Shear stress modulates VCAM-1 expression in response to TNF-α and dietary lipids via interferon regulatory factor-1 in cultured endothelium

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 305, Issue 8, 2013, Pages

  Deverse, J Sherrod ^a   Sandhu, Angad S ^a   Mendoza, Natalie ^a   Edwards, Christina M ^a   Sun, Chongxiu ^a   Simon, Scott I ^a   Passerini, Anthony G ^a  

^a Davis   (United States)

Author keywords

Atherosclerosis; Endothelial dysfunction; Hemodynamics; Hypertriglyceridemia; Inflammation; Tumor necrosis factor ; Vascular cell adhesion molecule 1

Indexed keywords

INTERFERON REGULATORY FACTOR 1; LIPOPROTEIN; SMALL INTERFERING RNA; TRIGLYCERIDE RICH LIPOPROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOTHELIUM CELL; FAT INTAKE; GENETIC TRANSFECTION; HEMODYNAMICS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MICROFLUIDICS; MOLECULAR MECHANICS; MONOLAYER CULTURE; NONHUMAN; PORCINE MODEL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SHEAR STRESS; UPREGULATION; WESTERN BLOTTING;

ATHEROSCLEROSIS; ENDOTHELIAL DYSFUNCTION; HEMODYNAMICS; HYPERTRIGLYCERIDEMIA; INFLAMMATION; TUMOR NECROSIS FACTOR-Α; VASCULAR CELL ADHESION MOLECULE 1;

ANIMALS; AORTA; CELLS, CULTURED; DIETARY FATS; ENDOTHELIAL CELLS; INTERFERON REGULATORY FACTOR-1; POSTPRANDIAL PERIOD; STRESS, MECHANICAL; SWINE; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84885662512     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00311.2013     Document Type: Article

References (45)

