Hypoxia induces downregulation of soluble guanylyl cyclase β1 by miR-34c-5p

Journal of Cell Science

Volumn 125, Issue 24, 2012, Pages 6117-6126

  Xu, Xiaojian ^a   Wang, Shumin ^b   Liu, Juan ^a   Dou, Dou ^a,c   Liu, Limei ^a,c   Chen, Zhengju ^a   Ye, Liping ^a   Liu, Huixia ^a   He, Qiong ^a   Raj, J Usha ^d   Gao, Yuansheng ^a,c  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b INSTITUTE OF ZOOLOGY   (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^d UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Hypoxia; MicroRNA; MiR 34c 5p; Soluble guanylyl cyclase

Indexed keywords

GUANYLATE CYCLASE; GUANYLYL CYCLASE BETA1; LUCIFERASE; MICRORNA; MICRORNA 34B; MICRORNA 34C; NITRIC OXIDE; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG; CELL RECEPTOR; MIRN34 MICRORNA, HUMAN; PROTEIN SUBUNIT; SOLUBLE GUANYLYL CYCLASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL STRAIN HEK293; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HEART; HYPOXIA; KIDNEY; LUNG PARENCHYMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; REAL TIME POLYMERASE CHAIN REACTION; SITE DIRECTED MUTAGENESIS; UPREGULATION; WESTERN BLOTTING; WILD TYPE; ANIMAL; CELL CULTURE; CELL HYPOXIA; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; CYTOLOGY; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN SUBUNIT; RANDOMIZATION; VASCULAR SMOOTH MUSCLE;

LENTIVIRUS;

ANIMALS; CELL HYPOXIA; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; DOWN-REGULATION; FEMALE; GUANYLATE CYCLASE; HEK293 CELLS; HUMANS; MICE; MICRORNAS; MUSCLE, SMOOTH, VASCULAR; PROTEIN SUBUNITS; RANDOM ALLOCATION; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84875630156     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.113381     Document Type: Article

References (66)

