The role of shear stress in atherosclerosis: Action through gene expression and inflammation?

Cell Biochemistry and Biophysics

Volumn 41, Issue 2, 2004, Pages 279-294

  Cheng, Caroline ^a,b   De Crom, Rini ^b   Van Haperen, Rien ^b   Helderman, Frank ^b   Gourabi, Babak Mousavi ^b   Van Damme, Luc C A ^b   Kirschbaum, Sharon W ^b   Slager, Cornelis J ^b   Van Der Steen, Anton F W ^b   Krams, Rob ^b  

^a ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Atherosclerosis; Gene expression; Inflammation; Shear stress

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; GREEN FLUORESCENT PROTEIN; PROSTAGLANDIN SYNTHASE; SUPEROXIDE DISMUTASE;

ANIMAL; ATHEROSCLEROSIS; BIOLOGICAL MODEL; BLOOD VESSEL; DISEASE MODEL; GENE EXPRESSION REGULATION; HUMAN; INFLAMMATION; MECHANICAL STRESS; METABOLISM; MOUSE; OSCILLOMETRY; PATHOLOGY; REVIEW;

ANIMALS; ATHEROSCLEROSIS; BLOOD VESSELS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GREEN FLUORESCENT PROTEINS; HUMANS; INFLAMMATION; MICE; MODELS, BIOLOGICAL; NITRIC OXIDE SYNTHASE TYPE III; OSCILLOMETRY; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; STRESS, MECHANICAL; SUPEROXIDE DISMUTASE;

ANIMALIA;

EID: 22844448375     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1385/CBB:41:2:279     Document Type: Review

References (97)

