Metastatic renal cell carcinoma cells growing in 3D on poly‑D‑lysine or laminin present a stem‑like phenotype and drug resistance
- Authors:
- Klaudia K. Brodaczewska
- Zofia F. Bielecka
- Kamila Maliszewska‑Olejniczak
- Cezary Szczylik
- Camillo Porta
- Ewa Bartnik
- Anna M. Czarnecka
-
Affiliations: Department of Oncology with Laboratory of Molecular Oncology, Military Institute of Medicine, 04‑141 Warsaw, Poland, Department of Internal Medicine and Therapeutics, University of Pavia, I‑27100 Pavia, Italy, Institute of Genetics and Biotechnology, Faculty of Biology, University of Warsaw, Poland - Published online on: September 18, 2019 https://doi.org/10.3892/or.2019.7321
- Pages: 1878-1892
-
Copyright: © Brodaczewska et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
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|
Meyerrose TE, Herrbrich P, Hess DA and Nolta JA: Immune-deficient mouse models for analysis of human stem cells. BioTechniques. 35:1262–1272. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Gedye C, Sirskyj D, Lobo NC, Meens J, Hyatt E, Robinette M, Fleshner N, Hamilton RJ, Kulkarni G, Zlotta A, et al: Cancer stem cells are underestimated by standard experimental methods in clear cell renal cell carcinoma. Sci Rep. 6:252202016. View Article : Google Scholar : PubMed/NCBI | |
|
Grotenhuis BA, Wijnhoven BP and van Lanschot JJ: Cancer stem cells and their potential implications for the treatment of solid tumors. J Surg Oncol. 106:209–215. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Buczek M, Escudier B, Bartnik E, Szczylik C and Czarnecka A: Resistance to tyrosine kinase inhibitors in clear cell renal cell carcinoma: From the patient's bed to molecular mechanisms. Biochim Biophys Acta. 1845:31–41. 2014.PubMed/NCBI | |
|
Bielecka ZF, Czarnecka AM, Solarek W, Kornakiewicz A and Szczylik C: Mechanisms of acquired resistance to tyrosine kinase inhibitors in clear-cell renal cell carcinoma (ccRCC). Curr Signal Transduct Ther. 8:218–228. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Bussolati B, Bruno S, Grange C, Ferrando U and Camussi G: Identification of a tumor-initiating stem cell population in human renal carcinomas. FASEB J. 22:3696–3705. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Czarnecka A, Matak D, Solarek W, Khan M and Szczylik C: Hypoxia response regulates clear cell renal cell carcinoma tumor initiating cells. BJU Int. 112:1–17. 2013. | |
|
Debeb BG, Zhang X, Krishnamurthy S, Gao H, Cohen E, Li L, Rodriguez AA, Landis MD, Lucci A, Ueno NT, et al: Characterizing cancer cells with cancer stem cell-like features in 293T human embryonic kidney cells. Mol Cancer. 9:1802010. View Article : Google Scholar : PubMed/NCBI | |
|
Gassenmaier M, Chen D, Buchner A, Henkel L, Schiemann M, Mack B, Schendel DJ, Zimmermann W and Pohla H: CXC chemokine receptor 4 is essential for maintenance of renal cell carcinoma-initiating cells and predicts metastasis. Stem Cells. 31:1467–1476. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Ueda K, Ogasawara S, Akiba J, Nakayama M, Todoroki K, Ueda K, Sanada S, Suekane S, Noguchi M, Matsuoka K and Yano H: Aldehyde dehydrogenase 1 identifies cells with cancer stem cell-like properties in a human renal cell carcinoma cell line. PLoS One. 8:e754632013. View Article : Google Scholar : PubMed/NCBI | |
|
Khan MI, Czarnecka AM, Lewicki S, Helbrecht I, Brodaczewska K, Koch I, Zdanowski R, Król M and Szczylik C: Comparative gene expression profiling of primary and metastatic renal cell carcinoma stem cell-like cancer cells. PLoS One. 11:e01657182016. View Article : Google Scholar : PubMed/NCBI | |
|
