Oxygen radicals elicit paralysis and collapse of spinal cord neuron growth cones upon exposure to proinflammatory cytokines

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Kuhn, Thomas B ^a  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE RECEPTOR; INTERLEUKIN 1BETA; PROTEIN P67; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TUMOR NECROSIS FACTOR ALPHA; AUTACOID;

ACTIN FILAMENT; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL MOTILITY; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; GROWTH CONE; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; NERVE DEGENERATION; NERVE FIBER GROWTH; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PERIKARYON; PROTEIN EXPRESSION; SPINAL CORD CELL CULTURE; ANIMAL; BIOLOGICAL MODEL; CELL BODY; CHICK EMBRYO; DRUG EFFECTS; ENZYMOLOGY; HUMAN; METABOLISM; NEURITE; OXIDATION REDUCTION REACTION; PARALYSIS; PATHOLOGY; SPINAL CORD;

ACTIN CYTOSKELETON; ANIMALS; CELL BODY; CHICK EMBRYO; GROWTH CONES; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; MODELS, BIOLOGICAL; NADPH OXIDASE; NEURITES; OXIDATION-REDUCTION; PARALYSIS; RAC1 GTP-BINDING PROTEIN; REACTIVE OXYGEN SPECIES; SPINAL CORD; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84904129315     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/191767     Document Type: Article

References (67)

1. Amor S., Puentes F., Baker D., van der Valk P., Inflammation in neurodegenerative diseases. Immunology 2010 129 2 154 169 2-s2.0-73949090103 10.1111/j.1365-2567.2009.03225.x
2. Cacquevel M., Lebeurrier N., Chéenne S., Vivien D., Cytokines in neuroinflammation and Alzheimer's disease. Current Drug Targets 2004 5 6 529 534 2-s2.0-3442893295 10.2174/1389450043345308 (Pubitemid 39004427)
3. Lucas S.-M., Rothwell N. J., Gibson R. M., The role of inflammation in CNS injury and disease. British Journal of Pharmacology 2006 147 supplement 1 S232 S240 2-s2.0-30444459031 10.1038/sj.bjp.0706400 (Pubitemid 43077281)
4. McCoy M. K., Tansey M. G., TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. Journal of Neuroinflammation 2008 5, article 45 2-s2.0-55949104665 10.1186/1742-2094-5-45
5. Mrak R. E., Griffin W. S. T., Glia and their cytokines in progression of neurodegeneration. Neurobiology of Aging 2005 26 3 349 354 2-s2.0-11444256801 10.1016/j.neurobiolaging.2004.05.010 (Pubitemid 40082718)
6. Viviani B., Bartesaghi S., Corsini E., Galli C. L., Marinovich M., Cytokines role in neurodegenerative events. Toxicology Letters 2004 149 1-3 85 89 2-s2.0-1842767224 10.1016/j.toxlet.2003.12.022 (Pubitemid 38469824)
7. Mathew S. J., Haubert D., Krönke M., Leptin M., Looking beyond death: a morphogenetic role for the TNF signalling pathway. Journal of Cell Science 2009 122 12 1939 1946 2-s2.0-68949178567 10.1242/jcs.044487
8. Münch G., Gasic-Milenkovic J., Dukic-Stefanovic S., Kuhla B., Heinrich K., Riederer P., Huttunen H. J., Founds H., Sajithlal G., Microglial activation induces cell death, inhibits neurite outgrowth and causes neurite retraction of differentiated neuroblastoma cells. Experimental Brain Research 2003 150 1 1 8 2-s2.0-0038077245 (Pubitemid 36543137)
9. Neumann H., Schweigreiter R., Yamashita T., Rosenkranz K., Wekerle H., Barde Y.-A., Tumor necrosis factor inhibits neurite outgrowth and branching of hippocampal neurons by a Rho-dependent mechanism. The Journal of Neuroscience 2002 22 3 854 862 2-s2.0-0036469263 (Pubitemid 34141766)
