Sp1 mediates a therapeutic role of miR-7a/b in angiotensin II-induced cardiac fibrosis via mechanism involving the TGF-β and MAPKs pathways in cardiac fibroblasts

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Li, Rui ^a   Xiao, Jie ^a   Qing, Xiaoteng ^a   Xing, Junhui ^a   Xia, Yanfei ^a   Qi, Jia ^b   Liu, Xiaojun ^b   Zhang, Sen ^c   Sheng, Xi ^a   Zhang, Xinyu ^a   Ji, Xiaoping ^a  

^a SHANDONG UNIVERSITY   (China)

^b Central Hospital of Zibo   (China)

^c QILU HOSPITAL OF SHANDONG UNIVERSITY QINGDAO   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; GELATINASE A; GELATINASE B; MICRORNA; MICRORNA 7A; MICRORNA 7B; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR SP1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ANGIOTENSIN II; MITHRAMYCIN; MMP2 PROTEIN, RAT; MMP9 PROTEIN, RAT;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL PROLIFERATION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HEART MUSCLE FIBROSIS; MIGRATION INHIBITION; MITOSIS INHIBITION; MYOFIBROBLAST; NEWBORN; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; ANIMAL; BIOSYNTHESIS; CARDIAC MUSCLE; CELL MOTION; CHEMICALLY INDUCED; DRUG EFFECTS; FIBROBLAST; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; WISTAR RAT;

ANGIOTENSIN II; ANIMALS; CELL MOVEMENT; COLLAGEN TYPE I; ENDOMYOCARDIAL FIBROSIS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; GENE EXPRESSION REGULATION; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICRORNAS; MYOCARDIUM; PLICAMYCIN; RATS; RATS, WISTAR; SP1 TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA;

EID: 84928673797     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125513     Document Type: Article

References (55)

1. Huang XR, Chung AC, Yang F, Yue W, Deng C, Lau CP, et al. Smad3 mediates cardiac inflammation and fibrosis in angiotensin II-induced hypertensive cardiac remodeling. Hypertension. 2010; 55(5):1165-71. doi: 10.1161/HYPERTENSIONAHA.109.147611 PMID: 20231525
2. Iwata M, Cowling RT, Yeo SJ, Greenberg B. Targeting the ACE2-Ang-(1-7) pathway in cardiac fibroblasts to treat cardiac remodeling and heart failure. Journal of molecular and cellular cardiology. 2011; 51(4):542-7. doi: 10.1016/j.yjmcc.2010.12.003 PMID: 21147120
3. Olson ER, Naugle JE, Zhang X, Bomser JA, Meszaros JG. Inhibition of cardiac fibroblast proliferation and myofibroblast differentiation by resveratrol. American journal of physiology Heart and circulatory physiology. 2005; 288(3):H1131-8. PMID: 15498824
4. Lijnen PJ, van Pelt JF, Fagard RH. Stimulation of reactive oxygen species and collagen synthesis by angiotensin II in cardiac fibroblasts. Cardiovascular therapeutics. 2012; 30(1):e1-8. doi: 10.1111/j.1755-5922.2010.00205.x PMID: 20626399
5. Olson ER, Shamhart PE, Naugle JE, Meszaros JG. Angiotensin II-induced extracellular signal-regulated kinase 1/2 activation is mediated by protein kinase Cdelta and intracellular calcium in adult rat cardiac fibroblasts. Hypertension. 2008; 51(3):704-11. doi: 10.1161/HYPERTENSIONAHA.107.098459 PMID: 18195168
6. Parthasarathy A, Gopi V, Umadevi S, Simna A, Sheik MJ, Divya H, et al. Suppression of atrial natriuretic peptide/natriuretic peptide receptor-A-mediated signaling upregulates angiotensin-II-induced collagen synthesis in adult cardiac fibroblasts. Molecular and cellular biochemistry. 2013; 378(1-2):217-28. doi: 10.1007/s11010-013-1579-9 PMID: 23580092
