全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2012 

Reactive Oxygen Species Regulate Protrusion Efficiency by Controlling Actin Dynamics

DOI: 10.1371/journal.pone.0041342

Full-Text   Cite this paper   Add to My Lib

Abstract:

Productive protrusions allowing motile cells to sense and migrate toward a chemotactic gradient of reactive oxygen species (ROS) require a tight control of the actin cytoskeleton. However, the mechanisms of how ROS affect cell protrusion and actin dynamics are not well elucidated yet. We show here that ROS induce the formation of a persistent protrusion. In migrating epithelial cells, protrusion of the leading edge requires the precise regulation of the lamellipodium and lamella F-actin networks. Using fluorescent speckle microscopy, we showed that, upon ROS stimulation, the F-actin retrograde flow is enhanced in the lamellipodium. This event coincides with an increase of cofilin activity, free barbed ends formation, Arp2/3 recruitment, and ERK activity at the cell edge. In addition, we observed an acceleration of the F-actin flow in the lamella of ROS-stimulated cells, which correlates with an enhancement of the cell contractility. Thus, this study demonstrates that ROS modulate both the lamellipodium and the lamella networks to control protrusion efficiency.

References

[1]  Bokoch GM, Knaus UG (2003) NADPH oxidases: not just for leukocytes anymore! Trends Biochem Sci. 28: 502–508.
[2]  Faggioni R, Gatti S, Demitri MT, Delgado R, Echtenacher B, et al. (1994) Role of xanthine oxidase and reactive oxygen intermediates in LPS- and TNF-induced pulmonary edema. J Lab Clin Med 123: 394–399.
[3]  Gottlieb RA (2003) Cytochrome P450: major player in reperfusion injury. Arch Biochem Biophys 420: 262–267.
[4]  Jaeschke H, Mitchell JR (1989) Mitochondria and xanthine oxidase both generate reactive oxygen species in isolated perfused rat liver after hypoxic injury. Biochem Biophys Res Commun 160: 140–147.
[5]  Thannickal VJ, Fanburg BL (2000) Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279: L1005–1028.
[6]  Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245–313.
[7]  Sadok A, Bourgarel-Rey V, Gattacceca F, Penel C, Lehmann M, et al. (2008) Nox1-dependent superoxide production controls colon adenocarcinoma cell migration. Biochim Biophys Acta 1783: 23–33.
[8]  Sadok A, Pierres A, Dahan L, Prevot C, Lehmann M, et al. (2009) NADPH oxidase 1 controls the persistence of directed cell migration by a Rho-dependent switch of alpha2/alpha3 integrins. Mol Cell Biol 29: 3915–3928.
[9]  Sundaresan M, Yu ZX, Ferrans VJ, Irani K, Finkel T (1995) Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270: 296–299.
[10]  Ushio-Fukai M, Tang Y, Fukai T, Dikalov SI, Ma Y, et al. (2002) Novel role of gp91(phox)-containing NAD(P)H oxidase in vascular endothelial growth factor-induced signaling and angiogenesis. Circ Res 91: 1160–1167.
[11]  Moldovan L, Moldovan NI, Sohn RH, Parikh SA, Goldschmidt-Clermont PJ (2000) Redox changes of cultured endothelial cells and actin dynamics. Circ Res 86: 549–557.
[12]  Niethammer P, Grabher C, Look AT, Mitchison TJ (2009) A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459: 996–999.
[13]  Higgs HN, Pollard TD (2001) Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu Rev Biochem 70: 649–676.
[14]  Kovar DR (2006) Molecular details of formin-mediated actin assembly. Curr Opin Cell Biol 18: 11–17.
[15]  Stossel TP, Condeelis J, Cooley L, Hartwig JH, Noegel A, et al. (2001) Filamins as integrators of cell mechanics and signalling. Nat Rev Mol Cell Biol 2: 138–145.
[16]  DesMarais V, Ghosh M, Eddy R, Condeelis J (2005) Cofilin takes the lead. J Cell Sci 118: 19–26.
[17]  Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G (2004) Two distinct actin networks drive the protrusion of migrating cells. Science 305: 1782–1786.
[18]  Ponti A, Matov A, Adams M, Gupton S, Waterman-Storer CM, et al. (2005) Periodic patterns of actin turnover in lamellipodia and lamellae of migrating epithelial cells analyzed by quantitative Fluorescent Speckle Microscopy. Biophys J 89: 3456–3469.
[19]  Svitkina TM, Borisy GG (1999) Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 145: 1009–1026.
[20]  Blanchoin L, Pollard TD, Hitchcock-DeGregori SE (2001) Inhibition of the Arp2/3 complex-nucleated actin polymerization and branch formation by tropomyosin. Curr Biol 11: 1300–1304.
[21]  Gupton SL, Anderson KL, Kole TP, Fischer RS, Ponti A, et al. (2005) Cell migration without a lamellipodium: translation of actin dynamics into cell movement mediated by tropomyosin. J Cell Biol 168: 619–631.
[22]  DalleDonne I, Milzani A, Colombo R (1995) H2O2-treated actin: assembly and polymer interactions with cross-linking proteins. Biophys J 69: 2710–2719.
[23]  Ikeda S, Yamaoka-Tojo M, Hilenski L, Patrushev NA, Anwar GM, et al. (2005) IQGAP1 regulates reactive oxygen species-dependent endothelial cell migration through interacting with Nox2. Arterioscler Thromb Vasc Biol 25: 2295–2300.
[24]  Nimnual AS, Taylor LJ, Bar-Sagi D (2003) Redox-dependent downregulation of Rho by Rac. Nat Cell Biol 5: 236–241.
[25]  Kim JS, Huang TY, Bokoch GM (2009) Reactive oxygen species regulate a slingshot-cofilin activation pathway. Mol Biol Cell 20: 2650–2660.
[26]  Delorme V, Machacek M, DerMardirossian C, Anderson KL, Wittmann T, et al. (2007) Cofilin activity downstream of Pak1 regulates cell protrusion efficiency by organizing lamellipodium and lamella actin networks. Dev Cell 13: 646–662.
[27]  Delorme-Walker VD, Peterson JR, Chernoff J, Waterman CM, Danuser G, et al. (2011) Pak1 regulates focal adhesion strength, myosin IIA distribution, and actin dynamics to optimize cell migration. J Cell Biol 193: 1289–1303.
[28]  Gupton SL, Waterman-Storer CM (2006) Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell 125: 1361–1374.
[29]  Gianni D, Diaz B, Taulet N, Fowler B, Courtneidge SA, et al. (2009) Novel p47(phox)-related organizers regulate localized NADPH oxidase 1 (Nox1) activity. Sci Signal 2: ra54.
[30]  Miller EW, Dickinson BC, Chang CJ (2010) Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc Natl Acad Sci U S A 107: 15681–15686.
[31]  Giandomenico AR, Cerniglia GE, Biaglow JE, Stevens CW, Koch CJ (1997) The importance of sodium pyruvate in assessing damage produced by hydrogen peroxide. Free Radic Biol Med 23: 426–434.
[32]  Danuser G, Waterman-Storer CM (2006) Quantitative fluorescent speckle microscopy of cytoskeleton dynamics. Annu Rev Biophys Biomol Struct 35: 361–387.
[33]  Bernstein BW, Bamburg JR (2010) ADF/cofilin: a functional node in cell biology. Trends Cell Biol 20: 187–195.
[34]  Chan C, Beltzner CC, Pollard TD (2009) Cofilin dissociates Arp2/3 complex and branches from actin filaments. Curr Biol 19: 537–545.
[35]  DesMarais V, Macaluso F, Condeelis J, Bailly M (2004) Synergistic interaction between the Arp2/3 complex and cofilin drives stimulated lamellipod extension. J Cell Sci 117: 3499–3510.
[36]  Ichetovkin I, Grant W, Condeelis J (2002) Cofilin produces newly polymerized actin filaments that are preferred for dendritic nucleation by the Arp2/3 complex. Curr Biol 12: 79–84.
[37]  Insall RH, Machesky LM (2009) Actin dynamics at the leading edge: from simple machinery to complex networks. Dev Cell 17: 310–322.
[38]  Mendoza MC, Er EE, Zhang W, Ballif BA, Elliott HL, et al. (2011) ERK-MAPK drives lamellipodia protrusion by activating the WAVE2 regulatory complex. Mol Cell 41: 661–671.
[39]  Wang CL, Coluccio LM (2010) New insights into the regulation of the actin cytoskeleton by tropomyosin. Int Rev Cell Mol Biol 281: 91–128.
[40]  Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ, et al. (2003) Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 299: 1743–1747.
[41]  Adelstein RS, Conti MA (1975) Phosphorylation of platelet myosin increases actin-activated myosin ATPase activity. Nature 256: 597–598.
[42]  Alexandrova AY, Kopnin PB, Vasiliev JM, Kopnin BP (2006) ROS up-regulation mediates Ras-induced changes of cell morphology and motility. Exp Cell Res 312: 2066–2073.
[43]  Fiaschi T, Cozzi G, Raugei G, Formigli L, Ramponi G, et al. (2006) Redox regulation of beta-actin during integrin-mediated cell adhesion. J Biol Chem 281: 22983–22991.
[44]  Huot J, Houle F, Marceau F, Landry J (1997) Oxidative stress-induced actin reorganization mediated by the p38 mitogen-activated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ Res 80: 383–392.
[45]  Bamburg JR (1999) Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu Rev Cell Dev Biol 15: 185–230.
[46]  Bamburg JR, McGough A, Ono S (1999) Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends Cell Biol 9: 364–370.
[47]  Carlier MF, Laurent V, Santolini J, Melki R, Didry D, et al. (1997) Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J Cell Biol 136: 1307–1322.
[48]  Lappalainen P, Drubin DG (1997) Cofilin promotes rapid actin filament turnover in vivo. Nature 388: 78–82.
[49]  Moon A, Drubin DG (1995) The ADF/cofilin proteins: stimulus-responsive modulators of actin dynamics. Mol Biol Cell 6: 1423–1431.
[50]  Dawe HR, Minamide LS, Bamburg JR, Cramer LP (2003) ADF/cofilin controls cell polarity during fibroblast migration. Curr Biol 13: 252–257.
[51]  Sidani M, Wessels D, Mouneimne G, Ghosh M, Goswami S, et al. (2007) Cofilin determines the migration behavior and turning frequency of metastatic cancer cells. J Cell Biol 179: 777–791.
[52]  Lee CK, Park HJ, So HH, Kim HJ, Lee KS, et al. (2006) Proteomic profiling and identification of cofilin responding to oxidative stress in vascular smooth muscle. Proteomics 6: 6455–6475.
[53]  San Martin A, Lee MY, Williams HC, Mizuno K, Lassegue B, et al. (2008) Dual regulation of cofilin activity by LIM kinase and Slingshot-1L phosphatase controls platelet-derived growth factor-induced migration of human aortic smooth muscle cells. Circ Res 102: 432–438.
[54]  Klemke M, Wabnitz GH, Funke F, Funk B, Kirchgessner H, et al. (2008) Oxidation of cofilin mediates T cell hyporesponsiveness under oxidative stress conditions. Immunity 29: 404–413.
[55]  Munnamalai V, Suter DM (2009) Reactive oxygen species regulate F-actin dynamics in neuronal growth cones and neurite outgrowth. J Neurochem 108: 644–661.
[56]  Andrianantoandro E, Pollard TD (2006) Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol Cell 24: 13–23.
[57]  Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, et al. (2004) Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304: 743–746.
[58]  Aikawa R, Komuro I, Yamazaki T, Zou Y, Kudoh S, et al. (1997) Oxidative stress activates extracellular signal-regulated kinases through Src and Ras in cultured cardiac myocytes of neonatal rats. J Clin Invest 100: 1813–1821.
[59]  Blanc A, Pandey NR, Srivastava AK (2004) Distinct roles of Ca2+, calmodulin, and protein kinase C in H2O2-induced activation of ERK1/2, p38 MAPK, and protein kinase B signaling in vascular smooth muscle cells. Antioxid Redox Signal 6: 353–366.
[60]  Mehdi MZ, Pandey NR, Pandey SK, Srivastava AK (2005) H2O2-induced phosphorylation of ERK1/2 and PKB requires tyrosine kinase activity of insulin receptor and c-Src. Antioxid Redox Signal 7: 1014–1020.
[61]  Yoo SK, Starnes TW, Deng Q, Huttenlocher A (2011) Lyn is a redox sensor that mediates leukocyte wound attraction in vivo. Nature 480: 109–112.
[62]  Huang C, Jacobson K, Schaller MD (2004) MAP kinases and cell migration. J Cell Sci 117: 4619–4628.
[63]  Pichon S, Bryckaert M, Berrou E (2004) Control of actin dynamics by p38 MAP kinase - Hsp27 distribution in the lamellipodium of smooth muscle cells. J Cell Sci 117: 2569–2577.
[64]  Jernigan NL, Walker BR, Resta TC (2008) Reactive oxygen species mediate RhoA/Rho kinase-induced Ca2+ sensitization in pulmonary vascular smooth muscle following chronic hypoxia. Am J Physiol Lung Cell Mol Physiol 295: L515–529.
[65]  Jin L, Ying Z, Webb RC (2004) Activation of Rho/Rho kinase signaling pathway by reactive oxygen species in rat aorta. Am J Physiol Heart Circ Physiol 287: H1495–1500.
[66]  Chew TL, Masaracchia RA, Goeckeler ZM, Wysolmerski RB (1998) Phosphorylation of non-muscle myosin II regulatory light chain by p21-activated kinase (gamma-PAK). J Muscle Res Cell Motil 19: 839–854.
[67]  Weber DS, Taniyama Y, Rocic P, Seshiah PN, Dechert MA, et al. (2004) Phosphoinositide-dependent kinase 1 and p21-activated protein kinase mediate reactive oxygen species-dependent regulation of platelet-derived growth factor-induced smooth muscle cell migration. Circ Res 94: 1219–1226.
[68]  Waterman-Storer C (2002) Fluorescent speckle microscopy (FSM) of microtubules and actin in living cells. Curr Protoc Cell Biol Chapter 4: Unit 4 10.
[69]  Symons MH, Mitchison TJ (1991) Control of actin polymerization in live and permeabilized fibroblasts. J Cell Biol 114: 503–513.
[70]  Salmon WC, Adams MC, Waterman-Storer CM (2002) Dual-wavelength fluorescent speckle microscopy reveals coupling of microtubule and actin movements in migrating cells. J Cell Biol 158: 31–37.
[71]  Ponti A, Vallotton P, Salmon WC, Waterman-Storer CM, Danuser G (2003) Computational analysis of F-actin turnover in cortical actin meshworks using fluorescent speckle microscopy. Biophys J 84: 3336–3352.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133