Estrous cycle variations in GABAA receptor phosphorylation enable rapid modulation by anabolic androgenic steroids in the medial preoptic area

Neuroscience

Volumn 226, Issue , 2012, Pages 397-410

  Oberlander, J G ^a   Porter, D M ^a   Onakomaiya, M M ^a   Penatti, C A A ^b   Vithlani, M ^c   Moss, S J ^c   Clark, A S ^d   Henderson, L P ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSIDADE NOVE DE JULHO   (Brazil)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DARTMOUTH COLLEGE   (United States)

Author keywords

Anabolic steroid; GABAA receptor; Inhibitory postsynaptic current; Medial preoptic area; Phosphorylation; PKC

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BETA2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA3; METHYLTESTOSTERONE; PROTEIN KINASE C; SERINE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DIESTRUS; DRUG MECHANISM; ENZYME ACTIVITY; ESTRUS CYCLE; FEMALE; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MEDIAL PREOPTIC AREA; MOUSE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROESTRUS; PROTEIN PHOSPHORYLATION;

ANABOLIC AGENTS; ANDROGENS; ANDROSTANE-3,17-DIOL; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; ESTROUS CYCLE; FEMALE; IMMUNOPRECIPITATION; MALE; METHYLTESTOSTERONE; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NESTING BEHAVIOR; PHOSPHORYLATION; PHOSPHOSERINE; PREOPTIC AREA; PROTEIN KINASE C; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, GABA-A; SEXUAL MATURATION;

EID: 84867417279     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.09.014     Document Type: Article

References (96)

