Skip to main content
Top
Published in: Clinical and Translational Oncology 9/2020

01-09-2020 | Breast Cancer | Research Article

Suppressive role of Viola odorata extract on malignant characters of mammosphere-derived breast cancer stem cells

Authors: S. Yousefnia, D. Naseri, F. Seyed Forootan, M. Tabatabaeian, F. Moattar, T. Ghafghazi, M. H. Nasr Esfahani, K. Ghaedi

Published in: Clinical and Translational Oncology | Issue 9/2020

Login to get access

Abstract

Background

Mammospheres are breast cancer stem cells (BCSCs) that could be yielded through culturing cells in non-adherent and non-differentiating condition. With regard to therapy resistance of cancer stem cells (CSCs), it is essential to discover efficient approaches targeting CSCs. Viola odorata extract has been considered as a traditional herbal anti-metastatic drug in several cancer cells. Effect of this drug on BCSCs has not been clearly identified. Current study tries to detect and to compare effect of Viola odorata extract on malignant characterization of breast cancer cell lines and BCSCs.

Materials and methods

MCF7 and SKBR3 and their derived mammospheres as BCSCs were used and the effect of alcoholic extraction of Viola odorata on apoptosis and malignant characters of MCF7, SKBR3 and their derived BCSCs were analyzed and compared.

Results

Viola odorata extract induced cell death in MCF7, SKBR3 and their derived mammospheres through apoptosis without any effects on MCF10A. Also, this extract showed anti-migratory, anti-invasion and anti-colony formation activity in MCF7, SKBR3 and their derived mammospheres which was significantly more in MCF7- and SKBR3-derived mammospheres. Also, this extract decreased size and volume of tumors generated by MCF7, SKBR3 and their derived mammospheres in chicken embryo model.