10. Gungabissoon R. A., Bamburg J. R., Regulation of growth cone actin dynamics by ADF/cofilin. Journal of Histochemistry and Cytochemistry 2003 51 4 411 420 2-s2.0-0037387965 (Pubitemid 36418037)
11. Luo L., Rho GTPases in neuronal morphogenesis. Nature Reviews Neuroscience 2000 1 3 173 180 2-s2.0-0034574572
12. Moldovan L., Irani K., Moldovan N. I., Finkel T., Goldschmidt-Clermont P. J., The actin cytoskeleton reorganization induced by Rac1 requires the production of superoxide. Antioxidants and Redox Signaling 1999 1 1 29 43 2-s2.0-0033086255 (Pubitemid 129619761)
13. Thannickal V. J., Fanburg B. L., Reactive oxygen species in cell signaling. American Journal of Physiology: Lung Cellular and Molecular Physiology 2000 279 6 L1005 L1028 2-s2.0-0034533082 (Pubitemid 32009487)
14. Barth B. M., Stewart-Smeets S., Kuhn T. B., Proinflammatory cytokines provoke oxidative damage to actin in neuronal cells mediated by Rac1 and NADPH oxidase. Molecular and Cellular Neuroscience 2009 41 2 274 285 2-s2.0-67349164761 10.1016/j.mcn.2009.03.007
15. Munnamalai V., Suter D. M., Reactive oxygen species regulate F-actin dynamics in neuronal growth cones and neurite outgrowth. Journal of Neurochemistry 2009 108 3 644 661 2-s2.0-58149336903 10.1111/j.1471-4159.2008. 05787.x
16. Chakraborty S., Kaushik D. K., Gupta M., Basu A., Inflammasome signaling at the heart of central nervous system pathology. Journal of Neuroscience Research 2010 88 8 1615 1631 2-s2.0-77952413047 10.1002/jnr.22343
17. Morgan M. J., Kim Y.-S., Liu Z., Lipid rafts and oxidative stress-induced cell death. Antioxidants and Redox Signaling 2007 9 9 1471 1483 2-s2.0-34547868171 10.1089/ars.2007.1658 (Pubitemid 47255027)
18. Kawahara B. T., Quinn M. T., Lambeth J. D., Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes. BMC Evolutionary Biology 2007 7, article 109 2-s2.0-34547697113 10.1186/1471-2148-7- 109 (Pubitemid 47218714)
19. Lambeth J. D., NOX enzymes and the biology of reactive oxygen. Nature Reviews Immunology 2004 4 3 181 189 2-s2.0-1542406446 (Pubitemid 38339084)
20. Groemping Y., Rittinger K., Activation and assembly of the NADPH oxidase: a structural perspective. Biochemical Journal 2005 386 3 401 416 2-s2.0-15944372262 10.1042/BJ20041835 (Pubitemid 40445864)
21. Leonardi A., Ellinger-Ziegelbauer H., Franzoso G., Brown K., Siebenlist U., Physical and functional interaction of filamin (actin-binding protein-280) and tumor necrosis factor receptor-associated factor 2. The Journal of Biological Chemistry 2000 275 1 271 278 2-s2.0-0034614656 10.1074/jbc.275.1.271 (Pubitemid 30038982)
22. Peppelenbosch M., Boone E., Jones G. E., van Deventer S. J. H., Haegeman G., Fiers W., Grooten J., Ridley A. J., Multiple signal transduction pathways regulate TNF-induced actin reorganization in macrophages: inhibition of Cdc42-mediated filopodium formation by TNF. Journal of Immunology 1999 162 2 837 845 2-s2.0-0033556172 (Pubitemid 29035407)
23. Singh R., Wang B., Shirvaikar A., Khan S., Kamat S., Schelling J. R., Konieczkowski M., Sedor J. R., The IL-1 receptor and rho directly associate to drive cell activation in inflammation. Journal of Clinical Investigation 1999 103 11 1561 1570 2-s2.0-0032702311
