NO points to epigenetics in vascular development

Cardiovascular Research

Volumn 90, Issue 3, 2011, Pages 447-456

  Illi, Barbara ^a   Colussi, Claudia ^b   Rosati, Jessica ^c   Spallotta, Francesco ^b   Nanni, Simona ^d   Farsetti, Antonella ^e   Capogrossi, Maurizio C ^c   Gaetano, Carlo ^c  

^a CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^b CENTRO CARDIOLOGICO MONZINO   (Italy)

^c LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^d CATHOLIC UNIVERSITY   (Italy)

^e CNR   (Italy)

Author keywords

Epigenetics; Nitric oxide; Vascular development

Indexed keywords

DNA; NITRIC OXIDE;

ACETYLATION; ARTICLE; DNA METHYLATION; DNA MODIFICATION; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; EPIGENETICS; HEART DEVELOPMENT; HISTONE MODIFICATION; HUMAN; MESODERM; METHYLATION; PRIORITY JOURNAL; SUMOYLATION; UBIQUITINATION;

ANIMALS; BLOOD VESSELS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; HUMANS; MESODERM; MODELS, CARDIOVASCULAR; MODELS, GENETIC; NITRIC OXIDE; SIGNAL TRANSDUCTION;

EID: 79957474768     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvr056     Document Type: Article

References (147)

