MicroRNA-101 protects cardiac fibroblasts from hypoxia-induced apoptosis via inhibition of the TGF-β signaling pathway

International Journal of Biochemistry and Cell Biology

Volumn 65, Issue , 2015, Pages 155-164

  Zhao, Xin ^a   Wang, Kejing ^a   Hu, Fen ^a   Qian, Cheng ^a   Guan, Hongquan ^a   Feng, Kaige ^a   Zhou, You ^a   Chen, Zhijian ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Apoptosis; Cardiac fibroblasts; Hypoxia; MicroRNA 101; Transforming growth factor signaling pathway

Indexed keywords

CASPASE 3; MICRORNA 101; MICRORNA 101A; MICRORNA 101B; PROTEIN BAX; PROTEIN BCL 2; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNCLASSIFIED DRUG; MICRORNA; MIRN101 MICRORNA, RAT; PROTEIN SERINE THREONINE KINASE; TGF-BETA TYPE I RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL HYPOXIA; CELL SURVIVAL; CELL VACUOLE; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; HEART FIBROBLAST; HEART PROTECTION; MITOCHONDRION SWELLING; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CARDIAC MUSCLE; CELL PROLIFERATION; CYTOLOGY; FIBROBLAST; GENETIC TRANSFECTION; GENETICS; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS; CELL HYPOXIA; CELL PROLIFERATION; DOWN-REGULATION; FIBROBLASTS; MICRORNAS; MYOCARDIUM; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84931268603     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2015.06.005     Document Type: Article

References (43)

