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Review ArticleReview Article

G Protein–Coupled Receptor Oligomerization Revisited: Functional and Pharmacological Perspectives

Sergi Ferré, Vicent Casadó, Lakshmi A. Devi, Marta Filizola, Ralf Jockers, Martin J. Lohse, Graeme Milligan, Jean-Philippe Pin and Xavier Guitart
Mark P. Mattson, ASSOCIATE EDITOR
Pharmacological Reviews April 2014, 66 (2) 413-434; DOI: https://doi.org/10.1124/pr.113.008052
Sergi Ferré
Integrative Neurobiology Section, National Institute on Drug Addiction, Intramural Research Program, National Institutes of Health, Department of Health and Human Services, Baltimore, Maryland (S.F., X.G.); Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain (V.C.); Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas, Barcelona, Spain (V.C.); Department of Pharmacology and Systems Therapeutics (L.A.D.) and Department of Structural and Chemical Biology (M.F.), Icahn School of Medicine at Mount Sinai, Mount Sinai, New York; Institut National de la Santé et de la Recherche Médicale, U1016, Institut Cochin, Paris, France (R.J.); Centre National de la Recherche Scientifique Unité Mixte de Recherche 8104, Paris, France (R.J.); Universite Paris Descartes, Sorbone Paris Cite, Paris, France (R.J.); Institute of Pharmacology and Toxicology and Rudolf Virchow Center, University of Würzburg, Würzburg, Germany (M.J.L.); Molecular Pharmacology Group, Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom (G.M.); Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5203, Institut de Génomique Fonctionnelle, Université Montpellier, Montpellier, France (J.-P.P.); and Institut National de la Santé et de la Recherche Médicale, U661, Montpellier, France (J.-P.P.)
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Vicent Casadó
Integrative Neurobiology Section, National Institute on Drug Addiction, Intramural Research Program, National Institutes of Health, Department of Health and Human Services, Baltimore, Maryland (S.F., X.G.); Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain (V.C.); Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas, Barcelona, Spain (V.C.); Department of Pharmacology and Systems Therapeutics (L.A.D.) and Department of Structural and Chemical Biology (M.F.), Icahn School of Medicine at Mount Sinai, Mount Sinai, New York; Institut National de la Santé et de la Recherche Médicale, U1016, Institut Cochin, Paris, France (R.J.); Centre National de la Recherche Scientifique Unité Mixte de Recherche 8104, Paris, France (R.J.); Universite Paris Descartes, Sorbone Paris Cite, Paris, France (R.J.); Institute of Pharmacology and Toxicology and Rudolf Virchow Center, University of Würzburg, Würzburg, Germany (M.J.L.); Molecular Pharmacology Group, Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom (G.M.); Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5203, Institut de Génomique Fonctionnelle, Université Montpellier, Montpellier, France (J.-P.P.); and Institut National de la Santé et de la Recherche Médicale, U661, Montpellier, France (J.-P.P.)
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Lakshmi A. Devi
Integrative Neurobiology Section, National Institute on Drug Addiction, Intramural Research Program, National Institutes of Health, Department of Health and Human Services, Baltimore, Maryland (S.F., X.G.); Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain (V.C.); Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas, Barcelona, Spain (V.C.); Department of Pharmacology and Systems Therapeutics (L.A.D.) and Department of Structural and Chemical Biology (M.F.), Icahn School of Medicine at Mount Sinai, Mount Sinai, New York; Institut National de la Santé et de la Recherche Médicale, U1016, Institut Cochin, Paris, France (R.J.); Centre National de la Recherche Scientifique Unité Mixte de Recherche 8104, Paris, France (R.J.); Universite Paris Descartes, Sorbone Paris Cite, Paris, France (R.J.); Institute of Pharmacology and Toxicology and Rudolf Virchow Center, University of Würzburg, Würzburg, Germany (M.J.L.); Molecular Pharmacology Group, Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom (G.M.); Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5203, Institut de Génomique Fonctionnelle, Université Montpellier, Montpellier, France (J.-P.P.); and Institut National de la Santé et de la Recherche Médicale, U661, Montpellier, France (J.-P.P.)
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Marta Filizola
Integrative Neurobiology Section, National Institute on Drug Addiction, Intramural Research Program, National Institutes of Health, Department of Health and Human Services, Baltimore, Maryland (S.F., X.G.); Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain (V.C.); Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas, Barcelona, Spain (V.C.); Department of Pharmacology and Systems Therapeutics (L.A.D.) and Department of Structural and Chemical Biology (M.F.), Icahn School of Medicine at Mount Sinai, Mount Sinai, New York; Institut National de la Santé et de la Recherche Médicale, U1016, Institut Cochin, Paris, France (R.J.); Centre National de la Recherche Scientifique Unité Mixte de Recherche 8104, Paris, France (R.J.); Universite Paris Descartes, Sorbone Paris Cite, Paris, France (R.J.); Institute of Pharmacology and Toxicology and Rudolf Virchow Center, University of Würzburg, Würzburg, Germany (M.J.L.); Molecular Pharmacology Group, Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom (G.M.); Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5203, Institut de Génomique Fonctionnelle, Université Montpellier, Montpellier, France (J.-P.P.); and Institut National de la Santé et de la Recherche Médicale, U661, Montpellier, France (J.-P.P.)
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Ralf Jockers
Integrative Neurobiology Section, National Institute on Drug Addiction, Intramural Research Program, National Institutes of Health, Department of Health and Human Services, Baltimore, Maryland (S.F., X.G.); Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain (V.C.); Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas, Barcelona, Spain (V.C.); Department of Pharmacology and Systems Therapeutics (L.A.D.) and Department of Structural and Chemical Biology (M.F.), Icahn School of Medicine at Mount Sinai, Mount Sinai, New York; Institut National de la Santé et de la Recherche Médicale, U1016, Institut Cochin, Paris, France (R.J.); Centre National de la Recherche Scientifique Unité Mixte de Recherche 8104, Paris, France (R.J.); Universite Paris Descartes, Sorbone Paris Cite, Paris, France (R.J.); Institute of Pharmacology and Toxicology and Rudolf Virchow Center, University of Würzburg, Würzburg, Germany (M.J.L.); Molecular Pharmacology Group, Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom (G.M.); Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5203, Institut de Génomique Fonctionnelle, Université Montpellier, Montpellier, France (J.-P.P.); and Institut National de la Santé et de la Recherche Médicale, U661, Montpellier, France (J.-P.P.)
