Advertisement

Mechanosensitive Pro-inflammatory Gene Expression in Vascular Cells

  • Marco Cattaruzza
  • Andreas H. Wagner
  • Markus HeckerEmail author
Chapter
Part of the Mechanosensitivity in Cells and Tissues book series (MECT, volume 5)

Abstract

A delicate balance between circumferential wall tension (CWT) or stretch and unidirectional fluid shear stress (FSS), the two principle haemodynamic forces to which the resident cells of the vessel wall are exposed to, governs their phenotype. FSS by virtue of its stimulatory effect on endothelial nitric oxide (NO) synthase activity and expression has been designated as an anti-inflammatory and homeostatic force. In contrast, CWT has been marked as a potentially detrimental pro-inflammatory force causing, e.g. formation of reactive oxygen species, stimulation of stress-activated protein kinases and a prolonged rise in intracellular free calcium. Moreover, with zyxin localised to focal adhesions, a mechanosensitive protein has been characterised that specially transduces an increase in CWT to the nucleus of both endothelial and smooth muscle cells where it orchestrates a complex and partially pro-inflammatory change in gene expression. Tilting the balance between FSS and CWT towards CWT as the result of an inadequately low FSS, e.g. at arterial bifurcations, or volume and/or pressure overload as, e.g. in hypertension, is generally thought to be responsible for both adaptive and maladaptive vascular remodelling processes including arteriogenesis, atherosclerosis, restenosis following angioplasty, and hypertension-induced arterial remodelling. Starting with a summary of the molecular mechanisms governing CWT and FSS-mediated signal transduction in vascular cells, the differential and variable impact of haemodynamically induced pro-inflammatory gene expression on these remodelling processes is discussed herein.

Keywords

Endothelial cells Vascular smooth muscle cells Stretch Shear stress Pro-inflammatory gene expression Transcriptional regulation Remodelling 

Notes

Acknowledgements

The authors work is supported by the German Research Foundation (DFG), the Federal Ministry of Research and Education (BMBF), the European Commission and the German Cardiac Society (DGK). We are indebted to Dr. Gerd König for the making of the figures and critically reading the manuscript.

References

  1. Abate C, Patel L, Rauscher FJ 3rd, Curran T (1990) Redox regulation of fos and jun DNA-binding activity in vitro. Science 249:1157–1161PubMedGoogle Scholar
  2. Amma H, Naruse K, Ishiguro N, Sokabe M (2005) Involvement of reactive oxygen species in cyclic stretch-induced NF-κB activation in human fibroblast cells. Br J Pharmacol 145:364–373PubMedGoogle Scholar
  3. Asif AR, Hecker M, Cattaruzza M (2009a) Disinhibition of SOD-2 expression to compensate for a genetically determined NO deficit in endothelial cells – brief report. Arterioscler Thromb Vasc Biol 29:1890–1893PubMedGoogle Scholar
  4. Asif AR, Oellerich M, Armstrong VW, Hecker M, Cattaruzza M (2009b) T-786C polymorphism of the NOS-3 gene and the endothelial cell response to fluid shear stress-a proteome analysis. J Proteome Res 8:3161–3168PubMedGoogle Scholar
  5. Bach I (2000) The LIM domain: regulation by association. Mech Dev 91:5–17PubMedGoogle Scholar
  6. Beckerle MC (1997) Zyxin: zinc fingers at sites of cell adhesion. Bioessays 19:949–957PubMedGoogle Scholar
  7. Behm CZ, Kaufmann BA, Carr C, Lankford M, Sanders JM, Rose CE, Kaul S, Lindner JR (2008) Molecular imaging of endothelial vascular cell adhesion molecule-1 expression and inflammatory cell recruitment during vasculogenesis and ischemia-mediated arteriogenesis. Circulation 117:2902–2911PubMedGoogle Scholar
