Deconstructing signaling in three dimensions

Biochemistry

Volumn 53, Issue 13, 2014, Pages 2078-2090

  Rubashkin, Matthew G ^a   Ou, Guanqing ^a   Weaver, Valerie M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; PHYSIOLOGY; THREE DIMENSIONAL;

CELL-CELL INTERACTION; DEVELOPMENT AND APPLICATIONS; DIFFERENT LENGTH SCALE; EXTRACELLULAR MATRICES; INTRACELLULAR SIGNALING; PHENOTYPIC DIFFERENCES; THREE-DIMENSIONAL CULTURE; THREE-DIMENSIONAL CULTURE MODEL;

CYTOLOGY;

ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; CELL SURVIVAL; EXTRACELLULAR MATRIX; IN VITRO STUDY; MICROENVIRONMENT; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

CELL ADHESION; CELL CULTURE TECHNIQUES; CELL SHAPE; DIFFUSION; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; HUMANS; IMAGING, THREE-DIMENSIONAL; PROTEINS; SIGNAL TRANSDUCTION;

EID: 84898026005     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401710d     Document Type: Article

References (131)

1. Yamada, K. M. and Cukierman, E. (2007) Modeling tissue morphogenesis and cancer in 3D Cell 130, 601-610
2. Cukierman, E., Pankov, R., Stevens, D. R., and Yamada, K. M. (2001) Taking cell-matrix adhesions to the third dimension Science 294, 1708-1712
3. Sutherland, R. M. and Durand, R. E. (1976) Radiation response of multicell spheroids: An in vitro tumour model Curr. Top. Radiat. Res. Q. 11, 87-139
4. Zahir, N. and Weaver, V. M. (2004) Death in the third dimension: Apoptosis regulation and tissue architecture Curr. Opin. Genet. Dev. 14, 71-80
5. Wang, F., Weaver, V. M., Petersen, O. W., Larabell, C. A., Dedhar, S., Briand, P., Lupu, R., and Bissell, M. J. (1998) Reciprocal interactions between β1-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. 95, 14821-14826
6. Bell, S. E., Mavila, A., Salazar, R., Bayless, K. J., Kanagala, S., Maxwell, S. A., and Davis, G. E. (2001) Differential gene expression during capillary morphogenesis in 3D collagen matrices: Regulated expression of genes involved in basement membrane matrix assembly, cell cycle progression, cellular differentiation and G-protein signaling J. Cell Sci. 114, 2755-2773
7. Tsuboi, N., Yoshida, H., Kawamura, T., Furukawa, Y., Hosoya, T., and Yamada, H. (2000) Three-dimensional matrix suppresses E2F-controlled gene expression in glomerular mesangial cells Kidney Int. 57, 1581-1589
8. Ghosh, S., Spagnoli, G. C., Martin, I., Ploegert, S., Demougin, P., Heberer, M., and Reschner, A. (2005) Three-dimensional culture of melanoma cells profoundly affects gene expression profile: A high density oligonucleotide array study J. Cell. Physiol. 204, 522-531
9. Lelièvre, S., Weaver, V. M., and Bissell, M. J. (1996) Extracellular Matrix Signaling from the Cellular Membrane Skeleton to the Nuclear Skeleton: A Model of Gene Regulation Recent Prog. Horm. Res. 51, 417-432
10. Weaver, V. M., Lelièvre, S., Lakins, J. N., Chrenek, M. A., Jones, J. C. R., Giancotti, F., Werb, Z., and Bissell, M. J. (2002) β4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium Cancer Cell 2, 205-216
11. Bhalla, U. S. (2004) Signaling in small subcellular volumes. I. Stochastic and diffusion effects on individual pathways Biophys. J. 87, 733-744
12. Dehmelt, L. and Bastiaens, P. I. H. (2010) Spatial organization of intracellular communication: Insights from imaging Nat. Rev. Mol. Cell Biol. 11, 440-452
13. DeWire, S. M., Ahn, S., Lefkowitz, R. J., and Shenoy, S. K. (2007) β-Arrestins and cell signaling Annu. Rev. Physiol. 69, 483-510
