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J Biol Chem, Vol. 275, Issue 11, 7862-7869, March 17, 2000

Subtypes of the Somatostatin Receptor Assemble as Functional Homo- and Heterodimers*

Magalie RochevilleDagger §, Daniela C. LangeDagger , Ujendra KumarDagger , Ramakrishnan SasiDagger , Ramesh C. Patel, and Yogesh C. PatelDagger ||

From the Dagger  Fraser Laboratories, Departments of Medicine, Pharmacology and Therapeutics, and Neurology and Neurosurgery, McGill University and Royal Victoria Hospital, Montreal, Quebec H3A 1A1, Canada and the  Department of Physics and Chemistry, Clarkson University, Potsdam, New York 13676

The existence of receptor dimers has been proposed for several G protein-coupled receptors. However, the question of whether G protein-coupled receptor dimers are necessary for activating or modulating normal receptor function is unclear. We address this question with somatostatin receptors (SSTRs) of which there are five distinct subtypes. By using transfected mutant and wild type receptors, as well as endogenous receptors, we provide pharmacological, biochemical, and physical evidence, based on fluorescence resonance energy transfer analysis, that activation by ligand induces SSTR dimerization, both homo- and heterodimerization with other members of the SSTR family, and that dimerization alters the functional properties of the receptor such as ligand binding affinity and agonist-induced receptor internalization and up-regulation. Double label confocal fluorescence microscopy showed that when SSTR1 and SSTR5 subtypes were coexpressed in Chinese hamster ovary-K1 cells and treated with agonist they underwent internalization and were colocalized in cytoplasmic vesicles. SSTR5 formed heterodimers with SSTR1 but not with SSTR4 suggesting that heterodimerization is a specific process that is restricted to some but not all receptor subtype combinations. Direct protein interaction between different members of the SSTR subfamily defines a new level of molecular cross-talk between subtypes of the SSTR and possibly related receptor families.

* This work was supported by grants from the Canadian Medical Research Council, National Institutes of Health Grant NS32160-04, and the United States Department of Defense.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

This paper is dedicated to the memory of Monique Pellerin Rocheville.

§ Recipient of studentship support from the Fonds De La Recherche En Sante Du Quebec (FRSQ) and from the Royal Victoria Hospital Research Institute.

|| Distinguished Scientist of the Canadian Medical Research Council. To whom correspondence should be addressed: Royal Victoria Hospital, Rm. M3-15, 687 Pine Ave. West, Montreal, Quebec H3A 1A1, Canada. Tel.: 514-842-1231 (ext. 5042); Fax: 514-849-3681; E-mail: yogesh.patel@muhc.mcgill.ca.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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L. J. Hofland, S. W.J. Lamberts, P. M. van Hagen, J.-C. Reubi, J. Schaeffer, M. Waaijers, P. M. van Koetsveld, A. Srinivasan, E. P. Krenning, and W. A.P. Breeman
Crucial Role for Somatostatin Receptor Subtype 2 in Determining the Uptake of [111In-DTPA-D-Phe1]Octreotide in Somatostatin Receptor-Positive Organs
J. Nucl. Med., August 1, 2003; 44(8): 1315 - 1321.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
S. Terrillon, T. Durroux, B. Mouillac, A. Breit, M. A. Ayoub, M. Taulan, R. Jockers, C. Barberis, and M. Bouvier
Oxytocin and Vasopressin V1a and V2 Receptors Form Constitutive Homo- and Heterodimers during Biosynthesis
Mol. Endocrinol., April 1, 2003; 17(4): 677 - 691.
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I. M. P. Joseph, Y. Zavros, J. L. Merchant, and D. Kirschner
A model for integrative study of human gastric acid secretion
J Appl Physiol, April 1, 2003; 94(4): 1602 - 1618.
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M. C. Dinger, J. E. Bader, A. D. Kobor, A. K. Kretzschmar, and A. G. Beck-Sickinger
Homodimerization of Neuropeptide Y Receptors Investigated by Fluorescence Resonance Energy Transfer in Living Cells
J. Biol. Chem., March 14, 2003; 278(12): 10562 - 10571.
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 J. Biol. Chem.Home page
J. Xu, J. He, A. M. Castleberry, S. Balasubramanian, A. G. Lau, and R. A. Hall
Heterodimerization of alpha 2A- and beta 1-Adrenergic Receptors
J. Biol. Chem., March 14, 2003; 278(12): 10770 - 10777.
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 Endocr. Rev.Home page
L. J. Hofland and S. W. J. Lamberts
The Pathophysiological Consequences of Somatostatin Receptor Internalization and Resistance
Endocr. Rev., February 1, 2003; 24(1): 28 - 47.
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A. C. Hanyaloglu, R. M. Seeber, T. A. Kohout, R. J. Lefkowitz, and K. A. Eidne
Homo- and Hetero-oligomerization of Thyrotropin-releasing Hormone (TRH) Receptor Subtypes. DIFFERENTIAL REGULATION OF beta -ARRESTINS 1 AND 2
J. Biol. Chem., December 20, 2002; 277(52): 50422 - 50430.
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 J. Clin. Endocrinol. Metab.Home page
A. Saveanu, E. Lavaque, G. Gunz, A. Barlier, S. Kim, J. E. Taylor, M. D. Culler, A. Enjalbert, and P. Jaquet
Demonstration of Enhanced Potency of a Chimeric Somatostatin-Dopamine Molecule, BIM-23A387, in Suppressing Growth Hormone and Prolactin Secretion from Human Pituitary Somatotroph Adenoma Cells
J. Clin. Endocrinol. Metab., December 1, 2002; 87(12): 5545 - 5552.
[Abstract] [Full Text] [PDF]

