GRK2 protein-mediated transphosphorylation contributes to loss of function of μ-opioid receptors induced by neuropeptide FF (NPFF 2) receptors

Journal of Biological Chemistry

Volumn 287, Issue 16, 2012, Pages 12736-12749

  Moulédous, Lionel ^a   Froment, Carine ^a   Dauvillier, Stéphanie ^a   Burlet Schiltz, Odile ^a   Zajac, Jean Marie ^a   Mollereau, Catherine ^a  

^a UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AFTER-TREATMENT; CENTRAL NERVOUS SYSTEMS; G PROTEIN; MASS SPECTROMETRIC ANALYSIS; MOLECULAR MECHANISM; NEUROBLASTOMA CELLS; NEUROPEPTIDES; OPIOID RECEPTORS; PERTUSSIS TOXIN; RECEPTOR ACTIVATION; RECEPTOR COMPLEX; RECEPTOR SIGNALING;

ENZYMES; MASS SPECTROMETRY; PROTEINS; SIGNAL TRANSDUCTION;

PHOSPHORYLATION;

BETA ARRESTIN 2; G PROTEIN COUPLED RECEPTOR KINASE 2; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; NEUROPEPTIDE FF2 RECEPTOR; NEUROPEPTIDE FF2 RECEPTOR AGONIST; NEUROPEPTIDE RECEPTOR; OPIATE AGONIST; PERTUSSIS TOXIN; PHOSPHOTRANSFERASE; SECOND MESSENGER DEPENDENT KINASE; SERINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANALGESICS, OPIOID; ARRESTINS; CELL LINE, TUMOR; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; G-PROTEIN-COUPLED RECEPTOR KINASE 2; GENE KNOCKDOWN TECHNIQUES; HETEROTRIMERIC GTP-BINDING PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; NEUROBLASTOMA; PHOSPHORYLATION; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROPEPTIDE; RECEPTORS, OPIOID, MU; SECOND MESSENGER SYSTEMS; SERINE; SIGNAL TRANSDUCTION;

EID: 84859758908     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.314617     Document Type: Article

References (72)

