Dynamic responses of endothelial cells to changes in blood flow during vascular remodeling of the mouse yolk sac

Development (Cambridge)

Volumn 140, Issue 19, 2013, Pages 4041-4050

  Udan, Ryan S ^a   Vadakkan, Tegy J ^a   Dickinson, Mary E ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Cell migration; Endothelial cell; Mouse; Vascular remodeling; Vessel fusion; Yolk sac

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD FLOW; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; IMMUNOCHEMISTRY; MOUSE; MOUSE EMBRYO; NONHUMAN; PRIORITY JOURNAL; YOLK SAC;

CELL MIGRATION; ENDOTHELIAL CELL; MOUSE; VASCULAR REMODELING; VESSEL FUSION; YOLK SAC;

ANIMALS; CELL MOVEMENT; EMBRYO, MAMMALIAN; ENDOTHELIAL CELLS; IMMUNOHISTOCHEMISTRY; MICE; MICE, MUTANT STRAINS; MYOSIN LIGHT CHAINS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; YOLK SAC;

EID: 84884236484     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.096255     Document Type: Article

References (49)

1. Argraves, W. S. and Drake, C. J. (2005). Genes critical to vasculogenesis as defined by systematic analysis of vascular defects in knockout mice. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 286, 875-884.
2. Armstrong, J. J., Larina, I. V., Dickinson, M. E., Zimmer, W. E. and Hirschi, K. K. (2010). Characterization of bacterial artificial chromosome transgenic mice expressing mCherry fluorescent protein substituted for the murine smooth muscle alpha-actin gene. Genesis 48, 457-463.
3. Califano, J. P. and Reinhart-King, C. A. (2010). Exogenous and endogenous force regulation of endothelial cell behavior. J. Biomech. 43, 79-86.
4. Chatzizisis, Y. S., Coskun, A. U., Jonas, M., Edelman, E. R., Feldman, C. L. and Stone, P. H. (2007). Role of endothelial shear stress in the natural history of coronary atherosclerosis and vascular remodeling: molecular, cellular, and vascular behavior. J. Am. Coll. Cardiol. 49, 2379-2393.
5. Chiu, J. J. and Chien, S. (2011). Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol. Rev. 91, 327-387.
6. Coffindaffer-Wilson, M., Craig, M. P. and Hove, J. R. (2011). Normal interstitial flow is critical for developmental lymphangiogenesis in the zebrafish. Lymphat. Res. Biol. 9, 151-158.
7. Culver, J. C. and Dickinson, M. E. (2010). The effects of hemodynamic force on embryonic development. Microcirculation 17, 164-178.
8. Davies, P. F., Remuzzi, A., Gordon, E. J., Dewey, C. F., Jr and Gimbrone, M. A., Jr (1986). Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro. Proc. Natl. Acad. Sci. USA 83, 2114-2117.
9. Drake, C. J. and Little, C. D. (1995). Exogenous vascular endothelial growth factor induces malformed and hyperfused vessels during embryonic neovascularization. Proc. Natl. Acad. Sci. USA 92, 7657-7661.
10. Dyer, M. A., Farrington, S. M., Mohn, D., Munday, J. R. and Baron, M. H. (2001). Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo. Development 128, 1717-1730.
11. Fong, G. H., Zhang, L., Bryce, D. M. and Peng, J. (1999). Increased hemangioblast commitment, not vascular disorganization, is the primary defect in flt-1 knock-out mice. Development 126, 3015-3025.
12. Franco, C. and Gerhardt, H. (2012). Tissue engineering: blood vessels on a chip. Nature 488, 465-466.
13. Fraser, S. T., Hadjantonakis, A. K., Sahr, K. E., Willey, S., Kelly, O. G., Jones, E. A., Dickinson, M. E. and Baron, M. H. (2005). Using a histone yellow fluorescent protein fusion for tagging and tracking endothelial cells in ES cells and mice. Genesis 42, 162-171.
