Optimization of aqueous biphasic tumor spheroid microtechnology for anti-cancer drug testing in 3D culture

Cellular and Molecular Bioengineering

Volumn 7, Issue 3, 2014, Pages 344-354

  Lemmo, Stephanie ^a   Atefi, Ehsan ^a   Luker, Gary D ^b,c   Tavana, Hossein ^a  

^a University of Akron   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

3D (three dimensional) culture; Anti cancer drug screening; Aqueous two phase system; High throughput; Tumor spheroid

Indexed keywords

CISPLATIN; DEXTRAN; MACROGOL; PACLITAXEL;

ARTICLE; BIOCHEMISTRY; CELL DENSITY; CELL SIZING (MEASUREMENT); CELL VIABILITY; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG DETERMINATION; DRUG SCREENING; HIGH THROUGHPUT SCREENING; IN VITRO STUDY; LIQUID PHASE MICROEXTRACTION; MICROTECHNOLOGY; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROCESS OPTIMIZATION; ROBOTICS; THREE DIMENSIONAL TUMOR CELL CULTURE; TUMOR CELL CULTURE; TUMOR SPHEROID;

EID: 84906939113     PISSN: 18655025     EISSN: 18655033     Source Type: Journal    
DOI: 10.1007/s12195-014-0349-4     Document Type: Article

References (48)

