Axonal GABA


Journal

The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262

Informations de publication

Date de publication:
09 2021
Historique:
received: 19 03 2021
accepted: 08 06 2021
pubmed: 27 6 2021
medline: 28 10 2021
entrez: 26 6 2021
Statut: ppublish

Résumé

GABA depolarized sural nerve axons and increased the electrical excitability of C-fibres via GABA GABA

Identifiants

pubmed: 34174096
doi: 10.1113/JP279664
doi:

Substances chimiques

Slc12a2 protein, mouse 0
Solute Carrier Family 12, Member 2 0
Solute Carrier Family 12, Member 3 0
Symporters 0
gamma-Aminobutyric Acid 56-12-2

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4065-4084

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2021 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.

Références

Agarwal N, Offermanns S & Kuner R (2004). Conditional gene deletion in primary nociceptive neurons of trigeminal ganglia and dorsal root ganglia. Genesis 38, 122-129.
Akaike N, Maruyama T, Sikdar SK & Yasui S (1987). Sodium-dependent suppression of gamma-aminobutyric-acid-gated chloride currents in internally perfused frog sensory neurones. J Physiol 392, 543-562.
Alvarez-Leefmans FJ, Gamino SM, Giraldez F & Nogueron I (1988). Intracellular chloride regulation in amphibian dorsal root ganglion neurones studied with ion-selective microelectrodes. J Physiol 406, 225-246.
Ballanyi K & Grafe P (1985). An intracellular analysis of gamma-aminobutyric-acid-associated ion movements in rat sympathetic neurones. J Physiol 365, 41-58.
Bannai H, Levi S, Schweizer C, Inoue T, Launey T, Racine V, Sibarita JB, Mikoshiba K & Triller A (2009). Activity-dependent tuning of inhibitory neurotransmission based on GABAAR diffusion dynamics. Neuron 62, 670-682.
Bardoni R, Takazawa T, Tong CK, Choudhury P, Scherrer G & Macdermott AB (2013). Pre- and postsynaptic inhibitory control in the spinal cord dorsal horn. Ann N Y Acad Sci 1279, 90-96.
Belelli D, Brown AR, Mitchell SJ, Gunn BG, Herd MB, Phillips G, Seifi M, Swinny JD & Lambert JJ (2017). Endogenous neurosteroids influence synaptic GABAA receptors during post-natal development. J Neuroendocrinol 30.
Ben-Ari Y (2002). Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3, 728-739.
Bhisitkul RB, Villa JE & Kocsis JD (1987). Axonal GABA receptors are selectively present on normal and regenerated sensory fibers in rat peripheral nerve. Exp Brain Res 66, 659-663.
Bianchi MT & Macdonald RL (2002). Slow phases of GABA(A) receptor desensitization: structural determinants and possible relevance for synaptic function. J Physiol 544, 3-18.
Bliss TV & Rosenberg ME (1979). Activity-dependent changes in conduction velocity in the olfactory nerve of the tortoise. Pflugers Arch 381, 209-216.
Bogdanov Y, Michels G, Armstrong-Gold C, Haydon PG, Lindstrom J, Pangalos M & Moss SJ (2006). Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts. EMBO J 25, 4381-4389.
Bonalume V, Caffino L, Castelnovo LF, Faroni A, Giavarini F, Liu S, Caruso D, Schmelz M, Fumagalli F, Carr RW & Magnaghi V (2020). Schwann cell autocrine and paracrine regulatory mechanisms, mediated by allopregnanolone and BDNF, modulate PKCepsilon in peripheral sensory neurons. Cells 9, 1874.
Bostock H, Campero M, Serra J & Ochoa J (2003). Velocity recovery cycles of C fibres innervating human skin. J Physiol 553, 649-663.
Brown DA & Marsh S (1978). Axonal GABA-receptors in mammalian peripheral nerve trunks. Brain Res 156, 187-191.
Brumback AC & Staley KJ (2008). Thermodynamic regulation of NKCC1-mediated Cl- cotransport underlies plasticity of GABA(A) signaling in neonatal neurons. J Neurosci 28, 1301-1312.
Carr RW, Sittl R, Fleckenstein J & Grafe P (2010). GABA increases electrical excitability in a subset of human unmyelinated peripheral axons. PLoS One 5, e8780.
Chen JT, Guo D, Campanelli D, Frattini F, Mayer F, Zhou L, Kuner R, Heppenstall PA, Knipper M & Hu J (2014). Presynaptic GABAergic inhibition regulated by BDNF contributes to neuropathic pain induction. Nat Commun 5, 5331.
Colciago A, Bonalume V, Melfi V & Magnaghi V (2020). Genomic and non-genomic action of neurosteroids in the peripheral nervous system. Front Neurosci 14, 796.
De Col R, Messlinger K & Carr RW (2008). Conduction velocity is regulated by sodium channel inactivation in unmyelinated axons innervating the rat cranial meninges. J Physiol 586, 1089-1103.
Dellal SS, Luo R & Otis TS (2012). GABAA receptors increase excitability and conduction velocity of cerebellar parallel fiber axons. J Neurophysiol 107, 2958-2970.