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Martin J. Lohse
Integrative Neurobiology Section, National Institute on Drug Addiction, Intramural Research Program, National Institutes of Health, Department of Health and Human Services, Baltimore, Maryland (S.F., X.G.); Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain (V.C.); Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas, Barcelona, Spain (V.C.); Department of Pharmacology and Systems Therapeutics (L.A.D.) and Department of Structural and Chemical Biology (M.F.), Icahn School of Medicine at Mount Sinai, Mount Sinai, New York; Institut National de la Santé et de la Recherche Médicale, U1016, Institut Cochin, Paris, France (R.J.); Centre National de la Recherche Scientifique Unité Mixte de Recherche 8104, Paris, France (R.J.); Universite Paris Descartes, Sorbone Paris Cite, Paris, France (R.J.); Institute of Pharmacology and Toxicology and Rudolf Virchow Center, University of Würzburg, Würzburg, Germany (M.J.L.); Molecular Pharmacology Group, Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom (G.M.); Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5203, Institut de Génomique Fonctionnelle, Université Montpellier, Montpellier, France (J.-P.P.); and Institut National de la Santé et de la Recherche Médicale, U661, Montpellier, France (J.-P.P.)
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Graeme Milligan
Integrative Neurobiology Section, National Institute on Drug Addiction, Intramural Research Program, National Institutes of Health, Department of Health and Human Services, Baltimore, Maryland (S.F., X.G.); Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain (V.C.); Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas, Barcelona, Spain (V.C.); Department of Pharmacology and Systems Therapeutics (L.A.D.) and Department of Structural and Chemical Biology (M.F.), Icahn School of Medicine at Mount Sinai, Mount Sinai, New York; Institut National de la Santé et de la Recherche Médicale, U1016, Institut Cochin, Paris, France (R.J.); Centre National de la Recherche Scientifique Unité Mixte de Recherche 8104, Paris, France (R.J.); Universite Paris Descartes, Sorbone Paris Cite, Paris, France (R.J.); Institute of Pharmacology and Toxicology and Rudolf Virchow Center, University of Würzburg, Würzburg, Germany (M.J.L.); Molecular Pharmacology Group, Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom (G.M.); Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5203, Institut de Génomique Fonctionnelle, Université Montpellier, Montpellier, France (J.-P.P.); and Institut National de la Santé et de la Recherche Médicale, U661, Montpellier, France (J.-P.P.)
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Jean-Philippe Pin
Integrative Neurobiology Section, National Institute on Drug Addiction, Intramural Research Program, National Institutes of Health, Department of Health and Human Services, Baltimore, Maryland (S.F., X.G.); Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain (V.C.); Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas, Barcelona, Spain (V.C.); Department of Pharmacology and Systems Therapeutics (L.A.D.) and Department of Structural and Chemical Biology (M.F.), Icahn School of Medicine at Mount Sinai, Mount Sinai, New York; Institut National de la Santé et de la Recherche Médicale, U1016, Institut Cochin, Paris, France (R.J.); Centre National de la Recherche Scientifique Unité Mixte de Recherche 8104, Paris, France (R.J.); Universite Paris Descartes, Sorbone Paris Cite, Paris, France (R.J.); Institute of Pharmacology and Toxicology and Rudolf Virchow Center, University of Würzburg, Würzburg, Germany (M.J.L.); Molecular Pharmacology Group, Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom (G.M.); Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5203, Institut de Génomique Fonctionnelle, Université Montpellier, Montpellier, France (J.-P.P.); and Institut National de la Santé et de la Recherche Médicale, U661, Montpellier, France (J.-P.P.)
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Xavier Guitart
Integrative Neurobiology Section, National Institute on Drug Addiction, Intramural Research Program, National Institutes of Health, Department of Health and Human Services, Baltimore, Maryland (S.F., X.G.); Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain (V.C.); Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas, Barcelona, Spain (V.C.); Department of Pharmacology and Systems Therapeutics (L.A.D.) and Department of Structural and Chemical Biology (M.F.), Icahn School of Medicine at Mount Sinai, Mount Sinai, New York; Institut National de la Santé et de la Recherche Médicale, U1016, Institut Cochin, Paris, France (R.J.); Centre National de la Recherche Scientifique Unité Mixte de Recherche 8104, Paris, France (R.J.); Universite Paris Descartes, Sorbone Paris Cite, Paris, France (R.J.); Institute of Pharmacology and Toxicology and Rudolf Virchow Center, University of Würzburg, Würzburg, Germany (M.J.L.); Molecular Pharmacology Group, Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom (G.M.); Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5203, Institut de Génomique Fonctionnelle, Université Montpellier, Montpellier, France (J.-P.P.); and Institut National de la Santé et de la Recherche Médicale, U661, Montpellier, France (J.-P.P.)
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Mark P. Mattson
Integrative Neurobiology Section, National Institute on Drug Addiction, Intramural Research Program, National Institutes of Health, Department of Health and Human Services, Baltimore, Maryland (S.F., X.G.); Department of Biochemistry and Molecular Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain (V.C.); Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas, Barcelona, Spain (V.C.); Department of Pharmacology and Systems Therapeutics (L.A.D.) and Department of Structural and Chemical Biology (M.F.), Icahn School of Medicine at Mount Sinai, Mount Sinai, New York; Institut National de la Santé et de la Recherche Médicale, U1016, Institut Cochin, Paris, France (R.J.); Centre National de la Recherche Scientifique Unité Mixte de Recherche 8104, Paris, France (R.J.); Universite Paris Descartes, Sorbone Paris Cite, Paris, France (R.J.); Institute of Pharmacology and Toxicology and Rudolf Virchow Center, University of Würzburg, Würzburg, Germany (M.J.L.); Molecular Pharmacology Group, Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom (G.M.); Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5203, Institut de Génomique Fonctionnelle, Université Montpellier, Montpellier, France (J.-P.P.); and Institut National de la Santé et de la Recherche Médicale, U661, Montpellier, France (J.-P.P.)
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Abstract

