A mechanistic role for DNA methylation in endothelial cell (EC)-enriched gene expression: relationship with DNA replication timing

Blood

Volumn 121, Issue 17, 2013, Pages 3531-3540

  Shirodkar, Apurva V ^a   Bernard, Rosanne St ^a   Gavryushova, Anna ^b   Kop, Anna ^b   Knight, Britta J ^b   Yan, Matthew Shu Ching ^a   Man, Hon Sum Jeffrey ^a   Sud, Maneesh ^a   Hebbel, Robert P ^c   Oettgen, Peter ^d   Aird, William C ^d   Marsden, Philip A ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; DNA METHYLTRANSFERASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 2; PADGEM PROTEIN; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VON WILLEBRAND FACTOR; CADHERIN; CELL ADHESION MOLECULE; LEUKOCYTE ANTIGEN;

ANIMAL CELL; ARTICLE; CELL CYCLE S PHASE; CELLS BY BODY ANATOMY; CONTROLLED STUDY; DNA FINGERPRINTING; DNA METHYLATION; DNA REPLICATION TIMING; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PYROSEQUENCING; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; AORTA; CATTLE; CELL CULTURE; CHROMATIN IMMUNOPRECIPITATION; COMPARATIVE STUDY; CYTOLOGY; DERMIS; GENE EXPRESSION REGULATION; GENETICS; KERATINOCYTE; LIVER CELL; METABOLISM; MOUSE; PHYSIOLOGY; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE;

ANIMALS; ANTIGENS, CD; AORTA; CADHERINS; CATTLE; CELL ADHESION MOLECULES; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; DERMIS; DNA METHYLATION; DNA REPLICATION TIMING; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION; HEPATOCYTES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; KERATINOCYTES; MICE; MUSCLE, SMOOTH, VASCULAR; NITRIC OXIDE SYNTHASE TYPE III; PROMOTER REGIONS, GENETIC; S PHASE; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; VON WILLEBRAND FACTOR;

MLCS; MLOWN;

EID: 84879361116     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-01-479170     Document Type: Article

References (48)

