Evidence that behavioral phenotypes of morphine in β-arr2-/- mice are due to the unmasking of JNK signaling

Neuropsychopharmacology

Volumn 37, Issue 8, 2012, Pages 1953-1962

  Mittal, Nitish ^a,b   Tan, Miao ^b   Egbuta, Onyemachi ^b   Desai, Nina ^b   Crawford, Cynthia ^a   Xie, Cui Wei ^b   Evans, Christopher ^b   Walwyn, Wendy ^b  

^a CALIFORNIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

arrestin 2; analgesia; JNK; locomotion; morphine; mu opioid receptor

Indexed keywords

3 [1 (3 AMINOPROPYL) 3 INDOLYL] 4 (1 METHYL 3 INDOLYL) 1H PYRROLE 2,5 DIONE; 4 (2,3 DIHYDROBENZO[B][1,4]DIOXIN 6 YL) 5 (5 NITROTHIAZOL 2 YLTHIO) 4H 1,2,4 TRIAZOL 3 OL; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BETA ARRESTIN; BI 78D 3; FENTANYL; MORPHINE; MU OPIATE RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; UNCLASSIFIED DRUG;

ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG SENSITIZATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; LOCOMOTION; MALE; MOUSE; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PSYCHOMOTOR PERFORMANCE; SIGNAL TRANSDUCTION; SPINAL CORD NERVE CELL; SPINAL GANGLION;

ANIMALS; ARRESTINS; CELLS, CULTURED; FEMALE; FENTANYL; GANGLIA, SPINAL; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MORPHINE; MOTOR ACTIVITY; PAIN MEASUREMENT; PHOSPHORYLATION; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS C-JUN; SIGNAL TRANSDUCTION;

EID: 84862315506     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.42     Document Type: Article

References (47)

