Expression of proteinase-activated receptor 1-4 (PAR 1-4) in human cancer

Journal of Molecular Histology

Volumn 41, Issue 2-3, 2010, Pages 89-99

  Elste, Andrea Pia ^a   Petersen, Iver ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Cancer; PAR; Thrombin

Indexed keywords

PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4;

ADENOCARCINOMA; BREAST CANCER; CARCINOGENESIS; DIGESTIVE SYSTEM CANCER; ENDOMETRIUM CANCER; GLIOBLASTOMA; HEAD AND NECK CANCER; HUMAN; KIDNEY CANCER; LEUKEMIA; LIVER CANCER; LUNG CANCER; MALIGNANT NEOPLASTIC DISEASE; MEDLINE; MELANOMA; MENINGIOMA; NEOPLASM; OSTEOSARCOMA; OVARY CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; SQUAMOUS CELL CARCINOMA; SYSTEMATIC REVIEW;

CELL LINE, TUMOR; HUMANS; NEOPLASMS; RECEPTOR, PAR-1; RECEPTOR, PAR-2; RECEPTORS, THROMBIN;

EID: 77955925169     PISSN: 15672379     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10735-010-9274-6     Document Type: Review

References (80)

1. A Agarwal L Covic LM Sevigny NC Kaneider K Lazarides G Azabdaftari, et al. 2008 Targeting a metalloprotease-PAR1 signaling system with cell-penetrating pepducins inhibits angiogenesis, ascites, and progression of ovarian cancer Mol Cancer Ther 7 2746 2757 10.1158/1535-7163.MCT-08-0177
2. R Ahmad L Knafo J Xu ST Sindhu J Menezes A Ahmad 2000 Thrombin induces apoptosis in human tumor cells Int J Cancer 87 707 715 10.1002/1097- 0215(20000901)87:5<707::AID-IJC13>3.0.CO;2-W
3. B al-Ani M Saifeddine MD Hollenberg 1995 Detection of functional receptors for the proteinase-activated-receptor-2-activating polypeptide, SLIGRL-NH2, in rat vascular and gastric smooth muscle Can J Physiol Pharmacol 73 1203 1207
4. P Arora BD Cuevas A Russo GL Johnson J Trejo 2008 Persistent transactivation of EGFR and ErbB2/HER2 by protease-activated receptor-1 promotes breast carcinoma cell invasion Oncogene 27 4434 4445 10.1038/onc.2008.84
5. LM Beaulieu FC Church 2007 Activated protein C promotes breast cancer cell migration through interactions with EPCR and PAR-1 Exp Cell Res 313 677 687 10.1016/j.yexcr.2006.11.019
6. PC Black GJ Mize P Karlin DL Greenberg SJ Hawley LD True, et al. 2007 Overexpression of protease-activated receptors-1,-2, and-4 (PAR-1, -2, and -4) in prostate cancer Prostate 67 743 756 10.1002/pros.20503
7. SK Bohm W Kong D Bromme SP Smeekens DC Anderson A Connolly, et al. 1996 Molecular cloning, expression and potential functions of the human proteinase-activated receptor-2 Biochem J 314 Pt 3 1009 1016
8. A Boire L Covic A Agarwal S Jacques S Sherifi A Kuliopulos 2005 PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells Cell 120 303 313 10.1016/j.cell.2004.12.018
9. MA Booden LB Eckert CJ Der J Trejo 2004 Persistent signaling by dysregulated thrombin receptor trafficking promotes breast carcinoma cell invasion Mol Cell Biol 24 1990 1999 10.1128/MCB.24.5.1990-1999.2004
10. CA Borgono IP Michael EP Diamandis 2004 Human tissue kallikreins: physiologic roles and applications in cancer Mol Cancer Res 2 257 280
11. ME Bromberg MA Bailly WH Konigsberg 2001 Role of protease-activated receptor 1 in tumor metastasis promoted by tissue factor Thromb Haemost 86 1210 1214
12. R Caruso F Pallone D Fina V Gioia I Peluso F Caprioli, et al. 2006 Protease-activated receptor-2 activation in gastric cancer cells promotes epidermal growth factor receptor trans-activation and proliferation Am J Pathol 169 268 278 10.2353/ajpath.2006.050841
13. CH Chay CR Cooper JD Gendernalik SM Dhanasekaran AM Chinnaiyan MA Rubin, et al. 2002 A functional thrombin receptor (PAR1) is expressed on bone-derived prostate cancer cell lines Urology 60 760 765 10.1016/S0090-4295(02)01969-6
