Development of a high-throughput three-dimensional invasion assay for anti-cancer drug discovery

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Evensen, Nikki A ^a   Li, Jian ^a,d   Yang, Jie ^a   Yu, Xiaojun ^b   Sampson, Nicole S ^a   Zucker, Stanley ^c   Cao, Jian ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b STEVENS INSTITUTE OF TECHNOLOGY   (United States)

^c Veterans Affair Medical Center   (United States)

^d JIMEI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BETA1 INTEGRIN; COLLAGEN TYPE 1; DIMETHYL SULFOXIDE; MATRIX METALLOPROTEINASE 14; NSC 607097; PACLITAXEL; PROPIDIUM IODIDE; QUINOCARCIN; STAUROSPORINE; TISSUE INHIBITOR OF METALLOPROTEINASE 2; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CELL INVASION; CELL SHAPE; CELL SIZE; CONTROLLED STUDY; DRUG DEVELOPMENT; HIGH THROUGHPUT SCREENING; HIGH THROUGHPUT THREE DIMENSIONAL SCREENING ASSAY; HUMAN; HUMAN CELL; MALE; TUMOR INVASION;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DRUG DISCOVERY; DRUG SCREENING ASSAYS, ANTITUMOR; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; NEOPLASM INVASIVENESS; REPRODUCIBILITY OF RESULTS; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED;

EID: 84892406857     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082811     Document Type: Article

References (43)

1. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674. doi:10.1016/j.cell.2011.02.013. PubMed: 21376230.
2. Normanno N, Morabito A, De Luca A, Piccirillo MC, Gallo M et al. (2009) Target-based therapies in breast cancer: current status and future perspective. Endocr Relat Cancer 16: 675-702. doi:10.1677/ERC-08-0208. PubMed: 19525314.
3. Wood LD, Parsons DW, Jones S, Lin J, Sjöblom T et al. (2007) The genomic landscapes of human breast and colorectal cancers. Science 318: 1108-1113. doi:10.1126/science.1145720. PubMed: 17932254.
4. Perret GY, Crépin M (2008) New pharmacological strategies against metastatic spread. Fundam Clin Pharmacol 22: 465-492. doi:10.1111/j.1472-8206. 2008.00614.x. PubMed: 18844722.
5. Sahai E (2007) Illuminating the metastatic process. Nat Rev Cancer 7: 737-749. doi:10.1038/nrc2229. PubMed: 17891189.
6. Kim MY, Oskarsson T, Acharyya S, Nguyen DX, Zhang XH et al. (2009) Tumor self-seeding by circulating cancer cells. Cell 139: 1315-1326. doi:10.1016/j.cell.2009.11.025. PubMed: 20064377.
7. Elsdale T, Bard J (1972) Collagen substrata for studies on cell behavior. J Cell Biol 54: 626-637. doi:10.1083/jcb.54.3.626. PubMed: 4339818.
8. 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.
9. Lee MY, Kumar RA, Sukumaran SM, Hogg MG, Clark DS et al. (2008) Three-dimensional cellular microarray for high-throughput toxicology assays. Proc Natl Acad Sci U S A 105: 59-63. PubMed: 18160535.
10. Ivascu A, Kubbies M (2006) Rapid generation of single-tumor spheroids for high-throughput cell function and toxicity analysis. J Biomol Screen 11: 922-932. PubMed: 16973921.
11. Cheng K, Lai Y, Kisaalita WS (2008) Three-dimensional polymer scaffolds for high throughput cell-based assay systems. Biomaterials 29: 2802-2812. doi:10.1016/j.biomaterials.2008.03.015. PubMed: 18405966.
12. Tung YC, Hsiao AY, Allen SG, Torisawa YS, Ho M et al. (2011) High-throughput 3D spheroid culture and drug testing using a 384 hanging drop array. Analyst 136: 473-478. doi:10.1039/c0an00609b. PubMed: 20967331.
13. Zhang X, Yang ST (2011) High-throughput 3-D cell-based proliferation and cytotoxicity assays for drug screening and bioprocess development. J Biotechnol 151: 186-193. doi:10.1016/j.jbiotec.2010.11.012. PubMed: 21115074.
14. Xu F, Celli J, Rizvi I, Moon S, Hasan T, et al. (2011) A three-dimensional in vitro ovarian cancer coculture model using a high-throughput cell patterning platform. Biotechnol J 6: 204-212
15. Fernandes TG, Kwon SJ, Bale SS, Lee MY, Diogo MM et al. (2010) Three-dimensional cell culture microarray for high-throughput studies of stem cell fate. Biotechnol Bioeng 106: 106-118. PubMed: 20069558.
16. Adanja I, Debeir O, Mégalizzi V, Kiss R, Warzée N et al. (2010) Automated tracking of unmarked cells migrating in three-dimensional matrices applied to anti-cancer drug screening. Exp Cell Res 316: 181-193. doi:10.1016/j.yexcr.2009.10.004. PubMed: 19835872.
17. Echeverria V, Meyvantsson I, Skoien A, Worzella T, Lamers C et al. (2010) An automated high-content assay for tumor cell migration through 3-dimensional matrices. J Biomol Screen 15: 1144-1151. doi:10.1177/1087057110378890. PubMed: 20930216.
18. 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. doi:10.1177/1087057110392995. PubMed: 21297102.
19. Grinnell F, Rocha LB, Iucu C, Rhee S, Jiang H (2006) Nested collagen matrices: a new model to study migration of human fibroblast populations in three dimensions. Exp Cell Res 312: 86-94. PubMed: 16256985.
20. Kunz-Schughart LA, Freyer JP, Hofstaedter F, Ebner R (2004) The use of 3-D cultures for high-throughput screening: the multicellular spheroid model. J Biomol Screen 9: 273-285. PubMed: 15191644.
21. Cao J, Chiarelli C, Richman O, Zarrabi K, Kozarekar P et al. (2008) Membrane type 1 matrix metalloproteinase induces epithelial-to-mesenchymal transition in prostate cancer. J Biol Chem 283: 6232-6240. doi:10.1074/jbc. M705759200. PubMed: 18174174.
22. Li J, Zucker S, Pulkoski-Gross A, Kuscu C, Karaayvaz M et al. (2012) Conversion of Stationary to Invasive Tumor Initiating Cells (TICs): Role of Hypoxia in Membrane Type 1-Matrix Metalloproteinase (MT1-MMP) Trafficking. PLOS ONE 7: e38403. PubMed: 22679501.
23. Cao J, Chiarelli C, Kozarekar P, Adler HL (2005) Membrane type 1-matrix metalloproteinase promotes human prostate cancer invasion and metastasis. Thromb Haemost 93: 770-778. PubMed: 15841326.
