Review Article

Three-Dimensional Manufactured Supports for Breast Cancer Stem Cell Population Characterization

Author(s): Emma Polonio-Alcalá, Marc Rabionet, Santiago Ruiz-Martínez, Joaquim Ciurana and Teresa Puig*

Volume 20, Issue 8, 2019

Page: [839 - 851] Pages: 13

DOI: 10.2174/1389450120666181122113300

Price: $65

Abstract

Breast Cancer (BC) is the most common cancer among women and the second cause of female death for cancer. When the tumor is not correctly eradicated, there is a high relapse risk and incidence of metastasis. Breast Cancer Stem Cells (BCSCs) are responsible for initiating tumors and are resistant to current anticancer therapies being in part responsible for tumor relapse and metastasis. The study of BCSCs is limited due to their low percentage within both tumors and established cell models. Hence, three-dimensional (3D) supports are presented as an interesting tool to keep the stem-like features in 3D cell culture. In this review, several 3D culture systems are discussed. Moreover, scaffolds are presented as a tool to enrich in BCSCs in order to find new specific therapeutic strategies against this malignant subpopulation. Anticancer treatments focused on BCSCs could be useful for BC patients, with particular interest in those that progress to current therapies.

Keywords: Breast cancer, cancer stem cells, breast cancer stem cells biomarkers, three-dimensional cell culture, scaffolds, electrospinning, fused filament fabrication, additive manufacturing.

Graphical Abstract

[1]
Siegel R, Miller KD, Ahmedin J. Cancer Statistics, 2017. CA Cancer J Clin 2017; 67(1): 7-30.
[2]
Sotiriou C, Pusztai L. Gene-expression signatures in breast cancer. N Engl J Med 2009; 360(8): 790-800.
[3]
Perou CM, Sørlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature 2000; 406(6797): 747-52.
[4]
Sørlie T, Perou CM, Tibshirani R, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001; 98(19): 10869-74.
[5]
Pathmanathan N, Provan PJ, Mahajan H, et al. Characteristics of HER2-positive breast cancer diagnosed following the introduction of universal HER2 testing. Breast 2012; 21(6): 724-9.
[6]
Osborne CK, Schiff R. Mechanisms of endocrine resistance in breast cancer. Annu Rev Med 2011; 62(1): 233-47.
[7]
Tang Y, Wang Y, Kiani MF, Wang B. Classification, treatment strategy, and associated drug resistance in breast cancer. Clin Breast Cancer 2016; 16(5): 335-43.
[8]
Davies C, Godwin J, Gray R, et al. Relevance of breast cancer hormone receptors and other factors to the efficacy of adjuvant tamoxifen: Patient-level meta-analysis of randomised trials. Lancet (London, England) 2011; 378(9793): 771-84.
[9]
Bose R, Kavuri SM, Searleman AC, et al. Activating HER2 mutations in HER2 gene amplification negative breast cancer. Cancer Discov 2013; 3(2): 224-37.
[10]
Arteaga CL, Sliwkowski MX, Osborne CK, et al. Treatment of HER2-positive breast cancer: Current status and future perspectives. Nat Rev Clin Oncol 2011; 9(1): 16-32.
[11]
Cortés J, Curigliano G, Diéras V. Expert perspectives on biosimilar monoclonal antibodies in breast cancer. Breast Cancer Res Treat 2014; 144(2): 233-9.
[12]
Capelan M, Pugliano L, De Azambuja E, et al. Pertuzumab: New hope for patients with HER2-positive breast cancer. Ann Oncol 2013; 24(2): 273-82.
[13]
Dent R, Trudeau M, Pritchard KI, et al. Triple-negative breast cancer: Clinical features and patterns of recurrence. Clin Cancer Res 2007; 13(15): 4429-34.
[14]
Hudis CA, Gianni L. Triple-negative breast cancer: An Unmet Medical Need. Oncologist 2011; 16(Suppl. 1): 1-11.
[15]
Anders C, Carey LA. Understanding and treating triple-negative breast cancer. Oncol 2008; 22(11): 1-9.
[16]
Perou CM. Molecular stratification of triple-negative breast cancers. Oncologist 2011; 16(Suppl. 1): 61-70.