14. CR Cooper CH Chay JD Gendernalik HL Lee J Bhatia RS Taichmann, et al. 2003 Stromal factors involved in prostate carcinoma metastasis to bone Cancer Cell 97 739 747
15. MR D'Andrea CK Derian RJ Santulli P Andrade-Gordon 2001 Differential expression of protease-activated receptors-1 and -2 in stromal fibroblasts of normal, benign, and malignant human tissues Am J Pathol 158 2031 2041
16. D Darmoul JC Marie H Devaud V Gratio M Laburthe 2001 Initiation of human colon cancer cell proliferation by trypsin acting at protease-activated receptor-2 Br J Cancer 85 772 779 10.1054/bjoc.2001.1976
17. D Darmoul V Gratio H Devaud T Lehy M Laburthe 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
18. I Depasquale WD Thompson 2008 Prognosis in human melanoma: PAR-1 expression is superior to other coagulation components and VEGF Histopathology 52 500 509 10.1111/j.1365-2559.2008.02978.x
19. KL Elzer DA Heitzman MI Chernin JF Novak 2008 Differential effects of serine proteases on the migration of normal and tumor cells: implications for tumor microenvironment Integr Cancer Ther 7 282 294 10.1177/1534735408327250
20. S Even-Ram B Uziely P Cohen S Grisaru-Granovsky M Maoz Y Ginzburg, et al. 1998 Thrombin receptor overexpression in malignant and physiological invasion processes Nat Med 4 909 914 10.1038/nm0898-909
21. SC Even-Ram S Grisaru-Granovsky D Pruss M Maoz Z Salah Y Yong-Jun, et al. 2003 The pattern of expression of protease-activated receptors (PARs) during early trophoblast development J Pathol 200 47 52 10.1002/path.1338
22. A Falanga 2005 Thrombophilia in cancer Semin Thromb Hemost 31 104 110 10.1055/s-2005-863812
23. D Fujimoto Y Hirono T Goi K Katayama K Hirose A Yamaguchi 2006 Expression of protease activated receptor-2 (PAR-2) in gastric cancer J Surg Oncol 93 139 144 10.1002/jso.20420
24. P Ghio S Cappia G Selvaggi S Novello P Lausi G Zecchina, et al. 2006 Prognostic role of protease-activated receptors 1 and 4 in resected stage IB non-small-cell lung cancer Clin Lung Cancer 7 395 400 10.3816/CLC.2006.n.023
25. I Gouin-Thibault MM Samama 1999 Laboratory diagnosis of the thrombophilic state in cancer patients Semin Thromb Hemost 25 167 172 10.1055/s-2007-994918
26. S Granovsky-Grisaru S Zaidoun D Grisaru Y Yekel D Prus U Beller, et al. 2006 The pattern of Protease Activated Receptor 1 (PAR1) expression in endometrial carcinoma Gynecol Oncol 103 802 806 10.1016/j.ygyno.2006.05.048
27. DL Greenberg GJ Mize TK Takayama 2003 Protease-activated receptor mediated RhoA signaling and cytoskeletal reorganization in LNCaP cells Biochemistry 42 702 709 10.1021/bi027100x
28. KK Hansen K Oikonomopoulou Y Li MD Hollenberg 2008 Proteinases, proteinase-activated receptors (PARs) and the pathophysiology of cancer and diseases of the cardiovascular, musculoskeletal, nervous and gastrointestinal systems Naunyn Schmiedebergs Arch Pharmacol 377 377 392 10.1007/s00210-007-0194- 2
29. P Hazarika MF McCarty VG Prieto S George D Babu D Koul, et al. 2004 Up-regulation of Flotillin-2 is associated with melanoma progression and modulates expression of the thrombin receptor protease activated receptor 1 Cancer Res 64 7361 7369 10.1158/0008-5472.CAN-04-0823
30. GM Hjortoe LC Petersen T Albrektsen BB Sorensen PL Norby SK Mandal, et al. 2004 Tissue factor-factor VIIa-specific up-regulation of IL-8 expression in MDA-MB-231 cells is mediated by PAR-2 and results in increased cell migration Blood 103 3029 3037 10.1182/blood-2003-10-3417
