Reactive oxygen species regulate F-actin dynamics in neuronal growth cones and neurite outgrowth

Journal of Neurochemistry

Volumn 108, Issue 3, 2009, Pages 644-661

  Munnamalai, Vidhya ^a   Suter, Daniel M ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

Actin dynamics; Growth cone; Neurite outgrowth; Reactive oxygen species; Rho; Signaling

Indexed keywords

F ACTIN; LIPOXYGENASE; N TERT BUTYL ALPHA PHENYLNITRONE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RHO FACTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; FLUORESCENCE MICROSCOPY; GROWTH INHIBITION; NERVE CELL CULTURE; NERVE CELL GROWTH; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN STRUCTURE;

ACTINS; ANIMALS; APLYSIA; CELLS, CULTURED; GROWTH CONES; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INDICATORS AND REAGENTS; LIPOXYGENASE; MICROSCOPY, FLUORESCENCE; MICROSCOPY, PHASE-CONTRAST; NADPH OXIDASE; NEURITES; REACTIVE OXYGEN SPECIES; RHO-ASSOCIATED KINASES;

EID: 58149336903     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05787.x     Document Type: Article

References (61)

1. Abo A., Pick E., Hall A., Totty N., Teahan C. G. Segal A. W. (1991) Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature 353, 668 670.
2. Alexandrova A. Y., Kopnin P. B., Vasiliev J. M. Kopnin B. P. (2006) ROS up-regulation mediates Ras-induced changes of cell morphology and motility. Exp. Cell Res. 312, 2066 2073.
3. Barrientos A. Moraes C. T. (1999) Titrating the effects of mitochondrial complex I impairment in the cell physiology. J. Biol. Chem. 274, 16188 16197.
4. Bedard K. Krause K. H. (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245 313.
5. Chang S., Rathjen F. G. Raper J. A. (1987) Extension of neurites on axons is impaired by antibodies against specific neural cell surface glycoproteins. J. Cell Biol. 104, 355 362.
6. Chiarugi P. (2005) PTPs versus PTKs: the redox side of the coin. Free Radic. Res. 39, 353 364.
7. Chiarugi P. Fiaschi T. (2007) Redox signalling in anchorage-dependent cell growth. Cell. Signal. 19, 672 682.
8. Chiarugi P., Pani G., Giannoni E., Taddei L., Colavitti R., Raugei G., Symons M., Borrello S., Galeotti T. Ramponi G. (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.
9. Crawford L. E., Milliken E. E., Irani K., Zweier J. L., Becker L. C., Johnson T. M., Eissa N. T., Crystal R. G., Finkel T. Goldschmidt-Clermont P. J. (1996) Superoxide-mediated actin response in post-hypoxic endothelial cells. J. Biol. Chem. 271, 26863 26867.
10. Cui Z. G., Kondo T. Matsumoto H. (2006) Enhancement of apoptosis by nitric oxide released from alpha-phenyl-tert-butyl nitrone under hyperthermic conditions. J. Cell. Physiol. 206, 468 476.
11. Duan Y., Gross R. A. Sheu S. S. (2007) Ca2+-dependent generation of mitochondrial reactive oxygen species serves as a signal for poly(ADP-ribose) polymerase-1 activation during glutamate excitotoxicity. J. Physiol. 585, 741 758.
12. Etienne-Manneville S. Hall A. (2002) Rho GTPases in cell biology. Nature 420, 629 635.
13. Fiaschi T., Cozzi G., Raugei G., Formigli L., Ramponi G. Chiarugi P. (2006) Redox regulation of beta-actin during integrin-mediated cell adhesion. J. Biol. Chem. 281, 22983 22991.
14. Forscher P. 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.
15. Gallo G. (2006) RhoA-kinase coordinates F-actin organization and myosin II activity during semaphorin-3A-induced axon retraction. J. Cell Sci. 119, 3413 3423.
16. Gallo G. Letourneau P. C. (2004) Regulation of growth cone actin filaments by guidance cues. J. Neurobiol. 58, 92 102.
17. Giniger E. (2002) How do Rho family GTPases direct axon growth and guidance? A proposal relating signaling pathways to growth cone mechanics. Differentiation 70, 385 396.
