Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Research Article

Selective Cytotoxicity and Changes in Protein Expression of T24 Bladder Carcinoma Permanent Cell Line after Treatment with Hemocyanins

Author(s): Aleksandar Dolashki, Olga Antonova, Lyudmila Velkova*, Dimitar Kaynarov, Wolfgang Voelter and Pavlina Dolashka*

Volume 29, Issue 42, 2022

Published on: 21 September, 2022

Page: [6479 - 6498] Pages: 20

DOI: 10.2174/0929867329666220820095122

Price: $65

Abstract

Background: Some molluscan hemocyanins (Hcs) have significant immunological and antitumor potential, enabling their application in oncology. The antitumor activity of Hcs from marine snails Rapana venosa (RvH), giant keyhole limpet Megathura crenulata (KLH) and garden snails Helix lucorum (HlH), as well as their different derivatives, were studied in vitro on a permanent T24 cell line of bladder cancer and normal urothelial cell line HL 10/29 compared to doxorubicin.

Methods: The antiproliferative activity of the tested Hcs was determined using the WST-1 assay and BrdU ELISA assay. Morphological changes in both urothelial cell lines were confirmed by fluorescence microscopy. The proteomic analysis of a bladder cancer cell line before and after treatment with functional unit (FU) βc-HlH-h using two-dimensional polyacrylamide gel electrophoresis (2D-PAGE) and mass spectrometry revealed differences in the expression of some proteins.

Results: Studies prove that the T24 tumor cell line is dose- and time-dependent, sensitive to the action of the tested isoforms, and it glycosylated FU of these hemocyanins. Selective inhibition of T24 cell growth was observed after incubation with structural subunits (βc-HlH, RvHI and RvHII) and FUs (βc-HlH-h and RvHII-e). Additionally, fluorescent microphotographs did not show apoptotic or necrotic alterations in the normal urothelial cell line HL 10/29. The FU βc-HlH-h demonstrated the highest antiproliferative effect (similarly to doxorubicin), in which predominantly apoptotic and less late apoptotic or necrotic changes in the tumor cells were observed. Several downand up-regulated proteins identified by proteome analysis may be associated with the apoptosis pathway.

Conclusion: The present study illustrated the selectivity of the cytotoxic effect of Hcs against the Т24 cancer cell line. This is the first report of protein expression in T24 human bladder cancer cells under the influence of FU βc-HlH-h. That is probably due to the specific oligosaccharide structures rich in methylated hexoses exposed on the surface of βc-HlH-h.

Keywords: Hemocyanins, cytotoxic effect, Т24 bladder carcinoma permanent cell line, proteomic analysis, apoptosis, protien expression.

[1]
Di Pierro, G.B.; Gulia, C.; Cristini, C.; Fraietta, G.; Marini, L.; Grande, P.; Gentile, V.; Piergentili, R. Bladder cancer: A simple model becomes complex. Curr. Genom., 2012, 13(5), 395-415.
[http://dx.doi.org/10.2174/138920212801619232] [PMID: 23372425]
[2]
Azevedo, R.; Peixoto, A.; Gaiteiro, C.; Fernandes, E.; Neves, M.; Lima, L.; Santos, L.L.; Ferreira, J.A. Over forty years of bladder cancer glycobiology: Where do glycans stand facing precision oncology? Oncotarget, 2017, 8(53), 91734-91764.
[http://dx.doi.org/10.18632/oncotarget.19433] [PMID: 29207682]
[3]
Cragg, G.M.; Pezzuto, J.M. Natural products as a vital source for the discovery of cancer chemotherapeutic and chemopreventive agents. Med. Princ. Pract., 2016, 25(Suppl. 2), 41-59.
[http://dx.doi.org/10.1159/000443404] [PMID: 26679767]
[4]
van Holde, K.E.; Miller, K.I.; Decker, H. Hemocyanins and invertebrate evolution. J. Biol. Chem., 2001, 276(19), 15563-15566.
[http://dx.doi.org/10.1074/jbc.R100010200] [PMID: 11279230]
[5]
Harris, J.R.; Markl, J. Keyhole limpet hemocyanin: Molecular structure of a potent marine immunoactivator. A review. Eur. Urol., 2000, 37(Suppl. 3), 24-33.