Hu J, Guan W, Liu P, Dai J, Tang K, Xiao H, Qian Y, Sharrow AC, Ye Z, Wu L and Xu H: Endoglin is essential for the maintenance of self-renewal and chemoresistance in renal cancer stem cells. Stem Cell Reports. 9:464–477. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Beaver CM, Ahmed A and Masters JR: Clonogenicity: Holoclones and meroclones contain stem cells. PLoS One. 9:e898342014. View Article : Google Scholar : PubMed/NCBI | |
|
Rappa G, Mercapide J, Anzanello F, Prasmickaite L, Xi Y, Ju J, Fodstad O and Lorico A: Growth of cancer cell lines under stem cell-like conditions has the potential to unveil therapeutic targets. Exp Cell Res. 314:2110–2122. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Lichner Z, Saleh C, Subramaniam V, Seivwright A, Prud'homme GJ and Yousef GM: miR-17 inhibition enhances the formation of kidney cancer spheres with stem cell/tumor initiating cell properties. Oncotarget. 6:5567–5581. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Matak D, Brodaczewska KK, Szczylik C, Koch I, Myszczyszyn A, Lipiec M, Lewicki S, Szymanski L, Zdanowski R and Czarnecka AM: Functional significance of CD105-positive cells in papillary renal cell carcinoma. BMC Cancer. 17:212017. View Article : Google Scholar : PubMed/NCBI | |
|
Matak D, Szymanski L, Szczylik C, Sledziewski R, Lian F, Bartnik E, Sobocinska A and Czarnecka AM: Biology of renal tumour cancer stem cells applied in medicine. Contemp Oncol (Pozn). 19:A44–A51. 2015.PubMed/NCBI | |
|
Czarnecka AM and Szczylik C: Renal cell carcinoma cancer stem cells as therapeutic targets. Curr Sign Trans Ther. 8:203–209. 2013. View Article : Google Scholar | |
|
Peired AJ, Sisti A and Romagnani P: Renal cancer stem cells: Characterization and targeted therapies. Stem Cells Int. 2016:83426252016. View Article : Google Scholar : PubMed/NCBI | |
|
Bomken S, Fiser K, Heidenreich O and Vormoor J: Understanding the cancer stem cell. Br J Cancer. 103:439–445. 2011. View Article : Google Scholar | |
|
Nakano I and Chiocca EA: Finding drugs against CD133+ glioma subpopulations. J Neurosurg. 114:648–650. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Qiu W, Wang X, Leibowitz B, Liu H, Barker N, Okada H, Oue N, Yasui W, Clevers H, Schoen RE, et al: Chemoprevention by nonsteroidal anti-inflammatory drugs eliminates oncogenic intestinal stem cells via SMAC-dependent apoptosis. Proc Natl Acad Sci USA. 107:20027–20032. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Prud'homme GJ, Glinka Y, Toulina A, Ace O, Subramaniam V and Jothy S: Breast cancer stem-like cells are inhibited by a non-toxic aryl hydrocarbon receptor agonist. PLoS One. 5:e138312010. View Article : Google Scholar : PubMed/NCBI | |
|
Morrison R, Schleicher SM, Sun Y, Niermann KJ, Kim S, Spratt DE, Chung CH and Lu B: Targeting the mechanisms of resistance to chemotherapy and radiotherapy with the cancer stem cell hypothesis. J Oncol. 2011:9418762011. View Article : Google Scholar : PubMed/NCBI | |
|
Escudier B, Eisen T, Stadler WM, Szczylik C, Oudard S, Siebels M, Negrier S, Chevreau C, Solska E, Desai AA, et al: Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med. 356:125–134. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Motzer RJ, Hutson TE, Tomczak P, Michaelson MD, Bukowski RM, Rixe O, Oudard S, Negrier S, Szczylik C, Kim ST, et al: Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med. 356:115–124. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Sternberg CN, Davis ID, Mardiak J, Szczylik C, Lee E, Wagstaff J, Barrios CH, Salman P, Gladkov OA, Kavina A, et al: Pazopanib in locally advanced or metastatic renal cell carcinoma: Results of a randomized phase III trial. J Clin Oncol. 28:1061–1068. 2011. View Article : Google Scholar | |
|
