Expression, intracellular localization and maturation of cysteine cathepsins in renal embryonic and cancer cell lines
- 作者: Frolova A.1,2, Tikhomirova N.3, Kireev I.3, Zernii E.3, Parodi A.2, Ivanov K.2, Zamyatnin A.1,2,3,4
-
隶属关系:
- Institute of Molecular Medicine, Sechenov First Moscow State Medical University
- Scientific Center for Translation Medicine, Sirius University of Science and Technology
- Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University
- Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University
- 期: 卷 88, 编号 7 (2023)
- 页面: 1268-1280
- 栏目: Articles
- URL: https://journals.rcsi.science/0320-9725/article/view/141469
- DOI: https://doi.org/10.31857/S032097252307014X
- EDN: https://elibrary.ru/FYLWMO
- ID: 141469
如何引用文章
详细
作者简介
A. Frolova
Institute of Molecular Medicine, Sechenov First Moscow State Medical University;Scientific Center for Translation Medicine, Sirius University of Science and Technology119991 Moscow, Russia;354340 Sochi, Russia
N. Tikhomirova
Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University119992 Moscow, Russia
I. Kireev
Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University119992 Moscow, Russia
E. Zernii
Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University119992 Moscow, Russia
A. Parodi
Scientific Center for Translation Medicine, Sirius University of Science and Technology354340 Sochi, Russia
K. Ivanov
Scientific Center for Translation Medicine, Sirius University of Science and Technology354340 Sochi, Russia
A. Zamyatnin
Institute of Molecular Medicine, Sechenov First Moscow State Medical University;Scientific Center for Translation Medicine, Sirius University of Science and Technology;Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University;Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University
Email: zamyat@belozersky.msu.ru
119991 Moscow, Russia;354340 Sochi, Russia;119992 Moscow, Russia;119234 Moscow, Russia
参考
- Yadati, T., Houben, T., Bitorina, A., and Shiri-Sverdlov, R. (2020) The ins and outs of cathepsins: physiological function and role in disease management, Cells, 9, 1679, doi: 10.3390/cells9071679.
- Manchanda, M., Fatima, N., Chauhan, S.S. (2017) Physiological and Pathological Functions of Cysteine Cathepsins. In: Proteases in Physiology and Pathology, Springer, Singapore, doi: 10.1007/978-981-10-2513-6_11.
- 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 Proteins Proteomics, 1824, 68-88, doi: 10.1016/j.bbapap.2011.10.002.
- Bestvater, F., Dallner, C., and Spiess, E. (2005) The C-terminal subunit of artificially truncated human cathepsin B mediates its nuclear targeting and contributes to cell viability, BMC Cell Biol., 6, 16, doi: 10.1186/1471-2121-6-16.
- Hsing, L. C., and Rudensky, A. Y. (2005) The lysosomal cysteine proteases in MHC class II antigen presentation, Immunol. Rev., 207, 229-241, doi: 10.1111/j.0105-2896.2005.00310.x.
- Stoeckle, C., Gouttefangeas, C., Hammer, M., Weber, E., Melms, A., and Tolosa, E. (2009) Cathepsin W expressed exclusively in CD8+ T cells and NK cells, is secreted during target cell killing but is not essential for cytotoxicity in human CTLs, Exp. Hematol., 37, 266-275, doi: 10.1016/J.EXPHEM.2008.10.011.
- Cheng, X., Ren, Z., Liu, Z., Sun, X., Qian, R., Cao, C., Liu, B., Wang, J., Wang, H., Guo, Y., et al. (2022) Cysteine cathepsin C: a novel potential biomarker for the diagnosis and prognosis of glioma, Cancer Cell Int., 22, 53, doi: 10.1186/S12935-021-02417-6.