31. MD Hollenberg S Houle 2005 Proteinases as hormone-like signal messengers Swiss Med Wkly 135 425 432
32. YQ Huang JJ Li S Karpatkin 2000 Thrombin inhibits tumor cell growth in association with up-regulation of p21(waf/cip1) and caspases via a p53-independent, STAT-1-dependent pathway J Biol Chem 275 6462 6468 10.1074/jbc.275.9.6462
33. O Ikeda H Egami T Ishiko S Ishikawa H Kamohara H Hidaka, et al. 2003 Expression of proteinase-activated receptor-2 in human pancreatic cancer: a possible relation to cancer invasion and induction of fibrosis Int J Oncol 22 295 300
34. O Ikeda H Egami T Ishiko S Ishikawa H Kamohara H Hidaka, et al. 2006 Signal of proteinase-activated receptor-2 contributes to highly malignant potential of human pancreatic cancer by up-regulation of interleukin-8 release Int J Oncol 28 939 946
35. I Jahan J Fujimoto SM Alam E Sato H Sakaguchi T Tamaya 2007 Expression of protease activated receptor-2 related to angiogenesis in tumor advancement of uterine endometrial cancers Oncol Rep 17 345 350
36. X Jiang MA Bailly TS Panetti M Cappello WH Konigsberg ME Bromberg 2004 Formation of tissue factor-factor VIIa-factor Xa complex promotes cellular signaling and migration of human breast cancer cells J Thromb Haemost 2 93 101 10.1111/j.1538-7836.2004.00545.x
37. A Jikuhara M Yoshii H Iwagaki S Mori M Nishibori N Tanaka 2003 MAP kinase-mediated proliferation of DLD-1 carcinoma by the stimulation of protease-activated receptor 2 Life Sci 73 2817 2829 10.1016/S0024-3205(03)00702- 1
38. E Jin M Fujiwara X Pan M Ghazizadeh S Arai Y Ohaki, et al. 2003 Protease-activated receptor (PAR)-1 and PAR-2 participate in the cell growth of alveolar capillary endothelium in primary lung adenocarcinomas Cancer 97 703 713 10.1002/cncr.11087
39. AK Kakkar 2004 Thrombosis and cancer Hematol J 5 Suppl 3 S20 S23 10.1038/sj.thj.6200416
40. L Kamath A Meydani F Foss A Kuliopulos 2001 Signaling from protease-activated receptor-1 inhibits migration and invasion of breast cancer cells Cancer Res 61 5933 5940
41. OH Kang HJ Jeong DK Kim SC Choi TH Kim YH Nah, et al. 2003 Trypsin induces tumour necrosis factor-alpha secretion from a human leukemic mast cell line Cell Biochem Funct 21 161 167 10.1002/cbf.1014
42. R Kaufmann S Rahn K Pollrich J Hertel Y Dittmar M Hommann, et al. 2007 Thrombin-mediated hepatocellular carcinoma cell migration: cooperative action via proteinase-activated receptors 1 and 4 J Cell Physiol 211 699 707 10.1002/jcp.21027
43. R Kaufmann S Patt H Schafberg R Kalff G Neupert G Nowak 1998 Functional thrombin receptor PAR1 in primary cultures of human glioblastoma cells Neuroreport 9 709 712 10.1097/00001756-199803090-00027
44. R Kaufmann S Patt M Zieger R Kraft G Nowak 1999 Presence of the proteinase-activated receptor-2 (PAR-2) in human brain tumor cells-trypsin- and SLIGRL-induced calcium response in primary cultured meningiomas Cancer Lett 139 109 113 10.1016/S0304-3835(99)00025-7
45. R Kaufmann S Patt M Zieger R Kraft S Tausch P Henklein, et al. 2000 The two-receptor system PAR-1/PAR-4 mediates alpha-thrombin-induced [Ca(2+)](i) mobilization in human astrocytoma cells J Cancer Res Clin Oncol 126 91 94 10.1007/PL00008481
46. R Kaufmann U Junker K Nuske M Westermann P Henklein J Scheele, et al. 2002 PAR-1- and PAR-3-type thrombin receptor expression in primary cultures of human renal cell carcinoma cells Int J Oncol 20 177 180
47. R Kaufmann B Schulze G Krause LM Mayr U Settmacher P Henklein 2005 Proteinase-activated receptors (PARs)-The PAR3 Neo-N-terminal peptide TFRGAP interacts with PAR1 Regul Pept 125 61 66 10.1016/j.regpep.2004.07.032
