Cathepsin B mediates the pH-dependent proinvasive activity of tumor-shed microvesicles

Neoplasia

Volumn 10, Issue 5, 2008, Pages 481-488

  Giusti, Ilaria ^a   D'Ascenzo, Sandra ^a   Millimaggi, Danilo ^a   Taraboletti, Giulia ^b   Carta, Gaspare ^c   Franceschini, Nicola ^c   Pavan, Antonio ^d   Dolo, Vincenza ^a,c  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^c UNIVERSITY OF L'AQUILA   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN B; GELATINASE A; GELATINASE B; TRANSFER RNA;

ACIDITY; ARTICLE; CANCER CELL; CANCER INVASION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; MEMBRANE VESICLE; OVARY CANCER; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING; ZYMOGRAPHY;

EID: 43249119195     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.08178     Document Type: Article

References (46)

1. L Yan L Shahied Y Tang P Kesavan MT Nakada Tumor-host interactions Preclinica 2 2004 422 426
2. P Zigrino S Loffek C Mauch Tumor-stroma interactions: their role in the control of tumor cell invasion Biochimie 87 2005 321 328
3. E Laconi The evolving concept of tumor microenvironments Bioessays 29 2007 738 744
4. G Taraboletti S D’Ascenzo P Borsotti R Giavazzi A Pavan V Dolo Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells Am J Pathol 160 2002 673 680
5. V Dolo A Ginestra G Ghersi H Nagase ML Vittorelli Human breast carcinoma cells cultured in the presence of serum shed membrane vesicles rich in gelatinolytic activities J Submicrosc Cytol Pathol 26 1994 173 810
6. V Dolo E Adobati S Canevari MA Picone ML Vittorelli Membrane vesicles shed into the extracellular medium by human breast carcinoma cells carry tumor-associated surface antigens Clin Exp Metastasis 13 1995 277 286
7. V Dolo A Ginestra D Cassara S Violini G Lucania MR Torrisi H Nagase S Canevari A Pavan ML Vittorelli Selective localization of matrix metalloproteinase 9, beta1 integrins, and human lymphocyte antigen class I molecules on membrane vesicles shed by 8701-BC breast carcinoma cells Cancer Res 58 1998 4468 4474
8. V Dolo S D’Ascenzo S Violini L Pompucci C Festuccia A Ginestra ML Vittorelli S Canevari A Pavan Matrix-degrading proteinases are shed in membrane vesicles by ovarian cancer cells in vivo and in vitro Clin Exp Metastasis 7 1999 131 140
9. A Ginestra S Monea G Seghezzi V Dolo H Nagase P Mignatti ML Vittorelli Urokinase plasminogen activator and gelatinases are associated with membrane vesicles shed by human HT-1080 fibrosarcoma cells J Biol Chem 272 1997 17216 17221
10. A Angelucci S D’Ascenzo C Festuccia GL Gravina M Bologna V Dolo A Pavan Vesicle-associated urokinase plasminogen activator promotes invasion in prostate cancer cell lines Clin Exp Metastasis 18 2000 163 170
11. G Poste GL Nicolson Arrest and metastasis of blood-borne tumor cells are modified by fusion of plasma membrane vesicles from highly metastatic cells Proc Natl Acad Sci USA 77 1980 399 403
12. K Shedden XT Xie P Chandaroy YT Chang GR Rosania Expulsion of small molecules in vesicles shed by cancer cells: association with gene expression and chemosensitivity profiles Cancer Res 63 2003 4331 4337
13. 3H thymidine incorporation, are neutralised by anti TGF-beta antibodies J Submicrosc Cytol Pathol 27 1995 535 541
14. J Albanese S Meterissian M Kontogiannea C Dubreuil A Hand S Sorba N Dainiak Biologically active Fas antigen and its cognate ligand are expressed on plasma membrane-derived extracellular vesicles Blood 91 1998 3862 3874
15. F Andre NE Schartz N Chaput C Flament G Raposo S Amigorena E Angevin L Zitvogel Tumor-derived exosomes: a new source of tumor rejection antigens Vaccine 20 2002 A28 A31
16. S Taverna G Ghersi A Ginestra S Rigogliuso S Pecorella G Alaimo F Saladino V Dolo P Dell’Era A Pavan Shedding of membrane vesicles mediates fibroblast growth factor-2 release from cells J Biol Chem 278 2003 51911 51919
17. CW Kim HM Lee TH Lee C Kang HK Kleinman YS Gho Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin Cancer Res 62 2002 6312 6317
18. A Janowska-Wieczorek M Wysoczynski J Kijowski L Marquez-Curtis B Machalinski J Ratajczak MZ Ratajczak Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer Int J Cancer 113 2005 752 760
19. G Taraboletti S D’Ascenzo I Giusti D Marchetti P Borsotti D Millimaggi R Giavazzi A Pavan V Dolo Bioavailability of VEGF in tumor-shed vesicles depends on vesicle burst induced by acidic pH Neoplasia 8 2006 96 103
20. D Millimaggi M Mari S D’Ascenzo E Carosa EA Jannini S Zucker G Carta A Pavan V Dolo Tumor vesicle-associated CD147 modulates the angiogenic capability of endothelial cells Neoplasia 9 2007 349 357
21. MM Mohamed BF Sloane Cysteine cathepsins: multifunctional enzymes in cancer Nat Rev Cancer 6 2006 764 765
22. C Jedeszko BF Sloane Cysteine cathepsins in human cancer Biol Chem 385 2004 1017 1027
23. PG Cavanaugh BF Sloane AS Bajkowski GJ Gasic TB Gasic KV Honn Involvement of a cathepsin B-like cysteine proteinase in platelet aggregation induced by tumor cells and their shed membrane vesicles Clin Exp Metastasis 1 1983 297 307
24. S Roshy BF Sloane K Moin Pericellular cathepsin B and malignant progression Cancer Metastasis Rev 22 2003 271 286
25. BF Sloane K Moin M Sameni LR Tait J Rozhin G Ziegler Membrane association of cathepsin B can be induced by transfection of human breast epithelial cells with c-Ha- ras oncogene J Cell Sci 107 1994 373 384
26. AA Sinha MP Jamuar MJ Wilson J Rozhin BF Sloane Plasma membrane association of cathepsin B in human prostate cancer: biochemical and immunogold electron microscopic analysis Prostate 49 2001 172 184
27. M Schmitt F Jänicke H Graeff Tumor-associated proteases Fibrinolysis 6 1997 3 26
28. G Kostoulas A Lang H Nagase A Baici Stimulation of angiogenesis through cathepsin B inactivation of the tissue inhibitors of matrix metalloproteinases FEBS Lett 455 1999 286 290
29. M Sameni K Moin BF Sloane Imaging proteolysis by living human breast cancer cells Neoplasia 2 2000 496 504
30. A Premzl V Zavasnik-Bergant V Turk J Kos Intracellular and extracellular cathepsin B facilitate invasion of MCF-10A neoT cells through reconstituted extracellular matrix in vitro Exp Cell Res 283 2003 206 214
31. V Dolo A Ginestra S Violini S Miotti C Festuccia D Miceli M Migliavacca C Rinaudo FM Romano F Brisdelli Ultrastructural and phenotypic characterization of CABA I, a new human ovarian cancer cell line Oncol Res 9 1997 129 138
32. G Taraboletti D Roberts LA Liotta R Giavazzi Platelet thrombospondin modulates endothelial cell adhesion, motility, and growth: a potential angiogenesis regulatory factor J Cell Biol 111 1990 765 772
33. A Yamamoto T Hara K Tomoo T Ishida T Fujii Y Hata M Murata K Kitamura Binding mode of CA-074, a specific irreversible inhibitor, to bovine cathepsin B as determined by X-ray crystal analysis of the complex J Biochem 121 1997 974 977
34. M Montaser G Lalmanach L Mach CA-074, but not its methyl ester CA-074Me, is a selective inhibitor of cathepsin B within living cells Biol Chem 383 2002 1305 1308
35. Q Shi X Le B Wang JL Abbruzzese Q Xiong Y He K Xie Regulation of vascular endothelial growth factor expression by acidosis in human cancer cells Oncogene 20 2001 3751 3756
36. DP Dickinson Cysteine peptidases of mammals: their biological roles and potential effects in the oral cavity and other tissues in health and disease Crit Rev Oral Biol Med 13 2002 238 275
37. S Zucker JM Wieman RM Lysik DP Wilkie N Ramamurthy B Lane Metastatic mouse melanoma cells release collagen-gelatin degrading metalloproteinases as components of shed membrane vesicles Biochim Biophys Acta 924 1987 225 237
38. MP Lerner SW Lucid GJ Wen RE Nordquist Selected area membrane shedding by tumor cells Cancer Lett 20 1983 125 130
39. JW Kim E Wieckowski DD Taylor TE Reichert S Watkins TL Whiteside Fas ligand-positive membranous vesicles isolated from sera of patients with oral cancer induce apoptosis of activated T lymphocytes Clin Cancer Res 11 2005 1010 1020
40. RA Gatenby RJ Gillies Why do cancers have high aerobic glycolysis? Nat Rev Cancer 4 2004 891 899
41. RA Gatenby ET Gawlinski AF Gmitro B Kaylor RJ Gillies Acid-mediated tumor invasion: a multidisciplinary study Cancer Res 66 10 2006 5216 5223
42. BE Linebaugh M Sameni NA Day BF Sloane D Keppler Exocytosis of active cathepsin B enzyme at pH 7.0, inhibition and molecular mass Eur J Biochem 264 1999 100 109
43. MR Buck DG Karustis NA Day KV Honn BF Sloane Degradation of extracellular-matrix proteins by human cathepsin B from normal and tumor tissues Biochem J 282 1992 273 278
44. J Mai M Sameni T Mikkelsen BF Sloane Degradation of extracellular matrix protein tenascin-C by cathepsin B: an interaction involved in the progression of gliomas Biol Chem 383 2002 1407 1413
45. S Yan M Sameni BF Sloane Cathepsin B and human tumor progression Biol Chem 379 1998 113 123
46. J Rozman J Stojan R Kuhelj V Turk B Turk Autocatalytic processing of recombinant human procathepsin B is a bimolecular process FEBS Lett 459 1999 358 362