The role of Hath6, a newly identified shear-stress-responsive transcription factor, in endothelial cell differentiation and function

Journal of Cell Science

Volumn 127, Issue 7, 2014, Pages 1428-1440

  Fang, Fang ^a   Wasserman, Scott M ^b   Torres Vazquez, Jesus ^c   Weinstein, Brant ^c   Cao, Feng ^d   Li, Zongjin ^d   Wilson, Kitchener D ^d   Yue, Wen ^a   Wu, Joseph C ^d,e   Xie, Xiaoyan ^a,e   Pei, Xuetao ^a  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^b AMGEN INC   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e STANFORD UNIVERSITY   (United States)

Author keywords

Endothelial differentiation; Hath6; Human embryonic stem cells

Indexed keywords

CD31 ANTIGEN; CD45 ANTIGEN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HUMAN ATONAL HOMOLOG 6; MESSENGER RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HATH6 PROTEIN, HUMAN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINE; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; ENZYME INHIBITION; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; LOSS OF FUNCTION MUTATION; MOUSE; MOUSE EMBRYO; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SHEAR STRESS; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ZEBRA FISH; ANIMAL; CYTOLOGY; METABOLISM; PHYSIOLOGY; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; GENE EXPRESSION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE;

EID: 84897373723     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.136358     Document Type: Article

References (40)

