Two-dimensional vs. Three-dimensional in vitro tumor migration and invasion assays

Methods in Molecular Biology

Volumn 986, Issue , 2013, Pages 227-252

  Zimmermann, Miriam ^a   Box, Carol ^a   Eccles, Suzanne A ^a  

^a NONE

Author keywords

3 dimensional cultures; Chemotaxis; Haptotaxis; Invasion; Matrix protein; Migration; Motility; Spheroid

Indexed keywords

ANTINEOPLASTIC AGENT;

ARTICLE; CELL MIGRATION; CELL MOTION; DRUG DEVELOPMENT; EXTRACELLULAR MATRIX; HUMAN; METASTASIS; METHODOLOGY; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL CULTURE; TUMOR INVASION; TUMOR MICROENVIRONMENT;

ANTINEOPLASTIC AGENTS; CELL MIGRATION ASSAYS; CELL MOVEMENT; DRUG DISCOVERY; EXTRACELLULAR MATRIX; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

MLCS; MLOWN;

EID: 84881263091     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-62703-311-4_15     Document Type: Article

References (134)

1. Francia G, Cruz-Munoz W, Man S et al (2011) Mouse models of advanced spontaneous metastasis for experimental therapeutics. Nat Rev Cancer 11:135-141
2. Eccles SA, Welch DR (2007) Metastasis: recent discoveries and novel treatment strategies. Lancet 369:1742-1757
3. Coleman R (2011) The use of bisphosphonates in cancer treatment. Ann N Y Acad Sci 1218:3-14
4. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646-674
5. Palmer TD, Ashby WJ, Lewis JD et al (2011) Targeting tumor cell motility to prevent metastasis. Adv Drug Deliv Rev 63:568-581
6. Eccles SA (2004) Parallels in invasion and angiogenesis provide pivotal points for therapeutic intervention. Int J Dev Biol 48: 583-598
7. Eccles SA, Court W, Patterson L et al (2009) In vitro assays for endothelial cell functions related to angiogenesis: proliferation, motility, tubular differentiation, and proteolysis. Methods Mol Biol 467:159-181
8. Brader S, Eccles SA (2004) Phosphoinositide 3-kinase signalling pathways in tumor progression, invasion and angiogenesis. Tumori 90:2-8
9. Eccles SA, Massey A, Raynaud FI et al (2008) NVP-AUY922: a novel heat shock protein 90 inhibitor active against xenograft tumor growth, angiogenesis, and metastasis. Cancer Res 68:2850-2860
10. Friedl P, Gilmour D (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10:445-457
11. Sahai E, Marshall CJ (2003) Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol 5:711-719
12. Strongin AY (2010) Proteolytic and nonproteolytic roles of membrane type-1 matrix metalloproteinase in malignancy. Biochim Biophys Acta 1803:133-141
13. Ebos JM, Kerbel RS (2011) Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat Rev Clin Oncol 8:210-221
14. Collins CS, Hong J, Sapinoso L et al (2006) A small interfering RNA screen for modulators of tumor cell motility identifies MAP4K4 as a promigratory kinase. Proc Natl Acad Sci USA 103:3775-3780
15. Roussos ET, Condeelis JS, Patsialou A (2011) Chemotaxis in cancer. Nat Rev Cancer 11: 573-587
16. Sawyer C, Sturge J, Bennett DC et al (2003) Regulation of breast cancer cell chemotaxis by the phosphoinositide 3-kinase p110delta. Cancer Res 63:1667-1675
17. Breckenridge MT, Egelhoff TT, Baskaran H (2010) A micro fluidic imaging chamber for the direct observation of chemotactic transmigration. Biomed Microdevices 12:543-553
18. Albini A, Noonan DM (2010) The 'chemoinvasion' assay, 25 years and still going strong: the use of reconstituted basement membranes to study cell invasion and angiogenesis. Curr Opin Cell Biol 22:677-689
19. Eccles SA, Box C, Court W (2005) Cell migration/invasion assays and their application in cancer drug discovery. Biotechnol Annu Rev 11:391-421
