Investigating breast cancer cell behavior using tissue engineering scaffolds

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Guiro, Khadidiatou ^a   Patel, Shyam A ^b   Greco, Steven J ^b   Rameshwar, Pranela ^b   Arinzeh, Treena L ^a  

^a NEW JERSEY INSTITUTE OF TECHNOLOGY   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOPLATIN; CD24 ANTIGEN; CYCLIN D1; HERMES ANTIGEN; OCTAMER TRANSCRIPTION FACTOR 4; POLYCAPROLACTONE; PROTEIN BCL 2; TRANSCRIPTION FACTOR SOX2; TUMOR MARKER;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER RESISTANCE; CELL COUNT; CELL CYCLE; CELL PROLIFERATION; CELL RENEWAL; CELL SHAPE; CELL VIABILITY; CONCENTRATION RESPONSE; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG RESISTANCE; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IC50; PHENOTYPE; PROTEIN EXPRESSION; TISSUE ENGINEERING; BREAST TUMOR; CELL CULTURE TECHNIQUE; CELL SURVIVAL; DRUG EFFECTS; FEMALE; METABOLISM; PROCEDURES; TISSUE SCAFFOLD; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

BIOMARKERS, TUMOR; BREAST NEOPLASMS; CARBOPLATIN; CELL COUNT; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TUMOR MICROENVIRONMENT;

EID: 84926631267     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118724     Document Type: Article

References (96)

1. Phillips TM, McBride WH, Pajonk F. The response of CD24 (-/low)/CD44+ breast cancer-initiating cells to radiation. Journal of the National Cancer Institute 2006;98:1777-85. PMID: 17179479
2. Kamangar F, Dores GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 2006;24:2137-50.
3. Significance of CD44 and CD24 as Cancer Stem Cell Markers: An Enduring Ambiguity 2012. doi: 10. 1155/2012/708036 PMID: 22693526
4. Patel SA, Ramkissoon SH, Bryan M, Pliner LF, Dontu G, Patel PS, et al. Delineation of breast cancer cell hierarchy identifies the subset responsible for dormancy. Scientific reports 2012;2:906. doi: 10. 1038/srep00906 PMID: 23205268
5. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. Journal of the National Cancer Institute 2008;100:672-9. doi: 10. 1093/jnci/djn123 PMID: 18445819
6. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009;458:780-3. doi: 10.1038/nature07733 PMID: 19194462
7. Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proceedings of the National Academy of Sciences of the United States of America 2009;106:13820-5. doi: 10.1073/pnas. 0905718106 PMID: 19666588
8. Wikman H, Vessella R, Pantel K. Cancer micrometastasis and tumour dormancy. APMIS: acta pathologica, microbiologica, et immunologica Scandinavica 2008;116:754-70. doi: 10.1111/j.1600-0463. 2008.01033.x PMID: 18834417
9. Becker S, Becker-Pergola G, Wallwiener D, Solomayer EF, Fehm T. Detection of cytokeratin-positive cells in the bone marrow of breast cancer patients undergoing adjuvant therapy. Breast cancer research and treatment 2006;97:91-6. PMID: 16319975
10. Botchkina IL, Rowehl RA, Rivadeneira DE, Karpeh MS Jr., Crawford H, Dufour A, et al. Phenotypic subpopulations of metastatic colon cancer stem cells: genomic analysis. Cancer genomics & proteomics 2009;6:19-29.
11. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America 2003;100:3983-8. PMID: 12629218
12. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer research 2009;69:1302-13. doi: 10.1158/0008-5472. CAN-08-2741 PMID: 19190339
13. Liu S, Wicha MS. Targeting breast cancer stem cells. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 2010;28:4006-12.
14. Luqmani YA. Mechanisms of drug resistance in cancer chemotherapy. Medical principles and practice: international journal of the Kuwait University, Health Science Centre 2005;14 Suppl 1:35-48.
15. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer research 2005;65:5506-11. PMID: 15994920
16. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nature medicine 1997;3:730-7. PMID: 9212098
17. Diehn M, Cho RW, Clarke MF. Therapeutic implications of the cancer stem cell hypothesis. Seminars in radiation oncology 2009;19:78-86. doi: 10.1016/j.semradonc.2008.11.002 PMID: 19249645
18. Braun S, Auer D, Marth C. The prognostic impact of bonemarrowmicrometastases in women with breast cancer. Cancer investigation 2009;27:598-603. doi: 10.1080/07357900802574496 PMID: 19557580
19. Gonzalez-Angulo AM, Morales-Vasquez F, Hortobagyi GN. Overview of resistance to systemic therapy in patients with breast cancer. Advances in experimental medicine and biology 2007;608:1-22. PMID: 17993229
20. Morris SR, Carey LA. Molecular profiling in breast cancer. Reviews in endocrine & metabolic disorders 2007;8:185-98.
21. Sorokin L. The impact of the extracellular matrix on inflammation. Nature reviews Immunology 2010;10:712-23. doi: 10.1038/nri2852 PMID: 20865019
22. Hutmacher DW, Loessner D, Rizzi S, Kaplan DL, Mooney DJ, Clements JA. Can tissue engineering concepts advance tumor biology research? Trends in biotechnology 2010;28:125-33. doi: 10.1016/j. tibtech.2009.12.001 PMID: 20056286
23. Box C, Rogers SJ, Mendiola M, Eccles SA. Tumour-microenvironmental interactions: paths to progression and targets for treatment. Seminars in cancer biology 2010;20:128-38. doi: 10.1016/j.semcancer. 2010.06.004 PMID: 20599506
24. Fidler IJ. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nature reviews Cancer 2003;3:453-8. PMID: 12778135
25. Benton G, George J, Kleinman HK, Arnaoutova IP. Advancing science and technology via 3D culture on basement membrane matrix. Journal of cellular physiology 2009;221:18-25. doi: 10.1002/jcp. 21832 PMID: 19492404
26. Meads MB, Gatenby RA, Dalton WS. Environment-mediated drug resistance: a major contributor to minimal residual disease. Nature reviews Cancer 2009;9:665-74. doi: 10.1038/nrc2714 PMID: 19693095
27. Zhang S. Beyond the Petri dish. Nature biotechnology 2004;22:151-2. PMID: 14755282
28. Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nature reviews Cancer 2010;10:9-22. doi: 10.1038/nrc2748 PMID: 20029421
29. Lutolf MP, Gilbert PM, Blau HM. Designing materials to direct stem-cell fate. Nature 2009;462:433-41. doi: 10.1038/nature08602 PMID: 19940913
30. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nature reviews Cancer 2009;9:239-52. doi: 10.1038/nrc2618 PMID: 19279573
31. Fletcher DA, Mullins RD. Cell mechanics and the cytoskeleton. Nature 2010;463:485-92. doi: 10. 1038/nature08908 PMID: 20110992
32. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010;141:52-67. doi: 10.1016/j.cell.2010.03.015 PMID: 20371345
33. Yamada KM, Cukierman E. Modeling tissue morphogenesis and cancer in 3D. Cell 2007;130:601-10. PMID: 17719539
34. Keely PJ, Wu JE, Santoro SA. The spatial and temporal expression of the alpha 2 beta 1 integrin and its ligands, collagen I, collagen IV, and laminin, suggest important roles in mouse mammary morphogenesis. Differentiation; research in biological diversity 1995;59:1-13. PMID: 7589890
35. Alowami S, Troup S, Al-Haddad S, Kirkpatrick I, Watson PH. Mammographic density is related to stroma and stromal proteoglycan expression. Breast cancer research: BCR 2003;5:R129-35. PMID: 12927043
36. Boyd NF, Dite GS, Stone J, Gunasekara A, English DR, McCredie MR, et al. Heritability of mammographic density, a risk factor for breast cancer. The New England journal of medicine 2002;347:886-94. PMID: 12239257
37. Provenzano PP, Eliceiri KW, Campbell JM, Inman DR, White JG, Keely PJ. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC medicine 2006;4:38. PMID: 17190588
38. Wolf K, Friedl P. Functional imaging of pericellular proteolysis in cancer cell invasion. Biochimie 2005;87:315-20. PMID: 15781318
39. Friedl P, Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nature reviews Molecular cell biology 2009;10:445-57. doi: 10.1038/nrm2720 PMID: 19546857
40. Hegerfeldt Y, Tusch M, Brocker EB, Friedl P. Collective cell movement in primary melanoma explants: plasticity of cell-cell interaction, beta1-integrin function, and migration strategies. Cancer research 2002;62:2125-30. PMID: 11929834
41. Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, Kunz-Schughart LA. Multicellular tumor spheroids: an underestimated tool is catching up again. Journal of biotechnology 2010;148:3-15. doi: 10.1016/j.jbiotec.2010.01.012 PMID: 20097238
42. Justice BA, Badr NA, Felder RA. 3D cell culture opens new dimensions in cell-based assays. Drug discovery today 2009;14:102-7. doi: 10.1016/j.drudis.2008.11.006 PMID: 19049902
43. Pampaloni F, Reynaud EG, Stelzer EH. The third dimension bridges the gap between cell culture and live tissue. Nature reviews Molecular cell biology 2007;8:839-45. PMID: 17684528
44. Mazzoleni G, Di Lorenzo D, Steimberg N. Modelling tissues in 3D: the next future of pharmaco-toxicology and food research? Genes & nutrition 2009;4:13-22.