[http://dx.doi.org/10.1159/000052389] [PMID: 10828684]
[6]
Mora Román, J.J.; Del Campo, M.; Villar, J.; Paolini, F.; Curzio, G.; Venuti, A.; Jara, L.; Ferreira, J.; Murgas, P.; Lladser, A.; Manubens, A.; Becker, M.I. Immunotherapeutic potential of mollusk hemocyanins in combination with human vaccine adjuvants in murine models of oral cancer. J. Immunol. Res., 2019, 2019, 7076942.
[http://dx.doi.org/10.1155/2019/7076942] [PMID: 30847353]
[7]
Arancibia, S.; Salazar, F.; Becker, M.I. Hemocyanins in the immunotherapy of superficial bladder cancer. Bladder Cancer-From Basic to Robotic Surgery; Canda, A.E., Ed.; InTech: Rijeka, Croatia, 2012, pp. 221-242.
[http://dx.doi.org/10.5772/28281]
[8]
Coates, C.J.; Decker, H. Immunological properties of oxygen-transport proteins: Hemoglobin, hemocyanin and hemerythrin. Cell. Mol. Life Sci., 2017, 74(2), 293-317.
[http://dx.doi.org/10.1007/s00018-016-2326-7] [PMID: 27518203]
[9]
Georgieva, A.; Todorova, K.; Iliev, I.; Dilcheva, V.; Vladov, I.; Petkova, S.; Toshkova, R.; Velkova, L.; Dolashki, A.; Dolashka, P. Hemocyanins from Helix and Rapana snails exhibit in vitro antitumor effects in human colorectal adenocarcinoma. Biomedicines, 2020, 8(7), 194.
[http://dx.doi.org/10.3390/biomedicines8070194] [PMID: 32635655]
[10]
Miles, D.; Roché, H.; Martin, M.; Perren, T.J.; Cameron, D.A.; Glaspy, J.; Dodwell, D.; Parker, J.; Mayordomo, J.; Tres, A.; Murray, J.L.; Ibrahim, N.K. Phase III multicenter clinical trial of the sialyl-TN (STn)-keyhole limpet hemocyanin (KLH) vaccine for metastatic breast cancer. Oncologist, 2011, 16(8), 1092-1100.
[http://dx.doi.org/10.1634/theoncologist.2010-0307] [PMID: 21572124]
[11]
Musselli, C.; Livingston, P.O.; Ragupathi, G. Keyhole limpet hemocyanin conjugate vaccines against cancer: The Memorial Sloan Kettering experience. J. Cancer Res. Clin. Oncol., 2001, 127(Suppl. 2), R20-R26.
[http://dx.doi.org/10.1007/BF01470995] [PMID: 11768620]
[12]
Neelapu, S.S.; Baskar, S.; Kwak, L.W. Detection of keyhole limpet hemocyanin (KLH)-specific immune responses by intracellular cytokine assay in patients vaccinated with idiotype-KLH vaccine. J. Cancer Res. Clin. Oncol., 2001, 127(Suppl. 2), R14-R19.
[http://dx.doi.org/10.1007/BF01470994] [PMID: 11768619]
[13]
Lammers, R.J.; Witjes, W.P.; Janzing-Pastors, M.H.; Caris, C.T.; Witjes, J.A. Intracutaneous and intravesical immunotherapy with keyhole limpet hemocyanin compared with intravesical mitomycin in patients with non-muscle-invasive bladder cancer: Results from a prospective randomized phase III trial. J. Clin. Oncol., 2012, 30(18), 2273-2279.
[http://dx.doi.org/10.1200/JCO.2011.39.2936] [PMID: 22585689]
[14]
Kurokawa, T.; Wuhrer, M.; Lochnit, G.; Geyer, H.; Markl, J.; Geyer, R. Hemocyanin from the keyhole limpet Megathura crenulata (KLH) carries a novel type of N-glycans with Gal(β1-6)Man-motifs. Eur. J. Biochem., 2002, 269(22), 5459-5473.
[http://dx.doi.org/10.1046/j.1432-1033.2002.03244.x] [PMID: 12423344]
[15]
Wuhrer, M.; Robijn, M.L.M.; Koeleman, C.A.M.; Balog, C.I.A.; Geyer, R.; Deelder, A.M.; Hokke, C.H. A novel Gal(beta1-4)Gal(beta1-4)Fuc(alpha1-6)-core modification attached to the proximal N-acetylglucosamine of keyhole limpet haemocyanin (KLH) N-glycans. Biochem. J., 2004, 378(Pt 2), 625-632.
