Three-dimensional microfluidic collagen hydrogels for investigating flow-mediated tumor-endothelial signaling and vascular organization

Tissue Engineering - Part C: Methods

Volumn 20, Issue 1, 2014, Pages 64-75

  Buchanan, Cara F ^a   Voigt, Elizabeth E ^b   Szot, Christopher S ^a   Freeman, Joseph W ^c   Vlachos, Pavlos P ^a,b   Rylander, Marissa Nichole ^a,b  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b State University   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD VESSELS; CELL CULTURE; COLLAGEN; ENDOTHELIAL CELLS; FLOW RATE; GENE EXPRESSION; HYDRODYNAMICS; HYDROGELS; MICROCHANNELS; MICROFLUIDICS; PHYSIOLOGICAL MODELS; PHYSIOLOGY; SELF ASSEMBLY; SHEAR STRESS; THREE DIMENSIONAL;

CYLINDRICAL MICROCHANNELS; HYDRODYNAMIC STRESS; INTERSTITIAL FLUID PRESSURES; MICRO PARTICLE IMAGE VELOCIMETRY; QUANTITATIVE MEASUREMENT; QUANTITATIVE RT-PCR; THREE-DIMENSIONAL MICROFLUIDICS; TUMOR MICROENVIRONMENT;

TUMORS;

COLLAGEN GEL;

ARTICLE; COCULTURE; ENDOTHELIUM CELL; FLOW RATE; HYDRODYNAMICS; HYDROGEL; MICROFLUIDICS; PARTICLE IMAGE VELOCIMETRY; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEAR STRESS; SIGNAL TRANSDUCTION; TUMOR CELL CULTURE; TUMOR VASCULARIZATION;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; COCULTURE TECHNIQUES; COLLAGEN; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HYDROGELS; MICROFLUIDIC ANALYTICAL TECHNIQUES; NEOPLASMS; RATS; REFRACTOMETRY; RHEOLOGY; SIGNAL TRANSDUCTION;

EID: 84890931713     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2012.0731     Document Type: Article

References (85)

