(R,R′)-4′-methoxy-1-naphthylfenoterol targets GPR55-mediated ligand internalization and impairs cancer cell motility

Biochemical Pharmacology

Volumn 87, Issue 4, 2014, Pages 547-561

  Paul, Rajib K ^a   Wnorowski, Artur ^b   Gonzalez Mariscal, Isabel ^a   Nayak, Surendra K ^c   Pajak, Karolina ^b   Moaddel, Ruin ^a   Indig, Fred E ^a   Bernier, Michel ^a   Wainer, Irving W ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b MEDICAL UNIVERSITY OF LUBLIN   (Poland)

^c SRI International (SKN)   (United States)

Author keywords

Cell motility; Cellular morphology; G protein coupled receptor; GPR55; Ligand internalization

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; CANNABINOID 1 RECEPTOR; DRUG DERIVATIVE; FENOTEROL; G PROTEIN COUPLED RECEPTOR; GPR55 PROTEIN, HUMAN; LIGAND; PIPERIDINE DERIVATIVE; PYRAZOLE DERIVATIVE;

ARTICLE; CELL MOTILITY; CELL MOTION; CELL STRAIN HEK293; CELL STRAIN HEPG2; CELLULAR MORPHOLOGY; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; ENDOCYTOSIS; G-PROTEIN COUPLED RECEPTOR; GPR55; HUMAN; INVERSE AGONISM; LIGAND INTERNALIZATION; METABOLISM; METHODOLOGY; MOLECULARLY TARGETED THERAPY; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

CELL MOTILITY; CELLULAR MORPHOLOGY; G-PROTEIN COUPLED RECEPTOR; GPR55; LIGAND INTERNALIZATION;

CELL MOVEMENT; DRUG INVERSE AGONISM; ENDOCYTOSIS; FENOTEROL; HEK293 CELLS; HEP G2 CELLS; HUMANS; LIGANDS; MOLECULAR TARGETED THERAPY; NEOPLASMS; PIPERIDINES; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84893806247     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2013.11.020     Document Type: Article

References (58)