Yuan ZX, Mo J, Zhao G, Shu G, Fu HL and Zhao W: Targeting strategies for renal cell carcinoma: From renal cancer cells to renal cancer stem cells. Front Pharmacol. 7:4232016. View Article : Google Scholar : PubMed/NCBI | |
|
Roskoski R Jr: Sunitinib: A VEGF and PDGF receptor protein kinase and angiogenesis inhibitor. Biochem Biophys Res Commun. 356:323–328. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, Chan KW, Ciceri P, Davis MI, Edeen PT, et al: A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol. 26:127–132. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Huang D, Ding Y, Li Y, Luo WM, Zhang ZF, Snider J, Vandenbeldt K, Qian CN and the BT: Sunitinib acts primarily on tumor endothelium rather than tumor cells to inhibit the growth of renal cell carcinoma. Cancer Res. 70:1053–1062. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Brossa A, Grange C, Mancuso L, Annaratone L, Satolli MA, Mazzone M, Camussi G and Bussolati B: Sunitinib but not VEGF blockade inhibits cancer stem cell endothelial differentiation. Oncotarget. 6:11295–11309. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Potapova O, Laird AD, Nannini MA, Barone A, Li G, Moss KG, Cherrington JM and Mendel DB: Contribution of individual targets to the antitumor efficacy of the multitargeted receptor tyrosine kinase inhibitor SU11248. Mol Cancer Ther. 5:1280–1289. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Abrams TJ, Murray LJ, Pesenti E, Holway VW, Colombo T, Lee LB, Cherrington JM and Pryer NK: Preclinical evaluation of the tyrosine kinase inhibitor SU11248 as a single agent and in combination with ‘standard of care’ therapeutic agents for the treatment of breast cancer. Mol Cancer Ther. 2:1011–1021. 2003.PubMed/NCBI | |
|
Czarnecka AM, Solarek W, Kornakiewicz A and Szczylik C: Tyrosine kinase inhibitors target cancer stem cells in renal cell cancer. Oncol Rep. 35:1433–1442. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Diaz R, Nguewa PA, Redrado M, Manrique I and Calvo A: Sunitinib reduces tumor hypoxia and angiogenesis, and radiosensitizes prostate cancer stem-like cells. Prostate. 75:1137–1149. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Varna M, Gapihan G, Feugeas JP, Ratajczak P, Tan S, Ferreira I, Leboeuf C, Setterblad N, Duval A, Verine J, et al: Stem cells increase in numbers in perinecrotic areas in human renal cancer. Clin Cancer Res. 21:916–924. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Zhu Y, Liu H, Xu L, An H, Liu W, Liu Y, Lin Z and Xu J: p21-activated kinase 1 determines stem-like phenotype and sunitinib resistance via NF-kappaB/IL-6 activation in renal cell carcinoma. Cell Death Dis. 6:e16372015. View Article : Google Scholar : PubMed/NCBI | |
|
Chinchar E, Makey KL, Gibson J, Chen F, Cole SA, Megason GC, Vijayakumar S, Miele L and Gu JW: Sunitinib significantly suppresses the proliferation, migration, apoptosis resistance, tumor angiogenesis and growth of triple-negative breast cancers but increases breast cancer stem cells. Vasc Cell. 6:122014. View Article : Google Scholar : PubMed/NCBI | |
|
Conley SJ, Gheordunescu E, Kakarala P, Newman B, Korkaya H, Heath AN, Clouthier SG and Wicha MS: Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Natl Acad Sci USA. 109:2784–2789. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Lamb R, Ozsvari B, Lisanti CL, Tanowitz HB, Howell A, Martinez-Outschoorn UE, Sotgia F and Lisanti MP: Antibiotics that target mitochondria effectively eradicate cancer stem cells, across multiple tumor types: Treating cancer like an infectious disease. Oncotarget. 6:4569–4584. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Relier S, Yazdani L, Ayad O, Choquet A, Bourgaux JF, Prudhomme M, Pannequin J, Macari F and David A: Antibiotics inhibit sphere-forming ability in suspension culture. Cancer Cell Int. 16:62016. View Article : Google Scholar : PubMed/NCBI | |
