Involvement of reactive oxygen species in long-term potentiation in the spinal cord dorsal horn

Journal of Neurophysiology

Volumn 103, Issue 1, 2010, Pages 382-391

  Lee, Kwan Yeop ^a   Chung, Kyungsoon ^a   Chung, Jin Mo ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; N TERT BUTYL ALPHA PHENYLNITRONE; REACTIVE OXYGEN METABOLITE; TEMPOL; TERT BUTYL HYDROPEROXIDE;

ACTION POTENTIAL; AFFERENT NERVE GROUP 1; ANIMAL EXPERIMENT; ARTICLE; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; LONG TERM POTENTIATION; MALE; NERVE FIBER C; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; RAT; SENSITIZATION; SPINAL CORD; SPINAL CORD DORSAL HORN; STIMULUS;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; CENTRAL NERVOUS SYSTEM AGENTS; CYCLIC N-OXIDES; EVOKED POTENTIALS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; FREE RADICAL SCAVENGERS; LONG-TERM POTENTIATION; MALE; NERVE FIBERS, MYELINATED; NERVE FIBERS, UNMYELINATED; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECEPTORS, N-METHYL-D-ASPARTATE; SPIN LABELS; SPINAL NERVE ROOTS; TERT-BUTYLHYDROPEROXIDE;

EID: 74049084153     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.90906.2008     Document Type: Article

References (68)

