)
160. Sanger D. J., Zivkovic B., Differential development of tolerance to the depressant effects of benzodiazepine and non-benzodiazepine agonists at the omega (BZ) modulatory sites of GABAA receptors Neuropharmacology 1992 31 7 693 700
161. Sanger D. J., Zivkovic B., Investigation of the development of tolerance to the actions of zolpidem and midazolam Neuropharmacology 1987 26 10 1513 1518 (Pubitemid 17149594)
162. Perrault G., Morel E., Sanger D. J., Zivkovic B., Lack of tolerance and physical dependence upon repeated treatment with the novel hypnotic zolpidem Journal of Pharmacology and Experimental Therapeutics 1992 263 1 298 303
163. Scherkl R., Kurudi D., Frey H. H., Clorazepate in dogs: tolerance to the anticonvulsant effect and signs of physical dependence Epilepsy Research 1989 3 2 144 150 (Pubitemid 19071183)
164. Atack J. R., Subtype-selective GABAA receptor modulation yields a novel pharmacological profile: the design and development of TPA023 Advances in Pharmacology 2009 57 137 185
165. Ator N. A., Zaleplon and triazolam: drug discrimination, plasma levels, and self-administration in baboons Drug and Alcohol Dependence 2000 61 1 55 68