1. Abdellatif, M. (2012). Differential expression of microRNAs in different disease states. Circ. Res. 110, 638-650.
2. Aranha, M. M., Santos, D. M., Solá , S., Steer, C. J. and Rodrigues, C. M. (2011). miR-34a regulates mouse neural stem cell differentiation. PLoS ONE 6, e21396.
3. Bae, Y., Yang, T., Zeng, H. C., Campeau, P. M., Chen, Y., Bertin, T., Dawson, B. C., Munivez, E., Tao, J. and Lee, B. H. (2012). miRNA-34c regulates Notch signaling during bone development. Hum. Mol. Genet. 21, 2991-3000.
4. Bauersachs, J., Bouloumié, A., Fraccarollo, D., Hu, K., Busse, R. and Ertl, G. (1999). Endothelial dysfunction in chronic myocardial infarction despite increased vascular endothelial nitric oxide synthase and soluble guanylate cyclase expression: role of enhanced vascular superoxide production. Circulation 100, 292-298.
5. Bouhallier, F., Allioli, N., Lavial, F., Chalmel, F., Perrard, M. H., Durand, P., Samarut, J., Pain, B. and Rouault, J. P. (2010). Role of miR-34c microRNA in the late steps of spermatogenesis. RNA 16, 720-731.
6. Cannell, I. G., Kong, Y. W., Johnston, S. J., Chen, M. L., Collins, H. M., Dobbyn, H. C., Elia, A., Kress, T. R., Dickens, M., Clemens, M. J. et al. (2010). p38 MAPK/ MK2-mediated induction of miR-34c following DNA damage prevents Mycdependent DNA replication. Proc. Natl. Acad. Sci. USA 107, 5375-5380.
7. Cardinaud, B., Moreilhon, C., Marcet, B., Robbe-Sermesant, K., LeBrigand, K., Mari, B., Eclache, V., Cymbalista, F., Raynaud, S. and Barbry, P. (2009). miR- 34b/miR-34c: a regulator of TCL1 expression in 11q- chronic lymphocytic leukaemia?. Leukemia 23, 2174-2177.
8. Carlsbecker, A., Lee, J. Y., Roberts, C. J., Dettmer, J., Lehesranta, S., Zhou, J., Lindgren, O., Moreno-Risueno, M. A., Vatén, A., Thitamadee, S. et al. (2010). Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465, 316-321.
9. Caruso, P., MacLean, M. R., Khanin, R., McClure, J., Soon, E., Southgate, M., MacDonald, R. A., Greig, J. A., Robertson, K. E., Masson, R. et al. (2010). Dynamic changes in lung microRNA profiles during the development of pulmonary hypertension due to chronic hypoxia and monocrotaline. Arterioscler. Thromb. Vasc. Biol. 30, 716-723.
10. Chan, R. W., Chan, M. C., Wong, A. C., Karamanska, R., Dell, A., Haslam, S. M., Sihoe, A. D., Chui, W. H., Triana-Baltzer, G., Li, Q. et al. (2009). DAS181 inhibits H5N1 influenza virus infection of human lung tissues. Antimicrob. Agents Chemother. 53, 3935-3941.
11. Choi, Y. J., Lin, C. P., Ho, J. J., He, X., Okada, N., Bu, P., Zhong, Y., Kim, S. Y., Bennett, M. J., Chen, C. et al. (2011). miR-34 miRNAs provide a barrier for somatic cell reprogramming. Nat. Cell Biol. 13, 1353-1360.
12. Corney, D. C., Flesken-Nikitin, A., Godwin, A. K., Wang, W. and Nikitin, A. Y. (2007). MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res. 67, 8433- 8438.
13. Courboulin, A., Paulin, R., Giguére, N. J., Saksouk, N., Perreault, T., Meloche, J., Paquet, E. R., Biardel, S., Provencher, S., Côté, J. et al. (2011). Role for miR-204 in human pulmonary arterial hypertension. J. Exp. Med. 208, 535-548.
14. Deng, M., Tang, H., Zhou, Y., Zhou, M., Xiong, W., Zheng, Y., Ye, Q., Zeng, X., Liao, Q., Guo, X. et al. (2011). miR-216b suppresses tumor growth and invasion by targeting KRAS in nasopharyngeal carcinoma. J. Cell Sci. 124, 2997-3005.
15. Du, C., Liu, C., Kang, J., Zhao, G., Ye, Z., Huang, S., Li, Z., Wu, Z. and Pei, G. (2009). MicroRNA miR-326 regulates TH-17 differentiation and is associated with the pathogenesis of multiple sclerosis. Nat. Immunol. 10, 1252-1259.
