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Evaluation of the Effect of RhoB Inhibition on Cancer Stem Cell Properties in NSCLC A549 Cells

Year 2020, Volume: 10, 29 - 36, 31.12.2020

Fathiya Rahmı Hiba Khaır Isık Didem Karagoz

Abstract

The cancer stem cells model suggests that a small subgroup of cancer cells can self-renew and substantially leads to the recurrence of tumors. Such cells are thought to be a reservoir for the regeneration of tumor-initiating mutant cells, which are insensitive to the chemotherapy currently being used. RhoB GTPase is implicated in regulating cell survival, tumorigenesis, angiogenesis, migration, and metastasis. Higher degrees of tumor progression and invasiveness are associated with RhoB expression. The contribution of Rho GTPases, in particular RhoB, in cancer stem cell properties, has not yet been fully explored. This study aims to explore the possible relationship between RhoB expression and the in vitro cancer stem cell-like characteristics of non-small cell lung cancer cells such as spheroid formation and self-renewal. To determine whether the depletion of RhoB could promote CSC-like characteristics, RhoB siRNA or AllStars siRNA negative control were transfected into A549 cells. The spheroid formation assay was used to evaluate the ability of cells to grow in anchorage-independent conditions to form spheroids. The results demonstrated that RhoB knockdown did not have a statistically significant effect in promoting cancer stem-like properties in A549 cells. This study may lead to further understanding of the contribution of RhoB to in vitro cancer stem cell features such as, the formation of tumorspheroids.

