The role of shear stress on ET-1, KLF2, and NOS-3 expression in the developing cardiovascular system of chicken embryos in a venous ligation model

Physiology

Volumn 22, Issue 6, 2007, Pages 380-389

  Groenendijk, Bianca C W ^a,b   Van Der Heiden, Kim ^b   Hierck, Beerend P ^b   Poelmann, Robert E ^b  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; KRUPPEL LIKE FACTOR;

ANIMAL; CHICK EMBRYO; CONGENITAL HEART MALFORMATION; DISEASE MODEL; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEART; HEART MUSCLE; HEMODYNAMICS; HUMAN; LIGATION; MECHANICAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PRENATAL DEVELOPMENT; PULSATILE FLOW; REVIEW; VEIN;

ANIMALS; CHICK EMBRYO; DISEASE MODELS, ANIMAL; ENDOTHELIN-1; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HEART DEFECTS, CONGENITAL; HEMODYNAMICS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LIGATION; MYOCARDIUM; NITRIC OXIDE SYNTHASE TYPE III; PULSATILE FLOW; STRESS, MECHANICAL; VEINS;

EID: 37149027583     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00023.2007     Document Type: Review

References (161)

1. Al Bhalal L, Akhtar M. Molecular basis of autosomal dominant polycystic kidney disease. Adv Anat Pathol 12: 126-133, 2005.
2. Baldini A. DiGeorge syndrome: an update. Curr Opin Cardiol 19: 201-204, 2004.
3. Barlow GM, Chen XN, Lyons GE, Kurnit DM, Celle L, Spinner NB, Zackai EH, Mjaatvedt CH, VanRiper AJ, Vekemans MJ, Korenberg JR. Down syndrome congenital heart disease: a narrowed region and a candidate gene. Genet Med 3: 91-101, 2001.
4. Basu P, Morris P, Wani MA, Lingrel JB, Lloyd JA. KLF2 is required for normal epsilon- and beta hl-globin expression. Blood Cells Mol Dis 34: 76, 2005.
5. Bergwerff M, DeRuiter MC, Poelmann RE, Gittenberger-de Groot AC. Onset of elastogenesis and downregulation of smooth muscle actin as distinguishing phenomena in artery differentiation in the chick embryo. Anat Embryol (Berl) 194: 545-557, 1996.
6. Bieker JJ. Kruppel-like factors: three fingers in many pies. J Biol Chem 276: 34355-34358, 2001.
7. Boon RA, Fledderus JO, Volger OL, van Wanrooij EJA, Pardali E, Weesie F, Kuiper J, Pannekoek H, ten Dijke P, Horrevoets AJG. KLF2 suppresses TGF-beta signaling in endothelium through induction of Smad7 and inhibition of AP-1. Arterioscler Thromb Vasc Biol 27: 532-539, 2007.
8. Boot MJ, Steegers-Theunissen RP, Poelmann RE, van Iperen L, Gittenberger-de Groot AC. Cardiac outflow tract malformations in chick embryos exposed to homocysteine. Cardiovasc Res 64: 365-373, 2004.
9. Bouman HGA, Broekhuizen MLA, Baasten AMJ, Gittenberger-de Groot AC, Wenink ACG. Stereological study of stage 34 chicken hearts with looping disturbances after retinoic acid treatment: disturbed growth of myocardium and atrioventricular cushion tissue. Anat Rec 248: 242-250, 1997.
10. Briffeuil P, Thibaut-Vercruyssen R, Ronveaux-Dupal MF. Ciliation of bovine aortic endothelial cells in culture. Atherosclerosis 106: 75-81, 1994.
11. Broekhuizen MLA, Hogers B, DeRuiter MC, Poelmann RE, Gittenberger-de Groot AC, Wladimiroff JW. Altered hemodynamics in chick embryos after extraembryonic venous obstruction. Ultrasound Obstet Gynecol 13: 437-445, 1999.
12. Broekhuizen MLA, Wladimiroff JW, Tibboel D, Poelmann RE, Wenink ACG, Gittenberger-de Groot AC. Induction of cardiac anomalies with all-trans retinoic acid in the chick embryo. Cardiol Young 2: 311-317, 1992.
13. Butcher JT, McQuinn TC, Sedmera D, Turner D, Markwald RR. Transitions in early embryonic atrioventricular valvular function correspond with changes in cushion biomechanics that are predictable by tissue composition. Circ Res 100: 1503-1511, 2007.
14. Bystrevskaya VB, Lichkun VV, Antonov AS, Perov NA. An ultrastructural study of centriolar complexes in adult and embryonic human aortic endothelial cells. Tissue Cell 20: 493-503, 1988.
15. Chlench S, Mecha DN, Hohberg M, Hoffmann C, Pohlkamp T, Beyer G, Bongrazio M, Da Silva-Azevedo L, Baum O, Pries AR, and Zakrzewicz A. Regulation of Foxo-1 and the angiopoietin-2/Tie2 system by shear stress. FEBS Lett 581: 673-680, 2007.
