Hypoxia, via stabilization of the hypoxia-inducible factor HIF-1α, is a direct and sufficient stimulus for brain-type natriuretic peptide induction

Biochemical Journal

Volumn 409, Issue 1, 2008, Pages 233-242

  Weidemann, Alexander ^a,b   Klanke, Bernd ^a   Wagner, Michael ^a   Volk, Tilmann ^a   Willam, Carsten ^a   Wiesener, Michael S ^a   Eckardt, Kai Uwe ^a   Warnecke, Christina ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain type natriuretic peptide; Heart failure; Hypoxia; Hypoxia inducible transcription factor; Hypoxia response element; Myocardial infarction

Indexed keywords

BIOASSAY; CELL CULTURE; DISEASES; HEMODYNAMICS; OXYGEN; PEPTIDES;

BRAIN-TYPE NATRIURETIC PEPTIDE; HEART FAILURE; HYPOXIA; HYPOXIA-INDUCIBLE TRANSCRIPTION FACTOR; HYPOXIA-RESPONSE ELEMENT; MYOCARDIAL INFARCTION;

HORMONES;

BRAIN NATRIURETIC PEPTIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; SMALL INTERFERING RNA; HIF1A PROTEIN, HUMAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; GEL MOBILITY SHIFT ASSAY; HEART FAILURE; HEART INFARCTION; HEART MUSCLE CELL; HEART PROTECTION; HUMAN; HUMAN CELL; HYPOXIA; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; RIBONUCLEASE PROTECTION ASSAY; ANIMAL; ANOXIA; CELL STRAIN 3T3; HEART MUSCLE; HEART MUSCLE ISCHEMIA; METABOLISM; PATHOLOGY; PROTEIN MOTIF; SPRAGUE DAWLEY RAT; WISTAR RAT;

RATTUS; RODENTIA;

3T3-L1 CELLS; AMINO ACID MOTIFS; ANIMALS; ANOXIA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MYOCARDIAL INFARCTION; MYOCARDIAL ISCHEMIA; MYOCARDIUM; NATRIURETIC PEPTIDE, BRAIN; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR;

EID: 38149110580     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20070629     Document Type: Article

References (49)

