DOI: 10.1126/science.2551039. Type I and Type II GABA <sub>A</sub> -Benzodiazepine Receptors Produced in Transfected Cells

Type I and Type II GABA A -Benzodiazepine Receptors Produced in Transfected Cells

10.1126/science.2551039

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

GABA A (γ-aminobutyric acid A)-benzodiazepine receptors expressed in mammalian cells and assembled from one of three different α subunit variants (α 1 , α 2 , or α 3 ) in combination with a β 1 and a γ 2 subunit display the pharmacological properties of either type I or type II receptor subtypes. These receptors contain high-affinity binding sites for benzodiazepines. However, CL 218 872, 2-oxoquazepam, and methyl β-carboline-3-carboxylate (β-CCM) show a temperature-modulated selectivity for α 1 subunit-containing receptors. There were no significant differences in the binding of clonazepam, diazepam, Ro 15-1788, or dimethoxy-4-ethyl-β-carboline-3-carboxylate (DMCM) to all three recombinant receptors. Receptors containing the α 3 subunit show greater GABA potentiation of benzodiazepine binding than receptors containing the α 1 or α 2 subunit, indicating that there are subtypes within the type II class. Thus, diversity in benzodiazepine pharmacology is generated by heterogeneity of the α subunit of the GABA A receptor.

Bibliography

Pritchett, D. B., LÃ¼ddens, H., & Seeburg, P. H. (1989). Type I and Type II GABA A -Benzodiazepine Receptors Produced in Transfected Cells. Science, 245(4924), 1389â1392.

Authors 3

Dolan B. Pritchett (first)
Hartmut Lüddens (additional)
Peter H. Seeburg (additional)