16. Ebert, M. S., Neilson, J. R. and Sharp, P. A. (2007). MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 4, 721-726.
17. Evgenov, O. V., Pacher, P., Schmidt, P. M., Haskó, G., Schmidt, H. H. and Stasch, J. P. (2006). NO-independent stimulators and activators of soluble guanylate cyclase: discovery and therapeutic potential. Nat. Rev. Drug Discov. 5, 755-768.
18. Filippov, G., Bloch, D. B. and Bloch, K. D. (1997). Nitric oxide decreases stability of mRNAs encoding soluble guanylate cyclase subunits in rat pulmonary artery smooth muscle cells. J. Clin. Invest. 100, 942-948.
19. Francis, S. H., Busch, J. L., Corbin, J. D. and Sibley, D. (2010). cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol. Rev. 62, 525-563.
20. Friebe, A. and Koesling, D. (2009). The function of NO-sensitive guanylyl cyclase: what we can learn from genetic mouse models. Nitric Oxide 21, 149-156. Gao, Y. and Raj, J. U. (2010). Regulation of the pulmonary circulation in the fetus and newborn. Physiol. Rev. 90, 1291-1335.
21. Gao, Y. and Raj, J. U. (2010). Regulation of the pulmonary circulation in the fetus and newborn. Physiol. Rev. 90, 1291-1335.
22. Gerassimou, C., Kotanidou, A., Zhou, Z., Simoes, D. C., Roussos, C. and Papapetropoulos, A. (2007). Regulation of the expression of soluble guanylyl cyclase by reactive oxygen species. Br. J. Pharmacol. 150, 1084-1091.
23. Grivel, J. C. and Margolis, L. (2009). Use of human tissue explants to study human infectious agents. Nat. Protoc. 4, 256-269.
24. Guo, H., Ingolia, N. T., Weissman, J. S. and Bartel, D. P. (2010). Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466, 835-840.
25. Guo, L., Qiu, Z., Wei, L., Yu, X., Gao, X., Jiang, S., Tian, H., Jiang, C. and Zhu, D. (2012). The microRNA-328 regulates hypoxic pulmonary hypertension by targeting at insulin growth factor 1 receptor and L-type calcium channel-a1C. Hypertension 59, 1006-1013.
26. Haramati, S., Navon, I., Issler, O., Ezra-Nevo, G., Gil, S., Zwang, R., Hornstein, E. and Chen, A. (2011). MicroRNA as repressors of stress-induced anxiety: the case of amygdalar miR-34. J. Neurosci. 31, 14191-14203.
27. He, L., He, X., Lim, L. P., de Stanchina, E., Xuan, Z., Liang, Y., Xue, W., Zender, L., Magnus, J., Ridzon, D. et al. (2007). A microRNA component of the p53 tumour suppressor network. Nature 447, 1130-1134.
28. Hermeking, H. (2010). The miR-34 family in cancer and apoptosis. Cell Death Differ. 17, 193-199.
29. Hussain, M. B., Hobbs, A. J. and MacAllister, R. J. (1999). Autoregulation of nitric oxide-soluble guanylate cyclase-cyclic GMP signalling in mouse thoracic aorta. Br. J. Pharmacol. 128, 1082-1088.
30. Kagota, S., Tamashiro, A., Yamaguchi, Y., Sugiura, R., Kuno, T., Nakamura, K. and Kunitomo, M. (2001). Downregulation of vascular soluble guanylate cyclase induced by high salt intake in spontaneously hypertensive rats. Br. J. Pharmacol. 134, 737-744.
31. Kasinski, A. L. and Slack, F. J. (2011). Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nat. Rev. Cancer 11, 849-864.
32. Kirsch, M., Kemp-Harper, B., Weissmann, N., Grimminger, F. and Schmidt, H. H. (2008). Sildenafil in hypoxic pulmonary hypertension potentiates a compensatory upregulation of NO-cGMP signaling. FASEB J. 22, 30-40.
33. Klö ss, S., Bouloumié, A. and Mü lsch, A. (2000). Aging and chronic hypertension decrease expression of rat aortic soluble guanylyl cyclase. Hypertension 35, 43-47.
