Fluid shear stress activation of egr-1 transcription in cultured human endothelial and epithelial cells is mediated via the extracellular signal- related kinase 1/2 mitogen-activated protein kinase pathway

Journal of Clinical Investigation

Volumn 101, Issue 11, 1998, Pages 2540-2549

  Schwachtgen, Jean Luc ^a   Houston, Parul ^a   Campbell, Callum ^a   Sukhatme, Vikas ^b   Braddock, Martin ^a  

^a GLAXOSMITHKLINE   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Autoregulation; Egr 1 promoter; Extracellular signal related kinase 1 2 mitogen activated protein kinase; Fluid shear stress; Vascular endothelial cells

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; ONCOPROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; CELL CULTURE; DNA FLANKING REGION; GENE DELETION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; REPORTER GENE; RNA TRANSLATION; SHEAR STRESS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

EID: 0032102209     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1404     Document Type: Article

References (68)

1. Franke, R.P., M. Grafe, H. Schnittler, D. Seiffge, C. Mittermayer, and D. Drenckhahn. 1984. Induction of human vascular endothelial stress fibers by fluid shear stress. Nature. 307:648-649.
2. Malek, A.M., and S. Izumo. 1996. Mechanism of endothelial cell shape change and cytoskeletal remodeling in response to fluid shear stress. J. Cell Sci. 109:713-726.
3. Cucina, A., A.V. Sterpetti, G. Pupelis, A. Fragale, S. Lepidi, A. Cavallaro, Q. Giustiniani, and D. Santoro. 1995. Shear stress induces changes in the morphology and cytoskeleton organisation of arterial endothelial cells. Eur. J. Vasc. Endovasc. Surg. 9:86-92.
4. Thoumine, O., R.M. Nerem, and P.R. Girard. 1995. Oscillatory shear stress and hydrostatic pressure modulate cell-matrix attachment proteins in cultured endothelial cells. In Vitro Cell Dev. Biol. Anim. 31:45-54.
5. Malek, A.M., and S. Izumo. 1995. Control of endothelial cell gene expression by flow. J. Biomech. 28:1515-1528.
6. Gimbrone, M. A., Jr., T. Nagel, and J.N. Topper. 1997. Biomechanical activation: an emerging paradigm in endothelial adhesion biology. J. Clin. Invest. 99:1809-1813.
7. Li, Y.S., J.Y. Shyy, S. Li, J. Lee, B. Su, M. Karin, and S. Chien. 1996. The Ras-JNK pathway is involved in shear-induced gene expression. Mol. Cell. Biol. 16:5947-5954.
8. Jacobs, E.R., C. Cheliakine, D. Gebremedhin, E.K. Birks, P.F. Davies, and D.R. Harder. 1995. Shear activated channels in cell-attached patches of cultured bovine aortic endothelial cells. Pflugers Arch. 431:129-131.
9. Gudi, S.R., C.B. Clark, and J.A. Frangos. 1996. Fluid flow rapidly activates G proteins in human endothelial cells. Involvement of G proteins in mechanochemical signal transduction. Circ. Res. 79:834-839.
10. Ishida, T., T.E. Peterson, N.L. Kovach, and B.C. Berk. 1996. MAP kinase activation by flow in endothelial cells. Role of beta 1 integrins and tyrosine kinases. Circ. Res. 79:310-316.
11. Takahashi, M., and B.C. Berk. 1996. Mitogen-activated protein kinase (ERK1/2) activation by shear stress and adhesion in endothelial cells. Essential role for a herbimycin-sensitive kinase. J. Clin. Invest. 98:2623-2631.
12. Pearce, M.J. T.M. McIntyre, S.M. Prescott, G.A. Zimmerman, and R.E. Whatley. 1996. Shear stress activates cytosolic phospholipase A2 (cPLA2) and MAP kinase in human endothelial cells. Biochem. Biophys. Res. Commun. 218: 500-504.
13. Berk, B.C., M.A. Corson, T.E. Peterson, and H. Tseng. 1995. Protein kinases as mediators of fluid shear stress stimulated signal transduction in endothelial cells: a hypothesis for calcium-dependent and calcium-independent events activated by flow. J. Biomech. 28:1439-1450.
