Endothelial actin depolymerization mediates NADPH oxidase-superoxide production during flow reversal

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 306, Issue 1, 2014, Pages

  Choy, Jenny S ^a   Lu, Xiao ^a   Yang, Junrong ^a   Zhang, Zhen Du ^a   Kassab, Ghassan S ^a,b  

^a Indiana University Purdue University Indianapolis   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Endothelial cells

Indexed keywords

ACTIN; APOCYNIN; CYTOCHALASIN D; GLYCOPROTEIN GP 91; JASPAMIDE; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD FLOW; CAROTID ARTERY; CONTROLLED STUDY; DEPOLYMERIZATION; ENDOTHELIUM CELL; ENZYME ASSAY; FEMALE; IMMUNOPRECIPITATION; IN VIVO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SHEAR STRESS; SWINE; VASCULAR ENDOTHELIUM;

EID: 84891520062     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00402.2013     Document Type: Article

References (47)

1. Babior BM. The NADPH oxidase of endothelial cells. IUBMB Life 50: 267-269, 2000.
2. Brakebusch C, Fassler R. The integrin-actin connection, an eternal love affair. EMBO J 22: 2324-2333, 2003.
3. Bubb MR, Senderowicz AM, Sausville EA, Duncan KL, Korn ED. Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J Biol Chem 269: 14869-14871, 1994.
4. Cardon AD, Bailey MR, Bennett BT. The Animal Welfare Act: from enactment to enforcement. J Am Assoc Lab Anim Sci 51: 301-305, 2012.
5. Casella JF, Flanagan MD, Lin S. Cytochalasin D inhibits actin polymerization and induces depolymerization of actin filaments formed during platelet shape change. Nature 293: 302-305, 1981.
6. Castier Y, Brandes RP, Leseche G, Tedgui A, Lehoux S. p47Phoxdependent NADPH oxidase regulates flow-induced vascular remodeling. Circ Res 97: 533-540, 2005.
7. Chiu JJ, Chien S. Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol Rev 91: 327-387, 2011.
8. Curnutte JT, Erickson RW, Ding J, Badwey JA. Reciprocal interactions between protein kinase C and components of the NADPH oxidase complex may regulate superoxide production by neutrophils stimulated with a phorbol ester. J Biol Chem 269: 10813-10819, 1994.
9. Daiber A, August M, Baldus S, Wendt M, Oelze M, Sydow K, Kleschyov AL, Munzel T. Measurement of NAD(P)H oxidase-derived superoxide with the luminol analogue L-012. Free Radic Biol Med 36: 101-111, 2004.
10. Daiber A, Oelze M, August M, Wendt M, Sydow K, Wieboldt H, Kleschyov AL, Munzel T. Detection of superoxide and peroxynitrite in model systems and mitochondria by the luminol analogue L-012. Free Radic Res 38: 259-269, 2004.
11. Davies PF. Flow-mediated endothelial mechanotransduction. Physiol Rev 75: 519-560, 1995.
12. Gharib M, Beizaie M. Correlation between negative near-wall shear stress in human aorta and various stages of congestive heart failure. Ann Biomed Eng 31: 678-685, 2003.
13. Gimbrone MA Jr, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann N Y Acad Sci 902: 230-239, 2000.
14. Gnasso A, Irace C, Carallo C, De Franceschi MS, Motti C, Mattioli PL, Pujia A. In vivo association between low wall shear stress and plaque in subjects with asymmetrical carotid atherosclerosis. Stroke 28: 993-998, 1997.
15. Godbole AS, Lu X, Guo X, Kassab GS. NADPH oxidase has a directional response to shear stress. Am J Physiol Heart Circ Physiol 296: H152-H158, 2009.
16. Goettsch C, Goettsch W, Brux M, Haschke C, Brunssen C, Muller G, Bornstein SR, Duerrschmidt N, Wagner AH, Morawietz H. Arterial flow reduces oxidative stress via an antioxidant response element and Oct-1 binding site within the NADPH oxidase 4 promoter in endothelial cells. Basic Res Cardiol 106: 551-561, 2011.
17. Gorlach A, Brandes RP, Nguyen K, Amidi M, Dehghani F, Busse R. A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall. Circ Res 87: 26-32, 2000.
18. Heumüller S, Wind S, Barbosa-Sicard E, Schmidt HH, Busse R, Schröder K, Brandes RP. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51: 211-217, 2008.
19. Hong NJ, Silva GB, Garvin JL. PKC-α mediates flow-stimulated superoxide production in thick ascending limbs. Am J Physiol Renal Physiol 298: F885-F891, 2010.
20. Hwang J, Ing MH, Salazar A, Lassègue B, Griendling K, Navab M, Sevanian A, Hsiai TK. Pulsatile versus oscillatory shear stress regulates NADPH oxidase subunit expression: implication for native LDL oxidation. Circ Res 93: 1225-1232, 2003.
21. Imagawa N, Nagasawa K, Nagai K, Kawakami-Honda N, Fujimoto S. Protein kinase C-independent pathway for NADPH oxidase activation in guinea pig peritoneal polymorphonuclear leukocytes by Cytochalasin D. Arch Biochem Biophys 438: 119-124, 2005.
22. Li JM, Shah AM. Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am J Physiol Regul Integr Comp Physiol 287: R1014-R1030, 2004.