48. V Kaushal M Kohli RA Dennis ER Siegel WW Chiles P Mukunyadzi 2006 Thrombin receptor expression is upregulated in prostate cancer Prostate 66 273 282 10.1002/pros.20326
49. A Kawabata M Saifeddine B Al-Ani L Leblond MD Hollenberg 1999 Evaluation of proteinase-activated receptor-1 (PAR1) agonists and antagonists using a cultured cell receptor desensitization assay: activation of PAR2 by PAR1-targeted ligands J Pharmacol Exp Ther 288 358 370
50. MS Kim H Jo JY Um JM Yi DK Kim SC Choi, et al. 2002 Agonists of proteinase-activated receptor 2 induce TNF-alpha secretion from astrocytoma cells Cell Biochem Funct 20 339 345 10.1002/cbf.982
51. Y Liu MZ Gilcrease Y Henderson XH Yuan GL Clayman Z Chen 2001 Expression of protease-activated receptor 1 in oral squamous cell carcinoma Cancer Lett 169 173 180 10.1016/S0304-3835(01)00504-3
52. J Liu M Bastian P Kohlschein P Schuff-Werner M Steiner 2003 Expression of functional protease-activated receptor 1 in human prostate cancer cell lines Urol Res 31 163 168 10.1007/s00240-003-0309-2
53. D Massi A Naldini C Ardinghi F Carraro A Franchi M Paglierani, et al. 2005 Expression of protease-activated receptors 1 and 2 in melanocytic nevi and malignant melanoma Hum Pathol 36 676 685 10.1016/j.humpath.2005.04.008
54. R Matej P Mandakova I Netikova P Pouckova T Olejar 2007 Proteinase-activated receptor-2 expression in breast cancer and the role of trypsin on growth and metabolism of breast cancer cell line MDA MB-231 Physiol Res 56 475 484
55. S Miyata N Koshikawa H Yasumitsu K Miyazaki 2000 Trypsin stimulates integrin alpha(5)beta(1)-dependent adhesion to fibronectin and proliferation of human gastric carcinoma cells through activation of proteinase-activated receptor-2 J Biol Chem 275 4592 4598 10.1074/jbc.275.7.4592
56. GJ Mize W Wang TK Takayama 2008 Prostate-specific kallikreins-2 and -4 enhance the proliferation of DU-145 prostate cancer cells through protease-activated receptors-1 and -2 Mol Cancer Res 6 1043 1051 10.1158/1541-7786.MCR-08-0096
57. QD Nguyen O De Wever E Bruyneel A Hendrix WZ Xie A Lombet, et al. 2005 Commutators of PAR-1 signaling in cancer cell invasion reveal an essential role of the Rho-Rho kinase axis and tumor microenvironment Oncogene 24 8240 8251 10.1038/sj.onc.1208990
58. T Ohta K Shimizu S Yi H Takamura K Amaya H Kitagawa, et al. 2003 Protease-activated receptor-2 expression and the role of trypsin in cell proliferation in human pancreatic cancers Int J Oncol 23 61 66
59. T Okamoto M Nishibori K Sawada H Iwagaki N Nakaya A Jikuhara, et al. 2001 The effects of stimulating protease-activated receptor-1 and -2 in A172 human glioblastoma J Neural Transm 108 125 140 10.1007/s007020170083
60. LC Petersen 2008 Microarray studies of factor VIIa-activated cancer cells Thromb Res 122 Suppl 1 S11 S13 10.1016/S0049-3848(08)70011-2
61. AR Radjabi K Sawada S Jagadeeswaran A Eichbichler HA Kenny A Montag, et al. 2008 Thrombin induces tumor invasion through the induction and association of matrix metalloproteinase-9 and beta1-integrin on the cell surface J Biol Chem 283 2822 2834 10.1074/jbc.M704855200
62. C Rudroff S Seibold R Kaufmann CC Zetina K Reise U Schafer, et al. 2002 Expression of the thrombin receptor PAR-1 correlates with tumour cell differentiation of pancreatic adenocarcinoma in vitro Clin Exp Metastasis 19 181 189 10.1023/A:1014598904644
63. W Ruf BM Mueller 2006 Thrombin generation and the pathogenesis of cancer Semin Thromb Hemost 32 Suppl 1 61 68 10.1055/s-2006-939555