1. Shaaban, A. M. and Duerinckx, A. J.. (2000) Wall shear stress and early atherosclerosis: a review. AJR Am. J. Roentgenol. 174, 1657-1665.
2. Barakat, A. and Lieu, D. (2003) Differential responsiveness of vascular endothelial cells to different types of fluid mechanical shear stress. Cell Biochem. Biophys. 38, 323-343.
3. McCormick, S. M., Frye, S. R., Eskin, S. G., Teng, C. L., Lu, C. M., Russell, C. G., et al. (2003) Microarray analysis of shear stressed endothelial cells. Biorheology 40, 5-11.
4. Shyy, J. Y. and Chien S.. (2002) Role of integrins in endothelial mechanosensing of shear stress. Circ. Res. 91, 769-775.
5. Malek, A. M. and Izumo S. (1995) Control of endothelial cell gene expression by flow. J. Biomech. 28, 1515-1528.
6. Takahashi, M., Ishida, T., Traub, O., Corson, M. A., and Berk B. C.. (1997) Mechanotransduction in endothelial cells: temporal signaling events in response to shear stress. J. Vasc. Res. 34, 212-219.
7. Wentzel, J. J., Kloet, J., Andhyiswara, I., Oomen, J. A., Schuurbiers, J. C., de Smet, B. J., et al. (2001) Shear-stress and wall-stress regulation of vascular remodeling after balloon angioplasty: effect of matrix metalloproteinase inhibition. Circulation 104, 91-96.
8. Wentzel, J. J., Krams, R., Schuurbiers, J. C., Oomen, J. A., Kloet, J., van Der Giessen, W. J., et al. (2001) Relationship between neointimal thickness and shear stress after Wallstent implantation in human coronary arteries. Circulation 103, 1740-1745.
9. Wentzel, J. J., Whelan, D. M., van der Giessen, W. J., van Beusekom, H. M., Andhyiswara, I., Serruys, P. W., et al. (2000) Coronary stent implantation changes 3-D vessel geometry and 3-D shear stress distribution. J. Biomech. 33, 1287-1295.
10. Krams, R., Wentzel, J. J., Cespedes, I., Vinke, R., Carlier, S., van der Steen, A. F., et al. (1999) Effect of catheter placement on 3-D velocity profiles in curved tubes resembling the human coronary system. Ultrasound Med. Biol. 25, 803-810.
11. Krams, R., Wentzel, J. J., Oomen, J. A., Schuurbiers, J. C., Andhyiswara, I., Kloet, J., et al. (1998) Shear stress in atherosclerosis, and vascular remodelling. Semin. Interv. Cardiol. 3, 39-44.
12. Krams, R., Wentzel, J. J., Oomen, J. A., Vinke, R., Schuurbiers, J. C., de Feyter, P. J., et al. (1997) Evaluation of endothelial shear stress and 3D geometry as factors determining the development of atherosclerosis and remodeling in human coronary arteries in vivo. Combining 3D reconstruction from angiography and IVUS (ANGUS) with computational fluid dynamics. Arterioscler. Thromb. Vasc. Biol. 17, 2061-2065.
13. Bom, N., de Korte, C. L., Wentzel, J. J., Krams, R., Carlier, S. G., van der Steen, A. W., et al. (2000) Quantification of plaque volume, shear stress on the endothelium, and mechanical properties of the arterial wall with intravascular ultrasound imaging. Z. Kardiol. 89, 105-111.
14. Carlier, S. G., van Damme, L. C., Blommerde, C. P., Wentzel, J. J., van Langehove, G., Verheye, S., et al. (2003) Augmentation of wall shear stress inhibits neointimal hyperplasia after stent implantation: inhibition through reduction of inflammation? Circulation 107, 2741-2746.
15. Doroudi, R., Gan, L. M., Selin Sjogren L., and Jern, S. (2000) Effects of shear stress on eicosanoid gene expression and metabolite production in vascular endothelium as studied in a novel biomechanical perfusion model. Biochem. Biophys. Res. Commun. 269, 257-264.
16. Galbraith, C. G., Skalak R., and Chien, S. (1998) Shear stress induces spatial reorganization of the endothelial cell cytoskeleton. Cell Motil. Cytoskeleton. 40, 317-330.
17. Gan, L., Miocic, M., Doroudi, R., Selin-Sjogren L., and Jern, S. (2000) Distinct regulation of vascular endothelial growth factor in intact human conduit vessels exposed to laminar fluid shear stress and pressure. Biochem. Biophys. Res. Commun. 272, 490-496.
18. Honda, H. M., Hsiai, T., Wortham, C. M., Chen, M., Lin, H., Navab, M., et al. (2001) A complex flow pattern of low shear stress and flow reversal promotes monocyte binding to endothelial cells. Atherosclerosis 158, 385-390.
19. Hsiai, T. K., Cho, S. K., Reddy S., Hama, S., Navab, M., Demer, L. L., et al. (2001) Pulsatile flow regulates monocyte adhesion to oxidized lipid-induced endothelial cells. Arterioscler. Thromb. Vasc. Biol. 21, 1770-1776.