20. Maliakal JC (2002) Quantitative high throughput endothelial cell migration and invasion assay system. Methods Enzymol 352: 175-182
21. Marshall J (2011) Transwell((R)) invasion assays. Methods Mol Biol 769:97-110
22. van Roosmalen W, Le Devedec SE, Zovko S et al (2011) Functional screening with a live cell imaging-based random cell migration assay. Methods Mol Biol 769:435-448
23. Ng MR, Brugge JS (2009) A stiff blow from the stroma: collagen crosslinking drives tumor progression. Cancer Cell 16:455-457
24. Kusama T, Mukai M, Tatsuta M et al (2006) Inhibition of transendothelial migration and invasion of human breast cancer cells by preventing geranylgeranylation of Rho. Int J Oncol 29:217-223
25. Burleson KM, Hansen LK, Skubitz AP (2004) Ovarian carcinoma spheroids disaggregate on type I collagen and invade live human mesothelial cell monolayers. Clin Exp Metastasis 21:685-697
26. Jung S, Kim HW, Lee JH et al (2002) Brain tumor invasion model system using organotypic brain-slice culture as an alternative to in vivo model. J Cancer Res Clin Oncol 128:469-476
27. Quintavalle M, Elia L, Price JH et al (2011) A cell-based high-content screening assay reveals activators and inhibitors of cancer cell invasion. Sci Signal 4:ra49
28. Nystrom ML, Thomas GJ, Stone M et al (2005) Development of a quantitative method to analyse tumour cell invasion in organotypic culture. J Pathol 205:468-475
29. Brekhman V, Neufeld G (2009) A novel asymmetric 3D in-vitro assay for the study of tumor cell invasion. BMC Cancer 9:415
30. Harma V, Virtanen J, Makela R et al (2010) A comprehensive panel of three-dimensional models for studies of prostate cancer growth, invasion and drug responses. PLoS One 5:e10431
31. Duong HS, Le AD, Zhang Q et al (2005) A novel 3-dimensional culture system as an in vitro model for studying oral cancer cell invasion. Int J Exp Pathol 86:365-374
32. David L, Dulong V, Le Cerf D et al (2004) Reticulated hyaluronan hydrogels: a model for examining cancer cell invasion in 3D. Matrix Biol 23:183-193
33. Truong HH, de Sonneville J, Ghotra VP et al (2012) Automated microinjection of cellpolymer suspensions in 3D ECM scaffolds for high-throughput quantitative cancer invasion screens. Biomaterials 33:181-188
34. Echeverria V, Meyvantsson I, Skoien A et al (2010) An automated high-content assay for tumor cell migration through 3-dimensional matrices. J Biomol Screen 15:1144-1151
35. Mareel MM, Van Roy FM, Messiaen LM et al (1987) Qualitative and quantitative analysis of tumour invasion in vivo and in vitro. J Cell Sci Suppl 8:141-163
36. Bracke ME, Boterberg T, Mareel MM (2001) Chick heart invasion assay. Methods Mol Med 58:91-102
37. Woodward JK, Nichols CE, Rennie IG et al (2002) An in vitro assay to assess uveal melanoma invasion across endothelial and basement membrane barriers. Invest Ophthalmol Vis Sci 43:1708-1714
38. Kataoka T, Umeda M, Shigeta T et al (2010) A new in vitro model of cancer invasion using AlloDerm, a human cadaveric dermal equivalent: a preliminary report. Kobe J Med Sci 55:E106-E115
39. Andjelkovic AV, Zochowski MR, Morgan F et al (2001) Qualitative and quantitative analysis of monocyte transendothelial migration by confocal microscopy and three-dimensional image reconstruction. In Vitro Cell Dev Biol Anim 37:111-120
40. Pilkington GJ, Bjerkvig R, De Ridder L et al (1997) In vitro and in vivo models for the study of brain tumour invasion. Anticancer Res 17:4107-4109
41. Yates C, Shepard CR, Papworth G et al (2007) Novel three-dimensional organotypic liver bioreactor to directly visualize early events in metastatic progression. Adv Cancer Res 97: 225-246