14. Kolch, W. (2005) Coordinating ERK/MAPK signalling through scaffolds and inhibitors Nat. Rev. Mol. Cell Biol. 6, 827-837
15. Kholodenko, B. N., Hancock, J. F., and Kolch, W. (2010) Signalling ballet in space and time Nat. Rev. Mol. Cell Biol. 11, 414-426
16. Webb, D. J., Donais, K., Whitmore, L. A., Thomas, S. M., Turner, C. E., Parsons, J. T., and Horwitz, A. F. (2004) FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly Nat. Cell Biol. 6, 154-161
17. Calalb, M. B., Zhang, X., Polte, T. R., and Hanks, S. K. (1996) Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src Biochem. Biophys. Res. Commun. 228, 662-668
18. Ishibe, S., Joly, D., Liu, Z.-X., and Cantley, L. G. (2004) Paxillin serves as an ERK-regulated scaffold for coordinating FAK and Rac activation in epithelial morphogenesis Mol. Cell 16, 257-267
19. Morén, A., Raja, E., Heldin, C.-H., and Moustakas, A. (2011) Negative regulation of TGFβ signaling by the kinase LKB1 and the scaffolding protein LIP1 J. Biol. Chem. 286, 341-353
20. Morrison, D. K. (2001) KSR: A MAPK scaffold of the Ras pathway? J. Cell Sci. 114, 1609-1612
21. Kortum, R. L. and Lewis, R. E. (2004) The Molecular Scaffold KSR1 Regulates the Proliferative and Oncogenic Potential of Cells Mol. Cell. Biol. 24, 4407-4416
22. Kubow, K. E., Conrad, S. K., and Horwitz, A. R. (2013) Matrix microarchitecture and myosin II determine adhesion in 3D matrices Curr. Biol. 23, 1607-1619
23. Petroll, W. M., Billiar, K., Starke, J., Maaser, K., Wehrle-Haller, B., and Friedl, P. (2013) Mechanotransduction of mesenchymal melanoma cell invasion into 3D collagen lattices: Filopod-mediated extension-relaxation cycles and force anisotropy Exp. Cell Res. 319, 2424-2433
24. Chung, I., Akita, R., Vandlen, R., Toomre, D., Schlessinger, J., and Mellman, I. (2010) Spatial control of EGF receptor activation by reversible dimerization on living cells Nature 464, 783-787
25. Pickl, M. and Ries, C. H. (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
26. Weigelt, B., Lo, A. T., Park, C. C., Gray, J. W., and Bissell, M. J. (2010) 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. 122, 35-43
27. Youle, R. J. and Strasser, A. (2008) The BCL-2 protein family: Opposing activities that mediate cell death Nat. Rev. Mol. Cell Biol. 9, 47-59
28. Lovell, J. F., Billen, L. P., Bindner, S., Shamas-Din, A., Fradin, C., Leber, B., and Andrews, D. W. (2008) Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax Cell 135, 1074-1084
29. De Jonge, N. and Ross, F. M. (2011) Electron microscopy of specimens in liquid Nat. Nanotechnol. 6, 695-704
30. Vic, P., Vignon, F., Derocq, D., and Rochefort, H. (1982) Effect of Estradiol on the Ultrastructure of the MCF7 Human Breast Cancer Cells in Culture Cancer Res. 42, 667-673
31. Loessner, D., Stok, K. S., Lutolf, M. P., Hutmacher, D. W., Clements, J. A., and Rizzi, S. C. (2010) Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells Biomaterials 31, 8494-8506
32. Stenoien, D. L., Patel, K., Mancini, M. G., Dutertre, M., Smith, C. L., O'Malley, B. W., and Mancini, M. A. (2001) FRAP reveals that mobility of oestrogen receptor-α is ligand- and proteasome-dependent Nat. Cell Biol. 3, 15-23
33. Chan, S. W., Lim, C. J., Loo, L. S., Chong, Y. F., Huang, C., and Hong, W. (2009) TEADs mediate nuclear retention of TAZ to promote oncogenic transformation J. Biol. Chem. 284, 14347-14358
