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Science 288 (5463): 154-157

Copyright © 2000 by the American Association for the Advancement of Science

Receptors for Dopamine and Somatostatin: Formation of Hetero-Oligomers with Enhanced Functional Activity

Magalie Rocheville, 1 Daniela C. Lange, 2 Ujendra Kumar, 1 Shutish C. Patel, 3 Ramesh C. Patel, 2 Yogesh C. Patel 1*

Somatostatin and dopamine are two major neurotransmitter systems that share a number of structural and functional characteristics. Somatostatin receptors and dopamine receptors are colocalized in neuronal subgroups, and somatostatin is involved in modulating dopamine-mediated control of motor activity. However, the molecular basis for such interaction between the two systems is unclear. Here, we show that dopamine receptor D2R and somatostatin receptor SSTR5 interact physically through hetero-oligomerization to create a novel receptor with enhanced functional activity. Our results provide evidence that receptors from different G protein (heterotrimeric guanine nucleotide binding protein)-coupled receptor families interact through oligomerization. Such direct intramembrane association defines a new level of molecular crosstalk between related G protein-coupled receptor subfamilies.

1 Fraser Laboratories, Departments of Medicine, Pharmacology, Therapeutics, Neurology, and Neurosurgery, McGill University and Royal Victoria Hospital, Montreal, Quebec H3A 1A1, Canada.
2 Departments of Physics and Chemistry, Clarkson University, Potsdam, NY 13699, USA.
3 VA Connecticut Healthcare System and New England Biomedical Research Center, Newington, CT 06111, USA.
*   To whom correspondence should be addressed. E-mail: yogesh.patel{at}muhc.mcgill.ca

