Bidirectional interactions between NOX 2‐type NADPH oxidase and the F‐actin cytoskeleton in neuronal growth cones
Open accessAbstract
NADPH oxidases are important for neuronal function but detailed subcellular localization studies have not been performed. Here, we provide the first evidence for the presence of functional NADPH oxidase 2 (NOX2)‐type complex in neuronal growth cones and its bidirectional relationship with the actin cytoskeleton. NADPH oxidase inhibition resulted in reduced F‐actin content, retrograde F‐actin flow, and neurite outgrowth. Stimulation of NADPH oxidase via protein kinase C activation increased levels of hydrogen peroxide in the growth cone periphery. The main enzymatic NADPH oxidase subunit NOX 2/gp91 phox localized to the growth cone plasma membrane and showed little overlap with the regulatory subunit p40 phox. p40 phox itself exhibited colocalization with filopodial actin bundles. Differential subcellular fractionation revealed preferential association of NOX 2/gp91 phox and p40 phox with the membrane and the cytoskeletal fraction, respectively. When neurite growth was evoked with beads coated with the cell adhesion molecule ap CAM, we observed a significant increase in colocalization of p40 phox with NOX 2/gp91 phox at ap CAM adhesion sites. Together, these findings suggest a bidirectional functional relationship between NADPH oxidase activity and the actin cytoskeleton in neuronal growth cones, which contributes to the control of neurite outgrowth.image We have previously shown that reactive oxygen species (ROS) are critical for actin organization and dynamics in neuronal growth cones as well as neurite outgrowth. Here, we report that the cytosolic subunit p40 phox of the NOX2‐type NADPH oxidase complex is partially associated with F‐actin in neuronal growth cones, while ROS produced by this complex regulates F‐actin dynamics and neurite growth. These findings provide evidence for a bidirectional relationship between NADPH oxidase activity and the actin cytoskeleton in neuronal growth cones.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
High blue light can cause ROS to regulate chloroplast light-avoiding movement by regulating the polymerization or depolymerization of actin filaments.
“High blue light can cause ROS (produced by high-energy concentrations to induce NADPH oxidase) to regulate chloroplast light-avoiding movement by regulating the polymerization or depolymerization of actin filaments”
From The action of enhancing weak light capture via phototropic growth and chloroplast movement in plants (2022) · cites this paper as Munnamalai et al., 2014
The Discussion (page not provided) says NADPH oxidase-derived ROS regulate actin organization and dynamics in neuronal growth cones. It does not address high-blue-light exposure or chloroplast light-avoidance movement, so the claim extends the reported mechanism to a different setting. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Ushio‐Fukai, M., Tang, Y., Fukai, T., Dikalov, S., Ma, Y., Fujimoto, M., Quinn, M. T., Pagano, P. J., Johnson, C., & Alexander, R. W. (2002) · Circulation Research · doi:10.1161/01.res.0000046227.65158.f8 · Cited by 463 · see citing works
Self-citationRetractedThe NOX Family of ROS-Generating NADPH Oxidases: Physiology and Pathophysiology
Bedard, K., & Krause, K.-H. (2007) · Physiological Reviews · doi:10.1152/physrev.00044.2005 · Cited by 6,989 · see citing works
Reconciling the chemistry and biology of reactive oxygen species
Winterbourn, C. C. (2008) · Nature Chemical Biology · doi:10.1038/nchembio.85 · Cited by 2,504 · see citing works
Signal transduction by reactive oxygen species
Finkel, T. (2011) · Journal of Cell Biology · doi:10.1083/jcb.201102095 · Cited by 2,322 · see citing works
Forscher, P., & Smith, S. J. (1988) · The Journal of cell biology · doi:10.1083/jcb.107.4.1505 · Cited by 854 · see citing works
Apocynin Is Not an Inhibitor of Vascular NADPH Oxidases but an Antioxidant
Heumüller, S., Wind, S., Barbosa-Sicard, E., Schmidt, H. H. H. W., Busse, R., Schröder, K., & Brandes, R. P. (2008) · Hypertension · doi:10.1161/hypertensionaha.107.100214 · Cited by 735 · see citing works
Sumimoto, H. (2008) · FEBS Journal · doi:10.1111/j.1742-4658.2008.06488.x · Cited by 718 · see citing works
NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation
Brennan, A. M., Suh, S. W., Won, S. J., Narasimhan, P., Kauppinen, T. M., Lee, H., Edling, Y., Chan, P. H., & Swanson, R. A. (2009) · Nature Neuroscience · doi:10.1038/nn.2334 · Cited by 538 · see citing works
Redox-dependent downregulation of Rho by Rac
Nimnual, A. S., Taylor, L. J., & Bar‐Sagi, D. (2003) · Nature Cell Biology · doi:10.1038/ncb938 · Cited by 523 · see citing works
The redox stress hypothesis of aging
Sohal, R. S., & Orr, W. C. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.10.445 · Cited by 473 · see citing works
NOX Enzymes in the Central Nervous System: From Signaling to Disease
Sorce, S., & Krause, K. (2009) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2578 · Cited by 472 · see citing works
Reactive oxygen species as essential mediators of cell adhesion
Chiarugi, P., Pani, G., Giannoni, E., Taddei, L., Colavitti, R., Raugei, G., Symons, M. C. R., Borrello, S., Galeotti, T., & Ramponi, G. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200211118 · Cited by 444 · see citing works
Fontayne, A., Dang, P. M., Gougerot‐Pocidalo, M., & Benna, J. E. (2002) · Biochemistry · doi:10.1021/bi011953s · Cited by 412 · see citing works
Li, J., & Shah, A. M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110073200 · Cited by 395 · see citing works
Localizing NADPH Oxidase–Derived ROS
Ushio‐Fukai, M. (2006) · Science s STKE · doi:10.1126/stke.3492006re8 · Cited by 387 · see citing works
The NOX toolbox: validating the role of NADPH oxidases in physiology and disease
Altenhöfer, S., Kleikers, P. W. M., Radermacher, K. A., Scheurer, P., Rob Hermans, J. J., Schiffers, P., Ho, H., Wingler, K., & Schmidt, H. H. H. W. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1010-9 · Cited by 371 · see citing works
Nauseef, W. M., Volpp, B. D., McCormick, S. J., Leidal, K. G., & Clark, R. A. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)67684-2 · Cited by 341 · see citing works
Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes
Kawahara, T., Quinn, M. T., & Lambeth, J. D. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-109 · Cited by 336 · see citing works
Self-citationNox2 redox signaling maintains essential cell populations in the brain
Dickinson, B. C., Peltier, J., Stone, D., Schaffer, D. V., & Chang, C. J. (2010) · Nature Chemical Biology · doi:10.1038/nchembio.497 · Cited by 273 · see citing works
TENFREYHAUS, H., HUNTGEBURTH, M., WINGLER, K., SCHNITKER, J., BAUMER, A., VANTLER, M., BEKHITE, M., WARTENBERG, M., SAUER, H., & ROSENKRANZ, S. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.01.022 · Cited by 259 · see citing works
Suzukawa, K., Miura, K., Mitsushita, J., Resau, J., Hirose, K., Crystal, R. G., & Kamata, T. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.18.13175 · Cited by 250 · see citing works
Small-Molecule NOX Inhibitors: ROS-Generating NADPH Oxidases as Therapeutic Targets
Jaquet, V., Scapozza, L., Clark, R. A., Krause, K. H., & Lambeth, J. D. (2009) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2585 · Cited by 243 · see citing works
Association of a Ras-related protein with cytochrome b of human neutrophils
Quinn, M. T., Parkos, C. A., Walker, L. E., Orkin, S. H., Dinauer, M. C., & Jesaitis, A. J. (1989) · Nature · doi:10.1038/342198a0 · Cited by 242 · see citing works
Self-citationComparative pharmacology of chemically distinct nadph oxidase inhibitors
Wind, S., Beuerlein, K., Eucker, T., Müller, H., Scheurer, P., Armitage, M., Ho, H., Schmidt, H., & Wingler, K. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00920.x · Cited by 241 · see citing works
Lee, M. Y., Martín, A. S., Mehta, P. K., Dikalova, A., Garrido, A. M., Datla, S. R., Lyons, E., Krause, K., Bánfi, B., Lambeth, J. D., et al. (2009) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.181925 · Cited by 234 · see citing works
NADPH oxidases: novel therapeutic targets for neurodegenerative diseases
Gao, H., Zhou, H., & Hong, J. (2012) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2012.03.008 · Cited by 212 · see citing works
Suter, D. M., Errante, L. D., Belotserkovsky, V., & Forscher, P. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.141.1.227 · Cited by 211 · see citing works
Self-citationSynaptic localization of a functional NADPH oxidase in the mouse hippocampus
Tejada-Simon, M. V., Serrano, F., Villasana, L., Kanterewicz, B. I., Wu, G., Quinn, M. T., & Klann, E. (2005) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.01.007 · Cited by 203 · see citing works
Self-citationReactive Oxygen Species Regulate a Slingshot-Cofilin Activation Pathway