20. Ishibashi, H., Sunamura, M., and Karino, T. (1995) Flow patterns and preferred sites of intimal thickening in end-to-end anastomosed vessels. Surgery 117, 409-420.
21. Ku, D. N., Giddens, D. P., Zarins, C. K., and Glagov, S. (1985) Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis 5, 293-302.
22. Cheng, C. P., Herfkens, R. J., and Taylor, C. A. (2003) Abdominal aortic hemodynamic conditions in healthy subjects aged 50-70 at rest and during lower limb exercise: in vivo quantification using MRI. Atherosclerosis 168, 323-331.
23. Cheng, C. P., Herfkens, R. J., and Taylor, C. A. (2003) Comparison of abdominal aortic hemodynamics between men and women at rest and during lower limb exercise. J. Vasc. Surg. 37, 118-123.
24. Buchanan Jr., J. R., Kleinstreuer, C., Truskey, G. A., and Lei, M. (1999) Relation between non-uniform hemodynamics and sites of altered permeability and lesion growth at the rabbit aorto-celiac junction. Atherosclerosis 143, 27-40.
25. Kanai, A. J., Strauss, H. C., Truskey, G. A., Crews, A. L., Grunfeld, S., and Malinski, T. (1995) Shear stress induces ATP-independent transient nitric oxide release from vascular endothelial cells, measured directly with a porphyrinic microsensor. Circ. Res. 77, 284-293.
26. Malinauskas, R. A., Sarraf, P., Barber, K. M., and Truskey, G. A. (1998) Association between secondary flow in models of the aorto-celiac junction and subendothelial macrophages in the normal rabbit. Atherosclerosis 140, 121-134.
27. Truskey, G. A., Herrmann, R. A., Kait, J. and Barber, K. M. (1999) Focal increases in vascular cell adhesion molecule-1 and intimal macrophages at atherosclerosis-susceptible sites in the rabbit aorta after short-term cholesterol feeding. Arterioscler. Thromb. Vasc. Biol. 19, 393-401.
28. Ando, J., Tsuboi, H., Korenaga, R., Takahashi, K., Kosaki, K., Isshiki, M., et al. (1996) Differential display and cloning of shear stress-responsive messenger RNAs in human endothelial cells. Biochem. Biophys. Res. Commun. 225, 347-351.
29. Bongrazio, M., Baumann, C., Zakrzewicz, A., Pries, A. R., and Gaehtgens, P. (2000) Evidence for modulation of genes involved in vascular adaptation by prolonged exposure of endothelial cells to shear stress. Cardiovasc. Res. 47, 384-393.
30. Topper, J. N., Cai, J., Qiu, Y., Anderson, K. R., Xu, Y. Y., Deeds, J. D., et al. (1997) Vascular MADs: two novel MAD-related genes selectively inducible by flow in human vascular endothelium. Proc. Natl. Acad. Sci. U. S. A. 94, 9314-9319.
31. Topper, J. N., Cai, J., Falb, D., and Gimbrone Jr., M. A. (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. U. S. A. 93, 10417-10422.
32. McCormick, S. M., Eskin, S. G., McIntire, L. V., Teng, C. L., Lu, C. M., Russell, C. G., et al. (2001) DNA microarray reveals changes in gene expression of shear stressed human umbilical vein endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 98, 8955-8960.
33. Dekker, R. J., van Soest, S., Fontijn, R. D., Salamanca, S., de Groot, P. G., VanBavel, E., et al. (2002) Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Kruppel-like factor (KLF2). Blood 100, 1689-1698.
34. McCormick, S. M., Eskin, S. G., McIntire, L. V., Teng, C. L., Lu, C. M., Russell, C. G., et al. (2001) DNA microarray reveals changes in gene expression of shear stressed human umbilical vein endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 98, 8955-8960.
35. Chen, B. P., Li, Y. S., Zhao, Y., Chen, K. D., Li, S., Lao, J., et al. (2001) DNA microarray analysis of gene expression in endothelial cells in response to 24-h shear stress. Physiol. Genomics 7, 55-63.
36. Brooks, A. R., Lelkes, P. I., and Rubanyi, G. M. (2002) Gene expression profiling of human aortic endothelial cells exposed to disturbed flow and steady laminar flow. Physiol. Genomics 9, 27-41.
37. Zhao, Y., Chen, B. P., Miao, H., Yuan, S., Li, Y. S., Hu, Y., et al. (2002) Improved significance test for DNA microarray data: temporal effects of shear stress on endothelial genes. Physiol. Genomics 12, 1-11.
38. Peters, D. G., Zhang, X. C., Benos, P. V., Heidrich-O'Hare, E., and Ferrell, R. E. (2002) Genomic analysis of immediate/early response to shear stress in human coronary artery endothelial cells. Physiol. Genomics 12, 25-33.