34. Gaborit, N., Larbouret, C., Vallaghe, J., Peyrusson, F., Bascoul-Mollevi, C., Crapez, E., Azria, D., Chardès, T., Poul, M.-A., Mathis, G., Bazin, H., and Pèlegrin, A. (2011) Time-resolved fluorescence resonance energy transfer (TR-FRET) to analyze the disruption of EGFR/HER2 dimers: A new method to evaluate the efficiency of targeted therapy using monoclonal antibodies J. Biol. Chem. 286, 11337-11345
35. Vilardaga, J.-P., Bünemann, M., Krasel, C., Castro, M., and Lohse, M. J. (2003) Measurement of the millisecond activation switch of G protein-coupled receptors in living cells Nat. Biotechnol. 21, 807-812
36. Grashoff, C., Hoffman, B. D., Brenner, M. D., Zhou, R., Parsons, M., Yang, M. T., McLean, M. A., Sligar, S. G., Chen, C. S., Ha, T., and Schwartz, M. A. (2010) Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics Nature 466, 263-266
37. Berezin, M. Y. and Achilefu, S. (2010) Fluorescence lifetime measurements and biological imaging Chem. Rev. 110, 2641-2684
38. Vogel, V. and Sheetz, M. (2006) Local force and geometry sensing regulate cell functions Nat. Rev. Mol. Cell Biol. 7, 265-275
39. Chen, C. S. (1997) Geometric Control of Cell Life and Death Science 276, 1425-1428
40. Zamir, E., Katz, B. z., Aota, S., Yamada, K. m., Geiger, B., and Kam, Z. (1999) Molecular diversity of cell-matrix adhesions J. Cell Sci. 112, 1655-1669
41. Aplin, A. E. (2003) Cell adhesion molecule regulation of nucleocytoplasmic trafficking FEBS Lett. 534, 11-14
42. Juliano, R. L. (2002) Signal Transduction by Cell Adhesion Receptors and the Cytoskeleton: Functions of Integrins, Cadherins, Selectins, and Immunoglobulin-Superfamily Members Annu. Rev. Pharmacol. Toxicol. 42, 283-323
43. Ochsner, M., Textor, M., Vogel, V., and Smith, M. L. (2010) Dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape PLoS One 5, e9445
44. Ghibaudo, M., Di Meglio, J.-M., Hersen, P., and Ladoux, B. (2011) Mechanics of cell spreading within 3D-micropatterned environments Lab Chip 11, 805-812
45. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K., and Chen, C. S. (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment Dev. Cell 6, 483-495
46. Engler, A. J., Sen, S., Sweeney, H. L., and Discher, D. E. (2006) Matrix Elasticity Directs Stem Cell Lineage Specification Cell 126, 677-689
47. Raucher, D. and Sheetz, M. P. (2000) Cell Spreading and Lamellipodial Extension Rate Is Regulated by Membrane Tension J. Cell Biol. 148, 127-136
48. Sheetz, M. P. and Dai, J. (1996) Modulation of membrane dynamics and cell motility by membrane tension Trends Cell Biol. 6, 85-89
49. Dai, J. and Sheetz, M. P. (1995) Regulation of Endocytosis, Exocytosis, and Shape by Membrane Tension Cold Spring Harbor Symp. Quant. Biol. 60, 567-571
50. Tarricone, C., Xiao, B., Justin, N., Walker, P. A., Rittinger, K., Gamblin, S. J., and Smerdon, S. J. (2001) The structural basis of Arfaptin-mediated cross-talk between Rac and Arf signalling pathways Nature 411, 215-219
51. Williger, B.-T., Ostermann, J., and Exton, J. H. (1999) Arfaptin 1, an ARF-binding protein, inhibits phospholipase D and endoplasmic reticulum/Golgi protein transport FEBS Lett. 443, 197-200
52. Van Aelst, L., Joneson, T., and Bar-Sagi, D. (1996) Identification of a novel Rac1-interacting protein involved in membrane ruffling EMBO J. 15, 3778-3786
