GABA receptor-mediated effects in the peripheral nervous system: A cross-interaction with neuroactive steroids

Journal of Molecular Neuroscience

Volumn 28, Issue 1, 2006, Pages 89-102

  Magnaghi, Valerio ^a   Ballabio, Marinella ^a   Consoli, Antonio ^a   Lambert, Jeremy J ^b   Roglio, Ilaria ^a   Melcangi, Roberto C ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Allopregnanolone; GABAA receptor; GABAB receptor; Myelin; Peripheral nervous system; Progesterone; Schwann cell

Indexed keywords

20ALPHA DIHYDROPROGESTERONE; 3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; BACLOFEN; BARBITURIC ACID DERIVATIVE; BICUCULLINE; CHLORDIAZEPOXIDE; DYDROGESTERONE; ESTRADIOL; GLYCOPROTEIN P; MIFEPRISTONE; MUSCIMOL; NEUROSTEROID; PERIPHERAL MYELIN PROTEIN 22; PICROTOXIN; PREGNENOLONE; PROGESTERONE; PROGESTERONE DERIVATIVE; PROTEIN SUBUNIT; STEROID;

BRAIN FUNCTION; BRAIN REGION; GABAERGIC SYSTEM; GLIA CELL; HORMONE SYNTHESIS; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MYELINATION; NERVE CELL DIFFERENTIATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL NERVOUS SYSTEM; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REVIEW; SCHWANN CELL; SCIATIC NERVE;

ANIMALS; LIGANDS; PERIPHERAL NERVOUS SYSTEM; PROTEIN SUBUNITS; RECEPTORS, GABA-A; RECEPTORS, GABA-B; SCHWANN CELLS; STEROIDS;

MAMMALIA;

EID: 33646866348     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1385/JMN:28:1:89     Document Type: Review

References (101)