39. Ziegler, T., Bouzourene, K., Harrison, V. J., Brunner, H. R., and Hayoz, D. (1998) Influence of oscillatory and unidirectional flow environments on the expression of endothelin and nitric oxide synthase in cultured endothelial cells. Arterioscler. Thromb. Vasc. Biol. 18, 686-692.
40. Silacci, P., Formentin, K., Bouzourene, K., Daniel, F., Brunner, H. R., and Hayoz, D. (2000) Unidirectional and oscillatory shear stress differentially modulate NOS III gene expression. Nitric Oxide 4, 47-56.
41. Chappell, D. C., Varner, S. E., Nerem, R. M., Medford, R. M., and Alexander, R. W. (1998) Oscillatory shear stress stimulates adhesion molecule expression in cultured human endothelium. Circ. Res. 82, 532-539.
42. Roach, M. R. and Stockley, D. (1980) The effects of the geometry of a stenosis on poststenotic flow in models and poststenotic vibration of canine carotid arteries in vivo. J. Biomech. 13, 623-634.
43. van Haperen, R., de Waard, M., van Deel, E., Mees, B., Kutryk, M., van Aken, T., et al. (2002) Reduction of blood pressure, plasma cholesterol, and atherosclerosis by elevated endothelial nitric oxide. J. Biol. Chem. 277, 48803-48807.
44. Blair, A., Shaul, P. W., Yuhanna, I. S., Conrad, P. A., and Smart, E. J. (1999) Oxidized low density lipoprotein displaces endothelial nitric-oxide synthase (eNOS) from plasmalemmal caveolae and impairs eNOS activation. J. Biol. Chem. 274, 32512-32519.
45. Gimbrone, Jr., M. A., Topper, J. N., Nagel, T., Anderson, K. R., and Garcia-Cardena, G. (2000) Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann. N. Y. Acad. Sci. 902, 230-9; discussion 239-240.
46. Takada, Y., Kato, C., Kondo, S., Korenaga, R., and Ando, J. (1997) Cloning of cDNAs encoding G protein-coupled receptor expressed in human endothelial cells exposed to fluid shear stress. Biochem. Biophys. Res. Commun. 240, 737-741.
47. Resnick, N., Yahav, H., Khachigian, L. M., Collins, T., Anderson, K. R., Dewey, F. C., et al. (1997) Endothelial gene regulation by laminar shear stress. Adv. Exp. Med. Biol. 430, 155-164.
48. Garcia-Cardena, G., Comander, J., Anderson, K. R., Blackman, B. R., and Gimbrone Jr., M. A. (2001) Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc. Natl. Acad. Sci. U. S. A. 98, 4478-4485.
49. Malek, A. M., Zhang, J., Jiang, J., Alper, S. L., and Izumo, S. (1999) Endothelin-1 gene suppression by shear stress: pharmacological evaluation of the role of tyrosine kinase, intracellular calcium, cytoskeleton, and mechanosensitive channels. J. Mol. Cell. Cardiol. 31, 387-399.
50. Gan, L. M., Selin-Sjogren, L., Doroudi, R., and Jern, S. (2000) Temporal regulation of endothelial ET-1 and eNOS expression in intact human conduit vessels exposed to different intraluminal pressure levels at physiological shear stress. Cardiovasc. Res. 48, 168-177.
51. Zhu, Z. G., Li, H. H., and Zhang, B. R. (1997) Expression of endothelin-1 and constitutional nitric oxide synthase messenger RNA in saphenous vein endothelial cells exposed to arterial flow shear stress. Ann. Thorac. Surg. 64, 1333-1338.
52. Morawietz, H., Talanow, R., Szibor, M., Rueckschloss, U., Schubert, A., Bartling, B., et al. (2000) Regulation of the endothelin system by shear stress in human endothelial cells. J. Physiol. 525 Pt 3, 761-770.
53. Malek, A. M., Greene, A. L., and Izumo, S. (1993) Regulation of endothelin 1 gene by fluid shear stress is transcriptionally mediated and independent of protein kinase C and cAMP. Proc. Natl. Acad. Sci. U. S. A. 90, 5999-6003.
54. Qiu, Y. and Tarbell, J. M. (2000) Interaction between wall shear stress and circumferential strain affects endothelial cell biochemical production. J. Vasc. Res. 37, 147-157.
55. Okahara, K., Sun, B., and Kambayashi, J. (1998) Upregulation of prostacyclin synthesis-related gene expression by shear stress in vascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 18, 1922-196.
56. Rieder, M. J., Carmona, R., Krieger, J. E., Pritchard Jr., K. A., and Greene, A. S. (1997) Suppression of angiotensin-converting enzyme expression and activity by shear stress. Circ. Res. 80, 312-319.
57. Woodman, C. R., Muller, J. M., Rush, J. W., Laughlin, M. H., and Price, E. M. (1999) Flow regulation of ecNOS and Cu/Zn SOD mRNA expression in porcine coronary arterioles. Am. J. Physiol. 276, H1058-H1063.