Du X, Hao H, Yang Y, Huang S, Wang C, Gigout S, Ramli R, Li X, Jaworska E, Edwards I, Deuchars J, Yanagawa Y, Qi J, Guan B, Jaffe DB, Zhang H & Gamper N (2017). Local GABAergic signaling within sensory ganglia controls peripheral nociceptive transmission. J Clin Invest 127, 1741-1756.
Faroni A, Melfi S, Castelnovo LF, Bonalume V, Colleoni D, Magni P, Arauzo-Bravo MJ, Reinbold R & Magnaghi V (2019). GABA-B1 receptor-null schwann cells exhibit compromised in vitro myelination. Mol Neurobiol 56, 1461-1474.
Farrant M & Nusser Z (2005). Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6, 215-229.
Funk K, Woitecki A, Franjic-Wurtz C, Gensch T, Mohrlen F & Frings S (2008). Modulation of chloride homeostasis by inflammatory mediators in dorsal root ganglion neurons. Mol Pain 4, 32.
Gao XB & van den Pol AN (2001). GABA, not glutamate, a primary transmitter driving action potentials in developing hypothalamic neurons. J Neurophysiol 85, 425-434.
Gielen MC, Lumb MJ & Smart TG (2012). Benzodiazepines modulate GABAA receptors by regulating the preactivation step after GABA binding. J Neurosci 32, 5707-5715.
Gilbert D, Franjic-Wurtz C, Funk K, Gensch T, Frings S & Mohrlen F (2007). Differential maturation of chloride homeostasis in primary afferent neurons of the somatosensory system. Int J Dev Neurosci 25, 479-489.
Grundy D (2015). Principles and standards for reporting animal experiments in The Journal of Physiology and Experimental Physiology. J Physiol London 593, 2547-2549.
Hanack C, Moroni M, Lima WC, Wende H, Kirchner M, Adelfinger L, Schrenk-Siemens K, Tappe-Theodor A, Wetzel C, Kuich PH, Gassmann M, Roggenkamp D, Bettler B, Lewin GR, Selbach M & Siemens J (2015). GABA blocks pathological but not acute TRPV1 pain signals. Cell 160, 759-770.
Hannan S, Minere M, Harris J, Izquierdo P, Thomas P, Tench B & Smart TG (2019). GABAAR isoform and subunit structural motifs determine synaptic and extrasynaptic receptor localisation. Neuropharmacology, 169, 107540.
Inomata N, Ishihara T & Akaike N (1988). Effects of diuretics on GABA-gated chloride current in frog isolated sensory neurones. Br J Pharmacol 93, 679-683.
Jackson DM, Pollard CE & Roberts SM (1992). The effect of nedocromil sodium on the isolated rabbit vagus nerve. Eur J Pharmacol 221, 175-177.
Kaneko H, Putzier I, Frings S, Kaupp UB & Gensch T (2004). Chloride accumulation in mammalian olfactory sensory neurons. J Neurosci 24, 7931-7938.
Kaneko H, Putzier I, Frings, S. & Gensch, T (2002). Determination of intracellular chloride concentration in dorsal root ganglion neurons by fluorescence lifetime imaging. In Calcium-Activated Chloride Channels, ed. Fuller CM, pp. 167-189.
Kennedy RT, Thompson JE & Vickroy TW (2002). In vivo monitoring of amino acids by direct sampling of brain extracellular fluid at ultralow flow rates and capillary electrophoresis. J Neurosci Methods 114, 39-49.
Lee KY, Charbonnet M & Gold MS (2012). Upregulation of high-affinity GABA(A) receptors in cultured rat dorsal root ganglion neurons. Neuroscience 208, 133-142.
Lerma J, Herranz AS, Herreras O, Abraira V & Martin del Rio R (1986). In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res 384, 145-155.
Lorenzo LE, Godin AG, Wang F, St-Louis M, Carbonetto S, Wiseman PW, Ribeiro-da-Silva A & De Koninck Y (2014). Gephyrin clusters are absent from small diameter primary afferent terminals despite the presence of GABA(A) receptors. J Neurosci 34, 8300-8317.
Lu J, Karadsheh M & Delpire E (1999). Developmental regulation of the neuronal-specific isoform of K-Cl cotransporter KCC2 in postnatal rat brains. J Neurobiol 39, 558-568.
Ma W, Saunders PA, Somogyi R, Poulter MO & Barker JL (1993). Ontogeny of GABAA receptor subunit mRNAs in rat spinal cord and dorsal root ganglia. J Comp Neurol 338, 337-359.
Maddox FN, Valeyev AY, Poth K, Holohean AM, Wood PM, Davidoff RA, Hackman JC & Luetje CW (2004). GABAA receptor subunit mRNA expression in cultured embryonic and adult human dorsal root ganglion neurons. Brain Res Dev Brain Res 149, 143-151.
Meera P, Wallner M & Otis TS (2011). Molecular basis for the high THIP/gaboxadol sensitivity of extrasynaptic GABA(A) receptors. J Neurophysiol 106, 2057-2064.
Milanese M, Tardito D, Musazzi L, Treccani G, Mallei A, Bonifacino T, Gabriel C, Mocaer E, Racagni G, Popoli M & Bonanno G (2013). Chronic treatment with agomelatine or venlafaxine reduces depolarization-evoked glutamate release from hippocampal synaptosomes. BMC Neurosci 14, 75.
Mitchell EA, Herd MB, Gunn BG, Lambert JJ & Belelli D (2008). Neurosteroid modulation of GABAA receptors: molecular determinants and significance in health and disease. Neurochem Int 52, 588-595.