  8. Boon RA, Horrevoets AJ (2009) Key transcriptional regulators of the vasoprotective effects of shear stress. Hamostaseologie 29:39–43PubMedGoogle Scholar
  9. Busse R, Fleming I (1996) Endothelial dysfunction in atherosclerosis. J Vasc Res 33:181–194PubMedGoogle Scholar
  10. Cattaruzza M, Hecker M (2008) Protein carbonylation and decarboylation: a new twist to the complex response of vascular cells to oxidative stress. Circ Res 102:273–274PubMedGoogle Scholar
  11. Cattaruzza M, Berger MM, Ochs M, Fayyazi A, Füzesi L, Richter J, Hecker M (2002a) Deformation-induced endothelin B receptor-mediated smooth muscle cell apoptosis is matrix-dependent. Cell Death Differ 9:219–226PubMedGoogle Scholar
  12. Cattaruzza M, Schäfer K, Hecker M (2002b) Cytokine-induced down-regulation of zfm1/splicing factor-1 promotes smooth muscle cell proliferation. J Biol Chem 277:6582–6589PubMedGoogle Scholar
  13. Cattaruzza M, Słodowski W, Stojakovic M, Krzesz R, Hecker M (2003) Interleukin-10 induction of nitric-oxide synthase expression attenuates CD40-mediated interleukin-12 synthesis in human endothelial cells. J Biol Chem 278:37874–37880PubMedGoogle Scholar
  14. Cattaruzza M, Guzik TJ, Słodowski W, Pelvan A, Becker J, Halle M, Buchwald AB, Channon KM, Hecker M (2004a) Shear stress insensitivity of endothelial nitric oxide synthase expression as a genetic risk factor for coronary heart disease. Circ Res 95:841–847PubMedGoogle Scholar
  15. Cattaruzza M, Lattrich C, Hecker M (2004b) Focal adhesion protein zyxin is a mechanosensitive modulator of gene expression in vascular smooth muscle cells. Hypertension 43:726–730PubMedGoogle Scholar
  16. Chen Z, Rubin J, Tzima E (2010) Role of PECAM-1 in arteriogenesis and specification of preexisting collaterals. Circ Res 107:1355–1363PubMedGoogle Scholar
  17. Cheng JJ, Wung BS, Chao YJ, Wang DL (1998) Cyclic strain-induced reactive oxygen species involved in ICAM-1 gene induction in endothelial cells. Hypertension 31:125–130PubMedGoogle Scholar
  18. Cheng JJ, Wung BS, Chao YJ, Wang DL (2001) Sequential activation of protein kinase C (PKC)-α and PKC- ε contributes to sustained Raf/ERK1/2 activation in endothelial cells under mechanical strain. J Biol Chem 276:31368–31375PubMedGoogle Scholar
  19. Choi C, Sellak H, Brown FM, Lincoln TM 2010 cGMP-dependent protein kinase and the regulation of vascular smooth muscle cell gene expression: possible involvement of Elk-1 sumoylation. Am J Physiol Heart Circ Physiol 299:H1660–H1670PubMedGoogle Scholar
  20. Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T (1995) Transcriptional regulation of endothelial cell adhesion molecules: NF-κB and cytokine-inducible enhancers. FASEB J 9:899–909PubMedGoogle Scholar
  21. Colombelli J, Besser A, Kress H, Reynaud EG, Girard P, Caussinus E, Haselmann U, Small JV, Schwarz US, Stelzer EH (2009) Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization. J Cell Sci 122:1665–1679PubMedGoogle Scholar
  22. Colombo MG, Paradossi U, Andreassi MG, Botto N, Manfredi S, Masetti S, Biagini A, Clerico A (2003) Endothelial nitric oxide synthase gene polymorphisms and risk of coronary artery disease. Clin Chem 49:389–395PubMedGoogle Scholar
  23. Crawford AW, Beckerle MC (1991) Purification and characterization of zyxin, an 82,000-dalton component of adherens junctions. J Biol Chem 266:5847–5853PubMedGoogle Scholar
  24. Crawford AW, Michelsen JW, Beckerle MC (1992) An interaction between zyxin and α-actinin. J Cell Biol 116:1381–1393PubMedGoogle Scholar
