Bidirectional interactions between NOX2-type NADPH oxidase and the F-actin cytoskeleton in neuronal growth cones

Journal of Neurochemistry

Volumn 130, Issue 4, 2014, Pages 526-540

  Munnamalai, Vidhya ^a   Weaver, Cory J ^a   Weisheit, Corinne E ^a   Venkatraman, Prahatha ^a   Agim, Zeynep Sena ^a   Quinn, Mark T ^b   Suter, Daniel M ^a,c  

^a PURDUE UNIVERSITY   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

F actin; growth cone; NADPH oxidase; NOX2; ROS

Indexed keywords

F ACTIN; HYDROGEN PEROXIDE; PROTEIN KINASE C; PROTEIN P40; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2;

ANIMAL CELL; APLYSIA; ARTICLE; CELL ADHESION; CELL FRACTIONATION; CELL MEMBRANE; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GROWTH CONE; HUMAN; NERVE CELL GROWTH; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

F-ACTIN; GROWTH CONE; NADPH OXIDASE; NOX2; P40PHOX; ROS;

ACTINS; ANIMALS; APLYSIA; BENZOXAZOLES; CYTOCHALASINS; CYTOSKELETON; GROWTH CONES; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MICROSCOPY, FLUORESCENCE; NADPH OXIDASE; NEURAL CELL ADHESION MOLECULES; NEURONS; PHOSPHOPROTEINS; PROTEIN KINASE C; REACTIVE OXYGEN SPECIES; TRIAZOLES; TRITERPENES;

EID: 84905725126     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12734     Document Type: Article

References (70)

