GRK3 suppresses L-DOPA-induced dyskinesia in the rat model of Parkinson's disease via its RGS homology domain

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Ahmed, Mohamed R ^a   Bychkov, Evgeny ^a,b   Li, Lingyong ^a,c   Gurevich, Vsevolod V ^a   Gurevich, Eugenia V ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b S M KIROV MILITARY MEDICAL ACADEMY   (Russian Federation)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR KINASE 3; LEVODOPA; RGS PROTEIN; SMALL INTERFERING RNA;

ANIMAL; ANIMAL BEHAVIOR; CHEMISTRY; COMPLICATION; CORPUS STRIATUM; DISEASE MODEL; DYSKINESIAS; GENE EXPRESSION; GENE SILENCING; GENETICS; METABOLISM; PARKINSON DISEASE; PROTEIN DOMAIN; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; BEHAVIOR, ANIMAL; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DYSKINESIAS; G-PROTEIN-COUPLED RECEPTOR KINASE 3; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; LEVODOPA; PARKINSON DISEASE; PROTEIN INTERACTION DOMAINS AND MOTIFS; RATS; RGS PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84930651645     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep10920     Document Type: Article

References (74)

1. Gurevich, E. V., & Gurevich, V. V. Arrestins: ubiquitous regulators of cellular signaling pathways. Genome Biol. 7, 236 (2006
2. Gurevich, V. V., & Gurevich, E. V. Overview of different mechanisms of arrestin-mediated signaling. Curr Protoc Pharmacol 67, 1-9 (2014
3. Gurevich, V. V., & Gurevich, E. V. The structural basis of arrestin-mediated regulation of G-protein-coupled receptors. Pharmacol Ther 110, 465-502 (2006
4. Kim, J. et al. Functional antagonism of different G protein-coupled receptor kinases for beta-arrestin-mediated angiotensin II receptor signaling. Proc. Nat. Acad. Sci. USA 102, 142-1447 (2005
5. Ren, X. R. et al. Different G protein-coupled receptor kinases govern G protein and beta-arrestin mediated signaling of V2 vasopressin receptor. Proc Nat Acad Sci USA 102, 1448-1453 (2005
6. Siderovski, D. P., Hessel, A., Chung, S., Mak, T. W., & Tyers, M. A new family of regulators of G-protein-coupled receptors?. Curr. Biol. 6, 211-212 (1996
7. Hollinger, S., & Hepler, J. R. Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol Rev 54, 527-559 (2002
8. Gurevich, E. V., Tesmer, J. J., Mushegian, A., & Gurevich, V. V. G protein-coupled receptor kinases: More than just kinases and not only for GPCRs. Pharmacol. Ther. 133, 40-69 (2011
9. Carman, C. V. et al. Selective regulation of Galpha(q/11) by an RGS domain in the G protein-coupled receptor kinase, GRK2. J Biol Chem 274, 34483-34492 (1999
10. Day, P. W., Carman, C. V., Sterne-Marr, R., Benovic, J. L., & Wedegaertner, P. B. Differential interaction of GRK2 with members of the Gaq family. Biochemistry 42, 9176-9184 (2003
11. Day, P. W., Wedegaertner, P. B., & Benovic, J. L. Analysis of G-protein-coupled receptor kinase RGS homology domains. Methods Enzymol. 390, 295-310 (2004
12. Sterne-Marr, R., Dhami, G. K., Tesmer, J. J., & Ferguson, S. S. Characterization of GRK2 RH domain-dependent regulation of GPCR coupling to heterotrimeric G proteins. Methods Enzymol. 390, 310-336 (2004
13. Sterne-Marr, R. et al. G protein-coupled receptor Kinase 2/G alpha q/11 interaction. A novel surface on a regulator of G protein signaling homology domain for binding G alpha subunits. J Biol Chem 278, 6050-6058 (2003
14. Dhami, G. K. et al. G Protein-coupled receptor kinase 2 regulator of G protein signaling homology domain binds to both metabotropic glutamate receptor 1a and Galphaq to attenuate signaling. J Biol Chem 279, 16614-16620 (2004
