Three-dimensional lung tumor microenvironment modulates therapeutic compound responsiveness in vitro - Implication for drug development

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Ekert, Jason E ^a   Johnson, Kjell ^b   Strake, Brandy ^c   Pardinas, Jose ^a   Jarantow, Stephen ^a   Perkinson, Robert ^a   Colter, David C ^a  

^a Biologics Research   (United States)

^b Lonnie E Grantham II   (United States)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

CETUXIMAB; CRIZOTINIB; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; METMAB; ONARTUZUMAB; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE TECHNIQUE; DRUG DEVELOPMENT; DRUG RESPONSE; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG TUMOR; MONOLAYER CULTURE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; THREE DIMENSIONAL SPHEROID CULTURE; TUMOR CELL LINE; TUMOR MICROENVIRONMENT; TUMOR SPHEROID;

ANTINEOPLASTIC AGENTS; CELL CULTURE TECHNIQUES; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; DRUG DISCOVERY; EPIDERMAL GROWTH FACTOR; HEPATOCYTE GROWTH FACTOR; HUMANS; LIGANDS; LUNG NEOPLASMS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-MET; RECEPTOR, EPIDERMAL GROWTH FACTOR; REPRODUCIBILITY OF RESULTS; SPHEROIDS, CELLULAR; TREATMENT OUTCOME; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

EID: 84898669815     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092248     Document Type: Article

References (70)

