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Oxidative Medicine and Cellular Longevity
Volume 2017 (2017), Article ID 2143875, 10 pages
https://doi.org/10.1155/2017/2143875
Research Article

The Transcription Factor Bach1 Suppresses the Developmental Angiogenesis of Zebrafish

1Department of Physiology and Pathophysiology, School of Basic Medical Sciences, Fudan University, Shanghai 200032, China
2Department of Cardiothoracic Surgery, Shanghai Children’s Medical Center, Shanghai Jiao Tong University School of Medicine, Shanghai 200127, China
3Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Fudan University, Shanghai 200032, China
4Department of Biomedical Engineering, School of Medicine, University of Alabama at Birmingham, Birmingham, AL 35294, USA

Correspondence should be addressed to Dan Meng

Received 20 January 2017; Accepted 23 February 2017; Published 14 March 2017

Academic Editor: Veronika A. Myasoedova

Copyright © 2017 Li Jiang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Corada, D. Nyqvist, F. Orsenigo et al., “The Wnt/β-catenin pathway modulates vascular remodeling and specification by upregulating Dll4/notch signaling,” Developmental Cell, vol. 18, no. 6, pp. 938–949, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. E. D. Cohen, Y. Tian, and E. E. Morrisey, “Wnt signaling: an essential regulator of cardiovascular differentiation, morphogenesis and progenitor self-renewal,” Development, vol. 135, no. 5, pp. 789–798, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. A. V. Gore, M. R. Swift, Y. R. Cha et al., “Rspo1/wnt signaling promotes angiogenesis via vegfc/vegfr3,” Development, vol. 138, no. 22, pp. 4875–4886, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Cattelino, S. Liebner, R. Gallini et al., “The conditional inactivation of the β-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility,” Journal of Cell Biology, vol. 162, no. 6, pp. 1111–1122, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. H.-C. Lee, Y.-Z. Lin, Y.-T. Lai et al., “Glycogen synthase kinase 3 beta in somites plays a role during the angiogenesis of zebrafish embryos,” FEBS Journal, vol. 281, no. 19, pp. 4367–4383, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Skurk, H. Maatz, E. Rocnik, A. Bialik, T. Force, and K. Walsh, “Glycogen-synthase kinase3β/β-catenin axis promotes angiogenesis through activation of vascular endothelial growth factor signaling in endothelial cells,” Circulation Research, vol. 96, no. 3, pp. 308–318, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. L. Lévy, C. Neuveut, C.-A. Renard et al., “Transcriptional activation of interleukin-8 by β-catenin-Tcf4,” Journal of Biological Chemistry, vol. 277, no. 44, pp. 42386–42393, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. E. Dejana, “The role of wnt signaling in physiological and pathological angiogenesis,” Circulation Research, vol. 107, no. 8, pp. 943–952, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Li, S. Dubey, M. L. Varney, B. J. Dave, and R. K. Singh, “IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis,” Journal of Immunology, vol. 170, no. 6, pp. 3369–3376, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. D. Liang, J. R. Chang, A. J. Chin et al., “The role of vascular endothelial growth factor (VEGF) in vasculogenesis, angiogenesis, and hematopoiesis in zebrafish development,” Mechanisms of Development, vol. 108, no. 1-2, pp. 29–43, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. S. J. Stoll, S. Bartsch, H. G. Augustin, and J. Kroll, “The transcription factor HOXC9 regulates endothelial cell quiescence and vascular morphogenesis in zebrafish via inhibition of interleukin 8,” Circulation Research, vol. 108, no. 11, pp. 1367–1377, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Oyake, K. Itoh, H. Motohashi et al., “Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site,” Molecular and Cellular Biology, vol. 16, no. 11, pp. 6083–6095, 1996. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Ogawa, J. Sun, S. Taketani et al., “Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1,” EMBO Journal, vol. 20, no. 11, pp. 2835–2843, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Jiang, M. Yin, X. Wei et al., “Bach1 represses wnt/beta-catenin signaling and angiogenesis,” Circulation Research, vol. 117, no. 4, pp. 364–375, 2015. View at Google Scholar
  15. X. Wang, J. Liu, L. Jiang et al., “Bach1 induces endothelial cell apoptosis and cell-cycle arrest through ROS generation,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 6234043, 13 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Fuse, H. Nakajima, Y. Nakajima-Takagi, O. Nakajima, and M. Kobayashi, “Heme-mediated inhibition of Bach1 regulates the liver specificity and transience of the Nrf2-dependent induction of zebrafish heme oxygenase 1,” Genes to Cells, vol. 20, no. 7, pp. 590–600, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Zhang, M. Xu, J. Huang et al., “Heme acts through the Bach1b/Nrf2a-MafK pathway to regulate exocrine peptidase precursor genes in porphyric zebrafish,” Disease Models and Mechanisms, vol. 7, no. 7, pp. 837–845, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. Q. Luo, C. Wu, S. Sun et al., “The spatial-temporal expression and functional divergence of bach homologs in zebrafish Danio rerio,” Journal of Fish Biology, vol. 88, no. 4, pp. 1584–1597, 2016. View at Publisher · View at Google Scholar · View at Scopus