[17]
Sikov WM, Berry DA, Perou CM, et al. Impact of the addition of carboplatin and/or bevacizumab to neoadjuvant once-per-week paclitaxel followed by dose-dense doxorubicin and cyclophosphamide on pathologic complete response rates in stage ii to iii triple-negative breast cancer: CALGB 40603 (Alliance). J Clin Oncol 2015; 33(1): 13-21.
[18]
von Minckwitz G, Schneeweiss A, Loibl S, et al. Neoadjuvant carboplatin in patients with triple-negative and HER2-positive early breast cancer (GeparSixto; GBG 66): A randomised phase 2 trial. Lancet Oncol 2014; 15(7): 747-56.
[19]
Tutt A, Tovey H, Cheang MCU, et al. Carboplatin in BRCA1/2-mutated and triple-negative breast cancer BRCAness subgroups: the TNT Trial. Nat Med 2018; 24(5): 628-37.
[20]
Carey LA, Dees EC, Sawyer L, et al. The triple negative paradox: Primary tumor chemosensitivity of breast cancer subtypes. Clin Cancer Res 2007; 13(8): 2329-34.
[21]
Broxterman H, Gotink K, Verheul H. Understanding the causes of multidrug resistance in cancer: A comparison of doxorubicin and sunitinib. Drug Resist Updat 2009; 12: 114-26.
[22]
Clarke MF, Dick JE, Dirks PB, et al. Cancer stem cells--perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006; 66(19): 9339-44.
[23]
Tirino V, Desiderio V, Paino F, et al. Cancer stem cells in solid tumors: An overview and new approaches for their isolation and characterization. FASEB J 2013; 27(1): 13-24.
[24]
Kyjacova L, Hubackova S, Krejcikova K, et al. Radiotherapy-induced plasticity of prostate cancer mobilizes stem-like non-adherent, Erk signaling-dependent cells. Cell Death Differ 2015; 22(6): 898-911.
[25]
Nakamura K, Iinuma H, Aoyagi Y, Shibuya H, Watanabe T. Predictive value of cancer stem-like cells and cancer-associated genetic markers for peritoneal recurrence of colorectal cancer in patients after curative surgery. Oncol 2010; 78(5–6): 309-15.
[26]
Ho MM, Ng AV, Lam S, Hung JY. Side Population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 2007; 67(10): 4827-33.
[27]
Diehn M, Cho RW, Lobo NA, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009; 458(7239): 780-3.
[28]
Matsui W, Wang Q, Barber JP, et al. Clonogenic multiple myeloma progenitors, stem cell properties, and drug resistance. Cancer Res 2008; 68(1): 190-7.
[29]
Shaw FL, Harrison H, Spence K, et al. A detailed mammosphere assay protocol for the quantification of breast stem cell activity. J Mammary Gland Biol Neoplasia 2012; 17(2): 111-7.
[30]
Giró-Perafita A, Rabionet M, Puig T, Ciurana J. Optimization of Poli(Ɛ-caprolactone) scaffolds suitable for 3D cancer cell culture. Procedia CIRP. 2016;49 (The Second CIRP Conference on Biomanufacturing): 61-6.
[31]
Bomken S, Fišer K, Heidenreich O, Vormoor J. Understanding the cancer stem cell. Br J Cancer 2010; 103(4): 439-45.
[32]
Ito T, Zimdahl B, Reya T. aSIRTing control over cancer stem cells. Cancer Cell 2012; 21(2): 140-2.
[33]
Wang T, Shigdar S, Gantier MP, et al. Cancer stem cell targeted therapy: Progress amid controversies a brief view of anticancer therapy. Oncotarget 2015; 6(42): 44191-206.
[34]
Furth J, Kahn MC, Breedis C. The Transmission of Leukemia of Mice with a Single Cell. Am J Cancer 1937; 31(2): 276-82.
[35]
Ishibashi K. Studies on the number of cells necessary for the transplantation of Yoshida sarcoma; transmission of the tumor with a single cell. Gan 1950; 41(1): 1-14.
[36]
Hewitt HB. Studies of the quantitative transplantation of mouse sarcoma. Br J Cancer 1953; 7(3): 367-83.