1. Butler, T.P., Grantham, F.H., and Gullino, P.M. Bulk transfer of fluid in the interstitial compartment of mammary tumors. Cancer Res 35, 3084, 1975.
2. Vaupel, P., Kallinowski, F., and Okunieff, P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 49, 6449, 1989.
3. Fukumura, D., and Jain, R.K. Tumor microenvironment abnormalities: causes, consequences, and strategies to normalize. J Cell Biochem 101, 937, 2007.
4. Jain, R.K. Determinants of tumor blood flow: a review. Cancer Res 48, 2641, 1988.
5. Jain, R.K. Vascular and Interstitial Biology of Tumors. Philadelphia: Elsevier, 2004.
6. Shieh, A.C. Biomechanical forces shape the tumor microenvironment. Ann Biomed Eng 39, 1379, 2011.
7. Jang, S.H., Wientjes, M.G., Lu, D., and Au, J.L. Drug delivery and transport to solid tumors. Pharm Res 20, 1337, 2003.
8. Tredan, O., Galmarini, C.M., Patel, K., and Tannock, I.F. Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst 99, 1441, 2007.
9. Galmarini, F.C., Galmarini, C.M., Sarchi, M.I., Abulafia, J., and Galmarini, D. Heterogeneous distribution of tumor blood supply affects the response to chemotherapy in patients with head and neck cancer. Microcirculation 7, 405, 2000.
10. Baxter, L.T., and Jain, R.K. Transport of fluid and macromolecules in tumors. I. Role of interstitial pressure and convection. Microvasc Res 37, 77, 1989.
11. Tarbell, J.M. Shear stress and the endothelial transport barrier. Cardiovasc Res 87, 320, 2010.
12. Miteva, D.O., Rutkowski, J.M., Dixon, J.B., Kilarski, W., Shields, J.D., and Swartz, M.A. Transmural flow modulates cell and fluid transport functions of lymphatic endothelium. Circ Res 106, 920, 2010.
13. Dewey, C.F., Jr., Bussolari, S.R., Gimbrone, M.A., Jr., and Davies, P.F. The dynamic response of vascular endothelial cells to fluid shear stress. J Biomech Eng 103, 177, 1981.
14. Lawler, K., Foran, E., O'Sullivan, G., Long, A., and Kenny, D. Mobility and invasiveness of metastatic esophageal cancer are potentiated by shear stress in a ROCK-and Ras-dependent manner. Am J f Physiol Cell Physiol 291, C668, 2006.
15. Chang, S.F., Chang, C.A., Lee, D.Y., Leet, P.L., Yeh, Y.M., Yeh, C.R., et al. Tumor cell cycle arrest induced by shear stress: roles of integrins and Smad. Proc Natl Acad Sci U S A 105, 3927, 2008.
16. Shieh, A.C., and Swartz, M.A. Regulation of tumor invasion by interstitial fluid flow. Phys Biol 8, 015012, 2011.
17. Polacheck, W.J., Charest, J.L., and Kamm, R.D. Interstitial flow influences direction of tumor cell migration through competing mechanisms. Proc Natl Acad Sci U S A 108, 11115, 2011.
18. Rutkowski, J.M., and Swartz, M.A. A driving force for change: interstitial flow as a morphoregulator. Trends Cell Biol 17, 44, 2007.
19. Shields, J.D., Fleury, M.E., Yong, C., Tomei, A.A., Randolph, G.J., and Swartz, M.A. Autologous chemotaxis as a mechanism of tumor cell homing to lymphatics via interstitial flow and autocrine CCR7 signaling. Cancer Cell 11, 526, 2007.
20. Hompland, T., Ellingsen, C., Ovrebo, K.M., and Rofstad, E.K. Interstitial fluid pressure and associated lymph node metastasis revealed in tumors by dynamic contrastenhanced MRI. Cancer Res 72, 4899, 2012.
21. Tchafa, A.M., Shah, A.D., Wang, S., Duong, M.T., and Shieh, A.C. Three-dimensional cell culture model for measuring the effects of interstitial fluid flow on tumor cell invasion. J Vis Exp 65, pii: 4159, 2012.
22. Haessler, U., Teo, J.C., Foretay, D., Renaud, P., and Swartz, M.A. Migration dynamics of breast cancer cells in a tunable 3D interstitial flow chamber. Integr Biol (Camb) 4, 401, 2012.