1. Arancio O, Kiebler M, Lee CJ, Lev-Ram V, Tsien RY, Kandel ER, and Hawkins RD. Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87: 1025-1035, 1996.
2. Auerbach JM, Segal M. Peroxide modulation of slow onset potentiation in rat hippocampus. J Neurosci 17: 8695-8701, 1997.
3. Baba H, Doubell TP, Woolf CJ. Peripheral inflammation facilitates Abeta fiber-mediated synaptic input to the substantia gelatinosa of the adult rat spinal cord. J Neurosci 19: 859-867, 1999.
4. Bennett GJ, Abdelmoumene M, Hayashi H, Dubner R. Physiology and morphology of substantia gelatinosa neurons intracellularly stained with horseradish peroxidase. J Comp Neurol 194: 809-827, 1980.
5. Bindokas VP, Jordan J, Lee CC, Miller RJ. Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J Neurosci 16: 1324-1336, 1996.
6. Bliss TV, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39, 1993.
7. 2+ ions is stimulated by t-butyl hydroperoxide and mediated by reactive oxygen species generated by mitochondria. Free Radic Biol Med 18: 479-486, 1995.
8. Chetkovich DM, Klann E, Sweatt JD. Nitric oxide synthase-independent long-term potentiation in area CA1 of hippocampus. Neuroreport 4: 919-922, 1993.
9. Collingridge GL, Kehl SJ, McLennan H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol 334: 33-46, 1983.
10. Contestabile A. Oxidative stress in neurodegeneration: mechanisms and therapeutic perspectives. Curr Top Med Chem 1: 553-568, 2001.
11. Cook AJ, Woolf CJ, Wall PD, McMahon SB. Dynamic receptive field plasticity in rat spinal cord dorsal horn following C-primary afferent input. Nature 325: 151-153, 1987.
12. Dringen R, Pawlowski PG, Hirrlinger J. Peroxide detoxification by brain cells. J Neurosci Res 79: 157-165, 2005.
13. Dugan LL, Sensi SL, Canzoniero LM, Handran SD, Rothman SM, Lin TS, Goldberg MP, Choi DW. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-d-aspartate. J Neurosci 15: 6377-6388, 1995.
14. +: implications for neurodegeneration. J Neurochem 63: 584-591, 1994.
15. Gao X, Kim HK, Chung JM, Chung K. Reactive oxygen species (ROS) are involved in enhancement of NMDA-receptor phosphorylation in animal models of pain. Pain 131: 262-271, 2007.
16. Garthwaite J, Boulton CL. Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57: 683-706, 1995.
17. Gunasekar PG, Kanthasamy AG, Borowitz JL, Isom GE. NMDA receptor activation produces concurrent generation of nitric oxide and reactive oxygen species: implication for cell death. J Neurochem 65: 2016-2021, 1995.
18. Ikeda H, Heinke B, Ruscheweyh R, Sandkuhler J. Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia. Science 299: 1237-1240, 2003.
19. Ikeda H, Ryu PD, Park JB, Tanifuji M, Asai T, Murase K. Optical responses evoked by single-pulse stimulation to the dorsal root in the rat spinal dorsal horn in slice. Brain Res 812: 81-90, 1998.
20. Jenner P. Oxidative damage in neurodegenerative disease. Lancet 344: 796-798, 1994.
21. Ji RR, Kohno T, Moore KA, Woolf CJ. Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 26: 696-705, 2003.
22. Kanterewicz BI, Knapp LT, Klann E. Stimulation of p42 and p44 mitogen-activated protein kinases by reactive oxygen species and nitric oxide in hippocampus. J Neurochem 70: 1009-1016, 1998.
23. Katsuki H, Nakanishi C, Saito H, Matsuki N. Biphasic effect of hydrogen peroxide on field potentials in rat hippocampal slices. Eur J Pharmacol 337: 213-218, 1997.
24. Kim HK, Park SK, Zhou JL, Taglialatela G, Chung K, Coggeshall RE, Chung JM. Reactive oxygen species (ROS) play an important role in a rat model of neuropathic pain. Pain 111: 116-124, 2004.
25. Klann E. Cell-permeable scavengers of superoxide prevent long-term potentiation in hippocampal area CA1. J Neurophysiol 80: 452-457, 1998.
26. Klann E, Roberson ED, Knapp LT, Sweatt JD. A role for superoxide in protein kinase C activation and induction of long-term potentiation. J Biol Chem 273: 4516-4522, 1998.
27. Knapp LT, Klann E. Potentiation of hippocampal synaptic transmission by superoxide requires the oxidative activation of protein kinase C. J Neurosci 22: 674-683, 2002.
28. Kukreja RC, Kontos HA, Hess ML, Ellis EF. PGH synthase and lipoxygenase generate superoxide in the presence of NADH or NADPH. Circ Res 59: 612-619, 1986.
29. Lee I, Kim HK, Kim JH, Chung K, Chung JM. The role of reactive oxygen species in capsaicin-induced mechanical hyperalgesia and in the activities of dorsal horn neurons. Pain 133: 9-17, 2007.
30. Liu XG, Sandkuhler J. Long-term potentiation of C-fiber-evoked potentials in the rat spinal dorsal horn is prevented by spinal N-methyl-d-aspartic acid receptor blockage. Neurosci Lett 191: 43-46, 1995.
31. Liu X, Sandkuhler J, Characterization of long-term potentiation of C-fiber-evoked potentials in spinal dorsal horn of adult rat: essential role of NK1 and NK2 receptors. J Neurophysiol 78: 1973-1982, 1997.
32. Liu XG, Sandkuhler J. Activation of spinal N-methyl-d- aspartate or neurokinin receptors induces long-term potentiation of spinal C-fiber-evoked potentials. Neuroscience 86: 1209-1216, 1998.
33. Magerl W, Fuchs PN, Meyer RA, Treede RD. Roles of capsaicin-insensitive nociceptors in cutaneous pain and secondary hyperalgesia. Brain 124: 1754-1764, 2001.
34. Malenka RC, Kauer JA, Zucker RS, Nicoll RA. Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. Science 242: 81-84, 1988.
