|
|
Phosphorylation of group I metabotropic glutamate receptors in drug addiction and translational research |
Limin Mao, John Q Wang* |
Department of Basic Medical Science, School of Medicine, University of Missouri-Kansas City, Kansas City, MO 64108, USA |
|
|
Abstract Protein phosphorylation is an important posttranslational modification of group I metabotropic glutamate receptors (mGluR1 and mGluR5 subtypes, mGluR1/5) which are widely distributed throughout the mammalian brain. Several common protein kinases are involved in this type of modification, including protein kinase A, protein kinase C, and extracellular signal-regulated kinase. Through constitutive and activity-dependent phosphorylation of mGluR1/5 at specific residues, protein kinases regulate trafficking, subcellular/subsynaptic distribution, and function of modified receptors. Increasing evidence demonstrates that mGluR1/5 phosphorylation in the mesolimbic reward circuitry is sensitive to chronic psychostimulant exposure and undergoes adaptive changes in its abundance and activity. These changes contribute to long-term excitatory synaptic plasticity related to the addictive property of drugs of abuse. The rapid progress in uncovering the neurochemical basis of addiction has fostered bench-to-bed translational research by targeting mGluR1/5 for developing effective pharmacotherapies for treating addiction in humans. This review summarizes recent data from the studies analyzing mGluR1/5 phosphorylation. Phosphorylation-dependent mechanisms in stimulant-induced mGluR1/5 and behavioral plasticity are also discussed in association with increasing interest in mGluR1/5 in translational medicine.
|
Keywords
mGluR
PKA
PKC
MAPK
ERK
striatum
nucleus accumbens
G protein-coupled receptors
|
Corresponding Author(s):
*John Qiang Wang, E-mail: wangjq@umkc.edu
|
Issue Date: 14 October 2016
|
|
[1] Niswender CM, Conn PJ. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol, 2010, 50: 295-322. [2] Traynelis SF, Wollmuth LP, McBain CJ, et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev, 2010, 62(3): 405-496. [3] Lujan R, Nusser Z, Roberts JD, et al. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci, 1996, 8(7): 1488-1500. [4] Kuwajima M, Hall RA, Aiba A, et al. Subcellular and subsynaptic localization of group I metabotropic glutamate receptors in the monkey subthalamic nucleus. J Comp Neurol, 2004, 474(4): 589-602. [5] Enz R. The trick of the tail: protein-protein interactions of metabotropic glutamate receptors. Bioessays, 2007, 29(1): 60-73. [6] Enz R. Metabotropic glutamate receptors and interacting proteins: evolving drug targets. Curr Drug Targets, 2012, 13(1): 145-156. [7] Fagni L. Diversity of metabotropic glutamate receptor-interacting proteins and pathophysiological functions. Adv Exp Med Biol, 2012, 970: 63-79. [8] Kim CH, Lee J, Lee JY, et al. Metabotropic glutamate receptors: phosphorylation and receptor signaling. J Neurosci Res, 2008, 86(1): 1-10. [9] Mao LM, Guo ML, Jin DZ, et al. Posttranslational modification biology of glutamate receptors and drug addiction. Front Neuroanat, 2011, 5: 19. [10] Shigemoto R, Nomura S, Ohishi H, et al. Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain. Neurosci Lett, 1993, 163(1): 53-57. [11] Poisik OV, Smith Y, Conn PJ. D1-and D2-like dopamine receptors regulate signaling properties of group I metabotropic glutamate receptors in the rat globus pallidus. Eur J Neurosci, 2007, 26(4): 852-862. [12] Uematsu K, Heiman M, Zelenina M, et al. Protein kinase A directly phosphorylates metabotropic glutamate receptor 5 to modulate its function. J Neurochem, 2015, 132(6): 677-686. [13] Peavy RD, Chang MS, Sanders-Bush E, et al. Metabotropic glutamate receptor 5-induced phosphorylation of extracellular signal-regulated kinase in astrocytes depends on transactivation of the epidermal growth factor receptor. J Neurosci, 2001, 21(24): 9619-9628. [14] Thandi S, Blank JL, Challiss RA. Group-I metabotropic glutamate receptors, mGluR1a and mGluR5a, couple to extracellular signal-regulated kinase (ERK) activation via distinct, but overlapping, signaling pathway. J Neurochem, 2002, 83(5): 1139-1153. [15] Mao LM, Yang L, Arora A, et al. Role of protein phosphatase 2A in mGluR5-regulated MEK/ERK phosphorylation in neurons. J Biol Chem, 2005, 280(13): 12602-12610. [16] Olive MF. Cognitive effects of group I metabotropic glutamate receptor ligands in the context of drug addiction. Eur J Pharmacol, 2010, 639(1-3): 47-58. [17] Chiamulera C, Epping-Jordan MP, Zocchi A, et al. Reinforcing and locomotor stimulant effects of cocaine are absent in mGluR5 null mutant mice. Nat Neurosci, 2001, 4(9): 873-874. [18] Alaluf S, Mulvihill ER, McIlhinney