|
Mays AN, Osheroff N, Xiao Y, Wiemels JL, Felix CA, Byl JA, Saravanamuttu K, Peniket A, Corser R, Chang C, et al: Evidence for direct involvement of epirubicin in the formation of chromosomal translocations in t(15;17) therapy-related acute promyelocytic leukemia. Blood. 115:326–330. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Jiang XL, Zhang Y, Luo CL and Wu XH: Targeting renal cell carcinoma with gambogic acid in combination with sunitinib in vitro and in vivo. Asian Pac J Cancer Prev. 13:6463–6468. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Bielecka ZF, Maliszewska-Olejniczak K, Safir IJ, Szczylik C and Czarnecka AM: Three-dimensional cell culture model utilization in cancer stem cell research. Biol Rev Camb Philos Soc. 92:1505–1520. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Brodaczewska KK, Szczylik C, Fiedorowicz M, Porta C and Czarnecka AM: Choosing the right cell line for renal cell cancer research. Mol Cancer. 15:832016. View Article : Google Scholar : PubMed/NCBI | |
|
Kim S and Alexander CM: Tumorsphere assay provides more accurate prediction of in vivo responses to chemotherapeutics. Biotechnol Lett. 36:481–488. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Wierzbicki PM, Klacz J, Rybarczyk A, Slebioda T, Stanislawowski M, Wronska A, Kowalczyk A, Matuszewski M and Kmiec Z: Identification of a suitable qPCR reference gene in metastatic clear cell renal cell carcinoma. Tumour Biol. 35:12473–12487. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Maliszewska-Olejniczak K, Brodaczewska KK, Bielecka ZF and Czarnecka AM: Three-dimensional cell culture model utilization in renal carcinoma cancer stem cell research. Methods Mol Biol. 1817:47–66. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Kaminska K, Szczylik C, Bielecka ZF, Bartnik E, Porta C, Lian F and Czarnecka AM: The role of the cell-cell interactions in cancer progression. J Cell Mol Med. 19:283–296. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Myszczyszyn A, Czarnecka AM, Matak D, Szymanski L, Lian F, Kornakiewicz A, Bartnik E, Kukwa W, Kieda C and Szczylik C: The role of hypoxia and cancer stem cells in renal cell carcinoma pathogenesis. Stem Cell Rev. 11:919–943. 2015. View Article : Google Scholar : | |
|
Khan MI, Debski KJ, Dabrowski M, Czarnecka AM and Szczylik C: Gene set enrichment analysis and ingenuity pathway analysis of metastatic clear cell renal cell carcinoma cell line. Am J Physiol Renal Physiol. 311:F424–F436. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou N, Lu F, Liu C, Xu K, Huang J, Yu D and Bi L: IL-8 induces the epithelial-mesenchymal transition of renal cell carcinoma cells through the activation of AKT signaling. Oncol Lett. 12:1915–1920. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Larson AR, Lee CW, Lezcano C, Zhan Q, Huang J, Fischer AH and Murphy GF: Melanoma spheroid formation involves laminin-associated vasculogenic mimicry. Am J Pathol. 184:71–78. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Langan LM, Dodd NJ, Owen SF, Purcell WM, Jackson SK and Jha AN: Direct Measurements of Oxygen Gradients in Spheroid Culture System Using Electron Parametric Resonance Oximetry. PLoS One. 11:e01494922016. View Article : Google Scholar : PubMed/NCBI | |
|
Zheng X, Wang X, Mao H, Wu W, Liu B and Jiang X: Hypoxia-specific ultrasensitive detection of tumours and cancer cells. Nat Commun. 6:58342015. View Article : Google Scholar : PubMed/NCBI | |
|
Lal A, Peters H, St Croix B, Haroon ZA, Dewhirst MW, Strausberg RL, Kaanders JH, van der Kogel AJ and Riggins GJ: Transcriptional response to hypoxia in human tumors. J Natl Cancer Inst. 93:1337–1343. 2019. View Article : Google Scholar | |
|
