Proteolysis of cystatin C by cathepsin D in the breast cancer microenvironment

FASEB Journal

Volumn 26, Issue 12, 2012, Pages 5172-5181

  Laurent Matha, Valérie ^a,b   Huesgen, Pitter F ^c   Masson, Olivier ^a,b   Derocq, Danielle ^a,b   Prébois, Christine ^a,b   Gary Bobo, Magali ^a,b   Lecaille, Fabien ^d   Rebière, Bertrand ^e   Meurice, Guillaume ^f   Oréar, Cédric ^f   Hollingsworth, Robert E ^g   Abrahamson, Magnus ^h   Lalmanach, Gilles ^d   Overall, Christopher M ^c   Liaudet Coopman, Emmanuelle ^a,b  

^a INSERM   (France)

^b CENTRE VAL D AURELLE   (France)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d UNIVERSITÉ DE TOURS   (France)

^e CNRS   (France)

^f INSTITUT GUSTAVE ROUSSY   (France)

^g MEDIMMUNE   (United States)

^h LUND UNIVERSITY   (Sweden)

Author keywords

Cancer; Protease web

Indexed keywords

CATHEPSIN D; CYSTATIN C; DECAY ACCELERATING FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER GROWTH; CELL PH; EMBRYO; EXTRACELLULAR MATRIX; FIBROBLAST; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN SECRETION; TUMOR MICROENVIRONMENT;

AMINO ACID SEQUENCE; ANIMALS; BREAST NEOPLASMS; CATHEPSIN D; CELLS, CULTURED; CYSTATIN C; EMBRYO, MAMMALIAN; ENZYME PRECURSORS; EXTRACELLULAR SPACE; FEMALE; FIBROBLASTS; HUMANS; HYDROGEN-ION CONCENTRATION; IMMUNOBLOTTING; MCF-7 CELLS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEOLYSIS; RNA INTERFERENCE; TUMOR MICROENVIRONMENT; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84870332620     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-205229     Document Type: Article

References (44)

