Epigenetic basis for the transcriptional hyporesponsiveness of the human inducible nitric oxide synthase gene in vascular endothelial cells

Journal of Immunology

Volumn 175, Issue 6, 2005, Pages 3846-3861

  Chan, Gary C ^a   Fish, Jason E ^a   Mawji, Imtiaz A ^a   Leung, Desmond D ^b   Rachlis, Alisa C ^b   Marsden, Philip A ^a,b,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AZACITIDINE; DINUCLEOTIDE; DNA; DNA METHYLTRANSFERASE INHIBITOR; HISTONE H3; INDUCIBLE NITRIC OXIDE SYNTHASE; LYSINE; METHYL CPG BINDING PROTEIN 2; REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN STRUCTURE; CIS TRANS ISOMERISM; COLON ADENOCARCINOMA; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ENDOTHELIUM CELL; EPIGENETICS; GENE INDUCTION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIVER CELL; LUNG ADENOCARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; REPRESSOR GENE; TRANSCRIPTION REGULATION; VASCULAR ENDOTHELIUM;

EID: 24744438447     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.6.3846     Document Type: Article

References (75)

1. Stuehr, D. J., and M. A. Marletta. 1985. Mammalian nitrate biosynthesis: mouse macrophages produce nitrite and nitrate in response to Escherichia coli lipopolysaccharide. Proc. Natl. Acad. Sci. USA 82: 7738-7742.
2. Balligand, J. L., D. Ungureanu-Longrois, W. W. Simmons, L. Kobzik, C. J. Lowenstein, S. Lamas, R. A. Kelly, T. W. Smith, and T. Michel. 1995. Induction of NO synthase in rat cardiac microvascular endothelial cells by IL-1β and IFN-γ. Am. J. Physiol. 268: H1293-H1303.
3. Marsden, P. A., and B. J. Ballermann. 1990. Tumor necrosis factor α activates soluble guanylate cyclase in bovine glomerular mesangial cells via an L-arginine-dependent mechanism. J. Exp. Med. 172: 1843-1852.
4. Lamas, S., T. Michel, B. M. Brenner, and P. A. Marsden. 1991. Nitric oxide synthesis in endothelial cells: evidence for a pathway inducible by TNF-α. Am. J. Physiol. 261: C634-C641.
5. Lamas, S., T. Michel, T. Collins, B. M. Brenner, and P. A. Marsden. 1992. Effects of interferon-γ on nitric oxide synthase activity and endothelin-1 production by vascular endothelial cells. J. Clin. Invest. 90: 879-887.
6. Radomski, M. W., R. M. Palmer, and S. Moncada. 1990. Glucocorticoids inhibit the expression of an inducible, but not the constitutive, nitric oxide synthase in vascular endothelial cells. Proc. Natl. Acad. Sci. USA 87: 10043-10047.
7. Rosenkranz-Weiss, P., W. C. Sessa, S. Milstien, S. Kaufman, C. A. Watson, and J. S. Pober. 1994. Regulation of nitric oxide synthesis by proinflammatory cytokines in human umbilical vein endothelial cells: elevations in tetrahydrobiopterin levels enhance endothelial nitric oxide synthase specific activity. J. Clin. Invest. 93: 2236-2243.
8. MacMicking, J., Q. W. Xie, and C. Nathan. 1997. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15: 323-350.
9. Zhang, X., V. E. Laubach, E. W. Alley, K. A. Edwards, P. A. Sherman, S. W. Russell, and W. J. Murphy. 1996. Transcriptional basis for hyporesponsiveness of the human inducible nitric oxide synthase gene to lipopolysaccharide/ Interferon-γ. J. Leukocyte Biol. 59: 575-585.
10. Nussler, A. K., M. Di Silvio, T. R. Billiar, R. A. Hoffman, D. A. Geller, R. Selby, J. Madariaga, and R. L. Simmons. 1992. Stimulation of the nitric oxide synthase pathway in human hepatocytes by cytokines and endotoxin. J. Exp. Med. 176: 261-264.
