Activated protein C enhances cell motility of endothelial cells and MDA-MB-231 breast cancer cells by intracellular signal transduction

Experimental Cell Research

Volumn 316, Issue 3, 2010, Pages 314-328

  Gramling, Mark W ^a   Beaulieu, Lea M ^a   Church, Frank C ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Activated Protein C; angiogenesis; aortic rings; EGFR; EPCR; migration invasion; PAR 1

Indexed keywords

ACTIVATED PROTEIN C; ENDOTHELIAL CELL PROTEIN C RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GELATINASE A; GELATINASE B; PROTEINASE ACTIVATED RECEPTOR 1; RECEPTOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL INVASION; CELL MOTILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

EID: 72149105589     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.10.024     Document Type: Article

References (54)

1. Foster D., and Davie E.W. Characterization of a cDNA coding for human protein C. Proc. Natl. Acad. Sci. U. S. A. 81 (1984) 4766-4770
2. Fukudome K., Kurosawa S., Stearns-Kurosawa D.J., He X., Rezaie A.R., and Esmon C.T. The endothelial cell protein C receptor. Cell surface expression and direct ligand binding by the soluble receptor. J. Biol. Chem. 271 (1996) 17491-17498
3. Kisiel W., Canfield W.M., Ericsson L.H., and Davie E.W. Anticoagulant properties of bovine plasma protein C following activation by thrombin. Biochemistry 16 (1977) 5824-5831
4. Marlar R.A., Kleiss A.J., and Griffin J.H. Human protein C: inactivation of factors V and VIII in plasma by the activated molecule. Ann. N.Y. Acad. Sci. 370 (1981) 303-310
5. Walker F.J., Sexton P.W., and Esmon C.T. The inhibition of blood coagulation by activated protein C through the selective inactivation of activated factor V. Biochim. Biophys. Acta 571 (1979) 333-342
6. Walker F.J. Regulation of activated protein C by a new protein. A possible function for bovine protein S. J. Biol. Chem. 255 (1980) 5521-5524
7. Walker F.J. Regulation of activated protein C by protein S. The role of phospholipid in factor Va inactivation. J. Biol. Chem. 256 (1981) 11128-11131
8. Bertina R.M., and Factor V. Leiden and other coagulation factor mutations affecting thrombotic risk. Clin. Chem. 43 (1997) 1678-1683
9. Bernard G.R., Vincent J.L., Laterre P.F., LaRosa S.P., Dhainaut J.F., Lopez-Rodriguez A., Steingrub J.S., Garber G.E., Helterbrand J.D., Ely E.W., and Fisher Jr. C.J. Efficacy and safety of recombinant human activated protein C for severe sepsis. N. Engl. J. Med. 344 (2001) 699-709
10. Kobayashi H., Moniwa N., Gotoh J., Sugimura M., and Terao T. Role of activated protein C in facilitating basement membrane invasion by tumor cells. Cancer Res. 54 (1994) 261-267
11. Rao N.K., Shi G.P., and Chapman H.A. Urokinase receptor is a multifunctional protein: influence of receptor occupancy on macrophage gene expression. J. Clin. Invest. 96 (1995) 465-474
12. Lakka S.S., Gondi C.S., Yanamandra N., Dinh D.H., Olivero W.C., Gujrati M., and Rao J.S. Synergistic down-regulation of urokinase plasminogen activator receptor and matrix metalloproteinase-9 in SNB19 glioblastoma cells efficiently inhibits glioma cell invasion, angiogenesis, and tumor growth. Cancer Res. 63 (2003) 2454-2461
13. Keski-Oja J., Lohi J., Tuuttila A., Tryggvason K., and Vartio T. Proteolytic processing of the 72,000-Da type IV collagenase by urokinase plasminogen activator. Exp. Cell. Res. 202 (1992) 471-476
14. Makowski G.S., and Ramsby M.L. Binding of latent matrix metalloproteinase 9 to fibrin: activation via a plasmin-dependent pathway. Inflammation 22 (1998) 287-305
15. Murphy G., Atkinson S., Ward R., Gavrilovic J., and Reynolds J.J. The role of plasminogen activators in the regulation of connective tissue metalloproteinases. Ann. N. Y. Acad. Sci. 667 (1992) 1-12
16. Jackson C., Nguyen M., Arkell J., and Sambrook P. Selective matrix metalloproteinase (MMP) inhibition in rheumatoid arthritis-targetting gelatinase A activation. Inflamm. Res. 50 (2001) 183-186
17. Jackson C.J., Xue M., Thompson P., Davey R.A., Whitmont K., Smith S., Buisson-Legendre N., Sztynda T., Furphy L.J., Cooper A., Sambrook P., and March L. Activated protein C prevents inflammation yet stimulates angiogenesis to promote cutaneous wound healing. Wound Repair Regen. 13 (2005) 284-294
