GINIP, a Gαi-Interacting protein, functions as a key modulator of peripheral GABAB receptor-mediated analgesia

Neuron

Volumn 84, Issue 1, 2014, Pages 123-136

  Gaillard, Stéphane ^a   Lo, Laure Re ^a   Mantilleri, Annabelle ^a   Hepp, Régine ^b,c   Urien, Louise ^a   Malapert, Pascale ^a   Alonso, Serge ^a   Deage, Michael ^d   Kambrun, Charline ^e,f   Landry, Marc ^e,f   Low, Sarah A ^g   Alloui, Abdelkrim ^h   Lambolez, Bertrand ^b,c   Scherrer, Grégory ^g   LeFeuvre, Yves ^e,f   Bourinet, Emmanuel ^d   Moqrich, Aziz ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c and Centre National de la Recherche Scientifique Unité Mixte de Recherche 8246   (France)

^d INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^e UNIVERSITÉ DE BORDEAUX   (France)

^f University of Bordeaux   (France)

^g StanfordNeurosciencesInstitute ^*  (United States)

^h UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; 4 [ALPHA (4 ALLYL 2,5 DIMETHYL 1 PIPERAZINYL) 3 METHOXYBENZYL] N,N DIETHYLBENZAMIDE; ADENYLATE CYCLASE; BACLOFEN; CARRAGEENAN; DELTA OPIATE RECEPTOR; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; FORSKOLIN; G PROTEIN COUPLED RECEPTOR; HOMEODOMAIN PROTEIN; METABOTROPIC RECEPTOR; MU OPIATE RECEPTOR; PROTEIN GINIP; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN;

ADULT; ANALGESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE; CHRONIC CONSTRICTION INJURY; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME REGULATION; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; INTERNEURON; MALE; MOUSE; NEUROMODULATION; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PRESYNAPTIC INHIBITION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSORY NERVE CELL; SPINAL GANGLION; SYNAPTIC TRANSMISSION; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; MOLECULAR GENETICS; PAIN MEASUREMENT; PHYSIOLOGY; PROCEDURES; RAT; TRANSGENIC MOUSE;

AMINO ACID SEQUENCE; ANALGESIA; ANIMALS; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; EXCITATORY POSTSYNAPTIC POTENTIALS; GANGLIA, SPINAL; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; PAIN MEASUREMENT; RATS; RECEPTORS, GABA-B;

EID: 84908014949     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.08.056     Document Type: Article

References (54)