1. Arrondeau J, Gan HK, Razak AR, Paoletti X, Le Tourneau C (2010) Development of anti-cancer drugs. Discov Med 10: 355-362
2. Hait WN (2010) Anticancer drug development: the grand challenges. Nat Rev Drug Discov 9: 253-254
3. Hopkins AL (2008) Network pharmacology: the next paradigm in drug discovery. Nat Chem Biol 4: 682-690
4. Kola I (2008) The state of innovation in drug development. Clin Pharmacol Ther 83: 227-230
5. Breslin S, O'Driscoll L (2013) Three-dimensional cell culture: the missing link in drug discovery. Drug Discov Today 18: 240-249
6. DiMasi JA, Grabowski HG (2007) Economics of new oncology drug development. J Clin Oncol 25: 209-216 (Pubitemid 350003036)
7. 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
8. Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, et al. (2010) Multicellular tumor spheroids: an underestimated tool is catching up again. J Biotechnol 148: 3-15
9. Ho WJ, Pham EA, Kim JW, Ng CW, Kim JH, et al. (2010) Incorporation of multicellular spheroids into 3-D polymeric scaffolds provides an improved tumor model for screening anticancer drugs. Cancer Sci 101: 2637-2643
10. Luca AC, Mersch S, Deenen R, Schmidt S, Messner I, et al. (2013) Impact of the 3D microenvironment on phenotype, gene expression, and EGFR inhibition of colorectal cancer cell lines. PLoS One 8: e59689
11. Fischbach C, Chen R, Matsumoto T, Schmelzle T, Brugge JS, et al. (2007) Engineering tumors with 3D scaffolds. Nat Methods 4: 855-860 (Pubitemid 350055585)
12. Sundstrom L, Biggs T, Laskowski A, Stoppini L (2012) OrganDots-An organotypic 3D tissue culture platform for drug development. Expert Opin Drug Discov 7: 525-534
13. Tung YC, Hsiao AY, Allen SG, Torisawa YS, Ho M, et al. (2011) Highthroughput 3D spheroid culture and drug testing using a 384 hanging drop array. Analyst 136: 473-478
14. Catros S, Guillemot F, Nandakumar A, Ziane S, Moroni L, et al. (2012) Layerby- layer tissue microfabrication supports cell proliferation in vitro and in vivo. Tissue Eng Part C Methods 18: 62-70
15. Friedl P (2004) Prespecification and plasticity: shifting mechanisms of cell migration. Curr Opin Cell Biol 16: 14-23 (Pubitemid 38368147)
16. Phung YT, Barbone D, Broaddus VC, Ho M (2011) Rapid generation of in vitro multicellular spheroids for the study of monoclonal antibody therapy. J Cancer 2: 507-514
17. Vinci M, Gowan S, Boxall F, Patterson L, Zimmermann M, et al. (2012) Advances in establishment and analysis of three-dimensional tumor spheroidbased functional assays for target validation and drug evaluation. BMC Biol 10: 29
18. Acunzo M, Romano G, Palmieri D, Lagana A, Garofalo M, et al. (2013) Crosstalk between MET and EGFR in non-small cell lung cancer involves miR-27a and Sprouty2. Proc Natl Acad Sci U S A 110: 8573-8578
19. Xu H, Stabile LP, Gubish CT, Gooding WE, Grandis JR, et al. (2011) Dual blockade of EGFR and c-Met abrogates redundant signaling and proliferation in head and neck carcinoma cells. Clin Cancer Res 17: 4425-4438
20. Puri N, Salgia R (2008) Synergism of EGFR and c-Met pathways, cross-talk and inhibition, in non-small cell lung cancer. J Carcinog 7: 9
21. Jo M, Stolz DB, Esplen JE, Dorko K, Michalopoulos GK, et al. (2000) Cross-talk between epidermal growth factor receptor and c-Met signal pathways in transformed cells. J Biol Chem 275: 8806-8811 (Pubitemid 30180235)
22. Miyamoto M, Ojima H, Iwasaki M, Shimizu H, Kokubu A, et al. (2011) Prognostic significance of overexpression of c-Met oncoprotein in cholangiocarcinoma. Br J Cancer 105: 131-138
23. Zucali PA, Ruiz MG, Giovannetti E, Destro A, Varella-Garcia M, et al. (2008) Role of cMET expression in non-small-cell lung cancer patients treated with EGFR tyrosine kinase inhibitors. Ann Oncol 19: 1605-1612
24. Workman P, Clarke PA (2011) Resisting targeted therapy: fifty ways to leave your EGFR. Cancer Cell 19: 437-440
25. Gonzalez de Castro D, Clarke PA, Al-Lazikani B, Workman P (2013) Personalized cancer medicine: molecular diagnostics, predictive biomarkers, and drug resistance. Clin Pharmacol Ther 93: 252-259
26. Nedergaard MK, Hedegaard CJ, Poulsen HS (2012) Targeting the epidermal growth factor receptor in solid tumor malignancies. BioDrugs 26: 83-99
27. Moritz W (2011) Effective Determination of Cellular Viability in Microtissue Spheroids. Promega Corporation
