Stress and GABAA receptors

Journal of Neurochemistry

Volumn 112, Issue 5, 2010, Pages 1115-1130

  Skilbeck, Kelly J ^a,b   Johnston, Graham A R ^a,b   Hinton, Tina ^a,b  

^a University of Sydney   (Australia)

^b SCHIZOPHRENIA RESEARCH INSTITUTE   (Australia)

Author keywords

Depression; Development; GABAA receptor; Schizophrenia; Sex differences; Stress

Indexed keywords

3ALPHA 5ALPHA TETRAHYDROPROGESTERONE; 3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID A RECEPTOR; ALCOHOL; ALLOTETRAHYDRODEOXYCORTICOSTERONE; ANESTHETIC AGENT; BARBITURIC ACID DERIVATIVE; BENZODIAZEPINE DERIVATIVE; BICUCULLINE; CALCIUM ION; CHLORIDE CHANNEL; CORTICOSTERONE; DIAZEPAM; FLAVONOID; FLUNITRAZEPAM; MAGNESIUM ION; MUSCIMOL; NEUROSTEROID; NEUROTRANSMITTER; PREGNENOLONE; PROGESTERONE; RADIOLIGAND; TERPENE DERIVATIVE; UNCLASSIFIED DRUG; ZINC ION;

ADULTHOOD; ALLOSTERISM; BEHAVIOR CHANGE; BINDING SITE; BRAIN CORTEX; CEREBELLUM; DEPRESSION; EARLY LIFE STRESS; ENVIRONMENTAL FACTOR; EXPERIMENTAL TEST; GENETICS; HIPPOCAMPUS; HORMONE SYNTHESIS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LIFESPAN; MENTAL DEVELOPMENT; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RECEPTOR BINDING; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REVIEW; SCHIZOPHRENIA; SEX DIFFERENCE;

ALLOSTERIC SITE; ANIMALS; GABA AGENTS; HUMANS; MODELS, ANIMAL; PHOSPHORYLATION; PROTEIN TRANSPORT; RECEPTORS, GABA; SEX FACTORS; STRESS, PSYCHOLOGICAL;

ANIMALIA;

EID: 75949089368     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06539.x     Document Type: Review

References (201)

