[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content

Advertisement

Springer Nature Link
Log in

Circ-sh3rf3/GATA-4/miR-29a regulatory axis in fibroblast–myofibroblast differentiation and myocardial fibrosis

  • Original Article
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

The transdifferentiation from cardiac fibroblasts to myofibroblasts is an important event in the initiation of cardiac fibrosis. However, the underlying mechanism is not fully understood. Circ-sh3rf3 (circular RNA SH3 domain containing Ring Finger 3) is a novel circular RNA which was induced in hypertrophied ventricles by isoproterenol hydrochloride, and our work has established that it is a potential regulator in cardiac hypertrophy, but whether circ-sh3rf3 plays a role in cardiac fibrosis remains unclear, especially in the conversion of cardiac fibroblasts into myofibroblasts. Here, we found that circ-sh3rf3 was down-regulated in isoproterenol-treated rat cardiac fibroblasts and cardiomyocytes as well as during fibroblast differentiation into myofibroblasts. We further confirmed that circ-sh3rf3 could interact with GATA-4 proteins and reduce the expression of GATA-4, which in turn abolishes GATA-4 repression of miR-29a expression and thus up-regulates miR-29a expression, thereby inhibiting fibroblast–myofibroblast differentiation and myocardial fibrosis. Our work has established a novel Circ-sh3rf3/GATA-4/miR-29a regulatory cascade in fibroblast–myofibroblast differentiation and myocardial fibrosis, which provides a new therapeutic target for myocardial fibrosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

All data generated during this study are included in this published article and its supplementary information files.

References

  1. Bevilacqua A, Willis MS, Bultman SJ (2014) SWI/SNF chromatin-remodeling complexes in cardiovascular development and disease. Cardiovasc Pathol 23:85–91. https://doi.org/10.1016/j.carpath.2013.09.003

    Article  CAS  PubMed  Google Scholar 

  2. Caja L, Dituri F, Mancarella S, Caballero-Diaz D, Moustakas A, Giannelli G, Fabregat I (2018) TGF-beta and the tissue microenvironment: relevance in fibrosis and cancer. Int J Mol Sci 19:1294. https://doi.org/10.3390/ijms19051294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Chothani S, Schafer S, Adami E, Viswanathan S, Widjaja AA, Langley SR, Tan J, Wang M, Quaife NM, Jian Pua C, D’Agostino G, Guna Shekeran S, George BL, Lim S, Yiqun Cao E, van Heesch S, Witte F, Felkin LE, Christodoulou EG, Dong J, Blachut S, Patone G, Barton PJR, Hubner N, Cook SA, Rackham OJL (2019) Widespread translational control of fibrosis in the human heart by RNA-binding proteins. Circulation 140:937–951. https://doi.org/10.1161/CIRCULATIONAHA.119.039596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. de Salvi GF, de Moraes WM, Bozi LH, Souza PR, Antonio EL, Bocalini DS, Tucci PJ, Ribeiro DA, Brum PC, Medeiros A (2017) Dexamethasone-induced cardiac deterioration is associated with both calcium handling abnormalities and calcineurin signaling pathway activation. Mol Cell Biochem 424:87–98. https://doi.org/10.1007/s11010-016-2846-3

    Article  CAS  Google Scholar 

  5. Dey S, Kwon JJ, Liu S, Hodge GA, Taleb S, Zimmers TA, Wan J, Kota J (2020) miR-29a is repressed by MYC in pancreatic cancer and its restoration drives tumor-suppressive effects via downregulation of LOXL2. Mol Cancer Res MCR 18:311–323. https://doi.org/10.1158/1541-7786.MCR-19-0594

    Article  CAS  PubMed  Google Scholar 

  6. Dobrzycki T, Lalwani M, Telfer C, Monteiro R, Patient R (2020) The roles and controls of GATA factors in blood and cardiac development. IUBMB Life 72:39–44. https://doi.org/10.1002/iub.2178