Kim, J., Huang, T. Y., & Bokoch, G. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-02-0131 · Cited by 188 · see citing works
Benna, J. E., Ruedi, J. M., & BABIOR, B. M. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)37436-7 · Cited by 187 · see citing works
Tammariello, T. P., Quinn, M. T., & Estus, S. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-01-j0006.2000 · Cited by 185 · see citing works
Self-citationRedox Changes of Cultured Endothelial Cells and Actin Dynamics
Moldovan, L., Moldovan, N. I., Sohn, R. H., Parikh, S. A., & Goldschmidt‐Clermont, P. J. (2000) · Circulation Research · doi:10.1161/01.res.86.5.549 · Cited by 176 · see citing works
Increased Nox2 expression in human cardiomyocytes after acute myocardial infarction
Krijnen, P. A. J., Meischl, C., Hack, C. E., Meijer, C. J. L. M., Visser, C. A., Roos, D., & Niessen, H. W. M. (2003) · Journal of Clinical Pathology · doi:10.1136/jcp.56.3.194 · Cited by 176 · see citing works
Hydrogen Peroxide Promotes Injury-Induced Peripheral Sensory Axon Regeneration in the Zebrafish Skin
Rieger, S., & Sagasti, A. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1000621 · Cited by 173 · see citing works
Wójciak‐Stothard, B., Tsang, L. Y. F., & Haworth, S. G. (2005) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00361.2004 · Cited by 167 · see citing works
Li, L., Hutchins, B. I., & Kalil, K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0183-09.2009 · Cited by 164 · see citing works
Kishida, K. T., Hoeffer, C. A., Hu, D., Pao, M., Holland, S. M., & Klann, E. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00269-06 · Cited by 159 · see citing works
Cytosolic Phox proteins interact with and regulate the assembly of coronin in neutrophils
Grogan, A., Reeves, E. P., Keep, N. H., Wientjes, F. B., Totty, N. F., Burlingame, A. L., Hsuan, J. J., & Segal, A. W. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.24.3071 · Cited by 150 · see citing works
Nox1 Mediates Basic Fibroblast Growth Factor-Induced Migration of Vascular Smooth Muscle Cells
Schröder, K., Helmcke, I., Pálfi, K., Krause, K., Busse, R., & Brandes, R. P. (2007) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.107.142117 · Cited by 143 · see citing works
Reactive Oxygen Species in Cancer Biology and Anticancer Therapy
Yang, Y., Karakhanova, S., Werner, J., & Bazhin, A. V. (2013) · Current Medicinal Chemistry · doi:10.2174/0929867311320999165 · Cited by 142 · see citing works
Ikeda, S., Yamaoka‐Tojo, M., Hilenski, L. L., Patrushev, N. A., Anwar, G. M., Quinn, M. T., & Ushio‐Fukai, M. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000187472.55437.af · Cited by 129 · see citing works
Self-citationNovel Nox inhibitor of oxLDL-induced reactive oxygen species formation in human endothelial cells
Stielow, C., Catar, R. A., Müller, G. M., Wingler, K., Scheurer, P., Schmidt, H. H. H. W., & Morawietz, H. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.03.114 · Cited by 125 · see citing works
Myosin II Activity Facilitates Microtubule Bundling in the Neuronal Growth Cone Neck
Burnette, D. T., Ji, L., Schaefer, A. W., Medeiros, N. A., Danuser, G. M., & Forscher, P. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.05.016 · Cited by 123 · see citing works
Reactive oxygen species regulate F‐actin dynamics in neuronal growth cones and neurite outgrowth
Munnamalai, V., & Suter, D. M. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05787.x · Cited by 123 · see citing works
Self-citationNADPH oxidase (NOX) isoforms are inhibited by celastrol with a dual mode of action
Jaquet, V., Marcoux, J., Forest, É., Leidal, K. G., McCormick, S. J., Westermaier, Y., Perozzo, R., Plastre, O., Fioraso-Cartier, L., Diebold, B. A., et al. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01439.x · Cited by 120 · see citing works
Microtubule Dynamics Are Necessary for Src Family Kinase-Dependent Growth Cone Steering
Suter, D. M., Schaefer, A. W., & Forscher, P. (2004) · Current Biology · doi:10.1016/j.cub.2004.06.049 · Cited by 114 · see citing works
Self-citationIntegrin-Mediated Cell Adhesion and Spreading Engage Different Sources of Reactive Oxygen Species
Taddei, M. L., Parri, M., Mello, T., Catalano, A., Levine, A. D., Raugei, G., Ramponi, G., & Chiarugi, P. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2006.1392 · Cited by 104 · see citing works