1. Albertsson, P.-A., and F. Tjerneld. Phase diagrams. Methods Enzymol. 228:3-13, 1994. (Pubitemid 24185032)
2. Andre, F., and C. C. Zielinski. Optimal strategies for the treatment of metastatic triple-negative breast cancer with currently approved agents. Ann. Oncol. 23(Suppl 6):46-51, 2012.
3. Atefi, E., S. Lemmo, D. Fyffe, G. D. Luker, and H. Tavana. High throughput, polymeric aqueous two-phase printing of tumor spheroids. Adv. Func. Mater. 2014, in press (doi:10.1002/adfm.201401302).
4. Blum, J. L., V. Dieras, P. M. Lo Russo, J. Horton, O. Rutman, et al. Multicenter, phase II study of capecitabine in taxane-pretreated metastatic breast carcinoma patients. Cancer 92:1759-1768, 2001. (Pubitemid 32952493)
5. Byrski, T., T. Huzarski, R. Dent, J. Gronwald, D. Zuziak, et al. Response to neoadjuvant therapy with cisplatin in BRCA1-positive breast cancer patients. Breast Cancer Res. Treat. 115:359-363, 2009.
6. Carlsson, J., and J. M. Yuhas. Liquid-overlay culture of cellular spheroids. Rec. Results Cancer Res. 95:1-23, 1984.
7. Chen, H., S. A. Quandt, J. G. Grzywacz, and T. A. Arcury. A distribution-based multiple imputation method for handling bivariate pesticide data with values below the limit of detection. Environ. Health Persp. 119:351-356, 2011.
8. Comerford, K. M., T. J. Wallace, J. Karhausen, N. A. Louis, M. C. Montalto, and S. P. Colgan. Hypoxiainducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res. 62:3387-3394, 2002. (Pubitemid 34651384)
9. Corey, J. M., C. C. Gertz, T. J. Sutton, Q. Chen, K. B. Mycek, et al. Patterning N-type and S-type neuroblastoma cells with Pluronic F108 and ECM proteins. J. Biomed. Mater. Res. A 93:673-686, 2010.
10. Desoize, B., and J. Jardillier. Multicellular resistance: a paradigm for clinical resistance? Crit. Rev. Oncol. Hematol. 36:193-207, 2000.
11. Desplats, P., B. Spencer, L. Crews, P. Pathel, D. Morvinski-Friedmann, et al. Alpha-synuclein induces alterations in adult neurogenesis in Parkinson disease models via p53-mediated repression of Notch1. J. Biol. Chem. 287:31691-31702, 2012.
12. Frankel, A., R. Buckman, and R. S. Kerbel. Abrogation of taxol-induced G2-M arrest and apoptosis in human ovarian cancer cells grown as multicellular tumor spheroids. Cancer Res. 57:2388-2393, 1997. (Pubitemid 27255896)
13. Friedrich, J., C. Seidel, R. Ebner, and L. A. Kunz-Schughart. Spheroid-based drug screen: considerations and practical approach. Nat. Protoc. 4:309-324, 2009.
14. Ghajar, C. M., and M. J. Bissell. Tumor engineering: the other face of tissue engineering. Tissue Eng. A 16:2153-2156, 2010.
15. Hirschhaeuser, F., H. Menne, C. Dittfeld, J. West, W. Mueller-Klieser, and L. A. Kunz-Schughart. Multicellular tumor spheroids: an underestimated tool is catching up again. J. Biotechnol. 148:3-15, 2010.
16. Holder, J. W., E. Elmore, and J. C. Barrett. Gap junction function and cancer. Cancer Res. 53:3475-3485, 1993. (Pubitemid 23229623)
17. Hsiao, A. Y., Y. C. Tung, C. H. Kuo, B. Mosadegh, R. Bedenis, et al. Micro-ring structures stabilize microdroplets to enable long term spheroid culture in 384 hanging drop array plates. Biomed. Microdev. 14:313-323, 2012.
18. Hutmacher, D. W., D. Loessner, S. Rizzi, D. L. Kaplan, D. J. Mooney, and J. A. CClements. Can tissue engineering concepts advance tumor biology research? Trends Biotechnol. 28:125-133, 2010.
19. Kelm, J. M., N. E. Timmins, C. J. Brown, M. Fussenegger, and L. K. Nielsen. Method for generation of homogeneous multicellular tumor spheroids applicable to a wide variety of cell types. Biotechnol. Bioeng. 83:173-180, 2003. (Pubitemid 36734131)
20. Kenny, P. A., G. Y. Lee, C. A. Myers, R. M. Neve, J. R. Semeiks, et al. The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression. Mol. Oncol. 1:84-96, 2007. (Pubitemid 46776616)
21. Kerbel, R. S., B. St Croix, V. A. Florenes, and J. Rak. Induction and reversal of cell adhesion-dependent multicellular drug resistance in solid breast tumors. Hum. Cell 9:257-264, 1996.
22. Kim, T., I. Doh, and Y. H. Cho. On-chip three-dimensional tumor spheroid formation and pump-less perfusion culture using gravity-driven cell aggregation and balanced droplet dispensing. Biomicrofluidics 6:34107, 2012.
23. Kobayashi, H., S. Man, C. H. Graham, S. J. Kapitain, B. A. Teicher, and R. S. Kerbel. Acquired multicellularmediated resistance to alkylating agents in cancer. PNAS 90:3294-3298, 1993. (Pubitemid 23111352)
24. Lemmo, S., S. Nasrollahi, and H. Tavana. Aqueous biphasic cancer cell migration assay enables robust, highthroughput screening of anti-cancer compounds. Biotechnol. J. 9:426-434, 2014.
