The K+ channel GIRK2 is both necessary and sufficient for peripheral opioid-mediated analgesia

EMBO Molecular Medicine

Volumn 5, Issue 8, 2013, Pages 1263-1277

  Nockemann, Dinah ^a   Rouault, Morgane ^a   Labuz, Dominika ^a   Hublitz, Philip ^b   Mcknelly, Kate ^b   Reis, Fernanda C ^b   Stein, Christoph ^a   Heppenstall, Paul A ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

Author keywords

Dorsal root ganglia; Ion channel; Opioids; Pain; Peripheral analgesia

Indexed keywords

OPIATE RECEPTOR; POTASSIUM CHANNEL;

ANALGESIA; ANIMAL CELL; ARTICLE; CENTRAL NERVOUS SYSTEM; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; POTASSIUM CHANNEL GIRK2 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY NERVE CELL; SIGNAL TRANSDUCTION;

DORSAL ROOT GANGLIA; ION CHANNEL; OPIOIDS; PAIN; PERIPHERAL ANALGESIA;

AGED; ANALGESIA; ANALGESICS, OPIOID; ANIMALS; ELECTROPHYSIOLOGY; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; HUMANS; INFLAMMATION; MICE; MICE, TRANSGENIC; NEURONS; PERIPHERAL NERVOUS SYSTEM; POTASSIUM CHANNELS; RATS; RECEPTORS, OPIOID; SIGNAL TRANSDUCTION; SKIN;

EID: 84881535160     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201201980     Document Type: Article

References (53)