1. Arttamangkul S, Quillinan N, Low MJ, von Zastrow M, Pintar J, Williams JT (2008). Differential activation and trafficking of micro-opioid receptors in brain slices. Mol Pharmacol 74: 972-979.
2. Becker A, Grecksch G, Kraus J, Peters B, Schroeder H, Schulz S et al. (2001). Loss of locomotor sensitisation in response to morphine in D1 receptor deficient mice. Naunyn Schmiedebergs Arch Pharmacol 363: 562-568. (Pubitemid 32417815)
3. Bohn LM, Gainetdinov RR, Sotnikova TD, Medvedev IO, Lefkowitz RJ, Dykstra LA et al. (2003). Enhanced rewarding properties of morphine, but not cocaine, in beta(arrestin)-2 knock-out mice. J Neurosci 23: 10265-10273. (Pubitemid 37444603)
4. Bohn LM, Lefkowitz RJ, Caron MG (2002). Differential mechanisms of morphine antinociceptive tolerance revealed in (beta)arrestin-2 knock-out mice. J Neurosci 22: 10494-10500. (Pubitemid 35416886)
5. Bohn LM, Lefkowitz RJ, Gainetdinov RR, Peppel K, Caron MG, Lin FT (1999). Enhanced morphine analgesia in mice lacking beta-arrestin 2. Science 286: 2495-2498.
6. Bohn LM, Xu F, Gainetdinov RR, Caron MG (2000). Potentiated opioid analgesia in norepinephrine transporter knock-out mice. J Neurosci 20: 9040-9045. (Pubitemid 32042905)
7. Borgkvist A, Usiello A, Greengard P, Fisone G (2007). Activation of the cAMP/PKA/DARPP-32 signaling pathway is required for morphine psychomotor stimulation but not for morphine reward. Neuropsychopharmacology 32: 1995-2003. (Pubitemid 47258515)
8. Borgkvist A, Valjent E, Santini E, Herve D, Girault JA, Fisone G (2008). Delayed, context- and dopamine D1 receptor-dependent activation of ERK in morphine-sensitized mice. Neuropharmacology 55: 230-237.
9. Borgland SL, Connor M, Osborne PB, Furness JB, Christie MJ (2003). Opioid agonists have different efficacy profiles for G protein activation, rapid desensitization, and endocytosis of muopioid receptors. J Biol Chem 278: 18776-18784. (Pubitemid 36799259)
10. Bruchas M, Chavkin C (2010). Kinase cascades and ligand-directed signaling at the kappa opioid receptor. Psychopharmacology 210: 137-147.
11. Chen Y, Geis C, Sommer C (2008). Activation of TRPV1 contributes to morphine tolerance: involvement of the mitogen-activated protein kinase signaling pathway. J Neurosci 28: 5836-5845.
12. Dang VC, Chieng B, Azriel Y, Christie MJ (2011). Cellular morphine tolerance produced by betaarrestin-2-dependent impairment of mu-opioid receptor resensitization. J Neurosci 31: 7122-7130.
13. Galandrin SGN, Oligny-Longpré GV, Bonin HLN, Ogawa K, Galés CL, Bouvier M (2008). Conformational rearrangements and signaling cascades involved in ligand-biased mitogen-activated protein kinase signaling through the b1-adrenergic receptor. Mol Pharmacol 74: 162-172.
14. Gee KW, Yamamura HI (1983). Selective anxiolytics: are the actions related to partial 00agonist00 activity or a preferential affinity for benzodiazepine receptor subtypes? Adv Biochem Psychopharmacol 38: 1-9.
15. Groer CE, Schmid CL, Jaeger AM, Bohn LM (2011). Agonist-directed interactions with specific {beta}arrestins determine MU opioid receptor trafficking, ubiquitination, and dephosphorylation. J Biol Chem 286: 31731-31741.
16. Hibi M, Lin A, Smeal T, Minden A, Karin M (1993). Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev 7: 2135-2148. (Pubitemid 23336140)
17. Lam H, Maga M, Pradhan A, Evans CJ, Maidment NT, Hales TG et al. (2011). Analgesic tone conferred by constitutively active mu opioid receptors in mice lacking beta-arrestin 2. Mol Pain 7: 24.
18. Lopez-Bergami P, Habelhah H, Bhoumik A, Zhang W, Wang LH, Ronai Z (2005). RACK1 mediates activation of JNK by protein kinase C [corrected]. Mol Cell 19: 309-320. (Pubitemid 41074887)
19. McDonald PH, Chow CW, Miller WE, Laporte SA, Field ME, Lin FT et al. (2000). Beta-arrestin 2: a receptor-regulated MAPK scaffold for the activation of JNK3. Science 290: 1574-1577.
20. McPherson J, Rivero G, Baptist M, Llorente J, Al-Sabah S, Krasel C et al. (2010). m-Opioid receptors: correlation of agonist efficacy for signalling with ability to activate internalization. Mol Pharmacol 78: 756-766.
21. Melief EJ, Miyatake M, Bruchas MR, Chavkin C (2010). Ligand-directed c-Jun N-terminal kinase activation disrupts opioid receptor signaling. Proc Natl Acad Sci USA 107: 11608-11613.
22. Miller WE, McDonald PH, Cai SF, Field ME, Davis RJ, Lefkowitz RJ (2001). Identification of a motif in the carboxyl terminus of beta-arrestin2 responsible for activation of JNK3. J Biol Chem 276: 27770-27777.
23. Peng Y, Zhang Q, Arora S, Keenan SM, Kortagere S, Wannemacher KM et al. (2009). Novel delta opioid receptor agonists exhibit differential stimulation of signaling pathways. Bioorg Med Chem 17: 6442-6450.