25. Mehta, G., A. Y. Hsiao, M. Ingram, G. D. Luker, and S. Takayama. Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy. J. Control. Release 164:192-204, 2012.
26. Mueller-Klieser, W. Three-dimensional cell cultures: from molecular mechanisms to clinical applications. Am. J. Physiol. 273:C1109-C1123, 1997. (Pubitemid 127797683)
27. Napolitano, A. P., D. M. Dean, A. J. Man, J. Youssef, D. N. Ho, et al. Scaffold-free three-dimensional cell culture utilizing micromolded nonadhesive hydrogels. BioTechniques 43(494):96-500, 2007.
28. Olive, P. L., and R. E. Durand. Drug and radiation resistance in spheroids: cell contact and kinetics. Cancer Metast. Rev. 13:121-138, 1994. (Pubitemid 24220001)
29. Petrak, D., E. Atefi, L. Yin, W. Chilian, and H. Tavana. Automated, spatio-temporally controlled cell microprinting with polymeric aqueous biphasic system. Biotechnol. Bioeng. 11:404-412, 2014.
30. Rivera, E., and H. Gomez. Chemotherapy resistance in metastatic breast cancer: the evolving role of ixabepilone. Breast Cancer Res. 12(Suppl 2):S2, 2010.
31. Seano, G., G. Chiaverina, P. A. Gagliardi, L. di Blasio, R. Sessa, et al. Modeling human tumor angiogenesis in a three-dimensional culture system. Blood 121:e129-e137, 2013.
32. Silver, D. P., A. L. Richardson, A. C. Eklund, Z. C. Wang, Z. Szallasi, et al. Efficacy of neoadjuvant cisplatin in triplenegative breast cancer. J. Clin. Oncol. 28:1145-1153, 2010.
33. Souza, G. R., J. R. Molina, R. M. Raphael, M. G. Ozawa, D. J. Stark, et al. Three-dimensional tissue culture based on magnetic cell levitation. Nat. Nanotechnol. 5:291-296, 2010.
34. Sutherland, R. M., J. A. McCredie, and W. R. Inch. Growth of multicell spheroids in tissue culture as a model of nodular carcinomas. J. Nat. Cancer Inst. 46:113-120, 1971.
35. Tavana, H., A. Jovic, B. Mosadegh, Q. Y. Lee, X. Liu, et al. Nanolitre liquid patterning in aqueous environments for spatially defined reagent delivery to mammalian cells. Nat. Mater. 8:736-741, 2009.
36. Tavana, H., B. Mosadegh, and S. Takayama. Polymeric aqueous biphasic systems for non-contact cell printing on cells: engineering heterocellular embryonic stem cell niches. Adv. Mater. 22:2628-2631, 2010.
37. Tavana, H., B. Mosadegh, P. Zamankhan, J. B. Grotberg, and S. Takayama. Microprinted feeder cells guide embryonic stem cell fate. Biotechnol. Bioeng. 108:2509-2516, 2011.
38. Tavana, H., K. Kaylan, T. Bersano-Begey, K. E. Luker, G. D. Luker, and S. Takayama. Polymeric aqueous biphasic system rehydration facilitates high throughput cell exclusion patterning for cell migration studies. Adv. Funct. Mater. 21:2920-2926, 2011.
39. Tekin, H., M. Anaya, M. D. Brigham, C. Nauman, R. Langer, and A. Khademhosseini. Stimuli-responsive microwells for formation and retrieval of cell aggregates. Lab Chip 10:2411-2418, 2010.
40. Thode, H. C. Testing for normality. New York: CRC Press, 2002.
41. Torisawa, Y. S., B. Mosadegh, G. D. Luker, M. Morell, K. S. O'Shea, and S. Takayama. Microfluidic hydrodynamic cellular patterning for systematic formation of co-culture spheroids. Integr. Biol. 1:649-654, 2009.
42. Tung, Y. C., A. Y. Hsiao, S. G. Allen, Y. S. Torisawa, M. Ho, and S. Takayama. High-throughput 3D spheroid culture and drug testing using a 384 hanging drop array. Analyst 136:473-478, 2011.
43. Vinci, M., S. Gowan, F. Boxall, L. Patterson, M. Zimmermann, et al. Advances in establishment and analysis of three-dimensional tumor spheroid-based functional assays for target validation and drug evaluation. BMC Biol. 10:29, 2012.
44. Wartenberg, M., F. Donmez, F. C. Ling, H. Acker, J. Hescheler, and H. Sauer. Tumor-induced angiogenesis studied in confrontation cultures of multicellular tumor spheroids and embryoid bodies grown from pluripotent embryonic stem cells. FASEB J. 15:995-1005, 2001. (Pubitemid 32290787)
45. Wong, E. Y., and S. L. Diamond. Advancing microarray assembly with acoustic dispensing technology. Anal. Chem. 81:509-514, 2009.
46. Xie, J., D. W. Li, X. W. Chen, F. Wang, and P. Dong. Expression and significance of hypoxia-inducible factor-1alpha and MDR1/P-glycoprotein in laryngeal carcinoma tissue and hypoxic Hep-2 cells. Oncol. Lett. 6:232-238, 2013.
47. Xie, Z., L. Cao, and J. Zhang. miR-21 modulates paclitaxel sensitivity and hypoxia-inducible factor-1alpha expression in human ovarian cancer cells. Oncol. Lett. 6:795-800, 2013.
48. Yamada, K. M., and E. Cukierman. Modeling tissue morphogenesis and cancer in 3D. Cell 130:601-610, 2007. (Pubitemid 47268064)