Peroxisome proliferator-activated receptor-α-mediated transcription of miR-199a2 attenuates endothelin-1 Expression via Hypoxia-inducible Factor-1α

Journal of Biological Chemistry

Volumn 289, Issue 52, 2014, Pages 36031-36047

  Li, Chen ^a   Mpollo, Marthe Srine Eiymo Mwa ^b   Gonsalves, Caryn S ^a   Tahara, Stanley M ^a   Malik, Punam ^b   Kalra, Vijay K ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION;

ERYTHROID PRECURSOR CELLS; HYPOXIA-INDUCIBLE FACTOR 1; MEDIATED TRANSCRIPTION; MOLECULAR LINKS; MUTATIONAL ANALYSIS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; PULMONARY HYPERTENSION; SICKLE CELL DISEASE;

ENDOTHELIAL CELLS;

DYNAMIN; DYNAMIN 3 OPPOSITE STRAND; ENDOTHELIN 1; FENOFIBRATE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; MICRORNA; MICRORNA 199A2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PLACENTAL GROWTH FACTOR; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; DYNAMIN III; HIF1A PROTEIN, HUMAN; MIRN199 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VIVO STUDY; MUTATION; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; SICKLE CELL ANEMIA; TRANSCRIPTION REGULATION; ANIMAL; BINDING SITE; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RNA INTERFERENCE;

MUS;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; BINDING SITES; CELLS, CULTURED; DYNAMIN III; ENDOTHELIN-1; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE, INBRED C57BL; MICRORNAS; MOLECULAR SEQUENCE DATA; PPAR ALPHA; RNA INTERFERENCE; TRANSCRIPTION, GENETIC;

EID: 84919783875     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.600775     Document Type: Article

References (48)