42. Hsiao AY, Torisawa YS, Tung YC et al (2009) Micro fluidic system for formation of PC-3 prostate cancer co-culture spheroids. Biomaterials 30:3020-3027
43. Unger RE, Halstenberg S, Sartoris A et al (2011) Human endothelial and osteoblast cocultures on 3D biomaterials. Methods Mol Biol 695:229-241
44. Sieh S, Lubik AA, Clements JA et al (2010) Interactions between human osteoblasts and prostate cancer cells in a novel 3D in vitro model. Organogenesis 6:181-188
45. Mastro AM, Vogler EA (2009) A threedimensional osteogenic tissue model for the study of metastatic tumor cell interactions with bone. Cancer Res 69:4097-4100
46. Niggemann B, Drell TL IV, Joseph J et al (2004) Tumor cell locomotion: differential dynamics of spontaneous and induced migration in a 3D collagen matrix. Exp Cell Res 298:178-187
47. Joyce JA, Pollard JW (2009) Microenvironmental regulation of metastasis. Nat Rev Cancer 9:239-252
48. Nyga A, Cheema U, Loizidou M (2011) 3D tumour models: novel in vitro approaches to cancer studies. J Cell Commun Signal 5: 239-248
49. Shirinifard A, Gens JS, Zaitlen BL et al (2009) 3D multi-cell simulation of tumor growth and angiogenesis. PLoS One 4:e7190
50. Smalley KS, Lioni M, Herlyn M (2006) Life isn't flat: taking cancer biology to the next dimension. In Vitro Cell Dev Biol Anim 42:242-247
51. Green SK, Francia G, Isidoro C et al (2004) Antiadhesive antibodies targeting E-cadherin sensitize multicellular tumor spheroids to chemotherapy in vitro. Mol Cancer Ther 3:149-159
52. Birgersdotter A, Sandberg R, Ernberg I (2005) Gene expression perturbation in vitro-a growing case for three-dimensional (3D) culture systems. Semin Cancer Biol 15:405-412
53. Cukierman E, Pankov R, Stevens DR et al (2001) Taking cell-matrix adhesions to the third dimension. Science 294:1708-1712
54. Kunz-Schughart LA, Freyer JP, Hofstaedter F et al (2004) The use of 3-D cultures for highthroughput screening: the multicellular spheroid model. J Biomol Screen 9:273-285
55. Takagi A, Watanabe M, Ishii Y et al (2007) Three-dimensional cellular spheroid formation provides human prostate tumor cells with tissue-like features. Anticancer Res 27: 45-53
56. Hirschhaeuser F, Menne H, Dittfeld C et al (2010) Multicellular tumor spheroids: an underestimated tool is catching up again. J Biotechnol 148:3-15
57. Scott RW, Hooper S, Crighton D et al (2010) LIM kinases are required for invasive path generation by tumor and tumor-associated stromal cells. J Cell Biol 191:169-185
58. Hardelauf H, Frimat JP, Stewart JD et al (2011) Microarrays for the scalable production of metabolically relevant tumour spheroids: a tool for modulating chemosensitivity traits. Lab Chip 11:419-428
59. Friedrich J, Seidel C, Ebner R et al (2009) Spheroid-based drug screen: considerations and practical approach. Nat Protoc 4:309-324
60. Tung YC, Hsiao AY, Allen SG et al (2011) High-throughput 3D spheroid culture and drug testing using a 384 hanging drop array. Analyst 136:473-478
61. Vinci M, Gowan S, Boxall F et al (2012) Advances in establishment and analysis of 3D tumour spheroid-based functional assays for target validation and drug evaluation. BMC Biol 10:29. doi: 10.1186/1741-7007-10-29
62. Lai Y, Asthana A, Kisaalita WS (2011) Biomarkers for simplifying HTS 3D cell culture platforms for drug discovery: the case for cytokines. Drug Discov Today 16:293-297
63. Ghosh S, Spagnoli GC, Martin I 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
64. Fischbach C, Kong HJ, Hsiong SX et al (2009) Cancer cell angiogenic capability is regulated by 3D culture and integrin engagement. Proc Natl Acad Sci U S A 106:399-404