1. Chi JT, Chang HY, Haraldsen G, et al. Endothelial cell diversity revealed by global expression profiling. Proc Natl Acad Sci USA. 2003;100(19): 10623-10628.
2. Aird WC. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res. 2007;100(2):158-173.
3. Bhasin M, Yuan L, Keskin DB, Otu HH, Libermann TA, Oettgen P. Bioinformatic identification and characterization of human endothelial cell-restricted genes. BMC Genomics. 2010;11:342.
4. Lister R, Pelizzola M, Dowen RH, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 2009;462(7271):315-322.
5. Irizarry RA, Ladd-Acosta C, Wen B, et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet. 2009; 41(2):178-186.
6. Wilcox JN, Subramanian RR, Sundell CL, Tracey WR, Pollock JS, Harrison DG, Marsden PA. Expression of multiple isoforms of nitric oxide synthase in normal and atherosclerotic vessels. Arterioscler Thromb Vasc Biol. 1997;17(11): 2479-2488.
7. Chan Y, Fish JE, D’Abreo C, et al. The cell-specific expression of endothelial nitric-oxide synthase: a role for DNA methylation. J Biol Chem. 2004;279(33):35087-35100.
8. Matouk CC, Marsden PA. Epigenetic regulation of vascular endothelial gene expression. Circ Res. 2008;102(8):873-887.
9. Shirodkar AV, Marsden PA. Epigenetics in cardiovascular disease. Curr Opin Cardiol. 2011; 26(3):209-215.
10. White EJ, Emanuelsson O, Scalzo D, et al. DNA replication-timing analysis of human chromosome 22 at high resolution and different developmental states. Proc Natl Acad Sci USA. 2004;101(51): 17771-17776.
11. ENCODE Project Consortium. A user’s guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 2011;9(4):e1001046.
12. Marsden PA, Schappert KT, Chen HS, et al. Molecular cloning and characterization of human endothelial nitric oxide synthase. FEBS Lett. 1992;307(3):287-293.
13. Flowers MA, Wang Y, Stewart RJ, Patel B, Marsden PA. Reciprocal regulation of endothelin-1 and endothelial constitutive NOS in proliferating endothelial cells. Am J Physiol. 1995;269(6 Pt 2): H1988-H1997.
14. Lin Y, Weisdorf DJ, Solovey A, Hebbel RP. Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest. 2000;105(1):71-77.
15. Azuara V. Profiling of DNA replication timing in unsynchronized cell populations. Nat Protoc. 2006;1(4):2171-2177.
16. Chan GC, Fish JE, Mawji IA, Leung DD, Rachlis AC, Marsden PA. Epigenetic basis for the transcriptional hyporesponsiveness of the human inducible nitric oxide synthase gene in vascular endothelial cells. J Immunol. 2005;175(6): 3846-3861.
17. Fish JE, Matouk CC, Rachlis A, Lin S, Tai SC, D’Abreo C, Marsden PA. The expression of endothelial nitric-oxide synthase is controlled by a cell-specific histone code. J Biol Chem. 2005; 280(26):24824-24838.
18. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, Schübeler D. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet. 2005;37(8): 853-862.
19. Guillot PV, Liu L, Kuivenhoven JA, Guan J, Rosenberg RD, Aird WC. Targeting of human eNOS promoter to the Hprt locus of mice leads to tissue-restricted transgene expression. Physiol Genomics. 2000;2(2):77-83.
20. Teichert AM, Scott JA, Robb GB, et al. Endothelial nitric oxide synthase gene expression during murine embryogenesis: commencement of expression in the embryo occurs with the establishment of a unidirectional circulatory system. Circ Res. 2008;103(1):24-33.
21. Jahroudi N, Lynch DC. Endothelial-cell-specific regulation of von Willebrand factor gene expression. Mol Cell Biol. 1994;14(2):999-1008.
22. Prandini MH, Dreher I, Bouillot S, Benkerri S, Moll T, Huber P. The human VE-cadherin promoter is subjected to organ-specific regulation and is activated in tumour angiogenesis. Oncogene. 2005;24(18):2992-3001.
23. Coombes MM, Briggs KL, Bone JR, Clayman GL, El-Naggar AK, Dent SY. Resetting the histone code at CDKN2A in HNSCC by inhibition of DNA methylation. Oncogene. 2003;22(55):8902-8911.
24. Zhang Y, Fatima N, Dufau ML. Coordinated changes in DNA methylation and histone modifications regulate silencing/derepression of luteinizing hormone receptor gene transcription. Mol Cell Biol. 2005;25(18):7929-7939.
25. Cameron EE, Bachman KE, Myöhänen S, Herman JG, Baylin SB. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet. 1999;21(1):103-107.
26. Tahiliani M, Koh KP, Shen Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 2009;324(5929):930-935.
27. Huang Y, Pastor WA, Shen Y, Tahiliani M, Liu DR, Rao A. The behaviour of 5-hydroxymethylcytosine in bisulfite sequencing. PLoS ONE. 2010;5(1): e8888.
28. Goll MG, Bestor TH. Eukaryotic cytosine methyltransferases. Annu Rev Biochem. 2005;74: 481-514.
29. Azuara V, Perry P, Sauer S, et al. Chromatin signatures of pluripotent cell lines. Nat Cell Biol. 2006;8(5):532-538.
30. Ginder GD, Gnanapragasam MN, Mian OY. The role of the epigenetic signal, DNA methylation, in gene regulation during erythroid development. Curr Top Dev Biol. 2008;82:85-116.
31. Perry P, Sauer S, Billon N, et al. A dynamic switch in the replication timing of key regulator genes in embryonic stem cells upon neural induction. Cell Cycle. 2004;3(12):1645-1650.
32. Kitsberg D, Selig S, Keshet I, Cedar H. Replication structure of the human beta-globin gene domain. Nature. 1993;366(6455):588-590.
33. Weddington N, Stuy A, Hiratani I, Ryba T, Yokochi T, Gilbert DM. ReplicationDomain: a visualization tool and comparative database for genome-wide replication timing data. BMC Bioinformatics. 2008; 9:530.
34. Yamada Y, Watanabe M, Yamanaka M, et al. Aberrant methylation of the vascular endothelial growth factor receptor-1 gene in prostate cancer. Cancer Sci. 2003;94(6):536-539.
35. Rao X, Zhong J, Zhang S, et al. Loss of methyl-CpG-binding domain protein 2 enhances endothelial angiogenesis and protects mice against hind-limb ischemic injury. Circulation. 2011;123(25):2964-2974.
36. Fong GH, Klingensmith J, Wood CR, Rossant J, Breitman ML. Regulation of flt-1 expression during mouse embryogenesis suggests a role in the establishment of vascular endothelium. Dev Dyn. 1996;207(1):1-10.
37. Dumont DJ, Fong GH, Puri MC, Gradwohl G, Alitalo K, Breitman ML. Vascularization of the mouse embryo: a study of flk-1, tek, tie, and vascular endothelial growth factor expression during development. Dev Dyn. 1995;203(1): 80-92.
38. Breier G, Breviario F, Caveda L, et al. Molecular cloning and expression of murine vascular endothelial-cadherin in early stage development of cardiovascular system. Blood. 1996;87(2): 630-641.
39. Dumont DJ, Yamaguchi TP, Conlon RA, Rossant J, Breitman ML. tek, a novel tyrosine kinase gene located on mouse chromosome 4, is expressed in endothelial cells and their presumptive precursors. Oncogene. 1992;7(8): 1471-1480.
40. Hiratani I, Ryba T, Itoh M, et al. Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 2008;6(10):e245.
41. Lin Y, Chang L, Solovey A, Healey JF, Lollar P, Hebbel RP. Use of blood outgrowth endothelial cells for gene therapy for hemophilia A. Blood. 2002;99(2):457-462.
42. Jevremovic D, Gulati R, Hennig I, et al. Use of blood outgrowth endothelial cells as virus-producing vectors for gene delivery to tumors. Am J Physiol Heart Circ Physiol. 2004;287(2): H494-H500.
43. Ohtani K, Vlachojannis GJ, Koyanagi M, et al. Epigenetic regulation of endothelial lineage committed genes in pro-angiogenic hematopoietic and endothelial progenitor cells. Circ Res. 2011;109(11): 1219-1229.
44. Webster AL, Yan MS, Marsden PA. Epigenetics and cardiovascular disease. Can J Cardiol. 2013; 29(1):46-57.
45. Won D, Zhu SN, Chen M, et al. Relative reduction of endothelial nitric-oxide synthase expression and transcription in atherosclerosis-prone regions of the mouse aorta and in an in vitro model of disturbed flow. Am J Pathol. 2007;171(5): 1691-1704.
46. Meyer LR, Zweig AS, Hinrichs AS, et al. The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res. 2013; 41(Database issue D1):D64-D69.
47. Gulati R, Jevremovic D, Peterson TE, Chatterjee S, Shah V, Vile RG, Simari RD. Diverse origin and function of cells with endothelial phenotype obtained from adult human blood. Circ Res. 2003; 93(11):1023-1025.
48. Hirschi KK, Ingram DA, Yoder MC. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol. 2008;28(9):1584-1595.