    Article  CAS  PubMed  Google Scholar 

  7. Driesen RB, Nagaraju CK, Abi-Char J, Coenen T, Lijnen PJ, Fagard RH, Sipido KR, Petrov VV (2014) Reversible and irreversible differentiation of cardiac fibroblasts. Cardiovasc Res 101:411–422. https://doi.org/10.1093/cvr/cvt338

    Article  CAS  PubMed  Google Scholar 

  8. Du WW, Yang W, Chen Y, Wu ZK, Foster FS, Yang Z, Li X, Yang BB (2017) Foxo3 circular RNA promotes cardiac senescence by modulating multiple factors associated with stress and senescence responses. Eur Heart J 38:1402–1412. https://doi.org/10.1093/eurheartj/ehw001

    Article  CAS  PubMed  Google Scholar 

  9. Du WW, Zhang C, Yang W, Yong T, Awan FM, Yang BB (2017) Identifying and characterizing circRNA-protein interaction. Theranostics 7:4183–4191. https://doi.org/10.7150/thno.21299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ellmers LJ, Scott NJ, Piuhola J, Maeda N, Smithies O, Frampton CM, Richards AM, Cameron VA (2007) Npr1-regulated gene pathways contributing to cardiac hypertrophy and fibrosis. J Mol Endocrinol 38:245–257. https://doi.org/10.1677/jme.1.02138

    Article  CAS  PubMed  Google Scholar 

  11. Eyholzer M, Schmid S, Wilkens L, Mueller BU, Pabst T (2010) The tumour-suppressive miR-29a/b1 cluster is regulated by CEBPA and blocked in human AML. Br J Cancer 103:275–284. https://doi.org/10.1038/sj.bjc.6605751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Fu DJ, Song J, Zhu T, Pang XJ, Wang SH, Zhang YB, Wu BW, Wang JW, Zi X, Zhang SY, Liu HM (2020) Discovery of novel tertiary amide derivatives as NEDDylation pathway activators to inhibit the tumor progression in vitro and in vivo. Eur J Med Chem 192:112153. https://doi.org/10.1016/j.ejmech.2020.112153

    Article  CAS  PubMed  Google Scholar 

  13. Garikipati VNS, Verma SK, Cheng Z, Liang D, Truongcao MM, Cimini M, Yue Y, Huang G, Wang C, Benedict C, Tang Y, Mallaredy V, Ibetti J, Grisanti L, Schumacher SM, Gao E, Rajan S, Wilusz JE, Goukassian D, Houser SR, Koch WJ, Kishore R (2019) Circular RNA CircFndc3b modulates cardiac repair after myocardial infarction via FUS/VEGF-A axis. Nat Commun 10:4317. https://doi.org/10.1038/s41467-019-11777-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Georges R, Nemer G, Morin M, Lefebvre C, Nemer M (2008) Distinct expression and function of alternatively spliced Tbx5 isoforms in cell growth and differentiation. Mol Cell Biol 28:4052–4067. https://doi.org/10.1128/MCB.02100-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Gurtner GC, Werner S, Barrandon Y, Longaker MT (2008) Wound repair and regeneration. Nature 453:314–321. https://doi.org/10.1038/nature07039

    Article  CAS  PubMed  Google Scholar 

  16. Hsu CH, Liu IF, Kuo HF, Li CY, Lian WS, Chang CY, Chen YH, Liu WL, Lu CY, Liu YR, Lin TC, Lee TY, Huang CY, Hsieh CC, Liu PL (2021) miR-29a-3p/THBS2 axis regulates PAH-induced cardiac fibrosis. Int J Mol Sci. https://doi.org/10.3390/ijms221910574