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J.-F. Mercier, A. Salahpour, S. Angers, A. Breit, and M. Bouvier
Quantitative Assessment of beta 1- and beta 2-Adrenergic Receptor Homo- and Heterodimerization by Bioluminescence Resonance Energy Transfer
J. Biol. Chem., November 15, 2002; 277(47): 44925 - 44931.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. Latif, P. Graves, and T. F. Davies
Ligand-dependent Inhibition of Oligomerization at the Human Thyrotropin Receptor
J. Biol. Chem., November 15, 2002; 277(47): 45059 - 45067.
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 J. Biol. Chem.Home page
P. Scholze, M. Freissmuth, and H. H. Sitte
Mutations within an Intramembrane Leucine Heptad Repeat Disrupt Oligomer Formation of the Rat GABA Transporter 1
J. Biol. Chem., November 8, 2002; 277(46): 43682 - 43690.
[Abstract] [Full Text] [PDF]

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 Protein Eng Des SelHome page
M. Filizola, O. Olmea, and H. Weinstein
Prediction of heterodimerization interfaces of G-protein coupled receptors with a new subtractive correlated mutation method
Protein Eng. Des. Sel., November 1, 2002; 15(11): 881 - 885.
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 Cancer Res.Home page
W.-Q. Ding, Z.-J. Cheng, J. McElhiney, S. M. Kuntz, and L. J. Miller
Silencing of Secretin Receptor Function by Dimerization with a Misspliced Variant Secretin Receptor in Ductal Pancreatic Adenocarcinoma
Cancer Res., September 15, 2002; 62(18): 5223 - 5229.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C. Lavoie, J.-F. Mercier, A. Salahpour, D. Umapathy, A. Breit, L.-R. Villeneuve, W.-Z. Zhu, R.-P. Xiao, E. G. Lakatta, M. Bouvier, et al.
beta 1/beta 2-Adrenergic Receptor Heterodimerization Regulates beta 2-Adrenergic Receptor Internalization and ERK Signaling Efficacy
J. Biol. Chem., September 13, 2002; 277(38): 35402 - 35410.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. M. J. Buchan, C.-Y. Lin, J. Choi, and D. L. Barber
Somatostatin, Acting at Receptor Subtype 1, Inhibits Rho Activity, the Assembly of Actin Stress Fibers, and Cell Migration
J. Biol. Chem., August 2, 2002; 277(32): 28431 - 28438.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
C. Chisholm and G. R. Greenberg
Somatostatin-28 regulates GLP-1 secretion via somatostatin receptor subtype 5 in rat intestinal cultures
Am J Physiol Endocrinol Metab, August 1, 2002; 283(2): E311 - E317.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C.-C. Zhu, L. B. Cook, and P. M. Hinkle
Dimerization and Phosphorylation of Thyrotropin-releasing Hormone Receptors Are Modulated by Agonist Stimulation
J. Biol. Chem., July 26, 2002; 277(31): 28228 - 28237.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. A. Ayoub, C. Couturier, E. Lucas-Meunier, S. Angers, P. Fossier, M. Bouvier, and R. Jockers
Monitoring of Ligand-independent Dimerization and Ligand-induced Conformational Changes of Melatonin Receptors in Living Cells by Bioluminescence Resonance Energy Transfer
J. Biol. Chem., June 7, 2002; 277(24): 21522 - 21528.
[Abstract] [Full Text] [PDF]