McKenna1 DJ, Errington R and Pors K: Current challenges and opportunities in treating hypoxic prostate tumors. J Cancer Metastasis Treat. 4:112018. View Article : Google Scholar | |
|
Ponte KF, Berro DH, Collet S, Constans JM, Emery E, Valable S and Guillamo JS: In vivo relationship between hypoxia and angiogenesis in human glioblastoma: A multimodal imaging study. J Nucl Med. 58:1574–1579. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Gunther S, Ruhe C, Derikito MG, Bose G, Sauer H and Wartenberg M: Polyphenols prevent cell shedding from mouse mammary cancer spheroids and inhibit cancer cell invasion in confrontation cultures derived from embryonic stem cells. Cancer Lett. 250:25–35. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Moreno-Manzano V, Rodriguez-Jimenez FJ, Acena-Bonilla JL, Fustero-Lardíes S, Erceg S, Dopazo J, Montaner D, Stojkovic M and Sánchez-Puelles JM: FM19G11, a new hypoxia-inducible factor (HIF) modulator, affects stem cell differentiation status. J Biol Chem. 285:1333–1342. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Covello KL, Kehler J, Yu H, Gordan JD, Arsham AM, Hu CJ, Labosky PA, Simon MC and Keith B: HIF-2alpha regulates Oct-4: Effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev. 20:557–570. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Mathieu J, Zhang Z, Zhou W, Wang AJ, Heddleston JM, Pinna CM, Hubaud A, Stadler B, Choi M, Bar M, et al: HIF induces human embryonic stem cell markers in cancer cells. Cancer Res. 71:4640–4652. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Min SO, Lee SW, Bak SY and Kim KS: Ideal sphere-forming culture conditions to maintain pluripotency in a hepatocellular carcinoma cell lines. Cancer Cell Int. 15:952015. View Article : Google Scholar : PubMed/NCBI | |
|
Gupta PB, Fillmore CM, Jiang G, Shapira SD, Tao K, Kuperwasser C and Lander ES: Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell. 146:633–644. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Chen YC, Cheng YH, Ingram P and Yoon E: Single cell proteolytic assays to investigate cancer clonal heterogeneity and cell dynamics using an efficient cell loading scheme. Sci Rep. 6:271542016. View Article : Google Scholar : PubMed/NCBI | |
|
Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, Bernard L, Viale G, Pelicci PG and Di Fiore PP: Biological and Molecular Heterogeneity of Breast Cancers Correlates with Their Cancer Stem Cell Content. Cell. 140:62–73. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Nguyen LK, Cavadas MA, Scholz CC, Fitzpatrick SF, Bruning U, Cummins EP, Tambuwala MM, Manresa MC, Kholodenko BN, Taylor CT and Cheong A: A dynamic model of the hypoxia-inducible factor 1α (HIF-1α) network. J Cell Sci. 126:1454–1463. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Lafleur VN, Richard S and Richard DE: Transcriptional repression of hypoxia-inducible factor-1 (HIF-1) by the protein arginine methyltransferase PRMT1. Mol Biol Cell. 25:925–935. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Wang X, Ryu D, Houtkooper RH and Auwerx J: Antibiotic use and abuse: a threat to mitochondria and chloroplasts with impact on research, health, and environment. Bioessays. 37:1045–1053. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Sancho P, Barneda D and Heeschen C: Hallmarks of cancer stem cell metabolism. Br J Cancer. 114:1305–1312. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Gialeli C, Theocharis AD and Karamanos NK: Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. Febs J. 278:16–27. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Sumi T, Nakatani T, Yoshida H, Hyun Y, Yasui T, Matsumoto Y, Nakagawa E, Sugimura K, Kawashima H and Ishiko O: Expression of matrix metalloproteinases 7 and 2 in human renal cell carcinoma. Oncol Rep. 10:567–570. 2003.PubMed/NCBI | |