14. Nagel, T., N. Resnick, W.J. Atkinson, C.F. Dewey, Jr., and M.A. Gimbrone, Jr. 1994. Shear stress selectively upregulates intercellular adhesion molecule-1 expression in cultured human vascular endothelial cells. J. Clin. Invest. 94:885-891.
15. Shyy, J. Y., M.C. Lin, J. Han, Y. Lu, M. Petrime, and S. Chien. 1995. The cis-acting phorbol ester "12-O-tetradecanoylphorbol 13-acetate"-responsive element is involved in shear stress-induced monocyte chemotactic protein 1 gene expression. Proc. Natl. Acad. Sci. USA. 92:8069-8073.
16. Lin, M.C., F. Almus-Jacobs, H.H. Chen, G.C. Parry, N. Mackman, J.Y. Shyy, and S. Chien. 1997. Shear stress induction of the tissue factor gene. J. Clin. Invest. 99:737-744.
17. Khachigian, L.M., N. Resnick, M.A. Gimbrone, Jr., and T. Collins. 1995. Nuclear factor-kappa B interacts functionally with the platelet-derived growth factor B-chain shear-stress response element in vascular endothelial cells exposed to fluid shear stress. J. Clin. Invest. 96:1169-1175.
18. Shyy, J.Y., Y.S. Li, M.C. Lin, W. Chen, S. Yuan, S. Usami, and S. Chien. 1995. Multiple cis-elements mediate shear stress-induced gene expression. J. Biomech. 28:1451-1457.
19. Lan, Q., K.O. Mercurius, and P.F. Davies. 1994. Stimulation of transcription factors NF kappa B and AP1 in endothelial cells subjected to shear stress. Biochem. Biophys. Res. Commun. 201:950-956.
20. Khachigian, L.M., V. Lindner, A.J. Williams, and T. Collins. 1996. Egr-1-induced endothelial gene expression: a common theme in vascular injury. Science. 271:1427-1431.
21. Gimbrone, M.A., Jr., N. Resnick, T. Nagel, L.M. Khachigian, T. Collins, and J.N. Topper. 1997. Hemodynamics, endothelial gene expression, and atherogenesis. Ann. N.Y. Acad. Sci. 811:1-10.
22. Khachigian, L.M., and T. Collins. 1997. Inducible expression of Egr-1-dependent genes. A paradigm of transcriptional activation in vascular endothelium. Circ. Res. 81:457-461.
23. Shyy, J.Y., and S. Chien. 1997. Role of integrins in cellular responses to mechanical stress and adhesion. Curr. Opin. Cell Biol. 9:707-713.
24. Khachigian, L.M., K.R. Anderson, N.J. Halnon, M.A. Gimbrone, Jr., N. Resnick, and T. Collins. 1997. Egr-1 is activated in endothelial cells exposed to fluid shear stress and interacts with a novel shear-stress-response element in the PDGF A-chain promoter. Arterioscler. Thromb. Vasc. Biol. 17:2280-2286.
25. Cui, M.Z., G.C. Parry, P. Oeth, H. Larson, M. Smith, R.P. Huang, E.D. Adamson, and N. Mackman. 1996. Transcriptional regulation of the tissue factor gene in human epithelial cells is mediated by Sp1 and EGR-1. J. Biol. Chem. 271:2731-2739.
26. Waters, C.M., D.C. Hancock, and G.I. Evan. 1990. Identification and characterisation of the egr-1 gene product as an inducible, short-lived, nuclear phosphoprotein. Oncogene. 5:669-674.
27. Sukhatme, V.P., X.M. Cao, L.C. Chang, C.H. Tsai-Morris, D. Stamenkovich, P.C. Ferreira, D.R. Cohen, S.A. Edwards, T.B. Shows, and T. Curran. 1988. A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization. Cell. 53:37-43.
28. Gashler, A., and V.P. Sukhatme. 1995. Early growth response protein 1 (Egr-1): prototype of a zinc-finger family of transcription factors. Prog. Nucleic Acid Res. Mol. Biol. 50:191-224.
29. McMahon, S.B., and J.G. Monroe. 1995. A ternary complex factor-dependent mechanism mediates induction of egr-1 through selective serum response elements following antigen receptor cross-linking in B lymphocytes. Mol. Cell. Biol. 15:1086-1093.
30. Rupprecht, H.D., V.P. Sukhatme, J. Lacy, R.B. Sterzel, and D.L. Coleman. 1993. PDGF-induced Egr-1 expression in rat mesangial cells is mediated through upstream serum response elements. Am. J. Physiol. 265:F351-F360.
31. Alexandropoulos, K., S.A. Qureshi, M. Rim, V.P. Sukhatme, and D.A. Foster. 1992. v-Fps-responsiveness in the Egr-1 promoter is mediated by serum response elements. Nucleic Acids. Res. 20:2355-2359.
