Extracellular matrix density regulates the rate of neovessel growth and branching in sprouting angiogenesis

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Edgar, Lowell T ^a,b   Underwood, Clayton J ^a,c   Guilkey, James E ^a   Hoying, James B ^d   Weiss, Jeffrey A ^a,b  

^a University of Utah   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c W L GORE AND ASSOCIATES   (United States)

^d UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; VASCULOTROPIN A;

ANGIOGENESIS; ARTICLE; BLOOD VESSEL PARAMETERS; CELL DENSITY; COMPUTER MODEL; CONCEPTUAL FRAMEWORK; EXTRACELLULAR MATRIX; GROWTH RATE; IN VITRO STUDY; MALE; NEOVESSEL BRANCHING; NEOVESSEL GROWTH; NONHUMAN; RAT; RIGIDITY; ALGORITHM; ANIMAL; BIOLOGICAL MODEL; COMPUTER SIMULATION; CONFOCAL MICROSCOPY; CYTOLOGY; DRUG EFFECTS; ENDOTHELIUM CELL; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROVASCULATURE; MORPHOGENESIS; ORGAN CULTURE TECHNIQUE; PHASE CONTRAST MICROSCOPY; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT; TIME;

ALGORITHMS; ANIMALS; COLLAGEN; COMPUTER SIMULATION; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; MALE; MICROSCOPY, CONFOCAL; MICROSCOPY, PHASE-CONTRAST; MICROVESSELS; MODELS, BIOLOGICAL; MORPHOGENESIS; NEOVASCULARIZATION, PHYSIOLOGIC; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84893933629     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085178     Document Type: Article

References (48)