53. Kubo, T., Yamashita, T., Yamaguchi, A., Sumimoto, H., Hosokawa, K., and Tohyama, M. (2002) A Novel FERM Domain Including Guanine Nucleotide Exchange Factor Is Involved in Rac Signaling and Regulates Neurite Remodeling J. Neurosci. 22, 8504-8513
54. Stefanova, N., Staneva, G., Petkova, D., Lupanova, T., Pankov, R., and Momchilova, A. (2009) Cell culturing in a three-dimensional matrix affects the localization and properties of plasma membrane cholesterol Cell Biol. Int. 33, 1079-1086
55. Caswell, P. T., Vadrevu, S., and Norman, J. C. (2009) Integrins: Masters and slaves of endocytic transport Nat. Rev. Mol. Cell Biol. 10, 843-853
56. Lingwood, D. and Simons, K. (2010) Lipid rafts as a membrane-organizing principle Science 327, 46-50
57. McAuliffe, P. F., Meric-Bernstam, F., Mills, G. B., and Gonzalez-Angulo, A. M. (2010) Deciphering the role of PI3K/Akt/mTOR pathway in breast cancer biology and pathogenesis. Clin Breast Cancer 10 (Suppl. 3) S59-S65
58. Vara, J. á. F., Casado, E., de Castro, J., Cejas, P., Belda-Iniesta, C., and González-Barón, M. (2004) PI3K/Akt signalling pathway and cancer Cancer Treat. Rev. 30, 193-204
59. Gao, X., Lowry, P. R., Zhou, X., Depry, C., Wei, Z., Wong, G. W., and Zhang, J. (2011) PI3K/Akt signaling requires spatial compartmentalization in plasma membrane microdomains Proc. Natl. Acad. Sci. U.S.A. 108, 14509-14514
60. Balasubramanian, N., Scott, D. W., Castle, J. D., Casanova, J. E., and Schwartz, M. A. (2007) Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts Nat. Cell Biol. 9, 1381-1391
61. Mañes, S., Ana Lacalle, R., Gómez-Moutón, C., and Martínez-A, C. (2003) From rafts to crafts: Membrane asymmetry in moving cells Trends Immunol. 24, 319-325
62. Matsuoka, T., Yashiro, M., Nishioka, N., Hirakawa, K., Olden, K., and Roberts, J. D. (2012) PI3K/Akt signalling is required for the attachment and spreading, and growth in vivo of metastatic scirrhous gastric carcinoma Br. J. Cancer 106, 1535-1542
63. Flusberg, D. A., Numaguchi, Y., and Ingber, D. E. (2001) Cooperative control of Akt phosphorylation, bcl-2 expression, and apoptosis by cytoskeletal microfilaments and microtubules in capillary endothelial cells Mol. Biol. Cell 12, 3087-3094
64. Oinuma, I., Kawada, K., Tsukagoshi, K., and Negishi, M. (2012) Rnd1 and Rnd3 targeting to lipid raft is required for p190 RhoGAP activation Mol. Biol. Cell 23, 1593-1604
65. Mammoto, A., Huang, S., and Ingber, D. E. (2007) Filamin links cell shape and cytoskeletal structure to Rho regulation by controlling accumulation of p190RhoGAP in lipid rafts J. Cell Sci. 120, 456-467
66. Nikolov, D. B., Xu, K., and Himanen, J. P. (2013) Eph/ephrin recognition and the role of Eph/ephrin clusters in signaling initiation Biochim. Biophys. Acta 1834, 2160-2165
67. Salaita, K., Nair, P. M., Petit, R. S., Neve, R. M., Das, D., Gray, J. W., and Groves, J. T. (2010) Restriction of receptor movement alters cellular response: Physical force sensing by EphA2 Science 327, 1380-1385
68. Malek, A. M. and Izumo, S. (1996) Mechanism of endothelial cell shape change and cytoskeletal remodeling in response to fluid shear stress J. Cell Sci. 109 (Part 4) 713-726
69. Chung, S., Sudo, R., Vickerman, V., Zervantonakis, I. K., and Kamm, R. D. (2010) Microfluidic platforms for studies of angiogenesis, cell migration, and cell-cell interactions Ann. Biomed. Eng. 38, 1164-1177
70. Gee, E., Milkiewicz, M., and Haas, T. L. (2010) p38 MAPK activity is stimulated by vascular endothelial growth factor receptor 2 activation and is essential for shear stress-induced angiogenesis J. Cell. Physiol. 222, 120-126
