A unique role of RGS9-2 in the striatum as a positive or negative regulator of opiate analgesia

Journal of Neuroscience

Volumn 31, Issue 15, 2011, Pages 5617-5624

  Psigfogeorgou, Kassi ^a   Terzi, Dimitra ^a   Papachatzaki, Maria Martha ^a   Varidaki, Artemis ^a   Ferguson, Deveroux ^b   Gold, Stephen J ^c   Zachariou, Venetia ^a  

^a UNIVERSITY OF CRETE   (Greece)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ARRESTIN 2; G PROTEIN COUPLED RECEPTOR; MEMBRANE PROTEIN; MORPHINE; MU OPIATE RECEPTOR; OPIATE; PROTEIN RGS9 2; UNCLASSIFIED DRUG;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; GENE DISRUPTION; IMMUNOPRECIPITATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANALGESICS, OPIOID; ANIMALS; ARRESTINS; BLOTTING, WESTERN; CORPUS STRIATUM; DRUG TOLERANCE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT; MORPHINE; PHOSPHOLIPASE C BETA; PHOSPHORYLATION; RECEPTORS, OPIOID, MU; RGS PROTEINS; SIGNAL TRANSDUCTION;

EID: 79955787551     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4146-10.2011     Document Type: Article

References (53)