32. Rim, M., S.A. Qureshi, D. Gius, J. Nho, V.P. Sukhatme, and D.A. Foster. 1992. Evidence that activation of the Egr-1 promoter by v-Raf involves serum response elements. Oncogene. 7:2065-2068.
33. Qureshi, S.A., X.M. Cao, V.P. Sukhatme, and D.A. Foster. 1991. v-Src activates mitogen-responsive transcription factor Egr-1 via serum response elements. J. Biol. Chem. 266:10802-10806.
34. Watanabe, S., H. Kubota, K.M. Sakamoto, and K. Arai. 1997. Characterization of cis-acting sequences and trans-acting signals regulating early growth response 1 and c-fos promoters through the granulocyte-macrophage colony-stimulating factor receptor in BA/F3 cells. Blood. 89:1197-1206.
35. Cohen, D.M., S.R. Gullans, and W.W. Chin. 1996. Urea inducibility of egr-1 in murine inner medullary collecting duct cells is mediated by the serum response element and adjacent Ets motifs. J. Biol. Chem. 271:12903-12908.
36. Patrick, C.W., Jr., and L.V. McIntire. 1995. Shear stress and cyclic strain modulation of gene expression in vascular endothelial cells. Blood Purif. 13: 112-124.
37. Su, S., R.G. Vivier, M.C. Dickson, N. Thomas, M.K. Kendrick, N.M. Williamson, J.G. Anson, J.G. Houston, and F.F. Craig. 1997. High-throughput RT-PCR analysis of multiple transcripts using a microplate RNA isolation procedure. Biotechniques. 22:1107-1113.
38. Gius, D., X.M. Cao, F.J. Rauscher III, D.R. Cohen, T. Curran, and V.P. Sukhatme. 1990. Transcriptional activation and repression by Fos are independent functions: the C terminus represses immediate-early gene expression via CArG elements. Mol. Cell. Biol. 10:4243-1255.
39. Madden, S.L., D.M. Cook, J.F. Morris, A. Gashler, V.P. Sukhatme, and F.J. Rauscher III. 1991. Transcriptional repression mediated by the WT1 Wilms tumor gene product. Science. 253:1550-1553.
40. Sakamoto, K.M., C. Bardeleben, K.E. Yates, M.A. Raines, D.W. Golde, and J.C. Gasson. 1991. 5′ upstream sequence and genomic structure of the human primary response gene. EGR-1/TIS8. Oncogene. 6:867-871.
41. Rouet, P., G. Raguenez, and J.P. Salier. 1992. Optimized assays for quantifying transient expressions of co-transfected beta-galactosidase and CAT reporter genes. Biotechniques. 13:700-701.
42. Eustice, D.C., P.A. Feldman, A.M. Colberg-Poley, R.M. Buckery, and R.H. Neubauer. 1991. A sensitive method for the detection of beta-galactosidase in transfected mammalian cells. Biotechniques. 11:739-743.
43. Lau, L.F., and D. Nathans. 1987. Expression of a set of growth-related immediate early genes in BALB/c 3T3 cells: coordinate regulation with c-fos or c-myc. Proc. Natl. Acad. Sci. USA. 84:1182-1186.
44. Cohen, D.M., and S.R. Gullans. 1993. Urea induces Egr-1 and c-fos expression in renal epithelial cells. Am. J. Physiol. 264:F593-F600.
45. Darland, T., M. Samuels, S.A. Edwards, V.P. Sukhatme, and E.D. Adamson. 1991. Regulation of Egr-1 (Zfp-6) and c-fos expression in differentiating embryonal carcinoma cells. Oncogene. 6:1367-1376.
46. Choi, A.M., R.W. Tucker, S.G. Carlson, G. Weigand, and N.J. Holbrook. 1994. Calcium mediates expression of stress-response genes in prostaglandin A2-induced growth arrest. FASEB (Fed. Am. Soc. Exp. Biol.) J. 8: 1048-1054.
47. Treisman, R. 1994. Ternary complex factors: growth factor-regulated transcriptional activators. Curr. Opin. Genet. Dev. 4:96-101.
48. Resnick. N., T. Collins, W. Atkinson, D.T. Bonthron, C.F. Dewey, Jr., and M.A. Gimbrone, Jr. 1993. Platelet-derived growth factor B chain promoter contains a cis-acting fluid shear-stress-responsive element. Proc. Natl. Acad. Sci. USA. 90:4591-4595.
49. Cao, X., R. Mahendran, G.R. Guy, and Y.H. Tan. 1993. Detection and characterization of cellular EGR-1 binding to its recognition site. J. Biol. Chem. 268:16949-16957.