    Article  PubMed  PubMed Central  Google Scholar 

  17. Jiang Q, Liu C, Li CP, Xu SS, Yao MD, Ge HM, Sun YN, Li XM, Zhang SJ, Shan K, Liu BH, Yao J, Zhao C, Yan B (2020) Circular RNA-ZNF532 regulates diabetes-induced retinal pericyte degeneration and vascular dysfunction. J Clin Investig 130:3833–3847. https://doi.org/10.1172/JCI123353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Jie M, Wu Y, Gao M, Li X, Liu C, Ouyang Q, Tang Q, Shan C, Lv Y, Zhang K, Dai Q, Chen Y, Zeng S, Li C, Wang L, He F, Hu C, Yang S (2020) CircMRPS35 suppresses gastric cancer progression via recruiting KAT7 to govern histone modification. Mol Cancer 19:56. https://doi.org/10.1186/s12943-020-01160-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Koivisto E, Kaikkonen L, Tokola H, Pikkarainen S, Aro J, Pennanen H, Karvonen T, Rysa J, Kerkela R, Ruskoaho H (2011) Distinct regulation of B-type natriuretic peptide transcription by p38 MAPK isoforms. Mol Cell Endocrinol 338:18–27. https://doi.org/10.1016/j.mce.2011.02.015

    Article  CAS  PubMed  Google Scholar 

  20. Kong P, Christia P, Frangogiannis NG (2013) The pathogenesis of cardiac fibrosis. Cell Mol Life Sci 71:549–574. https://doi.org/10.1007/s00018-013-1349-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kristensen LS, Andersen MS, Stagsted LVW, Ebbesen KK, Hansen TB, Kjems J (2019) The biogenesis, biology and characterization of circular RNAs. Nat Rev Genet 20:675–691. https://doi.org/10.1038/s41576-019-0158-7

    Article  CAS  PubMed  Google Scholar 

  22. Kudej RK, Iwase M, Uechi M, Vatner DE, Oka N, Ishikawa Y, Shannon RP, Bishop SP, Vatner SF (1997) Effects of chronic beta-adrenergic receptor stimulation in mice. J Mol Cell Cardiol 29:2735–2746. https://doi.org/10.1006/jmcc.1997.0508

    Article  CAS  PubMed  Google Scholar 

  23. Lei M, Zheng G, Ning Q, Zheng J, Dong D (2020) Translation and functional roles of circular RNAs in human cancer. Mol Cancer 19:30. https://doi.org/10.1186/s12943-020-1135-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Li M, Ding W, Tariq MA, Chang W, Zhang X, Xu W, Hou L, Wang Y, Wang J (2018) A circular transcript of ncx1 gene mediates ischemic myocardial injury by targeting miR-133a-3p. Theranostics 8:5855–5869. https://doi.org/10.7150/thno.27285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Liu D, Li S, Cui Y, Tong H, Li S, Yan Y (2019) Podocan affects C2C12 myogenic differentiation by enhancing Wnt/beta-catenin signaling. J Cell Physiol 234:11130–11139. https://doi.org/10.1002/jcp.27763

    Article  CAS  PubMed  Google Scholar 

  26. Liu Y, Afzal J, Vakrou S, Greenland GV, Talbot CC Jr, Hebl VB, Guan Y, Karmali R, Tardiff JC, Leinwand LA, Olgin JE, Das S, Fukunaga R, Abraham MR (2019) Differences in microRNA-29 and pro-fibrotic gene expression in mouse and human hypertrophic cardiomyopathy. Front Cardiovasc Med 6:170. https://doi.org/10.3389/fcvm.2019.00170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ma CX, Song YL, Xiao L, Xue LX, Li WJ, Laforest B, Komati H, Wang WP, Jia ZQ, Zhou CY, Zou Y, Nemer M, Zhang SF, Bai X, Wu H, Zang MX (2015) EGF is required for cardiac differentiation of P19CL6 cells through interaction with GATA-4 in a time- and dose-dependent manner. Cell Mol Life Sci CMLS 72:2005–2022. https://doi.org/10.1007/s00018-014-1795-9

    Article  CAS  PubMed  Google Scholar 

  28. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495:333–338. https://doi.org/10.1038/nature11928