1. Jacklet JW. Nitric oxide signaling in invertebrates. Invert Neurosci 1997;3:1-14. (Pubitemid 28379834)
2. Wilson ID, Neill SJ, Hancock JT. Nitric oxide synthesis and signalling in plants. Plant Cell Environ 2008;31:622-631. (Pubitemid 351503408)
3. Ridnour LA, Thomas DD, Mancardi D, Espey MG, Miranda KM, Paolocci N et al. The chemistry of nitrosative stress induced by nitric oxide and reactive nitrogen oxide species. Putting perspective on stressful biological situations. Biol Chem 2004;385: 1-10. (Pubitemid 38240288)
4. Hayashi T, Yano K, Matsui-Hirai H, Yokoo H, Hattori Y, Iguchi A. Nitric oxide and endothelial cellular senescence. Pharmacol Ther 2008;120:333-339.
5. Spinetti G, Kraenkel N, Emanueli C, Madeddu P. Diabetes and vessel wall remodelling: From mechanistic insights to regenerative therapies. Cardiovascular Research 2008;78:265-273. (Pubitemid 351556106)
6. Tsutsui M, Shimokawa H, Morishita T, Nakashima Y, Yanagihara N. Development of genetically engineered mice lacking all three nitric oxide synthases. J Pharmacol Sci 2006;102:147-154. (Pubitemid 44690971)
7. Braam B, de Roos R, Dijk A, Boer P, Post JA, Kemmeren PP et al. Nitric oxide donor induces temporal and dose-dependent reduction of gene expression in human endothelial cells. Am J Physiol 2004;287:H1977-H1986. (Pubitemid 39430733)
8. Illi B, Dello Russo C, Colussi C, Rosati J, Pallaoro M, Spallotta F et al. Nitric oxide modulates chromatin folding in human endothelial cells via protein phosphatase 2A activation and class II histone deacetylases nuclear shuttling. Circ Res 2008;102: 51-58.
9. Riccio A, Alvania RS, Lonze BE, Ramanan N, Kim T, Huang Y et al. A nitric oxide signaling pathway controls CREB-mediated gene expression in neurons. Mol Cell 2006;21:283-294. (Pubitemid 43099943)
10. Lichten LA, Liuzzi JP, Cousins RJ. Interleukin-1beta contributes via nitric oxide to the upregulation and functional activity of the zinc transporter Zip14 (Slc39a14) in murine hepatocytes. Am J Physiol Gastrointest Liver Physiol 2009;296:G860-G867.
11. Krause B, Sobrevia L, Casanello P. Epigenetics: New concepts of old phenomena in vascular physiology. Curr Vasc Pharmacol 2009;7:513-520.
12. Aguilera O, Fernandez AF, Munoz A, Fraga MF. Epigenetics and environment: A complex relationship. J Appl Physiol 2010;109:243-251.
13. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science (New York, NY) 2009;325:834-840.
14. Roloff TC, Nuber UA. Chromatin, epigenetics and stem cells. Eur J Cell Biol 2005;84: 123-135. (Pubitemid 40353057)
15. Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A. An operational definition of epigenetics. Genes Dev 2009;23:781-783.
16. Jenuwein T, Allis CD. Translating the histone code. Science (New York, NY) 2001;293: 1074-1080. (Pubitemid 32758077)
17. Prokhortchouk E, Defossez PA. The cell biology of DNA methylation in mammals. Biochim Biophys Acta 2008;1783:2167-2173.
18. Illi B, Colussi C, Grasselli A, Farsetti A, Capogrossi MC, Gaetano C. NO sparks off chromatin: Tales of a multifaceted epigenetic regulator. Pharmacol Ther 2009;123: 344-352.
19. Schotta G, Ebert A, Krauss V, Fischer A, Hoffmann J, Rea S et al. Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J 2002;21:1121-1131. (Pubitemid 34206185)
20. Stabell M, Eskeland R, Bjorkmo M, Larsson J, Aalen RB, Imhof A et al. The Drosophila G9a gene encodes a multi-catalytic histone methyltransferase required for normal development. Nucleic Acids Res 2006;34:4609-4621. (Pubitemid 44574154)
21. Cao R, Zhang Y. The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 2004;14:155-164. (Pubitemid 38520143)
22. Grewal SI, Jia S. Heterochromatin revisited. Nat Rev 2007;8:35-46. (Pubitemid 46006048)
23. Yang XJ, Seto E. HATs and HDACs: From structure, function and regulation to novel strategies for therapy and prevention. Oncogene 2007;26:5310-5318. (Pubitemid 47255917)
24. Zhang HM, Li L, Papadopoulou N, Hodgson G, Evans E, Galbraith M et al. Mitogeninduced recruitment of ERK and MSK to SRE promoter complexes by ternary complex factor Elk-1. Nucleic Acids Res 2008;36:2594-2607. (Pubitemid 351659574)
25. Sassone-Corsi P, Mizzen CA, Cheung P, Crosio C, Monaco L, Jacquot S et al. Requirement of Rsk-2 for epidermal growth factor-activated phosphorylation of histone H3. Science (New York, NY) 1999;285:886-891. (Pubitemid 29381988)
26. Peterson CL, Laniel MA. Histones and histone modifications. Curr Biol 2004;14: R546-R551.
27. Durr H, Korner C, Muller M, Hickmann V, Hopfner KP. X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 2005; 121:363-373. (Pubitemid 40692297)
28. Boeger H, Griesenbeck J, Strattan JS, Kornberg RD. Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Mol Cell 2004;14:667-673. (Pubitemid 38739088)
29. Yang X, Zaurin R, Beato M, Peterson CL. Swi3p controls SWI/SNF assembly and ATP-dependent H2A-H2B displacement. Nat Struct Mol Biol 2007;14:540-547. (Pubitemid 46871803)
30. Mizuguchi G, Shen X, Landry J, Wu WH, Sen S, Wu C. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science (New York, NY) 2004;303:343-348. (Pubitemid 38095768)
31. Kornberg RD, Lorch Y. Chromatin-modifying and -remodeling complexes. Curr Opin Genet Dev 1999;9:148-151. (Pubitemid 29158547)
32. Janowski BA, Huffman KE, Schwartz JC, Ram R, Hardy D, Shames DS et al. Inhibiting gene expression at transcription start sites in chromosomal DNA with antigene RNAs. Nat Chem Biol 2005;1:216-222.
33. Omi K, Hachiya NS, Tokunaga K, Kaneko K. siRNA-mediated inhibition of endogenous Huntington disease gene expression induces an aberrant configuration of the ER network in vitro. Biochem Biophys Res Commun 2005;338:1229-1235. (Pubitemid 41597768)
34. Zhang MX, Ou H, Shen YH, Wang J, Wang J, Coselli J et al. Regulation of endothelial nitric oxide synthase by small RNA. Proc Natl Acad Sci USA 2005;102:16967-16972. (Pubitemid 41692667)
35. Hawkins PG, Santoso S, Adams C, Anest V, Morris KV. Promoter targeted small RNAs induce long-term transcriptional gene silencing in human cells. Nucleic Acids Res 2009;37:2984-2995.
36. Malecova B, Morris KV. Transcriptional gene silencing through epigenetic changes mediated by non-coding RNAs. Curr Opin Mol Ther 2010;12:214-222.
37. Osorio FG, Varela I, Lara E, Puente XS, Espada J, Santoro R et al. Nuclear envelope alterations generate an aging-like epigenetic pattern in mice deficient in Zmpste24 metalloprotease. Aging Cell 2010;9:947-957.
38. Kee HJ, Kook H. Roles and targets of class I and IIa histone deacetylases in cardiac hypertrophy. J Biomed Biotechnol 2011;928326.
39. Morimoto T, Sunagawa Y, Fujita M, Hasegawa K. Novel heart failure therapy targeting transcriptional pathway in cardiomyocytes by a natural compound, curcumin. Circ J 2010;74:1059-1066.
40. Ribatti D. The discovery of endothelial progenitor cells. An historical review. Leuk Res 2007;31:439-444. (Pubitemid 46198947)
41. Fujimoto T, Ogawa M, Minegishi N, Yoshida H, Yokomizo T, Yamamoto M et al. Step-wise divergence of primitive and definitive haematopoietic and endothelial cell lineages during embryonic stem cell differentiation. Genes Cells 2001;6: 1113-1127. (Pubitemid 33133699)
42. Risau W. Development and differentiation of endothelium. Kidney Int 1998;67: S3-S6. (Pubitemid 28405671)
43. Yurugi-Kobayashi T, Itoh H, Yamashita J, Yamahara K, Hirai H, Kobayashi T et al. Effective contribution of transplanted vascular progenitor cells derived from embryonic stem cells to adult neovascularization in proper differentiation stage. Blood 2003;101:2675-2678. (Pubitemid 36857629)
44. Hirashima M, Kataoka H, Nishikawa S, Matsuyoshi N, Nishikawa S. Maturation of embryonic stem cells into endothelial cells in an in vitro model of vasculogenesis. Blood 1999;93:1253-1263. (Pubitemid 29076140)
45. Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol 1995;11:73-91. (Pubitemid 26019602)
46. Lindsley RC, Gill JG, Kyba M, Murphy TL, Murphy KM. Canonical Wnt signaling is required for development of embryonic stem cell-derived mesoderm. Development (Cambridge, England) 2006;133:3787-3796. (Pubitemid 44650957)
47. Narazaki G, Uosaki H, Teranishi M, Okita K, Kim B, Matsuoka S et al. Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation 2008;118:498-506.
48. Swift MR, Weinstein BM. Arterial-venous specification during development. Circ Res 2009;104:576-588.
49. Willey S, Ayuso-Sacido A, Zhang H, Fraser ST, Sahr KE, Adlam MJ et al. Acceleration of mesoderm development and expansion of hematopoietic progenitors in differentiating ES cells by the mouse Mix-like homeodomain transcription factor. Blood 2006; 107:3122-3130.
50. Goldberg Cohen I, Beck G, Ziskind A, Itskovitz-Eldor J. Human embryonic stem cells for vascular development and repair. Isr Med Assoc J 2006;8:573-578. (Pubitemid 44612825)
51. Iacobas I, Vats A, Hirschi KK. Vascular potential of human pluripotent stem cells. Arterioscler Thromb Vasc Biol 2010;30:1110-1117.
52. Desbaillets I, Ziegler U, Groscurth P, Gassmann M. Embryoid bodies: An in vitro model of mouse embryogenesis. Exp Physiol 2000;85:645-651.
53. Illi B, Scopece A, Nanni S, Farsetti A, Morgante L, Biglioli P et al. Epigenetic histone modification and cardiovascular lineage programming in mouse embryonic stem cells exposed to laminar shear stress. Circ Res 2005;96:501-508. (Pubitemid 40463458)
54. Lee JH, Hart SR, Skalnik DG. Histone deacetylase activity is required for embryonic stem cell differentiation. Genesis 2004;38:32-38. (Pubitemid 38197607)
55. Szutorisz H, Dillon N. The epigenetic basis for embryonic stem cell pluripotency. Bioessays 2005;27:1286-1293. (Pubitemid 43076172)
56. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006;125:315-326.
57. Meshorer E, Misteli T. Chromatin in pluripotent embryonic stem cells and differentiation. Nat Rev 2006;7:540-546. (Pubitemid 44036459)
58. Keenen B, de la Serna IL. Chromatin remodeling in embryonic stem cells: Regulating the balance between pluripotency and differentiation. J Cell Physiol 2009;219:1-7.
59. Bloushtain-Qimron N, Yao J, Shipitsin M, Maruyama R, Polyak K. Epigenetic patterns of embryonic and adult stem cells. Cell Cycle (Georgetown, Tex) 2009;8:809-817.
60. Pan G, Tian S, Nie J, Yang C, Ruotti V, Wei H et al. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 2007;1:299-312. (Pubitemid 47355329)
61. Zhao XD, Han X, Chew JL, Liu J, Chiu KP, Choo A et al. Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 2007;1:286-298. (Pubitemid 47370914)
62. Schulz WA, Hoffmann MJ. Transcription factor networks in embryonic stem cells and testicular cancer and the definition of epigenetics. Epigenetics 2007;2:37-42. (Pubitemid 46824848)
63. Spallotta F, Rosati J, Straino S, Nanni S, Grasselli A, Ambrosino V et al. Nitric oxide determines mesodermic differentiation of mouse embryonic stem cells by activating class IIa histone deacetylases: Potential therapeutic implications in a mouse model of hindlimb ischemia. Stem Cells (Dayton, Ohio) 2010;28:431-442.
64. Liang J, Wan M, Zhang Y, Gu P, Xin H, Jung SY et al. Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat Cell Biol 2008;10:731-739. (Pubitemid 351772939)
65. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006;441:349-353. (Pubitemid 44050199)
66. Jorgensen HF, Giadrossi S, Casanova M, Endoh M, Koseki H, Brockdorff N et al. Stem cells primed for action: Polycomb repressive complexes restrain the expression of lineage-specific regulators in embryonic stem cells. Cell Cycle (Georgetown, Tex) 2006;5:1411-1414. (Pubitemid 44153649)
67. Zhong X, Jin Y. Critical roles of coactivator p300 in mouse embryonic stem cell differentiation and Nanog expression. J Biol Chem 2009;284:9168-9175.
68. Illi B, Puri P, Morgante L, Capogrossi MC, Gaetano C. Nuclear factor-kappaB and cAMP response element binding protein mediate opposite transcriptional effects on the Flk-1/KDR gene promoter. Circ Res 2000;86:E110-E117.
69. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010;466:1129-1133.
70. Bibikova M, Laurent LC, Ren B, Loring JF, Fan JB. Unraveling epigenetic regulation in embryonic stem cells. Cell Stem Cell 2008;2:123-134. (Pubitemid 351168715)
71. Hemberger M. Genetic-epigenetic intersection in trophoblast differentiation: Implications for extraembryonic tissue function. Epigenetics 2010;5:24-29.
72. Loh YH, Zhang W, Chen X, George J, Ng HH. Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev 2007;21: 2545-2557. (Pubitemid 47607666)
73. Rossig L, Urbich C, Bruhl T, Dernbach E, Heeschen C, Chavakis E 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. (Pubitemid 41002901)
74. Dutta D, Ray S, Vivian JL, Paul S. Activation of the VEGFR1 chromatin domain: An angiogenic signal-ETS1/HIF-2alpha regulatory axis. J Biol Chem 2008;283: 25404-25413.
75. Hemberger M, Dean W, Reik W. Epigenetic dynamics of stem cells and cell lineage commitment: Digging Waddington's canal. Nat Rev 2009;10:526-537.
76. Smith J. Brachyury and the T-box genes. Curr Opin Genet Dev 1997;7:474-480. (Pubitemid 27404277)
77. Showell C, Binder O, Conlon FL. T-box genes in early embryogenesis. Dev Dyn 2004; 229:201-218. (Pubitemid 38036834)
78. Patient RK, McGhee JD. The GATA family (vertebrates and invertebrates). Curr Opin Genet Dev 2002;12:416-422. (Pubitemid 34722920)
79. Wardle FC, Papaioannou VE. Teasing out T-box targets in early mesoderm. Curr Opin Genet Dev 2008;18:418-425. (Pubitemid 50310296)
80. Izumi N, Era T, Akimaru H, Yasunaga M, Nishikawa S. Dissecting the molecular hierarchy for mesendoderm differentiation through a combination of embryonic stem cell culture and RNA interference. Stem Cells (Dayton, Ohio) 2007;25:1664-1674. (Pubitemid 47121843)
81. Cheong CY, Lufkin T. Transcriptional repression in ES cells. J Cell Biochem 2010;110: 288-293.
82. Gan Q, Yoshida T, McDonald OG, Owens GK. Concise review: Epigenetic mechanisms contribute to pluripotency and cell lineage determination of embryonic stem cells. Stem Cells (Dayton, Ohio) 2007;25:2-9. (Pubitemid 46052969)
83. Pietersen AM, van Lohuizen M. Stem cell regulation by polycomb repressors: Postponing commitment. Curr Opin Cell Biol 2008;20:201-207.
84. Shafa M, Krawetz R, Rancourt DE. Returning to the stem state: Epigenetics of recapitulating pre-differentiation chromatin structure. Bioessays 2010;32:791-799.
85. Hirabayashi Y, Gotoh Y. Epigenetic control of neural precursor cell fate during development. Nat Rev Neurosci 2010;11:377-388.
86. Zeineddine D, Papadimou E, Chebli K, Gineste M, Liu J, Grey C et al. Oct-3/4 dose dependently regulates specification of embryonic stem cells toward a cardiac lineage and early heart development. Dev Cell 2006;11:535-546. (Pubitemid 44430895)
87. de la Cruz CC, Fang J, Plath K, Worringer KA, Nusinow DA, Zhang Y et al. Developmental regulation of Suz 12 localization. Chromosoma 2005;114:183-192.
88. Klose RJ, Kallin EM, Zhang Y. JmjC-domain-containing proteins and histone demethylation. Nat Rev 2006;7:715-727. (Pubitemid 44260007)
89. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004;119:941-953. (Pubitemid 40037608)
90. Tenney K, Shilatifard A. A COMPASS in the voyage of defining the role of trithorax/ MLL-containing complexes: Linking leukemogensis to covalent modifications of chromatin. J Cell Biochem 2005;95:429-436. (Pubitemid 41420173)
91. Monzen K, Ito Y, Naito AT, Kasai H, Hiroi Y, Hayashi D et al. A crucial role of a high mobility group protein HMGA2 in cardiogenesis. Nat Cell Biol 2008;10:567-574. (Pubitemid 351627376)
92. Lakowski B, Roelens I, Jacob S. CoREST-like complexes regulate chromatin modification and neuronal gene expression. J Mol Neurosci 2006;29:227-239.
93. Kashyap V, Rezende NC, Scotland KB, Shaffer SM, Persson JL, Gudas LJ et al. Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev 2009; 18:1093-1108.
94. Baron M. Induction of embryonic hematopoietic and endothelial stem/progenitor cells by hedgehog-mediated signals. Differentiation 2001;68:175-185. (Pubitemid 33754990)
95. Cohen ED, Tian Y, Morrisey EE. Wnt signaling: An essential regulator of cardiovascular differentiation, morphogenesis and progenitor self-renewal. Development (Cambridge, England) 2008;135:789-798. (Pubitemid 351524132)
96. Ferguson JE III, Kelley RW, Patterson C. Mechanisms of endothelial differentiation in embryonic vasculogenesis. Arterioscler Thromb Vasc Biol 2005;25:2246-2254. (Pubitemid 41552639)
97. Yamashita JK. Differentiation and diversification of vascular cells from embryonic stem cells. Int J Hematol 2004;80:1-6. (Pubitemid 38937869)
98. Zorn AM, Wells JM. Molecular basis of vertebrate endoderm development. Int Rev Cytol 2007;259:49-111. (Pubitemid 46529407)
99. Shivdasani RA. Molecular regulation of vertebrate early endoderm development. Dev Biol 2002;249:191-203.
100. Jin SW, Patterson C. The opening act: Vasculogenesis and the origins of circulation. Arterioscler Thromb Vasc Biol 2009;29:623-629.
101. Li M, Marin-Muller C, Bharadwaj U, Chow KH, Yao Q, Chen C. MicroRNAs: Control and loss of control in human physiology and disease. World J Surg 2009;33:667-684.
102. Wang Y, Baskerville S, Shenoy A, Babiarz JE, Baehner L, Blelloch R. Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat Genet 2008;40:1478-1483.
103. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008;134:521-533.
104. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G. A common precursor for hematopoietic and endothelial cells. Development (Cambridge, England) 1998; 125:725-732. (Pubitemid 28108096)
105. Vodyanik MA, Bork JA, Thomson JA, Slukvin II. Human embryonic stem cell-derived CD34+ cells: Efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood 2005;105:617-626. (Pubitemid 40070744)
106. Kattman SJ, Huber TL, Keller GM. Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev Cell 2006;11:723-732. (Pubitemid 44644969)
107. Ben-Shoshan J, Maysel-Auslender S, Luboshits G, Barshack I, Polak-Charcon S, Tzahor E et al. Hypoxia-inducible factor-1alpha and -2alpha additively promote endothelial vasculogenic properties. J Vasc Res 2009;46:299-310.
108. Ohneda O, Nagano M, Fujii-Kuriyama Y. Role of hypoxia-inducible factor-2alpha in endothelial development and hematopoiesis. Methods Enzymol 2007;435:199-218.
109. Hanze J, Weissmann N, Grimminger F, Seeger W, Rose F. Cellular and molecular mechanisms of hypoxia-inducible factor driven vascular remodeling. Thromb Haemost 2007;97:774-787. (Pubitemid 46779962)
110. Ramirez-Bergeron DL, Runge A, Adelman DM, Gohil M, Simon MC. HIF-dependent hematopoietic factors regulate the development of the embryonic vasculature. Dev Cell 2006;11:81-92. (Pubitemid 43960804)
111. Hosseinkhani M, Hasegawa K, Ono K, Kawamura T, Takaya T, Morimoto T et al. Trichostatin A induces myocardial differentiation of monkey ES cells. Biochem Biophys Res Commun 2007;356:386-391. (Pubitemid 46452558)
112. Bendinelli P, Matteucci E, Maroni P, Desiderio MA. NF-kappaB activation, dependent on acetylation/deacetylation, contributes to HIF-1 activity and migration of bone metastatic breast carcinoma cells. Mol Cancer Res 2009;7:1328-1341.
113. Maltepe E, Krampitz GW, Okazaki KM, Red-Horse K, Mak W, Simon MC et al. Hypoxia-inducible factor-dependent histone deacetylase activity determines stem cell fate in the placenta. Development (Cambridge, England) 2005;132:3393-3403. (Pubitemid 41246115)
114. Mottet D, Bellahcene A, Pirotte S, Waltregny D, Deroanne C, Lamour V et al. Histone deacetylase 7 silencing alters endothelial cell migration, a key step in angiogenesis. Circ Res 2007;101:1237-1246. (Pubitemid 350294640)
115. Margariti A, Zampetaki A, Xiao Q, Zhou B, Karamariti E, Martin D et al. Histone deacetylase 7 controls endothelial cell growth through modulation of beta-catenin. Circ Res 2010;106:1202-1211.
116. Margariti A, Xiao Q, Zampetaki A, Zhang Z, Li H, Martin D et al. Splicing of HDAC7 modulates the SRF-myocardin complex during stem-cell differentiation towards smooth muscle cells. J Cell Sci 2009;122:460-470.
117. Illi B, Nanni S, Scopece A, Farsetti A, Biglioli P, Capogrossi MC et al. Shear stressmediated chromatin remodeling provides molecular basis for flow-dependent regulation of gene expression. Circ Res 2003;93:155-161. (Pubitemid 36919703)
118. McDonald OG, Owens GK. Programming smooth muscle plasticity with chromatin dynamics. Circ Res 2007;100:1428-1441. (Pubitemid 46834755)
119. Zhou J, Zhang M, Fang H, El-Mounayri O, Rodenberg JM, Imbalzano AN et al. The SWI/SNF chromatin remodeling complex regulates myocardin-induced smooth muscle-specific gene expression. Arterioscler Thromb Vasc Biol 2009;29:921-928.
120. Owens GK. Molecular control of vascular smooth muscle cell differentiation and phenotypic plasticity. Novartis Found Symp 2007;283:174-191.
121. Qiu P, Li L. Histone acetylation and recruitment of serum responsive factor and CREB-binding protein onto SM22 promoter during SM22 gene expression. Circ Res 2002;90:858-865. (Pubitemid 34633877)
122. McDonald OG,Wamhoff BR, Hoofnagle MH, Owens GK. Control of SRF binding to CArG box chromatin regulates smooth muscle gene expression in vivo. J Clin Invest 2006;116:36-48. (Pubitemid 43121789)
123. Jiang Y, Stojilkovic SS. Molecular cloning and characterization of alpha1-soluble guanylyl cyclase gene promoter in rat pituitary cells. J Mol Endocrinol 2006;37:503-515. (Pubitemid 46085175)
124. Chan Y, Fish JE, D'Abreo C, Lin S, Robb GB, Teichert AM et al. The cell-specific expression of endothelial nitric-oxide synthase: A role for DNA methylation. J Biol Chem 2004;279:35087-35100. (Pubitemid 39318145)
125. Fish JE, Matouk CC, Rachlis A, Lin S, Tai SC, D'Abreo C et al. The expression of endothelial nitric-oxide synthase is controlled by a cell-specific histone code. J Biol Chem 2005;280:24824-24838. (Pubitemid 40934573)
126. El Mansouri FE, Chabane N, Zayed N, Kapoor M, Benderdour M, Martel-Pelletier J et al. H3K4 methylation by Set1A contributes to IL-1-induced COX-2 and iNOS expression in human OA chondrocytes. Arthritis Rheum 2011;63:168-179.
127. Li Y, Zhao Y, Li G, Wang J, Li T, Li W et al. Regulation of neuronal nitric oxide synthase exon 1f gene expression by nuclear factor-kappaB acetylation in human neuroblastoma cells. J Neurochem 2007;101:1194-1204. (Pubitemid 46718805)
128. Hsiai TK, Wu JC. Hemodynamic forces regulate embryonic stem cell commitment to vascular progenitors. Curr Cardiol Rev 2008;4:269-274.
129. Sone M, Itoh H, Yamashita J, Yurugi-Kobayashi T, Suzuki Y, Kondo Y et al. Different differentiation kinetics of vascular progenitor cells in primate and mouse embryonic stem cells. Circulation 2003;107:2085-2088. (Pubitemid 36532188)
130. Mujoo K, Sharin VG, Bryan NS, Krumenacker JS, Sloan C, Parveen S et al. Role of nitric oxide signaling components in differentiation of embryonic stem cells into myocardial cells. Proc Natl Acad Sci USA 2008;105:18924-18929.
131. Bloch W, Fleischmann BK, Lorke DE, Andressen C, Hops B, Hescheler J et al. Nitric oxide synthase expression and role during cardiomyogenesis. Cardiovasc Res 1999; 43:675-684. (Pubitemid 29369266)
132. Zaccagnini G, Gaetano C, Della Pietra L, Nanni S, Grasselli A, Mangoni A et al. Telomerase mediates vascular endothelial growth factor-dependent responsiveness in a rat model of hind limb ischemia. J Biol Chem 2005;280:14790-14798. (Pubitemid 40562827)
133. Farsetti A, Grasselli A, Bacchetti S, Gaetano C, Capogrossi MC. The telomerase tale in vascular aging: Regulation by estrogens and nitric oxide signaling. J Appl Physiol 2009;106:333-337.
134. Grasselli A, Nanni S, Colussi C, Aiello A, Benvenuti V, Ragone G et al. Estrogen receptor-alpha and endothelial nitric oxide synthase nuclear complex regulates transcription of human telomerase. Circ Res 2008;103:34-42.
135. Zeng L, Xu Q. eNOS-ERalpha complex goes to telomerase. Circ Res 2008;103: 10-12.
136. Colussi C, Mozzetta C, Gurtner A, Illi B, Rosati J, Straino S et al. HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment. Proc Natl Acad Sci USA 2008;105: 19183-19187.
137. Nott A, Watson PM, Robinson JD, Crepaldi L, Riccio A. S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 2008;455:411-415.
138. Doyle K, Fitzpatrick FA. Redox signaling, alkylation (carbonylation) of conserved cysteines inactivates class I histone deacetylases 1, 2, and 3 and antagonizes their transcriptional repressor function. J Biol Chem 2010;285:17417-17424.
139. Colussi C, Gurtner A, Rosati J, Illi B, Ragone G, Piaggio G et al. Nitric oxide deficiency determines global chromatin changes in Duchenne muscular dystrophy. Faseb J 2009;23:2131-2141.
140. Urbich C, Rossig L, Kaluza D, Potente M, Boeckel JN, Knau A et al. HDAC5 is a repressor of angiogenesis and determines the angiogenic gene expression pattern of endothelial cells. Blood 2009;113:5669-5679.
141. Yang QC, Zeng BF, Shi ZM, Dong Y, Jiang ZM, Huang J et al. Inhibition of hypoxia-induced angiogenesis by trichostatin A via suppression of HIF-1a activity in human osteosarcoma. J Exp Clin Cancer Res 2006;25:593-599. (Pubitemid 46170683)
142. Zgouras D, Becker U, Loitsch S, Stein J. Modulation of angiogenesis-related protein synthesis by valproic acid. Biochem Biophys Res Comm 2004;316:693-697. (Pubitemid 38368008)
143. Rossig L, Li H, Fisslthaler B, Urbich C, Fleming I, Forstermann U et al. 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. (Pubitemid 35285082)
144. Kwon HJ, Kim MS, Kim MJ, Nakajima H, Kim KW. Histone deacetylase inhibitor FK228 inhibits tumor angiogenesis. Int J Cancer 2002;97:290-296. (Pubitemid 34049018)
145. Kim MS, Kwon HJ, Lee YM, Baek JH, Jang JE, Lee SW et al. Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes. Nat Med 2001;7:437-443. (Pubitemid 32298546)
146. Pons D, de Vries FR, van den Elsen PJ, Heijmans BT, Quax PH, Jukema JW. Epigenetic histone acetylation modifiers in vascular remodelling: New targets for therapy in cardiovascular disease. Eur Heart J 2009;30:266-277.
147. Dulac C. Brain function and chromatin plasticity. Nature 2010;465:728-735.