Hypoxic repression of endothelial nitric-oxide synthase transcription is coupled with eviction of promoter histones

Journal of Biological Chemistry

Volumn 285, Issue 2, 2010, Pages 810-826

  Fish, Jason E ^a,b   Yan, Matthew S ^a   Matouk, Charles C ^a   St Bernard, Rosanne ^a   Ho Jr , J J David ^a   Gavryushova, Anna ^a   Srivastava, Deepak ^b   Marsfen, Philip A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL DYSFUNCTION; ENDOTHELIAL NITRIC-OXIDE SYNTHASE (ENOS); HISTONE ACETYLATION; HISTONE H3; HISTONE MODIFICATION; HYPOXIC CELLS; MAMMALIAN CELLS; NITRIC-OXIDE SYNTHASE; NUCLEOSOMES; RE-ESTABLISHING; REOXYGENATION; TRANSCRIPTIONAL ACTIVATIONS; TRANSCRIPTIONAL ACTIVITY; TRANSCRIPTIONAL REPRESSION;

ACETYLATION; AMINO ACIDS; MAMMALS; SELF ASSEMBLY; TRANSCRIPTION;

PROTEINS;

BRG1 PROTEIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HISTONE;

ACETYLATION; ARTICLE; CELL HYPOXIA; CHROMATIN; CONTROLLED STUDY; GENE REPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROCESSING; REOXYGENATION; TRANSCRIPTION INITIATION;

ACETYLATION; CELL HYPOXIA; CELLS, CULTURED; DNA HELICASES; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HISTONES; HUMANS; NITRIC OXIDE SYNTHASE TYPE III; NUCLEAR PROTEINS; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 74049085411     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M109.067868     Document Type: Article

References (83)

