Loss of angiomir-126 and 130a in angiogenic early outgrowth cells from patients with chronic heart failure: Role for impaired in vivo neovascularization and cardiac repair capacity

Circulation

Volumn 126, Issue 25, 2012, Pages 2962-2975

  Jakob, Philipp ^a   Doerries, Carola ^a   Briand, Sylvie ^a   Mocharla, Pavani ^a   Kränkel, Nicolle ^a   Besler, Christian ^a   Mueller, Maja ^b   Manes, Costantina ^b   Templin, Christian ^b   Baltes, Christof ^a,b   Rudin, Markus ^a   Adams, Heiner ^b   Wolfrum, Mathias ^b   Noll, Georg ^b   Ruschitzka, Frank ^b   Lüscher, Thomas F ^a   Landmesser, Ulf ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

angiogenesis; cardiomyopathies; endothelial cells; heart failure; microRNAs; progenitor cells

Indexed keywords

MICRORNA; MICRORNA 126; MICRORNA 130A; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD34 SELECTION; CELL ISOLATION; CELL TYPE; CLINICAL ARTICLE; CONTROLLED STUDY; EARLY OUTGROWTH CELL; FEMALE; FLOW CYTOMETRY; GENE CONTROL; GENE EXPRESSION; GENE LOSS; GENETIC TRANSFECTION; HEART FAILURE; HEART FUNCTION; HEART INFARCTION; HEART SURGERY; HEART TRANSPLANTATION; HUMAN; IN VIVO STUDY; ISCHEMIC CARDIOMYOPATHY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIGENS, CD34; CHRONIC DISEASE; FEMALE; HEART; HEART FAILURE; HOMEODOMAIN PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MICE; MICRORNAS; MIDDLE AGED; MYOCARDIAL ISCHEMIA; NEOVASCULARIZATION, PHYSIOLOGIC;

EID: 84871322435     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.112.093906     Document Type: Article

References (52)

1. Fish JE, Srivastava D. MicroRNAs: opening a new vein in angiogenesis research. Sci Signal. 2009;2:pe1.
2. Wang S, Olson EN. AngiomiRs: key regulators of angiogenesis. Curr Opin Genet Dev. 2009;19:205-211.
3. Suarez Y, Sessa WC. MicroRNAs as novel regulators of angiogenesis. Circ Res. 2009;104:442-454.
4. Small EM, Frost RJ, Olson EN. MicroRNAs add a new dimension to cardiovascular disease. Circulation. 2010;121:1022-1032.
5. Kuehbacher A, Urbich C, Zeiher AM, Dimmeler S. Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ Res. 2007;101:59-68.
6. Suarez Y, Fernandez-Hernando C, Yu J, Gerber SA, Harrison KD, Pober JS, Iruela-Arispe ML, Merkenschlager M, Sessa WC. Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc Natl Acad Sci USA. 2008;105:14082-14087.
7. Fish JE, Santoro MM, Morton SU, Yu S, Yeh RF, Wythe JD, Ivey KN, Bruneau BG, Stainier DY, Srivastava D. miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell. 2008;15:272-284.
8. Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, Richardson JA, Bassel-Duby R, Olson EN. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008;15: 261-271.
9. Nicoli S, Standley C, Walker P, Hurlstone A, Fogarty KE, Lawson ND. MicroRNA-mediated integration of haemodynamics and VEGF signalling during angiogenesis. Nature. 2010;464:1196-1200.
10. van Solingen C, Seghers L, Bijkerk R, Duijs JM, Roeten MK, van Oeveren-Rietdijk AM, Baelde HJ, Monge M, Vos JB, de Boer HC, Quax PH, Rabelink TJ, van Zonneveld AJ. Antagomir-mediated silencing of endothelial cell specific microRNA-126 impairs ischemia-induced angio-genesis. J Cell Mol Med. 2009;13:1577-1585.
11. Chen Y, Gorski DH. Regulation of angiogenesis through a microRNA (miR-130a) that down-regulates antiangiogenic homeobox genes GAX and HOXA5. Blood. 2008;111:1217-1226.
12. Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, Burchfield J, Fox H, Doebele C, Ohtani K, Chavakis E, Potente M, Tjwa M, Urbich C, Zeiher AM, Dimmeler S. MicroRNA-92a controls angio-genesis and functional recovery of ischemic tissues in mice. Science. 2009;324:1710-1713.
13. Doebele C, Bonauer A, Fischer A, Scholz A, Reiss Y, Urbich C, Hofmann WK, Zeiher AM, Dimmeler S. Members of the microRNA-17-92 cluster exhibit a cell intrinsic anti-angiogenic function in endothelial cells. Blood. 2010;115:4944-4950.
14. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999;85:221-228.
15. Kawamoto A, Gwon HC, Iwaguro H, Yamaguchi JI, Uchida S, Masuda H, Silver M, Ma H, Kearney M, Isner JM, Asahara T. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation. 2001;103:634-637.
16. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM, Itescu S. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents car-diomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med. 2001;7:430-436.
17. Landmesser U, Drexler H. Chronic heart failure: an overview of conventional treatment versus novel approaches. Nat Clin Pract Cardiovasc Med. 2005;2:628-638.
18. Kawamoto A, Iwasaki H, Kusano K, Murayama T, Oyamada A, Silver M, Hulbert C, Gavin M, Hanley A, Ma H, Kearney M, Zak V, Asahara T, Losordo DW. CD34-positive cells exhibit increased potency and safety for therapeutic neovascularization after myocardial infarction compared with total mononuclear cells. Circulation. 2006;114:2163-2169.
19. Fazel S, Cimini M, Chen L, Li S, Angoulvant D, Fedak P, Verma S, Weisel RD, Keating A, Li RK. Cardioprotective c-kit+ cells are from the bone marrow and regulate the myocardial balance of angiogenic cyto-kines. J Clin Invest. 2006;116:1865-1877.
20. Erbs S, Linke A, Schachinger V, Assmus B, Thiele H, Diederich KW, Hoffmann C, Dimmeler S, Tonn T, Hambrecht R, Zeiher AM, Schuler G. 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. 2007; 116:366-374.
21. Cho HJ, Lee N, Lee JY, Choi YJ, Ii M, Wecker A, Jeong JO, Curry C, Qin G, Yoon YS. Role of host tissues for sustained humoral effects after endothelial progenitor cell transplantation into the ischemic heart. J Exp Med. 2007;204:3257-3269.
22. Segers VF, Lee RT. Stem-cell therapy for cardiac disease. Nature. 2008; 451:937-942.
23. Yoon CH, Koyanagi M, Iekushi K, Seeger F, Urbich C, Zeiher AM, Dimmeler S. Mechanism of improved cardiac function after bone marrow mononuclear cell therapy: role of cardiovascular lineage commitment. Circulation. 2010;121:2001-2011.
24. Wang J, Zhang S, Rabinovich B, Bidaut L, Soghomonyan S, Alauddin MM, Bankson JA, Shpall E, Willerson JT, Gelovani JG, Yeh ET. Human CD34+ cells in experimental myocardial infarction: long-term survival, sustained functional improvement, and mechanism of action. Circ Res. 2010;106:1904-1911.
25. Assmus B, Schachinger V, Teupe C, Britten M, Lehmann R, Dobert N, Grunwald F, Aicher A, Urbich C, Martin H, Hoelzer D, Dimmeler S, Zeiher AM. Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation. 2002;106:3009-3017.
26. Assmus B, Honold J, Schachinger V, Britten MB, Fischer-Rasokat U, Lehmann R, Teupe C, Pistorius K, Martin H, Abolmaali ND, Tonn T, Dimmeler S, Zeiher AM. Transcoronary transplantation of progenitor cells after myocardial infarction. N Engl J Med. 2006;355:1222-1232.
27. Landmesser U, Engberding N, Bahlmann FH, Schaefer A, Wiencke A, Heineke A, Spiekermann S, Hilfiker-Kleiner D, Templin C, Kotlarz D, Mueller M, Fuchs M, Hornig B, Haller H, Drexler H. 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. 2004;110:1933-1939.
28. Sorrentino SA, Bahlmann FH, Besler C, Muller M, Schulz S, Kirchhoff N, Doerries C, Horvath T, Limbourg A, Limbourg F, Fliser D, Haller H, Drexler H, Landmesser U. 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-gamma agonist rosiglitazone. Circulation. 2007;116: 163-173.
29. Giannotti G, Doerries C, Mocharla PS, Mueller MF, Bahlmann FH, Horvath T, Jiang H, Sorrentino SA, Steenken N, Manes C, Marzilli M, Rudolph KL, Luscher TF, Drexler H, Landmesser U. Impaired endothelial repair capacity of early endothelial progenitor cells in prehyper-tension: relation to endothelial dysfunction. Hypertension. 2010;55: 1389-1397.
30. Doerries C, Grote K, Hilfiker-Kleiner D, Luchtefeld M, Schaefer A, Holland SM, Sorrentino S, Manes C, Schieffer B, Drexler H, Landmesser U. Critical role of the NAD(P)H oxidase subunit p47phox for left ventricular remodeling/dysfunction and survival after myocardial infarction. Circ Res. 2007;100:894-903.
31. Sorrentino SA, Doerries C, Manes C, Speer T, Dessy C, Lobysheva I, Mohmand W, Akbar R, Bahlmann F, Besler C, Schaefer A, Hilfiker-Kleiner D, Luscher TF, Balligand JL, Drexler H, Landmesser U. Nebivolol exerts beneficial effects on endothelial function, early endothelial progenitor cells, myocardial neovascularization, and left ventricular dysfunction early after myocardial infarction beyond conventional beta1-blockade. J Am Coll Cardiol. 2011;57:601-611.
32. Iwasaki H, Kawamoto A, Ishikawa M, Oyamada A, Nakamori S, Nishimura H, Sadamoto K, Horii M, Matsumoto T, Murasawa S, Shibata T, Suehiro S, Asahara T. Dose-dependent contribution of CD34-positive cell transplantation to concurrent vasculogenesis and cardiomyogenesis for functional regenerative recovery after myocardial infarction. Circulation. 2006;113:1311-1325.
33. Tongers J, Losordo DW, Landmesser U. Stem and progenitor cell-based therapy in ischaemic heart disease: promise, uncertainties, and challenges. Eur Heart J. 2011;32:1197-1206.
34. Hirschi KK, Ingram DA, Yoder MC. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol. 2008; 28:1584-1595.
35. Deb A, Patterson C. Hard luck stories: the reality of endothelial progenitor cells continues to fall short of the promise. Circulation. 2010; 121:850-852.
36. Pearson JD. Endothelial progenitor cells: hype or hope? J Thromb Haemost. 2009;7:255-262.
37. Arras M, Ito WD, Scholz D, Winkler B, Schaper J, Schaper W. Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J Clin Invest. 1998;101:40-50.
38. Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003;9: 653-660.
39. Medina RJ, O'Neill CL, O'Doherty TM, Knott H, Guduric-Fuchs J, Gardiner TA, Stitt AW. Myeloid angiogenic cells act as alternative M2 macrophages and modulate angiogenesis through interleukin-8. Mol Med. 2011;17:1045-1055.
40. He H, Xu J, Warren CM, Duan D, Li X, Wu L, Iruela-Arispe ML. Endothelial cells provide an instructive niche for the differentiation and functional polarization of M2-like macrophages. Blood. 2012;120: 3152-3162.
41. Thum T, Galuppo P, Wolf C, Fiedler J, Kneitz S, van Laake LW, Doevendans PA, Mummery CL, Borlak J, Haverich A, Gross C, Engelhardt S, Ertl G, Bauersachs J. MicroRNAs in the human heart: a clue to fetal gene reprogramming in heart failure. Circulation. 2007;116: 258-267.
42. Naga Prasad SV, Duan ZH, Gupta MK, Surampudi VS, Volinia S, Calin GA, Liu CG, Kotwal A, Moravec CS, Starling RC, Perez DM, Sen S, Wu Q, Plow EF, Croce CM, Karnik S. Unique microRNA profile in end-stage heart failure indicates alterations in specific cardiovascular signaling networks. J Biol Chem. 2009;284:27487-27499.
43. Tijsen AJ, Creemers EE, Moerland PD, de Windt LJ, van der Wal AC, Kok WE, Pinto YM. MiR423-5p as a circulating biomarker for heart failure. Circ Res. 2010;106:1035-1039.
44. Lancrin C, Sroczynska P, Stephenson C, Allen T, Kouskoff V, Lacaud G. The haemangioblast generates haematopoietic cells through a hae-mogenic endothelium stage. Nature. 2009;457:892-895.
45. Yoder MC. Defining human endothelial progenitor cells. J Thromb Haemost. 2009;7(suppl 1):49-52.
46. Taniguchi K, Kohno R, Ayada T, Kato R, Ichiyama K, Morisada T, Oike Y, Yonemitsu Y, Maehara Y, Yoshimura A. Spreds are essential for embryonic lymphangiogenesis by regulating vascular endothelial growth factor receptor 3 signaling. Mol Cell Biol. 2007;27:4541-4550.
47. Rhoads K, Arderiu G, Charboneau A, Hansen SL, Hoffman W, Boudreau N. A role for Hox A5 in regulating angiogenesis and vascular patterning. Lymphat Res Biol. 2005;3:240-252.
48. Sahoo S, Klychko E, Thorne T, Misener S, Schultz KM, Millay M, Ito A, Liu T, Kamide C, Agrawal H, Perlman H, Qin G, Kishore R, Losordo DW. Exosomes from human CD34(+) stem cells mediate their proan-giogenic paracrine activity. Circ Res. 2011;109:724-728.
49. Wakioka T, Sasaki A, Kato R, Shouda T, Matsumoto A, Miyoshi K, Tsuneoka M, Komiya S, Baron R, Yoshimura A. Spred is a Sprouty-related suppressor of Ras signalling. Nature. 2001;412:647-651.
50. Pages G, Milanini J, Richard DE, Berra E, Gothie E, Vinals F, Pouyssegur J. Signaling angiogenesis via p42/p44 MAP kinase cascade. Ann N Y Acad Sci. 2000;902:187-200.
51. Fleissner F, Jazbutyte V, Fiedler J, Gupta SK, Yin X, Xu Q, Galuppo P, Kneitz S, Mayr M, Ertl G, Bauersachs J, Thum T. Short communication: asymmetric dimethylarginine impairs angiogenic progenitor cell function in patients with coronary artery disease through a microRNA-21-dependent mechanism. Circ Res. 2010;107:138-143.
52. Zernecke A, Bidzhekov K, Noels H, Shagdarsuren E, Gan L, Denecke B, Hristov M, Koppel T, Jahantigh MN, Lutgens E, Wang S, Olson EN, Schober A, Weber C. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal. 2009;2:ra81.