- Majc, B., Habič, A., Novak, M., Rotter, A., Porčnik, A., Mlakar, J., Župunski, V., Fonović, U. P., Knez, D., Zidar, N., et al. (2022) Upregulation of cathepsin X in glioblastoma: interplay with γ-enolase and the effects of selective cathepsin X inhibitors, Int. J. Mol. Sci., 23, 1784, doi: 10.3390/ijms23031784.
- Verbovšek, U., Motaln, H., Rotter, A., Atai, N. A., Gruden, K., Van Noorden, C. J. F., and Lah, T. T. (2014) Expression analysis of all protease genes reveals cathepsin K to be overexpressed in glioblastoma, PLoS One, 9, e0142116, doi: 10.1371/journal.pone.0111819.
- Xiao, Y., Cong, M., Li, J., He, D., Wu, Q., Tian, P., Wang, Y., Yang, S., Liang, C., Liang, Y., et al. (2021) Cathepsin C promotes breast cancer lung metastasis by modulating neutrophil infiltration and neutrophil extracellular Trap formation, Cancer Cell, 39, 423-437.e7, doi: 10.1016/J.CCELL.2020.12.012.
- Cairns, J., Ingle, J. N., Wickerham, L. D., Weinshilboum, R., Liu, M., and Wang, L. (2017) SNPs near the cysteine proteinase cathepsin O gene (CTSO) determine tamoxifen sensitivity in ERα-positive breast cancer through regulation of BRCA1, PLoS Genet., 13, e1007031, doi: 10.1371/JOURNAL.PGEN.1007031.
- Santamaría, I., Velasco, G., Cazorla, M., Fueyo, A., Campo, E., and López-Otín, C. (1998) Cathepsin L2, a novel human cysteine proteinase produced by breast and colorectal carcinomas, Cancer Res., 58, 1624-1630.
- Sereesongsaeng, N., McDowell, S. H., Burrows, J. F., Scott, C. J., and Burden, R. E. (2020) Cathepsin V suppresses GATA3 protein expression in luminal A breast cancer, Breast Cancer Res., 22, 139, doi: 10.1186/S13058-020-01376-6.
- Schweiger, A., Christensen, I. J., Nielsen, H. J., Sørensen, S., Brünner, N., and Kos, J. (2018) Serum cathepsin H as a potential prognostic marker in patients with colorectal cancer, Int. J. Biol. Markers, 19, 289-294, doi: 10.1177/172460080401900406.
- Tamhane, T., Njenga, R. W., Burden, R. E., Büth, H., Maelandsmo, G. M., Haugen, M. H., Scott, C. J., and Brix, K. (2021) Trafficking of full-length and N-terminally truncated cathepsin B in human colorectal carcinoma cells, Appl. Sci., 11, 11936, doi: 10.3390/app112411936.
- 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.
- Dheilly, E., Battistello, E., Katanayeva, N., Sungalee, S., Michaux, J., Duns, G., Wehrle, S., Sordet-Dessimoz, J., Mina, M., Racle, J., et al. (2020) Cathepsin S regulates antigen processing and T cell activity in non-Hodgkin lymphoma, Cancer Cell, 37, 674-689.e12, doi: 10.1016/j.ccell.2020.03.016.
- Haider, A. S., Peters, S. B., Kaporis, H., Cardinale, I., Fei, J., Ott, J., Blumenberg, M., Bowcock, A. M., Krueger, J. G., and Carucci, J. A. (2006) Genomic analysis defines a cancer-specific gene expression signature for human squamous cell carcinoma and distinguishes malignant hyperproliferation from benign hyperplasia, J. Invest. Dermatol., 126, 869-881, doi: 10.1038/sj.jid.5700157.
- Yang, L., Zeng, Q., Deng, Y., Qiu, Y., Yao, W., and Liao, Y. (2022) Glycosylated cathepsin V serves as a prognostic marker in lung cancer, Front. Oncol., 12, 876245, doi: 10.3389/fonc.2022.876245.