Most evidence indicates that, as for family C G protein–coupled receptors (GPCRs), family A GPCRs form homo- and heteromers. Homodimers seem to be a predominant species, with potential dynamic formation of higher-order oligomers, particularly tetramers. Although monomeric GPCRs can activate G proteins, the pentameric structure constituted by one GPCR homodimer and one heterotrimeric G protein may provide a main functional unit, and oligomeric entities can be viewed as multiples of dimers. It still needs to be resolved if GPCR heteromers are preferentially heterodimers or if they are mostly constituted by heteromers of homodimers. Allosteric mechanisms determine a multiplicity of possible unique pharmacological properties of GPCR homomers and heteromers. Some general mechanisms seem to apply, particularly at the level of ligand-binding properties. In the frame of the dimer-cooperativity model, the two-state dimer model provides the most practical method to analyze ligand–GPCR interactions when considering receptor homomers. In addition to ligand-binding properties, unique properties for each GPCR oligomer emerge in relation to different intrinsic efficacy of ligands for different signaling pathways (functional selectivity). This gives a rationale for the use of GPCR oligomers, and particularly heteromers, as novel targets for drug development. Herein, we review the functional and pharmacological properties of GPCR oligomers and provide some guidelines for the application of discrete direct screening and high-throughput screening approaches to the discovery of receptor-heteromer selective compounds.

