High-Throughput 3D Screening Reveals Differences in Drug Sensitivities between Culture Models of JIMT1 Breast Cancer Cells

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Hongisto, Vesa ^a   Jernström, Sandra ^a,b,c   Fey, Vidal ^a   Mpindi, John Patrick ^d   Kleivi Sahlberg, Kristine ^b,c,e   Kallioniemi, Olli ^a,d   Perälä, Merja ^a  

^a VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c UNIVERSITY OF OSLO   (Norway)

^d UNIVERSITY OF HELSINKI   (Finland)

^e VESTRE VIKEN HOSPITAL TRUST   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ALANTOLACTONE; CASPASE 3; CASPASE 7; COLCHICINE; MATRIGEL; METHOTREXATE; POLYMACON; TRICIRIBINE; ANTINEOPLASTIC AGENT; COLLAGEN; DRUG COMBINATION; LAMININ; PROTEOGLYCAN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL GROWTH; CELL PROLIFERATION; CELL SPECIFICITY; CELL STRAIN JIMT1; CELL STRAIN MCF 7; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE TECHNIQUE; DRUG RESPONSE; DRUG SENSITIVITY; GENE EXPRESSION PROFILING; GENOME ANALYSIS; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERMETHOD COMPARISON; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; SIGNAL TRANSDUCTION; THREE DIMENSIONAL CELL CULTURE; TUMOR XENOGRAFT; TWO DIMENSIONAL CELL CULTURE; BREAST NEOPLASMS; COMPARATIVE STUDY; DRUG COMBINATION; DRUG EFFECTS; DRUG SCREENING; FEMALE; GENE EXPRESSION REGULATION; PROCEDURES; STATISTICAL MODEL; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; COLLAGEN; DRUG COMBINATIONS; DRUG SCREENING ASSAYS, ANTITUMOR; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LAMININ; LINEAR MODELS; POLYHYDROXYETHYL METHACRYLATE; PROTEOGLYCANS;

EID: 84886028975     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077232     Document Type: Article

References (49)