24. Kuhn T. B., Growing and working with spinal motor neurons. Methods in Cell Biology 2003 71 67 87 10.1016/S0091-679X(03)01005-7 2-s2.0-1542674411 (Pubitemid 137639592)
25. Bottenstein J. E., Sato G. H., Growth of a rat neuroblastoma cell line in serum free supplemented medium. Proceedings of the National Academy of Sciences of the United States of America 1979 76 1 514 517 2-s2.0-0000854861 (Pubitemid 9106659)
26. Kuhn T. B., Brown M. D., Bamburg J. R., Rac1-dependent actin filament organization in growth cones is necessary for b1-integrin-mediated advance but not for growth on poly-D-lysine. Journal of Neurobiology 1998 37 524 540 (Pubitemid 28549215)
27. Owen Lockerbie R., Miller V. E., Pfenninger K. H., Regulated plasmalemmal expansion in nerve growth cones. The Journal of Cell Biology 1991 112 6 1215 1227 2-s2.0-0025969759 (Pubitemid 21909664)
28. Chang S., Rathjen F. G., Raper J. A., Extension of neurites on axons is impaired by antibodies against specific neural cell surface glycoproteins. The Journal of Cell Biology 1987 104 2 355 362 2-s2.0-0023294574
29. Stoeckli E. T., Kuhn T. B., Duc C. O., Ruegg M. A., Sonderegger P., The axonally secreted protein axonin-1 is a potent substratum for neurite growth. The Journal of Cell Biology 1991 112 3 449 455 2-s2.0-0025974195 10.1083/jcb.112.3.449 (Pubitemid 21925999)
30. Hall A., Rho GTpases and the actin cytoskeleton. Science 1998 279 5350 509 514 2-s2.0-0032559362 10.1126/science.279.5350.509 (Pubitemid 28067271)
31. Kuhn T. B., Brown M. D., Wilcox C. L., Raper J. A., Bamburg J. R., Myelin and collapsin-1 induce motor neuron growth cone collapse through different pathways: inhibition of collapse by opposing mutants of rac1. The Journal of Neuroscience 1999 19 6 1965 1975 2-s2.0-0033560132 (Pubitemid 29133375)
32. Brown M., Cornejo B., Kuhn T., Bamburg J., Cdc42 stimulates neurite outgrowth and formation of growth cone filopdia and lamellipodia. Journal of Neurobiology 2000 43 352 364 (Pubitemid 30409624)
33. Laemmli U. K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970 227 5259 680 685 2-s2.0-0014949207 10.1038/227680a0
34. Towbin H., Staehelin T., Gordon J., Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences of the United States of America 1979 76 9 4350 4354 2-s2.0-0009482260 (Pubitemid 9256559)
35. Kuhn T. B., Schmidt M. F., Kater S. B., Laminin and fibronectin guideposts signal sustained but opposite effects to passing growth cones. Neuron 1995 14 2 275 285 2-s2.0-0028872784
36. Wride M. A., Sanders E. J., Expression of tumor necrosis factor- α (TNF α)-cross-reactive proteins during early chick embryo development. Developmental Dynamics 1993 198 3 225 239 2-s2.0-0027762427 (Pubitemid 24010916)
37. Cypher C., Letourneau P. C., Identification of cytoskeletal, focal adhesion, and cell adhesion proteins in growth cone particles isolated from developing chick brain. Journal of Neuroscience Research 1991 30 1 259 265 2-s2.0-0026005822
38. Helmke S., Pfenninger K. H., Growth cone enrichment and cytoskeletal association of non-receptor tyrosine kinases. Cell Motility and the Cytoskeleton 1995 30 3 194 207 2-s2.0-0028948121 10.1002/cm.970300304
39. Negre-Aminou P., Pfenninger K. H., Arachidonic acid turnover and phospholipase A2 activity in neuronal growth cones. Journal of Neurochemistry 1993 60 3 1126 1136 2-s2.0-0027498020 (Pubitemid 23066736)