1. Aaltonen L., Erkkola R. Kanto J. (1983) Benzodiazepine receptors in the human fetus. Biol. Neonate 44, 54 57.
2. Abel E. L. Berman R. F. (1993) Effects of water immersion stress on convulsions induced by pentylenetetrazol. Pharmacol. Biochem. Behav. 45, 823 825.
3. A receptors in mouse brain. J. Neurochem. 60, 2212 2216.
4. A receptor binding in mouse forebrain membranes. Neurochem. Int. 31, 1 10.
5. Andrews N., Zharkovsky A. File S. E. (1992) Acute handling stress downregulates benzodiazepine receptors: reversal by diazepam. Eur. J. Pharmacol. 210, 247 251.
6. A receptor subunit messenger RNAs show differential expression during cortical development in the rat brain. Neuroscience 51, 583 591.
7. Arborelius L. Eklund M. B. (2007) Both long and brief maternal separation produces persistent changes in tissue levels of brain monoamines in middle-aged female rats. Neuroscience 145, 738 750.
8. Atkins C. M., Selcher J. C., Petraitis J. J., Trzaskos J. M. Sweatt J. D. (1998) The MAPK cascade is required for mammalian associative learning. Nat. Neurosci. 1, 602 609.
9. A circuits in hippocampus. Neuron 25, 449 457.
10. A receptor function after acute stress. Neuroendocrinology 63, 166 172.
11. Barbaccia M. L., Roscetti G., Trabucchi M., Purdy R. H., Mostallino M. C., Perra C., Concas A. Biggio G. (1996b) Isoniazid-induced inhibition of GABAergic transmission enhances neurosteroid content in the rat brain. Neuropharmacology 35, 1299 1305.
12. Barbaccia M. L., Concas A., Serra M. Biggio G. (1998) Stress and neurosteroids in adult and aged rats. Exp. Gerontol. 33, 697 712.
13. Barbaccia M. L., Serra M., Purdy R. H. Biggio G. (2001) Stress and neuroactive steroids. Int. Rev. Neurobiol. 46, 243 272.
14. Barker J. L., Harrison N. L., Lange G. D. Owen D. G. (1987) Potentiation of gamma-aminobutyric-acid-activated chloride conductance by a steroid anaesthetic in cultured rat spinal neurones. J. Physiol. (Lond.) 386, 485 501.
15. A receptors. Life Sci. 66, 1063 1070.
16. A receptors. J. Neurochem. 87, 325 332.
17. Belelli D. Lambert J. J. (2005) Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat. Rev. Neurosci. 6, 565 575.
18. A receptors. Neuropharmacology 43, 651 661.
19. A receptors: form, pharmacology, and function. J. Neurosci. 29, 12757 12763.
20. A receptor recruitment into synaptosomes following acute stress. Pharmacol. Biochem. Behav. 72, 497 506.
21. Biggio G., Corda M. G., Concas A., Demontis G., Rossetti Z. Gessa G. L. (1981) Rapid changes in GABA binding induced by stress in different areas of the rat brain. Brain Res. 229, 363 369.
22. Biggio G., Concas A., Serra M., Salis M., Corda M. G., Nurchi V., Crisponi C. Gessa G. L. (1984) Stress and beta-carbolines decrease the density of low affinity GABA binding sites; an effect reversed by diazepam. Brain Res. 305, 13 18.
23. Biggio G., Concas A., Mele S. Corda M. G. (1987) Changes in GABAergic transmission induced by stress, anxiogenic and anxiolytic beta-carbolines. Brain Res. Bull. 19, 301 308.
24. Biggio G., Concas A., Follesa P., Sanna E. Serra M. (2007) Stress, ethanol, and neuroactive steroids. Pharmacol. Ther. 116, 140 171.
25. 3H]flunitrazepam binding in rat brain. Eur. J. Pharmacol. 144, 105 107.
26. Bolden S. W., Hambley J. W., Johnston G. A. R. Rogers L. J. (1990) Neonatal stress and long-term modulation of GABA receptors in rat brain. Neurosci. Lett. 111, 258 262.
27. A receptor alpha subunits. J. Physiol. 545, 169 181.
28. Braestrup C., Nielsen M., Nielsen E. Lyon M. (1979) Benzodiazepine receptors in the brain as affected by different experimental stresses: the changes are small and not undirectional. Psychopharmacology 65, 273 277.
29. Brandon N. J. Moss S. J. (2000) Receptor cross talk: ligand-gated ion channels start to communicate. Sci. STKE 2000, PE1.
30. A receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway. J. Biol. Chem. 275, 38856 38862.
31. Brandon N. J., Jovanovic J. N., Smart T. G. Moss S. J. (2002) Receptor for activated C kinase-1 facilitates protein kinase C-dependent phosphorylation and functional modulation of GABA(A) receptors with the activation of G-protein-coupled receptors. J. Neurosci. 22, 6353 6361.
