Retinal endothelial cell apoptosis stimulates recruitment of endothelial progenitor cells

Investigative Ophthalmology and Visual Science

Volumn 50, Issue 10, 2009, Pages 4967-4973

  Bhatwadekar, Ashay D ^a,b   Glenn, Josephine V ^a   Curtis, Tim M ^a   Grant, Maria B ^b   Stitt, Alan W ^a   Gardiner, Tom A ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; VERTEPORFIN; CYTOKINE; INTERCELLULAR ADHESION MOLECULE 1; PHOTOSENSITIZING AGENT; PORPHYRIN; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN A;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE; CELL DAMAGE; CELL REGENERATION; CELL SIZE; CELL STIMULATION; CHEMOTAXIS; CONTROLLED STUDY; COW; MICROVASCULARIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA BLOOD VESSEL; RETINA CELL; RETINA ENDOTHELIUM CELL; STEM CELL; UPREGULATION; ANIMAL; CAPILLARY; CATTLE; CELL ADHESION; CELL CULTURE; CELL MOTION; CYTOLOGY; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIUM; WOUND HEALING;

ANIMALS; APOPTOSIS; CAPILLARIES; CATTLE; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; CHEMOTAXIS; CYTOKINES; E-SELECTIN; ENDOTHELIUM, VASCULAR; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; INTERCELLULAR ADHESION MOLECULE-1; PHOTOSENSITIZING AGENTS; PORPHYRINS; RETINAL VESSELS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STEM CELLS; UP-REGULATION; VASCULAR CELL ADHESION MOLECULE-1; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

EID: 70349561269     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-3616     Document Type: Article

References (54)

