Growth of lung cancer cells in three-dimensional microenvironments reveals key features of tumor malignancy

Integrative Biology

Volumn 4, Issue 4, 2012, Pages 440-448

  Cichon, Magdalena A ^a   Gainullin, Vladimir G ^b   Zhang, Ying ^a   Radisky, Derek C ^a  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CELL PROTEIN; LAMININ; LTBR PROTEIN; MGST1 3 PROTEIN; MLPH 1 PROTEIN; RIN2 PROTEIN; SLC27 PROTEIN; UNCLASSIFIED DRUG; USP46 PROTEIN; UVOMORULIN;

ARTICLE; CANCER GROWTH; CANCER PROGNOSIS; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; LARGE CELL CARCINOMA; LUNG ADENOCARCINOMA; LUNG CANCER; LUNG NON SMALL CELL CANCER; LUNG SQUAMOUS CELL CARCINOMA; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; TUMOR MICROENVIRONMENT; UPREGULATION;

ADENOCARCINOMA; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; COLLAGEN; DISEASE-FREE SURVIVAL; DOWN-REGULATION; DRUG COMBINATIONS; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KAPLAN-MEIER ESTIMATE; LAMININ; LUNG NEOPLASMS; NEOPLASM INVASIVENESS; PROGNOSIS; PROTEOGLYCANS; UP-REGULATION;

EID: 84859142802     PISSN: 17579694     EISSN: 17579708     Source Type: Journal    
DOI: 10.1039/c1ib00090j     Document Type: Article

References (55)

1. A. Jemal, M. M. Center and E. Ward, The convergence of lung cancer rates between blacks and whites under the age of 40, United States, Cancer Epidemiol., Biomarkers Prev., 2009, 18, 3349-52.
2. A. Jemal, R. Siegel, J. Xu and E. Ward, Cancer statistics, Ca-Cancer J. Clin., 2010, 60, 277-300.
3. A. F. Gazdar, L. Girard, W. W. Lockwood, W. L. Lam and J. D. Minna, Lung cancer cell lines as tools for biomedical discovery and research, J. Natl. Cancer Inst., 2010, 102, 1310-21.
4. (a) Wistuba, II, D. Bryant, C. Behrens, S. Milchgrub, A. K. Virmani, R. Ashfaq, J. D. Minna and A. F. Gazdar, Comparison of features of human lung cancer cell lines and their corresponding tumors, Clin. Cancer Res., 1999, 5, 991-1000;
5. (b) L. Ding, G. Getz, D. A. Wheeler, E. R. Mardis, M. D. McLellan, K. Cibulskis, C. Sougnez, H. Greulich, D. M. Muzny, M. B. Morgan, L. Fulton, R. S. Fulton, Q. Zhang, M. C. Wendl, M. S. Lawrence, D. E. Larson, K. Chen, D. J. Dooling, A. Sabo, A. C. Hawes, H. Shen, S. N. Jhangiani, L. R. Lewis, O. Hall, Y. Zhu, T. Mathew, Y. Ren, J. Yao, S. E. Scherer, K. Clerc, G. A. Metcalf, B. Ng, A. Milosavljevic, M. L. Gonzalez-Garay, J. R. Osborne, R. Meyer, X. Shi, Y. Tang, D. C. Koboldt, L. Lin, R. Abbott, T. L. Miner, C. Pohl, G. Fewell, C. Haipek, H. Schmidt, B. H. Dunford-Shore, A. Kraja, S. D. Crosby, C. S. Sawyer, T. Vickery, S. Sander, J. Robinson, W. Winckler, J. Baldwin, L. R. Chirieac, A. Dutt, T. Fennell, M. Hanna, B. E. Johnson, R. C. Onofrio, R. K. Thomas, G. Tonon, B. A. Weir, X. Zhao, L. Ziaugra, M. C. Zody, T. Giordano, M. B. Orringer, J. A. Roth, M. R. Spitz, Wistuba, II, B. Ozenberger, P. J. Good, A. C. Chang, D. G. Beer, M. A. Watson, M. Ladanyi, S. Broderick, A. Yoshizawa, W. D. Travis, W. Pao, M. A. Province, G. M. Weinstock, H. E. Varmus, S. B. Gabriel, E. S. Lander, R. A. Gibbs, M. Meyerson and R. K. Wilson, Somatic mutations affect key pathways in lung adenocarcinoma, Nature, 2008, 455, 1069-75.