7. Verrecchia F, Rossert J, Mauviel A. Blocking sp1 transcription factor broadly inhibits extracellular matrix gene expression in vitro and in vivo: implications for the treatment of tissue fibrosis. The Journal of investigative dermatology. 2001; 116(5):755-63. PMID: 11348466
8. Subramanian SV, Polikandriotis JA, Kelm RJ Jr., David JJ, Orosz CG, Strauch AR. Induction of vascular smooth muscle alpha-actin gene transcription in transforming growth factor beta1-activated myofibroblasts mediated by dynamic interplay between the Pur repressor proteins and Sp1/Smad coactivators. Molecular biology of the cell. 2004; 15(10):4532-43. PMID: 15282343
9. Reddy VS, Prabhu SD, Mummidi S, Valente AJ, Venkatesan B, Shanmugam P, et al. Interleukin-18 induces EMMPRIN expression in primary cardiomyocytes via JNK/Sp1 signaling and MMP-9 in part via EMMPRIN and through AP-1 and NF-kappaB activation. American journal of physiology Heart and circulatory physiology. 2010; 299(4):H1242-54. doi: 10.1152/ajpheart.00451.2010 PMID: 20693392
10. Wei LH, Huang XR, Zhang Y, Li YQ, Chen HY, Heuchel R, et al. Deficiency of Smad7 enhances cardiac remodeling induced by angiotensin II infusion in a mouse model of hypertension. PloS one. 2013; 8(7):e70195. doi: 10.1371/journal.pone.0070195 PMID: 23894614
11. Siddesha JM, Valente AJ, Yoshida T, Sakamuri SS, Delafontaine P, Iba H, et al. Docosahexaenoic acid reverses angiotensin II-induced RECK suppression and cardiac fibroblast migration. Cellular signalling. 2014; 26(5):933-41. doi: 10.1016/j.cellsig.2014.01.005 PMID: 24447911
12. Ihn H, Tamaki K. Competition analysis of the human alpha2(I) collagen promoter using synthetic oligonucleotides. The Journal of investigative dermatology. 2000; 114(5):1011-6. PMID: 10771485
13. Jiang L, Zhou Y, Xiong M, Fang L, Wen P, Cao H, et al. Sp1 mediates microRNA-29c-regulated type I collagen production in renal tubular epithelial cells. Experimental cell research. 2013; 319(14):2254-65. doi: 10.1016/j.yexcr.2013.06.007 PMID: 23806282
14. Chae YM, Park KK, Lee IK, Kim JK, Kim CH, Chang YC. Ring-Sp1 decoy oligonucleotide effectively suppresses extracellular matrix gene expression and fibrosis of rat kidney induced by unilateral ureteral obstruction. Gene therapy. 2006; 13(5):430-9. PMID: 16341057
15. Kum YS, Kim KH, Park TI, Suh IS, Oh HK, Cho CH, et al. Antifibrotic effect via the regulation of transcription factor Sp1 in lung fibrosis. Biochemical and biophysical research communications. 2007; 363(2):368-74. PMID: 17869213
16. Park JH, Jo JH, Kim KH, Kim SJ, Lee WR, Park KK, et al. Antifibrotic effect through the regulation of transcription factor using ring type-Sp1 decoy oligodeoxynucleotide in carbon tetrachloride-induced liver fibrosis. The journal of gene medicine. 2009; 11(9):824-33. doi: 10.1002/jgm.1355 PMID: 19554625
17. Wei LH, Huang XR, Zhang Y, Li YQ, Chen HY, Yan BP, et al. Smad7 inhibits angiotensin II-induced hypertensive cardiac remodelling. Cardiovascular research. 2013; 99(4):665-73. doi: 10.1093/cvr/cvt151 PMID: 23761400
18. Siddesha JM, Valente AJ, Sakamuri SS, Yoshida T, Gardner JD, Somanna N, et al. Angiotensin II stimulates cardiac fibroblast migration via the differential regulation of matrixins and RECK. Journal of molecular and cellular cardiology. 2013; 65:9-18. doi: 10.1016/j.yjmcc.2013.09.015 PMID: 24095877
19. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116(2):281-97. PMID: 14744438
20. Duisters RF, Tijsen AJ, Schroen B, Leenders JJ, Lentink V, van der Made I, et al. miR-133 and miR-30 regulate connective tissue growth factor: implications for a role of microRNAs in myocardial matrix remodeling. Circulation research. 2009; 104(2):170-8, 6p following 8. doi: 10.1161/CIRCRESAHA.108.182535 PMID: 19096030
21. Ferreira J, Coloma L, Fones E, Letelier ME, Repetto Y, Morello A, et al. Effects of t-butyl-4-hydroxyanisole and other phenolic antioxidants on tumoral cells and Trypanosoma parasites. FEBS letters. 1988; 234(2):485-8. PMID: 3292295
22. Roy S, Khanna S, Hussain SR, Biswas S, Azad A, Rink C, et al. MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovascular research. 2009; 82(1):21-9. doi: 10.1093/cvr/cvp015 PMID: 19147652
23. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, et al. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature. 2008; 456(7224):980-4. doi: 10.1038/nature07511 PMID: 19043405
24. Zhang Y, Huang XR, Wei LH, Chung AC, Yu CM, Lan HY. miR-29b as a therapeutic agent for angiotensin II-induced cardiac fibrosis by targeting TGF-beta/Smad3 signaling. Molecular therapy: the journal of the American Society of Gene Therapy. 2014; 22(5):974- 85.
25. Etoh M, Jinnin M, Makino K, Yamane K, Nakayama W, Aoi J, et al. microRNA-7 down-regulation mediates excessive collagen expression in localized scleroderma. Archives of dermatological research. 2013; 305(1):9-15. doi: 10.1007/s00403-012-1287-4 PMID: 22965811
26. Kajihara I, Jinnin M, Yamane K, Makino T, Honda N, Igata T, et al. Increased accumulation of extracellular thrombospondin-2 due to low degradation activity stimulates type I collagen expression in scleroderma fibroblasts. The American journal of pathology. 2012; 180(2):703-14. doi: 10.1016/j.ajpath.2011.10.030 PMID: 22142808
27. Feng HJ, Ouyang W, Liu JH, Sun YG, Hu R, Huang LH, et al. Global microRNA profiles and signaling pathways in the development of cardiac hypertrophy. Brazilian journal of medical and biological research. 2014; 47(5):361-8. PMID: 24728214
28. Wang WK, Wang B, Lu QH, Zhang W, Qin WD, Liu XJ, et al. Inhibition of high-mobility group box 1 improves myocardial fibrosis and dysfunction in diabetic cardiomyopathy. International journal of cardiology. 2014; 172(1):202-12. doi: 10.1016/j.ijcard.2014.01.011 PMID: 24485636
29. Li B, Li R, Zhang C, Bian HJ, Wang F, Xiao J, et al. MicroRNA-7a/b protects against cardiac myocyte injury in ischemia/reperfusion by targeting poly(ADP-ribose) polymerase. PloS one. 2014; 9(3):e90096. doi: 10.1371/journal.pone.0090096 PMID: 24594984
30. Li L, Chen W, Zhu Y, Wang X, Jiang DS, Huang F, et al. Caspase recruitment domain 6 protects against cardiac hypertrophy in response to pressure overload. Hypertension. 2014; 64(1):94-102. doi: 10.1161/HYPERTENSIONAHA.113.03021 PMID: 24777975
31. Gonzalez GE, Rhaleb NE, D'Ambrosio M A, Nakagawa P, Liu Y, Leung P, et al. Deletion of interleukin-6 prevents cardiac inflammation, fibrosis and dysfunction without affecting blood pressure in angiotensin II-high salt-induced hypertension. Journal of hypertension. 2015; 33(1):144-52. doi: 10.1097/HJH.0000000000000358 PMID: 25304471