1. Grantham, J. A., Borgeson, D. D. and Burnett, Jr, J. C. (1997) BNP: pathophysiological and potential therapeutic roles in acute congestive heart failure. Am. J. Physiol. 272, B1077-B1083
2. Yamamoto, K., Burnett, Jr, J. C. and Redfield, M. M. (1997) Effect of endogenous natriuretic peptide system on ventricular and coronary function in failing heart. Am. J. Physiol. 273, H2406-H2414
3. Song, D. L., Kohse, K. P. and Murad, F. (1988) Brain natriuretic factor. Augmentation of cellular cyclic GMP, activation of particulate guanylate cyclase and receptor binding. FEBS Lett. 232, 125-129
4. Cao, L. and Gardner, D. G. (1995) Natriuretic peptides inhibit DNA synthesis in cardiac fibroblasts. Hypertension 25, 227-234
5. D'Souza, S. P., Yellon, D. M., Martin, C., Schulz, B., Heusch, G., Onody, A., Ferdinandy, P. and Baxter, G. F. (2003) B-type natriuretic peptide limits infarct size in rat isolated hearts via KATP channel opening. Am. J. Physiol. Heart Circ. Physiol. 284, H1592-H1600
6. Ikeda, M., Kohno, M., Yasunari, K., Yokokawa, K., Horio, T., Ueda, M., Morisaki, N. and Yoshikawa, J. (1997) Natriuretic peptide family as a novel antimigration factor of vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 17, 731-736
7. Tamura, N., Ogawa, Y., Chusho, H., Nakamura, K., Nakao, K., Suda, M., Kasahara, M., Hashimoto, R., Katsuura, G., Mukoyama, M. et al. (2000) Cardiac fibrosis in mice lacking brain natriuretic peptide. Proc. Natl. Acad. Sci. U.S.A. 97, 4239-4244
8. Kikuta, K., Yasue, H., Yoshimura, M., Morita, E., Sumida, H., Kato, H., Kugiyama, K., Ogawa, H., Okumura, K., Ogawa, Y. and Nakao, K. (1996) Increased plasma levels of B-type natriuretic peptide in patients with unstable angina. Am. Heart. J. 132, 101-107
9. Morita, E., Yasue, H., Yoshimura, M., Ogawa, H., Jougasaki, M., Matsumura, T., Mukoyama, M. and Nakao, K. (1993) Increased plasma levels of brain natriuretic peptide in patients with acute myocardial infarction. Circulation 88, 82-91
10. Mukoyama, M., Nakao, K., Saito, Y., Ogawa, Y., Hosoda, K., Suga, S., Shirakami, G., Jougasaki, M. and Imura, H. (1990) Increased human brain natriuretic peptide in congestive heart failure. N. Engl. J. Med. 323, 757-758
11. Liang, F., Wu, J., Garami, M. and Gardner, D. G. (1997) Mechanical strain increases expression of the brain natriuretic peptide gene in rat cardiac myocytes. J. Biol. Chem. 272, 28050-28056
12. Hama, N., Itoh, H., Shirakami, G., Nakagawa, O., Suga, S., Ogawa, Y., Masuda, I., Nakanishi, K., Yoshimasa, T., Hashimoto, Y. et al. (1995) Rapid ventricular induction of brain natriuretic peptide gene expression in experimental acute myocardial infarction. Circulation 92, 1558-1564
13. He, Q., Wang, D., Yang, X. P., Carretero, O. A. and LaPointe, M. C. (2001) Inducible regulation of human brain natriuretic peptide promoter in transgenic mice. Am. J. Physiol. Heart Circ. Physiol. 280, H368-H376
14. Hill, N. S., Klinger, J. R., Warburton, R. R., Pietras, L. and Wrenn, D. S. (1994) Brain natriuretic peptide: possible role in the modulation of hypoxic pulmonary hypertension. Am. J. Physiol. 266, L308-L315
15. Perhonen, M., Takala, T. E., Vuolteenaho, O., Mantymaa, P., Leppaluoto, J. and Ruskoaho, H. (1997) Induction of cardiac natriuretic peptide gene expression in rats trained in hypobaric hypoxic conditions. Am. J. Physiol. 273, R344-R352
16. Toth, M., Vuorinen, K. H., Vuolteenaho, O., Hassinen, I. E., Uusimaa, P. A., Leppaluoto, J. and Ruskoaho, H. (1994) Hypoxia stimulates release of ANP and BNP from perfused rat ventricular myocardium. Am. J. Physiol. 266, H1572-H1580
17. Goetze, J. P., Gore, A., Moller, C. H., Steinbruchel, D. A., Rehfeld, J. F. and Nielsen, L. B. (2004) Acute myocardial hypoxia increases BNP gene expression. FASEB J. 18, 1928-1930
