The need for complex 3D culture models to unravel novel pathways and identify accurate biomarkers in breast cancer

Advanced Drug Delivery Reviews

Volumn 69-70, Issue , 2014, Pages 42-51

  Weigelt, Britta ^a   Ghajar, Cyrus M ^b   Bissell, Mina J ^c  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Breast cancer; Co culture; Microenvironment; Signaling pathway; Three dimensional cell culture; Tissue architecture

Indexed keywords

CELL CULTURE; DISEASES; PIGMENTS; SIGNALING;

BREAST CANCER; COCULTURE; MICROENVIRONMENTS; SIGNALING PATHWAYS; THREE DIMENSIONAL CELL CULTURE; TISSUE ARCHITECTURE;

THREE DIMENSIONAL;

TUMOR MARKER;

BIOLOGICAL MODEL; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL; CANCER GROWTH; CANCER MODEL; CANCER RESEARCH; CANCER RESISTANCE; COCULTURE; CULTURE TECHNIQUE; DISEASE ACTIVITY; DRUG RESEARCH; EXTRACELLULAR MATRIX; HIGH THROUGHPUT SCREENING; HUMAN; IN VITRO STUDY; METASTASIS POTENTIAL; MORPHOGENESIS; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TISSUE ENGINEERING; TUMOR MICROENVIRONMENT; TUMOR SPHEROID; TUMOR SUPPRESSOR GENE; ANIMAL; BREAST TUMOR; FEMALE; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; BREAST NEOPLASMS; CELL CULTURE TECHNIQUES; FEMALE; HUMANS; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL;

EID: 84899966772     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2014.01.001     Document Type: Review

References (147)

1. Reis-Filho J.S., Pusztai L. Gene expression profiling in breast cancer: classification, prognostication, and prediction. Lancet 2011, 378:1812-1823.
2. Hudson T.J., Anderson W., Artez A., Barker A.D., Bell C., Bernabe R.R., Bhan M.K., Calvo F., Eerola I., Gerhard D.S., Guttmacher A., Guyer M., Hemsley F.M., Jennings J.L., Kerr D., Klatt P., Kolar P., Kusada J., Lane D.P., Laplace F., Youyong L., Nettekoven G., Ozenberger B., Peterson J., Rao T.S., Remacle J., Schafer A.J., Shibata T., Stratton M.R., Vockley J.G., Watanabe K., Yang H., Yuen M.M., Knoppers B.M., Bobrow M., Cambon-Thomsen A., Dressler L.G., Dyke S.O., Joly Y., Kato K., Kennedy K.L., Nicolas P., Parker M.J., Rial-Sebbag E., Romeo-Casabona C.M., Shaw K.M., Wallace S., Wiesner G.L., Zeps N., Lichter P., Biankin A.V., Chabannon C., Chin L., Clement B., de Alava E., Degos F., Ferguson M.L., Geary P., Hayes D.N., Hudson T.J., Johns A.L., Kasprzyk A., Nakagawa H., Penny R., Piris M.A., Sarin R., Scarpa A., Shibata T., van de Vijver M., Futreal P.A., Aburatani H., Bayes M., Botwell D.D., Campbell P.J., Estivill X., et al. International network of cancer genome projects. Nature 2010, 464:993-998.
3. Kan Z., Jaiswal B.S., Stinson J., Janakiraman V., Bhatt D., Stern H.M., Yue P., Haverty P.M., Bourgon R., Zheng J., Moorhead M., Chaudhuri S., Tomsho L.P., Peters B.A., Pujara K., Cordes S., Davis D.P., Carlton V.E., Yuan W., Li L., Wang W., Eigenbrot C., Kaminker J.S., Eberhard D.A., Waring P., Schuster S.C., Modrusan Z., Zhang Z., Stokoe D., de Sauvage F.J., Faham M., Seshagiri S. Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 2010, 466:869-873.
4. Shah S.P., Roth A., Goya R., Oloumi A., Ha G., Zhao Y., Turashvili G., Ding J., Tse K., Haffari G., Bashashati A., Prentice L.M., Khattra J., Burleigh A., Yap D., Bernard V., McPherson A., Shumansky K., Crisan A., Giuliany R., Heravi-Moussavi A., Rosner J., Lai D., Birol I., Varhol R., Tam A., Dhalla N., Zeng T., Ma K., Chan S.K., Griffith M., Moradian A., Cheng S.W., Morin G.B., Watson P., Gelmon K., Chia S., Chin S.F., Curtis C., Rueda O.M., Pharoah P.D., Damaraju S., Mackey J., Hoon K., Harkins T., Tadigotla V., Sigaroudinia M., Gascard P., Tlsty T., Costello J.F., Meyer I.M., Eaves C.J., Wasserman W.W., Jones S., Huntsman D., Hirst M., Caldas C., Marra M.A., Aparicio S. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 2012, 486:395-399.
5. The Cancer Genome Atlas. Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70.
6. Stephens P.J., Tarpey P.S., Davies H., Van Loo P., Greenman C., Wedge D.C., Nik-Zainal S., Martin S., Varela I., Bignell G.R., Yates L.R., Papaemmanuil E., Beare D., Butler A., Cheverton A., Gamble J., Hinton J., Jia M., Jayakumar A., Jones D., Latimer C., Lau K.W., McLaren S., McBride D.J., Menzies A., Mudie L., Raine K., Rad R., Chapman M.S., Teague J., Easton D., Langerod A., Lee M.T., Shen C.Y., Tee B.T., Huimin B.W., Broeks A., Vargas A.C., Turashvili G., Martens J., Fatima A., Miron P., Chin S.F., Thomas G., Boyault S., Mariani O., Lakhani S.R., van de Vijver M., van 't Veer L., Foekens J., Desmedt C., Sotiriou C., Tutt A., Caldas C., Reis-Filho J.S., Aparicio S.A., Salomon A.V., Borresen-Dale A.L., Richardson A.L., Campbell P.J., Futreal P.A., Stratton M.R. The landscape of cancer genes and mutational processes in breast cancer. Nature 2012, 486:400-404.
