Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter June 1, 2005

Cysteine cathepsins in human cancer

  • Christopher Jedeszko and Bonnie F. Sloane
From the journal Biological Chemistry

Abstract

Proteases play causal roles in the malignant progression of human tumors. This review centers on the roles in this process of cysteine cathepsins, i.e., peptidases belonging to the papain family (C1) of the CA clan of cysteine proteases. Cysteine cathepsins, most likely along with matrix metalloproteases (MMPs) and serine proteases, degrade the extracellular matrix, thereby facilitating growth and invasion into surrounding tissue and vasculature. Studies on tumor tissues and cell lines have shown changes in expression, activity and distribution of cysteine cathepsins in numerous human cancers. Molecular, immunologic and pharmacological strategies to modulate expression and activity of cysteine cathepsins have provided evidence for a causal role for these enzymes in tumor progression and invasion. Clinically, the levels, activities and localization of cysteine cathepsins and their endogenous inhibitors have been shown to be of diagnostic and prognostic value. Understanding the roles that cysteine proteases play in cancer could lead to the development of more efficacious therapies.

:

Corresponding author e-mail:

References

Abrahamson, M., Alvarez-Fernandez, M., and Nathanson, C.M. (2003). Cystatins. Biochem. Soc. Symp.2003179–199.Search in Google Scholar

Adenis, A., Huet, G., Zerimech, F., Hecquet, B., Balduyck, M., and Peyrat, J.P. (1995). Cathepsin B, L, and D activities in colorectal carcinomas: relationship with clinico-pathological parameters. Cancer Lett.96, 267–275.10.1016/0304-3835(95)03930-USearch in Google Scholar

Berdowska, I. (2004). Cysteine proteases as disease markers. Clin. Chim. Acta342, 41–69.10.1016/j.cccn.2003.12.016Search in Google Scholar

Bernard, K., Litman, E., Fitzpatrick, J.L., Shellman, Y.G., Argast, G., Polvinen, K., Everett, A.D., Fukasawa, K., Norris, D.A., Ahn, N.G., and Resing, K.A. (2003). Functional proteomic analysis of melanoma progression. Cancer Res.63, 6716–6725.Search in Google Scholar

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, 447–455.10.1515/BC.2003.050Search in Google Scholar

Brubaker, K.D., Vessella, R.L., True, L.D., Thomas, R., and Corey, E. (2003). Cathepsin K mRNA and protein expression in prostate cancer progression. J. Bone Miner. Res.18, 222–230.10.1359/jbmr.2003.18.2.222Search in Google Scholar

Buck, M.R., Karustis, D.G., Day, N.A., Honn, K.V., and Sloane, B.F. (1992). Degradation of extracellular-matrix proteins by human cathepsin B from normal and tumour tissues. Biochem. J.282, 273–278.10.1042/bj2820273Search in Google Scholar

Buhling, F., Waldburg, N., Gerber, A., Hackel, C., Kruger, S., Reinhold, D., Bromme, D., Weber, E., Ansorge, S., and Welte, T. (2000). Cathepsin K expression in human lung. Adv. Exp. Med. Biol.477, 281–286.Search in Google Scholar

Campo, E., Munoz, J., Miquel, R., Palacin, A., Cardesa, A., Sloane, B.F., and Emmert-Buck, M.R. (1994). Cathepsin B expression in colorectal carcinomas correlates with tumor progression and shortened patient survival. Am. J. Pathol.145, 301–309.Search in Google Scholar

Cavallo-Medved, D., Dosescu, J., Linebaugh, B.E., Sameni, M., Rudy, D. and Sloane, B.F. (2003). Mutant K-ras regulates cathepsin B localization on the surface of human colorectal carcinoma cells. Neoplasia5, 507–519.10.1016/S1476-5586(03)80035-0Search in Google Scholar

Chabowski, A., Skrzydlewska, E., Sulkowska, M., Famulski, W., Sulkowski, S., and Chrzanowska, A. (2001). [The activity of cathepsin B in colorectal adenocarcinomas]. Pol. Merkuriusz Lek.11, 330–333.Search in Google Scholar

Colella, R., and Casey, S.F. (2003). Decreased activity of cathepsins L+B and decreased invasive ability of PC3 prostate cancer cells. Biotech. Histochem.78, 101–108.10.1080/10520290310001593856Search in Google Scholar

Colella, R., Goodwyn, E., and Gopal, P. (2002). Increased cell density decreases cysteine proteinase inhibitor activity and increases invasive ability of two prostate tumor cell lines. Cancer Lett.185, 163–172.10.1016/S0304-3835(02)00275-6Search in Google Scholar

del Re, E.C., Shuja, S., Cai, J., and Murnane, M.J. (2000). Alterations in cathepsin H activity and protein patterns in human colorectal carcinomas. Br. J. Cancer82, 1317–1326.10.1054/bjoc.1999.1098Search in Google Scholar

Delebecq, T.J., Porte, H., Zerimech, F., Copin, M.C., Gouyer, V., Dacquembronne, E., Balduyck, M., Wurtz, A., and Huet, G. (2000). Overexpression level of stromelysin 3 is related to the lymph node involvement in non-small cell lung cancer. Clin. Cancer Res.6, 1086–1092.Search in Google Scholar