  25. Davies PF, Civelek M, Fang Y, Guerraty MA, Passerini AG (2010) Endothelial heterogeneity associated with regional athero-susceptibility and adaptation to disturbed blood flow in vivo. Semin Thromb Hemost 36:265–275PubMedGoogle Scholar
  26. Davis B, Zou MH (2005) CD40 ligand-dependent tyrosine nitration of prostacyclin synthase in vivo. Circulation 112:2184–2192PubMedGoogle Scholar
  27. Davis ME, Grumbach IM, Fukai T, Cutchins A, Harrison DG (2004) Shear stress regulates endothelial nitric-oxide synthase promoter activity through nuclear factor κB binding. J Biol Chem 279:163–168PubMedGoogle Scholar
  28. Deliri H, McNamara CA (2007) Nox 4 regulation of vascular smooth muscle cell differentiation marker gene expression. Arterioscler Thromb Vasc Biol 27:12–14PubMedGoogle Scholar
  29. Demicheva E, Hecker M, Korff T (2008) Stretch-induced activation of the transcription factor activator protein-1 controls monocyte chemoattractant protein-1 expression during arteriogenesis. Circ Res 103:477–484PubMedGoogle Scholar
  30. Du W, Mills I, Sumpio BE (1995) Cyclic strain causes heterogeneous induction of transcription factors, AP-1, CRE binding protein and NF-κB, in endothelial cells: species and vascular bed diversity. J Biomech 28:1485–1491PubMedGoogle Scholar
  31. Du KL, Ip HS, Li J, Chen M, Dandre F, Yu W, Lu MM, Owens GK, Parmacek MS (2003) Myocardin is a critical serum response factor cofactor in the transcriptional program regulating smooth muscle cell differentiation. Mol Cell Biol 23:2425–2437PubMedGoogle Scholar
  32. Förstermann U, Kleinert H (1995) Nitric oxide synthase: expression and expressional control of the three isoforms. Naunyn Schmiedebergs Arch Pharmacol 352:351–364PubMedGoogle Scholar
  33. Frangos SG, Knox R, Yano Y, Chen E, Di Luozzo G, Chen AH, Sumpio BE (2001) The integrin-mediated cyclic strain-induced signaling pathway in vascular endothelial cells. Endothelium 8:1–10PubMedGoogle Scholar
  34. Glagov S, Zarins C, Giddens DP, Ku DN (1988) Hemodynamics and atherosclerosis. Insights and perspectives gained from studies of human arteries. Arch Pathol Lab Med 112:1018–1031PubMedGoogle Scholar
  35. Goettsch C, Goettsch W, Muller G, Seebach J, Schnittler HJ, Morawietz H (2009) Nox4 overexpression activates reactive oxygen species and p38 MAPK in human endothelial cells. Biochem Biophys Res Commun 380:355–360PubMedGoogle Scholar
  36. Gopalakrishna R, Jaken S (2000) Protein kinase C signaling and oxidative stress. Free Radic Biol Med 28:1349–1361PubMedGoogle Scholar
  37. Guest TM, Vlastos G, Alameddine FM, Taylor WR (2006) Mechanoregulation of monocyte chemoattractant protein-1 expression in rat vascular smooth muscle cells. Antioxid Redox Signal 8:1461–1471PubMedGoogle Scholar
  38. Guzik TJ, Mussa S, Gastaldi D, Sadowski J, Ratnatunga C, Pillari R, Channon KM (2002) Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation 105:1656–1662PubMedGoogle Scholar
  39. Hamik A, Lin Z, Kumar A, Balcells M, Sinha S, Katz J, Feinberg MW, Gerzsten RE, Edelman ER, Jain MK (2007) Kruppel-like factor 4 regulates endothelial inflammation. J Biol Chem 282:13769–13779PubMedGoogle Scholar
  40. Hansen MD, Beckerle MC (2006) Opposing roles of zyxin/LPP ACTA repeats and the LIM domain region in cell-cell adhesion. J Biol Chem 281:16178–16188PubMedGoogle Scholar
  41. Hastings NE, Simmers MB, McDonald OG, Wamhoff BR, Blackman BR (2007) Atherosclerosis-prone hemodynamics differentially regulates endothelial and smooth muscle cell phenotypes and promotes pro-inflammatory priming. Am J Physiol Cell Physiol 293:C1824–C1833PubMedGoogle Scholar