[37]
Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3(7): 730-7.
[38]
Al-hajj M, Wicha MS, Benito-hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100(7): 3983-8.
[39]
Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 2003; 4(1): 33-45.
[40]
Naor D, Wallach-Dayan SB, Zahalka MA, Sionov RV. Involvement of CD44, a molecule with a thousand faces, in cancer dissemination. Semin Cancer Biol 2008; 18(4): 260-7.
[41]
Leung EL-H, Fiscus RR, Tung JW, et al. Non-small cell lung cancer cells expressing CD44 are enriched for stem cell-like properties. Jin D-Y, editor. PLoS One 2010;5(11): e14062.
[42]
Weber GF, Bronson RT, Ilagan J, et al. Absence of the CD44 gene prevents sarcoma metastasis. Cancer Res 2002; 62(8): 2281-6.
[43]
Gao AC, Lou W, Dong JT, Isaacs JT. CD44 is a metastasis suppressor gene for prostatic cancer located on human chromosome 11p13. Cancer Res 1997; 57(5): 846-9.
[44]
Naor D, Nedvetzki S, Golan I, Melnik L, Faitelson Y. CD44 in Cancer. Crit Rev Clin Lab Sci 2002; 39(6): 527-79.
[45]
Lopez JI, Camenisch TD, Stevens MV, et al. CD44 attenuates metastatic invasion during breast cancer progression. Cancer Res 2005; 65(15): 6755-63.
[46]
Lee HJ, Choe G, Jheon S, et al. CD24, a novel cancer biomarker, predicting disease-free survival of non-small cell lung carcinomas: A retrospective study of prognostic factor analysis from the viewpoint of forthcoming (seventh) new TNM classification. J Thorac Oncol 2010; 5(5): 649-57.
[47]
Zheng J, Li Y, Yang J, et al. NDRG2 inhibits hepatocellular carcinoma adhesion, migration and invasion by regulating CD24 expression. BMC Cancer 2011; 11(1): 251.
[48]
Kristiansen G, Winzer K-J, Mayordomo E, et al. CD24 expression is a new prognostic marker in breast cancer. Clin Cancer Res 2003; 9(13): 4906-13.
[49]
Jaggupilli A, Elkord E. Significance of CD44 and CD24 as Cancer Stem Cell Markers: An Enduring Ambiguity. Clin Dev Immunol 2012; 2012: 1-11.
[50]
Park E, Park SY, Sun P-L, et al. Prognostic significance of stem cell-related marker expression and its correlation with histologic subtypes in lung adenocarcinoma. Oncotarget 2016; 7(27): 42502-12.
[51]
Park SY, Lee HE, Li H, et al. Heterogeneity for stem cell-related markers according to tumor subtype and histologic stage in breast cancer. Clin Cancer Res 2010; 16(3): 876-87.
[52]
Schabath H, Runz S, Joumaa S, Altevogt P. CD24 affects CXCR4 function in pre-B lymphocytes and breast carcinoma cells. J Cell Sci 2006; 119(Pt 2): 314-25.
[53]
Honeth G, Bendahl P-O, Ringnér M, et al. The CD44+/CD24- phenotype is enriched in basal-like breast tumors. Breast Cancer Res 2008; 10(3): R53.
[54]
Mylona E, Giannopoulou I, Fasomytakis E, et al. The clinicopathologic and prognostic significance of CD44+/CD24(-/low) and CD44-/CD24+ tumor cells in invasive breast carcinomas. Hum Pathol 2008; 39(7): 1096-102.
[55]
Stuelten CH, Mertins SD, Busch JI, et al. Complex display of putative tumor stem cell markers in the NCI60 tumor cell line panel. Stem Cells 2010; 28(4): 649-60.
[56]
Sheridan C, Kishimoto H, Fuchs RK, et al. CD44+/CD24- breast cancer cells exhibit enhanced invasive properties: An early step necessary for metastasis. Breast Cancer Res 2006; 8(5): R59.
[57]
Fillmore CM, Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 2008; 10(2): 1-13.
[58]
Ricardo S, Vieira AF, Gerhard R, et al. Breast cancer stem cell markers CD44, CD24 and ALDH1: Expression distribution within intrinsic molecular subtype. J Clin Pathol 2011; 64(11): 937-46.