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. doi:10.1038/nrm2236. PubMed: 17684528.
2. 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. doi:10.1016/j.molonc.2007.02.004. PubMed: 18516279.
3. Wang F, Weaver VM, Petersen OW, Larabell CA, Dedhar S, et al. (1998) Reciprocal interactions between beta1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: A different perspective in epithelial biology. Proc Natl Acad Sci U S A 95: 14821-14826. doi:10.1073/pnas.95.25.14821. PubMed: 9843973.
4. Kim H, Phung Y, Ho M, (2012) Changes in global gene expression associated with 3D structure of tumors: An ex vivo matrix-free mesothelioma spheroid model. PLOS ONE 7: e39556. doi:10.1371/journal.pone.0039556. PubMed: 22737246.
5. Ghosh S, Spagnoli GC, Martin I, Ploegert S, Demougin P, et al. (2005) Three-dimensional culture of melanoma cells profoundly affects gene expression profile: A high density oligonucleotide array study. J Cell Physiol 204: 522-531. doi:10.1002/jcp.20320. PubMed: 15744745.
6. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, et al. (1997) Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 137: 231-245. doi:10.1083/jcb.137.1.231. PubMed: 9105051.
7. Park CC, Zhang H, Pallavicini M, Gray JW, Baehner F, et al. (2006) Beta1 integrin inhibitory antibody induces apoptosis of breast cancer cells, inhibits growth, and distinguishes malignant from normal phenotype in three dimensional cultures and in vivo. Cancer Res 66: 1526-1535. doi:10.1158/0008-5472.CAN-05-3071. PubMed: 16452209.
8. Park CC, Zhang HJ, Yao ES, Park CJ, Bissell MJ, (2008) Beta1 integrin inhibition dramatically enhances radiotherapy efficacy in human breast cancer xenografts. Cancer Res 68: 4398-4405. doi:10.1158/0008-5472.CAN-07-6390. PubMed: 18519702.
9. Pickl M, Ries CH, (2009) Comparison of 3D and 2D tumor models reveals enhanced HER2 activation in 3D associated with an increased response to trastuzumab. Oncogene 28: 461-468. doi:10.1038/onc.2008.394. PubMed: 18978815.
10. Weigelt B, Lo AT, Park CC, Gray JW, Bissell MJ, (2010) HER2 signaling pathway activation and response of breast cancer cells to HER2-targeting agents is dependent strongly on the 3D microenvironment. Breast Cancer Res Treat 122: 35-43. doi:10.1007/s10549-009-0502-2. PubMed: 19701706.
11. Li Q, Chow AB, Mattingly RR, (2010) Three-dimensional overlay culture models of human breast cancer reveal a critical sensitivity to mitogen-activated protein kinase kinase inhibitors. J Pharmacol Exp Ther 332: 821-828. doi:10.1124/jpet.109.160390. PubMed: 19952304.
12. Loessner D, Stok KS, Lutolf MP, Hutmacher DW, Clements JA, et al. (2010) Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells. Biomaterials 31: 8494-8506. doi:10.1016/j.biomaterials.2010.07.064. PubMed: 20709389.
13. Horning JL, Sahoo SK, Vijayaraghavalu S, Dimitrijevic S, Vasir JK, et al. (2008) 3-D tumor model for in vitro evaluation of anticancer drugs. Mol Pharm 5: 849-862. doi:10.1021/mp800047v. PubMed: 18680382.
14. David L, Dulong V, Le Cerf D, Cazin L, Lamacz M, et al. (2008) Hyaluronan hydrogel: An appropriate three-dimensional model for evaluation of anticancer drug sensitivity. Acta Biomater 4: 256-263. doi:10.1016/j.actbio.2007.08.012. PubMed: 17936097.
15. Lan SF, Safiejko-Mroczka B, Starly B, (2010) Long-term cultivation of HepG2 liver cells encapsulated in alginate hydrogels: A study of cell viability, morphology and drug metabolism. Toxicol Vitro 24: 1314-1323. doi:10.1016/j.tiv.2010.02.015. PubMed: 20171269.
16. Erlichman C, Vidgen D, (1984) Cytotoxicity of adriamycin in MGH-U1 cells grown as monolayer cultures, spheroids, and xenografts in immune-deprived mice. Cancer Res 44: 5369-5375. PubMed: 6488191.
17. Tanner M, Kapanen AI, Junttila T, Raheem O, Grenman S, et al. (2004) Characterization of a novel cell line established from a patient with herceptin-resistant breast cancer. Mol Cancer Ther 3: 1585-1592. PubMed: 15634652.
18. Folkman J, Moscona A, (1978) Role of cell shape in growth control. Nature 273: 345-349. doi:10.1038/273345a0. PubMed: 661946.
19. Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, et al. (2006) RankProd: A bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 222825-2827. doi:10.1093/bioinformatics/btl476. PubMed: 16982708.
20. Edgar R, Domrachev M, Lash AE, (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210. doi:10.1093/nar/30.1.207. PubMed: 11752295.
21. Suzuki R, Shimodaira H, (2006) Pvclust: An R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 221540-1542. doi:10.1093/bioinformatics/btl117.
22. Martin B, Chadwick W, Yi T, Park SS, Lu D, et al. (2012) VENNTURE--a novel venn diagram investigational tool for multiple pharmacological dataset analysis. PLOS ONE 7: e36911. doi:10.1371/journal.pone.0036911. PubMed: 22606307.
23. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol 5R80. doi:10.1186/gb-2004-5-10-r80.
24. Lin SM, Du P, Huber W, Kibbe WA, (2008) Model-based variance-stabilizing transformation for illumina microarray data. Nucleic Acids Res 36: e11. doi:10.1093/nar/gkm1075. PubMed: 18178591.
25. Du P, Kibbe WA, Lin SM, (2008) Lumi: A pipeline for processing illumina microarray. Bioinformatics 241547-1548. doi:10.1093/bioinformatics/btn224. PubMed: 18467348.
26. Smyth GK, Michaud J, Scott HS, (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21: 2067-2075. doi:10.1093/bioinformatics/bti270. PubMed: 15657102.