32. Briones-Aranda A., Rocha L. Picazo O. (2005) Alterations in GABAergic function following forced swimming stress. Pharmacol. Biochem. Behav. 80, 463 470.
33. A receptor subunit composition. Ann. Neurol. 34, 687 693.
34. A receptors. Ann. NY Acad. Sci. 1007, 29 36.
35. Brussaard A. B., Wossink J., Lodder J. C. Kits K. S. (2000) Progesterone-metabolite prevents protein kinase C-dependent modulation of γ-aminobutyric acid type A receptors in oxytocin neurons. Proc. Natl Acad. Sci. USA 97, 3625 3630.
36. Cabib S., Puglisi-Allegra S. D'Amato F. R. (1993) Effects of postnatal stress on dopamine mesolimbic system responses to aversive experiences in adult life. Brain Res. 604, 232 239.
37. Caldji C., Diorio J. Meaney M. J. (2000a) Variations in maternal care in infancy regulate the development of stress reactivity. Biol. Psychiatry 48, 1164 1174.
38. A and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 22, 219 229.
39. Canetti B., Bachar E., Galili-Weisstub E., Kaplan D. A. Shalev A. Y. (1997) Parental bonding and mental health in adolescence. Adolescence 32, 381 394.
40. Cash D. J. Subbarao K. (1987) Channel opening of gamma-aminobutyric acid receptor from rat brain: molecular mechanisms of the receptor responses. Biochemistry 26, 7562 7570.
41. Concas A., Corda M. G. Biggio G. (1985) Involvement of benzodiazepine recognition sites in the foot shock-induced decrease of low affinity GABA receptors in the rat cerebral cortex. Brain Res. 341, 50 56.
42. 35S]TBPS) binding to rat brain: an autoradiographic study. Adv. Biochem. Psychopharmacol. 41, 227 238.
43. Concas A., Mele S. Biggio G. (1987) Foot shock stress decreases chloride efflux from rat brain synaptoneurosomes. Eur. J. Pharmacol. 135, 423 427.
44. 35S] butylbicyclophosphorothionate binding in the rat cerebral cortex, an effect opposite to anxiolytics and γ-aminobutyric acid mimetics. J. Neurochem. 51, 1868 1876.
45. 35S-TBPS binding induced by stress and gabaergic drugs. Adv. Biochem. Psychopharmacol. 45, 227 246.
46. A receptor complex in the rat brain. Prog. Neuropsychopharmacol. Biol. Psychiatry 17, 651 661.
47. A receptor plasticity by progesterone metabolites. Eur. J. Pharmacol. 375, 225 235.
48. Connolly C. N., Krishek B. J., McDonald B. J., Smart T. G. Moss S. J. (1996a) Assembly and cell surface expression of heteromeric and homomeric gamma-aminobutyric acid type A receptors. J. Biol. Chem. 271, 89 96.
49. Connolly C. N., Wooltorton J. R., Smart T. G. Moss S. J. (1996b) Subcellular localization of gamma-aminobutyric acid type A receptors is determined by receptor beta subunits. Proc. Natl Acad. Sci. USA 93, 9899 9904.
50. Connolly C. N., Kittler J. T., Thomas P., Uren J. M., Brandon N. J., Smart T. G. Moss S. J. (1999) Cell surface stability of gamma-aminobutyric acid type A receptors. Dependence on protein kinase C activity and subunit composition. J. Biol. Chem. 274, 36565 36572.
51. Corda M. G., Concas A. Biggio G. (1985) Selective blockade of benzodiazepine receptors by Ro15-1788 prevents foot shock-induced decrease of low affinity γ-aminobutyric acid receptors. Neurosci. Lett. 56, 265 269. (Pubitemid 15004672)
52. A receptor activity by alphaxalone. Br. J. Pharmacol. 90, 491 500.
53. A sites in the cerebral cortex. Pharmacol. Biochem. Behav. 44, 237 239.
54. D'Amato F. R., Cabib S., Ventura R. Orsini C. (1998) Long-term effects of postnatal manipulation on emotionality are prevented by maternal anxiolytic treatment in mice. Dev. Psychobiol. 32, 225 234.
55. Davis A. M., Penschuck S., Fritschy J. M. McCarthy M. M. (2000) Developmental switch in the expression of GABA(A) receptor subunits α(1) and α(2) in the hypothalamus and limbic system of the rat. Brain Res. Dev. Brain Res. 119, 127 138.
56. Deutsch S. I., Rosse R. B., Huntzinger J. A., Novitzki M. R. Mastropaolo J. (1990) Profound stress induced alterations in flurazepam's antiseizure efficacy can be attenuated. Brain Res. 520, 272 276.
57. Drugan R. C., McIntyre T. D., Alpern H. P. Maier S. F. (1985) Coping and seizure susceptibility: control over shock protects against bicuculline-induced seizures. Brain Res. 342, 9 17.