Footnotes

  • This work was supported by the Intramural Research Program of the National Institutes of Health [National Institute on Drug Abuse] (to S.F. and X.G.); the National Institutes of Health National Institute on Drug Abuse [Grants DA026434 and DA034049 (to M.F.) and Grants DA008863 and DA019521 (to L.A.D.)]; “Ministerio de Ciencia y Tecnología” [Grant SAF2011-23813], “Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas” [Grant PI2011/02-7], and “Fondation Jerome Lejeune” [FJL-01/01/2013] (to V.C.); “Agence Nationale de la Recherche” [Grants ANR RPIB 2012 “MED-HET-REC-2”, ANR-11-IDEX-0005-01, and ANR-11-LABX-0071 (to R.J.) and ANR-12-BSV2-0015 and ARN-09-BIOT-018 (to J.-P.P.)]; “Fondation Recherche Médicale” [Grant FRM DEQ20130326503], “Institut National de la Santé et de la Recherche Médicale,” and “Centre National de la Recherche Scientifique” (to R.J.); European Research Council Advanced Grant “Topas” (to M.J.L.); and Medical Research Council [Grant G0900050] (to G.M.).

  • dx.doi.org/10.1124/pr.113.008052.

  • U.S. Government work not protected by U.S. copyright
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Pharmacological Reviews: 66 (2)
Pharmacological Reviews
Vol. 66, Issue 2
1 Apr 2014
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Review ArticleReview Article

G Protein–Coupled Receptor Oligomerization

Sergi Ferré, Vicent Casadó, Lakshmi A. Devi, Marta Filizola, Ralf Jockers, Martin J. Lohse, Graeme Milligan, Jean-Philippe Pin and Xavier Guitart
Pharmacological Reviews April 1, 2014, 66 (2) 413-434; DOI: https://doi.org/10.1124/pr.113.008052

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G Protein–Coupled Receptor Oligomerization

Sergi Ferré, Vicent Casadó, Lakshmi A. Devi, Marta Filizola, Ralf Jockers, Martin J. Lohse, Graeme Milligan, Jean-Philippe Pin and Xavier Guitart
Pharmacological Reviews April 1, 2014, 66 (2) 413-434; DOI: https://doi.org/10.1124/pr.113.008052
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    • Abstract
    • I. Morphologic Aspects of G Protein–Coupled Receptor Oligomerization
    • II. Functional Aspects of G Protein–Coupled Receptor Oligomerization
    • III. G Protein–Coupled Receptor Oligomers as Novel Targets for Drug Development
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