32. Bracey NA, Gershkovich B, Chun J, Vilaysane A, Meijndert HC, Wright JR Jr., et al. Mitochondrial NLRP3 protein induces reactive oxygen species to promote Smad protein signaling and fibrosis independent from the inflammasome. The Journal of biological chemistry. 2014; 289(28):19571-84. doi: 10.1074/jbc.M114.550624 PMID: 24841199
33. Marzioni M, Agostinelli L, Candelaresi C, Saccomanno S, De Minicis S, Maroni L, et al. Activation of the developmental pathway neurogenin-3/microRNA-7a regulates cholangiocyte proliferation in response to injury. Hepatology. 2014; 60(4):1324-35. doi: 10.1002/hep.27262 PMID: 24925797
34. Cui Y, Xiao Z, Chen T, Wei J, Chen L, Liu L, et al. The miR-7 identified from collagen biomaterial-based three-dimensional cultured cells regulates neural stem cell differentiation. Stem cells and development. 2014; 23(4):393-405. doi: 10.1089/scd.2013.0342 PMID: 24200387
35. Ju H, Dixon IM. Effect of angiotensin II on myocardial collagen gene expression. Molecular and cellular biochemistry. 1996; 163-164:231-7.
36. Ihn H, Ohnishi K, Tamaki T, LeRoy EC, Trojanowska M. Transcriptional regulation of the human alpha2(I) collagen gene. Combined action of upstream stimulatory and inhibitory cis-acting elements. The Journal of biological chemistry. 1996; 271(43):26717-23. PMID: 8900150
37. Rippe RA, Almounajed G, Brenner DA. Sp1 binding activity increases in activated Ito cells. Hepatology. 1995; 22(1):241-51. PMID: 7601417.
38. Hitraya EG, Varga J, Artlett CM, Jimenez SA. Identification of elements in the promoter region of the alpha1(I) procollagen gene involved in its up-regulated expression in systemic sclerosis. Arthritis and rheumatism. 1998; 41(11):2048-58. PMID: 9811061
39. Haase M, Geyer P, Appold S, Schuh D, Kasper M, Muller M. Down-regulation of SP1 DNA binding activity in the process of radiation-induced pulmonary fibrosis. International journal of radiation biology. 2000; 76(4):487-92. PMID: 10815628
40. Jiang X, Ning Q, Wang J. Angiotensin II induced differentially expressed microRNAs in adult rat cardiac fibroblasts. The journal of physiological sciences: JPS. 2013; 63(1):31-8. doi: 10.1007/s12576-012-0230-y PMID: 23007623
41. Jia LF, Huang YP, Zheng YF, Lyu MY, Wei SB, Meng Z, et al. miR-29b suppresses proliferation, migration, and invasion of tongue squamous cell carcinoma through PTEN-AKT signaling pathway by targeting Sp1. Oral oncology. 2014; 50(11):1062-71. doi: 10.1016/j.oraloncology.2014.07.010 PMID: 25127200
42. Wang YT, Yang WB, Chang WC, Hung JJ. Interplay of posttranslational modifications in Sp1 mediates Sp1 stability during cell cycle progression. Journal of molecular biology. 2011; 414(1):1-14. doi: 10.1016/j.jmb.2011.09.027 PMID: 21983342
43. Yang HC, Chuang JY, Jeng WY, Liu CI, Wang AH, Lu PJ, et al. Pin1-mediated Sp1 phosphorylation by CDK1 increases Sp1 stability and decreases its DNA-binding activity during mitosis. Nucleic acids research. 2014; 42(22):13573-87. doi: 10.1093/nar/gku1145 PMID: 25398907
44. Wang YT, Chuang JY, Shen MR, Yang WB, Chang WC, Hung JJ. Sumoylation of specificity protein 1 augments its degradation by changing the localization and increasing the specificity protein 1 proteolytic process. Journal of molecular biology. 2008; 380(5):869-85. doi: 10.1016/j.jmb.2008.05.043 PMID: 18572193
