Three-dimensional cultures modeling premalignant progression of human breast epithelial cells: Role of cysteine cathepsins

Biological Chemistry

Volumn 393, Issue 12, 2012, Pages 1405-1416

  Mullins, Stefanie R ^a   Sameni, Mansoureh ^a   Blum, Galia ^b   Bogyo, Matthew ^b   Sloane, Bonnie F ^a   Moin, Kamiar ^a  

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

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Activity based probes; Breast cancer; Cysteine cathepsins; Premalignant progression; Protease inhibitors

Indexed keywords

CATHEPSIN B; CATHEPSIN L;

APOPTOSIS; BREAST EPITHELIUM; BREAST HYPERPLASIA; CELL PROLIFERATION; CELL STRUCTURE; CONFERENCE PAPER; CULTURE TECHNIQUE; HUMAN; HUMAN CELL; PRECANCER; PRIORITY JOURNAL; THREE DIMENSIONAL RECONSTITUTED BASEMENT MEMBRANE OVERLAY CULTURE;

APOPTOSIS; BREAST; BREAST NEOPLASMS; CATHEPSIN B; CATHEPSIN L; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; CYSTEINE PROTEINASE INHIBITORS; DIPEPTIDES; DISEASE PROGRESSION; EPITHELIAL CELLS; FEMALE; HUMANS; LEUCINE; MODELS, BIOLOGICAL;

MOUSE MAMMARY TUMOR VIRUS; MURINAE; MUS;

EID: 84869389974     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2012-0252     Document Type: Conference Paper

References (53)