1. L. Attisano, and J.L. Wrana Signal transduction by members of the transforming growth factor-beta superfamily Cytokine Growth Factor Rev. 7 4 1996 327 339
2. A.B. Aurora, A.I. Mahmoud, X. Luo, B.A. Johnson, E. van Rooij, S. Matsuzaki, K.M. Humphries, J.A. Hill, R. Bassel-Duby, H.A. Sadek, and E.N. Olson MicroRNA-214 protects the mouse heart from ischemic injury by controlling Ca(2)(+) overload and cell death J. Clin. Investig. 122 4 2012 1222 1232
3. I. Banerjee, K. Yekkala, T.K. Borg, and T.A. Baudino Dynamic interactions between myocytes, fibroblasts, and extracellular matrix Ann. N. Y. Acad. Sci. 1080 2006 76 84
4. J. Bauersachs, and T. Thum Biogenesis and regulation of cardiovascular microRNAs Circ. Res. 109 3 2011 334 347
5. D.M. Bers Calcium cycling and signaling in cardiac myocytes Annu. Rev. Physiol. 70 2008 23 49
6. Q. Bu, Y. Fang, Y. Cao, Q. Chen, and Y. Liu Enforced expression of miR-101 enhances cisplatin sensitivity in human bladder cancer cells by modulating the cyclooxygenase-2 pathway Mol. Med. Rep. 10 4 2014 2203 2209
7. T. Capiod The need for calcium channels in cell proliferation Recent Pat. Anticancer Drug Discov. 8 1 2013 4 17
8. M.J. Cha, J.K. Jang, O. Ham, B.W. Song, S.Y. Lee, C.Y. Lee, J.H. Park, J. Lee, H.H. Seo, E. Choi, W.M. Jeon, H.J. Hwang, H.T. Shin, E. Choi, and K.C. Hwang MicroRNA-145 suppresses ROS-induced Ca2+ overload of cardiomyocytes by targeting CaMKII delta Biochem. Biophys. Res. Commun. 435 4 2013 720 726
9. N. Chaudhari, P. Talwar, A. Parimisetty, D.C. Lefebvre, and P. Ravanan A molecular web: endoplasmic reticulum stress, inflammation, and oxidative stress Front. Cell Neurosci. 8 2014 213
10. W. Chu, X. Li, C. Li, L. Wan, H. Shi, X. Song, X. Liu, X. Chen, C. Zhang, H. Shan, Y. Lu, and B. Yang TGFBR3, a potential negative regulator of TGF-beta signaling, protects cardiac fibroblasts from hypoxia-induced apoptosis J. Cell. Physiol. 226 10 2011 2586 2594
11. R.M. Clancy, P. Zheng, M. O'Mahony, P. Izmirly, J. Zavadil, L. Gardner, and J.P. Buyon Role of hypoxia and cAMP in the transdifferentiation of human fetal cardiac fibroblasts: implications for progression to scarring in autoimmune-associated congenital heart block Arthr. Rheumatol. 56 12 2007 4120 4131
12. L. Deng, B. Huang, D. Qin, K. Ganguly, and N. El-Sherif Calcineurin inhibition ameliorates structural, contractile, and electrophysiologic consequences of postinfarction remodeling J. Cardiovasc. Electrophysiol. 12 9 2001 1055 1061
13. R. Derynck, and Y.E. Zhang Smad-dependent and Smad-independent pathways in TGF-beta family signalling Nature 425 6958 2003 577 584
14. V. Falanga, T.A. Martin, H. Takagi, R.S. Kirsner, T. Helfman, J. Pardes, and M.S. Ochoa Low oxygen tension increases mRNA levels of alpha 1 (I) procollagen in human dermal fibroblasts J. Cell. Physiol. 157 2 1993 408 412
15. M. Harada, X. Luo, T. Murohara, B. Yang, D. Dobrev, and S. Nattel MicroRNA regulation and cardiac calcium signaling: role in cardiac disease and therapeutic potential Circ. Res. 114 4 2014 689 705
16. S.R. Houser Ca(2+) signaling domains responsible for cardiac hypertrophy and arrhythmias Circ. Res. 104 4 2009 413 415
17. S. Ikeda, S.W. Kong, J. Lu, E. Bisping, H. Zhang, P.D. Allen, T.R. Golub, B. Pieske, and W.T. Pu Altered microRNA expression in human heart disease Physiol. Genomics 31 3 2007 367 373
18. J. Karlstad, Y. Sun, and B.B. Singh Ca(2+) signaling: an outlook on the characterization of Ca(2+) channels and their importance in cellular functions Adv. Exp. Med. Biol. 740 2012 143 157
19. P. Kohl, P. Camelliti, F.L. Burton, and G.L. Smith Electrical coupling of fibroblasts and myocytes: relevance for cardiac propagation J. Electrocardiol. 38 4 Suppl. 2005 45 50
20. K.B. Lai, J.E. Sanderson, and C.M. Yu High dose norepinephrine-induced apoptosis in cultured rat cardiac fibroblast Int. J. Cardiol. 136 1 2009 33 39
21. Q. Lu, B. Patel, E.O. Harrington, and S. Rounds Transforming growth factor-beta1 causes pulmonary microvascular endothelial cell apoptosis via ALK5 Am. J. Physiol. Lung Cell Mol. Physiol. 296 5 2009 L825 L838
22. K. Machaca Ca(2+) signaling, genes and the cell cycle Cell Calcium 49 5 2011 323 330
23. M. Mayorga, N. Bahi, M. Ballester, J.X. Comella, and D. Sanchis Bcl-2 is a key factor for cardiac fibroblast resistance to programmed cell death J. Biol. Chem. 279 33 2004 34882 34889