71. Jalali, S., Li, Y. S., Sotoudeh, M., Yuan, S., Li, S., Chien, S., and Shyy, J. Y. (1998) Shear stress activates p60src-Ras-MAPK signaling pathways in vascular endothelial cells Arterioscler., Thromb., Vasc. Biol. 18, 227-234
72. McEver, R. P. and Zhu, C. (2010) Rolling cell adhesion Annu. Rev. Cell Dev. Biol. 26, 363-396
73. Sorokin, L. (2010) The impact of the extracellular matrix on inflammation Nat. Rev. Immunol. 10, 712-723
74. Srinivasan, S., Wang, F., Glavas, S., Ott, A., Hofmann, F., Aktories, K., Kalman, D., and Bourne, H. R. (2003) Rac and Cdc42 play distinct roles in regulating PI(3,4,5)P3 and polarity during neutrophil chemotaxis J. Cell Biol. 160, 375-385
75. Chow, D., Nunalee, M. L., Lim, D. W., Simnick, A. J., and Chilkoti, A. (2008) Peptide-based Biopolymers in Biomedicine and Biotechnology Mater. Sci. Eng., R 62, 125-155
76. Stevenson, M. D., Piristine, H., Hogrebe, N. J., Nocera, T. M., Boehm, M. W., Reen, R. K., Koelling, K. W., Agarwal, G., Sarang-Sieminski, A. L., and Gooch, K. J. (2013) A self-assembling peptide matrix used to control stiffness and binding site density supports the formation of microvascular networks in three dimensions Acta Biomater. 9, 7651-7661
77. Mi, K., Wang, G., Liu, Z., Feng, Z., Huang, B., and Zhao, X. (2009) Influence of a self-assembling peptide, RADA16, compared with collagen I and Matrigel on the malignant phenotype of human breast-cancer cells in 3D cultures and in vivo Macromol. Biosci. 9, 437-443
78. Miroshnikova, Y. A., Jorgens, D. M., Spirio, L., Auer, M., Sarang-Sieminski, A. L., and Weaver, V. M. (2011) Engineering strategies to recapitulate epithelial morphogenesis within synthetic three-dimensional extracellular matrix with tunable mechanical properties Phys. Biol. 8, 026013
79. Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F. T., Csiszar, K., Giaccia, A., Weninger, W., Yamauchi, M., Gasser, D. L., and Weaver, V. M. (2009) Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling Cell 139, 891-906
80. Willits, R. K. and Skornia, S. L. (2004) Effect of collagen gel stiffness on neurite extension J. Biomater. Sci., Polym. Ed. 15, 1521-1531
81. Ashe, H. L. and Briscoe, J. (2006) The interpretation of morphogen gradients Development 133, 385-394
82. Lander, A. D., Nie, Q., and Wan, F. Y. (2002) Do Morphogen Gradients Arise by Diffusion? Dev. Cell 2, 785-796
83. Bollenbach, T., Pantazis, P., Kicheva, A., Bökel, C., González-Gaitán, M., and Jülicher, F. (2008) Precision of the Dpp gradient Development 135, 1137-1146
84. Häcker, U., Nybakken, K., and Perrimon, N. (2005) Heparan sulphate proteoglycans: The sweet side of development Nat. Rev. Mol. Cell Biol. 6, 530-541
85. Yu, S. R., Burkhardt, M., Nowak, M., Ries, J., Petrášek, Z., Scholpp, S., Schwille, P., and Brand, M. (2009) Fgf8 morphogen gradient forms by a source-sink mechanism with freely diffusing molecules Nature 461, 533-536
86. Jaeger, J., Surkova, S., Blagov, M., Janssens, H., Kosman, D., Kozlov, K. N., Manu, Myasnikova, E., Vanario-Alonso, C. E., Samsonova, M., Sharp, D. H., and Reinitz, J. (2004) Dynamic control of positional information in the early Drosophila embryo Nature 430, 368-371
87. Houchmandzadeh, B., Wieschaus, E., and Leibler, S. (2002) Establishment of developmental precision and proportions in the early Drosophila embryo Nature 415, 798-802