1. Bailey, C. P., and Connor, M. (2005) Opioids. Cellular mechanisms of tolerance and physical dependence. Curr. Opin. Pharmacol. 5, 60-68 (Pubitemid 40124536)
2. Christie, M. J. (2008) Cellular neuroadaptations to chronic opioids. Tolerance, withdrawal, and addiction. Br. J. Pharmacol. 154, 384-396
3. Dang, V. C., and Christie, M. J. (2012) Mechanisms of rapid opioid receptor desensitization, resensitization, and tolerance in brain neurons. Br. J. Pharmacol. 165, 1704-1716
4. Martini, L., and Whistler, J. L. (2007) The role of μ-opioid receptor desensitization and endocytosis in morphine tolerance and dependence. Curr. Opin. Neurobiol. 17, 556-564
5. Raehal, K. M., Schmid, C. L., Groer, C. E., and Bohn, L. M. (2011) Functional selectivity at the μ-opioid receptor. Implications for understanding opioid analgesia and tolerance. Pharmacol. Rev. 63, 1001-1019
6. Ossipov, M. H., Lai, J., King, T., Vanderah, T. W., and Porreca, F. (2005) Underlying mechanisms of pronociceptive consequences of prolonged morphine exposure. Biopolymers 80, 319-324 (Pubitemid 40791062)
7. Elhabazi, K., Trigo, J. M., Mollereau, C., Moulédous, L., Zajac, J. M., Bihel, F., Schmitt, M., Bourguignon, J. J., Meziane, H., Petit-demoulière, B., Bockel, F., Maldonado, R., and Simonin, F. (2012) Involvement of neuropeptide FF receptors in neuroadaptive responses to acute and chronic opiate treatments. Br. J. Pharmacol. 165, 424-435
8. Simonin, F., Schmitt, M., Laulin, J. P., Laboureyras, E., Jhamandas, J. H., MacTavish, D., Matifas, A., Mollereau, C., Laurent, P., Parmentier, M., Kieffer, B. L., Bourguignon, J. J., and Simonnet, G. (2006) RF9, a potent and selective neuropeptide FF receptor antagonist, prevents opioid-induced tolerance associated with hyperalgesia. Proc. Natl. Acad. Sci. U.S.A. 103, 466-471 (Pubitemid 43122424)
9. Panula, P., Aarnisalo, A. A., and Wasowicz, K. (1996) Neuropeptide FF, a mammalian neuropeptide with multiple functions. Prog. Neurobiol. 48, 461-487 (Pubitemid 26189425)
10. Vilim, F. S., Aarnisalo, A. A., Nieminen, M. L., Lintunen, M., Karlstedt, K., Kontinen, V. K., Kalso, E., States, B., Panula, P., and Ziff, E. (1999) Gene for pain modulatory neuropeptide NPFF. Induction in spinal cord by noxious stimuli. Mol. Pharmacol. 55, 804-811 (Pubitemid 29214599)
11. Zajac, J. M. (2001) Neuropeptide FF. New molecular insights. Trends Pharmacol. Sci. 22, 63
12. Yang, H. Y., Tao, T., and Iadarola, M. J. (2008) Modulatory role of neuropeptide FF system in nociception and opiate analgesia. Neuropeptides 42, 1-18 (Pubitemid 351187791)
13. Dupouy, V., and Zajac, J. M. (1995) Effects of neuropeptide FF analogs on morphine analgesia in the nucleus raphe dorsalis. Regul. Pept. 59, 349-356
14. Dupouy, V., and Zajac, J. M. (1997) Neuropeptide FF receptors control morphine-induced analgesia in the parafascicular nucleus and the dorsal raphe nucleus. Eur. J. Pharmacol. 330, 129-137 (Pubitemid 27296714)
15. Kotlinska, J., Pachuta, A., Dylag, T., and Silberring, J. (2007) Neuropeptide FF (NPFF) reduces the expression of morphine- but not of ethanol-induced conditioned place preference in rats. Peptides 28, 2235-2242 (Pubitemid 47600409)
16. Marchand, S., Betourne, A., Marty, V., Daumas, S., Halley, H., Lassalle, J. M., Zajac, J. M., and Frances, B. (2006) A neuropeptide FF agonist blocks the acquisition of conditioned place preference to morphine in C57Bl/6J mice. Peptides 27, 964-972
17. Moulédous, L., Mollereau, C., and Zajac, J. M. (2010) Opioid-modulating properties of the neuropeptide FF system. Biofactors 36, 423-429
18. Mollereau, C., Roumy, M., and Zajac, J. M. (2005) Opioid-modulating peptides. Mechanisms of action. Curr. Top. Med. Chem. 5, 341-355