1. Al-Dahan M. I. and Thalmann R. H. (1996) Progesterone regulates gamma-aminobutyric acid B (GABA-B) receptors in the neocortex of female rats. Brain Res. 727, 40-48.
2. Barbaccia M. L., Colombo G., Affricano D., Carai M. A., Vacca G., Melis S., et al. (2002) GABA(B) receptor-mediated increase of neurosteroids by gamma-hydroxybutyric acid. Neuropharmacology 42, 782-791.
3. Barres B. A., Koroshetz W. J., Swartz K. J., Chun L. L., and CoreyD. P. (1990) Ion channel expression by white matter glia: the O-2A glial progenitor cell. Neuron 4, 507-524.
4. Belelli D. and Lambert J. J. (2005) Neurosteroids: endogenous regulators of the GABA-A receptor. Nat. Rev. Neurosci. 6, 565-575.
5. Ben Ari Y. (2002) Excitatory actions of GABA during development the nature of the nurture. Nat. Rev. Neurosci. 3, 728-739.
6. Berger T., Walz W., Schnitzer J., and Kettenmann H. (1992) GABA- and glutamate-activated currents in glial cells of the mouse corpus callosum slice. J. Neurosci. Res. 31, 21-27.
7. Bettler B., Kaupmann K., Mosbacher J., and Gassmann M. (2004) Molecular structure and physiological functions of GABA(B) receptors. Physiol. Rev. 84, 835-867.
8. Bhisitkul R. B., Villa J. E., and Kocsis J. D. (1987) Axonal GABA receptors are selectively present on normal and regenerated sensory fibers in rat peripheral nerve. Exp. Brain Res. 66, 659-663.
9. Bovolin P., Santi M. R., Puia G., Costa E., and Grayson D. (1992) Expression patterns of gamma-aminobutyric acid type A receptor subunit mRNAs in primary cultures of granule neurons and astrocytes from neonatal rat cerebella. Proc. Natl. Acad. Sci. U. S. A. 89, 9344-9348.
10. B receptors: first of the functional metabotropic heterodimers. J. Pharmacol. Exp. Ther. 292, 2-7.
11. Bowery N. G., Doble A., Hill D. R., Hudson A. L., Shaw J. S., Turnbull M. J., and Warrington R. (1981) Bicuculline-insensitive GABA receptors on peripheral autonomic nerve terminals. Eur. J. Pharmacol. 71, 53-70.
12. Bowery N., Enna S. J., and Olsen R. W. (2004) Six decades of GABA. Biochem. Pharmacol. 68, 1477-1478.
13. Bowery N. G., Hill D. R., Hudson A. L., Doble A., Middlemiss D. N., Shaw J., and Turnbull M. (1980) (-)Baclofen decreases neurotransmitter release in the mammalian CNS by an action at a novel GABA receptor. Nature 283, 92-94.
14. Bronstein J. M. (2000) Function of tetraspan proteins in the myelin sheath. Curr. Opin. Neurobiol. 10, 552-557.
15. Brown D. A. and Marsh S. (1978) Axonal GABA-receptors in mammalian peripheral nerve trunks. Brain Res. 156, 187-191.
16. Brown D. A., Adams P. R., Higgins A. J., and Marsh S. (1979) Distribution of GABA-receptors and GABA-carriers in the mammalian nervous system. J. Physiol. (Paris) 75, 667-671.
17. Callachan H., Cottrell G. A., Hather N. Y., Lambert J. J., Nooney J. M., and Peters J. A. (1987) Modulation of the GABA-A receptor by progesterone metabolites. Proc. R. Soc. Lond. B. Biol. Sci. 231, 359-369.
18. B2 receptor subunits in the CNS differs from that in peripheral tissues. Neuroscience 100, 155-170.
19. Calver A. R., Robbins M. J., Cosio G., Rice S. Q., Babbs A. J. Hirst W. D., et al. (2001) The C-terminal domains of the GABA-B receptor subunits mediate intracellular trafficking but are not required for receptor signalling. J. Neurosci. 21, 1203-1210.
20. B receptor subunit expression in glia. Mol. Cell. Neurosci. 24, 214-223.
21. B2 subunits in rat brain, spinal cord and dorsal root ganglion. Neuroscience 106, 447-467.
22. B receptor gb2 in rat CNS. Brain Res. 860, 41-52.
23. Concas A., Mostallino M. C., Porcu P., Follesa P., Barbaccia M. L., Trabucchi M., et al. (1998) Role of brain allopregnanolone in the plasticità of γ-aminobutyric acid type A receptor in rat brain during pregnancy and after delivery. Proc. Natl. Acad. Sci. U. S. A. 95, 13284-13289.
24. Desarmenien M., Feltz P., Occhipinti G., Santangelo F., and Schlichter R. (1984) Coexistence of GABA-A and GABA-B receptors on A delta and C primary afferents. Br. J. Pharmacol. 81, 327-333.