Keywords

CSCs RhoB siRNA Spheroid formation Self-renewal

References

  • Adnane, J., Seijo, E., Chen, Z., Bizouarn, F., Leal, M., Sebti, S. M., & Muñoz-Antonia, T. (2002). RhoB, not RhoA, represses the transcription of the transforming growth factor β type II receptor by a mechanism involving activator protein 1. Journal of Biological Chemistry, 277(10), 8500-8507.
  • Aznar, S., & Lacal, J. C. (2001). Rho signals to cell growth and apoptosis. Cancer letters, 165(1), 1-10.
  • Bar-Sagi, D., & Hall, A. (2000). Ras and Rho GTPases: a family reunion. Cell, 103(2), 227-238.
  • Bertolini, G., Roz, L., Perego, P., Tortoreto, M., Fontanella, E., Gatti, L., ... & Roz, E. (2009). Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proceedings of the National Academy of Sciences, 106(38), 16281-16286.
  • Bishop, A. L., & Hall, A. (2000). Rho GTPases and their effector proteins. Biochemical Journal, 348(2), 241-255.
  • Bousquet, E., Mazières, J., Privat, M., Rizzati, V., Casanova, A., Ledoux, A., ... & Pradines, A. (2009). Loss of RhoB expression promotes migration and invasion of human bronchial cells via activation of AKT1. Cancer research, 69(15), 6092-6099.
  • Bousquet, E., Calvayrac, O., Mazieres, J., Lajoie-Mazenc, I., Boubekeur, N., Favre, G., & Pradines, A. (2016). RhoB loss induces Rac1-dependent mesenchymal cell invasion in lung cells through PP2A inhibition. Oncogene, 35(14), 1760-1769.
  • Calvayrac, O., Pradines, A., Raymond-Letron, I., Rouquette, I., Bousquet, E., Lauwers-Cances, V., ... & Milia, J. (2014). RhoB determines tumor aggressiveness in a murine EGFRL858R-induced adenocarcinoma model and is a potential prognostic biomarker for lepidic lung cancer. Clinical Cancer Research, 20(24), 6541-6550.
  • Calvayrac, O., Mazières, J., Figarol, S., Marty‐Detraves, C., Raymond‐Letron, I., Bousquet, E., ... & Guibert, N. (2017). The RAS‐related GTP ase RHOB confers resistance to EGFR‐tyrosine kinase inhibitors in non‐small‐cell lung cancer via an AKT‐dependent mechanism. EMBO molecular medicine, 9(2), 238-250.
  • De Cremoux, P., Gauville, C., Closson, V., Linares, G., Calvo, F., Tavitian, A., & Olofsson, B. (1994). EGF modulation of the ras‐related rhoB gene expression in human breast‐cancer cell lines. International journal of cancer, 59(3), 408-415.
  • Engel, M. E., Datta, P. K., & Moses, H. L. (1998). Signal transduction by transforming growth factor‐β: A cooperative paradigm with extensive negative regulation. Journal of Cellular Biochemistry, 72(S30‒31), 111-122.
  • Eramo, A., Lotti, F., Sette, G., Pilozzi, E., Biffoni, M., Di Virgilio, A., ... & De Maria, R. (2008). Identification and expansion of the tumorigenic lung cancer stem cell population. Cell death and differentiation, 15(3), 504.
  • Fang, D., Nguyen, T. K., Leishear, K., Finko, R., Kulp, A. N., Hotz, S., ... & Herlyn, M. (2005). A tumorigenic subpopulation with stem cell properties in melanomas. Cancer research, 65(20), 9328-9337.
  • Fritz, G., Kaina, B., & Aktories, K. (1995). The ras-related small GTP-binding protein RhoB is immediate-early inducible by DNA damaging treatments. Journal of Biological Chemistry, 270(42), 25172-25177.
  • Gibbs, C. P., Kukekov, V. G., Reith, J. D., Tchigrinova, O., Suslov, O. N., Scott, E. W., ... & Steindler, D. A. (2005). Stem-like cells in bone sarcomas: implications for tumorigenesis. Neoplasia, 7(11), 967-976.
  • Ho, M. M., Ng, A. V., Lam, S., & Hung, J. Y. (2007). Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer research, 67(10), 4827-4833.
  • Huang, M., & Prendergast, G. C. (2006). RhoB in cancer suppression. Histology and histopathology.
  • Ishiguro, T., Ohata, H., Sato, A., Yamawaki, K., Enomoto, T., & Okamoto, K. (2017). Tumor‐derived spheroids: relevance to cancer stem cells and clinical applications. Cancer science, 108(3), 283-289.
  • Jähner, D., & Hunter, T. O. N. Y. (1991). The ras-related gene rhoB is an immediate-early gene inducible by v-Fps, epidermal growth factor, and platelet-derived growth factor in rat fibroblasts. Molecular and Cellular Biology, 11(7), 3682-3690.
  • Jiang, F., Qiu, Q., Khanna, A., Todd, N. W., Deepak, J., Xing, L., ... & Katz, R. L. (2009). Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Molecular cancer research, 7(3), 330-338.
  • Jordan, C. T., Guzman, M. L., & Noble, M. (2006). Cancer stem cells. New England Journal of Medicine, 355(12), 1253-1261.
  • Kalemkerian, G. P., Akerley, W., Bogner, P., Borghaei, H., Chow, L. Q., Downey, R. J., ... & Hayman, J. (2013). Small cell lung cancer. Journal of the National Comprehensive Cancer Network, 11(1), 78-98.
  • Karlsson, R., Pedersen, E. D., Wang, Z., & Brakebusch, C. (2009). Rho GTPase function in tumorigenesis. Biochimica et Biophysica Acta (BBA)-Reviews on Cancer, 1796(2), 91-98.
  • Kato, H., Ichinose, Y., Ohta, M., Hata, E., Tsubota, N., Tada, H., ... & Ohta, M. (2004). A randomized trial of adjuvant chemotherapy with uracil–tegafur for adenocarcinoma of the lung. New England Journal of Medicine, 350(17), 1713-1721.