18. Grzywa E. L., Lee A. C., Lee G. U. Suter D. M. (2006) High-resolution analysis of neuronal growth cone morphology by comparative atomic force and optical microscopy. J. Neurobiol. 66, 1529 1543.
19. Hilburger E. W., Conte E. J., McGee D. W. Tammariello S. P. (2005) Localization of NADPH oxidase subunits in neonatal sympathetic neurons. Neurosci. Lett. 377, 16 19.
20. Jalink K., van Corven E. J., Hengeveld T., Morii N., Narumiya S. Moolenaar W. H. (1994) Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell Biol. 126, 801 810.
21. Knapp L. T. Klann E. (2002) Role of reactive oxygen species in hippocampal long-term potentiation: contributory or inhibitory? J. Neurosci. Res. 70, 1 7.
22. Kotake Y., Sang H., Miyajima T. Wallis G. L. (1998) Inhibition of NF-kappaB, iNOS mRNA, COX2 mRNA, and COX catalytic activity by phenyl-N-tert-butylnitrone (PBN). Biochim. Biophys. Acta 1448, 77 84.
23. Lambeth J. D. (2007) Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic. Biol. Med. 43, 332 347.
24. Le Cabec V. 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.
25. Lee A. C., Decourt B. Suter D. M. (2008) Neuronal cell cultures from Aplysia for high-resolution imaging of growth cones. J. Vis. Experim. 12, doi :.
26. Lewis A. K. Bridgman P. C. (1992) Nerve growth cone lamellipodia contain two populations of actin filaments that differ in organization and polarity. J. Cell Biol. 119, 1219 1243.
27. Luo J., Li N., Robinson J. P. Shi R. (2002) The increase of reactive oxygen species and their inhibition in an isolated guinea pig spinal cord compression model. Spinal Cord 40, 656 665.
28. Maher P. Schubert D. (2000) Signaling by reactive oxygen species in the nervous system. Cell. Mol. Life Sci. 57, 1287 1305.
29. Medeiros N. A., Burnette D. T. Forscher P. (2006) Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat. Cell Biol. 8, 215 226.
30. Meng T. C., Fukada T. Tonks N. K. (2002) Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell 9, 387 399.
31. Mikule K., Gatlin J. C., de la Houssaye B. A. Pfenninger K. H. (2002) Growth cone collapse induced by semaphorin 3A requires 12/15-lipoxygenase. J. Neurosci. 22, 4932 4941.
32. Miller Y. I., Chang M. K., Funk C. D., Feramisco J. R. Witztum J. L. (2001) 12/15-Lipoxygenase translocation enhances site-specific actin polymerization in macrophages phagocytosing apoptotic cells. J. Biol. Chem. 276, 19431 19439.
33. Moldovan L., Moldovan N. I., Sohn R. H., Parikh S. A. Goldschmidt-Clermont P. J. (2000) Redox changes of cultured endothelial cells and actin dynamics. Circ. Res. 86, 549 557.
34. Moldovan L., Mythreye K., Goldschmidt-Clermont P. J. Satterwhite L. L. (2006) Reactive oxygen species in vascular endothelial cell motility. Roles of NAD(P)H oxidase and Rac1. Cardiovasc. Res. 71, 236 246.
35. Nimnual A. S., Taylor L. J. Bar-Sagi D. (2003) Redox-dependent downregulation of Rho by Rac. Nat. Cell Biol. 5, 236 241.
36. Nishiyama M., Hoshino A., Tsai L., Henley J. R., Goshima Y., Tessier-Lavigne M., Poo M. M. Hong K. (2003) Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning. Nature 423, 990 995.
37. Patel M. (1998) Inhibition of neuronal apoptosis by a metalloporphyrin superoxide dismutase mimic. J. Neurochem. 71, 1068 1074.
38. Reynolds I. J. Hastings T. G. (1995) Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J. Neurosci. 15, 3318 3327.
39. Robles E., Woo S. Gomez T. M. (2005) Src-dependent tyrosine phosphorylation at the tips of growth cone filopodia promotes extension. J. Neurosci. 25, 7669 7681.
40. Rochlin M. W., Dailey M. E. Bridgman P. C. (1999) Polymerizing microtubules activate site-directed F-actin assembly in nerve growth cones. Mol. Biol. Cell 10, 2309 2327.