1. Abbenante, G. and Fairlie, D.P. (2005). Protease inhibitors in the clinic. Med. Chem. 1, 71-104.
2. Alencar, H., Funovics, M.A., Figueiredo, J., Sawaya, H., Weissleder, R., and Mahmood, U. (2007). Colonic adenocarcinomas: near-infrared microcatheter imaging of smart probes for early detection-study in mice. Radiology 244, 232-238.
3. Alley, M.C., Scudiero, D.A., Monks, A., Hursey, M.L., Czerwinski, M.J., Fine, D.L., Abbott, B.J., Mayo, J.G., Shoemaker, R.H., and Boyd, M.R. (1988). Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Res. 48, 589-601.
4. Basolo, F., Elliott, J., Tait, L., Chen, X.Q., Maloney, T., Russo, I.H., Pauley, R., Momiki, S., Caamano, J., Klein-Szanto, A.J. et al. (1991). Transformation of human breast epithelial cells by c-Ha-ras oncogene. Mol. Carcinog. 4, 25-35.
5. Benavides, F., Perez, C., Blando, J., Contreras, O., Shen, J., Coussen, L.M., Fischer, S.M., Kusewitt, D.F., Digiovanni, J. and Conti, C.J. (2011). Protective role of cathepsin L in mouse skin carcinogenesis. Mol. Carcinog. 51, 352-361.
6. Blum, G., Mullins, S.R., Keren, K., Fonovic, M., Jedeszko, C., Rice, M.J., Sloane, B.F. and Bogyo, M. (2005). Dynamic imaging of protease activity with fluorescently quenched activity-based probes. Nat. Chem. Biol. 1, 203-209.
7. Bervar, A., Zajc, I., Sever, N., Katunuma, N., Sloane, B.F., and Lah, T.T. (2003). Invasiveness of transformed human breast epithelial cell lines is related to cathepsin B and inhibited by cysteine proteinase inhibitors. Biol. Chem. 384, 447-455.
8. Chen, J., Tung, C.H., Mahmood, U., Ntziachristos, V., Gyurko, R., Fishman, M.C., Huang, P. L., and Weissleder, R. (2002). In vivo imaging of proteolytic activity in atherosclerosis. Circulation 105, 2766-2771.
9. Dawson, P.J., Wolman, S.R., Tait, L., Heppner, G.H., and Miller, F.R. (1996). MCF10AT: a model for the evolution of cancer from proliferative breast disease. Am. J. Pathol. 148, 313-319.
10. Debnath, J. and Brugge, J.S. (2005). Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer. 5, 675-688.
11. Debnath, J., Muthuswamy, S.K., and Brugge, J.S. (2003). Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256-268.
12. Dennem ärker, J., Lohmüller, T., Mayerle, J., Tacke, M., Lerch, M.M., Coussens, L.M., and Peters, C., Reinheckel, T. (2010). Deficiency for the cysteine protease cathepsin L promotes tumor progression in mouse epidermis. Oncogene 29, 1611-21.
13. Felbor, U., Kessler, B., Mothes, W., Goebel, H.H., Ploegh, H.L., Bronson, R.T., and Olsen, B.R. (2002). Neuronal loss and brain atrophy in mice lacking cathepsins B and L. Proc. Natl. Acad. Sci. USA 99, 7883-7888.
14. Gocheva, V., Zeng, W., Ke, D., Klimstra, D., Reinheckel, T., Peters, C., Hanahan, D., and Joyce, J.A. (2006). Distinct roles for cysteine cathepsin genes in multistage tumorigenesis. Genes Dev. 20, 543-556.
15. Gopinathan, A., Denicola, G.M., Frese, K.K., Cook, N., Karreth, F.A., Mayerle, J., Lerch, M.M., Reinheckel, T., and Tuveson D.A. (2012). Cathepsin B promotes the progression of pancreatic ductal adenocarcinoma in mice. Gut 61, 77-84.
16. Guicciardi, M.E., Miyoshi, H., Bronk, S.F., and Gores, G.J. (2001). Cathepsin B knockout mice are resistant to tumor necrosis factor-alpha-mediated hepatocyte apoptosis and liver injury: implications for therapeutic applications. Am. J. Pathol. 159, 2045-2054.
17. Halangk, W., Lerch, M.M., Brandt-Nedelev, B., Roth, W., Ruthenbuerger, M., Reinheckel, T., Domschke, W., Lippert, H., Peters, C., and Deussing, J. (2000). Role of cathepsin B in intracellular trypsinogen activation and the onset of acute pancreatitis. J. Clin. Invest. 106, 773-781.
18. Joyce, J.A., Baruch, A., Chehade, K., Meyer-Morse, N., Giraudo, E., Tsai, F. Y., Greenbaum, D.C., Hager, J.H., Bogyo, M., and Hanahan, D. (2004). Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis. Cancer Cell 5, 443-453.