1. A receptor subtypes that mediate tonic inhibition. J Biol Chem 2010, 285:41795-41805.
2. Ansonoff M.A., Etgen A.M. Estradiol elevates protein kinase C catalytic activity in the preoptic area of female rats. Endocrinology 1998, 139(7):3050-3056.
3. Basaria S. Androgen abuse in athletes: detection and consequences. J Clin Encodrinol Metab 2010, 95:1533-1543.
4. Bitran D., Hilvers R.J., Kellogg C.K. Ovarian endocrine status modulates the anxiolytic potency of diazepam and the efficacy of γ-aminobutyric acid-benzodiazepine receptor-mediated chloride ion transport. Behav Neurosci 1991, 105(5):653-662.
5. Blasberg M.E., Langan C.J., Clark A.S. The effects of 17α-methyltestosterone, methandrostenolone, and nandrolone decanoate on the rat estrous cycle. Physiol Behav 1997, 61(2):265-272.
6. Brandon N.J., Uren J.M., Kittler J.T., Wang H., Olsen R., Parker P.J., Moss S.J. Subunit-specific association of protein kinase C and the receptor for activated C kinase with GABA type A receptors. J Neurosci 1999, 19(21):9228-9234.
7. A receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway. J Biol Chem 2000, 275(49):38856-38862.
8. A receptor function and cell surface expression. Pharmacol Ther 2002, 94(1-2):113-122.
9. A receptor subunit expression. Neuron 1997, 19(5):1103-1114.
10. A-receptor function in the adult brain: insights from the oxytocin neurone. Trends Neurosci 2000, 23:190-195.
11. Clark A.S., Blasberg M.E., Brandling-Bennett E.M. Stanozolol, oxymetholone, and testosterone cypionate effects on the rat estrous cycle. Physiol Behav 1998, 63(2):287-295.
12. Clark A.S., Henderson L.P. Behavioral and physiological responses to anabolic-androgenic steroids. Neurosci Biobehav Rev 2003, 27(5):413-436.
13. Clark A.S., Kelton M.C., Whitney A.C. Chronic administration of anabolic steroids disrupts pubertal onset and estrous cyclicity in rats. Biol Reprod 2003, 68(2):465-471.
14. A receptor 2004, 119-141. CRC Press LLC, Boca Raton. S.S. Smith (Ed.).
15. Clark A.S., Costine B.A., Jones B.L., Kelton-Rehkopf M.C., Meerts S.H., Nutbrown-Greene L.L., Penatti C.A.A., Porter D.M., Yang P., Henderson L.P. Sex- and age-specific effects of anabolic androgenic steroids on reproductive behaviors and on GABAergic transmission in neuroendocrine control regions. Brain Res 2006, 1126:122-138.
16. Colquhoun D. Binding, gating, affinity and efficacy: the interpretation of structure-activity relationships for agonists and the effects of mutating receptors. Brit J Pharmacol 1998, 125:923-947.
17. Cooper R.L., Goldman J.M., Vandenbergh J.G. Monitoring of the estrous cycle in the laboratory rodent by vaginal lavage. Methods in toxicology 1993, 45-55. Academic Press, New York. J.J. Heindel, R.E. Chapin (Eds.).
18. Daly R.C., Su T.P., Schmidt P.J., Pickar D., Murphy D.L., Rubinow D.R. Cerebrospinal fluid and behavioral changes after methyltestosterone administration: preliminary findings. Arch Gen Psychiatry 2001, 58:172-177.
19. A receptor subunits α1 and α2 in the hypothalamus and limbic system of the rat. Dev Brain Res 2000, 119:127-138.
20. Deacon R.J. Assessing nest building in mice. Nat Protoc 2006, 1(3):1117-1119.
21. Deacon R.J. Digging and marble burying in mice. simple methods for in vivo identification of biological impacts. Nat Protoc 2006, 1(1):122-124.
22. Drouva S.V., Gorenne I., LaPlante E., Rérat E., Enjalbert A., Kordon C. Estradiol modulates protein kinase C activity in the rat pituitary in vivo and in vitro. Endocrinology 1990, 126(1):536-544.
23. Elliot D.L., Goldberg L. Women and anabolic steroids. Anabolic steroids in sport and exercise 2000, 225-246. Human Kinetics, Champaign, IL. 2nd ed. C.E. Yesalis (Ed.).
24. Fáncsik A., Linn D.M., Tasker J.G. Neurosteroid modulation of GABA IPSCs is phosphorylation dependent. J Neurosci 2000, 20(9):3067-3075.
25. A receptor complex. J Pharmacol Exp Ther 1993, 266:1374-1379.
26. Franke W.W., Berendonk B. Hormonal doping and androgenization of athletes: a secret program of the German Democratic Republic government. Clin Chem 1997, 43:1262-1279.
27. Freeman M. The neuroendocrine control of the ovarian cycle of the rat. The physiology of reproduction 1994, 613-658. Raven Press Ltd, New York. 2nd ed. E. Knobil, J.D. Neill (Eds.).
28. A receptors in the ventral tegmental area for lordosis of rats. Brain Res Bull 2008, 77:91-97.
29. Gaskill B.N., Gordon C.J., Pajor E.A., Lucas J.R., Davis J.K., Garner J.P. Heat or insulation: behavioral titration of mouse preference for warmth or access to a nest. PLoS One 2012, 7(3):e32799.
30. González-Flores O., Beyer C., Gómora-Arrati P., García-Juárez M., Lima-Hernández F.J., Soto-Sánchez A., Etgen A.M. A role for src-kinase in progestin facilitation of estrous behavior in estradiol-primed female rats. Horm Behav 2010, 58:223-229.