23. Shieh, A.C., Rozansky, H.A., Hinz, B., and Swartz, M.A. Tumor cell invasion is promoted by interstitial flow-induced matrix priming by stromal fibroblasts. Cancer Res 71, 790, 2011.
24. Hewett, P., Popplewell, A., Finney, H., and Murray, J.C. Changes in microvessel endothelial cell gene expression in an in vitro human breast tumour endothelial cell model. Angiogenesis 3, 221, 1999.
25. Khodarev, N.N., Yu, J., Labay, E., Darga, T., Brown, C.K., Mauceri, H.J., et al. Tumour-endothelium interactions in coculture: coordinated changes of gene expression profiles and phenotypic properties of endothelial cells. J Cell Sci 116, 1013, 2003.
26. Buchanan, C.F., Szot, C.S., Wilson, T.D., Akman, S., Metheny-Barlow, L.J., Robertson, J.L., et al. Cross-talk between endothelial and breast cancer cells regulates reciprocal expression of angiogenic factors in vitro. J Cell Biochem113, 1142, 2012.
27. Kaneko, T., Zhang, Z., Mantellini, M.G., Karl, E., Zeitlin, B., Verhaegen, M., et al. Bcl-2 orchestrates a cross-talk between endothelial and tumor cells that promotes tumor growth. Cancer Res 67, 9685, 2007.
28. Zeng, Q.H., Li, S.L., Chepeha, D.B., Giordano, T.J., Li, J., Zhang, H.L., et al. Crosstalk between tumor and endothelial cells promotes tumor angiogenesis by MAPK activation of Notch signaling. Cancer Cell 8, 13, 2005.
29. Kim, J.B. Three-dimensional tissue culture models in cancer biology. Semin Cancer Biol 15, 365, 2005.
30. Fischbach, C., Chen, R., Matsumoto, T., Schmelzle, T., Brugge, J.S., Polverini, P.J., et al. Engineering tumors with 3D scaffolds. Nat Methods 4, 855, 2007.
31. Cross, V.L., Zheng, Y., Choi, N.W., Verbridge, S.S., Sutermaster, B.A., Bonassar, L.J., et al. Dense type I collagen matrices that support cellular remodeling and microfabrication for studies of tumor angiogenesis and vasculogenesis in vitro. Biomaterials 31, 8596, 2010.
32. Fischbach, C., and Mooney, D.J. Polymers for pro-and antiangiogenic therapy. Biomaterials 28, 2069, 2007.
33. Szot, C.S., Buchanan, C.F., Freeman, J.W., and Rylander, M.N. 3D in vitro bioengineered tumors based on collagen I hydrogels. Biomaterials 32, 7905, 2011.
34. Song, J.W., Bazou, D., and Munn, L.L. Anastomosis of endothelial sprouts forms new vessels in a tissue analogue of angiogenesis. Integr Biol (Camb) 4, 857, 2012.
35. Zervantonakis, I.K., Hughes-Alford, S.K., Charest, J.L., Condeelis, J.S., Gertler, F.B., and Kamm, R.D. Three-dimensional microfluidic model for tumor cell intravasation and endothelial barrier function. Proc Natl Acad Sci U S A 109, 13515, 2012.
36. Zheng, Y., Chen, J., Craven, M., Choi, N.W., Totorica, S., Diaz-Santana, A., et al. In vitro microvessels for the study of angiogenesis and thrombosis. Proc Natl Acad Sci U S A 109, 9342, 2012.
37. Wereley, S.T., and Meinhart, C.D. Recent advances in microparticle image velocimetry. Annu Rev Fluid Mech42, 557, 2010.
38. Fouras, A., Kitchen, M.J., Dubsky, S., Lewis, R.A., Hooper, S.B., and Hourigan, K. The past, present, and future of x-ray technology for in vivo imaging of function and form. J Appl Phys 105, 102009, 2009.
39. Meinhart, C.D., Wereley, S.T., and Santiago, J.G. PIV measurements of a microchannel flow. Exp Fluids 27, 414, 1999.
40. Adrian, R.J. Particle-imaging techniques for experimental fluid-mechanics. Annu Rev Fluid Mech 23, 261, 1991.
41. Adrian, R.J. Twenty years of particle image velocimetry. Exp Fluids 39, 159, 2005.
42. Sitterley, G. Collagen Attachment Protocols, Solubility, and Stability. Bio Files. 3.8, 5th edition. St. Louis, MO: Sigma-Aldrich Co., LLC, 2008.
43. Netti, P.A., Berk, D.A., Swartz, M.A., Grodzinsky, A.J., and Jain, R.K. Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 60, 2497, 2000.