References 41 Referenced 615

BILLARD, W, SELECTIVE AFFINITY OF THE BENZODIAZEPINES QUAZEPAM AND 2-OXO-QUAZEPAM FOR BZ1 BINDING-SITE AND DEMONSTRATION OF H-3-2-OXO-QUAZEPAM AS A BZ1 SELECTIVE RADIOLIGAND, LIFE SCIENCES 42: 179 (1988). (10.1016/0024-3205(88)90681-9) / LIFE SCIENCES (1988)
CASALOTTI, S.O., SEPARATE SUBUNITS FOR AGONIST AND BENZODIAZEPINE BINDING IN THE GAMMA-AMINOBUTYRIC ACIDA RECEPTOR OLIGOMER, JOURNAL OF BIOLOGICAL CHEMISTRY 261: 15013 (1986). (10.1016/S0021-9258(18)66821-8) / JOURNAL OF BIOLOGICAL CHEMISTRY (1986)
CHENG, Y, RELATIONSHIP BETWEEN INHIBITION CONSTANT (K1) AND CONCENTRATION OF INHIBITOR WHICH CAUSES 50 PER CENT INHIBITION (I50) OF AN ENZYMATIC-REACTION, BIOCHEMICAL PHARMACOLOGY 22: 3099 (1973). (10.1016/0006-2952(73)90196-2) / BIOCHEMICAL PHARMACOLOGY (1973)
CORDA, M.G., PREFERENTIAL AFFINITY OF H-3-2-OXO-QUAZEPAM FOR TYPE-I BENZODIAZEPINE RECOGNITION SITES IN THE HUMAN-BRAIN, LIFE SCIENCES 42: 189 (1988). (10.1016/0024-3205(88)90682-0) / LIFE SCIENCES (1988)
EICHINGER, A, PHOTOAFFINITY-LABELING OF DIFFERENT BENZODIAZEPINE RECEPTORS AT PHYSIOLOGICAL TEMPERATURE, JOURNAL OF NEUROCHEMISTRY 43: 1745 (1984). (10.1111/j.1471-4159.1984.tb06103.x) / JOURNAL OF NEUROCHEMISTRY (1984)
EICHINGER, A, DIFFERENTIAL DEGRADATION OF DIFFERENT BENZODIAZEPINE BINDING-PROTEINS BY INCUBATION OF MEMBRANES FROM CEREBELLUM OR HIPPOCAMPUS WITH TRYPSIN, JOURNAL OF NEUROCHEMISTRY 45: 219 (1985). (10.1111/j.1471-4159.1985.tb05496.x) / JOURNAL OF NEUROCHEMISTRY (1985)
FUCHS, K, VARIOUS PROTEINS FROM RAT-BRAIN, SPECIFICALLY AND IRREVERSIBLY LABELED BY [H-3]FLUNITRAZEPAM, ARE DISTINCT ALPHA-SUBUNITS OF THE GABA BENZODIAZEPINE RECEPTOR COMPLEX, NEUROSCIENCE LETTERS 90: 314 (1988). (10.1016/0304-3940(88)90208-X) / NEUROSCIENCE LETTERS (1988)
GEE, K.W., THE INFLUENCE OF TEMPERATURE AND GAMMA-AMINOBUTYRIC ACID ON BENZODIAZEPINE RECEPTOR SUBTYPES IN THE HIPPOCAMPUS OF THE RAT, BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 106: 1134 (1982). (10.1016/0006-291X(82)91230-X) / BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS (1982)
GEE, K.W., REGIONAL HETEROGENEITY OF BENZODIAZEPINE RECEPTORS AT 37-DEGREES-C - AN INVITRO STUDY IN VARIOUS REGIONS OF THE RAT-BRAIN, LIFE SCIENCES 31: 1939 (1982). (10.1016/0024-3205(82)90032-7) / LIFE SCIENCES (1982)
KIRKNESS, E.F., ANTIBODIES DIRECTED AGAINST A NONAPEPTIDE SEQUENCE OF THE GAMMA-AMINOBUTYRATE (GABA) BENZODIAZEPINE RECEPTOR ALPHA-SUBUNIT - DETECTION OF A DISTINCT ALPHA-LIKE SUBUNIT IN PIG CEREBRAL-CORTEX BUT NOT CEREBELLUM, BIOCHEMICAL JOURNAL 256: 291 (1988). (10.1042/bj2560291) / BIOCHEMICAL JOURNAL (1988)
LEVITAN, E.S., STRUCTURAL AND FUNCTIONAL BASIS FOR GABAA RECEPTOR HETEROGENEITY, NATURE 335: 76 (1988). (10.1038/335076a0) / NATURE (1988)
LIPPA, A.S., SYNTHETIC NON-BENZODIAZEPINE LIGAND FOR BENZODIAZEPINE RECEPTORS - PROBE FOR INVESTIGATING NEURONAL SUBSTRATES OF ANXIETY, PHARMACOLOGY BIOCHEMISTRY AND BEHAVIOR 11: 99 (1979). (10.1016/0091-3057(79)90304-6) / PHARMACOLOGY BIOCHEMISTRY AND BEHAVIOR (1979)
LO, MMS, DIFFERENTIAL LOCALIZATION OF TYPE-I AND TYPE-II BENZODIAZEPINE BINDING-SITES IN SUBSTANTIA NIGRA, NATURE 306: 57 (1983). (10.1038/306057a0) / NATURE (1983)
LOLAIT, S.J., CLONING AND EXPRESSION OF A NOVEL RAT GABAA RECEPTOR, FEBS LETTERS 246: 145 (1989). (10.1016/0014-5793(89)80271-6) / FEBS LETTERS (1989)
MALLORGA, P, ONTOGENETIC CHANGES IN GABA MODULATION OF BRAIN BENZODIAZEPINE BINDING, NEUROPHARMACOLOGY 19: 405 (1980). (10.1016/0028-3908(80)90193-8) / NEUROPHARMACOLOGY (1980)
NIEHOFF, D.L., BINDING OF A RADIOLABELED TRIAZOLOPYRIDAZINE TO A SUBTYPE OF BENZODIAZEPINE RECEPTOR IN THE RAT CEREBELLUM, JOURNAL OF PHARMACOLOGY AND EXPERIMENTAL THERAPEUTICS 221: 670 (1982). / JOURNAL OF PHARMACOLOGY AND EXPERIMENTAL THERAPEUTICS (1982)
NIELSEN, M, ETHYL BETA-CARBOLINE-3-CARBOXYLATE SHOWS DIFFERENTIAL BENZODIAZEPINE RECEPTOR INTERACTION, NATURE 286: 606 (1980). (10.1038/286606a0) / NATURE (1980)
Olsen R. W. Benzodiazepine-GABA Receptors and Chloride Channels: Structural and Futcitonial Properties (1986).
PRITCHETT, D.B., IMPORTANCE OF A NOVEL GABAA RECEPTOR SUBUNIT FOR BENZODIAZEPINE PHARMACOLOGY, NATURE 338: 582 (1989). (10.1038/338582a0) / NATURE (1989)
10.1126/science.2848320
SATO, T.N., TYPE-I AND TYPE-II GAMMA-AMINOBUTYRIC ACID BENZODIAZEPINE RECEPTORS - PURIFICATION AND ANALYSIS OF NOVEL RECEPTOR COMPLEX FROM NEONATAL CORTEX, JOURNAL OF NEUROCHEMISTRY 52: 1114 (1989). (10.1111/j.1471-4159.1989.tb01855.x) / JOURNAL OF NEUROCHEMISTRY (1989)
