Endothelial Matrix Assembly during Capillary Morphogenesis: Insights from Chimeric TagRFP-Fibronectin Matrix

Journal of Histochemistry and Cytochemistry

Volumn 62, Issue 11, 2014, Pages 774-790

  Chang, Fumin ^a   Lemmon, Christopher A ^b   Nilaratanakul, Voraphoj ^a   Rotter, Varda ^c   Romer, Lewis ^a  

^a DEPARTMENT OF PATHOLOGY   (United States)

^b Virginia Commonwealth University   (United States)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

3D matrix; endothelium; fibronectin; vasculogenesis

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 4; FIBRONECTIN; PROTEIN TAGRFP; SCLEROPROTEIN; TELOMERASE REVERSE TRANSCRIPTASE; TENASCIN; UNCLASSIFIED DRUG; PHOTOPROTEIN; RED FLUORESCENT PROTEIN;

ARTICLE; CAPILLARY; CELL ADHESION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; HUMAN CELL; MORPHOGENESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; CELL CULTURE; CHEMISTRY; CYTOLOGY; ENDOTHELIUM CELL; METABOLISM; UMBILICAL VEIN ENDOTHELIAL CELL;

CAPILLARIES; CELLS, CULTURED; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; FIBRONECTINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LUMINESCENT PROTEINS;

EID: 84921025753     PISSN: 00221554     EISSN: 15515044     Source Type: Journal    
DOI: 10.1369/0022155414547419     Document Type: Article

References (51)

