Endothelial cells expressing low levels of CD143 (ACE) exhibit enhanced sprouting and potency in relieving tissue ischemia

Angiogenesis

Volumn 17, Issue 3, 2014, Pages 617-630

  Silva, Eduardo A ^a,b,d   Eseonu, Chikezie ^b,c   Mooney, David J ^a,b  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d University of California Davis   (United States)

Author keywords

3D sprouting assay; Alginate; Cell transplantation; Therapeutic angiogenesis

Indexed keywords

BIOLOGICAL MARKER; DIPEPTIDYL CARBOXYPEPTIDASE; FIBRIN GLUE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; L SELECTIN; NATRIURETIC PEPTIDE RECEPTOR A; RANTES; TELOMERASE; TISSUE PLASMINOGEN ACTIVATOR; TISSUE SCAFFOLD; TRYPSIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VASCULOTROPIN 165; FIBRIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD FLOW; BLOOD VESSEL; CELL ISOLATION; CELL PROLIFERATION; CELL SUBPOPULATION; CELL TRANSPLANTATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; GENOTYPE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; ISCHEMIA; MICROCARRIER CULTURE; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINGLE CELL ANALYSIS; TISSUE PERFUSION; UPREGULATION; ANIMAL; DRUG EFFECTS; ENDOTHELIUM CELL; FLOW CYTOMETRY; HINDLIMB; METABOLISM; PATHOLOGY; SCID MOUSE; VASCULARIZATION;

ANIMALS; ENDOTHELIAL CELLS; FEMALE; FIBRIN; FLOW CYTOMETRY; GENOTYPE; HINDLIMB; HUMANS; ISCHEMIA; MICE, SCID; NEOVASCULARIZATION, PHYSIOLOGIC; PEPTIDYL-DIPEPTIDASE A;

EID: 84903907228     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-014-9414-9     Document Type: Article

References (60)