58. Drugan R. C., Morrow A. L., Weizman R., Weizman A., Deutsch S. I., Crawley J. N. Paul S. M. (1989) Stress-induced behavioral depression in the rat is associated with a decrease in GABA-receptor-mediated chloride ion flux and brain benzodiazepine receptor occupancy. Brain Res. 487, 45 51.
59. 3H]muscimol binding in rats that do not develop stress-induced behavioral depression. Brain Res. 631, 270 276.
60. Drugan R. C., Basile A. S., Ha J.-H. Ferland R. J. (1994) The protective effects of stress control may be mediated by increased brain levels of benzodiazepine receptor agonists. Brain Res. 661, 127 136.
61. 50)? Mol. Pharmacol. 41, 1124 1129.
62. 2 subunit and gephyrin. Nat. Neurosci. 1, 563 571.
63. Fanscik A., Linn D. M. Tasker J. G. (2000) Neurosteroid modulation of GABA IPSCs is phosphorylation dependent. J. Neurosci. 20, 3067 3075.
64. Felitti V. J., Anda R. F., Nordenberg D., Williamson D. F., Spitz A. M., Edwards V., Koss M. P. Marks J. S. (1998) Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults: the Adverse Childhood Experiences (ACE) Study. Am. J. Prev. Med. 14, 245 258.
65. Fernandez-Teruel A., Escorihuela R. M., Nunez J. F., Zapata A., Boix F., Salazar W. Tobena A. (1991) The early acquisition of two-way (shuttle-box) avoidance as an anxiety-mediated behavior: psychopharmacological validation. Brain Res. Bull. 26, 173 176.
66. Filippova N., Sedelnikova A., Zong Y., Fortinberry H. Weiss D. S. (2000) Regulation of recombinant γ-aminobutyric acid (GABA)(A) and GABA(C) receptors by protein kinase C. Mol. Pharmacol. 57, 847 856.
67. A receptor complex during pregnancy and after delivery in the rat brain. Eur. J. Neurosci. 10, 2905 2912.
68. A-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J. Comp. Neurol. 359, 154 194.
69. Fritschy J. M., Paysan J., Enna A. Mohler H. (1994) Switch in the expression of rat GABA(A)-receptor subtypes during postnatal development: an immunohistochemical study. J. Neurosci. 14, 5302 5324.
70. Fuchs K. Sieghart W. (1989) Evidence for the existence of several different α- and β-subunits of the GABA/benzodiazepine receptor complex from rat brain. Neurosci. Lett. 97, 329 333.
71. A receptor alpha1 subunit mRNA in the rat brain. J. Neurobiol. 21, 1169 1179.
72. A receptor subunits in the developing rat brain. Neuroscience 45, 423 432.
73. 2 subunits in both cultured neurons and fibroblasts. J. Neurosci. 17, 6587 6596.
74. A receptor subunits: plasticity of expression during the estrous cycle. Neuroscience 136, 457 466.
75. Harris R. A. Allan A. M. (1985) Functional coupling of γ-aminobutyric acid receptors to chloride channels in brain membranes. Science 228, 1108.
76. Havoundjian H., Paul S. M. Skolnick P. (1986) Rapid, stress-induced modification of the benzodiazepine receptor-coupled chloride ionophore. Brain Res. 375, 401 406.
77. Heim C. Nemeroff C. B. (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 49, 1023 1039.
78. A receptor maturation in relation to eye opening in the rat visual cortex. Neuroscience 124, 161 171.
79. A-receptor and the type I benzodiazepine receptor near birth in macaque monkey visual cortex. Int. J. Dev. Neurosci. 12, 299 314.
80. Hodge C., Raber J., McMahon T., Walter H., Sanchez-Perez A., Olive M., Mehmert K., Morrow A. Messing R. (2002) Decreased anxiety-like behavior, reduced stress hormones, and neurosteroid supersensitivity in mice lacking protein kinase Cepsilon. J. Clin. Invest. 110, 1003 1010.
81. A receptors in the marmoset monkey: expression of distinct subtypes in pre- and postnatal brain. J. Comp. Neurol. 367, 413 430.
82. A receptors through two discrete transmembrane sites. Nature 444, 486 489.
83. A receptors and behavioral stress responses. Proc. Natl Acad. Sci. USA 100, 12213 12218.
84. A receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat. Rev. Neurosci. 9, 331 343.
85. A receptor pharmacology. Pharmacol.Ther. 69, 173 198.
86. A receptor channel pharmacology. Curr. Pharm. Des. 11, 1867 1885.
87. 1 subunit expression and paired-pulse depression are distinct properties of neonatal inhibitory GABAergic synaptic connections in the mouse superior colliculus. Eur. J. Neurosci. 13, 2088 2098.