7. Navin N., Kendall J., Troge J., Andrews P., Rodgers L., McIndoo J., Cook K., Stepansky A., Levy D., Esposito D., Muthuswamy L., Krasnitz A., McCombie W.R., Hicks J., Wigler M. Tumour evolution inferred by single-cell sequencing. Nature 2011, 472:90-94.
8. Nik-Zainal S., Van Loo P., Wedge D.C., Alexandrov L.B., Greenman C.D., Lau K.W., Raine K., Jones D., Marshall J., Ramakrishna M., Shlien A., Cooke S.L., Hinton J., Menzies A., Stebbings L.A., Leroy C., Jia M., Rance R., Mudie L.J., Gamble S.J., Stephens P.J., McLaren S., Tarpey P.S., Papaemmanuil E., Davies H.R., Varela I., McBride D.J., Bignell G.R., Leung K., Butler A.P., Teague J.W., Martin S., Jonsson G., Mariani O., Boyault S., Miron P., Fatima A., Langerod A., Aparicio S.A., Tutt A., Sieuwerts A.M., Borg A., Thomas G., Salomon A.V., Richardson A.L., Borresen-Dale A.L., Futreal P.A., Stratton M.R., Campbell P.J. The life history of 21 breast cancers. Cell 2012, 149:994-1007.
9. Ding L., Ellis M.J., Li S., Larson D.E., Chen K., Wallis J.W., Harris C.C., McLellan M.D., Fulton R.S., Fulton L.L., Abbott R.M., Hoog J., Dooling D.J., Koboldt D.C., Schmidt H., Kalicki J., Zhang Q., Chen L., Lin L., Wendl M.C., McMichael J.F., Magrini V.J., Cook L., McGrath S.D., Vickery T.L., Appelbaum E., Deschryver K., Davies S., Guintoli T., Lin L., Crowder R., Tao Y., Snider J.E., Smith S.M., Dukes A.F., Sanderson G.E., Pohl C.S., Delehaunty K.D., Fronick C.C., Pape K.A., Reed J.S., Robinson J.S., Hodges J.S., Schierding W., Dees N.D., Shen D., Locke D.P., Wiechert M.E., Eldred J.M., Peck J.B., Oberkfell B.J., Lolofie J.T., Du F., Hawkins A.E., O'Laughlin M.D., Bernard K.E., Cunningham M., Elliott G., Mason M.D., Thompson D.M., Ivanovich J.L., Goodfellow P.J., Perou C.M., Weinstock G.M., Aft R., Watson M., Ley T.J., Wilson R.K., Mardis E.R. Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 2010, 464:999-1005.
10. Shah S.P., Morin R.D., Khattra J., Prentice L., Pugh T., Burleigh A., Delaney A., Gelmon K., Guliany R., Senz J., Steidl C., Holt R.A., Jones S., Sun M., Leung G., Moore R., Severson T., Taylor G.A., Teschendorff A.E., Tse K., Turashvili G., Varhol R., Warren R.L., Watson P., Zhao Y., Caldas C., Huntsman D., Hirst M., Marra M.A., Aparicio S. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 2009, 461:809-813.
11. Turke A.B., Zejnullahu K., Wu Y.L., Song Y., Dias-Santagata D., Lifshits E., Toschi L., Rogers A., Mok T., Sequist L., Lindeman N.I., Murphy C., Akhavanfard S., Yeap B.Y., Xiao Y., Capelletti M., Iafrate A.J., Lee C., Christensen J.G., Engelman J.A., Janne P.A. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010, 17:77-88.
12. Misale S., Yaeger R., Hobor S., Scala E., Janakiraman M., Liska D., Valtorta E., Schiavo R., Buscarino M., Siravegna G., Bencardino K., Cercek A., Chen C.T., Veronese S., Zanon C., Sartore-Bianchi A., Gambacorta M., Gallicchio M., Vakiani E., Boscaro V., Medico E., Weiser M., Siena S., Di Nicolantonio F., Solit D., Bardelli A. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature 2012, 486:532-536.
13. Ellis M.J., Ding L., Shen D., Luo J., Suman V.J., Wallis J.W., Van Tine B.A., Hoog J., Goiffon R.J., Goldstein T.C., Ng S., Lin L., Crowder R., Snider J., Ballman K., Weber J., Chen K., Koboldt D.C., Kandoth C., Schierding W.S., McMichael J.F., Miller C.A., Lu C., Harris C.C., McLellan M.D., Wendl M.C., DeSchryver K., Allred D.C., Esserman L., Unzeitig G., Margenthaler J., Babiera G.V., Marcom P.K., Guenther J.M., Leitch M., Hunt K., Olson J., Tao Y., Maher C.A., Fulton L.L., Fulton R.S., Harrison M., Oberkfell B., Du F., Demeter R., Vickery T.L., Elhammali A., Piwnica-Worms H., McDonald S., Watson M., Dooling D.J., Ota D., Chang L.W., Bose R., Ley T.J., Piwnica-Worms D., Stuart J.M., Wilson R.K., Mardis E.R. Whole-genome analysis informs breast cancer response to aromatase inhibition. Nature 2012, 486:353-360.
14. Diaz L.A., Williams R.T., Wu J., Kinde I., Hecht J.R., Berlin J., Allen B., Bozic I., Reiter J.G., Nowak M.A., Kinzler K.W., Oliner K.S., Vogelstein B. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 2012, 486:537-540.
15. Bissell M.J. The differentiated state of normal and malignant cells or how to define a "normal" cell in culture. Int. Rev. Cytol. 1981, 70:27-100.
16. Teschendorff A.E., Miremadi A., Pinder S.E., Ellis I.O., Caldas C. An immune response gene expression module identifies a good prognosis subtype in estrogen receptor negative breast cancer. Genome Biol. 2007, 8:R157.
17. Denkert C., Loibl S., Noske A., Roller M., Muller B.M., Komor M., Budczies J., Darb-Esfahani S., Kronenwett R., Hanusch C., von Torne C., Weichert W., Engels K., Solbach C., Schrader I., Dietel M., von Minckwitz G. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J. Clin. Oncol. 2010, 28:105-113.
18. Mahmoud S.M., Paish E.C., Powe D.G., Macmillan R.D., Grainge M.J., Lee A.H., Ellis I.O., Green A.R. Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. J. Clin. Oncol. 2011, 29:1949-1955.
19. Loi S., Sirtaine N., Piette F., Salgado R., Viale G., Van Eenoo F., Rouas G., Francis P., Crown J.P., Hitre E., de Azambuja E., Quinaux E., Di Leo A., Michiels S., Piccart M.J., Sotiriou C. Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02-98. J. Clin. Oncol. 2013, 31:860-867.
20. Ronnov-Jessen L., Petersen O.W., Bissell M.J. Cellular changes involved in conversion of normal to malignant breast: importance of the stromal reaction. Physiol. Rev. 1996, 76:69-125.
21. Gusterson B.A., Warburton M.J., Mitchell D., Ellison M., Neville A.M., Rudland P.S. Distribution of myoepithelial cells and basement membrane proteins in the normal breast and in benign and malignant breast diseases. Cancer Res. 1982, 42:4763-4770.
22. Shekhar M.P., Pauley R., Heppner G. Host microenvironment in breast cancer development: extracellular matrix-stromal cell contribution to neoplastic phenotype of epithelial cells in the breast. Breast Cancer Res. 2003, 5:130-135.
23. Lewis C.E., Pollard J.W. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006, 66:605-612.
24. de Visser K.E., Eichten A., Coussens L.M. Paradoxical roles of the immune system during cancer development. Nat. Rev. Cancer 2006, 6:24-37.
25. Elsdale T., Bard J. Collagen substrata for studies on cell behavior. J. Cell Biol. 1972, 54:626-637.
26. Emerman J.T., Bartley J.C., Bissell M.J. Glucose metabolite patterns as markers of functional differentiation in freshly isolated and cultured mouse mammary epithelial cells. Exp. Cell Res. 1981, 134:241-250.
27. Emerman J.T., Pitelka D.R. Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes. In Vitro 1977, 13:316-328.
28. Michalopoulos G., Pitot H.C. Primary culture of parenchymal liver cells on collagen membranes. Morphological and biochemical observations. Exp. Cell Res. 1975, 94:70-78.
29. Lee E.Y., Lee W.H., Kaetzel C.S., Parry G., Bissell M.J. Interaction of mouse mammary epithelial cells with collagen substrata: regulation of casein gene expression and secretion. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:1419-1423.
30. Parry G., Lee E.Y., Farson D., Koval M., Bissell M.J. Collagenous substrata regulate the nature and distribution of glycosaminoglycans produced by differentiated cultures of mouse mammary epithelial cells. Exp. Cell Res. 1985, 156:487-499.
31. Streuli C.H., Bissell M.J. Expression of extracellular matrix components is regulated by substratum. J. Cell Biol. 1990, 110:1405-1415.
32. Boudreau N., Myers C., Bissell M.J. From laminin to lamin: regulation of tissue-specific gene expression by the ECM. Trends Cell Biol. 1995, 5:1-4.
33. Bosman F.T., Stamenkovic I. Functional structure and composition of the extracellular matrix. J. Pathol. 2003, 200:423-428.
34. Yurchenco P.D. Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb. Perspect. Biol. 2011, 3.
35. Bissell M.J., Hall H.G., Parry G. How does the extracellular matrix direct gene expression?. J. Theor. Biol. 1982, 99:31-68.
36. Orkin R.W., Gehron P., McGoodwin E.B., Martin G.R., Valentine T., Swarm R. A murine tumor producing a matrix of basement membrane. J. Exp. Med. 1977, 145:204-220.
37. Medina D., Li M.L., Oborn C.J., Bissell M.J. Casein gene expression in mouse mammary epithelial cell lines: dependence upon extracellular matrix and cell type. Exp. Cell Res. 1987, 172:192-203.
38. Li M.L., Aggeler J., Farson D.A., Hatier C., Hassell J., Bissell M.J. Influence of a reconstituted basement membrane and its components on casein gene expression and secretion in mouse mammary epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:136-140.
39. Barcellos-Hoff M.H., Aggeler J., Ram T.G., Bissell M.J. Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development 1989, 105:223-235.
40. Petersen O.W., Ronnov-Jessen L., Howlett A.R., Bissell M.J. 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, 89:9064-9068.
41. Bissell M.J., Hines W.C. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 2011, 17:320-329.
42. Kleinman H.K., McGarvey M.L., Liotta L.A., Robey P.G., Tryggvason K., Martin G.R. Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 1982, 21:6188-6193.
43. Vukicevic S., Kleinman H.K., Luyten F.P., Roberts A.B., Roche N.S., Reddi A.H. Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components. Exp. Cell Res. 1992, 202:1-8.
44. Alcaraz J., Xu R., Mori H., Nelson C.M., Mroue R., Spencer V.A., Brownfield D., Radisky D.C., Bustamante C., Bissell M.J. Laminin and biomimetic extracellular elasticity enhance functional differentiation in mammary epithelia. EMBO J. 2008, 27:2829-2838.
45. Lelievre S.A., Weaver V.M., Nickerson J.A., Larabell C.A., Bhaumik A., Petersen O.W., Bissell M.J. 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, 95:14711-14716.
46. Debnath J., Muthuswamy S.K., Brugge J.S. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003, 30:256-268.
47. Lee G.Y., Kenny P.A., Lee E.H., Bissell M.J. Three-dimensional culture models of normal and malignant breast epithelial cells. Nat. Methods 2007, 4:359-365.
48. Debnath J., Brugge J.S. Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer 2005, 5:675-688.
49. Kenny P.A., Lee G.Y., Myers C.A., Neve R.M., Semeiks J.R., Spellman P.T., Lorenz K., Lee E.H., Barcellos-Hoff M.H., Petersen O.W., Gray J.W., Bissell M.J. The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression. Mol. Oncol. 2007, 1:84-96.
50. Weigelt B., Bissell M.J. Unraveling the microenvironmental influences on the normal mammary gland and breast cancer. Semin. Cancer Biol. 2008, 18:311-321.
51. Beliveau A., Mott J.D., Lo A., Chen E.I., Koller A.A., Yaswen P., Muschler J., Bissell M.J. Raf-induced MMP9 disrupts tissue architecture of human breast cells in three-dimensional culture and is necessary for tumor growth in vivo. Genes Dev. 2010, 24:2800-2811.
52. Soman P., Kelber J.A., Lee J.W., Wright T.N., Vecchio K.S., Klemke R.L., Chen S. Cancer cell migration within 3D layer-by-layer microfabricated photocrosslinked PEG scaffolds with tunable stiffness. Biomaterials 2012, 33:7064-7070.
53. Roskelley C.D., Desprez P.Y., Bissell M.J. Extracellular matrix-dependent tissue-specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:12378-12382.
54. Wozniak M.A., Desai R., Solski P.A., Der C.J., Keely P.J. ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J. Cell Biol. 2003, 163:583-595.
55. Paszek M.J., Zahir N., Johnson K.R., Lakins J.N., Rozenberg G.I., Gefen A., Reinhart-King C.A., Margulies S.S., Dembo M., Boettiger D., Hammer D.A., Weaver V.M. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8:241-254.
56. Provenzano P.P., Inman D.R., Eliceiri K.W., Keely P.J. Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 2009, 28:4326-4343.
57. Shin S.I., Freedman V.H., Risser R., Pollack R. Tumorigenicity of virus-transformed cells in nude mice is correlated specifically with anchorage independent growth in vitro. Proc. Natl. Acad. Sci. U.S.A. 1975, 72:4435-4439.
58. Vinci M., Gowan S., Boxall F., Patterson L., Zimmermann M., Court W., Lomas C., Mendiola M., Hardisson D., Eccles S.A. Advances in establishment and analysis of three-dimensional tumor spheroid-based functional assays for target validation and drug evaluation. BMC Biol. 2012, 10:29.
59. Nelson C.M., Bissell M.J. Modeling dynamic reciprocity: engineering three-dimensional culture models of breast architecture, function, and neoplastic transformation. Semin. Cancer Biol. 2005, 15:342-352.
60. Griffith L.G., Swartz M.A. Capturing complex 3D tissue physiology in vitro. Nat. Rev. Mol. Cell Biol. 2006, 7:211-224.
61. Huh D., Hamilton G.A., Ingber D.E. From 3D cell culture to organs-on-chips. Trends Cell Biol. 2011, 21:745-754.
62. Nyga A., Cheema U., Loizidou M. 3D tumour models: novel in vitro approaches to cancer studies. J. Cell Commun. Signal. 2011, 5:239-248.
63. Tibbitt M.W., Anseth K.S. Dynamic microenvironments: the fourth dimension. Sci. Transl. Med. 2012, 4:160ps124.
64. Williams S.A., Anderson W.C., Santaguida M.T., Dylla S.J. Patient-derived xenografts, the cancer stem cell paradigm, and cancer pathobiology in the 21st century. Lab. Invest. 2013, 93:970-982.
65. Tentler J.J., Tan A.C., Weekes C.D., Jimeno A., Leong S., Pitts T.M., Arcaroli J.J., Messersmith W.A., Eckhardt S.G. Patient-derived tumour xenografts as models for oncology drug development. Nat. Rev. Clin. Oncol. 2012, 9:338-350.
66. Sato T., Stange D.E., Ferrante M., Vries R.G., Van Es J.H., Van den Brink S., Van Houdt W.J., Pronk A., Van Gorp J., Siersema P.D., Clevers H. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 2011, 141:1762-1772.
67. DeRose Y.S., Gligorich K.M., Wang G., Georgelas A., Bowman P., Courdy S.J., Welm A.L., Welm B.E. Patient-derived models of human breast cancer: protocols for in vitro and in vivo applications in tumor biology and translational medicine. Curr. Protoc. Pharmacol. 2013, 23. (Chapter 14, Unit14).
68. Marangoni E., Vincent-Salomon A., Auger N., Degeorges A., Assayag F., de Cremoux P., de Plater L., Guyader C., De Pinieux G., Judde J.G., Rebucci M., Tran-Perennou C., Sastre-Garau X., Sigal-Zafrani B., Delattre O., Dieras V., Poupon M.F. A new model of patient tumor-derived breast cancer xenografts for preclinical assays. Clin. Cancer Res. 2007, 13:3989-3998.
69. Cottu P., Marangoni E., Assayag F., de Cremoux P., Vincent-Salomon A., Guyader C., de Plater L., Elbaz C., Karboul N., Fontaine J.J., Chateau-Joubert S., Boudou-Rouquette P., Alran S., Dangles-Marie V., Gentien D., Poupon M.F., Decaudin D. Modeling of response to endocrine therapy in a panel of human luminal breast cancer xenografts. Breast Cancer Res. Treat. 2012, 133:595-606.
70. Gray J. Cancer: genomics of metastasis. Nature 2010, 464:989-990.
71. Radisky D., Hagios C., Bissell M.J. Tumors are unique organs defined by abnormal signaling and context. Semin. Cancer Biol. 2001, 11:87-95.
72. Cunha G.R., Hom Y.K. Role of mesenchymal-epithelial interactions in mammary gland development. J. Mammary Gland Biol. Neoplasia 1996, 1:21-35.
73. Gudjonsson T., Ronnov-Jessen L., Villadsen R., Rank F., Bissell M.J., Petersen O.W. Normal and tumor-derived myoepithelial cells differ in their ability to interact with luminal breast epithelial cells for polarity and basement membrane deposition. J. Cell Sci. 2002, 115:39-50.
74. Ronnov-Jessen L., Petersen O.W., Koteliansky V.E., Bissell M.J. The origin of the myofibroblasts in breast cancer. Recapitulation of tumor environment in culture unravels diversity and implicates converted fibroblasts and recruited smooth muscle cells. J. Clin. Invest. 1995, 95:859-873.
75. Elenbaas B., Weinberg R.A. Heterotypic signaling between epithelial tumor cells and fibroblasts in carcinoma formation. Exp. Cell Res. 2001, 264:169-184.
76. Kalluri R., Zeisberg M. Fibroblasts in cancer. Nat. Rev. Cancer 2006, 6:392-401.
77. Mukhtar R.A., Nseyo O., Campbell M.J., Esserman L.J. Tumor-associated macrophages in breast cancer as potential biomarkers for new treatments and diagnostics. Expert. Rev. Mol. Diagn. 2011, 11:91-100.
78. Ruffell B., Au A., Rugo H.S., Esserman L.J., Hwang E.S., Coussens L.M. Leukocyte composition of human breast cancer. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:2796-2801.
79. Shaw K.R., Wrobel C.N., Brugge J.S. Use of three-dimensional basement membrane cultures to model oncogene-induced changes in mammary epithelial morphogenesis. J. Mammary Gland Biol. Neoplasia 2004, 9:297-310.
80. Xu K., Buchsbaum R.J. Isolation of mammary epithelial cells from three-dimensional mixed-cell spheroid co-culture. J. Vis. Exp. 2012, 62. pii:3760.
81. Ghajar C.M., Peinado H., Mori H., Matei I.R., Evason K.J., Brazier H., Almeida D., Koller A., Hajjar K.A., Stainier D.Y., Chen E.I., Lyden D., Bissell M.J. The perivascular niche regulates breast tumour dormancy. Nat. Cell Biol. 2013, 15:807-817.
82. Noel A., Munaut C., Boulvain A., Calberg-Bacq C.M., Lambert C.A., Nusgens B., Lapiere C.M., Foidart J.M. Modulation of collagen and fibronectin synthesis in fibroblasts by normal and malignant cells. J. Cell. Biochem. 1992, 48:150-161.
83. Seidl P., Huettinger R., Knuechel R., Kunz-Schughart L.A. Three-dimensional fibroblast-tumor cell interaction causes downregulation of RACK1 mRNA expression in breast cancer cells in vitro. Int. J. Cancer 2002, 102:129-136.
84. Martinez-Outschoorn U.E., Pavlides S., Whitaker-Menezes D., Daumer K.M., Milliman J.N., Chiavarina B., Migneco G., Witkiewicz A.K., Martinez-Cantarin M.P., Flomenberg N., Howell A., Pestell R.G., Lisanti M.P., Sotgia F. Tumor cells induce the cancer associated fibroblast phenotype via caveolin-1 degradation: implications for breast cancer and DCIS therapy with autophagy inhibitors. Cell Cycle 2010, 9:2423-2433.
85. Olsen C.J., Moreira J., Lukanidin E.M., Ambartsumian N.S. Human mammary fibroblasts stimulate invasion of breast cancer cells in a three-dimensional culture and increase stroma development in mouse xenografts. BMC Cancer 2010, 10:444.
86. Kaur P., Ward B., Saha B., Young L., Groshen S., Techy G., Lu Y., Atkinson R., Taylor C.R., Ingram M., Imam S.A. Human breast cancer histoid: an in vitro 3-dimensional co-culture model that mimics breast cancer tissue. J. Histochem. Cytochem. 2011, 59:1087-1100.
87. Voronov E., Shouval D.S., Krelin Y., Cagnano E., Benharroch D., Iwakura Y., Dinarello C.A., Apte R.N. IL-1 is required for tumor invasiveness and angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:2645-2650.
88. Hou Z., Falcone D.J., Subbaramaiah K., Dannenberg A.J. Macrophages induce COX-2 expression in breast cancer cells: role of IL-1beta autoamplification. Carcinogenesis 2011, 32:695-702.
89. Huss F.R., Kratz G. Mammary epithelial cell and adipocyte co-culture in a 3-D matrix: the first step towards tissue-engineered human breast tissue. Cells Tissues Organs 2001, 169:361-367.
90. Manabe Y., Toda S., Miyazaki K., Sugihara H. Mature adipocytes, but not preadipocytes, promote the growth of breast carcinoma cells in collagen gel matrix culture through cancer-stromal cell interactions. J. Pathol. 2003, 201:221-228.
91. Salameh T.S., Le T.T., Nichols M.B., Bauer E., Cheng J., Camarillo I.G. An ex vivo co-culture model system to evaluate stromal-epithelial interactions in breast cancer. Int. J. Cancer 2013, 132:288-296.
92. Chottanapund S., Van Duursen M.B., Navasumrit P., Hunsonti P., Timtavorn S., Ruchirawat M., Van den Berg M. Effect of androgens on different breast cancer cells co-cultured with or without breast adipose fibroblasts. J. Steroid Biochem. Mol. Biol. 2013, 138C:54-62.
93. Rozenchan P.B., Carraro D.M., Brentani H., de Carvalho Mota L.D., Bastos E.P., e Ferreira E.N., Torres C.H., Katayama M.L., Roela R.A., Lyra E.C., Soares F.A., Folgueira M.A., Goes J.C., Brentani M.M. Reciprocal changes in gene expression profiles of cocultured breast epithelial cells and primary fibroblasts. Int. J. Cancer 2009, 125:2767-2777.
94. Santos R.P., Benvenuti T.T., Honda S.T., Del Valle P.R., Katayama M.L., Brentani H.P., Carraro D.M., Rozenchan P.B., Brentani M.M., de Lyra E.C., Torres C.H., Salzgeber M.B., Kaiano J.H., Goes J.C., Folgueira M.A. Influence of the interaction between nodal fibroblast and breast cancer cells on gene expression. Tumour Biol. 2011, 32:145-157.
95. Straussman R., Morikawa T., Shee K., Barzily-Rokni M., Qian Z.R., Du J., Davis A., Mongare M.M., Gould J., Frederick D.T., Cooper Z.A., Chapman P.B., Solit D.B., Ribas A., Lo R.S., Flaherty K.T., Ogino S., Wargo J.A., Golub T.R. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012, 487:500-504.
96. Wang X., Sun L., Maffini M.V., Soto A., Sonnenschein C., Kaplan D.L. A complex 3D human tissue culture system based on mammary stromal cells and silk scaffolds for modeling breast morphogenesis and function. Biomaterials 2010, 31:3920-3929.
97. Yang C.C., Burg K.J. Designing a tunable 3D heterocellular breast cancer tissue test system. J. Tissue Eng. Regen. Med. 2013, (Epub ahead of print).
98. Kaji H., Camci-Unal G., Langer R., Khademhosseini A. Engineering systems for the generation of patterned co-cultures for controlling cell-cell interactions. Biochim. Biophys. Acta 2011, 1810:239-250.
99. Briand P., Nielsen K.V., Madsen M.W., Petersen O.W. Trisomy 7p and malignant transformation of human breast epithelial cells following epidermal growth factor withdrawal. Cancer Res. 1996, 56:2039-2044.
100. Weaver V.M., Petersen O.W., Wang F., Larabell C.A., Briand P., Damsky C., Bissell M.J. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J. Cell Biol. 1997, 137:231-245.
101. Bissell M.J., Kenny P.A., Radisky D.C. Microenvironmental regulators of tissue structure and function also regulate tumor induction and progression: the role of extracellular matrix and its degrading enzymes. Cold Spring Harb. Symp. Quant. Biol. 2005, 70:343-356.
102. Wang F., Weaver V.M., Petersen O.W., Larabell C.A., Dedhar S., Briand P., Lupu R., Bissell M.J. Reciprocal interactions between beta1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: a different perspective in epithelial biology. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:14821-14826.
103. Wang F., Hansen R.K., Radisky D., Yoneda T., Barcellos-Hoff M.H., Petersen O.W., Turley E.A., Bissell M.J. Phenotypic reversion or death of cancer cells by altering signaling pathways in three-dimensional contexts. J. Natl. Cancer Inst. 2002, 94:1494-1503.
104. Liu H., Radisky D.C., Wang F., Bissell M.J. Polarity and proliferation are controlled by distinct signaling pathways downstream of PI3-kinase in breast epithelial tumor cells. J. Cell Biol. 2004, 164:603-612.
105. Bissell M.J., Rizki A., Mian I.S. Tissue architecture: the ultimate regulator of breast epithelial function. Curr. Opin. Cell Biol. 2003, 15:753-762.
106. Weaver V.M., Lelievre S., Lakins J.N., Chrenek M.A., Jones J.C., Giancotti F., Werb Z., Bissell M.J. beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2002, 2:205-216.
107. Park C.C., Zhang H., Pallavicini M., Gray J.W., Baehner F., Park C.J., Bissell M.J. Beta1 integrin inhibitory antibody induces apoptosis of breast cancer cells, inhibits growth, and distinguishes malignant from normal phenotype in three dimensional cultures and in vivo. Cancer Res. 2006, 66:1526-1535.
108. Park C.C., Zhang H.J., Yao E.S., Park C.J., Bissell M.J. Beta1 integrin inhibition dramatically enhances radiotherapy efficacy in human breast cancer xenografts. Cancer Res. 2008, 68:4398-4405.
109. Barkan D., Chambers A.F. beta1-integrin: a potential therapeutic target in the battle against cancer recurrence. Clin. Cancer Res. 2011, 17:7219-7223.
110. Lee S.Y., Meier R., Furuta S., Lenburg M.E., Kenny P.A., Xu R., Bissell M.J. FAM83A confers EGFR-TKI resistance in breast cancer cells and in mice. J. Clin. Invest. 2012, 122:3211-3220.
111. Muthuswamy S.K., Li D., Lelievre S., Bissell M.J., Brugge J.S. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat. Cell Biol. 2001, 3:785-792.
112. Spancake K.M., Anderson C.B., Weaver V.M., Matsunami N., Bissell M.J., White R.L. E7-transduced human breast epithelial cells show partial differentiation in three-dimensional culture. Cancer Res. 1999, 59:6042-6045.
113. Debnath J., Walker S.J., Brugge J.S. Akt activation disrupts mammary acinar architecture and enhances proliferation in an mTOR-dependent manner. J. Cell Biol. 2003, 163:315-326.
114. Wrobel C.N., Debnath J., Lin E., Beausoleil S., Roussel M.F., Brugge J.S. Autocrine CSF-1R activation promotes Src-dependent disruption of mammary epithelial architecture. J. Cell Biol. 2004, 165:263-273.
115. Lott S.T., Chen N., Chandler D.S., Yang Q., Wang L., Rodriguez M., Xie H., Balasenthil S., Buchholz T.A., Sahin A.A., Chaung K., Zhang B., Olufemi S.E., Chen J., Adams H., Band V., El-Naggar A.K., Frazier M.L., Keyomarsi K., Hunt K.K., Sen S., Haffty B., Hewitt S.M., Krahe R., Killary A.M. DEAR1 is a dominant regulator of acinar morphogenesis and an independent predictor of local recurrence-free survival in early-onset breast cancer. PLoS Med. 2009, 6:e1000068.
116. Worster D.T., Schmelzle T., Solimini N.L., Lightcap E.S., Millard B., Mills G.B., Brugge J.S., Albeck J.G. Akt and ERK control the proliferative response of mammary epithelial cells to the growth factors IGF-1 and EGF through the cell cycle inhibitor p57Kip2. Sci. Signal. 2012, 5:ra19.
117. Leslie K., Gao S.P., Berishaj M., Podsypanina K., Ho H., Ivashkiv L., Bromberg J. Differential interleukin-6/Stat3 signaling as a function of cellular context mediates Ras-induced transformation. Breast Cancer Res. 2010, 12:R80.
118. Pickl M., Ries C.H. Comparison of 3D and 2D tumor models reveals enhanced HER2 activation in 3D associated with an increased response to trastuzumab. Oncogene 2009, 28:461-468.
119. Weigelt B., Lo A.T., Park C.C., Gray J.W., Bissell M.J. HER2 signaling pathway activation and response of breast cancer cells to HER2-targeting agents is dependent strongly on the 3D microenvironment. Breast Cancer Res. Treat. 2010, 122:35-43.
120. Barretina J., Caponigro G., Stransky N., Venkatesan K., Margolin A.A., Kim S., Wilson C.J., Lehar J., Kryukov G.V., Sonkin D., Reddy A., Liu M., Murray L., Berger M.F., Monahan J.E., Morais P., Meltzer J., Korejwa A., Jane-Valbuena J., Mapa F.A., Thibault J., Bric-Furlong E., Raman P., Shipway A., Engels I.H., Cheng J., Yu G.K., Yu J., Aspesi P., de Silva M., Jagtap K., Jones M.D., Wang L., Hatton C., Palescandolo E., Gupta S., Mahan S., Sougnez C., Onofrio R.C., Liefeld T., MacConaill L., Winckler W., Reich M., Li N., Mesirov J.P., Gabriel S.B., Getz G., Ardlie K., Chan V., Myer V.E., Weber B.L., Porter J., Warmuth M., Finan P., Harris J.L., Meyerson M., Golub T.R., Morrissey M.P., Sellers W.R., Schlegel R., Garraway L.A. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012, 483:603-607.
121. Garnett M.J., Edelman E.J., Heidorn S.J., Greenman C.D., Dastur A., Lau K.W., Greninger P., Thompson I.R., Luo X., Soares J., Liu Q., Iorio F., Surdez D., Chen L., Milano R.J., Bignell G.R., Tam A.T., Davies H., Stevenson J.A., Barthorpe S., Lutz S.R., Kogera F., Lawrence K., McLaren-Douglas A., Mitropoulos X., Mironenko T., Thi H., Richardson L., Zhou W., Jewitt F., Zhang T., O'Brien P., Boisvert J.L., Price S., Hur W., Yang W., Deng X., Butler A., Choi H.G., Chang J.W., Baselga J., Stamenkovic I., Engelman J.A., Sharma S.V., Delattre O., Saez-Rodriguez J., Gray N.S., Settleman J., Futreal P.A., Haber D.A., Stratton M.R., Ramaswamy S., McDermott U., Benes C.H. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 2012, 483:570-575.
122. Yang W., Soares J., Greninger P., Edelman E.J., Lightfoot H., Forbes S., Bindal N., Beare D., Smith J.A., Thompson I.R., Ramaswamy S., Futreal P.A., Haber D.A., Stratton M.R., Benes C., McDermott U., Garnett M.J. Genomics of Drug Sensitivity in Cancer (GDSC): a resource for therapeutic biomarker discovery in cancer cells. Nucleic Acids Res. 2013, 41:D955-D961.
123. Farmer H., McCabe N., Lord C.J., Tutt A.N., Johnson D.A., Richardson T.B., Santarosa M., Dillon K.J., Hickson I., Knights C., Martin N.M., Jackson S.P., Smith G.C., Ashworth A. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434:917-921.
124. McDermott U., Sharma S.V., Dowell L., Greninger P., Montagut C., Lamb J., Archibald H., Raudales R., Tam A., Lee D., Rothenberg S.M., Supko J.G., Sordella R., Ulkus L.E., Iafrate A.J., Maheswaran S., Njauw C.N., Tsao H., Drew L., Hanke J.H., Ma X.J., Erlander M.G., Gray N.S., Haber D.A., Settleman J. Identification of genotype-correlated sensitivity to selective kinase inhibitors by using high-throughput tumor cell line profiling. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:19936-19941.
125. McDermott U., Iafrate A.J., Gray N.S., Shioda T., Classon M., Maheswaran S., Zhou W., Choi H.G., Smith S.L., Dowell L., Ulkus L.E., Kuhlmann G., Greninger P., Christensen J.G., Haber D.A., Settleman J. Genomic alterations of anaplastic lymphoma kinase may sensitize tumors to anaplastic lymphoma kinase inhibitors. Cancer Res. 2008, 68:3389-3395.
126. Fournier M.V., Martin K.J., Kenny P.A., Xhaja K., Bosch I., Yaswen P., Bissell M.J. Gene expression signature in organized and growth-arrested mammary acini predicts good outcome in breast cancer. Cancer Res. 2006, 66:7095-7102.
127. Martin K.J., Patrick D.R., Bissell M.J., Fournier M.V. Prognostic breast cancer signature identified from 3D culture model accurately predicts clinical outcome across independent datasets. PLoS One 2008, 3:e2994.
128. Correia A.L., Bissell M.J. The tumor microenvironment is a dominant force in multidrug resistance. Drug Resist. Updat. 2012, 15:39-49.
129. Li X., Zhang X., Zhao S., Wang J., Liu G., Du Y. Micro-scaffold array chip for upgrading cell-based high-throughput drug testing to 3D using benchtop equipment. Lab Chip 2014, 14:471-481.
130. Lei Y., Schaffer D.V. A fully defined and scalable 3D culture system for human pluripotent stem cell expansion and differentiation. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:E5039-E5048.
131. Datta P., Meli L., Li L., Migliore N., Schaefer E., Sharfstein S.T., Dordick J.S., Linhardt R.J. Microarray platform affords improved product analysis in mammalian cell growth studies. Biotechnol. J. 2013, (Epub ahead of print).
132. Timm D.M., Chen J., Sing D., Gage J.A., Haisler W.L., Neeley S.K., Raphael R.M., Dehghani M., Rosenblatt K.P., Killian T.C., Tseng H., Souza G.R. A high-throughput three-dimensional cell migration assay for toxicity screening with mobile device-based macroscopic image analysis. Sci. Rep. 2013, 3:3000.
133. Rimann M., Angres B., Patocchi-Tenzer I., Braum S., Graf-Hausner U. Automation of 3D cell culture using chemically defined hydrogels. J. Lab. Autom. 2013, (Epub ahead of print).
134. Simon K.A., Park K.M., Mosadegh B., Subramaniam A.B., Mazzeo A.D., Ngo P.M., Whitesides G.M. Polymer-based mesh as supports for multi-layered 3D cell culture and assays. Biomaterials 2014, 35:259-268.
135. Lee M.Y., Kumar R.A., Sukumaran S.M., Hogg M.G., Clark D.S., Dordick J.S. Three-dimensional cellular microarray for high-throughput toxicology assays. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:59-63.
136. Rimann M., Graf-Hausner U. Synthetic 3D multicellular systems for drug development. Curr. Opin. Biotechnol. 2012, 23:803-809.
137. Burgstaller G., Oehrle B., Koch I., Lindner M., Eickelberg O. Multiplex profiling of cellular invasion in 3D cell culture models. PLoS One 2013, 8:e63121.
138. Zhou Y., Arai T., Horiguchi Y., Ino K., Matsue T., Shiku H. Multiparameter analyses of three-dimensionally cultured tumor spheroids based on respiratory activity and comprehensive gene expression profiles. Anal. Biochem. 2013, 439:187-193.
139. Xu Z., Gao Y., Hao Y., Li E., Wang Y., Zhang J., Wang W., Gao Z., Wang Q. Application of a microfluidic chip-based 3D co-culture to test drug sensitivity for individualized treatment of lung cancer. Biomaterials 2013, 34:4109-4117.
140. Thoma C.R., Stroebel S., Rosch N., Calpe B., Krek W., Kelm J.M. A high-throughput-compatible 3D microtissue co-culture system for phenotypic RNAi screening applications. J. Biomol. Screen. 2013, 18:1330-1337.
141. Deiss F., Mazzeo A., Hong E., Ingber D.E., Derda R., Whitesides G.M. Platform for high-throughput testing of the effect of soluble compounds on 3D cell cultures. Anal. Chem. 2013, 85:8085-8094.
142. Hongisto V., Jernstrom S., Fey V., Mpindi J.P., Kleivi Sahlberg K., Kallioniemi O., Perala M. High-throughput 3D screening reveals differences in drug sensitivities between culture models of JIMT1 breast cancer cells. PLoS One 2013, 8:e77232.
143. Lin C.H., Lee J.K., LaBarge M.A. Fabrication and use of microenvironment microarrays (MEArrays). J. Vis. Exp. 2012, 68. pii:4152.
144. Markovitz-Bishitz Y., Tauber Y., Afrimzon E., Zurgil N., Sobolev M., Shafran Y., Deutsch A., Howitz S., Deutsch M. A polymer microstructure array for the formation, culturing, and high throughput drug screening of breast cancer spheroids. Biomaterials 2010, 31:8436-8444.
145. Tung Y.C., Hsiao A.Y., Allen S.G., Torisawa Y.S., Ho M., Takayama S. High-throughput 3D spheroid culture and drug testing using a 384 hanging drop array. Analyst 2011, 136:473-478.
146. Neve R.M., Chin K., Fridlyand J., Yeh J., Baehner F.L., Fevr T., Clark L., Bayani N., Coppe J.P., Tong F., Speed T., Spellman P.T., DeVries S., Lapuk A., Wang N.J., Kuo W.L., Stilwell J.L., Pinkel D., Albertson D.G., Waldman F.M., McCormick F., Dickson R.B., Johnson M.D., Lippman M., Ethier S., Gazdar A., Gray J.W. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006, 10:515-527.
147. Wendt M.K., Smith J.A., Schiemann W.P. Transforming growth factor-beta-induced epithelial-mesenchymal transition facilitates epidermal growth factor-dependent breast cancer progression. Oncogene 2010, 29:6485-6498.