Oxidative stress induced by Pollonein-LAAO, a new L-amino acid oxidase from Bothrops moojeni venom, prompts prostate tumor spheroid cell death and impairs the cellular invasion process in vitro.
[en] Cancer cells produce abnormal levels of reactive oxygen species (ROS) that contribute to promote their malignant phenotype. In this framework, we hypothesized that the change in ROS concentration above threshold could impair key events of prostate cancer cells (PC-3) progression. Our results demonstrated that Pollonein-LAAO, a new L-amino acid oxidase obtained from Bothrops moojeni venom, was cytotoxic to PC-3 cells in two-dimensional and in tumor spheroid assays. Pollonein-LAAO was able to increase the intracellular ROS generation that culminates in cell death from apoptosis by both intrinsic and extrinsic pathways due to the up-regulation of TP53, BAX, BAD, TNFRSF10B and CASP8. Additionally, Pollonein-LAAO reduced mitochondrial membrane potential and caused G0/G1 phase to delay, due to the up-regulation of CDKN1A and the down-regulation of the expression of CDK2 and E2F. Interestingly, Pollonein-LAAO inhibited critical steps of the cellular invasion process (migration, invasion and adhesion), due to the down-regulation of SNAI1, VIM, MMP2, ITGA2, ITGAV and ITGB3. Furthermore, the Pollonein-LAAO effects were associated with the intracellular ROS production, since the presence of catalase restored the invasiveness of PC-3 cells. In this sense, this study contributes to the potential use of Pollonein-LAAO as ROS-based agent to enhance the current understanding of cancer treatment strategies.
Disciplines :
Chemistry
Author, co-author :
Polloni, Lorena; Institute of Biotechnology, Federal University of Uberlândia - UFU, Uberlândia, MG, Brazil. Electronic address: polloni.lorena@gmail.com
Costa, Tássia Rafaella; Institute of Biotechnology, Federal University of Uberlândia - UFU, Uberlândia, MG, Brazil
Morais, Lorena Pinheiro; Institute of Biomedical Sciences, Federal University of Uberlândia - UFU, Uberlândia, MG, Brazil
Borges, Bruna Cristina; Institute of Biomedical Sciences, Federal University of Uberlândia - UFU, Uberlândia, MG, Brazil
Teixeira, Samuel Cota; Institute of Biomedical Sciences, Federal University of Uberlândia - UFU, Uberlândia, MG, Brazil
de Melo Fernandes, Thales Alves; Institute of Biotechnology, Federal University of Uberlândia - UFU, Uberlândia, MG, Brazil
Correia, Lucas Ian Veloso; Institute of Biotechnology, Federal University of Uberlândia - UFU, Uberlândia, MG, Brazil
Bastos, Luciana Machado; Institute of Biotechnology, Federal University of Uberlândia - UFU, Uberlândia, MG, Brazil
Gobbi Amorim, Fernanda ; Université de Liège - ULiège > Département de chimie (sciences) > Laboratoire de spectrométrie de masse (L.S.M.) ; Université de Liège - ULiège > Molecular Systems (MolSys)
Quinton, Loïc ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie biologique ; Université de Liège - ULiège > Département de chimie (sciences) > Laboratoire de spectrométrie de masse (L.S.M.)
Soares, Andreimar Martins; Oswaldo Cruz Foundation (FIOCRUZ) Rondônia, Federal University of Rondônia (UNIR), and National Institute of Science and Technology of Epidemiology of the Western Amazon (INCT-EPIAMO), Porto Velho, RO, Brazil
Silva, Marcelo José Barbosa; Institute of Biomedical Sciences, Federal University of Uberlândia - UFU, Uberlândia, MG, Brazil
Ferro, Eloisa Amália Vieira; Institute of Biomedical Sciences, Federal University of Uberlândia - UFU, Uberlândia, MG, Brazil
Lopes, Daiana Silva; Multidisciplinary Institute for Health, Federal University of Bahia - UFBA, Vitoria da Conquista, BA, Brazil
de Melo Rodrigues Ávila, Veridiana; Institute of Biotechnology, Federal University of Uberlândia - UFU, Uberlândia, MG, Brazil. Electronic address: veridiana@ufu.br
Oxidative stress induced by Pollonein-LAAO, a new L-amino acid oxidase from Bothrops moojeni venom, prompts prostate tumor spheroid cell death and impairs the cellular invasion process in vitro.