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 Pharmacol. Rev.Home page
A. Christopoulos and T. Kenakin
G Protein-Coupled Receptor Allosterism and Complexing
Pharmacol. Rev., June 1, 2002; 54(2): 323 - 374.
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 J. Biol. Chem.Home page
M. Pfeiffer, T. Koch, H. Schroder, M. Laugsch, V. Hollt, and S. Schulz
Heterodimerization of Somatostatin and Opioid Receptors Cross-modulates Phosphorylation, Internalization, and Desensitization
J. Biol. Chem., May 24, 2002; 277(22): 19762 - 19772.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
S. Grunewald, B. J. Schupp, S. R. Ikeda, R. Kuner, F. Steigerwald, H.-C. Kornau, and G. Kohr
Importance of the gamma -Aminobutyric AcidB Receptor C-Termini for G-Protein Coupling
Mol. Pharmacol., May 1, 2002; 61(5): 1070 - 1080.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
R. C. Patel, U. Kumar, D. C. Lamb, J. S. Eid, M. Rocheville, M. Grant, A. Rani, T. Hazlett, S. C. Patel, E. Gratton, et al.
Ligand binding to somatostatin receptors induces receptor-specific oligomer formation in live cells
PNAS, March 5, 2002; 99(5): 3294 - 3299.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
J. L. Ramirez, F. Gracia-Navarro, S. Garcia-Navarro, R. Torronteras, M. M. Malagon, and J. P. Castano
Somatostatin Stimulates GH Secretion in Two Porcine Somatotrope Subpopulations through a cAMP-Dependent Pathway
Endocrinology, March 1, 2002; 143(3): 889 - 897.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. J. Miret, L. Rakhilina, L. Silverman, and B. Oehlen
Functional Expression of Heteromeric Calcitonin Gene-related Peptide and Adrenomedullin Receptors in Yeast
J. Biol. Chem., February 22, 2002; 277(9): 6881 - 6887.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Z.-J. Cheng and L. J. Miller
Agonist-dependent Dissociation of Oligomeric Complexes of G Protein-coupled Cholecystokinin Receptors Demonstrated in Living Cells Using Bioluminescence Resonance Energy Transfer
J. Biol. Chem., December 14, 2001; 276(51): 48040 - 48047.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
L. Gama, S. G. Wilt, and G. E. Breitwieser
Heterodimerization of Calcium Sensing Receptors with Metabotropic Glutamate Receptors in Neurons
J. Biol. Chem., October 12, 2001; 276(42): 39053 - 39059.
[Abstract] [Full Text] [PDF]

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 Protein Eng Des SelHome page
P. R. Gouldson, M. K. Dean, C. R. Snell, R. P. Bywater, G. Gkoutos, and C. A. Reynolds
Lipid-facing correlated mutations and dimerization in G-protein coupled receptors
Protein Eng. Des. Sel., October 1, 2001; 14(10): 759 - 767.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
E. Ballare, L. Persani, A. G. Lania, M. Filopanti, E. Giammona, S. Corbetta, S. Mantovani, M. Arosio, P. Beck-Peccoz, G. Faglia, et al.
Mutation of Somatostatin Receptor Type 5 in an Acromegalic Patient Resistant to Somatostatin Analog Treatment
J. Clin. Endocrinol. Metab., August 1, 2001; 86(8): 3809 - 3814.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
N. Sharma, J. Hewett, L. J. Ozelius, V. Ramesh, P. J. McLean, X. O. Breakefield, and B. T. Hyman
A Close Association of TorsinA and {{alpha}}-Synuclein in Lewy Bodies : A Fluorescence Resonance Energy Transfer Study
Am. J. Pathol., July 1, 2001; 159(1): 339 - 344.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
K. Yoshioka, O. Saitoh, and H. Nakata
Heteromeric association creates a P2Y-like adenosine receptor
PNAS, May 30, 2001; (2001) 121587098.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
M. C. Zatelli, F. Tagliati, J. E. Taylor, R. Rossi, M. D. Culler, and E. C. degli Uberti
Somatostatin Receptor Subtypes 2 and 5 Differentially Affect Proliferation in Vitro of the Human Medullary Thyroid Carcinoma Cell Line TT
J. Clin. Endocrinol. Metab., May 1, 2001; 86(5): 2161 - 2169.
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G Milligan
Oligomerisation of G-protein-coupled receptors
J. Cell Sci., January 4, 2001; 114(7): 1265 - 1271.
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 J. Clin. Endocrinol. Metab.Home page
A. Saveanu, G. Gunz, H. Dufour, P. Caron, F. Fina, L. Ouafik, M. D. Culler, J. P. Moreau, A. Enjalbert, and P. Jaquet
BIM-23244, a Somatostatin Receptor Subtype 2- and 5-Selective Analog with Enhanced Efficacy in Suppressing Growth Hormone (GH) from Octreotide-Resistant Human GH-Secreting Adenomas
J. Clin. Endocrinol. Metab., January 1, 2001; 86(1): 140 - 145.
[Abstract] [Full Text]