18. Pekovich S.R., Bock P.E., and Hoover R.L. Thrombin-thrombomodulin activation of protein C facilitates the activation of progelatinase A. FEBS Lett. 494 (2001) 129-132
19. Xue M., Thompson P., Kelso I., and Jackson C. Activated protein C stimulates proliferation, migration and wound closure, inhibits apoptosis and upregulates MMP-2 activity in cultured human keratinocytes. Exp. Cell. Res. 299 (2004) 119-127
20. Uchiba M., Okajima K., Oike Y., Ito Y., Fukudome K., Isobe H., and Suda T. Activated protein C induces endothelial cell proliferation by mitogen-activated protein kinase activation in vitro and angiogenesis in vivo. Circ. Res. 95 (2004) 34-41
21. Russo A., Soh U.J., Paing M.M., Arora P., and Trejo J. Caveolae are required for protease-selective signaling by protease-activated receptor-1. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 6393-6397
22. Xue M., Campbell D., and Jackson C.J. Protein C is an autocrine growth factor for human skin keratinocytes. J. Biol. Chem. 282 (2007) 13610-13616
23. Beaulieu L.M., and Church F.C. Activated protein C promotes breast cancer cell migration through interactions with EPCR and PAR-1. Exp. Cell. Res. 313 (2007) 677-687
24. Belting M., Dorrell M.I., Sandgren S., Aguilar E., Ahamed J., Dorfleutner A., Carmeliet P., Mueller B.M., Friedlander M., and Ruf W. Regulation of angiogenesis by tissue factor cytoplasmic domain signaling. Nat. Med. 10 (2004) 502-509
25. Ullian M.E., Webb J.G., Chen R., Paul R.V., and Morinelli T.A. Mechanisms of vascular angiotensin II surface receptor regulation by epidermal growth factor. J. Cell. Physiol. 200 (2004) 451-457
26. Tong Q., Zheng L., Li B., Wang D., Huang C., Matuschak G.M., and Li D. Hypoxia-induced mitogenic factor enhances angiogenesis by promoting proliferation and migration of endothelial cells. Exp. Cell. Res. 312 (2006) 3559-3569
27. Enciso J.M., Gratzinger D., Camenisch T.D., Canosa S., Pinter E., and Madri J.A. Elevated glucose inhibits VEGF-A-mediated endocardial cushion formation: modulation by PECAM-1 and MMP-2. J. Cell. Biol. 160 (2003) 605-615
28. Palmieri D., Lee J.-W., Juliano R.L., and Church F.C. Plasminogen activator inhibitor-1 and -3 increase cell adhesion and motility of MDA-MB-435 breast cancer cells. J. Biol. Chem. 277 (2002) 40950-40957
29. Whitley B.R., Palmieri D., Twerdi C., and Church F.C. Expression of active plasminogen activator inhibitor-1 regulates cell migration and invasion in breast and gynecological cancer cells. Exp. Cell. Res. 296 (2004) 151-162
30. Thellin O., Zorzi W., Lakaye B., De Borman B., Coumans B., Hennen G., Grisar T., Igout A., and Heinen E. Housekeeping genes as internal standards: use and limits. J. Biotechnol. 75 (1999) 291-295
31. Kajanne R., Miettinen P., Mehlem A., Leivonen S.K., Birrer M., Foschi M., Kahari V.M., and Leppa S. EGF-R regulates MMP function in fibroblasts through MAPK and AP-1 pathways. J. Cell. Physiol. 212 (2007) 489-497
32. Marinissen M.J., Servitja J.M., Offermanns S., Simon M.I., and Gutkind J.S. Thrombin protease-activated receptor-1 signals through Gq- and G13-initiated MAPK cascades regulating c-Jun expression to induce cell transformation. J. Biol. Chem. 278 (2003) 46814-46825
33. Ho T.Y., and Bagnell C.A. Relaxin induces matrix metalloproteinase-9 through activation of nuclear factor kappa B in human THP-1 cells. Ann. N. Y. Acad. Sci. 1041 (2005) 314-316
34. Duxbury M.S., and Whang E.E. RRM2 induces NF-kappaB-dependent MMP-9 activation and enhances cellular invasiveness. Biochem. Biophys. Res. Commun. 354 (2007) 190-196
35. Brown K., Gerstberger S., Carlson L., Franzoso G., and Siebenlist U. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 267 (1995) 1485-1488
36. Domotor E., Benzakour O., Griffin J.H., Yule D., Fukudome K., and Zlokovic B.V. Activated protein C alters cytosolic calcium flux in human brain endothelium via binding to endothelial protein C receptor and activation of protease activated receptor-1. Blood 101 (2003) 4797-4801
37. White B., Schmidt M., Murphy C., Livingstone W., O'Toole D., Lawler M., O'Neill L., Kelleher D., Schwarz H.P., and Smith O.P. Activated protein C inhibits lipopolysaccharide-induced nuclear translocation of nuclear factor kappaB (NF-kappaB) and tumour necrosis factor alpha (TNF-alpha) production in the THP-1 monocytic cell line. Br. J. Haematol. 110 (2000) 130-134