16. Clark EB, Hu N, Frommelt P, Vandekieft GK, Dummett JL, Tomanek RJ. Effect of increased pressure on ventricular growth in stage 21 chick embryos. Am J Physiol Heart Circ Physiol 257: H55-H61, 1989.
17. Clouthier DE, Hosoda K, Richardson JA, Williams SC, Yanagisawa H, Kuwaki T, Kumada M, Hammer RE, Yanagisawa M. Cranial and cardiac neural crest defects in endothelin-A receptor-deficient mice. Development 125: 813-824, 1998.
18. Collod-Béroud G, Boileau C. Marfan syndrome in the third Millennium. Eur J Hum Genet 10: 673-681, 2002.
19. Davies PF, Spaan JA, Krams R. Shear stress biology of the endothelium. Ann Biomed Eng 33: 1714-1718, 2005.
20. de Nucci G, Thomas R, D'Orleans-Juste P, Antunes E, Walder C, Warner TD, Vane JR. Pressor effects of circulating endothelin are limited by its removal in the pulmonary circulation and by the release of prostacyclin and endothelium-derived relaxing factor. Proc Natl Acad Sci USA 85: 9797-9800, 1988.
21. Dealmeida A, McQuinn T, Sedmera D. Increased ventricular preload is compensated by myocyte proliferation in normal and hypoplastic fetal chick left ventricle. Circ Res 100: 1363-1370, 2007.
22. Dekker RJ, Van Soest S, Fontijn RD, Salamanca S, de Groot PG, VanBavel E, Pannekoek H, Horrevoets AJG. Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Krüppel-like factor (KLF2). Blood 100: 1689-1698, 2002.
23. Dekker RJ, van Thienen JV, Elderkamp YW, Seppen J, de Vries CJM, Biessen EA, van Berkel TJ, Pannekoek H, Horrevoets AJG. Endothelial KLF2 links local arterial shear stress levels to the expression of vascular-tone regulating genes. Am J Pathol 167: 609-618, 2005.
24. DeRuiter MC, Poelmann RE, VanderPlas-de Vries I, Mentink MMT, Gittenberger-de Groot AC. The development of the myocardium and endocardium in mouse embryos. Fusion of two heart tubes? Anat Embryol (Berl) 185: 461-473, 1992.
25. Dong F, Zhang X, Wold LE, Ren Q, Zhang Z, Ren J. Endothelin-1 enhances oxidative stress, cell proliferation and reduces apoptosis in human umbilical vein endothelial cells: role of ETB receptor, NADPH oxidase and caveolin-1. Br J Pharmacol 145: 323-333, 2005.
26. Eley L, Yates LM, Goodship JA. Cilia and disease. Curr Opin Genet Dev 15: 308-314, 2005.
27. Fagan KA, Fouty BW, Tyler RC, Morris KG Jr, Hepler LK, Sato K, LeCras TD, Abman SH, Weinberger HD, Huang PL, McMurtry IF, Rodman DM. The pulmonary circulation of homozygous or heterozygous eNOS-null mice is hyperresponsive to mild hypoxia. J Clin Invest 103: 291-299, 1999.
28. Feng Q, Song W, Lu X, Hamilton JA, Lei M, Peng T, Yee SP. Development of heart failure and congenital septal defects in mice lacking endothelial nitric oxide synthase. Circulation 106: 873-879, 2002.
29. Fledderus JO, van Thienen JV, Boon RA, Dekker RJ, Rohlena J, Volger OL, Bijnens APJJ, Daemen MJAP, Kuiper J, van Berkel TJC, Pannekoek H, Horrevoets AJG. Prolonged shear stress and KLF2 suppress constitutive pro-inflammatory transcription through inhibition of ATF2. Blood 109: 4249-4257, 2007.
30. Fujii S, Hirota A, Kamino K. Optical indications of pace-maker potential and rhythm generation in early embryonic chick heart. J Physiol 312: 253-263, 1981.
31. Fujisaki H, Ito H, Hirata Y, Tanaka M, Hata M, Lin MH, Adachi S, Akimoto H, Marumo F, Hiroe M. Natriuretic peptides inhibit angiotensin-Ii-induced proliferation of rat cardiac fibroblasts by blocking endothelin-1 gene-expression. J Clin Invest 96: 1059-1065, 1995.
32. Fukuhara S, Marinissen MJ, Chiariello M, Gutkind JS. Signaling from G protein-coupled receptors to ERK5/Big MAPK 1 involves Galpha q and Galpha 12/13 families of heterotrimeric G proteins. Evidence for the existence of a novel Ras AND Rho-independent pathway. J Biol Chem 275: 21730-21736, 2000.
