Mitochondrial reactive oxygen species are activated by mGluR5 through IP3 and activate ERK and PKA to increase excitability of amygdala neurons and pain behavior

Journal of Neuroscience

Volumn 31, Issue 3, 2011, Pages 1114-1127

  Li, Zhen ^a   Ji, Guangchen ^a   Neugebauer, Volker ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 2 CHLORO 5 HYDROXYPHENYL GLYCINE; 3 [(2 METHYL 4 THIAZOLYL)ETHYNYL]PYRIDINE; 3,5 DIHYDROXYPHENYLGLYCINE; 4 CARBOXY 2 METHYLPHENYLGLYCINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; INOSITOL 1,4,5 TRISPHOSPHATE; KT 5720; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5; METABOTROPIC RECEPTOR AGONIST; MITOGEN ACTIVATED PROTEIN KINASE; N(G) NITROARGININE METHYL ESTER; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TEMPOL; UNCLASSIFIED DRUG; XESTOSPONGIN C;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; EVOKED RESPONSE; HISTOPATHOLOGY; INTRACELLULAR SIGNALING; MALE; MITOCHONDRION; NERVE CELL EXCITABILITY; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT; SPINAL REFLEX; SYNAPSE;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; ANTIOXIDANTS; BENZOATES; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC N-OXIDES; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GLYCINE; INOSITOL 1,4,5-TRISPHOSPHATE; MACROCYCLIC COMPOUNDS; MITOCHONDRIA; NEURONS; NG-NITROARGININE METHYL ESTER; OXAZOLES; PAIN; PAIN MEASUREMENT; PAIN PERCEPTION; PATCH-CLAMP TECHNIQUES; PYRIDINES; REACTIVE OXYGEN SPECIES; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; SPIN LABELS; SUPEROXIDES; THIAZOLES; VOCALIZATION, ANIMAL;

EID: 78751528230     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5387-10.2011     Document Type: Article

References (81)