1. Balligand, J.-L., Feron, O. and Dessy, C. (2009). eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol. Rev. 89, 481-534.
2. Braddock, M., Schwachtgen, J.-L., Houston, P., Dickson, M. C., Lee, M. J. and Campbell, C. J. (1998). Fluid shear stress modulation of gene expression in endothelial cells. News Physiol Sci. 13, 241-246.
3. Chen, J., Dai, F., Balakrishnan-Renuka, A., Leese, F., Schempp, W., Schaller, F., Hoffmann, M. M., Morosan-Puopolo, G., Yusuf, F., Bisschoff, I. J. et al. (2011). Diversification and molecular evolution of ATOH8, a gene encoding a bHLH transcription factor. PLoS ONE 6, e23005.
4. Chen, Z., Bakhshi, F. R., Shajahan, A. N., Sharma, T., Mao, M., Trane, A., Bernatchez, P., van Nieuw Amerongen, G. P., Bonini, M. G., Skidgel, R. A. et al. (2012). Nitric oxide-dependent Src activation and resultant caveolin-1 phosphorylation promote eNOS/caveolin-1 binding and eNOS inhibition. Mol. Biol. Cell 23, 1388-1398.
5. Cheng, B.-B., Yan, Z.-Q., Yao, Q.-P., Shen, B.-R., Wang, J.-Y., Gao, L.-Z., Li, Y.-Q., Yuan, H.-T., Qi, Y.-X. and Jiang, Z.-L. (2012). Association of SIRT1 expression with shear stress induced endothelial progenitor cell differentiation. J. Cell. Biochem. 113, 3663-3671.
6. Chiu, J.-J., Lee, P.-L., Chang, S.-F., Chen, L.-J., Lee, C.-I., Lin, K.M., Usami, S. and Chien, S. (2005). Shear stress regulates gene expression in vascular endothelial cells in response to tumor necrosis factor-a: a study of the transcription profile with complementary DNA microarray. J. Biomed. Sci. 12, 481-502.
7. Coomber, B. L. and Gotlieb, A. I. (1990). In vitro endothelial wound repair. Interaction of cell migration and proliferation. Arterioscler. Thromb. Vasc. Biol. 10, 215-222.
8. Ferguson, J. E., III, Kelley, R. W. and Patterson, C. (2005). Mechanisms of endothelial differentiation in embryonic vasculogenesis. Arterioscler. Thromb. Vasc. Biol. 25, 2246-2254.
9. Go, Y.-M., Lee, H.-R. and Park, H. (2012). H(2)S inhibits oscillatory shear stressinduced monocyte binding to endothelial cells via nitric oxide production. Mol. Cells 34, 449-455.
10. Hauptmann, G. and Gerster, T. (1994). Two-color whole-mount in situ hybridization to vertebrate and Drosophila embryos. Trends Genet. 10, 266.
11. Hove, J. R., Köster, R. W., Forouhar, A. S., Acevedo-Bolton, G., Fraser, S. E. and Gharib, M. (2003). Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421, 172-177.
12. Hsiai, T. K. and Wu, J. C. (2008). Hemodynamic forces regulate embryonic stem cell commitment to vascular progenitors. Curr. Cardiol. Rev. 4, 269-274.
13. Huang, N. F., Fleissner, F., Sun, J. and Cooke, J. P. (2010). Role of nitric oxide signaling in endothelial differentiation of embryonic stem cells. Stem Cells Dev. 19, 1617-1626.
14. Inoue, C., Bae, S.-K., Takatsuka, K., Inoue, T., Bessho, Y. and Kageyama, R. (2001). Math6, a bHLH gene expressed in the developing nervous system, regulates neuronal versus glial differentiation. Genes Cells 6, 977-986.
15. Jain, R. K. (2003). Molecular regulation of vessel maturation. Nat. Med. 9, 685-693.
16. Le Bras, A., Vijayaraj, P. and Oettgen, P. (2010). Molecular mechanisms of endothelial differentiation. Vasc. Med. 15, 321-331.
17. Ledent, V. and Vervoort, M. (2001). The basic helix-loop-helix protein family: comparative genomics and phylogenetic analysis. Genome Res. 11, 754-770.
18. Lehoux, S., Castier, Y. and Tedgui, A. (2006). Molecular mechanisms of the vascular responses to haemodynamic forces. J. Intern. Med. 259, 381-392.
19. Lejoly-Boisseau, H., Appriou, M., Seigneur, M., Pruvost, A., Tribouley-Duret, J. and Tribouley, J. (1999). Schistosoma mansoni: in vitro adhesion of parasite eggs to the vascular endothelium. Subsequent inhibition by a monoclonal antibody directed to a carbohydrate epitope. Exp. Parasitol. 91, 20-29.
20. Li, Z., Wu, J. C., Sheikh, A. Y., Kraft, D., Cao, F., Xie, X., Patel, M., Gambhir, S. S., Robbins, R. C., Cooke, J. P. et al. (2007). Differentiation, survival, and function of embryonic stem cell derived endothelial cells for ischemic heart disease. Circulation 116 Suppl., I46-I54.
21. Li, Z., Wilson, K. D., Smith, B., Kraft, D. L., Jia, F., Huang, M., Xie, X., Robbins, R. C., Gambhir, S. S., Weissman, I. L. et al. (2009). Functional and transcriptional characterization of human embryonic stem cell-derived endothelial cells for treatment of myocardial infarction. PLoS ONE 4, e8443.