  • Leon, G., MacDonagh, L., Finn, S. P., Cuffe, S., & Barr, M. P. (2016). Cancer stem cells in drug resistant lung cancer: Targeting cell surface markers and signaling pathways. Pharmacology & therapeutics, 158, 71-90.
  • Levina, V., Marrangoni, A. M., DeMarco, R., Gorelik, E., & Lokshin, A. E. (2008). Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. PloS one, 3(8), e3077.
  • Liu, J., Xiao, Z., Wong, S. K. M., Tin, V. P. C., Ho, K. Y., Wang, J., ... & Wong, M. P. (2013). Lung cancer tumorigenicity and drug resistance are maintained through ALDHhiCD44hi tumor initiating cells. Oncotarget, 4(10), 1698.
  • Magee, J. A., Piskounova, E., & Morrison, S. J. (2012). Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer cell, 21(3), 283-296.
  • Mazieres, J., Antonia, T., Daste, G., Muro-Cacho, C., Berchery, D., Tillement, V., ... & Favre, G. (2004). Loss of RhoB expression in human lung cancer progression. Clinical cancer research, 10(8), 2742-2750.
  • Mazières, J., Tovar, D., He, B., Nieto-Acosta, J., Marty-Detraves, C., Clanet, C., ... & Favre, G. (2007). Epigenetic regulation of RhoB loss of expression in lung cancer. BMC cancer, 7(1), 220.
  • Miyata, T., Yoshimatsu, T., So, T., Oyama, T., Uramoto, H., Osaki, T., ... & Gotoh, A. (2015). Cancer stem cell markers in lung cancer. Personalized Medicine Universe, 4, 40-45.
  • O’Flaherty, J. D., Barr, M., Fennell, D., Richard, D., Reynolds, J., O’Leary, J., & O’Byrne, K. (2012). The cancer stem-cell hypothesis: its emerging role in lung cancer biology and its relevance for future therapy. Journal of thoracic oncology, 7(12), 1880-1890.
  • Parsons, A., Daley, A., Begh, R., & Aveyard, P. (2010). Influence of smoking cessation after diagnosis of early stage lung cancer on prognosis: systematic review of observational studies with meta-analysis. Bmj, 340, b5569.
  • Peacock, C. D., & Watkins, D. N. (2008). Cancer stem cells and the ontogeny of lung cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology, 26(17), 2883.
  • Pine, S. R., Marshall, B., & Varticovski, L. (2008). Lung cancer stem cells. Disease markers, 24(4-5), 257-266.
  • Ponti, D., Costa, A., Zaffaroni, N., Pratesi, G., Petrangolini, G., Coradini, D., ... & Daidone, M. G. (2005). Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer research, 65(13), 5506-5511.
  • Ridley, A. J. (2013). RhoA, RhoB and RhoC have different roles in cancer cell migration. Journal of microscopy, 251(3), 242-249.
  • Sahai, E., & Marshall, C. J. (2002). RHO–GTPases and cancer. Nature Reviews Cancer, 2(2), 133-142.
  • Sato, N., Fukui, T., Taniguchi, T., Yokoyama, T., Kondo, M., Nagasaka, T., ... & Minna, J. D. (2007). RhoB is frequently downregulated in non‐small‐cell lung cancer and resides in the 2p24 homozygous deletion region of a lung cancer cell line. International journal of cancer, 120(3), 543-551.
  • Siegel, R. L., Miller, K. D., & Jemal, A. (2016). Cancer statistics, 2016. CA: a cancer journal for clinicians, 66(1), 7-30.
  • Singh, S. K., Clarke, I. D., Terasaki, M., Bonn, V. E., Hawkins, C., Squire, J., & Dirks, P. B. (2003). Identification of a cancer stem cell in human brain tumors. Cancer research, 63(18), 5821-5828.
  • Visvader, J. E., & Lindeman, G. J. (2012). Cancer stem cells: current status and evolving complexities. Cell stem cell, 10(6), 717-728.
  • Walter, D., Satheesha, S., Albrecht, P., Bornhauser, B. C., D'Alessandro, V., Oesch, S. M., ... & Moch, H. (2011). CD133 positive embryonal rhabdomyosarcoma stem-like cell population is enriched in rhabdospheres. PloS one, 6(5), e19506
  • Wang, S., Yan-Neale, Y., Fischer, D., Zeremski, M., Cai, R., Zhu, J., ... & Cohen, D. (2003). Histone deacetylase 1 represses the small GTPase RhoB expression in human nonsmall lung carcinoma cell line. Oncogene, 22(40), 6204-6213.
  • Wang, P., Gao, Q., Suo, Z., Munthe, E., Solberg, S., Ma, L., ... & Gaudernack, G. (2013). Identification and characterization of cells with cancer stem cell properties in human primary lung cancer cell lines. PLoS one, 8(3), e57020.
  • Weiswald, L. B., Bellet, D., & Dangles-Marie, V. (2015). Spherical cancer models in tumor biology. Neoplasia, 17(1), 1-15.
  • Wicha, M. S., Liu, S., & Dontu, G. (2006). Cancer stem cells: an old idea—a paradigm shift. Cancer research, 66(4), 1883-1890.
  • Winton, T., Livingston, R., Johnson, D., Rigas, J., Johnston, M., Butts, C., ... & Fry, W. (2005). Vinorelbine plus cisplatin vs. observation in resected non–small-cell lung cancer. New England Journal of Medicine, 352(25), 2589-2597.
  • Zakaria, N., Satar, N. A., Halim, A., Hanis, N., Ngalim, S. H., Yusoff, N. M., ... & Yahaya, B. H. (2017). Targeting lung cancer stem cells: research and clinical impacts. Frontiers in oncology, 7, 80.
  • Zhong, Y., Guan, K., Guo, S., Zhou, C., Wang, D., Ma, W., ... & Zhang, S. (2010). Spheres derived from the human SK-RC-42 renal cell carcinoma cell line are enriched in cancer stem cells. Cancer letters, 299(2), 150-160.