- Teller, A., Jechorek, D., Hartig, R., Adolf, D., Reißig, K., Roessner, A., and Franke, S. (2015) Dysregulation of apoptotic signaling pathways by interaction of RPLP0 and cathepsin X/Z in gastric cancer, Pathol. Res. Pract., 211, 62-70, doi: 10.1016/j.prp.2014.09.005.
- Kiuchi, S., Tomaru, U., Ishizu, A., Imagawa, M., Kiuchi, T., Iwasaki, S., Suzuki, A., Otsuka, N., Deguchi, T., Shimizu, T., et al. (2017) Expression of cathepsins V and S in thymic epithelial tumors, Hum. Pathol., 60, 66-74, doi: 10.1016/j.humpath.2016.09.027.
- Rudzińska, M., Parodi, A., Maslova, V. D., Efremov, Y. M., Gorokhovets, N. V., Makarov, V. A., Popkov, V. A., Golovin, A. V., Zernii, E. Y., and Zamyatnin, A. A. (2020) Cysteine cathepsins inhibition affects their expression and human renal cancer cell phenotype, Cancers (Basel), 12, 1310, doi: 10.3390/cancers12051310.
- Caliò, A., Brunelli, M., Gobbo, S., Argani, P., Munari, E., Netto, G., and Martignoni, G. (2021) Cathepsin K: a novel diagnostic and predictive biomarker for renal tumors, Cancers (Basel), 13, 2441, doi: 10.3390/cancers13102441.
- Al-Hashimi, A., Venugopalan, V., Sereesongsaeng, N., Tedelind, S., Pinzaru, A. M., Hein, Z., Springer, S., Weber, E., Führer, D., Scott, C. J., et al. (2020) Significance of nuclear cathepsin V in normal thyroid epithelial and carcinoma cells, Biochim. Biophys. Acta Mol. Cell Res., 1867, 118846, doi: 10.1016/j.bbamcr.2020.118846.
- Tedelind, S., Poliakova, K., Valeta, A., Hunegnaw, R., Yemanaberhan, E. L., Heldin, N. E., Kurebayashi, J., Weber, E., Kopitar-Jerala, N., Turk, B., Bogyo, M., and Brix, K. (2010) Nuclear cysteine cathepsin variants in thyroid carcinoma cells, Biol. Chem., 391, 923-935, doi: 10.1515/BC.2010.109.
- Kothapalli, R., Bailey, R. D., Kusmartseva, I., Mane, S., Epling-Burnette, P. K., and Loughran, T. P. (2003) Constitutive expression of cytotoxic proteases and down-regulation of protease inhibitors in LGL leukemia, Int. J. Oncol., 22, 33-39, doi: 10.3892/ijo.22.1.33.
- Rudzinska-Radecka, M., Frolova, A. S., Balakireva, A. V., Gorokhovets, N. V., Pokrovsky, V. S., Sokolova, D. V., Korolev, D. O., Potoldykova, N. V., Vinarov, A. Z., Parodi, A., et al. (2022) In silico, in vitro, and clinical investigations of cathepsin B and stefin A mRNA expression and a correlation analysis in kidney cancer, Cells, 11, 1455, doi: 10.3390/CELLS11091455.
- El-Nadi, M., Hassan, H., Amer, M., Mohamed, M. M., El-Shinawi, M., and Ibrahim, S. A. (2019) Cathepsin L is a potential marker for triple-negative breast cancer, Egypt. Acad. J. Biol. Sci. C Physiol. Mol. Biol., 11, 29-36, doi: 10.21608/EAJBSC.2019.26817.
- Vizin, T., Christensen, I., Nielsen, H., and Kos, J. (2012) Cathepsin X in serum from patients with colorectal cancer: relation to prognosis, Radiol. Oncol., 46, 207, doi: 10.2478/V10019-012-0040-0.
- Tan, G.-J., Peng, Z.-K., Lu, J.-P., and Tang, F.-Q. (2013) Cathepsins mediate tumor metastasis, World J. Biol. Chem., 4, 91, doi: 10.4331/WJBC.V4.I4.91.