11. Nussler, A. K., M. Di Silvio, Z. Z. Liu, D. A. Geller, P. Freeswick, K. Dorko, F. Bartoli, and T. R. Billiar. 1995. Further characterization and comparison of inducible nitric oxide synthase in mouse, rat, and human hepatocytes. Hepatology 21: 1552-1560.
12. Rubanyi, G. M. 1998. Nitric oxide and circulatory shock. Adv. Exp. Med. Biol. 454: 165-172.
13. Pastor, C. M., and P. M. Suter. 1998. Evidence that humans produce less nitric oxide than experimental animals in septic shock. Crit. Care Med. 26: 1135.
14. St. Clair, E. W., W. E. Wilkinson, T. Lang, L. Sanders, M. A. Misukonis, G. S. Gilkeson, D. S. Pisetsky, D. I. Granger, and J. B. Weinberg. 1996. Increased expression of blood mononuclear cell nitric oxide synthase type 2 in rheumatoid arthritis patients. J. Exp. Med. 184: 1173-1178.
15. Nicholson, S., G. Bonecini-Almeida Mda, J. R. Lapa e Silva, C. Nathan, Q. W. Xie, R. Mumford, J. R. Weidner, J. Calaycay, J. Geng, N. Boechat, et al. 1996. Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J. Exp. Med. 183: 2293-2302.
16. Wilcox, J. N., R. R. Subramanian, C. L. Sundell, W. R. Tracey, J. S. Pollock, D. G. Harrison, and P. A. Marsden. 1997. Expression of multiple isoforms of nitric oxide synthase in normal and atherosclerotic vessels. Arterioscler. Thromb. Vasc. Biol. 17: 2479-2488.
17. Taylor, B. S., and D. A. Geller. 2000. Molecular regulation of the human inducible nitric oxide synthase (iNOS) gene. Shock 13: 413-424.
18. Warke, V. G., M. P. Nambiar, S. Krishnan, K. Tenbrock, D. A. Geller, N. P. Koritschoner, J. L. Atkins, D. L. Farber, and G. C. Tsokos. 2003. Transcriptional activation of the human inducible nitric-oxide synthase promoter by Kruppel-like factor 6. J. Biol. Chem. 278: 14812-14819.
19. Yu, Z., X. Xia, and B. C. Kone. 2005. Expression profile of a human inducible nitric oxide synthase promoter reporter in transgenic mice during endotoxemia. Am. J. Physiol. 288: F214-F220.
20. Chu, S. C., J. Marks-Konczalik, H. P. Wu, T. C. Banks, and J. Moss. 1998. Analysis of the cytokine-stimulated human inducible nitric oxide synthase (iNOS) gene: characterization of differences between human and mouse iNOS promoters. Biochem. Biophys. Res. Commun. 248: 871-878.
21. Marks-Konczalik, J., S. C. Chu, and J. Moss. 1998. Cytokine-mediated transcriptional induction of the human inducible nitric oxide synthase gene requires both activator protein 1 and nuclear factor κB-binding sites. J. Biol. Chem. 273: 22201-22208.
22. Taylor, B. S., M. E. de Vera, R. W. Ganster, Q. Wang, R. A. Shapiro, S. M. Morris, Jr., T. R. Billiar, and D. A. Geller. 1998. Multiple NF-κB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J. Biol. Chem. 273: 15148-15156.
23. Feng, X., Z. Guo, M. Nourbakhsh, H. Hauser, R. Ganster, L. Shao, and D. A. Geller. 2002. Identification of a negative response element in the human inducible nitric-oxide synthase (hiNOS) promoter: the role of NF-κB-repressing factor (NRF) in basal repression of the hiNOS gene. Proc. Natl. Acad. Sci. USA 99: 14212-14217.
24. Hsieh, C. L. 1994. Dependence of transcriptional repression on CpG methylation density. Mol. Cell. Biol. 14: 5487-5494.
25. Wenger, R. H., I. Kvietikova, A. Rolfs, G. Camenisch, and M. Gassmann. 1998. Oxygen-regulated erythropoietin gene expression is dependent on a CpG methylation-free hypoxia-inducible factor-1 DNA-binding site. Eur. J. Biochem. 253: 771-777.