SCHOFIELD, P.R., SEQUENCE AND EXPRESSION OF HUMAN GABAA RECEPTOR-ALPHA-1 AND RECEPTOR-BETA-1 SUBUNITS, FEBS LETTERS 244: 361 (1989). (10.1016/0014-5793(89)80563-0) / FEBS LETTERS (1989)
SCHOFIELD, P.R., SEQUENCE AND FUNCTIONAL EXPRESSION OF THE GABA-A RECEPTOR SHOWS A LIGAND-GATED RECEPTOR SUPER-FAMILY, NATURE 328: 221 (1987). (10.1038/328221a0) / NATURE (1987)
SHIBUYA, H, SUPER-SENSITIVITY TO GABA EFFECT ON BENZODIAZEPINE RECEPTORS DEVELOPS AFTER STRIATONIGRAL LESIONS, EUROPEAN JOURNAL OF PHARMACOLOGY 62: 243 (1980). (10.1016/0014-2999(80)90286-1) / EUROPEAN JOURNAL OF PHARMACOLOGY (1980)
SIEGHART, W, AFFINITY OF VARIOUS LIGANDS FOR BENZODIAZEPINE RECEPTORS IN RAT CEREBELLUM AND HIPPOCAMPUS, BIOCHEMICAL PHARMACOLOGY 33: 4033 (1984). (10.1016/0006-2952(84)90017-0) / BIOCHEMICAL PHARMACOLOGY (1984)
SIEGHART, W, PROPERTIES OF [H-3]-LABELED FLUNITRAZEPAM BINDING TO DIFFERENT BENZODIAZEPINE BINDING-PROTEINS, EUROPEAN JOURNAL OF PHARMACOLOGY 88: 291 (1983). (10.1016/0014-2999(83)90579-4) / EUROPEAN JOURNAL OF PHARMACOLOGY (1983)
SIEGHART, W, BENZODIAZEPINE RECEPTORS - MULTIPLE RECEPTORS OR MULTIPLE CONFORMATIONS, JOURNAL OF NEURAL TRANSMISSION 63: 191 (1985). (10.1007/BF01252025) / JOURNAL OF NEURAL TRANSMISSION (1985)
SIEGHART, W, IRREVERSIBLE BINDING OF [FLUNITRAZEPAM-H-3 TO DIFFERENT PROTEINS IN VARIOUS BRAIN-REGIONS, JOURNAL OF NEUROCHEMISTRY 41: 47 (1983). (10.1111/j.1471-4159.1983.tb11812.x) / JOURNAL OF NEUROCHEMISTRY (1983)
SIEGHART, W, COMPARISON OF TRYPTIC PEPTIDES OF BENZODIAZEPINE BINDING-PROTEINS PHOTOLABELED WITH [H-3] FLUNITRAZEPAM OR [H-3] RO-15-4513, JOURNAL OF NEUROCHEMISTRY 48: 1109 (1987). (10.1111/j.1471-4159.1987.tb05634.x) / JOURNAL OF NEUROCHEMISTRY (1987)
SIEGHART, W, MOLECULAR HETEROGENEITY OF BENZODIAZEPINE RECEPTORS, NATURE 286: 285 (1980). (10.1038/286285a0) / NATURE (1980)
SIEGHART, W, POSTNATAL-DEVELOPMENT OF PROTEINS IRREVERSIBLY LABELED BY [H-3]-LABELED FLUNITRAZEPAM, NEUROSCIENCE LETTERS 31: 71 (1982). (10.1016/0304-3940(82)90056-8) / NEUROSCIENCE LETTERS (1982)
SIEGHART, W, SEVERAL NEW BENZODIAZEPINES SELECTIVELY INTERACT WITH A BENZODIAZEPINE RECEPTOR SUBTYPE, NEUROSCIENCE LETTERS 38: 73 (1983). (10.1016/0304-3940(83)90113-1) / NEUROSCIENCE LETTERS (1983)
SONTHEIMER, H, FUNCTIONAL CHLORIDE CHANNELS BY MAMMALIAN-CELL EXPRESSION OF RAT GLYCINE RECEPTOR SUBUNIT, NEURON 2: 1491 (1989). (10.1016/0896-6273(89)90195-5) / NEURON (1989)
SQUIRES, R.F., BENZODIAZEPINE RECEPTOR MULTIPLICITY, NEUROPHARMACOLOGY 22: 1443 (1983). (10.1016/0028-3908(83)90112-0) / NEUROPHARMACOLOGY (1983)
SQUIRES, R.F., SOME PROPERTIES OF BRAIN SPECIFIC BENZODIAZEPINE RECEPTORS - NEW EVIDENCE FOR MULTIPLE RECEPTORS, PHARMACOLOGY BIOCHEMISTRY AND BEHAVIOR 10: 825 (1979). (10.1016/0091-3057(79)90341-1) / PHARMACOLOGY BIOCHEMISTRY AND BEHAVIOR (1979)
STEPHENSON, F.A., IDENTIFICATION OF THE ALPHA-3-SUBUNIT IN THE GABAA RECEPTOR PURIFIED FROM BOVINE BRAIN, FEBS LETTERS 243: 358 (1989). (10.1016/0014-5793(89)80161-9) / FEBS LETTERS (1989)
SUPAVILAI, P, HETEROGENEITY OF BENZODIAZEPINE RECEPTORS IN RAT CEREBELLUM AND HIPPOCAMPUS, EUROPEAN JOURNAL OF PHARMACOLOGY 64: 91 (1980). (10.1016/0014-2999(80)90374-X) / EUROPEAN JOURNAL OF PHARMACOLOGY (1980)
WISDEN, W, LOCALIZATION OF GABAA RECEPTOR ALPHA-SUBUNIT MESSENGER-RNAS IN RELATION TO RECEPTOR SUBTYPES, MOLECULAR BRAIN RESEARCH 5: 305 (1989). (10.1016/0169-328X(89)90065-X) / MOLECULAR BRAIN RESEARCH (1989)
WISDEN, W, DISTINCT GABAA RECEPTOR ALPHA-SUBUNIT MESSENGER-RNAS SHOW DIFFERENTIAL PATTERNS OF EXPRESSION IN BOVINE BRAIN, NEURON 1: 937 (1988). (10.1016/0896-6273(88)90151-1) / NEURON (1988)
YMER, S, GABAA RECEPTOR BETA-SUBUNIT HETEROGENEITY - FUNCTIONAL EXPRESSION OF CLONED CDNAS, EMBO JOURNAL 8: 1665 (1989). (10.1002/j.1460-2075.1989.tb03557.x) / EMBO JOURNAL (1989)
YOUNG, W.S., MULTIPLE BENZODIAZEPINE RECEPTOR LOCALIZATION BY LIGHT MICROSCOPIC RADIOHISTOCHEMISTRY, JOURNAL OF PHARMACOLOGY AND EXPERIMENTAL THERAPEUTICS 216: 425 (1981). / JOURNAL OF PHARMACOLOGY AND EXPERIMENTAL THERAPEUTICS (1981)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 5:21 p.m.)
Deposited	1 year, 7 months ago (Jan. 12, 2024, 6:21 p.m.)
Indexed	1 day, 2 hours ago (Sept. 4, 2025, 10:11 a.m.)
Issued	35 years, 11 months ago (Sept. 22, 1989)
Published	35 years, 11 months ago (Sept. 22, 1989)
Published Print	35 years, 11 months ago (Sept. 22, 1989)