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Preferential Formation of MT1/MT2 Melatonin Receptor Heterodimers with Distinct Ligand Interaction Properties Compared with MT2 Homodimers.
M. A. Ayoub, A. Levoye, P. Delagrange, and R. Jockers (2004)
Mol. Pharmacol. 66, 312-321
   Abstract »    Full Text »    PDF »
Hetero-oligomerization between {beta}2- and {beta}3-Adrenergic Receptors Generates a {beta}-Adrenergic Signaling Unit with Distinct Functional Properties.
A. Breit, M. Lagace, and M. Bouvier (2004)
J. Biol. Chem. 279, 28756-28765
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Molecular Structure and Physiological Functions of GABAB Receptors.
B. Bettler, K. Kaupmann, J. Mosbacher, and M. Gassmann (2004)
Physiol Rev 84, 835-867
   Abstract »    Full Text »    PDF »
G Protein-Coupled Receptor Dimerization: Function and Ligand Pharmacology.
G. Milligan (2004)
Mol. Pharmacol. 66, 1-7
   Abstract »    Full Text »    PDF »
Oligomerisation of angiotensin receptors: novel aspects in disease and drug therapy.
L. Barki-Harrington (2004)
Journal of Renin-Angiotensin-Aldosterone System 5, 49-52
   Abstract »    PDF »
Minireview: Diversity and Complexity of Signaling through Peptidergic G Protein-Coupled Receptors.
A. J. Rashid, B. F. O'Dowd, and S. R. George (2004)
Endocrinology 145, 2645-2652
   Abstract »    Full Text »    PDF »
Synaptic activity-independent persistent plasticity in endogenously active mammalian motoneurons.
C. M. Bocchiaro and J. L. Feldman (2004)
PNAS 101, 4292-4295
   Abstract »    Full Text »    PDF »
The Paired Activation of the Two Components of the Muscarinic M3 Receptor Dimer Is Required for Induction of ERK1/2 Phosphorylation.
F. Novi, M. Scarselli, G. U. Corsini, and R. Maggio (2004)
J. Biol. Chem. 279, 7476-7486
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Neuropeptide Y Y4 Receptor Homodimers Dissociate upon Agonist Stimulation.
M. M. Berglund, D. A. Schober, M. A. Esterman, and D. R. Gehlert (2003)
J. Pharmacol. Exp. Ther. 307, 1120-1126
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The Sleep-Modulating Peptide Cortistatin Augments the h-Current in Hippocampal Neurons.
P. Schweitzer, S. G. Madamba, and G. R. Siggins (2003)
J. Neurosci. 23, 10884-10891
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Adenosine A2A-Dopamine D2 Receptor-Receptor Heteromerization: QUALITATIVE AND QUANTITATIVE ASSESSMENT BY FLUORESCENCE AND BIOLUMINESCENCE ENERGY TRANSFER.
M. Canals, D. Marcellino, F. Fanelli, F. Ciruela, P. de Benedetti, S. R. Goldberg, K. Neve, K. Fuxe, L. F. Agnati, A. S. Woods, et al. (2003)
J. Biol. Chem. 278, 46741-46749
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Somatostatin Receptors 2 and 5 Are the Major Somatostatin Receptors in Insulinomas: An in Vivo and in Vitro Study.
J. Bertherat, F. Tenenbaum, K. Perlemoine, C. Videau, J. L. Alberini, B. Richard, B. Dousset, X. Bertagna, and J. Epelbaum (2003)
J. Clin. Endocrinol. Metab. 88, 5353-5360
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Suppression of Rat and Human Growth Hormone and Prolactin Secretion by a Novel Somatostatin/Dopaminergic Chimeric Ligand.
S.-G. Ren, S. Kim, J. Taylor, J. Dong, J.-P. Moreau, M. D. Culler, and S. Melmed (2003)
J. Clin. Endocrinol. Metab. 88, 5414-5421
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Dimers of Class A G Protein-coupled Receptors Function via Agonist-mediated Trans-activation of Associated G Proteins.
J. J. Carrillo, J. Pediani, and G. Milligan (2003)
J. Biol. Chem. 278, 42578-42587
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Ligand-independent CXCR2 Dimerization.
F. Trettel, S. Di Bartolomeo, C. Lauro, M. Catalano, M. T. Ciotti, and C. Limatola (2003)
J. Biol. Chem. 278, 40980-40988
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Oligomerization of the {alpha}1a- and {alpha}1b-Adrenergic Receptor Subtypes: POTENTIAL IMPLICATIONS IN RECEPTOR INTERNALIZATION.
L. Stanasila, J.-B. Perez, H. Vogel, and S. Cotecchia (2003)
J. Biol. Chem. 278, 40239-40251
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Experimental Evidence for Lack of Homodimerization of the G Protein-Coupled Human N-Formyl Peptide Receptor.
J. M. Gripentrog, K. P. Kantele, A. J. Jesaitis, and H. M. Miettinen (2003)
J. Immunol. 171, 3187-3193
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Functional Association of Somatostatin Receptor Subtypes 2 and 5 in Inhibiting Human Growth Hormone Secretion.
S.-G. Ren, J. Taylor, J. Dong, R. Yu, M. D. Culler, and S. Melmed (2003)
J. Clin. Endocrinol. Metab. 88, 4239-4245
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Molecular Mechanisms and Therapeutical Implications of Intramembrane Receptor/Receptor Interactions among Heptahelical Receptors with Examples from the Striatopallidal GABA Neurons.
L. F. Agnati, S. Ferre, C. Lluis, R. Franco, and K. Fuxe (2003)
Pharmacol. Rev. 55, 509-550
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Peptide Receptors as Molecular Targets for Cancer Diagnosis and Therapy.
J. C. Reubi (2003)
Endocr. Rev. 24, 389-427
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Activation of the Leptin Receptor by a Ligand-induced Conformational Change of Constitutive Receptor Dimers.
C. Couturier and R. Jockers (2003)
J. Biol. Chem. 278, 26604-26611
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Hypersensitization of the Orexin 1 Receptor by the CB1 Receptor: EVIDENCE FOR CROSS-TALK BLOCKED BY THE SPECIFIC CB1 ANTAGONIST, SR141716.
S. Hilairet, M. Bouaboula, D. Carriere, G. Le Fur, and P. Casellas (2003)
J. Biol. Chem. 278, 23731-23737
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The Alternatively Spliced {Delta}e13 Transcript of the Rabbit Calcitonin Receptor Dimerizes with the C1a Isoform and Inhibits Its Surface Expression.
T. Seck, R. Baron, and W. C. Horne (2003)
J. Biol. Chem. 278, 23085-23093
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Oxytocin and Vasopressin V1a and V2 Receptors Form Constitutive Homo- and Heterodimers during Biosynthesis.
S. Terrillon, T. Durroux, B. Mouillac, A. Breit, M. A. Ayoub, M. Taulan, R. Jockers, C. Barberis, and M. Bouvier (2003)
Mol. Endocrinol. 17, 677-691
   Abstract »    Full Text »    PDF »
Evidence for CD4-enchanced Signaling through the Chemokine Receptor CCR5.
R. Staudinger, S. K. Phogat, X. Xiao, X. Wang, D. S. Dimitrov, and S. Zolla-Pazner (2003)
J. Biol. Chem. 278, 10389-10392
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