Year 2020, Volume: 10, 29 - 36, 31.12.2020

Fathiya Rahmı Hiba Khaır Isık Didem Karagoz

Abstract

References

  • Adnane, J., Seijo, E., Chen, Z., Bizouarn, F., Leal, M., Sebti, S. M., & Muñoz-Antonia, T. (2002). RhoB, not RhoA, represses the transcription of the transforming growth factor β type II receptor by a mechanism involving activator protein 1. Journal of Biological Chemistry, 277(10), 8500-8507.
  • Aznar, S., & Lacal, J. C. (2001). Rho signals to cell growth and apoptosis. Cancer letters, 165(1), 1-10.
  • Bar-Sagi, D., & Hall, A. (2000). Ras and Rho GTPases: a family reunion. Cell, 103(2), 227-238.
  • Bertolini, G., Roz, L., Perego, P., Tortoreto, M., Fontanella, E., Gatti, L., ... & Roz, E. (2009). Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proceedings of the National Academy of Sciences, 106(38), 16281-16286.
  • Bishop, A. L., & Hall, A. (2000). Rho GTPases and their effector proteins. Biochemical Journal, 348(2), 241-255.
  • Bousquet, E., Mazières, J., Privat, M., Rizzati, V., Casanova, A., Ledoux, A., ... & Pradines, A. (2009). Loss of RhoB expression promotes migration and invasion of human bronchial cells via activation of AKT1. Cancer research, 69(15), 6092-6099.
  • Bousquet, E., Calvayrac, O., Mazieres, J., Lajoie-Mazenc, I., Boubekeur, N., Favre, G., & Pradines, A. (2016). RhoB loss induces Rac1-dependent mesenchymal cell invasion in lung cells through PP2A inhibition. Oncogene, 35(14), 1760-1769.
  • Calvayrac, O., Pradines, A., Raymond-Letron, I., Rouquette, I., Bousquet, E., Lauwers-Cances, V., ... & Milia, J. (2014). RhoB determines tumor aggressiveness in a murine EGFRL858R-induced adenocarcinoma model and is a potential prognostic biomarker for lepidic lung cancer. Clinical Cancer Research, 20(24), 6541-6550.
  • Calvayrac, O., Mazières, J., Figarol, S., Marty‐Detraves, C., Raymond‐Letron, I., Bousquet, E., ... & Guibert, N. (2017). The RAS‐related GTP ase RHOB confers resistance to EGFR‐tyrosine kinase inhibitors in non‐small‐cell lung cancer via an AKT‐dependent mechanism. EMBO molecular medicine, 9(2), 238-250.
  • De Cremoux, P., Gauville, C., Closson, V., Linares, G., Calvo, F., Tavitian, A., & Olofsson, B. (1994). EGF modulation of the ras‐related rhoB gene expression in human breast‐cancer cell lines. International journal of cancer, 59(3), 408-415.
  • Engel, M. E., Datta, P. K., & Moses, H. L. (1998). Signal transduction by transforming growth factor‐β: A cooperative paradigm with extensive negative regulation. Journal of Cellular Biochemistry, 72(S30‒31), 111-122.
  • Eramo, A., Lotti, F., Sette, G., Pilozzi, E., Biffoni, M., Di Virgilio, A., ... & De Maria, R. (2008). Identification and expansion of the tumorigenic lung cancer stem cell population. Cell death and differentiation, 15(3), 504.
  • Fang, D., Nguyen, T. K., Leishear, K., Finko, R., Kulp, A. N., Hotz, S., ... & Herlyn, M. (2005). A tumorigenic subpopulation with stem cell properties in melanomas. Cancer research, 65(20), 9328-9337.
  • Fritz, G., Kaina, B., & Aktories, K. (1995). The ras-related small GTP-binding protein RhoB is immediate-early inducible by DNA damaging treatments. Journal of Biological Chemistry, 270(42), 25172-25177.
  • Gibbs, C. P., Kukekov, V. G., Reith, J. D., Tchigrinova, O., Suslov, O. N., Scott, E. W., ... & Steindler, D. A. (2005). Stem-like cells in bone sarcomas: implications for tumorigenesis. Neoplasia, 7(11), 967-976.
  • Ho, M. M., Ng, A. V., Lam, S., & Hung, J. Y. (2007). Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer research, 67(10), 4827-4833.