33. Gimbrone MA Jr, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann NY Acad Sci 902: 230-239, 2000.
34. Gittenberger-de Groot AC, Bartelings MM, DeRuiter MC, Poelmann RE. Normal cardiac development. In: Ultrasound and the Fetal Heart, edited by Wladimiroff JW, Pilu G. New York: The Parthenon Publishing Group, 1996, p. 1-14.
35. Gittenberger-de Groot AC, Bartelings MM, DeRuiter MC, Poelmann RE. Basics of cardiac development for the understanding of congenital heart malformations. Pediatr Res 57: 169-176, 2005.
36. Gittenberger-de Groot AC, DeRuiter MC, Bartelings MM, Poelmann RE. Embryology of congenital heart disease. In: Cardiology, edited by Crawford MH, DiMarco JP. London: Mosby International, 2001, p. 2.1-2.10.
37. Gödecke A, Decking UK, Ding Z, Hirchenhain J, Bidmon HJ, Godecke S, Schrader J. Coronary hemodynamics in endothelial NO synthase knock-out mice. Circ Res 82: 186-194, 1998.
38. Gödecke A, Heinicke T, Kamkin A, Kiseleva I, Strasser RH, Decking UK, Stumpe T, Isenberg G, Schrader J. Inotropic response to beta-adrenergic receptor stimulation and anti-adrenergic effect of ACh in endothelial NO synthase-deficient mouse hearts. J Physiol 532: 195-204, 2001.
39. Goldsmith HL, Cokelet GR, Gaehtgens P. Robin Fahraeus: evolution of his concepts in cardiovascular physiology. Am J Physiol Heart Circ Physiol 257: H1005-H1015, 1989.
40. Gouverneur M, Berg B, Nieuwdorp M, Stroes E, Vink H. Vasculoprotective properties of the endothelial glycocalyx: effects of fluid shear stress. J Intern Med 259: 393-400, 2006.
41. Gregan B, Jurgensen J, Papsdorf G, Furkert J, Schaefer M, Beyermann M, Rosenthal W, Oksche A. Ligand-dependent differences in the internalization of endothelin A and endothelin B receptor heterodimers. J Biol Chem 279: 27679-27687, 2004.
42. Gregan B, Schaefer M, Rosenthal W, Oksche A. Fluorescence resonance energy transfer analysis reveals the existence of endothelin-A and endothelin-B receptor homodimers. J Cardiovasc Pharmacol 44: S30-S33, 2004.
43. Groenendijk BCW, Hierck BP, Gittenberger-de Groot AC, Poelmann RE. Development-related changes in the expression of shear stress responsive genes KLF-2, ET-1, and NOS-3 in the developing cardiovascular system of chicken embryos. Dev Dyn 230: 57-68, 2004.
44. Groenendijk BCW, Hierck BP, Vrolijk J, Baiker M, Pourquie MJBM, Gittenberger-de-Groot AC, Poelmann RE. Changes in shear stress-related gene expression after experimentally altered venous return in the chicken embryo. Circ Res 96: 1291-1298, 2005.
45. Groenendijk BCW, Vennemann P, Stekelenburg-de Vos S, Wladimiroff JW, Nieuwstadt FTM, Westerweel J, Hierck BP, Ursem NTC, Poelmann RE. The endothelin-1 pathway and the development of cardiovascular defects in the hemodynamically challenged chicken embryo. J Vasc Res. In press.
46. Guarda E, Katwa LC, Myers PR, Tyagi SC, Weber KT. Effects of endothelins on collagen turnover in cardiac fibroblasts. Cardiovasc Res 27: 2130-2134, 1993.
47. Hafizi S, Allen SP, Goodwin AT, Chester AH, Yacoub MH. Endothelin-1 stimulates proliferation of human coronary smooth muscle cells via the ETA receptor and is co-mitogenic with growth factors. Atherosclerosis 146: 351-359, 1999.
48. Hall CE, Hurtado R, Hewett KW, Shulimovich M, Poma CP, Reckova M, Justus C, Pennisi DJ, Tobita K, Sedmera D, Gourdie RG, Mikawa T. Hemodynamic-dependent patterning of endothelin converting enzyme 1 expression and differentiation of impulse-conducting Purkinje fibers in the embryonic heart. Development 131: 581-592, 2004.
49. Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. J Morphol 88: 49-92, 1951.
50. Haynes WG, Strachan FE, Webb DJ. Endothelin ETA and ETB receptors cause vasoconstriction of human resistance and capacitance vessels in vivo. Circulation 92: 357-363, 1995.
51. Haynes WG, Webb DJ. Endothelin as a regulator of cardiovascular function in health and disease. J Hypertens 16: 1081-1098, 1998.
52. Helderman F, Segers D, de CR, Hierck BP, Poelmann RE, Evans PC, Krams R. Effect of shear stress on vascular inflammation and plaque development. Curr Opin Lipidol 18: 527-533, 2007.