Demchik, L.L., Sameni, M., Nelson, K., Mikkelsen, T., and Sloane, B.F. (1999). Cathepsin B and glioma invasion. Int. J. Dev. Neurosci.17, 483–494.10.1016/S0736-5748(99)00011-8Search in Google Scholar

Dennhofer, R., Kurschat, P., Zigrino, P., Klose, A., Bosserhoff, A., van Muijen, G., Krieg, T., Mauch, C., and Hunzelmann, N. (2003). Invasion of melanoma cells into dermal connective tissue in vitro: evidence for an important role of cysteine proteases. Int. J. Cancer106, 316–323.10.1002/ijc.11255Search in Google Scholar

Ebert, W., Knoch, H., Werle, B., Trefz, G., Muley, T., and Spiess, E. (1994). Prognostic value of increased lung tumor tissue cathepsin B. Anticancer Res.14, 895–899.Search in Google Scholar

Ebert, E., Werle, B., Julke, B., Kopitar-Jerala, N., Kos, J., Lah, T., Abrahamson, M., Spiess, E., and Ebert W. (1997). Expression of cysteine protease inhibitors stefin A, stefin B, and cystatin C in human lung tumor tissue. Adv. Exp. Med. Biol.421, 259–265.10.1007/978-1-4757-9613-1_34Search in Google Scholar

Emmert-Buck, M.R., Roth, M.J., Zhuang, Z., Campo, E., Rozhin, J., Sloane, B.F., Liotta, L.A., and Stetler-Stevenson, W.G. (1994). Increased gelatinase A (MMP-2) and cathepsin B activity in invasive tumor regions of human colon cancer samples. Am. J. Pathol.145, 1285–1290.Search in Google Scholar

Fernandez, P.L., Farre, X., Nadal, A., Fernandez, E., Peiro, N., Sloane, B.F., Shi, G.P., Chapman, H.A., Campo, E., and Cardesa, A. (2001). Expression of cathepsins B and S in the progression of prostate carcinoma. Int. J. Cancer95, 51–55.10.1002/1097-0215(20010120)95:1<51::AID-IJC1009>3.0.CO;2-JSearch in Google Scholar

Flannery, T., Gibson, D., Mirakhur, M., McQuaid, S., Greenan, C., Trimble, A., Walker, B., McCormick, D., and Johnston, P.G. (2003). The clinical significance of cathepsin S expression in human astrocytomas. Am. J. Pathol.163, 175–182.10.1016/S0002-9440(10)63641-3Search in Google Scholar

Foekens, J.A., Kos, J., Peters, H.A., Krasovec, M., Look, M.P., Cimerman, N., Meijer-van Gelder, M.E., Henzen-Logmans, S.C., van Putten, W.L., and Klijn, J.G. (1998). Prognostic significance of cathepsins B and L in primary human breast cancer. J. Clin. Oncol.16, 1013–1021.10.1200/JCO.1998.16.3.1013Search in Google Scholar

Frade, R., Rodrigues-Lima, F., Huang, S., Xie, K., Guillaume, N., and Bar-Eli, M. (1998). Procathepsin-L, a proteinase that cleaves human C3 (the third component of complement), confers high tumorigenic and metastatic properties to human melanoma cells. Cancer Res.58, 2733–2736.10.1016/S0161-5890(98)90609-5Search in Google Scholar

Friedrich, B., Jung, K., Lein, M., Turk, I., Rudolph, B., Hampel, G., Schnorr, D., and Loening, S.A. (1999). Cathepsins B, H, L and cysteine protease inhibitors in malignant prostate cell lines, primary cultured prostatic cells and prostatic tissue. Eur. J. Cancer35, 138–144.10.1016/S0959-8049(98)00273-1Search in Google Scholar

Frohlich, E., Schlagenhauff, B., Mohrle, M., Weber, E., Klessen, C., and Rassner, G. (2001). Activity, expression, and transcription rate of the cathepsins B, D, H, and L in cutaneous malignant melanoma. Cancer91, 972–982.10.1002/1097-0142(20010301)91:5<972::AID-CNCR1087>3.0.CO;2-QSearch in Google Scholar

Fujise, N., Nanashim, A., Taniguchi, Y., Matsuo, S., Hatano, K., Matsumoto, Y., Tagawa, Y., and Ayabe, H. (2000). Prognostic impact of cathepsin B and matrix metalloproteinase-9 in pulmonary adenocarcinomas by immunohistochemical study. Lung Cancer27, 19–26.10.1016/S0169-5002(99)00088-4Search in Google Scholar

Gabrijelcic, D., Svetic, B., Spaic, D., Skrk, J., Budihna, J., and Turk, V. (1992a). Determination of cathepsins B, H, L and kininogen in breast cancer patients. Agents Actions (Suppl.) 38, 350–357.Search in Google Scholar

