Fluid shear stress threshold regulates angiogenic sprouting

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 22, 2014, Pages 7968-7973

  Galie, Peter A ^a,b   Nguyen, Duc Huy T ^a   Choi, Colin K ^a   Cohen, Daniel M ^a   Janmey, Paul A ^b   Chen, Christopher S ^a,c,d  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Boston University   (United States)

^d HARVARD UNIVERSITY   (United States)

Author keywords

Angiogenesis; Force; Mechanotransduction; Migration; Morphogenesis

Indexed keywords

INTERSTITIAL COLLAGENASE; VASCULAR ENDOTHELIAL CADHERIN;

ANGIOGENESIS; ARTICLE; BLOOD VESSEL DIAMETER; CAPILLARY; CELL INVASION; CELL JUNCTION; CELL MATURATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FINITE ELEMENT ANALYSIS; FLOW KINETICS; FLOW RATE; FLUID FLOW; GEOMETRY; INTERSTITIAL FLUID; LYMPH VESSEL; MICROFLUIDICS; MONOLAYER CULTURE; PRESSURE GRADIENT; PRIORITY JOURNAL; SHEAR STRESS; UPREGULATION; VASCULAR ENDOTHELIUM; VASCULARIZATION; VENULE;

ANGIOGENESIS; FORCE; MECHANOTRANSDUCTION; MIGRATION; MORPHOGENESIS;

ADENOVIRIDAE; CAPILLARIES; CELL MOVEMENT; ENDOTHELIAL CELLS; FINITE ELEMENT ANALYSIS; GENE SILENCING; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MATRIX METALLOPROTEINASE 1; MECHANOTRANSDUCTION, CELLULAR; MICROFLUIDICS; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; STRESS, MECHANICAL;

EID: 84901854355     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1310842111     Document Type: Article

References (36)