  • Huang, M., & Prendergast, G. C. (2006). RhoB in cancer suppression. Histology and histopathology.
  • Ishiguro, T., Ohata, H., Sato, A., Yamawaki, K., Enomoto, T., & Okamoto, K. (2017). Tumor‐derived spheroids: relevance to cancer stem cells and clinical applications. Cancer science, 108(3), 283-289.
  • Jähner, D., & Hunter, T. O. N. Y. (1991). The ras-related gene rhoB is an immediate-early gene inducible by v-Fps, epidermal growth factor, and platelet-derived growth factor in rat fibroblasts. Molecular and Cellular Biology, 11(7), 3682-3690.
  • Jiang, F., Qiu, Q., Khanna, A., Todd, N. W., Deepak, J., Xing, L., ... & Katz, R. L. (2009). Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Molecular cancer research, 7(3), 330-338.
  • Jordan, C. T., Guzman, M. L., & Noble, M. (2006). Cancer stem cells. New England Journal of Medicine, 355(12), 1253-1261.
  • Kalemkerian, G. P., Akerley, W., Bogner, P., Borghaei, H., Chow, L. Q., Downey, R. J., ... & Hayman, J. (2013). Small cell lung cancer. Journal of the National Comprehensive Cancer Network, 11(1), 78-98.
  • Karlsson, R., Pedersen, E. D., Wang, Z., & Brakebusch, C. (2009). Rho GTPase function in tumorigenesis. Biochimica et Biophysica Acta (BBA)-Reviews on Cancer, 1796(2), 91-98.
  • Kato, H., Ichinose, Y., Ohta, M., Hata, E., Tsubota, N., Tada, H., ... & Ohta, M. (2004). A randomized trial of adjuvant chemotherapy with uracil–tegafur for adenocarcinoma of the lung. New England Journal of Medicine, 350(17), 1713-1721.
  • Leon, G., MacDonagh, L., Finn, S. P., Cuffe, S., & Barr, M. P. (2016). Cancer stem cells in drug resistant lung cancer: Targeting cell surface markers and signaling pathways. Pharmacology & therapeutics, 158, 71-90.
  • Levina, V., Marrangoni, A. M., DeMarco, R., Gorelik, E., & Lokshin, A. E. (2008). Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. PloS one, 3(8), e3077.
  • Liu, J., Xiao, Z., Wong, S. K. M., Tin, V. P. C., Ho, K. Y., Wang, J., ... & Wong, M. P. (2013). Lung cancer tumorigenicity and drug resistance are maintained through ALDHhiCD44hi tumor initiating cells. Oncotarget, 4(10), 1698.
  • Magee, J. A., Piskounova, E., & Morrison, S. J. (2012). Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer cell, 21(3), 283-296.
  • Mazieres, J., Antonia, T., Daste, G., Muro-Cacho, C., Berchery, D., Tillement, V., ... & Favre, G. (2004). Loss of RhoB expression in human lung cancer progression. Clinical cancer research, 10(8), 2742-2750.
  • Mazières, J., Tovar, D., He, B., Nieto-Acosta, J., Marty-Detraves, C., Clanet, C., ... & Favre, G. (2007). Epigenetic regulation of RhoB loss of expression in lung cancer. BMC cancer, 7(1), 220.
  • Miyata, T., Yoshimatsu, T., So, T., Oyama, T., Uramoto, H., Osaki, T., ... & Gotoh, A. (2015). Cancer stem cell markers in lung cancer. Personalized Medicine Universe, 4, 40-45.
  • O’Flaherty, J. D., Barr, M., Fennell, D., Richard, D., Reynolds, J., O’Leary, J., & O’Byrne, K. (2012). The cancer stem-cell hypothesis: its emerging role in lung cancer biology and its relevance for future therapy. Journal of thoracic oncology, 7(12), 1880-1890.
  • Parsons, A., Daley, A., Begh, R., & Aveyard, P. (2010). Influence of smoking cessation after diagnosis of early stage lung cancer on prognosis: systematic review of observational studies with meta-analysis. Bmj, 340, b5569.
  • Peacock, C. D., & Watkins, D. N. (2008). Cancer stem cells and the ontogeny of lung cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology, 26(17), 2883.