65. Vaira V, Fedele G, Pyne S et al (2010) Preclinical model of organotypic culture for pharmacodynamic profiling of human tumors. Proc Natl Acad Sci USA 107:8352-8356
66. Keith B, Simon MC (2007) Hypoxiainducible factors, stem cells, and cancer. Cell 129:465-472
67. Rodriguez-Jimenez FJ, Moreno-Manzano V, Lucas-Dominguez R et al (2008) Hypoxia causes downregulation of mismatch repair system and genomic instability in stem cells. Stem Cells 26:2052-2062
68. Lin Q, Yun Z (2010) Impact of the hypoxic tumor microenvironment on the regulation of cancer stem cell characteristics. Cancer Biol Ther 9:949-956
69. Benita Y, Kikuchi H, Smith AD et al (2009) An integrative genomics approach identifies hypoxia inducible factor-1 (HIF-1)-target genes that form the core response to hypoxia. Nucleic Acids Res 37:4587-4602
70. Lu X, Kang Y (2010) Hypoxia and hypoxiainducible factors: master regulators of metastasis. Clin Cancer Res 16:5928-5935
71. DeClerck K, Elble RC (2010) The role of hypoxia and acidosis in promoting metastasis and resistance to chemotherapy. Front Biosci 15:213-225
72. Rohwer N, Cramer T (2011) Hypoxiamediated drug resistance: novel insights on the functional interaction of HIFs and cell death pathways. Drug Resist Updat 14:191-201
73. Li Z, Rich JN (2010) Hypoxia and hypoxia inducible factors in cancer stem cell maintenance. Curr Top Microbiol Immunol 345: 21-30
74. Yu H, Zhang CM, Wu YS (2010) Research progress in cancer stem cells and their drug resistance. Chin J Cancer 29:261-264
75. Ricci-Vitiani L, Lombardi DG, Pilozzi E et al (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445:111-115
76. Bartholoma P, Impidjati, Reininger-Mack A et al (2005) A more aggressive breast cancer spheroid model coupled to an electronic capillary sensor system for a high-content screening of cytotoxic agents in cancer therapy: 3-dimensional in vitro tumor spheroids as a screening model. J Biomol Screen 10:705-714
77. Zhang X, Wang W, Yu W et al (2005) Development of an in vitro multicellular tumor spheroid model using microencapsulation and its application in anticancer drug screening and testing. Biotechnol Prog 21:1289-1296
78. Weiswald LB, Richon S, Validire P et al (2009) Newly characterised ex vivo colospheres as a three-dimensional colon cancer cell model of tumour aggressiveness. Br J Cancer 101:473-482
79. Koo BK, Stange DE, Sato T et al (2012) Controlled gene expression in primary Lgr5 organoid cultures. Nat Methods 9:81-83
80. Kim JB (2005) Three-dimensional tissue culture models in cancer biology. Semin Cancer Biol 15:365-377
81. 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
82. Mazzoleni G, Di Lorenzo D, Steimberg N (2009) Modelling tissues in 3D: the next future of pharmaco-toxicology and food research? Genes Nutr 4:13-22
83. Haycock JW (2011) 3D cell culture: a review of current approaches and techniques. Methods Mol Biol 695:1-15
84. Prestwich GD, Liu Y, Yu B et al (2007) 3-D culture in synthetic extracellular matrices: new tissue models for drug toxicology and cancer drug discovery. Adv Enzyme Regul 47:196-207
85. Yamada KM, Cukierman E (2007) Modeling tissue morphogenesis and cancer in 3D. Cell 130:601-610
86. Wartenberg M, Donmez F, Ling FC et al (2001) 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
87. Unsworth BR, Lelkes PI (1998) Growing tissues in microgravity. Nat Med 4:901-907
88. Del Duca D, Werbowetski T, Del Maestro RF (2004) Spheroid preparation from hanging drops: characterization of a model of brain tumor invasion. J Neurooncol 67:295-303
89. Eicher C, Dewerth A, Kirchner B et al (2011) Development of a drug resistance model for hepatoblastoma. Int J Oncol 38:447-454