[59]
Chute JP, Muramoto GG, Whitesides J, et al. Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells. Proc Natl Acad Sci USA 2006; 103(31): 11707-12.
[60]
Ginestier C, Hur MH, Charafe-Jauffret E, et al. ALDH1 Is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007; 1(5): 555-67.
[61]
Liu S, Cong Y, Wang D, et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Reports 2014; 2(1): 78-91.
[62]
Lehmann BDB, Bauer J a J, Chen X, et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011; 121(7): 2750-67.
[63]
Fukudome K, Esmon CT. Identification, cloning, and regulation of a novel endothelial cell protein C/activated protein C receptor. J Biol Chem 1994; 269(42): 26486-91.
[64]
Schaffner F, Yokota N, Carneiro-Lobo T, et al. Endothelial protein c receptor function in murine and human breast cancer development. Derksen P, editor. PLoS One 2013; 8(4): e61071.
[65]
Wang D, Cai C, Dong X, et al. Identification of multipotent mammary stem cells by protein C receptor expression. Nature 2014; 517(7532): 81-4.
[66]
Wang D, Liu C, Wang J, et al. Protein C receptor stimulates multiple signaling pathways in breast cancer cells. J Biol Chem 2017; jbc.M117.814046.
[67]
D’Angelo RC, Ouzounova M, Davis A, et al. Notch reporter activity in breast cancer cell lines identifies a subset of cells with stem cell activity. Mol Cancer Ther 2015; 14(3): 779-87.
[68]
Pauklin S, Vallier L. Activin/Nodal signalling in stem cells. Development 2015; 142(4): 607-19.
[69]
Bodenstine TM, Chandler GS, Reed DW, et al. Nodal expression in triple-negative breast cancer: Cellular effects of its inhibition following doxorubicin treatment. Cell Cycle 2016; 15(9): 1295-302.
[70]
Kotiyal S, Bhattacharya S. Breast cancer stem cells, EMT and therapeutic targets. Biochem Biophys Res Commun 2014; 453(1): 112-6.
[71]
Nieto MA. Epithelial plasticity: A common theme in embryonic and cancer cells. Science 2013; 342(6159): 1234850.
[72]
Moreno-Bueno G, Portillo F, Cano A. Transcriptional regulation of cell polarity in EMT and cancer. Oncogene 2008; 27(55): 6958-69.
[73]
Mani SA, Guo W, Liao M-J, et al. The Epithelial-Mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133(4): 704-15.
[74]
Luo M, Brooks M, Wicha MS. Epithelial-mesenchymal plasticity of breast cancer stem cells: Implications for metastasis and therapeutic resistance. Curr Pharm Des 2015; 21(10): 1301-10.
[75]
Li W, Ma H, Zhang J, et al. Unraveling the roles of CD44/CD24 and ALDH1 as cancer stem cell markers in tumorigenesis and metastasis. Sci Rep 2017; 7(1): 13856.
[76]
Tanei T, Choi DS, Rodriguez AA, et al. Antitumor activity of Cetuximab in combination with Ixabepilone on triple negative breast cancer stem cells. Breast Cancer Res 2016; 18(1): 6.
[77]
Corominas-Faja B, Cuyàs E, Gumuzio J, et al. Chemical inhibition of acetyl-CoA carboxylase suppresses self-renewal growth of cancer stem cells. Oncotarget 2014; 5(18): 8306-16.
[78]
Diessner J, Bruttel V, Stein RG, et al. Targeting of preexisting and induced breast cancer stem cells with trastuzumab and trastuzumab emtansine (T-DM1). Cell Death Dis 2014; 5(3): e1149.
[79]
Naujokat C, Steinhart R. Salinomycin as a drug for targeting human cancer stem cells. J Biomed Biotechnol 2012; 2012: 44-6.
[80]
Yue W, Hamaï A, Tonelli G, et al. Inhibition of the autophagic flux by salinomycin in breast cancer stem-like/progenitor cells interferes with their maintenance. Autophagy 2013; 9(5): 714-29.