Conclusion

Viola odorata extract exerted anti-cancerous activity on both breast cancer cell lines and their derived BCSCs. Anti-cancerous activity of this extract was significantly more in MCF7-, SKBR3-derived mammospheres in comparison with dedicated cell lines. Data suggest that Viola odorata extract mostly targets cancerous cells, not normal cells with exception in high concentration. It acts in a cell-dependent manner.
Appendix
Available only for authorised users
Literature
1.
go back to reference Alanazi IO, Khan Z. Understanding EGFR signaling in breast cancer and breast cancer stem cells: overexpression and therapeutic implications. Asian Pac J Cancer Prev APJCP. 2016;17:445–53.PubMed Alanazi IO, Khan Z. Understanding EGFR signaling in breast cancer and breast cancer stem cells: overexpression and therapeutic implications. Asian Pac J Cancer Prev APJCP. 2016;17:445–53.PubMed
2.
go back to reference Nounou MI, ElAmrawy F, Ahmed N, Abdelraouf K, Goda S, Syed-Sha-Qhattal H. Breast cancer: conventional diagnosis and treatment modalities and recent patents and technologies. Breast Cancer. 2015;9:BCBCR–S29420. Nounou MI, ElAmrawy F, Ahmed N, Abdelraouf K, Goda S, Syed-Sha-Qhattal H. Breast cancer: conventional diagnosis and treatment modalities and recent patents and technologies. Breast Cancer. 2015;9:BCBCR–S29420.
3.
go back to reference Kamińska M, Ciszewski T, Łopacka-Szatan K, Miotła P, Starosławska E. Breast cancer risk factors. Przeglad menopauzalny= Menopause Rev. 2015;14:196. Kamińska M, Ciszewski T, Łopacka-Szatan K, Miotła P, Starosławska E. Breast cancer risk factors. Przeglad menopauzalny= Menopause Rev. 2015;14:196.
4.
go back to reference Wang Y, Li W, Patel SS, Cong J, Zhang N, Sabbatino F, Liu X, Qi Y, Huang P, Lee H. Blocking the formation of radiation–induced breast cancer stem cells. Oncotarget. 2014;5:3743.PubMedPubMedCentral Wang Y, Li W, Patel SS, Cong J, Zhang N, Sabbatino F, Liu X, Qi Y, Huang P, Lee H. Blocking the formation of radiation–induced breast cancer stem cells. Oncotarget. 2014;5:3743.PubMedPubMedCentral
5.
go back to reference Kern KM, Schroeder JR. Comparison of cantharidin toxicity in breast cancer cells to two common chemotherapeutics. Int J Breast Cancer. 2014;2014:423059.PubMedPubMedCentral Kern KM, Schroeder JR. Comparison of cantharidin toxicity in breast cancer cells to two common chemotherapeutics. Int J Breast Cancer. 2014;2014:423059.PubMedPubMedCentral
6.
go back to reference Prentice RL. Postmenopausal hormone therapy and the risks of coronary heart disease, breast cancer, and stroke. In Seminars in reproductive medicine. 2014; 32. p. 419. (NIH Public Access) Prentice RL. Postmenopausal hormone therapy and the risks of coronary heart disease, breast cancer, and stroke. In Seminars in reproductive medicine. 2014; 32. p. 419. (NIH Public Access)
7.
go back to reference Pavelic J. Editorial (thematic Issue: combined cancer therapy). Curr Pharm Des. 2014;20:6511–2.PubMed Pavelic J. Editorial (thematic Issue: combined cancer therapy). Curr Pharm Des. 2014;20:6511–2.PubMed
8.
go back to reference Lin CY, Barry-Holson KQ, Allison KH. Breast cancer stem cells: are we ready to go from bench to bedside? Histopathology. 2016;68:119–37.PubMed Lin CY, Barry-Holson KQ, Allison KH. Breast cancer stem cells: are we ready to go from bench to bedside? Histopathology. 2016;68:119–37.PubMed
9.
go back to reference Michor F, Polyak K. The origins and implications of intratumor heterogeneity. Cancer Prev Res. 2010;3:1361–4. Michor F, Polyak K. The origins and implications of intratumor heterogeneity. Cancer Prev Res. 2010;3:1361–4.
10.
go back to reference Louie E, Nik S, Chen J-S, Schmidt M, Song B, Pacson C, Chen XF, Park S, Ju J, Chen EI. Identification of a stem-like cell population by exposing metastatic breast cancer cell lines to repetitive cycles of hypoxia and reoxygenation. Breast Cancer Res. 2010;12:R94.PubMedPubMedCentral Louie E, Nik S, Chen J-S, Schmidt M, Song B, Pacson C, Chen XF, Park S, Ju J, Chen EI. Identification of a stem-like cell population by exposing metastatic breast cancer cell lines to repetitive cycles of hypoxia and reoxygenation. Breast Cancer Res. 2010;12:R94.PubMedPubMedCentral
11.
go back to reference Idowu MO, Kmieciak M, Dumur C, Burton RS, Grimes MM, Powers CN, Manjili MH. CD44+/CD24−/low cancer stem/progenitor cells are more abundant in triple-negative invasive breast carcinoma phenotype and are associated with poor outcome. Hum Pathol. 2012;43:364–73.PubMed Idowu MO, Kmieciak M, Dumur C, Burton RS, Grimes MM, Powers CN, Manjili MH. CD44+/CD24−/low cancer stem/progenitor cells are more abundant in triple-negative invasive breast carcinoma phenotype and are associated with poor outcome. Hum Pathol. 2012;43:364–73.PubMed
12.
go back to reference Patel SA, Ndabahaliye A, Lim PK, Milton R, Rameshwar P. Challenges in the development of future treatments for breast cancer stem cells. Breast Cancer. 2010;2:1.PubMed Patel SA, Ndabahaliye A, Lim PK, Milton R, Rameshwar P. Challenges in the development of future treatments for breast cancer stem cells. Breast Cancer. 2010;2:1.PubMed
13.