- Chen, C. H., Bhasin, S., Khanna, P., Joshi, M., Joslin, P. M., Saxena, R., Amin, S., Liu, S., Sindhu, S., Walker, S. R., et al. (2019) Study of cathepsin B inhibition in VEGFR TKI treated human renal cell carcinoma xenografts, Oncogenesis, 8, 15, doi: 10.1038/S41389-019-0121-7.
- Gondi, C. S., and Rao, J. S. (2013) Cathepsin B as a cancer target, Expert Opin. Ther. Targets, 17, 281, doi: 10.1517/14728222.2013.740461.
- Sevenich, L., Schurigt, U., Sachse, K., Gajda, M., Werner, F., Müller, S., Vasiljeva, O., Schwinde, A., Klemm, N., Deussing, J., et al. (2010) Synergistic antitumor effects of combined cathepsin B and cathepsin Z deficiencies on breast cancer progression and metastasis in mice, Proc. Natl. Acad. Sci. USA, 107, 2497, doi: 10.1073/PNAS.0907240107.
- Soond, S. M., Kozhevnikova, M. V., Frolova, A. S., Savvateeva, L. V., Plotnikov, E. Y., Townsend, P. A., Han, Y. P., and Zamyatnin, A. A. (2019) Lost or forgotten: the nuclear cathepsin protein isoforms in cancer, Cancer Lett., 462, 43-50, doi: 10.1016/j.canlet.2019.07.020.
- Hiwasa, T., and Sakiyama, S. (1996) Nuclear localization of procathepsin L/MEP in ras-transformed mouse fibroblasts, Cancer Lett., 99, 87-91, doi: 10.1016/0304-3835(95)04041-2.
- Sullivan, S., Tosetto, M., Kevans, D., Coss, A., Wang, L., O'Donoghue, D., Hyland, J., Sheahan, K., Mulcahy, H., and O'Sullivan, J. (2009) Localization of nuclear cathepsin L and its association with disease progression and poor outcome in colorectal cancer, Int. J. Cancer, 125, 54-61, doi: 10.1002/ijc.24275.
- Senin, I. I., Tikhomirova, N. K., Churumova, V. A., Grigoriev, I. I., Kolpakova, T. A., Zinchenko, D. V., Philippov, P. P., and Zernii, E. Y. (2011) Amino acid sequences of two immune-dominant epitopes of recoverin are involved in Ca2+/recoverin-dependent inhibition of phosphorylation of rhodopsin, Biochemistry (Moscow), 76, 332-338, doi: 10.1134/S0006297911030060.
- Dyer, R. B., and Herzog, N. K. (1995) Isolation of intact nuclei for nuclear extract preparation from a fragile B-lymphocyte cell line, Biotechniques, 19, 192-195.
- Olson, O. C., and Joyce, J. A. (2015) Cysteine cathepsin proteases: regulators of cancer progression and therapeutic response, Nat. Rev. Cancer, 15, 712-729, doi: 10.1038/nrc4027.
- Fujimoto, T., Tsunedomi, R., Matsukuma, S., Yoshimura, K., Oga, A., Fujiwara, N., Fujiwara, Y., Matsui, H., Shindo, Y., Tokumitsu, Y., et al. (2021) Cathepsin B is highly expressed in pancreatic cancer stem-like cells and is associated with patients' surgical outcomes, Oncol. Lett., 21, 30, doi: 10.3892/OL.2020.12291.
- Singh, N., Das, P., Gupta, S., Sachdev, V., Srivasatava, S., Datta Gupta, S., Pandey, R. M., Sahni, P., Chauhan, S. S., and Saraya, A. (2014) Plasma cathepsin L: a prognostic marker for pancreatic cancer, World J. Gastroenterol., 20, 17532, doi: 10.3748/WJG.V20.I46.17532.