Moalem G, Grafe P & Tracey DJ (2005). Chemical mediators enhance the excitability of unmyelinated sensory axons in normal and injured peripheral nerve of the rat. Neuroscience 134, 1399-1411.
Orefice LL, Zimmerman AL, Chirila AM, Sleboda SJ, Head JP & Ginty DD (2016). Peripheral mechanosensory neuron dysfunction underlies tactile and behavioral deficits in mouse models of ASDs. Cell 166, 299-313.
Pfaffl MW (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, 45e.
Price TJ, Cervero F, Gold MS, Hammond DL & Prescott SA (2009). Chloride regulation in the pain pathway. Brain Res Rev 60, 149-170.
Pugh JR & Jahr CE (2011). Axonal GABAA receptors increase cerebellar granule cell excitability and synaptic activity. J Neurosci 31, 565-574.
Rang HP & Ritchie JM (1968). On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations. J Physiol 196, 183-221.
Rivera C, Voipio J & Kaila K (2005). Two developmental switches in GABAergic signalling: the K+-Cl- cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol 562, 27-36.
Rocha-Gonzalez HI, Mao S & Alvarez-Leefmans FJ. (2008). Na+,K+,2Cl− cotransport and intracellular chloride regulation in rat primary sensory neurons: thermodynamic and kinetic aspects. J Neurophysiol 100, 169-184.
Rudomin P & Schmidt RF (1999). Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 129, 1-37.
Ruiz A, Campanac E, Scott RS, Rusakov DA & Kullmann DM (2010). Presynaptic GABAA receptors enhance transmission and LTP induction at hippocampal mossy fiber synapses. Nat Neurosci 13, 431-438.
Ruiz A, Fabian-Fine R, Scott R, Walker MC, Rusakov DA & Kullmann DM (2003). GABAA receptors at hippocampal mossy fibers. Neuron 39, 961-973.
Sassoe-Pognetto M, Frola E, Pregno G, Briatore F & Patrizi A (2011). Understanding the molecular diversity of GABAergic synapses. Front Cell Neurosci 5, 4.
Schobel N, Radtke D, Lubbert M, Gisselmann G, Lehmann R, Cichy A, Schreiner BS, Altmuller J, Spector AC, Spehr J, Hatt H & Wetzel CH (2012). Trigeminal ganglion neurons of mice show intracellular chloride accumulation and chloride-dependent amplification of capsaicin-induced responses. PLoS One 7, e48005.
Staley K, Smith R, Schaack J, Wilcox C & Jentsch TJ (1996). Alteration of GABAA receptor function following gene transfer of the CLC-2 chloride channel. Neuron 17, 543-551.
Staley KJ & Proctor WR (1999). Modulation of mammalian dendritic GABA(A) receptor function by the kinetics of Cl- and HCO3- transport. J Physiol 519 693-712.
Steen KH, Reeh PW, Anton F & Handwerker HO (1992). Protons selectively induce lasting excitation and sensitization to mechanical stimulation of nociceptors in rat skin, in vitro. J Neurosci 12, 86-95.
Sung KW, Kirby M, McDonald MP, Lovinger DM & Delpire E (2000). Abnormal GABAA receptor-mediated currents in dorsal root ganglion neurons isolated from Na-K-2Cl cotransporter null mice. J Neurosci 20, 7531-7538.
Thomas P, Mortensen M, Hosie AM & Smart TG (2005). Dynamic mobility of functional GABAA receptors at inhibitory synapses. Nat Neurosci 8, 889-897.
Tigerholm J, Petersson ME, Obreja O, Eberhardt E, Namer B, Weidner C, Lampert A, Carr RW, Schmelz M & Fransen E (2015). C-fiber recovery cycle supernormality depends on ion concentration and ion channel permeability. Biophys J 108, 1057-1071.
Tossman U, Jonsson G & Ungerstedt U (1986). Regional distribution and extracellular levels of amino acids in rat central nervous system. Acta Physiol Scand 127, 533-545.
Toyoda H, Yamada J, Ueno S, Okabe A, Kato H, Sato K, Hashimoto K & Fukuda A (2005). Differential functional expression of cation-Cl- cotransporter mRNAs (KCC1, KCC2, and NKCC1) in rat trigeminal nervous system. Brain Res Mol Brain Res 133, 12-18.
Tretter V, Jacob TC, Mukherjee J, Fritschy JM, Pangalos MN & Moss SJ (2008). The clustering of GABA(A) receptor subtypes at inhibitory synapses is facilitated via the direct binding of receptor alpha 2 subunits to gephyrin. J Neurosci 28, 1356-1365.
Zeilhofer HU, Wildner H & Yevenes GE (2012). Fast synaptic inhibition in spinal sensory processing and pain control. Physiol Rev 92, 193-235.
Zhang XL, Lee KY, Priest BT, Belfer I & Gold MS (2015). Inflammatory mediator-induced modulation of GABAA currents in human sensory neurons. Neuroscience 310, 401-409.
Zimmerman AL, Kovatsis EM, Pozsgai RY, Tasnim A, Zhang Q & Ginty DD (2019). Distinct modes of presynaptic inhibition of cutaneous afferents and their functions in behavior. Neuron 102, 420-434.e8.
Zurborg S, Piszczek A, Martinez C, Hublitz P, Al Banchaabouchi M, Moreira P, Perlas E & Heppenstall PA (2011). Generation and characterization of an Advillin-Cre driver mouse line. Mol Pain 7, 66.