[http://dx.doi.org/10.1042/bj20031380] [PMID: 14613482]
[16]
Wirguin, I.; Suturkova-Milosević, L.; Briani, C.; Latov, N. Keyhole limpet hemocyanin contains Gal(beta 1-3)-GalNAc determinants that are cross-reactive with the T antigen. Cancer Immunol. Immunother., 1995, 40(5), 307-310.
[PMID: 7600562]
[17]
Moltedo, B.; Faunes, F.; Haussmann, D.; De Ioannes, P.; De Ioannes, A.E.; Puente, J.; Becker, M.I. Immunotherapeutic effect of Concholepas hemocyanin in the murine bladder cancer model: Evidence for conserved antitumor properties among hemocyanins. J. Urol., 2006, 176(6 Pt 1), 2690-2695.
[http://dx.doi.org/10.1016/j.juro.2006.07.136] [PMID: 17085197]
[18]
Becker, M.I.; Arancibia, S.; Salazar, F.; Del Campo, M.; De Ioannes, A. Mollusk hemocyanins as natural immunostimulants in biomedical applications. In: Immune Response Activation; Guy, H.T.D., Ed.; InTech: Rijeka, Croatia, 2014, pp. 45-72.
[http://dx.doi.org/10.5772/57552]
[19]
Dolashka, P.; Velkova, L.; Iliev, I.; Beck, A.; Dolashki, A.; Yossifova, L.; Toshkova, R.; Voelter, W.; Zacharieva, S. Antitumor activity of glycosylated molluscan hemocyanins viaGuerin ascites tumor. Immunol. Invest., 2011, 40(2), 130-149.
[http://dx.doi.org/10.3109/08820139.2010.513408] [PMID: 20923331]
[20]
Riggs, D.R.; Jackson, B.J.; Vona-Davis, L.; Nigam, A.; McFadden, D.W. In vitro effects of keyhole limpet hemocyanin in breast and pancreatic cancer in regards to cell growth, cytokine production, and apoptosis. Am. J. Surg., 2005, 189(6), 680-684.
[http://dx.doi.org/10.1016/j.amjsurg.2004.10.005] [PMID: 15910720]
[21]
Dolashki, A.; Dolashka, P.; Stenzl, A.; Stevanovic, S.; Aicher, W.K.; Velkova, L.; Velikova, R.; Voelter, W. Antitumour activity of Helix hemocyanin against bladder carcinoma permanent cell lines. Biotechnol. Biotechnol. Equip., 2019, 33(1), 20-32.
[http://dx.doi.org/10.1080/13102818.2018.1507755]
[22]
Zheng, L.; Zhao, X.; Zhang, P.; Chen, C.; Liu, S.; Huang, R.; Zhong, M.; Wei, C.; Zhang, Y. Hemocyanin from Shrimp Litopenaeus vannamei has antiproliferative effect against HeLa cell in vitro. PLoS One, 2016, 11(3), e0151801.
[http://dx.doi.org/10.1371/journal.pone.0151801] [PMID: 27007573]
[23]
Boyanova, O.; Dolashka, P.; Toncheva, D.; Rammensee, H.G.; Stevanović, S. In vitro effect of molluscan hemocyanins on CAL-29 and T-24 bladder cancer cell lines. Biomed. Rep., 2013, 1(2), 235-238.
[http://dx.doi.org/10.3892/br.2012.46] [PMID: 24648926]
[24]
Antonova, O.; Dolashka, P.; Toncheva, D.; Rammensee, H.G.; Floetenmeyer, M.; Stevanovic, S. In vitro antiproliferative effect of Helix aspersa hemocyanin on multiple malignant cell lines. Z. Naturforsch. C.J. Biosci, 2014, 69(7-8), 325-334.
[http://dx.doi.org/10.5560/znc.2013-0148] [PMID: 25265853]
[25]
Dolashka-Angelova, P.; Beck, A.; Dolashki, A.; Stevanovic, S.; Beltramini, M.; Salvato, B.; Hristova, R.; Velkova, L.; Voelter, W. Carbohydrate moieties of molluscan Rapana venosa hemocyanin. Micron, 2004, 35(1-2), 101-104.
[http://dx.doi.org/10.1016/j.micron.2003.10.032] [PMID: 15036306]
[26]
Sandra, K.; Dolashka-Angelova, P.; Devreese, B.; Van Beeumen, J. New insights in Rapana venosa hemocyanin N-glycosylation resulting from on-line mass spectrometric analyses. Glycobiology, 2007, 17(2), 141-156.