go back to reference Apontes P, Leontieva OV, Demidenko ZN, Li F, Blagosklonny MV. Exploring long-term protection of normal human fibroblasts and epithelial cells from chemotherapy in cell culture. Oncotarget. 2011;2:222.PubMedPubMedCentral Apontes P, Leontieva OV, Demidenko ZN, Li F, Blagosklonny MV. Exploring long-term protection of normal human fibroblasts and epithelial cells from chemotherapy in cell culture. Oncotarget. 2011;2:222.PubMedPubMedCentral
14.
go back to reference Chen AC, Guo X, Derguini F, Gudas LJ. Human breast cancer cells and normal mammary epithelial cells: retinol metabolism and growth inhibition by the retinol metabolite 4-oxoretinol. Cancer Res. 1997;57:4642–51.PubMed Chen AC, Guo X, Derguini F, Gudas LJ. Human breast cancer cells and normal mammary epithelial cells: retinol metabolism and growth inhibition by the retinol metabolite 4-oxoretinol. Cancer Res. 1997;57:4642–51.PubMed
15.
go back to reference Wang S, Konorev EA, Kotamraju S, Joseph J, Kalivendi S, Kalyanaraman B. Doxorubicin induces apoptosis in normal and tumor cells via distinctly different mechanisms intermediacy of H2O2-and p53-dependent pathways. J Biol Chem. 2004;279:25535–43.PubMed Wang S, Konorev EA, Kotamraju S, Joseph J, Kalivendi S, Kalyanaraman B. Doxorubicin induces apoptosis in normal and tumor cells via distinctly different mechanisms intermediacy of H2O2-and p53-dependent pathways. J Biol Chem. 2004;279:25535–43.PubMed
16.
go back to reference Fleming T. PDR for herbal medicines. NJ: Medical Economics Montvale; 2000. Fleming T. PDR for herbal medicines. NJ: Medical Economics Montvale; 2000.
17.
go back to reference Koochek M, Pipelzadeh M, Mardani H. The effectiveness of Viola odorata in the prevention and treatment of formalin-induced lung damage in the rat. J Herbs Spices Med Plants. 2003;10:95–103. Koochek M, Pipelzadeh M, Mardani H. The effectiveness of Viola odorata in the prevention and treatment of formalin-induced lung damage in the rat. J Herbs Spices Med Plants. 2003;10:95–103.
18.
go back to reference Anca T, Philippe V, Ilioara O, Mircea T. Composition of essential oils of Viola tricolor and V. arvensis from Romania. Chem Nat Compd. 2009;45:91–2. Anca T, Philippe V, Ilioara O, Mircea T. Composition of essential oils of Viola tricolor and V. arvensis from Romania. Chem Nat Compd. 2009;45:91–2.
19.
go back to reference Siddiqi HS, Mehmood MH, Rehman NU, Gilani AH. Studies on the antihypertensive and antidyslipidemic activities of Viola odorata leaves extract. Lipids Health Dis. 2012;11:6.PubMedPubMedCentral Siddiqi HS, Mehmood MH, Rehman NU, Gilani AH. Studies on the antihypertensive and antidyslipidemic activities of Viola odorata leaves extract. Lipids Health Dis. 2012;11:6.PubMedPubMedCentral
20.
go back to reference Ebrahimzadeh MA, Nabavi SM, Nabavi SF, Bahramian F, Bekhradnia AR. Antioxidant and free radical scavenging activity of H. officinalisL. var. angustifolius, V. odorata, B. hyrcana and C. speciosum. Pak J Pharm Sci. 2010;23:29–34.PubMed Ebrahimzadeh MA, Nabavi SM, Nabavi SF, Bahramian F, Bekhradnia AR. Antioxidant and free radical scavenging activity of H. officinalisL. var. angustifolius, V. odorata, B. hyrcana and C. speciosum. Pak J Pharm Sci. 2010;23:29–34.PubMed
21.
go back to reference Gerlach SL, Rathinakumar R, Chakravarty G, Göransson U, Wimley WC, Darwin SP, Mondal D. Anticancer and chemosensitizing abilities of cycloviolacin O2 from Viola odorata and psyle cyclotides from Psychotria leptothyrsa. Pept Sci. 2010;94:617–25. Gerlach SL, Rathinakumar R, Chakravarty G, Göransson U, Wimley WC, Darwin SP, Mondal D. Anticancer and chemosensitizing abilities of cycloviolacin O2 from Viola odorata and psyle cyclotides from Psychotria leptothyrsa. Pept Sci. 2010;94:617–25.
22.
go back to reference Lindholm P, Göransson U, Johansson S, Claeson P, Gullbo J, Larsson R, Bohlin L, Backlund A. Cyclotides: a novel type of cytotoxic agents 1 PL and UG contributed equally to this manuscript. Mol Cancer Ther. 2002;1:365–9.PubMed Lindholm P, Göransson U, Johansson S, Claeson P, Gullbo J, Larsson R, Bohlin L, Backlund A. Cyclotides: a novel type of cytotoxic agents 1 PL and UG contributed equally to this manuscript. Mol Cancer Ther. 2002;1:365–9.PubMed
23.
go back to reference Saether O, Craik DJ, Campbell ID, Sletten K, Juul J, Norman DG. Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide kalata B1. Biochemistry. 1995;34:4147–58.PubMed Saether O, Craik DJ, Campbell ID, Sletten K, Juul J, Norman DG. Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide kalata B1. Biochemistry. 1995;34:4147–58.PubMed
24.
go back to reference Svangård E, Burman R, Gunasekera S, Lövborg H, Gullbo J, Göransson U. Mechanism of action of cytotoxic cyclotides: cycloviolacin O2 disrupts lipid membranes. J Nat Prod. 2007;70:643–7.PubMed Svangård E, Burman R, Gunasekera S, Lövborg H, Gullbo J, Göransson U. Mechanism of action of cytotoxic cyclotides: cycloviolacin O2 disrupts lipid membranes. J Nat Prod. 2007;70:643–7.PubMed
25.
go back to reference Duke JA. Handbook of medicinal herbs. Boca Raton: CRC Press; 2002. Duke JA. Handbook of medicinal herbs. Boca Raton: CRC Press; 2002.
27.