58. Inoue, N., Ramasamy, S., Fukai, T., Nerem, R. M., and Harrison, D. G. (1996) Shear stress modulates expression of Cu/Zn superoxide dismutase in human aortic endothelial cells. Circ. Res. 79, 32-37.
59. Hamilton, C. A., Berg, G., McIntyre, M., McPhaden, A. R., Reid, J. L., and Dominiczak, A. F. (1997) Effects of nitric oxide and superoxide on relaxation in human artery and vein. Atherosclerosis 133, 77-86.
60. Taner, C. B., Severson, S. R., Best, P. J., Lerman, A., and Miller, V. M. (2001) Treatment with endothelin-receptor antagonists increases NOS activity in hypercholesterolemia. J. Appl. Physiol. 90, 816-820.
61. Murakoshi, N., Miyauchi, T., Kakinuma, Y., Ohuchi, T., Goto, K., Yanagisawa, M., et al. (2002) Vascular endothelin-B receptor system in vivo plays a favorable inhibitory role in vascular remodeling after injury revealed by endothelin-B receptor-knockout mice. Circulation 106, 1991-1998.
62. Hendrickson, R. J., Cappadona, C., Yankah, E. N., Sitzmann, J. V., Cahill, P. A., and Redmond, E. M. (1999) Sustained pulsatile flow regulates endothelial nitric oxide synthase and cyclooxygenase expression in co-cultured vascular endothelial and smooth muscle cells. J. Mol. Cell. Cardiol. 31, 619-629.
63. Prasad, A., Zhu, J., Halcox, J. P., Waclawiw, M. A., Epstein, S. E., and Quyyumi, A. A. (2002) Predisposition to atherosclerosis by infections: role of endothelial dysfunction. Circulation 106, 184-190.
64. Wick, G., Perschinka, H., and Xu, Q. (1999) Autoimmunity and atherosclerosis. Am. Heart J. 138, S444-S449.
65. Millonig, G., Niederegger, H., Rabl, W., Hochleitner, B. W., Hoefer, D., Romani, N., et al. (2001) Network of vascular-associated dendritic cells in intima of healthy young individuals. Arterioscler. Thromb. Vasc. Biol. 21, 503-508.
66. Waltner-Romen, M., Falkensammer, G., Rabl, W., and Wick, G. (1998) A previously unrecognized site of local accumulation of mononuclear cells. The vascular-associated lymphoid tissue. J. Histochem. Cytochem. 46, 1347-1350.
67. Millonig, G., Malcom, G. T., and Wick, G. (2002) Early inflammatory-immunological lesions in juvenile atherosclerosis from the Pathobiological Determinants of Atherosclerosis in Youth (PDAY)-study Atherosclerosis 160, 441-448.
68. Wick, G., Perschinka, H., and Millonig, G. (2001) Atherosclerosis as an autoimmune disease: an update. Trends Immunol. 22, 665-669.
69. Libby P., Ridker, P. M., and Maseri, A. (2002) Inflammation and atherosclerosis. Circulation 105, 1135-1143.
70. Berk, B. C., Abe, J. I., Min, W., Surapisitchat, J., and Yan, C. (2001) Endothelial atheroprotective and anti-inflammatory mechanisms. Ann. N. Y. Acad. Sci. 947, 93-109; discussion 109-111.
71. Hansson, G. K. (2001) Regulation of immune mechanisms in atherosclerosis. Ann. N. Y. Acad Sci. 947, 157-65; discussion 165-166.
72. Frostegard, J., Ulfgren, A. K., Nyberg, P., Hedin, U., Swedenborg, J., Andersson, U., et al. (1999) Cytokine expression in advanced human atherosclerotic plaques: dominance of pro-inflammatory (Th1) and macrophage-stimulating cytokines. Atherosclerosis 145, 33-43.
73. de Boer, O. J., Hirsch, F., van der Wal, A. C., van der Loos, C. M., Das, P. K., and Becker, A. E. (1997) Costimulatory molecules in human atherosclerotic plaques: an indication of antigen specific T lymphocyte activation. Atherosclerosis 133, 227-234.
74. Mach, F., Schonbeck, U., and Libby, P. (1998) CD40 signaling in vascular cells: a key role in atherosclerosis? Atherosclerosis 137 Suppl, S89-S95.
75. Bobryshev, Y. V. and Lord, R. S. (1998) Mapping of vascular dendritic cells in atherosclerotic arteries suggests their involvement in local immune-inflammatory reactions. Cardiovasc. Res. 37, 799-810.
76. Korenaga, R., Ando, J., Kosaki, K., Isshiki, M., Takada, Y., and Kamiya, A. (1997) Negative transcriptional regulation of the VCAM-1 gene by fluid shear stress in murine endothelial cells. Am. J. Physiol. 273, C1506-C1515.
77. Tsao, P. S., Buitrago, R., Chan, J. R., and Cooke, J. P. (1996) Fluid flow inhibits endothelial adhesiveness. Nitric oxide and transcriptional regulation of VCAM-1. Circulation 94, 1682-1689.
78. Ishida, T., Takahashi, M., Corson, M. A., and Berk, B. C. (1997) Fluid shear stress-mediated signal transduction: how do endothelial cells transduce mechanical force into biological responses? Ann. N. Y. Acad. Sci. 811, 12-23; discussion 23-24.