1. Fisher C, Gilbertson-Beadling S, Powers EA, Petzold G, Poorman R, et al. (1994) Interstitial collagenase is required for angiogenesis in vitro. Dev Biol 162: 499-510. (Pubitemid 24144126)
2. Haas TL, Davis SJ, Madri JA (1998) Three-dimensional type I collagen lattices induce coordinate expression of matrix metalloproteinases MT1-MMP and MMP-2 in microvascular endothelial cells. J Biol Chem 273: 3604-3610. (Pubitemid 28109785)
3. Vernon RB, Sage EH (1999) A novel, quantitative model for study of endothelial cell migration and sprout formation within three-dimensional collagen matrices. . Microvasc Res 57: 118-133. (Pubitemid 29393289)
4. Rivilis I, Milkiewicz M, Boyd P, Goldstein J, Brown MD, et al. (2002) Differential involvement of MMP-2 and VEGF during muscle stretch- versus shear stress-induced angiogenesis. . Am J Physiol Heart Circ Physiol 283: H1430-H1438.
5. Tranqui L, Tracqui P (2000) Mechanical signalling and angiogenesis. The integration of cell- extracellular matrix couplings. CR Acad Sci Paris Life Sci 323: 31-47. (Pubitemid 30128744)
6. Vailhe B, Ronot X, Tracqui P, Usson Y, Tranqui L (1997) In vitro angiogenesis is modulated by the mechanical properties of fibrin gels and is related to alpha(v)beta3 integrin localization. In Vitro Cell Dev Biol Anim 33: 763-773. (Pubitemid 28068280)
7. Vernon RB, Sage EH (1996) Contraction of fibrillar type I collagen by endothelial cells: a study in vitro. J Cell Biochem 60: 185-197. (Pubitemid 26069214)
8. Hur SS, Zhao Y, Li YS, Botvinick E, Chen S (2009) Live cells exert 3-dimensional traction forces on their substrata. Cell Mole Bioeng 2: 425-436.
9. Lopez JI, Mouw JK, Weaver VM (2008) Biomechanical regulation of cell orientation and fate. Ocogene 27: 6981-6993.
10. Reinhart-King CA, Dembo M, Hammer DA (2008) Cell-cell mechanical communication through compliant substrates. Biophys J 95: 6044-6051.
11. Hoying JB, Boswell CA, Williams SK (1996) Angiogenic potential of microvessel fragments established in three-dimensional collagen gels. In Vitro Cell Dev Biol Anim 32: 409-419. (Pubitemid 26269495)
12. Krishnan L, Hoying JB, Nguyen H, Song H, Weiss JA (2007) Interaction of angiogenic microvessels with the extracellular matrix. Am J Physiol Heart Circ Physiol 293: H3650-3658. (Pubitemid 350230911)
13. Krishnan L, Underwood CJ, Maas S, Ellis BJ, Kode TC, et al. (2008) Effect of mechanical boundary conditions on orientation of angiogenic microvessels. Cardiovasc Res 78: 324-332. (Pubitemid 351556109)
14. Underwood CJ, Edgar LT, Maas SA, Krishnan L, Hoying JB, et al. The Effects of Geometry and Static Boundary Conditions on Microvessel Outgrowth in a 3D Model of Angiogenesis; Proc. ASME Summer Bioengineering Conference 2010. Naples, FL, USA.
15. Ghajar CM, Blevins KS, Hughes CC, George SC, Putnam AJ (2006) Mesenchymal stem cells enhance angiogenesis in mechanically viable prevascularized tissues via early matrix metalloproteinase upregulation. Tissue Eng 12: 2875-2888. (Pubitemid 46141254)
16. Ghajar CM, Chen X, Harris JW, Suresh V, Hughes CC, et al. (2008) The effect of matrix density on the regulation of 3-D capillary morphogenesis. Biophys J 94: 1930-1941.
17. Kniazeva E, Putnam AJ (2009) Endothelial cell traction and ECM density influence both capillary morphogenesis and maintenance in 3-D. Am J Physiol Cell Physiol 297: C179-C187.
18. Sieminski AL, Hebbel RP, Gooch KJ (2004) The relative magnitudes of endothelial force generation and matrix stiffness modulate capillary morphogenesis in vitro. Exp Cell Res 297: 574-584. (Pubitemid 38798416)
19. Yamamura N, Sudo R, Ikeda M, Tanishita K (2007) Effects of the Mechanical Properties of Collagen Gel on the In Vitro Formation of Microvessel Networks by Endothelial Cells. Tissue Eng 13: 1443-1453. (Pubitemid 47105753)
20. Califano JP, Reinhart-King CA (2008) A Balance of Substrate Mechanics and Matrix Chemistry Regulates Endothelial Cell Network Assembly. Cell Mol Bioeng 1: 122-132.
21. Peirce SM (2008) Computational and mathematical modeling of angiogenesis. Microcirculation 15: 739-751.
22. Edgar LT, Sibole SC, Underwood CJ, Guilkey J, Weiss JA (2013) A Computational Model of In Vitro Angiogenesis based on Extracellular Matrix Fiber Orientation. Comp Meth Biomech Biomed Eng 16: 790-801.
23. B.R S, Chen HY, Smith CM, Gruionu G, Williams SK, et al. (2004) Rapid perfusion and network remodeling in a microvascular construct after implantation. Arterioscler Thromb Vasc Biol 24: 898-904.
24. Chang CC, Hoying JB (2006) Directed three-dimensional growth of microvascular cells and isolated microvessel fragments. Cell Transplant 15: 533-540. (Pubitemid 44655944)