24. J.W. Mockridge, E.C. Benton, L.V. Andreeva, D.S. Latchman, M.S. Marber, and R.J. Heads IGF-1 regulates cardiac fibroblast apoptosis induced by osmotic stress Biochem. Biophys. Res. Commun. 273 1 2000 322 327
25. Z. Pan, X. Sun, H. Shan, N. Wang, J. Wang, J. Ren, S. Feng, L. Xie, C. Lu, Y. Yuan, Y. Zhang, Y. Wang, Y. Lu, and B. Yang MicroRNA-101 inhibited postinfarct cardiac fibrosis and improved left ventricular compliance via the FBJ osteosarcoma oncogene/transforming growth factor-beta1 pathway Circulation 126 7 2012 840 850
26. K.E. Porter, and N.A. Turner Cardiac fibroblasts: at the heart of myocardial remodeling Pharmacol. Ther. 123 2 2009 255 278
27. A. Rojas, M. Padidam, D. Cress, and W.M. Grady TGF-beta receptor levels regulate the specificity of signaling pathway activation and biological effects of TGF-beta Biochim. Biophys. Acta 1793 7 2009 1165 1173
28. A.Y. Tan, and P. Zimetbaum Atrial fibrillation and atrial fibrosis J. Cardiovasc. Pharmacol. 57 6 2011 625 629
29. T. Thum, D. Catalucci, and J. Bauersachs MicroRNAs: novel regulators in cardiac development and disease Cardiovasc. Res. 79 4 2008 562 570
30. X. Tu, H. Zhang, J. Zhang, S. Zhao, X. Zheng, Z. Zhang, J. Zhu, J. Chen, L. Dong, Y. Zang, and J. Zhang MicroRNA-101 suppresses liver fibrosis by targeting the TGFbeta signalling pathway J. Pathol. 234 1 2014 46 59
31. N.A. Turner, A. Das, P. Warburton, D.J. O'Regan, S.G. Ball, and K.E. Porter Interleukin-1alpha stimulates proinflammatory cytokine expression in human cardiac myofibroblasts Am. J. Physiol. Heart Circ. Physiol. 297 3 2009 H1117 H1127
32. E. van Rooij The art of microRNA research Circ. Res. 108 2 2011 219 234
33. E. van Rooij, L.B. Sutherland, J.E. Thatcher, J.M. DiMaio, R.H. Naseem, W.S. Marshall, J.A. Hill, and E.N. Olson Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis Proc. Natl. Acad. Sci. U. S. A. 105 35 2008 13027 13032
34. R. Ventura-Clapier, and G. Vassort Ionic bases of cardioplegic solutions. I. Some implications of the role of ionic equilibrium in the preservation of cardiac metabolism. Experimental study of hypoxia and calcium overloads Arch. Mal. Coeur Vaiss 76 12 1983 1456 1464
35. L. Wang, L. Li, R. Guo, X. Li, Y. Lu, X. Guan, S.C. Gitau, L. Wang, C. Xu, B. Yang, and H. Shan miR-101 promotes breast cancer cell apoptosis by targeting Janus kinase 2 Cell. Physiol. Biochem. 34 2 2014 413 422
36. C.J. Watson, P. Collier, I. Tea, R. Neary, J.A. Watson, C. Robinson, D. Phelan, M.T. Ledwidge, K.M. McDonald, A. McCann, O. Sharaf, and J.A. Baugh Hypoxia-induced epigenetic modifications are associated with cardiac tissue fibrosis and the development of a myofibroblast-like phenotype Hum. Mol. Genet. 23 8 2014 2176 2188
37. K.T. Weber, Y. Sun, S.K. Bhattacharya, R.A. Ahokas, and I.C. Gerling Myofibroblast-mediated mechanisms of pathological remodelling of the heart Nat. Rev. Cardiol. 10 1 2013 15 26
38. K.L. Yang, W.T. Chang, K.C. Hung, E.I. Li, and C.C. Chuang Inhibition of transforming growth factor-beta-induced liver fibrosis by a retinoic acid derivative via the suppression of Col 1A2 promoter activity Biochem. Biophys. Res. Commun. 373 2 2008 219 223
39. Y.F. Yang, C.C. Wu, W.P. Chen, and M.J. Su Transforming growth factor-beta type I receptor/ALK5 contributes to doxazosin-induced apoptosis in H9C2 cells Naunyn Schmiedebergs Arch. Pharmacol. 380 6 2009 561 567
40. B. Yang, K. He, F. Zheng, L. Wan, X. Yu, X. Wang, D. Zhao, Y. Bai, W. Chu, Y. Sun, and Y. Lu Over-expression of hypoxia-inducible factor-1 alpha in vitro protects the cardiac fibroblasts from hypoxia-induced apoptosis J. Cardiovasc. Med. (Hagerstown) 15 7 2014 579 586
41. X. Zhao, and M. Eghbali-Webb Gender-related differences in basal and hypoxia-induced activation of signal transduction pathways controlling cell cycle progression and apoptosis in cardiac fibroblasts Endocrine 18 2 2002 137 145
42. X. Zhao, K. Wang, Y. Liao, Q. Zeng, Y. Li, F. Hu, Y. Liu, K. Meng, C. Qian, Q. Zhang, H. Guan, K. Feng, Y. Zhou, Y. Du, and Z. Chen MicroRNA-101a inhibits cardiac fibrosis induced by hypoxia via targeting TGFbetaRI on cardiac fibroblasts Cell. Physiol. Biochem. 35 1 2015 213 226
43. Y. Zou, Z. Jiang, X. Yu, Y. Zhang, M. Sun, W. Wang, Z. Ge, W. De, and L. Sun MiR-101 regulates apoptosis of trophoblast HTR-8/SVneo cells by targeting endoplasmic reticulum (ER) protein 44 during preeclampsia J. Hum. Hypertens. 28 10 2014 610 616