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The multicellular tumor spheroid model for high-throughput cancer drug discovery

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Pages 819-830 | Published online: 12 Jul 2012

Bibliography

  • DeVita VT Jr, Chu E. A history of cancer chemotherapy. Cancer Res 2008;68:8643-53
  • Burger AM, Fiebig HH. Preclinical screening for new anticancer agents. Humana Press; Totowa, New Jersey: 2004
  • Boyd MR. The NCI in vitro anticancer drug discovery screen. Humana Press; Totowa: 1997
  • Shoemaker RH. The NCI60 human tumour cell line anticancer drug screen. Nat Rev Cancer 2006;6:813-23
  • Cragg GM. Paclitaxel (Taxol): a success story with valuable lessons for natural product drug discovery and development. Med Res Rev 1998;18:315-31
  • Gourmelon C, Frenel JS, Campone M. Eribulin mesylate for the treatment of late-stage breast cancer. Expert Opin Pharmacother 2011;12:2883-90
  • Bai RL, Paull KD, Herald CL, Halichondrin B and homohalichondrin B, marine natural products binding in the vinca domain of tubulin. Discovery of tubulin-based mechanism of action by analysis of differential cytotoxicity data. J Biol Chem 1991;266:15882-9
  • Hirata Y, Uemura D. Halichondrins-antitumor polyether macrolides from a marine sponge. Pure Appl Chem 1986;58:701-10
  • Yeung BK. Natural product drug discovery: the successful optimization of ISP-1 and halichondrin B. Curr Opin Chem Biol 2011;15:523-8
  • Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70
  • Kola I, Landis J. Can the pharmaceutical industry reduce attrition rates? Nat Rev Drug Discov 2004;3:711-15
  • Tamimi NAM, Ellis P. Drug development: from concept to marketing! Nephron Clin Pract. 2009;113:c125-c31
  • Persidis A. High-throughput screening. Advances in robotics and miniturization continue to accelerate drug lead identification. Nat Biotechnol 1998;16:488-9
  • Carnero A. High throughput screening in drug discovery. Clin Trans Oncol 2006;8:482-90
  • Pereira DA, Williams JA. Origin and evolution of high throughput screening. Br J Pharmacol 2007;152:53-61
  • Fox S, Farr-Jones S, Sopchak L, High-throughput screening: update on practices and success. J Biomol Screen 2006;11:864-9
  • Mayr LM, Bojanic D. Novel trends in high-throughput screening. Curr Opin Pharmacol 2009;9:580-8
  • An WF, Tolliday NJ. Introduction: cell-based assays for high-throughput screening. Methods Mol Biol 2009;486:1-12
  • Michelini E, Cevenini L, Mezzanotte L, Cell-based assays: fuelling drug discovery. Anal Bioanal Chem 2010;398:227-38
  • Pampaloni F, Reynaud EG, Stelzer EH. The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Bio 2007;8:839-45
  • Nelson C, Bissell M. Modeling dynamic reciprocity: engineering three-dimensional culture models of breast architecture, function, and neoplastic transformation. Semin Cancer Biol 2005;15:342-52
  • Abbott A. Cell culture: biology's new dimension. Nature 2003;424:870-2
  • Xu R, Boudreau A, Bissell MJ. Tissue architecture and function: dynamic reciprocity via extra- and intra-cellular matrices. Cancer Metastasisi Rev 2009;28:167-76
  • Bissell MJ, Radisky DC, Rizki A, The organizing principle: microenvironmental influences in the normal and malignant breast. Differentiation 2002;70:537-46
  • Spencer VA, Xu R, Bissell MJ. Gene expression in the third dimension: the ECM-nucleus connection. J Mammary Gland Biol Neoplasia 2010;15:65-71
  • Bissell MJ. Modelling molecular mechanisms of breast cancer and invasion: lessons from the normal gland. Biochem Soc Trans 2007;35:18-22
  • Bissell MJ, LaBarge MA. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell 2005;7:17-23
  • Bissell MJ, Radisky D. Putting tumours in context. Nat Rev Cancer 2001;1:46-54
  • Debnath J, Mills KR, Collins NL, The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 2002;111:29-40
  • Jacks T, Weinberg RA. Taking the study of cancer cell survival to a new dimension. Cell 2002;111:923-5
  • Ghosh S, Spagnoli GC, Martin I, Three-dimensional culture of melanoma cells profoundly affects gene expression profile: a high density oligonucleotide array study. J Cell Physiol 2005;204:522-31
  • Han J, Chang H, Giricz O, Molecular predictors of 3D morphogenesis by breast cancer cell lines in 3D culture. PLoS Comput Biol 2010;6:e1000684
  • Rowehl RA, Crawford H, Dufour A, Genomic analysis of prostate cancer stem cells isolated from a highly metastatic cell line. Cancer Genomics Proteomics 2008;5:301-10
  • Zahir N, Weaver VM. Death in the third dimension: apoptosis regulation and tissue architecture. Curr Opin Genet Dev 2004;14:71-80
  • Borgmann K, Zschenker O, Streichert T, Genome-wide gene expression analysis in cancer cells reveals 3D growth to affect ECM and processes associated with cell adhesion but not DNA repair. PLoS One 2012;7:e34279
  • Yamada K, Cukierman E. Modeling tissue morphogenesis and cancer in 3D. Cell 2007;130:601-10
  • Ideker T, Galitski T, Hood L. A new approach to decoding life: systems biology. Annu Rev Genomics Hum Genet 2001;2:343-72
  • Karsenti E. Towards an 'oceans systems biology'. Mol Syst Biol 2012;8:575
  • Kitano H. Systems biology: a brief overview. Science 2002;295:1662-4
  • Kreeger PK, Lauffenburger DA. Cancer systems biology: a network modeling perspective. Carcinogenesis 2010;31:2-8
  • Lemberger T. Systems biology in human health and disease. Mol Syst Biol 2007;3:136
  • Chignola R, Fabbro AD, Farina M, Milotti E. Computational challenges of tumor spheroid modeling. J Bioinform Comput Biol 2011;9:559-77
  • Kunz-Schughart LA, Freyer JP, Hofstaedter F, Ebner R. The use of 3-D cultures for high-throughput screening: the multicellular spheroid model. J Biomol Screen 2004;9:273-85
  • Sutherland RM, Inch WR, McCredie JA, Kruuv J. A multi-component radiation survival curve using an in vitro tumour model. Int J Radiat Biol Relat Stud Phys Chem Med 1970;18:491-5
  • Friedrich J, Ebner R, Kunz-Schughart LA. Experimental anti-tumor therapy in 3-D: spheroids–old hat or new challenge? Int J Radiat Biol 2007;83:849-71
  • Ackland ML, Ward J, Ackland CM, Extracellular matrix induces formation of organoids and changes in cell surface morphology in cultured human breast carcinoma cells PMC42-LA. In Vitro Cell Dev Biol Anim 2003;39:428-33
  • Weinberg RA. The biology of cancer. Garland Science; New York: 2007
  • Weaver VM, Petersen OW, Wang F, Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 1997;137:231-45
  • Wang F, Hansen RK, Radisky D, Phenotypic reversion or death of cancer cells by altering signaling pathways in three-dimensional contexts. J Natl Cancer Inst 2002;94:1494-503
  • Hirschhaeuser F, Menne H, Dittfeld C, Multicellular tumor spheroids: an underestimated tool is catching up again. J Biotechnol 2010;148:3-15
  • Fan F, Wood KV. Bioluminescent assays for high-throughput screening. Assay Drug Dev Technol 2007;5:127-36
  • Inglese J, Johnson RL, Simeonov A, High-throughput screening assays for the identification of chemical probes. Nat Chem Biol 2007;3:466-79
  • Haney SA, LaPan P, Pan J, Zhang J. High-content screening moves to the front of the line. Drug Discov Today 2006;11:889-94
  • Justice B, Badr N, Felder R. 3D cell culture opens new dimensions in cell-based assays. Drug Discov Today 2009;14:102-7
  • Ivascu A, Kubbies M. Rapid generation of single-tumor spheroids for high-throughput cell function and toxicity analysis. J Biomol Screen 2006;11:922-32
  • Kim JB. Three-dimensional tissue culture models in cancer biology. Semin Cancer Biol 2005;15:365-77
  • Santini MT, Rainaldi G. Three-dimensional spheroid model in tumor biology. Pathobiology 1999;67:148-57
  • Lee GY, Kenny PA, Lee EH, Bissell MJ. Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods 2007;4:359-65
  • Derda R, Laromaine A, Mammoto A, Paper-supported 3D cell culture for tissue-based bioassays. Proc Natl Acad Sci USA 2009;106:18457-62
  • Sodunke T, Turner K, Caldwell S, Micropatterns of Matrigel for three-dimensional epithelial cultures. Biomaterials 2007;28:4006-16
  • Kojima R, Yoshimoto K, Takahashi E, Spheroid array of fetal mouse liver cells constructed on a PEG-gel micropatterned surface: upregulation of hepatic functions by co-culture with nonparenchymal liver cells. Lab Chip 2009;9:1991-3
  • Frimat JP, Menne H, Michels A, Plasma stencilling methods for cell patterning. Anal Bioanal Chem 2009;395:601-9
  • Frimat JP, Sisnaiske J, Subbiah S, The network formation assay: a spatially standardized neurite outgrowth analytical display for neurotoxicity screening. Lab Chip 2010;10:701-9
  • Hardelauf H, Frimat JP, Stewart JD, Microarrays for the scalable production of metabolically relevant tumour spheroids: a tool for modulating chemosensitivity traits. Lab Chip 2011;11:419-28
  • Zhang X, Wang W, Yu W, Development of an in vitro multicellular tumor spheroid model using microencapsulation and its application in anticancer drug screening and testing. Biotechnol Prog 2005;21:1289-96
  • Agastin S, Giang UB, Geng Y, Continuously perfused microbubble array for 3D tumor spheroid model. Biomicrofluidics 2011;5:24110
  • Lin RZ, Chang HY. Recent advances in three-dimensional multicellular spheroid culture for biomedical research. Biotechnol J 2008;3:1172-84
  • Alvarez-Perez J, Ballesteros P, Cerdan S. Microscopic images of intraspheroidal pH by 1H magnetic resonance chemical shift imaging of pH sensitive indicators. MAGMA 2005;18:293-301
  • Hsiao AY, Tung YC, Kuo CH, Micro-ring structures stabilize microdroplets to enable long term spheroid culture in 384 hanging drop array plates. Biomed Microdevices 2012;14:313-23
  • Hsiao AY, Tung YC, Qu X, 384 hanging drop arrays give excellent Z-factors and allow versatile formation of co-culture spheroids. Biotechnol Bioeng 2012;109:1293-304
  • Tung YC, Hsiao AY, Allen SG, High-throughput 3D spheroid culture and drug testing using a 384 hanging drop array. Analyst 2011;136:473-8
  • Souza GR, Molina JR, Raphael RM, Three-dimensional tissue culture based on magnetic cell levitation. Nat Nanotechnol 2010;5:291-6
  • Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA. Spheroid-based drug screen: considerations and practical approach. Nat Protoc 2009;4:309-24
  • Li Q, Chen C, Kapadia A, 3D Models of epithelial-mesenchymal transition in breast cancer metastasis: high-throughput screening assay development, validation, and pilot screen. J Biomol Screen 2011;16:141-54
  • Vinci M, Gowan S, Boxall F, Advances in establishment and analysis of 3D tumour spheroid-based functional assays for target validation and drug evaluation. BMC Biol 2012;10:29
  • Wright MH, Calcagno AM, Salcido CD, Brca1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics. Breast Cancer Res 2008;10:R10
  • Takaishi S, Okumura T, Tu S, Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 2009;27:1006-20
  • Decker T, Lohmann-Matthes ML. A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J Immunol Methods 1988;115:61-9
  • De Witt Hamer PC, Jonker A, Leenstra S, Quantification of viability in organotypic multicellular spheroids of human malignant glioma using lactate dehydrogenase activity: a rapid and reliable automated assay. J Histochem Cytochem 2005;53:23-34
  • Friedrich J, Eder W, Castaneda J, A reliable tool to determine cell viability in complex 3-d culture: the acid phosphatase assay. J Biomol Screen 2007;12:925-37
  • McMillian MK, Li L, Parker JB, An improved resazurin-based cytotoxicity assay for hepatic cells. Cell Biol Toxicol 2002;18:157-73
  • Nakayama GR, Caton MC, Nova MP, Parandoosh Z. Assessment of the alamar blue assay for cellular growth and viability in vitro. J Immunol Methods 1997;204:205-8
  • Fesik SW. Promoting apoptosis as a strategy for cancer drug discovery. Nat Rev Cancer 2005;5:876-85
  • LaBarbera DV, Modzelewska K, Glazar AI, The marine alkaloid naamidine A promotes caspase-dependent apoptosis in tumor cells. Anticancer Drugs 2009;20:425-36
  • Reed JC. Apoptosis-based therapies. Nat Rev Drug Discov 2002;1:111-21
  • Kroemer G, Dallaporta B, Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol 1998;60:619-42
  • Shi Y. Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 2002;9:459-70
  • Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 1995;184:39-51
  • Yamaguchi S, Kobayashi H, Narita T, Novel photodynamic therapy using water-dispersed TiO2-polyethylene glycol compound: evaluation of antitumor effect on glioma cells and spheroids in vitro. Photochem Photobiol 2010;86:964-71
  • Markovitz-Bishitz Y, Tauber Y, Afrimzon E, A polymer microstructure array for the formation, culturing, and high throughput drug screening of breast cancer spheroids. Biomaterials 2010;31:8436-44
  • Kokkinos MI, Wafai R, Wong MK, Vimentin and epithelial-mesenchymal transition in human breast cancer–observations in vitro and in vivo. Cells Tissues Organs 2007;185:191-203
  • Rodriguez-Pinilla SM, Sarrio D, Honrado E, Vimentin and laminin expression is associated with basal-like phenotype in both sporadic and BRCA1-associated breast carcinomas. J Clin Pathol 2006;60:1006-12
  • Whitesell L, Lindquist SL. HSP90 and the chaperoning of cancer. Nat Rev Cancer 2005;5:761-72
  • Le Roux L, Volgin A, Maxwell D, Optimizing imaging of three-dimensional multicellular tumor spheroids with fluorescent reporter proteins using confocal microscopy. Mol Imaging 2008;7:214-21
  • Keith B, Johnson RS, Simon MC. HIF1alpha and HIF2alpha: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer 2012;12:9-22
  • Huang S, Vader D, Wang Z, Using magnetic resonance microscopy to study the growth dynamics of a glioma spheroid in collagen I: a case study. BMC Med Imaging 2008;8:3
  • Sharma M, Verma Y, Rao KD, Imaging growth dynamics of tumour spheroids using optical coherence tomography. Biotechnol Lett 2007;29:273-8
  • Naumov GN, Folkman J, Straume O. Tumor dormancy due to failure of angiogenesis: role of the microenvironment. Clin Exp Metastasis 2009;26:51-60

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