53. Hierck BP, Van der Heiden K, DeRuiter MC, Gittenberger-de-Groot AC, Poelmann RE. Fluid shear stress controls cardiovascular development. A functionomic approach. Wien Klin Wochenschr 119: 10-13, 2007.
54. Hogers B, DeRuiter MC, Baasten AMJ, Gittenberger-de Groot AC, Poelmann RE. Intracardiac blood flow patterns related to the yolk sac circulation of the chick embryo. Circ Res 76: 871-877, 1995.
55. Hogers B, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE. Unilateral vitelline vein ligation alters intracardiac blood flow patterns and morphogenesis in the chick embryo. Circ Res 80: 473-481, 1997.
56. Hogers B, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE. Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal. Cardiovasc Res 41: 87-99, 1999.
57. Hogers B, Gittenberger-de-Groot AC, DeRuiter MC, Mentink MMT, Poelmann RE. Cardiac inflow malformations are more lethal and precede cardiac outflow malformations. Chick embryonic venous clip model. In: The Role of Blood Flow in Normal and Abnormal Heart Development, edited by Hogers B. Wageningen, The Netherlands: Ponsen & Looijen, 1998, p. 79-100.
58. Hove JR. In vivo biofluid dynamic imaging in the developing zebrafish. Birth Defects Res C Embryo Today 72: 277-289, 2004.
59. Hove JR. Quantifying cardiovascular flow dynamics during early development. Pediatr Res 60: 6-13, 2006.
60. Hove JR, Koster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M. Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421: 172-177, 2003.
61. Hu N, Clark EB. Hemodynamics of the stage 12 to stage 29 chick embryo. Circ Res 65: 1665-1670, 1989.
62. Huang PL, Huang Z, Mashimo H, Bloch KD, Moskowitz MA, Bevan JA, Fishman MC. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 377: 239-242, 1995.
63. Huddleson JP, Ahmad N, Srinivasan S, Lingrel JB. Induction of KLF2 by fluid shear stress requires a novel promoter element activated by a phosphatidylinositol 3-kinase-dependent chromatinremodeling pathway. J Biol Chem 280: 23371-23379, 2005.
64. Iomini C, Tejada K, Mo W, Vaananen H, Piperno G. Primary cilia of human endothelial cells disassemble under laminar shear stress. J Cell Biol 164: 811-817, 2004.
65. Kapusta L, Haagmans ML, Steegers EA, Cuypers MH, Blom HJ, Eskes TK. Congenital heart defects and maternal derangement of homocysteine metabolism. J Pediatr 135: 773-774, 1999.
66. Kato Y, Zhao M, Morikawa A, Sugiyama T, Chakravortty D, Koide N, Yoshida T, Tapping RI, Yang Y, Yokochi T, Lee JD. Big mitogen-activated kinase regulates multiple members of the MEF2 protein family. J Biol Chem 275: 18534-18540, 2000.
67. Katritsis D, Kaiktsis L, Chaniotis A, Pantos J, Efstathopoulos EP, Marmarelis V. Wall shear stress: theoretical considerations and methods of measurement. Prog Cardiovasc Dis 49: 307-329, 2007.
68. Khachigian LM, Resnick N, Gimbrone MA, Collins T. Nuclear factor-kB 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, 1995.
69. Kirby ML, Waldo KL. Neural crest and cardiovascular patterning. Circ Res 77: 211-215, 1995.
70. Ku DN. Blood flow in arteries. Annu Rev Fluid Mech 29: 399-434, 1997.
71. Kumar A, Lin Z, SenBanerjee S, Jain MK. Tumor necrosis factor alpha-mediated reduction of KLF2 is due to inhibition of MEF2 by NF-kappaB and histone deacetylases. Mol Cell Biol 25: 5893-5903, 2005.
72. Kuo CT, Veselits ML, Barton KP, Lu MM, Clendenin C, Leiden JM. The LKLF transcription factor is required for normal tunica media formation and blood vessel stabilization during murine embryo-genesis. Genes Dev 11: 2996-3006, 1997.
73. Kurihara Y, Kurihara H, Oda H, Maemura K, Nagai R, Ishikawa T, Yazaki Y. Aortic arch malformations and ventricular septal defect in mice deficient in endothelin-1. J Clin Invest 96: 293-300, 1995.
74. Kurihara Y, Kurihara H, Suzuki H, Kodama T, Maemura K, Nagai R, Oda H, Kuwaki T, Cao WH, Kamada N, Jishage K, Ouchi Y, Azuma S, Toyoda Y, Ishikawa T, Kumada M, Yazaki Y. Elevated blood pressure and craniofacial abnormalities in mice deficient in endothelin -1. Nature 368: 703-710, 1994.
75. Lavallée M, Takamura M, Parent R, Thorin E. Crosstalk between endothelin and nitric oxide in the control of vascular tone. Heart Fail Rev 6: 265-276, 2001.
