Cross-talk between dopamine D1 and corticotropin releasing factor type 2 receptors leads to occlusion of their ERK1/2 signaling.
Animals
Corticotropin-Releasing Hormone
/ metabolism
Dopamine
/ metabolism
Dose-Response Relationship, Drug
HEK293 Cells
Humans
MAP Kinase Signaling System
/ drug effects
Male
Rats
Rats, Sprague-Dawley
Receptor Cross-Talk
/ drug effects
Receptors, Corticotropin-Releasing Hormone
/ agonists
Receptors, Dopamine D1
/ agonists
ERK signaling
dopamine D1 receptor
heteromerization
synaptosomes
type-2α CRF receptor
Journal
Journal of neurochemistry
ISSN: 1471-4159
Titre abrégé: J Neurochem
Pays: England
ID NLM: 2985190R
Informations de publication
Date de publication:
11 2020
11 2020
Historique:
received:
17
07
2019
revised:
04
02
2020
accepted:
12
03
2020
pubmed:
28
3
2020
medline:
11
3
2021
entrez:
28
3
2020
Statut:
ppublish
Résumé
One manner in which G protein-coupled receptors potentiate, increase, and change their functionality is through the formation of heteromers in a specific cellular context. Previously, we have shown that dopamine D1 receptor (D1R) and the corticotropin releasing factor receptor type-2α (CRF2α) heteromerize in HEK293T cells, enabling D1R to mobilize intracellular calcium in response to D1R agonists. In this study, we further investigated the pharmacological properties of the CRF2α-D1R heteromer and the consequences of the heteromerization in their signaling and subcellular localization when both receptors are co-expressed in HEK293T cells. Using immunoprecipitation assays, we observed that the addition of 10 μM dopamine in the incubation medium significantly decreased the amount of CRF2α on the cell surface of cells expressing both receptors. The presence of agonists of both receptors increased the interaction between CRF2α and D1R as assessed by co-immunoprecipitation. However, the presence of agonists of both receptors resulted in a lesser efficient activation of the mitogen-activated protein kinase/extracellular signal-regulated kinase. Using a synaptosomal preparation of rat prefrontal cortex devoid of post-synaptic elements, we found that CRF2α and D1R co-localize in synaptic terminals of the rat medial prefrontal cortex and that the simultaneous activation of both receptors also occluded phosphorylation of extracellular signal-regulated kinase. These results strengthen the idea that the heteromer CRF2a-D1R is an entity functionally different from each receptor that composes it and suggests that its formation is enhanced by CRF and dopamine co-transmission, as occurs in stress and addiction.
Substances chimiques
CRF receptor type 2
0
Drd1 protein, rat
0
Receptors, Corticotropin-Releasing Hormone
0
Receptors, Dopamine D1
0
Corticotropin-Releasing Hormone
9015-71-8
Dopamine
VTD58H1Z2X
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
264-273Informations de copyright
© 2020 International Society for Neurochemistry.
Références
AbdAlla, S., Zaki, E., Lother, H., & Quitterer, U. (1999). Involvement of the amino terminus of the B(2) receptor in agonist-induced receptor dimerization. Journal of Biological Chemistry, 274, 26079-26084.
Angers, S., Salahpour, A., & Bouvier, M. (2002). Dimerization: An emerging concept for G protein-coupled receptor ontogeny and function. Annual Review of Pharmacology and Toxicology, 42, 409-435.
Blacktop, J. M., Seubert, C., Baker, D. A., Ferda, N., Lee, G., Graf, E. N., & Mantsch, J. R. (2011). Augmented cocaine seeking in response to stress or CRF delivered into the ventral tegmental area following long-access self-administration is mediated by CRF receptor type 1 but not CRF receptor type 2. Journal of Neuroscience, 31, 11396-11403. https://doi.org/10.1523/JNEUROSCI.1393-11.2011
Bonfiglio, J. J., Inda, C., Senin, S., Maccarrone, G., Refojo, D., Giacomini, D., … Silberstein, S. (2013). B-Raf and CRHR1 internalization mediate biphasic ERK1/2 activation by CRH in hippocampal HT22 Cells. Molecular Endocrinology, 27, 491-510.
Brar, B. K., Chen, A., Perrin, M. H., & Vale, W. (2004). Specificity and regulation of extracellularly regulated kinase1/2 phosphorylation through corticotropin-releasing factor (CRF) receptors 1 and 2 beta by the CRF/urocortin family of peptides. Endocrinology, 145, 1718-1729.