[http://dx.doi.org/10.1093/glycob/cwl063] [PMID: 17068122]
[27]
Dolashka-Angelova, P.; Lieb, B.; Velkova, L.; Heilen, N.; Sandra, K.; Nikolaeva-Glomb, L.; Dolashki, A.; Galabov, A.S.; Van Beeumen, J.; Stevanovic, S.; Voelter, W.; Devreese, B. Identification of glycosylated sites in Rapana hemocyanin by mass spectrometry and gene sequence, and their antiviral effect. Bioconjug. Chem., 2009, 20(7), 1315-1322.
[http://dx.doi.org/10.1021/bc900034k] [PMID: 19499947]
[28]
Dolashka, P.; Velkova, L.; Shishkov, S.; Kostova, K.; Dolashki, A.; Dimitrov, I.; Atanasov, B.; Devreese, B.; Voelter, W.; Van Beeumen, J. Glycan structures and antiviral effect of the structural subunit RvH2 of Rapana hemocyanin. Carbohydr. Res., 2010, 345(16), 2361-2367.
[http://dx.doi.org/10.1016/j.carres.2010.08.005] [PMID: 20863484]
[29]
Velkova, L.; Dolashka, P.; Van Beeumen, J.; Devreese, B. N-glycan structures of β-HlH subunit of Helix lucorum hemocyanin. Carbohydr. Res., 2017, 449, 1-10.
[http://dx.doi.org/10.1016/j.carres.2017.06.012] [PMID: 28672164]
[30]
Velkova, L.; Dimitrov, I.; Schwarz, H.; Stevanovic, S.; Voelter, W.; Salvato, B.; Dolashka-Angelova, P. Structure of hemocyanin from garden snail Helix lucorum. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 2010, 157(1), 16-25.
[http://dx.doi.org/10.1016/j.cbpb.2010.04.012] [PMID: 20433940]
[31]
Dolashka-Angelova, P.; Schwarz, H.; Dolashki, A.; Stevanovic, S.; Fecker, M.; Saeed, M.; Voelter, W. Oligomeric stability of Rapana venosa hemocyanin (RvH) and its structural subunits. Biochim. Biophys. Acta, 2003, 1646(1-2), 77-85.
[http://dx.doi.org/10.1016/S1570-9639(02)00549-6] [PMID: 12637014]
[32]
Rosenfeld, J.; Capdevielle, J.; Guillemot, J.C.; Ferrara, P. In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal. Biochem., 1992, 203(1), 173-179.
[http://dx.doi.org/10.1016/0003-2697(92)90061-B] [PMID: 1524213]
[33]
Liu, T.; Song, P.; Märcher, A.; Kjems, J.; Yang, C.; Gothelf, K.V. Selective delivery of doxorubicin to EGFR+ cancer cells by cetuximab-DNA conjugates. ChemBioChem, 2019, 20(8), 1014-1018.
[http://dx.doi.org/10.1002/cbic.201800685] [PMID: 30589193]
[34]
Latosinska, A.; Makridakis, M.; Frantzi, M.; Borràs, D.M.; Janssen, B.; Mullen, W.; Zoidakis, J.; Merseburger, A.S.; Jankowski, V.; Mischak, H.; Vlahou, A. Integrative analysis of extracellular and intracellular bladder cancer cell line proteome with transcriptome: Improving coverage and validity of–omics findings. Sci. Rep., 2016, 6(1), 1-12.
[http://dx.doi.org/10.1038/srep25619] [PMID: 28442746]
[35]
Lei, T.; Zhao, X.; Jin, S.; Meng, Q.; Zhou, H.; Zhang, M. Discovery of potential bladder cancer biomarkers by comparative urine proteomics and analysis. Clin. Genitourin. Cancer, 2013, 11(1), 56-62.
[http://dx.doi.org/10.1016/j.clgc.2012.06.003] [PMID: 22982111]
[36]
Tisdale, E.J. Glyceraldehyde-3-phosphate dehydrogenase is phosphorylated by protein kinase Ciota /λ and plays a role in microtubule dynamics in the early secretory pathway. J. Biol. Chem., 2002, 277(5), 3334-3341.
[http://dx.doi.org/10.1074/jbc.M109744200] [PMID: 11724794]
[37]
Rahmat, J.N.; Esuvaranathan, K.; Mahendran, R. Bacillus Calmette-Guérin induces rapid gene expression changes in human bladder cancer cell lines that may modulate its survival. Oncol. Lett., 2018, 15(6), 9231-9241.