40. Jin Z., Strittmatter S. M., Rac1 mediates collapsin-1-induced growth cone collapse. The Journal of Neuroscience 1997 17 16 6256 6263 2-s2.0-0030809301 (Pubitemid 27329900)
41. Cooper C. E., Patel R. P., Brookes P. S., Darley-Usmar V. M., Nanotransducers in cellular redox signaling: modification of thiols by reactive oxygen and nitrogen species. Trends in Biochemical Sciences 2002 27 10 489 492 2-s2.0-0036803249 10.1016/S0968-0004(02)02191-6 (Pubitemid 35279586)
42. Dalle-Donne I., Rossi R., Milzani A., di Simplicio P., Colombo R., The actin cytoskeleton response to oxidants: from small heat shock protein phosphorylation to changes in the redox state of actin itself. Free Radical Biology and Medicine 2001 31 12 1624 1632 2-s2.0-0035893961 10.1016/S0891- 5849(01)00749-3 (Pubitemid 34024985)
43. Lassing I., Schmitzberger F., Björnstedt M., Holmgren A., Nordlund P., Schutt C. E., Lindberg U., Molecular and structural basis for redox regulation of β -actin. Journal of Molecular Biology 2007 370 2 331 348 2-s2.0-34249723277 10.1016/j.jmb.2007.04.056 (Pubitemid 46829216)
44. Nimnual A. S., Taylor L. J., Bar-Sagi D., Redox-dependent downregulation of Rho by Rac. Nature Cell Biology 2003 5 3 236 241 2-s2.0-0037341905 10.1038/ncb938 (Pubitemid 36322251)
45. Gustafson S. J., Dunlap K. L., McGill C. M., Kuhn T. B., A nonpolar blueberry fraction blunts NADPH oxidase activation in neuronal cells exposed to tumor necrosis factor- α Oxidative Medicine and Cellular Longevity 2012 2012 12 2-s2.0-84859747274 10.1155/2012/768101 768101
46. Merrill J. E., Tumor necrosis factor alpha, interleukin 1 and related cytokines in brain development: normal and pathological. Developmental Neuroscience 1992 14 1 1 10 2-s2.0-0026575543
47. Hordijk P. L., Regulation of NADPH oxidases: the role of Rac proteins. Circulation Research 2006 98 4 453 462 2-s2.0-33645285957 10.1161/01.RES. 0000204727.46710.5e
48. Noh K. M., Koh J. Y., Induction and activation by zinc of NADPH oxidase in cultured cortical neurons and astrocytes. The Journal of Neuroscience 2000 20 23, article RC111 2-s2.0-0034573392
49. Vallet P., Charnay Y., Steger K., Ogier-Denis E., Kovari E., Herrmann F., Michel J.-P., Szanto I., Neuronal expression of the NADPH oxidase NOX4, and its regulation in mouse experimental brain ischemia. Neuroscience 2005 132 2 233 238 2-s2.0-15744390035 10.1016/j.neuroscience.2004.12.038 (Pubitemid 40417898)
50. Dvorakova M., Höhler B., Richter E., Burritt J. B., Kummer W., Rat sensory neurons contain cytochrome b558 large subunit immunoreactivity. NeuroReport 1999 10 12 2615 2617 2-s2.0-0033588441 (Pubitemid 29418146)
51. Tammariello S. P., Quinn M. T., Estus S., NADPH oxidase contributes directly to oxidative stress and apoptosis in nerve growth factor-deprived sympathetic neurons. The Journal of Neuroscience 2000 20 1, article RC53 2-s2.0-17744417909
52. Puls A., Eliopoulos A. G., Nobes C. D., Bridges T., Young L. S., Hall A., Activation of the small GTPase Cdc42 by the inflammatory cytokines TNF α and IL-1, and by the Epstein-Barr virus transforming protein LMP1. Journal of Cell Science 1999 112 17 2983 2992 2-s2.0-0032841725 (Pubitemid 29430043)