  19. N. D. Lawson and B. M. Weinstein, “In vivo imaging of embryonic vascular development using transgenic zebrafish,” Developmental Biology, vol. 248, no. 2, pp. 307–318, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. R. I. Dorsky, L. C. Sheldahl, and R. T. Moon, “A transgenic lef1/β-catenin-dependent reporter is expressed in spatially restricted domains throughout zebrafish development,” Developmental Biology, vol. 241, no. 2, pp. 229–237, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Weidinger, C. J. Thorpe, K. Wuennenberg-Stapleton, J. Ngai, and R. T. Moon, “The Sp1-related transcription factors sp5 and sp5-like act downstream of Wnt/β-catenin signaling in mesoderm and neuroectoderm patterning,” Current Biology, vol. 15, no. 6, pp. 489–500, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. C. B. Kimmel, W. W. Ballard, S. R. Kimmel, B. Ullmann, and T. F. Schilling, “Stages of embryonic development of the zebrafish,” Developmental Dynamics, vol. 203, no. 3, pp. 253–310, 1995. View at Publisher · View at Google Scholar · View at Scopus
  23. D. Meng, D.-D. Lv, and J. Fang, “Insulin-like growth factor-I induces reactive oxygen species production and cell migration through Nox4 and Rac1 in vascular smooth muscle cells,” Cardiovascular Research, vol. 80, no. 2, pp. 299–308, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Meng, A. Mei, J. Liu et al., “NADPH oxidase 4 mediates insulin-stimulated HIF-1α and VEGF expression, and angiogenesis in vitro,” PLoS ONE, vol. 7, no. 10, Article ID e48393, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. D. Meng, X. Shi, B.-H. Jiang, and J. Fang, “Insulin-like growth factor-I (IGF-I) induces epidermal growth factor receptor transactivation and cell proliferation through reactive oxygen species,” Free Radical Biology and Medicine, vol. 42, no. 11, pp. 1651–1660, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Isogai, M. Horiguchi, and B. M. Weinstein, “The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development,” Developmental Biology, vol. 230, no. 2, pp. 278–301, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Nasevicius, J. Larson, and S. G. Ekker, “Distinct requirements for zebrafish angiogenesis revealed by a VEGF-A morphant,” Yeast, vol. 17, no. 4, pp. 294–301, 2000. View at Google Scholar · View at Scopus
  28. A. L. Koenig, K. Baltrunaite, N. I. Bower et al., “Vegfa signaling promotes zebrafish intestinal vasculature development through endothelial cell migration from the posterior cardinal vein,” Developmental Biology, vol. 411, no. 1, pp. 115–127, 2016. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Zhou, R. Ge, R. Wang et al., “Uxt potentiates angiogenesis by attenuating notch signaling,” Development (Cambridge), vol. 142, no. 4, pp. 774–786, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. S. H. B. Oehlers, M. V. Flores, C. J. Hall et al., “Expression of zebrafish cxcl8 (interleukin-8) and its receptors during development and in response to immune stimulation,” Developmental and Comparative Immunology, vol. 34, no. 3, pp. 352–359, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Zerlin, M. A. Julius, and J. Kitajewski, “Wnt/Frizzled signaling in angiogenesis,” Angiogenesis, vol. 11, no. 1, pp. 63–69, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Shivanna, I. Harrold, M. Shashar et al., “The C-Cbl ubiquitin ligase regulates nuclear β-catenin and angiogenesis by its tyrosine phosphorylation mediated through the Wnt signaling pathway,” Journal of Biological Chemistry, vol. 290, no. 20, pp. 12537–12546, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. V. Easwaran, S. H. Lee, L. Inge et al., “β-catenin regulates vascular endothelial growth factor expression in colon cancer,” Cancer Research, vol. 63, no. 12, pp. 3145–3153, 2003. View at Google Scholar · View at Scopus
  34. Y. Dohi, T. Ikura, Y. Hoshikawa et al., “Bach1 inhibits oxidative stress-induced cellular senescence by impeding p53 function on chromatin,” Nature Structural and Molecular Biology, vol. 15, no. 12, pp. 1246–1254, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Zhou, H. Wu, M. Zhao, C. Chang, and Q. Lu, “The bach family of transcription factors: a comprehensive review,” Clinical Reviews in Allergy and Immunology, vol. 50, no. 3, pp. 345–356, 2016. View at Publisher · View at Google Scholar · View at Scopus
  36. D. Meng, X. Wang, Q. Chang et al., “Arsenic promotes angiogenesis in vitro via a heme oxygenase-1-dependent mechanism,” Toxicology and Applied Pharmacology, vol. 244, no. 3, pp. 291–299, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. H.-H. Lin, Y.-H. Chen, P.-F. Chang, Y.-T. Lee, S.-F. Yet, and L.-Y. Chau, “Heme oxygenase-1 promotes neovascularization in ischemic heart by coinduction of VEGF and SDF-1,” Journal of Molecular and Cellular Cardiology, vol. 45, no. 1, pp. 44–55, 2008. View at Publisher · View at Google Scholar · View at Scopus