Nuclear localization of Formyl-Peptide Receptor 2 in human cancer cells

Archives of Biochemistry and Biophysics

Volumn 603, Issue , 2016, Pages 10-19

  Cattaneo, Fabio ^a   Parisi, Melania ^a   Fioretti, Tiziana ^a   Sarnataro, Daniela ^a,b   Esposito, Gabriella ^a,b   Ammendola, Rosario ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

Author keywords

FPR2; G protein coupled receptors; Nuclear localization; Signal transduction

Indexed keywords

AMINO ACID; FORMYL PEPTIDE RECEPTOR 2; FORMYLPEPTIDE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MYC PROTEIN; PROTEIN C JUN; UNCLASSIFIED DRUG; FPR2 PROTEIN, HUMAN; G PROTEIN COUPLED RECEPTOR; LIPOXIN RECEPTOR; MAPK1 PROTEIN, HUMAN; PROTEIN BINDING; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; BINDING ASSAY; CELL ISOLATION; CONTROLLED STUDY; GASTRIC CANCER CELL LINE; GENE OVEREXPRESSION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LUNG CANCER CELL LINE; LUNG CARCINOMA; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RADIOLIGAND BINDING ASSAY; SITE DIRECTED MUTAGENESIS; STOMACH ADENOCARCINOMA; WESTERN BLOTTING; CELL NUCLEUS; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; METABOLISM; MUTAGENESIS; NEOPLASM; NUCLEOCYTOPLASMIC TRANSPORT; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL LINE, TUMOR; CELL NUCLEUS; HEK293 CELLS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICROSCOPY, FLUORESCENCE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MUTAGENESIS; NEOPLASMS; PHOSPHORYLATION; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-MYC; RECEPTORS, FORMYL PEPTIDE; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, LIPOXIN; SIGNAL TRANSDUCTION;

EID: 84968830349     PISSN: 00039861     EISSN: 10960384     Source Type: Journal    
DOI: 10.1016/j.abb.2016.05.006     Document Type: Article

References (63)

