Matrix metalloproteinase-1 and thrombin differentially activate gene expression in endothelial cells via PAR-1 and promote angiogenesis

American Journal of Pathology

Volumn 173, Issue 6, 2008, Pages 1736-1746

  Blackburn, Jessica S ^a   Brinckerhoff, Constance E ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENASE; INTERSTITIAL COLLAGENASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR ANTAGONIST; SCH 79797; THROMBIN; THROMBIN RECEPTOR; UNCLASSIFIED DRUG;

ANGIOGENESIS; ARTICLE; CANCER GROWTH; CELL INVASION; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; METASTASIS POTENTIAL; MICROVASCULATURE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

EID: 57149094231     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2008.080512     Document Type: Article

References (60)

1. Page-McCaw A, Ewald A, Werb Z: Matrix metalloproteinases and the regulation of tissue remodeling. Nat Rev Mol Cell Bio 2007, 8:221-233
2. Ala-aho R, Kahari V-M: Collagenases in cancer. Biochimie 2005, 87:273-286
3. Brinckerhoff CE, Rutter JL, Benbow U: Interstitial collagenases as markers of tumor progression. Clin Cancer Res 2000, 6:4823-4830
4. Stamenkovic I: Matrix metalloproteinases in tumor invasion and metastasis. Semin Cancer Biol 2000, 10:415-433
5. Blackburn JS, Rhodes CH, Coon CI, Brinckerhoff CE: RNA interference inhibition of matrix metalloproteinase-1 prevents melanoma metastasis by reducing tumor collagenase activity and angiogenesis. Cancer Res 2007, 67:10849-10858
6. Eck SM, Hoopes PJ, Petrella BL, Coon CI, Brinckerhoff CE: Matrix metalloproteinase-1 promotes breast cancer angiogenesis and osteolysis in a novel in vivo model. Breast Cancer Res 2008 Epub ahead of print. DOI: 10.1007/s10549-008-0085-3
7. Boire A, Covic L, Agarwal A, Jacques S, Sherifi S, Kuliopulos A: PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell 2005, 120:303-313
8. Pulukuri SM, Rao JS: Matrix Metalloproteinase-1 promotes prostate tumor growth and metastasis. Int J Oncol 2008, 32:757-765
9. Sang O: Complex role of matrix metalloproteinases in angiogenesis. Cell Res 1998, 8:171-177
10. Ossovskaya V, Bunnett N: Protease-activated receptors: contribution to physiology and disease. Physiol Rev 2004, 84:579-621
11. Arora P, Ricks TK, Trejo J: Protease-activated receptor signalling, endocytic sorting and dysregulation in cancer. J Cell Sci 2007, 120:921-928
12. Hollenberg MD, Compton SJ: International Union of Pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol Rev 2002, 54:203-217
13. Dvorak H: Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 1986, 315:1650-1659
14. Tsopanoglou NE, Maragoudakis ME: Role of thrombin in angiogenesis and tumor progression. Sem Thromb Hemostasis 2004, 30:63-69
15. Rickles FR, Patierno S, Fernandez PM: Tissue factor, thrombin, and cancer. Chest 2003, 124:58S-68S
16. Maragoudakis ME, Tsopanoglou NE, Andriopoulou P: Mechanism of thrombin-induced angiogenesis. Biochem Soc Trans 2002, 30:173-177
17. Goerge T, Barg A, Schnaeker E-M, Poppelmann B, Shpacovitch V, Rattenholl A, Maaser C, Luger TA, Steinhoff M, Schneider SW: Tumor-derived matrix metalloproteinase-1 targets endothelial proteinaseactivated receptor 1 promoting endothelial cell activation. Cancer Res 2006, 66:7766-7774
18. Nesi A, Fragai M: Substrate specificities of matrix metalloproteinase 1 in PAR-1 exodomain proteolysis. ChemBioChem 2007, 8:1367-1369
19. Huntington JT, Shields JM, Der CJ, Wyatt CA, Benbow U, Slingluff CL, Jr., Brinckerhoff CE: Overexpression of collagenase 1 (MMP-1) is mediated by the ERK pathway in invasive melanoma cells. J Biol Chem 2004, 279:33168-33176