18. Luo, Y., Jiang, C., Belanger, A., Akita, G., Wadsworth, S., Gregory, R. and Vincent, K. (2006) A constitutively active HIF-1α/VP16 hybrid factor activates expression of the human B-type natriuretic peptide gene. Mol. Pharmacol. 69, 1953-1962
19. Semenza, G. L. (1998) Hypoxia-inducible factor 1 and the molecular physiology of oxygen homeostasis. J. Lab. Clin. Med. 131, 207-214
20. 2-reguiated gene expression. FASEB J. 16, 1151-1162
21. Bruick, R. K. and McKnight, S. L. (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294, 1337-1340
22. Epstein, A. C., Gleadle, J. M., McNeill, L. A., Hewitson, K. S., O'Rourke, J., Mole, D. R., Mukherji, M. et al. (2001) C. elegans. EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43-54
23. 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) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271-275
24. Cai, Z., Manalo, D. J., Wei, G., Rodriguez, E. R., Fox-Talbot, K., Lu, H., Zweier, J. L. and Semenza, G. L. (2003) Hearts from rodents exposed to intermittent hypoxia or erythropoietin are protected against ischemia-reperfusion injury. Circulation 108, 79-85
25. Jurgensen, J. S., Rosenberger, C., Wiesener, M. S., Warnecke, C., Horstrup, J. H., Grafe, M., Philipp, S., Griethe, W., Maxwell, P. H., Frei, U. et al. (2004) Persistent induction of HIF-1α and -2α in cardiomyocytes and stromal cells of ischemic myocardium. FASEB J. 18, 1415-1417
26. Wiesener, M. S., Jurgensen, J. S., Rosenberger, C., Scholze, C. K., Horstrup, J. H., Warnecke, C., Mandriota, S., Bechmann, I., Frei, U. A., Pugh, C. W., Ratcliffe, P. J. et al. (2003) Widespread hypoxia-inducible expression of HIF-2α in distinct cell populations of different organs. FASEB J. 17, 271-273
27. Jiang, C., Lu, H., Vincent, K. A., Shankara, S., Belanger, A. J., Cheng, S. H., Akita, G. Y., Kelly, R. A., Goldberg, M. A. and Gregory, R. J. (2002) Gene expression profiles in human cardiac cells subjected to hypoxia or expressing a hybrid form of HIF-1α. Physiol. Genomics 8, 23-32
28. Wang, V., Davis, D. A., Haque, M., Huang, L. E. and Yarchoan, R. (2005) Differential gene up-regulation by hypoxia-inducible factor-1α and hypoxia-inducible factor-2α in HEK293T cells. Cancer Res 65, 3299-3306
29. Isenberg, G. and Klockner, U. (1982) Calcium tolerant ventricular myocytes prepared by preincubation in a "KB medium." Pflugers Arch. 395, 6-18
30. + currents among the left ventricular free wall of rats with ascending aortic stenosis. J. Physiol. 530, 443-455
31. Maxwell, P. H., Pugh, C. W. and Ratcliffe, P. J. (1993) Inducible operation of the erythropoietin 3′ enhancer in multiple cell lines: evidence for a widespread oxygen-sensing mechanism. Proc. Natl. Acad. Sci. U.S.A. 90, 2423-2427
32. Warnecke, C., Zaborowska, Z., Kurreck, J., Erdmann, V. A., Frei, U., Wiesener, M. and Eckardt, K. U. (2004) Differentiating the functional role of hypoxia-inducible factor (HIF)-1α and HIF-2α (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2α target gene in Hep3B and Kelly cells. FASEB J. 18, 1462-1464
33. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K. and Tuschl, T. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498
34. Warnecke, C., Griethe, W., Weidemann, A., Jurgensen, J. S., Willam, C., Bachmann, S., Ivashchenko, Y., Wagner, I., Frei, U., Wiesener, M. and Eckardt, K. U. (2003) Activation of the hypoxia-inducible factor-pathway and stimulation of angiogenesis by application of prolyl hydroxylase inhibitors. FASEB J. 17, 1186-1188