Gabrijelcic, D., Svetic, B., Spaic, D., Skrk, J., Budihna, M., Dolenc, I., Popovic, T., Cotic, V., and Turk, V. (1992b). Cathepsins B, H and L in human breast carcinoma. Eur. J. Clin. Chem. Clin. Biochem.30, 69–74.Search in Google Scholar

Goldmann, T., Ribbert, D., Suter, L., Brode, M., and Otto, F. (1998). Tumor characteristics involved in the metastatic behaviour as an improvement in primary cutaneous melanoma prognostics. J. Exp. Clin. Cancer Res.17, 483–489.Search in Google Scholar

Goldmann, T., Suter, L., Ribbert, D., and Otto, F. (1999). The expression of proteolytic enzymes at the dermal invading front of primary cutaneous melanoma predicts metastasis. Pathol. Res. Pract.195, 171–175.10.1016/S0344-0338(99)80030-2Search in Google Scholar

Guo, M., Mathieu, P.A., Linebaugh, B., Sloane, B.F., and Reiners, J.J.Jr. (2002). Phorbol ester activation of a proteolytic cascade capable of activating latent transforming growth factor-bL a process initiated by the exocytosis of cathepsin B. J. Biol. Chem.277, 14829–14837.10.1074/jbc.M108180200Search in Google Scholar

Herszenyi, L., Plebani, M., Carraro, P., De Paoli, M., Roveroni, G., Cardin, R., Tulassay, Z., Naccarato, R., and Farinati, F. (1999). The role of cysteine and serine proteases in colorectal carcinoma. Cancer86, 1135–1142.10.1002/(SICI)1097-0142(19991001)86:7<1135::AID-CNCR6>3.0.CO;2-2Search in Google Scholar

Hirai, K., Yokoyama, M., Asano, G., and Tanaka, S. (1999). Expression of cathepsin B and cystatin C in human colorectal cancer. Hum. Pathol.30, 680–686.10.1016/S0046-8177(99)90094-1Search in Google Scholar

Iacobuzio-Donahue, C.A., Shuja, S., Cai, J., Peng, P., and Murnane, M.J. (1997). Elevations in cathepsin B protein content and enzyme activity occur independently of glycosylation during colorectal tumor progression. J. Biol. Chem.272, 29190–29199.10.1074/jbc.272.46.29190Search in Google Scholar

Inoue, T., Ishida, T., Sugio, K., and Sugimachi, K. (1994). Cathepsin B expression and laminin degradation as factors influencing prognosis of surgically treated patients with lung adenocarcinoma. Cancer Res.54, 6133–6136.Search in Google Scholar

Ishidoh, K., and Kominami, E. (1995). Procathepsin L degrades extracellular matrix proteins in the presence of glycosaminoglycans in vitro. Biochem. Biophys. Res. Commun.217, 624–631.10.1006/bbrc.1995.2820Search in Google Scholar

Jean, D., Bar-Eli, M., Huang, S., Xie, K., Rodrigues-Lima, F., Hermann, J., and Frade, R. (1996). A cysteine proteinase, which cleaves human C3, the third component of complement, is involved in tumorigenicity and metastasis of human melanoma. Cancer Res.56, 254–258.Search in Google Scholar

Kageshita, T., Yoshii, A., Kimura, T., Maruo, K., Ono, T., Himeno, M., and Nishimura, Y. (1995). Biochemical and immunohistochemical analysis of cathepsins B, H, L and D in human melanocytic tumours. Arch. Dermatol. Res.287, 266–272.10.1007/BF01105077Search in Google Scholar

Kayser, K., Richter, N., Hufnagl, P., Kayser, G., Kos, J., and Werle, B. (2003). Expression, proliferation activity and clinical significance of cathepsin B and cathepsin L in operated lung cancer. Anticancer Res.23, 2767–2772.Search in Google Scholar

Khan, A., Krishna, M., Baker, S.P., and Banner, B.F. (1998). Cathepsin B and tumor-associated laminin expression in the progression of colorectal adenoma to carcinoma. Mod. Pathol.11, 704–708.Search in Google Scholar

Kim, K., Kuo, T., Cai, J., Shuja, S., and Murnane, M.J. (1997). N-ras protein: frequent quantitative and qualitative changes occur in human colorectal carcinomas. Int. J. Cancer71, 767–775.10.1002/(SICI)1097-0215(19970529)71:5<767::AID-IJC13>3.0.CO;2-5Search in Google Scholar

Kim, K., Cai, J., Shuja, S., Kuo, T., and Murnane, M.J. (1998). Presence of activated ras correlates with increased cysteine proteinase activities in human colorectal carcinomas. Int. J. Cancer79, 324–333.10.1002/(SICI)1097-0215(19980821)79:4<324::AID-IJC4>3.0.CO;2-XSearch in Google Scholar

Koblinski, J.E., Ahram, M., and Sloane, B.F. (2000). Unraveling the role of proteases in cancer. Clin. Chim. Acta291, 113–135.10.1016/S0009-8981(99)00224-7Search in Google Scholar