38. Cheng T., Liu D., Griffin J.H., Fernandez J.A., Castellino F., Rosen E.D., Fukudome K., and Zlokovic B.V. Activated protein C blocks p53-mediated apoptosis in ischemic human brain endothelium and is neuroprotective. Nat. Med. 9 (2003) 338-342
39. Pianetti S., Arsura M., Romieu-Mourez R., Coffey R.J., and Sonenshein G.E. Her-2/neu overexpression induces NF-kappaB via a PI3-kinase/Akt pathway involving calpain-mediated degradation of IkappaB-alpha that can be inhibited by the tumor suppressor PTEN. Oncogene 20 (2001) 1287-1299
40. Zhou B.P., Hu M.C., Miller S.A., Yu Z., Xia W., Lin S.Y., and Hung M.C. HER-2/neu blocks tumor necrosis factor-induced apoptosis via the Akt/NF-kappaB pathway. J. Biol. Chem. 275 (2000) 8027-8031
41. Finco T.S., Westwick J.K., Norris J.L., Beg A.A., Der C.J., and Baldwin Jr. A.S. Oncogenic Ha-Ras-induced signaling activates NF-kappaB transcriptional activity, which is required for cellular transformation. J. Biol. Chem. 272 (1997) 24113-24116
42. Shibata M., Kumar S.R., Amar A., Fernandez J.A., Hofman F., Griffin J.H., and Zlokovic B.V. Anti-inflammatory, antithrombotic, and neuroprotective effects of activated protein C in a murine model of focal ischemic stroke. Circulation 103 (2001) 1799-1805
43. Mosnier L.O., and Griffin J.H. Inhibition of staurosporine-induced apoptosis of endothelial cells by activated protein C requires protease-activated receptor-1 and endothelial cell protein C receptor. Biochem. J. 373 (2003) 65-70
44. Hurtado M., Lozano J.J., Castellanos E., Lopez-Fernandez L.A., Harshman K., Martinez A.C., Ortiz A.R., Thomson T.M., and Paciucci R. Activation of the epidermal growth factor signalling pathway by tissue plasminogen activator in pancreas cancer cells. Gut 56 (2007) 1266-1274
45. Ortiz-Zapater E., Peiro S., Roda O., Corominas J.M., Aguilar S., Ampurdanes C., Real F.X., and Navarro P. Tissue plasminogen activator induces pancreatic cancer cell proliferation by a non-catalytic mechanism that requires extracellular signal-regulated kinase 1/2 activation through epidermal growth factor receptor and annexin A2. Am. J. Pathol. 170 (2007) 1573-1584
46. Biscardi J.S., Maa M.C., Tice D.A., Cox M.E., Leu T.H., and Parsons S.J. c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function. J. Biol. Chem. 274 (1999) 8335-8343
47. Feistritzer C., Lenta R., and Riewald M. Protease-activated receptors-1 and -2 can mediate endothelial barrier protection: role in factor Xa signaling. J. Thromb. Haemost. 3 (2005) 2798-2805
48. Gschwind A., Hart S., Fischer O.M., and Ullrich A. TACE cleavage of proamphiregulin regulates GPCR-induced proliferation and motility of cancer cells. EMBO J. 22 (2003) 2411-2421
49. Schafer B., Marg B., Gschwind A., and Ullrich A. Distinct ADAM metalloproteinases regulate G protein-coupled receptor-induced cell proliferation and survival. J. Biol. Chem. 279 (2004) 47929-47938
50. Gooz M., Gooz P., Luttrell L.M., and Raymond J.R. 5-HT2A receptor induces ERK phosphorylation and proliferation through ADAM-17 tumor necrosis factor-alpha-converting enzyme (TACE) activation and heparin-bound epidermal growth factor-like growth factor (HB-EGF) shedding in mesangial cells. J. Biol. Chem. 281 (2006) 21004-21012
51. Sunnarborg S.W., Hinkle C.L., Stevenson M., Russell W.E., Raska C.S., Peschon J.J., Castner B.J., Gerhart M.J., Paxton R.J., Black R.A., and Lee D.C. Tumor necrosis factor-alpha converting enzyme (TACE) regulates epidermal growth factor receptor ligand availability. J. Biol. Chem. 277 (2002) 12838-12845
52. Hart S., Fischer O.M., Prenzel N., Zwick-Wallasch E., Schneider M., Hennighausen L., and Ullrich A. GPCR-induced migration of breast carcinoma cells depends on both EGFR signal transactivation and EGFR-independent pathways. Biol. Chem. 386 (2005) 845-855
53. Rodriguez-Viciana P., Warne P.H., Dhand R., Vanhaesebroeck B., Gout I., Fry M.J., Waterfield M.D., and Downward J. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 370 (1994) 527-532
54. Nguyen M., Arkell J., and Jackson C.J. Activated protein C directly activates human endothelial gelatinase A. J. Biol. Chem. 275 (2000) 9095-9098