The requirement for fibroblasts in angiogenesis: Fibroblast-derived matrix proteins are essential for endothelial cell lumen formation

Molecular Biology of the Cell

Volumn 22, Issue 20, 2011, Pages 3791-3800

  Newman, Andrew C ^a   Nakatsu, Martin N ^a,c   Chou, Wayne ^a   Gershon, Paul D ^a   Hughes, Christopher C W ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California at Irvine   (United States)

^c JULES STEIN EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIN; ANGIOPOIETIN 1; COLLAGEN TYPE 1; GLYCOPROTEIN; INSULIN GROWTH FACTOR BINDING PROTEIN 7; MATRIX PROTEIN; OSTEONECTIN; PROCOLLAGEN C ENDOPEPTIDASE ENHANCER 1; SCATTER FACTOR; SMALL INTERFERING RNA; SOMATOMEDIN BINDING PROTEIN; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA INDUCED PROTEIN IG H3; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANGIOGENESIS; ARTICLE; BLOOD VESSEL FUNCTION; CELL CULTURE; COLUMN CHROMATOGRAPHY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FIBROBLAST; FLOW KINETICS; GEL PERMEATION CHROMATOGRAPHY; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; ION EXCHANGE CHROMATOGRAPHY; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN SECRETION; VESSEL SPROUTING;

ANGIOGENIC PROTEINS; CARRIER PROTEINS; CELL DIVISION; CELL LINE, TUMOR; CHROMATOGRAPHY; COLLAGEN; CULTURE MEDIA, CONDITIONED; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FIBROBLASTS; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; GLYCOPROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MASS SPECTROMETRY; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PREGNANCY PROTEINS; RHEOLOGY; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 80054712998     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-05-0393     Document Type: Article

References (59)