25. Deschennes M., Feltz P., and Lamour Y. (1976) A model for an estimate in vivo of the ionic basis of presynaptic inhibition: an intracellular analysis of the GABA-induced depolarization in rat dorsal root ganglia. Brain Res. 118, 486-493.
26. Do-Rego J. L., Mensah-Nyagan G. A., Beaujean D., Vaudry D., Sieghart W., Luu-The V., et al. (2000) γ-Aminobutyric acid, acting through γ-aminobutyric acid type A receptors, inhibits the biosynthesis of neurosteroids in the frog hypothalamus. Proc. Natl. Acad. Sci. U. S. A. 97, 13925-13930.
27. Farrant M. and Nusser Z. (2005) Variation of an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat. Rev. Neurosci. 6, 215-229.
28. Frye C. A., Duncan J. E., Basham M., and Erkine M. S. (1996a) Behavioral effects of 3alpha-androstanediol. II: hypothalamic and preoptic area actions via a GABAergic mechanism. Behav. Brain Res. 79, 119-130.
29. Frye C. A., Van Keuren K. R., and Erkine M. S. (1996b) Behavioral effects of 3alpha-androstanediol. I: modulation of sexual receptivity and promotion of GABA-stimulated chloride flux. Behav. Brain Res. 79, 109-118.
30. + progenitor proliferation, J. Neurosci. Res. 78, 770-783.
31. Galanopoulou A. S., Kyrozis A., Claudio O. I., Stanton P. K., and Moshe S. L. (2003) Sex-specific KCC2 expression and GABA(A) receptor function in rat substantia nigra. Exp. Neurol. 183, 628-637.
32. Gallagher J. P., Higashi H., and Nishi S. (1978) Characterization and ionic basis of GABA-induced depolarization recorded in vitro from cat primary afferent neurons. J. Physiol. (Lond.) 275, 263-282.
33. Gavrilovic J., Raff M., and Cohen J. (1984) GABA uptake by purified rat Schwann cells in culture. Brain Res. 303, 183-185.
34. Gilbert P., Kettenmann H., and Schachner M. (1984) Gamma-aminobutyric acid directly depolarizes cultured oligodendrocytes. J. Neurosci. 4, 561-569.
35. Guarneri P., Guarneri R., Cascio C., Piccoli F., and Papadopoulos V. (1995) γ-Aminobutyric acid type A/benzodiazepine receptors regulate rat retina neurosteroidogenesis. Brain Res. 683, 65-72.
36. Hosli E., Otten U., and Hosli L. (1997) Expression of GABA(A) receptors by reactive astrocytes in explant and primary cultures of rat CNS. Int. J. Dev. Neurosci. 15, 949-960.
37. B(2) receptor proteins in the rat cerebellum. Mol. Brain Res. 83, 72-80.
38. Inoue M. and Akaike N. (1988) Blockade of γ-aminobutyric acid-gated chloride current in frog sensory neurons by picrotoxin. Neurosci. Res. 5, 380-394.
39. B receptor. Biochem. Biophys. Res. Commun. 253, 10-15.
40. Israel J. M., Schipke C. G, Ohlemeyer C., Theodosis D. T., and Kettenmann H. (2003) GABAA receptor-expressing astrocytes in the supraoptic nucleus lack glutamate uptake and receptor currents. Glia 44, 102-110.
41. BR2. Nature 396, 674-679.
42. Jow F, Chiu D., Lim H. K., Novak T., and Lin S. (2004) Production of GABA by cultured hippocampal glial cells. Neurochem. Int. 45, 273-283.
43. Kang J., Jiang L., Goldman S. A., and Nedergaard M. (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat. Neurosci. 1, 683-692.
44. B receptors uncovers similarity to metabotropic glutamate receptors. Nature 386, 239-246.
45. B-receptor subtypes assemble into functional heteromeric complexes. Nature 396, 683-687.
46. Keller A. F., Breton J. D., Schlichter R., and Poisbeau P. (2004) Production of 5alpha-reduced neurosteroids is developmentally regulated and shapes GABA(A) miniature IPSCs in lamina II of the spinal cord. J. Neurosci. 24, 907-915.
47. Kelly M. J., Oiu J., Wagner E. J., and and Ronnekliev O. K. (2003) Rapid effects of estrogen on G protein-coupled receptor activation of potassium channels in the central nervous system (CNS). J. Steroid Biochem. Mol. Biol. 83, 187-193.
48. Kettenmann H., Gilbert P., and Schnachner M. (1984) Depolarization of cultured oligodendrocytes by glutamate and GABA. Neuroci. Lett. 47, 271-276.
49. i increase in murine precursor cells of the oligodendrocyte lineage. Eur. J. Neurosci. 4, 1049-1058.
50. B receptor function. Science 283, 74-77.
51. Kunkel D. D., Hendrickson A. E., Wu J.-Y., and Schwartzkroin P. A. (1986) Glutamic acid decarboxylase (GAD) immunocytochemistry of developing rabbit hippocampus. J. Neurosci. 6, 541-552.