45. Lee GY, Kenny PA, Lee EH, Bissell MJ. Three-dimensional culture models of normal and malignant breast epithelial cells. Nature methods 2007;4:359-65. PMID: 17396127
46. Cichon MA, Gainullin VG, Zhang Y, Radisky DC. Growth of lung cancer cells in three-dimensional microenvironments reveals key features of tumor malignancy. Integrative biology: quantitative biosciences from nano to macro 2012;4:440-8.
47. Taboas JM, Maddox RD, Krebsbach PH, Hollister SJ. Indirect solid free form fabrication of local and global porous, biomimetic and composite 3D polymer-ceramic scaffolds. Biomaterials 2003;24:181-94. PMID: 12417192
48. Debnath J, Brugge JS. Modelling glandular epithelial cancers in three-dimensional cultures. Nature reviews Cancer 2005;5:675-88. PMID: 16148884
49. Cukierman E, Pankov R, Stevens DR, Yamada KM. Taking cell-matrix adhesions to the third dimension. Science (New York, NY) 2001;294:1708-12. PMID: 11721053
50. Fischbach C, Chen R, Matsumoto T, Schmelzle T, Brugge JS, Polverini PJ, et al. Engineering tumors with 3D scaffolds. Nature methods 2007;4:855-60. PMID: 17767164
51. Wang F, Weaver VM, Petersen OW, Larabell CA, Dedhar S, Briand P, et al. Reciprocal interactions between β1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: A different perspective in epithelial biology. Proceedings of the National Academy of Sciences 1998;95:14821-6. PMID: 9843973
52. Lee Y-S, Collins G, Livingston Arinzeh T. Neurite extension of primary neurons on electrospun piezoelectric scaffolds. Acta Biomater 2011;7:3877-86. doi: 10.1016/j.actbio.2011.07.013 PMID: 21810489
53. Li D, Wang Y, Xia Y. Electrospinning nanofibers as uniaxially aligned arrays and layer-by-layer stacked films. Advanced Materials 2004;16:361-6.
54. Foroni L, Vasuri F, Valente S, Gualandi C, Focarete ML, Caprara G, et al. The role of 3D microenvironmental organization in MCF-7 epithelial-mesenchymal transition after 7 culture days. Experimental cell research 2013;319:1515-22. doi: 10.1016/j.yexcr.2013.03.035 PMID: 23583658
55. Wang F, Shor L, Darling A, Khalil S, Sun W, Güçeri S, et al. Precision extruding deposition and characterization of cellular poly-caprolactone tissue scaffolds. Rapid Prototyping Journal 2004;10:42-9.
