Chronic exposure to laminar shear stress induces Kruppel-like factor 2 in glomerular endothelial cells and modulates interactions with co-cultured podocytes

International Journal of Biochemistry and Cell Biology

Volumn 44, Issue 9, 2012, Pages 1482-1490

  Slater, Sadie C ^a   Ramnath, Raina D ^a   Uttridge, Kate ^a   Saleem, Moin A ^a   Cahill, Paul A ^b   Mathieson, Peter W ^a   Welsh, Gavin I ^a   Satchell, Simon C ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b DUBLIN CITY UNIVERSITY   (Ireland)

Author keywords

Endothelin; ERK5; Glomerulus; KLF2; Laminar shear stress; Nitric oxide

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; KRUPPEL LIKE FACTOR 2; MITOGEN ACTIVATED PROTEIN KINASE 7; NITRIC OXIDE; SERINE; THREONINE; THROMBOMODULIN; UO 126; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ARTICLE; CELL CULTURE; CELL INTERACTION; CONTROLLED STUDY; DRUG EFFECT; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; GLOMERULAR ENDOTHELIAL CELL; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; KIDNEY CELL; LONG TERM EXPOSURE; PODOCYTE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SHEAR STRESS;

BUTADIENES; CELL ADHESION MOLECULES; CELL COMMUNICATION; CELL LINE; COCULTURE TECHNIQUES; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; KIDNEY GLOMERULUS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICROFILAMENT PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 7; NITRIC OXIDE; NITRILES; PHOSPHOPROTEINS; PHOSPHORYLATION; PODOCYTES; SIGNAL TRANSDUCTION; SPERMINE; STRESS, MECHANICAL; TIME FACTORS;

EID: 84862756066     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2012.05.020     Document Type: Article

References (50)