19. Yang, H. Y., Fratta, W., Majane, E. A., and Costa, E. (1985) Isolation, sequencing, synthesis, and pharmacological characterization of two brain neuropeptides that modulate the action of morphine. Proc. Natl. Acad. Sci. U.S.A. 82, 7757-7761 (Pubitemid 16204428)
20. Gicquel, S., Mazarguil, H., Allard, M., Simonnet, G., and Zajac, J. M. (1992) Analogs of F8Famide resistant to degradation, with high affinity and in vivo effects. Eur. J. Pharmacol. 222, 61-67
21. Moulédous, L., Frances, B., and Zajac, J. M. (2010) Modulation of basal and morphine-induced neuronal activity by a NPFF(2) selective agonist measured by c-Fos mapping of the mouse brain. Synapse 64, 672-681
22. 2+ channels in rat spinal ganglion neurones. Neuroreport 7, 2979-2981
23. Mollereau, C., Mazarguil, H., Zajac, J. M., and Roumy, M. (2005) Neuropeptide FF (NPFF) analogs functionally antagonize opioid activities in NPFF2 receptor-transfected SH-SY5Y neuroblastoma cells. Mol. Pharmacol. 67, 965-975 (Pubitemid 40365344)
24. Chuang, T. T., Iacovelli, L., Sallese, M., and De Blasi, A. (1996) G protein-coupled receptors. Heterologous regulation of homologous desensitization and its implications. Trends Pharmacol. Sci. 17, 416-421 (Pubitemid 26401700)
25. Rozenfeld, R., and Devi, L. A. (2010) Receptor heteromerization and drug discovery. Trends Pharmacol. Sci. 31, 124-130
26. van Rijn, R. M., Whistler, J. L., and Waldhoer, M. (2010) Opioid-receptor-heteromer-specific trafficking and pharmacology. Curr. Opin. Pharmacol. 10, 73-79
27. Pfeiffer, M., Koch, T., Schröder, H., Laugsch, M., Höllt, V., and Schulz, S. (2002) Heterodimerization of somatostatin and opioid receptors crossmodulates phosphorylation, internalization, and desensitization. J. Biol. Chem. 277, 19762-19772 (Pubitemid 34967492)
28. Pfeiffer, M., Kirscht, S., Stumm, R., Koch, T., Wu, D., Laugsch, M., Schröder, H., Höllt, V., and Schulz, S. (2003) Heterodimerization of substance P and μ-opioid receptors regulates receptor trafficking and resensitization. J. Biol. Chem. 278, 51630-51637 (Pubitemid 38020408)
29. 2A-adrenergic receptors in neurons. J. Biol. Chem. 284, 6270-6281
30. Evans, R. M., You, H., Hameed, S., Altier, C., Mezghrani, A., Bourinet, E., and Zamponi, G. W. (2010) Heterodimerization of ORL1 and opioid receptors and its consequences for N-type calcium channel regulation. J. Biol. Chem. 285, 1032-1040
31. 2A- adrenergic and μ-opioid receptors controls cell signaling. Nat. Chem. Biol. 4, 126-131
32. Roumy, M., Lorenzo, C., Mazères, S., Bouchet, S., Zajac, J. M., and Mollereau, C. (2007) Physical association between neuropeptide FF and micro-opioid receptors as a possible molecular basis for anti-opioid activity. J. Biol. Chem. 282, 8332-8342 (Pubitemid 47093614)
33. Kersanté, F., Moulédous, L., Zajac, J. M., and Mollereau, C. (2010) Modulation by neuropeptide FF of the interaction of μ-opioid (MOP) receptor with G proteins. Neurochem. Int. 56, 768-773
34. Moulédous, L., Merker, S., Neasta, J., Roux, B., Zajac, J. M., and Mollereau, C. (2008) Neuropeptide FF-sensitive confinement of μ-opioid receptor does not involve lipid rafts in SH-SY5Y cells. Biochem. Biophys. Res. Commun. 373, 80-84
35. Chu, J., Zheng, H., Loh, H. H., and Law, P. Y. (2008) Morphine-induced μ-opioid receptor rapid desensitization is independent of receptor phosphorylation and β-arrestins. Cell. Signal. 20, 1616-1624
36. El Kouhen, R., Burd, A. L., Erickson-Herbrandson, L. J., Chang, C. Y., Law, P. Y., and Loh, H. H. (2001) Phosphorylation of Ser-363, Thr-370, and Ser-375 residues within the carboxyl tail differentially regulates μ-opioid receptor internalization. J. Biol. Chem. 276, 12774-12780
37. Schulz, S., Mayer, D., Pfeiffer, M., Stumm, R., Koch, T., and Höllt, V. (2004) Morphine induces terminal micro-opioid receptor desensitization by sustained phosphorylation of serine 375. EMBO J. 23, 3282-3289 (Pubitemid 39209152)