Breit, A., Lagacé, M., & Bouvier, M. (2004). Hetero-oligomerization between beta2- and beta3-adrenergic receptors generates a beta-adrenergic signalling unit with distinct functional properties. Journal of Biological Chemistry, 279, 28756-28765.
Burke, K. J. Jr, Keeshen, C. M., & Bender, K. J. (2018). Two Forms of Synaptic Depression Produced by Differential Neuromodulation of Presynaptic Calcium Channels. Neuron, 99, 969-984. https://doi.org/10.1016/j.neuron.2018.07.030
Calabresi, P., Picconi, B., Tozzi, A., Ghiglieri, V., & Di Filippo, M. (2014). Direct and indirect pathways of basal ganglia: A critical reappraisal. Nature Neuroscience, 17, 1022-1030. https://doi.org/10.1038/nn.3743
Chen, A., Perrin, M., Brar, B., Li, C., Jamieson, P., Digruccio, M., … Vale, W. (2005). Mouse corticotropin-releasing factor receptor type 2alpha gene: Isolation, distribution, pharmacological characterization and regulation by stress and glucocorticoids. Molecular Endocrinology, 19, 441-458.
Chun, L. S., Free, R. B., Doyle, T. B., Huang, X. P., Rankin, M. L., & Sibley, D. R. (2013). D1-D2 dopamine receptor synergy promotes calcium signalling via multiple mechanisms. Molecular Pharmacology, 84, 190-200.
Ciruela, F., Casadó, V., Rodrigues, R. J., Luján, R., Burgueño, J., Canals, M., … Franco, R. (2006). Presynaptic control of striatal glutamatergic neurotransmission by adenosine A1-A2A receptor heteromers. Journal of Neuroscience, 26, 2080-2087. https://doi.org/10.1523/JNEUROSCI.3574-05.2006
Corominas, M., Roncero, C., & Casas, M. (2010). Corticotropin releasing factor and neuroplasticity in cocaine addiction. Life Sciences, 86, 1-9. https://doi.org/10.1016/j.lfs.2009.11.005
Cvejic, S., & Devi, L. A. (1997). Dimerization of the delta opioid receptor: Implication for a role in receptor internalization. Journal of Biological Chemistry, 272, 26959-26964.
Devi, L. A. (2001). Heterodimerization of G-protein-coupled receptors: Pharmacology, signaling and trafficking. Trends in Pharmacological Sciences, 22, 532-537.
Everitt, B. J. (2014). Neural and psychological mechanisms underlying compulsive drug seeking habits and drug memories-indications for novel treatments of addiction. European Journal of Neuroscience, 40, 2163-2182.
Ferrada, C., Moreno, E., Casadó, V., Bongers, G., Cortés, A., Mallol, J., … Franco, R. (2009). Marked changes in signal transduction upon heteromerization of dopamine D1 and histamine H3 receptors. British Journal of Pharmacology, 157, 64-75.
Ferré, S., Lluís, C., Justinova, Z., Quiroz, C., Orru, M., Navarro, G., … Goldberg, S. R. (2010). Adenosine-cannabinoid receptor interactions. Implications for striatal function. British Journal of Pharmacology, 160, 443-453.
Fuenzalida, J., Galaz, P., Araya, K. A., Slater, P. G., Blanco, E. H., Campusano, J. M., … Gysling, K. (2014). Dopamine D1 and corticotrophin-releasing hormone type-2α receptors assemble into functionally interacting complexes in living cells. British Journal of Pharmacology, 171, 5650-5664.
Grammatopoulos, D. K., & Chrousos, G. P. (2002). Functional characteristics of CRH receptors and potential clinical applications of CRH-receptor antagonists. Trends in Endocrinology and Metabolism, 13, 436-444.
Gysling, K. (2012). Relevance of both type-1 and type-2 corticotropin releasing factor receptors in stress-induced relapse to cocaine seeking behaviour. Biochemical Pharmacology, 83, 1-5. https://doi.org/10.1016/j.bcp.2011.07.101
Hahn, J., Hopf, F. W., & Bonci, A. (2009). Chronic cocaine enhances corticotropin-releasing factor-dependent potentiation of excitatory transmission in ventral tegmental area dopamine neurons. Journal of Neuroscience, 29, 6535-6544. https://doi.org/10.1523/JNEUROSCI.4773-08.2009
Hauger, R. L., Olivares-Reyes, J. A., Braun, S., Hernandez-Aranda, J., Hudson, C. C., Gutknecht, E., … Oakley, R. H. (2013). Desensitization of human CRF2(a) receptor signalling governed by agonist potency and βarrestin2 recruitment. Regulatory Peptides, 186, 62-76.