Cabec, V. L., & Maridonneau‐Parini, I. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.5.2067 · Cited by 88 · see citing works
NADPH Oxidase and Neurodegeneration
Hernandes, M. S., & Britto, L. R. G. (2012) · Current Neuropharmacology · doi:10.2174/157015912804499483 · Cited by 83 · see citing works
The NADPH Oxidase Components p47phox and p40phox Bind to Moesin through Their PX Domain
Wientjes, F. B., Reeves, E. P., Šoškić, V., Furthmayr, H., & Segal, A. W. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.5982 · Cited by 82 · see citing works
NADPH Oxidase and Neurodegeneration
Hernandes, M. S., & Britto, L. R. G. (2012) · Current Neuropharmacology · doi:10.2174/157015912804143540 · Cited by 81 · see citing works
NOX1/NADPH oxidase negatively regulates nerve growth factor-induced neurite outgrowth
Ibi, M., Katsuyama, M., Fan, C., Iwata, K., Nishinaka, T., Yokoyama, T., & Yabe‐Nishimura, C. (2006) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2006.01.009 · Cited by 77 · see citing works
Rac regulates PtdInsP3 signaling and the chemotactic compass through a redox-mediated feedback loop
Kuiper, J. W., Sun, C., Magalhães, M. A. O., & Glogauer, M. (2011) · Blood · doi:10.1182/blood-2010-09-310383 · Cited by 70 · see citing works
Usatyuk, P. V., Romer, L. H., He, D., Parinandi, N. L., Kleinberg, M. E., Zhan, S., Jacobson, J. R., Dudek, S. M., Pendyala, S., Garcia, J. G. N., et al. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m700535200 · Cited by 65 · see citing works
Mitochondrial production of oxidants is necessary for physiological calcium oscillations
Camello‐Almaraz, C., Pozo, M. J., Murphy, M. P., & Camello, P. J. (2005) · Journal of Cellular Physiology · doi:10.1002/jcp.20498 · Cited by 56 · see citing works
Role of NADPH oxidase in the apoptotic death of cultured cerebellar granule neurons
Coyoy-Salgado, A., Valencia, A., Guemez‐Gamboa, A., & Morán, J. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.06.027 · Cited by 54 · see citing works
Benna, J. E., Dang, P. M., Andrieu, V., Vergnaud, S., Dewas, C., Cachia, O., Fay, M., Morel, F., Chollet‐Martin, S., Hakim, J., et al. (1999) · Journal of Leukocyte Biology · doi:10.1002/jlb.66.6.1014 · Cited by 54 · see citing works
Barth, B. M., Gustafson, S. J., & Kuhn, T. B. (2011) · Journal of Neuroscience Research · doi:10.1002/jnr.22748 · Cited by 53 · see citing works
Park, K. W., & Jin, B. K. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21571 · Cited by 43 · see citing works
Zhan, Y., He, D., Newburger, P. E., & Zhou, G. W. (2004) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20084 · Cited by 41 · see citing works
Thompson, C. A., Lin, C., & Forscher, P. (1996) · Journal of Cell Science · doi:10.1242/jcs.109.12.2843 · Cited by 41 · see citing works
Chen, J., He, R. L., Minshall, R. D., Dinauer, M. C., & Ye, R. D. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m704416200 · Cited by 32 · see citing works
Cao, X., Demel, S. L., Quinn, M. T., Galligan, J. J., & Kreulen, D. L. (2009) · Autonomic Neuroscience · doi:10.1016/j.autneu.2009.07.010 · Cited by 30 · see citing works
Self-citationZhang, X., & Forscher, P. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-07-0730 · Cited by 29 · see citing works
Neuregulin induces HaCaT keratinocyte migration via Rac1‐mediated NADPH‐oxidase activation
Kim, J., Bak, E., Lee, B., Kim, Y., Park, J., & Choi, I. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.22649 · Cited by 22 · see citing works
Live Cell Imaging of Neuronal Growth Cone Motility and Guidance In Vitro
Suter, D. M. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-207-6_6 · Cited by 21 · see citing works
Self-citationLocalization of NADPH oxidase subunits in neonatal sympathetic neurons
Hilburger, E. W., Conte, E. J., McGee, D. W., & Tammariello, S. P. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.11.066 · Cited by 20 · see citing works
Shao, D., Segal, A. W., & Dekker, L. V. (2010) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2010.07.009 · Cited by 19 · see citing works
Neuronal Cell Cultures from Aplysia for High-Resolution Imaging of Growth Cones
Lee, A. C., Decourt, B., & Suter, D. M. (2008) · Journal of Visualized Experiments · doi:10.3791/662 · Cited by 18 · see citing works
Self-citationGuemez‐Gamboa, A., & Morán, J. (2009) · Journal of Neuroscience Research · doi:10.1002/jnr.22079 · Cited by 15 · see citing works
Cloning and sequencing of rabbit leukocyte NADPH oxidase genes reveals a unique p67phoxhomolog
