Thrombin regulates the metastatic potential of human rhabdomyosarcoma cells: Distinct role of PAR1 and PAR3 signaling

Molecular Cancer Research

Volumn 8, Issue 5, 2010, Pages 677-690

  Wysoczynski, Marcin ^a   Liu, Rui ^a   Kucia, Magda ^a   Drukala, Justyna ^b   Ratajczak, Mariusz Z ^a,c  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b JAGIELLONIAN UNIVERSITY   (Poland)

^c POMERANIAN MEDICAL UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2BETA3 INTEGRIN; INTEGRIN; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 3; SHORT HAIRPIN RNA; THROMBIN; UNCLASSIFIED DRUG; PROTEASE-ACTIVATED RECEPTOR 3; THROMBIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ADHESION; CELL MOTILITY; CELL PROLIFERATION; CELL TRANSFER; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MALE; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RHABDOMYOSARCOMA; SARCOMA CELL; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; ANIMAL; CANCER TRANSPLANTATION; COMPARATIVE STUDY; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; RNA INTERFERENCE; SCID MOUSE; SECONDARY; TUMOR CELL LINE;

MUS;

ANIMALS; CELL ADHESION; CELL LINE, TUMOR; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, SCID; NEOPLASM TRANSPLANTATION; PHOSPHORYLATION; PLATELET ACTIVATION; RECEPTOR, PAR-1; RECEPTORS, THROMBIN; RHABDOMYOSARCOMA; RNA INTERFERENCE; THROMBIN;

EID: 77952942732     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-10-0019     Document Type: Article

References (53)