go back to reference Hu E, Wang D, Chen J, Tao X. Novel cyclotides from Hedyotis diffusa induce apoptosis and inhibit proliferation and migration of prostate cancer cells. Int J Clin Exper Med. 2015;8:4059. Hu E, Wang D, Chen J, Tao X. Novel cyclotides from Hedyotis diffusa induce apoptosis and inhibit proliferation and migration of prostate cancer cells. Int J Clin Exper Med. 2015;8:4059.
28.
go back to reference Yang R, Qi J, Zhang J, Wang F, Fan L. Effects of Paris polyphylla saponin VII plus silica nano composite on ovarian cancer drug resistance in vitro. Zhonghua yi xue za zhi. 2015;95:1859–61.PubMed Yang R, Qi J, Zhang J, Wang F, Fan L. Effects of Paris polyphylla saponin VII plus silica nano composite on ovarian cancer drug resistance in vitro. Zhonghua yi xue za zhi. 2015;95:1859–61.PubMed
29.
go back to reference Zhang Y, Bao J, Wang K, Jia X, Zhang C, Huang B, Chen M, Wan J-B, Su H, Wang Y. Pulsatilla saponin D inhibits autophagic flux and synergistically enhances the anticancer activity of chemotherapeutic agents against hela cells. Am J Chin Med. 2015;43:1657–70.PubMed Zhang Y, Bao J, Wang K, Jia X, Zhang C, Huang B, Chen M, Wan J-B, Su H, Wang Y. Pulsatilla saponin D inhibits autophagic flux and synergistically enhances the anticancer activity of chemotherapeutic agents against hela cells. Am J Chin Med. 2015;43:1657–70.PubMed
30.
go back to reference Zhao PJ, Song SC, Du LW, Zhou GH, Ma SL, Li JH, Feng JG, Zhu XH, Jiang H. Paris Saponins enhance radiosensitivity in a gefitinib-resistant lung adenocarcinoma cell line by inducing apoptosis and G2/M cell cycle phase arrest. Mol Med Rep. 2016;13:2878–84.PubMed Zhao PJ, Song SC, Du LW, Zhou GH, Ma SL, Li JH, Feng JG, Zhu XH, Jiang H. Paris Saponins enhance radiosensitivity in a gefitinib-resistant lung adenocarcinoma cell line by inducing apoptosis and G2/M cell cycle phase arrest. Mol Med Rep. 2016;13:2878–84.PubMed
31.
go back to reference Chen X-Y, Zhou J, Luo L-P, Han B, Li F, Chen J-Y, Zhu Y-F, Chen W, Yu X-P. Black rice anthocyanins suppress metastasis of breast cancer cells by targeting RAS/RAF/MAPK pathway. BioMed Res Int. 2015;2015:414250.PubMedPubMedCentral Chen X-Y, Zhou J, Luo L-P, Han B, Li F, Chen J-Y, Zhu Y-F, Chen W, Yu X-P. Black rice anthocyanins suppress metastasis of breast cancer cells by targeting RAS/RAF/MAPK pathway. BioMed Res Int. 2015;2015:414250.PubMedPubMedCentral
32.
go back to reference Li D, Wang P, Luo Y, Zhao M, Chen F. Health benefits of anthocyanins and molecular mechanisms: update from recent decade. Crit Rev Food Sci Nutr. 2017;57:1729–41.PubMed Li D, Wang P, Luo Y, Zhao M, Chen F. Health benefits of anthocyanins and molecular mechanisms: update from recent decade. Crit Rev Food Sci Nutr. 2017;57:1729–41.PubMed
33.
go back to reference Ma R-J, Liu Z-H, Zi C-T, Gao W, Dong F-W, Yang L, Li J-Y, Zhou J, Hu J-M. Oleanane-type triterpene saponins from Hydrocotyle nepalensis. Fitoterapia. 2016;110:66–71.PubMed Ma R-J, Liu Z-H, Zi C-T, Gao W, Dong F-W, Yang L, Li J-Y, Zhou J, Hu J-M. Oleanane-type triterpene saponins from Hydrocotyle nepalensis. Fitoterapia. 2016;110:66–71.PubMed
34.
go back to reference Plan MRR, Saska I, Cagauan AG, Craik DJ. Backbone cyclised peptides from plants show molluscicidal activity against the rice pest Pomacea canaliculata (golden apple snail). J Agric Food Chem. 2008;56:5237–41.PubMed Plan MRR, Saska I, Cagauan AG, Craik DJ. Backbone cyclised peptides from plants show molluscicidal activity against the rice pest Pomacea canaliculata (golden apple snail). J Agric Food Chem. 2008;56:5237–41.PubMed
35.
go back to reference Chandra D, Kohli G, Prasad K, Bisht G, Punetha VD, Khetwal K, Devrani MK, Pandey H. Phytochemical and ethnomedicinal uses of family Violaceae. Curr Res Chem. 2015;7:44–52. Chandra D, Kohli G, Prasad K, Bisht G, Punetha VD, Khetwal K, Devrani MK, Pandey H. Phytochemical and ethnomedicinal uses of family Violaceae. Curr Res Chem. 2015;7:44–52.
36.
go back to reference Ediriweera MK, Tennekoon KH, Samarakoon SR, Thabrew I, Dilip De Silva E. A study of the potential anticancer activity of Mangifera zeylanica bark: evaluation of cytotoxic and apoptotic effects of the hexane extract and bioassay-guided fractionation to identify phytochemical constituents. Oncol Lett. 2016;11:1335–444.PubMedPubMedCentral Ediriweera MK, Tennekoon KH, Samarakoon SR, Thabrew I, Dilip De Silva E. A study of the potential anticancer activity of Mangifera zeylanica bark: evaluation of cytotoxic and apoptotic effects of the hexane extract and bioassay-guided fractionation to identify phytochemical constituents. Oncol Lett. 2016;11:1335–444.PubMedPubMedCentral
37.
go back to reference Yousefnia S, Ghaedi K, Seyed Forootan F, Nasr Esfahani MH. Characterization of the stemness potency of mammospheres isolated from the breast cancer cell lines. Tumor Biol. 2019;41:1010428319869101. Yousefnia S, Ghaedi K, Seyed Forootan F, Nasr Esfahani MH. Characterization of the stemness potency of mammospheres isolated from the breast cancer cell lines. Tumor Biol. 2019;41:1010428319869101.
38.
