Dense type I collagen matrices that support cellular remodeling and microfabrication for studies of tumor angiogenesis and vasculogenesis in vitro

Biomaterials

Volumn 31, Issue 33, 2010, Pages 8596-8607

  Cross, Valerie L ^a   Zheng, Ying ^a   Won Choi, Nak ^a   Verbridge, Scott S ^a   Sutermaster, Bryan A ^a   Bonassar, Lawrence J ^a   Fischbach, Claudia ^a   Stroock, Abraham D ^a  

^a Cornell University   (United States)

Author keywords

Endothelial cells; Microfluidic biomaterials; Three dimensional; Tumor angiogenesis; Type I collagen; Vasculogenesis

Indexed keywords

CELLULAR PROCESS; COCULTURE; COLLAGEN MATRICES; CONFINED COMPRESSION; EXTRACELLULAR MATRICES; FIBER DIMENSIONS; GEOMETRICAL FEATURES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HYDRAULIC PERMEABILITY; IN-VITRO; IN-VIVO; LONGITUDINAL MODULUS; LOW MASS; MASS FRACTION; MICROFLUIDIC CONTROL; MICROFLUIDIC NETWORKS; QUANTITATIVE CHARACTERIZATION; THREE DIMENSIONAL CELL CULTURE; TISSUE CELLS; TISSUE ENGINEERED CONSTRUCTS; TUMOR ANGIOGENESIS; TUMOR CELLS; TYPE I COLLAGEN; VASCULARIZATION; VASCULOGENESIS;

ADHESION; ANIMAL CELL CULTURE; BIOLOGICAL MATERIALS; BIOMATERIALS; CELL ADHESION; CELL CULTURE; COLLAGEN; CONFOCAL MICROSCOPY; HYDRATES; HYDRATION; MICROANALYSIS; MICROFABRICATION; MICROFLUIDICS; MICROMACHINING; SCAFFOLDS; SELF ASSEMBLY; THREE DIMENSIONAL; TUMORS;

ENDOTHELIAL CELLS;

COLLAGEN TYPE 1;

ANGIOGENESIS; ARTICLE; CELL ADHESION; CELL GROWTH; COMPRESSION; CONFOCAL MICROSCOPY; DENSITY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYDRAULIC PERMEABILITY; IN VITRO STUDY; MICROFLUIDICS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; TISSUE CULTURE; TISSUE ENGINEERING; TUMOR CELL; YOUNG MODULUS;

ANIMALS; CELL LINE, TUMOR; COCULTURE TECHNIQUES; COLLAGEN TYPE I; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; GELS; HUMANS; MECHANICAL PHENOMENA; MICROFLUIDICS; MICROSCOPY, CONFOCAL; MICROTECHNOLOGY; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; POROSITY; RATS; TIME FACTORS;

EID: 77957307766     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2010.07.072     Document Type: Article

References (59)

