Lysosomal cathepsin B participates in the podosome-mediated extracellular matrix degradation and invasion via secreted lysosomes in v-Src fibroblasts

Cancer Research

Volumn 68, Issue 22, 2008, Pages 9147-9156

  Tu, Chun ^a,d,e,f   Ortega Cava, Cesar F ^a,d,e,f   Chen, Gengsheng ^d,e,f   Fernandes, Norvin D ^g   Cavallo Medved, Dora ^c   Sloane, Bonnie F ^c   Band, Vimla ^b,d,e,f   Band, Hamid ^a,b,d,e,f  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d EVANSTON NORTHWESTERN HEALTHCARE   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

^f NORTHWESTERN UNIVERSITY   (United States)

^g DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIUM CHLORIDE; BAFILOMYCIN A1; CATHEPSIN B; CHLOROQUINE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; SHORT HAIRPIN RNA;

ANIMAL CELL; ARTICLE; CANCER INVASION; CELL INVASION; CELL STRAIN 3T3; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; EXTRACELLULAR MATRIX; FIBROBLAST; LYSOSOME; MOUSE; NONHUMAN; PH; PODOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ACTINS; ANIMALS; CATHEPSIN B; CELL TRANSFORMATION, NEOPLASTIC; CELLULAR STRUCTURES; EXTRACELLULAR MATRIX; FIBROBLASTS; GELATIN; GENES, SRC; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MACROLIDES; MICE; NEOPLASM INVASIVENESS; NIH 3T3 CELLS;

EID: 56449113201     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-07-5127     Document Type: Article

References (50)