76. Lee JS, Yu Q, Shin JT, Sebzda E, Bertozzi C, Chen M, Mericko P, Stadtfeld M, Zhou D, Cheng L, Graf T, MacRae CA, Lepore JJ, Lo CW, Kahn ML. Klf2 is an essential regulator of vascular hemodynamic forces in vivo. Dev Cell 11: 845-857, 2006.
77. Lee TC, Zhao YD, Courtman DW, Stewart DJ. Abnormal aortic valve development in mice lacking endothelial nitric oxide synthase. Circulation 101: 2345-2348, 2000.
78. Lehoux S, Castier Y, Tedgui A. Molecular mechanisms of the vascular responses to haemodynamic forces. J Intern Med 259: 381-392, 2006.
79. Lin AE. The heart of Turner syndrome: small matters. Teratology 66: 63-64, 2002.
80. Lucitti JL, Tobita K, Keller BB. Arterial hemodynamics and mechanical properties after circulatory intervention in the chick embryo. J Exp Biol 208: 1877-1885, 2005.
81. Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA 282: 2035-2042, 1999.
82. Malek AM, Izumo S. Physiological fluid shear stress causes downregulation of endothelin-1 mRNA in bovine aortic endothelium. Am J Physiol Cell Physiol 263: C389-C396, 1992.
83. Malek AM, Izumo S. Control of endothelial cell gene expression by flow. J Biomech 28: 1515-1528, 1995.
84. Manasek FJ, Monroe RG. Early cardiac morphogenesis is independent of function. Dev Biol 27: 584-588, 1972.
85. Männer J. Cardiac looping in the chick embryo: a morphological review with special reference to terminological and biomechanical aspects of the looping process. Anat Rec 259: 248-262, 2000.
86. Männer J. On rotation, torsion, lateralization, and handedness of the embryonic heart loop: new insights from a simulation model for the heart loop of chick embryos. Anat Rec A Discov Mol Cell Evol Biol 278: 481-492, 2004.
87. Marinissen MJ, Chiariello M, Pallante M, Gutkind JS. A network of mitogen-activated protein kinases links G protein-coupled receptors to the c-jun promoter: a role for c-Jun NH2-terminal kinase, p38s, and extracellular signal-regulated kinase 5. Mol Cell Biol 19: 4289-4301, 1999.
88. Markwald RR, Fitzharris TP, Manasek FJ. Structural development of endocardial cushions. Am J Anat 148: 85-120, 1977.
89. Marsden PA, Schappert KT, Chen HS, Flowers M, Sundell CL, Wilcox JN, Lamas S, Michel T. Molecular cloning and characterization of human endothelial nitric oxide synthase. FEBS Lett 307: 287-293, 1992.
90. Marshall WF, Nonaka S. Cilia: tuning in to the cell's antenna. Curr Biol 16: R604-R614, 2006.
91. Masatsugu K, Itoh H, Chun TH, Ogawa Y, Tamura N, Yamashita J, Doi K, Inoue M, Fukunaga Y, Sawada N, Saito T, Korenaga R, Ando J, Nakao K. Physiologic shear stress suppresses endothelin-converting enzyme-1 expression in vascular endothelial cells. J Cardiovasc Pharmacol 31, Suppl 1: S42-S45, 1998.
92. Mattart M, Mazzolai L, Chambaz C, Hayoz D, Brunner HR, Silacci P. ET-1 and NOSIII gene expression regulation by plaque-free and plaque-prone hemodynamic conditions. Biorheology 40: 289-297, 2003.
93. McCormick SM, Eskin SG, McIntire LV, Teng CL, Lu CM, Russell CG, Chittur KK. DNA microarray reveals changes in gene expression of shear stressed human umbilical vein endothelial cells. Proc Natl Acad Sci USA 98: 8955-8960, 2001.
94. McGrath J, Somlo S, Makova S, Tian X, Brueckner M. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114: 61-73, 2003.
95. Miller CE, Wong CL, Sedmera D. Pressure overload alters stress-strain properties of the developing chick heart. Am J Physiol Heart Circ Physiol 285: H1849-H1856, 2003.
96. Moore JE, Xu C, Glagov S, Zarins CK, Ku DN. Fluid wall shear stress measurements in a model of the human abdominal aorta: oscillatory behavior and relationship to atherosclerosis. Atherosclerosis 110: 225-240, 1994.
97. Morawietz H, Talanow R, Szibor M, Rueckschloss U, Schubert A, Bartling B, Darmer D, Holtz J. Regulation of the endothelin system by shear stress in human endothelial cells. J Physiol 525: 761-770, 2000.
98. Morbidelli L, Orlando C, Maggi CA, Ledda F, Ziche M. Proliferation and migration of endothelial cells is promoted by endothelins via activation of ETB receptors. Am J Physiol Heart Circ Physiol 269: H686-H695, 1995.
99. Moroi M, Zhang L, Yasuda T, Virmani R, Gold HK, Fishman MC. Interaction of genetic deficiency of endothelial nitric oxide, gender, and pregnancy in vascular response to injury in mice. J Clin Invest 101: 1225-1232, 1998.