20. Haralabopoulos GC, Grant DS, Kleinman HK, Maragoudakis ME: Thrombin promotes endothelial cell alignment in Matrigel in vitro and angiogenesis in vivo. Am J Physiol Cell Physiol 1997, 273:C239-C245
21. Petrella BL, Lohi J, Brinckerhoff CE: Identification of membrane type-1 matrix metalloproteinase as a target of hypoxia-inducible factor-2a in von-Hippel-Lindau renal cell carcinoma. Oncogene 2005, 24244:1043-1052
22. Abramoff MD, Magelhaes PJ, Ram SJ: Image processing with ImageJ. Biophotonics International 2004, 11:36-42
23. Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2-[delta][delta]CT method. Methods 2001, 25:402-408
24. John A, Tuszynski G: The role of matrix metalloproteinases in tumor angiogenesis and tumor metastasis. Pathol Oncol Res 2001, 7:14-23
25. Auerbach R, Lewis R, Shinners B, Kubai L, Akhtar N: Angiogenesis assays: a critical overview. Clin Chem 2003, 49:32-40
26. Norrby K: In vivo models of angiogenesis. J Cell Mol Med 2006, 10:588-612
27. Tsopanoglou NE, Maragoudakis ME: Inhibition of angiogenesis by small-molecule antagonists of protease-activated receptor-1. Semin Thromb Hemost 2007, 33:680-687
28. Ahn H-S, Foster C, Boykow G, Stamford A, Manna M, Graziano M: Inhibition of cellular action of thrombin by N3-cyclopropyl-7-{[4-(1-methylethyl) phenylmethyl}-7H-pyrrolo[3,2-fquinazoline-1,3-diamine (SCH 79797), a nonpeptide thrombin receptor antagonist. Biochem Pharm 2000, 60:1425-1434
29. Hirano K, Kanaide H: Role of protease-activated receptors in the vascular system. J Atherscler Thromb 2003, 10:211-225
30. Tantivejkul K, Loberg R, Mawocha S, Day L, St. John L, Pienta B, Rubin M, Pienta R: PAR1-mediated NFkappaB activation promotes survival of prostate cancer cells through a Bcl-xL-dependent mechanism. J Cell Biochem 2005, 96:641-652
31. Eto M, Barandier C, Rathgeb L, Kozai T, Joch H, Yang Z, Luscher TF: Thrombin suppresses endothelial nitric oxide synthase and upregulates endothelin-converting enzyme-1 expression by distinct pathways: role of Rho/ROCK and mitogen-activated protein kinase. Circ Res 2001, 89:583-590
32. Macfarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R: Proteinaseactivated receptors. Pharmacol Rev 2001, 53:245-282
33. Ellis CA, Malik AB, Gilchrist A, Hamm H, Sandoval R, Voyno-Yasenetskaya T, Tiruppathi C: Thrombin induces proteinase-activated receptor-1 gene expression in endothelial cells via activation of Gi-linked Ras/mitogen- activated protein kinase pathway. J Biol Chem 1999, 274:13718-13727
34. McLaughlin JN, Mazzoni MR, Cleator JH, Earls L, Perdigoto AL, Brooks JD, Muldowney JAS III, Vaughan DE, Hamm HE: Thrombin modulates the expression of a set of genes including thrombospondin-1 in human microvascular endothelial cells. J Biol Chem 2005, 280:22172-22180
35. Chandrasekharan UM, Yang L, Walters A, Howe P, DiCorleto PE: Role of CL-100, a dual specificity phosphatase, in thrombin-induced endothelial cell activation. J Biol Chem 2004, 279:46678-46685
36. Avraamides CJ, Garmy-Susini B, Varner JA: Integrins in angiogenesis and lymphangiogenesis. Nat Rev Cancer 2008:1-14
37. Porta C, Subhra Kumar B, Larghi P, Rubino L, Mancino A, Sica A: Tumor promotion by tumor-associated macrophages. Adv Exp Med Biol 2007, 604:67-86
38. Rosenkilde M, Schwartz T: The chemokine system-a major regulator of angiogenesis in health and disease. APMIS 2004, 112:481-495
