Selective regulation of recombinantly expressed mGlu7 metabotropic glutamate receptors by G protein-coupled receptor kinases and arrestins

Neuropharmacology

Volumn 77, Issue , 2014, Pages 303-312

  Iacovelli, L ^a   Felicioni, M ^c   Nistico R ^a,c   Nicoletti, F ^a,d   De Blasi, A ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d IRCCS NEUROMED   (Italy)

Author keywords

Arrestins; GRK; Jun kinases; MAP kinases; mGlu7 receptors; Signaling regulation

Indexed keywords

ADENYLATE CYCLASE; BETA ARRESTIN 1; BETA ARRESTIN 2; G PROTEIN COUPLED RECEPTOR KINASE; G PROTEIN COUPLED RECEPTOR KINASE 2; G PROTEIN COUPLED RECEPTOR KINASE 4; ISOPROTEIN; METABOTROPIC RECEPTOR 7; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; RECEPTOR SUBTYPE; RECOMBINANT METABOTROPIC RECEPTOR 7; RECOMBINANT PROTEIN; RETINA S ANTIGEN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ARRESTINS; C-JUN N-TERMINAL KINASE; C-TERMINAL DOMAIN OF GRK2; FORSKOLIN; FSK; G PROTEIN-COUPLED RECEPTOR; G PROTEIN-COUPLED RECEPTOR KINASE; GPCR; GRK; GRK2-CTER; GRK2-K220R; JNK; JUN KINASES; KINASE-DEAD GRK2 MUTANT; L-2-AMINO-4-PHOSPHONOBUTANOATE; L-AP4; MAP KINASES; MAPK; METABOTROPIC GLUTAMATE RECEPTOR; MGLU; MGLU7 RECEPTORS; MYTOGEN ACTIVATED PROTEIN KINASES; SIGNALING REGULATION;

AMINOBUTYRATES; ARRESTINS; BENZHYDRYL COMPOUNDS; G-PROTEIN-COUPLED RECEPTOR KINASES; HEK293 CELLS; HUMANS; PHOSPHORYLATION; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION;

EID: 84887088263     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.10.013     Document Type: Article

References (60)