88. A receptor alpha 1 and gamma 2 subunits in human temporal lobe, hippocampus and basal ganglia: an implication for consideration on age-related epilepsy. Epilepsy Res. 71, 47 53.
89. A receptor pharmacological properties. Mol. Pharmacol. 55, 444 524.
90. Kavaliers M. Wiebe J. P. (1987) Analgesic effects of the progesterone metabolite, 3α-hydroxy-5α-pregnan-20-one, and possible modes of action in mice. Brain Res. 415, 393 398.
91. Kellogg C. K. Pleger G. L. (1989) GABA-stimulated chloride uptake and enhancement by diazepam in synaptoneurosomes from rat brain during prenatal and postnatal development. Brain Res. Dev. Brain Res. 49, 87 95.
92. Kittler J. T. Moss S. J. (2001) Neurotransmitter receptor trafficking and the regulation of synaptic strength. Traffic 2, 437 448.
93. α receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition. Curr. Opin. Neurobiol. 13, 341 347.
94. 2 subunit green fluorescent protein chimeras. Mol. Cell. Neurosci. 16, 440 452.
95. A receptor function. Trends Pharmacol. Sci. 16, 295 303.
96. Laurie D. J., Wisden W. Seeburg P. H. (1992) The distribution of thirteen GABA(A) receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J. Neurosci. 12, 4151 4172.
97. Levine S. (1957) Infantile experience and resistance to physiological stress. Science 126, 405.
98. Levine S. (1967) Maternal and environmental influences on the adrenocortical response to stress in weanling rats. Science 156, 258 260.
99. Lippa A. S., Beer B., Sano M. C., Vogel R. A. Meyerson L. R. (1981) Differential ontogeny of type 1 and type 2 benzodiazepine receptors. Life Sci. 28, 2343 2347.
100. Lissau I. Sorensen T. I. A. (1994) Parental neglect during childhood and increased risk of obesity in young adulthood. Lancet 343, 324 328.
101. 3 in the rat pre-Botzinger complex. J. Appl. Physiol. 96, 1825 1831.
102. 3 in brain stem nuclei of rats. Brain Res. 1098, 129 138.
103. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P. M. Meaney M. J. (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277, 1659 1662.
104. A receptor subunit in rat hippocampus. Dev. Brain Res. 148, 129 141. (Pubitemid 38147813)
105. A receptor subunit expression in the midbrain during the oestrous cycle in Wistar rats. Neuroscience 131, 397 405.
106. Low K., Crestani F., Keist R. et al. (2000) Molecular and neuronal substrate for the selective attenuation of anxiety. Science, 290, 131 134.
107. Luscher B. Keller C. A. (2004) Regulation of GABA-A receptor trafficking and channel activity in functional plasticity of inhibitory synapses. Pharmacol. Ther. 102, 195 221.
108. A receptor. Neuroscience 43, 369 380.
109. A receptors open? Neuron 12, 61 71.
110. Maguire J. L. Mody I. (2007) Neurosteroid synthesis-mediated regulation of GABAA Receptors: Relevance to the ovarian cycle and stress. J. Neurosci. 27, 2155 2162.
111. Maguire J. Mody I. (2008) GABA(A)R plasticity during pregnancy: relevance to postpartum depression. Neuron, 59, 207 213.
112. Maguire J. L., Stell B. M., Rafizadeh M. Mody I. (2005) Ovarian cycle-linked changes in GABA(A) receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat. Neurosci. 8, 797 804.
113. A receptor plasticity during pregnancy. J. Neurosci. 29, 9592 9601.
114. Majewska M. D. Schwartz R. D. (1987) Pregnenolone-sulfate: an endogenous antagonist of the gamma-aminobutyric acid receptor complex in brain? Brain Res. 404, 355 360.
115. Majewska M. D., Harrison N. L. Schwartz R. D. (1986) Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232, 1004 1007.
116. A receptor. Brain Res. 526, 143 146.
117. A receptor binding to ionophore function. Neurochem. Int. 29, 361 370.
118. Martijena I. D., Salvatierra N. A. Arce A. (1992) Benzodiazepine receptor recruitment after acute stress in synaptosomal membranes from forebrain of young chicks: action of Triton X-100. J. Neural Transm. 87, 97 104.
119. McCauley J., Kern D. E., Kolodner K., Dill L., Schroeder A. F., DeChant H. K., Ryden J., Derogatis L. R. Bass E. B. (1997) Clinical characteristics of women with a history of childhood abuse: unhealed wounds. JAMA 277, 1362 1368.