1. K. Jozwiak, C. Khalid, M.J. Tanga, I. Berzetei-Gurske, L. Jimenez, and J.A. Kozocas et al. Comparative molecular field analysis of the binding of the stereoisomers of fenoterol and fenoterol derivatives to the beta2 adrenergic receptor J Med Chem 50 2007 2903 2915 (Pubitemid 46980861)
2. K. Jozwiak, A.Y. Woo, M.J. Tanga, L. Toll, L. Jimenez, and J.A. Kozocas et al. Comparative molecular field analysis of fenoterol derivatives: a platform towards highly selective and effective beta(2)-adrenergic receptor agonists Bioorg Med Chem 18 2010 728 736
3. L. Toll, L. Jimenez, N. Waleh, K. Jozwiak, A.Y. Woo, and R.P. Xiao et al. Β2-adrenergic receptor agonists inhibit the proliferation of 1321N1 astrocytoma cells J Pharmacol Exp Ther 336 2011 524 532
4. R.K. Paul, A. Ramamoorthy, J. Scheers, R.P. Wersto, L. Toll, and L. Jimenez et al. Cannabinoid receptor activation correlates with the proapoptotic action of the beta2-adrenergic agonist (R,R′)-4-methoxy-1- naphthylfenoterol in HepG2 hepatocarcinoma cells J Pharmacol Exp Ther 343 2012 157 166
5. G. Milligan G protein-coupled receptor hetero-dimerization: contribution to pharmacology and function Br J Pharmacol 158 2009 5 14
6. B.D. Hudson, T.E. Hebert, and M.E. Kelly Physical and functional interaction between CB1 cannabinoid receptors and beta2-adrenoceptors Br J Pharmacol 160 2010 627 642
7. S.M. Gardiner, J.E. March, P.A. Kemp, and T. Bennett Involvement of CB1-receptors and beta-adrenoceptors in the regional hemodynamic responses to lipopolysaccharide infusion in conscious rats Am J Physiol Heart Circ Physiol 288 2005 H2280 H2288
8. J. Guindon, and A.G. Hohmann The endocannabinoid system and cancer: therapeutic implication Br J Pharmacol 163 2011 1447 1463
9. D.J. Hermanson, and L.J. Marnett Cannabinoids, endocannabinoids, and cancer Cancer Metastasis Rev 30 2011 599 612
10. W.J. Wu, Q. Yang, Q.F. Cao, Y.W. Zhang, Y.J. Xia, and X.W. Hu et al. Membrane cholesterol mediates the endocannabinoids-anandamide affection on HepG2 cells Zhonghua Gan Zang Bing Za Zhi 18 2010 204 208
11. A. Kapur, P. Zhao, H. Sharir, Y. Bai, M.G. Caron, and L.S. Barak et al. Atypical responsiveness of the orphan receptor GPR55 to cannabinoid ligands J Biol Chem 284 2009 29817 29827
12. H. Sharir, and M.E. Abood Pharmacological characterization of GPR55, a putative cannabinoid receptor Pharmacol Ther 126 2010 301 313
13. L.A. Ford, A.J. Roelofs, S. Anavi-Goffer, L. Mowat, D.G. Simpson, and A.J. Irving et al. A role for l-alpha-lysophosphatidylinositol and GPR55 in the modulation of migration, orientation and polarization of human breast cancer cells Br J Pharmacol 160 2010 762 771
14. C. Andradas, M.M. Caffarel, E. Perez-Gomez, M. Salazar, M. Lorente, and G. Velasco et al. The orphan G protein-coupled receptor GPR55 promotes cancer cell proliferation via ERK Oncogene 30 2011 245 252
15. R. Pineiro, T. Maffucci, and M. Falasca The putative cannabinoid receptor GPR55 defines a novel autocrine loop in cancer cell proliferation Oncogene 30 2011 142 152
16. E. Perez-Gomez, C. Andradas, J.M. Flores, M. Quintanilla, J.M. Paramio, and M. Guzman et al. The orphan receptor GPR55 drives skin carcinogenesis and is upregulated in human squamous cell carcinomas Oncogene 32 2013 2534 2542
17. M. Pietr, E. Kozela, R. Levy, N. Rimmerman, Y.H. Lin, and N. Stella et al. Differential changes in GPR55 during microglial cell activation FEBS Lett 583 2009 2071 2076
18. N.A. Balenga, E. Aflaki, J. Kargl, W. Platzer, R. Schroder, and S. Blattermann et al. GPR55 regulates cannabinoid 2 receptor-mediated responses in human neutrophils Cell Res 21 2011 1452 1469
19. C.J. Daly, R.A. Ross, J. Whyte, C.M. Henstridge, A.J. Irving, and J.C. McGrath Fluorescent ligand binding reveals heterogeneous distribution of adrenoceptors and 'cannabinoid-like' receptors in small arteries Br J Pharmacol 159 2010 787 796