[PMID: 29844825]
[38]
Hwang, N.R.; Yim, S.H.; Kim, Y.M.; Jeong, J.; Song, E.J.; Lee, Y.; Lee, J.H.; Choi, S.; Lee, K.J. Oxidative modifications of glyceraldehyde-3-phosphate dehydrogenase play a key role in its multiple cellular functions. Biochem. J., 2009, 423(2), 253-264.
[http://dx.doi.org/10.1042/BJ20090854] [PMID: 19650766]
[39]
Bogaards, J.J.; Venekamp, J.C.; van Bladeren, P.J. Stereoselective conjugation of prostaglandin A2 and prostaglandin J2 with glutathione, catalyzed by the human glutathione S-transferases A1-1, A2-2, M1a-1a, and P1-1. Chem. Res. Toxicol., 1997, 10(3), 310-317.
[http://dx.doi.org/10.1021/tx9601770] [PMID: 9084911]
[40]
Sun, K.H.; Chang, K.H.; Clawson, S.; Ghosh, S.; Mirzaei, H.; Regnier, F.; Shah, K. Glutathione-S-transferase P1 is a critical regulator of CDK5 kinase activity. J. Neurochem., 2011, 118(5), 902-914.
[http://dx.doi.org/10.1111/j.1471-4159.2011.07343.x] [PMID: 21668448]
[41]
Almeida-Souza, L.; Goethals, S.; de Winter, V.; Dierick, I.; Gallardo, R.; Van Durme, J.; Irobi, J.; Gettemans, J.; Rousseau, F.; Schymkowitz, J.; Timmerman, V.; Janssens, S. Increased monomerization of mutant HSPB1 leads to protein hyperactivity in Charcot-Marie-Tooth neuropathy. J. Biol. Chem., 2010, 285(17), 12778-12786.
[http://dx.doi.org/10.1074/jbc.M109.082644] [PMID: 20178975]
[42]
Kostenko, S.; Johannessen, M.; Moens, U. PKA-induced F-actin rearrangement requires phosphorylation of Hsp27 by the MAPKAP kinase MK5. Cell. Signal., 2009, 21(5), 712-718.
[http://dx.doi.org/10.1016/j.cellsig.2009.01.009] [PMID: 19166925]
[43]
Holmgren, A.; Bouhy, D.; De Winter, V.; Asselbergh, B.; Timmermans, J.P.; Irobi, J.; Timmerman, V. Charcot-Marie-Tooth causing HSPB1 mutations increase Cdk5-mediated phosphorylation of neurofilaments. Acta Neuropathol., 2013, 126(1), 93-108.
[http://dx.doi.org/10.1007/s00401-013-1133-6] [PMID: 23728742]
[44]
Winn, S.I.; Watson, H.C.; Harkins, R.N.; Fothergill, L.A. Structure and activity of phosphoglycerate mutase. Philos. Trans. R. Soc. Lond. B Biol. Sci., 1981, 293(1063), 121-130.
[http://dx.doi.org/10.1098/rstb.1981.0066] [PMID: 6115412]
[45]
Peng, X.C.; Gong, F.M.; Chen, Y.; Qiu, M.; Cheng, K.; Tang, J.; Ge, J.; Chen, N.; Zeng, H.; Liu, J.Y. Proteomics identification of PGAM1 as a potential therapeutic target for urothelial bladder cancer. J. Proteomics, 2016, 132, 85-92.
[http://dx.doi.org/10.1016/j.jprot.2015.11.027] [PMID: 26655504]
[46]
Richard, J.P. Kinetic parameters for the elimination reaction catalyzed by triosephosphate isomerase and an estimation of the reaction’s physiological significance. Biochemistry, 1991, 30(18), 4581-4585.
[http://dx.doi.org/10.1021/bi00232a031] [PMID: 2021650]
[47]
Rodríguez-Almazán, C.; Arreola, R.; Rodríguez-Larrea, D.; Aguirre-López, B.; de Gómez-Puyou, M.T.; Pérez-Montfort, R.; Costas, M.; Gómez-Puyou, A.; Torres-Larios, A. Structural basis of human triosephosphate isomerase deficiency: Mutation E104D is related to alterations of a conserved water network at the dimer interface. J. Biol. Chem., 2008, 283(34), 23254-23263.
[http://dx.doi.org/10.1074/jbc.M802145200] [PMID: 18562316]
[48]
Shao, G.; Zhou, H.; Zhang, Q.; Jin, Y.; Fu, C. Advancements of Annexin A1 in inflammation and tumorigenesis. OncoTargets Ther., 2019, 12, 3245-3254.