52. Lambert J. J., Belelli D., Peden E., Vardy A. W., and Peters J. A. (2003) Neurosteroid modulation of GABA-A receptors. Prog. Neurobiol. 71, 67-80.
53. LeBlanc A. C., Windebank A. J., and Poduslo J. F. (1992) Po gene expression in Schwann cells is modulated by an increase of cAMP which is dependent on the presence of axons. Mol. Brain Res. 12, 31-38.
54. Lee M. M., Badache A., and DeVries G. H. (1999) Phosphorylation of CREB in axon-induced Schwann cell proliferation. J. Neurosci. Res. 55, 702-712.
55. Liske S. and Morris M. E. (1994) Extrasynaptic effects of GABA (gamma-aminobutyric acid) agonists on myelinated axons of peripheral nerve. Can. J. Physiol. Pharmacol. 72, 368-374.
56. Liu Q. Y., Schaffner A. E., Chang Y. H., Maric D., and Barker J. L. (2000) Persistent activation of GABA(A) receptor/Cl- channels by astrocyted-derived GABA in cultured embryonic rat hippocampal neurons. J. Neurophysiol. 84, 1392-1403.
57. B receptors in Schwann cells influence proliferation and myelin protein expression. Eur. J. Neurosci. 19, 2641-2649.
58. Magnaghi V., Ballabio M., Gonzalez L. C., Leonelli E., Motta M., and Melcangi R. C. (2004b) The synthesis of glycoprotein Po and peripheral myelin protein 22 in sciatic nerve of male rats is modulated by testosterone metabolites. Mol. Brain Res. 126, 67-73.
59. Magnaghi V., Cavarretta I., Galbiati M., Martini L., and Melcangi R. C. (2001) Neuroactive steroids and peripheral myelin proteins. Brain Res. Rev. 37, 360-371.
60. Maguire J. L., Stell B. M., Rafizadeh M., and Mody I. (2005) Ovarian cycle-linked changes in GABA-A receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat. Rev. Neurosci. 8, 797-804.
61. Majewska M. D., Harrison N. L., Schwartz R. D., Barker J. L., and Paul S.M. (1986) Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232, 1004-1007.
62. Mantelas A., Stamatakis A., Kazanis I., Philippidis H., and Stylianopoulou F. (2003) Control of neuronal nitric oxide synthase and brain-derived neurotrophic factor levels by GABA-A receptors in the developing rat cortex. Dev. Brain Res. 145, 185-195.
63. B receptors in the rat central nervous system. J. Comp. Neurol. 405, 299-321.
64. B receptors - the first 7TM heterodimers. Trends Pharmacol. Sci. 20, 396-399.
65. McCarthy M. M., Amateau S. K., and Mong J. A. (2002) Steroid modulation of astrocytes in the neonatal brain: implications for adult reproductive function. Biol. Reprod. 67, 691-698.
66. Melcangi R. C., Azcoitia I., Ballabio M., Cavarretta I., Gonzalez L. C., Leonelli E., et al. (2003) Neuroactive steroids influence peripheral myelination: a promising opportunity for preventing or treating age-dependent disfunctions of peripheral nerves. Prog. Neurobiol. 71, 57-66.
67. Melcangi R. C., Cavarretta I. T. R., Ballabio M., Leonelli E., Schenone A., Azcoitia I., et al. (2005) Peripheral nerves: a target for the action of neuroactive steroids. Brain Res. Rev. 48, 328-338.
68. Melcangi R. C., Magnaghi V., Cavarretta I., Zucchi I., Bovolin P., D'Urso D., and Martini L. (1999) Progesterone derivatives are able to influence peripheral myelin protein 22 and Po gene expression: possible mechanisms of action. J. Neurosi. Res. 56, 349-357.
69. Melcangi R. C., Magnaghi V., Galbiati M., Ghelarducci B., Sebastiani L., and Martini L. (2000a) The action of steroid hormones on peripheral myelin proteins: a possible new tool for the rebuilding of myelin? J. Neurocytol. 29, 327-339.
70. Melcangi R. C., Magnaghi V., and Martini L. (2000b) Aging in peripheral nerves: regulation of myelin protein genes by steroid hormones. Prog. Neurobiol. 60, 291-308.
71. Mensah-Nyagan A. G., Do-Rego J. L., Beaujean D., Luuthe V., Pelletier G., and Vaudry H. (2001) Regulation of neurosteroi biosyntheis in the frog diencephalons by GABA and endozepines Horm. Behav. 40, 218-225.
72. Mirsky R. and Jessen K. R. (1999) The neurobiology of Schwann cells. Brain Pathol. 19, 293-311.
73. Mirsky R., Parkinson D. B., Dong Z., Meier C., Calle E., Brennan A., et al. (2001) Regulation of genes involved in Schwann cell development and differentiation. Prog. Brain Res. 132, 3-12.
