New insights into the therapeutic potential of Girk channels

Trends in Neurosciences

Volumn 37, Issue 1, 2014, Pages 20-29

  Luján, Rafael ^a   Marron Fernandez de Velasco, Ezequiel ^b   Aguado, Carolina ^a   Wickman, Kevin ^b  

^a Universidad Castilla La Mancha   (Spain)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; G PROTEIN COUPLED RECEPTOR; RGS PROTEIN; SORTING NEXIN; SORTING NEXIN 27; UNCLASSIFIED DRUG;

DRUG ABUSE; HUMAN; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; ADDICTION; BRAIN; METABOLISM; NERVE CELL PLASTICITY; PHYSIOLOGY;

BRAIN; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; HUMANS; NEURONAL PLASTICITY; SUBSTANCE-RELATED DISORDERS;

EID: 84891356685     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2013.10.006     Document Type: Review

References (125)

1. Luscher C., Slesinger P.A. Emerging roles for G protein-gated inwardly rectifying potassium (GIRK) channels in health and disease. Nat. Rev. Neurosci. 2010, 11:301-315.
2. Hibino H., et al. Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol. Rev. 2010, 90:291-366.
3. Wei J., et al. Characterization of murine Girk2 transcript isoforms: structure and differential expression. Genomics 1998, 51:379-390.
4. Zhu L., et al. Cloning and characterization of G protein-gated inward rectifier K+ channel (GIRK1) isoforms from heart and brain. J. Mol. Neurosci. 2001, 16:21-32.
5. Krapivinsky G., et al. The G-protein-gated atrial K+ channel IKACh is a heteromultimer of two inwardly rectifying K+-channel proteins. Nature 1995, 374:135-141.
6. Kennedy M.E., et al. GIRK4 confers appropriate processing and cell surface localization to G-protein-gated potassium channels. J. Biol. Chem. 1999, 274:2571-2582.
7. Ma D., et al. Diverse trafficking patterns due to multiple traffic motifs in G protein-activated inwardly rectifying potassium channels from brain and heart. Neuron 2002, 33:715-729.
8. Chan K.W., et al. Control of channel activity through a unique amino acid residue of a G protein-gated inwardly rectifying K+ channel subunit. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:14193-14198.
9. Karschin C., et al. IRK(1-3) and GIRK(1-4) inwardly rectifying K+ channel mRNAs are differentially expressed in the adult rat brain. J. Neurosci. 1996, 16:3559-3570.
10. Fernandez-Alacid L., et al. Developmental regulation of G protein-gated inwardly-rectifying K+ (GIRK/Kir3) channel subunits in the brain. Eur. J. Neurosci. 2011, 34:1724-1736.
11. Nishida M., MacKinnon R. Structural basis of inward rectification: cytoplasmic pore of the G protein-gated inward rectifier GIRK1 at 1.8A resolution. Cell 2002, 111:957-965.
12. Inanobe A., et al. Structural diversity in the cytoplasmic region of G protein-gated inward rectifier K+ channels. Channels 2007, 1:39-45.
13. Nishida M., et al. Crystal structure of a Kir3.1-prokaryotic Kir channel chimera. EMBO J. 2007, 26:4005-4015.
14. Inanobe A., et al. A structural determinant for the control of PIP2 sensitivity in G protein-gated inward rectifier K+ channels. J. Biol. Chem. 2010, 285:38517-38523.
15. Whorton M.R., MacKinnon R. Crystal structure of the mammalian GIRK2 K+ channel and gating regulation by G proteins, PIP2, and sodium. Cell 2011, 147:199-208.
16. Whorton M.R., MacKinnon R. X-ray structure of the mammalian GIRK2-betagamma G-protein complex. Nature 2013, 498:190-197.
17. Liao Y.J., et al. Heteromultimerization of G-protein-gated inwardly rectifying K+ channel proteins GIRK1 and GIRK2 and their altered expression in weaver brain. J. Neurosci. 1996, 16:7137-7150.