- 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, doi: 10.1101/gad.1407406.
- Loh, C. Y., Chai, J. Y., Tang, T. F., Wong, W. F., Sethi, G., Shanmugam, M. K., Chong, P. P., and Looi, C. Y. (2019) The E-cadherin and N-cadherin switch in epithelial-to-mesenchymal transition: signaling, therapeutic implications, and challenges, Cells, 8, 1118, doi: 10.3390/CELLS8101118.
- Jevnikar, Z., Rojnik, M., Jamnik, P., Doljak, B., Fonović, U. P., and Kos, J. (2013) Cathepsin H mediates the processing of talin and regulates migration of prostate cancer cells, J. Biol. Chem., 288, 2201-2209, doi: 10.1074/JBC.M112.436394.
- Wu, N., Wang, Y. Z., Wang, K. K., Zhong, B. Q., Liao, Y. H., Liang, J. M., and Jiang, N. (2022) Cathepsin K regulates the tumor growth and metastasis by IL-17/CTSK/EMT axis and mediates M2 macrophage polarization in castration-resistant prostate cancer, Cell Death Dis., 13, 813, doi: 10.1038/s41419-022-05215-8.
- Wang, J., Chen, L., Li, Y., and Guan, X. Y. (2011) Overexpression of cathepsin Z contributes to tumor metastasis by inducing epithelial-mesenchymal transition in hepatocellular carcinoma, PLoS One, 6, 24967, doi: 10.1371/JOURNAL.PONE.0024967.
- Sivaparvathi, M., Sawaya, R., Gokaslan, Z. L., Chintala, K. S., and Rao, J. S. (1996) Expression and the role of cathepsin H in human glioma progression and invasion, Cancer Lett., 104, 121-126, doi: 10.1016/0304-3835(96)04242-5.
- Rojnik, M., Jevnikar, Z., Mirkovic, B., Janes, D., Zidar, N., Kikelj, D., and Kos, J. (2011) Cathepsin H indirectly regulates morphogenetic protein-4 (BMP-4) in various human cell lines, Radiol. Oncol., 45, 259, doi: 10.2478/V10019-011-0034-3.
- Burton, L. J., Dougan, J., Jones, J., Smith, B. N., Randle, D., Henderson, V., and Odero-Marah, V. A. (2017) Targeting the nuclear cathepsin L CCAAT displacement protein/cut homeobox transcription factor-epithelial mesenchymal transition pathway in prostate and breast cancer cells with the Z-FY-CHO inhibitor, Mol. Cell. Biol., 37, e00297-16, doi: 10.1128/MCB.00297-16.
- Lamort, A. S., Hamon, Y., Czaplewski, C., Gieldon, A., Seren, S., Coquet, L., Lecaille, F., Lesner, A., Lalmanach, G., Gauthier, F., et al. (2019) Processing and maturation of cathepsin C zymogen: a biochemical and molecular modeling analysis, Int. J. Mol. Sci., 20, 4747, doi: 10.3390/IJMS20194747.
- Brodaczewska, K. K., Szczylik, C., Fiedorowicz, M., Porta, C., and Czarnecka, A. M. (2016) Choosing the right cell line for renal cell cancer research, Mol. Cancer, 15, 83, doi: 10.1186/S12943-016-0565-8.
- Sinha, R., Winer, A. G., Chevinsky, M., Jakubowski, C., Chen, Y. B., Dong, Y., Tickoo, S. K., Reuter, V. E., Russo, P., Coleman, J. A., et al. (2017) Analysis of renal cancer cell lines from two major resources enables genomics-guided cell line selection, Nat. Commun., 8, 15165, doi: 10.1038/ncomms15165.
- Carvalho, M., Ferreira, P. J., Mendes, V. S., Silva, R., Pereira, J. A., Jerónimo, C., and Silva, B. M. (2010) Human cancer cell antiproliferative and antioxidant activities of Juglans regia L., Food Chem. Toxicol., 48, 441-447, doi: 10.1016/j.fct.2009.10.043.