1. Aitkenhead M, Wang SJ, Nakatsu MN, Mestas J, Heard C, Hughes CC (2002). Identification of endothelial cell genes expressed in an in vitro model of angiogenesis: induction of ESM-1, (beta)ig-h3, and NrCAM. Microvasc Res 63, 159-171. (Pubitemid 34971632)
2. Albini A, Magnani E, Noonan DM (2010). The tumor microenvironment: biology of a complex cellular and tissue society. Q J Nucl Med Mol Imaging 54, 244-248.
3. Antoniades HN, Galanopoulos T, Neville-Golden J, Kiritsy CP, Lynch SE (1991). Injury induces in vivo expression of platelet-derived growth factor (PDGF) and PDGF receptor mRNAs in skin epithelial cells and PDGF mRNA in connective tissue fibroblasts. Proc Natl Acad Sci USA 88, 565-569. (Pubitemid 21915506)
4. Bayless KJ, Salazar R, Davis GE (2000). RGD-dependent vacuolation and lumen formation observed during endothelial cell morphogenesis in three-dimensional fibrin matrices involves the alpha(v)beta(3) and alpha(5)beta(1) integrins. Am J Pathol 156, 1673-1683. (Pubitemid 30646705)
5. Berthod F, Germain L, Tremblay N, Auger FA (2006). Extracellular matrix deposition by fibroblasts is necessary to promote capillary-like tube formation in vitro. J Cell Physiol 207, 491-498.
6. Bhowmick NA, Neilson EG, Moses HL (2004). Stromal fibroblasts in cancer initiation and progression. Nature 432, 332-337. (Pubitemid 39551661)
7. Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJ (2009). Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 4, 484-494.
8. Bradshaw AD (2009). The role of SPARC in extracellular matrix assembly. J Cell Commun Signal 3, 239-246.
9. Bradshaw AD, Puolakkainen P, Dasgupta J, Davidson JM, Wight TN, Helene Sage E (2003). SPARC-null mice display abnormalities in the dermis characterized by decreased collagen fibril diameter and reduced tensile strength. J Invest Dermatol 120, 949-955. (Pubitemid 36702902)
10. Brooks PC, Clark RA, Cheresh DA (1994). Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264, 569-571.
11. Bryan BA, D'Amore PA (2007). What tangled webs they weave: Rho-GTPase control of angiogenesis. Cell Mol Life Sci 64, 2053-2065. (Pubitemid 350092415)
12. Chang HY, Chi JT, Dudoit S, Bondre C, van de Rijn M, Botstein D, Brown PO (2002). Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci USA 99, 12877-12882.
13. Chang HY, Sneddon JB, Alizadeh AA, Sood R, West RB, Montgomery K, Chi JT, van de Rijn M, Botstein D, Brown PO (2004). Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLoS Biol 2, E7.
14. Critser PJ, Kreger ST, Voytik-Harbin SL, Yoder MC (2010). Collagen matrix physical properties modulate endothelial colony forming cell-derived vessels in vivo. Microvasc Res 80, 23-30.
15. Davis GE, Camarillo CW (1996). An alpha 2 beta 1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in threedimensional collagen matrix. Exp Cell Res 224, 39-51. (Pubitemid 26116886)
16. Davis GE, Senger DR (2008). Extracellular matrix mediates a molecular balance between vascular morphogenesis and regression. Curr Opin Hematol 15, 197-203. (Pubitemid 351507571)
17. Drake CJ, Cheresh DA, Little CD (1995). An antagonist of integrin alpha v beta 3 prevents maturation of blood vessels during embryonic neovascularization. J Cell Sci 108, 2655-2661.
18. Fligiel SE, Varani J, Datta SC, Kang S, Fisher GJ, Voorhees JJ (2003). Collagen degradation in aged/photodamaged skin in vivo and after exposure to matrix metalloproteinase-1 in vitro. J Invest Dermatol 120, 842-848. (Pubitemid 36529088)
19. Folkman J (1975). Tumor angiogenesis: a possible control point in tumor growth. Ann Intern Med 82, 96-100.
20. Folkman J (2002). Role of angiogenesis in tumor growth and metastasis. Semin Oncol 29, 15-18.
21. Friedland JC, Lee MH, Boettiger D (2009). Mechanically activated integrin switch controls alpha5beta1 function. Science 323, 642-644.
22. Fujimoto A, Onodera H, Mori A, Isobe N, Yasuda S, Oe H, Yonenaga Y, Tachibana T, Imamura M (2004). Vascular endothelial growth factor reduces mural cell coverage of endothelial cells and induces sprouting rather than luminal division in an HT1080 tumour angiogenesis model. Int J Exp Pathol 85, 355-364. (Pubitemid 39647364)
23. Fukumura D et al. (1998). Tumor induction of VEGF promoter activity in stromal cells. Cell 94, 715-725. (Pubitemid 28436004)
24. Griffith CK, Miller C, Sainson RC, Calvert JW, Jeon NL, Hughes CC, George SC (2005). Diffusion limits of an in vitro thick prevascularized tissue. Tissue Eng 11, 257-266. (Pubitemid 40515193)
25. Guo X, Oshima H, Kitmura T, Taketo MM, Oshima M (2008). Stromal fibroblasts activated by tumor cells promote angiogenesis in mouse gastric cancer. J Biol Chem 283, 19864-19871.
26. Hashimoto K et al. (1997). Characterization of a cartilage-derived 66-kDa protein (RGD-CAP/beta ig-h3) that binds to collagen. Biochim Biophys Acta 1355, 303-314. (Pubitemid 27091386)
27. Hohenester E, Sasaki T, Giudici C, Farndale RW, Bachinger HP (2008). Structural basis of sequence-specific collagen recognition by SPARC. Proc Natl Acad Sci USA 105, 18273-18277.
28. Hughes CC (2008). Endothelial-stromal interactions in angiogenesis. Curr Opin Hematol 15, 204-209.
29. Hynes RO (2009). The extracellular matrix: not just pretty fibrils. Science 326, 1216-1219.
30. Ilic D, Kovacic B, McDonagh S, Jin F, Baumbusch C, Gardner DG, Damsky CH (2003). Focal adhesion kinase is required for blood vessel morphogenesis. Circ Res 92, 300-307. (Pubitemid 36258552)