1. Langer R., Vacanti J.P. Tissue engineering. Science 1993, 260:920-926.
2. Pedersen J.A., Swartz M.A. Mechanobiology in the third dimension. Ann Biomed Eng 2005, 33:1469-1490.
3. Nelson C.M., Vanduijn M.M., Inman J.L., Fletcher D.A., Bissell M.J. Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures. Science 2006, 314:298-300.
4. Fidler I.J. Critical factors in the biology of human cancer metastasis: twenty-eighth G.H.A. Clowes memorial award lecture. Cancer Res 1990, 50:6130-6138.
5. Ferrara N. VEGF and the quest for tumour angiogenesis factors. Nat Rev Cancer 2002, 2:795-803.
6. Levenberg S., Rouwkema J., Macdonald M., Garfein E.S., Kohane D.S., Darland D.C., et al. Engineering vascularized skeletal muscle tissue. Nat Biotechnol 2005, 23:879-884.
7. Discher D.E., Janmey P., Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
8. Sieminski A.L., Hebbel R.P., Gooch K.J. The relative magnitudes of endothelial force generation and matrix stiffness modulate capillary morphogenesis in vitro. Exp Cell Res 2004, 297:574-584.
9. Reinhart-King C.A., Dembo M., Hammer D.A. Cell-cell mechanical communication through compliant substrates. Biophys J 2008, 95:6044-6051.
10. Fischbach C., Kong H.J., Hsiong S.X., Evangelista M.B., Yuen W., Mooney D.J. Cancer cell angiogenic capability is regulated by 3D culture and integrin engagement. Proc Natl Acad Sci U S A 2009, 106:399-404.
11. Anseth K.S., Bowman C.N., Brannon-Peppas L. Mechanical properties of hydrogels and their experimental determination. Biomaterials 1996, 17:1647-1657.
12. Jo S., Shin H., Mikos A.G. Modification of oligo(poly(ethylene glycol) fumarate) macromer with a GRGD peptide for the preparation of functionalized polymer networks. Biomacromolecules 2001, 2:255-261.
13. Kloxin A.M., Kasko A.M., Salinas C.N., Anseth K.S. Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science 2009, 324:59-63.
14. Lutolf M.P., Hubbell J.A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 2005, 23:47-55.
15. Choi N.W., Cabodi M., Held B., Gleghorn J.P., Bonassar L.J., Stroock A.D. Microfluidic scaffolds for tissue engineering. Nat Mater 2007, 6:908-915.
16. Williams B.R., Gelman R.A., Poppke D.C., Piez K.A. Collagen fibril formation- optimal in vitro conditions and preliminary kinetic results. J Biol Chem 1978, 253:6578-6585.
17. Elsdale T., Bard J. Collagen substrata for studies on cell behavior. J Cell Biol 1972, 54:626-637.
18. Folkman J., Haudenschild C. Angiogenesis in vitro. Nature 1980, 288:551-556.
19. Ceballos D., Navarro X., Dubey N., Wendelschafer-Crabb G., Kennedy W.R., Tranquillo R.T. Magnetically aligned collagen gel filling a collagen nerve guide improves peripheral nerve regeneration. Exp Neurol 1999, 158:290-300.
20. Eschenhagen T., Fink C., Remmers U., Scholz H., Wattchow J., Weil J., et al. Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system. FASEB J 1997, 11:683-694.
21. Davis G.E., Black S.M., Bayless K.J. Capillary morphogenesis during human endothelial cell invasion of three-dimensional collagen matrices. Vitro Cell Dev Biol Anim 2000, 36:513-519.
22. Bell E., Ivarsson B., Merrill C. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc Natl Acad Sci U S A 1979, 76:1274-1278.
23. Mueller-Klieser W. Tumor biology and experimental therapeutics. Crit Rev Oncol Hematol 2000, 36:123-139.
24. Knapp D.M., Barocas V.H., Moon A.G., Yoo K., Petzold L.R., Tranquillo R.T. Rheology of reconstituted type I collagen gel in confined compression. J Rheol 1997, 41:971-993.
25. Vernon R.B., Sage E.H. Contraction of fibrillar type I collagen by endothelial cells: a study in vitro. J Cell Biochem 1996, 60:185-197.
26. Ramanujan S., Pluen A., McKee T.D., Brown E.B., Boucher Y., Jain R.K. Diffusion and convection in collagen gels: implications for transport in the tumor interstitium. Biophys J 2002, 83:1650-1660.
27. Tien J., Nelson C.M., Chen C.S. Fabrication of aligned microstructures with a single elastomeric stamp. Proc Natl Acad Sci U S A 2002, 99:1758-1762.
28. Chrobak K.M., Potter D.R., Tien J. Formation of perfused, functional microvascular tubes in vitro. Microvasc Res 2006, 71:185-196.
29. Golden A.P., Tien J. Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. Lab Chip 2007, 7:720-725.
30. Yannas I.V., Burke J.F. Design of an artificial skin- basic design principles. J Biomed Mater Res 1980, 14:65-81.
31. Lee C.R., Grodzinsky A.J., Spector M. The effects of cross-linking of collagen-glycosaminoglycan scaffolds on compressive stiffness, chondrocyte-mediated contraction, proliferation and biosynthesis. Biomaterials 2001, 22:3145-3154.