15. Dhami, G. K., Anborgh, P. H., Dale, L. B., Sterne-Marr, R., & Ferguson, S. S. G. Phosphorylation-independent Regulation of Metabotropic Glutamate Receptor Signaling by G Protein-coupled Receptor Kinase 2. J. Biol. Chem. 277, 25266-25272 (2002
16. Bychkov, E., Ahmed, M. R., Dalby, K. N., & Gurevich, E. V. Dopamine depletion and subsequent treatment with L-DOPA, but not the long-lived dopamine agonist pergolide, enhances activity of the Akt pathway in the rat striatum. J. Neurochem. 102, 699-711 (2007
17. Gerfen, C. R., Miyachi, S., Paletzki, R., & Brown, P. D1 dopamine receptor supersensitivity in the dopamine-depleted striatum results from a switch in the regulation of ERK1/2 kinase. J. Neurosci. 22, 5042-5054 (2002
18. Santini, E. et al. Critical involvement of cAMP/DARPP-32 and extracellular signal-regulated protein kinase signaling in L-DOPAinduced dyskinesia. J. Neurosci. 27, 6995-7005 (2007
19. Ahmed, M. R. et al. Overexpression of GRK6 rescues L-DOPA-induced signaling abnormalities in the dopamine-depleted striatum of hemiparkinsonian rats. Exp Neurol 266, 42-54 (2015
20. Aubert, I. et al. Increased D1 dopamine receptor signaling in levodopa-induced dyskinesia. Ann. Neurol. 57, 17-26 (2005
21. Guigoni, C. et al. Pathogenesis of levodopa-induced dyskinesia: focus on D1 and D3 dopamine receptors. Parkinsonism Relat. Disord. 11 Suppl 1, S25-29 (2005
22. Gold, S. J. et al. RGS9 2 negatively modulates l-3,4-dihydroxyphenylalanine-Induced dyskinesia in experimental Parkinson's disease. J. Neurosci. 27, 14338-14348 (2007
23. Fahn, S. How do you treat motor complications in Parkinson's disease: Medicine, surgery, or both? Ann. Neurol. 64 Suppl 2, , S56-S64 (2008
24. Bezard, E. et al. L-DOPA reverses the MPTP-induced elevation of the arrestin2 and GRK6 expression and enhanced ERK activation in monkey brain. Neurobiol. Dis. 18, 323-335 (2005
25. Ahmed, M. R. et al. Lentiviral overexpression of GRK6 alleviates L-dopa-induced dyskinesia in experimental Parkinson's disease. Sci Transl Med 2, 28ra28 (2010
26. Ahmed, M. R., Bychkov, E. R., Gurevich, V. V., Benovic, J. L., & Gurevich, E. V. Altered expression and subcellular distribution of GRK subtypes in the dopamine-depleted rat basal ganglia is not normalized by L-DOPA treatment J Neurochem 104, 699-711 (2007
27. Bychkov, E., Zurkovsky, L., Garret, M., Ahmed, M. R., & Gurevich, E. V. Distinct cellular and subcellular distribution of G protein-coupled receptor kinase and arrestin isoforms in the striatum. PLoS One 7, e48912 (2013
28. Bychkov, E., Gurevich, V. V., Joyce, J. N., Benovic, J. L., & Gurevich, E. V. Arrestins and two receptor kinases are upregulated in Parkinson's disease with dementia. Neurobiol. Aging. 29, 379-396 (2008
29. Tamura, S., Morikawa, Y., Iwanishi, H., Hisaoka, T., & Senba, E. Foxp1 gene expression in projection neurons of the mouse striatum. Neuroscience 124, 261-267 (2004
30. Lazari, M. F., Liu, X., Nakamura, K., Benovic, J. L., & Ascoli, M. Role of G protein-coupled receptor kinases on the agonistinduced phosphorylation and internalization of the follitropin receptor. Mol. Endocrinol. 13, 866-878 (1999
31. Boguth, C. A., Singh, P., Huang, C. C., & Tesmer, J. J. Molecular basis for activation of G protein-coupled receptor kinases. EMBO J 29, 3249-3259 (2010
32. Lodowski, D. T., Pitcher, J. A., Capel, W. D., Lefkowitz, R. J., & Tesmer, J. J. Keeping G proteins at bay: a complex between G protein-coupled receptor kinase 2 and Gbetagamma. Science 300, 1256-1262 (2003
33. Pitcher, J. A., Touhara, K., Payne, E. S., & Lefkowitz, R. J. Pleckstrin homology domain-mediated membrane association and activation of the beta-adrenergic receptor kinase requires coordinate interaction with G beta gamma subunits and lipid. J Biol Chem 270, 11707-11710 (1995