18. Slesinger P.A., et al. Identification of structural elements involved in G protein gating of the GIRK1 potassium channel. Neuron 1995, 15:1145-1156.
19. Chan K.W., et al. Specific regions of heteromeric subunits involved in enhancement of G protein-gated K+ channel activity. J. Biol. Chem. 1997, 272:6548-6555.
20. Wydeven N., et al. Structural elements in the Girk1 subunit that potentiate G protein-gated potassium channel activity. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:21492-21497.
21. Medina I., et al. A switch mechanism for G beta gamma activation of I(KACh). J. Biol. Chem. 2000, 275:29709-29716.
22. Ivanina T., et al. Mapping the Gbetagamma-binding sites in GIRK1 and GIRK2 subunits of the G protein-activated K+ channel. J. Biol. Chem. 2003, 278:29174-29183.
23. Thomas A.M., et al. Differential phosphoinositide binding to components of the G protein-gated K+ channel. J. Membr. Biol. 2006, 211:43-53.
24. Rusinova R., et al. Mass spectrometric analysis reveals a functionally important PKA phosphorylation site in a Kir3 channel subunit. Pflugers Arch. 2009, 458:303-314.
25. Rubinstein M., et al. Divergent regulation of GIRK1 and GIRK2 subunits of the neuronal G protein gated K+ channel by GalphaiGDP and Gbetagamma. J. Physiol. 2009, 587:3473-3491.
26. Berlin S., et al. G alpha(i) and G betagamma jointly regulate the conformations of a G betagamma effector, the neuronal G protein-activated K+ channel (GIRK). J. Biol. Chem. 2010, 285:6179-6185.
27. Cruz H.G., et al. Bi-directional effects of GABA(B) receptor agonists on the mesolimbic dopamine system. Nat. Neurosci. 2004, 7:153-159.
28. Labouebe G., et al. RGS2 modulates coupling between GABAB receptors and GIRK channels in dopamine neurons of the ventral tegmental area. Nat. Neurosci. 2007, 10:1559-1568.
29. Jelacic T.M., et al. Functional and biochemical evidence for G-protein-gated inwardly rectifying K+ (GIRK) channels composed of GIRK2 and GIRK3. J. Biol. Chem. 2000, 275:36211-36216.
30. Lunn M.L., et al. A unique sorting nexin regulates trafficking of potassium channels via a PDZ domain interaction. Nat. Neurosci. 2007, 10:1249-1259.
31. Doupnik C.A. GPCR-Kir channel signaling complexes: defining rules of engagement. J. Recept. Signal Transduct. Res. 2008, 28:83-91.
32. Huang C.L., et al. Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gbetagamma. Nature 1998, 391:803-806.
33. Sui J.L., et al. Activation of the atrial KACh channel by the betagamma subunits of G proteins or intracellular Na+ ions depends on the presence of phosphatidylinositol phosphates. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:1307-1312.
34. Yokogawa M., et al. NMR analyses of the Gbetagamma binding and conformational rearrangements of the cytoplasmic pore of G protein-activated inwardly rectifying potassium channel 1 (GIRK1). J. Biol. Chem. 2011, 286:2215-2223.
35. Huang C.L., et al. Evidence that direct binding of G beta gamma to the GIRK1 G protein-gated inwardly rectifying K+ channel is important for channel activation. Neuron 1995, 15:1133-1143.
36. Clancy S.M., et al. Pertussis-toxin-sensitive Galpha subunits selectively bind to C-terminal domain of neuronal GIRK channels: evidence for a heterotrimeric G-protein-channel complex. Mol. Cell. Neurosci. 2005, 28:375-389.
37. Rebois R.V., et al. Heterotrimeric G proteins form stable complexes with adenylyl cyclase and Kir3.1 channels in living cells. J. Cell Sci. 2006, 119:2807-2818.
38. Mase Y., et al. Structural basis for modulation of gating property of G protein-gated inwardly rectifying potassium ion channel (GIRK) by i/o-family G protein alpha subunit (Galphai/o). J. Biol. Chem. 2012, 287:19537-19549.
39. Peleg S., et al. G(alpha)(i) controls the gating of the G protein-activated K+ channel, GIRK. Neuron 2002, 33:87-99.
40. Rubinstein M., et al. Galphai3 primes the G protein-activated K+ channels for activation by coexpressed Gbetagamma in intact Xenopus oocytes. J. Physiol. 2007, 581:17-32.
41. Rusinova R., et al. Specificity of Gbetagamma signaling to Kir3 channels depends on the helical domain of pertussis toxin-sensitive Galpha subunits. J. Biol. Chem. 2007, 282:34019-34030.
42. Nobles M., et al. Heterotrimeric G proteins precouple with G protein-coupled receptors in living cells. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:18706-18711.
43. Ciruela F., et al. Evidence for oligomerization between GABAB receptors and GIRK channels containing the GIRK1 and GIRK3 subunits. Eur. J. Neurosci. 2010, 32:1265-1277.
44. Fajardo-Serrano A., et al. Association of Rgs7/Gbeta5 complexes with Girk channels and GABA receptors in hippocampal CA1 pyramidal neurons. Hippocampus 2013, 10.1002/hipo.22161.
45. Raveh A., et al. Elucidation of the gating of the GIRK channel using a spectroscopic approach. J. Physiol. 2009, 587:5331-5335.
46. Pfeffer S.R. A nexus for receptor recycling. Nat. Cell Biol. 2013, 15:446-448.
47. Kajii Y., et al. A developmentally regulated and psychostimulant-inducible novel rat gene mrt1 encoding PDZ-PX proteins isolated in the neocortex. Mol. Psychiatry 2003, 8:434-444.
48. Wang X., et al. Loss of sorting nexin 27 contributes to excitatory synaptic dysfunction by modulating glutamate receptor recycling in Down's syndrome. Nat. Med. 2013, 19:473-480.
49. Carlton J.G., Cullen P.J. Sorting nexins. Curr. Biol. 2005, 15:R819-R820.
50. Balana B., et al. Mechanism underlying selective regulation of G protein-gated inwardly rectifying potassium channels by the psychostimulant-sensitive sorting nexin 27. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:5831-5836.
51. Balana B., et al. Ras-association domain of sorting Nexin 27 is critical for regulating expression of GIRK potassium channels. PLoS ONE 2013, 8:e59800.
52. Nassirpour R., Slesinger P.A. Subunit-specific regulation of Kir3 channels by sorting nexin 27. Channels 2007, 1:331-333.
53. Arora D., et al. Acute cocaine exposure weakens GABA(B) receptor-dependent G-protein-gated inwardly rectifying K+ signaling in dopamine neurons of the ventral tegmental area. J. Neurosci. 2011, 31:12251-12257.
54. Padgett C.L., et al. Methamphetamine-evoked depression of GABA(B) receptor signaling in GABA neurons of the VTA. Neuron 2012, 73:978-989.
55. Hearing M., et al. Repeated cocaine weakens GABA-Girk signaling in layer 5/6 pyramidal neurons in the prelimbic cortex. Neuron 2013, 80:159-170.
56. Harashima C., et al. Abnormal expression of the G-protein-activated inwardly rectifying potassium channel 2 (GIRK2) in hippocampus, frontal cortex, and substantia nigra of Ts65Dn mouse: a model of Down syndrome. J. Comp. Neurol. 2006, 494:815-833.
57. Best T.K., et al. Ts65Dn, a mouse model of Down syndrome, exhibits increased GABAB-induced potassium current. J. Neurophysiol. 2007, 97:892-900.
58. Cooper A., et al. Trisomy of the G protein-coupled K+ channel gene, Kcnj6, affects reward mechanisms, cognitive functions, and synaptic plasticity in mice. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:2642-2647.
59. Sjogren B. Regulator of G protein signaling proteins as drug targets: current state and future possibilities. Adv. Pharmacol. 2011, 62:315-347.
60. Doupnik C.A., et al. RGS proteins reconstitute the rapid gating kinetics of gbetagamma-activated inwardly rectifying K+ channels. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:10461-10466.
61. Anderson G.R., et al. The R7 RGS protein family: multi-subunit regulators of neuronal G protein signaling. Cell Biochem. Biophys. 2009, 54:33-46.
62. Cheever M.L., et al. Crystal structure of the multifunctional Gbeta5-RGS9 complex. Nat. Struct. Mol. Biol. 2008, 15:155-162.
63. Posokhova E., et al. RGS6/Gβ5 complex accelerates IKACh gating kinetics in atrial myocytes and modulates parasympathetic regulation of heart rate. Circ. Res. 2010, 107:1350-1354.
64. Yang J., et al. RGS6, a modulator of parasympathetic activation in heart. Circ. Res. 2010, 107:1345-1349.
65. Xie K., et al. Gbeta5 recruits R7 RGS proteins to GIRK channels to regulate the timing of neuronal inhibitory signaling. Nat. Neurosci. 2010, 13:661-663.
66. Maity B., et al. Regulator of G protein signaling 6 (RGS6) protein ensures coordination of motor movement by modulating GABAB receptor signaling. J. Biol. Chem. 2012, 287:4972-4981.
67. Zhou H., et al. GIRK channel modulation by assembly with allosterically regulated RGS proteins. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:19977-19982.
68. Stewart A., et al. RGS proteins in heart: brakes on the vagus. Front. Physiol. 2012, 3:95.
69. Chung H.J., et al. G protein-activated inwardly rectifying potassium channels mediate depotentiation of long-term potentiation. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:635-640.
70. Huang C.S., et al. Common molecular pathways mediate long-term potentiation of synaptic excitation and slow synaptic inhibition. Cell 2005, 123:105-118.
71. Chung H.J., et al. Neuronal activity regulates phosphorylation-dependent surface delivery of G protein-activated inwardly rectifying potassium channels. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:629-634.
72. Luscher C., Malenka R.C. Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 2011, 69:650-663.
73. Nassirpour R., et al. Morphine- and CaMKII-dependent enhancement of GIRK channel signaling in hippocampal neurons. J. Neurosci. 2010, 30:13419-13430.
74. Signorini S., et al. Normal cerebellar development but susceptibility to seizures in mice lacking G protein-coupled, inwardly rectifying K+ channel GIRK2. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:923-927.
75. Hashimoto N., et al. Characterization of in vivo and in vitro electrophysiological and antiarrhythmic effects of a novel IKACh blocker, NIP-151: a comparison with an IKr-blocker dofetilide. J. Cardiovasc. Pharmacol. 2008, 51:162-169.
76. Machida T., et al. Effects of a highly selective acetylcholine-activated K+ channel blocker on experimental atrial fibrillation. Circ. Arrhythm. Electrophysiol. 2011, 4:94-102.
77. Kobayashi T., et al. Ethanol opens G-protein-activated inwardly rectifying K+ channels. Nat. Neurosci. 1999, 2:1091-1097.
78. Lewohl J.M., et al. G-protein-coupled inwardly rectifying potassium channels are targets of alcohol action. Nat. Neurosci. 1999, 2:1084-1090.
79. Weigl L.G., Schreibmayer W. G protein-gated inwardly rectifying potassium channels are targets for volatile anesthetics. Mol. Pharmacol. 2001, 60:282-289.
80. Yamakura T., et al. Differential effects of general anesthetics on G protein-coupled inwardly rectifying and other potassium channels. Anesthesiology 2001, 95:144-153.
81. Yow T.T., et al. Naringin directly activates inwardly rectifying potassium channels at an overlapping binding site to tertiapin-Q. Br. J. Pharmacol. 2011, 163:1017-1033.
82. Kobayashi T., et al. Inhibition of G protein-activated inwardly rectifying K+ channels by different classes of antidepressants. PLoS ONE 2011, 6:e28208.
83. Wen W., et al. Discovery of 'molecular switches' within a GIRK activator scaffold that afford selective GIRK inhibitors. Bioorg. Med. Chem. Lett. 2013, 23:4562-4566.
84. Kaufmann K., et al. ML297 (VU0456810), the first potent and selective activator of the GIRK potassium channel, displays antiepileptic properties in mice. ACS Chem. Neurosci. 2013, 4:1278-1286.
85. Ramos-Hunter S.J., et al. Discovery and SAR of a novel series of GIRK1/2 and GIRK1/4 activators. Bioorg. Med. Chem. Lett. 2013, 23:5195-5198.
86. Wickman K., et al. Abnormal heart rate regulation in GIRK4 knockout mice. Neuron 1998, 20:103-114.
87. Bettahi I., et al. Contribution of the Kir3.1 subunit to the muscarinic-gated atrial potassium channel IKACh. J. Biol. Chem. 2002, 277:48282-48288.
88. Yang Y., et al. Identification of a Kir3.4 mutation in congenital long QT syndrome. Am. J. Hum. Genet. 2010, 86:872-880.
89. Jabbari J., et al. Common polymorphisms in KCNJ5 are associated with early-onset lone atrial fibrillation in Caucasians. Cardiology 2011, 118:116-120.
90. Wang F., et al. The phenotype characteristics of type-13 long QT syndrome with mutation in KCNJ5 (Kir3.4-G387R). Heart Rhythm 2013, 10:1500-1506.
91. Scholl U.I., Lifton R.P. New insights into aldosterone-producing adenomas and hereditary aldosteronism: mutations in the K+ channel KCNJ5. Curr. Opin. Nephrol. Hypertens. 2013, 22:141-147.
92. Mulatero P., et al. Role of KCNJ5 in familial and sporadic primary aldosteronism. Nat. Rev. Endocrinol. 2013, 9:104-112.
93. Mitrovic I., et al. Contribution of GIRK2-mediated postsynaptic signaling to opiate and alpha 2-adrenergic analgesia and analgesic sex differences. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:271-276.
94. Marker C.L., et al. Spinal G-protein-gated K+ channels formed by GIRK1 and GIRK2 subunits modulate thermal nociception and contribute to morphine analgesia. J. Neurosci. 2004, 24:2806-2812.
95. Blednov Y.A., et al. A pervasive mechanism for analgesia: activation of GIRK2 channels. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:277-282.
96. Marker C.L., et al. Spinal G-protein-gated potassium channels contribute in a dose-dependent manner to the analgesic effect of mu- and delta- but not kappa-opioids. J. Neurosci. 2005, 25:3551-3559.
97. Cruz H.G., et al. Absence and rescue of morphine withdrawal in GIRK/Kir3 knock-out mice. J. Neurosci. 2008, 28:4069-4077.
98. Smith S.B., et al. Quantitative trait locus and computational mapping identifies Kcnj9 (GIRK3) as a candidate gene affecting analgesia from multiple drug classes. Pharmacogenet. Genomics 2008, 18:231-241.
99. Nishizawa D., et al. Association between KCNJ6 (GIRK2) gene polymorphisms and postoperative analgesic requirements after major abdominal surgery. PLoS ONE 2009, 4:e7060.
100. Lotsch J., et al. A KCNJ6 (Kir3.2, GIRK2) gene polymorphism modulates opioid effects on analgesia and addiction but not on pupil size. Pharmacogenet. Genomics 2010, 20:291-297.
101. Blednov Y.A., et al. Hyperactivity and dopamine D1 receptor activation in mice lacking Girk2 channels. Psychopharmacology 2002, 159:370-378.
102. Morgan A.D., et al. Decreased cocaine self-administration in Kir3 potassium channel subunit knockout mice. Neuropsychopharmacology 2003, 28:932-938.
103. Arora D., et al. Altered neurotransmission in the mesolimbic reward system of Girk mice. J. Neurochem. 2010, 114:1487-1497.
104. Pravetoni M., Wickman K. Behavioral characterization of mice lacking GIRK/Kir3 channel subunits. Genes Brain Behav. 2008, 7:523-531.
105. Perry C.A., et al. Predisposition to late-onset obesity in GIRK4 knockout mice. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:8148-8153.
106. Blednov Y.A., et al. Potassium channels as targets for ethanol: studies of G-protein-coupled inwardly rectifying potassium channel 2 (GIRK2) null mutant mice. J. Pharmacol. Exp. Ther. 2001, 298:521-530.
107. Kozell L.B., et al. Mapping a barbiturate withdrawal locus to a 0.44Mb interval and analysis of a novel null mutant identify a role for Kcnj9 (GIRK3) in withdrawal from pentobarbital, zolpidem, and ethanol. J. Neurosci. 2009, 29:11662-11673.
108. Clarke T.K., et al. KCNJ6 is associated with adult alcohol dependence and involved in gene × early life stress interactions in adolescent alcohol drinking. Neuropsychopharmacology 2011, 36:1142-1148.
109. Wickman K., et al. Brain localization and behavioral impact of the G-protein-gated K+ channel subunit GIRK4. J. Neurosci. 2000, 20:5608-5615.
110. Blednov Y.A., et al. GIRK2 deficient mice. Evidence for hyperactivity and reduced anxiety. Physiol. Behav. 2001, 74:109-117.
111. Yamada K., et al. Association study of the KCNJ3 gene as a susceptibility candidate for schizophrenia in the Chinese population. Hum. Genet. 2012, 131:443-451.
112. Costa A.C., et al. G-protein-gated potassium (GIRK) channels containing the GIRK2 subunit are control hubs for pharmacologically induced hypothermic responses. J. Neurosci. 2005, 25:7801-7804.
113. Patil N., et al. A potassium channel mutation in weaver mice implicates membrane excitability in granule cell differentiation. Nat. Genet. 1995, 11:126-129.
114. Gregerson K.A., et al. Identification of G protein-coupled, inward rectifier potassium channel gene products from the rat anterior pituitary gland. Endocrinology 2001, 142:2820-2832.
115. Plummer H.K., et al. Expression of G-protein inwardly rectifying potassium channels (GIRKs) in lung cancer cell lines. BMC Cancer 2005, 5:104.
116. Iwanir S., Reuveny E. Adrenaline-induced hyperpolarization of mouse pancreatic islet cells is mediated by G protein-gated inwardly rectifying potassium (GIRK) channels. Pflugers Arch. 2008, 456:1097-1108.
117. Wagner V., et al. Cloning and characterisation of GIRK1 variants resulting from alternative RNA editing of the KCNJ3 gene transcript in a human breast cancer cell line. J. Cell. Biochem. 2010, 110:598-608.
118. Aguado C., et al. Cell type-specific subunit composition of G protein-gated potassium channels in the cerebellum. J. Neurochem. 2008, 105:497-511.
119. Inanobe A., et al. Characterization of G-protein-gated K+ channels composed of Kir3.2 subunits in dopaminergic neurons of the substantia nigra. J. Neurosci. 1999, 19:1006-1017.
120. Koyrakh L., et al. Molecular and cellular diversity of neuronal G-protein-gated potassium channels. J. Neurosci. 2005, 25:11468-11478.
121. Luscher C., et al. G protein-coupled inwardly rectifying K+ channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 1997, 19:687-695.
122. Ladera C., et al. Pre-synaptic GABA receptors inhibit glutamate release through GIRK channels in rat cerebral cortex. J. Neurochem. 2008, 107:1506-1517.
123. Fernandez-Alacid L., et al. Subcellular compartment-specific molecular diversity of pre- and post-synaptic GABA-activated GIRK channels in Purkinje cells. J. Neurochem. 2009, 110:1363-1376.
124. Michaeli A., Yaka R. Dopamine inhibits GABA(A) currents in ventral tegmental area dopamine neurons via activation of presynaptic G-protein coupled inwardly-rectifying potassium channels. Neuroscience 2010, 165:1159-1169.
125. Booker S.A., et al. Differential GABAB-receptor-mediated effects in perisomatic- and dendrite-targeting parvalbumin interneurons. J. Neurosci. 2013, 33:7961-7974.