Gauss, K. A., Mascolo, P. L., Siemsen, D. W., Nelson, L. K., Bunger, P. L., Pagano, P. J., & Quinn, M. T. (2002) · Journal of Leukocyte Biology · doi:10.1189/jlb.71.2.319 · Cited by 13 · see citing works
Self-citation
Flagged first, then by citations
1 of the 72 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Wilson, C., & González-Billault, C. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00381 · Cited by 238 · see citing works
Regulation of neuronal development and function by ROS
Oswald, M. C. W., Garnham, N., Sweeney, S. T., & Landgraf, M. (2018) · FEBS Letters · doi:10.1002/1873-3468.12972 · Cited by 210 · see citing works
Actin Post-translational Modifications: The Cinderella of Cytoskeletal Control
Varland, S., Vandekerckhove, J. S., & Drazic, A. (2019) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2018.11.010 · Cited by 149 · see citing works
From birth to death: A role for reactive oxygen species in neuronal development
Wilson, C., Muñoz-Palma, E., & González-Billault, C. E. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.09.012 · Cited by 129 · see citing works
Reactive oxygen species regulate activity-dependent neuronal plasticity in Drosophila
Oswald, M. C. W., Brooks, P. S., Zwart, M., Mukherjee, A., West, R. J. H., Giachello, C. N., Morarach, K., Baines, R., Sweeney, S. T., & Landgraf, M. (2018) · eLife · doi:10.7554/elife.39393 · Cited by 111 · see citing works
Focusing on mitochondria in the brain: from biology to therapeutics
Song, N., Mei, S., Wang, X.-X., Hu, G., & Lu, M. (2024) · Translational Neurodegeneration · doi:10.1186/s40035-024-00409-w · Cited by 102 · see citing works
Crosstalk between Rac1-mediated actin regulation and ROS production
Acevedo, A., & González-Billault, C. E. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.01.008 · Cited by 96 · see citing works
Hydrogen Peroxide and Redox Regulation of Developments
Rampon, C., Volovitch, M., Joliot, A., & Vriz, S. (2018) · Antioxidants · doi:10.3390/antiox7110159 · Cited by 95 · see citing works
Actin filaments—A target for redox regulation
Wilson, C., Terman, J. R., González-Billault, C. E., & Ahmed, G. (2016) · Cytoskeleton · doi:10.1002/cm.21315 · Cited by 87 · see citing works
Dissecting the role of redox signaling in neuronal development
Bórquez, D. A., Urrutia, P. J., Wilson, C., van Zundert, B., Núñez, M. T., & González-Billault, C. E. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13581 · Cited by 86 · see citing works
Oxidation and reduction of actin: Origin, impact in vitro and functional consequences in vivo
Rouyère, C., Serrano, T., Frémont, S., & Échard, A. (2022) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2022.151249 · Cited by 81 · see citing works
ROS Produced by NOX2 Controls In Vitro Development of Cerebellar Granule Neurons Development
Olguín‐Albuerne, M., & Morán, J. (2015) · ASN NEURO · doi:10.1177/1759091415578712 · Cited by 76 · see citing works
Contribution of NADPH-oxidase to the establishment of hippocampal neuronal polarity in culture
Wilson, C., Núñez, M. T., & González-Billault, C. E. (2015) · Journal of Cell Science · doi:10.1242/jcs.168567 · Cited by 70 · see citing works
The role of NADPH oxidases in neuronal development
Terzi, A., & Suter, D. M. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.04.027 · Cited by 65 · see citing works
Self-citationOxidative hotspots on actin promote skeletal muscle weakness in rheumatoid arthritis
Steinz, M. M., Persson, M., Aresh, B., Olsson, K., Cheng, A. J., Ahlstrand, E., Lilja, M. R., Lundberg, T. R., Rullman, E., Möller, K. Ä., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.126347 · Cited by 60 · see citing works
Wilson, C., Muñoz-Palma, E., Henríquez, D. R., Palmisano, I., Núñez, M. T., Giovanni, S. D., & González-Billault, C. E. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1455-16.2016 · Cited by 58 · see citing works
Redox Signaling Mechanisms in Nervous System Development
Olguín‐Albuerne, M., & Morán, J. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7284 · Cited by 58 · see citing works
The role of Nox-mediated oxidation in the regulation of cytoskeletal dynamics
Valdivia, A., Duran, C., & Martín, A. S. (2015) · Current Pharmaceutical Design · doi:10.2174/1381612821666151029112624 · Cited by 50 · see citing works
Nox, Nox, Are You There? The Role of NADPH Oxidases in the Peripheral Nervous System