Koblinski, J.E., Dosescu, J., Sameni, M., Moin, K., Clark, K., and Sloane, B.F. (2002). Interaction of human breast fibroblasts with collagen I increases secretion of procathepsin B. J. Biol. Chem.277, 32220–32227.10.1074/jbc.M204708200Search in Google Scholar

Konduri, S., Lakka, S.S., Tasiou, A., Yanamandra, N., Gondi, C.S., Dinh, D.H., Olivero, W.C., Gujrati, M., and Rao, J.S. (2001). Elevated levels of cathepsin B in human glioblastoma cell lines. Int. J. Oncol.19, 519–524.10.3892/ijo.19.3.519Search in Google Scholar

Konduri, S.D., Yanamandra, N., Siddique, K., Joseph, A., Dinh, D.H., Olivero, W.C., Gujrati, M., Kouraklis, G., Swaroop, A., Kyritsis, A.P., and Rao, J.S. (2002). Modulation of cystatin C expression impairs the invasive and tumorigenic potential of human glioblastoma cells. Oncogene21, 8705–8712.10.1038/sj.onc.1205949Search in Google Scholar

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.Search in Google Scholar

Kos, J., Stabuc, B., Schweiger, A., Krasovec, M., Cimerman, N., Kopitar-Jerala, N., and Vrhovec, I. (1997). Cathepsins B, H, and L and their inhibitors stefin A and cystatin C in sera of melanoma patients. Clin. Cancer Res.3, 1815–1822.Search in Google Scholar

Kos, J., Werle, B., Lah, T., and Brunner, N. (2000). Cysteine proteinases and their inhibitors in extracellular fluids: markers for diagnosis and prognosis in cancer. Int. J. Biol. Markers15, 84–89.10.1177/172460080001500116Search in Google Scholar

Kos, J., Sekirnik, A., Kopitar, G., Cimerman, N., Kayser, K., Stremmer, A., Fiehn, W., and Werle, B. (2001). Cathepsin S in tumours, regional lymph nodes and sera of patients with lung cancer: relation to prognosis. Br. J. Cancer85, 1193–1200.10.1054/bjoc.2001.2057Search in Google Scholar

Kozlowski, L., Wojtukiewicz, M.Z., and Ostrowska, H. (2000). Cathepsin A activity in primary and metastatic human melanocytic tumors. Arch. Dermatol. Res.292, 68–71.10.1007/s004030050012Search in Google Scholar

Krepela, E., Prochazka, J., Karova, B., Cermak, J., and Roubkova, H. (1997). Cathepsin B, thiols and cysteine protease inhibitors in squamous-cell lung cancer. Neoplasma44, 219–239.Search in Google Scholar

Krepela, E., Prochazka, J., Karova, B., Cermak, J., and Roubkova, H. (1998). Cysteine proteases and cysteine protease inhibitors in non-small cell lung cancer. Neoplasma45, 318–331.Search in Google Scholar

Kruszewski, W.J., Rzepko, R., Wojtacki, J., Skokowski, J., Kopacz, A., Jaskiewicz, K., and Drucis, K. (2004). Overexpression of cathepsin B correlates with angiogenesis in colon adenocarcinoma. Neoplasma51, 38–43.Search in Google Scholar

Lah, T.T., and Kos, J. (1998). Cysteine proteinases in cancer progression and their clinical relevance for prognosis. Biol. Chem.379, 125–130.Search in Google Scholar

Lah, T.T., Buck, M.R., Honn, K.V., Crissman, J.D., Rao, N.C., Liotta, L.A., and Sloane, B.F. (1989). Degradation of laminin by human tumor cathepsin B. Clin. Exp. Metastasis7, 461–468.10.1007/BF01753666Search in Google Scholar

Lah, T.T., Calaf, G., Kalman, E., Shinde, B.G., Russo, J., Jarosz, D., Zabrecky, J., Somers, R., and Daskal, I. (1995). Cathepsins D, B and L in breast carcinoma and in transformed human breast epithelial cells (HBEC). Biol. Chem. Hoppe-Seyler376, 357–363.10.1515/bchm3.1995.376.6.357Search in Google Scholar

Lah, T.T., Kos, J., Blejec, A., Frkovic-Georgio, S., Golouh, R., Vrhovec, I.I., and Turk, V.V. (1997). The expression of lysosomal proteinases and their inhibitors in breast cancer: possible relationship to prognosis of the disease. Pathol. Oncol. Res.3, 89–99.10.1007/BF02907801Search in Google Scholar

Lah, T.T., Kalman, E., Najjar, D., Gorodetsky, E., Brennan, P., Somers, R., and Daskal, I. (2000a). Cells producing cathepsins D, B, and L in human breast carcinoma and their association with prognosis. Hum. Pathol.31, 149–160.10.1016/S0046-8177(00)80214-2Search in Google Scholar

Lah, T.T., Strojnik, T., Levicar, N., Bervar, A., Zajc, I., Pilkington, G., and Kos, J. (2000b). Clinical and experimental studies of cysteine cathepsins and their inhibitors in human brain tumors. Int. J. Biol. Markers15, 90–93.10.1177/172460080001500117Search in Google Scholar