35. McCord JM, Fridovich I. The utility of superoxide dismutase in studying free radical reactions. I. Radicals generated by the interaction of sulfite, dimethyl sulfoxide, and oxygen. J Biol Chem 244: 6056-6063, 1969.
36. Meller ST, Gebhart GF. Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 52: 127-136, 1993.
37. Osborne MG, Coderre TJ. Effects of intrathecal administration of nitric oxide synthase inhibitors on carrageenan-induced thermal hyperalgesia. Br J Pharmacol 126: 1840-1846, 1999.
38. Pellmar TC, Hollinden GE, Sarvey JM. Free radicals accelerate the decay of long-term potentiation in field CA1 of guinea pig hippocampus. Neuroscience 44: 353-359, 1991.
39. Pou S, Pou WS, Bredt DS, Snyder SH, Rosen GM. Generation of superoxide by purified brain nitric oxide synthase. J Biol Chem 267: 24173-24176, 1992.
40. Randic M, Jiang MC, Cerne R. Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J Neurosci 13: 5228-5241, 1993.
41. Reynolds IJ, Hastings TG. Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J Neurosci 15: 3318-3327, 1995.
42. Salvemini D, Doyle TM, Cuzzocrea S. Superoxide, peroxynitrite and oxidative/nitrative stress in inflammation. Biochem Soc Trans 34: 965-970, 2006.
43. Sandkuhler J. Learning and memory in pain pathways. Pain 88: 113-118, 2000.
44. Sandkuhler J. Understanding LTP in pain pathways. Mol Pain 3: 9, 2007.
45. Sandkuhler J, Chen JG, Cheng G, Randic M. Low-frequency stimulation of afferent Adelta-fibers induces long-term depression at primary afferent synapses with substantia gelatinosa neurons in the rat. J Neurosci 17: 6483-6491, 1997.
46. Schmidt R, Schmelz M, Forster C, Ringkamp M, Torebjork E, Handwerker H. Novel classes of responsive and unresponsive C nociceptors in human skin. J Neurosci 15: 333-341, 1995.
47. Schmidt R, Willis WD. Encyclopedia of Pain. New York: Springer, 2007, vol. 1.
48. Schneider SP, Perl ER. Comparison of primary afferent and glutamate excitation of neurons in the mammalian spinal dorsal horn. J Neurosci 8: 2062-2073, 1988.
49. Schuman EM, Madison DV. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254: 1503-1506, 1991.
50. Schwartz ES, Kim HY, Wang J, Lee I, Klann E, Chung JM, Chung K. Persistent pain is dependent on spinal mitochondrial antioxidant levels. J Neurosci 29: 159-168, 2009.
51. Schwartz ES, Lee I, Chung K, Chung JM. Oxidative stress in the spinal cord is an important contributor in capsaicin-induced mechanical secondary hyperalgesia in mice. Pain 138: 514-524, 2008.
52. Svendsen F, Tjolsen A, Hole K. AMPA and NMDA receptor-dependent spinal LTP after nociceptive tetanic stimulation. Neuroreport 9: 1185-1190, 1998.
53. Tal M. A novel antioxidant alleviates heat hyperalgesia in rats with an experimental painful peripheral neuropathy. Neuroreport 7: 1382-1384, 1996.
54. Thiels E, Kanterewicz BI, Knapp LT, Barrionuevo G, Klann E. Protein phosphatase-mediated regulation of protein kinase C during long-term depression in the adult hippocampus in vivo. J Neurosci 20: 7199-7207, 2000a.
55. Thiels E, Urban NN, Gonzalez-Burgos GR, Kanterewicz BI, Barrionuevo G, Chu CT, Oury TD, Klann E. Impairment of long-term potentiation and associative memory in mice that overexpress extracellular superoxide dismutase. J Neurosci 20: 7631-7639, 2000b.
56. Wang ZQ, Porreca F, Cuzzocrea S, Galen K, Lightfoot R, Masini E, Muscoli C, Mollace V, Ndengele M, Ischiropoulos H, Salvemini D. A newly identified role for superoxide in inflammatory pain. J Pharmacol Exp Ther 309: 869-878, 2004.
57. Willis WD. Long-term potentiation in spinothalamic neurons. Brain Res Brain Res Rev 40: 202-214, 2002.
58. Willis WD, Coggeshall RE. Sensory mechanisms of the spinal cord. New York: Plenum, 2004.
59. Woolf CJ. Evidence for a central component of post-injury pain hypersensitivity. Nature 306: 686-688, 1983.
60. Woolf CJ. Central terminations of cutaneous mechanoreceptive afferents in the rat lumbar spinal cord. J Comp Neurol 261: 105-119, 1987.
61. Woolf CJ, Fitzgerald M. The properties of neurones recorded in the superficial dorsal horn of the rat spinal cord. J Comp Neurol 221: 313-328, 1983.
62. Wu J, Fang L, Lin Q, Willis WD. Nitric oxide synthase in spinal cord central sensitization following intradermal injection of capsaicin. Pain 94: 47-58, 2001.
63. Wu J, Lin Q, McAdoo DJ, Willis WD. Nitric oxide contributes to central sensitization following intradermal injection of capsaicin. Neuroreport 9: 589-592, 1998.
64. Xia Z, Storm DR. The role of calmodulin as a signal integrator for synaptic plasticity. Nat Rev Neurosci 6: 267-276, 2005.
65. Xin WJ, Gong QJ, Xu JT, Yang HW, Zang Y, Zhang T, Li YY, Liu XG. Role of phosphorylation of ERK in induction and maintenance of LTP of the C-fiber evoked field potentials in spinal dorsal horn. J Neurosci Res 84: 934-943, 2006.
66. Xu L, Mabuchi T, Katano T, Matsumura S, Okuda-Ashitaka E, Sakimura K, Mishina M, Ito S. Nitric oxide (NO) serves as a retrograde messenger to activate neuronal NO synthase in the spinal cord via NMDA receptors. Nitric Oxide 17: 18-24, 2007.
67. Yang HW, Hu XD, Zhang HM, Xin WJ, Li MT, Zhang T, Zhou LJ, Liu XG. Roles of CaMKII, PKA, and PKC in the induction and maintenance of LTP of C-fiber-evoked field potentials in rat spinal dorsal horn. J Neurophysiol 91: 1122-1133, 2004.
68. Zorumski CF, Izumi Y. Nitric oxide and hippocampal synaptic plasticity. Biochem Pharmacol 46: 777-785, 1993.