Hypoxia-inducible expression of a natural cis-antisense transcript inhibits endothelial nitric-oxide synthase

Journal of Biological Chemistry

Volumn 282, Issue 21, 2007, Pages 15652-15666

  Fish, Jason E ^a   Matouk, Charles C ^b   Yeboah, Elizabeth ^b   Bevan, Sian C ^a   Khan, Mukarram ^a   Patil, Kedar ^a   Ohh, Michael ^a   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

CIS-ANTISENSE TRANSCRIPT; HIPPEL-LINDAU PROTEIN; NORMOXIC CELLS; VASCULAR DISEASES;

ENDOTHELIAL CELLS; NITRIC OXIDE; PATHOGENS; PULMONARY DISEASES; RNA; TRANSCRIPTION; VIRUSES;

ENZYMES;

AUTOPHAGY 9 LIKE 2; COMPLEMENTARY RNA; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MESSENGER RNA; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN; ATG9B PROTEIN, HUMAN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN CONTAINING PROTEIN 1; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; MEMBRANE PROTEIN; NOS3 PROTEIN, HUMAN; VHL PROTEIN, HUMAN;

ANIMAL EXPERIMENT; AORTA; ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CELL STIMULATION; CONTROLLED STUDY; ENZYME REGULATION; GENE EXPRESSION; GENE INDUCTION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MALE; NONHUMAN; NUCLEIC ACID PROBE; POLYSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STABILITY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; UPREGULATION; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL HYPOXIA; ENDOTHELIUM CELL; ENZYMOLOGY; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PULMONARY HYPERTENSION; RNA STABILITY;

RATTUS;

ANIMALS; AORTA; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; CELL NUCLEUS; CELLS, CULTURED; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; HYPERTENSION, PULMONARY; MEMBRANE PROTEINS; NITRIC OXIDE SYNTHASE TYPE III; POLYRIBOSOMES; RATS; RNA STABILITY; RNA, ANTISENSE; RNA, MESSENGER; UP-REGULATION; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 34447543034     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M608318200     Document Type: Article

References (76)