28. Albrecht C, Helmreich M, Tichy B, Marlovits S, Plasenzotti R, et al. (2009) Impact of 3D-culture on the expression of differentiation markers and hormone receptors in growth plate chondrocytes as compared to articular chondrocytes. Int J Mol Med 23: 347-355
29. Kiss DL, Windus LC, Avery VM (2013) Chemokine receptor expression on integrin-mediated stellate projections of prostate cancer cells in 3D culture. Cytokine 64: 122-130
30. Windus LC, Kiss DL, Glover T, Avery VM (2012) In vivo biomarker expression patterns are preserved in 3D cultures of Prostate Cancer. Exp Cell Res 318: 2507-2519
31. Burga LN, Hu H, Juvekar A, Tung NM, Troyan SL, et al. (2011) Loss of BRCA1 leads to an increase in epidermal growth factor receptor expression in mammary epithelial cells, and epidermal growth factor receptor inhibition prevents estrogen receptor-negative cancers in BRCA1-mutant mice. Breast Cancer Res 13: R30
32. Liu TF, Cohen KA, Ramage JG, Willingham MC, Thorburn AM, et al. (2003) A diphtheria toxin-epidermal growth factor fusion protein is cytotoxic to human glioblastoma multiforme cells. Cancer Res 63: 1834-1837 (Pubitemid 36460845)
33. Uramoto H, Shimokawa H, Hanagiri T, Kuwano M, Ono M (2011) Expression of selected gene for acquired drug resistance to EGFR-TKI in lung adenocarcinoma. Lung Cancer 73: 361-365
34. Yano S, Yamada T, Takeuchi S, Tachibana K, Minami Y, et al. (2011) Hepatocyte growth factor expression in EGFR mutant lung cancer with intrinsic and acquired resistance to tyrosine kinase inhibitors in a Japanese cohort. J Thorac Oncol 6: 2011-2017
35. Lama R, Zhang L, Naim JM, Williams J, Zhou A, et al. (2013) Development, validation and pilot screening of an in vitro multi-cellular three-dimensional cancer spheroid assay for anti-cancer drug testing. Bioorg Med Chem 21: 922-931
36. Tanizaki J, Okamoto I, Sakai K, Nakagawa K (2011) Differential roles of transphosphorylated EGFR, HER2, HER3, and RET as heterodimerisation partners of MET in lung cancer with MET amplification. Br J Cancer 105: 807-813
37. Longati P, Jia X, Eimer J, Wagman A, Witt MR, et al. (2013) 3D pancreatic carcinoma spheroids induce a matrix-rich, chemoresistant phenotype offering a better model for drug testing. BMC Cancer 13: 95
38. Singhirunnusorn P, Ueno Y, Matsuo M, Suzuki S, Saiki I, et al. (2007) Transient suppression of ligand-mediated activation of epidermal growth factor receptor by tumor necrosis factor-Alpha through the TAK1-p38 signaling pathway. J Biol Chem 282: 12698-12706 (Pubitemid 47100631)
39. Yamada T, Matsumoto K, Wang W, Li Q, Nishioka Y, et al. (2010) Hepatocyte growth factor reduces susceptibility to an irreversible epidermal growth factor receptor inhibitor in EGFR-T790M mutant lung cancer. Clin Cancer Res 16: 174-183
40. Yano S, Wang W, Li Q, Matsumoto K, Sakurama H, et al. (2008) Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-Activating mutations. Cancer Res 68: 9479-9487
41. Wang W, Li Q, Yamada T, Matsumoto K, Matsumoto I, et al. (2009) Crosstalk to stromal fibroblasts induces resistance of lung cancer to epidermal growth factor receptor tyrosine kinase inhibitors. Clin Cancer Res 15: 6630-6638
42. Christensen JG, Burrows J, Salgia R (2005) c-Met as a target for human cancer and characterization of inhibitors for therapeutic intervention. Cancer Lett 225: 1-26 (Pubitemid 40732764)
43. Barnes DW (1982) Epidermal growth factor inhibits growth of A431 human epidermoid carcinoma in serum-free cell culture. J Cell Biol 93: 1-4
44. Yamada T, Takeuchi S, Kita K, Bando H, Nakamura T, et al. (2012) Hepatocyte growth factor induces resistance to anti-epidermal growth factor receptor antibody in lung cancer. J Thorac Oncol 7: 272-280
45. Yamada T, Takeuchi S, Nakade J, Kita K, Nakagawa T, et al. (2012) Paracrine receptor activation by microenvironment triggers bypass survival signals and ALK inhibitor resistance in EML4-ALK lung cancer cells. Clin Cancer Res 18: 3592-3602
46. Nakagawa T, Takeuchi S, Yamada T, Nanjo S, Ishikawa D, et al. (2012) Combined therapy with mutant-selective EGFR inhibitor and Met kinase inhibitor for overcoming erlotinib resistance in EGFR-mutant lung cancer. Mol Cancer Ther 11: 2149-2157
47. Thomson S, Buck E, Petti F, Griffin G, Brown E, et al. (2005) Epithelial to mesenchymal transition is a determinant of sensitivity of non-small-cell lung carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition. Cancer Res 65: 9455-9462 (Pubitemid 41508014)
48. Tang Z, Du R, Jiang S, Wu C, Barkauskas DS, et al. (2008) Dual MET-EGFR combinatorial inhibition against T790M-EGFR-mediated erlotinib-resistant lung cancer. Br J Cancer 99: 911-922
49. Sos ML, Koker M, Weir BA, Heynck S, Rabinovsky R, et al. (2009) PTEN loss contributes to erlotinib resistance in EGFR-mutant lung cancer by activation of Akt and EGFR. Cancer Res 69: 3256-3261
50. Graveel CR, Tolbert D, Vande Woude GF (2013) MET: a critical player in tumorigenesis and therapeutic target. Cold Spring Harb Perspect Biol 5
51. Surati M, Patel P, Peterson A, Salgia R (2011) Role of MetMAb (OA-5D5) in c- MET active lung malignancies. Expert Opin Biol Ther 11: 1655-1662
52. Peschard P, Park M (2007) From Tpr-Met to Met, tumorigenesis and tubes. Oncogene 26: 1276-1285 (Pubitemid 46328462)
53. Castoldi R, Ecker V, Wiehle L, Majety M, Busl-Schuller R, et al. (2013) A novel bispecific EGFR/Met antibody blocks tumor-promoting phenotypic effects induced by resistance to EGFR inhibition and has potent antitumor activity. Oncogene
54. Spigel DR, Burris HA 3rd, Greco FA, Shipley DL, Friedman EK, et al. (2011) Randomized, double-blind, placebo-controlled, phase II trial of sorafenib and erlotinib or erlotinib alone in previously treated advanced non-small-cell lung cancer. J Clin Oncol 29: 2582-2589
55. Jin H, Yang R, Zheng Z, Romero M, Ross J, et al. (2008) MetMAb, the onearmed 5D5 anti-c-Met antibody, inhibits orthotopic pancreatic tumor growth and improves survival. Cancer Res 68: 4360-4368
56. Takata M, Chikumi H, Miyake N, Adachi K, Kanamori Y, et al. (2012) Lack of AKT activation in lung cancer cells with EGFR mutation is a novel marker of cetuximab sensitivity. Cancer Biol Ther 13: 369-378
57. Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA (2009) Spheroid-based drug screen: considerations and practical approach. Nat Protoc 4: 309-324
58. Kim SH, Choi SJ, Kim YC, Kuh HJ (2009) Anti-tumor activity of noble indirubin derivatives in human solid tumor models in vitro. Arch Pharm Res 32: 915-922
59. Li Q, Chow AB, Mattingly RR (2010) Three-dimensional overlay culture models of human breast cancer reveal a critical sensitivity to mitogen-Activated protein kinase kinase inhibitors. J Pharmacol Exp Ther 332: 821-828
60. David L, Dulong V, Le Cerf D, Cazin L, Lamacz M, et al. (2008) Hyaluronan hydrogel: an appropriate three-dimensional model for evaluation of anticancer drug sensitivity. Acta Biomater 4: 256-263 (Pubitemid 351218095)
61. 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
62. Howes AL, Chiang GG, Lang ES, Ho CB, Powis G, 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 (Pubitemid 47480416)
63. Linardou H, Dahabreh IJ, Kanaloupiti D, Siannis F, Bafaloukos D, et al. (2008) Assessment of somatic k-RAS mutations as a mechanism associated with resistance to EGFR-targeted agents: a systematic review and meta-Analysis of studies in advanced non-small-cell lung cancer and metastatic colorectal cancer. Lancet Oncol 9: 962-972
64. Kurtze I, Sonnemann J, Beck JF (2011) KRAS-mutated non-small cell lung cancer cells are responsive to either co-treatment with erlotinib or gefitinib and histone deacetylase inhibitors or single treatment with lapatinib. Oncol Rep 25: 1021-1029
65. Sun R, Zhang Q, Guo L, Chen MY, Sun Y, et al. (2012) HGF stimulates proliferation through the HGF/c-Met pathway in nasopharyngeal carcinoma cells. Oncol Lett 3: 1124-1128
66. Martens T, Schmidt NO, Eckerich C, Fillbrandt R, Merchant M, et al. (2006) A novel one-Armed anti-c-Met antibody inhibits glioblastoma growth in vivo. Clin Cancer Res 12: 6144-6152 (Pubitemid 44703780)
67. Schulte A, Liffers K, Kathagen A, Riethdorf S, Zapf S, et al. (2013) Erlotinib resistance in EGFR-Amplified glioblastoma cells is associated with upregulation of EGFRvIII and PI3Kp110delta. Neuro Oncol
68. Vinci M, Box C, Zimmermann M, Eccles SA (2013) Tumor spheroid-based migration assays for evaluation of therapeutic agents. Methods Mol Biol 986: 253-266
69. Ilina O, Friedl P (2009) Mechanisms of collective cell migration at a glance. J Cell Sci 122: 3203-3208
70. Garay T, Juhasz E, Molnar E, Eisenbauer M, Czirok A, et al. (2013) Cell migration or cytokinesis and proliferation?-revisiting the "go or grow" hypothesis in cancer cells in vitro. Exp Cell Res 319: 3094-3103