The present study was supported by the Federal University of Uberlândia (UFU) , the Coordination for the Improvement of Higher Education Personnel (CAPES) , the National Council for Scientific and Technological Development (CNPq) , the Foundation for Support to the Development of Scientific and Technological Actions of Minas Gerais state (FAPEMIG) , the National Institute of Science and Technology in Theranostics and Nanobiotechnology (INCT-TeraNano) , the Foundation for Support to the Development of Scientific and Technological Actions of the Rondônia Research (FAPERO) , PDTIS/FIOCRUZ platforms , the Center for the Study of Biomolecules Applied to Health-CEBio/FIOCRUZ-RO and the Research Excellence Program (PROEP-FIOCRUZ) .The authors thank the GIGA-Proteomics platform (ERDF funding) for the technical support, specially Maximilien Fléron and Dominique Baiwir from GIGA-Proteomics Facility of the University of Liège for the use of the mass spectrometer instruments. Q-Exactive mass spectrometer was funded by ERDF and the Walloon Region grant and Peaks X+ version Studio 10.5 software were funded by ERDF grant: BIOMED HUB Technology Support (number 2.2.1/996 ). The authors thank the Felipe Andrés Cordero da Luz, Ph. D., for perform partial eta squared statistical analysis.The present study was supported by the Federal University of Uberlândia (UFU), the Coordination for the Improvement of Higher Education Personnel (CAPES), the National Council for Scientific and Technological Development (CNPq), the Foundation for Support to the Development of Scientific and Technological Actions of Minas Gerais state (FAPEMIG), the National Institute of Science and Technology in Theranostics and Nanobiotechnology (INCT-TeraNano), the Foundation for Support to the Development of Scientific and Technological Actions of the Rondônia Research (FAPERO), PDTIS/FIOCRUZ platforms, the Center for the Study of Biomolecules Applied to Health-CEBio/FIOCRUZ-RO and the Research Excellence Program (PROEP-FIOCRUZ).The authors thank the GIGA-Proteomics platform (ERDF funding) for the technical support, specially Maximilien Fléron and Dominique Baiwir from GIGA-Proteomics Facility of the University of Liège for the use of the mass spectrometer instruments. Q-Exactive mass spectrometer was funded by ERDF and the Walloon Region grant and Peaks X+ version Studio 10.5 software were funded by ERDF grant: BIOMED HUB Technology Support (number 2.2.1/996). The authors thank the Felipe Andrés Cordero da Luz, Ph. D. for perform partial eta squared statistical analysis.
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Perillo, B., Donato, M., Pezone, A., Zazzo, E., Giovannelli, P., Galasso, G., Castoria, G., Migliaccio, A., ROS in cancer therapy: the bright side of the moon. Exp. Mol. Med. 52:2 (2020), 192–203, 10.1038/s12276-020-0384-2.
Wang, Y., Qi, H., Liu, Y., Duan, C., Liu, X., Xia, T., Chen, D., Piao, H.L., Liu, H.X., The double-edged roles of ROS in cancer prevention and therapy. Theranostics, 11(10), 2021, 4839, 10.7150/thno.56747.
Kim, S.J., Kim, H.S., Seo, Y.R., Understanding of ROS-inducing strategy in anticancer therapy. Oxidative Med. Cell. Longev., 2019, 10.1155/2019/5381692.
Reczek, C.R., Chandel, N.S., The two faces of reactive oxygen species in cancer. Annu. Rev. Cancer Biol., 1, 2017, 4.1-4.20, 10.1146/annurev-cancerbio-041916-065808.
Redza-Dutordoir, M., Averill-Bates, D.A., Activation of apoptosis signaling pathways by reactive oxygen species. Biochim. Biophys. Acta, Mol. Cell Res. 2016 (1863), 2977–2992, 10.1016/j.bbamcr.2016.09.012.
Aggarwal, V., Tuli, H.S., Varol, A., Thakral, F., Yerer, M.B., Sak, K., Varol, M., Jain, A., Khan, M.A., Sethi, G., Role of reactive oxygen species in cancer progression: molecular mechanisms and recent advancements. Biomolecules, 9(11), 2019, 735, 10.3390/biom9110735.