Eid, S., Savelieff, M. G., Eid, A. A., & Feldman, E. L. (2021) · Antioxidants and Redox Signaling · doi:10.1089/ars.2021.0135 · Cited by 50 · see citing works
Cofilactin filaments regulate filopodial structure and dynamics in neuronal growth cones
Hylton, R. K., Heebner, J. E., Grillo, M. A., & Swulius, M. T. (2022) · Nature Communications · doi:10.1038/s41467-022-30116-x · Cited by 45 · see citing works
Expression dynamics of NADPH oxidases during early zebrafish development
Weaver, C. J., Leung, Y. F., & Suter, D. M. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23938 · Cited by 39 · see citing works
Self-citationOlthoff, J. T., Lindsay, A., Abo‐Zahrah, R., Baltgalvis, K. A., Patrinostro, X., Belanto, J. J., Yu, D., Perrin, B. J., Garry, D. J., Rodney, G. G., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07639-3 · Cited by 38 · see citing works
Wang, J., Bai, Y., Zhao, X., Ru, J., Kang, N., Tian, T., Tang, L., An, Y., & Li, P. (2018) · Bioscience Reports · doi:10.1042/bsr20180283 · Cited by 34 · see citing works
André‐Lévigne, D., Pignel, R., Boet, S., Jaquet, V., Kalbermatten, D. F., & Madduri, S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25042030 · Cited by 35 · see citing works
Neural plasticity and adult neurogenesis: the deep biology perspective
Colangelo, A. M., Westerhoff, H. V., Cirillo, G., Alberghina, L., & Papa, M. (2018) · Neural Regeneration Research · doi:10.4103/1673-5374.244775 · Cited by 31 · see citing works
Paolo, A. D., Eastman, G., Mesquita-Ribeiro, R., Farías, J., Macklin, A. M., Kislinger, T., Colburn, N. H., Munroe, D. J., Sosa, J. R. S., Dajas‐Bailador, F., et al. (2020) · RNA · doi:10.1261/rna.075424.120 · Cited by 28 · see citing works
Neuronal NADPH oxidase 2 regulates growth cone guidance downstream of slit2/robo2
Terzi, A., Roeder, H., Weaver, C. J., & Suter, D. M. (2020) · Developmental Neurobiology · doi:10.1002/dneu.22791 · Cited by 28 · see citing works
Self-citationDhawan, S., Myers, P., Bailey, D. M., Ostrovsky, A. D., Evers, J. F., & Landgraf, M. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.641802 · Cited by 27 · see citing works
nox2/cybb Deficiency Affects Zebrafish Retinotectal Connectivity
Weaver, C. J., Terzi, A., Roeder, H., Gurol, T., Deng, Q., Leung, Y. F., & Suter, D. M. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1483-16.2018 · Cited by 27 · see citing works
Self-citationValek, L., Häußler, A., Dröse, S., Eaton, P., Schröder, K., & Tegeder, I. (2016) · Redox Biology · doi:10.1016/j.redox.2016.12.004 · Cited by 25 · see citing works
Brenig, K., Grube, L., Schwarzländer, M., Köhrer, K., Stühler, K., & Poschmann, G. (2020) · Journal of Proteome Research · doi:10.1021/acs.jproteome.9b00752 · Cited by 24 · see citing works
Zafar, S., Younas, N., Sheikh, N., Tahir, W., Shafiq, M., Schmitz, M., Ferrer, I., Andréoletti, O., & Zerr, I. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0589-0 · Cited by 24 · see citing works
Wnt5a Signaling Promotes Host Defense against Leishmania donovani Infection
Chakraborty, A., Kurati, S. P., Mahata, S. K., Sundar, S., Roy, S., & Sen, M. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601927 · Cited by 22 · see citing works
Chen, Y., Dangol, S., Wang, J., & Jwa, N. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21176196 · Cited by 22 · see citing works
Chloroplast avoidance movement: a novel paradigm of ROS signalling
Majumdar, A., & Kar, R. K. (2020) · Photosynthesis Research · doi:10.1007/s11120-020-00736-9 · Cited by 21 · see citing works
Oxidative Stress Induces Disruption of the Axon Initial Segment
Clark, K. C., Sword, B. A., & Dupree, J. L. (2017) · ASN NEURO · doi:10.1177/1759091417745426 · Cited by 21 · see citing works
Liggi, S., Drakakis, G., Koutsoukas, A., Cortés‐Ciriano, I., Martínez–Alonso, P., Malliavin, T. E., Velázquez‐Campoy, A., Brewerton, S. C., Bodkin, M. J., Evans, D. A. P., et al. (2014) · Future Medicinal Chemistry · doi:10.4155/fmc.14.137 · Cited by 19 · see citing works
The action of enhancing weak light capture via phototropic growth and chloroplast movement in plants
Xin, G.-Y., Li, L.-P., Wang, P.-T., Li, X.-Y., Han, Y.-J., & Zhao, X. (2022) · Stress Biology · doi:10.1007/s44154-022-00066-x · Cited by 17 · see citing works
“ROS function in actin filament polymerization/stabilization in plant systems in neural growth cones, where ROS reduce the content, kinetics, and contractility of F-actin (Munnamalai et al., 2014; Wilson and González-Billault, 2015).”
BackgroundZheng, L., Boeren, S. A., Liu, C., Bakker, W., Wang, H., Rietjens, I. M. C. M., & Saccenti, E. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.132859 · Cited by 15 · see citing works
Terzi, A., Ngo, K. J., & Mourrain, P. (2024) · Journal of Comparative Physiology B · doi:10.1007/s00360-023-01530-4 · Cited by 12 · see citing works
Bano, N., Khan, S., Ahamad, S., Dar, N. J., Alanazi, H. H., Nazir, A., & Bhat, S. A. (2025) · Ageing Research Reviews · doi:10.1016/j.arr.2025.102735 · Cited by 12 · see citing works
Xiang, Y., Niu, Y., Xie, Y., Chen, S., Zhu, F., Shen, W., & Zeng, L. (2021) · Brain and Behavior · doi:10.1002/brb3.2266 · Cited by 12 · see citing works
Activity-regulated growth of motoneurons at the neuromuscular junction is mediated by NADPH oxidases
Sobrido‐Cameán, D., Oswald, M. C. W., Bailey, D. M., Mukherjee, A., & Landgraf, M. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.1106593 · Cited by 12 · see citing works
Choi, E., Choi, H., Kwon, K. W., Kim, H., Ryu, J.-H., Hong, J. J., & Shin, S. J. (2024) · PLoS Pathogens · doi:10.1371/journal.ppat.1012500 · Cited by 11 · see citing works
A Role for Second Messengers in Axodendritic Neuronal Polarity
Urrutia, P. J., & González-Billault, C. (2023) · The Journal of Neuroscience · doi:10.1523/jneurosci.1065-19.2023 · Cited by 9 · see citing works
ROS Live Cell Imaging During Neuronal Development
Terzi, A., Alam, S. M. S., & Suter, D. M. (2021) · Journal of Visualized Experiments · doi:10.3791/62165 · Cited by 9 · see citing works
Self-citationFunctional interactions between NADPH oxidase 5 and actin
Richter, S. M., Massman, L., Stuehr, D. J., & Sweeny, E. A. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1116833 · Cited by 8 · see citing works
Villegas, L. D., Nørremølle, A., Freude, K., & Vilhardt, F. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.736734 · Cited by 8 · see citing works
ROS produced by NOX promote the neurite growth in a PI3K /Akt independent manner
Mora‐Zenil, J., & Morán, J. (2023) · Journal of Neuroscience Research · doi:10.1002/jnr.25259 · Cited by 6 · see citing works
Neuronal NADPH oxidase is required for neurite regeneration of Aplysia bag cell neurons
Alam, S. M. S., Watanabe, Y., Steeno, B. L., Dutta, S., Szilagyi, H., Wei, A., & Suter, D. M. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15977 · Cited by 6 · see citing works
Self-citationHydrogen Peroxide Gates a Voltage-Dependent Cation Current inAplysiaNeuroendocrine Cells
Chauhan, A. K., & Magoski, N. S. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1460-19.2019 · Cited by 6 · see citing works
Wu, P., Dai, J., Wang, Q., Zhang, G., Tan, S., Li, M., & Ye, H. (2015) · Inflammation Research · doi:10.1007/s00011-015-0866-1 · Cited by 5 · see citing works
Redox-regulated brain development
Berndt, C., Wilms, C., Thauvin, M., & Vriz, S. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-818606-0.00028-6 · Cited by 1 · see citing works
Scapin, G., Gasparotto, M., Peterle, D., Tescari, S., Porcellato, E., Piovesan, A., Righetto, I., Acquasaliente, L., Filippis, V. D., & Filippini, F. (2021) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2021.10.005 · Cited by 4 · see citing works
Muñoz-Palma, E., Acosta-Tapia, N., Villablanca, C., Wilson, C., Hidalgo, C., & González-Billault, C. E. (2026) · Redox Biology · doi:10.1016/j.redox.2026.104027 · Cited by 4 · see citing works
MR study on white matter injury in patients with acute diquat poisoning
Cao, X., Sui, B., Wu, B., Geng, Z., & Song, B. (2024) · NeuroToxicology · doi:10.1016/j.neuro.2024.12.002 · Cited by 3 · see citing works
Chauhan, A. K., Lee, K. H., & Magoski, N. S. (2021) · The Journal of Physiology · doi:10.1113/jp282302 · Cited by 3 · see citing works
NOG-Derived Peptides Can Restore Neuritogenesis on a CRASH Syndrome Cell Model
Gasparotto, M., Suemi, Y., Peterle, D., Grinzato, A., Zen, F. D., Pontarollo, G., Acquasaliente, L., Scapin, G., Bergantino, E., Filippis, V. D., et al. (2022) · Biomedicines · doi:10.3390/biomedicines10010102 · Cited by 3 · see citing works
Gasparotto, M., Dall'Ara, E., Vacca, M., & Filippini, F. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242417326 · Cited by 2 · see citing works
A potential role for NADPH oxidase (NOX1/2) in mutant huntingtin-induced anomalous neurite outgrowth
Villegas, L. D., Mathiesen, A. V., Rasmussen, I., von Broich, M., Qvist, F. L., Skotte, N. H., Bardile, C. F., Budtz–Jørgensen, E., Freude, K., Schmid, B., et al. (2025) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2025.104012 · Cited by 2 · see citing works
Litschel, T., Vavylonis, D., & Weitz, D. A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.19.644260 · Cited by 2 · see citing works
Activation of S1P2 is protective against cisplatin‐induced peripheral neuropathy
Lam, B. W. S., Xiang, P., Peng, B., Soon, L. J. J., Yam, T. Y. A., Lim, C. M. H., Zheng, Y., Nguyen, L. N., Herr, D. R., & Le, M. T. N. (2023) · Cell Proliferation · doi:10.1111/cpr.13549 · Cited by 1 · see citing works
Making sense of subcellular H2O2 in mammals
Waldeck‐Weiermair, M., Covington, T. A., Pandey, A. K., & Michel, T. M. (2026) · Redox Biochemistry and Chemistry · doi:10.1016/j.rbc.2026.100080 · Cited by 1 · see citing works
Keyes, J. D., Mehta, S., & Zhang, J. (2022) · Neuromethods · doi:10.1007/978-1-0716-2525-5_11 · Cited by 1 · see citing works
Activity-regulated growth of motoneurons at the neuromuscular junction is mediated by NADPH oxidasesPreprint
Sobrido‐Cameán, D., Oswald, M. C. W., Bailey, D. M. D., Mukherjee, A., & Landgraf, M. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.10.27.514147 · Cited by 1 · see citing works
Muñoz-Palma, E., Wilson, C., Hidalgo, C., & González-Billault, C. E. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.18.638875 · Cited by 1 · see citing works
ROS regulation of axonal mitochondrial transport
Liao, P. (2016) · Purdue e-Pubs (Purdue University System)
Alam, S. M. S., & Suter, D. M. (2023) · Springer eBooks · doi:10.1007/978-3-031-23752-2_29
Self-citationDual roles of reactive oxygen species in ascidian brain regeneration and degeneration
Nogueira, T. D. S., Mello, A. D. A., Nogueira, N. D. S., & de Barros, C. M. (2025) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2025.111150
3D printing of cytoskeletal networks: Optical generation of ROS promotes actin polymerization
Litschel, T., Vavylonis, D., & Weitz, D. A. (2026) · Newton · doi:10.1016/j.newton.2026.100714
- Authors
- Munnamalai, V., Weaver, C. J., Weisheit, C. E., Venkatraman, P., Agim, Z. S., Quinn, M. T., & Suter, D. M.
- Affiliations
- Purdue University West Lafayette (US)
- Department of Biological Sciences Purdue University West Lafayette Indiana USA
- Montana State University (US)
- Venue
- Journal of Neurochemistry
- Publisher
- Wiley
- Published
- 2014-04-25
- Volume
- 130
- Issue
- 4
- Pages
- 526-540
- ISSN
- 0022-3042 (ISSN-L)
- 1471-4159
- PMC
- PMC4126878
- OpenAlex
- W2056498047
- Cited by
- 70
- References
- 72
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 6 · 2023: 8 · 2022: 6 · 2021: 7 · 2020: 6 · 2019: 4 · 2018: 8 · 2017: 5 · 2016: 5 · 2015: 6 · 2014: 1
- FWCI
- 2.59
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neurochemistry (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (R01 NS049233, P20 GM103500)
- NSF (1146944-IOS)
- Bindley Bioscience Center at Purdue University
- Purdue University
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Keywords
- NADPH oxidase, NOX2, gp91phox, p40phox, F-actin, actin cytoskeleton, growth cones, neurite outgrowth, reactive oxygen species, hydrogen peroxide, protein kinase C, filopodia, subcellular localization, actin dynamics
- MeSH terms
- Actins, Animals, Aplysia, Benzoxazoles, Cytochalasins, Cytoskeleton, Image Processing, Computer-Assisted, Immunohistochemistry, Microscopy, Fluorescence, Neurons, Phosphoproteins, Protein Kinase C, Triazoles, Triterpenes, Reactive Oxygen Species, Neural Cell Adhesion Molecules, NADPH Oxidases, Growth Cones, Immunoprecipitation, Pentacyclic Triterpenes
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
