Investigating endothelial invasion and sprouting behavior in three-dimensional collagen matrices (original) (raw)

• Egeblad, M. et al. Visualizing stromal cell dynamics in different tumor microenvironments by spinning disk confocal microscopy. Dis. Model. Mech. 1, 155–167 (2008); discussion 165.
  Article PubMed PubMed Central Google Scholar
• Kedrin, D. et al. Intravital imaging of metastatic behavior through a mammary imaging window. Nat. Methods 5, 1019–1021 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Kedrin, D., Wyckoff, J., Sahai, E., Condeelis, J. & Segall, J.E. Imaging tumor cell movement in vivo. Current Protocols in Cell Biology Unit 19.7 (2007).
• Wolf, K. et al. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol. 9, 893–904 (2007).
  Article CAS PubMed Google Scholar
• Weiss, P. & Garber, B. Shape and movement of mesenchyme cells as functions of the physical structure of the medium: contributions to a quantitative morphology. Proc. Natl. Acad. Sci. USA 38, 264–280 (1952).
  Article CAS PubMed Google Scholar
• Harrison, R.G. The outgrowth of the nerve fiber as a mode of protoplasmic movement. J. Exp. Zool. 9, 787–846 (1910).
  Article Google Scholar
• Ehrmann, R.L. & Gey, G.O. The growth of cells on a transparent gel of reconstituted rat-tail collagen. J. Natl. Cancer Inst. 16, 1375–1403 (1956).
  CAS PubMed Google Scholar
• Elsdale, T. & Bard, J. Collagen substrata for studies on cell behavior. J. Cell Biol. 54, 626–637 (1972).
  Article CAS PubMed PubMed Central Google Scholar
• Davis, G.E. & Camarillo, C.W. An alpha 2 beta 1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix. Exp. Cell Res. 224, 39–51 (1996).
  Article CAS PubMed Google Scholar
• Aplin, A.C., Fogel, E., Zorzi, P. & Nicosia, R.F. The aortic ring model of angiogenesis. Methods Enzymol. 443, 119–136 (2008).
  Article CAS PubMed Google Scholar
• Liu, Y. & Senger, D.R. Matrix-specific activation of Src and Rho initiates capillary morphogenesis of endothelial cells. FASEB. J. 18, 457–468 (2004).
  Article CAS PubMed Google Scholar
• Sweeney, S.M. et al. Angiogenesis in collagen I requires alpha2beta1 ligation of a GFP*GER sequence and possibly p38 MAPK activation and focal adhesion disassembly. J. Biol. Chem. 278, 30516–30524 (2003).
  Article CAS PubMed Google Scholar
• Bayless, K.J. & Davis, G.E. Sphingosine-1-phosphate markedly induces matrix metalloproteinase and integrin-dependent human endothelial cell invasion and lumen formation in three-dimensional collagen and fibrin matrices. Biochem. Biophys. Res. Commun. 312, 903–913 (2003).
  Article CAS PubMed Google Scholar
• Koh, W., Stratman, A.N., Sacharidou, A. & Davis, G.E. In vitro three dimensional collagen matrix models of endothelial lumen formation during vasculogenesis and angiogenesis. Methods Enzymol. 443, 83–101 (2008).
  Article CAS PubMed Google Scholar
• Nakatsu, M.N. et al. Angiogenic sprouting and capillary lumen formation modeled by human umbilical vein endothelial cells (HUVEC) in fibrin gels: the role of fibroblasts and angiopoietin-1. Microvasc. Res. 66, 102–112 (2003).
  Article CAS PubMed Google Scholar
• Nicosia, R.F. & Madri, J.A. The microvascular extracellular matrix. Developmental changes during angiogenesis in the aortic ring-plasma clot model. Am. J. Pathol. 128, 78–90 (1987).