38. Doll, C., Konietzko, J., Pöll, F., Koch, T., Höllt, V., and Schulz, S. (2011) Agonist-selective patterns of μ-opioid receptor phosphorylation revealed by phosphosite-specific antibodies. Br. J. Pharmacol. 164, 298-307
39. Celver, J. P., Lowe, J., Kovoor, A., Gurevich, V. V., and Chavkin, C. (2001) Threonine 180 is required for G protein-coupled receptor kinase 3- and β-arrestin 2-mediated desensitization of the μ-opioid receptor in Xenopus oocytes. J. Biol. Chem. 276, 4894-4900
40. Talmont, F., Garcia, L. P., Mazarguil, H., Zajac, J. M., and Mollereau, C. (2009) Characterization of two novel tritiated radioligands for labeling neuropeptide FF (NPFF(1) and NPFF(2)) receptors. Neurochem. Int. 55, 815-819
41. Kilpatrick, L. E., Briddon, S. J., Hill, S. J., and Holliday, N. D. (2010) Quantitative analysis of neuropeptide Y receptor association with β-arrestin2 measured by bimolecular fluorescence complementation. Br. J. Pharmacol. 160, 892-906
42. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
43. Mouton-Barbosa, E., Roux-Dalvai, F., Bouyssié, D., Berger, F., Schmidt, E., Righetti, P. G., Guerrier, L., Boschetti, E., Burlet-Schiltz, O., Monsarrat, B., and Gonzalez de Peredo, A. (2010) In-depth exploration of cerebrospinal fluid by combining peptide ligand library treatment and label-free protein quantification. Mol. Cell. Proteomics 9, 1006-1021
44. Kohout, T. A., and Lefkowitz, R. J. (2003) Regulation of G protein-coupled receptor kinases and arrestins during receptor desensitization. Mol. Pharmacol. 63, 9-18 (Pubitemid 36043803)
45. Chen, Y., Long, H., Wu, Z., Jiang, X., and Ma, L. (2008) EGF transregulates opioid receptors through EGFR-mediated GRK2 phosphorylation and activation. Mol. Biol. Cell 19, 2973-2983
46. Prenzel, N., Zwick, E., Daub, H., Leserer, M., Abraham, R., Wallasch, C., and Ullrich, A. (1999) EGF receptor transactivation by G protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402, 884-888
47. Offermanns, S., Bombien, E., and Schultz, G. (1993) Stimulation of tyrosine phosphorylation and mitogen-activated protein (MAP) kinase activity in human SH-SY5Y neuroblastoma cells by carbachol. Biochem. J. 294, 545-550 (Pubitemid 23268859)
48. Rose, R. H., Briddon, S. J., and Holliday, N. D. (2010) Bimolecular fluorescence complementation. Lighting up seven transmembrane domain receptor signaling networks. Br. J. Pharmacol. 159, 738-750
49. Groer, C. E., Schmid, C. L., Jaeger, A. M., and Bohn, L. M. (2011) Agonist-directed interactions with specific β-arrestins determine μ-opioid receptor trafficking, ubiquitination, and dephosphorylation. J. Biol. Chem. 286, 31731-31741
50. Lau, E. K., Trester-Zedlitz, M., Trinidad, J. C., Kotowski, S. J., Krutchinsky, A. N., Burlingame, A. L., and von Zastrow, M. (2011) Quantitative encoding of the effect of a partial agonist on individual opioid receptors by multisite phosphorylation and threshold detection. Sci. Signal. 4, ra52
51. Busillo, J. M., Armando, S., Sengupta, R., Meucci, O., Bouvier, M., and Benovic, J. L. (2010) Site-specific phosphorylation of CXCR4 is dynamically regulated by multiple kinases and results in differential modulation of CXCR4 signaling. J. Biol. Chem. 285, 7805-7817
52. Butcher, A. J., Prihandoko, R., Kong, K. C., McWilliams, P., Edwards, J. M., Bottrill, A., Mistry, S., and Tobin, A. B. (2011) Differential G protein-coupled receptor phosphorylation provides evidence for a signaling bar code. J. Biol. Chem. 286, 11506-11518
53. Tobin, A. B., Butcher, A. J., and Kong, K. C. (2008) Location, location, location. Site-specific GPCR phosphorylation offers a mechanism for cell-type-specific signaling. Trends Pharmacol. Sci. 29, 413-420
54. Kelly, E., Bailey, C. P., and Henderson, G. (2008) Agonist-selective mechanisms of GPCR desensitization. Br. J. Pharmacol. 153, S379-S388 (Pubitemid 351340999)