1. Altenhofer S., Kleikers P. W., Radermacher K. A., Scheurer P., Rob Hermans J. J., Schiffers P., Ho H., Wingler K., and, Schmidt H. H., (2012) The NOX toolbox: validating the role of NADPH oxidases in physiology and disease. Cell. Mol. Life Sci. 69, 2327-2343.
2. Barth B. M., Gustafson S. J., and, Kuhn T. B., (2012) Neutral sphingomyelinase activation precedes NADPH oxidase-dependent damage in neurons exposed to the proinflammatory cytokine tumor necrosis factor-alpha. J. Neurosci. Res. 90, 229-242.
3. Bedard K., and, Krause K. H., (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245-313.
4. Brennan A. M., Suh S. W., Won S. J., Narasimhan P., Kauppinen T. M., Lee H., Edling Y., Chan P. H., and, Swanson R. A., (2009) NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat. Neurosci. 12, 857-863.
5. Burnette D. T., Ji L., Schaefer A. W., Medeiros N. A., Danuser G., and, Forscher P., (2008) Myosin II activity facilitates microtubule bundling in the neuronal growth cone neck. Dev. Cell 15, 163-169.
6. Camello-Almaraz M. C., Pozo M. J., Murphy M. P., and, Camello P. J., (2006) Mitochondrial production of oxidants is necessary for physiological calcium oscillations. J. Cell. Physiol. 206, 487-494.
7. Cao X., Demel S. L., Quinn M. T., Galligan J. J., and, Kreulen D., (2009) Localization of NADPH oxidase in sympathetic and sensory ganglion neurons and perivascular nerve fibers. Auton. Neurosci. 151, 90-97.
8. Chen J., He R., Minshall R. D., Dinauer M. C., and, Ye R. D., (2007) Characterization of a mutation in the Phox homology domain of the NADPH oxidase component p40phox identifies a mechanism for negative regulation of superoxide production. J. Biol. Chem. 282, 30273-30284.
9. Chiarugi P., Pani G., Giannoni E., et al,. (2003) Reactive oxygen species as essential mediators of cell adhesion: the oxidative inhibition of a FAK tyrosine phosphatase is required for cell adhesion. J. Cell Biol. 161, 933-944.
10. Coyoy A., Valencia A., Guemez-Gamboa A., and, Moran J., (2008) Role of NADPH oxidase in the apoptotic death of cultured cerebellar granule neurons. Free Radic. Biol. Med. 45, 1056-1064.
11. Dickinson B. C., Peltier J., Stone D., Schaffer D. V., and, Chang C. J., (2011) Nox2 redox signaling maintains essential cell populations in the brain. Nat. Chem. Biol. 7, 106-112.
12. El Benna J., Ruedi J. M., and, Babior B. M., (1994) Cytosolic guanine nucleotide-binding protein Rac2 operates in vivo as a component of the neutrophil respiratory burst oxidase. Transfer of Rac2 and the cytosolic oxidase components p47phox and p67phox to the submembranous actin cytoskeleton during oxidase activation. J. Biol. Chem. 269, 6729-6734.
13. El Benna J., Dang P. M., Andrieu V., et al,. (1999) P40phox associates with the neutrophil Triton X-100-insoluble cytoskeletal fraction and PMA-activated membrane skeleton: a comparative study with P67phox and P47phox. J. Leukoc. Biol. 66, 1014-1020.
14. Finkel T., (2011) Signal transduction by reactive oxygen species. J. Cell Biol. 194, 7-15.
15. Fontayne A., Dang P. M., Gougerot-Pocidalo M. A., and, El-Benna J., (2002) Phosphorylation of p47phox sites by PKC alpha, beta II, delta, and zeta: effect on binding to p22phox and on NADPH oxidase activation. Biochemistry 41, 7743-7750.
16. Forscher P., and, Smith S. J., (1988) Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107, 1505-1516.
17. ten Freyhaus H., Huntgeburth M., Wingler K., et al,. (2006) Novel Nox inhibitor VAS2870 attenuates PDGF-dependent smooth muscle cell chemotaxis, but not proliferation. Cardiovasc. Res. 71, 331-341.
18. Gao H. M., Zhou H., and, Hong J. S., (2012) NADPH oxidases: novel therapeutic targets for neurodegenerative diseases. Trends Pharmacol. Sci. 33, 295-303.
19. Gauss K. A., Mascolo P. L., Siemsen D. W., Nelson L. K., Bunger P. L., Pagano P. J., and, Quinn M. T., (2002) Cloning and sequencing of rabbit leukocyte NADPH oxidase genes reveals a unique p67(phox) homolog. J. Leukoc. Biol. 71, 319-328.
20. Grogan A., Reeves E., Keep N., Wientjes F., Totty N. F., Burlingame A. L., Hsuan J. J., and, Segal A. W., (1997) Cytosolic phox proteins interact with and regulate the assembly of coronin in neutrophils. J. Cell Sci. 110 (Pt 24), 3071-3081.
21. Guemez-Gamboa A., and, Moran J., (2009) NOX2 mediates apoptotic death induced by staurosporine but not by potassium deprivation in cerebellar granule neurons. J. Neurosci. Res. 87, 2531-2540.
22. Hernandes M. S., and, Britto L. R., (2012) NADPH oxidase and neurodegeneration. Curr. Neuropharmacol. 10, 321-327.