44. Paszek, M.J., Zahir, N., Johnson, K.R., Lakins, J.N., Rozenberg, G.I., Gefen, A., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241, 2005.
45. Chrobak, K.M., Potter, D.R., and Tien, J. Formation of perfused, functional microvascular tubes in vitro. Microvasc Res 71, 185, 2006.
46. Daimon, M., and Masumura, A. Measurement of the refractive index of distilled water from the near-infrared region to the ultraviolet region. Appl Opt 46, 3811, 2007.
47. Focus on: FEP. In: Zeus, ed. Raritan, NJ: Zeus Industrial Products, Inc., 2006.
48. Corning® 18x18mm Square #1 Cover Glass (Product #2885-18). Kennebunk, ME: Corning, Inc., 2011.
49. Topper, J.N., and Gimbrone, M.A., Jr. Blood flow and vascular gene expression: fluid shear stress as a modulator of endothelial phenotype. Mol Med Today 5, 40, 1999.
50. Inoguchi, H., Tanaka, T., Maehara, Y., and Matsuda, T. The effect of gradually graded shear stress on the morphological integrity of a huvec-seeded compliant small-diameter vascular graft. Biomaterials 28, 486, 2007.
51. Verbridge, S.S., Choi, N.W., Zheng, Y., Brooks, D.J., Stroock, A.D., and Fischbach, C. Oxygen-controlled three-dimensional cultures to analyze tumor angiogenesis. Tissue Eng Part A 16, 2133, 2010.
52. Whitney, J.R., Rodgers, A., Harvie, E., Carswell, W.F., Torti, S., Puretzky, A.A., et al. Spatial and temporal measurements of temperature and cell viability in response to nanoparticlemediated photothermal therapy. Nanomedicine (Lond) 7, 1729, 2012.
53. Eckstein, A., and Vlachos, P.P. Assessment of advanced windowing techniques for digital particle image velocimetry (DPIV). Meas Sci Technol 20, 075402, 2009.
54. Eckstein, A., and Vlachos, P.P. Digital particle image velocimetry (DPIV) robust phase correlation. Meas Sci Technol 20, 055401, 2009.
55. Eckstein, A.C., Charonko, J., and Vlachos, P. Phase correlation processing for DPIV measurements. Exp Fluids 45, 485, 2008.
56. Westerweel, J., Dabiri, D., and Gharib, M. The effect of a discrete window offset on the accuracy of cross-correlation analysis of digital PIV recordings. Exp Fluids 23, 20, 1997.
57. Westerweel, J., and Scarano, F. Universal outlier detection for PIV data. Exp Fluids 39, 1096, 2005.
58. Delnoij, E., Westerweel, J., Deen, N.G., Kuipers, J.A.M., and van Swaaij, W.P.M. Ensemble correlation PIV applied to bubble plumes rising in a bubble column. Chem Eng Sci 54, 5159, 1999.
59. Karri, S., Charonko, J., and Vlachos, P.P. Robust wall gradient estimation using radial basis functions and proper orthogonal decomposition (POD) for particle image velocimetry (PIV) measured fields. Meas Sci Technol 20, 045401, 2009.
60. Voigt, E.E., Buchanan, C.F., Rylander, M.N., and Vlachos, P.P. Wall shear stress measurements in an arterial flow bioreactor. Cardiovasc Eng Technol 3, 101, 2012.
61. Carmeliet, P., and Jain, R.K. Angiogenesis in cancer and other diseases. Nature 407, 249, 2000.
62. Livak, K.J., and Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402, 2001.
63. Butcher, D.T., Alliston, T., and Weaver, V.M. A tense situation: forcing tumour progression. Nat Rev Cancer 9, 108, 2009.
64. Fischbach, C., Kong, H.J., Hsiong, S.X., Evangelista, M.B., Yuen, W., and Mooney, D.J. Cancer cell angiogenic capability is regulated by 3D culture and integrin engagement. Proc Natl Acad Sci U S A 106, 399, 2009.
65. Song, J.W., and Munn, L.L. Fluid forces control endothelial sprouting. Proc Natl Acad Sci U S A 108, 15342, 2011.
66. Less, J.R., Skalak, T.C., Sevick, E.M., and Jain, R.K. Microvascular architecture in a mammary carcinoma: branching patterns and vessel dimensions. Cancer Res 51, 265, 1991.