1. I. Aramori, S.S. Ferguson, P.D. Bieniasz, J. Zhang, B. Cullen, and M.G. Caron Molecular mechanism of desensitization of the chemokine receptor CCR-5: receptor signaling and internalization are dissociable from its role as an HIV-1 coreceptor EMBO J. 16 1997 4606 4616
2. S. Ahn, H. Wei, T.R. Garrison, and R.J. Lefkowitz Reciprocal regulation of angiotensin receptor-activated extracellular signal-regulated kinases by beta-arrestins 1 and 2 J. Biol. Chem. 279 2004 7807 7811
3. N. Barden Implication of the hypothalamic-pituitary-adrenal axis in the physiopathology of depression J. Psychiatry Neurosci. 29 2004 185 193
4. F. Bertaso, C. Zhang, A. Scheschonka, F. de Bock, P. Fontanaud, P. Marin, R.L. Huganir, H. Betz, J. Bockaert, L. Fagni, and M. Lerner-Natoli PICK1 uncoupling from mGluR7a causes absence-like seizures Nat. Neurosci. 11 2008 940 948
5. T.J. Bushell, G. Sansig, V.J. Collett, H. van der Putten, and G.L. Collingridge Altered short-term synaptic plasticity in mice lacking the metabotropic glutamate receptor mGlu7 ScientificWorldJournal 2 2002 730 737
6. G. Calabrese, M. Sallese, A. Stornaiuolo, L. Stuppia, G. Palka, and A. De Blasi Chromosome mapping of the human arrestin (SAG), beta-arrestin 2 (ARRB2), and beta-adrenergic receptor kinase 2 (ADRBK2) genes Genomics 23 1994 286 288
7. Z. Callaerts-Vegh, T. Beckers, S.M. Ball, F. Baeyens, P.F. Callaerts, J.F. Cryan, E. Molnar, and R. D'Hooge Concomitant deficits in working memory and fear extinction are functionally dissociated from reduced anxiety in metabotropic glutamate receptor 7-deficient mice J. Neurosci. 26 2006 6573 6582
8. P.J. Conn, and C.M. Niswender mGluR7's lucky number Proc. Natl. Acad. Sci. U. S. A. 103 2006 251 252
9. J.F. Cryan, P.H. Kelly, H.C. Neijt, G. Sansig, P.J. Flor, and H. van Der Putten Antidepressant and anxiolytic-like effects in mice lacking the group III metabotropic glutamate receptor mGluR7 Eur. J. Neurosci. 17 2003 2409 2417
10. S.M. DeWire, S. Ahn, R.J. Lefkowitz, and S.K. Shenoy Beta-arrestins and cell signalling Annu. Rev. Physiol. 69 2007 483 510
11. G.K. Dhami, L.B. Dale, P.H. Anborgh, K.E. O'Connor-Halligan, R. Sterne-Marr, and S.S. Ferguson G protein-coupled receptor kinase 2 regulator of G protein signaling homology domain binds to both metabotropic glutamate receptor 1a and Gαq to attenuate signaling J. Biol. Chem. 279 2004 16614 16620
12. T. Eichmann, K. Lorenz, M. Hoffmann, J. Brockmann, C. Krasel, M.J. Lohse, and U. Quitterer The amino-terminal domain of G-protein-coupled receptor kinase 2 is a regulatory Gbeta gamma binding site J. Biol. Chem. 278 2003 8052 8057
13. S.S. Ferguson Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling Pharmacol. Rev. 53 2001 1 24
14. J.J. Ferrero, D. Bartolomé-Martín, M. Torres, and J. Sánchez-Prieto Potentiation of mGlu7 receptor-mediated glutamate release at nerve terminals containing N and P/Q type Ca2+ channels Neuropharmacology 67 2013 213 222
15. J.J. Ferrero, M. Torres, and J. Sánchez-Prieto Inhibitors of diacylglycerol metabolism reduce time to the onset of glutamate release potentation by mGlu7 receptors Neurosci. Lett. 500 2011 144 147
16. P.J. Flor, H. Van Der Putten, D. Rüegg, S. Lukic, T. Leonhardt, M. Bence, G. Sansig, T. Knöpfel, and R. Kuhn A novel splice variant of a metabotropic glutamate receptor, human mGluR7b Neuropharmacology 36 1997 153 159