Paloschi, M.V., Pontes, A.S., Soares, A.M., Zuliani, J.P., An update on potential molecular mechanisms underlying the actions of Snake venom L-amino acid oxidases (LAAOs). Curr. Med. Chem. 25:21 (2018), 2520–2530, 10.2174/0929867324666171109114125.
Tan, K.K., Bay, B.H., Gopalakrishnakone, P., L-amino acid oxidase from snake venom and its anticancer potential. Toxicon 144 (2018), 7–13, 10.1016/j.toxicon.2018.01.015.
Arfin, S., Jha, N.K., Jha, S.K., Kesari, K.K., Ruokolainen, J., Roychoudhury, S., Rathi, B., Kumar, D., Oxidative stress in cancer cell metabolism. Antioxidants, 10(5), 2021, 642, 10.3390/antiox10050642.
Carone, S.E.I., Costa, T.R., Burin, S.M., Cintra, A.C.O., Zoccal, K.F., Bianchini, F.J., Tucci, L.F.F., Franco, J.J., Torqueti, M.R., Faccioli, L.H., Albuquerque, S., Castro, F.A., Sampaio, S.V., A new l-amino acid oxidase from Bothrops jararacussu snake venom: isolation, partial characterization, and assessment of pro-apoptotic and antiprotozoal activities. Int. J. Biol. Macromol. 103 (2017), 25–35, 10.1016/j.ijbiomac.2017.05.025.
Matsumoto, H., Haniu, H., Komori, N., Determination of protein molecular weights on SDS-PAGE. Methods Mol. Biol. 2019 (1855), 101–105, 10.1007/978-1-4939-8793-1_10.
Bordon, K.C.F., Wiezel, G.A., Cabral, H., Arantes, E.C., Bordonein-L, a new L-amino acid oxidase from Crotalus durissus terrificus snake venom: isolation, preliminary characterization and enzyme stability. J. Venom Anim. Toxins Incl. Trop. Dis. 21 (2015), 1–9, 10.1186/1678-9199-21-1.
Ma, B., Zhang, K., Hendrie, C., Liang, C., Li, M., Doherty-Kirby, A., Lajoie, G., PEAKS: powerful software for peptide de novo sequencing by tandem mass spectrometry. Rev. Cardiovasc. Med. 17:20 (2003), 2337–2342, 10.1002/rcm.1196.
The UniProt Consortium, UniProt: the universal protein knowledgebase in 2023. Nucleic Acids Res. 51:D1 (2023), D523–D531, 10.1093/nar/gkac1052.
Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., Bourne, P.E., The Protein Data Bank. Nucleic Acids Res. 28:1 (2000), 235–242, 10.1093/nar/28.1.235.
Madeira, F., Pearce, M., Tivey, A.R.N., Basutkar, P., Lee, J., Edbali, O., Madhusoodanan, N., Kolesnikov, A., Lopez, R., Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Res. 50:W1 (2022), W276–W279, 10.1093/nar/gkac240.
Feliciano, P.R., Rustiguel, J.K., Soares, R.O., Sampaio, S.V., Nonato, M.C., Crystal structure and molecular dynamics studies of L-amino acid oxidase from Bothrops atrox. Toxicon 128 (2017), 50–59, 10.1016/j.toxicon.2017.01.017.
McGuffin, L.J., Bryson, K., Jones, D.T., The PSIPRED protein structure prediction server. Bioinformatics 16:4 (2000), 404–405, 10.1093/bioinformatics/16.4.404.
Friedrich, J., Seidel, C., Ebner, R., Kunz-Schughart, L.A., Spheroid-based drug screen: considerations and practical approach. Nat. Protoc. 4 (2009), 309–324, 10.1038/nprot.2008.226.
Cheng, G., Tse, J., Jain, R.K., Munn, L.L., Micro-environmental mechanical stress controls tumor spheroid size and morphology by suppressing proliferation and inducing apoptosis in cancer cells. PLoS One, 4(2), 2009, e4632, 10.1371/journal.pone.0004632.
Zanoni, M., Piccinini, F., Arienti, C., Zamagni, A., Santi, S., Polico, R., Bevilacqua, A., Tesei, A., 3D tumor spheroid models for in vitro therapeutic screening: a systematic approach to enhance the biological relevance of data obtained. Sci. Rep. 6:1 (2016), 1–11, 10.1038/srep19103.