100. Morris CD. Epidemiology of congenital heart disease. In: Cardiology, edited by Crawford MH, DiMarco JP. London: Mosby International, 2001, p. 1.1-1.8.
101. Namiki A, Hirata Y, Ishikawa M, Moroi M, Aikawa J, Machii K. Endothelin-1- and endothelin-3-induced vasorelaxation via common generation of endothelium-derived nitric oxide. Life Sci 50: 677-682, 1992.
102. Nishida K, Harrison DG, Navas JP, Fisher AA, Dockery SP, Uematsu M, Nerem RM, Alexander RW, Murphy TJ. Molecular cloning and characterization of the constitutive bovine aortic endothelial cell nitric oxide synthase. J Clin Invest 90: 2092-2096, 1992.
103. Noris M, Morigi M, Donadelli R, Aiello S, Foppolo M, Todeschini M, Orisio S, Remuzzi G, Remuzzi A. Nitric oxide synthesis by cultured endothelial cells is modulated by flow conditions. Circ Res 76: 536-543, 1995.
104. Ohashi Y, Kawashima S, Hirata K, Yamashita T, Ishida T, Inoue N, Sakoda T, Kurihara H, Yazaki Y, Yokoyama M. Hypotension and reduced nitric oxide-elicited vasorelaxation in transgenic mice overexpressing endothelial nitric oxide synthase. J Clin Invest 102: 2061-2071, 1998.
105. Olson EN, Srivastava D. Molecular pathways controlling heart development. Science 272: 671-676, 1996.
106. Philipsen S, Suske G. A tale of three fingers: the family of mammalian Sp/XKLF transcription factors. Nucleic Acids Res 27: 2991-3000, 1999.
107. Praetorius HA, Spring KR. Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 184: 71-79, 2001.
108. Purcell EM. Life at low Reynolds number. Am J Physiol 45: 3-9, 1977.
109. Qiu YC, Tarbell JM. Interaction between wall shear stress and circumferential strain affects endothelial cell biochemical production. J Vasc Res 37: 147-157, 2000.
110. Resnick N, Yahav H, Khachigian LM, Collins T, Anderson KR, Dewey FC, Gimbrone MA Jr. Endothelial gene regulation by laminar shear stress. Adv Exp Med Biol 430: 155-164, 1997.
111. Resnick N, Yahav H, Shay-Salit A, Shushy M, Schubert S, Zilberman LC, Wofovitz E. Fluid shear stress and the vascular endothelium: for better and for worse. Prog Biophys Mol Biol 81: 177-199, 2003.
112. Rudic RD, Shesely EG, Maeda N, Smithies O, Segal SS, Sessa WC. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J Clin Invest 101: 731-736, 1998.
113. Sauvageau S, Thorin E, Caron A, Dupuis J. Evaluation of endothelin-1-induced pulmonary vasoconstriction following myocardial infarction. Exp Biol Med 231: 840-846, 2006.
114. Sauvageau S, Thorin E, Caron A, Dupuis J. Endothelin-1-induced pulmonary vasoreactivity is regulated by ET(A) and ET(B) receptor interactions. J Vasc Res 44: 375-381, 2007.
115. Schroder EA, Tobita K, Tinney JP, Foldes JK, Keller BB. Microtubule involvement in the adaptation to altered mechanical load in developing chick myocardium. Circ Res 91: 353-359, 2002.
116. Sedmera D, Pexieder T, Rychterova V, Hu N, Clark EB. Remodeling of chick embryonic ventricular myoarchitecture under experimentally changed loading conditions. Anat Rec 254: 238-252, 1999.
117. SenBanerjee S, Lin Z, Atkins GB, Greif DM, Rao RM, Kumar A, Feinberg MW, Chen Z, Simon DI, Luscinskas FW, Michel TM, Gimbrone MA Jr, Garcia-Cardena G, Jain MK. KLF2 Is a novel transcriptional regulator of endothelial proinflammatory activation. J Exp Med 199: 1305-1315, 2004.
118. Sharefkin JB, Diamond SL, Eskin SG, McIntire LV, Dieffenbach CW. Fluid flow decreases preproendothelin mRNA levels and suppresses endothelin-1 peptide release in cultured human endothelial cells. J Vasc Surg 14: 1-9, 1991.
119. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, Sherman PA, Sessa WC, Smithies O. Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci USA 93: 13176-13181, 1996.
120. Shubeita HE, McDonough PM, Harris AN, Knowlton KU, Glembotski CC, Brown JH, Chien KR. Endothelin induction of inositol phospholipid hydrolysis, sarcomere assembly, and cardiac gene expression in ventricular myocytes. A paracrine mechanism for myocardial cell hypertrophy. J Biol Chem 265: 20555-20562, 1990.