Lakka, S.S., Gondi, C.S., Yanamandra, N., Olivero, W.C., Dinh, D.H., Gujrati, M., and Rao, J.S. (2004). Inhibition of cathepsin B and MMP-9 gene expression in glioblastoma cell line via RNA interference reduces tumor cell invasion, tumor growth and angiogenesis. Oncogene23, 4681–4689.10.1038/sj.onc.1207616Search in Google Scholar

Ledakis, P., Tester, W.T., Rosenberg, N., Romero-Fischmann, D., Daskal, I., and Lah, T.T. (1996). Cathepsins D, B, and L in malignant human lung tissue. Clin. Cancer Res.2, 561–568.Search in Google Scholar

Levicar, N., Kos, J., Blejec, A., Golouh, R., Vrhovec, I., Frkovic-Grazio, S., and Lah, T.T. (2002a). Comparison of potential biological markers cathepsin B, cathepsin L, stefin A and stefin B with urokinase and plasminogen activator inhibitor-1 and clinicopathological data of breast carcinoma patients. Cancer Detect. Prev.26, 42–49.10.1016/S0361-090X(02)00015-6Search in Google Scholar

Levicar, N., Strojnik, T., Kos, J., Dewey, R.A., Pilkington, G.J., and Lah, T.T. (2002b). Lysosomal enzymes, cathepsins in brain tumour invasion. J. Neurooncol.58, 21–32.10.1023/A:1015892911420Search in Google Scholar

Levicar, N., Dewey, R.A., Daley, E., Bates, T.E., Davies, D., Kos, J., Pilkington, G.J., and Lah, T.T. (2003). Selective suppression of cathepsin L by antisense cDNA impairs human brain tumor cell invasion in vitro and promotes apoptosis. Cancer Gene Ther.10, 141–151.10.1038/sj.cgt.7700546Search in Google Scholar PubMed

Littlewood-Evans, A.J., Bilbe, G., Bowler, W.B., Farley, D., Wlodarski, B., Kokubo, T., Inaoka, T., Sloane, J., Evans, D.B., and Gallagher, J.A. (1997). The osteoclast-associated protease cathepsin K is expressed in human breast carcinoma. Cancer Res.57, 5386–5390.Search in Google Scholar

Maguire, T.M., Shering, S.G., Duggan, C.M., McDermott, E.W., O’Higgins, N.J., and Duffy, M.J. (1998). High levels of cathepsin B predict poor outcome in patients with breast cancer. Int. J. Biol. Markers13, 139–144.10.1177/172460089801300303Search in Google Scholar

Mai, J., Finley Jr., R.L., Waisman, D.M., and Sloane, B.F. (2000). Human procathepsin B interacts with the annexin II tetramer on the surface of tumor cells. J. Biol. Chem.275, 12806–12812.10.1074/jbc.275.17.12806Search in Google Scholar PubMed

Mareel, M., and Leroy, A. (2003). Clinical, cellular, and molecular aspects of cancer invasion. Physiol. Rev.83, 337–376.10.1152/physrev.00024.2002Search in Google Scholar PubMed

Mayer, P., Schmid, H., Schaber, B., and Fierlbeck, G. (1997). Tumor-associated cysteine proteinase activities in human melanoma cells and fibroblasts of different origin. Eur. J. Cell. Biol.73, 344–351.Search in Google Scholar

McKerrow, J.H., Bhargava, V., Hansell, E., Huling, S., Kuwahara, T., Matley, M., Coussens, L., and Warren, R. (2000). A functional proteomics screen of proteases in colorectal carcinoma. Mol. Med.6, 450–460.10.1007/BF03401787Search in Google Scholar

Mikkelsen, T., Yan, P.S., Ho, K.L., Sameni, M., Sloane, B.F., andz Rosenblum, M.L. (1995). Immunolocalization of cathepsin B in human glioma: implications for tumor invasion and angiogenesis. J. Neurosurg.83, 285–290.10.3171/jns.1995.83.2.0285Search in Google Scholar PubMed

Mohanam, S., Jasti, S.L., Kondraganti, S.R., Chandrasekar, N., Lakka, S.S., Kin, Y., Fuller, G.N., Yung, A.W., Kyritsis, A.P., Dinh, D.H., et al. (2001). Down-regulation of cathepsin B expression impairs the invasive and tumorigenic potential of human glioblastoma cells. Oncogene20, 3665–3673.10.1038/sj.onc.1204480Search in Google Scholar PubMed

Nagler, D.K., Kruger, S., Kellner, A., Ziomek, E., Menard, R., Buhtz, P., Krams, M., Roessner, A., and Kellner, U. (2004). Up-regulation of cathepsin X in prostate cancer and prostatic intraepithelial neoplasia. Prostate60, 109–119.10.1002/pros.20046Search in Google Scholar

Otto, F.J., Goldmann, T., Biess, B., Lippold, A., Suter, L., and Westhoff, U. (1999). Prognostic classification of malignant melanomas by combining clinical, histological, and immunohistochemical parameters. Oncology56, 208–214.10.1159/000011967Search in Google Scholar