26. Nan, X., H. H. Ng, C. A. Johnson, C. D. Laherty, B. M. Turner, R. N. Eisenman, and A. Bird. 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393: 386-389.
27. Georgel, P. T., R. A. Horowitz-Scherer, N. Adkins, C. L. Woodcock, P. A. Wade, and J. C. Hansen. 2003. Chromatin compaction by human MeCP2. Assembly of novel secondary chromatin structures in the absence of DNA methylation. J. Biol. Chem. 278: 32181-32188.
28. Fuks, F., P. J. Hurd, D. Wolf, X. Nan, A. P. Bird, and T. Kouzarides. 2003. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem. 278: 4035-4040.
29. Jenuwein, T., and C. D. Allis. 2001. Translating the histone code. Science 293: 1074-1080.
30. Struhl, K. 1998. Histone acetylation and transcriptional regulatory mechanisms. Genes Dev. 12: 599-606.
31. Zegerman, P., B. Canas, D. Pappin, and T. Kouzarides. 2002. Histone H3 lysine 4 methylation disrupts binding of nucleosome remodeling and deacetylase (NuRD) repressor complex. J. Biol. Chem. 277: 11621-11624.
32. Lachner, M., D. O'Carroll, S. Rea, K. Mechtler, and T. Jenuwein. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116-120.
33. Stewart, R. J., T. S. Kashour, and P. A. Marsden. 1996. Vascular endothelial platelet endothelial adhesion molecule-1 (PECAM-1) expression is decreased by TNF-α and IFN-γ: evidence for cytokine-induced destabilization of messenger ribonucleic acid transcripts in bovine endothelial cells. J. Immunol. 156: 1221-1228.
34. Pope, M., P. A. Marsden, E. Cole, S. Sloan, L. S. Fung, Q. Ning, J. W. Ding, J. L. Leibowitz, M. J. Phillips, and G. A. Levy. 1998. Resistance to murine hepatitis virus strain 3 is dependent on production of nitric oxide. J. Virol. 72: 7084-7090.
35. Chan, Y., J. E. Fish, C. D'Abreo, S. Lin, G. B. Robb, A. M. Teichert, F. Karantzoulis-Fegaras, A. Keightley, B. M. Steer, and P. A. Marsden. 2004. The cell-specific expression of endothelial nitric-oxide synthase: a role for DNA methylation. J. Biol. Chem. 279: 35087-35100.
36. Pogribny, I., P. Yi, and S. J. James. 1999. A sensitive new method for rapid detection of abnormal methylation patterns in global DNA and within CpG islands. Biochem. Biophys. Res. Commun. 262: 624-628.
37. Marsden, P. A., H. H. Heng, C. L. Duff, X. M. Shi, L. C. Tsui, and A. V. Hall. 1994. Localization of the human gene for inducible nitric oxide synthase (NOS2) to chromosome 17q11.2-q12. Genomics 19: 183-185.
38. Lara-Marquez, M. L., V. Mehta, M. P. Michalsky, J. B. Fleming, and G. E. Besner. 2002. Heparin-binding EGF-like growth factor down regulates proinflammatory cytokine-induced nitric oxide and inducible nitric oxide synthase production in intestinal epithelial cells. Nitric Oxide 6: 142-152.
39. Nissen, R. M., and K. R. Yamamoto. 2000. The glucocorticoid receptor inhibits NFκB by interfering with serine-2 phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 14: 2314-2329.
40. Robb, G. B., A. R. Carson, S. C. Tai, J. E. Fish, S. Singh, T. Yamada, S. W. Scherer, K. Nakabayashi, and P. A. Marsden. 2004. Post-transcriptional regulation of endothelial nitric-oxide synthase by an overlapping antisense mRNA transcript. J. Biol. Chem. 279: 37982-37996.
41. Fish, J. E., C. C. Matouk, A. Rachlis, S. Lin, S. C. Tai, C. D'Abreo, and P. A. Marsden. 2005. The expression of endothelial nitric oxide synthase is controlled by a cell-specific histone code. J. Biol. Chem. 280: 24824-24838.