121. Singla V, Reiter JF. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313: 629-633, 2006.
122. Sirviö ML, Metsärinne K, Saijonmaa O, Fyhrquist F. Tissue distribution and half-life of I-125 endothelin in the Rat: importance of pulmonary clearance. Biochem Biophys Res Commun 167: 1191-1195, 1990.
123. Stekelenburg-de Vos S, Steendijk P, Ursem NT, Wladimiroff JW, Delfos R, Poelmann RE. Systolic and diastolic ventricular function assessed by pressure-volume loops in the stage 21 venous clipped chick embryo. Pediatr Res 57: 16-21, 2005.
124. Stekelenburg-de Vos S, Ursem NTC, Hop WCJ, Wladimiroff JW, Gittenberger-de Groot AC, Poelmann RE. Acutely altered hemodynamics following venous obstruction in the early chick embryo. J Exp Biol 206: 1051-1057, 2003.
125. Steudel W, Ichinose F, Huang PL, Hurford WE, Jones RC, Bevan JA, Fishman MC, Zapol WM. Pulmonary vasoconstriction and hypertension in mice with targeted disruption of the endothelial nitric oxide synthase (NOS 3) gene. Circ Res 81: 34-41, 1997.
126. Sun HW, Li CJ, Chen HQ, Lin HL, Lv HX, Zhang Y, Zhang M. Involvement of integrins, MAPK, and NF-kappaB in regulation of the shear stress-induced MMP-9 expression in endothelial cells. Biochem Biophys Res Commun 353: 152-158, 2007.
127. Tamaoki J, Kanemura T, Sakai N, Isono K, Kobayashi K, Takizawa T. Endothelin stimulates ciliary beat frequency and chloride secretion in canine cultured tracheal epithelium. Am J Respir Cell Mol Biol 4: 426-431, 1991.
128. Taniguchi T, Muramatsu I. Pharmacological knock-out of endothelin ET(A) receptors. Life Sci 74: 405-409, 2003.
129. Tobita K, Garrison JB, Liu LJ, Tinney JP, Keller BB. Three-dimensional myofiber architecture of the embryonic left ventricle during normal development and altered mechanical loads. Anat Rec A Discov Mol Cell Evol Biol 283: 193-201, 2005.
130. Tobita K, Schroder EA, Tinney JP, Garrison JB, Keller BB. Regional passive ventricular stress-strain relations during development of altered loads in chick embryo. Am J Physiol Heart Circ Physiol 282: H2386-H2396, 2002.
131. Topper JN, Gimbrone MA Jr. Blood flow and vascular gene expression: fluid shear stress as a modulator of endothelial phenotype. Mol Med Today 5: 40-46, 1999.
132. Traub O, Berk BC. Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force. Arterioscler Thromb Vasc Biol 18: 677-685, 1998.
133. Tsukahara H, Ende H, Magazine HI, Bahou WF, Goligorsky MS. Molecular and functional characterization of the non-isopeptide-selective ETB receptor in endothelial cells. Receptor coupling to nitric oxide synthase. J Biol Chem 269: 21778-21785, 1994.
134. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, Cao G, DeLisser H, Schwartz MA. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437: 426-431, 2005.
135. Ursem NTC, Stekelenburg-de Vos S, Wladimiroff JW, Poelmann RE, Gittenberger-de Groot AC, Hu N, Clark EB. Ventricular diastolic filling characteristics in stage-24 chick embryos after extra-embryonic venous obstruction. J Exp Biol 207: 1487-1490, 2004.
136. Van der Heiden K, Groenendijk BCW, Hierck BP, Hogers B, Koerten HK, Mommaas AM, Gittenberger-de-Groot AC, Poelmann RE. Monocilia on chicken embryonic endocardium in low shear stress areas. Dev Dyn 235: 19-28, 2006.
137. Van der Heiden K, Hierck BP, Krams R, de Crom R, Cheng C, Baiker M, Pourquie MJBM, Alkemade FE, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE. Endothelial primary cilia in areas of disturbed flow are at the base of atherosclerosis. Atherosclerosis. In Press. doi:10.1016/j. atherosclerosis.2007.05.030.
138. Vennemann P, Kiger KT, Lindken R, Groenendijk BCW, Stekelenburg-de Vos S, ten Hagen TLM, Ursem NTC, Poelmann RE, Westerweel J, Hierck BP. In vivo micro particle image velocimetry measurements of blood-plasma in the embryonic avian heart. J Biomech 39: 1191-1200, 2006.
139. Verhaar MC, Strachan FE, Newby DE, Cruden NL, Koomans HA, Rabelink TJ, Webb DJ. Endothelin-A receptor antagonist-mediated vasodilatation is attenuated by inhibition of nitric oxide synthesis and by endothelin-B receptor blockade. Circulation 97: 752-756, 1998.
140. Wagner OF, Christ G, Wojta J, Vierhapper H, Parzer S, Nowotny PJ, Schneider B, Waldhausl W, Binder BR. Polar secretion of endothelin-1 by cultured endothelial cells. J Biol Chem 267: 16066-16068, 1992.
141. Walshe TE, Ferguson G, Connell P, O'Brien C, Cahill PA. Pulsatile flow increases the expression of eNOS, ET-1, and prostacyclin in a novel in vitro coculture model of the retinal vasculature. Invest Ophthalmol Vis Sci 46: 375-382, 2005.
142. Wang CY, Bassingthwaighte JB. Blood flow in small curved tubes. J Biomech Eng 125: 910-913, 2003.
143. Wang G, Cai S, Deng X, Ouyang K, Xie G, Guidoin R. Secretory response of endothelin-1 in cultured human glomerular microvascular endothelial cells to shear stress. Biorheology 37: 291-299, 2000.
144. Wang GX, Cai SX, Wang PQ, Ouyang KQ, Wang YL, Xu SR. Shear-induced changes in endothelin-1 secretion of microvascular endothelial cells. Microvasc Res 63: 209-217, 2002.
145. Wang NP, Miao H, Li YS, Zhang P, Haga JH, Hu YL, Young A, Yuan SL, Nguyen P, Wu CC, Chien S. Shear stress regulation of Kruppel-like factor 2 expression is flow pattern-specific. Biochem Biophys Res Commun 341: 1244-1251, 2006.
146. Wani MA, Means RT Jr, Lingrel JB. Loss of LKLF function results in embryonic lethality in mice. Transgenic Res 7: 229-238, 1998.
147. Weinbaum S, Zhang X, Han Y, Vink H, Cowin SC. Mechanotransduction and flow across the endothelial glycocalyx. Proc Natl Acad Sci USA 100: 7988-7995, 2003.
148. Womersley JR. Method for the calculation of velocity, rate of flow and viscous drag in arteries when the pressure gradient is known. J Physiol 127: 553-563, 1955.
149. Xue C, Botkin SJ, Johns RA. Localization of endothelial NOS at the basal microtubule membrane in ciliated epithelium of rat lung. J Histochem Cytochem 44: 463-471, 1996.
150. Yamazaki T, Komuro I, Kudoh S, Zou Y, Shiojima I, Hiroi Y, Mizuno T, Maemura K, Kurihara H, Aikawa R, Takano H, Yazaki Y. Endothelin-1 is involved in mechanical stress-induced cardiomyocyte hypertrophy. J Biol Chem 271: 3221-3228, 1996.
151. Yan C, Takahashi M, Okuda M, Lee JD, Berk BC. Fluid shear stress stimulates big mitogen-activated protein kinase 1 (BMK1) activity in endothelial cells. Dependence on tyrosine kinases and intracellular calcium. J Biol Chem 274: 143-150, 1999.
152. Yanagisawa H, Yanagisawa M, Kapur RP, Richardson JA, Williams SC, Clouthier DE, de Wit D, Emoto N, Hammer RE. Dual genetic pathways of endothelin-mediated intercellular signaling revealed by targeted disruption of endothelin converting enzyme-1 gene. Development 125: 825-836, 1998.
153. Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, Yazaki Y, Goto K, Masaki T. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332: 411-415, 1988.
154. Yang CC, Ornatsky OI, McDermott JC, Cruz TF, Prody CA. Interaction of myocyte enhancer factor 2 (MEF2) with a mitogen-activated protein kinase, ERK5/BMK1. Nucleic Acids Res 26: 4771-4777, 1998.
155. Yang Z, Krasnici N, Luscher TF. Endothelin-1 potentiates human smooth muscle cell growth to PDGF: effects of ETA and ETB receptor blockade. Circulation 100: 5-8, 1999.
156. Yoshimoto S, Ishizaki Y, Mori A, Sasaki T, Takakura K, Murota SI. The role of cerebral microvessel endothelium in regulation of cerebral blood-flow through production of endothelin-1. J Cardiovasc Pharmacol 17: S260-S263, 1991.
157. Yoshizumi M, Kurihara H, Sugiyama T, Takaku F, Yanagisawa M, Masaki T, Yasaki Y. Hemodynamic shear stress stimulates endothelin production by cultured endothelial cells. Biochim Biophys Res Commun 161: 859-864, 1989.
158. Yost HJ. Left-right asymmetry: nodal cilia make and catch a wave. Curr Biol 13: R808-R809, 2003.
159. Zhang YM, Wang KQ, Zhou GM, Zuo J, Ge JB. Endothelin-1 promoted proliferation of vascular smooth muscle cell through pathway of extracellular signal-regulated kinase and cyclin D1. Acta Pharmacol Sin 24: 563-568, 2003.
160. Ziegler T, Bouzourene K, Harrison VJ, Brunner HR, Hayoz D. 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, 1998.
161. Ziegler T, Silacci P, Harrison VJ, Hayoz D. Nitric oxide synthase expression in endothelial cells exposed to mechanical forces. Hypertension 32: 351-355, 1998.