Promise of endothelial progenitor cell for treatment of diabetic retinopathy

Expert Review of Endocrinology and Metabolism

Volumn 5, Issue 1, 2010, Pages 29-37

  Bhatwadekar, Ashay D ^a   Shaw, Lynn C ^a   Grant, Maria B ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Diabetic retinopathy; Endothelial nitric oxide synthase; Endothelial progenitor cell

Indexed keywords

CD45 ANTIGEN; NITRIC OXIDE;

ACUTE HEART INFARCTION; BONE MARROW; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CELL REGENERATION; DIABETIC RETINOPATHY; ENDOTHELIAL PROGENITOR CELL; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MAGNETIC SEPARATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; RETINA BLOOD VESSEL; RETINA ISCHEMIA; RETINA MACULA EDEMA; RETINA NEOVASCULARIZATION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION;

EID: 77949837340     PISSN: 17446651     EISSN: None     Source Type: Journal    
DOI: 10.1586/eem.09.75     Document Type: Review

References (83)

1. Fong DS, Sharza M, Chen W, Paschal JF, Ariyasu RG, Lee PP. Vision loss among diabetics in a group model health maintenance organization (HMO). Am. J. Ophthalmol. 133(2), 236-241 (2002).
2. Early Treatment Diabetic Retinopathy Study Research Group. Early photocoagulation for diabetic retinopathy. ETDRS report number 9. Ophthalmology 98(5 Suppl.), 766-785 (1991).
3. Early Treatment Diabetic Retinopathy Study Research Group.Focal photocoagulation treatment of diabetic macular edema. Relationship of treatment effect to fluorescein angiographic and other retinal characteristics at baseline: ETDRS report no. 19. Arch. Ophthalmol. 113(9), 1144-1155 (1995).
4. Asahara T, Murohara T, Sullivan A, Silver M, Van Der Zee R, Li T. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275, 964-967 (1997).
5. Ingram DA, Mead LE, Moore DB, Woodard W, Fenoglio A, Yoder MC. Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood 105(7), 2783-2786 (2005).
6. Grant MB, May WS, Caballero S et al. Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat. Med. 8(6), 607-612 (2002).
7. Bailey AS, Jiang S, Afentoulis M et al. Transplanted adult hematopoietic stems cells differentiate into functional endothelial cells. Blood 103(1), 13-19 (2004).
8. Loomans CJ, Van Haperen R, Duijs JM et al. Differentiation of bone marrowderived endothelial progenitor cells is shifted into a proinflammatory phenotype by hyperglycemia. Mol. Med. 15(5-6), 152-159 (2009).
9. Case J, Ingram DA, Haneline LS. Oxidative stress impairs endothelial progenitor cell function. Antioxid. Redox Signal. 10(11), 1895-1907 (2008).
10. Loomans CJ, De Koning EJ, Staal FJ et al. Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of Type 1 diabetes. Diabetes 53(1), 195-199 (2004).
11. Funada J, Sekiya M, Hamada M, Hiwada K. Postprandial elevation of remnant lipoprotein leads to endothelial dysfunction. Circ. J. 66(2), 127-132 (2002).
12. Imanishi T, Hano T, Sawamura T, Nishio I. Oxidized low-density lipoprotein induces endothelial progenitor cell senescence, leading to cellular dysfunction. Clin. Exp. Pharmacol. Physiol. 31(7), 407-413 (2004).
13. Zhu J, Xu ZK, Miao Y, Liu XL, Zhang H. Changes of inducible protein-10 and regulated upon activation, normal t cell expressed and secreted protein in acute rejection of pancreas transplantation in rats. World J. Gastroenterol. 12(26), 4156-4160 (2006).
14. Tamarat R, Silvestre JS, Le Ricousse- Roussanne S et al. Impairment in ischemiainduced neovascularization in diabetes: bone marrow mononuclear cell dysfunction and therapeutic potential of placenta growth factor treatment. Am. J. Pathol. 164(2), 457-466 (2004).
15. Kern TS, Engerman RL. Pharmacological inhibition of diabetic retinopathy: aminoguanidine and aspirin. Diabetes 50(7), 1636-1642 (2001).
16. Caballero S, Sengupta N, Afzal A et al. Ischemic vascular damage can be repaired by healthy, but not diabetic, endothelial progenitor cells. Diabetes 56(4), 960-967 (2007).
17. Fadini GP, Sartore S, Baesso I et al. Endothelial progenitor cells and the diabetic paradox. Diabetes Care 29(3), 714-716 (2006).
18. Lee IG, Chae SL, Kim JC. Involvement of circulating endothelial progenitor cells and vasculogenic factors in the pathogenesis of diabetic retinopathy. Eye (Lond.) 20(5), 546-552 (2006).
19. Rafat N, Beck GC, Schulte J, Tuettenberg J, Vajkoczy P. Circulating endothelial progenitor cells in malignant gliomas. J. Neurosurg. (2009) (Epub ahead of print).
20. Gehling UM, Ergun S, Schumacher U et al. In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 95(10), 3106-3112 (2000).
21. Lin Y, Weisdorf DJ, Solovey A, Hebbel RP. Origins of circulating endothelial cells and endothelial outgrowth from blood. J. Clin. Invest. 105(1), 71-77 (2000).
22. Gulati R, Jevremovic D, Peterson TE et al. Diverse origin and function of cells with endothelial phenotype obtained from adult human blood. Circ. Res. 93(11), 1023-1025 (2003).
23. Gulati R, Jevremovic D, Peterson TE et al. Autologous culture-modified mononuclear cells confer vascular protection after arterial injury. Circulation 108(12), 1520-1526 (2003).
24. Asahara T, Takahashi T, Masuda H et al. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J. 18(14), 3964-3972 (1999).
25. Wijelath ES, Murray J, Rahman S et al. Novel vascular endothelial growth factor binding domains of fibronectin enhance vascular endothelial growth factor biological activity. Circ. Res. 91(1), 25-31 (2002).
26. Eggermann J, Kliche S, Jarmy G et al. Endothelial progenitor cell culture and differentiation in vitro: a methodological comparison using human umbilical cord blood. Cardiovasc. Res. 58(2), 478-486 (2003).
27. Fernandez Pujol B, Lucibello FC, Gehling UM et al. Endothelial-like cells derived from human CD14 positive monocytes. Differentiation 65(5), 287-300 (2000).
28. Hur J, Yoon CH, Kim HS et al. Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler. Thromb. Vasc. Biol. 24(2), 288-293 (2004).
29. Delorme B, Basire A, Gentile C et al. Presence of endothelial progenitor cells, distinct from mature endothelial cells, within human CD146+ blood cells. Thromb. Haemost. 94(6), 1270-1279 (2005).
30. Crosby JR, Kaminski WE, Schatteman G et al. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ. Res. 87(9), 728-730. (2000).
31. Yoon CH, Hur J, Park KW et al. Synergistic neovascularization by mixed transplantation of early endothelial progenitor cells and late outgrowth endothelial cells: the role of angiogenic cytokines and matrix metalloproteinases. Circulation 112(11), 1618-1627 (2005).
32. Schatteman GC, Dunnwald M, Jiao C. Biology of bone marrow-derived endothelial cell precursors. Am. J. Physiol. Heart Circ. Physiol. 292(1), H1-H18 (2007).
33. 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. 86(12), 1198-1202. (2000).
34. Harraz M, Jiao C, Hanlon HD, Hartley RS, Schatteman GC. CD34- blood-derived human endothelial cell progenitors. Stem Cells 19(4), 304-312 (2001).
35. Romagnani P, Annunziato F, Liotta F et al. CD14+CD34low cells with stem cell phenotypic and functional features are the major source of circulating endothelial progenitors. Circ. Res. 97(4), 314-322 (2005).
36. Awad O, Dedkov EI, Jiao C, Bloomer S, Tomanek RJ, Schatteman GC. Differential healing activities of CD34+ and CD14+ endothelial cell progenitors. Arterioscler. Thromb. Vasc. Biol. 26(4), 758-764 (2006).
37. Cho HJ, Kim HS, Lee MM et al. Mobilized endothelial progenitor cells by granulocyte-macrophage colonystimulating factor accelerate reendothelialization and reduce vascular inflammation after intravascular radiation. Circulation 108(23), 2918-2925 (2003).
38. George J, Herz I, Goldstein E et al. Number and adhesive properties of circulating endothelial progenitor cells in patients with in-stent restenosis. Arterioscler. Thromb. Vasc. Biol. 23(12), e57-e60 (2003).
39. Ghani U, Shuaib A, Salam A et al. Endothelial progenitor cells during cerebrovascular disease. Stroke 36(1), 151-153 (2005).
40. Loomans CJ, Wan H, De Crom R et al. Angiogenic murine endothelial progenitor cells are derived from a myeloid bone marrow fraction and can be identified by endothelial no synthase expression. Arterioscler. Thromb. Vasc. Biol. 26(8), 1760-1767 (2006).
41. Aicher A, Zeiher AM, Dimmeler S. Mobilizing endothelial progenitor cells. Hypertension 45(3), 321-325 (2005).
42. Heissig B, Hattori K, Dias S et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109(5), 625-637 (2002).
43. Heissig B, Werb Z, Rafii S, Hattori K. Role of c-kit/kit ligand signaling in regulating vasculogenesis. Thromb. Haemost. 90(4), 570-576 (2003).
44. Shintani S, Murohara T, Ikeda H et al. Augmentation of postnatal neovascularization with autologous bone marrow transplantation. Circulation 103(6), 897-903 (2001).
45. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by AKT-dependent phosphorylation. Nature 399(6736), 601-605. (1999).
46. Sorrentino SA, Bahlmann FH, Besler C et al. Oxidant stress impairs in vivo reendothelialization capacity of endothelial progenitor cells from patients with Type 2 diabetes mellitus: Restoration by the peroxisome proliferator-activated receptor-g agonist rosiglitazone. Circulation 116(2), 163-173 (2007).
47. Thum T, Fraccarollo D, Schultheiss M et al. Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes. Diabetes 56(3), 666-674 (2007).
48. Vasa M, Breitschopf K, Zeiher AM, Dimmeler S. Nitric oxide activates telomerase and delays endothelial cell senescence. Circ. Res. 87(7), 540-542 (2000).
49. Li Calzi S, Purich DL, Chang KH et al. Carbon monoxide and nitric oxide mediate cytoskeletal reorganization in microvascular cells via vasodilatorstimulated phosphoprotein (VASP) phosphorylation: evidence for blunted responsiveness in diabetes. Diabetes 57(9), 2488-2494 (2008).
50. Segal MS, Shah R, Afzal A et al. Nitric oxide cytoskeletal-induced alterations reverse the endothelial progenitor cell migratory defect associated with diabetes. Diabetes 55(1), 102-109 (2006).
51. Chang KH, Chan-Ling T, Mcfarland EL et al. IGF binding protein-3 regulates hematopoietic stem cell and endothelial precursor cell function during vascular development. Proc. Natl Acad. Sci. USA 104(25), 10595-10600 (2007).
52. Ma FX, Zhou B, Chen Z et al. Oxidized low density lipoprotein impairs endothelial progenitor cells by regulation of endothelial nitric oxide synthase. J. Lipid Res. 47(6), 1227-1237 (2006).
53. Shin T, Weinstock D, Castro MD et al. Immunohistochemical localization of endothelial and inducible nitric oxide synthase within neurons of cattle with rabies. J. Vet. Med. Sci. 66(5), 539-541 (2004).
54. Stadler K, Bonini MG, Dallas S, Duma D, Mason RP, Kadiiska MB. Direct evidence of inos-mediated in vivo free radical production and protein oxidation in acetone-induced ketosis. Am. J. Physiol. Endocrinol. Metab. 295(2), E456-462 (2008).
55. Leal EC, Manivannan A, Hosoya K et al. Inducible nitric oxide synthase isoform is a key mediator of leukostasis and blood- retinal barrier breakdown in diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 48(11), 5257-5265 (2007).
56. Nagareddy PR, Xia Z, Mcneill JH, Macleod KM. Increased expression of iNOS is associated with endothelial dysfunction and impaired pressor responsiveness in streptozotocin-induced diabetes. Am. J. Physiol. Heart Circ. Physiol. 289(5), H2144-H2152 (2005).
57. Cheng X, Cheng XS, Kuo KH, Pang CC. Inhibition of iNOS augments cardiovascular action of noradrenaline in streptozotocin-induced diabetes. Cardiovasc. Res. 64(2), 298-307 (2004).
58. Ellis EA, Guberski DL, Hutson B, Grant MB. Time course of NADH oxidase, inducible nitric oxide synthase and peroxynitrite in diabetic retinopathy in the BBZ/WOR rat. Nitric Oxide 6(3), 295-304 (2002).
59. Szabo C, Mabley JG, Moeller SM et al. Part I: pathogenetic role of peroxynitrite in the development of diabetes and diabetic vascular complications: studies with FP15, a novel potent peroxynitrite decomposition catalyst. Mol. Med. 8(10), 571-580 (2002).
60. Kobayashi T, Taguchi K, Takenouchi Y, Matsumoto T, Kamata K. Insulininduced impairment via peroxynitrite production of endothelium-dependent relaxation and sarco/endoplasmic reticulum Ca2+-ATPase function in aortas from diabetic rats. Free Radic. Biol. Med. 43(3), 431-443 (2007).
61. Camici GG, Schiavoni M, Francia P et al. Genetic deletion of p66(shc) adaptor protein prevents hyperglycemia-induced endothelial dysfunction and oxidative stress. Proc. Natl Acad. Sci. USA 104(12), 5217-5222 (2007).
62. Sasaki N, Yamashita T, Takaya T et al. Augmentation of vascular remodeling by uncoupled endothelial nitric oxide synthase in a mouse model of diabetes mellitus. Arterioscler. Thromb. Vasc. Biol. 28(6), 1068-1076 (2008).
63. Munzel T, Sayegh H, Freeman BA, Tarpey MM, Harrison DG. Evidence for enhanced vascular superoxide anion production in nitrate tolerance. A novel mechanism underlying tolerance and cross-tolerance. J. Clin. Invest. 95(1), 187-194 (1995).
64. Gao J, Zhao WX, Zhou LJ et al. Protective effects of propofol on lipopolysaccharideactivated endothelial cell barrier dysfunction. Inflamm. Res. 55(9), 385-392 (2006).
65. Luo T, Xia Z, Ansley DM et al. Propofol dose-dependently reduces tumor necrosis factor-a-induced human umbilical vein endothelial cell apoptosis: Effects on Bcl-2 and Bax expression and nitric oxide generation. Anesth. Analg. 100(6), 1653-1659 (2005).
66. Chen YS, Chen KH, Liu CC et al. Propofol-induced vascular permeability change is related to the nitric oxide signaling pathway and occludin phosphorylation. J. Biomed. Sci. 14(5), 629-636 (2007).
67. Sasaki K, Heeschen C, Aicher A et al. Ex vivo pretreatment of bone marrow mononuclear cells with endothelial NO synthase enhancer AVE9488 enhances their functional activity for cell therapy. Proc. Natl Acad. Sci. USA 103(39), 14537-14541 (2006).
68. Dimmeler S, Aicher A, Vasa M et al. HMG-COA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/AKT pathway. J. Clin. Invest. 108(3), 391-397. (2001).
69. Landmesser U, Engberding N, Bahlmann FH et al. Statin-induced improvement of endothelial progenitor cell mobilization, myocardial neovascularization, left ventricular function, and survival after experimental myocardial infarction requires endothelial nitric oxide synthase. Circulation 110(14), 1933-1939 (2004).
70. Verma S, Szmitko PE, Anderson TJ. Endothelial function: Ready for prime time? Can. J. Cardiol. 20(13), 1335-1339 (2004).
71. Forstermann U, Munzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 113(13), 1708-1714 (2006).
72. Thum T, Bauersachs J. Spotlight on endothelial progenitor cell inhibitors: short review. Vasc. Med. 10(Suppl. 1), S59-S64 (2005).
73. Achan V, Broadhead M, Malaki M et al. Asymmetric dimethylarginine causes hypertension and cardiac dysfunction in humans and is actively metabolized by dimethylarginine dimethylaminohydrolase. Arterioscler. Thromb. Vasc. Biol. 23(8), 1455-1459 (2003).
74. Dayoub H, Achan V, Adimoolam S et al. Dimethylarginine dimethylaminohydrolase regulates nitric oxide synthesis: genetic and physiological evidence. Circulation 108(24), 3042-3047 (2003).
75. Busik JV, Tikhonenko M, Bhatwadekar A, Opreanu M et al. Diabetic retinopathy is associated with bone marrow neuropathy and a depressed peripheral clock. J. Exp. Med. DOI: jem.20090889v1- jem.20090889 (2009) (Epub ahead of print).
76. Naveiras O, Nardi V, Wenzel PL, Hauschka PV, Fahey F, Daley GQ. Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature 460(7252), 259-263 (2009).
77. Digman C, Borto D, Nasraway SA Jr. Hyperglycemia in the critically ill. Nutr. Clin. Care 8(2), 93-101 (2005).
78. Maaravi Y, Stessman J. Mild, reversible pancytopenia induced by rosiglitazone. Diabetes Care 28(6), 1536 (2005).
79. Berria R, Glass L, Mahankali A et al. Reduction in hematocrit and hemoglobin following pioglitazone treatment is not hemodilutional in Type II diabetes mellitus. Clin. Pharmacol. Ther. 82(3), 275-281 (2007).
80. Lazarenko OP, Rzonca SO, Hogue WR, Swain FL, Suva LJ, Lecka-Czernik B. Rosiglitazone induces decreases in bone mass and strength that are reminiscent of aged bone. Endocrinology 148(6), 2669-2680 (2007).
81. Khan SS, Solomon MA, Mccoy JP Jr. Detection of circulating endothelial cells and endothelial progenitor cells by flow cytometry. Cytometry B Clin. Cytom. 64(1), 1-8 (2005).
82. Schachinger V, Erbs S, Elsasser A et al. Improved clinical outcome after intracoronary administration of bonemarrow- derived progenitor cells in acute myocardial infarction: final 1-year results of the REPAIR-AMI trial. Eur. Heart J. 27(23), 2775-2783 (2006).
83. Erbs S, Linke A, Schachinger V et al. Restoration of microvascular function in the infarct-related artery by intracoronary transplantation of bone marrow progenitor cells in patients with acute myocardial infarction: the Doppler substudy of the reinfusion of enriched progenitor cells and infarct remodeling in acute myocardial infarction (REPAIR-AMI) trial. Circulation 116(4), 366-374 (2007).