Funders 0

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BibTeX

@article{Pritchett_1989, title={Type I and Type II GABA A -Benzodiazepine Receptors Produced in Transfected Cells}, volume={245}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.2551039}, DOI={10.1126/science.2551039}, number={4924}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Pritchett, Dolan B. and Lüddens, Hartmut and Seeburg, Peter H.}, year={1989}, month=sep, pages={1389–1392} }

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  "abstract": "<jats:p>\n            GABA\n            <jats:sub>A</jats:sub>\n            (\u03b3-aminobutyric acid A)-benzodiazepine receptors expressed in mammalian cells and assembled from one of three different \u03b1 subunit variants (\u03b1\n            <jats:sub>1</jats:sub>\n            , \u03b1\n            <jats:sub>2</jats:sub>\n            , or \u03b1\n            <jats:sub>3</jats:sub>\n            ) in combination with a \u03b2\n            <jats:sub>1</jats:sub>\n            and a \u03b3\n            <jats:sub>2</jats:sub>\n            subunit display the pharmacological properties of either type I or type II receptor subtypes. These receptors contain high-affinity binding sites for benzodiazepines. However, CL 218 872, 2-oxoquazepam, and methyl \u03b2-carboline-3-carboxylate (\u03b2-CCM) show a temperature-modulated selectivity for \u03b1\n            <jats:sub>1</jats:sub>\n            subunit-containing receptors. There were no significant differences in the binding of clonazepam, diazepam, Ro 15-1788, or dimethoxy-4-ethyl-\u03b2-carboline-3-carboxylate (DMCM) to all three recombinant receptors. Receptors containing the \u03b1\n            <jats:sub>3</jats:sub>\n            subunit show greater GABA potentiation of benzodiazepine binding than receptors containing the \u03b1\n            <jats:sub>1</jats:sub>\n            or \u03b1\n            <jats:sub>2</jats:sub>\n            subunit, indicating that there are subtypes within the type II class. Thus, diversity in benzodiazepine pharmacology is generated by heterogeneity of the \u03b1 subunit of the GABA\n            <jats:sub>A</jats:sub>\n            receptor.\n          </jats:p>",
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      "key": "e_1_2_1_18_1",
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      "first-page": "221",
      "DOI": "10.1038/328221a0",
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