go back to reference Lombardo Y, de Giorgio A, Coombes CR, Stebbing J, Castellano L. Mammosphere formation assay from human breast cancer tissues and cell lines. J Vis Exp JoVE. 2015;97:e52671. Lombardo Y, de Giorgio A, Coombes CR, Stebbing J, Castellano L. Mammosphere formation assay from human breast cancer tissues and cell lines. J Vis Exp JoVE. 2015;97:e52671.
39.
go back to reference Cioce M, Gherardi S, Viglietto G, Strano S, Blandino G, Muti P, Ciliberto G. Mammosphere-forming cells from breast cancer cell lines as a tool for the identification of CSC-like-and early progenitor-targeting drugs. Cell Cycle. 2010;9:2950–9. Cioce M, Gherardi S, Viglietto G, Strano S, Blandino G, Muti P, Ciliberto G. Mammosphere-forming cells from breast cancer cell lines as a tool for the identification of CSC-like-and early progenitor-targeting drugs. Cell Cycle. 2010;9:2950–9.
40.
go back to reference Wang R, Lv Q, Meng W, Tan Q, Zhang S, Mo X, Yang X. Comparison of mammosphere formation from breast cancer cell lines and primary breast tumors. J Thorac Dis. 2014;6:829.PubMedPubMedCentral Wang R, Lv Q, Meng W, Tan Q, Zhang S, Mo X, Yang X. Comparison of mammosphere formation from breast cancer cell lines and primary breast tumors. J Thorac Dis. 2014;6:829.PubMedPubMedCentral
41.
go back to reference Sadeghnia HR, Ghorbani Hesari T, Mortazavian SM, Mousavi SH, Tayarani-Najaran Z, Ghorbani A. Viola tricolor induces apoptosis in cancer cells and exhibits antiangiogenic activity on chicken chorioallantoic membrane. BioMed Res Int. 2014 Sadeghnia HR, Ghorbani Hesari T, Mortazavian SM, Mousavi SH, Tayarani-Najaran Z, Ghorbani A. Viola tricolor induces apoptosis in cancer cells and exhibits antiangiogenic activity on chicken chorioallantoic membrane. BioMed Res Int. 2014
42.
go back to reference Vishal A, Parveen K, Pooja S, Kannappan N, Kumar S. Diuretic, laxative and toxicity Studies of Viola odorata aerial parts. Pharmacol Online. 2009;1:739–48. Vishal A, Parveen K, Pooja S, Kannappan N, Kumar S. Diuretic, laxative and toxicity Studies of Viola odorata aerial parts. Pharmacol Online. 2009;1:739–48.
43.
go back to reference Meyer VR. Practical high-performance liquid chromatography. New Jersey: Wiley; 2013. Meyer VR. Practical high-performance liquid chromatography. New Jersey: Wiley; 2013.
44.
go back to reference Zhang LC, Jin X, Huang Z, Yan ZN, Li PB, Duan RF, Feng H, Jiang JH, Peng H, Liu W. Protective effects of choline against hypoxia-induced injuries of vessels and endothelial cells. Exp Ther Med. 2017;13:2316–24.PubMedPubMedCentral Zhang LC, Jin X, Huang Z, Yan ZN, Li PB, Duan RF, Feng H, Jiang JH, Peng H, Liu W. Protective effects of choline against hypoxia-induced injuries of vessels and endothelial cells. Exp Ther Med. 2017;13:2316–24.PubMedPubMedCentral
45.
go back to reference Yang T, Zhai H, Yan R, Zhou Z, Gao L, Wang L. lncRNA CCAT1 promotes cell proliferation, migration, and invasion by down-regulation of miR-143 in FTC-133 thyroid carcinoma cell line. Braz J Med Biol Res. 2018;51:e7046.PubMedPubMedCentral Yang T, Zhai H, Yan R, Zhou Z, Gao L, Wang L. lncRNA CCAT1 promotes cell proliferation, migration, and invasion by down-regulation of miR-143 in FTC-133 thyroid carcinoma cell line. Braz J Med Biol Res. 2018;51:e7046.PubMedPubMedCentral
46.
go back to reference Horibata S, Vo TV, Subramanian V, Thompson PR, Coonrod SA. Utilization of the soft agar colony formation assay to identify inhibitors of tumorigenicity in breast cancer cells. JoVE. 2015;99:e52727. Horibata S, Vo TV, Subramanian V, Thompson PR, Coonrod SA. Utilization of the soft agar colony formation assay to identify inhibitors of tumorigenicity in breast cancer cells. JoVE. 2015;99:e52727.
47.
go back to reference Tufan AC, Satiroglu-Tufan NL. The chick embryo chorioallantoic membrane as a model system for the study of tumor angiogenesis, invasion and development of anti-angiogenic agents. Curr Cancer Drug Targets. 2005;5:249–66.PubMed Tufan AC, Satiroglu-Tufan NL. The chick embryo chorioallantoic membrane as a model system for the study of tumor angiogenesis, invasion and development of anti-angiogenic agents. Curr Cancer Drug Targets. 2005;5:249–66.PubMed
48.
go back to reference Wang C, Yan Q, Hu M, Qin D, Feng Z. Effect of AURKA gene expression knockdown on angiogenesis and tumorigenesis of human ovarian cancer cell lines. Target oncol. 2016;11:771–81.PubMed Wang C, Yan Q, Hu M, Qin D, Feng Z. Effect of AURKA gene expression knockdown on angiogenesis and tumorigenesis of human ovarian cancer cell lines. Target oncol. 2016;11:771–81.PubMed
49.
go back to reference Sys GM, Lapeire L, Stevens N, Favoreel H, Forsyth R, Bracke M, De Wever O. The in ovo CAM-assay as a xenograft model for sarcoma. J Vis Exp JoVE. 2013;77:e50522. Sys GM, Lapeire L, Stevens N, Favoreel H, Forsyth R, Bracke M, De Wever O. The in ovo CAM-assay as a xenograft model for sarcoma. J Vis Exp JoVE. 2013;77:e50522.
50.
go back to reference Lokman NA, Elder AS, Ricciardelli C, Oehler MK. Chick chorioallantoic membrane (CAM) assay as an in vivo model to study the effect of newly identified molecules on ovarian cancer invasion and metastasis. Int J Mol Sci. 2012;13:9959–70.PubMedPubMedCentral Lokman NA, Elder AS, Ricciardelli C, Oehler MK. Chick chorioallantoic membrane (CAM) assay as an in vivo model to study the effect of newly identified molecules on ovarian cancer invasion and metastasis. Int J Mol Sci. 2012;13:9959–70.PubMedPubMedCentral