1. Abrahamsen B., Zhao J., Asante C.O., Cendan C.M., Marsh S., Martinez-Barbera J.P., Nassar M.A., Dickenson A.H., Wood J.N. The cell and molecular basis of mechanical, cold, and inflammatory pain. Science 2008, 321:702-705.
2. Agarwal N., Pacher P., Tegeder I., Amaya F., Constantin C.E., Brenner G.J., Rubino T., Michalski C.W., Marsicano G., Monory K., et al. Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat. Neurosci. 2007, 10:870-879.
3. Ataka T., Kumamoto E., Shimoji K., Yoshimura M. Baclofen inhibits more effectively C-afferent than Adelta-afferent glutamatergic transmission in substantia gelatinosa neurons of adult rat spinal cord slices. Pain 2000, 86:273-282.
4. Barak L.S., Salahpour A., Zhang X., Masri B., Sotnikova T.D., Ramsey A.J., Violin J.D., Lefkowitz R.J., Caron M.G., Gainetdinov R.R. Pharmacological characterization of membrane-expressed human trace amine-associated receptor 1 (TAAR1) by a bioluminescence resonance energy transfer cAMP biosensor. Mol. Pharmacol. 2008, 74:585-594.
5. Bardoni R., Tawfik V.L., Wang D., François A., Solorzano C., Shuster S.A., Choudhury P., Betelli C., Cassidy C., Smith K., et al. Delta opioid receptors presynaptically regulate cutaneous mechanosensory neuron input to the spinal cord dorsal horn. Neuron 2014, 81:1312-1327.
6. Campbell J.N., Raja S.N., Meyer R.A., Mackinnon S.E. Myelinated afferents signal the hyperalgesia associated with nerve injury. Pain 1988, 32:89-94.
7. Castro A.R., Pinto M., Lima D., Tavares I. Nociceptive spinal neurons expressing NK1 and GABAB receptors are located in lamina I. Brain Res. 2004, 1003:77-85.
8. Cavanaugh D.J., Lee H., Lo L., Shields S.D., Zylka M.J., Basbaum A.I., Anderson D.J. Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc. Natl. Acad. Sci. USA 2009, 106:9075-9080.
9. Charles K.J., Evans M.L., Robbins M.J., Calver A.R., Leslie R.A., Pangalos M.N. Comparative immunohistochemical localisation of GABA(B1a), GABA(B1b) and GABA(B2) subunits in rat brain, spinal cord and dorsal root ganglion. Neuroscience 2001, 106:447-467.
10. Decosterd I., Woolf C.J. Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 2000, 87:149-158.
11. Delfini M.C., Mantilleri A., Gaillard S., Hao J., Reynders A., Malapert P., Alonso S., François A., Barrere C., Seal R., et al. TAFA4, a chemokine-like protein, modulates injury-induced mechanical and chemical pain hypersensitivity in mice. Cell Rep 2013, 5:378-388.
12. Descoeur J., Pereira V., Pizzoccaro A., Francois A., Ling B., Maffre V., Couette B., Busserolles J., Courteix C., Noel J., et al. Oxaliplatin-induced cold hypersensitivity is due to remodelling of ion channel expression in nociceptors. EMBO Mol Med 2011, 3:266-278.
13. Dirig D.M., Yaksh T.L. Intrathecal baclofen and muscimol, but not midazolam, are antinociceptive using the rat-formalin model. J.Pharmacol. Exp. Ther. 1995, 275:219-227.
14. Engle M.P., Merrill M.A., Marquez De Prado B., Hammond D.L. Spinal nerve ligation decreases γ-aminobutyric acidB receptors on specific populations of immunohistochemically identified neurons in L5 dorsal root ganglion of the rat. J.Comp. Neurol. 2012, 520:1663-1677.
15. Gangadharan V., Agarwal N., Brugger S., Tegeder I., Bettler B., Kuner R., Kurejova M. Conditional gene deletion reveals functional redundancy of GABAB receptors in peripheral nociceptors invivo. Mol. Pain 2009, 5:68.
16. Gassmann M., Shaban H., Vigot R., Sansig G., Haller C., Barbieri S., Humeau Y., Schuler V., Müller M., Kinzel B., et al. Redistribution ofGABAB(1) protein and atypical GABAB responses in GABAB(2)-deficient mice. J.Neurosci. 2004, 24:6086-6097.
17. Gervasi N., Hepp R., Tricoire L., Zhang J., Lambolez B., Paupardin-Tritsch D., Vincent P. Dynamics of protein kinase A signaling at the membrane, in the cytosol, and in the nucleus of neurons in mouse brain slices. J.Neurosci. 2007, 27:2744-2750.
18. Han L., Ma C., Liu Q., Weng H.J., Cui Y., Tang Z., Kim Y., Nie H., Qu L., Patel K.N., et al. A subpopulation of nociceptors specifically linked to itch. Nat. Neurosci. 2013, 16:174-182.
19. Hepp R., Tricoire L., Hu E., Gervasi N., Paupardin-Tritsch D., Lambolez B., Vincent P. Phosphodiesterase type 2 and the homeostasis of cyclic GMP in living thalamic neurons. J.Neurochem. 2007, 102:1875-1886.
20. Hollinger S., Hepler J.R. Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol. Rev. 2002, 54:527-559.
21. Hwang J.H., Yaksh T.L. The effect of spinal GABA receptor agonists on tactile allodynia in a surgically-induced neuropathic pain model in the rat. Pain 1997, 70:15-22.
22. Ibuki T., Hama A.T., Wang X.T., Pappas G.D., Sagen J. Loss of GABA-immunoreactivity in the spinal dorsal horn of rats with peripheral nerve injury and promotion of recovery by adrenal medullary grafts. Neuroscience 1997, 76:845-858.
23. Iyadomi M., Iyadomi I., Kumamoto E., Tomokuni K., Yoshimura M. Presynaptic inhibition by baclofen of miniature EPSCs and IPSCs insubstantia gelatinosa neurons of the adult rat spinal dorsal horn. Pain 2000, 85:385-393.
24. Janson W., Stein C. Peripheral opioid analgesia. Curr. Pharm. Biotechnol. 2003, 4:270-274.
25. Jasmin L., Rabkin S.D., Granato A., Boudah A., Ohara P.T. Analgesia and hyperalgesia from GABA-mediated modulation of the cerebral cortex. Nature 2003, 424:316-320.