64. A Rullier N Senant W Kisiel P Bioulac-Sage C Balabaud B Le Bail, et al. 2006 Expression of protease-activated receptors and tissue factor in human liver Virchows Arch 448 46 51 10.1007/s00428-005-0078-0
65. PE Sanchez-Hernandez MG Ramirez-Duenas B Albarran-Somoza T Garcia-Iglesias A del Toro-Arreola R Franco-Topete, et al. 2008 Protease-activated receptor-2 (PAR-2) in cervical cancer proliferation Gynecol Oncol 108 19 26 10.1016/j.ygyno.2007.08.083
66. H Schafberg G Nowak R Kaufmann 1997 Thrombin has a bimodal effect on glioma cell growth Br J Cancer 76 1592 1595
67. H Schiller T Bartscht A Arlt MO Zahn A Seifert T Bruhn, et al. 2002 Thrombin as a survival factor for cancer cells: thrombin activation in malignant effusions in vivo and inhibition of idarubicin-induced cell death in vitro Int J Clin Pharmacol Ther 40 329 335
68. JH Seo KH Kim H Kim 2007 Role of proteinase-activated receptor-2 on cyclooxygenase-2 expression in H. pylori-infected gastric epithelial cells Ann N Y Acad Sci 1096 29 36 10.1196/annals.1397.067
69. X Shi B Gangadharan LF Brass W Ruf BM Mueller 2004 Protease-activated receptors (PAR1 and PAR2) contribute to tumor cell motility and metastasis Mol Cancer Res 2 395 402
70. K Shibata K Yada T Matsumoto A Sasaki M Ohta S Kitano 2004 Protease-activating-receptor-2 is frequently expressed in papillary adenocarcinoma of the gallbladder Oncol Rep 12 1013 1016
71. C Tellez M Bar-Eli 2003 Role and regulation of the thrombin receptor (PAR-1) in human melanoma Oncogene 22 3130 3137 10.1038/sj.onc.1206453
72. CS Tellez DW Davis VG Prieto JE Gershenwald MM Johnson MF McCarty, et al. 2007 Quantitative analysis of melanocytic tissue array reveals inverse correlation between activator protein-2alpha and protease-activated receptor-1 expression during melanoma progression J Invest Dermatol 127 387 393 10.1038/sj.jid.5700539
73. NE Tsopanoglou ME Maragoudakis 2004 Role of thrombin in angiogenesis and tumor progression Semin Thromb Hemost 30 63 69 10.1055/s-2004-822971
74. N Vergnolle NW Bunnett KA Sharkey V Brussee SJ Compton EF Grady, et al. 2001 Proteinase-activated receptor-2 and hyperalgesia: a novel pain pathway Nat Med 7 821 826 10.1038/89945
75. HH Versteeg F Schaffner M Kerver LG Ellies P Andrade-Gordon BM Mueller, et al. 2008 Protease-activated receptor (PAR) 2, but not PAR1, signaling promotes the development of mammary adenocarcinoma in polyoma middle T mice Cancer Res 68 7219 7227 10.1158/0008-5472.CAN-08-0419
76. TK Vu DT Hung VI Wheaton SR Coughlin 1991 Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation Cell 64 1057 1068 10.1016/0092-8674(91)90261-V
77. YJ Yin V Katz Z Salah M Maoz I Cohen B Uziely H Turm S Grisaru-Granovsky H Suzuki R Bar-Shavit 2006 Mammary gland tissue targeted overexpression of human protease-activated receptor 1 reveals a novel link to B-Catenin stabilization Cancer Res 66 10 5224 5233 10.1158/0008-5472.CAN-05-4234
78. M Yoshii A Jikuhara S Mori H Iwagaki HK Takahashi M Nishibori, et al. 2005 Mast cell tryptase stimulates DLD-1 carcinoma through prostaglandin- and MAP kinase-dependent manners J Pharmacol Sci 98 450 458 10.1254/jphs.FPJ05002X
79. J Zain YQ Huang X Feng ML Nierodzik JJ Li S Karpatkin 2000 Concentration-dependent dual effect of thrombin on impaired growth/apoptosis or mitogenesis in tumor cells Blood 95 3133 3138
80. X Zhang JL Hunt DP Landsittel S Muller K Adler-Storthz RL Ferris, et al. 2004 Correlation of protease-activated receptor-1 with differentiation markers in squamous cell carcinoma of the head and neck and its implication in lymph node metastasis Clin Cancer Res 10 8451 8459 10.1158/1078-0432.CCR-04-0546