Histone deacetylase 9 promotes angiogenesis by targeting the antiangiogenic MicroRNA-17-92 cluster in endothelial cells

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 3, 2013, Pages 533-543

  Kaluza, David ^a   Kroll, Jens ^b,c   Gesierich, Sabine ^b   Manavski, Yosif ^a   Boeckel, Jes Niels ^a   Doebele, Carmen ^a   Zelent, Arthur ^d   Rössig, Lothar ^a   Zeiher, Andreas M ^a   Augustin, Hellmut G ^b,c   Urbich, Carmen ^a   Dimmeler, Stefanie ^a  

^a GOETHE UNIVERSITY   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

angiogenesis; histone deacetylase 9 and histone deacetylase 5; histone deacetylases; microRNAs; miR 17

Indexed keywords

HISTONE DEACETYLASE; HISTONE DEACETYLASE 9; MATRIGEL; MICRORNA; MICRORNA 17-92; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD FLOW; BLOOD VESSEL; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; HINDLIMB; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIMB ISCHEMIA; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA BLOOD VESSEL; SUMOYLATION; ZEBRA FISH;

ANIMALS; DISEASE MODELS, ANIMAL; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HINDLIMB; HISTONE DEACETYLASES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; ISCHEMIA; MICE; MICE, KNOCKOUT; MICRORNAS; MUSCLE, SKELETAL; MUTATION; NEOVASCULARIZATION, PHYSIOLOGIC; REGIONAL BLOOD FLOW; REPRESSOR PROTEINS; RETINAL NEOVASCULARIZATION; RNA INTERFERENCE; TRANSFECTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84874380158     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.300415     Document Type: Article

References (44)

1. Johnson CA, Turner BM. Histone deacetylases: complex transducers of nuclear signals. Semin Cell Dev Biol. 1999;10:179-188.
2. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M. Lysine acetylation targets protein complexes and coregulates major cellular functions. Science. 2009;325:834-840.
3. Kim MS, Kwon HJ, Lee YM, Baek JH, Jang JE, Lee SW, Moon EJ, Kim HS, Lee SK, Chung HY, Kim CW, Kim KW. Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes. Nat Med. 2001;7:437-443.
4. Rössig L, Li H, Fisslthaler B, Urbich C, Fleming I, Förstermann U, Zeiher AM, Dimmeler S. Inhibitors of histone deacetylation downregulate the expression of endothelial nitric oxide synthase and compromise endothelial cell function in vasorelaxation and angiogenesis. Circ Res. 2002;91:837-844.
5. Qian DZ, Kato Y, Shabbeer S, Wei Y, Verheul HM, Salumbides B, Sanni T, Atadja P, Pili R. Targeting tumor angiogenesis with histone deacetylase inhibitors: the hydroxamic acid derivative LBH589. Clin Cancer Res. 2006;12:634-642.
6. Carew JS, Giles FJ, Nawrocki ST. Histone deacetylase inhibitors: mechanisms of cell death and promise in combination cancer therapy. Cancer Lett. 2008;269:7-17.
7. Mottet D, Castronovo V. Histone deacetylases: anti-angiogenic targets in cancer therapy. Curr Cancer Drug Targets. 2010;10:898-913.
8. Kaluza D, Kroll J, Gesierich S, Yao TP, Boon RA, Hergenreider E, Tjwa M, Rössig L, Seto E, Augustin HG, Zeiher AM, Dimmeler S, Urbich C. Class IIb HDAC6 regulates endothelial cell migration and angiogenesis by deacetylation of cortactin. EMBO J. 2011;30:4142-4156.
9. Chang S, Young BD, Li S, Qi X, Richardson JA, Olson EN. Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase Cell. 2006;126:321-334.
10. Mottet D, Bellahcène A, Pirotte S, Waltregny D, Deroanne C, Lamour V, Lidereau R, Castronovo V. Histone deacetylase 7 silencing alters endothelial cell migration, a key step in angiogenesis. Circ Res. 2007;101:1237-1246.
11. Martin M, Potente M, Janssens V, Vertommen D, Twizere JC, Rider MH, Goris J, Dimmeler S, Kettmann R, Dequiedt F. Protein phosphatase 2A controls the activity of histone deacetylase 7 during T cell apoptosis and angiogenesis. Proc Natl Acad Sci USA. 2008;105:4727-4732.
12. Margariti A, Zampetaki A, Xiao Q, Zhou B, Karamariti E, Martin D, Yin X, Mayr M, Li H, Zhang Z, De Falco E, Hu Y, Cockerill G, Xu Q, Zeng L. Histone deacetylase 7 controls endothelial cell growth through modulation of beta-catenin. Circ Res. 2010;106:1202-1211.
13. Urbich C, Rössig L, Kaluza D, Potente M, Boeckel JN, Knau A, Diehl F, Geng JG, Hofmann WK, Zeiher AM, Dimmeler S. HDAC5 is a repressor of angiogenesis and determines the angiogenic gene expression pattern of endothelial cells. Blood. 2009;113:5669-5679.
14. Ha CH, Wang W, Jhun BS, Wong C, Hausser A, Pfizenmaier K, McKinsey TA, Olson EN, Jin ZG. Protein kinase D-dependent phosphorylation and nuclear export of histone deacetylase 5 mediates vascular endothelial growth factor-induced gene expression and angiogenesis. J Biol Chem. 2008;283:14590-14599.
15. Chang S, McKinsey TA, Zhang CL, Richardson JA, Hill JA, Olson EN. Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol Cell Biol. 2004;24:8467-8476.
16. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol. 2009;10:126-139.
17. Thum T. MicroRNA therapeutics in cardiovascular medicine. EMBO Mol Med. 2012;4:3-14.
18. 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.
19. Suárez Y, Fernández-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.
20. Bonauer A, Boon RA, Dimmeler S. Vascular microRNAs. Curr Drug Targets. 2010;11:943-949.
21. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, Jacks T. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell. 2008;132:875-886.
22. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT, Thomas-Tikhonenko A. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet. 2006;38:1060-1065.
23. 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 antiangiogenic function in endothelial cells. Blood. 2010;115:4944-4950.
24. Shan SW, Lee DY, Deng Z, Shatseva T, Jeyapalan Z, Du WW, Zhang Y, Xuan JW, Yee SP, Siragam V, Yang BB. MicroRNA MiR-17 retards tissue growth and represses fibronectin expression. Nat Cell Biol. 2009;11:1031-1038.
25. Bonauer A, Carmona G, Iwasaki M, et al. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science. 2009;324:1710-1713.
26. Bonauer A, Dimmeler S. The microRNA-17-92 cluster: still a miRacle? Cell Cycle. 2009;8:3866-3873.
27. Pospisil V, Vargova K, Kokavec J, Rybarova J, Savvulidi F, Jonasova A, Necas E, Zavadil J, Laslo P, Stopka T. Epigenetic silencing of the oncogenic miR-17-92 cluster during PU.1-directed macrophage differentiation. EMBO J. 2011;30:4450-4464.
28. Scott GK, Mattie MD, Berger CE, Benz SC, Benz CC. Rapid alteration of microRNA levels by histone deacetylase inhibition. Cancer Res. 2006;66:1277-1281.
29. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature. 2001;411:494-498.
30. Petrie K, Guidez F, Howell L, Healy L, Waxman S, Greaves M, Zelent A. The histone deacetylase 9 gene encodes multiple protein isoforms. J Biol Chem. 2003;278:16059-16072.
31. Ji M, Rao E, Ramachandrareddy H, Shen Y, Jiang C, Chen J, Hu Y, Rizzino A, Chan WC, Fu K, McKeithan TW. The miR-17-92 microRNA cluster is regulated by multiple mechanisms in B-cell malignancies. Am J Pathol. 2011;179:1645-1656.
32. Diehl F, Rössig L, Zeiher AM, Dimmeler S, Urbich C. The histone methyltransferase MLL is an upstream regulator of endothelial-cell sprout formation. Blood. 2007;109:1472-1478.
33. Carmona G, Göttig S, Orlandi A, Scheele J, Bäuerle T, Jugold M, Kiessling F, Henschler R, Zeiher AM, Dimmeler S, Chavakis E. Role of the small GTPase Rap1 for integrin activity regulation in endothelial cells and angiogenesis. Blood. 2009;113:488-497.
34. Zhang CL, McKinsey TA, Chang S, Antos CL, Hill JA, Olson EN. Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell. 2002;110:479-488.
35. Rössig L, Urbich C, Brühl T, et al. Histone deacetylase activity is essential for the expression of HoxA9 and for endothelial commitment of progenitor cells. J Exp Med. 2005;201:1825-1835.
36. Guarani V, Deflorian G, Franco CA, et al. Acetylation-dependent regulation of endothelial Notch signalling by the SIRT1 deacetylase. Nature. 2011;473:234-238.
37. Alajati A, Laib AM, Weber H, Boos AM, Bartol A, Ikenberg K, Korff T, Zentgraf H, Obodozie C, Graeser R, Christian S, Finkenzeller G, Stark GB, Héroult M, Augustin HG. Spheroid-based engineering of a human vasculature in mice. Nat Methods. 2008;5:439-445.
38. Laib AM, Bartol A, Alajati A, Korff T, Weber H, Augustin HG. Spheroidbased human endothelial cell microvessel formation in vivo. Nat Protoc. 2009;4:1202-1215.
39. Lawson ND, Vogel AM, Weinstein BM. Sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev Cell. 2002;3:127-136.
40. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn. 1995;203:253-310.
41. Epting D, Wendik B, Bennewitz K, Dietz CT, Driever W, Kroll J. The Rac1 regulator ELMO1 controls vascular morphogenesis in zebrafish. Circ Res. 2010;107:45-55.
42. van Rooij E, Fielitz J, Sutherland LB, Thijssen VL, Crijns HJ, Dimaio MJ, Shelton J, De Windt LJ, Hill JA, Olson EN. Myocyte enhancer factor 2 and class II histone deacetylases control a gender-specific pathway of cardioprotection mediated by the estrogen receptor. Circ Res. 2010;106:155-165.
43. Zhou X, Richon VM, Rifkind RA, Marks PA. Identification of a transcriptional repressor related to the noncatalytic domain of histone deacetylases 4 and 5. Proc Natl Acad Sci USA. 2000;97:1056-1061.
44. Humphreys KJ, Cobiac L, Le Leu RK, Van der Hoek MB, Michael MZ. Histone deacetylase inhibition in colorectal cancer cells reveals competing roles for members of the oncogenic miR-17-92 cluster. Mol Carcinog. 2012