14. Garriock, R. J., Czeisler, C., Ishii, Y., Navetta, A. M. and Mikawa, T. (2010). An anteroposterior wave of vascular inhibitor downregulation signals aortae fusion along the embryonic midline axis. Development 137, 3697-3706.
15. Gödde, R. and Kurz, H. (2001). Structural and biophysical simulation of angiogenesis and vascular remodeling. Dev. Dyn. 220, 387-401.
16. Graupera, M., Guillermet-Guibert, J., Foukas, L. C., Phng, L. K., Cain, R. J., Salpekar, A., Pearce, W., Meek, S., Millan, J., Cutillas, P. R. et al. (2008). Angiogenesis selectively requires the p110alpha isoform of PI3K to control endothelial cell migration. Nature 453, 662-666.
17. Haessler, U., Teo, J. C., Foretay, D., Renaud, P. and Swartz, M. A. (2012). Migration dynamics of breast cancer cells in a tunable 3D interstitial flow chamber. Integr. Biol. (Camb.) 4, 401-409.
18. Hahn, C. and Schwartz, M. A. (2009). Mechanotransduction in vascular physiology and atherogenesis. Nat. Rev. Mol. Cell Biol. 10, 53-62.
19. He, C., Hu, H., Braren, R., Fong, S. Y., Trumpp, A., Carlson, T. R. and Wang, R. A. (2008). c-myc in the hematopoietic lineage is crucial for its angiogenic function in the mouse embryo. Development 135, 2467-2477.
20. Huang, C., Sheikh, F., Hollander, M., Cai, C., Becker, D., Chu, P. H., Evans, S. and Chen, J. (2003). Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis. Development 130, 6111-6119.
21. Jakobsson, L., Bentley, K. and Gerhardt, H. (2009). VEGFRs and Notch: a dynamic collaboration in vascular patterning. Biochem. Soc. Trans. 37, 1233-1236.
22. Jones, E. A., Baron, M. H., Fraser, S. E. and Dickinson, M. E. (2004). Measuring hemodynamic changes during mammalian development. Am. J. Physiol. 287, H1561-H1569.
23. Koushik, S. V., Wang, J., Rogers, R., Moskophidis, D., Lambert, N. A., Creazzo, T. L. and Conway, S. J. (2001). Targeted inactivation of the sodiumcalcium exchanger (Ncx1) results in the lack of a heartbeat and abnormal myofibrillar organization. FASEB J. 15, 1209-1211.
24. Larina, I. V., Shen, W., Kelly, O. G., Hadjantonakis, A. K., Baron, M. H. and Dickinson, M. E. (2009). A membrane associated mCherry fluorescent reporter line for studying vascular remodeling and cardiac function during murine embryonic development. Anat. Rec. (Hoboken) 292, 333-341.
25. le Noble, F., Moyon, D., Pardanaud, L., Yuan, L., Djonov, V., Matthijsen, R., Bréant, C., Fleury, V. and Eichmann, A. (2004). Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development 131, 361-375.
26. Li, Y. S., Haga, J. H. and Chien, S. (2005). Molecular basis of the effects of shear stress on vascular endothelial cells. J. Biomech. 38, 1949-1971.
27. Lucitti, J. L., Jones, E. A., Huang, C., Chen, J., Fraser, S. E. and Dickinson, M. E. (2007). Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development 134, 3317-3326.
28. May, S. R., Stewart, N. J., Chang, W. and Peterson, A. S. (2004). A Titin mutation defines roles for circulation in endothelial morphogenesis. Dev. Biol. 270, 31-46.
29. Murray, C. D. (1926). The physiological principle of minimum work: I. the vascular system and the cost of blood volume. Proc. Natl. Acad. Sci. USA 12, 207-214.
30. Nemeno-Guanzon, J. G., Lee, S., Berg, J. R., Jo, Y. H., Yeo, J. E., Nam, B. M., Koh, Y. G. and Lee, J. I. (2012). Trends in tissue engineering for blood vessels. J. Biomed. Biotechnol. 2012, 956345.
31. Poché, R. A., Larina, I. V., Scott, M. L., Saik, J. E., West, J. L. and Dickinson, M. E. (2009). The Flk1-myr:mCherry mouse as a useful reporter to characterize multiple aspects of ocular blood vessel development and disease. Dev. Dyn. 238, 2318-2326.