Padilla, D., Cubo, T., Molina, J.M., Garcia, M., De la Osa, G., Palomino, T., Pardo, R., Martin, J., Arevalo, E., and Hernandez Calvo, J. (2003). [Prognostic significance and clinic utility of serum and immunohistochemical cathepsin B levels in colorectal cancer]. Ann. Med. Intern.20, 521–525.Search in Google Scholar

Podgorski, I., and Sloane, B.F. (2003). Cathepsin B and its role(s) in cancer progression. Biochem. Soc. Symp.2003263–276.Search in Google Scholar

Podgorski, I.L., Mansoureh, S., Jedeszko, C., Bhagat, S., Cher, M.L., and Sloane, B.F. (2004). Bone microenvironment modulates expression and activity of cathepsin B in prostate cancer. Neoplasia, in press.Search in Google Scholar

Poole, A.R., Tiltman, K.J., Recklies, A.D., and Stoker, T.A. (1978). Differences in secretion of the proteinase cathepsin B at the edges of human breast carcinomas and fibroadenomas. Nature273, 545–57.10.1038/273545a0Search in Google Scholar

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, 853–857.10.1515/bchm.2001.382.5.853Search in Google Scholar

Premzl, A., Zavasnik-Bergant, V., Turk, V., and Kos, J. (2003). Intracellular and extracellular cathepsin B facilitate invasion of MCF-10A neoT cells through reconstituted extracellular matrix in vitro. Exp. Cell Res.283, 206–214.10.1016/S0014-4827(02)00055-1Search in Google Scholar

Rao, J.S. (2003). Molecular mechanisms of glioma invasiveness: the role of proteases. Nat. Rev. Cancer3, 489–501.10.1038/nrc1121Search in Google Scholar PubMed

Rempel, S.A., Rosenblum, M.L., Mikkelsen, T., Yan, P.S., Ellis, K.D., Golembieski, W.A., Sameni, M., Rozhin, J., Ziegler, G., and Sloane, B.F. (1994). Cathepsin B expression and localization in glioma progression and invasion. Cancer Res.54, 6027–6031.Search in Google Scholar

Roshy, S., Sloane, B.F., and Moin, K. (2003). Pericellular cathepsin B and malignant progression. Cancer Metastasis Rev.22, 271–286.10.1023/A:1023007717757Search in Google Scholar

Saleh, Y., Siewinski, M., Sebzda, T., Jelen, M., Ziolkowski, P., Gutowicz, J., Grybos, M., and Pawelec, M. (2003). Inhibition of cathepsin B activity in human breast cancer tissue by cysteine peptidase inhibitor isolated from human placenta: immunohistochemical and biochemical studies. Folia Histochem. Cytobiol.41, 161–167.Search in Google Scholar

Sameni, M., Elliott, E., Ziegler, G., Fortgens, P.H., Dennison, C., and Sloane, B.F. (1995). Cathepsin B and D are localized at the surface of human breast cancer cells. Pathol. Oncol. Res.1, 43–53.10.1007/BF02893583Search in Google Scholar PubMed

Sameni, M., Dosescu, J., Moin, K., and Sloane, B.F. (2003). Functional imaging of proteolysis: stromal and inflammatory cells increase tumor proteolysis. Mol. Imaging2, 159–175.10.1162/153535003322556903Search in Google Scholar PubMed

Schwartz, D.R., Wu, R., Kardia, S.L., Levin, A.M., Huang, C.C., Shedden, K.A., Kuick, R., Misek, D.E., Hanash, S.M., Taylor, J.M., et al. (2003). Novel candidate targets of beta-catenin/T-cell factor signaling identified by gene expression profiling of ovarian endometrioid adenocarcinomas. Cancer Res.63, 2913–2922.Search in Google Scholar

Schweiger, A., Staib, A., Werle, B., Krasovec, M., Lah, T.T., Ebert, W., Turk, V., and Kos, J. (2000). Cysteine proteinase cathepsin H in tumours and sera of lung cancer patients: relation to prognosis and cigarette smoking. Br. J. Cancer82, 782–788.10.1054/bjoc.1999.0999Search in Google Scholar PubMed PubMed Central

Shridhar, R., Zhang, J., Song, J., Booth, B.A., Kevil, C.G., Sotiropoulou, G., Sloane, B.F., and Keppler, D. (2004). Cystatin M suppresses the malignant phenotype of human MDA-MB-435S cells. Oncogene23, 2206–2215.10.1038/sj.onc.1207340Search in Google Scholar

Sinha, A.A., Wilson, M.J., Gleason, D.F., Reddy, P.K., Sameni, M., and Sloane, B.F. (1995). Immunohistochemical localization of cathepsin B in neoplastic human prostate. Prostate26, 171–178.10.1002/pros.2990260402Search in Google Scholar

Sinha, A.A., Quast, B.J., Wilson, M.J., Reddy, P.K., Gleason, D.F., and Sloane, B.F. (1998). Codistribution of procathepsin B and mature cathepsin B forms in human prostate tumors detected by confocal and immunofluorescence microscopy. Anat. Rec.252, 281–289.10.1002/(SICI)1097-0185(199810)252:2<281::AID-AR14>3.0.CO;2-JSearch in Google Scholar