31. Haage D., Johansson S. Neurosteroid modulation of synaptic and GABA-evoked currents in neurons from the rat medial preoptic nucleus. J Neurophysiol 1999, 82(1):143-151.
32. A receptors in rat CA1 and dentate gyrus neurones. Neuropharmacology 2003, 45(6):873-883.
33. A receptor-mediated transmission in the hypothalamus: effects on reproductive function. Neuropharmacology 2007, 52:1439-1453.
34. Henderson L.P., Jorge J.C. Steroid modulation of GABAA receptors: CNS roles in reproduction, dysfunction and drug abuse. Advances in molecular and cell biology. Molecular insights into ion channel biology in health and disease 2004, vol. 32. Elsevier, Amsterdam, pp. 217-249.
35. Hunt J.L., Zaretsky D.V., Sarkar S., DiMicco J.A. Dorsomedial hypothalamus mediates autonomic, neuroendocrine, and locomotor responses evoked from the medial preoptic area. Am J Physiol/Regul Integr Comp Physiol 2010, 298:R130-R140.
36. Ishiwata T., Saito T., Hasegawa H., Yazawa T., Kotani Y., Otokawa M., Aihara Y. Changes of body temperature and thermoregulatory responses of freely moving rats during GABAergic pharmacological stimulation to the preoptic area and anterior hypothalamus in several ambient temperatures. Brain Res 2005, 1048:32-40.
37. A receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat Rev Neurosci 2008, 9:331-343.
38. Jacobson C.D., Terkel J., Gorski R.A., Sawyer C.H. Effects of small medial preoptic area lesions on maternal behavior: retrieving and nest building in the rat. Brain Res 1980, 194(2):471-478.
39. A receptors. J Physiol (Lond) 2006, 573:571-593.
40. A receptors change with hormonal state in the adult mouse. J Neurobiol 2002, 50(2):137-149.
41. Joubert-Bression D., Brandi A.M., Birman P., Peillon F. Effect of oestradiol on dopamine receptors in the rat pituitary: binding of oestradiol to pituitary membranes. Ciba Found Symp 1990, 153:156-168.
42. A receptor phosphorylation, activity, and cell-surface stability. J Neurosci 2004, 24(2):522-530.
43. A receptors. The dynamic synapse: Molecular methods in ionotropic receptor biology 2006, CRC Press, Boca Raton, [Chapter 4]. J.T. Kittler, S.J. Moss (Eds.).
44. Kanayama G., Brower K.J., Wood R.I., Hudson J.I., Pope H.G. Treatment of anabolic-androgenic steroid dependence: emerging evidence and its implications. Drug Alcohol Depend 2010, 109:6-13.
45. A receptor phosphorylation and membrane trafficking by phospholipase C-related inactive protein/protein phosphatase 1 and 2A signaling complex underlying brain-derived neurotrophic factor-dependent regulation of GABAergic inhibition. J Biol Chem 2006, 281(31):22180-22189.
46. Kelly M.J., Rønnekleiv O.K., Ibrahim N., Lagrange A.H., Wagner E.J. Estrogen modulation of K+ channel activity in hypothalamic neurons involved in the control of the reproductive axis. Steroids 2002, 67:447-456.
47. A receptor-mediated currents: role of phosphorylation. J Neurochem 2011, 116:1043-1056.
48. Kobayashi E., Nakano H., Morimoto M., Tamaoki T. Calphoston C (UCN-1028C), a novel microbial compound, is a highly potent and specific inhibitor of protein kinase C. Biochem Biophys Res Comm 1989, 159(2):548-553.
49. A receptor clustering determines GABA synapse plasticity in rat oxytocin neurons around parturition and the onset of lactation. Mol Cell Neurosci 2005, 28:128-140.
50. A receptors in supraoptic nucleus around parturition. J Neurosci 2003, 23:788-797.
51. Lachowicz A., Rebas E. Gender differences in steroid modulation of angiotensin II-induced protein kinase C activity in anterior pituitary of the rat. Biochem Biophys Res Comm 2002, 294:95-100.
52. T method. Methods 2001, 25:402-408.
53. A receptor plasticity during pregnancy. J Neurosci 2009, 29(30):9592-9601.
54. A receptors: relevance to the ovarian cycle and stress. J Neurosci 2007, 27(9):2155-2162.
55. AR plasticity. Psychoneuroendocrinology 2009, 34(Suppl 1):S84-S90.
56. A receptor. Neurosci Lett 1995, 189(1):35-38.
57. A receptor subunit mRNAs in the mouse forebrain. Neuropharmacology 2002, 43:634-645.
58. A receptors: molecular determinants and significance in health and disease. Neurochem Int 2008, 52:588-595.
59. A receptors in neurons expressing γ1 subunit mRNA in the preoptic area of the rat. J Neurophysiol 1999, 81:192-203.
60. Njung'e K., Handley S.L. Evaluation of marble-burying behavior as a model of anxiety. Pharmacol Biochem Behav 1991, 38(1):63-67.
61. Oberlander J.G., Henderson L.P. Corticotropin releasing factor modulation of forebrain GABAergic transmission plays a pivotal role in the expression of anabolic steroid induced anxiety in the female mouse. Neuropysychopharmacology 2012, 37(6):1483-1499.
62. Oberlander J.G., Henderson L.P. The Sturm und Drang of anabolic steroid use: angst, anxiety, and aggression. Trends Neurosci 2012, 35(6):382-392.