[81]
Lamb R, Ozsvari B, Lisanti CL, et al. Antibiotics that target mitochondria effectively eradicate cancer stem cells, across multiple tumor types: Treating cancer like an infectious disease. Oncotarget 2015; 6(7): 4569-84.
[82]
Kwok JM-M, Myatt SS, Marson CM, et al. Thiostrepton selectively targets breast cancer cells through inhibition of forkhead box M1 expression. Mol Cancer Ther 2008; 7(7): 2022-32.
[83]
Yang N, Zhou T-C, Lei X, et al. Inhibition of sonic hedgehog signaling pathway by thiazole antibiotic thiostrepton attenuates the cd44+/cd24-stem-like population and sphere-forming capacity in triple-negative breast cancer. Cell Physiol Biochem 2016; 38(3): 1157-70.
[84]
Li J, Xu W, Yuan X, et al. Polymer-lipid hybrid anti-HER2 nanoparticles for targeted salinomycin delivery to HER2-positive breast cancer stem cells and cancer cells. Int J Nanomedicine 2017; 12: 6909-21.
[85]
Liu P, Kumar IS, Brown S, et al. Disulfiram targets cancer stem-like cells and reverses resistance and cross-resistance in acquired paclitaxel-resistant triple-negative breast cancer cells. Br J Cancer 2013; 109(7): 1876-85.
[86]
Liu P, Brown S, Goktug T, et al. Cytotoxic effect of disulfiram/copper on human glioblastoma cell lines and ALDH-positive cancer-stem-like cells. Br J Cancer 2012; 107(9): 1488-97.
[87]
Yip NC, Fombon IS, Liu P, et al. Disulfiram modulated ROS-MAPK and NFκB pathways and targeted breast cancer cells with cancer stem cell-like properties. Br J Cancer 2011; 104(10): 1564-74.
[88]
Liu P, Wang Z, Brown S, et al. Liposome encapsulated Disulfiram inhibits NFκB pathway and targets breast cancer stem cells in vitro and in vivo. Oncotarget 2014; 5(17): 7471-85.
[89]
Eliaz RE, Szoka FC. Liposome-encapsulated doxorubicin targeted to CD44: a strategy to kill CD44-overexpressing tumor cells. Cancer Res 2001; 61(6): 2592-601.
[90]
Auzenne E, Ghosh SC, Khodadadian M, et al. Hyaluronic acid-paclitaxel: Antitumor efficacy against CD44(+) human ovarian carcinoma xenografts. Neoplasia 2007; 9(6): 479-86.
[91]
Coradini D, Pellizzaro C, Miglierini G, Daidone MG, Perbellini A. Hyaluronic acid as drug delivery for sodium butyrate: Improvement of the anti-proliferative activity on a breast-cancer cell line. Int J Cancer 1999; 81(3): 411-6.
[92]
Han N-K, Shin DH, Kim JS, et al. Hyaluronan-conjugated liposomes encapsulating gemcitabine for breast cancer stem cells. Int J Nanomedicine 2016; 11: 1413-25.
[93]
López-Lázaro M. Anticancer and carcinogenic properties of curcumin: Considerations for its clinical development as a cancer chemopreventive and chemotherapeutic agent. Mol Nutr Food Res 2008; 52(Suppl. 1): S103-27.
[94]
Yang CS, Wang X, Lu G, Picinich SC. Cancer prevention by tea: animal studies, molecular mechanisms and human relevance. Nat Rev Cancer 2009; 9(6): 429-39.
[95]
Giró-Perafita A, Palomeras S, Lum DH, et al. Preclinical evaluation of fatty acid synthase and egfr inhibition in triple negative breast cancer. Clin Cancer Res 2016; 22(13): 4687-97.
[96]
Charpentier MS, Whipple RA, Vitolo MI, et al. Curcumin targets breast cancer stem-like cells with microtentacles that persist in mammospheres and promote reattachment. Cancer Res 2014; 74(4): 1250-60.
[97]
Chung SS, Vadgama JV. Curcumin and epigallocatechin gallate inhibit the cancer stem cell phenotype via down-regulation of STAT3-NFκB signaling. Anticancer Res 2015; 35(1): 39-46.
