3D cultures of prostate cancer cells cultured in a novel high-throughput culture platform are more resistant to chemotherapeutics compared to cells cultured in monolayer

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Chambers, Karen F ^a,b   Mosaad, Eman M O ^a,b   Russell, Pamela J ^a,b   Clements, Judith A ^a,b   Doran, Michael R ^a,b,c  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b TRANSLATIONAL RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; DOCETAXEL; BAYSILON; DIMETICONE;

3D CULTURE; APOPTOSIS; ARTICLE; CANCER RESISTANCE; CANCER TISSUE; CELL AGGREGATION; CELL GROWTH; CELL POLARITY; CELL VIABILITY; CHEMOTHERAPY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; CULTURE TECHNIQUE; DRUG RESPONSE; DRUG SCREENING; DRUG SENSITIVITY; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IN VIVO STUDY; MICROWELL PLATE; MONOLAYER CULTURE; PROSTATE CANCER CELL LINE; CELL CULTURE TECHNIQUE; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; COMPARATIVE STUDY; DRUG EFFECTS; DRUG RESISTANCE; MALE; PATHOLOGY; PROCEDURES; PROSTATIC NEOPLASMS; TISSUE MICROARRAY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL AGGREGATION; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DIMETHYLPOLYSILOXANES; DRUG RESISTANCE, NEOPLASM; HUMANS; MALE; PROSTATIC NEOPLASMS; TISSUE ARRAY ANALYSIS;

EID: 84915749674     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0111029     Document Type: Article

References (43)

1. Pampaloni F, Reynaud EG, Stelzer EH (2007) The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Biol 8: 839-845.
2. Bissell MJ (1981) The differentiated state of normal and malignant cells or how to define a "normal" cell in culture. Int Rev Cytol 70: 27-100.
3. Kenny PA, Lee GY, Myers CA, Neve RM, Semeiks JR, et al. (2007) The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression. Mol Oncol 1: 84-96.
4. Rhee S, Grinnell F (2007) Fibroblast mechanics in 3D collagen matrices. Adv Drug Deliv Rev 59: 1299-1305.
5. Amatangelo MD, Bassi DE, Klein-Szanto AJ, Cukierman E (2005) Stromaderived three-dimensional matrices are necessary and sufficient to promote desmoplastic differentiation of normal fibroblasts. Am J Pathol 167: 475-488.
6. Li Q, Chen C, Kapadia A, Zhou Q, Harper MK, et al. (2011) 3D models of epithelial-mesenchymal transition in breast cancer metastasis: high-throughput screening assay development, validation, and pilot screen. J Biomol Screen 16: 141-154.
7. Griffith LG, Swartz MA (2006) Capturing complex 3D tissue physiology in vitro. Nature reviews Molecular cell biology 7: 211-224.
8. Ohmori T, Yang JL, Price JO, Arteaga CL (1998) Blockade of tumor cell transforming growth factor-betas enhances cell cycle progression and sensitizes human breast carcinoma cells to cytotoxic chemotherapy. Experimental cell research 245: 350-359.
9. Takagi A, Watanabe M, Ishii Y, Morita J, Hirokawa Y, et al. (2007) Threedimensional cellular spheroid formation provides human prostate tumor cells with tissue-like features. Anticancer research 27: 45-53.
10. Hartman O, Zhang C, Adams EL, Farach-Carson MC, Petrelli NJ, et al. (2010) Biofunctionalization of electrospun PCL-based scaffolds with perlecan domain IV peptide to create a 3-D pharmacokinetic cancer model. Biomaterials 31: 5700-5718.
11. Grantab R, Sivananthan S, Tannock IF (2006) The penetration of anticancer drugs through tumor tissue as a function of cellular adhesion and packing density of tumor cells. Cancer research 66: 1033-1039.
12. Winkenwerder JJ, Palechek PL, Reece JS, Saarinen MA, Arnold MA, et al. (2003) Evaluating prostate cancer cell culturing methods: a comparison of cell morphologies and metabolic activity. Oncology reports 10: 783-789.
13. Babur BK, Ghanavi P, Levett P, Lott WB, Klein T, et al. (2013) The interplay between chondrocyte redifferentiation pellet size and oxygen concentration. PLoS One 8: e58865.
14. Cook MM, Futrega K, Osiecki M, Kabiri M, Kul B, et al. (2012) Micromarrows-three-dimensional coculture of hematopoietic stem cells and mesenchymal stromal cells. Tissue engineering Part C, Methods 18: 319-328.
15. Bello D, Webber MM, Kleinman HK, Wartinger DD, Rhim JS (1997) Androgen responsive adult human prostatic epithelial cell lines immortalized by human papillomavirus 18. Carcinogenesis 18: 1215-1223.
16. Horoszewicz JS, Leong SS, Chu TM, Wajsman ZL, Friedman M, et al. (1980) The LNCaP cell line-a new model for studies on human prostatic carcinoma. Prog Clin Biol Res 37: 115-132.
17. Chambers KF, Bacon JR, Kemsley EK, Mills RD, Ball RY, et al. (2009) Gene expression profile of primary prostate epithelial and stromal cells in response to sulforaphane or iberin exposure. The Prostate 69: 1411-1421.
18. Chambers KF, Pearson JF, Aziz N, O'Toole P, Garrod D, et al. (2011) Stroma regulates increased epithelial lateral cell adhesion in 3D culture: a role for actin/cadherin dynamics. PLoS One 6: e18796.
19. Chambers KF, Pearson JF, Pellacani D, Aziz N, Guzvic M, et al. (2011) Stromal upregulation of lateral epithelial adhesions: gene expression analysis of signalling pathways in prostate epithelium. J Biomed Sci 18: 45.
20. Hakanson M, Textor M, Charnley M (2011) Engineered 3D environments to elucidate the effect of environmental parameters on drug response in cancer. Integrative biology: quantitative biosciences from nano to macro 3: 31-38.
21. Xia Y, Whitesides GM (1998) Soft Lithography. Angewandte Chemie International Edition 37: 550-575.
22. Ochsner M, Dusseiller MR, Grandin HM, Luna-Morris S, Textor M, et al. (2007) Micro-well arrays for 3D shape control and high resolution analysis of single cells. Lab on a chip 7: 1074-1077.
23. Kim JE, O'Sullivan ML, Sanchez CA, Hwang M, Israel MA, et al. (2011) Investigating synapse formation and function using human pluripotent stem cellderived neurons. Proceedings of the National Academy of Sciences of the United States of America 108: 3005-3010.
24. Markway BD, Tan GK, Brooke G, Hudson JE, Cooper-White JJ, et al. (2010) Enhanced chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in low oxygen environment micropellet cultures. Cell transplantation 19: 29-42.
25. Kabiri M, Kul B, Lott WB, Futrega K, Ghanavi P, et al. (2012) 3D mesenchymal stem/stromal cell osteogenesis and autocrine signalling. Biochemical and biophysical research communications 419: 142-147.
26. Quent VM, Loessner D, Friis T, Reichert JC, Hutmacher DW (2010) Discrepancies between metabolic activity and DNA content as tool to assess cell proliferation in cancer research. Journal of cellular and molecular medicine 14: 1003-1013.
27. Geiger B, Spatz JP, Bershadsky AD (2009) Environmental sensing through focal adhesions. Nature reviews Molecular cell biology 10: 21-33.
28. Plachot C, Chaboub LS, Adissu HA, Wang L, Urazaev A, et al. (2009) Factors necessary to produce basoapical polarity in human glandular epithelium formed in conventional and high-throughput three-dimensional culture: example of the breast epithelium. BMC biology 7: 77.
29. Hebner C, Weaver VM, Debnath J (2008) Modeling morphogenesis and oncogenesis in three-dimensional breast epithelial cultures. Annual review of pathology 3: 313-339.
30. Dow LE, Kauffman JS, Caddy J, Zarbalis K, Peterson AS, et al. (2007) The tumour-suppressor Scribble dictates cell polarity during directed epithelial migration: regulation of Rho GTPase recruitment to the leading edge. Oncogene 26: 2272-2282.
31. Kollmannsberger P, Bidan CM, Dunlop JWC, Fratzl P (2011) The physics of tissue patterning and extracellular matrix organisation: how cells join forces. Soft matter 7: 9549-9560.
32. Howlett AR, Bissell MJ (1993) The influence of tissue microenvironment (stroma and extracellular matrix) on the development and function of mammary epithelium. Epithelial cell biology 2: 79-89.
33. Bello-DeOcampo D, Kleinman HK, Webber MM (2001) The role of alpha 6 beta 1 integrin and EGF in normal and malignant acinar morphogenesis of human prostatic epithelial cells. Mutation research 480-481: 209-217.
34. Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, et al. (2010) Multicellular tumor spheroids: an underestimated tool is catching up again. Journal of biotechnology 148: 3-15.
35. Dufau I, Frongia C, Sicard F, Dedieu L, Cordelier P, et al. (2012) Multicellular tumor spheroid model to evaluate spatio-temporal dynamics effect of chemotherapeutics: application to the gemcitabine/CHK1 inhibitor combination in pancreatic cancer. BMC Cancer 12: 15.
36. Ballangrud AM, Yang WH, Dnistrian A, Lampen NM, Sgouros G (1999) Growth and characterization of LNCaP prostate cancer cell spheroids. Clinical cancer research: an official journal of the American Association for Cancer Research 5: 3171s-3176s.
37. Sieh S, Taubenberger AV, Rizzi SC, Sadowski M, Lehman ML, et al. (2012) Phenotypic characterization of prostate cancer LNCaP cells cultured within a bioengineered microenvironment. PLoS One 7: e40217.
38. Doran MR, Markway BD, Clark A, Athanasas-Platsis S, Brooke G, et al. (2010) Membrane bioreactors enhance microenvironmental conditioning and tissue development. Tissue engineering Part C, Methods 16: 407-415.
39. Mackler NJ, Pienta KJ (2005) Drug insight: Use of docetaxel in prostate and urothelial cancers. Nature clinical practice Urology 2: 92-100; quiz 101 p following 112.
40. Hongisto V, Jernstrom S, Fey V, Mpindi JP, Kleivi Sahlberg K, et al. (2013) High-throughput 3D screening reveals differences in drug sensitivities between culture models of JIMT1 breast cancer cells. PLoS One 8: e77232.
41. Montero A, Fossella F, Hortobagyi G, Valero V (2005) Docetaxel for treatment of solid tumours: a systematic review of clinical data. The lancet oncology 6: 229-239.
42. Minchinton AI, Tannock IF (2006) Drug penetration in solid tumours. Nature reviews Cancer 6: 583-592.
43. Au JL, Jang SH, Zheng J, Chen CT, Song S, et al. (2001) Determinants of drug delivery and transport to solid tumors. Journal of controlled release: official journal of the Controlled Release Society 74: 31-46.