1. Arvidsson U, Riedl M, Chakrabarti S, Lee JH, Nakano AH, Dado RJ, Loh HH, Law PY, Wessendorf MW, Elde R (1995) Distribution and targeting of a mu-opioid receptor (MOR1) in brain and spinal cord. J Neurosci 15:3328-3341.
2. Baliki MN, Geha PY, Fields HL, Apkarian AV (2010) Predicting value of pain and analgesia: nucleus accumbens response to noxious stimuli changes in the presence of chronic pain. Neuron 66:149-160.
3. Ballon DR, Flanary PL, Gladue DP, Konopka JB, Dohlman HG, Thorner J (2006) DEP-domain-mediated regulation of GPCR signaling responses. Cell 126:1079-1093.
4. Berman DM, Gilman AG (1998) Mammalian RGS proteins: barbarians at the gates. J Biol Chem 273:1269-1272.
5. Bohn LM, Lefkowitz RJ, Gainetdinov RR, Peppel K, Caron MG, Lin FT (1999) Enhanced morphine analgesia in mice lacking β-arrestin 2. Science 286:2495-2498.
6. 2+ channel inhibition in rat striatal cholinergic in-terneurons. Proc Natl Acad Sci USA 101:16339-16344.
7. Chakrabarti S, Liu NJ, Gintzler AR (2003) Reciprocal modulation of phos-pholipase C beta isoforms: adaptation to chronic morphine. Proc Natl Acad Sci USA 100:13686-13691.
8. Charlton JJ, Allen PB, Psifogeorgou K, Chakravarty S, Gomes I, Neve RL, Devi LA, Greengard P, Nestler EJ, Zachariou V (2008) Multiple actions of spinophilin modulate mu opioid receptor function. Neuron 58:238-247.
9. Cheever ML, Snyder JT, Gershburg S, Siderovski DP, Harden TK, Sondek J (2008) Crystal structure of the multifunctional RGS9-2-Gb5 complex. Nat Struct Mol Biol 15:155-162.
10. Chen CK, Eversole-Cire P, Zhang H, Mancino V, Chen YJ, He W, Wensel TG, Simon MI (2003) Instability of GGL domain containing RGS proteins in mice lacking the G protein beta subunit Gβ5. Proc Natl Acad Sci USA 100:6604-6609.
11. Contet C, Kieffer BL, Befort K (2004) Mu opioid receptor: a gateway to drug addiction. Curr Opin Neurobiol 14:370-378.
12. Dohlman HG, Thorner J (1997) RGS proteins and signaling by heterotri-meric G proteins. J Biol Chem 272:3871-3874.
13. Eitan S, Bryant CD, Saliminejad N, Yang YC, Vojdani E, Keith D Jr, Polakie-wicz R, Evans CJ (2003) Brain region-specific mechanisms for acute morphinmitogen-activated protein kinase modulation and distinct patterns of activation during analgesic tolerance and locomotor sensitization. J Neurosci 23:8360-8369.
14. Gold SJ, Ni YG, Dohlman HG, Nestler EJ (1997) Regulators of G-protein signaling (RGS) proteins: region-specific expression of nine subtypes in rat brain. J Neurosci 17:8024-8037.
15. Gold SJ, Hoang CV, Potts BW, Porras G, Pioli E, Kim KW, Nadjar A, Qin C, LaHoste GJ, Li Q, Bioulac BH, Waugh JL, Gurevich E, Neve RL, Bezard E (2007) RGS9-2 negatively modulates L-3,4-dihydroxyphenylalanine-induced dyskinesia in experimental Parkinson's disease. J Neurosci 27: 14338-14348.
16. Gupta A, Mulder J, Gomes I, Rozenfeld R, Bushlin I, Ong E, Lim M, Maillet E, Junek M, Cahill CM, Harkany T, Devi LA (2010) Increased abundance of opioid receptor heteromers after chronic morphine administration. Sci Signal 3:ra54.
17. Haberstock-Debic H, Kim KA, Yu YJ, von Zastrow M (2005) Morphine promotes rapid, arrestin-dependent endocytosis of μ-opioid receptors in striatal neurons. J Neurosci 25:7847-7857.
18. Han MH, Renthal W, Ring RH, Rahman Z, Psifogeorgou K, Howland D, Birnbaum S, Young K, Neve R, Nestler EJ, Zachariou V (2010) Brain region specific actions of regulator of G protein signaling 4 oppose morphine reward and dependence but promote analgesia. Biol Psychiatry 67:761-769.
19. He W, Lu L, Zhang X, El-Hodiri HM, Chen CK, Slep KC, Simon MI, Jamrich M, Wensel TG (2000) Modules in the photoreceptor RGS9-1.Gbeta 5L GTPase-accelerating protein complex control effector coupling, GTPase acceleration, protein folding, and stability. J Biol Chem 275:37093-37100.
20. Hepler JR, Berman DM, Gilman AG, Kozasa T (1997) RGS and GAIP are GTPase activating proteins for Gq alpha and block activation of phospho-lipase C beta by gamma-thio-GTP-Gq-alpha. Proc Natl Acad Sci USA 94:428-432.
21. Huang C, Hepler JR, Gilman AG, Mumby SM (1997) Attenuation of Gi-and Gq-mediated signaling by expression of RGS4 or GAIP in mammalian cells. Proc Natl Acad Sci USA 94:6159-6163.
22. Inturrisi CE (2002) Clinical pharmacology of opioids for pain. Clin J Pain 18 [Suppl 4]:S3-13.
23. Jayaraman M, Zhou H, Jia L, Cain MD, Blumer KJ (2009) R9AP and R7BP: traffic cops for the RGS7 family in phototransduction and neuronal GPCR signaling. Trends Pharmacol Sci 30:17-24.
24. Jin J, Kittanakom S, Wong V, Reyes BA, Van Bockstaele EJ, Stagljar I, Berret-tini W, Levenson R (2010) Interaction of the mu-opioid receptor with GPR177 (Wntless) inhibits Wnt secretion: potential implications for opioid dependence. BMC Neurosci 11:33-37.
25. Koch T, Widera A, Bartzsch K, Schulz S, Brandenburg LO, Wundrack N, Beyer A, Grecksch G, Hollt V (2005) Receptor endocytosis counteracts the development of opioid tolerance. Mol Pharmacol 67:280-287.
26. Kovoor A, Seyffarth P, Ebert J, Barghshoon S, Chen CK, Schwarz S, Axelrod JD, Cheyette BN, Simon MI, Lester HA, Schwarz J (2005) D2 dopamine receptors colocalize regulator of G protein signalling 9-2 via the RGS9 DEP domain, and RGS9 knockout mice develop dyskinesias associated with dopamine pathways. J Neurosci 25:2157-2165.