1. T. Asakura, and T. Karino Flow patterns and spatial distribution of atherosclerotic lesions in human coronary arteries Circulation Research 66 1990 1045 1066
2. B.J. Ballermann, A. Dardik, E. Eng, and A. Liu Shear stress and the endothelium Kidney International 54 1998 100 108
3. J.L. Balligand, O. Feron, and C. Dessy eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues Physiological Reviews 89 2009 481 534
4. B. Beltran, A. Mathur, M.R. Duchen, J.D. Erusalimsky, and S. Moncada The effect of nitric oxide on cell respiration: a key to understanding its role in cell survival or death Proceedings of the National Academy of Sciences of the United States of America 97 2000 14602 14607
5. H.S. Bevan, S.C. Slater, H. Clarke, P.A. Cahill, P.W. Mathieson, and G.I. Welsh Acute laminar shear stress reversibly increases human glomerular endothelial cell permeability via the activation of endothelial nitric oxide synthase American Journal of Physiology. Renal Physiology 301 2011 F733 F742
6. S. Burghoff, and J. Schrader Secretome of human endothelial cells under shear stress Journal of Proteome Research 10 2011 1160 1169
7. E. Butt, K. Abel, M. Krieger, D. Palm, V. Hoppe, and J. Hoppe cAMP- and cGMP-dependent protein kinase phosphorylation sites of the focal adhesion vasodilator-stimulated phosphoprotein (VASP) in vitro and in intact human platelets Journal of Biological Chemistry 269 1994 14509 14517
8. O.C. Colgan, G. Ferguson, N.T. Collins, R.P. Murphy, G. Meade, and P.A. Cahill Regulation of bovine brain microvascular endothelial tight junction assembly and barrier function by laminar shear stress American Journal of Physiology - Heart and Circulatory Physiology 292 2007 H3190 H3197
9. R.J. Dekker, R.A. Boon, M.G. Rondaij, A. Kragt, O.L. Volger, and Y.W. Elderkamp KLF2 provokes a gene expression pattern that establishes functional quiescent differentiation of the endothelium Blood 107 2006 4354 4363
10. R.J. Dekker, S. van Soest, R.D. Fontijn, S. Salamanca, P.G. de Groot, and E. VanBavel Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Kruppel-like factor (KLF2) Blood 100 2002 1689 1698
11. R.J. Dekker, J.V. van Thienen, J. Rohlena, S.C. de Jager, Y.W. Elderkamp, and J. Seppen Endothelial KLF2 links local arterial shear stress levels to the expression of vascular tone-regulating genes American Journal of Pathology 167 2005 609 618
12. N. DePaola, J.E. Phelps, L. Florez, C.R. Keese, F.L. Minnear, and I. Giaever Electrical impedance of cultured endothelium under fluid flow Annals of Biomedical Engineering 29 2001 648 656
13. S. Dimmeler, I. Fleming, B. Fisslthaler, C. Hermann, R. Busse, and A.M. Zeiher Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation Nature 399 1999 601 605
14. E. Eng, and B.J. Ballermann Diminished NF-kappaB activation and PDGF-B expression in glomerular endothelial cells subjected to chronic shear stress Microvascular Research 65 2003 137 144
15. V. Eremina, J.A. Jefferson, J. Kowalewska, H. Hochster, M. Haas, and J. Weisstuch VEGF inhibition and renal thrombotic microangiopathy New England Journal of Medicine 358 2008 1129 1136
16. V. Eremina, M. Sood, J. Haigh, A. Nagy, G. Lajoie, and N. Ferrara Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases Journal of Clinical Investigation 111 2003 707 716
17. I. Fleming, B. Fisslthaler, S. Dimmeler, B.E. Kemp, and R. Busse Phosphorylation of Thr(495) regulates Ca(2+)/calmodulin-dependent endothelial nitric oxide synthase activity Circulation Research 88 2001 E68 E75
18. R.R. Foster, S.C. Slater, J. Seckley, D. Kerjaschki, D.O. Bates, and P.W. Mathieson Vascular endothelial growth factor-C, a potential paracrine regulator of glomerular permeability increases glomerular endothelial cell monolayer integrity and intracellular calcium American Journal of Pathology 173 2008 938 948
19. C. Friedrich, N. Endlich, W. Kriz, and K. Endlich Podocytes are sensitive to fluid shear stress in vitro American Journal of Physiology. Renal Physiology 291 2006 F856 F865
20. I.M. Grumbach, W. Chen, S.A. Mertens, and D.G. Harrison A negative feedback mechanism involving nitric oxide and nuclear factor kappa-B modulates endothelial nitric oxide synthase transcription Journal of Molecular and Cellular Cardiology 39 2005 595 603
21. B. Haraldsson, J. Nystrom, and W.M. Deen Properties of the glomerular barrier and mechanisms of proteinuria Physiological Reviews 88 2008 451 487
22. H. Jo, R.O. Dull, T.M. Hollis, and J.M. Tarbell Endothelial albumin permeability is shear dependent, time dependent, and reversible American Journal of Physiology 260 1991 H1992 H1996
23. S. Kamakura, T. Moriguchi, and E. Nishida Activation of the protein kinase ERK5/BMK1 by receptor tyrosine kinases Identification and characterization of a signaling pathway to the nucleus Journal of Biological Chemistry 274 1999 26563 26571
24. K. Kawamura, S. Okada, B. Li, M. Suwa, J. Yao, and T. Morioka Turbulence of glomerular hemodynamics involved in progressive glomerulosclerosis Kidney International 69 2006 1792 1798
25. Z. Lin, V. Natesan, H. Shi, F. Dong, D. Kawanami, and G.H. Mahabeleshwar Kruppel-like factor 2 regulates endothelial barrier function Arteriosclerosis, Thrombosis, and Vascular Biology 30 2010 1952 1959
26. M. Mattart, L. Mazzolai, C. Chambaz, D. Hayoz, H.R. Brunner, and P. Silacci ET-1 and NOS III gene expression regulation by plaque-free and plaque-prone hemodynamic conditions Biorheology 40 2003 289 297