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 Proc. Natl. Acad. Sci. USAHome page
B. A. Jordan, N. Trapaidze, I. Gomes, R. Nivarthi, and L. A. Devi
Oligomerization of opioid receptors with beta 2-adrenergic receptors: A role in trafficking and mitogen-activated protein kinase activation
PNAS, December 22, 2000; (2000) 11384898.
[Abstract] [Full Text]

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 EndocrinologyHome page
S. Park, J. Kamegai, T. A. Johnson, L. A. Frohman, and R. D. Kineman
Modulation of Pituitary Somatostatin Receptor Subtype (sst1-5) Messenger Ribonucleic Acid Levels by Changes in the Growth Hormone Axis
Endocrinology, October 1, 2000; 141(10): 3556 - 3563.
[Abstract] [Full Text] [PDF]

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 ScienceHome page
M. Rocheville, D. C. Lange, U. Kumar, S. C. Patel, R. C. Patel, and Y. C. Patel
Receptors for Dopamine and Somatostatin: Formation of Hetero-Oligomers with Enhanced Functional Activity
Science, April 7, 2000; 288(5463): 154 - 157.
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 J. Biol. Chem.Home page
M. Pfeiffer, T. Koch, H. Schroder, M. Klutzny, S. Kirscht, H.-J. Kreienkamp, V. Hollt, and S. Schulz
Homo- and Heterodimerization of Somatostatin Receptor Subtypes. INACTIVATION OF sst3 RECEPTOR FUNCTION BY HETERODIMERIZATION WITH sst2A
J. Biol. Chem., April 20, 2001; 276(17): 14027 - 14036.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. A. Schmid, P. Scholze, O. Kudlacek, M. Freissmuth, E. A. Singer, and H. H. Sitte
Oligomerization of the Human Serotonin Transporter and of the Rat GABA Transporter 1 Visualized by Fluorescence Resonance Energy Transfer Microscopy in Living Cells
J. Biol. Chem., February 2, 2001; 276(6): 3805 - 3810.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. Cornea, J. A. Janovick, G. Maya-Nunez, and P. M. Conn
Gonadotropin-releasing Hormone Receptor Microaggregation. RATE MONITORED BY FLUORESCENCE RESONANCE ENERGY TRANSFER
J. Biol. Chem., January 12, 2001; 276(3): 2153 - 2158.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. McVey, D. Ramsay, E. Kellett, S. Rees, S. Wilson, A. J. Pope, and G. Milligan
Monitoring Receptor Oligomerization Using Time-resolved Fluorescence Resonance Energy Transfer and Bioluminescence Resonance Energy Transfer. THE HUMAN delta -OPIOID RECEPTOR DISPLAYS CONSTITUTIVE OLIGOMERIZATION AT THE CELL SURFACE, WHICH IS NOT REGULATED BY RECEPTOR OCCUPANCY
J. Biol. Chem., April 20, 2001; 276(17): 14092 - 14099.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. M. Kroeger, A. C. Hanyaloglu, R. M. Seeber, L. E. C. Miles, and K. A. Eidne
Constitutive and Agonist-dependent Homo-oligomerization of the Thyrotropin-releasing Hormone Receptor. DETECTION IN LIVING CELLS USING BIOLUMINESCENCE RESONANCE ENERGY TRANSFER
J. Biol. Chem., April 13, 2001; 276(16): 12736 - 12743.
[Abstract] [Full Text] [PDF]


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