[98]
Fani S, Kamalidehghan B, Lo KM, et al. Synthesis, structural characterization, and anticancer activity of a monobenzyltin compound against MCF-7 breast cancer cells. Drug Des Devel Ther 2015; 9: 6191-201.
[99]
Fani S, Dehghan F, Karimian H, et al. monobenzyltin complex c1 induces apoptosis in mcf-7 breast cancer cells through the intrinsic signaling pathway and through the targeting of mcf-7-derived breast cancer stem cells via the wnt/β-catenin signaling pathway. PLoS One 2016; 11(8): e0160836.
[100]
Ringer S. Concerning the influence exerted by each of the constituents of the blood on the contraction of the ventricle. J Physiol 1882; 3: 380-93.
[101]
Ringer S. A further contribution regarding the influence of the different constituents of the blood on the contraction of the heart. J Physiol 1883; 4: 29-42.
[102]
Roux W. Beiträge zur Entwicklungsmechanik des Embryo 1885
[103]
Loeb L. Über die enstehung von bindegewebe, leucocyten und roten blutkörperchen aus epithel und über eine methode. Chicago: Stern 1897; pp. 1-56.
[104]
Jolly J. Sur la durée de la vie et de la multiplication des cellules animales en dehors de l’organisme Comptes rendus des Séances la Société Biol 1903; 55: 1266-8.
[105]
Harrison R, Greenman M, Mall F, Jackson C. Observations of the living developing nerve fiber. Anat Rec 1907; 1(5): 116-28.
[106]
Earle WR, Stark TH, Straus NP, Brown MF, Shelton E. Production of Malignancy in Vitro; IV: The mouse fibroblast cultures and changes seen in the living cells. J Natl Cancer Inst 1943; 4(2): 165-212.
[107]
Gey G, Coffman W, Kubicek M. Tissue culture studies of the proliferative capacity of cervical carcinoma and normal epithelium. Cancer Res 1952; 12: 264-5.
[108]
Ehrmann RL, Gey GO. The growth of cells on a transparent gel of reconstituted rat-tail collagen. JNCI J Natl Cancer Inst 1956; 16(6): 1375-403.
[109]
Amstein CF, Hartman PA. Adaptation of plastic surfaces for tissue culture by glow discharge. J Clin Microbiol 1975; 2(1): 46-54.
[110]
Ryhan JA. Evolution of cell culture surfaces. Biofiles 2008; 3(8): 21-4.
[111]
Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a glance. J Cell Sci 2010; 123(Pt 24): 4195-200.
[112]
Theocharis AD, Skandalis SS, Gialeli C, Karamanos NK. Extracellular matrix structure. Adv Drug Deliv Rev 2016; 97: 4-27.
[113]
Thomas CH, Collier JH, Sfeir CS, Healy KE. Engineering gene expression and protein synthesis by modulation of nuclear shape. Proc Natl Acad Sci USA 2002; 99(4): 1972-7.
[114]
Vergani L, Grattarola M, Nicolini C. Modifications of chromatin structure and gene expression following induced alterations of cellular shape. Int J Biochem Cell Biol 2004; 36(8): 1447-61.
[115]
Xu F, Burg ÆKJL. Three-dimensional polymeric systems for cancer cell studies 2007; 135-43.
[116]
Hale JS, Li M, Lathia JD. The malignant social network: Cell-cell adhesion and communication in cancer stem cells. Cell Adhes Migr 2012; 6(4): 346-55.
[117]
Reynolds BA, Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 1996; 175(1): 1-13.
[118]
Weiss S, Reynolds BA, Vescovi AL, et al. Is there a neural stem cell in the mammalian forebrain? Trends Neurosci 1996; 19(9): 387-93.
[119]
Dontu G, Abdallah WM, Foley JM, et al. In vitro propagation and transcriptional profiling of human mammary stem / progenitor cells. Genes Dev 2003; 17(10): 1253-70.
[120]
Wichterle O, Lím D. Hydrophilic gels for biological use. Nature 1960; 185(4706): 117-8.
[121]
Ciurana J, Rodríguez CA. Trends in nanomaterials and processing for drug delivery of polyphenols in the treatment of cancer and other therapies. Curr Drug Targets 2017; 18(2): 135-46.