27. H. Morawietz, R. Talanow, M. Szibor, U. Rueckschloss, A. Schubert, and B. Bartling Regulation of the endothelin system by shear stress in human endothelial cells Journal of Physiology 525 Pt 3 2000 761 770
28. Y. Ohashi, S. Kawashima, K. Hirata, T. Yamashita, T. Ishida, and N. Inoue Hypotension and reduced nitric oxide-elicited vasorelaxation in transgenic mice overexpressing endothelial nitric oxide synthase Journal of Clinical Investigation 102 1998 2061 2071
29. K.M. Parmar, H.B. Larman, G. Dai, Y. Zhang, E.T. Wang, and S.N. Moorthy Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2 Journal of Clinical Investigation 116 2006 49 58
30. H. Pavenstadt, W. Kriz, and M. Kretzler Cell biology of the glomerular podocyte Physiological Reviews 83 2003 253 307
31. Y. Qiu, and J.M. Tarbell Interaction between wall shear stress and circumferential strain affects endothelial cell biochemical production Journal of Vascular Research 37 2000 147 157
32. K. Sako, S. Fukuhara, T. Minami, T. Hamakubo, H. Song, and T. Kodama Angiopoietin-1 induces Kruppel-like factor 2 expression through a phosphoinositide 3-kinase/AKT-dependent activation of myocyte enhancer factor 2 Journal of Biological Chemistry 284 2009 5592 5601
33. M.A. Saleem, M.J. O'Hare, J. Reiser, R.J. Coward, C.D. Inward, and T. Farren A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression Journal of the American Society of Nephrology 13 2002 630 638
34. S.C. Satchell, K.L. Anderson, and P.W. Mathieson Angiopoietin 1 and vascular endothelial growth factor modulate human glomerular endothelial cell barrier properties Journal of the American Society of Nephrology 15 2004 566 574
35. S.C. Satchell, S.J. Harper, J.E. Tooke, D. Kerjaschki, M.A. Saleem, and P.W. Mathieson Human podocytes express angiopoietin 1 a potential regulator of glomerular vascular endothelial growth factor Journal of the American Society of Nephrology 13 2002 544 550
36. S.C. Satchell, C.H. Tasman, A. Singh, L. Ni, J. Geelen, and C.J. von Ruhland Conditionally immortalized human glomerular endothelial cells expressing fenestrations in response to VEGF Kidney International 69 2006 1633 1640
37. S. SenBanerjee, Z. Lin, G.B. Atkins, D.M. Greif, R.M. Rao, and A. Kumar KLF2 Is a novel transcriptional regulator of endothelial proinflammatory activation Journal of Experimental Medicine 199 2004 1305 1315
38. H.W. Sill, Y.S. Chang, J.R. Artman, J.A. Frangos, T.M. Hollis, and J.M. Tarbell Shear stress increases hydraulic conductivity of cultured endothelial monolayers American Journal of Physiology 268 1995 H535 H543
39. A. Singh, S.C. Satchell, C.R. Neal, E.A. McKenzie, J.E. Tooke, and P.W. Mathieson Glomerular endothelial glycocalyx constitutes a barrier to protein permeability Journal of the American Society of Nephrology 18 2007 2885 2893
40. S.J. Sohn, D. Li, L.K. Lee, and A. Winoto Transcriptional regulation of tissue-specific genes by the ERK5 mitogen-activated protein kinase Molecular and Cellular Biology 25 2005 8553 8566
41. T. Srivastava, E.T. McCarthy, R. Sharma, P.A. Cudmore, M. Sharma, and M.L. Johnson Prostaglandin E(2) is crucial in the response of podocytes to fluid flow shear stress Journal of Cell Communication and Signaling 4 2010 79 90
42. O. Traub, and B.C. Berk Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force Arteriosclerosis, Thrombosis, and Vascular Biology 18 1998 677 685
43. M.C. Tsai, L. Chen, J. Zhou, Z. Tang, T.F. Hsu, and Y. Wang Shear stress induces synthetic-to-contractile phenotypic modulation in smooth muscle cells via peroxisome proliferator-activated receptor alpha/delta activations by prostacyclin released by sheared endothelial cells Circulation Research 105 2009 471 480
44. T.E. Walshe, P. Connell, L. Cryan, G. Ferguson, C. O'Brien, and P.A. Cahill The role of pulsatile flow in controlling microvascular retinal endothelial and pericyte cell apoptosis and proliferation Cardiovascular Research 89 2011 661 670
45. T.E. Walshe, G. Ferguson, P. Connell, C. O'Brien, and P.A. Cahill Pulsatile flow increases the expression of eNOS, ET-1 and prostacyclin in a novel in vitro coculture model of the retinal vasculature Investigative Ophthalmology and Visual Science 46 2005 375 382
46. G. Wang, S. Cai, X. Deng, K. Ouyang, G. Xie, and R. Guidoin Secretory response of endothelin-1 in cultured human glomerular microvascular endothelial cells to shear stress Biorheology 37 2000 291 299
47. G.X. Wang, S.X. Cai, P.Q. Wang, K.Q. Ouyang, Y.L. Wang, and S.R. Xu Shear-induced changes in endothelin-1 secretion of microvascular endothelial cells Microvascular Research 63 2002 209 217
48. N. Wang, H. Miao, Y.S. Li, P. Zhang, J.H. Haga, and Y. Hu Shear stress regulation of Kruppel-like factor 2 expression is flow pattern-specific Biochemical and Biophysical Research Communications 341 2006 1244 1251
49. C. Yan, M. Takahashi, M. Okuda, J.D. Lee, and B.C. Berk Fluid shear stress stimulates big mitogen-activated protein kinase 1 (BMK1) activity in endothelial cells. Dependence on tyrosine kinases and intracellular calcium Journal of Biological Chemistry 274 1999 143 150
50. M. Yoshizumi, H. Kurihara, T. Sugiyama, F. Takaku, M. Yanagisawa, and T. Masaki Hemodynamic shear stress stimulates endothelin production by cultured endothelial cells Biochemical and Biophysical Research Communications 161 1989 859 864