  42. Hay DC, Beers C, Cameron V, Thomson L, Flitney FW, Hay RT (2003) Activation of NF-κB nuclear transcription factor by flow in human endothelial cells. Biochim Biophys Acta 1642:33–44PubMedGoogle Scholar
  43. Hecker M, Mülsch A, Bassenge E, Busse R (1993) Vasoconstriction and increased flow: two principal mechanisms of shear stress-dependent endothelial autacoid release. Am J Physiol 265:H828–H833PubMedGoogle Scholar
  44. Hellstrand P, Albinsson S (2005) Stretch-dependent growth and differentiation in vascular smooth muscle: role of the actin cytoskeleton. Can J Physiol Pharmacol 83:869–875PubMedGoogle Scholar
  45. Helmke BP, Davies PF (2002) The cytoskeleton under external fluid mechanical forces: hemodynamic forces acting on the endothelium. Ann Biomed Eng 30:284–296PubMedGoogle Scholar
  46. Hildebrandt A, Hecker M, Wagner AH (2009) Cyclic stretch-mediated tyrosine nitration of CD40 impairs CD40 ligand-stimulated IL12p40 expression in human endothelial cells. Acta Physiol 195:O529Google Scholar
  47. Hill-Eubanks DC, Gomez MF, Stevenson AS, Nelson MT (2003) NFAT regulation in smooth muscle. Trends Cardiovasc Med 13:56–62PubMedGoogle Scholar
  48. Hirata H, Tatsumi H, Sokabe M (2008a) Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-dependent manner. J Cell Sci 121:2795–2804PubMedGoogle Scholar
  49. Hirata H, Tatsumi H, Sokabe M (2008b) Zyxin emerges as a key player in the mechanotransduction at cell adhesive structures. Commun Integr Biol 1:192–195PubMedGoogle Scholar
  50. Hoffman LM, Jensen CC, Kloeker S, Wang CL, Yoshigi M, Beckerle MC (2006) Genetic ablation of zyxin causes Mena/VASP mislocalization, increased motility, and deficits in actin remodeling. J Cell Biol 172:771–782PubMedGoogle Scholar
  51. Hojo Y, Saito Y, Tanimoto T, Hoefen RJ, Baines CP, Yamamoto K, Haendeler J, Asmis R, Berk BC (2002) Fluid shear stress attenuates hydrogen peroxide-induced c-Jun NH2-terminal kinase activation via a glutathione reductase-mediated mechanism. Circ Res 91:712–718PubMedGoogle Scholar
  52. Howard AB, Alexander RW, Nerem RM, Griendling KK, Taylor WR (1997) Cyclic strain induces an oxidative stress in endothelial cells. Am J Physiol 272:C421–C427PubMedGoogle Scholar
  53. Hsiai TK, Cho SK, Wong PK, Ing M, Salazar A, Sevanian A, Navab M, Demer LL, Ho CM (2003) Monocyte recruitment to endothelial cells in response to oscillatory shear stress. FASEB J 17:1648–1657PubMedGoogle Scholar
  54. Ishibashi M, Hiasa K, Zhao Q, Inoue S, Ohtani K, Kitamoto S, Tsuchihashi M, Sugaya T, Charo IF, Kura S, Tsuzuki T, Ishibashi T, Takeshita A, Egashira K (2004) Critical role of monocyte chemoattractant protein-1 receptor CCR2 on monocytes in hypertension-induced vascular inflammation and remodeling. Circ Res 94:1203–1210PubMedGoogle Scholar
  55. Kanungo J, Pratt SJ, Marie H, Longmore GD (2000) Ajuba, a cytosolic LIM protein, shuttles into the nucleus and affects embryonal cell proliferation and fate decisions. Mol Biol Cell 11:3299–3313PubMedGoogle Scholar
  56. Karin M, Liu Z, Zandi E (1997) AP-1 function and regulation. Curr Opin Cell Biol 9:240–246PubMedGoogle Scholar
  57. Kato T, Muraski J, Chen Y, Tsujita Y, Wall J, Glembotski CC, Schaefer E, Beckerle M, Sussman MA (2005) Atrial natriuretic peptide promotes cardiomyocyte survival by cGMP-dependent nuclear accumulation of zyxin and Akt. J Clin Invest 115:2716–2730PubMedGoogle Scholar
  58. Kawai-Kowase K, Owens GK (2007) Multiple repressor pathways contribute to phenotypic switching of vascular smooth muscle cells. Am J Physiol Cell Physiol 292:C59–C69PubMedGoogle Scholar
  59. Kawashima S, Yokoyama M (2004) Dysfunction of endothelial nitric oxide synthase and atherosclerosis. Arterioscler Thromb Vasc Biol 24:998–1005PubMedGoogle Scholar