120. A receptor β subunits determine regulation by cAMP-dependent protein kinase. Nat. Neurosci. 1, 23 28.
121. McIntosh J., Anisman H. Merali Z. (1999) Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Dev. Brain Res. 113, 97 106.
122. McIntyre T. D., Trullas R. Skolnick P. (1988) Asymmetrical activation of GABA-gated chloride channels in cerebral cortex. Pharmacol. Biochem. Behav. 30, 911 916.
123. A receptor α-subunits in rat brain during development. FEBS Lett. 286, 44 46.
124. Meaney M. J., Aitken D. H., Viau V., Sharma S. Sarrieau A. (1989) Neonatal handling alters adrenocortical negative feedback sensitivity and hippocampal type II glucocorticoid receptor binding in the rat. Neuroendocrinology 50, 597 604.
125. Meaney M. J., Diorio J., Francis D., Widdowson J., LaPlante P., Caldji C., Sharma S., Seckl J. R. Plotsky P. M. (1996) Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev. Neurosci. 18, 49 72.
126. Medina J. H., Novas M. L. De Robertis E. (1983a) Changes in benzodiazepine receptors by acute stress: different effect of chronic diazepam or Ro 15-1788 treatment. Eur. J. Pharmacol. 96, 181 185.
127. Medina J. H., Novas M. L., Wolfman C., Levi de Stein M. De Robertis E. (1983b) Benzodiazepine receptors in rat cerebral cortex and hippocampus undergo rapid and reversible changes after acute stress. Neuroscience 9, 331 335.
128. Meerlo P., Horvath K., Nagy G., Bohus B. Koolhaas K. M. (1999) The influence of postnatal handling on adult neuroendocrine and behavioural stress reactivity. J. Neuroendocrinol. 11, 925 933.
129. 1R/LacZ transgenic mice in response to restraint stress. J. Neurochem. 89, 1471 1478.
130. Mihalek R. M., Banerjee P. K., Korpi E. R. et al. (1999) Attenuated sensitivity to neuroactive steroids in γ-aminobutyrate type A receptor delta subunit knockout mice. Proc. Natl Acad. Sci. USA 96, 12905 12910.
131. Miller L. G., Thompson M. L., Greenblatt D. J., Deutsch S. I., Shader R. I. Paul S. M. (1987) Rapid increase in brain benzodiazepine receptor binding following defeat stress in mice. Brain Res. 414, 395 400.
132. Moles A., Rizzi R. D'Amato F. R. (2004) Postnatal stress in mice: does stressing the mother have the same effect as stressing the pups? Dev. Psychobiol. 44, 230 237.
133. Morrow A. L. (2007) Recent developments in the significance and therapeutic relevance of neuroactive steroids - Introduction to the special issue. Pharmacol. Ther., 116, 1 6.
134. Moss S. J. Smart T. G. (1996) Modulation of amino acid activated ligand gated ion channels by protein phosphorylation. Int. Rev. Neurosci. 39, 1 42.
135. A receptors by tyrosine phosphorylation. Nature 377, 344 348.
136. B receptors, in the rat cerebral cortex. Neurochem. Int. 23, 327 330.
137. Nunez J. F., Ferre P., Garcia E., Escorihuela R. M., Fernandez-Teruel A. Tobena A. (1995) Postnatal handling reduces emotionality ratings and accelerates two-way active avoidance in female rats. Physiol. Behav. 57, 831 835.
138. A receptor binding in rat brain slices. Brain Res. 850, 158 165.
139. Okada M., Onodera K., Van Renterghem C., Sieghart W. Takahashi T. (2000) Functional correlation of GABA(A) receptor α subunits expression with the properties of IPSCs in the developing thalamus. J. Neurosci. 20, 2202 2208.
140. A-receptor complexes in the guinea pig isolated ileum. Neurosci. Lett. 82, 101 106.
141. A antagonist in the guinea-pig isolated ileum. J. Pharm. Pharmacol. 42, 662 664.
142. Owens M. J., Ritchie J. C. Nemeroff C. B. (1992) 5α-Pregnane- 3α,21-diol-20-one (THDOC) attenuates mild stress-induced increases in plasma corticosterone via a non-glucocorticoid mechanism: comparison with alprazolam. Brain Res. 573, 353 355.
143. Padoin M. J., Cadore L. P., Gomes C. M., Barros H. M. T. Lucion A. B. (2001) Long-lasting effects of neonatal stimulation on the behavior of rats. Behav. Neurosci. 115, 1332 1340.
144. Park C. H., Hitri A., Lukacs L. G. Deutsch S. I. (1993) Swim stress selectively alters the specific binding of a benzodiazepine antagonist in mice. Pharmacol. Biochem. Behav. 45, 299 304.