19. Khokha, R. and Werb Z. (2011). Mammary gland reprogramming: metalloproteinases couple form with function. Cold Spring Harb. Perspect. Biol. 3, 4.
20. Kleifeld, O., Kotra, L.P., Gervasi, D.C., Brown, S., Bernardo, M.M., Fridman, R., Mobashery, S., and Sagi, I. (2001). X-ray absorption studies of human matrix metalloproteinase-2 (MMP-2) bound to a highly selective mechanism-based inhibitor. Comparison with the latent and active forms of the enzyme. J. Biol. Chem. 276, 17125-17131.
21. Korkola, J.E., DeVries, S., Fridlyand, J., Hwang, E.S., Estep, A.L., Chen, Y.Y., Chew, K.L., Dairkee, S.H., Jensen, R.M., and Waldman, F.M. (2003). Differentiation of lobular versus ductal breast carcinomas by expression microarray analysis. Cancer Res. 63, 7167-7175.
22. Kroemer, G. and Jaattela, M. (2005). Lysosomes and autophagy in cell death control. Nat. Rev. Cancer 5, 886-897.
23. Li, Q., Mullins, S.R., Sloane, B.F., and Mattingly, R.R. (2008). p21-Activated kinase 1 coordinates aberrant cell survival and pericellular proteolysis in a three-dimensional culture model for premalignant progression of human breast cancer. Neoplasia 10, 314-329.
24. Li, Q., Chow, A.B., and Mattingly, R.R. (2010). Three-dimensional overlay culture models of human breast cancer reveal a critical sensitivity to mitogen-activated protein kinase kinase inhibitors. J. Pharmacol. Exp. Ther. 332, 821-828.
25. Liu, J., Sukhova, G.K., Yang, J.T., Sun, J., Ma, L., Ren, A., Xu, W.H., Fu, H., Dolganov, G.M., Hu, C. et al. (2006a). Cathepsin L expression and regulation in human abdominal aortic aneurysm, atherosclerosis, and vascular cells. Atherosclerosis 184, 302-311.
26. Liu, J., Ma, L., Yang, J., Ren, A., Sun, Z., Yan, G., Sun, J., Fu, H., Xu, W., Hu, C. et al. (2006b). Increased serum cathepsin S in patients with atherosclerosis and diabetes. Atherosclerosis 186, 411-419.
27. Lo, A.T., Mori, H., Mott, J. and Bissell, M.J. (2012). Constructing three-dimensional models to study mammary gland branching morphogenesis and functional differentiation. J. Mammary Gland. Biol. Neoplasia. 17, 103-10.
28. Lutgens, S.P., Cleutjens, K.B., Daemen, M.J., and Heeneman, S. (2007). Cathepsin cysteine proteases in cardiovascular disease. Faseb J. 21, 3029-3041.
29. Martin, K.J., Patrick, D.R., Bissell, M.J., and Fournier, M.V. (2008). Prognostic breast cancer signature identified from 3D culture model accurately predicts clinical outcome across independent datasets. PLoS One 3, 1-9.
30. McGowan, E.B., Becker, E., and Detwiler, T.C. (1989). Inhibition of calpain in intact platelets by the thiol protease inhibitor E-64d. Biochem. Biophys. Res. Commun. 158, 432-435.
31. Miller, F.R., Soule, H.D., Tait, L., Pauley, R.J., Wolman, S.R., Dawson, P.J., and Heppner, G. H. (1993). Xenograft model of progressive human proliferative breast disease. J. Natl. Cancer Inst. 85, 1725-1732.
32. Mohamed, M.M. and Sloane, B.F. (2006). Cysteine cathepsins: multifunctional enzymes in cancer. Nat. Rev. Cancer. 6, 764-775.
33. Moin, K., Day, N.A., Sameni, M., Hasnain, S., Hirama, T., and Sloane, B.F. (1992). Human tumour cathepsin B. Comparison with normal liver cathepsin B. Biochem. J. 285, 427-434.
34. Montaser, M., Lalmanach, G., and Mach, L. (2002). CA-074, but not its methyl ester CA-074Me, is a selective inhibitor of cathepsin B within living cells. Biol. Chem. 383, 1305-1308.
35. Nedvetsky, P.I., Kwon, S.H., Debnath, J., and Mostov, K.E. (2012). cAMP regulates formation of mammary epithelial acini in vitro. Mol. Biol. Cell. 23, 2973-2980. 2012 Jun 6. [Epub ahead of print].
36. Obermajer, N., Jevnikar, Z., Doljak, B., and Kos, J. (2008). Role of cysteine cathepsins in matrix degradation and cell signalling. Connect Tissue Res. 49, 193-196.