1. Akamatsu H,Ichihara-Tanaka K,Ozono K,Kamiike W,Matsuda H,Sekiguchi K.Suppression of transformed phenotypes of human fibrosarcoma cells by overexpression of recombinant fibronectin.Cancer research. 1996;56:4541-4546
2. Benton G,George J,Kleinman HK,Arnaoutova IP.Advancing science and technology via 3D culture on basement membrane matrix.J Cell Physiol. 2009;221:18-25
3. Bernstein EF,Chen YQ,Kopp JB,Fisher L,Brown DB,Hahn PJ,Robey FA,Lakkakorpi J,Uitto J.Long-term sun exposure alters the collagen of the papillary dermis. Comparison of sun-protected and photoaged skin by northern analysis, immunohistochemical staining, and confocal laser scanning microscopy.J Am Acad Dermatol. 1996;34:209-218
4. Burns JS,Kristiansen M,Kristensen LP,Larsen KH,Nielsen MO,Christiansen H,Nehlin J,Andersen JS,Kassem M.Decellularized matrix from tumorigenic human mesenchymal stem cells promotes neovascularization with galectin-1 dependent endothelial interaction.PLoS One. 2011;6:e21888
5. Chalupowicz DG,Chowdhury ZA,Bach TL,Barsigian C,Martinez J.Fibrin II induces endothelial cell capillary tube formation.J Cell Biol. 1995;130:207-215
6. Chang F,Lemmon CA,Park D,Romer LH.FAK potentiates Rac1 activation and localization to matrix adhesion sites: a role for betaPIX. Mol Biol Cell. 2007;18:253-264
7. Chen X,Thibeault SL.Novel isolation and biochemical characterization of immortalized fibroblasts for tissue engineering vocal fold lamina propria.Tissue Eng Part C Methods. 2009;15:201-212
8. Chung CY,Erickson HP.Glycosaminoglycans modulate fibronectin matrix assembly and are essential for matrix incorporation of tenascin-C.J Cell Sci 110 (Pt 12):. 1997;:1413-1419
9. Dzamba BJ,Peters DM.Arrangement of cellular fibronectin in noncollagenous fibrils in human fibroblast cultures.J Cell Sci 100 (Pt 3):. 1991;:605-612
10. Fraley SI,Feng Y,Krishnamurthy R,Kim DH,Celedon A,Longmore GD,Wirtz D.A distinctive role for focal adhesion proteins in three-dimensional cell motility.Nat Cell Biol. 2010;12:598-604
11. Genis L,Gonzalo P,Tutor AS,Galvez BG,Martinez-Ruiz A,Zaragoza C,Lamas S,Tryggvason K,Apte SS,Arroyo AG.Functional interplay between endothelial nitric oxide synthase and membrane type 1 matrix metalloproteinase in migrating endothelial cells.Blood. 2007;110:2916-2923
12. Grant DS,Lelkes PI,Fukuda K,Kleinman HK.Intracellular mechanisms involved in basement membrane induced blood vessel differentiation in vitro.In Vitro Cell Dev Biol 27A:. 1991;:327-336
13. Hotary KB,Allen ED,Brooks PC,Datta NS,Long MW,Weiss SJ.Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix.Cell. 2003;114:33-45
14. Howard BV,Macarak EJ,Gunson D,Kefalides NA.Characterization of the collagen synthesized by endothelial cells in culture.Proc Natl Acad Sci U S A. 1976;73:2361-2364
15. Hughes CS,Postovit LM,Lajoie GA.Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics. 2010;10:1886-1890
16. Jones JA,Beck C,Barbour JR,Zavadzkas JA,Mukherjee R,Spinale FG,Ikonomidis JS.Alterations in aortic cellular constituents during thoracic aortic aneurysm development: myofibroblast-mediated vascular remodeling. Am J Pathol. 2009;175:1746-1756
17. Kleinman HK,Martin GR.Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol. 2005;15:378-386
18. Kutys ML,Doyle AD,Yamada KM.Regulation of cell adhesion and migration by cell-derived matrices.Exp Cell Res. 2013;319:2434-2439
19. Kwiatkowska A,Kijewska M,Lipko M,Hibner U,Kaminska B.Downregulation of Akt and FAK phosphorylation reduces invasion of glioblastoma cells by impairment of MT1-MMP shuttling to lamellipodia and downregulates MMPs expression.Biochim Biophys Acta. 2011;1813:655-667
20. Laemmli UK,Beguin F,Gujer-Kellenberger G.A factor preventing the major head protein of bacteriophage T4 from random aggregation.J Mol Biol. 1970;47:69-85
21. Lopez JI,Kang I,You WK,McDonald DM,Weaver VM.In situ force mapping of mammary gland transformation.Integr Biol (Camb). 2011;3:910-921
22. Luque T,Melo E,Garreta E,Cortiella J,Nichols J,Farre R,Navajas D.Local micromechanical properties of decellularized lung scaffolds measured with atomic force microscopy.Acta Biomater. 2013;9:6852-6859
23. Lutolf MP,Hubbell JA.Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering.Nat Biotechnol. 2005;23:47-55
24. Macchiarini P,Jungebluth P,Go T,Asnaghi MA,Rees LE,Cogan TA,Dodson A,Martorell J,Bellini S,Parnigotto PP,Dickinson SC,Hollander AP,Mantero S,Conconi MT,Birchall MA.Clinical transplantation of a tissue-engineered airway.Lancet. 2008;372:2023-2030
25. McKeown-Longo PJ,Mosher DF.Binding of plasma fibronectin to cell layers of human skin fibroblasts.J Cell Biol. 1983;97:466-472