Quiñones, J.P., Roschger, C., Iturmendi, A., Henke, H., Zierer, A., Peniche-Covas, C., Brüggemann, O., Polyphosphazene-based nanocarriers for the release of camptothecin and epirubicin. Pharmaceutics 14:169 (2022), 1–21, 10.3390/pharmaceutics14010169.
Saraiva, D.P., Matias, A.T., Braga, S., Jacinto, A., Cabral, M.G., Establishment of a 3D co-culture with MDA-MB-231 breast cancer cell line and patient-derived immune cells for application in the development of immunotherapies. Front. Oncol., 10, 2020, 1543, 10.3389/fonc.2020.01543.
Yue, P.Y.K., Leung, E.P.Y., Mak, N.K., Wong, R.N.S., A simplified method for quantifying cell migration/wound healing in 96-well plates. SLAS Discov. 15:4 (2010), 427–433, 10.1177/1087057110361772.
Polloni, L., Azevedo, F.V.P.V., Teixeira, S.C., Moura, E., Costa, T.R., Gimenes, S.N.C., Correia, L.I.V., Freitas, V., Yoneyama, K.A.G., Rodrigues, R.S., Lopes, D.S., Rodrigues, V.M., Antiangiogenic effects of phospholipase A2 Lys49 BnSP-7 from Bothrops pauloensis snake venom on endothelial cells: an in vitro and ex vivo approach. Toxicol. in Vitro, 72, 2021, 105099, 10.1016/j.tiv.2021.105099.
Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆c T method. Methods 25:4 (2001), 402–408, 10.1006/meth.2001.1262.
Herzig, V., Cristofori-Armstrong, B., Israel, M.R., Nixon, S.A., Vetter, I., King, G.F., Animal toxins — Nature's evolutionary-refined toolkit for basic research and drug discovery. Biochem. Pharmacol., 18, 2020, 114096, 10.1016/j.bcp.2020.114096.
Oliveira, A.L., Viegas, M.F., Silva, S.L., Soares, A.M., Ramos, M.J., Fernandes, P.A., The chemistry of snake venom and its medicinal potential. Nat. Rev. Chem. 6 (2022), 451–469, 10.1038/s41570-022-00393-7.
Costa, T.R., Burin, S.M., Menaldo, D.L., Castro, F.A., Sampaio, S.V., Snake venom L-amino acid oxidases: an overview on their antitumor effects. J. Venom Anim. Toxins Incl. Trop. Dis. 20 (2014), 1–7, 10.1186/1678-9199-20-1.
Ullah, A., Structure–function studies and mechanism of action of snake venom L-amino acid oxidases. Front. Pharmacol., 11, 2020, 110, 10.3389/fphar.2020.00110.
Stábeli, R.G., Sant'Ana, C.D., Ribeiro, P.H., Costa, T.R., Ticli, F.K., Pires, M.G., Nomizo, A., Albuquerque, S., Malta-Neto, N.R., Marins, M., Sampaio, S.V., Soares, A.M., Cytotoxic L-amino acid oxidase from Bothrops moojeni: biochemical and functional characterization. Int. J. Macromol. 41:2 (2007), 132–140, 10.1016/j.ijbiomac.2007.01.006.
Bhat, S.K., Joshi, M.B., Vasishta, S., Jagadale, R.N., Biligiri, S.G., Coronado, M.A., Arni, R.K., Satyamoorthy, K., P-I metalloproteinases and L-amino acid oxidases from Bothrops species inhibit angiogenesis. J. Venom Anim. Toxins Incl. Trop. Dis. 27 (2021), 1–15, 10.1590/1678-9199-jvatitd-2020-0180.
Barbosa, L.G., Costa, T.R., Borges, I.P., Costa, M.S., Carneiro, A.C., Borges, B.C., Silva, M.J.B., Amorim, F.G., Quinton, L., Yoneyama, K.A.G., Rodrigues, V.M., Sampaio, S.V., Rodrigues, R.S., A comparative study on the leishmanicidal activity of the L-amino acid oxidases BjussuLAAO-II and BmooLAAO-II isolated from Brazilian Bothrops snake venoms. Int. J. Biol. Macromol. 15:167 (2021), 267–278, 10.1016/j.ijbiomac.2020.11.146.