1. Ansah OB, Gonçalves L, Almeida A, Pertovaara A (2009) Enhanced pronociception by amygdaloid group I metabotropic glutamate receptors in nerve-injured animals. Exp Neurol 216:66-74.
2. Ansah OB, Bourbia N, Gonçalves L, Almeida A, Pertovaara A (2010) Influence of amygdaloid glutamatergic receptors on sensory and emotional pain-related behavior in the neuropathic rat. Behav Brain Res 209:174-178.
3. Bird GC, Lash LL, Han JS, Zou X, Willis WD, Neugebauer V (2005) Protein kinase A-dependent enhanced NMDA receptor function in pain-related synaptic plasticity in rat amygdala neurones. J Physiol 564:907-921.
4. Birnbaum SG, Varga AW, Yuan LL, Anderson AE, Sweatt JD, Schrader LA (2004) Structure and function of Kv4-family transient potassium channels. Physiol Rev 84:803-833.
5. Cabell L, Audesirk G (1993) Effects of selective inhibition of protein kinase C, cyclic AMP-dependentdependent protein kinase, and Ca(2+)-calmodulin- dependent protein kinase on neurite development in cultured rat hippocampal neurons. Int J Dev Neurosci 11:357-368.
6. Carrasquillo Y, GereauRW4th (2007) Activation of the extracellular signal-regulated kinase in the amygdala modulates pain perception. J Neurosci 27:1543-1551.
7. Carrasquillo Y, Gereau RW 4th (2008) Hemispheric lateralization of a molecular signal for pain modulation in the amygdala. Mol Pain 4:24.
8. Chinopoulos C, Adam-Vizi V (2006) Calcium, mitochondria and oxidative stress in neuronal pathology: novel aspects of an enduring theme. FEBS J 273:433-450.
9. Chung JM (2004) The role of reactive oxygen species (ROS) in persistent pain. Mol Interv 4:248-250.
10. Conn PJ (2003) Physiological roles and therapeutic potential of metabotropic glutamate receptors. Ann NY Acad Sci 1003:12-21.
11. 3 receptor ligand. Mol Pharmacol 77:995-1004.
12. Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, Feeser WS, Van Dyk DE, Pitts WJ, Earl RA, Hobbs F, Copeland RA, Magolda RL, Scherle PA, Trzaskos JM (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273:18623-18632.
13. Freire MA, Guimarães JS, Leal WG, Pereira A (2009) Pain modulation by nitric oxide in the spinal cord. Front Neurosci 3:175-181.
14. Fu Y, Neugebauer V (2008) Differential mechanisms of CRF1 and CRF2 receptor functions in the amygdala in pain-related synaptic facilitation and behavior. J Neurosci 28:3861-3876.
15. Fu Y, Han J, Ishola T, Scerbo M, Adwanikar H, Ramsey C, Neugebauer V (2008) PKA and ERK, but not PKC, in the amygdala contribute to pain-related synaptic plasticity and behavior. Mol Pain 4:26-46.
16. Gao X, Kim HK, Chung JM, ChungK (2007) Reactive oxygen species (ROS) are involved in enhancement of NMDA-receptor phosphorylation in animal models of pain. Pain 131:262-271. (Pubitemid 47374329)
17. Gauriau C, Bernard JF (2002) Pain pathways and parabrachial circuits in the rat. Exp Physiol 87:251-258.
18. Gebhart GF (2004) Descending modulation of pain. Neurosci Biobehav Rev 27:729-737.
19. Gereau RW 4th, Heinemann SF (1998) Role of protein kinase C phosphorylation in rapid desensitization of metabotropic glutamate receptor 5. Neuron 20:143-151.
20. Giles PA, Trezise DJ, King AE (2007) Differential activation of protein kinases in the dorsal horn in vitro of normal and inflamed rats by group I metabotropic glutamate receptor subtypes. Neuropharmacology 53:58-70.
21. 2+ uptake in apoptosis. Cell Calcium 40:553-560.
22. Han JS, Neugebauer V (2005) mGluR1 and mGluR5 antagonists in the amygdala inhibit different components of audible and ultrasonic vocalizations in a model of arthritic pain. Pain 113:211-222.
23. Han JS, Bird GC, Li W, Jones J, Neugebauer V (2005a) Computerized analysis of audible and ultrasonic vocalizations of rats as a standardized measure of pain-related behavior. J Neurosci Methods 141:261-269.
24. Han JS, Li W, Neugebauer V (2005b) Critical role of calcitonin gene-related peptide 1 receptors in the amygdala in synaptic plasticity and pain behavior. J Neurosci 25:10717-10728.
25. Han JS, Adwanikar H, Li Z, Ji G, Neugebauer V (2010) Facilitation of synaptic transmission and pain responses by CGRP in the amygdala of normal rats. Mol Pain 6:10-23.
26. Harrigan EA, Magnuson DJ, Thunstedt GM, Gray TS (1994) Corticotropin releasing factor neurons are innervated by calcitonin gene-related peptide terminals in the rat central amygdaloid nucleus. Brain Res Bull 33: 529-534.
27. Hidalgo C, Donoso P (2008) Crosstalk between calcium and redox signaling: from molecular mechanisms to health implications. Antioxid Redox Signal 10:1275-1312. (Pubitemid 351634396)
28. Hu D, Serrano F, Oury TD, Klann E (2006) Aging-dependent alterations in synaptic plasticity and memory in mice that overexpress extracellular superoxide dismutase. J Neurosci 26:3933-3941.
29. + currents. J Neurophysiol 90:1671-1679.
30. Huddleston AT, Tang W, Takeshima H, Hamilton SL, Klann E (2008) Superoxide-induced potentiation in the hippocampus requires activation of ryanodine receptor type 3 and ERK. J Neurophysiol 99:1565-1571.
31. Ji G, Neugebauer V (2007) Differential effects of CRF1 and CRF2 receptor antagonists on pain-related sensitization of neurons in the central nucleus of the amygdala. J Neurophysiol 97:3893-3904.