26. Milyavsky M,Shats I,Erez N,Tang X,Senderovich S,Meerson A,Tabach Y,Goldfinger N,Ginsberg D,Harris CC,Rotter V.Prolonged culture of telomerase-immortalized human fibroblasts leads to a premalignant phenotype.Cancer Res. 2003;63:7147-7157
27. Nardi JB.Neuronal pathfinding in developing wings of the moth Manduca sexta.Dev Biol. 1983;95:163-174
28. Newman AC,Chou W,Welch-Reardon KM,Fong AH,Popson SA,Phan DT,Sandoval DR,Nguyen DP,Gershon PD,Hughes CC.Analysis of stromal cell secretomes reveals a critical role for stromal cell-derived hepatocyte growth factor and fibronectin in angiogenesis.Arterioscler Thromb Vasc Biol. 2013;33:513-522
29. Ohashi T,Kiehart DP,Erickson HP.Dual labeling of the fibronectin matrix and actin cytoskeleton with green fluorescent protein variants.J Cell Sci. 2002;115:1221-1229
30. Ohashi T,Kiehart DP,Erickson HP.Dynamics and elasticity of the fibronectin matrix in living cell culture visualized by fibronectin-green fluorescent protein.Proceedings of the National Academy of Sciences of the United States of America. 1999;96:2153-2158
31. Orkin RW,Gehron P,McGoodwin EB,Martin GR,Valentine T,Swarm R.A murine tumor producing a matrix of basement membrane.J Exp Med. 1977;145:204-220
32. Ott HC,Matthiesen TS,Goh SK,Black LD,Kren SM,Netoff TI,Taylor DA.Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart.Nat Med. 2008;14:213-221
33. Pignolo RJ,Martin BG,Horton JH,Kalbach AN,Cristofalo VJ.The pathway of cell senescence: WI-38 cells arrest in late G1 and are unable to traverse the cell cycle from a true G0 state.Exp Gerontol. 1998;33:67-80
34. Raman P,Harry C,Weber M,Krukovets I,Stenina OI.A novel transcriptional mechanism of cell type-specific regulation of vascular gene expression by glucose.Arterioscler Thromb Vasc Biol. 2011;31:634-642
35. Sabatelli P,Bonaldo P,Lattanzi G,Braghetta P,Bergamin N,Capanni C,Mattioli E,Columbaro M,Ognibene A,Pepe G,Bertini E,Merlini L,Maraldi NM,Squarzoni S.Collagen VI deficiency affects the organization of fibronectin in the extracellular matrix of cultured fibroblasts.Matrix Biol. 2001;20:475-486
36. Savarese JJ,Erickson H,Scully SP.Articular chondrocyte tenascin-C production and assembly into de novo extracellular matrix.J Orthop Res. 1996;14:273-281
37. Schor AM,Ellis I,Schor SL.Chemotaxis and Chemokinesis in 3D Macromolecular Matrices: Relevance to Angiogenesis. Methods Mol Med. 2001;46:163-183
38. Sieminski AL,Hebbel RP,Gooch KJ.The relative magnitudes of endothelial force generation and matrix stiffness modulate capillary morphogenesis in vitro.Exp Cell Res. 2004;297:574-584
39. Sottile J,Hocking DC.Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions.Mol Biol Cell. 2002;13:3546-3559
40. Soucy PA,Romer LH.Endothelial cell adhesion, signaling, and morphogenesis in fibroblast-derived matrix.Matrix Biol. 2009;28:273-283
41. Soucy PA,Werbin J,Heinz W,Hoh JH,Romer LH.Microelastic properties of lung cell-derived extracellular matrix.Acta Biomaterialia. 2011a;7:96-105
42. Soucy PA,Werbin J,Heinz W,Hoh JH,Romer LH.Microelastic properties of lung cell-derived extracellular matrix.Acta Biomater. 2011b;7:96-105
43. Takino T,Tsuge H,Ozawa T,Sato H.MT1-MMP promotes cell growth and ERK activation through c-Src and paxillin in three-dimensional collagen matrix.Biochem Biophys Res Commun. 2010;396:1042-1047
44. Van Duyn Graham L,Sweetwyne MT,Pallero MA,Murphy-Ullrich JE.Intracellular calreticulin regulates multiple steps in fibrillar collagen expression, trafficking, and processing into the extracellular matrix.J Biol Chem. 2010;285:7067-7078
45. Vukicevic S,Kleinman HK,Luyten FP,Roberts AB,Roche NS,Reddi AH.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. 1992;202:1-8
46. Wang H,Su Y.Collagen IV contributes to nitric oxide-induced angiogenesis of lung endothelial cells.Am J Physiol Cell Physiol. 2011;300:C979-988
47. Wierzbicka-Patynowski I,Mao Y,Schwarzbauer JE.Analysis of fibronectin matrix assembly.Curr Protoc Cell Biol. 2004;:
48. Wu X,Gan B,Yoo Y,Guan JL.FAK-mediated src phosphorylation of endophilin A2 inhibits endocytosis of MT1-MMP and promotes ECM degradation.Dev Cell. 2005;9:185-196
49. Xue X,Wang J,Zhu Y,Tu Q,Huang N.Biocompatibility of pure titanium modified by human endothelial cell-derived extracellular matrix.Applied Surface Science. 2010;256:3866-3873
50. Yan HC,Pilewski JM,Zhang Q,DeLisser HM,Romer L,Albelda SM.Localization of multiple functional domains on human PECAM-1 (CD31) by monoclonal antibody epitope mapping.Cell Adhes Commun. 1995;3:45-66
51. Zhou X,Rowe RG,Hiraoka N,George JP,Wirtz D,Mosher DF,Virtanen I,Chernousov MA,Weiss SJ.Fibronectin fibrillogenesis regulates three-dimensional neovessel formation.Genes Dev. 2008;22:1231-1243