31. Ishihama Y, Rappsilber J, Mann M (2006). Modular stop and go extraction tips with stacked disks for parallel and multidimensional peptide fractionation in proteomics. J Proteome Res 5, 988-994.
32. Karamysheva AF (2008). Mechanisms of angiogenesis. Biochemistry (Mosc) 73, 751-762.
33. Kellouche S, Mourah S, Bonnefoy A, Schoevaert D, Podgorniak MP, Calvo F, Hoylaerts MF, Legrand C, Dosquet C (2007). Platelets, thrombospondin- 1 and human dermal fibroblasts cooperate for stimulation of endothelial cell tubulogenesis through VEGF and PAI-1 regulation. Exp Cell Res 313, 486-499. (Pubitemid 46201809)
34. Kim JH, Asthagiri AR (2011). Matrix stiffening sensitizes epithelial cells to EGF and enables the loss of contact inhibition of proliferation. J Cell Sci 124, 1280-1287.
35. Koh W, Mahan RD, Davis GE (2008). Cdc42- and Rac1-mediated endothelial lumen formation requires Pak2, Pak4 and Par3, and PKC-dependent signaling. J Cell Sci 121, 989-1001. (Pubitemid 351639418)
36. Kronenberg D, Vadon-Le Goff S, Bourhis JM, Font B, Eichenberger D, Hulmes DJ, Moali C (2009). Strong cooperativity and loose geometry between CUB domains are the basis for procollagen C-proteinase enhancer activity. J Biol Chem 284, 33437-33446.
37. Kutsukake M et al. (2008). Circulating IGF-binding protein 7 (IGFBP7) levels are elevated in patients with endometriosis or undergoing diabetic hemodialysis. Reprod Biol Endocrinol 6, 54.
38. Li SW, Sieron AL, Fertala A, Hojima Y, Arnold WV, Prockop DJ (1996). The C-proteinase that processes procollagens to fibrillar collagens is identical to the protein previously identified as bone morphogenic protein-1. Proc Natl Acad Sci USA 93, 5127-5130. (Pubitemid 26162882)
39. Liu Y, Senger DR (2004). Matrix-specific activation of Src and Rho initiates capillary morphogenesis of endothelial cells. FASEB J 18, 457-468. (Pubitemid 38326302)
40. Maeda T, Desouky J, Friedl A (2006). Syndecan-1 expression by stromal fibroblasts promotes breast carcinoma growth in vivo and stimulates tumor angiogenesis. Oncogene 25, 1408-1412. (Pubitemid 43336469)
41. Masuda T, Tomita M, Ishihama Y (2008). Phase transfer surfactant-aided trypsin digestion for membrane proteome analysis. J Proteome Res 7, 731-740. (Pubitemid 351294035)
42. Montesano R, Orci L, Vassalli P (1983). In vitro rapid organization of endothelial cells into capillary-like networks is promoted by collagen matrices. J Cell Biol 97, 1648-1652. (Pubitemid 14230229)
43. Montesano R, Pepper MS, Orci L (1993). Paracrine induction of angiogenesis in vitro by Swiss 3T3 fibroblasts. J Cell Sci 105 (Pt 4),1013-1024. (Pubitemid 23258664)
44. Myers KA, Applegate KT, Danuser G, Fischer RS, Waterman CM (2011). Distinct ECM mechanosensing pathways regulate microtubule dynamics to control endothelial cell branching morphogenesis. J Cell Biol 192, 321-334.
45. Nakatsu MN, Hughes CC (2008). An optimized three-dimensional in vitro model for the analysis of angiogenesis. Methods Enzymol 443, 65-82.
46. Nakatsu MN, Sainson RC, Aoto JN, Taylor KL, Aitkenhead M, Perez-del-Pulgar S, Carpenter PM, Hughes CC (2003). 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. (Pubitemid 36962872)
47. Nam JO, Kim JE, Jeong HW, Lee SJ, Lee BH, Choi JY, Park RW, Park JY, Kim IS (2003). Identification of the alphavbeta3 integrin-interacting motif of betaig-h3 and its anti-angiogenic effect. J Biol Chem 278, 25902-25909. (Pubitemid 36835352)
48. 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)
49. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, Carey VJ, Richardson AL, Weinberg RA (2005). Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121, 335-348. (Pubitemid 40692295)
50. Paunescu V et al. (2011). Tumor-associated fibroblasts and mesenchymal stem cells: more similarities than differences. J Cell Mol Med 15, 635-646.
51. Payne SL, Hendrix MJ, Kirschmann DA (2007). Paradoxical roles for lysyl oxidases in cancer - a prospect. J Cell Biochem 101, 1338-1354. (Pubitemid 47242767)
52. Pen A, Moreno MJ, Martin J, Stanimirovic DB (2007). Molecular markers of extracellular matrix remodeling in glioblastoma vessels: microarray study of laser-captured glioblastoma vessels. Glia 55, 559-572. (Pubitemid 46474298)
53. Pietras K, Pahler J, Bergers G, Hanahan D (2008). Functions of paracrine PDGF signaling in the proangiogenic tumor stroma revealed by pharmacological targeting. PLoS Med 5, e19.
54. Sato N, Fukushima N, Maehara N, Matsubayashi H, Koopmann J, Su GH, Hruban RH, Goggins M (2003). SPARC/osteonectin is a frequent target for aberrant methylation in pancreatic adenocarcinoma and a mediator of tumor-stromal interactions. Oncogene 22, 5021-5030. (Pubitemid 37026400)
55. Sato N, Maehara N, Goggins M (2004). Gene expression profiling of tumor-stromal interactions between pancreatic cancer cells and stromal fibroblasts. Cancer Res 64, 6950-6956. (Pubitemid 39331004)
56. St Croix B et al. (2000). Genes expressed in human tumor endothelium. Science 289, 1197-1202. (Pubitemid 30650733)
57. Stratman AN, Malotte KM, Mahan RD, Davis MJ, Davis GE (2009). Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood 114, 5091-5101.
58. Tille JC, Pepper MS (2002). Mesenchymal cells potentiate vascular endothelial growth factor-induced angiogenesis in vitro. Exp Cell Res 280, 179-191.
59. Velazquez OC, Snyder R, Liu ZJ, Fairman RM, Herlyn M (2002). Fibroblast-dependent differentiation of human microvascular endothelial cells into capillary-like 3-dimensional networks. FASEB J 16, 1316-1318.