1. Ruymann FB, Newton WA, Ragab AH, Donaldson MH, Foulkes M. Bone marrow metastases at diagnosis in children and adolescents with rhabdomyosarcoma. Cancer 1984;53:368-373
2. Dickman PS, Tsokos M, Triche TJ. Biology of rhabdomyosarcoma: cell culture, xenografts and animal models. In: Maurer HM, Ruymann FB, Pochedly C, editors. Rhabdomyosarcoma and Related Tumours in Children and Adolescents. Boca Raton (FL): CRC Press; 1991, p. 49-88.
3. Sandberg AA, Stone JF, Czarnecki L, Cohen JD. Hematologic masquerade of rhabdomyosarcoma. Am J Hematol 2001;68:51-57
4. Barr FG, Galili N, Holick J, Biegel JA, Rovera G, Emanuel BS. Rearrangement of the PAX3 paired box gene in the paediatric solid tumour alveolar rhabdomyosarcoma. Nat Genet 1993;3: 113-117 (Pubitemid 23079791)
5. Anderson MJ, Shelton GD, Cavenee KW, Arden KC. Embryonic expression of the tumour-associated PAX3-FKHR fusion protein interferes with the developmental functions of PAX3. Proc Natl Acad Sci U S A 2001;98:1589-1594
6. Davis RJ, Barr FG. Fusion genes resulting from alternative chromosomal translocations are overexpressed by gene-specific mechanisms in alveolar rhabdomyosarcoma. Proc Natl Acad Sci U S A 1997;94:8047-8051
7. Davis RJ, D'Cruz CM, Lovell MA, Biegel JA, Barr FG. Fusion of PAX7 to FKHR by the variant t(1;13)(p36;q14) translocation in alveolar rhabdomyosarcoma. Cancer Res 1994;54:2869-2872
8. Collins MH, Zhao H, Womer RB, Barr FG. Proliferative and apoptotic differences between alveolar rhabdomyosarcoma subtypes: a comparative study of tumors containing PAX3-FKHR gene fusions. Med Pediatr Oncol 2000;37:83-89
9. Bennicelli JL, Advani S, Schafer BW, Barr FG. PAX3 and PAX7 exhibit conserved cis-acting transcription repression domains and utilize a common gain of function mechanism in alveolar rhabdomyosarcoma. Oncogene 1999;18:4348-4356
10. Kelly KM, Womer RB, Barr F. 3-FKHR and PAX7-FKHR fusions in rhabdomyosarcoma. J Pediatr Hematol Oncol 1998;20:517-518
11. Libura J, Drukala J, Majka M, et al. CXCR4-SDF-1 signaling is active in rhabdomyosarcoma cells and regulates locomotion, chemotaxis, and adhesion. Blood 2002;100:2597-2606
12. Jankowski K, Kucia M, Wysoczynski M, et al. Both hepatocyte growth factor (HGF) and stromal-derived factor-1 regulate the metastatic behavior of human rhabdomyosarcoma cells, but only HGF enhances their resistance to radiochemotherapy. Cancer Res 2003;63:7926-7935
13. Wysoczynski M, Miekus K, Jankowski K, et al. Leukemia inhibitory factor: a newly identified metastatic factor in rhabdomyosarcomas. Cancer Res 2007;67:2131-2140
14. Grymula K, Tarnowski M, Wysoczynski M, et al. Overlapping and distinct role of CXCR7-SDF-1/ITAC and CXCR4-SDF-1 axes in regulating metastatic behavior of human rhabdomyosarcomas. Int J Cancer. Epub 2010 Feb 16. doi: 10.1002/ijc.25245.
15. Fiegl M, Weltermann A, Stindl R, Fonatsch C, Lechner K, Gisslinger H. Massive disseminated intravascular coagulation and hyperfibrinolysis in alveolar rhabdomyosarcoma: case report and review of the literature. Ann Hematol 1999;78:335-338
16. Sills RH, Stockman JA III, Miller ML, Stuart MJ. Consumptive coagulopathy. A complication of therapy of solid tumors in childhood. Am J Dis Child 1978;132:870-872
17. Semino A, Danova M, Perlini S, Palladini G, Riccardi A, Perfetti V. Unusual manifestations of disseminated neoplasia at presentation: right-sided heart failure due to a massive cardiac metastasis and autoimmune thrombocytopenia in pleomorphic rhabdomyosarcoma of the adult. Am J Clin Oncol 2006;29:102-103
18. Baron JA, Gridley G, Weiderpass E, Nyren O, Linet M. Venous thromboembolism and cancer. Lancet 1998;351:1077-1080
19. Gerber DE, Grossman SA, Streiff MB. Management of venous thromboembolism in patients with primary and metastatic brain tumors. J Clin Oncol 2006;24:1310-1318
20. Falanga A, Zacharski L. Deep vein thrombosis in cancer: the scale of the problem and approaches to management. Ann Oncol 2005; 16:696-701.
21. Hilson AJW, Sorensen HT, MellemkjAer L, Olsen JH. Cancer and venous thromboembolism. New Eng J Med 1998;339:703-713
22. Blom JW, Osanto S, Rosendaal FR. The risk of a venous thrombotic event in lung cancer patients: higher risk for adenocarcinoma than squamous cell carcinoma. J Thromb Haemost 2004;2:1760-1765
23. Caine GJ, Lip GY, Stonelake PS, Ryan P, Blann AD. Platelet activation, coagulation and angiogenesis in breast and prostate carcinoma. Thromb Haemost 2004;92:185-190
24. Chew HK, Davies AM, Wun T, Harvey D, Zhou H, White RH. The incidence of venous thromboembolism among patients with primary lung cancer. J Thromb Haemost 2008;6:601-608
25. Wun T, Chew HK, Zhou H, Harvey D, White RH. Cause of death among patients with local or regional stage cancer of the breast, colon and lung who develop venous thromboembolism (VTE). Blood 2006;108:433a.