88. Teleman, A. A. and Cohen, S. M. (2000) Dpp Gradient Formation in the Drosophila Wing Imaginal Disc Cell 103, 971-980
89. Belenkaya, T. Y., Han, C., Yan, D., Opoka, R. J., Khodoun, M., Liu, H., and Lin, X. (2004) Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans Cell 119, 231-244
90. Rogers, K. W. and Schier, A. F. (2011) Morphogen gradients: From generation to interpretation Annu. Rev. Cell Dev. Biol. 27, 377-407
91. Tucker, J. A., Mintzer, K. A., and Mullins, M. C. (2008) The BMP signaling gradient patterns dorsoventral tissues in a temporally progressive manner along the anteroposterior axis Dev. Cell 14, 108-119
92. Hogan, B. L. (1996) Bone morphogenetic proteins: Multifunctional regulators of vertebrate development Genes Dev. 10, 1580-1594
93. Yu, S. R., Burkhardt, M., Nowak, M., Ries, J., Petrásek, Z., Scholpp, S., Schwille, P., and Brand, M. (2009) Fgf8 morphogen gradient forms by a source-sink mechanism with freely diffusing molecules Nature 461, 533-536
94. Dessaud, E., Yang, L. L., Hill, K., Cox, B., Ulloa, F., Ribeiro, A., Mynett, A., Novitch, B. G., and Briscoe, J. (2007) Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism Nature 450, 717-720
95. Kretzschmar, K. and Watt, F. M. (2012) Lineage Tracing Cell 148, 33-45
96. Swartz, M. A. and Fleury, M. E. (2007) Interstitial Flow and Its Effects in Soft Tissues Annu. Rev. Biomed. Eng. 9, 229-256
97. Pouysségur, J., Volmat, V., and Lenormand, P. (2002) Fidelity and spatio-temporal control in MAP kinase (ERKs) signalling Biochem. Pharmacol. 64, 755-763
98. Vaupel, P. and Mayer, A. (2007) Hypoxia in cancer: Significance and impact on clinical outcome Cancer Metastasis Rev. 26, 225-239
99. Harris, A. L. (2002) Hypoxia: A key regulatory factor in tumour growth Nat. Rev. Cancer 2, 38-47
100. Warburton, D., Bellusci, S., De Langhe, S., Del Moral, P.-M., Fleury, V., Mailleux, A., Tefft, D., Unbekandt, M., Wang, K., and Shi, W. (2005) Molecular mechanisms of early lung specification and branching morphogenesis Pediatr. Res. 57, 26R-37R
101. Fleury, M. E., Boardman, K. C., and Swartz, M. A. (2006) Autologous Morphogen Gradients by Subtle Interstitial Flow and Matrix Interactions Biophys. J. 91, 113-121
102. Fischbach, C., Kong, H. J., Hsiong, S. X., Evangelista, M. B., Yuen, W., and Mooney, D. J. (2009) Cancer cell angiogenic capability is regulated by 3D culture and integrin engagement Proc. Natl. Acad. Sci. U.S.A. 106, 399-404
103. Liu, H., Radisky, D. C., Wang, F., and Bissell, M. J. (2004) Polarity and proliferation are controlled by distinct signaling pathways downstream of PI3-kinase in breast epithelial tumor cells J. Cell Biol. 164, 603-612
104. Khademhosseini, A., Ferreira, L., Blumling, J., III, Yeh, J., Karp, J. M., Fukuda, J., and Langer, R. (2006) Co-culture of human embryonic stem cells with murine embryonic fibroblasts on microwell-patterned substrates Biomaterials 27, 5968-5977
105. Ludwig, T. E., Levenstein, M. E., Jones, J. M., Berggren, W. T., Mitchen, E. R., Frane, J. L., Crandall, L. J., Daigh, C. A., Conard, K. R., Piekarczyk, M. S., Llanas, R. A., and Thomson, J. A. (2006) Derivation of human embryonic stem cells in defined conditions Nat. Biotechnol. 24, 185-187
106. Amit, M. and Itskovitz-Eldor, J. (2006) in Feeder-Free Culture of Human Embryonic Stem Cells (Klimanskaya, I. and Lanza, R., Eds.) pp 37-49, Academic Press, New York.