1. Vignon, F., Capony, F., Chambon, M., Freiss, G., Garcia, M., and Rochefort, H. (1986) Autocrine growth stimulation of the MCF 7 breast cancer cells by the estrogen-regulated 52 K protein. Endocrinology 118, 1537-1545 (Pubitemid 16078532)
2. Capony, F., Rougeot, C., Montcourrier, P., Cavailles, V., Salazar, G., and Rochefort, H. (1989) Increased secretion, altered processing, and glycosylation of pro-cathepsin D in human mammary cancer cells. Cancer Res. 49, 3904-3909 (Pubitemid 19197419)
3. Foekens, J. A., Look, M. P., Bolt-de Vries, J., Meijer-van Gelder, M. E., van Putten, W. L., and Klijn, J. G. (1999) Cathepsin-D in primary breast cancer: prognostic evaluation involving 2810 patients. Br. J. Cancer 79, 300-307 (Pubitemid 29002300)
4. Ferrandina, G., Scambia, G., Bardelli, F., Benedetti Panici, P., Mancuso, S., and Messori, A. (1997) Relationship between cathepsin-D content and disease-free survival in node-negative breast cancer patients: a meta-analysis. Br. J. Cancer 76, 661-666 (Pubitemid 27354682)
5. Berchem, G., Glondu, M., Gleizes, M., Brouillet, J. P., Vignon, F., Garcia, M., and Liaudet-Coopman, E. (2002) Cathepsin-D affects multiple tumor progression steps in vivo: proliferation, angiogenesis and apoptosis. Oncogene 21, 5951-5955 (Pubitemid 35007248)
6. Glondu, M., Coopman, P., Laurent-Matha, V., Garcia, M., Rochefort, H., and Liaudet-Coopman, E. (2001) A mutated cathepsin-D devoid of its catalytic activity stimulates the growth of cancer cells. Oncogene 20, 6920-6929 (Pubitemid 33052181)
7. Laurent-Matha, V., Maruani-Herrmann, S., Prebois, C., Beaujouin, M., Glondu, M., Noel, A., Alvarez-Gonzalez, M. L., Blacher, S., Coopman, P., Baghdiguian, S., Gilles, C., Loncarek, J., Freiss, G., Vignon, F., and Liaudet-Coopman, E. (2005) Catalytically inactive human cathepsin D triggers fibroblast invasive growth. J. Cell Biol. 168, 489-499 (Pubitemid 40205070)
8. Beaujouin, M., Prebois, C., Derocq, D., Laurent-Matha, V., Masson, O., Pattingre, S., Coopman, P., Bettache, N., Grossfield, J., Hollingsworth, R. E., Zhang, H., Yao, Z., Hyman, B. T., van der Geer, P., Smith, G. K., and Liaudet-Coopman, E. (2010) Pro-cathepsin D interacts with the extracellular domain of the beta chain of LRP1 and promotes LRP1-dependent fibroblast outgrowth. J. Cell Sci. 123, 3336-3346
9. Hu, L., Roth, J. M., Brooks, P., Luty, J., and Karpatkin, S. (2008) Thrombin up-regulates cathepsin D which enhances angiogenesis, growth, and metastasis. Cancer Res. 68, 4666-4673
10. Glondu, M., Liaudet-Coopman, E., Derocq, D., Platet, N., Rochefort, H., and Garcia, M. (2002) Down-regulation of cathepsin-D expression by antisense gene transfer inhibits tumor growth and experimental lung metastasis of human breast cancer cells. Oncogene 21, 5127-5134
11. Hasilik, A., von Figura, K., Conzelmann, E., Nehrkorn, H., and Sandhoff, K. (1982) Lysosomal enzyme precursors in human fibroblasts. Activation of cathepsin D precursor in vitro and activity of beta-hexosaminidase A precursor towards ganglioside GM2. Eur. J. Biochem. 125, 317-321 (Pubitemid 12047906)
12. Stubbs, M., McSheehy, P. M., Griffiths, J. R., and Bashford, C. L. (2000) Causes and consequences of tumour acidity and implications for treatment. Mol. Med. Today 6, 15-19 (Pubitemid 30010232)
13. Schornack, P. A., and Gillies, R. J. (2003) Contributions of cell metabolism and H+ diffusion to the acidic pH of tumors. Neoplasia 5, 135-145
14. Griffiths, J. R., McIntyre, D. J., Howe, F. A., and Stubbs, M. (2001) Why are cancers acidic? A carrier-mediated diffusion model for H+ transport in the interstitial fluid. Novartis Found. Symp. 240, 46-62; discussion 62-67, 152-153
15. Mohamed, M. M., and Sloane, B. F. (2006) Cysteine cathepsins: multifunctional enzymes in cancer. Nat. Rev. Cancer 6, 764-775 (Pubitemid 44450465)
16. Wallin, H., Bjarnadottir, M., Vogel, L. K., Wasselius, J., Ekstrom, U., and Abrahamson, M. (2010) Cystatins- extra- and intracel- lular cysteine protease inhibitors: high-level secretion and uptake of cystatin C in human neuroblastoma cells. Biochimie (Paris) 92, 1625-1634
17. Mason, S. D., and Joyce, J. A. (2011) Proteolytic networks in cancer. Trends Cell Biol. 21, 228-237
18. Overall, C. M., and Dean, R. A. (2006) Degradomics: systems biology of the protease web. Pleiotropic roles of MMPs in cancer. Cancer Metastasis Rev. 25, 69-75 (Pubitemid 43723983)
19. Kleifeld, O., Doucet, A., auf dem Keller, U., Prudova, A., Schilling, O., Kainthan, R. K., Starr, A. E., Foster, L. J., Kizhakkedathu, J. N., and Overall, C. M. (2010) Isotopic labeling of terminal amines in complex samples identifies protein N-termini and protease cleavage products. Nat. Biotechnol. 28, 281-288
20. Kleifeld, O., Doucet, A., Prudova, A., Auf dem Keller, U., Gioia, M., Kizhakkedathu, J. N., and Overall, C. M. (2011) Identifying and quantifying proteolytic events and the natural N terminome by terminal amine isotopic labeling of substrates. Nat. Protoc. 6, 1578-1611
21. Craig, R., and Beavis, R. C. (2004) TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20, 1466-1467 (Pubitemid 38931421)
22. Auf dem Keller, U., Prudova, A., Gioia, M., Butler, G. S., and Overall, C. M. (2010) A statistics-based platform for quantitative N-terminome analysis and identification of protease cleavage products. Mol. Cell. Proteomics 9, 912-927