51.
go back to reference Chambers AF, Shafir R, Ling V. A model system for studying metastasis using the embryonic chick. Cancer Res. 1982;42:4018–25.PubMed Chambers AF, Shafir R, Ling V. A model system for studying metastasis using the embryonic chick. Cancer Res. 1982;42:4018–25.PubMed
52.
go back to reference Chang JHM, Lin CH, Shibu MA, Chou YC, Liu JY, Chou YH, Shen CY, Yeh YL, Viswanadha VP, Huang CY. Cryptotanshinone (Dsh-003) from Salvia miltiorrhiza Bunge inhibits prostaglandin E2-induced survival and invasion effects in HA22T hepatocellular carcinoma cells. Environ Toxicol. 2018;33:1254–60.PubMed Chang JHM, Lin CH, Shibu MA, Chou YC, Liu JY, Chou YH, Shen CY, Yeh YL, Viswanadha VP, Huang CY. Cryptotanshinone (Dsh-003) from Salvia miltiorrhiza Bunge inhibits prostaglandin E2-induced survival and invasion effects in HA22T hepatocellular carcinoma cells. Environ Toxicol. 2018;33:1254–60.PubMed
53.
go back to reference Peng K-T, Chiang Y-C, Ko H-H, Chi P-L, Tsai C-L, Ko M-I, Lee M-H, Hsu L-F, Lee C-W. Mechanism of Lakoochin a inducing apoptosis of A375. S2 melanoma cells through mitochondrial ROS and MAPKs pathway. Int J Mol Sci. 2018;19:2649.PubMedCentral Peng K-T, Chiang Y-C, Ko H-H, Chi P-L, Tsai C-L, Ko M-I, Lee M-H, Hsu L-F, Lee C-W. Mechanism of Lakoochin a inducing apoptosis of A375. S2 melanoma cells through mitochondrial ROS and MAPKs pathway. Int J Mol Sci. 2018;19:2649.PubMedCentral
54.
go back to reference Lu MC, Li TY, Hsieh YC, Hsieh PC, Chu YL. Chemical evaluation and cytotoxic mechanism investigation of Clinacanthus nutans extract in lymphoma SUP-T1 cells. Environ Toxicol. 2018;33:1229–366.PubMed Lu MC, Li TY, Hsieh YC, Hsieh PC, Chu YL. Chemical evaluation and cytotoxic mechanism investigation of Clinacanthus nutans extract in lymphoma SUP-T1 cells. Environ Toxicol. 2018;33:1229–366.PubMed
55.
go back to reference Chang T-C, Chin Y-T, Nana AW, Wang S-H, Liao Y-M, Chen Y-R, Shih Y-J, Changou CA, Yang Y-CS, Wang K. Enhancement by nano-diamino-tetrac of antiproliferative action of Gefitinib on colorectal cancer cells: mediation by EGFR sialylation and PI3K activation. Horm Cancer. 2018;9:420–32.PubMedPubMedCentral Chang T-C, Chin Y-T, Nana AW, Wang S-H, Liao Y-M, Chen Y-R, Shih Y-J, Changou CA, Yang Y-CS, Wang K. Enhancement by nano-diamino-tetrac of antiproliferative action of Gefitinib on colorectal cancer cells: mediation by EGFR sialylation and PI3K activation. Horm Cancer. 2018;9:420–32.PubMedPubMedCentral
56.
go back to reference Yao XJ, Lai H, Leung E, Liu L, Wang Y, Li Y, Jiang Z, Duan F, Luo LX. Krukovine suppresses KRAS-mutated lung cancer cell growth and proliferation by inhibiting the RAF-ERK pathway and inactivating AKT. Front Pharmacol. 2018;9:958.PubMedPubMedCentral Yao XJ, Lai H, Leung E, Liu L, Wang Y, Li Y, Jiang Z, Duan F, Luo LX. Krukovine suppresses KRAS-mutated lung cancer cell growth and proliferation by inhibiting the RAF-ERK pathway and inactivating AKT. Front Pharmacol. 2018;9:958.PubMedPubMedCentral
57.
go back to reference Alessandra-Perini J, Perini JA, Rodrigues-Baptista KC, de Moura RS, Junior AP, dos Santos TA, Souza PJC, Nasciutti LE, Machado DE. Euterpe oleracea extract inhibits tumorigenesis effect of the chemical carcinogen DMBA in breast experimental cancer. BMC Complement Altern Med. 2018;18:116.PubMedPubMedCentral Alessandra-Perini J, Perini JA, Rodrigues-Baptista KC, de Moura RS, Junior AP, dos Santos TA, Souza PJC, Nasciutti LE, Machado DE. Euterpe oleracea extract inhibits tumorigenesis effect of the chemical carcinogen DMBA in breast experimental cancer. BMC Complement Altern Med. 2018;18:116.PubMedPubMedCentral
58.
go back to reference Koh RY, Lim FP, Ling LSY, Ng CPL, Liew SF, Yew MY, Tiong YL, Ling APK, Chye SM, Ng KY. Anticancer mechanisms of Strobilanthes crispa Blume hexane extract on liver and breast cancer cell lines. Oncol Lett. 2017;14:4957–64.PubMedPubMedCentral Koh RY, Lim FP, Ling LSY, Ng CPL, Liew SF, Yew MY, Tiong YL, Ling APK, Chye SM, Ng KY. Anticancer mechanisms of Strobilanthes crispa Blume hexane extract on liver and breast cancer cell lines. Oncol Lett. 2017;14:4957–64.PubMedPubMedCentral
59.
go back to reference Yi X, Zuo J, Tan C, Xian S, Luo C, Chen S, Yu L, Luo Y. Kaempferol, a flavonoid compound from Gynura medica induced apoptosis and growth inhibition in MCF-7 breast cancer cell. Afr J Tradit Complement Altern Med. 2016;13:210–5.PubMedPubMedCentral Yi X, Zuo J, Tan C, Xian S, Luo C, Chen S, Yu L, Luo Y. Kaempferol, a flavonoid compound from Gynura medica induced apoptosis and growth inhibition in MCF-7 breast cancer cell. Afr J Tradit Complement Altern Med. 2016;13:210–5.PubMedPubMedCentral
60.
go back to reference Nguyen LT, Lee Y-H, Sharma AR, Park J-B, Jagga S, Sharma G, Lee S-S, Nam J-S. Quercetin induces apoptosis and cell cycle arrest in triple-negative breast cancer cells through modulation of Foxo3a activity. Korean J Physiol Pharmacol. 2017;21:205–13.PubMedPubMedCentral Nguyen LT, Lee Y-H, Sharma AR, Park J-B, Jagga S, Sharma G, Lee S-S, Nam J-S. Quercetin induces apoptosis and cell cycle arrest in triple-negative breast cancer cells through modulation of Foxo3a activity. Korean J Physiol Pharmacol. 2017;21:205–13.PubMedPubMedCentral