35. Rosenberger, C., Mandriota, S., Jurgensen, J. S., Wiesener, M. S., Horstrup, J. H., Frei, U., Ratcliffe, P. J., Maxwell, P. H., Bachmann, S. and Eckardt, K. U. (2002) Expression of hypoxia-inducible factor-1α and -2α in hypoxic and ischemic rat kidneys. J. Am. Soc. Nephrol. 13, 1721-1732
36. Lau, K. W., Tian, Y. M., Raval, R. R., Ratcliffe, P. J. and Pugh, C. W. (2007) Target gene selectivity of hypoxia-inducible factor-α in renal cancer cells is conveyed by post-DNA-binding mechanisms. Br. J. Cancer 96, 1284-1292
37. Semenza, G. L. and Wang, G. L. (1992) A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell. Biol. 12, 5447-5454
38. Willam, C., Maxwell, P. H., Nichols, L., Lygate, C., Tian, Y. M., Bernhardt, W., Wiesener, M., Ratcliffe, P. J., Eckardt, K. U. and Pugh, C. W. (2006) HIF prolyl hydroxylases in the rat; organ distribution and changes in expression following hypoxia and coronary artery ligation. J. Mol. Cell. Cardiol. 41, 68-77
39. Yin, Z., Haynie, J., Yang, X., Han, B., Kiatchoosakun, S., Restivo, J., Yuan, S., Prabhakar, N. R., Herrup, K., Conlon, R. A. et al. (2002) The essential role of Cited2, a negative regulator for HIF-1α, in heart development and neurulation. Proc. Natl. Acad. Sci. U.S.A. 99, 10488-10493
40. Harada, M., Saito, Y., Nakagawa, C., Miyamoto, Y., Ishikawa, M., Kuwahara, K., Ogawa, E., Nakayama, M., Kamitani, S., Hamanaka, I. et al. (1997) Role of cardiac nonmyocytes in cyclic mechanical stretch-induced myocyte hypertrophy. Heart Vessels Suppl 12, 198-200
41. Kim, C. H., Cho, Y. S., Chun, Y. S., Park, J. W. and Kim, M. S. (2002) Early expression of myocardial HIF-1α in response to mechanical stresses: regulation by stretch-activated channels and the phosphatidylinositol 3-kinase signaling pathway. Circ. Res. 90, E25-E33
42. Shyu, K. G., Lu, M. J., Chang, H., Sun, H. Y., Wang, B. W. and Kuan, P. (2005) Carvedilol modulates the expression of hypoxia-inducible factor-1α and vascular endothelial growth factor in a rat model of volume-overload heart failure. J. Card. Fail. 11, 152-159
43. Chang, H., Shyu, K. G., Wang, B. W. and Kuan, P. (2003) Regulation of hypoxia-inducible factor-1α by cyclical mechanical stretch in rat vascular smooth muscle cells. Clin. Sci. 105, 447-456
44. Tian, H., McKnight, S. L. and Russell, D. W. (1997) Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev. 11, 72-82
45. Chavez, J. C., Baranova, O., Lin, J. and Pichiule, P. (2006) The transcriptional activator hypoxia inducible factor 2 (HIF-2/EPAS-1) regulates the oxygen-dependent expression of erythropoietin in cortical astrocytes. J. Neurosci. 26, 9471-9481
46. Kimura, H., Weisz, A., Ogura, T., Hitomi, Y., Kurashima, Y., Hashimoto, K., D'Acquisto, F., Makuuchi, M. and Esumi, H. (2001) Identification of hypoxia-inducible factor 1 ancillary sequence and its function in vascular endothelial growth factor gene induction by hypoxia and nitric oxide. J. Biol. Chem. 276, 2292-2298
47. Yet, S. F., Perrella, M. A., Layne, M. D., Hsieh, C. M., Maemura, K., Kobzik, L., Wiesel, P., Christou, H., Kourembanas, S. and Lee, M. E. (1999) Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J. Clin. Invest. 103, R23-R29
48. Bernhardt, W. M., Campean, V., Kany, S., Jurgensen, J. S., Weidemann, A., Warnecke, C., Arend, M., Klaus, S., Gunzler, V., Amann, K. et al. (2006) Preconditional activation of hypoxia-inducible factors ameliorates ischemic acute renal failure. J. Am. Soc. Nephrol. 17, 1970-1978
49. Philipp, S., Jurgensen, J. S., Fielitz, J., Bernhardt, W. M., Weidemann, A., Schiche, A., Pilz, B., Dietz, R., Regitz-Zagrosek, V., Eckardt, K. U. and Willenbrock, R. (2006) Stabilization of hypoxia inducible factor rather than modulation of collagen metabolism improves cardiac function after acute myocardial infarction in rats. Eur. J. Heart. Fail. 8, 347-354