[http://dx.doi.org/10.2147/OTT.S202271] [PMID: 31118675]
[49]
Yu, S.; Meng, Q.; Hu, H.; Zhang, M. Correlation of ANXA1 expression with drug resistance and relapse in bladder cancer. Int. J. Clin. Exp. Pathol., 2014, 7(9), 5538-5548.
[PMID: 25337195]
[50]
Challa, A.A.; Stefanovic, B. A novel role of vimentin filaments: Binding and stabilization of collagen mRNAs. Mol. Cell. Biol., 2011, 31(18), 3773-3789.
[http://dx.doi.org/10.1128/MCB.05263-11] [PMID: 21746880]
[51]
Partridge, A.H.; Burstein, H.J.; Winer, E.P. Side effects of chemotherapy and combined chemohormonal therapy in women with early-stage breast cancer. J. Natl. Cancer Inst. Monogr., 2001, 2001(30), 135-142.
[http://dx.doi.org/10.1093/oxfordjournals.jncimonographs.a003451] [PMID: 11773307]
[52]
Bayat Mokhtari, R.; Homayouni, T.S.; Baluch, N.; Morgatskaya, E.; Kumar, S.; Das, B.; Yeger, H. Combination therapy in combating cancer. Oncotarget, 2017, 8(23), 38022-38043.
[http://dx.doi.org/10.18632/oncotarget.16723] [PMID: 28410237]
[53]
Roh, Y.G.; Mun, M.H.; Jeong, M.S.; Kim, W.T.; Lee, S.R.; Chung, J.W.; Kim, S.I.; Kim, T.N.; Nam, J.K.; Leem, S.H. Drug resistance of bladder cancer cells through activation of ABCG2 by FOXM1. BMB Rep., 2018, 51(2), 98-103.
[http://dx.doi.org/10.5483/BMBRep.2018.51.2.222] [PMID: 29397866]
[54]
Chen, Y.; Zhu, G.; Wu, K.; Gao, Y.; Zeng, J.; Shi, Q.; Guo, P.; Wang, X.; Chang, L.S.; Li, L.; He, D. FGF2-mediated reciprocal tumor cell-endothelial cell interplay contributes to the growth of chemoresistant cells: A potential mechanism for superficial bladder cancer recurrence. Tumour Biol., 2016, 37(4), 4313-4321.
[http://dx.doi.org/10.1007/s13277-015-4214-4] [PMID: 26493998]
[55]
Toshkova, R.; Ivanova, E.; Hristova, R.; Voelter, W.; Dolashka-Angelova, P. Effect of Rapana venosa hemocyanin on antibody-dependent cell cytotoxicicity (ADCC) and mitogen responsibility of lymphocytes from hamsters with progressing myeloid tumors. World J. Med. Sci., 2009, 4(2), 135-142.
[56]
Kobata, A. A journey to the world of glycobiology. Glycoconj. J., 2000, 17(7-9), 443-464.
[http://dx.doi.org/10.1023/A:1011006122704] [PMID: 11421342]
[57]
Gorelik, E.; Galili, U.; Raz, A. On the role of cell surface carbohydrates and their binding proteins (lectins) in tumor metastasis. Cancer Metastasis Rev., 2001, 20(3-4), 245-277.
[http://dx.doi.org/10.1023/A:1015535427597] [PMID: 12085965]
[58]
Pocheć, E.; Lityńska, A.; Amoresano, A.; Casbarra, A. Glycosylation profile of integrin α 3 β 1 changes with melanoma progression. Biochim. Biophys. Acta, 2003, 1643(1-3), 113-123.
[http://dx.doi.org/10.1016/j.bbamcr.2003.10.004] [PMID: 14654234]
[59]
Ben-Ze’ev, A. Cytoskeletal and adhesion proteins as tumor suppressors. Curr. Opin. Cell Biol., 1997, 9(1), 99-108.
[http://dx.doi.org/10.1016/S0955-0674(97)80158-5] [PMID: 9013672]
[60]
Becker, K.F.; Höfler, H. Mutant cell surface receptors as targets for individualized cancer diagnosis and therapy. Curr. Cancer Drug Targets, 2001, 1(2), 121-128.
[http://dx.doi.org/10.2174/1568009013334205] [PMID: 12188885]
[61]
Lekka, M.; Laidler, P.; Labedź, M.; Kulik, A.J.; Lekki, J.; Zając, W.; Stachura, Z. Specific detection of glycans on a plasma membrane of living cells with atomic force microscopy. Chem. Biol., 2006, 13(5), 505-512.