- Griffith, T. S., Fialkov, J. M., Williams, R. D., Scott, D. L., Azuhata, T., Sandler, A. D., Wall, N. R., and Altieri, D. C. (2002) Induction and regulation of tumor necrosis factor-related apoptosis-inducing ligand/Apo-2 ligand-mediated apoptosis in renal cell carcinoma, Cancer Res., 62, 3093-3099.
- Yang, Z., Liu, Y., Qin, L., Wu, P., Xia, Z., Luo, M., Zeng, Y., Tsukamoto, H., Ju, Z., Su, D., et al. (2017) Cathepsin H-mediated degradation of HDAC4 for matrix metalloproteinase expression in hepatic stellate cells, Am. J. Pathol., 187, 781-797, doi: 10.1016/J.AJPATH.2016.12.001.
- Goulet, B., Sansregret, L., Leduy, L., Bogyo, M., Weber, E., Chauhan, S. S., and Nepveu, A. (2007) Increased expression and activity of nuclear cathepsin L in cancer cells suggests a novel mechanism of cell transformation, Mol. Cancer Res., 5, 899-907, doi: 10.1158/1541-7786.MCR-07-0160.
- Tamhane, T., Lllukkumbura, R., Lu, S., Maelandsmo, G. M., Haugen, M. H., and Brix, K. (2016) Nuclear cathepsin L activity is required for cell cycle progression of colorectal carcinoma cells, Biochimie, 122, 208-218, doi: 10.1016/j.biochi.2015.09.003.
- Maubach, G., Lim, M. C., and Zhuo, L. (2008) Nuclear cathepsin F regulates activation markers in rat hepatic stellate cells, Mol. Biol. Cell, 19, 4238-4248, doi: 10.1091/mbc.e08-03-0291.
- Goulet, B., Truscott, M., and Nepveu, A. A. (2006) Novel proteolytically processed CDP/Cux isoform of 90 kDa is generated by cathepsin L, Biol. Chem., 387, 1285-1293, doi: 10.1515/BC.2006.159.
- Feng, F., Zhao, Z., Zhou, Y., Cheng, Y., Wu, X., and Heng, X. (2021) CUX1 facilitates the development of oncogenic properties via activating Wnt/β-catenin signaling pathway in glioma, Front. Mol. Biosci., 8, 705008, doi: 10.3389/FMOLB.2021.705008.
- Zhao, M., Mishra, L., and Deng, C. X. (2018) The role of TGF-β/SMAD4 signaling in cancer, Int. J. Biol. Sci., 14, 111, doi: 10.7150/IJBS.23230.
- MaruYama, T., Chen, W. J., and Shibata, H. (2022) TGF-β and cancer immunotherapy, Biol. Pharm. Bull., 45, 155-161, doi: 10.1248/BPB.B21-00966.
- Turk, B., Dolenc, I., Lenarcic, B., Krizaj, I., Turk, V., Bieth, J. G., and Björk, I. (1999) Acidic pH as a physiological regulator of human cathepsin L activity, Eur. J. Biochem., 259, 926-932, doi: 10.1046/j.1432-1327.1999.00145.x.
- Turk, B., Dolenc, I., Zerovnik, E., Turk, D., Gubensek, F., and Turk, V. (1994) Human cathepsin B is a metastable enzyme stabilized by specific ionic interactions associated with the active site, Biochemistry, 33, 14800-14806, doi: 10.1021/bi00253a019.
- Paraoan, L., Ratnayaka, A., Spiller, D. G., Hiscott, P., White, M. R. H., and Grierson, I. (2004) Unexpected intracellular localization of the AMD-associated cystatin C variant, Traffic, 5, 884-895, doi: 10.1111/J.1600-0854.2004.00230.X.
![](/img/style/loading.gif)