1. Linder S, Aepfelbacher M. Podosomes: adhesion hotspots of invasive cells. Trends Cell Biol 2003;13:376-85.
2. Chen WT. Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J Exp Zool 1989;251:167-85.
3. Nakahara H, Nomizu M, Akiyama SK, Yamada Y, Yeh Y, Chen WT. A mechanism for regulation of melanoma invasion. Ligation of α6β1 integrin by laminin G peptides. J Biol Chem 1996;271:27221-4.
4. Kelly T, Yan Y, Osborne RL, et al. Proteolysis of extracellular matrix by invadopodia facilitates human breast cancer cell invasion and is mediated by matrix metalloproteinases. Clin Exp Metastasis 1998;16:501-12.
5. Weaver AM. Invadopodia: specialized cell structures for cancer invasion. Clin Exp Metastasis 2006;23:97-105.
6. Gimona M, Buccione R. Adhesions that mediate invasion. Int J Biochem Cell Biol 2006;38:1875-92.
7. Linder S. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol 2007;17:107-17.
8. Linder S, Nelson D, Weiss M, Aepfelbacher M. Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc Natl Acad Sci U S A 1999;96:9648-53.
9. Berdeaux RL, Diaz B, Kim L, Martin GS. Active Rho is localized to podosomes induced by oncogenic Src and is required for their assembly and function. J Cell Biol 2004;166:317-23.
10. Tehrani S, Faccio R, Chandrasekar I, Ross FP, Cooper JA. Cortactin has an essential and specific role in osteoclast actin assembly. Mol Biol Cell 2006;17:2882-95.
11. Yamaguchi H, Lorenz M, Kempiak S, et al. Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J Cell Biol 2005;168:441-52.
12. Gatesman A, Walker VG, Baisden JM, Weed SA, Flynn DC. Protein kinase Cα activates c-Src and induces podosome formation via AFAP-110. Mol Cell Biol 2004;24:7578-97.
13. Seals DF, Azucena EF, Jr., Pass I, et al. The adaptor protein Tks5/Fish is required for podosome formation and function, and for the protease-driven invasion of cancer cells. Cancer Cell 2005;7:155-65.
14. Freije JM, Balbin M, Pendas AM, Sánchez LM, Puente XS, López-Otín C. Matrix metalloproteinases and tumor progression. Adv Exp Med Biol 2003;532:91-107.
15. Bauvois B. Transmembrane proteases in cell growth and invasion: new contributors to angiogenesis? Oncogene 2004;23:317-29.
16. Joyce JA, Hanahan D. Multiple roles for cysteine cathepsins in cancer. Cell Cycle 2004;3:1516-619.
17. Mohamed MM, Sloane BF. Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer 2006;6:764-75.
18. Jedeszko C, Sloane BF. Cysteine cathepsins in human cancer. Biol Chem 2004;385:1017-27.
19. Gocheva V, Zeng W, Ke D, et al. Distinct roles for cysteine cathepsin genes in multistage tumorigenesis. Genes Dev 2006;20:543-56.
20. Monsky WL, Kelly T, Lin CY, et al. Binding and localization of M(r) 72,000 matrix metalloproteinase at cell surface invadopodia. Cancer Res 1993;53:3159-64.
21. Nakahara H, Howard L, Thompson EW, et al. Transmembrane/cytoplasmic domain-mediated membrane type 1-matrix metalloprotease docking to invadopodia is required for cell invasion. Proc Natl Acad Sci U S A 1997;94:7959-64.
22. Monsky WL, Lin CY, Aoyama A, et al. A potential marker protease of invasiveness, seprase, is localized on invadopodia of human malignant melanoma cells. Cancer Res 1994;54:5702-10.
23. Ghersi G, Zhao Q, Salamone M, Yeh Y, Zucker S, Chen WT. The protease complex consisting of dipeptidyl peptidase IV and seprase plays a role in the migration and invasion of human endothelial cells in collagenous matrices. Cancer Res 2006;66:4652-61.
24. Artym VV, Kindzelskii AL, Chen WT, Petty HR. Molecular proximity of seprase and the urokinase-type plasminogen activator receptor on malignant melanoma cell membranes: dependence on β1 integrins and the cytoskeleton. Carcinogenesis 2002;23:1593-601.
25. Saftig P, Hunziker E, Wehmeyer O, et al. Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc Natl Acad Sci U S A 1998;95:13453-8.
26. Zhao H, Laitala-Leinonen T, Parikka V, Vaananen HK. Downregulation of small GTPase Rab7 impairs osteoclast polarization and bone resorption. J Biol Chem 2001;276:39295-302.
27. Zhao H, Ettala O, Vaananen HK. Intracellular membrane trafficking pathways in bone-resorbing osteoclasts revealed by cloning and subcellular localization studies of small GTP-binding rab proteins. Biochem Biophys Res Commun 2002;293:1060-5.