32. Polacheck, W. J., Charest, J. L. and Kamm, R. D. (2011). Interstitial flow influences direction of tumor cell migration through competing mechanisms. Proc. Natl. Acad. Sci. USA 108, 11115-11120.
33. Roca, C. and Adams, R. H. (2007). Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 21, 2511-2524.
34. Sato, Y., Poynter, G., Huss, D., Filla, M. B., Czirok, A., Rongish, B. J., Little, C. D., Fraser, S. E. and Lansford, R. (2010). Dynamic analysis of vascular morphogenesis using transgenic quail embryos. PLoS ONE 5, e12674.
35. Sengupta, A., Chakraborty, S., Paik, J., Yutzey, K. E. and Evans-Anderson, H. J. (2012). FoxO1 is required in endothelial but not myocardial cell lineages during cardiovascular development. Dev. Dyn. 241, 803-813.
36. Sherman, T. F. (1981). On connecting large vessels to small. The meaning of Murray's law. J. Gen. Physiol. 78, 431-453.
37. Song, J. W. and Munn, L. L. (2011). Fluid forces control endothelial sprouting. Proc. Natl. Acad. Sci. USA 108, 15342-15347.
38. Szczerba, D., Kurz, H. and Szekely, G. (2009). A computational model of intussusceptive microvascular growth and remodeling. J. Theor. Biol. 261, 570-583.
39. Taber, L. A., Ng, S., Quesnel, A. M., Whatman, J. and Carmen, C. J. (2001). Investigating Murray's law in the chick embryo. J. Biomech. 34, 121-124.
40. Takahashi, T., Takahashi, K., St John, P. L., Fleming, P. A., Tomemori, T., Watanabe, T., Abrahamson, D. R., Drake, C. J., Shirasawa, T. and Daniel, T. O. (2003). A mutant receptor tyrosine phosphatase, CD148, causes defects in vascular development. Mol. Cell. Biol. 23, 1817-1831.
41. Tardy, Y., Resnick, N., Nagel, T., Gimbrone, M. A., Jr and Dewey, C. F., Jr (1997). Shear stress gradients remodel endothelial monolayers in vitro via a cell proliferation-migration-loss cycle. Arterioscler. Thromb. Vasc. Biol. 17, 3102-3106.
42. Thoma, R. (1893). Untersuchungen über die Histogenese und Histomechanikdes Gefässsystems. Stuttgart: Ferdinand Enke.
43. Tricot, O., Mallat, Z., Heymes, C., Belmin, J., Lesèche, G. and Tedgui, A. (2000). Relation between endothelial cell apoptosis and blood flow direction in human atherosclerotic plaques. Circulation 101, 2450-2453.
44. Tzima, E., Irani-Tehrani, M., Kiosses, W. B., Dejana, E., Schultz, D. A., Engelhardt, B., Cao, G., DeLisser, H. and Schwartz, M. A. (2005). A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437, 426-431.
45. Udan, R. S. and Dickinson, M. E. (2010). Imaging mouse embryonic development. Methods Enzymol. 476, 329-349.
46. Udan, R. S., Culver, J. C. and Dickinson, M. E. (2013). Understanding vascular development. Wiley Interdiscip. Rev. Dev. Biol. 2, 327-346.
47. Yuan, L., Sakamoto, N., Song, G. and Sato, M. (2012). Migration of human mesenchymal stem cells under low shear stress mediated by mitogenactivated protein kinase signaling. Stem Cells Dev. 21, 2520-2530.
48. Zeng, G., Taylor, S. M., McColm, J. R., Kappas, N. C., Kearney, J. B., Williams, L. H., Hartnett, M. E. and Bautch, V. L. (2007). Orientation of endothelial cell division is regulated by VEGF signaling during blood vessel formation. Blood 109, 1345-1352.
49. Zheng, Y., Chen, J., Craven, M., Choi, N. W., Totorica, S., Diaz-Santana, A., Kermani, P., Hempstead, B., Fischbach-Teschl, C., López, J. A. et al. (2012). In vitro microvessels for the study of angiogenesis and thrombosis. Proc. Natl. Acad. Sci. USA 109, 9342-9347.