1. Beacham DW, Blackmer T, M OG, Hanson GT (2010) Cell-based potassium ion channel screening using the FluxOR assay. J Biomol Screen 15: 441-446
2. Belknap JK, Riggan J, Cross S, Young ER, Gallaher EJ, Crabbe JC (1998) Genetic determinants of morphine activity and thermal responses in 15 inbred mouse strains. Pharmacol Biochem Behav 59: 353-360
3. Borgland SL, Connor M, Christie MJ (2001) Nociceptin inhibits calcium channel currents in a subpopulation of small nociceptive trigeminal ganglion neurons in mouse. J Physiol 536: 35-47
4. Boue J, Blanpied C, Djata-Cabral M, Pelletier L, Vergnolle N, Dietrich G (2012) Immune conditions associated with CD4+ T effector-induced opioid release and analgesia. Pain 153: 485-493
5. Caspani O, Zurborg S, Labuz D, Heppenstall PA (2009) The contribution of TRPM8 and TRPA1 channels to cold allodynia and neuropathic pain. PLoS ONE 4: e7383
6. Cavanaugh DJ, Lee H, Lo L, Shields SD, Zylka MJ, Basbaum AI, Anderson DJ (2009) Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc Natl Acad Sci USA 106: 9075-9080
7. Chung HJ, Qian X, Ehlers M, Jan YN, Jan LY (2009) Neuronal activity regulates phosphorylation-dependent surface delivery of G protein-activated inwardly rectifying potassium channels. Proc Natl Acad Sci USA 106: 629-634
8. Cunha TM, Roman-Campos D, Lotufo CM, Duarte HL, Souza GR, Verri WA, Jr., Funez MI, Dias QM, Schivo IR, Domingues AC, et al (2010) Morphine peripheral analgesia depends on activation of the PI3Kgamma/AKT/nNOS/NO/KATP signaling pathway. Proc Natl Acad Sci USA 107: 4442-4447
9. Elmer GI, Pieper JO, Negus SS, Woods JH (1998) Genetic variance in nociception and its relationship to the potency of morphine-induced analgesia in thermal and chemical tests. Pain 75: 129-140
10. Endres-Becker J, Heppenstall PA, Mousa SA, Labuz D, Oksche A, Schafer M, Stein C, Zollner C (2007) Mu-opioid receptor activation modulates transient receptor potential vanilloid 1 (TRPV1) currents in sensory neurons in a model of inflammatory pain. Mol Pharmacol 71: 12-18
11. Gao XF, Zhang HL, You ZD, Lu CL, He C (2007) G protein-coupled inwardly rectifying potassium channels in dorsal root ganglion neurons. Acta Pharmacol Sin 28: 185-190
12. Gaveriaux-Ruff C, Nozaki C, Nadal X, Hever XC, Weibel R, Matifas A, Reiss D, Filliol D, Nassar MA, Wood JN, et al (2011) Genetic ablation of delta opioid receptors in nociceptive sensory neurons increases chronic pain and abolishes opioid analgesia. Pain 152: 1238-1248
13. Goins WF, Cohen JB, Glorioso JC (2012) Gene therapy for the treatment of chronic peripheral nervous system pain. Neurobiol Dis 48: 155-170
14. Gonzalez-Rodriguez S, Hidalgo A, Baamonde A, Menendez L (2010) Involvement of Gi/o proteins and GIRK channels in the potentiation of morphine-induced spinal analgesia in acutely inflamed mice. Naunyn-Schmiedeberg's Arch Pharmacol 381: 59-71
15. Gross RA, Macdonald RL (1987) Dynorphin A selectively reduces a large transient (N-type) calcium current of mouse dorsal root ganglion neurons in cell culture. Proc Natl Acad Sci USA 84: 5469-5473
16. Han J, Kang D, Kim D (2003) Properties and modulation of the G protein-coupled K+ channel in rat cerebellar granule neurons: ATP versus phosphatidylinositol 4, 5-bisphosphate. J Physiol 550: 693-706
17. Hassan AH, Ableitner A, Stein C, Herz A (1993) Inflammation of the rat paw enhances axonal transport of opioid receptors in the sciatic nerve and increases their density in the inflamed tissue. Neuroscience 55: 185-195
18. Hernandez L, Romero A, Almela P, Garcia-Nogales P, Laorden ML, Puig MM (2009) Tolerance to the antinociceptive effects of peripherally administered opioids. Expression of beta-arrestins. Brain Res 1248: 31-39
19. Huser D, Weger S, Heilbronn R (2002) Kinetics and frequency of adeno-associated virus site-specific integration into human chromosome 19 monitored by quantitative real-time PCR. J Virol 76: 7554-7559
20. Kalso E, Smith L, McQuay HJ, Andrew Moore R (2002) No pain, no gain: clinical excellence and scientific rigour-lessons learned from IA morphine. Pain 98: 269-275
21. Kanjhan R, Coulson EJ, Adams DJ, Bellingham MC (2005) Tertiapin-Q blocks recombinant and native large conductance K+ channels in a use-dependent manner. J Pharmacol Exp Ther 314: 1353-1361
22. Karschin C, Dissmann E, Stuhmer W, Karschin A (1996) IRK(1-3) and GIRK(1-4) inwardly rectifying K+ channel mRNAs are differentially expressed in the adult rat brain. J Neurosci 16: 3559-3570
23. Keane TM, Goodstadt L, Danecek P, White MA, Wong K, Yalcin B, Heger A, Agam A, Slater G, Goodson M, et al (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477: 289-294
24. Khodorova A, Navarro B, Jouaville LS, Murphy JE, Rice FL, Mazurkiewicz JE, Long-Woodward D, Stoffel M, Strichartz GR, Yukhananov R, et al (2003) Endothelin-B receptor activation triggers an endogenous analgesic cascade at sites of peripheral injury. Nat Med 9: 1055-1061
25. Labuz D, Schmidt Y, Schreiter A, Rittner HL, Mousa SA, Machelska H (2009) Immune cell-derived opioids protect against neuropathic pain in mice. J Clin Invest 119: 278-286
26. Li JL, Ding YQ, Li YQ, Li JS, Nomura S, Kaneko T, Mizuno N (1998) Immunocytochemical localization of mu-opioid receptor in primary afferent neurons containing substance P or calcitonin gene-related peptide. A light and electron microscope study in the rat. Brain Res 794: 347-352