Inda, C., Dos Santos Claro, P. A., Bonfiglio, J. J., Senin, S. A., Maccarrone, G., Turck, C. W., & Silberstein, S. (2016). Different cAMP sources are critically involved in G protein-coupled receptor CRHR1 signalling. Journal of Cell Biology, 214, 181-195.
Kalivas, P. W., & Duffy, P. (1995). D1 receptors modulate glutamate transmission in the ventral tegmental area. Journal of Neuroscience, 15, 5379-5388. https://doi.org/10.1523/JNEUROSCI.15-07-05379.1995
Kalivas, P. W., & Duffy, P. (1998). Repeated cocaine administration alters extracellular glutamate in the ventral tegmental area. Journal of Neurochemistry, 70, 1497-1502. https://doi.org/10.1046/j.1471-4159.1998.70041497.x
Kotowski, S. J., Hopf, F. W., Seif, T., Bonci, A., & von Zastrow, M. (2011). Endocytosis promotes rapid dopaminergic signalling. Neuron, 71, 278-290.
Lin, T. Y., Lin, Y. W., Lu, C. W., Huang, S. K., & Wang, S. J. (2013). Berberine inhibits the release of glutamate in nerve terminals from rat cerebral cortex. PLoS ONE, 8, e67215. https://doi.org/10.1371/journal.pone.0067215
Lin, T. Y., Yang, T. T., Lu, C. W., & Wang, S. J. (2011). Inhibition of glutamate release by bupropion in rat cerebral cortex nerve terminals. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 35, 598-606. https://doi.org/10.1016/j.pnpbp.2010.12.029
Liu, J., Yu, B., Orozco-Cabal, L., Grigoriadis, D. E., Rivier, J., Vale, W. W., … Gallagher, J. P. (2005). Chronic cocaine administration switches corticotropin-releasing factor 2 receptor-mediated depression to facilitation of glutamatergic transmission in the lateral septum. Journal of Neuroscience, 25, 577-583. https://doi.org/10.1523/JNEUROSCI.4196-04.2005
Luttrell, L. M., & Lefkowitz, R. J. (2002). The role of beta-arrestins in the termination and transduction of G-protein-coupled receptor signals. Journal of Cell Science, 115, 455-465.
Magalhaes, A. C., Dunn, H., & Ferguson, S. S. (2012). Regulation of GPCR activity, trafficking and localization by GPCR-interacting proteins. British Journal of Pharmacology, 165, 1717-1736.
Magalhaes, A. C., Holmes, K. D., Dale, L. B., Comps-Agrar, L., Lee, D., Yadav, P. N., … Ferguson, S. S. (2010). CRF receptor 1 regulates anxiety behavior via sensitization of 5-HT2 receptor signalling. Nature Neuroscience, 13, 622-629.
Markovic, D., Punn, A., Lehnert, H., & Grammatopoulos, D. K. (2008). Intracellular mechanisms regulating corticotropin-releasing hormone receptor-2beta endocytosis and interaction with extracellularly regulated kinase 1/2 and p38 mitogen-activated protein kinase signalling cascades. Molecular Endocrinology, 22, 689-706.
Mellado, M., Rodríguez-Frade, J. M., Vila-Coro, A. J., Fernández, S., Martín de Ana, A., Jones, D. R., … Martínez-A, C. (2001). Chemokine receptor homo- or heterodimerization activates distinct signalling pathways. EMBO Journal, 20, 2497-2507.
Navarro, G., Quiroz, C., Moreno-Delgado, D., Sierakowiak, A., McDowell, K., Moreno, E., … McCormick, P. J. (2015). Orexin-corticotropin-releasing factor receptor heteromers in the ventral tegmental area as targets for cocaine. Journal of Neuroscience, 35, 6639-6653. https://doi.org/10.1523/JNEUROSCI.4364-14.2015
Neve, K. A., Seamans, J. K., & Trantham-Davidson, H. (2004). Dopamine receptor signalling. J. Recept. Signal Transduct. Res., 24, 165-205.
O'Dowd, B. F., Ji, X., Alijaniaram, M., Nguyen, T., & George, S. R. (2011). Separation and reformation of cell surface dopamine receptor oligomers visualized in cells. European Journal of Pharmacology, 658, 74-83.