1. Chi, J. T., Wang, Z., Nuyten, D. S., Rodriguez, E. H., Schaner, M. E., Salim, A., Wang, Y., Kristensen, G. B., Helland, A., Børresen-Dale, A. L., Giaccia, A., Longaker, M. T., Hastie, T., Yang, G. P., van de Vijver, M. J., and Brown, P. O. (2006) PLoS Med. 3, e47
2. Kourembanas, S., Marsden, P. A., McQuillan, L. P., and Faller, D. V. (1991) J. Clin. Invest. 88, 1054-1057
3. Kourembanas, S., Hannan, R. L., and Faller, D. V. (1990) J. Clin. Invest. 86, 670-674
4. McQuillan, L. P., Leung, G. K., Marsden, P. A., Kostyk, S. K., and Kourembanas, S. (1994) Am. J. Physiol. 267, H1921-1927
5. Moudgil, R., Michelakis, E. D., and Archer, S. L. (2005) J. Appl. Physiol. 98, 390-403
6. Humbert, M., Morrell, N. W., Archer, S. L., Stenmark, K. R., MacLean, M. R., Lang, I. M., Christman, B. W., Weir, E. K., Eickelberg, O., Voelkel, N. F., and Rabinovitch, M. (2004) J. Am. Coll. Cardiol. 43, 13S-24S
7. Fagan, K. A., Fouty, B. W., Tyler, R. C., Morris, K. G., Jr., Hepler, L. K., Sato, K., LeCras, T. D., Abman, S. H., Weinberger, H. D., Huang, P. L., Mc-Murtry, I. F., and Rodman, D. M. (1999) J. Clin. Invest. 103, 291-299
8. Ozaki, M., Kawashima, S., Yamashita, T., Ohashi, Y., Rikitake, Y., Inoue, N., Hirata, K. I., Hayashi, Y., Itoh, H., and Yokoyama, M. (2001) Hypertension 37, 322-327
9. Giaid, A., and Saleh, D. (1995) N. Engl. J. Med. 333, 214-221
10. Champion, H. C., Bivalacqua, T. J., Greenberg, S. S., Giles, T. D., Hyman, A. L., and Kadowitz, P. J. (2002) Proc. Natl. Acad. Sci. U.S.A. 99, 13248-13253
11. Denko, N., Wernke-Dollries, K., Johnson, A. B., Hammond, E., Chiang, C. M., and Barton, M. C. (2003) J. Biol. Chem. 278, 5744-5749
12. Ivanov, S. V., Salnikow, K., Ivanova, A. V., Bai, L., and Lerman, M. I. (2007) Oncogene 26, 802-812
13. Kitamuro, T., Takahashi, K., Ogawa, K., Udono-Fujimori, R., Takeda, K., Furuyama, K., Nakayama, M., Sun, J., Fujita, H., Hida, W., Hattori, T., Shirato, K., Igarashi, K., and Shibahara, S. (2003) J. Biol. Chem. 278, 9125-9133
14. Nakamura, H., Tanimoto, K., Hiyama, K., Yunokawa, M., Kawamoto, T., Kato, Y., Yoshiga, K., Poellinger, L., Hiyama, E., and Nishiyama, M. (2008) Oncogene 27, 4200-4209
15. Choi, S. M., Cho, H. J., Cho, H., Kim, K. H., Kim, J. B., and Park, H. (2008) Nucleic Acids Res. 36, 6372-6385
16. Mazure, N. M., Chauvet, C., Bois-Joyeux, B., Bernard, M. A., Nacer-Chérif, H., and Danan, J. L. (2002) Cancer Res. 62, 1158-1165
17. Chen, K. F., Lai, Y. Y., Sun, H. S., and Tsai, S. J. (2005) Nucleic Acids Res. 33, 5190-5198
18. Eltzschig, H. K., Abdulla, P., Hoffman, E., Hamilton, K. E., Daniels, D., Schönfeld, C., Löffler, M., Reyes, G., Duszenko, M., Karhausen, J., Robinson, A., Westerman, K. A., Coe, I. R., and Colgan, S. P. (2005) J. Exp. Med. 202, 1493-1505
19. Fish, J. E., Matouk, C. C., Rachlis, A., Lin, S., Tai, S. C., D'Abreo, C., and Marsden, P. A. (2005) J. Biol. Chem. 280, 24824-24838
20. Mihaylova, V. T., Bindra, R. S., Yuan, J., Campisi, D., Narayanan, L., Jensen, R., Giordano, F., Johnson, R. S., Rockwell, S., and Glazer, P. M. (2003) Mol. Cell. Biol. 23, 3265-3273
21. Kim, M. S., Kwon, H. J., Lee, Y. M., Baek, J. H., Jang, J. E., Lee, S. W., Moon, E. J., Kim, H. S., Lee, S. K., Chung, H. Y., Kim, C. W., and Kim, K. W. (2001) Nat. Med. 7, 437-443
22. Islam, K. N., and Mendelson, C. R. (2006) Mol. Cell. Biol. 26, 2901-2912
23. Chen, H., Yan, Y., Davidson, T. L., Shinkai, Y., and Costa, M. (2006) Cancer Res. 66, 9009-9016
24. Li, Q., and Costa, M. (2009) Biochimie 91, 1307-1310
25. Marsden, P. A., Schappert, K. T., Chen, H. S., Flowers, M., Sundell, C. L., Wilcox, J. N., Lamas, S., and Michel, T. (1992) FEBS Lett. 307, 287-293
26. Guillemette, B., Bataille, A. R., Gévry, N., Adam, M., Blanchette, M., Robert, F., and Gaudreau, L. (2005) PLoS. Biol. 3, e384