53. Wojciak-Stothard B., Entwistle A., Garg R., Ridley A., Regulation of TNF alpha-induced reorganization of the actin cytoskeleton and cell-cell junctions by rho, rac, and cdc42 in human endothelial cells. Journal of Cell Physiology 1998 176 150 165 (Pubitemid 28277205)
54. Hall A., Nobes C. D., Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton. Philosophical Transactions of the Royal Society B: Biological Sciences 2000 355 1399 965 970 2-s2.0-0034729916 (Pubitemid 30613321)
55. Meyer G., Feldman E. L., Signaling mechanisms that regulate actin-based motility processes in the nervous system. Journal of Neurochemistry 2002 83 3 490 503 2-s2.0-0036828324 10.1046/j.1471-4159.2002.01185.x (Pubitemid 35231803)
56. Suzukawa K., Miura K., Mitsushita J., Resau J., Hirose K., Crystal R., Kamata T., Nerve growth factor-induced neuronal differentiation requires generation of rac1-regulated reactive oxygen species. The Journal of Biological Chemistry 2000 275 18 13175 13178 10.1074/jbc.275.18.13175 (Pubitemid 30257368)
57. Freeman J. L., Abo A., Lambeth J. D., Rac "insert region" is a novel effector region that is implicated in the activation of NADPH oxidase, but not PAK65. The Journal of Biological Chemistry 1996 271 33 19794 19801 2-s2.0-0029814413 10.1074/jbc.271.33.19794 (Pubitemid 26281718)
58. Joneson T., Bar-Sagi D., A Rac1 effector site controlling mitogenesis through superoxide production. The Journal of Biological Chemistry 1998 273 29 17991 17994 2-s2.0-0032541085 10.1074/jbc.273.29.17991 (Pubitemid 28334708)
59. Karnoub A. E., Der C. J., Campbell S. L., The insert region of Rac1 is essential for membrane ruffling but not cellular transformation. Molecular and Cellular Biology 2001 21 8 2847 2857 2-s2.0-0035076234 10.1128/MCB.21.8.2847- 2857.2001 (Pubitemid 32244928)
60. Allan S. M., Rothwell N. J., Cytokines and acute neurodegeneration. Nature Reviews Neuroscience 2001 2 10 734 744 2-s2.0-0035487313 10.1038/35094583 (Pubitemid 33674819)
61. Sei Y., Vitkovic L., Yokoyama M. M., Cytokines in the central nervous system: regulatory roles in neuronal function, cell death and repair. Neuroimmunomodulation 1995 2 3 121 133 2-s2.0-0028828155 10.1159/000096881
62. Vitkovic L., Bockaert J., Jacque C., "Inflammatory" cytokines: neuromodulators in normal brain? Journal of Neurochemistry 2000 74 2 457 471 2-s2.0-0033983153 10.1046/j.1471-4159.2000.740457.x (Pubitemid 30053717)
63. Bedard K., Krause K.-H., The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiological Reviews 2007 87 1 245 313 2-s2.0-33846794822 10.1152/physrev.00044.2005 (Pubitemid 46209993)
64. Kawahara T., Lambeth J. D., Molecular evolution of Phox-related regulatory subunits for NADPH oxidase enzymes. BMC Evolutionary Biology 2007 7, article 178 2-s2.0-36849064316 10.1186/1471-2148-7-178 (Pubitemid 350233621)
65. Krause K.-H., Lambeth D., Krönke M., NOX enzymes as drug targets. Cellular and Molecular Life Sciences 2012 69 14 2279 2282 2-s2.0-84864362404 10.1007/s00018-012-1006-5
66. Lambeth J. D., Krause K.-H., Clark R. A., NOX enzymes as novel targets for drug development. Seminars in Immunopathology 2008 30 3 339 363 2-s2.0-47149098182 10.1007/s00281-008-0123-6
67. Gao H.-M., Zhou H., Hong J.-S., NADPH oxidases: novel therapeutic targets for neurodegenerative diseases. Trends in Pharmacological Sciences 2012 33 6 295 303 2-s2.0-84861854211 10.1016/j.tips.2012.03.008