  CAS PubMed PubMed Central Google Scholar
• Nicosia, R.F., McCormick, J.F. & Bielunas, J. The formation of endothelial webs and channels in plasma clot culture. Scan. Electron Microsc. (Pt 2): 793–799 (1984).
• Nicosia, R.F., Tchao, R. & Leighton, J. Histotypic angiogenesis in vitro: light microscopic, ultrastructural, and radioautographic studies. In vitro 18, 538–549 (1982).
  Article CAS PubMed Google Scholar
• Nehls, V. & Drenckhahn, D. A novel, microcarrier-based in vitro assay for rapid and reliable quantification of three-dimensional cell migration and angiogenesis. Microvasc. Res. 50, 311–322 (1995).
  Article CAS PubMed Google Scholar
• Nehls, V., Schuchardt, E. & Drenckhahn, D. The effect of fibroblasts, vascular smooth muscle cells, and pericytes on sprout formation of endothelial cells in a fibrin gel angiogenesis system. Microvasc. Res. 48, 349–363 (1994).
  Article CAS PubMed Google Scholar
• Bell, S.E. et al. 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 (Pt 15): 2755–2773 (2001).
  CAS PubMed Google Scholar
• Su, S.C., Mendoza, E.A., Kwak, H.I. & Bayless, K.J. Molecular profile of endothelial invasion of three-dimensional collagen matrices: insights into angiogenic sprout induction in wound healing. Am. J. Physiol. 295, C1215–C1229 (2008).
  Article CAS Google Scholar
• Hahn, C.N. et al. Expression profiling reveals functionally important genes and coordinately regulated signaling pathway genes during in vitro angiogenesis. Physiol. Genomics 22, 57–69 (2005).
  Article CAS PubMed Google Scholar
• Kahn, J. et al. Gene expression profiling in an in vitro model of angiogenesis. Am. J. Pathol. 156, 1887–1900 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Koh, W., Mahan, R.D. & Davis, G.E. Cdc42- and Rac1-mediated endothelial lumen formation requires Pak2, Pak4 and Par3, and PKC-dependent signaling. J. Cell Sci. 121 (Pt 7): 989–1001 (2008).
  Article CAS PubMed Google Scholar
• Koh, W. et al. Formation of endothelial lumens requires a coordinated PKC{epsilon}-, Src-, Pak- and Raf-kinase-dependent signaling cascade downstream of Cdc42 activation. J. Cell Sci. 122 (Pt 11): 1812–1822 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Saunders, W.B. et al. Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3. J. Cell Biol. 175, 179–191 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Stratman, A.N. et al. Endothelial cell lumen and vascular guidance tunnel formation requires MT1-MMP-dependent proteolysis in 3D collagen matrices. Blood 114, 237–247 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Sainson, R.C. et al. Cell-autonomous notch signaling regulates endothelial cell branching and proliferation during vascular tubulogenesis. FASEB. J. 19, 1027–1029 (2005).
  Article CAS PubMed Google Scholar
• Sainson, R.C. et al. TNF primes endothelial cells for angiogenic sprouting by inducing a tip cell phenotype. Blood 111, 4997–5007 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Bayless, K.J. & Davis, G.E. The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. J. Cell Sci. 115 (Pt 6): 1123–1136 (2002).
  CAS PubMed Google Scholar
• Kamei, M., Saunders, W.B., Bayless, K.J., Dye, L., Davis, G.E. & Weinstein, B.M. Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 442, 453–456 (2006).
  Article CAS PubMed Google Scholar
• Kang, H., Bayless, K.J. & Kaunas, R. Fluid shear stress modulates endothelial cell invasion into three-dimensional collagen matrices. Am. J. Physiol. Heart Circ. Physiol. 295, H2087–H2097 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Lee, P.F., Yeh, A.T. & Bayless, K.J. Nonlinear optical microscopy reveals invading endothelial cells anisotropically alter three-dimensional collagen matrices. Exp. Cell Res. 315, 396–410 (2009).