  60. Kelkenberg U, Wagner AH, Sarhaddar J, Hecker M, von der Leyen HE (2002) CCAAT/enhancer-binding protein decoy oligodeoxynucleotide inhibition of macrophage-rich vascular lesion formation in hypercholesterolemic rabbits. Arterioscler Thromb Vasc Biol 22:949–954PubMedGoogle Scholar
  61. Kida T, Chuma H, Murata T, Yamawaki H, Matsumoto S, Hori M, Ozaki H (2010) Chronic treatment with PDGF-BB and endothelin-1 synergistically induces vascular hyperplasia and loss of contractility in organ-cultured rat tail artery. Atherosclerosis. [PMID: 21129745, Epub ahead of print]Google Scholar
  62. Kinlay S, Libby P, Ganz P (2001) Endothelial function and coronary artery disease. Curr Opin Lipidol 12:383–389PubMedGoogle Scholar
  63. Klotz LO, Schroeder P, Sies H (2002) Peroxynitrite signaling: receptor tyrosine kinases and activation of stress-responsive pathways. Free Radic Biol Med 33:737–743PubMedGoogle Scholar
  64. Korff T, Aufgebauer K, Hecker M (2007) Cyclic stretch controls the expression of CD40 in endothelial cells by changing their transforming growth factor-β1 response. Circulation 116:2288–2297PubMedGoogle Scholar
  65. Korff T, Braun J, Pfaff D, Augustin HG, Hecker M (2008) Role of ephrinB2 expression in endothelial cells during arteriogenesis: Impact on smooth muscle cell migration and monocyte recruitment. Blood 112:73–81PubMedGoogle Scholar
  66. Kumar A, Knox AJ, Boriek AM (2003) CCAAT/enhancer-binding protein and activator protein-1 transcription factors regulate the expression of interleukin-8 through the mitogen-activated protein kinase pathways in response to mechanical stretch of human airway smooth muscle cells. J Biol Chem 278:18868–18876PubMedGoogle Scholar
  67. Kuwahara K, Kinoshita H, Kuwabara Y, Nakagawa Y, Usami S, Minami T, Yamada Y, Fujiwara M, Nakao K (2010) Myocardin-related transcription factor A is a common mediator of mechanical stress- and neurohumoral stimulation-induced cardiac hypertrophic signaling leading to activation of brain natriuretic peptide gene expression. Mol Cell Biol. 30:4134–4148PubMedGoogle Scholar
  68. Laumonnier Y, Nadaud S, Agrapart M, Soubrier F (2000) Characterization of an upstream enhancer region in the promoter of the human endothelial nitric-oxide synthase gene. J Biol Chem 275:40732–40741PubMedGoogle Scholar
  69. Lauth M, Wagner AH, Cattaruzza M, Orzechowski HD, Paul M, Hecker M (2000) Transcriptional control of deformation-induced preproendothelin-1 gene expression in endothelial cells. J Mol Med 78:441–450PubMedGoogle Scholar
  70. Lehoux S, Castier Y, Tedgui A (2006) Molecular mechanisms of the vascular responses to haemodynamic forces. J Intern Med 259:381–392PubMedGoogle Scholar
  71. Libby P (2007) Inflammatory mechanisms: the molecular basis of inflammation and disease. Nutr Rev 65:S140–S146PubMedGoogle Scholar
  72. Lutgens E, Gorelik L, Daemen MJ, de Muinck ED, Grewal IS, Koteliansky VE, Flavell RA (1999) Requirement for CD154 in the progression of atherosclerosis. Nat Med 5:1313–1316PubMedGoogle Scholar
  73. Macarthur H, Warner TD, Wood EG, Corder R, Vane JR (1994) Endothelin-1 release from endothelial cells in culture is elevated both acutely and chronically by short periods of mechanical stretch. Biochem Biophys Res Commun 200:395–400PubMedGoogle Scholar
  74. McCubrey JA, Lahair MM, Franklin RA (2006) Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid Redox Signal 8:1775–1789PubMedGoogle Scholar
  75. Melchers I, Blaschke S, Hecker M, Cattaruzza M (2006) The -786C/T single-nucleotide polymorphism in the promoter of the gene for endothelial nitric oxide synthase: insensitivity to physiologic stimuli as a risk factor for rheumatoid arthritis. Arthritis Rheum 54:3144–3151PubMedGoogle Scholar