39. Zipin-Roitman A, Meshel T, Sagi-Assif O, Shalmon B, Avivi C, Pfeffer R, Witz I, Ben-Baruch A: CXCL10 promotes invasion-related properties in human colorectal carcinoma cells. Cancer Res 2007, 67:3396-3405
40. Yu Q: The dynamic role of angiopoietins in tumor angiogenesis. Future Oncol 2005, 1:475-484
41. Sainson RC, Johnston DA, Chu HC, Holderfield MT, Nakatsu MN, Crampton SP, Davis J, Conn E, Hughes CC: TNF primes endothelial cells for angiogenic spouting by inducing a tip cell phenotype. Blood 2008, 111:4997-5007
42. Delafontaine P, Song YH, Li Y: Expression, regulation and function of IGF-1. IGF-1R and IGF-1 binding proteins in blood vessels Arterioiscler Thromb Vasc Biol 2004, 24:435-444
43. Veikkola T, Alitalo K: VEGFs, receptors and angiogenesis. Semin Cancer Biol 1999, 9:211-220
44. Birkedal-Hansen H, Moore WG, Bodden MK, Windsor LJ, Birkedal-Hansen B, DeCarlo A, Engler JA: Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 1993, 4:197-250
45. Bigg H, Clark I, Cawston T: Fragments of human fibroblast collagenase: interaction with metalloproteinase inhibitors and substrates. Biochim Biophys Acta 1994, 1208:157-165
46. Clark I, Cawston T: Fragments of the human fibroblast collagenase. Purification and charaterization. Biochem J 1989, 263:201-206
47. Tlsty TD, Coussens LM: Tumor stroma and regulation of cancer development. Annu Rev Path 2006, 1:119-150
48. Smalley KS, Lioni M, Herlyn M: Targeting the stromal fibroblasts: a novel approach to melanoma therapy. Exp Rev Anticancer Ther 2005, 5:1069-1078
49. Ucuzian A, Greisler H: In vitro models of angiogenesis. World J Surg 2007, 31:654-663
50. Zain J, Huang Y-Q, Feng X, Nierodzik ML, Li J-J, Karpatkin S: Concentration-dependent dual effect of thrombin on impaired growth/ apoptosis or mitogenesis in tumor cells. Blood 2000, 95:3133-3138
51. Ornstein DL, Zacharski LR: Treatment of cancer with anticoagulents: rationale in the treatment of melanoma. Int J Onc 2001, 73:157-161
52. Maragoudakis ME, Tsopanoglou NE, Andriopoulou P, Maragoudakis MM: Effects of thrombin/thrombosis in angiogenesis and tumour progression. Matrix Biol 2000, 19:345-351
53. Vincenti MP, Brinckerhoff CE: Signal transduction and cell-type specific regulation of matrix metalloproteinase gene expression: can MMPs be good for you? J Cell Physiol 2007, 213:355-364
54. Handsley MM, Edwards DR: Metalloproteinases and their inhibitors in tumor angiogenesis. Int J Cancer 2005, 115:849-860
55. Nierodzik ML, Karpatkin S: Thrombin induces tumor growth, metastasis, and angiogenesis: evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell 2006, 10:355-362
56. Marshall CJ: Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 1995, 80:179-185
57. Murphy LO, Smith S, Chen R-H, Fingar DC, Blenis J: Molecular interpretation of ERK signal duration by immediate early gene products. Nat Cell Biol 2003, 4:556-564
58. Davis G, Allen K, Salazar R, Maxwell S: Matrix metalloproteinase-1 and -9 activation by plasmin regulates a novel endothelial cell-mediated mechanism of collagen gel contraction and capillary tube regression in three-dimensional collagen matrices. J Cell Sci 2000, 114:917-930
59. Saunders W, Bayless K, Davis G: MMP-1 activation by serine proteases and MMP-10 induces human capillary tubular network collapse and regression in 3D collagen matrices. J Cell Sci 2005, 118:2325-2340
60. Zacharski LR, Memoli VA, Morain WD, Schlaeppi JM, Rousseau SM: Cellular localization of enzymatically active thrombin in intact human tissues by hirudin binding. Thromb Haemost 1995, 73:793-797