Altered protease-activated receptor-1 expression and signaling in a malignant pleural mesothelioma cell line, NCI-H28, with homozygous deletion of the β-catenin gene

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Fazzini, Alessandra ^a   D'antongiovanni, Vanessa ^a   Giusti, Laura ^a   Da Valle, Ylenia ^a   Ciregia, Federica ^a   Piano, Ilaria ^a   Caputo, Antonella ^a   D'Ursi, Anna Maria ^b   Gargini, Claudia ^a   Lucacchini, Antonio ^a   Mazzoni, Maria Rosa ^a  

^a UNIVERSITY OF PISA   (Italy)

^b UNIVERSITY OF SALERNO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEINASE ACTIVATED RECEPTOR 1; THROMBIN;

ADULT; ARTICLE; CANCER GROWTH; CELL MEMBRANE; CELL PROLIFERATION; CELL SURFACE; CONTROLLED STUDY; CTNNB1 GENE; ENZYME ACTIVATION; GENE DELETION; HOMOZYGOSITY; HUMAN; HUMAN CELL; MESOTHELIOMA CELL LINE; PLEURA MESOTHELIOMA; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; AGONISTS; DRUG EFFECTS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; HOMOZYGOTE; INTRACELLULAR SPACE; LUNG TUMOR; MESOTHELIOMA; METABOLISM; PLEURA TUMOR; PROTEIN TRANSPORT; TUMOR CELL LINE;

BETA CATENIN; CELL LINE, TUMOR; CELL MEMBRANE; CELL PROLIFERATION; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMOZYGOTE; HUMANS; INTRACELLULAR SPACE; LUNG NEOPLASMS; MESOTHELIOMA; PLEURAL NEOPLASMS; PROTEIN TRANSPORT; RECEPTOR, PAR-1; SIGNAL TRANSDUCTION;

EID: 84909619249     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0111550     Document Type: Article

References (55)

