Expression of angiogenic MicroRNAs in endothelial progenitor cells from type 1 diabetic patients with and without diabetic retinopathy

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 6, 2015, Pages 4090-4098

  de la Torre, Nuria García ^a   Fernández Durango, Raquel ^a   Gómez, Raquel ^a   Fuentes, Manuel ^a   Roldán Pallarés, Manuela ^a   Donate, Juan ^a   Barabash, Ana ^a   Alonso, Bárbara ^a   Runkle, Isabelle ^a   Durán, Alejandra ^a   Rubio, Miguel Angel ^a   Calle Pascual, Alfonso L ^a  

^a HOSPITAL CLÍNICO SAN CARLOS   (Spain)

Author keywords

Endothelial progenitor cells (EPCs); miR 126; miR 221; miR 222

Indexed keywords

ANGIOTENSIN RECEPTOR ANTAGONIST; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; HEMOGLOBIN A1C; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MICRORNA; MICRORNA 126; MICRORNA 221; MICRORNA 222; MONOCLONAL ANTIBODY; MIRN126 MICRORNA, HUMAN; MIRN221 MICRORNA, HUMAN; MIRN222 MICRORNA, HUMAN;

ADULT; APOPTOSIS; ARTICLE; BODY MASS; CELLS BY BODY ANATOMY; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC RETINOPATHY; DIASTOLIC BLOOD PRESSURE; DISEASE COURSE; ENDOTHELIAL PROGENITOR CELL; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; TRIACYLGLYCEROL BLOOD LEVEL; VENOUS BLOOD; AGED; CASE CONTROL STUDY; METABOLISM;

ADULT; AGED; CASE-CONTROL STUDIES; DIABETES MELLITUS, TYPE 1; DIABETIC RETINOPATHY; ENDOTHELIAL PROGENITOR CELLS; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; MICRORNAS; MIDDLE AGED; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84939824216     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.15-16498     Document Type: Article

References (43)

1. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997; 275:964-967.
2. Takahashi T, Kalka C, Masuda H, et al. Ischemia- and cytokineinduced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med. 1999;5:434- 438.
3. Otani A, Kinder K, Ewalt K, Otero FJ, Schimmel P, Friedlander M. Bone marrow-derived stem cells target retinal astrocytes and can promote or inhibit retinal angiogenesis. Nat Med. 2002;8:1004-1010.
4. 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.
5. Tamarat R, Silvestre JS, Le Ricousse-Roussanne S, et al. Impairment in ischemia-induced neovascularization in diabetes: bone marrow mononuclear cell dysfunction and therapeutic potential of placenta growth factor treatment. Am J Pathol. 2004;164:457-466.
6. 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.
7. Fadini GP, Miorin M, Facco M, et al. Circulating endothelial progenitor cells are reduced in peripheral vascular complications of type 2 diabetes mellitus. J Am Coll Cardiol. 2005;45: 1449-1457.
8. 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. 2004;53:195-199.
9. Kusuyama T, Omura T, Nishiya D, et al. Effects of treatment for diabetes mellitus on circulating vascular progenitor cells. J Pharmacol Sci. 2006;102:96-102.
10. Lee IG, Chae SL, Kim JC. Involvement of circulating endothelial progenitor cells and vasculogenic factors in the pathogenesis of diabetic retinopathy. Eye (Lond). 2006;20: 546-552.
11. Brunner S, Schernthaner GH, Satler M, et al. Correlation of different circulating endothelial progenitor cells to stages of diabetic retinopathy: first in vivo data. Invest Ophthalmol Vis Sci. 2009;50:392-398.
12. Tepper OM, Galiano RD, Capla JM, et al. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation. 2002;106:2781-2786.
13. Tan K, Lessieur E, Cutler A, et al. Impaired function of circulating CD34+ CD45-ells in patients with proliferative diabetic retinopathy. Exp Eye Res. 2010;91:229-237.
14. Hristov M, Weber C. Endothelial progenitor cells in vascular repair and remodeling. Pharmacol Res. 2008;58:148-151.
15. Yoder MC. Endothelial progenitor cell: a blood cell by many other names may serve similar functions. J Mol Med (Berl). 2013;91:285-295.
16. Werling NJ, Thorpe R, Zhao Y. A systematic approach to the establishment and characterization of endothelial progenitor cells for gene therapy. Hum Gene Ther Methods. 2013;24: 171-184.
17. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell. 2006; 125:1111-1124.
18. Anand S. A brief primer on microRNAs and their roles in angiogenesis. Vasc Cell. 2013;5:2.
19. Liu X, Cheng Y, Yang J, Xu L, Zhang C. Cell-specific effects of miR-221/222 in vessels: molecular mechanism and therapeutic application. J Mol Cell Cardiol. 2012;52:245-255.
20. Poliseno L, Tuccoli A, Mariani L, et al. MicroRNAs modulate the angiogenic properties of HUVECs. Blood. 2006;108:3068- 3071.
21. Li Y, Song YH, Li F, Yang T, Lu YW, Geng YJ. MicroRNA-221 regulates high glucose-induced endothelial dysfunction. Biochem Biophys Res Commun. 2009;381:81-83.
22. Meng S, Cao JT, Zhang B, Zhou Q, Shen CX, Wang CQ. Downregulation of microRNA-126 in endothelial progenitor cells from diabetes patients, impairs their functional properties, via target gene Spred-1. J Mol Cell Cardiol. 2012;53:64- 72.
23. Jansen F, Yang X, Hoelscher M, et al. Endothelial microparticlemediated transfer of micro-RNA-126 promotes vascular endothelial cell repair via SPRED1 and is abrogated in glucosedamaged endothelial microparticles. Circulation. 2013;128: 2026-2038.
24. Early Treatment Diabetic Retinopathy Study Research Group. Grading diabetic retinopathy from stereoscopic color fundus photographs-an extension of the modified Airlie House classification. ETDRS report number 10. Ophthalmology. 1991;98(suppl 5):786-806.
25. Hristov M, Schmitz S, Nauwelaers F, Weber C. A flow cytometric protocol for enumeration of endothelial progenitor cells and monocyte subsets in human blood. J Immunol Methods. 2012;381:9-13.
26. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25:402-408.
27. Hörtenhuber T, Rami-Mehar B, Satler M, et al. Endothelial progenitor cells are related to glycemic control in children with type 1 diabetes over time. Diabetes Care. 2013;36:1647- 1653.
28. DiMeglio LA, Tosh A, Saha C, et al. Endothelial abnormalities in adolescents with type 1 diabetes: a biomarker for vascular sequelae? J Pediatr. 2010;157:540-546.
29. Hernandez SL, Gong JH, Chen L, et al. Characterization of circulating and endothelial progenitor cells in patients with extreme-duration type 1 diabetes. Diabetes Care. 2014;37: 2193-2201.
30. Fadini GP, Losordo D, Dimmeler S. Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res. 2012;110:624-637.
31. Liu Y, Gao G, Yang C, et al. The role of circulating microRNA- 126 (miR-126): a novel biomarker for screening prediabetes and newly diagnosed type 2 diabetes mellitus. Int J Mol Sci. 2014;15:10567-10577.
32. Zampetaki A, Kiechl S, Drozdov I, et al. Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res. 2010;107:810-817.
33. Fichtlscherer S, De Rosa S, Fox H, et al. Circulating microRNAs in patients with coronary artery disease. Circ Res. 2010;107: 677-684.
34. Kontaraki JE, Marketou ME, Zacharis EA, Parthenakis FI, Vardas PE. MicroRNA-9 and microRNA-126 expression levels in patients with essential hypertension: potential markers of target-organ damage. J Am Soc Hypertens. 2014;8:368-375.
35. Bijkerk R, van Solingen C, de Boer HC, et al. Hematopoietic microRNA-126 protects against renal ischemia/reperfusion injury by promoting vascular integrity. J Am Soc Nephrol. 2014;25:1710-1722.
36. Zhang X, Mao H, Chen JY, et al. Increased expression of microRNA-221 inhibits PAK1 in endothelial progenitor cells and impairs its function via c-Raf/MEK/ERK pathway. Biochem Biophys Res Commun. 2013;431:404-408.
37. Dodson PM, Galton DJ, Winder AF. Retinal vascular abnormalities in the hyperlipidemias. Trans Ophthalmol Soc U K. 1981; 101:17-21.
38. Keech A, Simes RJ, Barter P, et al. Effects of long-term fenofibrate therapy on cardiovascular events in 9795 people with type 2 diabetes mellitus (the FIELD study): randomised controlled trial. Lancet. 2005;366:1849-1861.
39. Chew EY, Ambrosius WT, Davis MD, et al.; for the ACCORD Eye Study Group. Effects of medical therapies on retinopathy progression in type 2 diabetes. N Engl J Med. 2010;363:233- 244.
40. Wright AD, Dodson PM. Medical management of diabetic retinopathy: fenofibrate and ACCORD Eye studies. Eye (Lond). 2011;25:843-849.
41. Westenskow PD, Kurihara T, Aguilar E, et al. Ras pathway inhibition prevents neovascularization by repressing endothelial cell sprouting. J Clin Invest. 2013;123:4900-4908.
42. Chen N, Wang J, Hu Y, et al. MicroRNA-410 reduces the expression of vascular endothelial growth factor and inhibits oxygen induced retinal neovascularization. PLoS One. 2014;9: e95665.
43. Bai Y, Bai X, Wang Z, Zhang X, Ruan C, Miao J. MicroRNA-126 inhibits ischemia-induced retinal neovascularization via regulating angiogenic growth factors. Exp Mol Pathol. 2011;91: 471-477.