34. Li, D., Zhou, N. and Johns, R. A. (1999). Soluble guanylate cyclase gene expression and localization in rat lung after exposure to hypoxia. Am. J. Physiol. 277, L841- L847.
35. Li, Q., Song, X. W., Zou, J., Wang, G. K., Kremneva, E., Li, X. Q., Zhu, N., Sun, T., Lappalainen, P., Yuan, W. J. et al. (2010). Attenuation of microRNA-1 derepresses the cytoskeleton regulatory protein twinfilin-1 to provoke cardiac hypertrophy. J. Cell Sci. 123, 2444-2452.
36. Liu, N., Landreh, M., Cao, K., Abe, M., Hendriks, G. J., Kennerdell, J. R., Zhu, Y., Wang, L. S. and Bonini, N. M. (2012a). The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila. Nature 482, 519-523.
37. Liu, W. M., Pang, R. T., Chiu, P. C., Wong, B. P., Lao, K., Lee, K. F. and Yeung, W. S. (2012b). Sperm-borne microRNA-34c is required for the first cleavage division in mouse. Proc. Natl. Acad. Sci. USA 109, 490-494.
38. Loscalzo, J. (2010). The cellular response to hypoxia: tuning the system with microRNAs. J. Clin. Invest. 120, 3815-3817.
39. Ma, F., Xu, S., Liu, X., Zhang, Q., Xu, X., Liu, M., Hua, M., Li, N., Yao, H. and Cao, X. (2011). The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-c. Nat. Immunol. 12, 861-869.
40. McNeilly, T. N., Tennant, P., Luján, L., Pérez, M. and Harkiss, G. D. (2007). Differential infection efficiencies of peripheral lung and tracheal tissues in sheep infected with Visna/maedi virus via the respiratory tract. J. Gen. Virol. 88, 670-679.
41. Melichar, V. O., Behr-Roussel, D., Zabel, U., Uttenthal, L. O., Rodrigo, J., Rupin, A., Verbeuren, T. J., Kumar, H. S. and Schmidt, H. H. (2004). Reduced cGMP signaling associated with neointimal proliferation and vascular dysfunction in latestage atherosclerosis. Proc. Natl. Acad. Sci. USA 101, 16671-16676.
42. Oppermann, M., Dao, V. T., Suvorava, T., Bas, M. and Kojda, G. (2008). Effect of oral organic nitrates on expression and activity of vascular soluble guanylyl cyclase. Br. J. Pharmacol. 155, 335-342.
43. Parikh, V. N., Jin, R. C., Rabello, S., Gulbahce, N., White, K., Hale, A., Cottrill, K. A., Shaik, R. S., Waxman, A. B., Zhang, Y. Y. et al. (2012). MicroRNA-21 integrates pathogenic signaling to control pulmonary hypertension: results of a network bioinformatics approach. Circulation 125, 1520-1532.
44. Pedraza, C. E., Baltrons, M. A., Heneka, M. T. and Garciá, A. (2003). Interleukin-1 beta and lipopolysaccharide decrease soluble guanylyl cyclase in brain cells: NOindependent destabilization of protein and NO-dependent decrease of mRNA. J. Neuroimmunol. 144, 80-90.
45. Pullamsetti, S. S., Doebele, C., Fischer, A., Savai, R., Kojonazarov, B., Dahal, B. K., Ghofrani, H. A., Weissmann, N., Grimminger, F., Bonauer, A. et al. (2012). Inhibition of microRNA-17 improves lung and heart function in experimental pulmonary hypertension. Am. J. Respir. Crit. Care Med. 185, 409-419.
46. Qin, X., Wang, X., Wang, Y., Tang, Z., Cui, Q., Xi, J., Li, Y. S., Chien, S. and Wang, N. (2010). MicroRNA-19a mediates the suppressive effect of laminar flow on cyclin D1 expression in human umbilical vein endothelial cells. Proc. Natl. Acad. Sci. USA 107, 3240-3244.
47. Sayed, N., Baskaran, P., Ma, X., van den Akker, F. and Beuve, A. (2007). Desensitization of soluble guanylyl cyclase, the NO receptor, by S-nitrosylation. Proc. Natl. Acad. Sci. USA 104, 12312-12317.