41. Salari H., Braquet P. Borgeat P. (1984) Comparative effects of indomethacin, acetylenic acids, 15-HETE, nordihydroguaiaretic acid and BW755C on the metabolism of arachidonic acid in human leukocytes and platelets. Prostaglandins Leukot. Med. 13, 53 60.
42. Schaefer A. W., Kabir N. Forscher P. (2002) Filopodia and actin arcs guide the assembly and transport of two populations of microtubules with unique dynamic parameters in neuronal growth cones. J. Cell Biol. 158, 139 152.
43. Stolk J., Hiltermann T. J., Dijkman J. H. Verhoeven A. J. (1994) 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.
44. Sturgess N. C., Rustad A., Fonnum F. Lock E. A. (2000) Neurotoxic effect of L-2-chloropropionic acid on primary cultures of rat cerebellar granule cells. Arch. Toxicol. 74, 153 160.
45. Suter D. M. Forscher P. (2001) Transmission of growth cone traction force through apCAM-cytoskeletal linkages is regulated by Src family tyrosine kinase activity. J. Cell Biol. 155, 427 438.
46. Suter D. M., Errante L. D., Belotserkovsky V. Forscher P. (1998) The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J. Cell Biol. 141, 227 240.
47. Suter D. M., Schaefer A. W. Forscher P. (2004) Microtubule dynamics are necessary for SRC family kinase-dependent growth cone steering. Curr. Biol. 14, 1194 1199.
48. Suzukawa K., Miura K., Mitsushita J., Resau J., Hirose K., Crystal R. Kamata T. (2000) Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species. J. Biol. Chem. 275, 13175 13178.
49. Tabner B. J., Turnbull S., El-Agnaf O. Allsop D. (2001) Production of reactive oxygen species from aggregating proteins implicated in Alzheimer's disease, Parkinson's disease and other neurodegenerative diseases. Curr. Top. Med. Chem. 1, 507 517.
50. Tejada-Simon M. V., Serrano F., Villasana L. E., Kanterewicz B. I., Wu G. Y., Quinn M. T. Klann E. (2005) Synaptic localization of a functional NADPH oxidase in the mouse hippocampus. Mol. Cell. Neurosci. 29, 97 106.
51. Thannickal V. J. Fanburg B. L. (2000) Reactive oxygen species in cell signaling. Am. J. Physiol. Lung Cell Mol. Physiol. 279, L1005 L1028.
52. Thomas C. E., Ohlweiler D. F., Taylor V. L. Schmidt C. J. (1997) Radical trapping and inhibition of iron-dependent CNS damage by cyclic nitrone spin traps. J. Neurochem. 68, 1173 1182.
53. 2 are key components of hypoxia-sensing in neonatal rat adrenomedullary chromaffin cells. Neuroscience 145, 130 141.
54. Ushio-Fukai M. (2006) Localizing NADPH oxidase-derived ROS. Sci. STKE 349, re8.
55. Waterman-Storer C. M., Desai A., Bulinski J. C. Salmon E. D. (1998) Fluorescent speckle microscopy, a method to visualize the dynamics of protein assemblies in living cells. Curr. Biol. 8, 1227 1230.
56. Wojciak-Stothard B., Tsang L. Y. 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.
57. Woo C. H., Eom Y. W., Yoo M. H., You H. J., Han H. J., Song W. K., Yoo Y. J., Chun J. S. Kim J. H. (2000) Tumor necrosis factor-alpha generates reactive oxygen species via a cytosolic phospholipase A2-linked cascade. J. Biol. Chem. 275, 32357 32362.
58. Xu W., Chi L., Xu R., Ke Y., Luo C., Cai J., Qiu M., Gozal D. Liu R. (2005) Increased production of reactive oxygen species contributes to motor neuron death in a compression mouse model of spinal cord injury. Spinal Cord 43, 204 213.
59. Zhang X. F., Schaefer A. W., Burnette D. T., Schoonderwoert V. T. Forscher P. (2003) Rho-dependent contractile responses in the neuronal growth cone are independent of classical peripheral retrograde actin flow. Neuron 40, 931 944.
60. Zhao Y. Davis H. W. (1998) Hydrogen peroxide-induced cytoskeletal rearrangement in cultured pulmonary endothelial cells. J. Cell. Physiol. 174, 370 379.
61. Zini I., Tomasi A., Grimaldi R., Vannini V. Agnati L. F. (1992) Detection of free radicals during brain ischemia and reperfusion by spin trapping and microdialysis. Neurosci. Lett. 138, 279 282.