50. Price, M.A., A.E. Rogers, and R. Treisman. 1995. Comparative analysis of the ternary complex factors Elk-1, SAP-1a, and SAP-2 (ERP/NET). EMBO (Eur. Mol. Biol. Organ.) J. 14:2589-2601.
51. Maltzman, J.S., J.A. Carman, and J.G. Monroe. 1996. Role of EGR1 in regulation of stimulus-dependent CD44 transcription in B lymphocytes. Mol. Cell Biol. 16:2283-2294.
52. Lee, H.J., R.C. Mignacca, and K.M. Sakamoto. 1995. Transcriptional activation of egr-1 by granulocyte-macrophage colony-stimulating factor but not interleukin 3 requires phosphorylation of cAMP response element-binding protein (CREB) on serine 133. J. Biol. Chem. 270:15979-15983.
53. Jo, H., K. Sipos, Y.M. Go, R. Law, J. Rong, and J.M. McDonald. 1997. Differential effect of shear stress on extracellular signal-regulated kinase and N-terminal Jun kinase in endothelial cells. Gi2-and Gbeta/gamma-dependent signaling pathways. J. Biol. Chem. 272:1395-1401.
54. Cohen, D.M. 1996. Urea-inducible Egr-1 transcription in renal inner medullary collecting duct (mIMCD3) cells is mediated by extracellular signal-regulated kinase activation. Proc. Natl. Acad. Sci. USA. 93:11242-11247.
55. Topper, J.N., S.M. Wasserman, K.R. Anderson, J. Cai, D. Falb, and M.A. Gimbrone. 1997. Expression of the bumetanide-sensitive Na-K-Cl cotransporter BSC2 is differentially regulated by fluid mechanical and inflammatory cytokine stimuli in vascular endothelium. J. Clin. Invest. 99:2941-2949.
56. Ando, J., H. Tsuboi, R. Korenaga, K. Takahashi, K. Kosaki, M. Isshiki, T. Tojo, Y. Takada, and A. Kamiya. 1996. Differential display and cloning of shear stress-responsive messenger RNAs in human endothelial cells. Biochem. Biophys. Res. Commun. 225:347-351.
57. Topper, J.N., J. Cai, D. Falb, and M.A. Gimbrone. Jr. 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. USA. 93:10417-10422.
58. Braddock, M., P. Houston, M.C. Dickson, J. McVey, and C.J. Campbell. 1996. Fluid shear stress activates the tissue factor promoter in vascular endothelial cells via upregulation of the cellular transcription factor, EGR-1. J. Vasc. Res. 33:11a. (Abstr.)
59. Ku, D.N., D.P. Giddens, C.K. Zarins, and S. Glagov. 1985. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis. 5:293-302.
60. Lei, M., C. Kleinstreuer, and G.A. Truskey. 1996. A focal stress gradient-dependent mass transfer mechanism for atherogenesis in branching arteries. Med. Eng. Phys. 18:326-332.
61. Henry, P.D., O.A. Cabello, and C.H. Chen. 1995. Hypercholesterolemia and endothelial dysfunction. Curr. Opin. Lipidol. 6:190-195.
62. Yoshida, Y., M. Okano, S. Wang, M. Kobayashi, M. Kawasumi, H. Hagiwara, and M. Mitsumata. 1995. Hemodynamic-force-induced difference of interendothelial junctional complexes. Ann. N.Y. Acad. Sci. 748:104-120.
63. Langille, B.L., and M. Ojha. 1997. Blood flow dynamics, atherosclerosis, and bypass graft failure. Trends Cardiovasc. Med. 7:111-118.
64. Dimmeler, S., J. Haendeler, V. Rippmann, M. Nehls, and A.M. Zeiher. 1996. Shear stress inhibits apoptosis of human endothelial cells. FEBS Lett. 399: 71-74.
65. Kaiser, D., M.A. Freyberg, and P. Friedl. 1997. Lack of hemodynamic forces triggers apoptosis in vascular endothelial cells. Biochem. Biophys. Res. Commun. 231:586-590.
66. Dimmeler, S., J. Haendeler, M. Nehls, and A.M. Zeiher. 1997. Suppression of apoptosis by nitric oxide via inhibition of interleukin-1 β-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases. J. Exp. Med. 185:601-607.
67. Bodin, P., P. Millier, J. Marshall, and G. Burnstock. 1995. Cytokines suppress the shear stress-stimulated release of vasoactive peptides from human endothelial cells. Peptides. 16:1433-1438.
68. Tsao, P.S., R. Buitrago, J.R. Chan, and J.P. Cooke. 1996. Fluid flow inhibits endothelial adhesiveness. Nitric oxide and transcriptional regulation of VCAM-1. Circulation. 94:1682-1689.