6. M. J. Bissell and D. Radisky, Nat. Rev. Cancer, 2001, 1, 46-54.
7. K. L. Schmeichel and M. J. Bissell, Modeling tissue-specific signaling and organ function in three dimensions, J. Cell Sci., 2003, 116, 2377-88.
8. G. Y. Lee, P. A. Kenny, E. H. Lee and M. J. Bissell, Three-dimensional culture models of normal and malignant breast epithelial cells, Nat. Methods, 2007, 4, 359-65. (Pubitemid 46766981)
9. S. E. Al-Batran, S. T. Astner, M. Supthut, F. Gamarra, K. Brueckner, U. Welsch, R. Knuechel and R. M. Huber, Three-dimensional in vitro cocultivation of lung carcinoma cells with human bronchial organ culture as a model for bronchial carcinoma, Am. J. Respir. Cell Mol. Biol., 1999, 21, 200-8.
10. (a) H. Y. Chen, S. L. Yu, C. H. Chen, G. C. Chang, C. Y. Chen, A. Yuan, C. L. Cheng, C. H. Wang, H. J. Terng, S. F. Kao, W. K. Chan, H. N. Li, C. C. Liu, S. Singh, W. J. Chen, J. J. Chen and P. C. Yang, A five-gene signature and clinical outcome in non-small-cell lung cancer, N. Engl. J. Med., 2007, 356, 11-20;
11. (b) M. Raponi, Y. Zhang, J. Yu, G. Chen, G. Lee, J. M. Taylor, J. Macdonald, D. Thomas, C. Moskaluk, Y. Wang and D. G. Beer, Gene expression signatures for predicting prognosis of squamous cell and adenocarcinomas of the lung, Cancer Res., 2006, 66, 7466-72;
12. (c) K. Shedden, J. M. Taylor, S. A. Enkemann, M. S. Tsao, T. J. Yeatman, W. L. Gerald, S. Eschrich, I. Jurisica, T. J. Giordano, D. E. Misek, A. C. Chang, C. Q. Zhu, D. Strumpf, S. Hanash, F. A. Shepherd, K. Ding, L. Seymour, K. Naoki, N. Pennell, B. Weir, R. Verhaak, C. Ladd-Acosta, T. Golub, M. Gruidl, A. Sharma, J. Szoke, M. Zakowski, V. Rusch, M. Kris, A. Viale, N. Motoi, W. Travis, B. Conley, V. E. Seshan, M. Meyerson, R. Kuick, K. K. Dobbin, T. Lively, J. W. Jacobson and D. G. Beer, Gene expression-based survival prediction in lung adenocarcinoma: a multi-site, blinded validation study, Nat. Med., 2008, 14, 822-7;
13. (d) D. G. Beer, S. L. Kardia, C. C. Huang, T. J. Giordano, A. M. Levin, D. E. Misek, L. Lin, G. Chen, T. G. Gharib, D. G. Thomas, M. L. Lizyness, R. Kuick, S. Hayasaka, J. M. Taylor, M. D. Iannettoni, M. B. Orringer and S. Hanash, Gene-expression profiles predict survival of patients with lung adenocarcinoma, Nat. Med., 2002, 8, 816-24;
14. (e) H. Kadara, C. Behrens, P. Yuan, L. Solis, D. Liu, X. Gu, J. D. Minna, J. J. Lee, E. Kim, W. K. Hong, Wistuba, II and R. Lotan, A five-gene and corresponding protein signature for stage-I lung adenocarcinoma prognosis, Clin. Cancer Res., 2011, 17, 1490-501;
15. (f) S. K. Lau, P. C. Boutros, M. Pintilie, F. H. Blackhall, C. Q. Zhu, D. Strumpf, M. R. Johnston, G. Darling, S. Keshavjee, T. K. Waddell, N. Liu, D. Lau, L. Z. Penn, F. A. Shepherd, I. Jurisica, S. D. Der and M. S. Tsao, Three-gene prognostic classifier for early-stage non small-cell lung cancer, J. Clin. Oncol., 2007, 25, 5562-9;
16. (g) C. E. Reed, A. Graham, R. S. Hoda, A. Khoor, E. Garrett- Mayer, M. B. Wallace and M. Mitas, A simple two-gene prognostic model for adenocarcinoma of the lung, J. Thorac. Cardiovasc. Surg., 2008, 135, 627-34;
17. (h) Y. W. Wan, E. Sabbagh, R. Raese, Y. Qian, D. Luo, J. Denvir, V. Vallyathan, V. Castranova and N. L. Guo, Hybrid models identified a 12-gene signature for lung cancer prognosis and chemoresponse prediction, PLoS One, 2010, 5, e12222.