1. Berk BC, Abe JI, Min W, Surapisitchat J, Yan C. Endothelial athero-protective and anti-inflammatory mechanisms. Ann NY Acad Sci 947: 93-111, 2001.
2. Bhullar IS, Li YS, Miao H, Zandi E, Kim M, Shyy JY, Chien S. Fluid shear stress activation of IkappaB kinase is integrin-dependent. J Biol Chem 273: 30544-30549, 1998.
3. Boon RA, Horrevoets AJ. Key transcriptional regulators of the vasopro-tective effects of shear stress. Hamostaseologie 29: 33-41, 2009.
4. Chappell DC, Varner SE, Nerem RM, Medford RM, Alexander RW. Oscillatory shear stress stimulates adhesion molecule expression in cultured human endothelium. Circ Res 82: 532-539, 1998.
5. Cheng C, Tempel D, van Haperen R, van der Baan A, Grosveld F, Daemen MJ, Krams R, de Crom R. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation 113: 2744-2753, 2006.
6. Chiu JJ, Chien S. Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol Rev 91: 327-387, 2011.
7. Chiu JJ, Lee PL, Chen CN, Lee CI, Chang SF, Chen LJ, Lien SC, Ko YC, Usami S, Chien S. Shear stress increases ICAM-1 and decreases VCAM-1 and E-selectin expressions induced by tumor necrosis factor-a in endothelial cells. Arterioscler Thromb Vase Biol 24: 73-79, 2004.
8. Civelek M, Manduchi E, Riley RJ, Stoeckert CJ Jr, Davies PF. Chronic endoplasmic reticulum stress activates unfolded protein response in arterial endothelium in regions of susceptibility to atherosclerosis. Circ Res 105: 453-461, 2009.
9. Collins T, Cybulsky MI. NF-kB: pivotal mediator or innocent bystander in atherogenesis? J Clin Invest 107: 255-264, 2001.
10. Dagia NM, Harii N, Meli AE, Sun X, Lewis CJ, Kohn LD, Goetz DJ. Phenyl methimazole inhibits TNF-α-induced VCAM-1 expression in an IFN regulatory factor-1-dependent manner and reduces monocytic cell adhesion to endothelial cells. J Immunol 173: 2041-2049, 2004.
11. Dai G, Kaazempur-Mofrad MR, Natarajan S, Zhang Y, Vaughn S, Blackman BR, Kamm RD, Garcia-Cardena G, Gimbrone MA Jr. Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and-resistant regions of human vascula-ture. Proc Natl Acad Sci USA 101: 14871-14876, 2004.
12. Davies PF, Civelek M, Fang Y, Guerraty MA, Passerini AG. Endothelial heterogeneity associated with regional athero-susceptibility and adaptation to disturbed blood flow in vivo. Semin Thromb Hemost 36: 265-275, 2010.
13. DeVerse JS, Bailey KA, Foster GA, Mittal V, Altman SM, Simon SI, Passerini AG. On-chip endothelial inflammatory phenotyping. J Vis Exper: e4169, 2012.
14. Deverse JS, Bailey KA, Jackson KN, Passerini AG. Shear stress modulates RAGE-mediated inflammation in a model of diabetes-induced metabolic stress. Am J Physiol Heart Circ Physiol 302: H2498-H2508, 2012.
15. Fang Y, Shi C, Manduchi E, Civelek M, Davies PF. MicroRNA-10a regulation of proinflammatory phenotype in athero-susceptible endothelium in vivo and in vitro. Proc Natl Acad Sci USA 107: 13450-13455, 2010.
16. Glagov S, Zarins C, Giddens DP, Ku DN. Hemodynamics and atherosclerosis. Insights and perspectives gained from studies of human arteries. Arch Pathol Lab Med 112: 1018-1031, 1988.
17. Gower RM, Wu H, Foster GA, Devaraj S, Jialal I, Ballantyne CM, Knowlton AA, Simon SI. CD11c/CD18 expression is upregulated on blood monocytes during hypertriglyceridemia and enhances adhesion to vascular cell adhesion molecule-1. Arterioscler Thromb Vase Biol 31: 160-166, 2011.
18. Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C. Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 109: 433-438, 2004.
19. Harry BL, Sanders JM, Feaver RE, Lansey M, Deem TL, Zarbock A, Bruce AC, Pryor AW, Gelfand BD, Blackman BR, Schwartz MA, Ley K. Endothelial cell PECAM-1 promotes atherosclerotic lesions in areas of disturbed flow in ApoE-deficient mice. Arterioscler Thromb Vase Biol 28: 2003-2008, 2008.
20. Holvoet P, Davey PC, De Keyzer D, Doukoure M, Deridder E, Bochaton-Piallat ML, Gabbiani G, Beaufort E, Bishay K, Andrieux N, Benhabiles N, Marguerie G. Oxidized low-density lipoprotein correlates positively with toll-like receptor 2 and interferon regulatory factor-1 and inversely with superoxide dismutase-1 expression: studies in hypercholes-terolemic swine and THP-1 cells. Arterioscler Thromb Vase Biol 26: 1558-1565, 2006.
21. Hotamisligil GS. Inflammation and metabolic disorders. Nature 444: 860-867, 2006.
22. Huo Y, Hafezi-Moghadam A, Ley K. Role of vascular cell adhesion molecule-1 and fibronectin connecting segment-1 in monocyte rolling and adhesion on early atherosclerotic lesions. Circ Res 87: 153-159, 2000.
