Haemodynamic and extracellular matrix cues regulate the mechanical phenotype and stiffness of aortic endothelial cells

Nature Communications

Volumn 5, Issue , 2014, Pages

  Collins, Caitlin ^a   Osborne, Lukas D ^b   Guilluy, Christophe ^a   Chen, Zhongming ^a   O'Brien III, E Tim ^b   Reader, John S ^a   Burridge, Keith ^a,c   Superfine, Richard ^a   Tzima, Ellie ^a,c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b The University of North Carolina at Chapel Hill   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; COLLAGEN; CYCLIC AMP DEPENDENT PROTEIN KINASE; FIBRONECTIN; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

BIOCHEMISTRY; BIOMECHANICS; BLOOD; COLLAGEN; ENZYME ACTIVITY; MECHANICAL PROPERTY; PHENOTYPE;

ANIMAL CELL; ANIMAL EXPERIMENT; AORTA; ARTICLE; BLOOD VESSEL; CELL ADHESION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME INACTIVATION; EXTRACELLULAR MATRIX; FOCAL ADHESION; FORCE; HEMODYNAMICS; MALE; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; RIGIDITY; SHEAR STRESS; TENSION; ANIMAL; C57BL MOUSE; CYTOLOGY; ENZYMOLOGY; METABOLISM; PHYSIOLOGY; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIGENS, CD31; AORTA; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; HEMODYNAMICS; MALE; MICE; MICE, INBRED C57BL; RHOA GTP-BINDING PROTEIN;

EID: 84902312401     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4984     Document Type: Article

References (36)