1. Sekido Y (2013) Molecular pathogenesis of malignant mesothelioma. Carcinogenesis 34:1413-1418.
2. Li T, Li H, Wang Y, Harvard C, Tan JL, et al. (2011) The expression of CXCR4, CXCL12 and CXCR7 in malignant pleural mesothelioma. J Pathol 223:519-530.
3. Dorsam RT, Gutkind JS (2007) G-protein-coupled receptors and cancers. Nat Rev Cancer 7:79-94.
4. Lappano R, Maggiolini M (2011) G protein-coupled receptors: novel targets for drug discovery in cancer. Nat Rev Drug Discov 10:47-60.
5. Macfarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R (2001) Proteinaseactivated receptors. Pharmacol Rev 53:245-282.
6. Vu TK, Hung DT, Wheaton VI, Coughlin SR (1991) Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64:1057-1068.
7. 2+ mobilization. FEBS Lett 288:123-128.
8. Nystedt S, Emilsson K, Larsson AK, Strömbeck B, Sundelin J (1995) Molecular cloning and functional expression of the gene encoding the human proteinaseactivated receptor 2. Eu. J Biochem 232:84-89.
9. Ishihara H, Connolly AJ, Zeng D, Kahn ML, Zheng YW, et al. (1997) Proteaseactivated receptor 3 is a second thrombin receptor in humans. Nature 386:502-506.
10. Xu WF, Andersen H, Whitmore TE, Presnell SR, Yee DP, et al. (1998) Cloning and characterization of human protease-activated receptor 4. Proc Natl Acad Sci U. S. A. 95:6642-6646.
11. Soh UJ, Dores MR, Chen B, Trejo J (2010) Signal transduction by proteaseactivated receptors. Br J Pharmacol 160:191-203.
12. Coughlin SR (2005) Protease-activated receptors in hemostasis, thrombosis and vascular biology. J Thromb Haemost 3:1800-1814.
13. Ramachandran R, Noorbakhsh F, Defea K, Hollenberg MD (2012) Targeting proteinase-activated receptors: therapeutic potential and challenges. Nat Rev Drug Discov 11:69-86.
14. Tellez C, Bar-Eli M (2003) Role and regulation of the thrombin receptor (PAR-1) in human melanoma. Oncogene 22:3130-3137.
15. Darmoul D, Gratio V, Devaud H, Lehy T, Laburthe M (2003) Aberrant expression and activation of the thrombin receptor protease-activated receptor-1 induces cell proliferation and motility in human colon cancer cells. Am J Pathol 162:1503-1513.
16. Chay CH, Cooper CR, Gendernalik JD, Dhanasekaran SM, Chinnaiyan AM, et al. (2002) A functional thrombin receptor (PAR1) is expressed on bone-derived prostate cancer cell lines. Urology 60:760-765.
17. Even-Ram S, Uziely B, Cohen P, Grisaru-Granovsky S, Moaz M, et al. (1998) Thrombin receptor overexpression in malignant and physiological invasion processes. Nat Med 4:909-914.
18. Even-Ram SC, Maoz M, Pokroy E, Reich R, Katz BZ, et al. (2001) Tumor cell invasion is promoted by activation of protease activated receptor-1 in cooperation with the avb5 integrin. J Biol Chem 276:10952-10962.
19. Bar-Shavit R, Turm H, Salah Z, Maoz M, Cohen I, et al. (2011) PAR1 plays a role in epithelial malignancies: transcriptional regulation and novel signaling pathway. IUBMB Life 63:397-402.
20. Booden MA, Eckert LB, der CJ, Trejo J (2004) Persistent signaling by dysregulated thrombin receptor trafficking promotes breast carcinoma cell invasion. Mol Cell Biol 24:1990-1999.
21. Arora P, Ricks TK, Trejo J (2007) Protease-activated receptor signalling, endocytic sorting and dysregulation in cancer. J Cell Sci 120:921-928.
22. Keshava S, Sahoo S, Tucker TA, Idell S, Rao LV, et al. (2013) Endothelial cell protein C receptor opposes mesothelioma growth driven by tissue factor. Cancer Res 73:3963-3973.
23. Shigemitsu K, Sekido Y, Usami N, Mori S, Sato M, et al. (2001) Genetic alteration of the b-catenin gene (CTNNB1) in human lung cancer and malignant mesothelioma and identification of a new 3p21.3 homozygous deletion. Oncogene 20:4249-4257.
24. Nocchi L, Tomasetti M, Amati M, Neuzil J, Santarelli L, et al. (2011) Thrombomodulin is silenced in malignant mesothelioma by a poly (ADP-ribose) polymerase-1-mediated epigenetic mechanism. J Biol Chem 286:19478-19488.
25. Ades EW, Candal FJ, Swerlick RA, George VG, Summers S, et al. (1992) HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 99:683-690.
26. Smythe WR, Kaiser LR, Hwang HC, Amin KM, Pilewski JM, et al. (1994) Successful adenovirus-mediated gene transfer in an in vivo model of human malignant mesothelioma. Ann Thorac Surg 57:1395-1401.
27. Pinton G, Thomas W, Bellini P, Manente AG, Favoni RE, et al. (2010) Estrogen receptor b exerts tumor repressive functions in human malignant pleural mesothelioma via EGFR inactivation and affects response to gefitinib. PLOS ONE 5:e14110.
28. Versnel MA, Hoogsteden HC, Hagemeijer A, Bouts MJ, Van Der Kwast TH, et al. (1989) Characterization of three human malignant mesothelioma cell lines. Cancer Genet Cytogenet 42:115-128.
29. Orengo AM, Spoletini L, Procopio A, Favoni RE, De Cupis A, et al. (1999) Establishment of four new mesothelioma cell lines: characterization by ultrastructural and immunophenotypic analysis. Eur Respir J 13:527-534.
30. D'Ursi AM, Giusti L, Albrizio S, Porchia F, Esposito C, et al. (2006) A membrane-permeable peptide containing the last 21 residues of the Gas carboxyl terminus inhibits Gs-coupled receptor signaling in intact cells: correlations between peptide structure and biological activity. Mol Pharmacol 69:727-736.