74. Morris M. E., Di Costanzo G. A., Fox S., and Werman R. (1983) Depolarizing action of GABA (γ-aminobutyric acid) on myelinated fibers of peripheral nerves. Brain Res. 278, 117-126.
75. Naef R. and Suter U. (1998) Many facets of the peripheral myelin protein PMP22 in myelination and disease. Microsc. Res. Tech. 41, 359-371.
76. B receptor activity. J. Biol. Chem. 274, 7607-7610.
77. Obrietan K., Gao X. B., and Van Den Pol A. N. (2002) Excitatory actions of GABA increase BDNF expression via a MAPK-CREB-dependent mechanism; a positive feedback circuit in developing neurons. J. Neurophysiol. 88, 1005-1015.
78. 3H]bicuculline methochloride. Eur. J. Pharmacol. 99, 247-248.
79. Owens D. F. and Kriegstein A. R. (2002) Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 3, 715-727.
80. Park-Chung M., Malayev A., Purdy R. H., Gibbs T. T., and Farb D. H. (1999) Sulfated and unsulfated steroids modulate gamma-aminobutyric acid A receptor function through distinct sites. Brain Res. 830, 72-87.
81. BR1 receptor. Eur. J. Neurosci. 11, 2874-2882.
82. A receptors. Neuron 4, 759-765.
83. Quarles R. H. (1997) Glycoproteins of myelin sheaths. J. Mol. Neurosci. 8, 1-12.
84. Reddy D. S. (2003) Pharmacology of endogenous neuroactive steroids. Crit. Rev. Neurobiol. 15, 197-234.
85. Rupprecht R. and Holsboer F. (1999) Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives. Trends Neurosci. 22, 410-416.
86. B1 subunit null mice. Auton. Autacoid. Pharmacol. 22, 147-154.
87. Sanna E., Talani G., Busonero F., Pisu M. G., Purdy R. H., Serra M., and Biggio G. (2004) Brain steroidogenesis mediates ethanol modulation of GABA-A receptor activity in rat hippocampus. J. Neurosci. 24, 6521-6530.
88. Semyanov A., Walker M. C., and Kullmann D. M. (2003) GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat. Neurosci. 6, 484-490.
89. Shu H.-J., Eisenman L. N., Jinadasa D., Covey D.F., Zorumski C. F., and Mennerick S. (2004) Slow actions of neuroactive steroids at GABA-A receptors. J. Neurosci. 24, 6667-6675.
90. Sieghart W. and Sperk G. (2002) Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr. Top. Med. Chem. 2, 795-816.
91. Steiger J. L., Bandyopadhyay S., Farb D. H., and Russek S. J. (2004) cAMP response element-binding brotein, activating transcription factor-4, and upstream stimulatory factor differentially control hippocampal GABA-BR1a and GABA-BR1b subunit gene expression through alternative promoters. J. Neurosci. 24, 6115-6124.
92. Sun B. B. and Chiu S. Y. (1999) N-type calcium channels and their regulation by GABA-B receptors in axons of neonatal rat optic nerve. J. Neurosci. 19, 5185-5194.
93. Thalmann R. H. and Tehrani M. H. J. (2000) Regulation of neocortical GABA-B receptor subunits by RU486 and progesterone. Soc. Neurosci. Abs. 8127.
94. B receptor protein and mRNA distribution in rat spinal cord and dorsal root ganglia. Eur. J. Neurosci. 12, 3201-3210.
95. Valeyev A. Y., Hackman J. C., Holohean A. M., Wood P. M., Katz J. L., and Davidoff R. A. (1999) GABA-induced Cl- current in cultured embryonic human dorsal root ganglion neurons. J. Neurophysiol. 82, 1-9.
96. B receptor. Nature 396, 679-682.
97. Whiting P. J., McAllister G., Vasilatis D., Bonnert T. P., Heavens R. P., Smith D.W., et al. (1997) Neuronally restricted splicing regulates the expression of a novel GABAA receptor subunit conferring atypical functional properties. J. Neurosci. 17, 5027-5037.
98. A receptor subtypes. Int. Rev. Neurobiol. 38, 95-138.
99. Wu F. S., Gibbs T. T., and Farb D. H. (1991) Pregnenolone sulfate: a positive allosteric modulator at the N-methyl-D-aspartate receptor. Mol. Pharmacol. 40, 333-336.
100. Yu R., Follesa P., and Ticku M. K. (1996) Down-regulation of the GABA receptor subunits mRNA levels in mammalian cultured cortical neurons following chronic neurosteroid treatment. Mol. Brain Res. 41, 163-168.
101. Zagorodnyuk V. P., D'Antona G., Brookes S. J., and Costa M. (2002) Functional GABA-B receptors are present in guinea pig nodose ganglion cell bodies but not in peripheral mechanosensitive endings. Auton. Neurosci. 29, 20-29.