32. Vernon R.B., Gooden M.D., Lara S.L., Wight T.N. Native fibrillar collagen membranes of micron-scale and submicron thicknesses for cell support and perfusion. Biomaterials 2005, 26:1109-1117.
33. Goo H.C., Hwang Y.S., Choi Y.R., Cho H.N., Suh H. Development of collagenase-resistant collagen and its interaction with adult human dermal fibroblasts. Biomaterials 2003, 24:5099-5113.
34. Helary C., Ovtracht L., Coulomb B., Godeau G., Giraud-Guille M.M. Dense fibrillar collagen matrices: a model to study myofibroblast behaviour during wound healing. Biomaterials 2006, 27:4443-4452.
35. Davis G.E., Senger D.R. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res 2005, 97:1093-1107.
36. Fischbach C., Chen R., Matsumoto T., Schmelzle T., Brugge J.S., Polverini P.J., et al. Engineering tumors with 3D scaffolds. Nat Methods 2007, 4:855-860.
37. Bornstein M.B. Reconstituted rattail collagen used as substrate for tissue cultures on coverslips in maximow slides and roller tubes. Lab Invest 1958, 7:134-137.
38. Whitesides G.M., Ostuni E., Takayama S., Jiang X., Ingber D.E. Soft lithography in biology and biochemistry. Annu Rev Biomed Eng 2001, 3:335-373.
39. Hermanson G. Bioconjugate techniques 1996, Elsevier Science, San Diego, CA.
40. Brightman A.O., Rajwa B.P., Sturgis J.E., McCallister M.E., Robinson J.P., Voytik-Harbin S.L. Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro. Biopolymers 2000, 54:222-234.
41. Roy R., Boskey A., Bonassar L.J. Processing of type I collagen gels using nonenzymatic glycation. J Biomed Mater Res A 2009.
42. Quinn T.M., Grodzinsky A.J. Longitudinal modulus and hydraulic permeability of poly(methacrylic acid) gels - effects of charge-density and solvent content. Macromolecules 1993, 26:4332-4338.
43. Barocas V.H., Tranquillo R.T. An anisotropic biphasic theory of tissue-equivalent mechanics: the interplay among cell traction, fibrillar network deformation, fibril alignment, and cell contact guidance. J Biomech Eng 1997, 119:137-145.
44. Pluen A., Netti P.A., Jain R.K., Berk D.A. Diffusion of macromolecules in agarose gels: comparison of linear and globular configurations. Biophys J 1999, 77:542-552.
45. Levick J.R. Flow through interstitium and other fibrous matrices. Q J Exp Physiol 1987, 72:409-437.
46. Verbridge S.S., Choi N.W., Zheng Y., Brooks D.J., Stroock A.D., Fischbach C. Oxygen-controlled three-dimensional cultures to analyze tumor angiogenesis. Tissue Eng Part A 2010, 16:2133-2141.
47. Kuntz R.M., Saltzman W.M. Neutrophil motility in extracellular matrix gels: mesh size and adhesion affect speed of migration. Biophys J 1997, 72:1472-1480.
48. Roeder B.A., Kokini K., Sturgis J.E., Robinson J.P., Voytik-Harbin S.L. Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure. J Biomech Eng 2002, 124:214-222.
49. Nakagawa S., Pawelek P., Grinnell F. Extracellular matrix organization modulates fibroblast growth and growth factor responsiveness. Exp Cell Res 1989, 182:572-582.
50. Engler A.J., Sweeney H.L., Discher D.E., Schwarzbauer J.E. Extracellular matrix elasticity directs stem cell differentiation. J Musculoskelet Neuronal Interact 2007, 7:335.
51. Oster G.F., Murray J.D., Harris A.K. Mechanical aspects of mesenchymal morphogenesis. J Embryol Exp Morphol 1983, 78:83-125.
52. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
53. Netti P.A., Berk D.A., Swartz M.A., Grodzinsky A.J., Jain R.K. Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 2000, 60:2497-2503.
54. Levick J.R. Flow through interstitium and other fibrous matrices. Q J Exp Physiol Cogn Med Sci 1987, 72:409-438.
55. Tang M.D., Golden A.P., Tien J. Molding of three-dimensional microstructures of gels. J Am Chem Soc 2003, 125:12988-12989.
56. Cabodi M., Cross V.L., Qu Z., Havenstrite K.L., Schwartz S., Stroock A.D. An active wound dressing for controlled convective mass transfer with the wound bed. J Biomed Mater Res B Appl Biomater 2007, 82:210-222.
57. Perry R.H., Green D.W. Chemical Engineers' Handbook 1997, McGraw-Hill, New York.
58. Davis G.E., Pintar Allen K.A., Salazar R., Maxwell S.A. Matrix metalloproteinase-1 and -9 activation by plasmin regulates a novel endothelial cell-mediated mechanism of collagen gel contraction and capillary tube regression in three-dimensional collagen matrices. J Cell Sci 2001, 114:917-930.
59. Stroock A.D., Fischbach C. Microfluidic culture models of tumor angiogenesis. Tissue Eng Part A 2010, 16:2143-2146.