24. Ping P (2003). Identification of novel signaling complexes by functional proteomics. Circ Res 93: 595-603.
25. Pontrelli P, Ranieri E, Ursi M, Ghosh-Choudhury G, Gesualdo L, Paolo Schena F et al. (2004). jun-N-terminal kinase regulates thrombin-induced PAI-1 gene expression in proximal tubular epithelial cells. Kidney Int 65: 2249-2261. (Pubitemid 38670011)
26. Pradhan AA, Walwyn W, Nozaki C, Filliol D, Erbs E, Matifas A et al. (2010). Ligand-directed trafficking of the delta-opioid receptor in vivo: two paths toward analgesic tolerance. J Neurosci 30: 16459-16468.
27. Quillinan N, Lau EK, Virk M, von Zastrow M, Williams JT (2011). Recovery from mu-opioid receptor desensitization after chronic treatment with morphine and methadone. J Neurosci 31: 4434-4443.
28. Raehal KM, Bohn LM (2011). The role of beta-arrestin2 in the severity of antinociceptive tolerance and physical dependence induced by different opioid pain therapeutics. Neuropharmacology 60: 58-65.
29. Reiter E, Ahn S, Shukla AK, Lefkowitz RJ (2012). Molecular mechanism of beta-arrestin-biased agonism at seven-transmembrane receptors. Annu Rev Pharmacol Toxicol 52: 179-197.
30. Robinson TE, Berridge KC (1993). The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18: 247-291. (Pubitemid 23219500)
31. Shenoy SK, Lefkowitz RJ (2011). beta-arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol Sci 32: 521-533.
32. Shin M, Yan C, Boyd D (2002). An inhibitor of c-jun aminoterminal kinase (SP600125) represses c-Jun activation, DNA-binding and PMA-inducible 92-kDa type IV collagenase expression. Biochim Biophys Acta 1589: 311-316. (Pubitemid 34603302)
33. Shukla AK, Xiao K, Lefkowitz RJ (2011). Emerging paradigms of beta-arrestin-dependent seven transmembrane receptor signaling. Trends Biochem Sci 36: 457-469.
34. Song X, Coffa S, Fu H, Gurevich VV (2009). How does arrestin assemble MAPKs into a signaling complex? J Biol Chem 284: 685-695.
35. Song X, Raman D, Gurevich EV, Vishnivetskiy SA, Gurevich VV (2006). Visual and both non-visual arrestins in their "inactive" conformation bind JNK3 and Mdm2 and relocalize them from the nucleus to the cytoplasm. J Biol Chem 281: 21491-21499. (Pubitemid 44115487)
36. Sora I, Takahashi N, Funada M, Ujike H, Revay RS, Donovan DM et al. (1997). Opiate receptor knockout mice define mu receptor roles in endogenous nociceptive responses and morphine-induced analgesia. Proc Natl Acad Sci USA 94: 1544-1549. (Pubitemid 27087888)
37. Stebbins JL, De SK, Machleidt T, Becattini B, Vazquez J, Kuntzen C et al. (2008). Identification of a new JNK inhibitor targeting the JNK-JIP interaction site. Proc Natl Acad Sci USA 105: 16809-16813.
38. Tan M, Groszer M, Tan AM, Pandya A, Liu X, Xie CW (2003). Phosphoinositide 3-kinase cascade facilitates mu-opioid desensitization in sensory neurons by altering G-protein-effector interactions. J Neurosci 23: 10292-10301. (Pubitemid 37444606)
39. Urban JD, Clarke WP, von Zastrow M, Nichols DE, Kobilka B, Weinstein H et al. (2007). Functional selectivity and classical concepts of quantitative pharmacology. J Pharmacol Exp Ther 320: 1-13. (Pubitemid 46025713)
40. Urs NM, Daigle TL, Caron MG (2011). A dopamine D1 receptor-dependent [beta]-arrestin signaling complex potentially regulates morphine-induced psychomotor activation but not reward in mice. Neuropsychopharmacology 36: 551-558.
41. Vanderschuren LJ, Pierce RC (2011). Sensitization processes in drug addiction. Curr Top Behav Neurosci 3: 179-195.
42. Walwyn W, Evans CJ, Hales TG (2007). Beta-arrestin2 and c-Src regulate the constitutive activity and recycling of mu opioid receptors in dorsal root ganglion neurons. J Neurosci 27: 5092-5104. (Pubitemid 46741772)
43. Wilkinson SE, Parker PJ, Nixon JS (1993). Isoenzyme specificity of bisindolylmaleimides, selective inhibitors of protein kinase C. Biochem J 294(Part 2): 335-337. (Pubitemid 23268828)
44. Willoughby EA, Collins MK (2005). Dynamic interaction between the dual specificity phosphatase MKP7 and the JNK3 scaffold protein beta-arrestin 2. J Biol Chem 280: 25651-25658. (Pubitemid 40962274)
45. Xiao K, McClatchy DB, Shukla AK, Zhao Y, Chen M, Shenoy SK et al. (2007). Functional specialization of beta-arrestin interactions revealed by proteomic analysis. Proc Natl Acad Sci USA 104: 12011-12016. (Pubitemid 47185621)
46. Xiao K, Sun J, Kim J, Rajagopal S, Zhai B, Villen J et al. (2010). Global phosphorylation analysis of beta-arrestin-mediated signaling downstream of a seven transmembrane receptor (7TMR). Proc Natl Acad Sci USA 107: 15299-15304.
47. Zheng H, Chu J, Zhang Y, Loh HH, Law PY (2011). Modulating micro-opioid receptor phosphorylation switches agonist-dependent signaling as reflected in PKCepsilon activation and dendritic spine stability. J Biol Chem 286: 12724-12733.