  76. Mohamed JS, Lopez MA, Boriek AM (2010) Mechanical stretch up-regulates microRNA-26a and induces human airway smooth muscle hypertrophy by suppressing glycogen synthase kinase-3β. J Biol Chem 285:29336–29347PubMedGoogle Scholar
  77. Molavi B, Mehta JL (2004) Oxidative stress in cardiovascular disease: molecular basis of its deleterious effects, its detection, and therapeutic considerations. Curr Opin Cardiol 19:488–493PubMedGoogle Scholar
  78. Musunuru K, Kathiresan S (2010) Genetics of coronary artery disease. Annu Rev Genomics Hum Genet 11:91–108PubMedGoogle Scholar
  79. Ngu H, Feng Y, Lu L, Oswald SJ, Longmore GD, Yin FC (2010) Effect of focal adhesion proteins on endothelial cell adhesion, motility and orientation response to cyclic strain. Ann Biomed Eng 38:208–222PubMedGoogle Scholar
  80. Nilsson LM, Sun ZW, Nilsson J, Nordström I, Chen YW, Molkentin JD, Wide-Swensson D, Hellstrand P, Lydrup ML, Gomez MF (2006) Novel blocker of NFAT activation inhibits IL-6 production in human myometrial arteries and reduces vascular smooth muscle cell proliferation. Am J Physiol Cell Physiol 292:C1167–C1178PubMedGoogle Scholar
  81. Nix DA, Fradelizi J, Bockholt S, Menichi B, Louvard D, Friederich E, Beckerle MC (2001) Targeting of zyxin to sites of actin membrane interaction and to the nucleus. J Biol Chem 276:34759–34767PubMedGoogle Scholar
  82. Pan S (2009) Molecular mechanisms responsible for the atheroprotective effects of laminar shear stress. Antioxid Redox Signal 11:1669–1682PubMedGoogle Scholar
  83. Petit MM, Fradelizi J, Golsteyn RM, Ayoubi TA, Menichi B, Louvard D, Van de Ven WJ, Friederich E (2000) LPP, an actin cytoskeleton protein related to zyxin, harbors a nuclear export signal and transcriptional activation capacity. Mol Biol Cell 11:117–129PubMedGoogle Scholar
  84. Phipps RP, Koumas L, Leung E, Reddy SY, Blieden T, Kaufman J (2001) The CD40-CD40 ligand system: a potential therapeutic target in atherosclerosis. Curr Opin Investig Drugs 2:773–777PubMedGoogle Scholar
  85. Porreca E, Di Febbo C, Reale M, Castellani ML, Baccante G, Barbacane R, Conti P, Cuccurullo F, Poggi A (1997) Monocyte chemotactic protein 1 (MCP-1) is a mitogen for cultured rat vascular smooth muscle cells. J Vasc Res 34:58–65PubMedGoogle Scholar
  86. Reinhard M, Jouvenal K, Tripier D, Walter U (1995) Identification, purification, and characterization of a zyxin-related protein that binds the focal adhesion and microfilament protein VASP (vasodilator-stimulated phosphoprotein. Proc Natl Acad Sci USA 92:7956–7960PubMedGoogle Scholar
  87. Reinhard M, Zumbrunn J, Jaquemar D, Kuhn M, Walter U, Trueb B (1999) An α-actinin binding site of zyxin is essential for subcellular zyxin localization and α-actinin recruitment. J Biol Chem 274:13410–13418PubMedGoogle Scholar
  88. Rossi GP, Taddei S, Virdis A, Cavallin M, Ghiadoni L, Favilla S, Versari D, Sudano I, Pessina AC, Salvetti A (2003) The T-786C and Glu298Asp polymorphisms of the endothelial nitric oxide gene affect the forearm blood flow responses of Caucasian hypertensive patients. J Am Coll Cardiol 41:938–945PubMedGoogle Scholar
  89. Schaper W (2009) Collateral circulation: past and present. Basic Res Cardiol 104:5–21PubMedGoogle Scholar
  90. Schaper W, Scholz D (2003) Factors regulating arteriogenesis. Arterioscler Thromb Vasc Biol 23:1143–1151PubMedGoogle Scholar
  91. Schepers A, Eefting D, Bonta PI, Grimbergen JM, de Vries MR, van Weel V, de Vries CJ, Egashira K, van Bockel JH, Quax PH (2006) Anti-MCP-1 gene therapy inhibits vascular smooth muscle cells proliferation and attenuates vein graft thickening both in vitro and in vivo. Arterioscler Thromb Vasc Biol 26:2063–2069PubMedGoogle Scholar