27. Castaño, E., Gross, P., Wang, Z., Roeder, R. G., and Oelgeschläger, T. (2000) Proc. Natl. Acad. Sci. U.S.A. 97, 7184-7189
28. Lemos, F. B., Ijzermans, J. N., Zondervan, P. E., Peeters, A. M., van den Engel, S., Mol, W. M., Weimar, W., and Baan, C. C. (2003) J. Am. Soc. Nephrol. 14, 3278-3287
29. Robb, G. B., Carson, A. R., Tai, S. C., Fish, J. E., Singh, S., Yamada, T., Scherer, S. W., Nakabayashi, K., and Marsden, P. A. (2004) J. Biol. Chem. 279, 37982-37996
30. Chan, Y., Fish, J. E., D'Abreo, C., Lin, S., Robb, G. B., Teichert, A. M., Karantzoulis-Fegaras, F., Keightley, A., Steer, B. M., and Marsden, P. A. (2004) J. Biol. Chem. 279, 35087-35100
31. Karantzoulis-Fegaras, F., Antoniou, H., Lai, S. L., Kulkarni, G., D'Abreo, C., Wong, G. K., Miller, T. L., Chan, Y., Atkins, J., Wang, Y., and Marsden, P. A. (1999) J. Biol. Chem. 274, 3076-3093
32. Karimi, M., Johansson, S., Stach, D., Corcoran, M., Grandér, D., Schalling, M., Bakalkin, G., Lyko, F., Larsson, C., and Ekström, T. J. (2006) Exp. Cell Res. 312, 1989-1995
33. Rao, S., Procko, E., and Shannon, M. F. (2001) J. Immunol. 167, 4494-4503
34. Fish, J. E., Matouk, C. C., Yeboah, E., Bevan, S. C., Khan, M., Patil, K., Ohh, M., and Marsden, P. A. (2007) J. Biol. Chem. 282, 15652-15666
35. Phelan, M. W., and Faller, D. V. (1996) J. Cell. Physiol. 167, 469-476
36. Ward, M. E., Toporsian, M., Scott, J. A., Teoh, H., Govindaraju, V., Quan, A., Wener, A. D., Wang, G., Bevan, S. C., Newton, D. C., and Marsden, P. A. (2005) J. Clin. Invest. 115, 3128-3139
37. Coulet, F., Nadaud, S., Agrapart, M., and Soubrier, F. (2003) J. Biol. Chem. 278, 46230-46240
38. Bentley, D. (1999) Curr. Opin. Cell Biol. 11, 347-351
39. Batsché, E., Yaniv, M., and Muchardt, C. (2006) Nat. Struct. Mol. Biol. 13, 22-29
40. Tai, S. C., Robb, G. B., and Marsden, P. A. (2004) Arterioscler. Thromb. Vasc. Biol. 24, 405-412
41. Jung, J. E., Lee, H. G., Cho, I. H., Chung, D. H., Yoon, S. H., Yang, Y. M., Lee, J. W., Choi, S., Park, J. W., Ye, S. K., and Chung, M. H. (2005) FASEB J. 19, 1296-1298
42. Chan, G. C., Fish, J. E., Mawji, I. A., Leung, D. D., Rachlis, A. C., and Marsden, P. A. (2005) J. Immunol. 175, 3846-3861
43. Wellmann, S., Bettkober, M., Zelmer, A., Seeger, K., Faigle, M., Eltzschig, H. K., and Bührer, C. (2008) Biochem. Biophys. Res. Commun. 372, 892-897
44. Hu, C. J., Chen, S. D., Yang, D. I., Lin, T. N., Chen, C. M., Huang, T. H., and Hsu, C. Y. (2006) J. Cereb. Blood Flow Metab. 26, 1519-1526
45. Bindra, R. S., Schaffer, P. J., Meng, A., Woo, J., Måseide, K., Roth, M. E., Lizardi, P., Hedley, D. W., Bristow, R. G., and Glazer, P. M. (2004) Mol. Cell. Biol. 24, 8504-8518
46. Li, B., Pattenden, S. G., Lee, D., Gutiérrez, J., Chen, J., Seidel, C., Gerton, J., and Workman, J. L. (2005) Proc. Natl. Acad. Sci. U.S.A. 102, 18385-18390
47. Raisner, R. M., Hartley, P. D., Meneghini, M. D., Bao, M. Z., Liu, C. L., Schreiber, S. L., Rando, O. J., and Madhani, H. D. (2005) Cell 123, 233-248
48. Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., and Zhao, K. (2007) Cell 129, 823-837
49. Jin, C., Zang, C., Wei, G., Cui, K., Peng, W., Zhao, K., and Felsenfeld, G. (2009) Nat. Genet. 41, 941-945
50. Millar, C. B., Xu, F., Zhang, K., and Grunstein, M. (2006) Genes Dev. 20, 711-722
51. Harikrishnan, K. N., Chow, M. Z., Baker, E. K., Pal, S., Bassal, S., Brasacchio, D., Wang, L., Craig, J. M., Jones, P. L., Sif, S., and El-Osta, A. (2005) Nat. Genet. 37, 254-264
52. Coisy, M., Roure, V., Ribot, M., Philips, A., Muchardt, C., Blanchard, J. M., and Dantonel, J. C. (2004) Mol. Cell 15, 43-56
53. Baker, K. M., Wei, G., Schaffner, A. E., and Ostrowski, M. C. (2003) J. Biol. Chem. 278, 17876-17884