1. Kedzierski, R. M., and Yanagisawa, M. (2001) Endothelin system: the dou-ble-edged sword in health and disease. Annu. Rev. Pharmacol. Toxicol. 41, 851-876
2. Kisanuki, Y. Y., Emoto, N., Ohuchi, T., Widyantoro, B., Yagi, K., Nakayama, K., Kedzierski, R. M., Hammer, R. E., Yanagisawa, H., Williams, S. C., Richardson, J. A., Suzuki, T., and Yanagisawa, M. (2010) Low blood pressure in endothelial cell-specific endothelin 1 knockout mice. Hypertension 56, 121-128
3. Gladwin, M. T., Sachdev, V., Jison, M. L., Shizukuda, Y., Plehn, J. F., Minter, K., Brown, B., Coles, W. A., Nichols, J. S., Ernst, I., Hunter, L. A., Blackwelder, W. C., Schechter, A. N., Rodgers, G. P., Castro, O., and Ognibene, F. P. (2004) Pulmonary hypertension as a risk factor for death in patients with sickle cell disease. New Engl. J. Med. 350, 886-895
4. Minniti, C. P., Machado, R. F., Coles, W. A., Sachdev, V., Gladwin, M. T., and Kato, G. J. (2009) Endothelin receptor antagonists for pulmonary hypertension in adult patients with sickle cell disease. Br. J. Haematol. 147, 737-743
5. Klings, E. S. (2008) Pulmonary hypertension of sickle cell disease: more than just another lung disease. Am. J. Hematol. 83, 4-5
6. Ataga, K. I., Moore, C. G., Hillery, C. A., Jones, S., Whinna, H. C., Strayhorn, D., Sohier, C., Hinderliter, A., Parise, L. V., and Orringer E. P. (2008) Coagulation activation and inflammation in sickle cell disease-associated pulmonary hypertension. Haematologica 93, 20-26
7. Morris, C. R., Suh, J. H., Hagar, W., Larkin, S., Bland, D. A., Steinberg, M. H., Vichinsky, E. P., Shigenaga, M., Ames, B., Kuypers, F. A., and Klings, E. S. (2008) Erythrocyte glutamine depletion, altered redox environment, and pulmonary hypertension in sickle cell disease. Blood 111, 402-410
8. Miller, A. C., and Gladwin, M. T. (2012) Pulmonary complications of sickle cell disease. Am. J. Respir. Crit. Care Med. 185, 1154-1165
9. Zhang, X., Zhang, W., Ma, S.-F., Desai, A. A., Saraf, S., Miasniakova, G., Sergueeva, A., Ammosova, T., Xu, M., Nekhai, S., Abbasi, T., Casanova, N. G., Steinberg, M. H., Baldwin, C. T., Sebastiani, P., Prchal, J. T., Kittles, R., Garcia, J. G., Machado, R. F., and Gordeuk, V. R. (2014) Hypoxic re-sponse contributes to altered gene expression and precapillary pulmonary hypertension in patients with sickle cell disease. Circulation 129, 1650-1658
10. Klings, E. S., Machado, R. F., Barst, R. J., Morris, C. R., Mubarak, K. K., Gordeuk, V. R., Kato, G. J., Ataga, K. I., Gibbs, J. S., Castro, O., Rosenzweig, E. B., Sood, N., Hsu, L., Wilson, K. C., Telen, M. J., Decastro, L. M., Krishnamurti, L., Steinberg, M. H., Badesch, D. B., and Gladwin, M. T. (2014) An official american thoracic society clinical practice guideline: diagnosis, risk stratification, and management of pulmonary hypertension of sickle cell disease. Am. J. Respir. Crit. Care Med. 189, 727-740
11. Hsu, L. L., Champion, H. C., Campbell-Lee, S. A., Bivalacqua, T. J., Manci, E. A., Diwan, B. A., Schimel, D. M., Cochard, A. E., Wang, X., Schechter, A. N., Noguchi, C. T., and Gladwin, M. T. (2007) Hemolysis in sickle cell mice causes pulmonary hypertension due to global impairment in nitric oxide bioavailability. Blood 109, 3088-3098
12. Bunn, H. F., Nathan, D. G., Dover, G. J., Hebbel, R. P., Platt, O. S., Rosse, W. F., and Ware, R. E. (2010) Pulmonary hypertension and nitric oxide depletion in sickle cell disease. Blood 116, 687-692
13. Wood, K. C., Cortese-Krott, M. M., Kovacic, J. C., Noguchi, A., Liu, V. B., Wang, X., Raghavachari, N., Boehm, M., Kato, G. J., Kelm, M., and Gladwin, M. T. (2013) Circulating blood endothelial nitric oxide synthase contributes to the regulation of systemic blood pressure and nitrite homeostasis. Arterioscler. Thromb. Vasc. Biol. 33, 1861-1871
14. Nouraie, M., Lee, J. S., Zhang, Y., Kanias, T., Zhao, X., Xiong, Z., Oriss, T. B., Zeng, Q., Kato, G. J., Gibbs, J. S., Hildesheim, M. E., Sachdev, V., Barst, R. J., Machado, R. F., Hassell, K. L., Little, J. A., Schraufnagel, D. E., Krishnamurti, L., Novelli, E., Girgis, R. E., Morris, C. R., Rosenzweig, E. B., Badesch, D. B., Lanzkron, S., Castro, O. L., Goldsmith, J. C., Gordeuk, V. R., and Gladwin, M. T. (2013) The relationship between the severity of hemolysis, clinical manifestations and risk of death in 415 patients with sickle cell anemia in the US and Europe. Haematologica 98, 464-472