|
Lin YW, Lee LM, Lee WJ, Chu CY, Tan P, Yang YC, Chen WY, Yang SF, Hsiao M and Chien MH: Melatonin inhibits MMP-9 transactivation and renal cell carcinoma metastasis by suppressing Akt-MAPKs pathway and NF-κB DNA-binding activity. J Pineal Res. 60:277–290. 2017. View Article : Google Scholar | |
|
Roomi MW, Ivanov V, Kalinovsky T, Niedzwiecki A and Rath M: Modulation of human renal cell carcinoma 786-0 MMP-2 and MMP-9 activity by inhibitors and inducers in vitro. Med Oncol. 23:245–250. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Shrivastava S, Steele R, Sowadski M, Crawford SE, Varvares M and Ray RB: Identification of molecular signature of head and neck cancer stem-like cells. Sci Rep. 5:78192015. View Article : Google Scholar : PubMed/NCBI | |
|
Xin H, Zhang C, Herrmann A, Du Y, Figlin R and Yu H: Sunitinib inhibition of Stat3 induces renal cell carcinoma tumor cell apoptosis and reduces immunosuppressive cells. Cancer Res. 69:2506–2513. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Gotink KJ, Broxterman HJ, Labots M, de Haas RR, Dekker H, Honeywell RJ, Rudek MA, Beerepoot LV, Musters RJ, Jansen G, et al: Lysosomal sequestration of sunitinib: A novel mechanism of drug resistance. Clin Cancer Res. 17:7337–7346. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Liu H, Wang H, Li C, Zhang T, Meng X, Zhang Y and Qian H: Spheres from cervical cancer cells display stemness and cancer drug resistance. Oncol Lett. 12:2184–2188. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Sun FF, Hu YH, Xiong LP, Tu XY, Zhao JH, Chen SS, Song J and Ye XQ: Enhanced expression of stem cell markers and drug resistance in sphere-forming non-small cell lung cancer cells. Int J Clin Exp Pathol. 8:6287–6300. 2015.PubMed/NCBI | |
|
Chen SF, Chang YC, Nieh S, Liu CL, Yang CY and Lin YS: Nonadhesive culture system as a model of rapid sphere formation with cancer stem cell properties. PLoS One. 7:e318642012. View Article : Google Scholar : PubMed/NCBI | |
|
Harper LJ, Costea DE, Gammon L, Fazil B, Biddle A and Mackenzie IC: Normal and malignant epithelial cells with stem-like properties have an extended G2 cell cycle phase that is associated with apoptotic resistance. BMC Cancer. 10:1662010. View Article : Google Scholar : PubMed/NCBI | |
|
Fernandez-Fuente G, Mollinedo P, Grande L, Vazquez-Barquero A and Fernandez-Luna JL: Culture dimensionality influences the resistance of glioblastoma stem-like cells to multikinase inhibitors. Mol Cancer Ther. 13:1664–1672. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Chen W, Dong J, Haiech J, Kilhoffer MC and Zeniou M: Cancer stem cell quiescence and plasticity as major challenges in cancer therapy. Stem Cells Int. 2016:17409362016. View Article : Google Scholar : PubMed/NCBI | |
|
Moore N and Lyle S: Quiescent, slow-cycling stem cell populations in cancer: A review of the evidence and discussion of significance. J Oncol. 2011:3960762011. View Article : Google Scholar : PubMed/NCBI | |
|
Hedenfalk IA, Baldetorp B, Borg A and Oredsson SM: Activated cell cycle checkpoints in epirubicin-treated breast cancer cells studied by BrdUrd-flow cytometry. Cytometry. 29:321–327. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Grabarczyk P, Nahse V, Delin M, Przybylski G, Depke M, Hildebrandt P, Völker U and Schmidt CA: Increased expression of bcl11b leads to chemoresistance accompanied by G1 accumulation. PLoS One. 5(pii): e125322010. View Article : Google Scholar : PubMed/NCBI | |
|
Wang L, Guo H, Lin C, Yang L and Wang X: Enrichment and characterization of cancer stemlike cells from a cervical cancer cell line. Mol Med Rep. 9:2117–2123. 2014. View Article : Google Scholar : PubMed/NCBI |