26. Sgouros J, Maraveyas A. Excess premature (3-month) mortality in advanced pancreatic cancer could be related to fatal vascular thromboembolic events. A hypothesis based on a systematic review of phase III chemotherapy studies in advanced pancreatic cancer. Acta Oncol 2007;43:1-10.
27. Kasthuri RS, Taubman MB, Mackman N. Role of tissue factor in cancer. J Clin Oncol 2009;27:4834-4838
28. Rak J, Milsom C, Magnus N, Yu J. Tissue factor in tumour progression. Best Pract Res Clin Haematol 2009;22:71-83.
29. Janowska-Wieczorek A, Wysoczynski M, Kijowski J, et al. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer 2005;113:752-760
30. Janowska-Wieczorek A, Marquez-Curtis LA, Wysoczynski M, Ratajczak MZ. Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion 2006; 46:1199-1209
31. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature 2000;407:258-264
32. Vu TK, Hung DT, Wheaton VI, Coughlin SR. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 1991;64:1057-1068
33. Ishihara H, Connolly AJ, Zeng D, et al. Protease-activated receptor 3 is a second thrombin receptor in humans. Nature 1997;386:502-506
34. Xu WF, Andersen H, Whitmore TE, et al. Cloning and characterization of human protease-activated receptor 4. Proc Natl Acad Sci U S A 1998;95:6642-6646
35. Molino M, Barnathan ES, Numerof R, et al. Interactions of mast cell tryptase with thrombin receptors and PAR-2. J Biol Chem 1997;272: 4043-4049
36. Kawabata A, Saifeddine M, Al-Ani B, Leblond L, Hollenberg MD. 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 1999;288:358-370
37. Al-Ani B, Saifeddine M, Kawabata A, et al. Proteinase-activated receptor 2 (PAR(2)): development of a ligand-binding assay correlating with activation of PAR(2) by PAR(1)- and PAR(2)-derived peptide ligands. J Pharmacol Exp Ther 1999;290:753-760
38. Hu L, Lee L, Campbell W, Perez-Soler R, Karpatkin S. Role of endogenous thrombin in tumor implantation, seeding and spontaneous metastasis. Blood 2004;104:2746-2751
39. Klepfish A, Greco M, Karpatkin S. Thrombin stimulates melanoma tumor-cell binding to endothelial cells and subendothelial matrix. Int J Cancer 1993;53:978-982
40. Nierodzik M, Kajumo F, Karpatkin S. Effect of thrombin treatment of tumor cells on adhesion of tumor cells to platelets in vitro and metastasis in vivo. Cancer Res 1992;52:3267-3272
41. Nierodzik M, Chen K, Takeshita K, et al. Protease-activated receptor 1 (PAR-1) is required and rate-limiting for thrombin-enhanced experimental pulmonary metastasis. Blood 1998;92:3694-3700
42. Shi X, Gangadharan B, Brass L, Ruf W, Mueller B. Protease-activated receptors (PAR1 and PAR2) contribute to tumor cell motility and metastasis, Mol. Cancer Res 2004;2:395-402.
43. Hu L, Roth JM, Brooks P, Ibrahim S, Karpatkin S. Twist is required for thrombin-induced tumor angiogenesis and growth. Cancer Res 2008;68:4296-4302
44. Gruler H, Nucitelli R. Neural creast cell galvanotaxis: new data and a novel approach to the analysis of both galvanotaxis and chemotaxis. Cell Motil Cytoskeleton 1991;19:121-133
45. Friedl P, Noble PB, Zanker KS. Lymphocyte locomotion in three-dimensional collagen gels. Comparison of three quantitative methods for analysing cell trajectories. J Immunol Methods 1993; 165:157-165
46. Korohoda W, Drukala J, Sroka J, Madeja Z. Isolation, spreading, locomotion on various substrata, and the effect of hypotonicity on locomotion of fish keratinocytes. Biochem Cell Biol 1997;75:277-286
47. Miekus K, Czernik M, Sroka J, Czyz J, Madeja Z. Contact stimulation of prostate cancer cell migration: the role of gap junctional coupling and migration stimulated by heterotypic cell-to-cell contacts in determination of the metastatic phenotype of Dunning rat prostate cancer cells. Biol Cell 2005;97:893-903.
48. Coughlin SR. How the protease thrombin talks to cells. Proc Natl Acad Sci U S A 1999;96:11023-11027
49. Hansen KK, Saifeddine M, Hollenberg MD. Tethered ligand-derived peptides of proteinase-activated receptor 3 (PAR3) activate PAR1 and PAR2 in Jurkat T cells. Immunology 2004;112:183-190
50. Wysoczynski M, Shin DM, Kucia M, Ratajczak MZ. Selective upregulation of interleukin-8 by human rhabdomyosarcomas in response to hypoxia: therapeutic implications. Int J Cancer 2009; 126:371-381
51. Hu L, Ibrahim S, Liu C, Skaar J, Pagano M, Karpatkin S. Thrombin induces tumor cell cycle activation and spontaneous growth by down-regulation of p27Kip1, in association with the up-regulation of Skp2 and MiR-222. Cancer Res 2009;69:3374-3381
52. D'Amico AV, Nelson AC, Babayan RK. Thrombin: implications for intratumor therapy against metastasis. J Cancer Res Clin Oncol 1988;114:129-132
53. McLaughlin JN,PattersonMM,MalikAB. Protease-activated receptor-3 (PAR3) regulates PAR1 signaling by receptor dimerization. Proc Natl Acad Sci U S A 2007;104:5662-5667