61.
go back to reference Palko-Labuz A, Sroda-Pomianek K, Uryga A, Kostrzewa-Suslow E, Michalak K. Anticancer activity of baicalein and luteolin studied in colorectal adenocarcinoma LoVo cells and in drug-resistant LoVo/Dx cells. Biomed Pharmacother. 2017;88:232–41.PubMed Palko-Labuz A, Sroda-Pomianek K, Uryga A, Kostrzewa-Suslow E, Michalak K. Anticancer activity of baicalein and luteolin studied in colorectal adenocarcinoma LoVo cells and in drug-resistant LoVo/Dx cells. Biomed Pharmacother. 2017;88:232–41.PubMed
62.
go back to reference Talero E, García-Mauriño S, Ávila-Román J, Rodríguez-Luna A, Alcaide A, Motilva V. Bioactive compounds isolated from microalgae in chronic inflammation and cancer. Mar Drugs. 2015;13:6152–209.PubMedPubMedCentral Talero E, García-Mauriño S, Ávila-Román J, Rodríguez-Luna A, Alcaide A, Motilva V. Bioactive compounds isolated from microalgae in chronic inflammation and cancer. Mar Drugs. 2015;13:6152–209.PubMedPubMedCentral
63.
go back to reference Jabeen A, Reeder B, Hisaindee S, Ashraf S, Al Darmaki N, Battah S, Al-Zuhair S. Effect of enzymatic pre-treatment of microalgae extracts on their anti-tumor activity. Biomed J. 2017;40:339–46.PubMed Jabeen A, Reeder B, Hisaindee S, Ashraf S, Al Darmaki N, Battah S, Al-Zuhair S. Effect of enzymatic pre-treatment of microalgae extracts on their anti-tumor activity. Biomed J. 2017;40:339–46.PubMed
64.
go back to reference Lee SY, Ju MK, Jeon HM, Jeong EK, Lee YJ, Kim CH, Park HG, Han SI, Kang HS. Regulation of tumor progression by programmed necrosis. Oxid Med Cell Longev. 2018 Lee SY, Ju MK, Jeon HM, Jeong EK, Lee YJ, Kim CH, Park HG, Han SI, Kang HS. Regulation of tumor progression by programmed necrosis. Oxid Med Cell Longev. 2018
65.
go back to reference Nikoletopoulou V, Markaki M, Palikaras K, Tavernarakis N. Crosstalk between apoptosis, necrosis and autophagy. Biochimica et Biophysica Acta (BBA). Mol Cell Res. 2013;1833:3448–599. Nikoletopoulou V, Markaki M, Palikaras K, Tavernarakis N. Crosstalk between apoptosis, necrosis and autophagy. Biochimica et Biophysica Acta (BBA). Mol Cell Res. 2013;1833:3448–599.
66.
go back to reference Wu T, Cui H, Xu Y, Du Q, Zhao E, Cao J, Nie L, Fu G, Ren A. The effect of tubeimoside-1 on the proliferation, metastasis and apoptosis of oral squamous cell carcinoma in vitro. OncoTargets Ther. 2018;11:3989. Wu T, Cui H, Xu Y, Du Q, Zhao E, Cao J, Nie L, Fu G, Ren A. The effect of tubeimoside-1 on the proliferation, metastasis and apoptosis of oral squamous cell carcinoma in vitro. OncoTargets Ther. 2018;11:3989.
67.
go back to reference Kang HM, Park BS, Kang HK, Park HR, Yu SB, Kim IR. Delphinidin induces apoptosis and inhibits epithelial-to-mesenchymal transition via the ERK/p38 MAPK-signaling pathway in human osteosarcoma cell lines. Environ Toxicol. 2018;33:640–9.PubMedPubMedCentral Kang HM, Park BS, Kang HK, Park HR, Yu SB, Kim IR. Delphinidin induces apoptosis and inhibits epithelial-to-mesenchymal transition via the ERK/p38 MAPK-signaling pathway in human osteosarcoma cell lines. Environ Toxicol. 2018;33:640–9.PubMedPubMedCentral
68.
go back to reference Zhou J, Zhu Y-F, Chen X-Y, Han B, Li F, Chen J-Y, Peng X-L, Luo L-P, Chen W, Yu X-P. Black rice-derived anthocyanins inhibit HER-2-positive breast cancer epithelial-mesenchymal transition-mediated metastasis in vitro by suppressing FAK signaling. Int J Mol Med. 2017;40:1649–56.PubMedPubMedCentral Zhou J, Zhu Y-F, Chen X-Y, Han B, Li F, Chen J-Y, Peng X-L, Luo L-P, Chen W, Yu X-P. Black rice-derived anthocyanins inhibit HER-2-positive breast cancer epithelial-mesenchymal transition-mediated metastasis in vitro by suppressing FAK signaling. Int J Mol Med. 2017;40:1649–56.PubMedPubMedCentral
69.
go back to reference Li S, Yan T, Deng R, Jiang X, Xiong H, Wang Y, Yu Q, Wang X, Chen C, Zhu Y. Low dose of kaempferol suppresses the migration and invasion of triple-negative breast cancer cells by downregulating the activities of RhoA and Rac1. OncoTargets Ther. 2017;10:4809. Li S, Yan T, Deng R, Jiang X, Xiong H, Wang Y, Yu Q, Wang X, Chen C, Zhu Y. Low dose of kaempferol suppresses the migration and invasion of triple-negative breast cancer cells by downregulating the activities of RhoA and Rac1. OncoTargets Ther. 2017;10:4809.
70.
go back to reference Qian Y, Han Q-H, Wang L-C, Guo Q, Wang X-D, Tu P-F, Zeng K-W, Liang H. Total saponins of Albiziae Cortex show anti-hepatoma carcinoma effects by inducing S phase arrest and mitochondrial apoptosis pathway activation. J Ethnopharmacol. 2018;221:20–9.PubMed Qian Y, Han Q-H, Wang L-C, Guo Q, Wang X-D, Tu P-F, Zeng K-W, Liang H. Total saponins of Albiziae Cortex show anti-hepatoma carcinoma effects by inducing S phase arrest and mitochondrial apoptosis pathway activation. J Ethnopharmacol. 2018;221:20–9.PubMed
71.