26. Laffray S., Bouali-Benazzouz R., Papon M.A., Favereaux A., Jiang Y., Holm T., Spriet C., Desbarats P., Fossat P., Le Feuvre Y., et al. Impairment of GABAB receptor dimer by endogenous 14-3-3ζ in chronic pain conditions. EMBO J. 2012, 31:3239-3251.
27. Latremoliere A., Woolf C.J. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J.Pain 2009, 10:895-926.
28. Legha W., Gaillard S., Gascon E., Malapert P., Hocine M., Alonso S., Moqrich A. stac1 and stac2 genes define discrete and distinct subsets of dorsal root ganglia neurons. Gene Expr. Patterns 2010, 10:368-375.
29. Li L., Rutlin M., Abraira V.E., Cassidy C., Kus L., Gong S., Jankowski M.P., Luo W., Heintz N., Koerber H.R., et al. The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 2011, 147:1615-1627.
30. Lüscher C., Slesinger P.A. Emerging roles for G protein-gated inwardly rectifying potassium (GIRK) channels in health and disease. Nat. Rev. Neurosci. 2010, 11:301-315.
31. McGlone F., Wessberg J., Olausson H. Discriminative and affective touch: sensing and feeling. Neuron 2014, 82:737-755.
32. Moore K.A., Kohno T., Karchewski L.A., Scholz J., Baba H., Woolf C.J. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J.Neurosci. 2002, 22:6724-6731.
33. Moqrich A., Earley T.J., Watson J., Andahazy M., Backus C., Martin-Zanca D., Wright D.E., Reichardt L.F., Patapoutian A. Expressing TrkC from the TrkA locus causes a subset of dorsal root ganglia neurons to switch fate. Nat. Neurosci. 2004, 7:812-818.
34. Nockemann D., Rouault M., Labuz D., Hublitz P., McKnelly K., Reis F.C., Stein C., Heppenstall P.A. The K(+) channel GIRK2 is both necessary and sufficient for peripheral opioid-mediated analgesia. EMBO Mol Med 2013, 5:1263-1277.
35. Patel S., Naeem S., Kesingland A., Froestl W., Capogna M., Urban L., Fox A. The effects of GABA(B) agonists and gabapentin on mechanical hyperalgesia in models of neuropathic and inflammatory pain in the rat. Pain 2001, 90:217-226.
36. Polito M., Klarenbeek J., Jalink K., Paupardin-Tritsch D., Vincent P., Castro L.R. The NO/cGMP pathway inhibits transient cAMP signals through the activation of PDE2 in striatal neurons. Front Cell Neurosci 2013, 7:211.
37. Price G.W., Kelly J.S., Bowery N.G. The location of GABAB receptor binding sites in mammalian spinal cord. Synapse 1987, 1:530-538.
38. Remondes M., Schuman E.M. Molecular mechanisms contributing to long-lasting synaptic plasticity at the temporoammonic-CA1 synapse. Learn. Mem. 2003, 10:247-252.
39. Scherrer G., Imamachi N., Cao Y.Q., Contet C., Mennicken F., O'Donnell D., Kieffer B.L., Basbaum A.I. Dissociation of the opioid receptor mechanisms that control mechanical and heat pain. Cell 2009, 137:1148-1159.
40. Schuler V., Lüscher C., Blanchet C., Klix N., Sansig G., Klebs K., Schmutz M., Heid J., Gentry C., Urban L., et al. Epilepsy, hyperalgesia, impaired memory, and loss of pre- and postsynaptic GABA(B) responses in mice lacking GABA(B(1)). Neuron 2001, 31:47-58.
41. Schwenk F., Baron U., Rajewsky K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 1995, 23:5080-5081.
42. Seal R.P., Wang X., Guan Y., Raja S.N., Woodbury C.J., Basbaum A.I., Edwards R.H. Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. Nature 2009, 462:651-655.
43. Shields S.D., Cavanaugh D.J., Lee H., Anderson D.J., Basbaum A.I. Pain behavior in the formalin test persists after ablation of the great majority of C-fiber nociceptors. Pain 2010, 151:422-429.
44. Smith G.D., Harrison S.M., Birch P.J., Elliott P.J., Malcangio M., Bowery N.G. Increased sensitivity to the antinociceptive activity of (+/-)-baclofen in an animal model of chronic neuropathic, but not chronic inflammatory hyperalgesia. Neuropharmacology 1994, 33:1103-1108.
45. Takeda M., Tanimoto T., Ikeda M., Kadoi J., Matsumoto S. Activaton of GABAB receptor inhibits the excitability of rat small diameter trigeminal root ganglion neurons. Neuroscience 2004, 123:491-505.
46. Tatebayashi H., Ogata N. Kinetic analysis of the GABAB-mediated inhibition of the high-threshold Ca2+ current in cultured rat sensory neurones. J.Physiol. 1992, 447:391-407.
47. Tedford H.W., Zamponi G.W. Direct G protein modulation of Cav2 calcium channels. Pharmacol. Rev. 2006, 58:837-862.
48. Towers S., Princivalle A., Billinton A., Edmunds M., Bettler B., Urban L., Castro-Lopes J., Bowery N.G. GABAB receptor protein and mRNA distribution in rat spinal cord and dorsal root ganglia. Eur. J. Neurosci. 2000, 12:3201-3210.
49. Vilar B., Busserolles J., Ling B., Laffray S., Ulmann L., Malhaire F., Chapuy E., Aissouni Y., Etienne M., Bourinet E., et al. Alleviating pain hypersensitivity through activation of type 4 metabotropic glutamate receptor. J.Neurosci. 2013, 33:18951-18965.
50. Vrontou S., Wong A.M., Rau K.K., Koerber H.R., Anderson D.J. Genetic identification of C fibres that detect massage-like stroking of hairy skin invivo. Nature 2013, 493:669-673.
51. Wang X.L., Zhang H.M., Chen S.R., Pan H.L. Altered synaptic input and GABAB receptor function in spinal superficial dorsal horn neurons in rats with diabetic neuropathy. J.Physiol. 2007, 579:849-861.
52. Yang K., Wang D., Li Y.Q. Distribution and depression of the GABA(B) receptor in the spinal dorsal horn of adult rat. Brain Res. Bull. 2001, 55:479-485.
53. Zotterman Y. Touch, pain and tickling: an electro-physiological investigation on cutaneous sensory nerves. J.Physiol. 1939, 95:1-28.
54. Zylka M.J., Rice F.L., Anderson D.J. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron 2005, 45:17-25.