18. J. J. Chen, K. Peck, T. M. Hong, S. C. Yang, Y. P. Sher, J. Y. Shih, R. Wu, J. L. Cheng, S. R. Roffler, C. W. Wu and P. C. Yang, Global analysis of gene expression in invasion by a lung cancer model, Cancer Res., 2001, 61, 5223-30.
19. M. E. Garber, O. G. Troyanskaya, K. Schluens, S. Petersen, Z. Thaesler, M. Pacyna-Gengelbach, M. van de Rijn, G. D. Rosen, C. M. Perou, R. I. Whyte, R. B. Altman, P. O. Brown, D. Botstein and I. Petersen, Diversity of gene expression in adenocarcinoma of the lung, Proc. Natl. Acad. Sci. U. S. A., 2001, 98, 13784-9. (Pubitemid 33115976)
20. P. A. Kenny, G. Y. Lee, C. A. Myers, R. M. Neve, J. R. Semeiks, P. T. Spellman, K. Lorenz, E. H. Lee, M. H. Barcellos-Hoff, O. W. Petersen, J. W. Gray and M. J. Bissell, The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression, Mol. Oncol., 2007, 1, 84-96. (Pubitemid 46776616)
21. (a)M. V. Fournier, K. J. Martin, P. A. Kenny, K. Xhaja, I. Bosch, P. Yaswen and M. J. Bissell, Gene expression signature in organized and growth-arrested mammary acini predicts good outcome in breast cancer, Cancer Res., 2006, 66, 7095-102;
22. (b) K. J. Martin, D. R. Patrick, M. J. Bissell and M. V. Fournier, Prognostic breast cancer signature identified from 3D culture model accurately predicts clinical outcome across independent datasets, PLoS One, 2008, 3, e2994.
23. M. Ashburner, C. A. Ball, J. A. Blake, D. Botstein, H. Butler, J. M. Cherry, A. P. Davis, K. Dolinski, S. S. Dwight, J. T. Eppig, M. A. Harris, D. P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J. C. Matese, J. E. Richardson, M. Ringwald, G. M. Rubin and G. Sherlock, Gene ontology: tool for the unification of biology. The Gene Ontology Consortium, Nat. Genet., 2000, 25, 25-9. (Pubitemid 30257031)
24. M. Boyd, S. Bressendorff, J. Moller, J. Olsen and J. T. Troelsen, Mapping of HNF4alpha target genes in intestinal epithelial cells, BMC Gastroenterol., 2009, 9, 68.
25. A. M. Marshall, V. P. Pai, M. A. Sartor and N. D. Horseman, In vitro multipotent differentiation and barrier function of a human mammary epithelium, Cell Tissue Res., 2009, 335, 383-95.
26. M. Hussain, M. Rao, A. E. Humphries, J. A. Hong, F. Liu, M. Yang, D. Caragacianu and D. S. Schrump, Tobacco smoke induces polycomb-mediated repression of Dickkopf-1 in lung cancer cells, Cancer Res., 2009, 69, 3570-8.
27. H. Maunders, S. Patwardhan, J. Phillips, A. Clack and A. Richter, Human bronchial epithelial cell transcriptome: gene expression changes following acute exposure to whole cigarette smoke in vitro, Am. J. Physiol.: Lung Cell. Mol. Phys., 2007, 292, L1248-56.
28. A. H. Bild, G. Yao, J. T. Chang, Q. Wang, A. Potti, D. Chasse, M. B. Joshi, D. Harpole, J. M. Lancaster, A. Berchuck, J. A. Olson, Jr., J. R. Marks, H. K. Dressman, M. West and J. R. Nevins, Oncogenic pathway signatures in human cancers as a guide to targeted therapies, Nature, 2006, 439, 353-7.
29. F. C. Detterbeck, D. J. Boffa and L. T. Tanoue, The new lung cancer staging system, Chest, 2009, 136, 260-71.
30. P. C. Boutros, S. K. Lau, M. Pintilie, N. Liu, F. A. Shepherd, S. D. Der, M. S. Tsao, L. Z. Penn and I. Jurisica, Prognostic gene signatures for non-small-cell lung cancer, Proc. Natl. Acad. Sci. U. S. A., 2009, 106, 2824-8.
31. (a) P. C. Boutros, M. Pintilie, T. John, M. H. Starmans, S. D. Der, F. A. Shepherd, M. S. Tsao and I. Jurisica, Re: Gene expressionbased prognostic signatures in lung cancer: ready for clinical use?, J. Natl. Cancer Inst., 2010, 102, 1677-8; author reply 1678-9;
32. (b) J. Subramanian and R. Simon, Gene expression-based prognostic signatures in lung cancer: ready for clinical use?, J. Natl. Cancer Inst., 2010, 102, 464-74.
33. (a) M. H. Barcellos-Hoff, J. Aggeler, T. G. Ram and M. J. Bissell, Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane, Development, 1989, 105, 223-35;
34. (b) O. W. Petersen, L. Ronnov-Jessen, A. R. Howlett and M. J. Bissell, Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells, Proc. Natl. Acad. Sci. U. S. A., 1992, 89, 9064-8;
35. (c) V.M. Weaver, O. W. Petersen, F. Wang, C. A. Larabell, P. Briand, C. Damsky and M. J. Bissell, Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies, J. Cell Biol., 1997, 137, 231-45.
36. M. B. Vaughan, R. D. Ramirez, W. E. Wright, J. D. Minna and J. W. Shay, A three-dimensional model of differentiation of immortalized human bronchial epithelial cells, Differentiation, 2006, 74, 141-8.
37. (a) J. Fukuoka, T. Fujii, J. H. Shih, T. Dracheva, D. Meerzaman, A. Player, K. Hong, S. Settnek, A. Gupta, K. Buetow, S. Hewitt, W. D. Travis and J. Jen, Chromatin remodeling factors and BRM/BRG1 expression as prognostic indicators in non-small cell lung cancer, Clin. Cancer Res., 2004, 10, 4314-24;
38. (b) D. N. Reisman, J. Sciarrotta, W. Wang, W. K. Funkhouser and B. E. Weissman, Loss of BRG1/BRM in human lung cancer cell lines and primary lung cancers: correlation with poor prognosis, Cancer Res., 2003, 63, 560-6.
39. F. Bertucci, V. Nasser, S. Granjeaud, F. Eisinger, J. Adelaide, R. Tagett, B. Loriod, A. Giaconia, A. Benziane, E. Devilard, J. Jacquemier, P. Viens, C. Nguyen, D. Birnbaum and R. Houlgatte, Gene expression profiles of poor-prognosis primary breast cancer correlate with survival, Hum. Mol. Genet., 2002, 11, 863-72. (Pubitemid 34449774)
40. N. M. Linnerth, K. Sirbovan and R. A. Moorehead, Use of a transgenic mouse model to identify markers of human lung tumors, Int. J. Cancer, 2005, 114, 977-82.
41. P. A. Kenny and M. J. Bissell, Tumor reversion: correction of malignant behavior by microenvironmental cues, Int. J. Cancer, 2003, 107, 688-95. (Pubitemid 37339720)
42. D. A. Glesne, W. Zhang, S. Mandava, L. Ursos, M. E. Buell, L. Makowski and D. J. Rodi, Subtractivetranscriptomics: establishing polarity drives in vitro human endothelial morphogenesis, Cancer Res., 2006, 66, 4030-40.
43. (a) J. E. Casanova, X. Wang, R. Kumar, S. G. Bhartur, J. Navarre, J. E. Woodrum, Y. Altschuler, G. S. Ray and J. R. Goldenring, Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells, Mol. Biol. Cell, 1999, 10, 47-61;
44. (b) A. Swiatecka-Urban, L. Talebian, E. Kanno, S. Moreau-Marquis, B. Coutermarsh, K. Hansen, K. H. Karlson, R. Barnaby, R. E. Cheney, G. M. Langford, M. Fukuda and B. A. Stanton, Myosin Vb is required for trafficking of the cystic fibrosis transmembrane conductance regulator in Rab11a-specific apical recycling endosomes in polarized human airway epithelial cells, J. Biol. Chem., 2007, 282, 23725-36. (Pubitemid 47311948)
45. D. C. Radisky and M. J. Bissell, Matrix metalloproteinase-induced genomic instability, Curr. Opin. Genet. Dev., 2006, 16, 45-50.
46. P. Ji, S.Diederichs,W.Wang, S. Boing,R. Metzger, P. M. Schneider, N. Tidow, B. Brandt, H. Buerger, E. Bulk, M. Thomas,W. E. Berdel, H. Serve and C. Muller-Tidow, MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer, Oncogene, 2003, 22, 8031-41.
47. V. Tripathi, J. D. Ellis, Z. Shen, D. Y. Song, Q. Pan, A. T. Watt, S. M. Freier, C. F. Bennett, A. Sharma, P. A. Bubulya, B. J. Blencowe, S. G. Prasanth and K. V. Prasanth, The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation, Mol. Cell, 2010, 39, 925-38.
48. K. Tano, R. Mizuno, T. Okada, R. Rakwal, J. Shibato, Y. Masuo, K. Ijiri and N. Akimitsu, MALAT-1 enhances cell motility of lung adenocarcinoma cells by influencing the expression of motility-related genes, FEBS Lett., 2010, 584, 4575-80.
49. (a) J. Le Beyec, R. Xu, S. Y. Lee, C. M. Nelson, A. Rizki, J. Alcaraz and M. J. Bissell, Cell shape regulates global histone acetylation in human mammary epithelial cells, Exp. Cell Res., 2007, 313, 3066-75;
50. (b) C. A. Myers, C. Schmidhauser, J. Mellentin-Michelotti, G. Fragoso, C. D. Roskelley, G. Casperson, R. Mossi, P. Pujuguet, G. Hager and M. J. Bissell, Characterization of BCE-1, a transcriptional enhancer regulated by prolactin and extracellular matrix and modulated by the state of histone acetylation, Mol. Cell Biol., 1998, 18, 2184-95;
51. (c) P. Pujuguet, D. Radisky, D. Levy, C. Lacza and M. J. Bissell, Trichostatin A inhibits beta-casein expression in mammary epithelial cells, J. Cell. Biochem., 2001, 83, 660-70;
52. (d) R. Xu, V. A. Spencer and M. J. Bissell, Extracellular matrix-regulated gene expression requires cooperation of SWI/SNF and transcription factors, J. Biol. Chem., 2007, 282, 14992-9. (Pubitemid 47093328)
53. (a) S. A. Lelievre, V. M. Weaver, J. A. Nickerson, C. A. Larabell, A. Bhaumik, O. W. Petersen and M. J. Bissell, Tissue phenotype depends on reciprocal interactions between the extracellular matrix and the structural organization of the nucleus, Proc. Natl. Acad. Sci. U. S. A., 1998, 95, 14711-6;
54. (b) M. J. Bissell, H. G. Hall and G. Parry, How does the extracellular matrix direct gene expression?, J. Theor. Biol., 1982, 99, 31-68. (Pubitemid 13209096)
55. C. S. Chen, C. M. Nelson, D. Khauv, S. Bennett, E. S. Radisky, Y. Hirai, M. J. Bissell and D. C. Radisky, Homology with vesicle fusion mediator syntaxin-1a predicts determinants of epimorphin/syntaxin-2 function in mammary epithelial morphogenesis, J. Biol. Chem., 2009, 284, 6877-84.