55. Zheng, H., Chu, J., Zhang, Y., Loh, H. H., and Law, P. Y. (2011) Modulating micro-opioid receptor phosphorylation switches agonist-dependent signaling as reflected in PKCε activation and dendritic spine stability. J. Biol. Chem. 286, 12724-12733
56. Maurice, P., Kamal, M., and Jockers, R. (2011) Asymmetry of GPCR oligomers supports their functional relevance. Trends Pharmacol. Sci. 32, 514-520
57. Chen, C., Li, J., Bot, G., Szabo, I., Rogers, T. J., and Liu-Chen, L. Y. (2004) Heterodimerization and cross-desensitization between the μ-opioid receptor and the chemokine CCR5 receptor. Eur. J. Pharmacol. 483, 175-186 (Pubitemid 38068398)
58. 5-ol]enkephalin-induced μ-opioid receptor phosphorylation. Mol. Pharmacol. 68, 447-456
59. Shi, G. W., Chen, J., Concepcion, F., Motamedchaboki, K., Marjoram, P., and Langen, R. (2005) Light causes phosphorylation of nonactivated visual pigments in intact mouse rod photoreceptor cells. J. Biol. Chem. 280, 41184-41191 (Pubitemid 41832172)
60. Hüttenrauch, F., Pollok-Kopp, B., and Oppermann, M. (2005) G protein-coupled receptor kinases promote phosphorylation and β-arrestin-mediated internalization of CCR5 homo- and hetero-oligomers. J. Biol. Chem. 280, 37503-37515 (Pubitemid 41642359)
61. Estes, A. M., McAllen, K., Parker, M. S., Sah, R., Sweatman, T., Park, E. A., Balasubramaniam, A., Sallee, F. R., Walker, M. W., and Parker, S. L. (2011) Maintenance of Y receptor dimers in epithelial cells depends on interaction with G protein heterotrimers. Amino Acids 40, 371-380
62. Law, P. Y., Erickson-Herbrandson, L. J., Zha, Q. Q., Solberg, J., Chu, J., Sarre, A., and Loh, H. H. (2005) Heterodimerization of μ- and δ-opioid receptors occurs at the cell surface only and requires receptor-G protein interactions. J. Biol. Chem. 280, 11152-11164 (Pubitemid 40418422)
63. Parker, S. L., Parker, M. S., Sallee, F. R., and Balasubramaniam, A. (2007) Oligomerization of neuropeptide Y (NPY) Y2 receptors in CHO cells depends on functional pertussis toxin-sensitive G proteins. Regul. Pept. 144,72-81 (Pubitemid 350030301)
64. 2, and GRK2. FASEB J. 24, 4733-4743
65. 2 dopamine receptor expression and signaling independently of receptor phosphorylation.J. Biol. Chem. 284, 34103-34115
66. Fernandez, N., Gottardo, F. L., Alonso, M. N., Monczor, F., Shayo, C., and Davio, C. (2011) Roles of phosphorylation-dependent and -independent mechanisms in the regulation of histamine H2 receptor by G protein-coupled receptor kinase 2. J. Biol. Chem. 286, 28697-28706
67. Pao, C. S., and Benovic, J. L. (2002) Phosphorylation-independent desensitization of G protein-coupled receptors? Sci. STKE 2002, pe42
68. Pak, Y., O'Dowd, B. F., and George, S. R. (1997) Agonist-induced desensitization of the μ-opioid receptor is determined by threonine 394 preceded by acidic amino acids in the C-terminal tail. J. Biol. Chem. 272, 24961-24965 (Pubitemid 27415673)
69. Feng, B., Li, Z., and Wang, J. B. (2011) Protein kinase C-mediated phosphorylation of the μ-opioid receptor and its effects on receptor signaling. Mol. Pharmacol. 79, 768-775
70. Porrello, E. R., Pfleger, K. D., Seeber, R. M., Qian, H., Oro, C., Abogadie, F., Delbridge, L. M., and Thomas, W. G. (2011) Heteromerization of angiotensin receptors changes trafficking and arrestin recruitment profiles. Cell. Signal. 23, 1767-1776
71. Gurevich, V. V., and Gurevich, E. V. (2006) The structural basis of arrestin-mediated regulation of G protein-coupled receptors. Pharmacol. Ther. 110, 465-502
72. McPherson, J., Rivero, G., Baptist, M., Llorente, J., Al-Sabah, S., Krasel, C., Dewey, W. L., Bailey, C. P., Rosethorne, E. M., Charlton, S. J., Henderson, G., and Kelly, E. (2010) μ-Opioid receptors. Correlation of agonist efficacy for signaling with ability to activate internalization. Mol. Pharmacol. 78, 756-766