56. Lee YS, Collins G, Arinzeh TL. Neurite extension of primary neurons on electrospun piezoelectric scaffolds. Acta biomaterialia 2011;7:3877-86. doi: 10.1016/j.actbio.2011.07.013 PMID: 21810489
57. Patlolla A, Collins G, Arinzeh TL. Solvent-dependent properties of electrospun fibrous composites for bone tissue regeneration. Acta biomaterialia 2010;6:90-101. doi: 10.1016/j.actbio.2009.07.028 PMID: 19631769
58. Adams JM, Cory S. The Bcl-2 protein family: arbiters of cell survival. Science (New York, NY) 1998;281:1322-6. PMID: 9735050
59. Beck MT, Peirce SK, Chen WY. Regulation of bcl-2 gene expression in human breast cancer cells by prolactin and its antagonist, hPRL-G129R. Oncogene 2002;21:5047-55. PMID: 12140755
60. Richardson A, Kaye SB. Pharmacological inhibition of the Bcl-2 family of apoptosis regulators as cancer therapy. Current molecular pharmacology 2008;1:244-54. PMID: 20021437
61. Weigelt B, Peterse JL, van't Veer LJ. Breast cancer metastasis: markers and models. Nature reviews Cancer 2005;5:591-602. PMID: 16056258
62. Holyoake T, Jiang X, Eaves C, Eaves A. Isolation of a highly quiescent subpopulation of primitive leukemic cells in chronic myeloid leukemia. Blood 1999;94:2056-64. PMID: 10477735
63. Jorgensen HG, Allan EK, Graham SM, Godden JL, Richmond L, Elliott MA, et al. Lonafarnib reduces the resistance of primitive quiescent CML cells to imatinib mesylate in vitro. Leukemia 2005;19:1184-91. PMID: 15889158
64. Hu M, Polyak K. Molecular characterisation of the tumour microenvironment in breast cancer. European journal of cancer (Oxford, England: 1990) 2008;44:2760-5. doi: 10.1016/j.ejca.2008.09.038 PMID: 19026532
65. De Wever O, Demetter P, Mareel M, Bracke M. Stromal myofibroblasts are drivers of invasive cancer growth. International journal of cancer Journal international du cancer 2008;123:2229-38. doi: 10. 1002/ijc.23925 PMID: 18777559
66. Kong HJ, Boontheekul T, Mooney DJ. Quantifying the relation between adhesion ligand-receptor bond formation and cell phenotype. Proceedings of the National Academy of Sciences of the United States of America 2006;103:18534-9. PMID: 17124175
67. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. 'Green mice' as a source of ubiquitous green cells. FEBS letters 1997;407:313-9. PMID: 9175875
68. Goerges AL, Nugent MA. Regulation of vascular endothelial growth factor binding and activity by extracellular pH. The Journal of biological chemistry 2003;278:19518-25. PMID: 12637571
69. Kuschert GS, Hoogewerf AJ, Proudfoot AE, Chung CW, Cooke RM, Hubbard RE, et al. Identification of a glycosaminoglycan binding surface on human interleukin-8. Biochemistry 1998;37:11193-201. PMID: 9698365
70. Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nature reviews Cancer 2003;3:895-902. PMID: 14737120
71. Eliopoulos AG, Kerr DJ, Herod J, Hodgkins L, Krajewski S, Reed JC, et al. The control of apoptosis and drug resistance in ovarian cancer: influence of p53 and Bcl-2. Oncogene 1995;11:1217-28. PMID: 7478541
72. Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 2005;26:5474-91. PMID: 15860204
73. Gotz HE, Muller M, Emmel A, Holzwarth U, Erben RG, Stangl R. Effect of surface finish on the osseointegration of laser-treated titanium alloy implants. Biomaterials 2004;25:4057-64. PMID: 15046896
74. Cheng N, Wauthier E, Reid LM. Mature human hepatocytes from ex vivo differentiation of alginate-encapsulated hepatoblasts. Tissue engineering Part A 2008;14:1-7. doi: 10.1089/ten. a.2007.0131 PMID: 18333800
75. McLane JS, Rivet CJ, Gilbert RJ, Ligon LA. A biomaterial model of tumor stromal microenvironment promotes mesenchymal morphology but not epithelial to mesenchymal transition in epithelial cells. Acta biomaterialia 2014;10:4811-21. doi: 10.1016/j.actbio.2014.07.016 PMID: 25058401
76. Fisher RF, Hayes BP. The elastic constants and ultrastructure organization of regenerated basement membrane (lens capsule). Quarterly journal of experimental physiology (Cambridge, England) 1982;67:213-24. PMID: 6177018