90. Zhang Q, Nguyen AL, Shi S et al (2011) Three-dimensional spheroid culture of human gingiva-derived mesenchymal stem cells enhances mitigation of chemotherapy-induced oral mucositis. Stem Cells Dev 21(6):937-947
91. Ivascu A, Kubbies M (2006) Rapid generation of single-tumor spheroids for highthroughput cell function and toxicity analysis. J Biomol Screen 11:922-932
92. Lee GY, Kenny PA, Lee EH et al (2007) Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods 4:359-365
93. McMillin DW, Delmore J, Weisberg E et al (2010) Tumor cell-specific bioluminescence platform to identify stroma-induced changes to anticancer drug activity. Nat Med 16:483-489
94. Holliday DL, Brouilette KT, Markert A et al (2009) Novel multicellular organotypic models of normal and malignant breast: tools for dissecting the role of the microenvironment in breast cancer progression. Breast Cancer Res 11:R3
95. Rhee HW, Zhau HE, Pathak S et al (2001) Permanent phenotypic and genotypic changes of prostate cancer cells cultured in a threedimensional rotating-wall vessel. In Vitro Cell Dev Biol Anim 37:127-140
96. Walter-Yohrling J, Pratt BM, Ledbetter S et al (2003) Myofibroblasts enable invasion of endothelial cells into three-dimensional tumor cell clusters: a novel in vitro tumor model. Cancer Chemother Pharmacol 52:263-269
97. Li Q, Chen C, Kapadia A 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
98. Fischbach C, Chen R, Matsumoto T et al (2007) Engineering tumors with 3D scaffolds. Nat Methods 4:855-860
99. Agudelo-Garcia PA, De Jesus JK, Williams SP et al (2011) Glioma cell migration on threedimensional nanofiber scaffolds is regulated by substrate topography and abolished by inhibition of STAT3 signaling. Neoplasia 13: 831-840
100. de Ridder L, Cornelissen M, de Ridder D (2000) Autologous spheroid culture: a screening tool for human brain tumour invasion. Crit Rev Oncol Hematol 36:107-122
101. Biggs T, Foreman J, Sundstrom L et al (2011) Antitumor compound testing in glioblastoma organotypic brain cultures. J Biomol Screen 16:805-817
102. Bruyere F, Melen-Lamalle L, Blacher S et al (2008) Modeling lymphangiogenesis in a three-dimensional culture system. Nat Methods 5:431-437
103. O-Charoenrat P, Rhys-Evans P, Modjtahedi H et al (2000) Overexpression of epidermal growth factor receptor in human head and neck squamous carcinoma cell lines correlates with matrix metalloproteinase-9 expression and in vitro invasion. Int J Cancer 86: 307-317
104. Kleinman HK, Jacob K (2001) Invasion assays. Curr Protoc Cell Biol Chapter 12:Unit 12 12
105. Decaestecker C, Debeir O, Van Ham P et al (2007) Can anti-migratory drugs be screened in vitro? A review of 2D and 3D assays for the quantitative analysis of cell migration. Med Res Rev 27:149-176
106. 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
107. Weaver VM, Petersen OW, Wang F 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
108. Leslie K, Gao SP, Berishaj M et al (2010) Differential interleukin-6/Stat3 signaling as a function of cellular context mediates Rasinduced transformation. Breast Cancer Res 12:R80
109. Kobayashi H, Man S, Graham CH et al (1993) Acquired multicellular- mediated resistance to alkylating agents in cancer. Proc Natl Acad Sci USA 90:3294-3298
110. Thurber AE, Douglas G, Sturm EC et al (2011) Inverse expression states of the BRN2 and MITF transcription factors in melanoma spheres and tumour xenografts regulate the NOTCH pathway. Oncogene 30:3036-3048
111. Howes AL, Chiang GG, Lang ES et al (2007) The phosphatidylinositol 3-kinase inhibitor, PX-866, is a potent inhibitor of cancer cell motility and growth in three-dimensional cultures. Mol Cancer Ther 6:2505-2514
