Nicotine reduces effectiveness of doxorubicin chemotherapy and promotes CD44+CD24‑ cancer stem cells in MCF‑7 cell populations

Türker Şener,Leyla; Güven,Celal; Şener,Aziz; Adin Çinar,Suzan; Solakoğlu,Seyhun; Albeniz,Işil

doi:10.3892/etm.2018.6149

Nicotine reduces effectiveness of doxorubicin chemotherapy and promotes CD44+CD24‑ cancer stem cells in MCF‑7 cell populations

Authors:
- Leyla Türker Şener
- Celal Güven
- Aziz Şener
- Suzan Adin Çinar
- Seyhun Solakoğlu
- Işil Albeniz
View Affiliations

Affiliations: Department of Biophysics, Istanbul Faculty of Medicine, Istanbul University, 34093 Istanbul, Turkey, Department of Biophysics, Faculty of Medicine, Niğde Ömer Halisdemir, 02040 Nigde, Turkey, Department of General Surgery, Kanuni Sultan Suleyman Training and Research Hospital, 34306 Istanbul, Turkey, Department of Immunology, Institute of Experimental Medicine, Istanbul University, 34093 Istanbul, Turkey, Department of Histology and Embryology, Istanbul Faculty of Medicine, Istanbul University, 34093 Istanbul, Turkey
Published online on: May 10, 2018 https://doi.org/10.3892/etm.2018.6149
Pages: 21-28
Copyright: © Türker Şener et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Breast cancer is the most common type of cancer in females and the second most common cause of cancer mortality after lung cancer. Cancer stem cells represent a novel approach to target cancer and reduce cancer recurrence and metastasis. Many patients with breast cancer continue to smoke after receiving their diagnosis. Nicotine is a key factor in tobacco addiction and also changes some cellular functions, such as activation of mitogenic pathways, angiogenesis and cell proliferation. In the present study, the impact of nicotine was assessed in a population of MCF‑7 human breast cancer cells. Cluster of differentiation (CD)44+CD24‑ cancer stem cell population of MCF‑7 cells were evaluated using flow cytometry and scanning electron microscopy. Chemoresistance effects of nicotine were demonstrated in these cells. These findings demonstrated harmful effects of nicotine following metastasis of cancer, owing to the chemoresistance produced through uninterrupted smoking, which may impact the effectiveness of treatment.