1. Carmeliet P, Jain R (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473(7347):298-307. doi: 10.1038/nature10144
2. Semenza G (2011) Oxygen sensing, homeostasis, and disease. New Engl J Med 365(6):537-547. doi: 10.1056/NEJMra1011165
3. Potente M, Gerhardt H, Carmeliet P (2011) Basic and therapeutic aspects of angiogenesis. Cell 146(6):873-887. doi: 10.1016/j.cell.2011.08.039
4. Davis G, Senger D (2005) Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res 97(11):1093-1107. doi: 10.1161/01.RES.0000191547.64391. e3
5. Ribatti D, Crivellato E (2012) "Sprouting angiogenesis", a reappraisal. Dev Biol 372(2):157-165. doi: 10.1016/j.ydbio.2012.09.018
6. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161(6):1163-1177. doi: 10.1083/jcb.200302047
7. Blancas AA, Wong LE, Glaser DE, McCloskey KE (2013) Specialized tip/stalk-like and phalanx-like endothelial cells from embryonic stem cells. Stem Cells Dev. doi: 10.1089/scd.2012.0376
8. Carmeliet P, De Smet F, Loges S, Mazzone M (2009) Branching morphogenesis and antiangiogenesis candidates: tip cells lead the way. Nat Rev Clin Oncol 6(6):315-326. doi: 10.1038/nrclinonc.2009.64
9. Staton C, Reed M, Brown N (2009) A critical analysis of current in vitro and in vivo angiogenesis assays. Int J Exp Pathol 90(3):195-221. doi: 10.1111/j.1365-2613.2008.00633.x
10. Arnaoutova I, George J, Kleinman H, Benton G (2009) The endothelial cell tube formation assay on basement membrane turns 20: state of the science and the art. Angiogenesis 12(3):267-274. doi: 10.1007/s10456-009-9146-4
11. Iruela-Arispe ML, George ED (2009) Cellular and molecular mechanisms of vascular lumen formation. Dev Cell 16. doi: 10.1016/j.devcel.2009.01.013
12. Li X, Claesson-Welsh L (2009) Embryonic stem cell models in vascular biology. JTH 7(Suppl 1):53-56. doi: 10.1111/j.1538-7836.2009.03427.x
13. Nakatsu M, CCW Hughes (2008) An optimized three-dimensional in vitro model for the analysis of angiogenesis. Methods Enzymol 443. doi: 10.1016/s0076-6879(08)02004-1
14. Zeitlin B, Dong Z, Nör J (2012) RAIN-droplet: a novel 3D in vitro angiogenesis model. Lab Invest 92(7):988-998. doi: 10.1038/labinvest.2012.77
15. Auerbach R, Lewis R, Shinners B, Kubai L, Akhtar N (2003) Angiogenesis assays: a critical overview. Clin Chem 49(1):32-40. doi: 10.1373/49.1.32
16. Jain R, Schlenger K, Höckel M, Yuan F (1997) Quantitative angiogenesis assays: progress and problems. Nat Med 3(11):1203-1208. doi: 10.1038/nm1197-1203
17. Parikh S, Edelman E (2000) Endothelial cell delivery for cardiovascular therapy. Adv Drug Deliv Rev 42(1-2):139-161. doi: 10.1016/S0169-409X(00)00058-2
18. Losordo D, Dimmeler S (2004) Therapeutic angiogenesis and vasculogenesis for ischemic disease: part II: cell-based therapies. Circulation 109(22):2692-2697. doi: 10.1161/01.CIR.0000128596.49339.05
19. Dong Z, Neiva K, Jin T, Zhang Z, Hall D, Mooney D, Polverini P, Nör J (2007) Quantification of human angiogenesis in immunodeficient mice using a photon counting-based method. Biotechniques 43(1):73-77
20. Nör J, Peters M, Christensen J, Sutorik M, Linn S, Khan M, Addison C, Mooney D, Polverini P (2001) Engineering and characterization of functional human microvessels in immunodeficient mice. Lab Invest 81(4):453-463. doi: 10.1038/labinvest.3780253
21. Taraboletti G, Giavazzi R (2004) Modelling approaches for angiogenesis. Eur J Cancer 40(6):881-889. doi: 10.1016/j.ejca.2004.01.002 Oxford, England: 1990
22. Newman A, Nakatsu M, Chou W, Gershon P, Hughes C (2011) The requirement for fibroblasts in angiogenesis: fibroblast-derived matrix proteins are essential for endothelial cell lumen formation. Mol Biol Cell 22(20):3791-3800. doi: 10.1091/mbc.E11-05-0393