1. Engstrom, P. G., Suzuki, H., Ninomiya, N., Akalin, A., Sessa, L., Lavorgna, G., Brozzi, A., Luzi, L., Tan, S. L., Yang, L., Kunarso, G., Ng, E. L., Batalov, S., Wahlestedt, C., Kai, C., Kawai, J., Carninci, P., Hayashizaki, Y., Wells, C., Bajic, V. B., Orlando, V., Reid, J. F., Lenhard, B., and Lipovich, L. (2006) PLoS Genet. 2, e47
2. Uchida, T., Rossignol, F., Matthay, M. A., Mounier, R., Couette, S., Clottes, E., and Clerici, C. (2004) J. Biol. Chem. 279, 14871-14878
3. Coudert, A. E., Pibouin, L., Vi-Fane, B., Thomas, B. L., Macdougall, M., Choudhury, A., Robert, B., Sharpe, P. T., Berdal, A., and Lezot, F. (2005) Nucleic Acids Res. 33, 5208-5218
4. Katayama, S., Tomaru, Y., Kasukawa, T., Waki, K., Nakanishi, M., Nakamura, M., Nishida, H., Yap, C. C., Suzuki, M., Kawai, J., Suzuki, H., Carninci, P., Hayashizaki, Y., Wells, C., Frith, M., Ravasi, T., Pang, K. C., Hallinan, J., Mattick, J., Hume, D. A., Lipovich, L., Batalov, S., Engstrom, P. G., Mizuno, Y., Faghihi, M. A., Sandelin, A., Chalk, A. M., Mottagui-Tabar, S., Liang, Z., Lenhard, B., and Wahlestedt, C. (2005) Science 309, 1564-1566
5. Sun, M., Hurst, L. D., Carmichael, G. G., and Chen, J. (2005) Nucleic Acids Res. 33, 5533-5543
6. Xie, X., Lu, J., Kulbokas, E. J., Golub, T. R., Mootha, V., Lindblad-Toh, K., Lander, E. S., and Kellis, M. (2005) Nature 434, 338-345
7. Wu, L., Fan, J., and Belasco, J. G. (2006) Proc. Natl. Acad. Sci. U. S. A. 103, 4034-4039
8. 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
9. McQuillan, L. P., Leung, G. K., Marsden, P. A., Kostyk, S. K., and Kourembanas, S. (1994) Am. J. Physiol. 267, H1921-H1927
10. Takemoto, M., Sun, J., Hiroki, J., Shimokawa, H., and Liao, J. K. (2002) Circulation 106, 57-62
11. Liao, J. K., Zulueta, J. J., Yu, F. S., Peng, H. B., Cote, C. G., and Hassoun, P. M. (1995) J. Clin. Invest. 96, 2661-2666
12. Tai, S. C., Robb, G. B., and Marsden, P. A. (2004) Arterioscler. Thromb. Vasc. Biol. 24, 405-412
13. Yang, E., van Nimwegen, E., Zavolan, M., Rajewsky, N., Schroeder, M., Magnasco, M., and Darnell, J. E., Jr. (2003) Genome Res. 13, 1863-1872
14. Alonso, J., Sanchez de Miguel, L., Monton, M., Casado, S., and Lopez-Farre, A. (1997) Mol. Cell. Biol. 17, 5719-5726
15. Sanchez de Miguel, L., Alonso, J., Gonzalez-Fernandez, F., de la Osada, J., Monton, M., Rodriguez-Feo, J. A., Guerra, J. I., Arriero, M. M., Rico, L., Casado, S., and Lopez-Farre, A. (1999) J. Vasc. Res. 36, 201-208
16. Searles, C. D., Miwa, Y., Harrison, D. G., and Ramasamy, S. (1999) Circ. Res. 85, 588-595
17. 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
18. Kibel, A., Iliopoulos, O., DeCaprio, J. A., and Kaelin, W. G., Jr. (1995) Science 269, 1444-1446
19. Kondo, K., Kim, W. Y., Lechpammer, M., and Kaelin, W. G., Jr. (2003) PLoS Biol. 1, E83
20. Das, R., Dufu, K., Romney, B., Feldt, M., Elenko, M., and Reed, R. (2006) Genes Dev. 20, 1100-1109
21. 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
22. Livak, K. J., and Schmittgen, T. D. (2001) Methods 25, 402-408
23. 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
24. Wang, Y., Goligorsky, M. S., Lin, M., Wilcox, J. N., and Marsden, P. A. (1997) J. Biol. Chem. 272, 11392-11401
25. Taha, C., Liu, Z., Jin, J., Al-Hasani, H., Sonenberg, N., and Klip, A. (1999) J. Biol. Chem. 274, 33085-33091
26. Wang, G. L., and Semenza, G. L. (1993) Blood 82, 3610-3615
27. Gleadle, J. M., Ebert, B. L., Firth, J. D., and Ratcliffe, P. J. (1995) Am. J. Physiol. 268, C1362-C1368
28. Coulet, F., Nadaud, S., Agrapart, M., and Soubrier, F. (2003) J. Biol. Chem. 278, 46230-46240
29. Chi, J. T., Wang, Z., Nuyten, D. S., Rodriguez, E. H., Schaner, M. E., Salim, A., Wang, Y., Kristensen, G. B., Helland, A., Borresen-Dale, A. L., Giaccia, A., Longaker, M. T., Hastie, T., Yang, G. P., Vijver, M. J., and Brown, P. O. (2006) PLoS Med. 3, e47
30. Toporsian, M., Govindaraju, K., Nagi, M., Eidelman, D., Thibault, G., and Ward, M. E. (2000) Circ. Res. 86, 671-675
31. Shih, S. C., and Claffey, K. P. (1998) Int. J. Exp. Pathol. 79, 347-357
32. Batsche, E., Yaniv, M., and Muchardt, C. (2006) Nat. Struct. Mol. Biol. 13, 22-29
33. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R., and Ratcliffe, P. J. (1999) Nature 399, 271-275
34. Ohh, M., Park, C. W., Ivan, M., Hoffman, M. A., Kim, T. Y., Huang, L. E., Pavletich, N., Chau, V., and Kaelin, W. G. (2000) Nat. Cell Biol. 2, 423-427