1. Heissig B, Hattori K, Friedrich M, Rafii S, Werb Z. Angiogenesis: vascular remodeling of the extracellular matrix involves metalloproteinases. Curr Opin Hematol. 2003;10:136-141.
2. Feng Y, vom Hagen F, Lin J, Hammes HP. Incipient diabetic retinopathy: insights from an experimental model. Ophthalmologica. 2007;221:269-274.
3. Mizutani M, Kern TS, Lorenzi M. Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy. J Clin Invest. 1996;97:2883-2890.
4. Hermans MP. Diabetes and the endothelium. Acta Clin Belg. 2007; 62:97-101.
5. Boyd-White J, Williams JC Jr. Effect of cross-linking on matrix permeability: a model for AGE-modified basement membranes. Diabetes. 1996;45:348-353.
6. Wells-Knecht KJ, Zyzak DV, Litchfield JE, Thorpe SR, Baynes JW. Mechanism of autoxidative glycosylation: identification of glyoxal and arabinose as intermediates in the autoxidative modification of proteins by glucose. Biochemistry. 1995;34:3702-3709.
7. Dobler D, Ahmed N, Song L, Eboigbodin KE, Thornalley PJ. Increased dicarbonyl metabolism in endothelial cells in hyperglycemia induces anoikis and impairs angiogenesis by RGD and GFOGER motif modification. Diabetes. 2006;55:1961-1969.
8. Yamagishi S, Imaizumi T. Diabetic vascular complications: pathophysiology, biochemical basis and potential therapeutic strategy. Curr Pharm Des. 2005;11:2279-2299.
9. Yamashiro K, Tsujikawa A, Ishida S, et al. Platelets accumulate in the diabetic retinal vasculature following endothelial death and suppress blood-retinal barrier breakdown. Am J Pathol. 2003;163: 253-259.
10. Butler JM, Guthrie SM, Koc M, et al. SDF-1 is both necessary and sufficient to promote proliferative retinopathy. J Clin Invest. 2005; 115:86-93.
11. Urbich C, Dimmeler S. Endothelial progenitor cells: characterization and role in vascular biology. Circ Res. 2004;95:343-353.
12. Henson PM, Bratton DL, Fadok VA. Apoptotic cell removal. Curr Biol. 2001;11:R795-R805.
13. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275: 964-967.
14. Grant MB, May WS, Caballero S, et al. Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat Med. 2002;8:607-612.
15. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med. 2003; 9:702-712.
16. Hibbert B, Olsen S, O'Brien E. Involvement of progenitor cells in vascular repair. Trends Cardiovasc Med. 2003;13:322-326.
17. Wijelath ES, Rahman S, Murray J, Patel Y, Savidge G, Sobel M. Fibronectin promotes VEGF-induced CD34 cell differentiation into endothelial cells. J Vasc Surg. 2004;39:655-660.
18. Hristov M, Erl W, Linder S, Weber PC. Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro. Blood. 2004; 104:2761-2766.
19. Stitt AW, Chakravarthy U, Archer DB, Gardiner TA. Increased endocytosis in retinal vascular endothelial cells grown in high glucose medium is modulated by inhibitors of nonenzymatic glycosylation. Diabetologia. 1995;38:1271-1275.
20. Bhatwadekar AD, Glenn JV, Li G, Curtis TM, Gardiner TA, Stitt AW. Advanced glycation of fibronectin impairs vascular repair by endothelial progenitor cells: implications for vasodegeneration in diabetic retinopathy. Invest Ophthalmol Vis Sci. 2008;49:1232-1241.
21. Mills JC, Stone NL, Erhardt J, Pittman RN. Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation. J Cell Biol. 1998;140:627-636.
22. Messam CA, Pittman RN. Asynchrony and commitment to die during apoptosis. Exp Cell Res. 1998;238:389-398.
23. Levy JG. Photosensitizers in photodynamic therapy. Semin Oncol. 1994;21:4-10.
24. Granville DJ, Shaw JR, Leong S, et al. Release of cytochrome c, Bax migration, Bid cleavage, and activation of caspases 2, 3, 6, 7, 8, and 9 during endothelial cell apoptosis. Am J Pathol. 1999;155:1021-1025.
25. Caballero S, Sengupta N, Afzal A, et al. Ischemic vascular damage can be repaired by healthy, but not diabetic, endothelial progenitor cells. Diabetes. 2007;56:960-967.
26. Yoon CH, Hur J, Oh IY, et al. Intercellular adhesion molecule-1 is upregulated in ischemic muscle, which mediates trafficking of endothelial progenitor cells. Arterioscler Thromb Vasc Biol. 2006; 26:1066-1072.
27. Shreeniwas R, Koga S, Karakurum M, et al. Hypoxia-mediated induction of endothelial cell interleukin-1 alpha: an autocrine mechanism promoting expression of leukocyte adhesion molecules on the vessel surface. J Clin Invest. 1992;90:2333-2339.
28. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia. 2006;20:1487-1495.
29. Puro DG. Physiology and pathobiology of the pericyte-containing retinal microvasculature: new developments. Microcirculation. 2007;14:1-10.
30. Mallat Z, Benamer H, Hugel B, et al. Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation. 2000;101:841-843.
31. McLaughlin R, Kelly CJ, Kay E, Bouchier-Hayes D. The role of apoptotic cell death in cardiovascular disease. Ir J Med Sci. 2001; 170:132-140.
32. Gill M, Dias S, Hattori K, et al. Vascular trauma induces rapid but transient mobilization of VEGFR2()AC133() endothelial precursor cells. Circ Res. 2001;88:167-174.
33. Lauber K, Blumenthal SG, Waibel M, Wesselborg S. Clearance of apoptotic cells: getting rid of the corpses. Mol Cell. 2004;14:277-287.
34. Harrington EO, Stefanec T, Newton J, Rounds S. Release of soluble E-selectin from activated endothelial cells upon apoptosis. Lung. 2006;184:259-266.
35. Subramaniam M, Koedam JA, Wagner DD. Divergent fates of P- and E-selectins after their expression on the plasma membrane. Mol Biol Cell. 1993;4:791-801.
36. Houle JM, Strong A. Clinical pharmacokinetics of verteporfin. J Clin Pharmacol. 2002;42:547-557.
37. Zen K, Okigaki M, Hosokawa Y, et al. Myocardium-targeted delivery of endothelial progenitor cells by ultrasound-mediated microbubble destruction improves cardiac function via an angiogenic response. J Mol Cell Cardiol. 2006;40:799-809.
38. van Buul JD, Voermans C, van den Berg V, et al. Migration of human hematopoietic progenitor cells across bone marrow endothelium is regulated by vascular endothelial cadherin. J Immunol. 2002;168:588-596.
39. Joussen AM, Poulaki V, Le ML, et al. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J. 2004;18: 1450-1452.
40. Caldwell RB, Bartoli M, Behzadian MA, et al. Vascular endothelial growth factor and diabetic retinopathy: pathophysiological mechanisms and treatment perspectives. Diabetes Metab Res Rev. 2003; 19:442-455.
41. Kalka C, Masuda H, Takahashi T, et al. Vascular endothelial growth factor(165) gene transfer augments circulating endothelial progenitor cells in human subjects. Circ Res. 2000;86:1198-1202.
42. Iwaguro H, Yamaguchi J, Kalka C, et al. Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation. 2002;105:732-738.
43. Yun HJ, Jo DY. Production of stromal cell-derived factor-1 (SDF-1) and expression of CXCR4 in human bone marrow endothelial cells. J Korean Med Sci. 2003;18:679-685.
44. Lima e Silva R, Shen J, Hackett SF, et al. The SDF-1/CXCR4 ligand/ receptor pair is an important contributor to several types of ocular neovascularization. FASEB J. 2007;21(12):3219-3230.
45. Du R, Lu KV, Petritsch C, et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell. 2008;13:206-220.
46. Massberg S, Konrad I, Schurzinger K, et al. Platelets secrete stromal cell-derived factor 1alpha and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo. J Exp Med. 2006;203: 1221-1233.
47. Gaugler MH, Squiban C, Mouthon MA, Gourmelon P, van der Meeren A. Irradiation enhances the support of haemopoietic cell transmigration, proliferation and differentiation by endothelial cells. Br J Haematol. 2001;113:940-950.
48. Lee PC, Ho IC, Lee TC. Oxidative stress mediates sodium arseniteinduced expression of heme oxygenase-1, monocyte chemoattractant protein-1, and interleukin-6 in vascular smooth muscle cells. Toxicol Sci. 2005;85:541-550.
49. Fan Y, Ye J, Shen F, et al. Interleukin-6 stimulates circulating blood-derived endothelial progenitor cell angiogenesis in vitro. J Cereb Blood Flow Metab. 2008;28(1):90-98.
50. Li N, Eljaafari A, Bensoussan D, et al. Human umbilical vein endothelial cells increase ex vivo expansion of human CD34() PBPC through IL-6 secretion. Cytotherapy. 2006;8:335-342.
51. Hernandez C, Segura RM, Fonollosa A, Carrasco E, Francisco G, Simo R. Interleukin-8, monocyte chemoattractant protein-1 and IL-10 in the vitreous fluid of patients with proliferative diabetic retinopathy. Diabet Med. 2005;22:719-722.
52. Schomig K, Busch G, Steppich B, et al. Interleukin-8 is associated with circulating CD133 progenitor cells in acute myocardial infarction. Eur Heart J. 2006;27:1032-1037.
53. Goukassian DA, Qin G, Dolan C, et al. Tumor necrosis factor-alpha receptor p75 is required in ischemia-induced neovascularization. Circulation. 2007;115:752-762.
54. Ablin JN, Boguslavski V, Aloush V, et al. Effect of anti-TNFalpha treatment on circulating endothelial progenitor cells (EPCs) in rheumatoid arthritis. Life Sci. 2006;79:2364-2369.