    Article  CAS  PubMed  Google Scholar 

  29. Morin S, Charron F, Robitaille L, Nemer M (2000) GATA-dependent recruitment of MEF2 proteins to target promoters. EMBO J 19:2046–2055. https://doi.org/10.1093/emboj/19.9.2046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Ni H, Li W, Zhuge Y, Xu S, Wang Y, Chen Y, Shen G, Wang F (2019) Inhibition of circHIPK3 prevents angiotensin II-induced cardiac fibrosis by sponging miR-29b-3p. Int J Cardiol 292:188–196. https://doi.org/10.1016/j.ijcard.2019.04.006

    Article  PubMed  Google Scholar 

  31. Park S, Ranjbarvaziri S, Lay FD, Zhao P, Miller MJ, Dhaliwal JS, Huertas-Vazquez A, Wu X, Qiao R, Soffer JM, Rau C, Wang Y, Mikkola HKA, Lusis AJ, Ardehali R (2018) Genetic regulation of fibroblast activation and proliferation in cardiac fibrosis. Circulation 138:1224–1235. https://doi.org/10.1161/CIRCULATIONAHA.118.035420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Park SW, Persaud SD, Ogokeh S, Meyers TA, Townsend D, Wei LN (2018) CRABP1 protects the heart from isoproterenol-induced acute and chronic remodeling. J Endocrinol 236:151–165. https://doi.org/10.1530/JOE-17-0613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Paz I, Kosti I, Ares M Jr, Cline M, Mandel-Gutfreund Y (2014) RBPmap: a web server for mapping binding sites of RNA-binding proteins. Nucleic Acids Res 42:W361-367. https://doi.org/10.1093/nar/gku406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Qin RH, Tao H, Ni SH, Shi P, Dai C, Shi KH (2018) microRNA-29a inhibits cardiac fibrosis in Sprague–Dawley rats by downregulating the expression of DNMT3A. Anatol J Cardiol 20:198–205. https://doi.org/10.14744/AnatolJCardiol.2018.98511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Rodriguez P, Sassi Y, Troncone L, Benard L, Ishikawa K, Gordon RE, Lamas S, Laborda J, Hajjar RJ, Lebeche D (2019) Deletion of delta-like 1 homologue accelerates fibroblast-myofibroblast differentiation and induces myocardial fibrosis. Eur Heart J 40:967–978. https://doi.org/10.1093/eurheartj/ehy188

    Article  CAS  PubMed  Google Scholar 

  36. Schreiner S, Didio A, Hung LH, Bindereif A (2020) Design and application of circular RNAs with protein-sponge function. Nucleic Acids Res 48:12326–12335. https://doi.org/10.1093/nar/gkaa1085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Tarbit E, Singh I, Peart JN, Rose’Meyer RB (2019) Biomarkers for the identification of cardiac fibroblast and myofibroblast cells. Heart Fail Rev 24:1–15. https://doi.org/10.1007/s10741-018-9720-1

    Article  CAS  PubMed  Google Scholar 

  38. Temsah R, Nemer M (2005) GATA factors and transcriptional regulation of cardiac natriuretic peptide genes. Regul Pept 128:177–185. https://doi.org/10.1016/j.regpep.2004.12.026

    Article  CAS  PubMed  Google Scholar 

  39. Tian R, Guan X, Qian H, Wang L, Shen Z, Fang L, Liu Z (2021) Restoration of NRF2 attenuates myocardial ischemia reperfusion injury through mediating microRNA-29a-3p/CCNT2 axis. BioFactors. https://doi.org/10.1002/biof.1712

    Article  PubMed  Google Scholar 

  40. Travers JG, Kamal FA, Robbins J, Yutzey KE, Blaxall BC (2016) Cardiac fibrosis: the fibroblast awakens. Circ Res 118:1021–1040. https://doi.org/10.1161/CIRCRESAHA.115.306565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Wang K, Long B, Liu F, Wang JX, Liu CY, Zhao B, Zhou LY, Sun T, Wang M, Yu T, Gong Y, Liu J, Dong YH, Li N, Li PF (2016) A circular RNA protects the heart from pathological hypertrophy and heart failure by targeting miR-223. Eur Heart J 37:2602–2611. https://doi.org/10.1093/eurheartj/ehv713