Orozco-Cabal, L., Liu, J., Pollandt, S., Schmidt, K., Shinnick-Gallagher, P., & Gallagher, J. P. (2008). Dopamine and corticotropin-releasing factor synergistically alter basolateral amygdala-to-medial prefrontal cortex synaptic transmission: Functional switch after chronic cocaine administration. Journal of Neuroscience, 28, 529-542. https://doi.org/10.1523/JNEUROSCI.2666-07.2008
Paxinos, G., & Watson, C. (2007). The Rat Brain in StereotaxicCoordinates. San Diego: Academic Press.
Rodrigues, R. J., Alfaro, T. M., Rebola, N., Oliveira, C. R., & Cunha, R. A. (2005). Co-localization and functional interaction between adenosine A(2A) and metabotropic group 5 receptors in glutamatergic nerve terminals of the rat striatum. Journal of Neurochemistry, 92, 433-441. https://doi.org/10.1111/j.1471-4159.2004.02887.x
Rossant, C. J., Pinnock, R. D., Hughes, J., Hall, M. D., & McNulty, S. (1999). Corticotropin-releasing factor type 1 and type 2alpha receptors regulate phosphorylation of calcium/cyclic adenosine 3',5'-monophosphate response element-binding protein and activation of p42/p44 mitogen-activated protein kinase. Endocrinology, 140, 1525-1536.
Rutz, C., Renner, A., Alken, M., Schulz, K., Beyermann, M., Wiesner, B., … Schülein, R. (2006). The corticotropin-releasing factor receptor type 2a contains an N-terminal pseudo signal peptide. Journal of Biological Chemistry, 281, 24910-24921.
Slater, P. G., & Yarur, H. E., Gysling, K. (2016) Corticotropin-releasing factor receptors and their interacting proteins: functional consequences. Molecular Pharmacology 90, 627-632.
Stoppel, L. J., Auerbach, B. D., Senter, R. K., Preza, A. R., Lefkowitz, R. J., & Bear, M. F. (2017). β-Arrestin2 Couples Metabotropic Glutamate Receptor 5 to Neuronal Protein Synthesis and is a Potential Target to Treat Fragile X. Cell Reports, 18, 2807-2814. https://doi.org/10.1016/j.celrep.2017.02.075
Tu, H., Kastin, A. J., & Pan, W. (2007). Corticotropin-releasing hormone receptor (CRHR)1 and CRHR2 are both trafficking and signalling receptors for urocortin. Molecular Endocrinology, 21, 700-711.
Vilardaga, J. P., Nikolaev, V. O., Lorenz, K., Ferrandon, S., Zhuang, Z., & Lohse, M. J. (2008). Conformational cross-talk between alpha2A-adrenergic and mu-opioid receptors controls cell signaling. Nature Chemical Biology, 4, 126-131.
Wang, B., Shaham, Y., Zitzman, D., Azari, S., Wise, R. A., & You, Z. B. (2005). Cocaine experience establishes control of midbrain glutamate and dopamine by corticotropin-releasing factor: A role in stress-induced relapse to drug seeking. Journal of Neuroscience, 25, 5389-5396. https://doi.org/10.1523/JNEUROSCI.0955-05.2005
Wang, B., You, Z. B., Rice, K. C., & Wise, R. A. (2007). Stress-induced relapse to cocaine seeking: Roles for the CRF (2) receptor and CRF-binding protein in the ventral tegmental area of the rat. Psychopharmacology (Berl), 193, 283-294. https://doi.org/10.1007/s00213-007-0782-3
Waselus, M., Nazzaro, C., Valentino, R. J., & Van Bockstaele, E. J. (2009). Stress-induced redistribution of corticotropin-releasing factor receptor subtypes in the dorsal raphe nucleus. Biological Psychiatry, 66, 76-83.
Williams, C. L., Buchta, W. C., & Riegel, A. C. (2014). CRF-R2 and the heterosynaptic regulation of VTA glutamate during reinstatement of cocaine seeking. Journal of Neuroscience, 34, 10402-10414. https://doi.org/10.1523/JNEUROSCI.0911-13.2014
Zorrilla, E. P., Logrip, M. L., & Koob, G. F. (2014). Corticotropin releasing factor: A key role in the neurobiology of addiction. Frontiers in Neuroendocrinology, 35, 234-244. https://doi.org/10.1016/j.yfrne.2014.01.001