Chromatin-remodelling factor Brg1 regulates myocardial proliferation and regeneration in zebrafish

Nature Communications

Volumn 7, Issue , 2016, Pages

  Xiao, Chenglu ^a   Gao, Lu ^a   Hou, Yu ^a   Xu, Congfei ^b,c   Chang, Nannan ^a   Wang, Fang ^a   Hu, Keping ^d,e   He, Aibin ^a   Luo, Ying ^a   Wang, Jun ^b,c   Peng, Jinrong ^f   Tang, Fuchou ^a   Zhu, Xiaojun ^a   Xiong, Jing Wei ^a  

^a PEKING UNIVERSITY   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^d INSTITUTE OF MEDICINAL PLANT DEVELOPMENT   (China)

^e PEKING UNION MEDICAL COLLEGE   (China)

^f ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BRG1 PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1C; SMALL INTERFERING RNA; TAMOXIFEN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMARCA4 PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

ADULT; CARDIOVASCULAR DISEASE; CYPRINID; GENE EXPRESSION; INHIBITOR; MITOCHONDRIAL DNA; PROTEIN; REGROWTH;

ADULT; ARTICLE; CARDIAC MUSCLE; CELL PROLIFERATION; CELL REGENERATION; CHROMATIN; CONTROLLED STUDY; DISEASE SEVERITY; DNA METHYLATION; GENE EXPRESSION; HEART MUSCLE FIBROSIS; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN METHYLATION; RNA SEQUENCE; TRANSGENIC ZEBRAFISH; ANIMAL; CYTOLOGY; HEART; METABOLISM; PHYSIOLOGY; REGENERATION; TRANSGENIC ANIMAL; UPREGULATION; ZEBRA FISH;

DANIO RERIO;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P57; DNA METHYLATION; HEART; MYOCARDIUM; REGENERATION; UP-REGULATION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 85002625663     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms13787     Document Type: Article

References (68)