1. Wu, C. C. et al. Directional shear flow and Rho activation prevent the endothelial cell apoptosis induced by micropatterned anisotropic geometry. Proc. Natl Acad. Sci. USA 104, 1254-1259 (2007).
2. Ohura, N. et al. Global analysis of shear stress-responsive genes in vascular endothelial cells. J. Atheroscler. Thromb. 10, 304-313 (2003).
3. Mammoto, A. et al. A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457, 1103-1108 (2009).
4. Chicurel, M. E., Singer, R. H., Meyer, C. J. & Ingber, D. E. Integrin binding and mechanical tension induce movement of mRNA and ribosomes to focal adhesions. Nature 392, 730-733 (1998). (Pubitemid 28207796)
5. Weber, G. F., Bjerke, M. A. & DeSimone, D. W. A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev. Cell 22, 104-115 (2012).
6. Matthews, B. D., Overby, D. R., Mannix, R. & Ingber, D. E. Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J. Cell Sci. 119, 508-518 (2006).
7. Guilluy, C. et al. The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins. Nat. Cell Biol. 13, 722-727 (2011).
8. Kuo, J. C., Han, X., Hsiao, C. T., Yates, 3rd J. R. & Waterman, C. M. Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for beta-Pix in negative regulation of focal adhesion maturation. Nat. Cell Biol. 13, 383-393 (2011).
9. Hirai, T., Sasayama, S., Kawasaki, T. & Yagi, S. Stiffness of systemic arteries in patients with myocardial infarction. A noninvasive method to predict severity of coronary atherosclerosis. Circulation 80, 78-86 (1989). (Pubitemid 19178640)
10. Wang, Y. X. et al. Increased aortic stiffness assessed by pulse wave velocity in apolipoprotein E-deficient mice. Am. J. Physiol. Heart Circ. Physiol. 278, H428-H434 (2000).
11. Huynh, J. et al. Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration. Sci. Transl. Med. 3, 112ra122 (2011).
12. Collins, C. et al. Localized tensional forces on PECAM-1 elicit a global mechanotransduction response via the integrin-RhoA pathway. Curr. Biol. 22, 2087-2094 (2012).
13. Huveneers, S. et al. Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling. J. Cell Biol. 196, 641-652 (2012).
14. le Duc, Q. et al. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J. Cell Biol. 189, 1107-1115 (2010).
15. Tzima, E. et al. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437, 426-431 (2005). (Pubitemid 41613506)
16. Orr, A. W., Ginsberg, M. H., Shattil, S. J., Deckmyn, H. & Schwartz, M. A. Matrix-specific suppression of integrin activation in shear stress signaling. Mol. Biol. Cell 17, 4686-4697 (2006). (Pubitemid 44665739)
17. Jalali, S. et al. Integrin-mediated mechanotransduction requires its dynamic interaction with specific extracellular matrix (ECM) ligands. Proc. Natl Acad. Sci. USA 98, 1042-1046 (2001). (Pubitemid 32121183)
18. Funk, S. D. et al. Matrix-specific protein kinase A signaling regulates p21-activated kinase activation by flow in endothelial cells. Circ. Res. 106, 1394-1403 (2010).
19. Riveline, D. et al. Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J. Cell Biol. 153, 1175-1186 (2001).
20. Ellerbroek, S. M., Wennerberg, K. & Burridge, K. Serine phosphorylation negatively regulates RhoA in vivo. J. Biol. Chem. 278, 19023-19031 (2003). (Pubitemid 36799287)
21. Mott, R. E. & Helmke, B. P. Mapping the dynamics of shear stress-induced structural changes in endothelial cells. Am. J. Physiol. Cell Physiol. 293, C1616-C1626 (2007). (Pubitemid 350085637)
22. Davies, P. F., Robotewskyj, A. & Griem, M. L. Quantitative studies of endothelial cell adhesion. Directional remodeling of focal adhesion sites in response to flow forces. J. Clin. Invest. 93, 2031-2038 (1994).
23. Hoffman, B. D., Massiera, G., Van Citters, K. M. & Crocker, J. C. The consensus mechanics of cultured mammalian cells. Proc. Natl Acad. Sci. USA 103, 10259-10264 (2006). (Pubitemid 44051154)
24. Wirtz, D. Particle-tracking microrheology of living cells: principles and applications. Annu. Rev. Biophys. 38, 301-326 (2009).
25. Jin, H. et al. A PKA-Csk-pp60Src signaling pathway regulates the switch between endothelial cell invasion and cell-cell adhesion during vascular sprouting. Blood 116, 5773-5783 (2010).
26. Qiao, J., Huang, F. & Lum, H. PKA inhibits RhoA activation: a protection mechanism against endothelial barrier dysfunction. Am. J. Physiol. Lung Cell Mol. Physiol. 284, L972-L980 (2003). (Pubitemid 36687132)
27. Birukova, A. A. et al. Rac GTPase is a hub for protein kinase A and Epac signaling in endothelial barrier protection by cAMP. Microvasc. Res. 79, 128-138 (2010).
28. Tkachenko, E. et al. Protein kinase A governs a RhoA-RhoGDI protrusionretraction pacemaker in migrating cells. Nat. Cell Biol. 13, 660-667 (2011).
29. Lang, P. et al. Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J. 15, 510-519 (1996). (Pubitemid 26044564)
30. Forget, M. A., Desrosiers, R. R., Gingras, D. & Beliveau, R. Phosphorylation states of Cdc42 and RhoA regulate their interactions with Rho GDP dissociation inhibitor and their extraction from biological membranes. Biochem. J. 361, 243-254 (2002). (Pubitemid 34174491)
31. Howe, A. K. & Juliano, R. L. Regulation of anchorage-dependent signal transduction by protein kinase A and p21-activated kinase. Nat. Cell Biol. 2, 593-600 (2000).
32. Howe, A. K., Hogan, B. P. & Juliano, R. L. Regulation of vasodilator-stimulated phosphoprotein phosphorylation and interaction with Abl by protein kinase A and cell adhesion. J. Biol. Chem. 277, 38121-38126 (2002). (Pubitemid 35154664)
33. Whittard, J. D. & Akiyama, S. K. Positive regulation of cell-cell and cellsubstrate adhesion by protein kinase A. J. Cell Sci. 114, 3265-3272 (2001). (Pubitemid 32998903)
34. Yang, B., Radel, C., Hughes, D., Kelemen, S. & Rizzo, V. p190 RhoGTPaseactivating protein links the beta1 integrin/caveolin-1 mechanosignaling complex to RhoA and actin remodeling. Arterioscler. Thromb. Vasc. Biol. 31, 376-383 (2011).
35. Meiri, D. et al. Modulation of Rho guanine exchange factor Lfc activity by protein kinase A-mediated phosphorylation. Mol. Cell Biol. 29, 5963-5973 (2009).
36. Tzima, E., del Pozo, M. A., Shattil, S. J., Chien, S. & Schwartz, M. A. Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. EMBO J. 20, 4639-4647 (2001). (Pubitemid 32848617)