145. Patchev V. K., Hassan A. H. S., Holsboer F. Almeida O. F. X. (1992) The neurosteroid tetrahydroprogesterone attenuates the endocrine response to stress and exerts glucocorticoid-like effects on vasopressin gene transcription in the rat hypothalamus. Neuropsychopharmacology 15, 533 540.
146. Patchev V. K., Shoaib M., Holsboer F. Almeida O. F. X. (1994) The neurosteroid tetrahydroprogesterone counteracts corticotropin-releasing hormone-induced anxiety and alters the release and gene expression of corticotropin-releasing hormone in the rat hypothalamus. Neuroscience 62, 265 271.
147. 1 subunit, an early marker for area specification in developing rat cerebral cortex. J. Comp. Neurol. 350, 133 149.
148. Pericic D., Jazvinscak M., Svob D. Mirkovic K. (2001) Swim stress alters the behavioural response of mice to GABA-related and some GABA-unrelated convulsions. Epilepsy Res. 43, 145 152.
149. Ploj K., Pham T. M., Bergstrom L., Mohammed A. H., Henriksson B. G. Nylander I. (1999) Neonatal handling in rats induces long-term effects on dynorphin peptides. Neuropeptides 33, 468 474.
150. Plotsky P. M. Meaney M. J. (1993) Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Mol. Brain Res. 18, 195 200.
151. Plotsky P. M., Thrivikraman K. V., Nemeroff C. B., Caldji C., Sharma S. Meaney M. J. (2005) Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology 30, 2192 2204.
152. A receptor alpha subunit mRNAs in the developing rat CNS. J. Neurosci. 12, 2888 2900.
153. 2 subunit messenger RNAs during embryogenesis and early postnatal development of the rat central nervous system. Neuroscience 53, 1019 1033.
154. Primus R. J. Kellogg C. K. (1991) Experience influences environmental modulation of function at the benzodiazepine (BZD)/GABA receptor chloride channel complex. Brain Res. 545, 257 264.
155. A receptor subunit for benzodiazepine pharmacology. Nature 338, 582 585. (Pubitemid 19102309)
156. Pryce C. R. Feldon J. (2003) Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci. Biobehav. Rev. 27, 57 71.
157. Pryce C. R., Bettschen D. Feldon J. (2001) Comparison of the effects of early handling and early deprivation on maternal care in the rat. Dev. Psychobiol. 38, 239 251.
158. Pryce C. R., Ruedi-Bettschen D., Dettling A. C. Feldon J. (2002) Early life stress: long-term physiological impact in rodents and primates. News Physiol. Sci. 17, 150 155.
159. Pryce C. R., Bettschen D., Nanz-Bahr N. I. Feldon J. (2003) Comparison of the effects of early handling and early deprivation on conditioned stimulus, context, and spatial learning and memory in adult rats. Behav. Neurosci. 117, 883 893.
160. A receptor. Neuron 4, 759 765.
161. Purdy R. H., Morrow A. L., Moore P. H. Paul S. M. 1991) Stress-induced elevations of γ-aminobutyric acid type A receptor-active steroids in the rat brain. Proc. Natl Acad. Sci. USA 88, 4553 4557.
162. A receptors from rat brain. Eur. J. Pharmacol. 290, 175 181.
163. Rago L., Kiivet R.-A., Harro J. Pold M. (1989) Central- and peripheral-type benzodiazepine receptors: similar regulation by stress and GABA receptor agonists. Pharmacol. Biochem. Behav. 32, 879 883.
164. Reichelt R., Hofmann D., Füdisch H.-J., Möhler H., Knapp M. Hebebrand J. (1991) Ontogeny of the benzodiazepine receptor in human brain: fluorographic, immunochemical, and reversible binding studies. J. Neurochem. 57, 1128 1135.
165. A receptor isoforms. J. Neurosci. 23, 8608 8617.
166. Robel P., Schumacher M. Baulieu E.-E. (1999) Neurosteroids: from definition and biochemistry to physiopathological function, in Neurosteroids: A New Regulatory Function in the Nervous System (Baulieu E.-E., Robel P. Schumacher M., eds pp. 17. Humana Press, New Jersey.
167. Russak L. G. Schwartz G. E. (1997) Feelings of parental care predict health status in midlife: a 35 year follow-up of the Harvard Mastery of Stress Study. J. Behav. Med. 20, 1 11.
168. Salvatierra N. A., Marin R. H., Arce A. Martijena I. D. (1994) Chick imprinting performance and susceptibility to acute stress associated to flunitrazepam receptor increase. Brain Res. 648, 39 45.
169. Sanna E., Mostallino M. C., Murru L., Carta M., Talani G., Zucca S., Mura M. L., Maciocco E. Giovanni B. (2009) Changes in expression and function of extrasynaptic GABAA receptors in the rat hippocampus during pregnancy and after delivery. J. Neurosci. 29, 1755 1765.