42. Neish, A. S., L. M. Khachigian, A. Park, V. R. Baichwal, and T. Collins. 1995. Sp1 is a component of the cytokine-inducible enhancer in the promoter of vascular cell adhesion molecule-1. J. Biol. Chem. 270: 28903-28909.
43. Neish, A. S., M. A. Read, D. Thanos, R. Pine, T. Maniatis, and T. Collins. 1995. Endothelial interferon regulatory factor 1 cooperates with NF-κB as a transcriptional activator of vascular cell adhesion molecule 1. Mol. Cell. Biol. 15: 2558-2569.
44. Laubach, V. E., C. X. Zhang, S. W. Russell, W. J. Murphy, and P. A. Sherman. 1997. Analysis of expression and promoter function of the human inducible nitric oxide synthase gene in DLD-1 cells and monkey hepatocytes. Biochim. Biophys. Acta 1351: 287-295.
45. Ramsahoye, B. H., D. Biniszkiewicz, F. Lyko, V. Clark, A. P. Bird, and R. Jaenisch. 2000. Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc. Natl. Acad. Sci. USA 97: 5237-5242.
46. Bruniquel, D., and R. H. Schwartz. 2003. Selective, stable demethylation of the interleukin-2 gene enhances transcription by an active process. Nat. Immunol. 4: 235-240.
47. Boyes, J., and A. Bird. 1992. Repression of genes by DNA methylation depends on CpG density and promoter strength: evidence for involvement of a methyl-CpG binding protein. EMBO J. 11: 327-333.
48. Cameron, E. E., K. E. Bachman, S. Myohanen, J. G. Herman, and S. B. Baylin. 1999. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat. Genet. 21: 103-107.
49. Bender, C. M., M. L. Gonzalgo, F. A. Gonzales, C. T. Nguyen, K. D. Robertson, and P. A. Jones. 1999. Roles of cell division and gene transcription in the methylation of CpG islands. Mol. Cell. Biol. 19: 6690-6698.
50. Michalowsky, L. A., and P. A. Jones. 1989. Gene structure and transcription in mouse cells with extensively demethylated DNA. Mol. Cell. Biol. 9: 885-892.
51. Alikhani-Koopaei, R., F. Fouladkou, F. J. Frey, and B. M. Frey. 2004. Epigenetic regulation of 11β-hydroxysteroid dehydrogenase type 2 expression. J. Clin. Invest. 114: 1146-1157.
52. Taddei, A., C. Maison, D. Roche, and G. Almouzni. 2001. Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat. Cell. Biol. 3: 114-120.
53. Kondo, Y., L. Shen, and J. P. Issa. 2003. Critical role of histone methylation in tumor suppressor gene silencing in colorectal cancer. Mol. Cell. Biol. 23: 206-215.
54. Saccani, S., and G. Natoli. 2002. Dynamic changes in histone H3 Lys 9 methylation occurring at tightly regulated inducible inflammatory genes. Genes Dev. 16: 2219-2224.
55. Edelstein, L. C., A. Pan, and T. Collins. 2005. Chromatin modification and the endothelial-specific activation of the E-selectin gene. J. Biol. Chem. 280: 11192-11202.
56. Gardiner-Garden, M., and M. Frommer. 1987. CpG islands in vertebrate genomes. J. Mol. Biol. 196: 261-282.
57. Tzeng, E., T. R. Billiar, P. D. Robbins, M. Loftus, and D. J. Stuehr. 1995. Expression of human inducible nitric oxide synthase in a tetrahydrobiopterin (H4B)-deficient cell line: H4B promotes assembly of enzyme subunits into an active dimer. Proc. Natl. Acad. Sci. USA 92: 11771-11775.
58. Yu, Z., and B. C. Kone. 2004. Hypermethylation of the inducible nitric oxide synthase gene promoter inhibits its transcription. J. Biol. Chem. 279: 46954-46961.
59. MacNaul, K. L., and N. I. Hutchinson. 1993. Differential expression of iNOS and cNOS mRNA in human vascular smooth muscle cells and endothelial cells under normal and inflammatory conditions. Biochem. Biophys. Res. Commun. 196: 1330-1334.