20. R. Lan, Q. Liu, P. Fan, S. Lin, S.R. Fernando, and D. McCallion et al. Structure-activity relationships of pyrazole derivatives as cannabinoid receptor antagonists J Med Chem 42 1999 769 776 (Pubitemid 29110792)
21. E. Ryberg, N. Larsson, S. Sjogren, S. Hjorth, N.O. Hermansson, and J. Leonova et al. The orphan receptor GPR55 is a novel cannabinoid receptor Br J Pharmacol 152 2007 1092 1101 (Pubitemid 350166046)
22. M. Rinaldi-Carmona, F. Barth, M. Heaulme, R. Alonso, D. Shire, and C. Congy et al. Biochemical and pharmacological characterisation of SR141716A, the first potent and selective brain cannabinoid receptor antagonist Life Sci 56 1995 1941 1947
23. R.A. Ross, H.C. Brockie, L.A. Stevenson, V.L. Murphy, F. Templeton, and A. Makriyannis et al. Agonist-inverse agonist characterization at CB1 and CB2 cannabinoid receptors of L759633, L759656, and AM630 Br J Pharmacol 126 1999 665 672 (Pubitemid 29087845)
24. C.C. Felder, K.E. Joyce, E.M. Briley, J. Mansouri, K. Mackie, and O. Blond et al. Comparison of the pharmacology and signal transduction of the human cannabinoid CB1 and CB2 receptors Mol Pharmacol 48 1995 443 450
25. S. Oka, K. Nakajima, A. Yamashita, S. Kishimoto, and T. Sugiura Identification of GPR55 as a lysophosphatidylinositol receptor Biochem Biophys Res Commun 362 2007 928 934 (Pubitemid 47390663)
26. V.M. Showalter, D.R. Compton, B.R. Martin, and M.E. Abood Evaluation of binding in a transfected cell line expressing a peripheral cannabinoid receptor (CB2): identification of cannabinoid receptor subtype selective ligands J Pharmacol Exp Ther 278 1996 989 999 (Pubitemid 27166944)
27. C.M. Henstridge, N.A. Balenga, R. Schroder, J.K. Kargl, W. Platzer, and L. Martini et al. GPR55 ligands promote receptor coupling to multiple signalling pathways Br J Pharmacol 160 2010 604 614
28. J.L. Fiori, T.N. Zhu, M.P. O'Connell, K.S. Hoek, F.E. Indig, and B.P. Frank et al. Filamin A modulates kinase activation and intracellular trafficking of epidermal growth factor receptors in human melanoma cells Endocrinology 150 2009 2551 2560
29. O. Hegener, L. Prenner, F. Runkel, S.L. Baader, J. Kappler, and H. Haberlein Dynamics of beta2-adrenergic receptor-ligand complexes on living cells Biochemistry 43 2004 6190 6199 (Pubitemid 38669487)
30. J.L. Fiori, M. Sanghvi, M.P. O'Connell, S.M. Krzysik-Walker, R. Moaddel, and M. Bernier The cannabinoid receptor inverse agonist AM251 regulates the expression of the EGF receptor and its ligands via destabilization of oestrogen-related receptor alpha protein Br J Pharmacol 164 2011 1026 1040
31. P. Wu, P. Wee, J. Jiang, X. Chen, and Z. Wang Differential regulation of transcription factors by location-specific EGF receptor signaling via a spatio-temporal interplay of ERK activation PLoS One 7 2012 e41354
32. D.S. Lidke, K.A. Lidke, B. Rieger, T.M. Jovin, and D.J. Arndt-Jovin Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors J Cell Biol 170 2005 619 626 (Pubitemid 41186936)
33. X. Zhang, Y. Maor, J.F. Wang, G. Kunos, and J.E. Groopman Endocannabinoid-like N-arachidonoyl serine is a novel pro-angiogenic mediator Br J Pharmacol 160 2010 1583 1594
34. R. Pineiro, and M. Falasca Lysophosphatidylinositol signalling: new wine from an old bottle Biochim Biophys Acta 1821 2012 694 705
35. 2+ signaling in endothelial cells via GPR55 by protection against CB1-receptor-triggered repression J Cell Sci 121 2008 1704 1717 (Pubitemid 351911827)
36. P. Carriba, G. Navarro, F. Ciruela, S. Ferre, V. Casado, and L. Agnati et al. Detection of heteromerization of more than two proteins by sequential BRET-FRET Nat Methods 5 2008 727 733
37. M. Hojo, Y. Sudo, Y. Ando, K. Minami, M. Takada, and T. Matsubara et al. mu-Opioid receptor forms a functional heterodimer with cannabinoid CB1 receptor: electrophysiological and FRET assay analysis J Pharmacol Sci 108 2008 308 319
38. L. Callen, E. Moreno, P. Barroso-Chinea, D. Moreno-Delgado, A. Cortes, and J. Mallol et al. Cannabinoid receptors CB1 and CB2 form functional heteromers in brain J Biol Chem 287 2012 20851 20865