23. Heumuller S., Wind S., Barbosa-Sicard E., Schmidt H. H., Busse R., Schroder K., and, Brandes R. P., (2008) Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51, 211-217.
24. Hilburger E. W., Conte E. J., McGee D. W., and, Tammariello S. P., (2005) Localization of NADPH oxidase subunits in neonatal sympathetic neurons. Neurosci. Lett. 377, 16-19.
25. Ibi M., Katsuyama M., Fan C., Iwata K., Nishinaka T., Yokoyama T., and, Yabe-Nishimura C., (2006) NOX1/NADPH oxidase negatively regulates nerve growth factor-induced neurite outgrowth. Free Radic. Biol. Med. 40, 1785-1795.
26. Ikeda S., Yamaoka-Tojo M., Hilenski L., Patrushev N. A., Anwar G. M., Quinn M. T., and, Ushio-Fukai M., (2005) IQGAP1 regulates reactive oxygen species-dependent endothelial cell migration through interacting with Nox2. Arterioscler. Thromb. Vasc. Biol. 25, 2295-2300.
27. Jaquet V., Scapozza L., Clark R. A., Krause K. H., and, Lambeth J. D., (2009) Small-molecule NOX inhibitors: ROS-generating NADPH oxidases as therapeutic targets. Antioxid. Redox Signal. 11, 2535-2552.
28. Jaquet V., Marcoux J., Forest E., et al,. (2011) NADPH oxidase (NOX) isoforms are inhibited by celastrol with a dual mode of action. Br. J. Pharmacol. 164, 507-520.
29. Kawahara B. T., Quinn M. T., and, Lambeth J. D., (2007) Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes. BMC Evol. Biol. 7, 109.
30. Kim J. S., Huang T. Y., and, Bokoch G. M., (2009) Reactive oxygen species regulate a slingshot-cofilin activation pathway. Mol. Biol. Cell 20, 2650-2660.
31. Kim J. S., Bak E. J., Lee B. C., Kim Y. S., Park J. B., and, Choi I. G., (2011) Neuregulin induces HaCaT keratinocyte migration via Rac1-mediated NADPH-oxidase activation. J. Cell. Physiol. 226, 3014-3021.
32. Kishida K. T., Hoeffer C. A., Hu D., Pao M., Holland S. M., and, Klann E., (2006) Synaptic plasticity deficits and mild memory impairments in mouse models of chronic granulomatous disease. Mol. Cell. Biol. 26, 5908-5920.
33. Krijnen P. A., Meischl C., Hack C. E., Meijer C. J., Visser C. A., Roos D., and, Niessen H. W., (2003) Increased Nox2 expression in human cardiomyocytes after acute myocardial infarction. J. Clin. Pathol. 56, 194-199.
34. Kuiper J. W., Sun C., Magalhaes M. A., and, Glogauer M., (2011) Rac regulates PtdInsP(3) signaling and the chemotactic compass through a redox-mediated feedback loop. Blood 118, 6164-6171.
35. Le Cabec V., and, Maridonneau-Parini I., (1995) Complete and reversible inhibition of NADPH oxidase in human neutrophils by phenylarsine oxide at a step distal to membrane translocation of the enzyme subunits. J. Biol. Chem. 270, 2067-2073.
36. Lee A. C., Decourt B., and, Suter D., (2008) Neuronal cell cultures from aplysia for high-resolution imaging of growth cones. J. Vis. Exp. 12, 662.
37. Lee M. Y., San Martin A., Mehta P. K., et al,. (2009) Mechanisms of vascular smooth muscle NADPH oxidase 1 (Nox1) contribution to injury-induced neointimal formation. Arterioscler. Thromb. Vasc. Biol. 29, 480-487.
38. Li J. M., and, Shah A. M., (2002) Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells. J. Biol. Chem. 277, 19952-19960.
39. Li L., Hutchins B. I., and, Kalil K., (2009) Wnt5a induces simultaneous cortical axon outgrowth and repulsive axon guidance through distinct signaling mechanisms. J. Neurosci. 29, 5873-5883.
40. Moldovan L., Moldovan N. I., Sohn R. H., Parikh S. A., and, Goldschmidt-Clermont P. J., (2000) Redox changes of cultured endothelial cells and actin dynamics. Circ. Res. 86, 549-557.
41. Munnamalai V., and, Suter D. M., (2009) Reactive oxygen species regulate F-actin dynamics in neuronal growth cones and neurite outgrowth. J. Neurochem. 108, 644-661.
42. Nauseef W. M., Volpp B. D., McCormick S., Leidal K. G., and, Clark R. A., (1991) Assembly of the neutrophil respiratory burst oxidase. Protein kinase C promotes cytoskeletal and membrane association of cytosolic oxidase components. J. Biol. Chem. 266, 5911-5917.
43. Nimnual A. S., Taylor L. J., and, Bar-Sagi D., (2003) Redox-dependent downregulation of Rho by Rac. Nat. Cell Biol. 5, 236-241.
44. Park K. W., and, Jin B. K., (2008) Thrombin-induced oxidative stress contributes to the death of hippocampal neurons: role of neuronal NADPH oxidase. J. Neurosci. Res. 86, 1053-1063.
45. Quinn M. T., Parkos C. A., Walker L., Orkin S. H., Dinauer M. C., and, Jesaitis A. J., (1989) Association of a Ras-related protein with cytochrome b of human neutrophils. Nature 342, 198-200.
46. Rieger S., and, Sagasti A., (2011) Hydrogen peroxide promotes injury-induced peripheral sensory axon regeneration in the zebrafish skin. PLoS Biol. 9, e1000621.
47. Schroder K., Helmcke I., Palfi K., Krause K. H., Busse R., and, Brandes R. P., (2007) Nox1 mediates basic fibroblast growth factor-induced migration of vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 27, 1736-1743.
48. Shao D., Segal A. W., and, Dekker L. V., (2010) Subcellular localisation of the p40phox component of NADPH oxidase involves direct interactions between the Phox homology domain and F-actin. Int. J. Biochem. Cell Biol. 42, 1736-1743.
49. Sohal R. S., and, Orr W. C., (2012) The redox stress hypothesis of aging. Free Radic. Biol. Med. 52, 539-555.
50. Sorce S., and, Krause K. H., (2009) NOX enzymes in the central nervous system: from signaling to disease. Antioxid. Redox Signal. 11, 2481-2504.
51. Stielow C., Catar R. A., Muller G., Wingler K., Scheurer P., Schmidt H. H., and, Morawietz H., (2006) Novel Nox inhibitor of oxLDL-induced reactive oxygen species formation in human endothelial cells. Biochem. Biophys. Res. Commun. 344, 200-205.
52. Sumimoto H., (2008) Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J. 275, 3249-3277.
53. Suter D. M., (2011) Live cell imaging of neuronal growth cone motility and guidance in vitro. Methods Mol. Biol. 769, 65-86.
54. Suter D. M., Errante L. D., Belotserkovsky V., and, Forscher P., (1998) The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J. Cell Biol. 141, 227-240.
55. Suter D. M., Schaefer A. W., and, Forscher P., (2004) Microtubule dynamics are necessary for SRC family kinase-dependent growth cone steering. Curr. Biol. 14, 1194-1199.
56. Suzukawa K., Miura K., Mitsushita J., Resau J., Hirose K., Crystal R., and, Kamata T., (2000) Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species. J. Biol. Chem. 275, 13175-13178.
57. Taddei M. L., Parri M., Mello T., Catalano A., Levine A. D., Raugei G., Ramponi G., and, Chiarugi P., (2007) Integrin-mediated cell adhesion and spreading engage different sources of reactive oxygen species. Antioxid. Redox Signal. 9, 469-481.
58. Tammariello S. P., Quinn M. T., and, Estus S., (2000) NADPH oxidase contributes directly to oxidative stress and apoptosis in nerve growth factor-deprived sympathetic neurons. J. Neurosci., 20, RC53.
59. Tejada-Simon M. V., Serrano F., Villasana L. E., Kanterewicz B. I., Wu G. Y., Quinn M. T., and, Klann E., (2005) Synaptic localization of a functional NADPH oxidase in the mouse hippocampus. Mol. Cell. Neurosci. 29, 97-106.
60. Thompson C., Lin C. H., and, Forscher P., (1996) An Aplysia cell adhesion molecule associated with site-directed actin filament assembly in neuronal growth cones. J. Cell Sci. 109 (Pt 12), 2843-2854.
61. Usatyuk P. V., Romer L. H., He D., et al,. (2007) Regulation of hyperoxia-induced NADPH oxidase activation in human lung endothelial cells by the actin cytoskeleton and cortactin. J. Biol. Chem. 282, 23284-23295.
62. Ushio-Fukai M., (2006) Localizing NADPH oxidase-derived ROS. Sci. STKE, 2006, re8.
63. Ushio-Fukai M., Tang Y., Fukai T., 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.
64. Wientjes F. B., Reeves E. P., Soskic V., Furthmayr H., and, Segal A. W., (2001) The NADPH oxidase components p47(phox) and p40(phox) bind to moesin through their PX domain. Biochem. Biophys. Res. Commun. 289, 382-388.
65. Wind S., Beuerlein K., Eucker T., Muller H., Scheurer P., Armitage M. E., Ho H., Schmidt H. H., and, Wingler K., (2010) Comparative pharmacology of chemically distinct NADPH oxidase inhibitors. Br. J. Pharmacol. 161, 885-898.
66. Winterbourn C. C., (2008) Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 4, 278-286.
67. Wojciak-Stothard B., Tsang L. Y., and, Haworth S. G., (2005) Rac and Rho play opposing roles in the regulation of hypoxia/reoxygenation-induced permeability changes in pulmonary artery endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 288, L749-L760.
68. Yang Y., Karakhanova S., Werner J., and, Bazhin A. V., (2013) Reactive oxygen species in cancer biology and anticancer therapy. Curr. Med. Chem. 20, 3677-3692.
69. Zhan Y., He D., Newburger P. E., and, Zhou G. W., (2004) p47(phox) PX domain of NADPH oxidase targets cell membrane via moesin-mediated association with the actin cytoskeleton. J. Cell. Biochem. 92, 795-809.
70. Zhang X. F., and, Forscher P., (2009) Rac1 modulates stimulus-evoked Ca2 + release in neuronal growth cones via parallel effects on microtubule/ER dynamics and ROS production. Mol. Biol. Cell 20, 3700-3712.