Sinha, A.A., Quast, B.J., Korkowski, J.C., Wilson, M.J., Reddy, P.K., Ewing, S.L., Sloane, B.F., and Gleason, D.F. (1999). The relationship of cathepsin B and stefin A mRNA localization identifies a potentially aggressive variant of human prostate cancer within a Gleason histologic score. Anticancer Res.19, 2821–2829.Search in Google Scholar

Sinha, A.A., Quast, B.J., Wilson, M.J., Fernandes, E.T., Reddy, P.K., Ewing, S.L., Sloane, B.F., and Gleason, D.F. (2001a). Ratio of cathepsin B to stefin A identifies heterogeneity within Gleason histologic scores for human prostate cancer. Prostate48, 274–284.10.1002/pros.1107Search in Google Scholar

Sinha, A.A., Jamuar, M.P., Wilson, M.J., Rozhin, J., and Sloane, B.F. (2001b). Plasma membrane association of cathepsin B in human prostate cancer: biochemical and immunogold electron microscopic analysis. Prostate49, 172–184.10.1002/pros.1132Search in Google Scholar

Sinha, A.A., Quast, B.J., Wilson, M.J., Fernandes, E.T., Reddy, P.K., Ewing, S.L., and Gleason, D.F. (2002). Prediction of pelvic lymph node metastasis by the ratio of cathepsin B to stefin A in patients with prostate carcinoma. Cancer94, 3141–3149.10.1002/cncr.10604Search in Google Scholar

Sivaparvathi, M., Sawaya, R., Gokaslan, Z.L., Chintala, S.K., Rao, J.S., and Chintala, K.S. (1996a). Expression and the role of cathepsin H in human glioma progression and invasion. Cancer Lett.104, 121–126.10.1016/0304-3835(96)04242-5Search in Google Scholar

Sivaparvathi, M., McCutcheon, I., Sawaya, R., Nicolson, G.L., and Rao, J.S. (1996b). Expression of cysteine protease inhibitors in human gliomas and meningiomas. Clin. Exp. Metastasis14, 344–350.10.1007/BF00123393Search in Google Scholar

Sloane, B.F., Moin, K., Sameni, M., Tait, L.R., Rozhin, J., and Ziegler, G. (1994). Membrane association of cathepsin B can be induced by transfection of human breast epithelial cells with c-Ha-ras oncogene. J. Cell Sci.107, 373–384.10.1242/jcs.107.2.373Search in Google Scholar

Sloane, B.F., Yana, S., Podgorski, I., Linebaugh, B., Cher, M.L., Mai, J., Cavallo-Medved, D., Sameni, M., Dosescu, J., and Moin, K. (2004). Cathepsin B and tumor proteolysis: contribution of the tumor microenvironment. Semin. Cancer Biol., in press.Search in Google Scholar

Srivastav, S., Verma, M., and Henson, D.E. (2001). Biomarkers for early detection of colon cancer. Clin. Cancer Res.7, 1118–1126.Search in Google Scholar

Strojnik, T., Kos, J., Zidanik, B., Golouh, R., and Lah, T. (1999). Cathepsin B immunohistochemical staining in tumor and endothelial cells is a new prognostic factor for survival in patients with brain tumors. Clin. Cancer Res.5, 559–567.Search in Google Scholar

Sukoh, N., Abe, S., Ogura, S., Isobe, H., Takekawa, H., Inoue, K., and Kawakami, Y. (1994). Immunohistochemical study of cathepsin B. Prognostic significance in human lung cancer. Cancer74, 46–51.Search in Google Scholar

Szpaderska, A.M., and Frankfater, A. (2001). An intracellular form of cathepsin B contributes to invasiveness in cancer. Cancer Res.61, 3493–3500.Search in Google Scholar

Talieri, M., Papadopoulou, S., Scorilas, A., Xynopoulos, D., Arnogianaki, N., Plataniotis, G., Yotis, J., and Agnanti, N. (2004). Cathepsin B and cathepsin D expression in the progression of colorectal adenoma to carcinoma. Cancer Lett.205, 97–106.10.1016/j.canlet.2003.09.033Search in Google Scholar

Thomssen, C., Schmitt, M., Goretzki, L., Oppelt, P., Pache, L., Dettmar, P., Janicke, F., and Graeff, H. (1995). Prognostic value of the cysteine proteases cathepsins B and cathepsin L in human breast cancer. Clin. Cancer Res.1, 741–746.Search in Google Scholar

Turk, V., Turk, B., and Turk, D. (2001). Lysosomal cysteine proteases: facts and opportunities. EMBO J.20, 4629–4633.10.1093/emboj/20.17.4629Search in Google Scholar

Ulmer, A., Korber, V., Schmid, H., and Fierlbeck, G. (1998). Increased activity of cathepsin B in fibroblasts isolated from primary melanoma in comparison to fibroblasts from normal skin. Exp. Dermatol.7, 14–17.10.1111/j.1600-0625.1998.tb00297.xSearch in Google Scholar