67. Montesano, R., Pepper, M.S., and Orci, L. Paracrine induction of angiogenesis in vitro by Swiss 3T3 fibroblasts. J Cell Sci 105, 1013, 1993.
68. Correa de Sampaio, P., Auslaender, D., Krubasik, D., Failla, A.V., Skepper, J.N., Murphy, G., et al. A heterogeneous in vitro three dimensional model of tumour-stroma interactions regulating sprouting angiogenesis. PLoS One 7, e30753. 2012.
69. Etebari, A., and Vlachos, P.P. Improvements on the accuracy of derivative estimation from DPIV velocity measurements. Exp Fluids 39, 1040, 2005.
70. Ali Etebari, J.C., and Vlachos, P. On the Accuracy of Wall Shear Stress using DPIV. Presented at the Heat Transfer/Fluids Engineering Summer Conference, Charlotte, NC.
71. Santiago, J.G., Wereley, S.T., Meinhart, C.D., Beebe, D.J., and Adrian, R.J. A particle image velocimetry system for microfluidics. Exp Fluids 25, 316, 1998.
72. De Boodt, S., Truscello, S., Ozcan, S.E., Leroy, T., Van Oosterwyck, H., Berckmans, D., et al. Bi-modular flow characterization in tissue engineering scaffolds using computational fluid dynamics and particle imaging velocimetry. Tissue Eng Part C Methods 16, 1553, 2010.
73. Stroock, A.D., and Fischbach, C. Microfluidic culture models of tumor angiogenesis. Tissue Eng Part A 16, 2143, 2010.
74. Walsh, C.L., Babin, B.M., Kasinskas, R.W., Foster, J.A., McGarry, M.J., and Forbes, N.S. A multipurpose microfluidic device designed to mimic microenvironment gradients and develop targeted cancer therapeutics. Lab Chip 9, 545, 2009.
75. Wlodkowic, D., and Cooper, J.M. Tumors on chips: oncology meets microfluidics. Curr Opin Chem Biol 14, 556, 2010.
76. Squires, T.M., and Quake, S.R. Microfluidics: fluid physics at the nanoliter scale. Rev Modern Phys 77, 977, 2005.
77. Vickerman, V., Blundo, J., Chung, S., and Kamm, R. Design, fabrication and implementation of a novel multi-parameter control microfluidic platform for three-dimensional cell culture and real-time imaging. Lab Chip 8, 1468, 2008.
78. Chung, S., Sudo, R., Mack, P.J., Wan, C.R., Vickerman, V., and Kamm, R.D. Cell migration into scaffolds under coculture conditions in a microfluidic platform. Lab Chip 9, 269, 2009.
79. Cheng, S.Y., Heilman, S., Wasserman, M., Archer, S., Shuler, M.L., and Wu, M.M. Ahydrogel-based microfluidic device for the studies of directed cell migration. Lab Chip 7, 763, 2007.
80. Chung, S., Sudo, R., Vickerman, V., Zervantonakis, I.K., and Kamm, R.D. Microfluidic platforms for studies of angiogenesis, cell migration, and cell-cell interactions. Sixth International Bio-Fluid Mechanics Symposium and Workshop March 28-30, 2008 Pasadena, California. Ann Biomed Eng 38, 1164, 2010.
81. Cheng, G., Liao, S., Kit Wong, H., Lacorre, D.A., di Tomaso, E., Au, P., et al. Engineered blood vessel networks connect to host vasculature via wrapping-and-tapping anastomosis. Blood 118, 4740, 2011.
82. Song, J.W., Daubriac, J., Tse, J.M., Bazou, D., and Munn, L.L. RhoA mediates flow-induced endothelial sprouting in a 3-D tissue analogue of angiogenesis. Lab Chip 12, 5000, 2012.
83. Polacheck, W.J., Zervantonakis, I.K., and Kamm, R.D. Tumor cell migration in complex microenvironments. Cell Mol Life Sci 70, 1335, 2013.
84. Saadi, W., Rhee, S.W., Lin, F., Vahidi, B., Chung, B.G., and Jeon, N.L. Generation of stable concentration gradients in 2D and 3D environments using a microfluidic ladder chamber. Biomed Microdevices 9, 627, 2007.
85. Shin, Y., Han, S., Jeon, J.S., Yamamoto, K., Zervantonakis, I.K., Sudo, R., et al. Microfluidic assay for simultaneous culture of multiple cell types on surfaces or within hydrogels. Nat Protoc 7, 1247, 2012.