Auteurs

Veronica Bonalume (V)

Department of Pharmacological and Biomolecular Sciences, Università degli Studi di Milano, Milan, Italy.

Lucia Caffino (L)

Department of Pharmacological and Biomolecular Sciences, Università degli Studi di Milano, Milan, Italy.

Luca F Castelnovo (LF)

Department of Pharmacological and Biomolecular Sciences, Università degli Studi di Milano, Milan, Italy.
Marine Science Institute, University of Texas at Austin, Port Aransas, TX, USA.

Alessandro Faroni (A)

Blond McIndoe Laboratories, Division of Cell Matrix Biology and Regenerative Medicine, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, UK.

Sheng Liu (S)

Institute of Pharmacology, Heidelberg University, Mannheim, Germany.

Jing Hu (J)

Institute of Pharmacology, Heidelberg University, Mannheim, Germany.

Marco Milanese (M)

Department of Pharmacy (DIFAR), Pharmacology and Toxicology Unit, Università degli Studi di Genova, Genova, Italy.

Giambattista Bonanno (G)

Department of Pharmacy (DIFAR), Pharmacology and Toxicology Unit, Università degli Studi di Genova, Genova, Italy.
Ospedale Policlinico San Martino, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Genova, Italy.

Kyra Sohns (K)

Experimental Pain Research, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Tal Hoffmann (T)

Institute for Physiology and Pathophysiology, Friedrich-Alexander University, Erlangen, Germany.

Roberto De Col (R)

Experimental Pain Research, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Martin Schmelz (M)

Experimental Pain Research, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Fabio Fumagalli (F)

Department of Pharmacological and Biomolecular Sciences, Università degli Studi di Milano, Milan, Italy.

Valerio Magnaghi (V)

Department of Pharmacological and Biomolecular Sciences, Università degli Studi di Milano, Milan, Italy.

Richard Carr (R)

Experimental Pain Research, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

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