79. Gonzales, R. S. and Wick, T. M. (1996) Hemodynamic modulation of monocytic cell adherence to vascular endothelium. Ann. Biomed. Eng. 24, 382-393.
80. Dirksen, M. T., van der Wal, A. C., van den Berg, F. M., van der Loos, C. M., and Becker, A. E. (1998)Distribution of inflammatory cells in atherosclerotic plaques relates to the direction of flow. Circulation 98, 2000-2003.
81. Aikawa, M., Rabkin, E., Okada, Y., Voglic, S. J., Clinton, S. K., Brinckerhoff, C. E., et al. (1998) Lipid lowering by diet reduces matrix metalloproteinase activity and increases collagen content of rabbit atheroma: a potential mechanism of lesion stabilization. Circulation 97, 2433-2344.
82. Fukumoto, Y., Libby, P., Rabkin, E., Hill, C. C., Enomoto, M., Hirouchi, Y., et al. (2001) Statins alter smooth muscle cell accumulation and collagen content in established atheroma of watanabe heritable hyperlipidemic rabbits. Circulation 103, 993-999.
83. Galis, Z. S., Sukhova, G. K., Lark, M. W., and Libby, P. (1994) Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J. Clin. Invest. 94, 2493-2503.
84. Z. S. Galis and J. J. Khatri. (2002)Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res. 90, 251-262.
85. Mohan, S., Mohan, N., Valente, A. J., and Sprague, E. A. (1999) Regulation of low shear flow-induced HAEC VCAM-1 expression and monocyte adhesion. Am. J. Physiol. 276, C1100-C1107.
86. Morigi, M., Zoja, C., Figliuzzi, M., Foppolo, M., Micheletti, G., Bontempelli, M., et al. (1995) Fluid shear stress modulates surface expression of adhesion molecules by endothelial cells. Blood 85, 1696-1703.
87. Houston, P., Dickson, M. C., Ludbrook, V., White, B., Schwachtgen, J. L., McVey, J. H. et al. (1999) Fluid shear stress induction of the tissue factor promoter in vitro and in vivo is mediated by Egr-1. Arterioscler. Thromb. Vasc. Biol. 19, 281-289.
88. Murase, T., Kume, N., Korenaga, R., Ando, J., Sawamura, T., Masaki, T., et al. (1998) Fluid shear stress transcriptionally induces lectin-like oxidized LDL receptor-1 in vascular endothelial cells. Circ. Res. 83, 328-333.
89. Harrison, D. G., Sayegh, H., Ohara, Y., Inoue N., and Venema, R. C. (1996) Regulation of expression of the endothelial cell nitric oxide synthase. Clin. Exp. Pharmacol. Physiol. 23, 251-255.
90. Resnick, N., Collins, T., Atkinson, W., Bonthron, D. T., Dewey Jr., C. F., and Gimbrone Jr., M. A. (1993) Platelet-derived growth factor B chain promoter contains a cis-acting fluid shear-stress-responsive element [published erratum appears in Proc. Natl. Acad. Sci. U. S. A. 1993 Aug 15;90:7908]. Proc. Natl. Acad. Sci. U. S. A. 90, 4591-4595.
91. Ohno, M., Cooke, J.P., Dzau, V.J., and Gibbons, G.H. (1995) Fluid shear stress induces endothelial transforming growth factor β-1 transcription and production. Modulation by potassium channel blockade. J. Clin. Invest. 95, 1363-1369.
92. Walpola, P. L., Gotlieb, A. I., Cybulsky, M. I., and Langille, B. L. (1995) Expression of ICAM-1 and VCAM-1 and monocyte adherence in arteries exposed to altered shear stress. Arterioscler. Thromb. Vasc. Biol. 15, 2-10.
93. Singh, T. M., Abe, K. Y., Sasaki, T., Zhuang, Y. J., Masuda, H., and Zarins, C. K. (1998) Basic fibroblast growth factor expression precedes flow-induced arterial enlargement. J. Surg. Res. 77, 165-173.
94. Tulis, D.A., and Prewitt, R.L. (1998) Medial and endothelial platelet-derived growth factor A chain expression is regulated by in vivo exposure to elevated flow. J. Vasc. Res. 35, 413-420.
95. Bassiouny H.S., Song, R.H., Hong, X.F., Singh, A., Kocharyan, H., and Glagov, S. (1998) Flow regulation of 72-kD collagenase IV (MMP-2) after experimental arterial injury. Circulation 98, 157-163.
96. Yoshisue, H., Suzuki, K,. Kawabata, A., Ohya, T., Zhao, H., Sakurada, K., et al. (2002) Large scale isolation of non-uniform shear stress-responsive genes from cultured human endothelial cells through the preparation of a subtracted cDNA library. Atherosclerosis 162, 323-334.
97. Wasserman, S. M., Mehraban, P., Komuves, L. G., Yang, R. B., Tomlinson, J. E., Zhang, Y. et al. (2002) Gene expression profile of human endothelial cells exposed to sustained fluid shear stress. Physiol. Genomics 12, 13-23.