23. Li JM, Shah AM. Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells. J Biol Chem 277: 19952-19960, 2002.
24. Li YS, Haga JH, Chien S. Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech 38: 1949-1971, 2005.
25. Liu Y, Li H, Bubolz AH, Zhang DX, Gutterman DD. Endothelial cytoskeletal elements are critical for flow-mediated dilation in human coronary arterioles. Med Biol Eng Comput 46: 469-478, 2008.
26. Lu X, Dang CQ, Guo X, Molloi S, Wassall CD, Kemple MD, Kassab GS. Elevated oxidative stress and endothelial dysfunction in right coronary artery of right ventricular hypertrophy. J Appl Physiol 110: 1674-1681, 2011.
27. Marrero MB, Schieffer B, Paxton WG, Heerdt L, Berk BC, Delafontaine P, Bernstein KE. Direct stimulation of Jak/STAT pathway by the angiotensin II AT1 receptor. Nature 375: 247-250, 1995.
28. Matrougui K, Tanko LB, Loufrani L, Gorny D, Levy BI, Tedgui A, Henrion D. Involvement of Rho-kinase and the actin filament network in angiotensin II-induced contraction and extracellular signal-regulated kinase activity in intact rat mesenteric resistance arteries. Arterioscler Thromb Vasc Biol 21: 1288-1293, 2001.
29. Moldovan L, Irani K, Moldovan NI, Finkel T, Goldschmidt-Clermont PJ. The actin cytoskeleton reorganization induced by Rac1 requires the production of superoxide. Antioxid Redox Signal 1: 29-43, 1999.
30. Morimatsu T, Kawagoshi A, Yoshida K, Tamura M. Actin enhances the activation of human neutrophil NADPH oxidase in a cell-free system. Biochem Biophys Res Commun 230: 206-210, 1997.
31. Morton WM, Ayscough KR, McLaughlin PJ. Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat Cell Biol 2: 376-378, 2000.
32. Nakagawara A, Minakami S. Role of cytoskeletal elements in cytochalasin E-induced superoxide production by human polymorphonuclear leukocytes. Biochim Biophys Acta 584: 143-148, 1979.
33. Nam D, Ni CW, Rezvan A, Suo J, Budzyn K, Llanos A, Harrison D, Giddens D, Jo H. Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am J Physiol Heart Circ Physiol 297: H1535-H1543, 2009.
34. National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the Care and Use of Laboratory Animals (8th ed.). Washington, DC: National Academies Press, 2011.
35. Qian Y, Liu KJ, Chen Y, Flynn DC, Castranova V, Shi X. Cdc42 regulates arsenic-induced NADPH oxidase activation and cell migration through actin filament reorganization. J Biol Chem 280: 3875-3884, 2005.
36. Saitoh T, Dobkins KR. Protein kinase C in human brain and its inhibition by calmodulin. Brain Research 379: 196-199, 1986.
37. 2+ increase in smooth muscle cells from SHR is regulated by actin and microtubule networks. Am J Physiol Heart Circ Physiol 277: H834-H841, 1999.
38. Snow HM, Markos F, O'Regan D, Pollock K. Characteristics of arterial wall shear stress which cause endothelium-dependent vasodilatation in the anaesthetized dog. J Physiol 531: 843-848, 2001.
39. Sohn HY, Gloe T, Keller M, Schoenafinger K, Pohl U. Sensitive superoxide detection in vascular cells by the new chemiluminescence dye L-012. J Vasc Res 36: 456-464, 1999.
40. Stolk J, Hiltermann TJ, Dijkman JH, Verhoeven AJ. Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted catechol. Am J Respir Cell Mol Biol 11: 95-102, 1994.
41. Tamura M, Itoh K, Akita H, Takano K, Oku S. Identification of an actin-binding site in p47phox an organizer protein of NADPH oxidase. FEBS Lett 580: 261-267, 2006.
42. Tamura M, Kai T, Tsunawaki S, Lambeth JD, Kameda K. Direct interaction of actin with p47(phox) of neutrophil NADPH oxidase. Biochem Biophys Res Commun 276: 1186-1190, 2000.
43. Teng L, Fan LM, Meijles D, Li JM. Divergent effects of p47(phox) phosphorylation at S303-4 or S379 on tumor necrosis factor-α signaling via TRAF4 and MAPK in endothelial cells. Arterioscler Thromb Vasc Biol 32: 1488-1496, 2012.
44. Touyz RM. Apocynin, NADPH oxidase, and vascular cells: a complex matter. Hypertension 51: 172-174, 2008.
45. Usatyuk PV, Romer LH, He D, Parinandi NL, Kleinberg ME, Zhan S, Jacobson JR, Dudek SM, Pendyala S, Garcia JG, Natarajan V. Regulation of hyperoxia-induced NADPH oxidase activation in human lung endothelial cells by the actin cytoskeleton and cortactin. J Biol Chem 282: 23284-23295, 2007.
46. Waschke J, Curry FE, Adamson RH, Drenckhahn D. Regulation of actin dynamics is critical for endothelial barrier functions. Am J Physiol Heart Circ Physiol 288: H1296-H1305, 2005.
47. Wu RF, Gu Y, Xu YC, Nwariaku FE, Terada LS. Vascular endothelial growth factor causes translocation of p47phox to membrane ruffles through WAVE1. J Biol Chem 278: 36830-36840, 2003.