  • Pine, S. R., Marshall, B., & Varticovski, L. (2008). Lung cancer stem cells. Disease markers, 24(4-5), 257-266.
  • Ponti, D., Costa, A., Zaffaroni, N., Pratesi, G., Petrangolini, G., Coradini, D., ... & Daidone, M. G. (2005). Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer research, 65(13), 5506-5511.
  • Ridley, A. J. (2013). RhoA, RhoB and RhoC have different roles in cancer cell migration. Journal of microscopy, 251(3), 242-249.
  • Sahai, E., & Marshall, C. J. (2002). RHO–GTPases and cancer. Nature Reviews Cancer, 2(2), 133-142.
  • Sato, N., Fukui, T., Taniguchi, T., Yokoyama, T., Kondo, M., Nagasaka, T., ... & Minna, J. D. (2007). RhoB is frequently downregulated in non‐small‐cell lung cancer and resides in the 2p24 homozygous deletion region of a lung cancer cell line. International journal of cancer, 120(3), 543-551.
  • Siegel, R. L., Miller, K. D., & Jemal, A. (2016). Cancer statistics, 2016. CA: a cancer journal for clinicians, 66(1), 7-30.
  • Singh, S. K., Clarke, I. D., Terasaki, M., Bonn, V. E., Hawkins, C., Squire, J., & Dirks, P. B. (2003). Identification of a cancer stem cell in human brain tumors. Cancer research, 63(18), 5821-5828.
  • Visvader, J. E., & Lindeman, G. J. (2012). Cancer stem cells: current status and evolving complexities. Cell stem cell, 10(6), 717-728.
  • Walter, D., Satheesha, S., Albrecht, P., Bornhauser, B. C., D'Alessandro, V., Oesch, S. M., ... & Moch, H. (2011). CD133 positive embryonal rhabdomyosarcoma stem-like cell population is enriched in rhabdospheres. PloS one, 6(5), e19506
  • Wang, S., Yan-Neale, Y., Fischer, D., Zeremski, M., Cai, R., Zhu, J., ... & Cohen, D. (2003). Histone deacetylase 1 represses the small GTPase RhoB expression in human nonsmall lung carcinoma cell line. Oncogene, 22(40), 6204-6213.
  • Wang, P., Gao, Q., Suo, Z., Munthe, E., Solberg, S., Ma, L., ... & Gaudernack, G. (2013). Identification and characterization of cells with cancer stem cell properties in human primary lung cancer cell lines. PLoS one, 8(3), e57020.
  • Weiswald, L. B., Bellet, D., & Dangles-Marie, V. (2015). Spherical cancer models in tumor biology. Neoplasia, 17(1), 1-15.
  • Wicha, M. S., Liu, S., & Dontu, G. (2006). Cancer stem cells: an old idea—a paradigm shift. Cancer research, 66(4), 1883-1890.
  • Winton, T., Livingston, R., Johnson, D., Rigas, J., Johnston, M., Butts, C., ... & Fry, W. (2005). Vinorelbine plus cisplatin vs. observation in resected non–small-cell lung cancer. New England Journal of Medicine, 352(25), 2589-2597.
  • Zakaria, N., Satar, N. A., Halim, A., Hanis, N., Ngalim, S. H., Yusoff, N. M., ... & Yahaya, B. H. (2017). Targeting lung cancer stem cells: research and clinical impacts. Frontiers in oncology, 7, 80.
  • Zhong, Y., Guan, K., Guo, S., Zhou, C., Wang, D., Ma, W., ... & Zhang, S. (2010). Spheres derived from the human SK-RC-42 renal cell carcinoma cell line are enriched in cancer stem cells. Cancer letters, 299(2), 150-160.
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Details

Primary Language English
Subjects Engineering
Journal Section Articles
Authors

Fathiya Rahmı

Hiba Khaır

Isık Didem Karagoz

Publication Date December 31, 2020
Published in Issue Year 2020Volume: 10

Cite

APA Rahmı, F., Khaır, H., & Karagoz, I. D. (2020). Evaluation of the Effect of RhoB Inhibition on Cancer Stem Cell Properties in NSCLC A549 Cells. The Eurasia Proceedings of Science Technology Engineering and Mathematics, 10, 29-36.
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