48. Sayed, N., Kim, D. D., Fioramonti, X., Iwahashi, T., Durán, W. N. and Beuve, A. (2008). Nitroglycerin-induced S-nitrosylation and desensitization of soluble guanylyl cyclase contribute to nitrate tolerance. Circ. Res. 103, 606-614.
49. Schramedei, K., Mörbt, N., Pfeifer, G., Läuter, J., Rosolowski, M., Tomm, J. M., von Bergen, M., Horn, F. and Brocke-Heidrich, K. (2011). MicroRNA-21 targets tumor suppressor genes ANP32A and SMARCA4. Oncogene 30, 2975-2985.
50. Selbach, M., Schwanhäusser, B., Thierfelder, N., Fang, Z., Khanin, R. and Rajewsky, N. (2008). Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58-63.
51. Semenza, G. L. (2012). Hypoxia-inducible factors in physiology and medicine. Cell 148, 399-408.
52. Sharina, I. G., Martin, E., Thomas, A., Uray, K. L. and Murad, F. (2003). CCAATbinding factor regulates expression of the beta1 subunit of soluble guanylyl cyclase gene in the BE2 human neuroblastoma cell line. Proc. Natl. Acad. Sci. USA 100, 11523-11528.
53. Sharina, I. G., Cote, G. J., Martin, E., Doursout, M. F. and Murad, F. (2011). RNA splicing in regulation of nitric oxide receptor soluble guanylyl cyclase. Nitric Oxide 25, 265-274.
54. Shi, R. and Chiang, V. L. (2005). Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39, 519-525.
55. Smith-Vikos, T. and Slack, F. J. (2012). MicroRNAs and their roles in aging. J. Cell Sci. 125, 7-17.
56. Stasch, J. P., Pacher, P. and Evgenov, O. V. (2011). Soluble guanylate cyclase as an emerging therapeutic target in cardiopulmonary disease. Circulation 123, 2263-2273.
57. Sylvester, J. T., Shimoda, L. A., Aaronson, P. I. and Ward, J. P. (2012). Hypoxic pulmonary vasoconstriction. Physiol. Rev. 92, 367-520.
58. Thum, T. (2012). MicroRNA therapeutics in cardiovascular medicine. EMBO Mol. Med 4, 3-14.
59. Valastyan, S., Reinhardt, F., Benaich, N., Calogrias, D., Szász, A. M., Wang, Z. C., Brock, J. E., Richardson, A. L. and Weinberg, R. A. (2009). A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 137, 1032-1046.
60. Wang, K., Long, B., Zhou, J. and Li, P. F. (2010a). miR-9 and NFATc3 regulate myocardin in cardiac hypertrophy. J. Biol. Chem. 285, 11903-11912.
61. Wang, S. M., Fu, L. J., Duan, X. L., Crooks, D. R., Yu, P., Qian, Z. M., Di, X. J., Li, J., Rouault, T. A. and Chang, Y. Z. (2010b). Role of hepcidin in murine brain iron metabolism. Cell. Mol. Life Sci. 67, 123-133.
62. Wong, K. Y., Yu, L. and Chim, C. S. (2011). DNA methylation of tumor suppressor miRNA genes: a lesson from the miR-34 family. Epigenomics 3, 83-92.
63. Yang, J. H., Li, J. H., Shao, P., Zhou, H., Chen, Y. Q. and Qu, L. H. (2011). starBase: a database for exploring microRNA-mRNA interaction maps from Argonaute CLIPSeq and Degradome-Seq data. Nucleic Acids Res. 39 Database issue, D202-D209.
64. Yu, F., Jiao, Y., Zhu, Y., Wang, Y., Zhu, J., Cui, X., Liu, Y., He, Y., Park, E. Y., Zhang, H. et al. (2012). MicroRNA 34c gene down-regulation via DNA methylation promotes self-renewal and epithelial-mesenchymal transition in breast tumorinitiating cells. J. Biol. Chem. 287, 465-473.
65. Zheng, X., Ying, L., Liu, J., Dou, D., He, Q., Leung, S. W., Man, R. Y., Vanhoutte, P. M. and Gao, Y. (2011). Role of sulfhydryl-dependent dimerization of soluble guanylyl cyclase in relaxation of porcine coronary artery to nitric oxide. Cardiovasc. Res. 90, 565-572.
66. Zovoilis, A., Agbemenyah, H. Y., Agis-Balboa, R. C., Stilling, R. M., Edbauer, D., Rao, P., Farinelli, L., Delalle, I., Schmitt, A., Falkai, P. et al. (2011). microRNA- 34c is a novel target to treat dementias. EMBO J. 30, 4299-4308.