23. Huo Y, Ley K. Adhesion molecules and atherogenesis. Acta Physiol Scand 173: 35-43, 2001.
24. Libby P. Inflammation in atherosclerosis. Nature 420: 868-874, 2002.
25. Mestas J, Ley K. Monocyte-endothelial cell interactions in the development of atherosclerosis. Trends Cardiovasc Med 18: 228-232, 2008.
26. Miller M, Stone NJ, Ballantyne C, Bittner V, Criqui MH, Ginsberg HN, Goldberg AC, Howard WJ, Jacobson MS, Kris-Etherton PM, Lennie TA, Levi M, Mazzone T, Pennathur S. Triglycerides and cardiovascular disease: a scientific statement from the American Heart Association. Circulation 123: 2292-2333, 2011.
27. Mohan S, Mohan N, Valente AJ, Sprague EA. Regulation of low shear flow-induced HAEC VCAM-1 expression and monocyte adhesion. Am J Physiol Cell Physiol 276: C1100-C1107, 1999.
28. Nam D, Ni CW, Rezvan A, Suo J, Budzyn K, Llanos A, Harrison D, Giddens D, Jo H. Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am J Physiol Heart Circ Physiol 297: H1535-H1543, 2009.
29. Neish AS, Khachigian LM, Park A, Baichwal VR, Collins T. Sp1 is a component of the cytokine-inducible enhancer in the promoter of vascular cell adhesion molecule-1. J Biol Chem 270: 28903-28909, 1995.
30. Neish AS, Read MA, Thanos D, Pine R, Maniatis T, Collins T. Endothelial interferon regulatory factor 1 cooperates with NF-kB as a transcriptional activator of vascular cell adhesion molecule 1. Mol Cell Biol 15: 2558-2569, 1995.
31. Nigro P, Abe J, Berk BC. Flow shear stress and atherosclerosis: a matter of site specificity. Antioxid Redox Signal 15: 1405-1414, 2011.
32. Passerini AG, Polacek DC, Shi C, Francesco NM, Manduchi E, Grant GR, Pritchard WF, Powell S, Chang GY, Stoeckert CJ Jr, Davies PF. Coexisting proinflammatory and antioxidative endothelial transcription profiles in a disturbed flow region of the adult porcine aorta. Proc Natl Acad Sci USA 101: 2482-2487, 2004.
33. Patsch JR, Miesenbock G, Hopferwieser T, Muhlberger V, Knapp E, Dunn JK, Gotto AM Jr, Patsch W. Relation of triglyceride metabolism and coronary artery disease. Studies in the postprandial state. Arterioscler Thromb 12: 1336-1345, 1992.
34. Rossi J, Rouleau L, Emmott A, Tardif JC, Leask RL. Laminar shear stress prevents simvastatin-induced adhesion molecule expression in cy-tokine activated endothelial cells. Eur J Pharmacol 649: 268-276, 2010.
35. Saha B, Jyothi Prasanna S, Chandrasekar B, Nandi D. Gene modulation and immunoregulatory roles of interferon gamma. Cytokine 50: 1-14, 2010.
36. Sun C, Alkhoury K, Wang YI, Foster GA, Radecke CE, Tarn K, Edwards CM, Facciotti MT, Armstrong EJ, Knowlton AA, Newman JW, Passerini AG, Simon SI. IRF-1 and miRNA126 modulate VCAM-1 expression in response to a high-fat meal. Circ Res 111: 1054-1064, 2012.
37. Suo J, Ferrara DE, Sorescu D, Guldberg RE, Taylor WR, Giddens DP. Hemodynamic shear stresses in mouse aortas: implications for atherogenesis. Arterioscler Thromb Vase Biol 27: 346-351, 2007.
38. Tamura T, Yanai H, Savitsky D, Taniguchi T. The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol 26: 535-584, 2008.
39. Ting HJ, Stice JP, Schaff UY, Hui DY, Rutledge JC, Knowlton AA, Passerini AG, Simon SI. Triglyceride-rich lipoproteins prime aortic endothelium for an enhanced inflammatory response to tumor necrosis factor-a. Circ Res 100: 381-390, 2007.
40. Tsou JK, Gower RM, Ting HJ, Schaff UY, Insana MF, Passerini AG, Simon SI. Spatial regulation of inflammation by human aortic endothelial cells in a linear gradient of shear stress. Microcirculation 15: 311-323, 2008.
41. Usami S, Chen HH, Zhao Y, Chien S, Skalak R. Design and construction of a linear shear stress flow chamber. Ann Biomed Eng 21: 77-83, 1993.
42. Vogel RA, Corretti MC, Plotnick GD. Effect of a single high-fat meal on endothelial function in healthy subjects. Am J Cardiol 79: 350-354, 1997.
43. Wang F, Xia W, Liu F, Li J, Wang G, Gu J. Interferon regulator factor 1/retinoic inducible gene I (IRF1/RIG-I) axis mediates 25-hydroxycholes-terol-induced interleukin-8 production in atherosclerosis. Cardiovasc Res 93: 190-199, 2012.
44. Wang YI, Schulze J, Raymond N, Tomita T, Tarn K, Simon SI, Passerini AG. Endothelial inflammation correlates with subject triglycerides and waist size after a high-fat meal. Am J Physiol Heart Circ Physiol 300: H784-H791, 2011.
45. Zilversmit DB. Atherogenesis: a postprandial phenomenon. Circulation 60: 473-485, 1979.