    Article  CAS  PubMed  Google Scholar 

  42. Wang R, Peng L, Lv D, Shang F, Yan J, Li G, Li D, Ouyang J, Yang J (2021) Leonurine attenuates myocardial fibrosis through upregulation of miR-29a-3p in mice post-myocardial infarction. J Cardiovasc Pharmacol 77:189–199. https://doi.org/10.1097/FJC.0000000000000957

    Article  CAS  PubMed  Google Scholar 

  43. Wang Y, Li C, Zhao R, Qiu Z, Shen C, Wang Z, Liu W, Zhang W, Ge J, Shi B (2021) CircUbe3a from M2 macrophage-derived small extracellular vesicles mediates myocardial fibrosis after acute myocardial infarction. Theranostics 11:6315–6333. https://doi.org/10.7150/thno.52843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Wang Y, Zhao R, Liu W, Wang Z, Rong J, Long X, Liu Z, Ge J, Shi B (2019) Exosomal circHIPK3 released from hypoxia-pretreated cardiomyocytes regulates oxidative damage in cardiac microvascular endothelial cells via the miR-29a/IGF-1 pathway. Oxid Med Cell Longev 2019:7954657. https://doi.org/10.1155/2019/7954657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Wu N, Yuan Z, Du KY, Fang L, Lyu J, Zhang C, He A, Eshaghi E, Zeng K, Ma J, Du WW, Yang BB (2019) Translation of yes-associated protein (YAP) was antagonized by its circular RNA via suppressing the assembly of the translation initiation machinery. Cell Death Differ 26:2758–2773. https://doi.org/10.1038/s41418-019-0337-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Xu X, Zhang J, Tian Y, Gao Y, Dong X, Chen W, Yuan X, Yin W, Xu J, Chen K, He C, Wei L (2020) CircRNA inhibits DNA damage repair by interacting with host gene. Mol Cancer 19:128. https://doi.org/10.1186/s12943-020-01246-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Yang F, Hu A, Li D, Wang J, Guo Y, Liu Y, Li H, Chen Y, Wang X, Huang K, Zheng L, Tong Q (2019) Circ-HuR suppresses HuR expression and gastric cancer progression by inhibiting CNBP transactivation. Mol Cancer 18:158. https://doi.org/10.1186/s12943-019-1094-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Yang MH, Wang H, Han SN, Jia X, Zhang S, Dai FF, Zhou MJ, Yin Z, Wang TQ, Zang MX, Xue LX (2020) Circular RNA expression in isoproterenol hydrochloride-induced cardiac hypertrophy. Aging (Albany NY) 12:2530–2544. https://doi.org/10.18632/aging.102761

    Article  CAS  PubMed  Google Scholar 

  49. Yao CX, Wei QX, Zhang YY, Wang WP, Xue LX, Yang F, Zhang SF, Xiong CJ, Li WY, Wei ZR, Zou Y, Zang MX (2013) miR-200b targets GATA-4 during cell growth and differentiation. RNA Biol 10:465–480. https://doi.org/10.4161/rna.24370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Yuan S, Liang J, Zhang M, Zhu J, Pan R, Li H, Zeng N, Wen Y, Yi Z, Shan Z (2019) CircRNA_005647 inhibits expressions of fibrosis-related genes in mouse cardiac fibroblasts via sponging miR-27b-3p. Nan Fang Yi Ke Da Xue Xue Bao 39:1312–1319. https://doi.org/10.12122/j.issn.1673-4254.2019.11.08

    Article  CAS  PubMed  Google Scholar 

  51. Yücel D, Solinsky J, van Berlo JH (2020) Isolation of cardiomyocytes from fixed hearts for immunocytochemistry and ploidy analysis. J Vis Exp JoVE. https://doi.org/10.3791/60938