[122]
Saha K, Pollock JF, Schaffer DV, Healy KE. Designing synthetic materials to control stem cell phenotype. Curr Opin Chem Biol 2007; 11(4): 381-7.
[123]
Kleinman HK, Martin GR. Matrigel: Basement membrane matrix with biological activity. Semin Cancer Biol 2005; 15(5): 378-86.
[124]
Palomeras S, Rabionet M, Ferrer I, et al. Breast cancer stem cell culture and enrichment using poly(ϵ-Caprolactone) scaffolds. Molecules 2016; 21(4): 1-14.
[125]
Rabionet M, Yeste M, Puig T, Ciurana J. Electrospinning PCL scaffolds manufacture for three-dimensional breast cancer cell culture. Polymers (Basel) 2017; 9(8): 1-15.
[126]
Poincloux R, Lizárraga F, Chavrier P. Matrix invasion by tumour cells: A focus on MT1-MMP trafficking to invadopodia. J Cell Sci 2009; 122(Pt 17): 3015-24.
[127]
Knight E, Przyborski S. Advances in 3D cell culture technologies enabling tissue-like structures to be created in vitro. J Anat 2014; 1-11.
[128]
Domingos M, Dinucci D, Cometa S, et al. polycaprolactone scaffolds fabricated via bioextrusion for tissue engineering applications. Int J Biomater 2009; 2009: 1-9.
[129]
De Ciurana J, Serenó L, Vallès È. Selecting process parameters in RepRap additive manufacturing system for PLA scaffolds manufacture. In: Procedia CIRP 2013; pp. 152-7.
[130]
Bartolo P, Domingos M. Gloria a., Ciurana J. BioCell Printing: Integrated automated assembly system for tissue engineering constructs. CIRP Ann - Manuf Technol 2011; 60(1): 271-4.
[131]
Tan YJ, Tan X, Yeong WY, Tor SB. Additive manufacturing of patient-customizable scaffolds for tubular tissues using the melt-drawing method. Mater (Basel, Switzerland) 2016; 9(11): E893.
[132]
Rathore A, Cleary M, Naito Y, Rocco K, Breuer C. Development of tissue engineered vascular grafts and application of nanomedicine. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2012; 4(3): 257-72.
[133]
Barton SP, Marks R. Measurement of collagen-fibre diameter in human skin. J Cutan Pathol 1984; 11(1): 18-26.
[134]
Hartman O, Zhang C, Adams EL, et al. Microfabricated electrospun collagen membranes for 3-D cancer models and drug screening applications. Biomacromolecules 2009; 10(8): 2019-32.
[135]
Azari P, Luan NS, Gan SN, et al. Electrospun biopolyesters as drug screening platforms for corneal keratocytes. Int J Polym Mater Polym Biomater 2015; 64(15): 785-91.
[136]
Garg T, Singh O, Arora S, Murthy RSR. Scaffold: a novel carrier for cell and drug delivery. Crit Rev Ther Drug Carrier Syst 2012; 29(1): 1-63.
[137]
Faccendini A, Vigani B, Rossi S, et al. Nanofiber scaffolds as drug delivery systems to bridge spinal cord injury. Pharmaceuticals 2017; 10(4): 63.
[138]
Dai J, Jin J, Yang S, Li G. Doxorubicin-loaded PLA/pearl electrospun nanofibrous scaffold for drug delivery and tumor cell treatment. Mater Res Express 2017; 4(7): 075403.
[139]
Charafe-jauffret E, Ginestier C, Iovino F, et al. Breast cancer cell lines contain funtional cancer stem cells with metastatic capacity and distinct molecular signature. Cancer Res 2009; 69(4): 1302-13.
[140]
Tsuyada A, Chow A, Wu J, et al. CCL2 mediates cross-talk between cancer cells and stromal fibroblasts that regulates breast cancer stem cells. Cancer Res 2012; 72(11): 2768-79.
[141]
Feng S, Duan X, Lo P-K, et al. Expansion of breast cancer stem cells with fibrous scaffolds. Integr Biol (Camb) 2013; 5(5): 768-77.
[142]
Sims-Mourtada J. Niamat R a., Samuel S, Eskridge C, Kmiec EB. Enrichment of breast cancer stem-like cells by growth on electrospun polycaprolactone-chitosan nanofiber scaffolds. Int J Nanomedicine 2014; 9(1): 995-1003.