28. Mulari MT, Zhao H, Lakkakorpi PT, Vaananen HK. Osteoclast ruffled border has distinct subdomains for secretion and degraded matrix uptake. Traffic 2003;4:113-25.
29. Blair HC, Teitelbaum SL, Ghiselli R, Gluck S. Osteoclastic bone resorption by a polarized vacuolar proton pump. Science 1989;245:855-7.
30. Carreno S, Gouze ME, Schaak S, Emorine LJ, Maridonneau-Parini I. Lack of palmitoylation redirects p59Hck from the plasma membrane to p61Hck-positive lysosomes. J Biol Chem 2000;275:36223-9.
31. Cougoule C, Carreno S, Castandet J, et al. Activation of the lysosome-associated p61Hck isoform triggers the biogenesis of podosomes. Traffic 2005;6:682-94.
32. Kasahara K, Nakayama Y, Kihara A, et al. Rapid trafficking of c-Src, a non-palmitoylated Src-family kinase, between the plasma membrane and late endosomes/ lysosomes. Exp Cell Res 2007;313:2651-66.
33. Moin K, Day NA, Sameni M, Hasnain S, Hirama T, Sloane BF. Human tumour cathepsin B. Comparison with normal liver cathepsin B. Biochem J 1992;285:427-34.
34. Oda K, Nishimura Y, Ikehara Y, Kato K. Bafilomycin A1 inhibits the targeting of lysosomal acid hydrolases in cultured hepatocytes. Biochem Biophys Res Commun 1991;178:369-77.
35. Mueller SC, Yeh Y, Chen WT. Tyrosine phosphorylation of membrane proteins mediates cellular invasion by transformed cells. J Cell Biol 1992;119:1309-25.
36. Lorenzo K, Ton P, Clark JL, Coulibaly S, Mach L. Invasive properties of murine squamous carcinoma cells: secretion of matrix-degrading cathepsins is attributable to a deficiency in the mannose 6-phosphate/ insulin-like growth factor II receptor. Cancer Res 2000;60:4070-6.
37. Coopman P, Do M, Thompson E, Mueller SC. H Phagocytosis of cross-linked gelatin matrix by human breast carcinoma cells correlates with their invasive capacity. Clin Cancer ReHs 1998;4:507-15.
38. Yoshimori T, Yamamoto A, Moriyama Y, Futai M, Tashiro Y. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem 1991;266:17707-12.
39. Tapper H, Sundler R. Bafilomycin A1 inhibits lysosomal, phagosomal, and plasma membrane H(+)-ATPase and induces lysosomal enzyme secretion in macrophages. J Cell Physiol 1995;163:137-44.
40. Buck MR, Karustis DG, Day NA, Honn KV, Sloane BF. Degradation of extracellular-matrix proteins by human cathepsin B from normal and tumour tissues. Biochem J 1992;282:273-78.
41. Kobayashi H, Schmitt M, Goretzki L, et al. Cathepsin B efficiently activates the soluble and the tumor cell receptor-bound form of the proenzyme urokinase-type plasminogen activator (Pro-uPA). J Biol Chem 1991;266:5147-52.
42. Guo M, Mathieu PA, Linebaugh B, Sloane BF, Reiners JJ, Jr. Phorbol ester activation of a proteolytic cascade capable of activating latent transforming growth factor-αL a process initiated by the exocytosis of cathepsin B. J Biol Chem 2002;277:14829-37.
43. Kostoulas G, Lang A, Nagase H, Baici A. Stimulation of angiogenesis through cathepsin B inactivation of the tissue inhibitors of matrix metalloproteinases. FEBS Lett 1999;455:286-90.
44. Dalet-Fumeron V, Guinec N, Pagano M. In vitro activation of pro-cathepsin B by three serine proteinases: leucocyte elastase, cathepsin G, and the urokinase-type plasminogen activator. FEBS Lett 1993;332:251-4.
45. Cardone RA, Casavola V, Reshkin SJ. The role of disturbed pH dynamics and the Na+/H+ exchanger in metastasis. Nat Rev Cancer 2005;5:786-95.
46. Rofstad EK, Mathiesen B, Kindem K, Galappathi K. Acidic extracellular pH promotes experimental metastasis of human melanoma cells in athymic nude mice. Cancer Res 2006;66:6699-707.
47. Glunde K, Guggino SE, Solaiyappan M, Pathak AP, Ichikawa Y, Bhujwalla ZM. Extracellular acidification alters lysosomal trafficking in human breast cancer cells. Neoplasia 2003;5:533-45.
48. Rozhin J, Sameni M, Ziegler G, Sloane BF. Pericellular pH affects distribution and secretion of cathepsin B in malignant cells. Cancer Res 1994;54:6517-25.
49. Kim M, Tezuka T, Tanaka K, Yamamoto T. Cbl-c suppresses v-Src-induced transformation through ubiquitin-dependent protein degradation. Oncogene 2004;23:1645-55. Erratum in: Oncogene 2004;23:7903-4.
50. Vincent C, Maridonneau-Parini I, Le Clainche C, Gounon P, Labrousse A. Activation of p61Hck triggers WASp- and Arp2/3-dependent actin-comet tail biogenesis and accelerates lysosomes. J Biol Chem 2007;282:19565-74.