Visscher, D.W., Hoyhtya, M., Ottosen, S.K., Liang, C.M., Sarkar, F.H., Crissman, J.D., and Fridman, R. (1994). Enhanced expression of tissue inhibitor of metalloproteinase-2 (TIMP-2) in the stroma of breast carcinomas correlates with tumor recurrence. Int. J. Cancer59, 339–344.10.1002/ijc.2910590308Search in Google Scholar

Waghray, A., Schober, M., Feroze, F., Yao, F., Virgin, J., and Chen, Y.Q. (2001). Identification of differentially expressed genes by serial analysis of gene expression in human prostate cancer. Cancer Res.61, 4283–4286.Search in Google Scholar

Waghray, A., Keppler, D., Sloane, B.F., Schuger, L., and Chen, Y.Q. (2002). Analysis of a truncated form of cathepsin H in human prostate tumor cells. J. Biol. Chem.277, 11533–11538.10.1074/jbc.M109557200Search in Google Scholar

Werle, B., Ebert, W., Klein, W., and Spiess, E. (1994). Cathepsin B in tumors, normal tissue and isolated cells from the human lung. Anticancer Res.14, 1169–1176.Search in Google Scholar

Werle, B., Ebert, W., Klein, W., and Spiess, E. (1995). Assessment of cathepsin L activity by use of the inhibitor CA-074 compared to cathepsin B activity in human lung tumor tissue. Biol. Chem. Hoppe-Seyler376, 157–164.10.1515/bchm3.1995.376.3.157Search in Google Scholar

Werle, B., Lotterle, H., Schanzenbacher, U., Lah, T.T., Kalman, E., Kayser, K., Bulzebruck, H., Schirren, J., Krasovec, M., Kos, J., and Spiess, E. (1999). Immunochemical analysis of cathepsin B in lung tumours: an independent prognostic factor for squamous cell carcinoma patients. Br. J. Cancer81, 510–519.10.1038/sj.bjc.6690723Search in Google Scholar

Werle, B., Kraft, C., Lah, T.T., Kos, J., Schanzenbacher, U., Kayser, K., Ebert, W., and Spiess, E. (2000). Cathepsin B in infiltrated lymph nodes is of prognostic significance for patients with nonsmall cell lung carcinoma. Cancer89, 2282–2291.10.1002/1097-0142(20001201)89:11<2282::AID-CNCR17>3.0.CO;2-4Search in Google Scholar

Wulfkuhle, J.D., Sgroi, D.C., Krutzsch, H., McLean, K., Mc-Garvey, 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.Search in Google Scholar

Yan, S., and Sloane, B.F. (2003). Molecular regulation of human cathepsin B: implication in pathologies. Biol. Chem.384, 845–854.10.1515/BC.2003.095Search in Google Scholar

Yanamandra, N., Gumidyala, K.V., Waldron, K.G., Gujrati, M., Olivero, W.C., Dinh, D.H., Rao, J.S., and Mohanam, S. (2004). Blockade of cathepsin B expression in human glioblastoma cells is associated with suppression of angiogenesis. Oncogene23, 2224–2230.10.1038/sj.onc.1207338Search in Google Scholar

Yano, M., Hirai, K., Naito, Z., Yokoyama, M., Ishiwata, T., Shiraki, Y., Inokuchi, M., and Asano, G. (2001). Expression of cathepsin B and cystatin C in human breast cancer. Surg. Today31, 385–389.10.1007/s005950170126Search in Google Scholar

Yoshii, A., Kageshita, T., Tsushima, H., and Ono, T. (1995). Clinical relevance of cathepsin B-like enzyme activity and cysteine proteinase inhibitor in melanocytic tumours. Arch. Dermatol. Res.287, 209–213.10.1007/BF01262334Search in Google Scholar

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, 185–190.10.1016/S0304-3835(02)00452-4Search in Google Scholar

Zhao, H., Bernardo, M.M., Osenkowski, P., Sohail, A., Pei, D., Nagase, H., Kashiwagi, M., Soloway, P.D., DeClerck, Y.A., and Fridman, R. (2004). Differential inhibition of membrane type 3 (MT3)-matrix metalloproteinase (MMP) and MT1-MMP by tissue inhibitor of metalloproteinase (TIMP)-2 and TIMP-3 regulates pro-MMP-2 activation. J. Biol. Chem.279, 8592–8601.10.1074/jbc.M308708200Search in Google Scholar PubMed

Zore, I., Krasovec, M., Cimerman, N., Kuhelj, R., Werle, B., Nielsen, H.J., Brunner, N., and Kos, J. (2001). Cathepsin B/cystatin C complex levels in sera from patients with lung and colorectal cancer. Biol. Chem.382, 805–810.10.1515/bchm.2001.382.5.805Search in Google Scholar

Published Online: 2005-06-01
Published in Print: 2004-11-01

© Walter de Gruyter

Downloaded on 23.4.2024 from https://www.degruyter.com/document/doi/10.1515/BC.2004.132/html
Scroll to top button