35. Stratmann, R., Krieg, M., Haas, R., and Plate, K. H. (1997) J Neuropathol. Exp. Neurol. 56, 1242-1252
36. Nakamura, E., Abreu-e-Lima, P., Awakura, Y., Inoue, T., Kamoto, T., Ogawa, O., Kotani, H., Manabe, T., Zhang, G. J., Kondo, K., Nose, V., and Kaelin, W. G., Jr. (2006) Am. J. Pathol. 168, 574-584
37. Calzada, M. J., Esteban, M. A., Feijoo-Cuaresma, M., Castellanos, M. C., Naranjo-Suarez, S., Temes, E., Mendez, F., Yanez-Mo, M., Ohh, M., and Landazuri, M. O. (2006) Cancer Res. 66, 1553-1560
38. Hoffman, M. A., Ohh, M., Yang, H., Klco, J. M., Ivan, M., and Kaelin, W. G., Jr. (2001) Hum. Mol. Genet. 10, 1019-1027
39. Carroll, V. A., and Ashcroft, M. (2006) Cancer Res. 66, 6264-6270
40. Liu, Y., Cox, S. R., Morita, T., and Kourembanas, S. (1995) Circ. Res. 77, 638-643
41. 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
42. Buhler, M., Wilkinson, M. F., and Muhlemann, O. (2002) EMBO Rep. 3, 646-651
43. Muhlemann, O., Mock-Casagrande, C. S., Wang, J., Li, S., Custodio, N., Carmo-Fonseca, M., Wilkinson, M. F., and Moore, M. J. (2001) Mol. Cell 8, 33-43
44. Kiyosawa, H., Mise, N., Iwase, S., Hayashizaki, Y., and Abe, K. (2005) Genome Res. 15, 463-474
45. DeCerbo, J., and Carmichael, G. G. (2005) Curr. Opin. Cell Biol. 17, 302-308
46. Shweiki, D., Itin, A., Soffer, D., and Keshet, E. (1992) Nature 359, 843-845
47. Graven, K. K., Troxler, R. F., Kornfeld, H., Panchenko, M. V., and Farber, H. W. (1994) J. Biol. Chem. 269, 24446-24453
48. 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., McMurtry, I. F., and Rodman, D. M. (1999) J. Clin. Invest. 103, 291-299
49. Steudel, W., Scherrer-Crosbie, M., Bloch, K. D., Weimann, J., Huang, P. L., Jones, R. C., Picard, M. H., and Zapol, W. M. (1998) J. Clin. Invest. 101, 2468-2477
50. 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
51. 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
52. Levy, N. S., Chung, S., Furneaux, H., and Levy, A. P. (1998) J. Biol. Chem. 273, 6417-6423
53. Datta, K., Mondal, S., Sinha, S., Li, J., Wang, E., Knebelmann, B., Karumanchi, S. A., and Mukhopadhyay, D. (2005) Oncogene 24, 7850-7858
54. Fan, X. C., and Steitz, J. A. (1998) EMBO J. 17, 3448-3460
55. Stebbins, C. E., Kaelin, W. G., Jr., and Pavletich, N. P. (1999) Science 284, 455-461
56. Yamada, T., Carson, A. R., Caniggia, I., Umebayashi, K., Yoshimori, T., Nakabayashi, K., and Scherer, S. W. (2005) J. Biol. Chem. 280, 18283-18290
57. Mitchener, J. S., Shelburne, J. D., Bradford, W. D., and Hawkins, H. K. (1976) Am. J. Pathol. 83, 485-491
58. Decker, R. S., and Wildenthal, K. (1980) Am. J. Pathol. 98, 425-444
59. Nelson, P. T., Hatzigeorgiou, A. G., and Mourelatos, Z. (2004) RNA 10, 387-394
60. Kim, J., Krichevsky, A., Grad, Y., Hayes, G. D., Kosik, K. S., Church, G. M., and Ruvkun, G. (2004) Proc. Natl. Acad. Sci. U. S. A. 101, 360-365
61. Petersen, C. P., Bordeleau, M. E., Pelletier, J., and Sharp, P. A. (2006) Mol. Cell 21, 533-542
62. Lehner, B., Williams, G., Campbell, R. D., and Sanderson, C. M. (2002) Trends Genet. 18, 63-65
63. Weber, M., Hagedorn, C. H., Harrison, D. G., and Searles, C. D. (2005) Circ. Res. 96, 1161-1168
64. Yoshizumi, M., Perrella, M. A., Burnett, J. C., Jr., and Lee, M. E. (1993) Circ. Res. 73, 205-209
65. Ubeda, M., Schmitt-Ney, M., Ferrer, J., and Habener, J. F. (1999) Biochem. Biophys. Res. Commun. 262, 31-38
66. McManus, M. T., and Sharp, P. A. (2002) Nat. Rev. Genet. 3, 737-747
67. Borsani, O., Zhu, J., Verslues, P. E., Sunkar, R., and Zhu, J. K. (2005) Cell 123, 1279-1291
68. Aravin, A. A., Lagos-Quintana, M., Yalcin, A., Zavolan, M., Marks, D., Snyder, B., Gaasterland, T., Meyer, J., and Tuschl, T. (2003) Dev. Cell 5, 337-350
69. Aravin, A., and Tuschl, T. (2005) FEBS Lett. 579, 5830-5840
70. Yang, N., and Kazazian, H. H., Jr. (2006) Nat. Struct. Mol. Biol. 13, 763-771
71. Faghihi, M. A., and Wahlestedt, C. (2006) Genome. Biol. 7, R38
72. Robertson, H. D., and Mathews, M. B. (1996) Biochimie (Paris) 78, 909-914
73. Wouters, B. G., van den Beucken, T., Magagnin, M. G., Koritzinsky, M., Fels, D., and Koumenis, C. (2005) Semin. Cell Dev. Biol. 16, 487-501
74. Berezhna, S. Y., Supekova, L., Supek, F., Schultz, P. G., and Deniz, A. A. (2006) Proc. Natl. Acad. Sci. U. S. A. 103, 7682-7687
75. Robb, G. B., Brown, K. M., Khurana, J., and Rana, T. M. (2005) Nat. Struct. Mol. Biol. 12, 133-137
76. Valencia-Sanchez, M. A., Liu, J., Hannon, G. J., and Parker, R. (2006) Genes Dev. 20, 515-524