15. Rybicki, A. C., and Benjamin, L. J. (1998) Increased levels of endothelin-1 in plasma of sickle cell anemia patients. Blood 92, 2594-2596
16. Sundaram, N., Tailor, A., Mendelsohn, L., Wansapura, J., Wang, X., Higashimoto, T., Pauciulo, M. W., Gottliebson, W., Kalra, V. K., Nichols, W. C., Kato, G. J., and Malik, P. (2010) High levels of placenta growth factor in sickle cell disease promote pulmonary hypertension. Blood 116, 109-112
17. Shao, D., Park, J. E., and Wort, S. J. (2011) The role of endothelin-1 in the pathogenesis of pulmonary arterial hypertension. Pharmacol. Res. 63, 504-511
18. Yamashita, K., Discher, D. J., Hu, J., Bishopric, N. H., and Webster, K. A. (2001) Molecular regulation of the endothelin-1 gene by hypoxia: contributions of hypoxia-inducible factor-1, activator protein-1, GATA-2,AND p300/CBP. J. Biol. Chem. 276, 12645-12653
19. Patel, N., Gonsalves, C. S., Malik, P., and Kalra, V. K. (2008) Placenta growth factor augments endothelin-1 and endothelin-B receptor expression via hypoxia-inducible factor-1α. Blood 112, 856-865
20. Perelman, N., Selvaraj, S. K., Batra, S., Luck, L. R., Erdreich-Epstein, A., Coates, T. D., Kalra, V. K., and Malik, P. (2003) Placenta growth factor activates monocytes and correlates with sickle cell disease severity. Blood 102, 1506-1514
21. Patel, N., Tahara, S. M., Malik, P., and Kalra, V. K. (2011) Involvement of miR-30c and miR-301a in immediate induction of plasminogen activator inhibitor-1by placenta growth factor in human pulmopnary endothelial cells. Biochem. J. 434, 473-482
22. Ding, G., Huang, G., Liu, H.-D., Liang, H.-X., Ni, Y.-F., Ding, Z.-H., Ni, G.-Y., and Hua, H. W. (2013) MiR-199a suppresses the hypoxia-induced proliferation of non-small cell lung cancer cells through targeting HIF1α. Mol. Cell Biochem. 384, 173-180
23. Loebel, D. A., Tsoi, B., Wong, N., and Tam, P. P. (2005) A conserved noncoding intronic transcript at the mouse Dnm3 locus. Genomics 85, 782-789
24. el Azzouzi, H., Leptidis, S., Dirkx, E., Hoeks, J., van Bree, B., Brand, K., McClellan, E. A., Poels, E., Sluimer, J. C., van den Hoogenhof, M. M., Armand, A.-S., Yin, X., Langley, S., Bourajjaj, M., Olieslagers, S., Krishnan, J., Vooijs, M., Kurihara, H., Stubbs, A., Pinto, Y. M., Krek, W., Mayr, M., da Costa Martins, P. A., Schrauwen, P., and De Windt, L. J. (2013) The hy-poxia-inducible microRNA cluster miR-199a∼214 targets myocardial PPARδ and impairs mitochondrial fatty acid oxidation. Cell Metab. 18, 341-354
25. Glineur, C., Gross, B., Neve, B., Rommens, C., Chew, G. T., Martin-Nizard, F., Rodríguez-Pascual, F., Lamas, S., Watts, G. F., and Staels, B. (2013) Fenofibrate inhibits endothelin-1 expression by peroxisome proliferatoractivated receptor α-dependent and independent mechanisms in human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 33, 621-628
26. Pászty, C., Brion, C. M., Manci, E., Witkowska, H. E., Stevens, M. E., Mohandas, N., and Rubin, E. M. (1997) Transgenic knockout mice with exclusively human sickle hemoglobin and sickle cell disease. Science 278, 876-878
27. Patel, N., Sundaram, N., Yang, M., Madigan, C., Kalra, V. K., and Malik, P. (2010) Placenta Growth Factor (PlGF), a novel inducer of plasminogen activator inhibitor-1 (PAI-1) in sickle cell disease (SCD). J. Biol. Chem. 285, 16713-16722
28. Kim, K. S., Rajagopal, V., Gonsalves, C., Johnson, C., and Kalra, V. K. (2006) A novel role of hypoxia-inducible factor in cobalt chloride- and hypoxia-mediated expression of IL-8 chemokine in human endothelial cells. J. Immunol. 177, 7211-7224
29. Patel, N., Gonsalves, C. S., Yang, M., Malik, P., and Kalra, V. K. (2009) Placenta growth factor induces 5-lipoxygenase-activating protein to increase leukotriene formation in sickle cell disease. Blood 113, 1129-1138