27. Kreek MJ (2001) Drug addictions. Molecular and cellular endpoints. Ann NY Acad Sci 937:27-49.
28. Martemyanov KA, Lishko PV, Calero N, Keresztes G, Sokolov M, Strissel KJ, Leskov IB, Hopp JA, Kolesnikov AV, Chen CK, Lem J, Heller S, Burns ME, Arshavsky VY (2003) The DEP domain determines subcellular targeting of the GTPase activating protein RGS9 in vivo. J Neurosci 23:10175-10181.
29. Martemyanov KA, Yoo PJ, Skiba NP, Arshavsky VY (2005) R7BP, a novel neuronal protein interacting with RGS proteins and the R7 subfamily J Biol Chem 280:5133-5136.
30. Muller DL, Unterwald EM (2004) In vivo regulation of extracellular signal-regulated protein kinase (ERK) and protein kinase B (Akt) phosphorylation by acute and chronic morphine. J Pharmacol Exp Ther 310:774-782.
31. Mumby SM, Gilman AG (1991) Synthetic peptide antisera with determined specificity for G protein alpha or beta subunits. Methods Enzymol 195:215-233.
32. Mundell SJ, Loudon RP, Benovic JL (1999) Characterization of G protein-coupled receptor regulation in antisense mRNA-expressing cells with reduced arrestin levels. Biochemistry 38:8723-8732.
33. Narita M, Suzuki M, Narita M, Niikura K, Nakamura A, Miyatake M, Yajima Y, Suzuki T (2006) mu-Opioid receptor internalization-dependent and -independent mechanisms of the development of tolerance to mu-opioid receptor agonists: comparison between etorphine and morphine. Neuro-science 138:609-619.
34. Nestler EJ (2001) Molecular basis of long-term underlying addiction. Nat Rev Neurosci 2:119-128.
35. Pan YX, Xu J, Bolan E, Moskowitz HS, Xu M, Pasternak GW (2005) Identification of four novel exon 5 splice variants of the mouse mu-opioid receptor gene: functional consequences of C-terminal splicing. Mol Pharmacol 68:866-875.
36. Piros ET, Hales TG, Evans CJ (1996) Functional analysis of cloned opioid receptors in transfected cell lines. Neurochem Res 21:1277-1285.
37. Posner BA, Mukhopadhyay S, Tesmer JJ, Gilman AG, Ross EM (1999) Modulation of the affinity and selectivity of RGS protein interaction with G alpha subunits by a conserved asparagine/serine residue. Biochemistry 38:7773-7779.
38. Psifogeorgou K, Papakosta P, Russo SJ, Neve RL, Kardassis D, Gold SJ, Zachariou V (2007) RGS9-2 is a negative modulator of mu opioid receptor function. J Neurochem 103:617-625.
39. Rahman Z, Gold SJ, Potenza MN, Cowan CW, Ni YG, He W, Wensel TG, Nestler EJ (1999) Cloning and characterization of RGS9-2, a striatal enriched alternatively spliced product of the RGS9 gene. J Neurosci 19: 2016-2026.
40. Rahman Z, Schwarz J, Gold SJ, Zachariou V, Wein MN, Choi KH, Kovoor A, Chen CK, DiLeone RJ, Schwarz SC, Selley DE, Sim-Selley LJ, Barrot M, Luedtke RR, Self D, Neve RL, Lester HA, Simon MI, Nestler EJ (2003) RGS9 modulates dopamine signaling in the basal ganglia. Neuron 38: 941-952.
41. Rozenfeld R, Devi LA (2007) Receptor heterodimerization leads to a switch in signaling: beta-arrestin2-mediated ERK activation by mu-delta opioid receptor heterodimers. FASEB J 21:2455-2465.
42. Shen J, Benedict Gomes A, Gallagher A, Stafford K, Yoburn BC (2000) Role of cAMP-dependent protein kinase (PKA) in opioid agonist-induced mu-opioid receptor downregulation and tolerance in mice. Synapse 38: 322-327.
43. Sondek J, Siderovski DP (2001) G-y like domains: new frontiers in G protein signalling and /3-propeller scaffolding. Biochem Pharmacol 61:1329-1337.
44. Terzi D, Stergiou E, King SL, Zachariou V (2009) RGS proteins in neuro-psychiatric disorders. Prog Mol Biol Translational Sci Vol 86C:299-333.
45. Tesmer VM, Kawano T, Shankaranarayanan A, Kozasa T, Tesmer JJ (2005) Snapshot of activated G proteins at the membrane: the Galphaq-GRK2-Gbetagamma complex. Science 310:1686-1690.
46. Traynor JR, Neubig RR (2005) Regulators of G protein signaling and drugs of abuse. Mol Interv5:30-41.
47. Traynor JR, Terzi D, Caldarone BJ, Zachariou V (2009) RGS9-2: probing an intracellular modulator of behaviour as a drug target. Trends Pharmacol Sci 30:105-111.
48. Whistler JL, von Zastrow M (1998) Morphine-activated opioid receptors elude desensitization by beta-arrestin. Proc Natl Acad Sci USA 95: 9914-9919.
49. Witherow DS, Tovey SC, Wang Q, Willars GB, Slepak VZ (2003) G beta 5.RGS7 inhibits Galpha q-mediated signaling via a direct protein-protein interaction. J Biol Chem 278:21307-21313.
50. Xie W, Samoriski GM, McLaughlin JP, Romoser VA, Smrcka A, Hinkle PM, Bidlack JM, Gross RA, Jiang H, Wu D (1999) Genetic alterations in phospholipase C beta3 expression modulates behavioral and cellular responses to opioids. Proc Natl Acad Sci USA 96:10385-10390.
51. Xie WY, He Y, Yang YR, Li YF, Kang K, Xing BM, Wang Y (2009) Disruption of Cdk5 associated phosphorylation of residue threonine-161 of the S-opioid receptor: impaired receptor function and attenuated morphine antinociceptive tolerance. J Neurosci 29:3551-35564.
52. Zachariou V, Georgescu D, Sanchez N, Rahman Z, DiLeone R, Berton O, Neve RL, Sim-Selley LJ, Selley DE, Gold SJ, Nestler EJ (2003) Essential role for RGS9 in opiate action. Proc Natl Acad Sci 100:13656-13661.
53. Zachariou V, Bolanos CA, Selley DE, Theobald D, Cassidy MP, Kelz MB, Shaw-Lutchman T, Berton O, Sim-Selley LJ, Dileone RJ, Kumar A, Nestler EJ (2006) An essential role for DeltaFosB in the nucleus accumbens in morphine action. Nat Neurosci 9:205-211.