107. Xu, C., Inokuma, M. S., Denham, J., Golds, K., Kundu, P., Gold, J. D., and Carpenter, M. K. (2001) Feeder-free growth of undifferentiated human embryonic stem cells Nat. Biotechnol. 19, 971-974
108. Ludwig, T. E., Bergendahl, V., Levenstein, M. E., Yu, J., Probasco, M. D., and Thomson, J. A. (2006) Feeder-independent culture of human embryonic stem cells Nat. Methods 3, 637-646
109. Alvarez-Maubecin, V., García-Hernández, F., Williams, J. T., and Van Bockstaele, E. J. (2000) Functional Coupling between Neurons and Glia J. Neurosci. 20, 4091-4098
110. Huang, H., Kamm, R. D., and Lee, R. T. (2004) Cell mechanics and mechanotransduction: Pathways, probes, and physiology Am. J. Physiol. 287, C1-C11
111. Halassa, M. M. and Haydon, P. G. (2010) Integrated Brain Circuits: Astrocytic Networks Modulate Neuronal Activity and Behavior Annu. Rev. Physiol. 72, 335-355
112. Haydon, P. G. (2000) Neuroglial networks: Neurons and glia talk to each other Curr. Biol. 10, R712-R714
113. Ullian, E. M., Christopherson, K. S., and Barres, B. A. (2004) Role for glia in synaptogenesis Glia 47, 209-216
114. Zhang, M. Y., Lee, P. J., Hung, P. J., Johnson, T., Lee, L. P., and Mofrad, M. R. K. (2008) Microfluidic environment for high density hepatocyte culture Biomed. Microdevices 10, 117-121
115. Powers, M. J., Janigian, D. M., Wack, K. E., Baker, C. S., Stolz, D. B., and Griffith, L. G. (2002) Functional Behavior of Primary Rat Liver Cells in a Three-Dimensional Perfused Microarray Bioreactor Tissue Eng. 8, 499-513
116. Powers, M. J., Domansky, K., Kaazempur-Mofrad, M. R., Kalezi, A., Capitano, A., Upadhyaya, A., Kurzawski, P., Wack, K. E., Stolz, D. B., Kamm, R., and Griffith, L. G. (2002) A microfabricated array bioreactor for perfused 3D liver culture Biotechnol. Bioeng. 78, 257-269
117. Lee, P. J., Hung, P. J., and Lee, L. P. (2007) An artificial liver sinusoid with a microfluidic endothelial-like barrier for primary hepatocyte culture Biotechnol. Bioeng. 97, 1340-1346
118. Tibbitt, M. W. and Anseth, K. S. (2009) Hydrogels as extracellular matrix mimics for 3D cell culture Biotechnol. Bioeng. 103, 655-663
119. Whitesides, G. M., Ostuni, E., Takayama, S., Jiang, X., and Ingber, D. E. (2001) Soft lithography in biology and biochemistry Annu. Rev. Biomed. Eng. 3, 335-373
120. Kane, R. S., Takayama, S., Ostuni, E., Ingber, D. E., and Whitesides, G. M. (1999) Patterning proteins and cells using soft lithography Biomaterials 20, 2363-2376
121. Sung, J. H., Kam, C., and Shuler, M. L. (2010) A microfluidic device for a pharmacokinetic-pharmacodynamic (PK-PD) model on a chip Lab Chip 10, 446-455
122. Miller, J. S., Stevens, K. R., Yang, M. T., Baker, B. M., Nguyen, D.-H. T., Cohen, D. M., Toro, E., Chen, A. A., Galie, P. A., Yu, X., Chaturvedi, R., Bhatia, S. N., and Chen, C. S. (2012) Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues Nat. Mater. 11, 768-774
123. Huh, D., Matthews, B. D., Mammoto, A., Montoya-Zavala, M., Hsin, H. Y., and Ingber, D. E. (2010) Reconstituting Organ-Level Lung Functions on a Chip Science 328, 1662-1668
124. Nakao, Y., Kimura, H., Sakai, Y., and Fujii, T. (2011) Bile canaliculi formation by aligning rat primary hepatocytes in a microfluidic device Biomicrofluidics 5, 022212
125. Allen, J. W., Khetani, S. R., and Bhatia, S. N. (2005) In Vitro Zonation and Toxicity in a Hepatocyte Bioreactor Toxicol. Sci. 84, 110-119
126. Jang, K.-J. and Suh, K.-Y. (2010) A multi-layer microfluidic device for efficient culture and analysis of renal tubular cells Lab Chip 10, 36-42
127. Griffith, L. G. and Swartz, M. A. (2006) Capturing complex 3D tissue physiology in vitro Nat. Rev. Mol. Cell Biol. 7, 211-224
128. Lee, G. Y., Kenny, P. A., Lee, E. H., and Bissell, M. J. (2007) Three-dimensional culture models of normal and malignant breast epithelial cells Nat. Methods 4, 359-365
129. Van Vlierberghe, S., Dubruel, P., and Schacht, E. (2011) Biopolymer-based hydrogels as scaffolds for tissue engineering applications: A review Biomacromolecules 12, 1387-1408
130. Patterson, J., Martino, M. M., and Hubbell, J. A. (2010) Biomimetic materials in tissue engineering Mater. Today 13, 14-22
131. Huh, D., Hamilton, G. A., and Ingber, D. E. (2011) From 3D cell culture to organs-on-chips Trends Cell Biol. 21, 745-754