112. Wu YM, Tang J, Zhao P et al (2009) Morphological changes and molecular expressions of hepatocellular carcinoma cells in three-dimensional culture model. Exp Mol Pathol 87:133-140
113. Xiang X, Phung Y, Feng M et al (2011) The development and characterization of a human mesothelioma in vitro 3D model to investigate immunotoxin therapy. PLoS One 6:e14640
114. Wolf K, Mazo I, Leung H et al (2003) Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J Cell Biol 160:267-277
115. Pinco KA, He W, Yang JT (2002) alpha4beta1 integrin regulates lamellipodia protrusion via a focal complex/focal adhesion-independent mechanism. Mol Biol Cell 13:3203-3217
116. Keese CR, Wegener J, Walker SR et al (2004) Electrical wound-healing assay for cells in vitro. Proc Natl Acad Sci USA 101:1554-1559
117. Lampugnani MG (1999) Cell migration into a wounded area in vitro. Methods Mol Biol 96:177-182
118. Yarrow JC, Perlman ZE, Westwood NJ et al (2004) A high-throughput cell migration assay using scratch wound healing, a comparison of image-based readout methods. BMC Biotechnol 4:21
119. Zigmond SH (1977) Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J Cell Biol 75:606-616
120. Zicha D, Dunn GA, Brown AF (1991) A new direct-viewing chemotaxis chamber. J Cell Sci 99(Pt 4):769-775
121. Muinonen-Martin AJ, Veltman DM, Kalna G et al (2010) An improved chamber for direct visualisation of chemotaxis. PLoS One 5:e15309
122. Cai G, Lian J, Shapiro SS et al (2000) Evaluation of endothelial cell migration with a novel in vitro assay system. Methods Cell Sci 22:107-114
123. Pratt BM, Harris AS, Morrow JS et al (1984) Mechanisms of cytoskeletal regulation. Modulation of aortic endothelial cell spectrin by the extracellular matrix. Am J Pathol 117: 349-354
124. Albini A, Iwamoto Y, Kleinman HK et al (1987) A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res 47:3239-3245
125. Ohnishi T, Matsumura H, Izumoto S et al (1998) A novel model of glioma cell invasion using organotypic brain slice culture. Cancer Res 58:2935-2940
126. Deryugina EI, Bourdon MA (1996) Tenascin mediates human glioma cell migration and modulates cell migration onfibronectin. J Cell Sci 109(Pt 3):643-652
127. Rosen EM, Meromsky L, Setter E et al (1990) Quantitation of cytokine-stimulated migration of endothelium and epithelium by a new assay using microcarrier beads. Exp Cell Res 186:22-31
128. Hart IR, Fidler IF (1978) An in vitro quantitative assay for tumor cell invasion. Cancer Res 38:3218-3224
129. Armstrong PB, Quigley JP, Sidebottom E (1982) Transepithelial invasion and intramesenchymal infiltration of the chick embryo chorioallantois by tumor cell lines. Cancer Res 42:1826-1837
130. An Z, Gluck CB, Choy ML et al (2010) Suberoylanilide hydroxamic acid limits migration and invasion of glioma cells in two and three dimensional culture. Cancer Lett 292: 215-227
131. Stein AM, Demuth T, Mobley D et al (2007) A mathematical model of glioblastoma tumor spheroid invasion in a three-dimensional in vitro experiment. Biophys J 92:356-365
132. Friedl P, Noble PB, Walton PA et al (1995) Migration of coordinated cell clusters in mesenchymal and epithelial cancer explants in vitro. Cancer Res 55:4557-4560
133. Wartenberg M, Finkensieper A, Hescheler J et al (2006) Confrontation cultures of embryonic stem cells with multicellular tumor spheroids to study tumor-induced angiogenesis. Methods Mol Biol 331:313-328
134. Fjellbirkeland L, Bjerkvig R, Laerum OD (1998) Non-small-cell lung carcinoma cells invade human bronchial mucosa in vitro. In Vitro Cell Dev Biol Anim 34:333-340