George, S., Abrahamse, H., Redox potential of antioxidants in Cancer progression and prevention. Antioxidants, 9(11), 2020, 1156, 10.3390/antiox9111156.
Abdelkafi-koubaa, Z., ElBini-Dhouib, I., Souid, S., Jebali, J., Doghri, R., Srairi-Abid, N., Essafi-Benkhadir, K., Micheau, O., Marrakchi, N., Pharmacological investigation of CC-LAAO, an L-amino acid oxidase from Cerastes cerastes Snake venom. Toxins 13:904 (2021), 1–16, 10.3390/toxins13120904.
Mahfouz, D.H., El-Magd, M.A., Mansour, G.H., Wahab, A.H.A., Abdelhamid, I.A., Elzayat, E., Therapeutic potential of snake venom, l-amino oxidase and sorafenib in hepatocellular carcinoma. Mol. Cell. Toxicol., 2021, 1–12, 10.1007/s13273-021-00151-8.
Nikodijevic, D.D., Jovankic, J.V., Cvtkovic, D.M., Andelkovic, M.Z., Nikezic, A.G., Milutinovic, M.G., L-amino acid oxidase from snake venom: biotransformation and induction of apoptosis in human colon cancer cells. Eur. J. Pharmacol., 910, 2021, 174466, 10.1016/j.ejphar.2021.174466.
Salama, W.H., Ibrahim, N.M., El Hakim, A.E., Bassuiny, R.I., Mohamed, M.M., Mousa, F.M., Ali, M.M., L-amino acid oxidase from Cerastes vipera snake venom: isolation, characterization, and biological effects on bacteria and tumor cell lines. Toxicon 150 (2018), 270–279, 10.1016/j.toxicon.2018.06.064.
Carneiro, B.A., El-Deiry, W.S., Targeting apoptosis in cancer therapy. Nat. Rev. Clin. Oncol. 17:7 (2020), 395–417, 10.1038/s41571-020-0341-y.
Chota, A., George, B.P., Abrahamse, H., Interactions of multidomain pro-apoptotic and anti-apoptotic proteins in cancer cell death. Oncotarget 12:16 (2021), 1615–1626, 10.18632/oncotarget.28031.
Neophytou, C.M., Panagi, M., Stylianopoulos, T., Papageorgis, P., The role of tumor microenvironment in cancer metastasis: molecular mechanisms and therapeutic opportunities. Cancers, 13(9), 2021, 2053, 10.3390/cancers13092053.
Mukherjee, A.K., Saviola, A.J., Burns, P.D., Apoptosis induction in human breast cancer (MCF-7) cells by a novel venom L-amino acid oxidase (Rusvinoxidase) is independent of its enzymatic activity and is accompanied by caspase-7 activation and reactive oxygen species production. Apoptosis 20:10 (2015), 1358–1372, 10.1007/s10495-015-1157-6.
Costa, T.R., Menaldo, D.L., Zoccal, K.F., Burin, S.M., Aissa, A.F., Castro, F.A., Faccioli, L.H., Antunes, L.M.G., Sampaio, S.V., CR-LAAO, an L-amino acid oxidase from Calloselasma rhodostoma venom, as a potential tool for developing novel immunotherapeutic strategies against cancer. Sci. Rep. 7:1 (2017), 1–12, 10.1038/srep42673.
Wong, R.S.Y., Apoptosis in cancer: from pathogenesis to treatment. J. Exp. Clin. Cancer Res. 30:1 (2011), 1–14, 10.1186/1756-9966-30-87.
Nguyen, C., Pandey, S., Exploiting mitochondrial vulnerabilities to trigger apoptosis selectively in cancer cells. Cancers, 11(7), 2019, 916, 10.3390/cancers11070916.
Engeland, K., Cell cycle regulation: p53-p21-RB signaling. Cell Death Differ. 29:5 (2022), 946–960, 10.1038/s41418-022-00988-z.
Mattews, H.K., Bertoli, C., Bruin, R.A.M., Cell cycle control in cancer. Nat. Rev. Mol. Cell Biol. 23:1 (2022), 74–88, 10.1038/s41580-021-00404-3.