22. Lynn, F. C., Sanchez, L., Gomis, R., German, M. S. and Gasa, R. (2008). Identification of the bHLH factor Math6 as a novel component of the embryonic pancreas transcriptional network. PLoS ONE 3, e2430.
23. Massari, M. E. and Murre, C. (2000). Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol. 20, 429-440.
24. Nguyen, Q.-G. V., Buskin, J. N., Himeda, C. L., Shield, M. A. and Hauschka, S. D. (2003). Differences in the function of three conserved E-boxes of the muscle creatine kinase gene in cultured myocytes and in transgenic mouse skeletal and cardiac muscle. J. Biol. Chem. 278, 46494-46505.
25. Nonaka, S., Shiratori, H., Saijoh, Y. and Hamada, H. (2002). Determination of leftright patterning of the mouse embryo by artificial nodal flow. Nature 418, 96-99.
26. Ross, M. D., Martinka, S., Mukherjee, A., Sedor, J. R., Vinson, C. and Bruggeman, L. A. (2006). Math6 expression during kidney development and altered expression in a mouse model of glomerulosclerosis. Dev. Dyn. 235, 3102-3109.
27. Sumanas, S. and Lin, S. (2006). Ets1-related protein is a key regulator of vasculogenesis in zebrafish. PLoS Biol. 4, e10.
28. Sumanas, S., Gomez, G., Zhao, Y., Park, C., Choi, K. and Lin, S. (2008). Interplay among Etsrp/ER71, Scl, and Alk8 signaling controls endothelial and myeloid cell formation. Blood 111, 4500-4510.
29. Teichert, A. M., Miller, T. L., Tai, S. C., Wang, Y., Bei, X., Robb, G. B., Phillips, M. J. and Marsden, P. A. (2000). In vivo expression profile of an endothelial nitric oxide synthase promoter-reporter transgene. Am. J. Physiol. 278, H1352-H1361.
30. Topper, J. N., Cai, J., Falb, D. and Gimbrone, M. A., Jr (1996). Identification of vascular endothelial genes differentially responsive to fluid mechanical stimuli: cyclooxygenase-2, manganese superoxide dismutase, and endothelial cell nitric oxide synthase are selectively up-regulated by steady laminar shear stress. Proc. Natl. Acad. Sci. USA 93, 10417-10422.
31. Vittet, D., Prandini, M., Berthier, R., Schweitzer, A., Martin-Sisteron, H., Uzan, G. and Dejana, E. (1996). Embryonic stem cells differentiate in vitro to endothelial cells through successive maturation steps. Blood 88, 3424-3431.
32. Wang, Y., Hu, Y., Sun, C., Zhang, X. and He, W. (2006). Mechanism of arsenic trioxide inhibiting angiogenesis in multiple myeloma. J. Huazhong Univ. Sci. Technolog. Med. Sci. 26, 43-46.
33. Wang, Z. Z., Au, P., Chen, T., Shao, Y., Daheron, L. M., Bai, H., Arzigian, M., Fukumura, D., Jain, R. K. and Scadden, D. T. (2007). Endothelial cells derived from human embryonic stem cells form durable blood vessels in vivo. Nat. Biotechnol. 25, 317-318.
34. Wang, Y., Chen, K., Yao, Q., Zheng, X. and Yang, Z. (2009). Phylogenetic analysis of zebrafish basic helix-loop-helix transcription factors. J. Mol. Evol. 68, 629-640.
35. Wasserman, S. M., Mehraban, F., Komuves, L. G., Yang, R.-B., Tomlinson, J. E., Zhang, Y., Spriggs, F. and Topper, J. N. (2002). Gene expression profile of human endothelial cells exposed to sustained fluid shear stress. Physiol. Genomics 12, 13-23.
36. Yamamoto, K., Sokabe, T., Watabe, T., Miyazono, K., Yamashita, J. K., Obi, S., Ohura, N., Matsushita, A., Kamiya, A. and Ando, J. (2005). Fluid shear stress induces differentiation of Flk-1-positive embryonic stem cells into vascular endothelial cells in vitro. Am. J. Physiol. 288, H1915-H1924.
37. Yao, J., Zhou, J., Liu, Q., Lu, D., Wang, L., Qiao, X. and Jia, W. (2010). Atoh8, a bHLH transcription factor, is required for the development of retina and skeletal muscle in zebrafish. PLoS ONE 5, e10945.
38. Yu, C., Liu, Y., Miao, Z., Yin, M., Lu, W., Lv, Y., Ding, M. and Deng, H. (2010). Retinoic acid enhances the generation of hematopoietic progenitors from human embryonic stem cell-derived hemato-vascular precursors. Blood 116, 4786-4794.
39. Zeng, L., Xiao, Q., Margariti, A., Zhang, Z., Zampetaki, A., Patel, S., Capogrossi, M. C., Hu, Y. and Xu, Q. (2006). HDAC3 is crucial in shearand VEGF-induced stem cell differentiation toward endothelial cells. J. Cell Biol. 174, 1059-1069.
40. Zhang, P., Li, J., Tan, Z., Wang, C., Liu, T., Chen, L., Yong, J., Jiang, W., Sun, X., Du, L. et al. (2008). Short-term BMP-4 treatment initiates mesoderm induction in human embryonic stem cells. Blood 111, 1933-1941.