17. R.A. Friedman, L. Van Laer, M.J. Huentelman, S.S. Sheth, E. Van Eyken, J.J. Corneveaux, W.D. Tembe, R.F. Halperin, A.Q. Thorburn, S. Thys, S. Bonneux, E. Fransen, J. Huyghe, I. Pyykkö, C.W. Cremers, H. Kremer, I. Dhooge, D. Stephens, E. Orzan, M. Pfister, M. Bille, A. Parving, M. Sorri, P.H. Van de Heyning, L. Makmura, J.D. Ohmen, F.H. Linthicum Jr., J.N. Fayad, J.V. Pearson, D.W. Craig, D.A. Stephan, and G. Van Camp GRM7 variants confer susceptibility to age-related hearing impairment Hum. Mol. Genet. 18 2009 785 796
18. O.B. Goodman Jr., J.G. Krupnick, F. Santini, V.V. Gurevich, R.B. Penn, A.W. Gagnon, J.H. Keen, and J.L. Benovic Beta-arrestin acts as a clathrin adaptor in endocytosis of the beta2-adrenergic receptor Nature 383 1996 447 450
19. H. Hikichi, T. Murai, S. Okuda, S. Maehara, A. Satow, S. Ise, M. Nishino, G. Suzuki, H. Takehana, M. Hata, and H. Ohta Effects of a novel metabotropic glutamate receptor 7 negative allosteric modulator,6-(4-methoxyphenyl)-5-methyl- 3-pyridin-4-ylisoxazonolo[4,5-c]pyridin-4(5H)-one (MMPIP), on the central nervous system in rodents Eur. J. Pharmacol. 639 2010 106 114
20. L. Iacovelli, V. Bruno, L. Salvatore, D. Melchiorri, R. Gradini, A. Caricasole, E. Barletta, A. De Blasi, and F. Nicoletti Native group-III metabotropic glutamate receptors are coupled to the mitogen-activated protein kinase/phosphatidylinositol-3-kinase pathways J. Neurochem. 82 2002 216 223
21. L. Iacovelli, L. Capobianco, M. Iula, V. Di Giorgi Gerevini, A. Picascia, J. Blahos, D. Melchiorri, F. Nicoletti, and A. De Blasi Regulation of mGlu4 metabotropic glutamate receptor signaling by type-2 G-protein coupled receptor kinase (GRK2) Mol. Pharmacol. 65 2004 1103 1110
22. L. Iacovelli, G. Molinaro, G. Battaglia, M. Motolese, L. Di Menna, M. Alfiero, J. Blahos, F. Matrisciano, M. Corsi, C. Corti, V. Bruno, A. De Blasi, and F. Nicoletti Regulation of group II metabotropic glutamate receptors by G protein-coupled receptor kinases: mGlu2 receptors are resistant to homologous desensitization Mol. Pharmacol. 75 2009 991 1003
23. L. Iacovelli, F. Nicoletti, and A. De Blasi Molecular mechanisms that desensitize metabotropic glutamate receptor signaling: an overview Neuropharmacology 66 2013 24 30
24. L. Iacovelli, L. Salvatore, L. Capobianco, A. Picascia, E. Barletta, M. Storto, S. Mariggiò, M. Sallese, A. Porcellini, F. Nicoletti, and A. De Blasi Role of G protein-coupled receptor kinase 4 and beta-arrestin 1 in agonist-stimulated metabotropic glutamate receptor 1 internalization and activation of mitogen-activated protein kinases J. Biol. Chem. 278 2003 12433 12442
25. M. Julio-Pieper, P.J. Flor, T.G. Dinan, and J.F. Cryan Exciting times beyond the brain: metabotropic glutamate receptors in peripheral and non-neural tissues Pharmacol. Rev. 63 2011 35 58
26. M. Julio-Pieper, N.P. Hyland, J.A. Bravo, T.G. Dinan, and J.F. Cryan A novel role for the metabotropic glutamate receptor-7: modulation of faecal water content and colonic electrolyte transport in the mouse Br. J. Pharmacol. 160 2010 367 375
27. M. Kalinichev, M. Rouillier, F. Girard, I. Royer-Urios, B. Bournique, T. Finn, D. Charvin, B. Campo, E. Le Poul, V. Mutel, S. Poli, S.A. Neale, T.E. Salt, and R. Lütjens ADX71743, a potent and selective negative allosteric modulator of metabotropic glutamate receptor 7: in vitro and in vivo characterization J. Pharmacol. Exp. Ther. 344 2013 624 636
28. A. Kinoshita, R. Shigemoto, H. Ohishi, H. van der Putten, and N. Mizuno Immunohistochemical localization of metabotropic glutamate receptors, mGluR7a and mGluR7b, in the central nervous system of the adult rat and mouse: a light and electron microscopic study J. Comp. Neurol. 393 1998 332 352
29. T.A. Kohout, and R.J. Lefkowitz Regulation of G protein-coupled receptor kinases and arrestins during receptor desensitization Mol. Pharmacol. 63 2003 9 18