60. Bernstein, B. E., M. Kamal, K. Lindblad-Toh, S. Bekiranov, D. K. Bailey, D. J. Huebert, S. McMahon, E. K. Karlsson, E. J. Kulbokas III, T. R. Gingeras, et al. 2005. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120: 169-181.
61. Waterston, R. H., K. Lindblad-Toh, E. Birney, J. Rogers, J. F. Abril, P. Agarwal, R. Agarwala, R. Ainscough, M. Alexandersson, P. An, et al. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562.
62. Rice, J. C., S. D. Briggs, B. Ueberheide, C. M. Barber, J. Shabanowitz, D. F. Hunt, Y. Shinkai, and C. D. Allis. 2003. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol. Cell. 12: 1591-1598.
63. Saito, Y., Y. Kanai, M. Sakamoto, H. Saito, H. Ishii, and S. Hirohashi. 2002. Overexpression of a splice variant of DNA methyltransferase 3b, DNMT3b4, associated with DNA hypomethylation on pericentromeric satellite regions during human hepatocarcinogenesis. Proc. Natl. Acad. Sci. USA 99: 10060-10065.
64. Jackson, M. 2003. Duplicate, decouple, disperse: the evolutionary transience of human centromeric regions. Curr. Opin. Genet. Dev. 13: 629-635.
65. Park, S. S., P. Stankiewicz, W. Bi, C. Shaw, J. Lehoczky, K. Dewar, B. Birren, and J. R. Lupski. 2002. Structure and evolution of the Smith-Magenis syndrome repeat gene clusters, SMS-REPs. Genome Res. 12: 729-738.
66. Xu, W., I. G. Charles, L. Liu, P. A. Koni, S. Moncada, and P. Emson. 1995. Molecular genetic analysis of the duplication of human inducible nitric oxide synthase (NOS2) sequences. Biochem. Biophys. Res. Commun. 212: 466-472.
67. Jesch, N. K., M. Dorger, G. Enders, G. Rieder, C. Vogelmeier, K. Messmer, and F. Krombach. 1997. Expression of inducible nitric oxide synthase and formation of nitric oxide by alveolar macrophages: an interspecies comparison. Environ Health Perspect 105(Suppl. 5): 1297-300.
68. Dorger, M., N. K. Jesch, G. Rieder, M. R. Hirvonen, K. Savolainen, F. Krombach, and K. Messmer. 1997. Species differences in NO formation by rat and hamster alveolar macrophages in vitro. Am. J. Respir. Cell Mol. Biol. 16: 413-420.
69. Koraeev, S. A., J. H. Park, and M. O'Shea. 1999. Neuronal expression of neural nitric oxide synthase (nNOS) protein is suppressed by an antisense RNA transcribed from an NOS pseudogene. J. Neurosci. 19: 7711-7720.
70. Hirotsune, S., N. Yoshida, A. Chen, L. Garrett, F. Sugiyama, S. Takahashi, K. Yagami, A. Wynshaw-Boris, and A. Yoshiki. 2003. An expressed pseudogene regulates the messenger-RNA stability of its homologous coding gene. Nature 423: 91-96.
71. Kricker, M. C., J. W. Drake, and M. Radman. 1992. Duplication-targeted DNA methylation and mutagenesis in the evolution of eukaryotic chromosomes. Proc. Natl. Acad. Sci. USA 89: 1075-1079.
72. Matzke, M. A., M. F. Mette, and A. J. Matzke. 2000. Transgene silencing by the host genome defense: implications for the evolution of epigenetic control mechanisms in plants and vertebrates. Plant Mol. Biol. 43: 401-415.
73. Teichert, A. M., T. L. Miller, S. C. Tai, Y. Wang, X. Bei, G. B. Robb, M. J. Phillips, and P. A. Marsden. 2000. In vivo expression profile of an endothelial nitric oxide synthase promoter-reporter transgene. Am. J. Physiol. 278: H1352-H1361.
74. Tamaru, H., and E. U. Selker. 2001. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414: 277-283.
75. Jackson, J. P., A. M. Lindroth, X. Cao, and S. E. Jacobsen. 2002. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556-560.