31. Paing MM, Johnston CA, Siderovski DP, Trejo J (2006) Clathrin adaptor AP2 regulates thrombin receptor constitutive internalization and endothelial cell resensitization. Mol Cell Biol 26:3231-3242.
32. Asteriti S, Daniele S, Porchia F, Dell'Anno MT, Fazzini A, et al. (2012) Modulation of PAR1 signalling by benzimidazole compounds. Br J Pharmacol 167:80-94.
33. Porchia F, Papucci M, Gargini C, Asta A, De Marco G, et al. (2008) Endothelin-1 up-regulates p115RhoGEF in embryonic rat cardiomyocytes during the hypertrophic response. J Recept Signal Transduct Res 28:265-283.
34. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Intern 11:36-42.
35. Paing MM, Stutts AB, Kohout TA, Lefkowitz RJ, Trejo J (2002) b-Arrestins regulate protease-activated receptor-1 desensitization but not internalization or down-regulation. J Biol Chem 277:1292-12300.
36. Lee YC, Knight DA, Lane KB, Cheng DS, Koay MA, et al. (2005) Activation of proteinase-activated receptor-2 in mesothelial cells induces pleural inflammation. Am J Physiol Lung Cell Mol Physiol 288:L734-740.
37. Belling F, Ribeiro A, Wörnle M, Ladurner R, Mussack T, et al. (2013) PAR-1 mediates the thrombin-induced mesothelial cell overproduction of VEGF and PAI-1. Int J Artif Organs 36:97-104.
38. Matsushita Y, Yoshiie K, Imamura Y, Ogawa H, Imamura H, et al. (1998) A subcloned human esophageal squamous cell carcinoma cell line with low thrombomodulin expression showed increased invasiveness compared with a high thrombomodulin-expressing clone - thrombomodulin as a possible candidate for an adhesion molecule of squamous cell carcinoma. Cancer Lett. 127:195-201.
39. Ogawa H, Yonezawa S, Maruyama I, Matsushita Y, Tezuka Y, et al. (2000) Expression of thrombomodulin in squamous cell carcinoma of the lung: its relationship to lynph node metastasis and prognosis of the patients. Cancer Lett 149:95-103.
40. Liu PL, Tsai JR, Chiu CC, Hwang JJ, Chou SH, et al. (2010) Decreased expression of thrombomodulin is correlated with tumor cell invasiveness and poor prognosis in nonsmall cell lung cancer. Mol Carcinog 49:874-881.
41. Vouret-Craviari V, Grall D, Chambard JC, Rasmussen UB, Pouysségur J, et al. (1995) Post-translational and activation-dependent modifications of the G protein-coupled thrombin receptor. J Biol Chem 270:8367-8372.
42. Kuliopulos A, Covic L, Seeley SK, Sheridan PJ, Helin J, et al. (1999) Plasmin desensitization of the PAR1 thrombin receptor: kinetics, sites of truncation, and implications for thrombolytic therapy. Biochemistry 38:4572-4585.
43. Soto AG, Trejo J (2010) N-linked glycosylation of protease-activated receptor-1 second extracellular loop: a critical determinant for ligand-induced receptor activation and internalization. J Biol Chem, 285:18781-18793.
44. Kronstein R, Seebach J, Grossklaus S, Minten C, Engelhardt B, et al. (2012) Caveolin-1 opens endothelial cell junctions by targeting catenins. Cardiovasc Res 93:130-140.
45. Patel HH, Murray F, Insel PA (2008) Caveolae has organizers of pharmacologically relevant signal transduction molecules. Annu Rev Pharmacol Toxicol 48:359-391.
46. Russo A, Soh UJ, Paing MM, Arora P, Trejo J (2009) Caveolae are required for protease-selective signaling by protease-activated receptor-1. Proc Natl Acad Sci U. S. A. 106:6393-6397.
47. Nierodzik ML, Karpatkin S (2006) Thrombin induces tumor growth, metastasis, and angiogenesis: Evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell 10:355-362.
48. Nguyen D, Lee SJ, Libby E, Verschraegen C (2008) Rate of thromboembolic events in mesothelioma. Ann Thorac Surg 85:1032-1038.
49. Blackhart BD, Ruslim-Litrus L, Lu CC, Alves VL, Teng W, et al. (2000) Extracellular mutations of protease-activated receptor-1 result in differential activation by thrombin and thrombin receptor agonist peptide. Mol Pharmacol 58:1178-1187.
50. McLaughlin JN, Shen L, Holinstat M, Brooks JD, Di Benedetto E, et al. (2005) Functional selectivity of G protein signaling by agonist peptides and thrombin for the protease-activated receptor-1. J Biol Chem 280:25048-25059.
51. O'Brien PJ, Prevost N, Molino M, Hollinger MK, Woolkalis MJ, et al. (2000) Thrombin responses in human endothelial cells. Contributions from receptors other than PAR1 include the transactivation of PAR2 by thrombin-cleaved PAR1. J Biol Chem 275:13502-13509.
52. Cooper D M F (2003) Regulation and organization of adenylyl cyclases and cAMP. Biochem J 375:517-529.
53. Trejo J, Connolly AJ, Coughlin SR (1996) The cloned thrombin receptor is necessary and sufficient for activation of mitogen-activated protein kinase and mitogenesis in mouse lung fibroblast. Loss of responses in fibroblasts from receptor knockout mice. J Biol Chem 271:21536-21541.
54. Calizo RC, Scarlata S (2012) A role for G-proteins in directing G-proteincoupled receptor-caveolae localization. Biochemistry 51:9513-9523.
55. Sato M, Hutchinson DS, Halls ML, Furness SG, Bengtsson T, et al. (2012) Interaction with caveolin-1 modulates G protein coupling of mouse b3-adrenoceptor. J Biol Chem 287:20674-20688.