30. L.M. Luttrell, and R.J. Lefkowitz The role of beta-arrestins in the termination and transduction of G-protein-coupled receptor signals J. Cell Sci. 115 2002 455 465
31. L.M. Luttrell, F.L. Roudabush, E.W. Choy, W.E. Miller, M.E. Field, K.L. Pierce, and R.J. Lefkowitz Activation and targeting of extracellular signal-regulated kinases by beta-arrestin scaffolds Proc. Natl. Acad. Sci. U. S. A. 98 2001 2449 2454
32. R. Martín, D. Bartolomé-Martín, M. Torres, and J. Sánchez-Prieto Non-additive potentiation of glutamate release by phorbol esters and metabotropic mGlu7 receptor in cerebrocortical nerve terminals J. Neurochem. 116 2011 476 485
33. R. Martín, T. Durroux, F. Ciruela, M. Torres, J.P. Pin, and J. Sánchez-Prieto The metabotropic glutamate receptor mGlu7 activates phospholipase C, translocates munc-13-1 protein, and potentiates glutamate release at cerebrocortical nerve terminals J. Biol. Chem. 285 2010 17907 17917
34. R. Martín, C. Ladera, D. Bartolomé-Martín, M. Torres, and J. Sánchez-Prieto The inhibition of release by mGlu7 receptors is independent of the Ca2+ channel type but associated to GABAB and adenosine A1 receptors Neuropharmacology 55 2008 464 473
35. C. Millán, R. Luján, R. Shigemoto, and J. Sánchez-Prieto The inhibition of glutamate release by metabotropic glutamate receptor 7 affects both [Ca2+]c and cAMP: evidence for a strong reduction of Ca2+ entry in single nerve terminals J. Biol. Chem. 277 2002 14092 14101
36. K. Mitsukawa, C. Mombereau, E. Lötscher, D.P. Uzunov, H. van der Putten, P.J. Flor, and J.F. Cryan Metabotropic glutamate receptor subtype 7 ablation causes dysregulation of the HPA axis and increases hippocampal BDNF protein levels: implications for stress-related psychiatric disorders Neuropsychopharmacology 31 2006 1112 1122
37. K. Mitsukawa, R. Yamamoto, S. Ofner, J. Nozulak, O. Pescott, S. Lukic, N. Stoehr, C. Mombereau, R. Kuhn, K.H. McAllister, H. van der Putten, J.F. Cryan, and P.J. Flor A selective metabotropic glutamate receptor 7 agonist: activation of receptor signaling via an allosteric site modulates stress parameters in vivo Proc. Natl. Acad. Sci. U. S. A. 102 2005 18712 18717
38. S.J. Mundell, G. Pula, K. Carswell, P.J. Roberts, and E. Kelly Agonist-induced internalization of metabotropic glutamate receptor 1A: structural determinants for protein kinase C- and G protein-coupled receptor kinase-mediated internalization J. Neurochem. 84 2003 294 304
39. F. Nicoletti, J. Bockaert, G.L. Collingridge, P.J. Conn, F. Ferraguti, D.D. Schoepp, J.T. Wroblewski, and J.P. Pin Metabotropic glutamate receptors: from the workbench to the bedside Neuropharmacology 60 2011 1017 1041
40. C.M. Niswender, and P.J. Conn Metabotropic glutamate receptors: physiology, pharmacology, and disease Annu. Rev. Pharmacol. Toxicol. 50 2010 295 322
41. R.M. O'Connor, B.C. Finger, P.J. Flor, and J.F. Cryan Metabotropic glutamate receptor 7: at the interface of cognition and emotion Eur. J. Pharmacol. 639 2010 123 131
42. A. Pałucha-Poniewiera, and A. Pilc A selective mGlu7 receptor antagonist MMPIP reversed antidepressant-like effects of AMN082 in rats Behav. Brain Res. 238 2013 109 112
43. K.A. Pelkey, X. Yuan, G. Lavezzari, K.W. Roche, and C.J. McBain mGluR7 undergoes rapid internalization in response to activation by the allosteric agonist AMN082 Neuropharmacology 52 2007 108 117
44. J. Perroy, S. Richard, J. Nargeot, J. Bockaert, and L. Fagni Permissive effect of voltage on mGlu 7 receptor subtype signaling in neurons J. Biol. Chem. 277 2002 1223 1228