27. Luscher C, Slesinger PA (2010) Emerging roles for G protein-gated inwardly rectifying potassium (GIRK) channels in health and disease. Nat Rev Neurosci 11: 301-315
28. Luscher C, Jan LY, Stoffel M, Malenka RC, Nicoll RA (1997) G protein-coupled inwardly rectifying K+ channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19: 687-695
29. Makman MH, Dvorkin B, Crain SM (1988) Modulation of adenylate cyclase activity of mouse spinal cord-ganglion explants by opioids, serotonin and pertussis toxin. Brain Res 445: 303-313
30. Mao J, Li L, McManus M, Wu J, Cui N, Jiang C (2002) Molecular determinants for activation of G-protein-coupled inward rectifier K+ (GIRK) channels by extracellular acidosis. J Biol Chem 277: 46166-46171
31. Marker CL, Stoffel M, Wickman K (2004) Spinal G-protein-gated K+ channels formed by GIRK1 and GIRK2 subunits modulate thermal nociception and contribute to morphine analgesia. J Neurosci 24: 2806-2812
32. Mitrovic I, Margeta-Mitrovic M, Bader S, Stoffel M, Jan LY, Basbaum AI (2003) Contribution of GIRK2-mediated postsynaptic signaling to opiate and alpha 2-adrenergic analgesia and analgesic sex differences. Proc Natl Acad Sci USA 100: 271-276
33. Mogil JS (2009) Animal models of pain: progress and challenges. Nat Rev Neurosci 10: 283-294
34. Obara I, Parkitna JR, Korostynski M, Makuch W, Kaminska D, Przewlocka B, Przewlocki R (2009) Local peripheral opioid effects and expression of opioid genes in the spinal cord and dorsal root ganglia in neuropathic and inflammatory pain. Pain 141: 283-291
35. Paulozzi L, Baldwin G, Franklin G, Kerlikowske RG, Jones CM, Ghiya N, Popovic T (2012) CDC grand rounds: prescription drug overdoses - a U.S. epidemic. MMWR Morb Mortal Wkly Rep 61: 10-13
36. Perry MJ, Lawson SN, Robertson J (1991) Neurofilament immunoreactivity in populations of rat primary afferent neurons: a quantitative study of phosphorylated and non-phosphorylated subunits. J Neurocytol 20: 746-758
37. Raveh A, Cooper A, Guy-David L, Reuveny E (2010) Nonenzymatic rapid control of GIRK channel function by a G protein-coupled receptor kinase. Cell 143: 750-760
38. Scherrer G, Imamachi N, Cao YQ, Contet C, Mennicken F, O'Donnell D, Kieffer BL, Basbaum AI (2009) Dissociation of the opioid receptor mechanisms that control mechanical and heat pain. Cell 137: 1148-1159
39. 2+ currents, but spares a sustained current. Neuron 6: 13-20
40. Schumacher MA, Basbaum AI, Way WL (2009) Opioid analgesics and antagonists. In Basic and clinical pharmacology, 11th ed., Vol. 9, Katzung BG, Masters SB, Trevor AJ (eds); pp. 531-552. McGraw-Hill Medical
41. Seward E, Hammond C, Henderson G (1991) Mu-opioid-receptor-mediated inhibition of the N-type calcium-channel current. Proc Biol Sci 244: 129-135
42. Shekarabi M, Moldrich RX, Rasheed S, Salin-Cantegrel A, Laganiere J, Rochefort D, Hince P, Huot K, Gaudet R, Kurniawan N, et al (2012) Loss of neuronal potassium/chloride cotransporter 3 (KCC3) is responsible for the degenerative phenotype in a conditional mouse model of hereditary motor and sensory neuropathy associated with agenesis of the corpus callosum. J Neurosci 32: 3865-3876
43. Shields SD, Ahn HS, Yang Y, Han C, Seal RP, Wood JN, Waxman SG, Dib-Hajj SD (2012) Na(v)1.8 expression is not restricted to nociceptors in mouse peripheral nervous system. Pain 153: 2017-2030
44. Smith SB, Marker CL, Perry C, Liao G, Sotocinal SG, Austin JS, Melmed K, Clark JD, Peltz G, Wickman K, et al (2008) Quantitative trait locus and computational mapping identifies Kcnj9 (GIRK3) as a candidate gene affecting analgesia from multiple drug classes. Pharmacogenet Genomics 18: 231-241
45. Stein C, Machelska H (2011) Modulation of peripheral sensory neurons by the immune system: implications for pain therapy. Pharmacol Rev 63: 860-881
46. Stein C, Millan MJ, Shippenberg TS, Peter K, Herz A (1989) Peripheral opioid receptors mediating antinociception in inflammation. Evidence for involvement of mu, delta and kappa receptors. J Pharmacol Exp Ther 248: 1269-1275
47. Stein C, Schafer M, Machelska H (2003) Attacking pain at its source: new perspectives on opioids. Nat Med 9: 1003-1008
48. Stucky CL, Lewin GR (1999) Isolectin B(4)-positive and -negative nociceptors are functionally distinct. J Neurosci 19: 6497-6505
49. Torrecilla M, Marker CL, Cintora SC, Stoffel M, Williams JT, Wickman K (2002) G-protein-gated potassium channels containing Kir3.2 and Kir3.3 subunits mediate the acute inhibitory effects of opioids on locus ceruleus neurons. J Neurosci 22: 4328-4334
50. Vadivelu N, Mitra S, Hines RL (2011) Peripheral opioid receptor agonists for analgesia: a comprehensive review. J Opioid Manag 7: 55-68
51. Wang HB, Zhao B, Zhong YQ, Li KC, Li ZY, Wang Q, Lu YJ, Zhang ZN, He SQ, Zheng HC, et al (2010) Coexpression of delta- and mu-opioid receptors in nociceptive sensory neurons. Proc Natl Acad Sci USA 107: 13117-13122
52. Wickman K, Seldin MF, Gendler SJ, Clapham DE (1997) Partial structure, chromosome localization, and expression of the mouse Girk4 gene. Genomics 40: 395-401
53. 2+ currents. Neuroscience 153: 1256-1267