1. K.L. Pierce, R.T. Premont, and R.J. Lefkowitz Seven-transmembrane receptors Nat. Rev. Mol. Cell. Biol. 3 2002 639 650
2. T.B. Patel Single transmembrane spanning heterotrimeric g protein-coupled receptors and their signaling cascades Pharmacol. Rev. 56 2004 371 385
3. B. Boivin, C. Lavoie, G. Vaniotis, A. Baragli, L. Villeneuve, N. Ethier, P. Trieu, B.G. Allen, and T.E. Hébert Functional β-adrenergic receptor signalling on nuclear membranes in adult rat and mouse ventricular cardiomyocytes Cardiovasc. Res. 71 2006 69 78
4. B. Boivin, L. Villeneuve, N. Farhat, and D. Chevalier Sub-cellular distribution of endothelin signaling pathway components in ventricular myocytes and heart: lack of preformed caveolar signalosomes J. Mol. Cell. Cardiol. 38 2005 665 676
5. F. Gobeil Jr., S.G. Bernier, A. Vazquez-Tello, S. Brault, M.H. Beauchamp, C. Quiniou, A.M. Marrache, D. Checchin, F. Sennlaub, X. Hou, M. Nader, G. Bkaily, A. Ribeiro-da-Silva, E.J. Goetzl, and S. Chemtob Modulation of pro-inflammatory gene expression by nuclear lysophosphatidic acid receptor type-1 J. Biol. Chem. 278 2003 38875 38883
6. F. Gobeil Jr., I. Dumont, A.M. Marrache, A. Vazquez-Tello, S.G. Bernier, D. Abran, X. Hou, M.H. Beauchamp, C. Quiniou, A. Bouayad, S. Choufani, M. Bhattacharya, S. Molotchnikoff, A. Ribeiro-Da-Silva, D.R. Varma, G. Bkaily, and S. Chemtob Regulation of eNOS expression in brain endothelial cells by perinuclear EP(3) receptors Circ. Res. 90 2002 682 689
7. D. Lu, H. Yang, G. Shaw, and M. Raizada Raizada Angiotensin II-induced nuclear targeting of the angiotensin type 1 (AT1) receptor in brain neurons Endocrinology 139 1998 365 375
8. A.M. Marrache, F. Gobeil Jr., S.G. Bernier, J. Stankova, M. Rola-Pleszczynski, S. Choufani, G. Bkaily, A. Bourdeau, M.G. Sirois, A. Vazquez-Tello, L. Fan, J.S. Joyal, J.G. Filep, D.R. Varma, A. Ribeiro-Da-Silva, and S. Chemtob Proinflammatory gene induction by platelet-activating factor mediated via its cognate nuclear receptor J. Immunol. 169 2002 6474 6481
9. K. O'Malley, Y. Jong, Y. Gonchar, A. Burkhalter, and C. Romano Activation of metabotropic glutamate receptor mGlu5 on nuclear membranes mediates intranuclear Ca2+ changes in heterologous cell types and neurons J. Biol. Chem. 278 2003 28210 28219
10. A.S. Don-Salu-Hewage, S.Y. Chan, K.M. McAndrews, M.A. Chetram, M.R. Dawson, D.A. Bethea, and C.V. Hinton Cysteine (C)-x-C receptor 4 undergoes transportin 1-dependent nuclear localization and remains functional at the nucleus of metastatic prostate cancer cells PLoS One 8 2 2013 e57194
11. A. Tadevosyan, G. Vaniotis, B.G. Allen, T.E. Hébert, and S. Nattel G protein-coupled receptor signalling in the cardiac nuclear membrane: evidence and possible roles in physiological and pathophysiological function J. Physiol. 590 2012 1313 1330
12. G. Vaniotis, B.G. Allen, and T.E. Hébert Nuclear GPCRs in cardiomyocytes: an insider's view of β-adrenergic receptor signaling Am. J. Physiol. Heart Circ. Physiol. 301 2011 H1754 H1764
13. E.J. Goetzl Diverse pathways for nuclear signaling by G protein-coupled receptors and their ligands FASEB J. 21 2007 638 642
14. F. Gobeil, A. Fortier, T. Zhu, M. Bossolasco, M. Leduc, M. Grandbois, N. Heveker, G. Bkaily, S. Chemtob, and D. Barbaz G-protein-coupled receptors signalling at the cell nucleus: an emerging paradigm Can. J. Physiol. Pharmacol. 84 2006 287 297
15. C. Nielsen, J. Campbell, J. Ohd, M. Morgelin, K. Riesbeck, G. Landberg, and A. Sjölander A novel localization of the G-protein-coupled CysLT1 receptor in the nucleus of colorectal adenocarcinoma cells Cancer Res. 65 2005 732 742