[http://dx.doi.org/10.1016/j.chembiol.2006.03.006] [PMID: 16720271]
[62]
Przybyło, M.; Lityńska, A.; Pocheć, E. Different adhesion and migration properties of human HCV29 non-malignant urothelial and T24 bladder cancer cells: Role of glycosylation. Biochimie, 2005, 87(2), 133-142.
[http://dx.doi.org/10.1016/j.biochi.2004.12.003] [PMID: 15760705]
[63]
Geyer, H.; Wuhrer, M.; Resemann, A.; Geyer, R. Identification and characterization of keyhole limpet hemocyanin N-glycans mediating cross-reactivity with Schistosoma mansoni. J. Biol. Chem., 2005, 280(49), 40731-40748.
[http://dx.doi.org/10.1074/jbc.M505985200] [PMID: 16135511]
[64]
Antonova, O.; Yossifova, L.; Staneva, R.; Stevanovic, S.; Dolashka, P.; Toncheva, D. Changes in the gene expression profile of the bladder cancer cell lines after treatment with Helix lucorum and Rapana venosa hemocyanin. J. BUON, 2015, 20(1), 180-187.
[PMID: 25778314]
[65]
Stenzl, A.; Dolashki, A.; Stevanovic, S.; Voelter, W.; Aicher, W.; Dolashka, P. Cytotoxic effects of Rapana venosa hemocyanin on bladder cancer permanent cell lines. J. US. China Med. Sci., 2016, 13, 79-188.
[66]
Kaps, A.; Gwiazdoń, P.; Chodurek, E. Nanoformulations for delivery of pentacyclic triterpenoids in anticancer therapies. Molecules, 2021, 26(6), 1764.
[http://dx.doi.org/10.3390/molecules26061764] [PMID: 33801096]
[67]
Chaabane, W.; User, S.D.; El-Gazzah, M.; Jaksik, R.; Sajjadi, E.; Rzeszowska-Wolny, J.; Los, M.J. Autophagy, apoptosis, mitoptosis and necrosis: Interdependence between those pathways and effects on cancer. Arch. Immunol. Ther. Exp. (Warsz.), 2013, 61(1), 43-58.
[http://dx.doi.org/10.1007/s00005-012-0205-y] [PMID: 23229678]
[68]
El Ouar, I.; Braicu, C.; Naimi, D.; Irimie, A.; Berindan-Neagoe, I. Effect of Helix aspersa extract on TNFα, NF-κB and some tumor suppressor genes in breast cancer cell line Hs578T. Pharmacogn. Mag., 2017, 13(50), 281-285.
[http://dx.doi.org/10.4103/0973-1296.204618] [PMID: 28539722]
[69]
Somasundar, P.; Riggs, D.R.; Jackson, B.J.; McFadden, D.W. Inhibition of melanoma growth by hemocyanin occurs via early apoptotic pathways. Am. J. Surg., 2005, 190(5), 713-716.
[http://dx.doi.org/10.1016/j.amjsurg.2005.07.008] [PMID: 16226945]
[70]
Ischia, J.; So, A.I. The role of heat shock proteins in bladder cancer. Nat. Rev. Urol., 2013, 10(7), 386-395.
[http://dx.doi.org/10.1038/nrurol.2013.108] [PMID: 23670183]
[71]
Kamada, M.; So, A.; Muramaki, M.; Rocchi, P.; Beraldi, E.; Gleave, M. Hsp27 knockdown using nucleotide-based therapies inhibit tumor growth and enhance chemotherapy in human bladder cancer cells. Mol. Cancer Ther., 2007, 6(1), 299-308.
[http://dx.doi.org/10.1158/1535-7163.MCT-06-0417] [PMID: 17218637]
[72]
Bauer, K.; Nitsche, U.; Slotta-Huspenina, J.; Drecoll, E.; von Weyhern, C.H.; Rosenberg, R.; Höfler, H.; Langer, R. High HSP27 and HSP70 expression levels are independent adverse prognostic factors in primary resected colon cancer. Cell Oncol. (Dordr.), 2012, 35(3), 197-205.
[http://dx.doi.org/10.1007/s13402-012-0079-3] [PMID: 22535481]
[73]
Pavan, S.; Musiani, D.; Torchiaro, E.; Migliardi, G.; Gai, M.; Di Cunto, F.; Erriquez, J.; Olivero, M.; Di Renzo, M.F. HSP27 is required for invasion and metastasis triggered by hepatocyte growth factor. Int. J. Cancer, 2014, 134(6), 1289-1299.