25. Nunes SS, Greer KA, Stiening CM, Chen HY, Kidd KR, et al. (2010) Implanted microvessels progress through distinct neovascularization phenotypes. Microvasc Res 79: 10-20.
26. Chang CC, Nunes SS, Sibole SC, Krishnan L, Williams SK, et al. (2010) Angiogenesis in a microvascular construct for transplantation depends on the method of chamber circulation. Tissue Eng Part A 16: 795-805.
27. Nunes SS, Krishnan L, Gerard CS, Dale JR, Maddie MA, et al. (2010) Angiogenic potential of microvessel fragments is independent of the tissue of origin and can be influenced by the cellular composition of the implants. Microcirculation 17: 557-567.
28. Chang CC, Krishnan L, Nunes SS, Church KH, Edgar LT, et al. (2012) Determinants of microvascular network topologies in implanted neovasculatures. Arterioscler Thromb Vasc Biol 32: 5-14.
29. Bottenstein JE, Sato GH (1979) Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci USA 76: 514-517. (Pubitemid 9106659)
30. Liu Y, Griffith M, Watsky MA, Forrester JV, Kuffova L, et al. (2006) Properties of porcine and recombinant human collagen matrices for optically clear tissue engineering applications. Biomacromolecules 7: 1819-1828. (Pubitemid 43985103)
31. Wood GC, Keech MK (1960) The formation of fibrils from collagen solutions. 1. The effect of experimental conditions: kinetic and electron-microscope studies. Biochem J 75: 588-598.
32. Richter SJ, Richter C (2012) A Method for Determining Equivalence in Industrial Applications. Quality Engng 14: 375-380.
33. Nicosia RF, Ottinetti A (1990) Modulation of microvascular growth and morphogenesis by reconstituted basement membrane gel in three-dimensional cultures of rat aorta: a comparative study of angiogenesis in matrigel, collagen, fibrin, and plasma clot. In Vitro Cell Dev Biol 26: 119-128. (Pubitemid 20094385)
34. Nicosia RF, Ottinetti A (1990) Growth of microvessels in serum-free matrix culture of rat aorta. A quantitative assay of angiogenesis in vitro. Lab Invest 63: 115-122. (Pubitemid 20234680)
35. Krishnan L, Weiss JA, Wessman MD, Hoying JB (2004) Design and application of a test system for viscoelastic characterization of collagen gels. Tissue Eng 10: 241-252. (Pubitemid 38199379)
36. Roeder BA, Kokini K, Sturgis JE, Robinson JP, Voytik-Harbin SL (2002) Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure. J Biomech Eng 124: 214-222. (Pubitemid 34407065)
37. Rao RR, Peterson AW, Ceccarelli J, Putnam AJ, Stegemann JP (2012) Matrix composition regulates three-dimensional network formation by endothelial cells and mesenchymal stem cells in collagen/fibrin materials. Angiogenesis 15: 253-264.
38. Kniazeva E, Kachgal S, Putnam AJ (2011) Effects of extracellular matrix density and mesenchymal stem cells on neovascularization in vivo. Tissue engineering Part A 17: 905-914.
39. Huot J, Houle F, Rousseau S, Deschesnes RG, Shah GM, et al. (1998) SAPK2/p38-dependent F-actin reorganization regulates early membrane blebbing during stress-induced apoptosis. The Journal of cell biology 143: 1361-1373. (Pubitemid 28559836)
40. van Nieuw Amerongen GP, Koolwijk P, Versteilen A, van Hinsbergh VW (2003) Involvement of RhoA/Rho kinase signaling in VEGF-induced endothelial cell migration and angiogenesis in vitro. Arteriosclerosis, thrombosis, and vascular biology 23: 211-217. (Pubitemid 36231930)
41. Yang MT, Reich DH, Chen CS (2011) Measurement and analysis of traction force dynamics in response to vasoactive agonists. Integrative biology : quantitative biosciences from nano to macro 3: 663-674.
42. Shiu YT, Weiss JA, Hoying JB, Iwamoto MN, Joung IS, et al. (2005) The role of mechanical stresses in angiogenesis. Crit Rev Biomed Eng 33: 431-510. (Pubitemid 41191814)
43. Korff T, Augustin H (1999) Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J Cell Sci 112: 3249-3258. (Pubitemid 29507205)
44. Ingber D (2002) Mechanical Signaling and the Cellular Response to Extracellular Matrix in Angiogenesis and Cardiovascular Physiology. Circ Res 91: 877-887.
45. Bauer A, Jackson TL, Jiang Y (2009) Topography of Extracellular Matrix Mediates Vascular Morphogenesis and Migration Speeds in Angiogenesis. PLOS Comp Biol 5.
46. Guo WH, Frey MT, Burnham NA, Wang YL (2006) Substrate rigidity regulates the formation and maintenance of tissues. Biophysical journal 90: 2213-2220.
47. Parker KK, Brock AL, Brangwynne C, Mannix RJ, Wang N, et al. (2002) Directional control of lamellipodia extension by constraining cell shape and orienting cell tractional forces. FASEB journal : official publication of the Federation of American Societies for Experimental Biology 16: 1195-1204.
48. Kirkpatrick ND, Andreou S, Hoying JB, Utzinger U (2007) Live imaging of collagen remodeling during angiogenesis. Am J Physiol Heart Circ Physiol 292: H3198-3206. (Pubitemid 47084576)