1. Sahara, M., Santoro, F. & Chien, K. R. Programming and reprogramming a human heart cell. EMBO J. 34, 710-738 (2015).
2. Lin, Z. & Pu, W. T. Strategies for cardiac regeneration and repair. Sci. Transl. Med. 6, 239rv231 (2014).
3. Garbern, J. C. & Lee, R. T. Cardiac stem cell therapy and the promise of heart regeneration. Cell Stem Cell 12, 689-698 (2013).
4. Chong, J. J. et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510, 273-277 (2014).
5. Poss, K. D., Wilson, L. G. & Keating, M. T. Heart regeneration in zebrafish. Science 298, 2188-2190 (2002).
6. Jopling, C., Boue, S. & Izpisua Belmonte, J. C. Dedifferentiation, transdifferentiation and reprogramming: three routes to regeneration. Nat. Rev. Mol. Cell Biol. 12, 79-89 (2011).
7. Kikuchi, K. et al. Primary contribution to zebrafish heart regeneration by Gata4+ cardiomyocytes. Nature 464, 601-605 (2010).
8. Gupta, V. & Poss, K. D. Clonally dominant cardiomyocytes direct heart morphogenesis. Nature 484, 479-484 (2012).
9. Porrello, E. R. et al. Transient regenerative potential of the neonatal mouse heart. Science 331, 1078-1080 (2011).
10. Bergmann, O. et al. Evidence for cardiomyocyte renewal in humans. Science 324, 98-102 (2009).
11. Mollova, M. et al. Cardiomyocyte proliferation contributes to heart growth in young humans. Proc. Natl Acad. Sci. USA 110, 1446-1451 (2013).
12. Senyo, S. E., Lee, R. T. & Kuhn, B. Cardiac regeneration based on mechanisms of cardiomyocyte proliferation and differentiation. Stem Cell Res. 13, 532-541 (2014).
13. Ho, L. & Crabtree, G. R. Chromatin remodelling during development. Nature 463, 474-484 (2010).
14. Bultman, S. J. et al. Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev. 20, 1744-1754 (2006).
15. Bultman, S. J., Gebuhr, T. C. & Magnuson, T. A Brg1 mutation that uncouples ATPase activity from chromatin remodeling reveals an essential role for SWI/SNF-related complexes in beta-globin expression and erythroid development. Genes Dev. 19, 2849-2861 (2005).
16. Stankunas, K. et al. Endocardial Brg1 represses ADAMTS1 to maintain the microenvironment for myocardial morphogenesis. Dev. Cell 14, 298-311 (2008).
17. Hang, C. T. et al. Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature 466, 62-67 (2010).
18. Eroglu, B., Wang, G., Tu, N., Sun, X. & Mivechi, N. F. Critical role of Brg1 member of the SWI/SNF chromatin remodeling complex during neurogenesis and neural crest induction in zebrafish. Dev. Dyn. 235, 2722-2735 (2006).
19. Seo, S., Richardson, G. A. & Kroll, K. L. The SWI/SNF chromatin remodeling protein Brg1 is required for vertebrate neurogenesis and mediates transactivation of Ngn and NeuroD. Development 132, 105-115 (2005).
20. Lickert, H. et al. Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 432, 107-112 (2004).
21. Wang, Z. et al. Polybromo protein BAF180 functions in mammalian cardiac chamber maturation. Genes Dev. 18, 3106-3116 (2004).
22. Lei, I., Gao, X., Sham, M. H. & Wang, Z. SWI/SNF protein component BAF250a regulates cardiac progenitor cell differentiation by modulating chromatin accessibility during second heart field development. J. Biol. Chem. 287, 24255-24262 (2012).
23. Bultman, S. et al. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol. Cell 6, 1287-1295 (2000).
24. Li, W. et al. Brg1 governs distinct pathways to direct multiple aspects of mammalian neural crest cell development. Proc. Natl Acad. Sci. USA 110, 1738-1743 (2013).
25. Takeuchi, J. K. et al. Chromatin remodelling complex dosage modulates transcription factor function in heart development. Nat. Commun. 2, 187 (2011).
26. Xiong, Y. et al. Brg1 governs a positive feedback circuit in the hair follicle for tissue regeneration and repair. Dev. Cell 25, 169-181 (2013).
27. Rubart, M. & Field, L. J. Cardiac regeneration: repopulating the heart. Annu. Rev. Physiol. 68, 29-49 (2006).
28. Rubart, M. & Field, L. J. Cardiac repair by embryonic stem-derived cells. Handb. Exp. Pharmacol. 174, 73-100 (2006).
29. Rubart, M. & Field, L. J. Cell-based approaches for cardiac repair. Ann. N Y Acad. Sci. 1080, 34-48 (2006).
30. Wang, W et al. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J. 15, 5370-5382 (1996).
31. Halloran, M. C. et al. Laser-induced gene expression in specific cells of transgenic zebrafish. Development 127, 1953-1960 (2000).
32. Jopling, C. et al. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464, 606-609 (2010).
33. Wu, Q. et al. Talin1 is required for cardiac Z-disk stabilization and endothelial integrity in zebrafish. FASEB J. 29, 4989-5005 (2015).
34. Bu, Y. et al. Protein tyrosine phosphatase PTPN9 regulates erythroid cell development through STAT3 dephosphorylation in zebrafish. J. Cell Sci. 127, 2761-2770 (2014).
35. Kikuchi, K. et al. Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dev. Cell 20, 397-404 (2011).