View Figures

View References

1	Gonzalez-Angulo AM, Morales-Vasquez F and Hortobagyi GN: Overview of resistance to systemic therapy in patients with breast cancer. Adv Exp Med Biol. 608:1–22. 2007. View Article : Google Scholar : PubMed/NCBI
2	Quail DF and Joyce JA: Microenvironmental regulation of tumor progression and metastasis. Nat Med. 19:1423–1437. 2013. View Article : Google Scholar : PubMed/NCBI
3	De Laurentiis A, Pardo OE, Palamidessi A, Jackson SP, Schoenwaelder SM, Reichmann E, Scita G and Arcaro A: The catalytic class I(A) PI3K isoforms play divergent roles in breast cancer cell migration. Cell Signal. 23:529–541. 2011. View Article : Google Scholar : PubMed/NCBI
4	Bailly C: topoisomerase I poisons and suppressors as anticancer drugs. Curr Med Chem. 7:39–58. 2000. View Article : Google Scholar : PubMed/NCBI
5	Housman G, Byler S, Heerboth S, Lapinska K, Longacre M, Snyder N and Sarkar S: drug resistance in cancer: An overview. Cancers (Basel). 6:1769–1792. 2014. View Article : Google Scholar : PubMed/NCBI
6	Samet JM, Avila-Tang E, Boffetta P, Hannan LM, Olivo-Marston S, Thun MJ and Rudin CH: Lung cancer in never smokers: Clinical epidemiology and environmental risk factors. Clin Cancer Res. 15:5626–5645. 2009. View Article : Google Scholar : PubMed/NCBI
7	Cancer among adults from exposure to secondhand smoke, The health consequences of involuntary exposure to tobacco smoke: A Report of the Surgeon General. Atlanta (GA): Centers for Disease Control and Prevention (US); 2006
8	Benowitz NL: Biomarkers of Cigarette SmokingMonograph 7: The FTC Cigarette Test Method for Detemining Tar, Nicotine, and Carbon Monoxide Yields of U.S. Cigarettes. National Cancer Institute; Bethesda, MD: pp. 93–111. 1988
9	Centers for Disease Control and Prevention (US); National Center for Chronic Disease Prevention and Health Promotion (US); Office on Smoking and Health (US): Nicotine Addiction: Past and PresentHow Tobacco Smoke Causes Disease: The Biology and Behavioral Basis for Smoking-Attributable Disease: A Report of the Surgeon General. Centers for Disease Control and Prevention (US); Atlanta, GA: 2010
10	Dani JA and De Biasi M: Cellular mechanisms of nicotine addiction. Pharmacol Biochem Behav. 70:439–446. 2001. View Article : Google Scholar : PubMed/NCBI
11	Clark CA, McEachern MD, Shah SH, Rong Y, Rong X, Smelley CL, Caldito GC, Abreo FW and Nathan CO: Curcumin inhibits carcinogen and nicotine-induced mammalian target of rapamycin pathway activation in head and neck squamous cell carcinoma. Cancer Prev Res (Phila). 3:1586–1595. 2010. View Article : Google Scholar : PubMed/NCBI
12	Schaal C and Chellappan SP: Nicotine-mediated cell proliferation and tumor progression in smoking-related cancers. Mol Cancer Res. 12:14–23. 2014. View Article : Google Scholar : PubMed/NCBI
13	Heeschen C, Jang JJ, Weis M, Pathak A, Kaji S, Hu RS, Tsao PS, Johnson FL and Cooke JP: Nicotine stimulates angiogenesis and promotes tumor growth and atherosclerosis. Nat Med. 7:833–839. 2001. View Article : Google Scholar : PubMed/NCBI
14	Petros WP, Younis IR, Ford JN and Weed SA: Effects of tobacco smoking and nicotine on cancer treatment. Pharmacotherapy. 32:920–931. 2012. View Article : Google Scholar : PubMed/NCBI
15	Singh S, Pillai S and Chellappan S: Nicotinic acetylcholine receptor signaling in tumor growth and metastasis. J Oncol. 2011:4567432011. View Article : Google Scholar : PubMed/NCBI
16	Suraneni MV and Badeaux MD: Tumor-Initiating cells, cancer metastasis and therapeutic implications, madame curie bioscience databaseMadame Curie Bioscience Database [Internet]. Landes Bioscience; Austin, TX: 2013
17	Davis R, Rizwani W, Banerjee S, Kovacs M, Haura E, Coppola D and Chellappan S: Nicotine promotes tumor growth and metastasis in mouse models of lung cancer. PLoS One. 4:e75242009. View Article : Google Scholar : PubMed/NCBI
18	Honeth G, Bendahl PO, Ringner M, Saal LH, Gruvberger-Saal SK, Lövgren K, Grabau D, Fernö M, Borg A and Hegardt C: The CD44⁺/CD24⁻ phenotype is enriched in basal-like breast tumors. Breast Cancer Res. 10:R532008. View Article : Google Scholar : PubMed/NCBI
19	Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ and Clarke MF: Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 100:3983–3988. 2003. View Article : Google Scholar : PubMed/NCBI
20	Lorico A and Rappa G: Phenotypic heterogeneity of breast cancer stem cells. J Oncol. 2011:1350392011. View Article : Google Scholar : PubMed/NCBI
21	Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, Huang Y, Hu X, Su F, Lieberman J and Song E: let-7 Regulates self renewal and tumorigenicity of breast cancer cells. Cell. 131:1109–1123. 2007. View Article : Google Scholar : PubMed/NCBI