34. Cenci, M. A. Transcription factors involved in the pathogenesis of L-DOPA-induced dyskinesia in a rat model of Parkinson's disease. Amino Acids 23, 105-109 (2002
35. Gurevich, E. V., & Gurevich, V. V. Dopamine receptors and the treatment of Parkinson's disease, in Dopamine Receptors. (ed. K. Neve) 525-584 (Humana Press, New York; 2010
36. Bezard, E. et al. Attenuation of levodopa-induced dyskinesia by normalizing dopamine D3 receptor function. Nature Med. 9, 762-767 (2003
37. Violin, J. D. et al. beta2-adrenergic receptor signaling and desensitization elucidated by quantitative modeling of real time cAMP dynamics. J. Biol. Chem. 283, 2949-2961 (2008
38. Willets, J. M., Challiss, R. A., & Nahorski, S. R. Non-visual GRKs: are we seeing the whole picture? Trends Pharmacol. Sci. 24, 626-633 (2003
39. Gainetdinov, R. R. et al. Dopaminergic supersensitivity in G protein-coupled receptor kinase 6-deficient mice. Neuron 38, 291-303 (2003
40. Gainetdinov, R. R. et al. Muscarinic supersensitivity and impaired receptor desensitization in G protein-coupled receptor kinase 5-deficient mice. Neuron 24, 1029-1036 (1999
41. Bruchas, M. R., Macey, T. A., Lowe, J. D., & Chavkin, C. Kappa opioid receptor activation of p38 MAPK is GRK3-and arrestindependent in neurons and astrocytes. J Biol Chem. 281, 18081-18089 (2006
42. Terman, G. W. et al. G-protein receptor kinase 3 (GRK3) influences opioid analgesic tolerance but not opioid withdrawal. Br J Pharmacol 141, 55-64 (2004
43. Lodowski, D. T., Tesmer, V. M., Benovic, J. L., & Tesmer, J. J. The structure of G protein-coupled receptor kinase (GRK)-6 defines a second lineage of GRKs. J Biol Chem. 281, 16785-16793 (2006
44. Usui, I. et al. GRK2 is an endogenous protein inhibitor of the insulin signaling pathway for glucose transport stimulation. EMBO J 23, 2821-2829 (2004
45. Cao, X. et al. Striatal overexpression of DeltaFosB reproduces chronic levodopa-induced involuntary movements. J Neurosci 30, 7335-7343 (2010
46. Ding, W. Q., Larsson, C., & Alling, C. Stimulation of muscarinic receptors induces expression of individual fos and jun genes through different transduction pathways. J Neurochem 70, 1722-1729 (1998
47. Robison, A. J. et al. Behavioral and structural responses to chronic cocaine require a feedforward loop involving ? FosB and calcium/calmodulin-dependent protein kinase II in the nucleus accumbens shell. J Neurosci 33, 4295-4307 (2013
48. Gerfen, C. R. Dopamine-mediated gene regulation in models of Parkinson's disease. Ann. Neurol. 47 (Suppl), S42-S50 (2000
49. Le Moine, C., & Bloch, B. D1 and D2 dopamine receptor gene expression in the rat striatum: sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNAs in distinct neuronal populations of the dorsal and ventral striatum. J. Comp. Neurol. 355, 418-426 (1995
50. Ciliax, B. J. et al. Dopamine D5 receptor immunolocalization in rat and monkey brain. Synapse 37, 125-145 (2000
51. Khan, Z. U. et al. Dopamine D5 receptors of rat and human brain. Neuroscience 100, 689-699 (2000
52. Medvedev, I. O. et al. D1 dopamine receptor coupling to PLC? regulates forward locomotion in mice. J Neurosci 33, 18125-18133 (2013
53. Sahu, A., Tyeryar, K. R., Vongtau, H. O., Sibley, D. R., & Undieh, A. S. D5 dopamine receptors are required for dopaminergic activation of phospholipase C. Mol Pharmacol 75, 447-453 (2009
54. Rashid, A. J., O'Dowd, B. F., Verma, V., & George, S. R. Neuronal Gq/11-coupled dopamine receptors: an uncharted role for dopamine. Trends Pharmacol. Sci. 28, 551-555 (2007
55. Rashid, A. J. et al. D1-D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc. Natl. Acad. Sci. USA 104, 654-659 (2007
56. Aubert, I., Ghorayeb, I., Normand, E., & Bloch, B. Phenotypical characterization of the neurons expressing the D1 and D2 dopamine receptors in the monkey striatum. J. Comp. Neurol. 418, 22-32 (2000
57. Perreault, M. L. et al. The dopamine D1-D2 receptor heteromer localizes in dynorphin/enkephalin neurons: increased high affinity state following amphetamine and in schizophrenia. J Biol Chem 285, 36625-36634 (2010
58. Surmeier, D. J., Song, W. J., & Yan, Z. Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J. Neurosci. 16, 6579-6591 (1996
59. Testa, C. M., Standaert, D. G., Landwehrmeyer, G. B., Penney, J. B. J., & Young, A. B. Differential expression of mGluR5 metabotropic glutamate receptor mRNA by rat striatal neurons. J Comp Neurol 354, 241-252 (1995
60. Testa, C. M., Friberg, I. K., Weiss, S. W., & Standaert, D. G. Immunohistochemical localization of metabotropic glutamate receptors mGluR1a and mGluR2/3 in the rat basal ganglia. J Comp Neurol 390, 5-19 (1998
61. Paquet, M., & Smith, Y. Group I metabotropic glutamate receptors in the monkey striatum: subsynaptic association with glutamatergic and dopaminergic afferents. J Neurosci 23, 7659-7669 (2003
62. Smith, Y., Charara, A., Hanson, J. E., Paquet, M., & Levey, A. I. GABA(B) and group I metabotropic glutamate receptors in the striatopallidal complex in primates. J Anat 196, 555-576 (2000
63. Mela, F. et al. Antagonism of metabotropic glutamate receptor type 5 attenuates l-DOPA-induced dyskinesia and its molecular and neurochemical correlates in a rat model of Parkinson's disease. J. Neurochem. 101, 483-497 (2007
64. Rylander, D. et al. Pharmacological modulation of glutamate transmission in a rat model of L-DOPA-induced dyskinesia: effects on motor behavior and striatal nuclear signaling. J Pharmacol Exper Ther 330, 227-235 (2009
65. Bubser, M., Backstrom, J. R., Sanders-Bush, E., Roth, B. L., & Deutch, A. Y. Distribution of serotonin 5-HT2A receptors in afferents of the rat striatum. Synapse 39, 297-304 (2001
66. Huot, P., Fox, S. H., Newman-Tancredi, A., & Brotchie, J. M. Anatomically selective serotonergic type 1A and serotonergic type 2A therapies for Parkinson's disease: an approach to reducing dyskinesia without exacerbating parkinsonism? J Pharmacol Exper Ther 339, 2-8 (2011
67. Calabresi, P., Centonze, D., Gubellini, P., Pisani, A., & Bernardi, G. Acetylcholine-mediated modulation of striatal function. Trends Neurosci. 23, 120-126 (2000
68. Pisani, A., Bernardi, G., Ding, J., & Surmeier, D. J. Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci. 30, 545-553 (2007
69. Lundblad, M. et al. Pharmacological validation of behavioural measures of akinesia and dyskinesia in a rat model of Parkinson's disease. Eur. J. Neurosci. 15, 120-132 (2002
70. Cenci, M. A., & Lundblad, M. Ratings of L-DOPA-induced dyskinesia in the unilateral 6-OHDA lesion model of Parkinson's disease in rats and mice. Curr. Protoc. Neurosci. 9 (2007
71. Lee, C. S., Cenci, M. A., Schulzer, M., & Björklund, A. Embryonic ventral mesencephalic grafts improve levodopa-induced dyskinesia in a rat model of Parkinson's disease. Brain 123, 1365-1379 (2000
72. Ahmed, M. R. et al. Ubiquitin ligase parkin promotes Mdm2-arrestin interaction but inhibits arrestin ubiquitination. Biochemistry 50, 3749-3763 (2011
73. Gimenez, L. E. et al. The role of receptor-attached phosphates in the binding of visual and non-visual arrestins to G proteincoupled receptors. J Biol Chem 287, 9028-9040 (2012
74. Li, L. et al. G protein-coupled receptor kinases of the GRK4 subfamily phosphorylate inactive GPCRs. J Biol Chem 290, 10775-10790 (2015).