36. Lepilina, A. et al. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127, 607-619 (2006).
37. Mahmoud, A. I. et al. Meis1 regulates postnatal cardiomyocyte cell cycle arrest. Nature 497, 249-253 (2013).
38. Datta, J. Physical and functional interaction of DNA methyltransferase 3A with Mbd3 and Brg1 in mouse lymphosarcoma cells. Cancer Res. 65, 10891-10900 (2005).
39. Han, P. et al. Epigenetic response to environmental stress: assembly of BRG1-G9a/GLP-DNMT3 repressive chromatin complex on Myh6 promoter in pathologically stressed hearts. Biochim. Biophys. Acta. 1863, 1772-1781 2016.
40. Diao, J. et al. PEG-PLA nanoparticles facilitate siRNA knockdown in adult zebrafish heart. Dev. Biol. 406, 196-202 (2015).
41. Chi, T. H. et al. Reciprocal regulation of CD4/CD8 expression by SWI/SNF-like BAF complexes. Nature 418, 195-199 (2002).
42. Chi, Y., Senyuk, V., Chakraborty, S. & Nucifora, G. EVI1 promotes cell proliferation by interacting with BRG1 and blocking the repression of BRG1 on E2F1 activity. J. Biol. Chem. 278, 49806-49811 (2003).
43. Son, E. Y. & Crabtree, G. R. The role of BAF (mSWI/SNF) complexes in mammalian neural development. Am. J. Med. Genet. C Semin. Med. Genet. 166C, 333-349 (2014).
44. Lessard, J. et al. An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55, 201-215 (2007).
45. Yoo, A. S., Staahl, B. T., Chen, L. & Crabtree, G. R. MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 460, 642-646 (2009).
46. Petrik, D. et al. Chromatin remodeling factor Brg1 supports the early maintenance and late responsiveness of nestin-lineage adult neural stem and progenitor cells. Stem Cells 33, 3655-3665 (2015).
47. Attanasio, C. et al. Tissue-specific SMARCA4 binding at active and repressed regulatory elements during embryogenesis. Genome Res. 24, 920-929 (2014).
48. Nagl, Jr N. G., Wang, X., Patsialou, A., Van Scoy, M. & Moran, E. Distinct mammalian SWI/SNF chromatin remodeling complexes with opposing roles in cell-cycle control. EMBO J. 26, 752-763 (2007).
49. Banine, F. et al. SWI/SNF chromatin-remodeling factors induce changes in DNA methylation to promote transcriptional activation. Cancer Res. 65, 3542-3547 (2005).
50. Okano, M., Bell, D. W., Haber, D. A. & Li, E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257 (1999).
51. Rhee, I. et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 416, 552-556 (2002).
52. Aasland, R., Gibson, T. J. & Stewart, A. F. The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem. Sci. 20, 56-59 (1995).
53. Aasland, R. & Stewart, A. F. The chromo shadow domain, a second chromo domain in heterochromatin-binding protein 1, HP1. Nucleic acids Res. 23, 3168-3173 (1995).
54. Fuks, F., Burgers, W. A., Brehm, A., Hughes-Davies, L. & Kouzarides, T. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat. Genet. 24, 88-91 (2000).
55. Robertson, K. D. et al. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat. Genet. 25, 338-342 (2000).
56. Bachman, K. E., Rountree, M. R. & Baylin, S. B. Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J. Biol. Chem. 276, 32282-32287 (2001).
57. Kawakami, K. et al. A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev. Cell 7, 133-144 (2004).
58. Ochi, H., Hans, S. & Westerfield, M. Smarcd3 regulates the timing of zebrafish myogenesis onset. J. Biol. Chem. 283, 3529-3536 (2008).
59. Mosimann, C. et al. Ubiquitous transgene expression and Cre-based recombination driven by the ubiquitin promoter in zebrafish. Development 138, 169-177 (2011).
60. Li, Y. J. & Hu, B. Establishment of multi-site infection model in zebrafish larvae for studying Staphylococcus aureus infectious disease. J. Genet. Genomics 39, 521-534 (2012).
61. Roman, B. L. et al. Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels. Development 129, 3009-3019 (2002).
62. Heicklen-Klein, A., McReynolds, L. J. & Evans, T. Using the zebrafish model to study GATA transcription factors. Semin. Cell Dev. Biol. 16, 95-106 (2005).
63. Kikuchi, K. et al. tcf21+ epicardial cells adopt non-myocardial fates during zebrafish heart development and regeneration. Development 138, 2895-2902 (2011).
64. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009).
65. Yang, X. Z. et al. Systemic delivery of siRNA with cationic lipid assisted PEG-PLA nanoparticles for cancer therapy. J. Controlled Release 156, 203-211 (2011).
66. Liu, J. et al. Functionalized dendrimer-based delivery of angiotensin type 1 receptor siRNA for preserving cardiac function following infarction. Biomaterials 34, 3729-3736 (2013).
67. Khavari, P. A., Peterson, C. L., Tamkun, J. W., Mendel, D. B. & Crabtree, G. R. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature 366, 170-174 (1993).
68. Zhang, J. et al. Rad GTPase inhibits cardiac fibrosis through connective tissue growth factor. Cardiovasc. Res. 91, 90-98 (2011).