    Article  PubMed  Google Scholar 

  52. Zhang S-B, Lin S-Y, Liu M, Liu C-C, Ding H-H, Sun Y, Ma C, Guo R-X, Lv Y-Y, Wu S-L, Xu T, Xin W-J (2019) CircAnks1a in the spinal cord regulates hypersensitivity in a rodent model of neuropathic pain. Nat Commun 10:4119. https://doi.org/10.1038/s41467-019-12049-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Zhang S, Yin Z, Dai FF, Wang H, Zhou MJ, Yang MH, Zhang SF, Fu ZF, Mei YW, Zang MX, Xue L (2019) miR-29a attenuates cardiac hypertrophy through inhibition of PPARδ expression. J Cell Physiol 234:13252–13262. https://doi.org/10.1002/jcp.27997

    Article  CAS  PubMed  Google Scholar 

  54. Zhou L, Miao K, Yin B, Li H, Fan J, Zhu Y, Ba H, Zhang Z, Chen F, Wang J, Zhao C, Li Z, Wang DW (2018) Cardioprotective role of myeloid-derived suppressor cells in heart failure. Circulation 138:181–197. https://doi.org/10.1161/CIRCULATIONAHA.117.030811

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to members of the Zang’s lab for helpful discussions. We thank Xiu-Hua Ren for histological sections.

Funding

This study was supported by the National Natural Science Foundation of China (Nos. 82072975, 81771631, and 32171179), the High-Level Talents of Henan Province, particularly the support for the Central Plains Thousand Talents Program, which are the leading talents of Central Plains Basic Research (ZYQR201810120); the key project of discipline construction of Zhengzhou University in 2020 (XKZDQY202002), 2022 Henan Province Science and Technology R&D Program Joint Fund (Cultivation of Superior Disciplines, 222301420094), and Henan Province Science and Technology Projects (202102310057).

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Zhengzhou University, Ke Xue Da Dao 100, Zheng Zhou, 450001, China

    Cai-Xia Ma, Tong Sun, Ming-Hui Yang, Yu-Qie Sun, Kun-Lun Kai, Meng-Jiao Zhou, Zi-Wei Wang, Jing Chen, Wei Li, Tian-Qi Wang, Shan-Feng Zhang & Ming-Xi Zang

  2. The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China

    Zhi-Ru Wei & Jia-Chen Shi

  3. Medical Research Center, Peking University Third Hospital, 49 Huayuan North Road, Beijing, 100191, China

    Lixiang Xue & Qianqian Yin

  4. Cardiovascular Division, Department of Cardiology, King’s College London British Heart Foundation Centre of Research Excellence, London, UK

    Min Zhang

Authors
  1. Cai-Xia Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhi-Ru Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tong Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ming-Hui Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yu-Qie Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kun-Lun Kai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jia-Chen Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Meng-Jiao Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zi-Wei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jing Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Wei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Tian-Qi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Shan-Feng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Lixiang Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Min Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Qianqian Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Ming-Xi Zang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YQ and M-XZ conceived, designed, and supervised the study. C-XM, Zh-RW, K-LK, Y-QS, M-HY, J-CS, M-JZ, TS, and Z-WW performed the experiments. JC, WL, T-QW, S-FZ, LX, and MZ provided the technical support and contributed to the discussion of the project and article. YQ and M-XZ analysed the data and wrote the article.

Corresponding authors

Correspondence to Qianqian Yin or Ming-Xi Zang.

Ethics declarations

Competing interest

The authors declare no competing interest.

Ethics approval and consent to participate

All animal experiments were approved by the Animal Ethics Committee of Zhengzhou University and carried out in accordance with the Guide for the Care and Use of Laboratory Animals (US NIH, 2011).

Consent for publication

The author’s consent to publication.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, CX., Wei, ZR., Sun, T. et al. Circ-sh3rf3/GATA-4/miR-29a regulatory axis in fibroblast–myofibroblast differentiation and myocardial fibrosis. Cell. Mol. Life Sci. 80, 50 (2023). https://doi.org/10.1007/s00018-023-04699-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00018-023-04699-7

Keywords

Search

Navigation