27. Shi Y, Bao YL, Wu Y, Yu CL, Huang YX, et al. (2011) Alantolactone inhibits cell proliferation by interrupting the interaction between cripto-1 and activin receptor type II A in activin signaling pathway. J Biomol Screen 16: 525-535. doi:10.1177/1087057111398486. PubMed: 21378277.
28. Schmeichel KL, Bissell MJ, (2003) Modeling tissue-specific signaling and organ function in three dimensions. J Cell Sci 116: 2377-2388. doi:10.1242/jcs.00503. PubMed: 12766184.
29. Kokkinos MI, Wafai R, Wong MK, Newgreen DF, Thompson EW, et al. (2007) Vimentin and epithelial-mesenchymal transition in human breast cancer--observations in vitro and in vivo. Cells Tissues Organs 185: 191-203. doi:10.1159/000101320. PubMed: 17587825.
30. Cheng WY, Kandel JJ, Yamashiro DJ, Canoll P, Anastassiou D, (2012) A multi-cancer mesenchymal transition gene expression signature is associated with prolonged time to recurrence in glioblastoma. PLOS ONE 7: e34705. doi:10.1371/journal.pone.0034705. PubMed: 22493711.
31. Lin Y, Buckhaults PJ, Lee JR, Xiong H, Farrell C, et al. (2009) Association of the actin-binding protein transgelin with lymph node metastasis in human colorectal cancer. Neoplasia 11: 864-873. PubMed: 19724680.
32. Lee GY, Kenny PA, Lee EH, Bissell MJ, (2007) Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods 4: 359-365. doi:10.1038/nmeth1015. PubMed: 17396127.
33. Gurski LA, Jha AK, Zhang C, Jia X, Farach-Carson MC, (2009) Hyaluronic acid-based hydrogels as 3D matrices for in vitro evaluation of chemotherapeutic drugs using poorly adherent prostate cancer cells. Biomaterials 30: 6076-6085. doi:10.1016/j.biomaterials.2009.07.054. PubMed: 19695694.
34. Serebriiskii I, Castelló-Cros R, Lamb A, Golemis EA, Cukierman E, (2008) Fibroblast-derived 3D matrix differentially regulates the growth and drug-responsiveness of human cancer cells. Matrix Biol 27: 573-585. doi:10.1016/j.matbio.2008.02.008. PubMed: 18411046.
35. Li ML, Aggeler J, Farson DA, Hatier C, Hassell J, et al. (1987) Influence of a reconstituted basement membrane and its components on casein gene expression and secretion in mouse mammary epithelial cells. Proc Natl Acad Sci U S A 84: 136-140. doi:10.1073/pnas.84.1.136. PubMed: 3467345.
36. Werb Z, Tremble P, Damsky CH, (1990) Regulation of extracellular matrix degradation by cell-extracellular matrix interactions. Cell Differ Dev 32: 299-306. doi:10.1016/0922-3371(90)90043-V. PubMed: 2151566.
37. Kobayashi H, Man S, Graham CH, Kapitain SJ, Teicher BA, et al. (1993) Acquired multicellular-mediated resistance to alkylating agents in cancer. Proc Natl Acad Sci U S A 90: 3294-3298. doi:10.1073/pnas.90.8.3294. PubMed: 8475071.
38. Heiser LM, Sadanandam A, Kuo WL, Benz SC, Goldstein TC, et al. (2012) Subtype and pathway specific responses to anticancer compounds in breast cancer. supplementary information. Proc Natl Acad Sci U S A 109: 2724-2729. doi:10.1073/pnas.1018854108. PubMed: 22003129.
39. Badiner GJ, Hamilton RD, Li LH, Bhuyan BK, (1987) Drug sensitivity of ten human tumor cell lines compared to mouse leukemia (L1210) cells. Invest New Drugs 5: 219-229. PubMed: 3667160.
40. Desoize B, Jardillier J, (2000) Multicellular resistance: A paradigm for clinical resistance? Crit. Rev Oncol 36: 193-207. doi:10.1016/S1040-8428(00)00086-X.
41. Miller BE, Miller FR, Heppner GH, (1985) Factors affecting growth and drug sensitivity of mouse mammary tumor lines in collagen gel cultures. Cancer Res 45: 4200-4205. PubMed: 4028010.
42. Pelletier H, Millot JM, Chauffert B, Manfait M, Genne P, et al. (1990) Mechanisms of resistance of confluent human and rat colon cancer cells to anthracyclines: Alteration of drug passive diffusion. Cancer Res 50: 6626-6631. PubMed: 2208125.
43. Garrido C, Chauffert B, Pinard D, Tibaut F, Genne P, et al. (1995) Circumvention of confluence-dependent resistance in a human multi-drug-resistant colon-cancer cell line. Int J Cancer 61: 873-879. doi:10.1002/ijc.2910610621. PubMed: 7790124.
44. Dimanche-Boitrel MT, Pelletier H, Genne P, Petit JM, Le Grimellec C, et al. (1992) Confluence-dependent resistance in human colon cancer cells: Role of reduced drug accumulation and low intrinsic chemosensitivity of resting cells. Int J Cancer 50: 677-682. doi:10.1002/ijc.2910500502. PubMed: 1544702.
45. Fernando A, Glaysher S, Conroy M, Pekalski M, Smith J, et al. (2006) Effect of culture conditions on the chemosensitivity of ovarian cancer cell lines. Anti Cancer Drugs 17: 913-919. doi:10.1097/01.cad.0000224445.23953.d9. PubMed: 16940801.
46. Bissell MJ, Kenny PA, Radisky DC, (2005) Microenvironmental regulators of tissue structure and function also regulate tumor induction and progression: The role of extracellular matrix and its degrading enzymes. Cold Spring Harb Symp Quant Biol 70: 343-356. doi:10.1101/sqb.2005.70.013. PubMed: 16869771.
47. Kuczek T, Axelrod DE, (1987) Tumor cell heterogeneity: Divided-colony assay for measuring drug response. Proc Natl Acad Sci U S A 84: 4490-4494. doi:10.1073/pnas.84.13.4490. PubMed: 3299370.
48. Miller FR, McEachern D, Miller BE, (1989) Growth regulation of mouse mammary tumor cells in collagen gel cultures by diffusible factors produced by normal mammary gland epithelium and stromal fibroblasts. Cancer Res 49: 6091-6097. PubMed: 2790822.
49. Aceto N, Duss S, Macdonald G, Meyer DS, Roloff TC, et al. (2012) Co-expression of HER2 and HER3 receptor tyrosine kinases enhances invasion of breast cells via stimulation of interleukin-8 autocrine secretion. Breast Cancer Res 14R131. doi:10.1186/bcr3329. PubMed: 23062209.