Bertoli, C., Skotheim, J.M., Bruin, R.A.M., Control of cell cycle transcription during G1 and S phases. Nat. Rev. Mol. Cell Biol. 14:8 (2013), 518–528, 10.1038/nrm3629.
Kajstura, M., Halicka, H.D., Pryjma, J., Darzynkiewicz, Z., Discontinuous fragmentation of nuclear DNA during apoptosis revealed by discrete “sub-G1” peaks on DNA content histograms. Cytom.: J. Int. Soc. Anal. Cytol. 71:3 (2007), 125–131, 10.1002/cyto.a.20357.
Wan, G., Tao, J.G., Wang, G.D., Liu, S.P., Zhao, H.X., Liang, Q.D., In vitro antitumor activity of the ethyl acetate extract of Potentilla chinensis in osteosarcoma cancer cells. Mol. Med. Rep. 14:4 (2016), 3634–3640, 10.3892/mmr.2016.5679.
Kämmerer, P.W., Engel, V., Plocksties, F., Jonitz-Heincke, A., Timmermann, D., Engel, N., Frerich, B., Bader, R., Thiem, D.G.E., Skorska, A., David, R., Al-Nawas, B., Dau, M., Continuous electrical stimulation affects initial growth and proliferation of adipose-derived stem cells. Biomedicines, 8(11), 2020, 482, 10.3390/biomedicines8110482.
Abdelkafi-Koubaa, Z., Aissa, I., Morjen, M., Kharrat, N., Ayeb, M.E., Gargouri, Y., Srairi-Abid, N., Marrakchi, N., Interaction of a snake venom L-amino acid oxidase with different cell types membrane. Int. J. Biol. Macromol. 82 (2016), 757–764, 10.1016/j.ijbiomac.2015.09.065.
Suhr, S.M., Kim, D.S., Comparison of the apoptotic pathways induced by L-amino acid oxidase and hydrogen peroxide. J. Biochem. 125 (1999), 305–309, 10.1093/oxfordjournals.jbchem.a022287.
Suhr, S.M., Kim, D.S., Identification of the snake venom substance that induces apoptosis. Biochem. Biophys. Res. Commun. 224:1 (1996), 134–139, 10.1006/bbrc.1996.0996.
Lee, M.L., Fung, S.Y., Chung, I., Pailoor, J., Cheah, S.H., Tan, N.H., King cobra (Ophiophagus hannah) venom L-amino acid oxidase induces apoptosis in PC-3 cells and suppresses PC-3 solid tumor growth in a tumor xenograft mouse model. Int. J. Med. Sci. 11:6 (2014), 593–601, 10.7150/ijms.8096.
Han, S.J., Kwon, S., Kim, K.S., Challenges of applying multicellular tumor spheroids in preclinical phase. Cancer Cell Int. 21:1 (2021), 1–19, 10.1186/s12935-021-01853-8.
Mehta, G., Hsiao, A.Y., Ingram, M., Luker, G.D., Takayama, S., Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy. J. Control. Release 164:2 (2012), 192–204, 10.1016/j.jconrel.2012.04.045.
Pinto, B., Henriques, A.C., Silva, P.M.A., Bousbaa, H., Three-dimensional spheroids as in vitro preclinical models for cancer research. Pharmaceutics, 12(12), 2020, 1186, 10.3390/pharmaceutics12121186.
Welch, D.R., Hurst, D.R., Defining the hallmarks of metastasis. Cancer Res. 79:12 (2019), 3011–3027, 10.1158/0008-5472.CAN-19-0458.
Deep, G., Jain, A.K., Ramteke, A., Ting, H., Vijendra, K.C., Gangar, S.C., Agarwal, C., Agarwal, R., SNAI1 is critical for the aggressiveness of prostate cancer cells with low E-cadherin. Mol. Cancer 13:1 (2014), 1–15, 10.1186/1476-4598-13-37.
Poblete, C.E., Fulla, J., Gallardo, M., Muñoz, V., Castellón, E.A., Gallegos, I., Contreras, H.R., Increased SNAIL expression and low syndecan levels are associated with high Gleason grade in prostate cancer. Int. J. Oncol. 44 (2014), 647–654, 10.3892/ijo.2014.2254.