24. Ghajar CM, Suresh V, Peyton SR, Raub CB, Meyskens FL Jr et al. (2007) A novel three-dimensional model to quantify metastatic melanoma invasion. Mol Cancer Ther 6: 552-561. doi: 10.1158/1535-7163.MCT-06-0593. PubMed: 17267658.
25. Cao J, Kozarekar P, Pavlaki M, Chiarelli C, Bahou WF et al. (2004) Distinct roles for the catalytic and hemopexin domains of membrane type 1-matrix metalloproteinase in substrate degradation and cell migration. J Biol Chem 279: 14129-14139. PubMed: 14729674.
26. Wang P, Nie J, Pei D (2004) The hemopexin domain of membrane-type matrix metalloproteinase-1 (MT1-MMP) Is not required for its activation of proMMP2 on cell surface but is essential for MT1-MMP-mediated invasion in three-dimensional type I collagen. J Biol Chem 279: 51148-51155. doi:10.1074/jbc.M409074200. PubMed: 15381707.
27. Zhu YK, Umino T, Liu XD, Wang HJ, Romberger DJ et al. (2001) Contraction of fibroblast-containing collagen gels: Initial collagen concentration regulates the degree of contraction and cell survival. In Vitro Cell Dev Biol Anim 37: 10-16. doi:10.1290/1071-2690(2001)037. PubMed: 11249200.
28. Nien YD, Han YP, Tawil B, Chan LS, Tuan TL et al. (2003) Fibrinogen inhibits fibroblast-mediated contraction of collagen. Wound Repair Regen 11: 380-385. doi:10.1046/j.1524-475X.2003.11511.x. PubMed: 12950643.
29. Etienne Schacht BB, An Van Den Bulcke, Nadine De Rooze (1997) Hydrogels prepared by crosslinking of gelatin with dextran dialdehyde. Reactive and Functional Polymers 33: 109-116
30. Zhang JH, Chung TD, Oldenburg KR (1999) A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. Journal of Biomol-Screen 4: 67-73.
31. Xue LY, Chiu SM, Oleinick NL (2003) Staurosporine-induced death of MCF-7 human breast cancer cells: a distinction between caspase-3-dependent steps of apoptosis and the critical lethal lesions. Exp Cell Res 283: 135-145. doi:10.1016/S0014-4827(02)00032-0. PubMed: 12581734.
32. Zhang XD, Gillespie SK, Hersey P (2004) Staurosporine induces apoptosis of melanoma by both caspase-dependent and -independent apoptotic pathways. Mol Cancer Ther 3: 187-197. PubMed: 14985459.
33. Yvon AMC, Wadsworth P, Jordan MA (1999) Taxol suppresses dynamics of individual microtubules in living human tumor cells. Mol Biol Cell 10: 947-959. doi:10.1091/mbc.10.4.947. PubMed: 10198049.
34. Terzis AJ, Thorsen F, Heese O, Visted T, Bjerkvig R et al. (1997) Proliferation, migration and invasion of human glioma cells exposed to paclitaxel (Taxol). In Vitro - British Journal of Cancer 75: 1744-1752. doi:10.1038/bjc.1997.298.
35. Kahsai AW, Zhu ST, Wardrop DJ, Lane WS, Fenteany G (2006) Quinocarmycin analog DX-52-1 inhibits cell migration and targets radixin, disrupting interactions of radixin with actin and CD44. Chem Biol 13: 973-983. PubMed: 16984887.
36. Drews J (2000) Drug discovery: a historical perspective. Science 287: 1960-1964. doi:10.1126/science.287.5460.1960. PubMed: 10720314.
37. Butcher EC (2005) Can cell systems biology rescue drug discovery? Nat-Rev-Drug Discov 4: 461-467. PubMed: 1724950115915152.
38. Hart CP (2005) Finding the target after screening the phenotype. Drug Discov Today 10: 513-519. PubMed: 15809197.
39. Vinodh Kanth S, Ramaraj A, Raghava Rao J, Unni Nair B (2009) Stabilization of type I collagen using dialdehyde cellulose. Process Biochemistry 44: 869-874. doi:10.1016/j.procbio.2009.04.008.
40. Draye JP, Delaey B, Van de Voorde A, Van Den Bulcke A, Bogdanov B et al. (1998) In vitro release characteristics of bioactive molecules from dextran dialdehyde cross-linked gelatin hydrogel films. Biomaterials 19: 99-107. doi:10.1016/S0142-9612(97)00164-6. PubMed: 9678856.
41. Cortesi R, Esposito E, Osti M, Squarzoni G, Menegatti E et al. (1999) Dextran cross-linked gelatin microspheres as a drug delivery system. Eur J Pharm Biopharm 47: 153-160. doi:10.1016/S0939-6411(98)00076-9. PubMed: 10234540.
42. Lauwaet T, Oliveira MJ, Mareel M, Leroy A (2000) Molecular mechanisms of invasion by cancer cells, leukocytes and microorganisms. Microbes Infect 2: 923-931. doi:10.1016/S1286-4579(00)00394-4. PubMed: 10962276.
43. Tickle C, Crawley A (1979) Infiltration and survival: the behaviour of normal, invasive cells implanted to the developing chick wing. J Cell Sci 40: 257-270. PubMed: 317080.