39. J. Kargl, N. Balenga, G.P. Parzmair, A.J. Brown, A. Heinemann, and M. Waldhoer The cannabinoid receptor CB1 modulates the signaling properties of the lysophosphatidylinositol receptor GPR55 J Biol Chem 287 2012 44234 44248
40. 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 (Pubitemid 34182973)
41. P.G. Charest, S. Terrillon, and M. Bouvier Monitoring agonist-promoted conformational changes of beta-arrestin in living cells by intramolecular BRET EMBO Rep 6 2005 334 340 (Pubitemid 40561625)
42. H. Yin, A. Chu, W. Li, B. Wang, F. Shelton, and F. Otero et al. Lipid G protein-coupled receptor ligand identification using beta-arrestin PathHunter assay J Biol Chem 284 2009 12328 12338
43. L.M. Luttrell, S.S. Ferguson, Y. Daaka, W.E. Miller, S. Maudsley, and G.J. Della Rocca et al. Beta-arrestin-dependent formation of beta2 adrenergic receptor-Src protein kinase complexes Science 283 1999 655 661
44. Z.J. Cheng, J. Zhao, Y. Sun, W. Hu, Y.L. Wu, and B. Cen et al. beta-arrestin differentially regulates the chemokine receptor CXCR4-mediated signaling and receptor internalization, and this implicates multiple interaction sites between beta-arrestin and CXCR4 J Biol Chem 275 2000 2479 2485 (Pubitemid 30082009)
45. T. Nevalainen, and A.J. Irving GPR55, a lysophosphatidylinositol receptor with cannabinoid sensitivity? Curr Top Med Chem 10 2010 799 813
46. S. Anavi-Goffer, G. Baillie, A.J. Irving, J. Gertsch, I.R. Greig, and R.G. Pertwee et al. Modulation of l-alpha-lysophosphatidylinositol/GPR55 mitogen-activated protein kinase (MAPK) signaling by cannabinoids J Biol Chem 287 2012 91 104
47. M.R. Price, G.L. Baillie, A. Thomas, L.A. Stevenson, M. Easson, and R. Goodwin et al. Allosteric modulation of the cannabinoid CB1 receptor Mol Pharmacol 68 2005 1484 1495 (Pubitemid 41540004)
48. M.C. Mendoza, E.E. Er, W. Zhang, B.A. Ballif, H.L. Elliott, and G. Danuser et al. ERK-MAPK drives lamellipodia protrusion by activating the WAVE2 regulatory complex Mol Cell 41 2011 661 671
49. J. Min Defea K. β-arrestin-dependent actin reorganization: bringing the right players together at the leading edge Mol Pharmacol 80 2011 760 768
50. M.E. Castro, P.J. Harrison, A. Pazos, and T. Sharp Affinity of (+/-)-pindolol, (-)-penbutolol, and (-)-tertatolol for pre- and postsynaptic serotonin 5-HT(1A) receptors in human and rat brain J Neurochem 75 2000 755 762 (Pubitemid 30485458)
51. M. Hachisu, and T. Koeda Study on the pharmacological actions of beta-adrenoceptor blockers with reference to their physico-chemical properties J Pharmacobiodyn 3 1980 183 190 (Pubitemid 10000413)
52. W.P. Koella CNS-related (side-)effects of beta-blockers with special reference to mechanisms of action Eur J Clin Pharmacol 28 Suppl 1985 55 63 (Pubitemid 16218643)
53. S. Imai Pharmacologic characterization of beta blockers with special reference to the significance of nonspecific membrane effects Am J Cardiol 67 1991 8B 12B
54. J.W. Wisler, S.M. DeWire, E.J. Whalen, J.D. Violin, M.T. Drake, and S. Ahn et al. A unique mechanism of beta-blocker action: carvedilol stimulates beta-arrestin signaling PNAS 104 2007 16657 16662 (Pubitemid 350211072)
55. I.M. Kim, D.G. Tilley, J. Chen, N.C. Salazar, E.J. Whalen, and J.D. Violin et al. Beta-blockers alprenolol and carvedilol stimulate beta-arrestin-mediated EGFR transactivation PNAS 105 2008 14555 14560
56. C. Valant, J. Robert Lane, P.M. Sexton, and A. Christopoulos The best of both worlds? Bitopic orthosteric/allosteric ligands of g protein-coupled receptors Annu Rev Pharmacol Toxicol 52 2012 153 178
57. P. Karellas, M. McNaughton, S.P. Baker, and P.J. Scammells Synthesis of bivalent beta2-adrenergic and adenosine A1 receptor ligands J Med Chem 51 2008 6128 6137
58. P.K. Wrzal, E. Goupil, S.A. Laporte, T.E. Hebert, and H.H. Zingg Functional interactions between the oxytocin receptor and the beta2-adrenergic receptor: implications for ERK1/2 activation in human myometrial cells Cell Signal 24 2012 333 341