Gkretsi, V., Stylianopoulos, T., Cell adhesion and matrix stiffness: coordinating cancer cell invasion and metastasis. Front. Oncol., 8, 2018, 145, 10.3389/fonc.2018.00145.
Jiang, W.G., Sanders, A.J., Katoh, M., Ungefroren, H., Gieseler, F., Prince, M., Thompson, S.K., Zollo, M., Spano, D., Dhawan, P., Sliva, D., Subbarayan, P.R., Sarkar, M., Honoki, K., Fujii, H., Georgakilas, A.G., Amedei, A., Niccolai, E., Amin, A., Ashraf, S.S., Ye, L., Helferich, W.G., Yang, X., Boosani, C.S., Guha, G., Ciriolo, M.R., Aquilano, K., Chen, S., Azmi, A.S., Keith, W.N., Bilsland, A., Bhakta, D., Halicka, D., Nowsheen, S., Pantano, F., Santini, D., Tissue invasion and metastasis: molecular, biological and clinical perspectives. Semin. Cancer Biol. 35 (2015), S244–S275, 10.1016/j.semcancer.2015.03.008.
Chaves, L.P., Melo, C.M., Saggioro, F.P., Reis, R.B., Squire, J.A., Epithelial–mesenchymal transition signaling and prostate cancer stem cells: emerging biomarkers and opportunities for precision therapeutics. Genes, 12, 2021, 1900, 10.3390/genes12121900.
Liu, C.Y., Lin, H.H., Tang, M.J., Wang, Y.K., Vimentin contributes to epithelial-mesenchymal transition cancer cell mechanics by mediating cytoskeletal organization and focal adhesion maturation. Oncotarget, 6(18), 2015, 15966, 10.18632/oncotarget.3862.
Kuburich, N.A., Hollander, P.D., Pietz, J.T., Mani, S.A., Vimentin and cytokeratin: good alone, bad together. Semin. Cancer Biol. 86 (2022), 816–826, 10.1016/j.semcancer.2021.12.006.
Pan, B., Guo, J., Liao, Q., Zhao, Y., β1 and β3 integrins in breast, prostate and pancreatic cancer: a novel implication (review). Oncol. Lett. 15 (2018), 5412–5416, 10.3892/ol.2018.8076.
Juan-Rivera, M.C., Martínez-Ferrer, M., Integrin inhibitors in prostate cancer. Cancers, 10(2), 2018, 44, 10.3390/cancers10020044.
Cooper, C.R., Chay, C.H., Pienta, K.J., The role of αvβ3 in prostate cancer progression. Neoplasia 4:3 (2002), 191–194, 10.1038/sj.neo.7900224.
Goel, H.L., Li, J., Kogan, S., Languino, L.R., Integrins in prostate cancer progression. Endocr.-Relat. Cancer 15:3 (2008), 657–664, 10.1677/ERC-08-0019.
Adorno-Cruz, V., Liu, H., Regulation and functions of integrin α2 in cell adhesion and disease. Genes Dis. 6 (2019), 16–24, 10.1016/j.gendis.2018.12.003.
Fares, J., Fares, M.Y., Khachfe, H.H., Salhab, H.A., Fares, Y., Molecular principles of metastasis: a hallmark of cancer revisited. Signal Transduct. Ther. 5:28 (2020), 1–17, 10.1038/s41392-020-0134-x.
Abdel-Hamid, N.M., Abass, S.A., Matrix metalloproteinase contribution in management of cancer proliferation, metastasis and drug targeting. Mol. Biol. Rep. 48 (2021), 6525–6538, 10.1007/s11033-021-06635-z.
Gong, Y., Chippada-Venkata, U.D., Oh, W.K., Roles of matrix metalloproteinases and their natural inhibitors in prostate cancer progression. Cancers 6 (2014), 1298–1327, 10.3390/cancers6031298.
Zhang, L., Shi, J., Feng, J., Klocker, H., Lee, C., Zhang, J., Type IV collagenase (matrix metalloproteinase-2 and -9) in prostate cancer. Prostate Cancer Prostatic Dis. 7 (2004), 327–332, 10.1038/sj.pcan.4500750.
Xie, T., Dong, B., Yan, Y., Hu, G., Xu, Y., Association between MMP-2 expression and prostate cancer: a meta-analysis. Biomed. Rep. 4 (2016), 241–245, 10.3892/br.2015.553.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.