30. Lin, M., Chamoto, K., Gibney, B. C., Lee, G. S., Collings-Simpson, D., Houdek, J., Konerding, M. A., Tsuda, A., and Mentzer, S. J. (2011) Angiogenesis gene expression in murine endothelial cells during post-pneumonectomy lung growth. Respir. Res. 12, 98
31. Kang, J., Ramu, S., Lee, S., Aguilar, B., Ganesan, S. K., Yoo, J., Kalra, V. K., Koh, C. J., and Hong, Y. K. (2009) Phosphate-buffered saline-based nucleofection of primary endothelial cells. Anal. Biochem. 386, 251-255
32. Giri, R. K., Selvaraj, S. K., and Kalra, V. K. (2003) Amyloid peptide-induced cytokine and chemokine expression in THP-1 monocytes is blocked by small inhibitory RNA duplexes for early growth response-1 messenger RNA. J. Immunol. 170, 5281-5294
33. Lee, Y.-B., Bantounas, I., Lee, D.-Y., Phylactou, L., Caldwell, M. A., and Uney, J. B. (2009) Twist-1 regulates the miR-199a/214 cluster during development. Nucleic Acids Res. 37, 123-128
34. Semenza, G. L. (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148, 399-408
35. Pereira, E. R., Frudd, K., Awad, W., and Hendershot, L. M. (2014) Endoplasmic reticulum (ER) stress and hypoxia response pathways interact to potentiate hypoxia-inducible factor 1 (HIF-1) transcriptional activity on targets like vascular endothelial growth factor (VEGF). J. Biol. Chem. 289, 3352-3364
36. Gervois, P., Fruchart, J. C., and Staels, B. (2007) Drug Insight: mechanisms of action and therapeutic applications for agonists of peroxisome prolif-erator-activated receptors. Nat. Clin. Pract. Endocrinol. Metab. 3, 145-156
37. Zhou, J., Zhang, S., Xue, J., Avery, J., Wu, J., Lind, S. E., and Ding, W. Q. (2012) Activation of peroxisome proliferator-activated receptor α (PPARα) suppresses hypoxia-inducible factor-1α (HIF-1α) signaling in cancer cells. J. Biol. Chem. 287, 35161-35169
38. Hu, J., Discher, D. J., Bishopric, N. H., and Webster, K. A. (1998) Hypoxia regulates expression of the endothelin-1 gene through a proximal hypox-ia-inducible factor-1 binding site on the antisense strand. Biochem. Biophys. Res. Commun. 245, 894-899
39. Rane, S., He, M., Sayed, D., Vashistha, H., Malhotra, A., Sadoshima, J., Vatner, D. E., Vatner, S. F., and Abdellatif, M. (2009) Downregulation of miR-199a derepresses hypoxia-inducible factor-1α and sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circ. Res. 104, 879-886
40. Nallamshetty, S., Chan, S. Y., and Loscalzo, J. (2013) Hypoxia: a master regulator of microRNA biogenesis and activity. Free Radical Biol. Med. 64, 20-30
41. Gonsalves, C. S., and Kalra, V. K. (2010) Hypoxia-mediated expression of 5-lipoxygenase-activating protein involves HIF-1α and NF-κB and microRNAs 135a and 199a-5p. J. Immunol. 184, 3878-3888
42. Watanabe, T., Sato, T., Amano, T., Kawamura, Y., Kawamura, N., Kawa-guchi, H., Yamashita, N., Kurihara, H., and Nakaoka, T. (2008) Dnm3os, a non-coding RNA, is required for normal growth and skeletal development in mice. Dev. Dyn. 237, 3738-3748
43. Desvignes, T., Contreras, A., and Postlethwait, J. H. (2014) Evolution of the miR199-214 cluster and vertebrate skeletal development. RNA Biol. 11, 281-294
44. Kourembanas, S., Marsden, P. A., McQuillan, L. P., and Faller, D. V. (1991) Hypoxia induces endothelin gene expression and secretion in cultured human endothelium. J. Clin. Invest. 88, 1054-1057
45. Delerive, P., Martin-Nizard, F., Chinetti, G., Trottein, F., Fruchart, J.-C., Najib, J., Duriez, P., and Staels, B. (1999) Peroxisome proliferator-activated receptor activators inhibit thrombin-induced endothelin-1 production in human vascular endothelial cells by inhibiting the activator protein-1 signaling pathway. Circ. Res. 85, 394-402
46. Lalloyer, F., and Staels, B. (2010) Fibrates, glitazones, and peroxisome proliferator-activated receptors. Arterioscler. Thromb. Vasc. Biol. 30, 894-899
47. Chen, Y., Hu, Y., Lin, M., Jenkins, A. J., Keech, A. C., Mott, R., Lyons, T. J., and Ma, J. X. (2013) Therapeutic effects of PPARα agonists on diabetic retinopathy in type 1 diabetes models. Diabetes 62, 261-272
48. Gonsalves, C. S., Eiymo Mwa Mpollo, M.-S., Malik, P., Tahara, S. M., and Kalra, V. K. (2014) miR-648 targets ET-1 mRNA and is co-transcriptionally regulated with MICAL3 by PAX5. Mol. Cell. Biol. 10.1128/MCB.01199-14