45. E. Reiter, S. Ahn, A.K. Shukla, and R.J. Lefkowitz Molecular mechanism of β-arrestin-biased agonism at seven-transmembrane receptors Annu. Rev. Pharmacol. Toxicol. 52 2012 179 197
46. X.R. Ren, E. Reiter, S. Ahn, J. Kim, W. Chen, and R.J. Lefkowitz Different G protein-coupled receptor kinases govern G protein and beta-arrestin-mediated signaling of V2 vasopressin receptor Proc. Natl. Acad. Sci. U. S. A. 102 2005 1448 1453
47. M. Sallese, L. Salvatore, E. D'Urbano, G. Sala, M. Storto, T. Launey, F. Nicoletti, T. Knopfel, and A. De Blasi The G-protein-coupled receptor kinase GRK4 mediates homologous desensitization of metabotropic glutamate receptor 1 FASEB J. 14 2000 2569 2580
48. G. Sansig, T.J. Bushell, V.R. Clarke, A. Rozov, N. Burnashev, C. Portet, F. Gasparini, M. Schmutz, K. Klebs, R. Shigemoto, P.J. Flor, R. Kuhn, T. Knoepfel, M. Schroeder, D.R. Hampson, V.J. Collett, C. Zhang, R.M. Duvoisin, G.L. Collingridge, and H. van Der Putten Increased seizure susceptibility in mice lacking metabotropic glutamate receptor 7 J. Neurosci. 21 2001 8734 8745
49. J.A. Saugstad, J.M. Kinzie, E.R. Mulvihill, T.P. Segerson, and G.L. Westbrook Cloning and expression of a new member of the L-2-amino-4- phosphonobutyric acid-sensitive class of metabotropic glutamate receptors Mol. Pharmacol. 45 1994 367 372
50. T. Sherrin, T. Blank, and C. Todorovic c-Jun N-terminal kinases in memory and synaptic plasticity Rev. Neurosci. 22 2011 403 410
51. D.D. Schoepp, D.E. Jane, and J.A. Monn Pharmacological agents acting at subtypes of metabotropic glutamate receptors Neuropharmacology 38 1999 1431 1476
52. A. Simonyi, L.A. Miller, and G.Y. Sun Region-specific decline in the expression of metabotropic glutamate receptor 7 mRNA in rat brain during aging Brain Res. Mol. Brain Res. 82 2000 101 106
53. S.D. Sorensen, and P.J. Conn G protein-coupled receptor kinases regulate metabotropic glutamate receptor 5 function and expression Neuropharmacology 44 2003 699 706
54. Y.H. Suh, J.Y. Park, S. Park, I. Jou, P.A. Roche, and K.W. Roche Regulation of metabotropic glutamate receptor 7 (mGluR7) internalization and surface expression by Ser/Thr protein phosphatase 1 J. Biol. Chem. 288 2013 17544 17551
55. M. Summa, S. Di Prisco, M. Grilli, C. Usai, M. Marchi, and A. Pittaluga Presynaptic mGlu7 receptors control GABA release in mouse hippocampus Neuropharmacology 66 2013 215 224
56. G. Suzuki, N. Tsukamoto, H. Fushiki, A. Kawagishi, M. Nakamura, H. Kurihara, M. Mitsuya, M. Ohkubo, and H. Ohta In vitro pharmacological characterization of novel isoxazolopyridone derivatives as allosteric metabotropic glutamate receptor 7 antagonists J. Pharmacol. Exp. Ther. 323 2007 147 156
57. T. Takarada, E. Hinoi, V.J. Balcar, H. Taniura, and Y. Yoneda Possible expression of functional glutamate transporters in the rat testis J. Endocrinol. 181 2004 233 244
58. Y. Tian, Y. Liu, X. Chen, Q. Kang, J. Zhang, Q. Shi, and H. Zhang AMN082 promotes the proliferation and differentiation of neural progenitor cells with influence on phosphorylation of MAPK signaling pathways Neurochem. Int. 57 2010 8 15
59. A. Tohgo, E.W. Choy, D. Gesty-Palmer, K.L. Pierce, S. Laporte, R.H. Oakley, M.G. Caron, R.J. Lefkowitz, and L.M. Luttrell The stability of the G protein-coupled receptor-beta-arrestin interaction determines the mechanism and functional consequence of ERK activation J. Biol. Chem. 278 2003 6258 6267
60. H. Watanabe, J. Xu, C. Bengra, P.A. Jose, and R.A. Felder Desensitization of human renal D1 dopamine receptors by G protein-coupled receptor kinase 4 Kidney Int. 62 2002 790 798