16. M. Takano, and S. Matsuyama Intracellular and nuclear bradykinin B2 receptors Eur. J. Pharmacol. 732 2014 169 172
17. F. Gobeil Jr., T. Zhu, S. Brault, A. Geha, A. Vazquez-Tello, A. Fortier, D. Barbaz, D. Checchin, X. Hou, M. Nader, G. Bkaily, J.P. Gratton, N. Heveker, A. Ribeiro-da-Silva, K. Peri, H. Bard, A. Chorvatova, P. D'Orléans-Juste, E.J. Goetzl, and S. Chemtob Nitric oxide signaling via nuclearized endothelial nitric-oxide synthase modulates expression of the immediate early genes iNOS and mPGES-1 J. Biol. Chem. 281 2006 16058 16067
18. F.S. Willard, and M.F. Crouch Nuclear and cytoskeletal translocation and localization of heterotrimeric G-proteins Immunol. Cell. Biol. 78 2000 387 394
19. F. Gobeil Jr., A. Vazquez-Tello, A.M. Marrache, M. Bhattacharya, D. Checchin, G. Bkaily, P. Lachapelle, A. Ribeiro-Da-Silva, and S. Chemtob Nuclear prostaglandin signaling system: biogenesis and actions via heptahelical receptors Can. J. Physiol. Pharmacol. 81 2003 196 204
20. A.M. Marrache, F. Gobeil, T. Zhu, and S. Chemtob Intracellular signaling of lipid mediators via cognate nuclear G protein-coupled receptors Endothelium 12 2005 63 72
21. G. Bkaily, L. Avedanian, J. Al-Khoury, C. Provost, M. Nader, P. D'Orléans-Juste, and D. Jacques Nuclear membrane receptors for ET-1 in cardiovascular function Am. J. Physiol. Regul. Integr. Comp. Physiol. 300 2011 R251 R263
22. G. Vaniotis, D. Del Duca, P. Trieu, C.V. Rohlicek, T.E. Hébert, and B.G. Allen Nuclear β-adrenergic receptors modulate gene expression in adult rat heart Cell Signal 23 2011 89 98
23. H. Kobayashi, Y. Narita, M. Nishida, and H. Kurose Beta-arrestin2 enhances beta2-adrenergic receptor-mediated nuclear translocation of ERK Cell. Signal 17 2005 1248 1253
24. B. Boivin, G. Vaniotis, B.G. Allen, and T.E. Hébert G protein-coupled receptors in and on the cell nucleus: a new signaling paradigm? J. Recept. Signal. Transduct. Res. 28 2008 15 28
25. B. Miguel, M. Calcerrada, L. Martin, R. Catalan, and A. Martinez Increase of phosphoinositide hydrolysis and diacylglycerol production by PAF in isolated rat liver nuclei Prostagl. Other Lipid Mediat 65 2001 159 166
26. D. Pétrin, and T.E. Hébert Imaging-based approaches to understanding g protein-coupled receptor signalling complexes Methods Mol. Biol. 756 2011 37 60
27. D.J. Dupré, M. Robitaille, R.V. Rebois, and T.E. Hébert The role of Gbetagamma subunits in the organization, assembly, and function of GPCR signaling complexes Annu. Rev. Pharmacol. Toxicol. 49 2009 31 56
28. B.D. Spiegelberg, and H.E. Hamm G betagamma binds histone deacetylase 5 (HDAC5) and inhibits its transcriptional co-repression activity J. Biol. Chem. 280 2005 41769 41776
29. J.G. Park, A. Muise, G.P. He, S.W. Kim, and H.S. Ro Transcriptional regulation by the gamma5 subunit of a heterotrimeric G protein during adipogenesis EMBO J. 18 1999 4004 4012
30. C.D. Wright, S.C. Wu, E.F. Dahl, A.J. Sazama, and T.D. O'Connell Nuclear localization drives α1-adrenergic receptor oligomerization and signaling in cardiac myocytes Cell. Signal 24 2012 794 802
31. D.K. Lee, A.J. Lança, R. Cheng, T. Nguyen, X.D. Ji, F. Gobeil Jr., S. Chemtob, S.R. George, and B.F O'Dowd Agonist-independent nuclear localization of the Apelin, angiotensin AT1, and bradykinin B2 receptors J. Biol. Chem. 279 2004 7901 7908
32. D. Christophe, C. Christophe-Hobertus, and B. Pichon Nuclear targeting of proteins: how many different signals? Cell. Signal 12 2000 337 341