1. Tuder RM, Flook BE, Voelkel NF (1995) Increased gene expression for VEGF and the VEGF receptors KDR/Flk and Flt in lungs exposed to acute or to chronic hypoxia. Modulation of gene expression by nitric oxide. J Clin Invest 95(4):1798-1807.
2. Potente M, Gerhardt H, Carmeliet P (2011) Basic and therapeutic aspects of angiogenesis. Cell 146(6):873-887.
3. Kuo L, Davis MJ, ChilianWM (1990) Endothelium-dependent, flow-induced dilation of isolated coronary arterioles. Am J Physiol 259(4 Pt 2):H1063-H1070.
4. Dawson JM, Hudlická O (1989) The effects of long term administration of prazosin on the microcirculation in skeletal muscles. Cardiovasc Res 23(11):913-920. (Pubitemid 19284854)
5. Egginton S, Zhou AL, Brown MD, Hudlická O (2001) Unorthodox angiogenesis in skeletal muscle. Cardiovasc Res 49(3):634-646. (Pubitemid 32146427)
6. Colgan OC, et al. (2007) Regulation of bovine brain microvascular endothelial tight junction assembly and barrier function by laminar shear stress. Am J Physiol Heart Circ Physiol 292(6):H3190-H3197. (Pubitemid 47084575)
7. Tarbell JM (2010) Shear stress and the endothelial transport barrier. Cardiovasc Res 87(2):320-330.
8. Price GM, et al. (2010) Effect of mechanical factors on the function of engineered human blood microvessels in microfluidic collagen gels. Biomaterials 31(24):6182-6189.
9. Song JW, Munn LL (2011) Fluid forces control endothelial sprouting. Proc Natl Acad Sci USA 108(37):15342-15347.
10. Hernández Vera R, et al. (2009) Interstitial fluid flow intensity modulates endothelial sprouting in restricted Src-activated cell clusters during capillary morphogenesis. Tissue Eng Part A 15(1):175-185.
11. Semino CE, Kamm RD, Lauffenburger DA (2006) Autocrine EGF receptor activation mediates endothelial cell migration and vascular morphogenesis induced by VEGF under interstitial flow. Exp Cell Res 312(3):289-298. (Pubitemid 41814838)
12. Tarbell JM, Weinbaum S, Kamm RD (2005) Cellular fluid mechanics and mechanotransduction. Ann Biomed Eng 33(12):1719-1723. (Pubitemid 43037541)
13. Tarbell JM, Demaio L, Zaw MM (1999) Effect of pressure on hydraulic conductivity of endothelial monolayers: Role of endothelial cleft shear stress. J Appl Physiol (1985) 87(1):261-268.
14. Parker JC, Stevens T, Randall J, Weber DS, King JA (2006) Hydraulic conductance of pulmonary microvascular and macrovascular endothelial cell monolayers. Am J Physiol Lung Cell Mol Physiol 291(1):L30-L37.
15. Galie PA, Spilker RL, Stegemann JP (2011) A linear, biphasic model incorporating a brinkman term to describe the mechanics of cell-seeded collagen hydrogels. Ann Biomed Eng 39(11):2767-2779.
16. Carmeliet P, et al. (1999) Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98(2):147-157. (Pubitemid 29344903)
17. Tzima E, et al. (2005) A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437(7057):426-431. (Pubitemid 41613506)
18. Jinga VV, Bogdan I, Fruchter J (1986) Experimental model for the quantitative estimation of transendothelial transport in vitro; a two-compartment system. Physiologie 23(4):227-236.
19. Chrobak KM, Potter DR, Tien J (2006) Formation of perfused, functional microvascular tubes in vitro. Microvasc Res 71(3):185-196. (Pubitemid 43794856)
20. Partridge CR, Hawker JR, Jr., Forough R (2000) Overexpression of a secretory form of FGF-1 promotes MMP-1-mediated endothelial cell migration. J Cell Biochem 78(3):487-499. (Pubitemid 30491076)
21. Nguyen DH, et al. (2013) Biomimetic model to reconstitute angiogenic sprouting morphogenesis in vitro. Proc Natl Acad Sci USA 110(17):6712-6717.
22. Kang H, Bayless KJ, Kaunas R (2008) Fluid shear stress modulates endothelial cell invasion into three-dimensional collagen matrices. Am J Physiol Heart Circ Physiol 295(5):H2087-H2097.
23. Kang H, Kwak HI, Kaunas R, Bayless KJ (2011) Fluid shear stress and sphingosine 1-phosphate activate calpain to promote membrane type 1 matrix metalloproteinase (MT1-MMP) membrane translocation and endothelial invasion into three-dimensional collagen matrices. J Biol Chem 286(49):42017-42026.
24. Chouinard-Pelletier G, Jahnsen ED, Jones EA (2013) Increased shear stress inhibits angiogenesis in veins and not arteries during vascular development. Angiogenesis 16(1):71-83.
25. Yamamoto K, et al. (2005) Fluid shear stress induces differentiation of Flk-1-positive embryonic stem cells into vascular endothelial cells in vitro. Am J Physiol Heart Circ Physiol 288(4):H1915-H1924. (Pubitemid 40418021)
26. Wang DM, Tarbell JM (1995) Modeling interstitial flow in an artery wall allows estimation of wall shear stress on smooth muscle cells. J Biomech Eng 117(3):358-363.
27. Galie PA, Russell MW, Westfall MV, Stegemann JP (2012) Interstitial fluid flow and cyclic strain differentially regulate cardiac fibroblast activation via AT1R and TGF-β1. Exp Cell Res 318(1):75-84.
28. Ng CP, Hinz B, Swartz MA (2005) Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. J Cell Sci 118(Pt 20):4731-4739. (Pubitemid 41646383)
29. Polacheck WJ, Charest JL, Kamm RD (2011) Interstitial flow influences direction of tumor cell migration through competing mechanisms. Proc Natl Acad Sci USA 108(27):11115-11120.
30. Shi ZD, Ji XY, Qazi H, Tarbell JM (2009) Interstitial flow promotes vascular fibroblast, myofibroblast, and smooth muscle cell motility in 3-D collagen I via upregulation of MMP-1. Am J Physiol Heart Circ Physiol 297(4):H1225-H1234.
31. Shi ZD, Ji XY, Berardi DE, Qazi H, Tarbell JM (2010) Interstitial flow induces MMP-1 expression and vascular SMC migration in collagen I gels via an ERK1/2-dependent and c-Jun-mediated mechanism. Am J Physiol Heart Circ Physiol 298(1):H127-H135.
32. Milkiewicz M, Kelland C, Colgan S, Haas TL (2006) Nitric oxide and p38 MAP kinase mediate shear stress-dependent inhibition of MMP-2 production in microvascular endothelial cells. J Cell Physiol 208(1):229-237. (Pubitemid 43849009)
33. Rivilis I, et al. (2002) Differential involvement of MMP-2 and VEGF during muscle stretch-versus shear stress-induced angiogenesis. Am J Physiol Heart Circ Physiol 283(4):H1430-H1438.
34. Sho E, et al. (2002) Arterial enlargement in response to high flow requires early expression of matrix metalloproteinases to degrade extracellular matrix. Exp Mol Pathol 73(2):142-153.
35. Yun S, et al. (2002) Transcription factor Sp1 phosphorylation induced by shear stress inhibits membrane type 1-matrix metalloproteinase expression in endothelium. J Biol Chem 277(38):34808-34814.
36. Isogai S, Lawson ND, Torrealday S, Horiguchi M, Weinstein BM (2003) Angiogenic network formation in the developing vertebrate trunk. Development 130:5281-5290. (Pubitemid 37369685)