23. Nakatsu M, Sainson R, Aoto J, Taylor K, Aitkenhead M, Pérez-del-Pulgar S, Carpenter P, Hughes C (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(2):102-112. doi: 10.1016/s0026-2862(03)00045-1
24. Couffinhal T, Silver M, Kearney M, Sullivan A, Witzenbichler B, Magner M, Annex B, Peters K, Isner JM (1999) Impaired collateral vessel development associated with reduced expression of vascular endothelial growth factor in ApoE-/- mice. Circulation 99(24):3188-3198
25. Silva EA, Mooney DJ (2010) Effects of VEGF temporal and spatial presentation on angiogenesis. Biomaterials 31(6):1235-1241. doi: 10.1016/j.biomaterials.2009.10.052
26. Silva EA, Kim ES, Kong HJ, Mooney DJ (2008) Material-based deployment enhances efficacy of endothelial progenitor cells. Proc Natl Acad Sci USA 105(38):14347-14352. doi: 10.1073/pnas.0803873105
27. Chen RR, Silva EA, Yuen WW, Brock AA, Fischbach C, Lin AS, Guldberg RE, Mooney DJ (2007) Integrated approach to designing growth factor delivery systems. FASEB J 21(14):3896-3903. doi: 10.1096/fj.06-7873com
28. Yuen WW, Du NR, Chan CH, Silva EA, Mooney DJ (2010) Mimicking nature by codelivery of stimulant and inhibitor to create temporally stable and spatially restricted angiogenic zones. Proc Natl Acad Sci USA 107(42):17933-17938. doi: 10.1073/pnas.1001192107
29. Silva EA, Mooney DJ (2007) Spatiotemporal control of vascular endothelial growth factor delivery from injectable hydrogels enhances angiogenesis. J Thromb Haemost 5(3):590-598. doi: 10.1111/j.1538-7836.2007.02386.x
30. Iruela-Arispe M, Davis G (2009) Cellular and molecular mechanisms of vascular lumen formation. Dev Cell 16(2):222-231. doi: 10.1016/j.devcel.2009.01. 013
31. Nakatsu M, Davis J, Hughes C (2007) Optimized fibrin gel bead assay for the study of angiogenesis. J Vis Exp 3:186. doi: 10.3791/186
32. Sieminski AL, Hebbel RP, Gooch KJ (2005) Improved microvascular network in vitro by human blood outgrowth endothelial cells relative to vessel-derived endothelial cells. Tissue Eng 11(9-10):1332-1345. doi: 10.1089/ten.2005.11.1332
33. Fantin A, Vieira JM, Plein A, Denti L, Fruttiger M, Pollard JW, Ruhrberg C (2013) NRP1 acts cell autonomously in endothelium to promote tip cell function during sprouting angiogenesis. Blood 121(12):2352-2362. doi: 10.1182/blood-2012-05-424713
34. Law AY, Wong CK (2013) Stanniocalcin-1 and -2 promote angiogenic sprouting in HUVECs via VEGF/VEGFR2 and angiopoietin signaling pathways. Mol Cell Endocrinol 374(1-2):73-81. doi: 10.1016/j.mce.2013.04.024
35. Hou TC, Lin JJ, Wen HC, Chen LC, Hsu SP, Lee WS (2013) Folic acid inhibits endothelial cell migration through inhibiting the RhoA activity mediated by activating the folic acid receptor/cSrc/p190RhoGAP-signaling pathway. Biochem Pharmacol 85(3):376-384. doi: 10.1016/j.bcp.2012.11.011
36. Spindler V, Schlegel N, Waschke J (2010) Role of GTPases in control of microvascular permeability. Cardiovasc Res 87(2):243-253. doi: 10.1093/cvr/cvq086
37. 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. Arterioscler Thromb Vasc Biol 23(2):211-217
38. Wacker A, Gerhardt H (2011) Endothelial development taking shape. Curr Opin Cell Biol 23(6):676-685. doi: 10.1016/j.ceb.2011.10.002
39. Blanco R, Gerhardt H (2013) VEGF and Notch in tip and stalk cell selection. Cold Spring Harb Perspect Med 3(1). doi: 10.1101/cshperspect.a006569
40. Kume T (2012) Ligand-dependent notch signaling in vascular formation. Adv Exp Med Biol 727:210-222. doi: 10.1007/978-1-4614-0899-4-16
41. del Toro R, Prahst C, Mathivet T, Siegfried G, Kaminker JS, Larrivee B, Breant C, Duarte A, Takakura N, Fukamizu A, Penninger J, Eichmann A (2010) Identification and functional analysis of endothelial tip cell-enriched genes. Blood 116(19):4025-4033. doi: 10.1182/blood-2010-02-270819
42. Lei Y, Zouani OF, Rami L, Chanseau C, Durrieu MC (2012) Modulation of lumen formation by microgeometrical bioactive cues and migration mode of actin machinery. Small. doi: 10.1002/smll.201202410
43. Napoli C, Hayashi T, Cacciatore F, Casamassimi A, Casini C, Al-Omran M, Ignarro LJ (2011) Endothelial progenitor cells as therapeutic agents in the microcirculation: an update. Atherosclerosis 215(1):9-22. doi: 10.1016/j.atherosclerosis.2010.10.039
44. Gerhardt H (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161. doi: 10.1083/jcb.200302047
45. Hercus TR, Broughton SE, Ekert PG, Ramshaw HS, Perugini M, Grimbaldeston M, Woodcock JM, Thomas D, Pitson S, Hughes T, D'Andrea RJ, Parker MW, Lopez AF (2012) The GM-CSF receptor family: mechanism of activation and implications for disease. Growth Factors 30(2):63-75. doi: 10.3109/08977194.2011.649919
46. Stamenkovic I (1995) The L-selectin adhesion system. Curr Opin Hematol 2(1):68-75
47. Shah IM, Macrae IM, Di Napoli M (2009) Neuroinflammation and neuroprotective strategies in acute ischaemic stroke - from bench to bedside. Curr Mol Med 9(3):336-354
48. Suffee N, Richard B, Hlawaty H, Oudar O, Charnaux N, Sutton A (2011) Angiogenic properties of the chemokine RANTES/CCL5. Biochem Soc Trans 39(6):1649-1653. doi: 10.1042/BST20110651
49. Bourghardt Peebo B, Fagerholm P, Traneus-Rockert C, Lagali N (2011) Time-lapse in vivo imaging of corneal angiogenesis: the role of inflammatory cells in capillary sprouting. Invest Ophthalmol Vis Sci 52(6):3060-3068. doi: 10.1167/iovs.10-6101
50. Arroyo AG, Iruela-Arispe ML (2010) Extracellular matrix, inflammation, and the angiogenic response. Cardiovasc Res 86(2):226-235. doi: 10.1093/cvr/cvq049
51. Crackower MA, Sarao R, Oudit GY, Yagil C, Kozieradzki I, Scanga SE, Oliveira-dos-Santos AJ, da Costa J, Zhang L, Pei Y, Scholey J, Ferrario CM, Manoukian AS, Chappell MC, Backx PH, Yagil Y, Penninger JM (2002) Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature 417(6891):822-828. doi: 10.1038/nature00786
52. English WR, Corvol P, Murphy G (2012) LPS activates ADAM9 dependent shedding of ACE from endothelial cells. Biochem Biophys Res Commun 421(1):70-75. doi: 10.1016/j.bbrc.2012.03.113
53. Corvol P, Michaud A, Soubrier F, Williams TA (1995) Recent advances in knowledge of the structure and function of the angiotensin I converting enzyme. J Hypertens Suppl 13(3):S3-10
54. Niu T, Chen X, Xu X (2002) Angiotensin converting enzyme gene insertion/deletion polymorphism and cardiovascular disease: therapeutic implications. Drugs 62(7):977-993
55. Kohlstedt K, Trouvain C, Boettger T, Shi L, Fisslthaler B, Fleming I (2013) The AMP-activated protein kinase regulates endothelial cell angiotensin-converting enzyme expression via p53 and the post-transcriptional regulation of microRNA-143/145. Circ Res. doi: 10.1161/CIRCRESAHA.113.301282
56. Paulis L, Unger T (2010) Novel therapeutic targets for hypertension. Nat Rev Cardiol 7(8):431-441. doi: 10.1038/nrcardio.2010.85
57. Hamdi HK, Castellon R (2003) ACE inhibition actively promotes cell survival by altering gene expression. Biochem Biophy Res Commun 310(4):1227-1235
58. Rubin H (1997) Cell aging in vivo and in vitro. Mech Ageing Dev 98(1):1-35
59. Ljungberg LU, Persson K (2008) Effect of nicotine and nicotine metabolites on angiotensin-converting enzyme in human endothelial cells. Endothelium 15(5-6):239-245. doi: 10.1080/10623320802487627
60. Mima Y, Fukumoto S, Koyama H, Okada M, Tanaka S, Shoji T, Emoto M, Furuzono T, Nishizawa Y, Inaba M (2012) Enhancement of cell-based therapeutic angiogenesis using a novel type of injectable scaffolds of hydroxyapatite- polymer nanocomposite microspheres. PLoS ONE 7(4):e35199. doi: 10.1371/journal.pone.0035199