go back to reference Charepalli V, Reddivari L, Vadde R, Walia S, Radhakrishnan S, Vanamala JK. Eugenia jambolana (Java plum) fruit extract exhibits anti-cancer activity against early stage human HCT-116 colon cancer cells and colon cancer stem cells. Cancers. 2016;8:29.PubMedCentral Charepalli V, Reddivari L, Vadde R, Walia S, Radhakrishnan S, Vanamala JK. Eugenia jambolana (Java plum) fruit extract exhibits anti-cancer activity against early stage human HCT-116 colon cancer cells and colon cancer stem cells. Cancers. 2016;8:29.PubMedCentral
72.
go back to reference Nair HK, Rao KV, Aalinkeel R, Mahajan S, Chawda R, Schwartz SA. Inhibition of prostate cancer cell colony formation by the flavonoid quercetin correlates with modulation of specific regulatory genes. Clin Diagn Lab Immunol. 2004;11:63–9.PubMedPubMedCentral Nair HK, Rao KV, Aalinkeel R, Mahajan S, Chawda R, Schwartz SA. Inhibition of prostate cancer cell colony formation by the flavonoid quercetin correlates with modulation of specific regulatory genes. Clin Diagn Lab Immunol. 2004;11:63–9.PubMedPubMedCentral
73.
go back to reference Abdal Dayem A, Choi HY, Yang G-M, Kim K, Saha SK, Cho S-G. The anti-cancer effect of polyphenols against breast cancer and cancer stem cells: molecular mechanisms. Nutrients. 2016;8:581.PubMedCentral Abdal Dayem A, Choi HY, Yang G-M, Kim K, Saha SK, Cho S-G. The anti-cancer effect of polyphenols against breast cancer and cancer stem cells: molecular mechanisms. Nutrients. 2016;8:581.PubMedCentral
74.
go back to reference Chen D, Pamu S, Cui Q, Chan TH, Dou QP. Novel epigallocatechin gallate (EGCG) analogs activate AMP-activated protein kinase pathway and target cancer stem cells. Bioorg Med Chem. 2012;20:3031–7.PubMedPubMedCentral Chen D, Pamu S, Cui Q, Chan TH, Dou QP. Novel epigallocatechin gallate (EGCG) analogs activate AMP-activated protein kinase pathway and target cancer stem cells. Bioorg Med Chem. 2012;20:3031–7.PubMedPubMedCentral
75.
go back to reference Dandawate PR, Subramaniam D, Jensen RA, Anant S. Targeting cancer stem cells and signaling pathways by phytochemicals: novel approach for breast cancer therapy. In Seminars in cancer biology. 2016; 40. pp. 192–208 (Elsevier). Dandawate PR, Subramaniam D, Jensen RA, Anant S. Targeting cancer stem cells and signaling pathways by phytochemicals: novel approach for breast cancer therapy. In Seminars in cancer biology. 2016; 40. pp. 192–208 (Elsevier).
76.
go back to reference Manupati K, Dhoke NR, Debnath T, Yeeravalli R, Guguloth K, Saeidpour S, De UC, Debnath S, Das A. Inhibiting epidermal growth factor receptor signalling potentiates mesenchymal–epithelial transition of breast cancer stem cells and their responsiveness to anticancer drugs. FEBS J. 2017;284:1830–54.PubMed Manupati K, Dhoke NR, Debnath T, Yeeravalli R, Guguloth K, Saeidpour S, De UC, Debnath S, Das A. Inhibiting epidermal growth factor receptor signalling potentiates mesenchymal–epithelial transition of breast cancer stem cells and their responsiveness to anticancer drugs. FEBS J. 2017;284:1830–54.PubMed
77.
go back to reference Sandoval TA, Urueña CP, Llano M, Gómez-Cadena A, Hernández JF, Sequeda LG, Loaiza AE, Barreto A, Li S, Fiorentino S. Standardized extract from Caesalpinia spinosa is cytotoxic over cancer stem cells and enhance anticancer activity of doxorubicin. Am J Chin Med. 2016;44:1693–717.PubMed Sandoval TA, Urueña CP, Llano M, Gómez-Cadena A, Hernández JF, Sequeda LG, Loaiza AE, Barreto A, Li S, Fiorentino S. Standardized extract from Caesalpinia spinosa is cytotoxic over cancer stem cells and enhance anticancer activity of doxorubicin. Am J Chin Med. 2016;44:1693–717.PubMed
78.
go back to reference Sotillo WS, Villagomez R, Smiljanic S, Huang X, Malakpour A, Kempengren S, Rodrigo G, Almanza G, Sterner O, Oredsson S. Anti-cancer stem cell activity of a sesquiterpene lactone isolated from Ambrosia arborescens and of a synthetic derivative. PLoS ONE. 2017;12:e0184304.PubMedPubMedCentral Sotillo WS, Villagomez R, Smiljanic S, Huang X, Malakpour A, Kempengren S, Rodrigo G, Almanza G, Sterner O, Oredsson S. Anti-cancer stem cell activity of a sesquiterpene lactone isolated from Ambrosia arborescens and of a synthetic derivative. PLoS ONE. 2017;12:e0184304.PubMedPubMedCentral
79.
go back to reference Woo Y, Oh J, Kim J-S. Suppression of Nrf2 activity by chestnut leaf extract increases chemosensitivity of breast cancer stem cells to paclitaxel. Nutrients. 2017;9:760.PubMedCentral Woo Y, Oh J, Kim J-S. Suppression of Nrf2 activity by chestnut leaf extract increases chemosensitivity of breast cancer stem cells to paclitaxel. Nutrients. 2017;9:760.PubMedCentral
Metadata
Title
Suppressive role of Viola odorata extract on malignant characters of mammosphere-derived breast cancer stem cells
Authors
S. Yousefnia
D. Naseri
F. Seyed Forootan
M. Tabatabaeian
F. Moattar
T. Ghafghazi
M. H. Nasr Esfahani
K. Ghaedi
Publication date
01-09-2020
Publisher
Springer International Publishing
Published in
Clinical and Translational Oncology / Issue 9/2020
Print ISSN: 1699-048X
Electronic ISSN: 1699-3055
DOI
https://doi.org/10.1007/s12094-020-02307-9

Other articles of this Issue 9/2020

Clinical and Translational Oncology 9/2020 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine