Epigenetics: New concepts of old phenomena in vascular physiology

Current Vascular Pharmacology

Volumn 7, Issue 4, 2009, Pages 513-520

  Krause, Bernardo ^a   Sobrevia, Luis ^a   Casanello, Paola ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

Endothelium; Epigenetics; Human; Smooth muscle cell; Vascular

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1; ADENOSINE TRIPHOSPHATE; ALPHA ACTIN; ANGIOPOIETIN RECEPTOR; DNA; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOCORTICOID RECEPTOR; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 4; HISTONE H2A; HISTONE H2B; HISTONE H3; HISTONE H4; HISTONE METHYLTRANSFERASE; NOTCH RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; TIE 1 RECEPTOR; TRANSCRIPTION FACTOR PDX 1; TRANSCRIPTION FACTOR SNF; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNTRANSLATED RNA; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; CARDIOVASCULAR DISEASE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; EPIGENETICS; FETUS DEVELOPMENT; GENE EXPRESSION REGULATION; HUMAN; INSULIN RESISTANCE; INTRAUTERINE GROWTH RETARDATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PHENOTYPIC PLASTICITY; PREECLAMPSIA; PREGNANCY DIABETES MELLITUS; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION;

BLOOD VESSELS; DIABETES, GESTATIONAL; EPIGENESIS, GENETIC; FEMALE; FETAL DEVELOPMENT; FETAL GROWTH RETARDATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; PRE-ECLAMPSIA; PREGNANCY;

EID: 69549096691     PISSN: 15701611     EISSN: None     Source Type: Journal    
DOI: 10.2174/157016109789043883     Document Type: Review

References (84)

1. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 2007; 447: 425-32.
2. McDonald OG, Owens GK. Programming smooth muscle plasticity with chromatin dynamics. Circ Res. 2007; 100: 1428-41.
3. Matouk CC, Marsden PA. Epigenetic regulation of vascular endothelial gene expression. Circ Res 2008; 102: 873-87.
4. Casanello P, Escudero C, Sobrevia L. Equilibrative nucleoside (ENTs) and cationic amino acid (CATs) transporters: implications in foetal endothelial dysfunction in human pregnancy diseases. Curr Vasc Pharmacol 2007; 5: 69-84.
5. Escudero C, Sobrevia L. A Hypothesis for preeclampsia: adenosine and inducible nitric oxide synthase in human placental microvascular endothelium. Placenta 2008; 29: 469-83.
6. Kimura A, Matsubara K, Horikoshi M. A decade of histone acetylation: marking eukaryotic chromosomes with specific codes. J Biochem 2005; 138: 647-62.
7. Bird A. Perceptions of epigenetics. Nature 2007; 447: 396-8.
8. Jablonka E, Lamb MJ. The changing concept of epigenetics. Ann N Y Acad Sci 2002; 981: 82-96.
9. Goldberg AD, Allis CD, Bernstein E. Epigenetics: a landscape takes shape. Cell 2007; 128: 635-8.
10. Van Speybroeck L. From epigenesis to epigenetics: the case of C. H. Waddington. Ann N Y Acad Sci 2002; 981: 61-81.
11. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet 2007; 8: 253-62.
12. Goll MG, Bestor TH. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 2005; 74: 481-514.
13. Wu H, Sun YE. Epigenetic regulation of stem cell differentiation. Pediatr Res 2006; 59: 21R-25R.
14. Buryanov YI, Shevchuk TV. DNA methyltransferases and structural-functional specificity of eukaryotic DNA modification. Biochemistry 2005; 70: 730-42.
15. Miranda TB, Jones PA. DNA methylation: the nuts and bolts of repression. J Cell Physiol 2007; 213: 384-90.
16. Collas P, Noer A, Timoskainen S. Programming the genome in embryonic and somatic stem cells. J Cell Mol Med 2007; 11: 602-20.
17. Klose RJ, Bird AP. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 2006; 31: 89-97.
18. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007; 447: 407-12.
19. Cosgrove MS, Wolberger C. How does the histone code work? Biochem Cell Biol 2005; 83: 468-76.
20. Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293: 1074-80.
21. Wang GG, Allis CD, Chi P. Chromatin remodeling and cancer, Part I: Covalent histone modifications. Trends Mol Med 2007; 13: 363-72.
22. Kouzarides T. Chromatin modifications and their function. Cell 2007; 128: 693-705.
23. Thiagalingam S, Cheng KH, Lee HJ, Mineva N, Thiagalingam A, Ponte JF. Histone deacetylases: unique players in shaping the epigenetic histone code. Ann N Y Acad Sci 2003; 983: 84-100.
24. Trojer P, Reinberg D. Histone lysine demethylases and their impact on epigenetics. Cell 2006; 125: 213-7.
25. Becker PB, Hörz W. ATP-dependent nucleosome remodeling. Annu Rev Biochem 2002; 71: 247-73.
26. Wang GG, Allis CD, Chi P. Chromatin remodeling and cancer, Part II: ATP-dependent chromatin remodeling. Trends Mol Med 2007; 13: 373-80.
27. Britten RJ, Davidson EH. Gene regulation for higher cells: a theory. Science 1969; 165: 349-57.
28. Morris KV. siRNA-mediated transcriptional gene silencing: the potential mechanism and a possible role in the histone code. Cell Mol Life Sci 2005; 62: 3057-66.
29. Chu CY, Rana TM. Small RNAs: regulators and guardians of the genome. J Cell Physiol 2007; 213: 412-9.
30. Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986; 1: 1077-81.
31. Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 1991; 303: 1019-22.
32. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 1993; 36: 62-7.
33. McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 2005; 85: 571-633.
34. Cutfield WS, Hofman PL, Mitchell M, Morison IM. Could epigenetics play a role in the developmental origins of health and disease? Pediatr Res 2007; 61: 68R-75R.
35. Fowden AL, Sibley C, Reik W, Constancia M. Imprinted genes, placental development and fetal growth. Horm Res 2006; 65: S50-S58.
36. McMinn J, Wei M, Sadovsky Y, Thaker HM, Tycko B. Imprinting of PEG1/MEST isoform 2 in human placenta. Placenta 2006; 27: 119-26.
37. Dokras A, Coffin J, Field L, Frakes A, Lee H, Madan A, et al. Epigenetic regulation of maspin expression in the human placenta. Mol Hum Reprod 2006; 12: 611-7.
38. Kimura AP, Sizova D, Handwerger S, Cooke NE, Liebhaber SA. Epigenetic activation of the human growth hormone gene cluster during placental cytotrophoblast differentiation. Mol Cell Biol 2007; 27: 6555-68.
39. McMinn J, Wei M, Schupf N, Cusmai J, Johnson EB, Smith AC, et al. Unbalanced placental expression of imprinted genes in human intrauterine growth restriction. Placenta 2006; 27: 540-9.
40. Guo L, Choufani S, Ferreira J, Smith A, Chitayat D, Shuman C, et al. Altered gene expression and methylation of the human chromosome 11 imprinted region in small for gestational age (SGA) placentae. Dev Biol 2008; 320: 79-91.
41. Monk D, Arnaud P, Apostolidou S, Hills FA, Kelsey G, Stanier P, et al. Limited evolutionary conservation of imprinting in the human placenta. Proc Natl Acad Sci 2006; 103: 6623-8.
42. Chelbi ST, Mondon F, Jammes H, Buffat C, Mignot TM, Tost J, et al. Expressional and epigenetic alterations of placental serine protease inhibitors: SERPINA3 is a potential marker of preeclampsia. Hypertension 2007; 49: 76-83.
43. Murphy R, Ellard S, Hattersley AT. Clinical implications of a molecular genetic classification of monogenic beta-cell diabetes. Nat Clin Pract Endocrinol Metab 2008; 4: 200-13.
44. Wren JD, Garner HR. Data-mining analysis suggests an epigenetic pathogenesis for type 2 diabetes. J Biomed Biotechnol 2005; 2: 104-12.
45. Park JH, Stoffers DA, Nicholls RD, Simmons RA. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest 2008; 118: 2316-24.
46. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 2005; 135: 1382-6.
47. Lillycrop KA, Slater-Jefferies JL, Hanson MA, Godfrey KM, Jackson AA, Burdge GC. Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr 2007; 97: 1064-73.
48. Fu Q, McKnight RA, Yu X, Wang L, Callaway CW, Lane RH. Uteroplacental insufficiency induces site-specific changes in histone H3 covalent modifications and affects DNA-histone H3 positioning in day 0 IUGR rat liver. Physiol Genomics 2004; 20: 108-16.
49. Fu Q, McKnight RA, Yu X, Callaway CW, Lane RH. Growth retardation alters the epigenetic characteristics of hepatic dual specificity phosphatase 5. FASEB J 2006; 20: 1441-50.
50. Raychaudhuri N, Raychaudhuri S, Thamotharan M, Devaskar SU. Histone code modifications repress glucose transporter 4 expression in the intrauterine growth-restricted offspring. J Biol Chem 2008; 283: 13611-26.
51. Ke X, Lei Q, James SJ, Kelleher SL, Melnyk S, Jernigan S, et al. Uteroplacental insufficiency affects epigenetic determinants of chromatin structure in brains of neonatal and juvenile IUGR rats. Physiol Genomics 2006; 25: 16-28.
52. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, et al. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7: 847-54.
53. Weaver IC, Champagne FA, Brown SE, Dymov S, Sharma S, Meaney MJ, et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci 2005; 25: 11045-54.
54. Bogdarina I, Welham S, King PJ, Burns SP, Clark AJ. Epigenetic modification of the renin-angiotensin system in the fetal programming of hypertension. Circ Res 2007; 100: 520-626.
55. Risau W. Mechanisms of angiogenesis. Nature 1997; 386: 671-4.
56. Hamik A, Wang B, Jain MK. Transcriptional regulators of angiogenesis. Arterioscler Thromb Vasc Biol 2006; 26: 1936-47.
57. Jones EA, le Noble F, Eichmann A. What determines blood vessel structure? Genetic prespecification vs. Hemodynamics. Physiology 2006; 21: 388-95.
58. Hirashima M, Suda T. Differentiation of arterial and venous endothelial cells and vascular morphogenesis. Endothelium 2006; 13: 137-45.
59. le Noble F, Klein C, Tintu A, Pries A, Buschmann I. Neural guidance molecules, tip cells, and mechanical factors in vascular development. Cardiovasc Res 2008; 78: 232-41.
60. Fish JE, Marsden PA. Endothelial nitric oxide synthase: insight into cell-specific gene regulation in the vascular endothelium. Cell Mol Life Sci 2006; 63: 144-62.
61. Dekker RJ, Boon RA, Rondaij MG, Kragt A, Volger OL, Elderkamp YW, et al. KLF2 provokes a gene expression pattern that establishes functional quiescent differentiation of the endothelium. Blood 2006; 107: 4354-63.
62. 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: 437-43.
63. 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: 501-8.
64. Zeng L, Xiao Q, Margariti A, Zhang Z, Zampetaki A, Patel S, et al. HDAC3 is crucial in shear- and VEGF-induced stem cell differentiation toward endothelial cells. J Cell Biol 2006; 174: 1059-69.
65. Deroanne CF, Bonjean K, Servotte S, Devy L, Colige A, Clausse N, et al. Histone deacetylases inhibitors as anti-angiogenic agents altering vascular endothelial growth factor signaling. Oncogene 2002; 21: 427-36.
66. Peng Y, Jahroudi N. The NFY transcription factor inhibits von Willebrand factor promoter activation in non-endothelial cells through recruitment of histone deacetylases. J Biol Chem 2003; 278: 8385-94.
67. Wu J, Iwata F, Grass JA, Osborne CS, Elnitski L, Fraser P, et al. Molecular determinants of NOTCH4 transcription in vascular endothelium. Mol Cell Biol 2005; 25: 1458-74.
68. Rössig L, Li H, Fisslthaler B, Urbich C, Fleming I, Förstermann 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: 837-44.
69. 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: 1472-8.
70. 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: 35087-100.
71. Lagarkova MA, Volchkov PY, Philonenko ES, Kiselev SL. Efficient differentiation of hESCs into endothelial cells in vitro is secured by epigenetic changes. Cell Cycle 2008; 7: 2929-35.
72. El-Osta A, Brasacchio D, Yao D, Pocai A, Jones PL, Roeder RG, et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 2008; 205: 2409-17.
73. Wang DZ, Olson EN. Control of smooth muscle development by the myocardin family of transcriptional coactivators. Curr Opin Genet Dev 2004; 14: 558-66.
74. Manabe I, Owens GK. Recruitment of serum response factor and hyperacetylation of histones at smooth muscle-specific regulatory regions during differentiation of a novel P19-derived in vitro smooth muscle differentiation system. Circ Res 2001; 88: 1127-34.
75. 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: 858-65.
76. 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.
77. Cao D, Wang Z, Zhang CL, Oh J, Xing W, Li S, et al. Modulation of smooth muscle gene expression by association of histone acetyl-transferases and deacetylases with myocardin. Mol Cell Biol 2005; 25: 364-76.
78. Davis CA, Haberland M, Arnold MA, Sutherland LB, McDonald OG, Richardson JA, et al. PRISM/PRDM6, a transcriptional repressor that promotes the proliferative gene program in smooth muscle cells. Mol Cell Biol 2006; 26: 2626-36.
79. Glenisson W, Castronovo V, Waltregny D. Histone deacetylase 4 is required for TGFβ1-induced myofibroblastic differentiation. Biochim Biophys Acta 2007; 1773: 1572-82.
80. Reddy MA, Villeneuve LM, Wang M, Lanting L, Natarajan R. Role of the lysine-specific demethylase 1 in the proinflammatory phenotype of vascular smooth muscle cells of diabetic mice. Circ Res 2008; 103: 615-23.
81. Villeneuve LM, Reddy MA, Lanting LL, Wang M, Meng L, Natarajan R. Epigenetic histone H3 lysine 9 methylation in metabolic memory and inflammatory phenotype of vascular smooth muscle cells in diabetes. Proc Natl Acad Sci 2008; 105: 9047-52.
82. Okazaki K, Maltepe E. Oxygen, epigenetics and stem cell fate. Regen Med 2006; 1: 71-83.
83. Grasselli A, Nanni S, Colussi C, Aiello A, Benvenuti V, Ragone G, et al. Estrogen receptor-α and endothelial nitric oxide synthase nuclear complex regulates transcription of human telomerase. Circ Res 2008; doi: 10.1161/circresaha.107.169037.
84. 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: 51-8.