33. F. Cattaneo, M. Parisi, and R. Ammendola Distinct signaling cascades elicited by different formyl peptide receptor 2 (FPR2) agonists Int. J. Mol. Sci. 14 2013 7193 7230
34. A. Iaccio, F. Cattaneo, M. Mauro, and R. Ammendola FPRL1-mediated induction of superoxide in LL-37-stimulated IMR90 human fibroblast Arch. Biochem. Biophys. 481 2009 94 100
35. F. Cattaneo, G. Guerra, and R. Ammendola Expression and signaling of formyl-peptide receptors in the brain Neurochem. Res. 35 2010 2018 2026
36. S.H. Baek, J.K. Seo, C.-B. Chae, P.G. Suh, and S.H. Ryu Identification of the peptides that stimulate the phosphoinositide hydrolysis and induction of superoxide generation in human neutrophils J. Biol. Chem. 271 1996 8170 8175
37. A. Iaccio, A. Angiolillo, and R. Ammendola Intracellular signaling triggered by formyl-peptide receptors in nonphagocytic cells Curr. Signal. Transduct. Ther. 3 2008 88 96
38. R. Ammendola, L. Russo, C. De Felice, F. Esposito, T. Russo, and F. Cimino Low affinity receptor-mediated induction of superoxide by N-formyl-methionyl-leucyl-phenylalanine and WKYMVm in IMR90 human fibroblasts Free Radic. Biol. Med. 36 2004 189 200
39. A. Iaccio, C. Collinet, N. Montesano Gesualdi, and R. Ammendola Protein kinase C-α and -δ are required for NADPH oxidase activation in WKYMVm-stimulated IMR90 human fibroblasts Arch. Biochem. Biophys. 459 2007 288 294
40. F. Cattaneo, A. Iaccio, G. Guerra, S. Montagnani, and R. Ammendola NADPH-oxidase-dependent reactive oxygen species mediate EGFR transactivation by FPRL1 in WKYMVm-stimulated human lung cancer cells Free Radic. Biol. Med. 51 2011 1126 1136
41. F. Cattaneo, M. Parisi, and R. Ammendola WKYMVm-induced cross-talk between FPR2 and HGF receptor in human prostate epithelial cell line PNT1A FEBS Lett. 587 2013 1536 1542
42. F. Cattaneo, G. Guerra, M. Parisi, M. De Marinis, D. Tafuri, M. Cinelli, and R. Ammendola Cell-surface receptors transactivation mediated by G protein-coupled receptors Int. J. Mol. Sci. 15 2014 19700 19728
43. F. Cattaneo, G. Guerra, M. Parisi, A. Lucariello, A. De Luca, N. De Rosa, G. Mazzarella, A. Bianco, and R. Ammendola Expression of formyl-peptide receptors in human lung carcinoma Anticancer Res. 35 2015 2769 2774
44. R. Ammendola, M.R. Ruocchio, G. Chirico, L. Russo, C. De Felice, F. Esposito, T. Russo, and F. Cimino Inhibition of NADH/NADPH oxidase affects signal transduction by growth factor receptors in normal fibroblasts Arch. Biochem. Biophys. 397 2002 253 257
45. B. Boivin, D. Chevalier, L.R. Villeneuve, E. Rousseau, and B.G. Allen Functional endothelin receptors are present on nuclei in cardiac ventricular myocytes J. Biol. Chem. 278 2003 29153 29163
46. Y.J. Jong, V. Kumar, A.E. Kingston, C. Romano, and K.L. O'Malley Functional metabotropic glutamate receptors on nuclei from brain and primary cultured striatal neurons. Role of transporters in delivering ligand J. Biol. Chem. 280 2005 30469 30480
47. W.C. De Mello Intracellular and extracellular renin have opposite effects on the regulation of heart cell volume. Implications for myocardial ischaemia J. Renin Angiotensin Aldosterone Syst. 9 2008 112 118
48. N. Prevete, F. Liotti, C. Visciano, G. Marone, R.M. Melillo, and A. de Paulis The formyl peptide receptor 1 exerts a tumor suppressor function in human gastric cancer by inhibiting angiogenesis Oncogene 34 2015 3826 3838