[143]
Saha S, Duan X, Wu L, et al. Electrospun fibrous scaffolds promote breast cancer cell alignment and epithelial-mesenchymal transition. Langmuir 2012; 28(4): 2028-34.
[144]
Rabionet M, Puig T, Ciurana J. Electrospinning parameters selection to manufacture polycaprolactone scaffolds for three-dimensional breast cancer cell culture and enrichment. Procedia CIRP [Internet]. 2017; 65: 267-72. Available from: http:// linkinghub.elsevier.com/retrieve/pii/S2212827117306479
[145]
Hinderer S, Schesny M, Bayrak A, et al. Engineering of fibrillar decorin matrices for a tissue-engineered trachea. Biomaterials 2012; 33(21): 5259-66.
[146]
Qian Y, Li L, Jiang C, et al. The effect of hyaluronan on the motility of skin dermal fibroblasts in nanofibrous scaffolds. Int J Biol Macromol 2015; 79: 133-43.
[147]
Wise SG, Byrom MJ, Waterhouse A, et al. A multilayered synthetic human elastin/polycaprolactone hybrid vascular graft with tailored mechanical properties. Acta Biomater 2011; 7(1): 295-303.
[148]
Lim SH, Mao H-Q. Electrospun scaffolds for stem cell engineering. Adv Drug Deliv Rev 2009; 61(12): 1084-96.
[149]
Srouji S, Kizhner T, Suss-Tobi E, Livne E, Zussman E. 3-D Nanofibrous electrospun multilayered construct is an alternative ECM mimicking scaffold. J Mater Sci Mater Med 2008; 19(3): 1249-55.
[150]
Yang X, Yang F, Walboomers XF, et al. The performance of dental pulp stem cells on nanofibrous PCL/gelatin/nHA scaffolds. J Biomed Mater Res 2009; 93(1)
[151]
Senthil R, Berly R, Ram TB, Gobi N. Electrospun poly(vinyl) alcohol/collagen nanofibrous scaffold hybridized by graphene oxide for accelerated wound healing. Int J Artif Organs 2018; 41(8): 467-73.
[152]
Pektok E, Nottelet B, Tille J-C, et al. Degradation and healing characteristics of small-diameter poly(epsilon-caprolactone) vascular grafts in the rat systemic arterial circulation. Circulation 2008; 118(24): 2563-70.
[153]
Cao H, Mchugh K, Chew SY, Anderson JM. The topographical effect of electrospun nanofibrous scaffolds on the in vivo and in vitro foreign body reaction. J Biomed Mater Res 2009; 93(3)
[154]
Joy J, Pereira J, Aid-Launais R, et al. Gelatin — Oxidized carboxymethyl cellulose blend based tubular electrospun scaffold for vascular tissue engineering. Int J Biol Macromol 2018; 107: 1922-35.
[155]
Chen ZCC, Ekaputra AK, Gauthaman K, et al. In vitro and in vivo analysis of co-electrospun scaffolds made of medical grade poly(3-caprolactone) and porcine collagen. J Biomater Sci Polym Ed 2008; 19(5): 693-707.
[156]
Tillman BW, Yazdani SK, Lee SJ, et al. The in vivo stability of electrospun polycaprolactone–collagen scaffolds in vascular reconstruction. Biomaterials 2009; 30(4): 583-8.
[157]
Huang Y, Shi R, Gong M, et al. Icariin-loaded electrospun PCL/gelatin sub-microfiber mat for preventing epidural adhesions after laminectomy. Int J Nanomedicine 2018; 13: 4831-44.
[158]
Li W-J, Chiang H, Kuo T-F, et al. Evaluation of articular cartilage repair using biodegradable nanofibrous scaffolds in a swine model: a pilot study. J Tissue Eng Regen Med 2009; 3(1): 1-10.
[159]
Buscemi S, Palumbo VD, Maffongelli A, et al. Electrospun PHEA-PLA/PCL scaffold for vascular regeneration: A Preliminary in Vivo Evaluation. Transplant Proc 2017; 49(4): 716-21.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy