Incorporation of multicellular spheroids into 3-D polymeric scaffolds provides an improved tumor model for screening anticancer drugs

Cancer Science

Volumn 101, Issue 12, 2010, Pages 2637-2643

  Ho, Won Jin ^a   Pham, Edward A ^a   Kim, Jun W ^a   Ng, Christopher W ^a   Kim, Jae H ^a   Kamei, Daniel T ^a   Wu, Benjamin M ^a  

^a University of California   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; DOXORUBICIN; IRINOTECAN; LACTIC ACID; MOLECULAR SCAFFOLD; POLYMER;

ARTICLE; CANCER CELL CULTURE; CANCER RESISTANCE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG PENETRATION; DRUG SCREENING; IN VITRO STUDY; LACTIC ACIDOSIS; MONOLAYER CULTURE; MULTICELLULAR SPHEROID; POROSITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR MODEL;

DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; SPHEROIDS, CELLULAR; TISSUE SCAFFOLDS; TUMOR CELLS, CULTURED;

EID: 78449290991     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2010.01723.x     Document Type: Article

References (44)

1. Griffith L, Swartz M. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol 2006; 7: 211-24.
2. Newman MJ, Rodarte JC, Benbatoul KD et al. Discovery and characterization of OC144-093, a novel inhibitor of P-glycoprotein-mediated multidrug resistance. Cancer Res 2000; 60: 2964-72.
3. Torrance CJ, Agrawal V, Vogelstein B, Kinzler KW. Use of isogenic human cancer cells for high-throughput screening and drug discovery. Nat Biotechnol 2001; 19: 940-5.
4. Holtfreter J. A study of the mechanics of gastrulation. J Exp Zool 1944; 95: 171-212.
5. Moscona A. Cell suspensions from organ rudiments of chick embryos. Exp Cell Res 1952; 3: 535-9.
6. Li C. Survival advantages of multicellular spheroids vs. monolayers of HepG2 cells in vitro. Oncol Rep 2008; 20: 1465-71.
7. Lin R, Chang H. Recent advances in three-dimensional multicellular spheroid culture for biomedical research. Biotechnol J 2008; 3: 1172-84.
8. Mueller-Klieser W. Method for the determination of oxygen consumption rates and diffusion coefficients in multicellular spheroids. Biophys J 1984; 46: 343-8.
9. De Witt Hamer P, Van Tilborg A, Eijk P et al. The genomic profile of human malignant glioma is altered early in primary cell culture and preserved in spheroids. Oncogene 2008; 27: 2091-6.
10. Nederman T, Carlsson J, Malmqvist M. Penetration of substances into tumour tissue-- a methodological study on cellular spheroids. In Vitro 1981; 17: 290-8.
11. Desoize B. Anticancer drug resistance and inhibition of apoptosis. Anticancer Res 1994; 14: 2291-4.
12. Glimelius B, Norling B, Nederman T, Carlsson J. Extracellular matrices in multicellular spheroids of human glioma origin: increased incorporation of proteoglycans and fibronectin as compared to monolayer cultures. APMIS 1988; 96: 433-44.
13. Horning J, Sahoo S, Vijayaraghavalu S et al. 3-D tumor model for in vitro evaluation of anticancer drugs. Mol Pharm 2008; 5: 849-62.
14. Lu H, El-Amin S, Scott K, Laurencin C. Three-dimensional, bioactive, biodegradable, polymer-bioactive glass composite scaffolds with improved mechanical properties support collagen synthesis and mineralization of human osteoblast-like cells in vitro. J Biomed Mater Res A 2003; 64: 465-74.
15. Lee M, Chen T, Iruela-Arispe M, Wu B, Dunn J. Modulation of protein delivery from modular polymer scaffolds. Biomaterials 2007; 28: 1862-70.
16. Wang X, Wenk E, Zhang X, Meinel L, Vunjak-Novakovic G, Kaplan D. Growth factor gradients via microsphere delivery in biopolymer scaffolds for osteochondral tissue engineering. J Control Release 2009; 134: 81-90.
17. Battista S, Guarnieri D, Borselli C et al. The effect of matrix composition of 3D constructs on embryonic stem cell differentiation. Biomaterials 2005; 26: 6194-207.
18. Zhu H, Ji J, Barbosa M, Shen J. Protein electrostatic self-assembly on poly(DL-lactide) scaffold to promote osteoblast growth. J Biomed Mater Res B Appl Biomater 2004; 71: 159-65.
19. Harley B, Kim H, Zaman M, Yannas I, Lauffenburger D, Gibson L. Microarchitecture of three-dimensional scaffolds influences cell migration behavior via junction interactions. Biophys J 2008; 95: 4013-24.