77. Grant CA, Brockwell DJ, Radford SE, Thomson NH. Tuning the elastic modulus of hydrated collagen fibrils. Biophysical Journal 2009;97:2985-92. doi: 10.1016/j.bpj.2009.09.010 PMID: 19948128
78. Chen AA, Khetani SR, Lee S, Bhatia SN, Van Vliet KJ. Modulation of hepatocyte phenotype in vitro via chemomechanical tuning of polyelectrolyte multilayers. Biomaterials 2009;30:1113-20. doi: 10.1016/j. biomaterials.2008.10.055 PMID: 19046762
79. Yeung T, Georges PC, Flanagan LA, Marg B, Ortiz M, Funaki M, et al. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell motility and the cytoskeleton 2005;60:24-34. PMID: 15573414
80. Hartman O, Zhang C, Adams EL, Farach-Carson MC, Petrelli NJ, Chase BD, et al. Microfabricated electrospun collagen membranes for 3-D cancer models and drug screening applications. Biomacromolecules 2009;10:2019-32. doi: 10.1021/bm8012764 PMID: 19624098
81. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009;139:891-906. doi: 10.1016/j.cell.2009.10.027 PMID: 19931152
82. Pajerowski JD, Dahl KN, Zhong FL, Sammak PJ, Discher DE. Physical plasticity of the nucleus in stem cell differentiation. Proceedings of the National Academy of Sciences of the United States of America 2007;104:15619-24. PMID: 17893336
83. Simon DN, Wilson KL. The nucleoskeleton as a genome-associated dynamic 'network of networks'. Nature reviews Molecular cell biology 2011;12:695-708. doi: 10.1038/nrm3207 PMID: 21971041
84. Titushkin I, Cho M. Modulation of cellular mechanics during osteogenic differentiation of human mesenchymal stem cells. Biophysical journal 2007;93:3693-702. PMID: 17675345
85. Chowdhury F, Na S, Li D, Poh YC, Tanaka TS, Wang F, et al. Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nature materials 2010;9:82-8. doi: 10.1038/nmat2563 PMID: 19838182
86. Guck J, Schinkinger S, Lincoln B, Wottawah F, Ebert S, Romeyke M, et al. Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophysical journal 2005;88:3689-98. PMID: 15722433
87. Remmerbach TW, Wottawah F, Dietrich J, Lincoln B, Wittekind C, Guck J. Oral cancer diagnosis by mechanical phenotyping. Cancer research 2009;69:1728-32. doi: 10.1158/0008-5472. CAN-08-4073 PMID: 19223529
88. Beil M, Micoulet A, von Wichert G, Paschke S, Walther P, Omary MB, et al. Sphingosylphosphorylcholine regulates keratin network architecture and visco-elastic properties of human cancer cells. Nature cell biology 2003;5:803-11. PMID: 12942086
89. Swaminathan V, Mythreye K, O'Brien ET, Berchuck A, Blobe GC, Superfine R. Mechanical stiffness grades metastatic potential in patient tumor cells and in cancer cell lines. Cancer research 2011;71:5075-80. doi: 10.1158/0008-5472. CAN-11-0247 PMID: 21642375
90. Friedl P, Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nature reviews Cancer 2003;3:362-74. PMID: 12724734
91. Lu JY, Chen HC, Chu RY, Lin TC, Hsu PI, Huang MS, et al. Establishment of red fluorescent proteintagged HeLa tumor metastasis models: determination of DsRed2 insertion effects and comparison of metastatic patterns after subcutaneous, intraperitoneal, or intravenous injection. Clinical & experimental metastasis 2003;20:121-33.
92. Wang TC, Cardiff RD, Zukerberg L, Lees E, Arnold A, Schmidt EV. Mammary hyperplasia and carcinoma in MMTV-cyclin D1 transgenic mice. Nature 1994;369:669-71. PMID: 8208295
93. Lammie GA, Peters G. Chromosome 11q13 abnormalities in human cancer. Cancer cells (Cold Spring Harbor, NY: 1989) 1991;3:413-20. PMID: 1760243
94. Motokura T, Bloom T, Kim HG, Juppner H, Ruderman JV, Kronenberg HM, et al. A novel cyclin encoded by a bcl1-linked candidate oncogene. Nature 1991;350:512-5. PMID: 1826542
95. Hitomi M, Stacey DW. Cyclin D1 production in cycling cells depends on ras in a cell-cycle-specific manner. Current biology: CB 1999;9:1075-84. PMID: 10531005
96. Stacey DW. Cyclin D1 serves as a cell cycle regulatory switch in actively proliferating cells. Current opinion in cell biology 2003;15:158-63. PMID: 12648671