Mutagenesis and computational docking studies support the existence of a histamine binding site at the extracellular β3+β3- interface of homooligomeric β3 GABAA receptors

Neuropharmacology

Volumn 108, Issue , 2016, Pages 252-263

  Hoerbelt, Paul ^a,c   Ramerstorfer, Joachim ^b   Ernst, Margot ^b   Sieghart, Werner ^b   Thomson, Jeffrey L ^a   Hough, Lindsay B ^a   Fleck, Mark W ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

^b Medical University of Vienna   (Austria)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bicuculline; Docking; GABAA receptor; Histamine; Ligand gated ion channel; Mutagenesis

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR BETA3; BICUCULLINE; HETEROOLIGOMER; HISTAMINE; HOMOOLIGOMER; OLIGOMER; UNCLASSIFIED DRUG; ZINC ION; 4 AMINOBUTYRIC ACID A RECEPTOR; GABRB3 PROTEIN, RAT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL LINE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CRYSTAL STRUCTURE; FEMALE; HEK293T CELL LINE; INHIBITION KINETICS; LIGAND BINDING; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN SUBUNIT; STRUCTURE ANALYSIS; VOLTAGE CLAMP TECHNIQUE; ANIMAL; CHEMISTRY; DOSE RESPONSE; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR DOCKING; PHYSIOLOGY; PROCEDURES; PROTEIN SECONDARY STRUCTURE; RAT; XENOPUS LAEVIS;

ANIMALS; BINDING SITES; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HEK293 CELLS; HISTAMINE; HUMANS; MOLECULAR DOCKING SIMULATION; MUTAGENESIS; PROTEIN STRUCTURE, SECONDARY; RATS; RECEPTORS, GABA-A; XENOPUS LAEVIS;

EID: 84969640950     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2016.04.042     Document Type: Article

References (69)

1. J. Amin, and D.S. Weiss GABAA receptor needs two homologous domains of the beta-subunit for activation by GABA but not by pentobarbital Nature 366 1993 565 569
2. S.W. Baumann, R. Baur, and E. Sigel Subunit arrangement of gamma-aminobutyric acid type A receptors J. Biol. Chem. 276 39 2001 36275 36280
3. S.W. Baumann, R. Baur, and E. Sigel Individual properties of the two functional agonist sites in GABA(A) receptors J. Neurosci. 23 2003 11158 11166
4. M.T. Bianchi, A.G. Clark, and J.L. Fisher The wake-promoting transmitter histamine preferentially enhances alpha-4 subunit-containing GABAA receptors Neuropharmacology 61 2011 747 752 10.1016/j.neuropharm.2011.05.020
5. A.J. Boileau, A.R. Evers, A.F. Davis, and C. Czajkowski Mapping the agonist binding site of the GABAA receptor: evidence for a beta-strand J. Neurosci. 19 1999 4847 4854
6. A.J. Boileau, R.A. Pearce, and C. Czajkowski The short splice variant of the gamma 2 subunit acts as an external modulator of GABA(A) receptor function J. Neurosci. 30 14 2010 4895 4903 10.1523/JNEUROSCI.5039-09.2010
7. J.A. Borycz, J. Borycz, A. Kubow, R. Kostyleva, and I.A. Meinertzhagen Histamine compartments of the Drosophila brain with an estimate of the quantum content at the photoreceptor synapse J. Neurophysiol. 93 2005 1611 1619
8. S.G. Brickley, and I. Mody Extrasynaptic GABA(A) receptors: their function in the CNS and implications for disease Neuron 73 1 2012 23 34 10.1016/j.neuron.2011.12.012
9. I.N. Cestari, I. Uchida, L. Li, D. Burt, and J. Yang The agonistic action of pentobarbital on GABAA beta-subunit homomeric receptors Neuroreport 7 1996 943 947
10. D.C. Chiara, S.S. Jayakar, X. Zhou, X. Zhang, P.Y. Savechenkov, K.S. Bruzik, K.W. Miller, and J.B. Cohen Specificity of intersubunit general anesthetic-binding sites in the transmembrane domain of the human alpha1beta3gamma2 gamma-aminobutyric acid type A (GABAA) receptor J. Biol. Chem. 288 2013 19343 19357 10.1074/jbc.M113.479725
11. E.L. Dunne, A.M. Hosie, J.R. Wooltorton, I.C. Duguid, K. Harvey, S.J. Moss, R.J. Harvey, and T.G. Smart An N-terminal histidine regulates Zn(2+) inhibition on the murine GABA(A) receptor beta3 subunit Br. J. Pharmacol. 137 2002 29 38
12. V. Ebert, P. Scholze, and W. Sieghart Extensive heterogeneity of recombinant gamma-aminobutyric acidA receptors expressed in alpha 4 beta 3 gamma 2-transfected human embryonic kidney 293 cells Neuropharmacology 35 9-10 1996 1323 1330
13. H.J. Feng, M.T. Bianchi, and R.L. Macdonald Pentobarbital differentially modulates alpha1beta3delta and alpha1beta3gamma2L GABAA receptor currents Mol. Pharmacol. 66 4 2004 988 1003
14. M.W. Fleck Molecular actions of (S)-desmethylzopiclone (SEP-174559), an anxiolytic metabolite of zopiclone J. Pharmacol. Exp. Ther. 302 2 2002 612 618
15. M.W. Fleck, J.L. Thomson, and L.B. Hough Histamine-gated ion channels in mammals? Biochem. Pharmacol. 83 2012 1127 1135 10.1016/j.bcp.2011.12.011
16. P.S. Garcia, S.E. Kolesky, and A. Jenkins General anesthetic actions on GABA(A) receptors Curr. Neuropharmacol. 8 1 2010 2 9 10.2174/157015910790909502
17. G. Gisselmann, H. Pusch, B.T. Hovemann, and H. Hatt Two cDNAs coding for histamine-gated ion channels in D. melanogaster Nat. Neurosci. 5 2002 11 12
18. J. Grudzinska, R. Schemm, S. Haeger, A. Nicke, G. Schmalzing, H. Betz, and B. Laube The beta subunit determines the ligand binding properties of synaptic glycine receptors Neuron 45 5 2005 727 739
19. H.L. Haas, O.A. Sergeeva, and O. Selbach Histamine in the nervous system Physiol. Rev. 88 3 2008 1183 1241 10.1152/physrev.00043.2007
20. G.I. Hatton, and Q.Z. Yang Ionotropic histamine receptors and H2 receptors modulate supraoptic oxytocin neuronal excitability and dye coupling J. Neurosci. 21 2001 2974 2982
21. R.E. Hibbs, and E. Gouaux Principles of activation and permeation in an anion-selective Cys-loop receptor Nature 474 2011 54 60 10.1038/nature10139
22. P. Hoerbelt, T.A. Lindsley, and M.W. Fleck Dopamine directly modulates GABAA receptors J. Neurosci. 35 8 2015 3525 3536 10.1523/JNEUROSCI.4390-14.2015
23. J.H. Holden, and C. Czajkowski Different residues in the GABA(A) receptor alpha 1T60-alpha 1K70 region mediate GABA and SR-95531 actions J. Biol. Chem. 277 21 2002 18785 18792
24. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1 1996 33 38 27-28
25. F. Iqbal, R. Ellwood, M. Mortensen, T.G. Smart, and J.R. Baker Synthesis and evaluation of highly potent GABA(A) receptor antagonists based on gabazine (SR-95531) Bioorg Med. Chem. Lett. 21 2011 4252 4254 10.1016/j.bmcl.2011.05.067
26. H. Jhoti, and A.R. Leach Structure-based Drug Discovery 2007 Springer Dordrecht, The Netherlands 10.1021/ja076951v
27. R. Jurd, M. Arras, S. Lambert, B. Drexler, R. Siegwart, F. Crestani, M. Zaugg, K.E. Vogt, B. Ledermann, B. Antkowiak, and U. Rudolph General anesthetic actions in vivo strongly attenuated by a point mutation in the GABA(A) receptor beta3 subunit FASEB J. 17 2 2003 250 252
28. O. Kletke, O.A. Sergeeva, P. Lorenz, S. Oberland, J.C. Meier, H. Hatt, and G. Gisselmann New insights in endogenous modulation of ligand-gated ion channels: histamine is an inverse agonist at strychnine sensitive glycine receptors Eur. J. Pharmacol. 710 1-3 2013 59 66 10.1016/j.ejphar.2013.04.002
29. A.M. Kucken, D.A. Wagner, P.R. Ward, J.A. Teissére, A.J. Boileau, and C. Czajkowski Identification of benzodiazepine binding site residues in the gamma2 subunit of the gamma-aminobutyric acid(A) receptor Mol. Pharmacol. 57 2000 932 939
30. T. Lynagh, and S.A. Pless Principles of agonist recognition in Cys-loop receptors Front. Physiol. 5 2014 160 10.3389/fphys.2014.00160
31. A receptor channel by the intravenous anesthetics propofol, etomidate and pentobarbital Neuropharmacology 105 2016 207 214 10.1016/j.neuropharm.2016.01.003
32. P.S. Miller, and A.R. Aricescu Crystal structure of a human GABAA receptor Nature 512 7514 2014 270 275 10.1038/nature13293
33. P.S. Miller, and T.G. Smart Binding, activation and modulation of Cys-loop receptors Trends Pharmacol. Sci. 31 4 2010 161 174 10.1016/j.tips.2009.12.005
34. M. Mortensen, and T.G. Smart Extrasynaptic alphabeta subunit GABAA receptors on rat hippocampal pyramidal neurons J. Physiol. 15 577 Pt 3 2006 841 856
35. J.G. Newell, M. Davies, A.N. Bateson, and S.M. Dunn Tyrosine 62 of the gamma-aminobutyric acid type A receptor beta 2 subunit is an important determinant of high affinity agonist binding J. Biol. Chem. 275 19 2000 14198 14204
36. S. Nishino, E. Sakurai, S. Nevsimalova, Y. Yoshida, T. Watanabe, K. Yanai, and E. Mignot Decreased CSF histamine in narcolepsy with and without low CSF hypocretin-1 in comparison to healthy controls Sleep 32 2 2009 175 180
37. L.D. Ochoa-de la Paz, A. Estrada-Mondragon, A. Limon, R. Miledi, and A. Martinez-Torres Dopamine and serotonin modulate human GABArho1 receptors expressed in Xenopus laevis oocytes ACS Chem. Neurosci. 3 2012 96 104 10.1021/cn200083m
38. R.W. Olsen, and W. Sieghart International Union of Pharmacology. LXX. Subtypes of gamma-aminobutyric acid(A) receptors: classification on the basis of subunit composition, pharmacology, and function. Update Pharmacol. Rev. 60 2008 243 260 10.1124/pr.108.00505
39. C.N. Pace, G. Horn, E.J. Hebert, J. Bechert, K. Shaw, L. Urbanikova, J.M. Scholtz, and J. Sevcik Tyrosine hydrogen bonds make a large contribution to protein stability J. Mol. Biol. 312 2001 393 404
40. P. Panula, P.L. Chazot, M. Cowart, R. Gutzmer, R. Leurs, W.L. Liu, H. Stark, R.L. Thurmond, and H.L. Haas International Union of Basic and Clinical Pharmacology. XCVIII. Histamine receptors Pharmacol. Rev. 67 3 2015 601 655 10.1124/pr.114.010249
41. P. Panula, and S. Nuutinen The histaminergic network in the brain: basic organization and role in disease Nat. Rev. Neurosci. 14 2013 472 487 10.1038/nrn3526
42. T.N. Petersen, S. Brunak, G. von Heijne, and H. Nielsen SignalP 4.0: discriminating signal peptides from transmembrane regions Nat. Methods 8 2011 785 786 10.1038/nmeth.1701
43. J.K. Pirri, A.D. McPherson, J.L. Donnelly, M.M. Francis, and M.J. Alkema A tyramine-gated chloride channel coordinates distinct motor programs of a Caenorhabditis elegans escape response Neuron 62 2009 526 538 10.1016/j.neuron.2009.04.013
44. J. Ramerstorfer, V. Foppa, H. Thiery, P. Hermange, S. Janody, M.L. Berger, R.H. Dodd, and W. Sieghart GABA(A) receptor subtype-selectivity of novel bicuculline derivatives Curr. Med. Chem. 22 6 2015 771 780
45. J. Ramerstorfer, R. Furtmuller, I. Sarto-Jackson, Z. Varagic, W. Sieghart, and M. Ernst The GABAA receptor alpha+beta- interface: a novel target for subtype selective drugs J. Neurosci. 31 2011 870 877 10.1523/JNEUROSCI.5012-10.2011
46. N. Ringstad, N. Abe, and H.R. Horvitz Ligand-gated chloride channels are receptors for biogenic amines in C. elegans Science 325 2009 96 100 10.1126/science.1169243
47. U. Rudolph, and H. Möhler GABAA receptor subtypes: therapeutic potential in down syndrome, affective disorders, schizophrenia, and autism Annu. Rev. Pharmacol. Toxicol. 54 2014 483 507 10.1146/annurev-pharmtox-011613-135947
48. B.D. Safratowich, M. Hossain, L. Bianchi, and L. Carvelli Amphetamine potentiates the effects of beta-phenylethylamine through activation of an amine-gated chloride channel J. Neurosci. 34 2014 4686 4691 10.1523/JNEUROSCI.3100-13.2014
49. B.D. Safratowich, C. Lor, L. Bianchi, and L. Carvelli Amphetamine activates an amine-gated chloride channel to generate behavioral effects in Caenorhabditis elegans J. Biol. Chem. 288 2013 21630 21637 10.1074/jbc.M113.484139
50. N. Saligrama, L.K. Case, R. del Rio, R. Noubade, and C. Teuscher Systemic lack of canonical histamine receptor signaling results in increased resistance to autoimmune encephalomyelitis J. Immunol. 191 2013 614 622 10.4049/jimmunol.1203137
51. T. Sander, B. Frolund, A.T. Bruun, I. Ivanov, J.A. McCammon, and T. Balle New insights into the GABA(A) receptor structure and orthosteric ligand binding: receptor modeling guided by experimental data Proteins 79 2011 1458 1477 10.1002/prot.22975
52. A. Saras, G. Gisselmann, A.K. Vogt-Eisele, K.S. Erlkamp, O. Kletke, H. Pusch, and H. Hatt Histamine action on vertebrate GABAA receptors: direct channel gating and potentiation of GABA responses J. Biol. Chem. 283 2008 10470 10475 10.1074/jbc.M709993200
53. C. Seeger, T. Christopeit, K. Fuchs, K. Grote, W. Sieghart, and U.H. Danielson Histaminergic pharmacology of homo-oligomeric beta3 gamma-aminobutyric acid type A receptors characterized by surface plasmon resonance biosensor technology Biochem. Pharmacol. 84 2012 341 351 10.1016/j.bcp.2012.04.008
54. W. Sieghart Allosteric modulation of GABAA receptors via multiple drug-binding sites Adv. Pharmacol. 72 2015 53 96 10.1016/bs.apha.2014.10.002
55. W. Sieghart Structure and pharmacology of gamma-aminobutyric acidA receptor subtypes Pharmacol. Rev. 47 1995 181 234
56. W. Sieghart, and G. Sperk Subunit composition, distribution and function of GABA(A) receptor subtypes Curr. Top. Med. Chem. 2 8 2002 795 816
57. E. Sigel, R. Baur, S. Kellenberger, and P. Malherbe Point mutations affecting antagonist affinity and agonist dependent gating of GABAA receptor channels EMBO J. 11 1992 2017 2023
58. A. Slany, J. Zezula, V. Tretter, and W. Sieghart Rat beta 3 subunits expressed in human embryonic kidney 293 cells form high affinity [35S]t-butylbicyclophosphorothionate binding sites modulated by several allosteric ligands of gamma-aminobutyric acid type A receptors Mol. Pharmacol. 48 3 1995 385 391
59. G.B. Smith, and R.W. Olsen Functional domains of GABAA receptors Trends Pharmacol. Sci. 16 1995 162 168
60. M. Szczot, M. Kisiel, M.M. Czyzewska, and J.W. Mozrzymas alpha1F64 residue at GABA(A) receptor binding site is involved in gating by influencing the receptor flipping transitions J. Neurosci. 34 2014 3193 3209 10.1523/JNEUROSCI.2533-13.2014
61. U. Thiel, S.J. Platt, S. Wolf, H. Hatt, and G. Gisselmann Identification of amino acids involved in histamine potentiation of GABAA receptors Front. Pharmacol. 6 2015 106 10.3389/fphar.2015.00106
62. S.A. Thompson, P.B. Wingrove, L. Connelly, P.J. Whiting, and K.A. Wafford Tracazolate reveals a novel type of allosteric interaction with recombinant gamma-aminobutyric acid(A) receptors Mol. Pharmacol. 61 4 2002 861 869
63. V. Tretter, N. Ehya, K. Fuchs, and W. Sieghart Stoichiometry and assembly of a recombinant GABAA receptor subtype J. Neurosci. 17 8 1997 2728 2737
64. S. Ueno, J. Bracamontes, C. Zorumski, D.S. Weiss, and J.H. Steinbach Bicuculline and gabazine are allosteric inhibitors of channel opening of the GABAA receptor J. Neurosci. 17 1997 625 634
65. M.L. Verdonk, J.C. Cole, M.J. Hartshorn, C.W. Murray, and R.D. Taylor Improved protein-ligand docking using GOLD Proteins 52 4 2003 609 623
66. C.G. Wong, T. Bottiglieri, and O.C. Snead 3rd GABA, gamma-hydroxybutyric acid, and neurological disease Ann. Neurol. 54 Suppl. 6 2003 S3 S12
67. J.R. Wooltorton, B.J. McDonald, S.J. Moss, and T.G. Smart Identification of a Zn2+ binding site on the murine GABAA receptor complex: dependence on the second transmembrane domain of beta subunits J. Physiol. 505 Pt 3 1997 633 640
68. Q.Z. Yang, and G.I. Hatton Histamine mediates fast synaptic inhibition of rat supraoptic oxytocin neurons via chloride conductance activation Neuroscience 61 1994 955 964
69. X. Yu, Z. Ye, C.M. Houston, A.Y. Zecharia, Y. Ma, Z. Zhang, D.S. Uygun, S. Parker, A.L. Vyssotski, R. Yustos, N.P. Franks, S.G. Brickley, and W. Wisden Wakefulness is governed by GABA and histamine cotransmission Neuron 87 1 2015 164 178 10.1016/j.neuron.2015.06.003