54. Wang, S., Zhang, B., and Faller, D. V. (2002) EMBO J. 21, 3019-3028
55. Murphy, D. J., Hardy, S., and Engel, D. A. (1999) Mol. Cell. Biol. 19, 2724-2733
56. Wilcox, J. N., Subramanian, R. R., Sundell, C. L., Tracey, W. R., Pollock, J. S., Harrison, D. G., and Marsden, P. A. (1997) Arterioscler. Thromb. Vasc. Biol. 17, 2479-2488
57. Pearson, D. L., Dawling, S., Walsh, W. F., Haines, J. L., Christman, B. W., Bazyk, A., Scott, N., and Summar, M. L. (2001) N. Engl. J. Med. 344, 1832-1838
58. Teichert, A. M., Miller, T. L., Tai, S. C., Wang, Y., Bei, X., Robb, G. B., Phillips, M. J., and Marsden, P. A. (2000) Am. J. Physiol. Heart Circ. Physiol. 278, H1352-1361
59. Gan, Y., Shen, Y. H., Wang, J., Wang, X., Utama, B., Wang, J., and Wang, X. L. (2005) J. Biol. Chem. 280, 16467-16475
60. Fish, J. E., and Marsden, P. A. (2006) Cell Mol Life Sci. 63, 144-162
61. Matouk, C. C., and Marsden, P. A. (2008) Circ. Res. 102, 873-887
62. Liu, Y., Cox, S. R., Morita, T., and Kourembanas, S. (1995) Circ. Res. 77, 638-643
63. Schioppa, T., Uranchimeg, B., Saccani, A., Biswas, S. K., Doni, A., Rapisarda, A., Bernasconi, S., Saccani, S., Nebuloni, M., Vago, L., Mantovani, A., Melillo, G., and Sica, A. (2003) J. Exp. Med. 198, 1391-1402
64. Ceradini, D. J., Kulkarni, A. R., Callaghan, M. J., Tepper, O. M., Bastidas, N., Kleinman, M. E., Capla, J. M., Galiano, R. D., Levine, J. P., and Gurtner, G. C. (2004) Nat. Med. 10, 858-864
65. Arany, Z., Huang, L. E., Eckner, R., Bhattacharya, S., Jiang, C., Goldberg, M. A., Bunn, H. F., and Livingston, D. M. (1996) Proc. Natl. Acad. Sci. U.S.A. 93, 12969-12973
66. Mahon, P. C., Hirota, K., and Semenza, G. L. (2001) Genes Dev. 15, 2675-2686
67. Li, Z., Wang, D., Na, X., Schoen, S. R., Messing, E. M., and Wu, G. (2003) EMBO J. 22, 1857-1867
68. Ozer, A., Wu, L. C., and Bruick, R. K. (2005) Proc. Natl. Acad. Sci. U.S.A. 102, 7481-7486
69. Flavin, M., Cappabianca, L., Kress, C., Thomassin, H., and Grange, T. (2004) Mol. Cell. Biol. 24, 7891-7901
70. Chen, X., Wang, J., Woltring, D., Gerondakis, S., and Shannon, M. F. (2005) Mol. Cell. Biol. 25, 3209-3219
71. Zhao, J., Herrera-Diaz, J., and Gross, D. S. (2005) Mol. Cell. Biol. 25, 8985-8999
72. Linger, J., and Tyler, J. K. (2006) Eukaryot. Cell 5, 1780-1787
73. Sobel, R. E., Cook, R. G., Perry, C. A., Annunziato, A. T., and Allis, C. D. (1995) Proc. Natl. Acad. Sci. U.S.A. 92, 1237-1241
74. Hammond, E. M., Denko, N. C., Dorie, M. J., Abraham, R. T., and Giaccia, A. J. (2002) Mol. Cell. Biol. 22, 1834-1843
75. Loyola, A., Bonaldi, T., Roche, D., Imhof, A., and Almouzni, G. (2006) Mol. Cell 24, 309-316
76. Jang, M. K., Mochizuki, K., Zhou, M., Jeong, H. S., Brady, J. N., and Ozato, K. (2005) Mol. Cell 19, 523-534
77. Martinez-Campa, C., Politis, P., Moreau, J. L., Kent, N., Goodall, J., Mellor, J., and Goding, C. R. (2004) Mol. Cell 15, 69-81
78. Peña, P. V., Davrazou, F., Shi, X., Walter, K. L., Verkhusha, V. V., Gozani, O., Zhao, R., and Kutateladze, T. G. (2006) Nature 442, 100-103
79. Wysocka, J., Swigut, T., Xiao, H., Milne, T. A., Kwon, S. Y., Landry, J., Kauer, M., Tackett, A. J., Chait, B. T., Badenhorst, P., Wu, C., and Allis, C. D. (2006) Nature 442, 86-90
80. Guccione, E., Martinato, F., Finocchiaro, G., Luzi, L., Tizzoni, L., Dall'Olio, V., Zardo, G., Nervi, C., Bernard, L., and Amati, B. (2006) Nat. Cell Biol. 8, 764-770
81. Strobeck, M. W., Knudsen, K. E., Fribourg, A. F., DeCristofaro, M. F., Weissman, B. E., Imbalzano, A. N., and Knudsen, E. S. (2000) Proc. Natl. Acad. Sci. U.S.A. 97, 7748-7753
82. Bazett-Jones, D. P., Côté, J., Landel, C. C., Peterson, C. L., and Workman, J. L. (1999) Mol. Cell. Biol. 19, 1470-1478
83. Roberts, C. W., and Orkin, S. H. (2004) Nat. Rev. Cancer 4, 133-142