63. Oberlander J.G., Penatti C.A.A., Porter D.M., Henderson L.P. The buzz about anabolic androgenic steroids: electrophysiological effects in excitable tissues. Neuroendocrinology 2012, 2012. doi:http://dx.doi.org/10.1159/000339123.
64. Oberlander J.G., Porter D.M., Penatti C.A., Henderson L.P. Anabolic androgenic steroid abuse: multiple mechanisms of regulation of GABAergic synapses in neuroendocrine control regions of the rodent forebrain. J Neuroendocrinol 2012, 24(1):202-214.
65. Peirson S.N., Butler J.N., Foster R.G. Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res 2003, 31(14):e73.
66. 5-receptor-mediated GABAergic transmission and neural signaling in the forebrain of female mice. Neuroscience 2009, 161:526-537.
67. A receptor-mediated synaptic transmission disrupts the firing of gonadotropin releasing hormone neurons in male mice under conditions of steroid abuse. J Neurosci 2010, 30(19):6497-6506.
68. Penatti C.A.A., Oberlander J.G., Davis M.C., Porter D.M., Henderson L.P. Chronic exposure to anabolic androgenic steroids alters activity and synaptic function in neuroendocrine control regions of the female mouse. Neuropharmacology 2011, 61(4):653-664.
69. A receptor expression and function in adolescent mice. Neuroscience 2005, 135(2):533-543.
70. A receptor immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 2000, 101:815-850.
71. Reddy D.S. Neuroendocrine aspects of catamenial epilepsy. Horm Behav 2012, 10.1016/j.yhbeh.2012.04.016.
72. Rusyniak D.E., Zaretsky D.V., Zaretskaia M.V., DiMicco J.A. The role of orexin-1 receptors in physiologic responses evoked by microinjection of PgE2 or muscimol into the medial preoptic area. Neurosci Lett 2011, 498:162-166.
73. A receptors triggers anxiety at puberty. Nat Neurosci 2007, 10(4):469-477.
74. A receptor subunit expression in rat CA1 hippocampus: pharmacological and behavioral effects. Neuropharmacology 2005, 49:573-586.
75. A receptors in shaping learning deficits at puberty in mice. Science 2010, 327:1515-1518.
76. A receptor plasticity. Psychoneuroendocrinology 2009, 34(Suppl. 1):S91-S103.
77. A receptors. Cell Mol Life Sci 2005, 62:119-127.
78. Strömberg J., Haage D., Taube M., Bäckström T., Lundgren P. Neurosteroid modulation of allopregnanolone and GABA effect on the GABA-A receptor. Neuroscience 2006, 143:73-81.
79. Strömberg J., Lundgren P., Taube M., Bäckström T., Wang M., Haage D. The effect of the neuroactive steroid 5β-pregnane-3β, 20(R)-diol on the time course of GABA evoked currents is different to that of pregnenolone sulphate. Eur J Pharmacol 2009, 605:78-86.
80. Tasker J. Coregulation of ion channels by neurosteroids and phosphorylation. Sci STKE 2000, 21(59):p1.
81. Tasker J. Teaching resources. Regulation of GABA receptor activity by neurosteroids and phosphorylation. Sci STKE 2004, 18(234):tr4.
82. A receptors by intimately associated protein kinase C activity underlie compromised synaptic inhibition during status epilepticus. J Neurosci 2008, 28(2):376-384.
83. Vergnano A.M., Schlichter R., Poisbeau P. PKC activation sets an upper limit to the functional plasticity of GABAergic transmission induced by endogenous neurosteroids. Eur J Neurosci 2007, 26:1173-1182.
84. A receptor 2004, 63-75. CRC Press LLC, Boca Raton. S.S. Smith (Ed.).
85. AR phosphorylation in the construction of inhibitory synapses and the efficacy of neuronal inhibition. Biochem Soc Trans 2010, 37(Pt. 6):1355-1358.
86. A receptor trafficking and its role in regulating the plasticity of inhibitory synapses. Physiol Rev 2011, 91(3):1009-1022.
87. Warnock J.K., Swanson S.G., Borel R.W., Zipfel L.M., Brennan J.J., ESTRATEST Clinical Study Group Combined esterified estrogens and methyltestosterone versus esterified estrogens alone in the treatment of loss of sexual interest in surgically menopausal women. Menopause 2005, 12(4):374-384.
88. 4 subunit expression in cultured cerebral cortical neurons. J Neurochem 2011, 116(4):554-563.
89. A receptor stimulation during the oestrous cycle of the rat. Br J Pharmacol 1991, 103(2):1580-1584.
90. Wisden W., Laurie D.J., Monyer H., Seeburg P.H. The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 1992, 12:1040-1062.
91. Wood R.I. Anabolic-androgenic steroid dependence? Insights from animals and humans. Front Neuroendocrinol 2008, 29(4):490-506.
92. Wood R.I., Stanton S.J. Testosterone and sport: current perspectives. Horm Behav 2012, 61:147-155.
93. Wu F.C. Endocrine aspects of anabolic steroid. Clin Chem 1997, 43:1289-1292.
94. A receptors. Neuropharmacology 2002, 43:619-633.
95. A receptors by anabolic androgenic steroids. Neuropharmacology 2005, 49:300-316.
96. Zaretsky D.V., Hunt J.L., Zaretskaia M.V., DiMicco J.A. Microinjection of prostaglandin E2 and muscimol into the preoptic area in conscious rats: comparison of effects on plasma adrenocorticotrophic hormone (ACTH), body temperature, locomotor activity, and cardiovascular function. Neurosci Lett 2006, 397:291-296.