23. Watabe, S., and Yago, N. (1983) Phospholipids activate cathepsin D. Biochem. Biophys. Res. Commun. 110, 934-939 (Pubitemid 13146733)
24. Tholen, S., Biniossek, M. L., Gessler, A. L., Muller, S., Weisser, J., Kizhakkedathu, J. N., Reinheckel, T., and Schilling, O. (2011) Contribution of cathepsin L to secretome composition and cleavage pattern of mouse embryonic fibroblasts. Biol. Chem. 392, 961-971
25. Lenarcic, B., Krasovec, M., Ritonja, A., Olafsson, I., and Turk, V. (1991) Inactivation of human cystatin C and kininogen by human cathepsin D. FEBS Lett. 280, 211-215
26. Kopitz, C., Anton, M., Gansbacher, B., and Kruger, A. (2005) Reduction of experimental human fibrosarcoma lung metastasis in mice by adenovirus-mediated cystatin C overexpression in the host. Cancer Res. 65, 8608-8612 (Pubitemid 41377344)
27. Huh, C. G., Hakansson, K., Nathanson, C. M., Thorgeirsson, U. P., Jonsson, N., Grubb, A., Abrahamson, M., and Karlsson, S. (1999) Decreased metastatic spread in mice homozygous for a null allele of the cystatin C protease inhibitor gene. Mol. Pathol. 52, 332-340 (Pubitemid 30002765)
28. Wegiel, B., Jiborn, T., Abrahamson, M., Helczynski, L., Otterbein, L., Persson, J. L., and Bjartell, A. (2009) Cystatin C is downregulated in prostate cancer and modulates invasion of prostate cancer cells via MAPK/Erk and androgen receptor pathways. PLoS One 4, e7953
29. Bell-McGuinn, K. M., Garfall, A. L., Bogyo, M., Hanahan, D., and Joyce, J. A. (2007) Inhibition of cysteine cathepsin protease activity enhances chemotherapy regimens by decreasing tumor growth and invasiveness in a mouse model of multistage cancer. Cancer Res. 67, 7378-7385 (Pubitemid 47206568)
30. Abboud-Jarrous, G., Atzmon, R., Peretz, T., Palermo, C., Gadea, B. B., Joyce, J. A., and Vlodavsky, I. (2008) Cathepsin L is responsible for processing and activation of proheparanase through multiple cleavages of a linker segment. J. Biol. Chem. 283, 18167-18176
31. Turk, B. (2006) Targeting proteases: successes, failures and future prospects. Nat. Rev. Drug Discov. 5, 785-799
32. Turk, V., Kos, J., and Turk, B. (2004) Cysteine cathepsins (proteases)-on the main stage of cancer? Cancer Cell 5, 409-410 (Pubitemid 38610242)
33. Dean, R. A., and Overall, C. M. (2007) Proteomics discovery of metalloproteinase substrates in the cellular context by iTRAQ labeling reveals a diverse MMP-2 substrate degradome. Mol. Cell. Proteomics 6, 611-623 (Pubitemid 46630094)
34. Derocq, D., Prebois, C., Beaujouin, M., Laurent-Matha, V., Pattingre, S., Smith, G. K., and Liaudet-Coopman, E. (2012) Cathepsin D is partly endocytosed by the LRP1 receptor and inhibits LRP1-regulated intramembrane proteolysis. Oncogene 31, 3202-3212
35. Laurent-Matha, V., Lucas, A., Huttler, S., Sandhoff, K., Garcia, M., and Rochefort, H. (2002) Procathepsin D interacts with prosaposin in cancer cells but its internalization is not mediated by LDL receptor-related protein. Exp. Cell Res. 277, 210-219 (Pubitemid 34757102)
36. Dean, R. A., Butler, G. S., Hamma-Kourbali, Y., Delbe, J., Brigstock, D. R., Courty, J., and Overall, C. M. (2007) Identification of candidate angiogenic inhibitors processed by matrix metalloproteinase 2 (MMP-2) in cell-based proteomic screens: disruption of vascular endothelial growth factor (VEGF)/heparin affin regulatory peptide (pleiotrophin) and VEGF/connective tissue growth factor angiogenic inhibitory complexes by MMP-2 proteolysis. Mol. Cell. Biol. 27, 8454-8465
37. Dunn, B. M., and Hung, S. (2000) The two sides of enzymesubstrate specificity: lessons from the aspartic proteinases. Biochim. Biophys. Acta 1477, 231-240 (Pubitemid 30119903)
38. Lenarcic, B., Kos, J., Dolenc, I., Lucovnik, P., Krizaj, I., and Turk, V. (1988) Cathepsin D inactivates cysteine proteinase inhibitors, cystatins. Biochem. Biophys. Res. Commun. 154, 765-772
39. Griffiths, J. R. (1991) Are cancer cells acidic? Br. J. Cancer 64, 425-427
40. Martino, S., Tiribuzi, R., Ciraci, E., Makrypidi, G., D'Angelo, F., di Girolamo, I., Gritti, A., de Angelis, G. M., Papaccio, G., Sampaolesi, M., Berardi, A. C., Datti, A., and Orlacchio, A. (2011) Coordinated involvement of cathepsins S, D and cystatin C in the commitment of hematopoietic stem cells to dendritic cells. Int. J. Biochem. Cell Biol. 43, 775-783
41. Van der Stappen, J. W., Williams, A. C., Maciewicz, R. A., and Paraskeva, C. (1996) Activation of cathepsin B, secreted by a colorectal cancer cell line requires low pH and is mediated by cathepsin D. Int. J. Cancer 67, 547-554 (Pubitemid 26274113)
42. Gillet, L., Roger, S., Besson, P., Lecaille, F., Gore, J., Bougnoux, P., Lalmanach, G., and Le Guennec, J. Y. (2009) Voltage-gated sodium channel activity promotes cysteine cathepsin-dependent invasiveness and colony growth of human cancer cells. J. Biol. Chem. 284, 8680-8691
43. Jelassi, B., Chantome, A., Alcaraz-Perez, F., Baroja-Mazo, A., Cayuela, M. L., Pelegrin, P., Surprenant, A., and Roger, S. (2011) P2X(7) receptor activation enhances SK3 channels- and cystein cathepsin-dependent cancer cells invasiveness. Oncogene 30, 2108-2122
44. Brisson, L., Gillet, L., Calaghan, S., Besson, P., Le Guennec, J. Y., Roger, S., and Gore, J. (2011) Na(V)1.5 enhances breast cancer cell invasiveness by increasing NHE1-dependent H(+) efflux in caveolae. Oncogene 30, 2070-2076