20. Fischbach C, Chen R, Matsumoto T et al. Engineering tumors with 3D scaffolds. Nat Methods 2007; 4: 855-60.
21. 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.
22. Kolchinsky A, Roninson I. Drug resistance conferred by MDR1 expression in spheroids formed by glioblastoma cell lines. Anticancer Res 1997; 17: 3321-7.
23. Durand R. Slow penetration of anthracyclins into spheroids and tumors: a therapeutic disadvantage? Cancer Chemother Pharmacol 1990; 26: 198-204.
24. Xu R, Pelicano H, Zhou Y et al. Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia. Cancer Res 2005; 65: 613-21.
25. Fukumura D, Xu L, Chen Y, Gohongi T, Seed B, Jain RK. Hypoxia and acidosis independently up-regulate vascular endothelial growth factor transcription in brain tumors in vivo. Cancer Res 2001; 61: 6020-4.
26. Schlueter C, Weber H, Meyer B et al. Angiogenetic signaling through hypoxia: HMGB1: an angiogenetic switch molecule. Am J Pathol 2005; 166: 1259-63.
27. Harmey J, Bouchier-Hayes D. Vascular endothelial growth factor (VEGF), a survival factor for tumour cells: implications for anti-angiogenic therapy. Bioessays 2002; 24: 280-3.
28. Song S, Wientjes M, Gan Y, Au J. Fibroblast growth factors: an epigenetic mechanism of broad spectrum resistance to anticancer drugs. Proc Natl Acad Sci U S A 2000; 97: 8658-63.
29. Wiles M, Bell C, Landfair D, Lynam E, Bendele R. Anthracycline efficacy in vitro: cytotoxicity of liposomal/nonliposomal daunorubicin and doxorubicin for multiple tumor cell types. Drug Deliv 1997; 4: 255-62.
30. Matsumoto Y, Fujiwara T, Honjo Y, Sasaoka N, Tsuchida T, Nagao S. Quantitative analysis of DNA topoisomerase I activity in human and rat glioma: characterization and mechanism of resistance to antitopoisomerase chemical, camptothecin-11. J Surg Oncol 1993; 53: 97-103.
31. Fabel K, Dietrich J, Hau P et al. Long-term stabilization in patients with malignant glioma after treatment with liposomal doxorubicin. Cancer 2001; 92: 1936-42.
32. Nobel C, Krauze M, Drummond D et al. Novel nanoliposomal CPT-11 infused by convection-enhanced delivery in intracranial tumors: pharmacology and efficacy. Cancer Res 2006; 66: 2801-6.
33. Wishart D, Knox C, Guo A et al. DrugBank: a knowledgebase for drugs, drug actions and drug targets. Nucleic Acids Res 2008; 36: D901-6.
34. Ivascu A, Kubbies M. Diversity of cell-mediated adhesions in breast cancer spheroids. Int J Oncol 2007; 31: 1403-13.
35. Bhuyan B, Folz S, DeZwaan J et al. Cytotoxicity of tetraplatin and cisplatin for human and rodent cell lines cultured as monolayers and multicellular spheroids. Cancer Commun 1991; 3: 53-9.
36. Erlichman C, Vidgen D, Wu A. Cytotoxicity of cisplatin and cisdiammine-1, 1-cyclobutane dicarboxylate in MGH-U1 cells grown in monolayers, spheroids, and xenografts. J Natl Cancer Inst 1985; 75: 499-505.
37. Kim T, Park T. Biomimicking extracellular matrix: cell adhesive RGD peptide modified electrospun poly(D, L-lactic-co-glycolic acid) nanofiber mesh. Tissue Eng 2006; 12: 221-33.
38. Desoize B, Gimonet D, Jardiller J. Cell culture as spheroids: an approach to multicellular resistance. Anticancer Res 1998; 18: 4147-58.
39. Erlanson M, Daniel-Szolgay E, Carlsson J. Relations between the penetration, binding and average concentration of cytostatic drugs in human tumour spheroids. Cancer Chemother Pharmacol 1992; 29: 343-53.
40. Durand R. A possible indirect radiosensitizer of hypoxic tumor cells. Radiology 1976; 119: 217-22.
41. Nakayama K, Kanzaki A, Hata K et al. Hypoxia-inducible factor 1 alpha (HIF-1 alpha) gene expression in human ovarian carcinoma. Cancer Lett 2002; 176: 215-23.
42. Calvani M, Rapisarda A, Uranchimeg B, Shoemaker R, Melillo G. Hypoxic induction of an HIF-1alpha-dependent bFGF autocrine loop drives angiogenesis in human endothelial cells. Blood 2006; 107: 2705-12.
43. Halin C, Rondini S, Nilsson F et al. Enhancement of the antitumor activity of interleukin-12 by targeted delivery to neovasculature. Nat Biotechnol 2002; 20: 264-9.
44. Dunn S, Hardman R, Kari F, Barrett J. Insulin-like growth factor 1 (IGF-1) alters drug sensitivity of HBL100 human breast cancer cells by inhibition of apoptosis induced by diverse anticancer drugs. Cancer Res 1997; 57: 2687-93.