RA. Rapid agonist mediated phosphorylation of the metabotropic glutamate receptor 1 alpha by protein kinase C in permanently transfected BHK cells. FEBS Lett, 1995, 367(3): 301-305. [19] Ciruela F, Giacometti A, McIlhinney RAJ. Functional regulation of metabotropic glutamate receptor type 1c: a role for phosphorylation in the desensitization of the receptor. FEBS Lett, 1999, 462(3): 278-282. [20] Minakami R, Jinnai N, Sugiyama H. Phosphorylation and calmodulin binding of the metabotropic glutamate receptor subtype 5 (mGluR5) are antagonistic in vitro. J Biol Chem, 1997, 272(32): 20291-20298. [21] Kawabata S, Tsutsumi R, Kohara A, et al. Control of calcium oscillations by phosphorylation of metabotropic glutamate receptors. Nature, 1996, 383(6595): 89-92. [22] Uchino M, Sakai N, Kashiwagi K, et al. Isoform-specific phosphorylation of metabotropic glutamate receptor 5 by protein kinase C (PKC) blocks Ca2+ oscillation and oscillatory translocation of Ca2+-dependent PKC. J Biol Chem, 2004, 279(3): 2254-2261. [23] Kim CH, Braud S, Isaac JT, et al. Protein kinase C phosphorylation of the metabotropic glutamate receptor mGluR5 on serine 839 regulates Ca2+ oscillations. J Biol Chem, 2005, 280(27): 25409-25415. [24] Lefkowitz RJ. G protein-coupled receptor kinases. Cell, 1993, 74(3): 409-412. [25] Catania MV, Aronica E, Sortino MA, et al. Desensitization of metabotropic glutamate receptors in neuronal cultures. J Neurochem 1991, 56(4): 1329-1335. [26] Aronica E, Dell’Albani P, Condorelli DF, et al. Mechanisms underlying developmental changes in the expression of metabotropic glutamate receptors in cultured cerebellar granule cells: homologous desensitization and interactive effects involving N-methyl-D-aspartate receptors. Mol Pharmacol, 1993, 44(5): 981-989. [27] Gereau Ⅳ RW, Heinemann SF. Role of protein kinase C phosphorylation in rapid desensitization of metabotropic glutamate receptor 5. Neuron, 1998, 20(1): 143-151. [28] Schoepp DD, Johnson BG. Selective inhibition of excitatory amino acid-stimulated phosphoinositide hydrolysis in the rat hippocampus by activation of protein kinase C. Biochem Pharmacol, 1988, 37(22): 4299-4305. [29] Olive MF, Newton PM. Protein kinase C isozymes as regulators of sensitivity to and self-administration of drugs of abuse-studies with genetically modified mice. Behav Pharmacol, 2010, 21(5-6): 493-499. [30] Bellone C, Mameli M, Luscher C. In utero exposure to cocaine delays postnatal synaptic maturation of glutamatergic transmission in the VTA. Nat Neurosci, 2011, 14(11): 1439-1446. [31] Bakshi K, Parihar R, Goswami SK, et al. Prenatal cocaine exposure uncouples mGluR1 from Homer1 and Gq proteins. PLoS One, 2014, 9(3): e91671. [32] Loweth JA, Scheyer AF, Milovanovic M, et al. Synaptic depression via mGluR1 positive allosteric modulation suppresses cue-induced cocaine craving. Nat Neurosci, 2014, 17(1): 73-80. [33] Schmidt HD, Schassburger RL, Guercio LA, et al. Stimulation of mGluR5 in the accumbens shell promotes cocaine seeking by activating PKC gamma. J Neurosci, 2013, 33(35): 14160-14169. [34] Volmat V, Pouyssegur J. Spatiotemporal regulation of the p42/p44 MAPK pathway. Biol Cell, 2001, 93(1-2): 71-79. [35] Gallo KA, Johnson GL. Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat Rev Mol Cell Biol, 2002, 3(9): 663-672. [36] Songyang Z, Lu KP, Kwon YT, et al. A structure basis for substrate specificities of protein Ser/Thr kinases: primary sequence preference of casein kinases I and Ⅱ, NIMA, phosphorylase kinase, calmodulin-dependent kinase Ⅱ, CDK5, and Erk1. Mol Cell Biol, 1996, 16(11): 6486-6493. [37] Hu JH, Yang L, Kammermeier PJ, et al. Preso1 dynamically regulates group I metabotropic glutamate receptors. Nat Neurosci, 2012, 15(6): 836-844. [38] Segal RA, Greenberg ME. Intracellular signaling pathways activated by neurotrophic factors. Annu Rev Neurosci, 1996, 19: 463-489. [39] Park JM, Hu JH, Milshteyn A, et al. A prolyl-isomerase mediates dopamine-dependent plasticity and cocaine motor sensitization. Cell, 2013, 154(3): 637-650. [40] Pascoli V, Turlault M, Luscher C. Reversal of cocaine-evoked synaptic potentiation resets during-induced adaptive behaviour. Nature, 2012, 481(7379): 71-75. [41] Centozne D, Costa C, Rossi S, et al. Chronic cocaine prevents depotentiation at corticostriatal synapses. Biol Psychiatry, 2006, 60(5): 436-443. [42] Olive MF. Metabotropic glutamate receptor ligands as potential therapeutics for addiction. Curr Drug Abuse Rev, 2009, 2(1): 83-98. [43] Jaeschke G, Wettstein JG, Nordquist RE, et al. mGlu5 receptor antagonist and their therapeutic potential. Exp Opin Ther Patents, 2008, 18(2): 123-142. |
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|