  92. Schlossmann J, Desch M (2009) cGK substrates. Handb Exp Pharmacol 191:163–193PubMedGoogle Scholar
  93. Schwartz RS, Chronos NA, Virmani R (2004) Preclinical restenosis models and drug-eluting stents: still important, still much to learn. J Am Coll Cardiol 44:1373–1385PubMedGoogle Scholar
  94. Scott DW, Loo G (2007) Curcumin-induced GADD153 upregulation: modulation by glutathione. J Cell Biochem 101:307–320PubMedGoogle Scholar
  95. Sen CK, Packer L (1996) Antioxidant and redox regulation of gene transcription. FASEB J 10:709–720PubMedGoogle Scholar
  96. 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, García-Cardeña G, Jain MK (2004) KLF2 Is a novel transcriptional regulator of endothelial proinflammatory activation. J Exp Med 199:1305–1315PubMedGoogle Scholar
  97. Sessa WC, Pritchard K, Seyedi N, Wang J, Hintze TH (1994) Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide synthase gene expression. Circ Res 74:349–353PubMedGoogle Scholar
  98. Sharma GD, Nguyen HT, Antonov AS, Gerrity RG, von Geldern T, Pandey KN (2002) Expression of atrial natriuretic peptide receptor-A antagonizes the mitogen-activated protein kinases (Erk2 and P38MAPK) in cultured human vascular smooth muscle cells. Mol Cell Biochem 233:165–173PubMedGoogle Scholar
  99. Sharma SK, Sweeny J, Kini AS (2010) Coronary bifurcation lesions: a current update. Cardiol Clin 28:55–70PubMedGoogle Scholar
  100. Silacci P, Formentin K, Bouzourène K, Daniel F, Brunner HR, Hayoz D (2000) Unidirectional and oscillatory shear stress differentially modulate NOS III gene expression. Nitric Oxide 4:47–56PubMedGoogle Scholar
  101. Silacci P, Desgeorges A, Mazzolai L, Chambaz C, Hayoz D (2001) Flow pulsatility is a critical determinant of oxidative stress in endothelial cells. Hypertension 38:1162–1166PubMedGoogle Scholar
  102. Souza JM, Choi I, Chen Q, Weisse M, Daikhin E, Yudkoff M, Obin M, Ara J, Horwitz J, Ischiropoulos H (2000) Proteolytic degradation of tyrosine nitrated proteins. Arch Biochem Biophys 380:360–366PubMedGoogle Scholar
  103. Tedgui A, Mallat Z (2001) Anti-inflammatory mechanisms in the vascular wall. Circ Res 88:877–887PubMedGoogle Scholar
  104. Uematsu M, Ohara Y, Navas JP, Nishida K, Murphy TJ, Alexander RW, Nerem RM, Harrison DG (1995) Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress. Am J Physiol 269:C1371–C1378PubMedGoogle Scholar
  105. van Halm VP, Peters MJ, Voskuyl AE, Boers M, Lems WF, Visser M, Stehouwer CD, Spijkerman AM, Dekker JM, Nijpels G, Heine RJ, Bouter LM, Smulders YM, Dijkmans BA, Nurmohamed MT (2009) Rheumatoid arthritis versus diabetes as a risk factor for cardiovascular disease: a cross-sectional study, the CARRE Investigation. Ann Rheum Dis 68:1395–1400PubMedGoogle Scholar
  106. Vasioukhin V, Bauer C, Yin M, Fuchs E (2000) Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100:209–219PubMedGoogle Scholar
  107. Wagner AH, Schroeter MR, Hecker M (2001) 17β-Estradiol inhibition of NADPH oxidase expression in human endothelial cells. FASEB J 15:2121–2130PubMedGoogle Scholar
  108. Wagner AH, Kautz O, Fricke K, Zerr-Fouineau M, Demicheva E, Güldenzoph B, Bermejo JL, Korff T, Hecker M (2009) Upregulation of glutathione peroxidase offsets stretch-induced proatherogenic gene expression in human endothelial cells. Arterioscler Thromb Vasc Biol 29:1894–1901PubMedGoogle Scholar
  109. Wang DS, Proffit D, Tsao PS (2001) Mechanotransduction of endothelial oxidative stress induced by cyclic strain. Endothelium 8:283–291PubMedGoogle Scholar
  110. Wang Y, Gilmore TD (2003) Zyxin and paxillin proteins: focal adhesion plaque LIM domain proteins go nuclear. Biochim Biophys Acta 1593:115–120PubMedGoogle Scholar
  111. Wang Z, Wang DZ, Hockemeyer D, McAnally J, Nordheim A, Olson EN (2004) Myocardin and ternary complex factors compete for SRF to control smooth muscle gene expression. Nature 428:185–189PubMedGoogle Scholar
  112. Weber M, Baker MB, Moore JP, Searles CD (2010) MiR-21 is induced in endothelial cells by shear stress and modulates apoptosis and eNOS activity. Biochem Biophys Res Commun 393:643–648PubMedGoogle Scholar
  113. Wójtowicz A, Babu SS, Li L, Gretz N, Hecker M, Cattaruzza M (2010) Zyxin mediation of stretch-induced gene expression in human endothelial cells. Circ Res 107:898–902PubMedGoogle Scholar
  114. Won D, Zhu SN, Chen M, Teichert AM, Fish JE, Matouk CC, Bonert M, Ojha M, Marsden PA, Cybulsky MI (2007) Relative reduction of endothelial nitric-oxide synthase expression and transcription in atherosclerosis-prone regions of the mouse aorta and in an in vitro model of disturbed flow. Am J Pathol 171:1691–1704PubMedGoogle Scholar
  115. Wung BS, Cheng JJ, Hsieh HJ, Shyy YJ, Wang DL (1997) Cyclic strain-induced monocyte chemotactic protein-1 gene expression in endothelial cells involves reactive oxygen species activation of activator protein 1. Circ Res 81:1–7PubMedGoogle Scholar
  116. Xin M, Small EM, Sutherland LB, Qi X, McAnally J, Plato CF, Richardson JA, Bassel-Duby R, Olson EN (2009) MicroRNAs miR-143 and miR-145 modulate cytoskeletal dynamics and responsiveness of smooth muscle cells to injury. Genes Dev 23:2166–2178PubMedGoogle Scholar
  117. Yoshida T, Sinha S, Dandré F, Wamhoff BR, Hoofnagle MH, Kremer BE, Wang DZ, Olson EN, Owens GK (2003) Myocardin is a key regulator of CArG-dependent transcription of multiple smooth muscle marker genes. Circ Res 92:856–864PubMedGoogle Scholar
  118. Yoshigi M, Hoffman LM, Jensen CC, Yost HJ, Beckerle MC (2005) Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J Cell Biol 171:209–215PubMedGoogle Scholar
  119. Yue TL, Wang X, Sung CP, Olson B, McKenna PJ, Gu JL, Feuerstein GZ (1994) Interleukin-8. A mitogen and chemoattractant for vascular smooth muscle cells. Circ Res 75:1–7PubMedGoogle Scholar
  120. Zeiher AM, Fisslthaler B, Schray-Utz B, Busse R (1995) Nitric oxide modulates the expression of monocyte chemoattractant protein 1 in cultured human endothelial cells. Circ Res 76:980–986PubMedGoogle Scholar
  121. Zhang D, Childs G (1998b) Human ZFM1 protein is a transcriptional repressor that interacts with the transcription activation domain of stage-specific activator protein. J Biol Chem 273:6868–6877PubMedGoogle Scholar
  122. Zhang D, Paley AJ, Childs G (1998a) The transcriptional repressor ZFM1 interacts with and modulates the ability of EWS to activate transcription. J Biol Chem 273:18086–18091PubMedGoogle Scholar
  123. Zhao S, Suciu A, Ziegler T, Moore JEJR, Burki E, Meister JJ, Brunner HR (1995) Synergistic effects of fluid shear stress and cyclic circumferential stretch on vascular endothelial cell morphology and cytoskeleton. Arterioscler Thromb Vasc Biol 15:1781–1786PubMedGoogle Scholar
  124. Ziegler T, Silacci P, Harrison VJ, Hayoz D (1998) Nitric oxide synthase expression in endothelial cells exposed to mechanical forces. Hypertension 32:351–355PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Marco Cattaruzza
    • 1
  • Andreas H. Wagner
    • 1
  • Markus Hecker
    • 1
    Email author
  1. 1.Division of Cardiovascular Physiology, Institute of Physiology and PathophysiologyUniversity of HeidelbergHeidelbergGermany

Personalised recommendations