[http://dx.doi.org/10.1002/ijc.28464] [PMID: 23996744]
[74]
Wang, X.; Chen, M.; Zhou, J.; Zhang, X. HSP27, 70 and 90, anti-apoptotic proteins, in clinical cancer therapy (Review). Int. J. Oncol., 2014, 45(1), 18-30.
[http://dx.doi.org/10.3892/ijo.2014.2399] [PMID: 24789222]
[75]
Kang, W.Y.; Chen, W.T.; Huang, Y.C.; Su, Y.C.; Chai, C.Y. Overexpression of annexin 1 in the development and differentiation of urothelial carcinoma. Kaohsiung J. Med. Sci., 2012, 28(3), 145-150.
[http://dx.doi.org/10.1016/j.kjms.2011.10.004] [PMID: 22385607]
[76]
Chen, T.; Huang, Z.; Tian, Y.; Lin, B.; He, R.; Wang, H.; Ouyang, P.; Chen, H.; Wu, L. Clinical significance and prognostic value of triosephosphate isomerase expression in gastric cancer. Medicine (Baltimore), 2017, 96(19), e6865.
[http://dx.doi.org/10.1097/MD.0000000000006865] [PMID: 28489783]
[77]
Montgomerie, J.Z.; Gracy, R.W.; Holshuh, H.J.; Keyser, A.J.; Bennett, C.J.; Schick, D.G. The 28K protein in urinary bladder, squamous metaplasia and urine is triosephosphate isomerase. Clin. Biochem., 1997, 30(8), 613-618.
[http://dx.doi.org/10.1016/S0009-9120(97)00115-X] [PMID: 9455614]
[78]
Liu, K.; Tang, Z.; Huang, A.; Chen, P.; Liu, P.; Yang, J.; Lu, W.; Liao, J.; Sun, Y.; Wen, S.; Hu, Y.; Huang, P. Glyceraldehyde-3-phosphate dehydrogenase promotes cancer growth and metastasis through upregulation of SNAIL expression. Int. J. Oncol., 2017, 50(1), 252-262.
[http://dx.doi.org/10.3892/ijo.2016.3774] [PMID: 27878251]
[79]
Ganapathy-Kanniappan, S.; Kunjithapatham, R.; Geschwind, J.F. Glyceraldehyde-3-phosphate dehydrogenase: A promising target for molecular therapy in hepatocellular carcinoma. Oncotarget, 2012, 3(9), 940-953.
[http://dx.doi.org/10.18632/oncotarget.623] [PMID: 22964488]
[80]
Krasnov, G.S.; Dmitriev, A.A.; Snezhkina, A.V.; Kudryavtseva, A.V. Deregulation of glycolysis in cancer: Glyceraldehyde-3-phosphate dehydrogenase as a therapeutic target. Expert Opin. Ther. Targets, 2013, 17(6), 681-693.
[http://dx.doi.org/10.1517/14728222.2013.775253] [PMID: 23445303]
[81]
Lazarev, V.F.; Guzhova, I.V.; Margulis, B.A. Glyceraldehyde-3-phosphate dehydrogenase is a multifaceted therapeutic target. Pharmaceutics, 2020, 12(5), 416.
[http://dx.doi.org/10.3390/pharmaceutics12050416] [PMID: 32370188]
[82]
Li, T.; Tan, X.; Yang, R.; Miao, Y.; Zhang, M.; Xi, Y.; Guo, R.; Zheng, M.; Li, B. Discovery of novel glyceraldehyde-3-phosphate dehydrogenase inhibitor via docking-based virtual screening. Bioorg. Chem., 2020, 96, 103620.
[http://dx.doi.org/10.1016/j.bioorg.2020.103620] [PMID: 32028064]
[83]
Tamada, M.; Suematsu, M.; Saya, H. Pyruvate kinase M2: Multiple faces for conferring benefits on cancer cells. Clin. Cancer Res., 2012, 18(20), 5554-5561.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-0859] [PMID: 23071357]
[84]
Zhu, Q.; Hong, B.; Zhang, L.; Wang, J. Pyruvate kinase M2 inhibits the progression of bladder cancer by targeting MAKP pathway. J. Cancer Res. Ther., 2018, 14(10), S616-S621.
[http://dx.doi.org/10.4103/0973-1482.187302] [PMID: 30249877]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy