A complex 3D human tissue culture system based on mammary stromal cells and silk scaffolds for modeling breast morphogenesis and function

Biomaterials

Volumn 31, Issue 14, 2010, Pages 3920-3929

  Wang, Xiuli ^a   Sun, Lin ^a   Maffini, Maricel V ^b   Soto, Ana ^b   Sonnenschein, Carlos ^b   Kaplan, David L ^a,b  

^a TUFTS UNIVERSITY   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adipocyte; Co culture; Epithelial cells; Fibroblasts; Silk; Tri culture

Indexed keywords

ADIPOCYTES; ALVEOLAR STRUCTURE; BREAST TISSUES; CO-CULTURES; COCULTURE; CULTURE SYSTEMS; EMBRYONIC DEVELOPMENT; EPITHELIAL CELLS; EXPERIMENTAL MODELS; HUMAN BREAST; HUMAN BREAST TISSUE; HUMAN FIBROBLAST; HUMAN MAMMARY EPITHELIAL CELLS; HUMAN TISSUES; IN-VITRO; IN-VIVO; MAMMARY EPITHELIAL CELLS; MICROENVIRONMENTS; MRNA EXPRESSION; NEOPLASTIC TRANSFORMATION; SILK PROTEINS; SILK SCAFFOLD; STROMAL CELLS; THREE-DIMENSIONAL (3D); UNDERLYING MECHANISM;

CASEIN; CELL PROLIFERATION; COMPLEXATION; FIBROBLASTS; GENE EXPRESSION; HUMAN ENGINEERING; MOLECULAR WEIGHT; MORPHOLOGY; SCAFFOLDS; SILK; THREE DIMENSIONAL; TISSUE; TISSUE CULTURE;

CELL CULTURE;

CASEIN; MESSENGER RNA;

ADIPOCYTE; ARTICLE; BIOENGINEERING; BREAST; CELL CULTURE; CELL DIFFERENTIATION; CELL GROWTH; CELL POLARITY; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; MORPHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROMA CELL; THREE DIMENSIONAL IMAGING; TRANSMISSION ELECTRON MICROSCOPY;

CASEINS; CELL DIFFERENTIATION; CELL LINE; CELL POLARITY; CELL PROLIFERATION; CELL SHAPE; CELL SURVIVAL; DNA; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; MAMMARY GLANDS, HUMAN; MODELS, BIOLOGICAL; MORPHOGENESIS; RNA, MESSENGER; SILK; STROMAL CELLS; TISSUE CULTURE TECHNIQUES; TISSUE SCAFFOLDS;

EID: 77649275280     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2010.01.118     Document Type: Article

References (46)

1. Mettlin C. Global breast cancer mortality statistics. CA Cancer J Clin 49 (1999) 138-144
2. Thomsen A., and Kolesar J.M. Chemoprevention of breast cancer. Am J Health Syst Pharm 65 (2008) 2221-2228
3. Howlett A.R., and Bissell M.J. The influence of tissue microenvironment (stroma and extracellular matrix) on the development and function of mammary epithelium. Epithelial Cell Biol 2 (1993) 79-89
4. Haslam S.Z., and Woodward T.L. Reciprocal regulation of extracellular matrix proteins and ovarian steroid activity in the mammary gland. Breast Cancer Res 3 (2001) 365-372
5. Cunha G.R., Cooke P.S., and Kurita T. Role of stromal-epithelial interactions in hormonal responses. Arch Histol Cytol 67 (2004) 417-434
6. Moinfar F., Man Y.G., Arnould L., Bratthauer G.L., Ratschek M., and Tavassoli F.A. Concurrent and independent genetic alterations in the stromal and epithelial cells of mammary carcinoma: implications for tumorigenesis. Cancer Res 60 (2000) 2562-2566
7. Schor S.L., and Schor A.M. Phenotypic and genetic alterations in mammary stroma: implications for tumour progression. Breast Cancer Res 3 (2001) 373-379
8. Haslam S.Z., and Woodward T.L. Host microenvironment in breast cancer development: epithelial-cell-stromal-cell interactions and steroid hormone action in normal and cancerous mammary gland. Breast Cancer Res 5 (2003) 208-215
9. Maffini M.V., Soto A.M., Calabro J.M., Ucci A.A., and Sonnenschein C. The stroma as a crucial target in rat mammary gland carcinogenesis. J Cell Sci 117 (2004) 1495-1502
10. Bissell M.J., Rizki A., and Mian I.S. Tissue architecture: the ultimate regulator of breast epithelial function. Curr Opin Cell Biol 15 (2003) 753-762
11. Pickl M., and Ries C.H. Comparison of 3D and 2D tumor models reveals enhanced HER2 activation in 3D associated with an increased response to trastuzumab. Oncogene 28 (2009) 461-468
12. Kim B.W., Lee E.R., Min H.M., Jeong H.S., Ahn J.Y., Kim J.H., et al. Sustained ERK activation is involved in the kaempferol-induced apoptosis of breast cancer cells and is more evident under 3-D culture condition. Cancer Biol Ther 7 (2008) 1080-1089
13. Eigeliene N., Härkönen P., and Erkkola R. Effect of estradiol and medroxyprogesterone acetate on morphology, proliferation and apoptosis of human breast tissue in organ cultures. BMC Cancer 6 (2006) 246-259
14. Mehta R., and Lansky E.P. Breast cancer chemopreventive properties of pomegranate (Punica granatum) fruit extracts in a mouse mammary organ culture. Eur J Cancer Prev 13 (2004) 345-348
15. Li A.P., Bode C., and Sakai Y. A novel in vitro system, the integrated discrete multiple organ cell culture (IdMOC) system, for the evaluation of human drug toxicity: comparative cytotoxicity of tamoxifen towards normal human cells from five major organs and MCF-7 adenocarcinoma breast cancer cells. Chem Biol Interact 150 (2004) 129-136
16. Malewicz B., Wang Z., Jiang C., Guo J., Cleary M.P., Grande J.P., et al. Enhancement of mammary carcinogenesis in two rodent models by silymarin dietary supplements. Carcinogenesis 27 (2006) 1739-1747
17. Provenzano P.P., Inman D.R., Eliceiri K.W., Beggs H.E., and Keely P.J. Mammary epithelial-specific disruption of focal adhesion kinase retards tumor formation and metastasis in a transgenic mouse model of human breast cancer. Am J Pathol 173 (2008) 1551-1565
18. Gusterson B.A., Williams J., Bunnage H., O'Hare M.J., and Dubois J.D. Human breast epithelium transplanted into nude mice: proliferation and milk protein production in response to pregnancy. Virchows Arch A Pathol Anat Histopathol 404 (1984) 325-333
19. Barcellos-Hoff M.H., Aggeler J., Ram T.G., and Bissell M.J. Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development 105 (1989) 223-235
20. Roskelley C.D., Desprez P.Y., and 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 USA 91 (1994) 12378-12382
21. Nelson C.M., and Bissell M.J. Modeling dynamic reciprocity: engineering three-dimensional culture models of breast architecture, function, and neoplastic transformation. Semin Cancer Biol 15 (2005) 342-352
22. Olumi A.F., Grossfeld G.D., Hayward S.W., Carroll P.R., Tlsty T.D., and Cunha G.R. Carcinoma-associated fibroblasts direct tumour progression of initiated human prostatic epithelium. Cancer Res 59 (1999) 5002-5011
23. Darcy K.M., Zangani D., Shea-Eaton W., Shoemaker S.F., Lee P.P., Mead L.H., et al. Mammary fibroblasts stimulate growth, alveolar morphogenesis, and differentiation of normal rat mammary epithelial cells. Vitro Cell Dev Biol Anim 36 (2000) 578-592
24. Shekhar M.P., Werdell J., and Tait L. Interaction with endothelial cells is prerequisite for branching ductal-alveolar morphogenesis and hyperplasia of preneoplastic human breast epithelial cells: regulation by estrogen. Cancer Res 60 (2000) 439-449
25. Proia D.A., and Kuperwasser C. Reconstruction of human mammary tissue in a mouse model. Nat Protoc 1 (2006) 206-214
26. Krause S., Maffini M.V., Soto A.M., and Sonnenschein C. A novel 3D in vitro culture model to study stromal-epithelial interactions in the mammary gland. Tissue Eng Part C Methods 14 (2008) 261-271
27. Wang X.L., Zhang X.H., Sun L., Subramanian B., Maffini M.V., Soto A.M., et al. Preadipocytes stimulate ductal morphogenesis and functional differentiation of human mammary epithelial cells in 3D silk scaffolds. Tissue Eng Part A 15 (2009) 3087-3098
28. Debnath J., Muthuswamy S.K., and Brugge J.S. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Method 30 (2003) 256-268
29. Wozniak M.A., and Keely P.J. Use of three-dimensional collagen gels to study mechanotransuction in T47D breast epithelial cells. Biol Proced Online 7 (2005) 144-161
30. Dhiman H.K., Ray A.R., and Panda A.K. Characterization and evaluation of chitosan matrix for in vitro growth of MCF-7 breast cancer cell lines. Biomaterials 25 (2004) 5147-5154
31. Sahoo S.K., Panda A.K., and Labhasetwar V. Characterization of porous PLGA/PLA microparticles as a scaffold for three dimensional growth of breast cancer cells. Biomacromolecules 6 (2005) 1132-1139
32. Wang Y., Kim H.J., Vunjak-Novakovic G., and Kaplan D.L. Stem cell-based tissue engineering with silk biomaterials. Biomaterials 27 (2006) 6064-6082
33. Hofmann S., Knecht S., Langer R., Kaplan D.L., Vunjak-Novakovic G., Merkle H.P., et al. Cartilage-like tissue engineering using silk scaffolds and mesenchymal stem cells. Tissue Eng 12 (2006) 2729-2738
34. Mauney J.R., Nguyen T., Gillen K., Kirker-Head C., Gimble J.M., and Kaplan D.L. Engineering adipose-like tissue in vitro and in vivo utilizing human bone marrow and adipose-derived mesenchymal stem cells with silk fibroin 3D scaffolds. Biomaterials 28 (2007) 5280-5290
35. Soffer L., Wang X., Zhang X., Kluge J., Dorfmann L., Kaplan D.L., et al. Silk-based electrospun tubular scaffolds for tissue-engineered vascular grafts. J Biomater Sci Polym Ed 19 (2008) 653-664
36. Wang X., Wang W., Ma J., Guo X., and Ma X. Proliferation and differentiation of mouse embryonic stem cells in APA microcapsule: a model for studying the interaction between stem cells and their niche. Biotechnol Prog 22 (2006) 791-800
37. Gumbiner B.M. Regulation of cadherin adhesive activity. J Cell Biol 148 (2000) 399-404
38. Kim J.B., Stein R., and O'Hare M.J. Three-dimensional in vitro tissue models of breast cancer. Breast Cancer Res Treat 85 (2004) 281-291
39. Bergstraesser L.M., and Weitzman S.A. Culture of normal and malignant primary epithelial cell in a physiological manner simulates in vivo patterns and allows discrimination of cell type. Cancer Res 53 (1993) 2644-2654
40. Parrinello S., Coppe J.P., Krtolica A., and Campisi J. Stromal-epithelial interactions in aging and cancer: senescent fibroblasts alter epithelial cell differentiation. J Cell Sci 118 (2005) 485-496
41. Soriano J.V., Pepper M.S., Nakamura T., Orci L., and Montesano R. Hepatocyte growth factor stimulates extensive development of branching duct-like structures by cloned mammary gland epithelial cells. J Cell Sci 108 (1995) 413-430
42. Paszek M.J., and Weaver V.M. The tension mounts: mechanics meets morphogenesis and malignancy. J Mammary gland Biol Neoplasia 9 (2004) 325-342
43. Yeaman C., Grinidstaff K.K., and Nelson W.J. New perspective on mechanisms involved in generating epithelial cell polarity. Physiol Rev 79 (1999) 73-98
44. Gudjonsson T., Rønnov-Jessen L., Villadsen R., Rank F., Bissell M.J., and 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 115 (2002) 39-50
45. Zangani D., Darcy K.M., Shoemaker S., and Ip M.M. Adipocyte-epithelial interactions regulate the in vitro development of normal mammary epithelial cells. Exp Cell Res 247 (1999) 399-409
46. Schmidhauser C., Bissell M.J., Myers C.A., and Casperson G.F. Extracellular matrix and hormones transcriptionally regulate bovine 18-casein 5′ sequences in stably transfected mouse mammary cells. Proc Natl Acad Sci 87 (1990) 9118-9122