45. Zhao X, Wu J, Zheng M, Gao F, Ju G. Specification and maintenance of oligodendrocyte precursor cells from neural progenitor cells: involvement of microRNA-7a. Molecular biology of the cell. 2012; 23(15):2867-78. doi: 10.1091/mbc.E12-04-0270 PMID: 22696677
46. Hori Y, Kashimoto T, Yonezawa T, Sano N, Saitoh R, Igarashi S, et al. Matrix metalloproteinase-2 stimulates collagen-I expression through phosphorylation of focal adhesion kinase in rat cardiac fibroblasts. American journal of physiology Cell physiology. 2012; 303(9):C947-53. doi: 10.1152/ajpcell.00401.2011 PMID: 22914642
47. Li YY, Feng YQ, Kadokami T, McTiernan CF, Draviam R, Watkins SC, et al. Myocardial extracellular matrix remodeling in transgenic mice overexpressing tumor necrosis factor alpha can be modulated by anti-tumor necrosis factor alpha therapy. Proceedings of the National Academy of Sciences of the United States of America. 2000; 97(23):12746-51. PMID: 11070088
48. Pires PW, Rogers CT, McClain JL, Garver HS, Fink GD, Dorrance AM. Doxycycline, a matrix metalloprotease inhibitor, reduces vascular remodeling and damage after cerebral ischemia in stroke-prone spontaneously hypertensive rats. American journal of physiology Heart and circulatory physiology. 2011; 301(1):H87-97. doi: 10.1152/ajpheart.01206.2010 PMID: 21551278
49. Jiang B, Li D, Deng Y, Teng F, Chen J, Xue S, et al. Salvianolic acid A, a novel matrix metalloproteinase-9 inhibitor, prevents cardiac remodeling in spontaneously hypertensive rats. PloS one. 2013; 8(3):e59621. doi: 10.1371/journal.pone.0059621 PMID: 23533637
50. Cutroneo KR. Human SP1 but not human AP1 binding to the TGF-beta element in the 5′ flanking region of the rat PROalpha1(I) collagen gene. Molecular biology reports. 2000; 27(3):191-4. PMID: 11254109
51. Inagaki Y, Truter S, Tanaka S, Di Liberto M, Ramirez F. Overlapping pathways mediate the opposing actions of tumor necrosis factor-alpha and transforming growth factor-beta on alpha 2(I) collagen gene transcription. The Journal of biological chemistry. 1995; 270(7):3353-8. PMID: 7852421
52. Zhang W, Ou J, Inagaki Y, Greenwel P, Ramirez F. Synergistic cooperation between Sp1 and Smad3/Smad4 mediates transforming growth factor beta1 stimulation of alpha 2(I)-collagen (COL1A2) transcription. The Journal of biological chemistry. 2000; 275(50):39237-45. PMID: 11007770
53. Papakrivopoulou J, Lindahl GE, Bishop JE, Laurent GJ. Differential roles of extracellular signal-regulated kinase 1/2 and p38MAPK in mechanical load-induced procollagen alpha1(I) gene expression in cardiac fibroblasts. Cardiovascular research. 2004; 61(4):736-44. PMID: 14985070
54. Okada M, Yamawaki H, Hara Y. Angiotensin II enhances interleukin-1 beta-induced MMP-9 secretion in adult rat cardiac fibroblasts. The Journal of veterinary medical science / the Japanese Society of Veterinary Science. 2010; 72(6):735-9. PMID: 20145375
55. Sano M, Fukuda K, Sato T, Kawaguchi H, Suematsu M, Matsuda S, et al. ERK and p38 MAPK, but not NF-kappaB, are critically involved in reactive oxygen species-mediated induction of IL-6 by angiotensin II in cardiac fibroblasts. Circulation research. 2001; 89(8):661-9. PMID: 11597988