170. Sato T. N. Neale J. H. (1989) Type I and type II γ-aminobutyric acid/benzodiazepine receptors: purification and analysis of novel receptor complex from neonatal cortex. J. Neurochem. 52, 1114 1122.
171. A receptor subunits: role of the δ subunit. J. Neurosci. 14, 7077 7086.
172. Schlumpf M., Richards J. G., Lichtensteiger W. Mohler H. (1983) An autoradiographic study of the prenatal development of benzodiazepine binding sites in rat brain. J. Neurosci. 3, 1478 1487.
173. Schwartz R. D., Wess M. J., Labarca R., Skolnick P. Paul S. M. (1987) Acute stress enhances the activity of the GABA receptor-gated chloride ion channel in brain. Brain Res. 411, 151 155.
174. Shaw C. A., Cameron L., March D., Cynader M., Zielinski B. S. Hendrickson A. (1991) Pre- and postnatal development of GABA receptors in Macaca monkey visual cortex. J. Neurosci. 11, 3943 3959.
175. A receptor subunit expression in rat CA1 hippocampus: pharmacological and behavioural effects. Neuropharmacology 49, 573 586.
176. A receptors triggers anxiety at puberty. Nat. Neurosci. 10, 469 477.
177. A receptors. Neurochem. Int. 34, 379 385. (Pubitemid 29240634)
178. Skerritt J. H., Trisdikoon P. Johnston G. A. R. (1981) Increased GABA binding in mouse brain following acute swim stress. Brain Res. 215, 398 403.
179. 3H]GABA binding. Neurochem. Int. 52, 1212 1219.
180. A receptor alpha subunit. J. Biol. Chem. 269, 20380 20387.
181. 4 and δ subunits. Pharmacol. Ther. 116, 58 76. (Pubitemid 47391031)
182. 3H] flunitrazepam cortical binding following stressful manipulations in rats. Brain Res. 189, 505 517.
183. 35S]t-Butylbicyclophosphorothionate binds with high affinity to brain-specific sites coupled to γ-aminobutyric acid-A and ion recognition sites. Mol. Pharmacol. 23, 326 336.
184. Steimer T., Escorihuela R. M., Fernandez-teruel A. Driscoll P. (1998) Long-term behavioural and neuroendocrine changes in roman HIGH-(RHA/Verh) and LOW-(RLA-Verh) avoidance rats following neonatal handling. Int. J. Dev. Neurosci. 16, 165 174.
185. A receptors. Proc. Natl Acad. Sci. USA 100, 14439 14444.
186. A receptors on clathrin-coated vesicles during chronic benzodiazepine administration in vivo. J. Pharmacol. Exp. Ther. 283, 384 390.
187. A receptors. Brain Res. 776, 195 203.
188. A receptors at inhibitory synapses. Nat. Neurosci. 8, 889 897.
189. Tokuyama S., Takahashi M. Kaneto H. (1992) Participation of GABAergic systems in the production of antinociception by various stresses in mice. Jpn. J. Pharmacol. 60, 105 110.
190. Vallee M., Mayo W., Dellu F., Le Moal M., Simon H. Maccari S. (1997) Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J. Neurosci. 17, 2626 2636.
191. A/benzodiazepine receptor complex during development of the rat brain. J. Neurochem. 54, 187 194.
192. Wan Q., Xiong Z. G., Man H. Y., Ackerley C. A., Braunton J., Lu W. Y., Becker L. E., MacDonald J. F. Wang Y. T. (1997) Recruitment of functional GABA receptors to postsynaptic domains by insulin. Nature 388, 686 690.
193. Washbourne P., Dityatev A., Scheiffele P., Biederer T., Weiner J. A., Christopherson K. S. El-Husseini A. (2004) Cell adhesion molecules in synapse formation. J. Neurosci. 24, 9244 9249.
194. A receptor subtypes in the brain: a paradigm for CNS drug discovery? Drug Discov. Today 8, 445 450.
195. A receptor subtypes. Int. Rev. Neurobiol. 38, 95 135.
196. A receptor alpha 4 subunit. FEBS Lett. 289, 227 230.
197. A receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J. Neurosci. 12, 1040 1062.
198. Yeung J. Y. T., Canning K. J., Zhu G., Pennefather P., Macdonald J. F. Orser B. A. (2003) Tonically activated GABA-A receptors in hippocampal neurons are high affinity, low conductance sensors for extracellular GABA. Mol. Pharmacol. 63, 2 8.
199. 3) in the rat forebrain. J. Comp. Neurol. 308, 586 613.
200. 1 subunit mRNA in the rat forebrain. Mol. Brain Res. 16, 193 203.
201. Zheng G., Zhang X., Chen Y., Zhang Y., Luo W. Chen J. (2007) Evidence for a role of GABAA receptor in the acute restraint stress-induced enhancement of spatial memory. Brain Res. 1181, 61 73.