49. T. Senbonmatsu, T. Saito, E.J. Landon, O. Watanabe, E. Price Jr., R.L. Roberts, H. Imboden, T.G. Fitzgerald, F.A. Gaffney, and T. Inagami A novel angiotensin II type 2 receptor signaling pathway: possible role in cardiac hypertrophy EMBO J. 22 2003 646471 646482
50. M. Toy-Miou-Leong, C.M. Bachelet, D. Pélaprat, W. Rostène, and P. Forgez NT agonist regulates expression of nuclear high-affinity neurotensin receptors J. Histochem. Cytochem 52 2004 335 345
51. T.T. Nguyen, M. Létourneau, D. Chatenet, and A. Fournier Presence of urotensin-II receptors at the cell nucleus: specific tissue distribution and hypoxia-induced modulation Int. J. Biochem. Cell. Biol. 44 2012 639 647
52. G. Giebing, M. Tölle, J. Jürgensen, J. Eichhorst, J. Furkert, M. Beyermann, F. Neuschäfer-Rube, W. Rosenthal, W. Zidek, M. van der Giet, and A. Oksche Arrestin-independent internalization and recycling of the urotensin receptor contribute to long-lasting urotensin II-mediated vasoconstriction Circ. Res. 97 2005 707 715
53. S. Kosugi, M. Hasebe, M. Tomita, and H. Yanagawa Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs Proc. Natl. Acad. Sci. U. S. A. 106 2009 10171 10176
54. D. Chatenet, T.T. Nguyen, M. Létourneau, and A. Fournier Update on the urotensinergic system: new trends in receptor localization, activation, and drug design Front. Endocrinol. 3 2013 174 10.3389/fendo.2012.00174
55. R.H. Chen, C. Sarnecki, and J. Blenis Nuclear localization and regulation of erk- and rsk-encoded protein kinases Mol. Cell. Biol. 12 1992 915 927
56. C.J. Caunt, and C.A. McArdle Stimulus-induced uncoupling of extracellular signal-regulated kinase phosphorylation from nuclear localization is dependent on docking domain interactions J. Cell. Sci. 123 2010 4310 4320
57. D. Dworakowska, E. Wlodek, C.A. Leontiou, S. Igreja, M. Cakir, M. Teng, N. Prodromou, M.I. Góth, S. Grozinsky-Glasberg, M. Gueorguiev, B. Kola, M. Korbonits, and A.B. Grossman Activation of RAF/MEK/ERK and PI3K/AKT/mTOR pathways in pituitary adenomas and their effects on downstream effectors Endocr. Relat. Cancer 16 2009 1329 1338
58. A.Y. Kam, T.T. Tse, D.H. Kwan, and Y.H. Wong Formyl peptide receptor like 1 differentially requires mitogen-activated protein kinases for the induction of glial fibrillary acidic protein and interleukin-1alpha in human U87 astrocytoma cells Cell. Signal 19 2007 2106 2117
59. I. Schreck, M. Al-Rawi, J.M. Mingot, C. Scholl, M.E. Diefenbacher, P. O'Donnell, D. Bohmann, and C. Weiss c-Jun localizes to the nucleus independent of its phosphorylation by and interaction with JNK and vice versa promotes nuclear accumulation of JNK Biochem. Biophys. Res. Commun. 407 2011 735 740
60. K.P. Smith, M. Byron, B.C. O'Connell, R. Tam, C. Schorl, I. Guney, L.L. Hall, P. Agrawal, J.M. Sedivy, and J.B. Lawrence c-Myc localization within the nucleus: evidence for association with the PML nuclear body J. Cell. Biochem. 93 2004 1282 1296
61. F. Chang, L.S. Steelman, J.T. Lee, J.G. Shelton, P.M. Navolanic, W.L. Blalock, R.A. Franklin, and J.A. McCubrey Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcription factors: potential targeting for therapeutic intervention Leukemia 17 2003 1263 1293
62. M. Bhattacharya, K.G. Peri, G. Almazan, A. Ribeiro-da-Silva, H. Shichi, Y. Durocher, M. Abramovitz, X. Hou, D.R. Varma, and S. Chemtob Nuclear localization of prostaglandin E2 receptors Proc. Natl. Acad. Sci. USA 95 1998 15792 15797
63. A.G. Spencer, J.W. Woods, T. Arakawa, I.I. Singer, and W.L. Smith Subcellular localization of prostaglandin endoperoxide H synthases-1 and -2 by immunoelectron microscopy J. Biol. Chem. 273 1998 9886 9893