  Article CAS PubMed Google Scholar
• Emonard, H. et al. Interactions between fibroblasts and a reconstituted basement membrane matrix. J. Invest. Dermatol. 89, 156–163 (1987).
  Article CAS PubMed Google Scholar
• Bikfalvi, A., Cramer, E.M., Tenza, D. & Tobelem, G. Phenotypic modulations of human umbilical vein endothelial cells and human dermal fibroblasts using two angiogenic assays. Biol. Cell 72, 275–278 (1991).
  Article CAS PubMed Google Scholar
• 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. 202, 1–8 (1992).
  Article CAS PubMed Google Scholar
• Hoying, J.B., Boswell, C.A. & Williams, S.K. Angiogenic potential of microvessel fragments established in three-dimensional collagen gels. In Vitro Cell Dev. Biol. Anim. 32, 409–419 (1996).
  Article CAS PubMed Google Scholar
• Hughes, C.C. Endothelial-stromal interactions in angiogenesis. Curr. Opin. Hematol. 15, 204–209 (2008).
  Article PubMed Google Scholar
• Bornstein, M.B. Reconstituted rattail collagen used as substrate for tissue cultures on coverslips in Maximow slides and roller tubes. Lab. Invest. 7, 134–137 (1958).
  CAS PubMed Google Scholar
• Rajan, N., Habermehl, J., Cote, M.F., Doillon, C.J. & Mantovani, D. Preparation of ready-to-use, storable and reconstituted type I collagen from rat tail tendon for tissue engineering applications. Nat. Protoc. 1, 2753–2758 (2006).
  Article CAS PubMed Google Scholar
• Dunlap, K.A. et al. Progesterone and placentation increase secreted phosphoprotein one (SPP1 or osteopontin) in uterine glands and stroma for histotrophic and hematotrophic support of ovine pregnancy. Biol. Reprod. 79, 983–990 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Engelse, M.A., Laurens, N., Verloop, R.E., Koolwijk, P. & van Hinsbergh, V.W. Differential gene expression analysis of tubule forming and non-tubule forming endothelial cells: CDC42GAP as a counter-regulator in tubule formation. Angiogenesis 11, 153–167 (2008).
  Article CAS PubMed Google Scholar
• Fisher, K.E., Pop, A., Koh, W., Anthis, N.J., Saunders, W.B. & Davis, G.E. Tumor cell invasion of collagen matrices requires coordinate lipid agonist-induced G-protein and membrane-type matrix metalloproteinase-1-dependent signaling. Mol. Cancer 5, 69 (2006).
  Article PubMed PubMed Central Google Scholar
• Kwak, H.I., Mendoza, E.A. & Bayless, K.J. ADAM17 co-purifies with TIMP-3 and modulates endothelial invasion responses in three-dimensional collagen matrices. Matrix Biol. 28, 470–479 (2009).
  Article CAS PubMed Google Scholar
• Kim, A., Lakshman, N. & Petroll, W.M. Quantitative assessment of local collagen matrix remodeling in 3-D culture: the role of Rho kinase. Exp. Cell Res. 312, 3683–3692 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Maciag, T., Cerundolo, J., Ilsley, S., Kelley, P.R. & Forand, R. An endothelial cell growth factor from bovine hypothalamus: identification and partial characterization. Proc. Natl. Acad. Sci. USA 76, 5674–5678 (1979).
  Article CAS PubMed Google Scholar
• Davis, G.E., Black, S.M. & Bayless, K.J. Capillary morphogenesis during human endothelial cell invasion of three-dimensional collagen matrices. In Vitro Cell Dev. Biol. Anim. 36, 513–519 (2000).
  Article CAS PubMed Google Scholar
• Iruela-Arispe, M.L. & Davis, G.E. Cellular and molecular mechanisms of vascular lumen formation. Dev. Cell 16, 222–231 (2009).
  Article CAS PubMed Google Scholar