22	De Laurentiis M, Cianniello D, Caputo R, Stanzione B, Arpino G, Cinieri S, Lorusso V and De Placido S: Treatment of triple negative breast cancer (TNBC): Current options and future perspectives. Cancer Treat Rev. 36 Suppl 3:S80–S86. 2010. View Article : Google Scholar : PubMed/NCBI
23	Muñoz-Pinedo C, El Mjiyad N and Ricci JE: Cancer metabolism: Current perspectives and future directions. Cell Death Dis. 3:e2482012. View Article : Google Scholar : PubMed/NCBI
24	Rivera E and Gomez H: Chemotherapy resistance in metastatic breast cancer: The evolving role of ixabepilone. Breast Cancer Res. 12 Suppl 2:S22010. View Article : Google Scholar : PubMed/NCBI
25	Park SY, Lee HE, Li H, Shipitsin M, Gelman R and Polyak K: Heterogeneity for stemcell-related markers according to tumor subtype and histologic stage in breast cancer. Clin Cancer Res. 16:876–887. 2010. View Article : Google Scholar : PubMed/NCBI
26	Hussain T and Nguyen QT: Molecular imaging for cancer diagnosis and surgery. Adv Drug Deliv Rev. 66:90–100. 2014. View Article : Google Scholar : PubMed/NCBI
27	Groebel K, Hoelzle K, Wittenbrink MM, Ziegler U and Hoelzle LE: Mycoplasma suis invades porcine erythrocytes. Infect Immun. 77:576–584. 2009. View Article : Google Scholar : PubMed/NCBI
28	Varol B, Bektaş M, Nurten R and Bermek E: The cytotoxic effect of diphtheria toxin on the actin cytoskeleton. Cell Mol Biol Lett. 17:49–61. 2012. View Article : Google Scholar : PubMed/NCBI
29	Mitchell RR, Szabo E, Benoit YD, Case DT, Mechael R, Alamilla J, Lee HJ, Fiebig-Comyn A, Gillespie DC and Bhatia M: Activation of neural cell fate programs toward direct conversion of adult human fibroblasts into tri-potent neural progenitors using OCT-4. Stem Cells Dev. 23:1937–1946. 2014. View Article : Google Scholar : PubMed/NCBI
30	Jensen K, Afroze S, Munshi MK, Guerrier M and Glaser SS: Mechanisms for nicotine in the development and progression of gastrointestinal cancers. Transl Gastrointest Cancer. 1:81–87. 2012.PubMed/NCBI
31	Karamboulas C and Ailles L: Developmental signaling pathways in cancer stem cells of solid tumors. Biochim Biophys Acta. 1830:2481–2495. 2013. View Article : Google Scholar : PubMed/NCBI
32	Pereira ML, Carvalho JC, Peres F, Gutierres M and Fernandes MH: Behaviour of human osteoblastic cells cultured on plasma-sprayed titanium implants in the presence of nicotine. Clin Oral Implants Res. 19:582–589. 2008. View Article : Google Scholar : PubMed/NCBI
33	Berger MR and Zeller WJ: Interaction of nicotine with anticancer treatment. Klin Wochenschr. 66 Suppl 11:S127–S133. 1988.
34	Benowitz NL, Hukkanen J and Jacob P III: Nicotine chemistry, metabolism, kinetics and biomarkers. Handb Exp Pharmacol. 29–60. 2009. View Article : Google Scholar : PubMed/NCBI
35	Hukkanen J, Jacob P III and Benowitz NL: Metabolism and disposition kinetics of nicotine. Pharmacol Rev. 57:79–115. 2005. View Article : Google Scholar : PubMed/NCBI
36	Russell MA, Feyerabend C and Cole PV: Plasma nicotine levels after cigarette smoking and chewing nicotine gum. Br Med J. 1:1043–1046. 1976. View Article : Google Scholar : PubMed/NCBI
37	Sobus SL and Warren GW: The biologic effects of cigarette smoke on cancer cells. Cancer. 120:3617–2627. 2014. View Article : Google Scholar : PubMed/NCBI
38	Warren GW and Singh AK: Nicotine and lung cancer. J Carcinog. 12:12013. View Article : Google Scholar : PubMed/NCBI
39	Wei W and Lewis MT: Identifying and targeting tumor-initiating cells in the treatment of breast cancer. Endocr Relat Cancer. 22:R135–R155. 2015. View Article : Google Scholar : PubMed/NCBI
40	Murin S and Inciardi J: Cigarette smoking and the risk of pulmonary metastasis from breast cancer. Chest. 119:1635–1640. 2001. View Article : Google Scholar : PubMed/NCBI
41	Pomorski P, Wasik A, Kołodziejczyk J, GrêBecka L and Kłopocka W: Nicotine affects behaviour, morphology and cortical cytoskeleton of amoeba proteus. Acta Protozool. 43:193–198. 2004.
42	Krause RM, Buisson B, Bertrand S, Corringer PJ, Galzi JL, Changeux JP and Bertrand D: Ivermectin: A possible allosteric effector of the alpha 7 neuronal nicotinic acetylcholine receptor. Mol Pharmacol. 53:283–294. 1998. View Article : Google Scholar : PubMed/NCBI
43	Dean M, Fojo T and Bates S: Tumour stem cells and drug resistance. Nat Rev Cancer. 5:275–284. 2005. View Article : Google Scholar : PubMed/NCBI
44	Sak K: Chemotherapy and dietary phytochemical agents. Chemother Res Pract. 2012:2825702012.PubMed/NCBI
45	You HB and Park K: Targeted drug delivery to tumors: Myths, reality and possibility. J Control Release. 153:198–205. 2011. View Article : Google Scholar : PubMed/NCBI