37. Premzl, A., Puizdar, V., Zavasnik-Bergant, V., Kopitar-Jerala, N., Lah, T.T., Katunuma, N., Sloane, B.F., Turk, V., and Kos, J. (2001). Invasion of ras-transformed breast epithelial cells depends on the proteolytic activity of cysteine and aspartic proteinases. Biol. Chem. 382, 853-857.
38. Reinheckel, T., Hagemann, S., Dollwet-Mack, S., Martinez, E., Lohmuller, T., Zlatkovic, G., Tobin, D.J., Maas-Szabowski, N., and Peters, C. (2005). The lysosomal cysteine protease cathepsin L regulates keratinocyte proliferation by control of growth factor recycling. J Cell Sci. 118, 3387-3395.
39. Reiser, J., Adair, B., and Reinheckel, T. (2010). Specialized roles for cysteine cathepsins in health and disease. J. Clin. Invest. 120, 3421-3431.
40. Repnik, U., Stoka, V., Turk, V., and Turk, B. (2012). Lysosomes and lysosomal cathepsins in cell death. Biochim. Biophys. Acta 1824, 22-23.
41. Sameni, M., Mullins, S.R., Moin, K., Sloane, B.F., and Osuala, K. (2012). Modeling breast cancer progression in 4D. In: Breast Cancer Metastasis and Drug Resistance: Challenges and Progress, A. Ahmad, ed. (Springer, New York, in press).
42. Sevenich, L., Werner, F., Gajda, M., Schurigt, U., Sieber, C., Müller, S., Follo, M., Peters, C., and Reinheckel, T. (2011). Transgenic expression of human cathepsin B promotes progression and metastasis of polyoma-middle-T-induced breast cancer in mice. Oncogene 30, 54-6 4.
43. Seyfried, D.M., Veyna, R., Han, Y., Li, K., Tang, N., Betts, R.L., Weinsheimer, S., Chopp, M., and Anagli, J. (2001). A selective cysteine protease inhibitor is non-toxic and cerebroprotective in rats undergoing transient middle cerebral artery ischemia. Brain Res. 901, 94-101.
44. Sloane, B.F. (2012). On How Mammary Gland Reprogramming Metalloproteinases Couple Form with Function. Cold Spring Harb. Perspect. Biol. 4, p. 7.
45. Turk, V., Stoka, V., Vasiljeva, O., Renko, M., Sun, T., Turk, B., and Turk, D. (2012). Cysteine cathepsins: from structure, function and regulation to new frontiers. Biochim. Biophys. Acta. 1824, 68-88.
46. Vasiljeva, O., Papazoglou, A., Kruger, A., Brodoefel, H., Korovin, M., Deussing, J., Augustin, N., Nielsen, B.S., Almholt, K., Bogyo, M., et al. (2006). Tumor cell-derived and macrophage-derived cathepsin B promotes progression and lung metastasis of mammary cancer. Cancer Res. 66, 5242-5250.
47. Vasiljeva, O., Korovin, M., Gajda, M., Brodoefel, H., Bojic, L., Kruger, A., Schurigt, U., Sevenich, L., Turk, B., Peters, C., et al. (2008). Reduced tumour cell proliferation and delayed development of high-grade mammary carcinomas in cathepsin B-deficient mice. Oncogene 27, 4191-4199.
48. Wang, B., Sun, J., Kitamoto, S., Yang, M., Grubb, A., Chapman, H.A., Kalluri, R., and Shi, G.P. (2006). Cathepsin S controls angiogenesis and tumor growth via matrix-derived angiogenic factors. J. Biol. Chem. 281, 6020-6029.
49. Watson, C.J. and Kreuzaler, P.A. (2009). The role of cathepsins in involution and breast cancer. J. Mammary Gland Biol. Neoplasia 14, 171-179.
50. Wilcox, D. and Mason, R.W. (1992). Inhibition of cysteine proteinases in lysosomes and whole cells. Biochem. J. 285, 495-502.
51. Wulfkuhle, J.D., Sgroi, D.C., Krutzsch, H., McLean, K., McGarvey, K., Knowlton, M., Chen, S., Shu, H., Sahin, A., Kurek, R., et al. (2002). Proteomics of human breast ductal carcinoma in situ. Cancer Res. 62, 6740-6749.
52. Yasuda, Y., Kaleta, J., and Bromme, D. (2005). The role of cathepsins in osteoporosis and arthritis: rationale for the design of new therapeutics. Adv. Drug Deliv. Rev. 57, 973-993.
53. Zajc, I., Sever, N., Bervar, A., and Lah, T.T. (2002). Expression of cysteine peptidase cathepsin L and its inhibitors stefins A and B in relation to tumorigenicity of breast cancer cell lines. Cancer Lett. 187, 185-190.