32. Ji G, Neugebauer V (2009) Hemispheric lateralization of pain processing by amygdala neurons. J Neurophysiol 102:2253-2264.
33. Ji G, Neugebauer V (2010) Reactive oxygen species are involved in group I mGluR-mediated facilitation of nociceptive processing in amygdala neurons. J Neurophysiol 104:218-229.
34. Ji G, Sun H, Fu Y, Li Z, Pais-Vieira M, Galhardo V, Neugebauer V (2010) Cognitive impairment in pain through amygdala-driven prefrontal cortical deactivation. J Neurosci 30:5451-5464.
35. Joly C, Gomeza J, Brabet I, Curry K, Bockaert J, Pin JP (1995) Molecular, functional, and pharmacological characterization of the metabotropic glutamate receptor type 5 splice variants: comparison with mGluR1. J Neurosci 15:3970-3981.
36. Karim F, Wang CC, Gereau RW 4th (2001) Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice. J Neurosci 21:3771-3779.
37. Keeble JE, Bodkin JV, Liang L, Wodarski R, Davies M, Fernandes ES, Coelho Cde F, Russell F, Graepel R, Muscara MN, Malcangio M, Brain SD (2009) Hydrogen peroxide is a novel mediator of inflammatory hyperalgesia, acting via transient receptor potential vanilloid 1-dependent and independent mechanisms. Pain 141:135-142.
38. Kemmerling U, Muñoz P, Müller M, Sánchez G, Aylwin ML, Klann E, Carrasco MA, Hidalgo C (2007) Calcium release by ryanodine receptors mediates hydrogen peroxide-induced activation of ERK and CREB phosphorylation in N2a cells and hippocampal neurons. Cell Calcium 41:491-502. (Pubitemid 46404814)
39. Kim HK, Park SK, Zhou JL, Taglialatela G, Chung K, Coggeshall RE, Chung JM (2004) Reactive oxygen species (ROS) play an important role in a rat model of neuropathic pain. Pain 111:116-124.
40. Kim HY, Wang J, Lu Y, Chung JM, Chung K (2009) Superoxide signaling in pain is independent of nitric oxide signaling. Neuroreport 20:1424-1428.
41. Kingston AE, Griffey K, Johnson MP, Chamberlain MJ, Kelly G, Tomlinson R, Wright RA, Johnson BG, Schoepp DD, Harris JR, Clark BP, Baker RS, Tizzano JT (2002) Inhibition of group I metabotropic glutamate receptor responses in vivo in rats by a new generation of carboxyphenylglycinelike amino acid antagonists. Neurosci Lett 330:127-130.
42. Kishida KT, Klann E (2007) Sources and targets of reactive oxygen species in synaptic plasticity and memory. Antioxid Redox Signal 9:233-244.
43. Klann E (1998) Cell-permeable scavengers of superoxide prevent long-term potentiation in hippocampal area CA1. J Neurophysiol 80:452-457.
44. Knapp LT, Klann E (2002) Role of reactive oxygen species in hippocampal long-term potentiation: contributory or inhibitory? J Neurosci Res 70:1-7.
45. Kolber BJ, Montana MC, Carrasquillo Y, Xu J, Heinemann SF, Muglia LJ, GereauRW4th (2010) Activation of metabotropic glutamate receptor 5 in the amygdala modulates pain-like behavior. J Neurosci 30:8203-8213.
46. Kotake Y (1999) Pharmacologic properties of phenyl N-tert-butylnitrone. Antioxid Redox Signal 1:481-499.
47. Lea PM 4th, Faden AI (2006) Metabotropic glutamate receptor subtype 5 antagonists MPEP and MTEP. CNS Drug Rev 12:149-166.
48. Lee I, Kim HK, Kim JH, Chung K, Chung JM (2007) The role of reactive oxygen species in capsaicin-induced mechanical hyperalgesia and in the activities of dorsal horn neurons. Pain 133:9-17.
49. Lee KY, Chung K, Chung JM (2010) Involvement of reactive oxygen species in long-term potentiation in the spinal cord dorsal horn. J Neurophysiol 103:382-391.
50. Lesage ASJ (2004) Role of group I metabotropic glutamate receptors mGlu1 and mGlu5 in nociceptive signalling. Curr Neuropharmacol 2:363-393. (Pubitemid 39276630)
51. Li W, Neugebauer V (2004) Differential roles of mGluR1 and mGluR5 in brief and prolonged nociceptive processing in central amygdala neurons. J Neurophysiol 91:13-24.
52. Liu T, Hannafon B, Gill L, Kelly W, Benbrook D (2007) Flex-Hets differentially induce apoptosis in cancer over normal cells by directly targeting mitochondria. Mol Cancer Ther 6:1814-1822.
53. Maher P, Schubert D (2000) Signaling by reactive oxygen species in the nervous system. Cell Mol Life Sci 57:1287-1305.
54. Mallozzi C, Martire A, Domenici MR, Metere A, Popoli P, Di Stasi AM (2007) L-NAME reverses quinolinic acid-induced toxicity in rat corticostriatal slices: Involvement of src family kinases. J Neurosci Res 85:2770-2777.
55. Maren S (2005) Synaptic mechanisms of associative memory in the amygdala. Neuron 47:783-786.
56. MinamiM (2009) Neuronal mechanisms for pain-induced aversion behavioral studies using a conditioned place aversion test. Int Rev Neurobiol 85:135-144.
57. Myers B, Greenwood-Van Meerveld B (2010) Divergent effects of amygdala glucocorticoid and mineralocorticoid receptors in the regulation of visceral and somatic pain. Am J Physiol Gastrointest Liver Physiol 298: G295-G303.
58. Myers B, Dittmeyer K, Greenwood-Van Meerveld B (2007) Involvement of amygdaloid corticosterone in altered visceral and somatic sensation. Behav Brain Res 181:163-167.
59. Neugebauer V (2007) Glutamate receptor ligands. Handb Exp Pharmacol 177:217-249.
60. Neugebauer V, Li W, Bird GC, Bhave G, Gereau RW 4th (2003) Synaptic plasticity in the amygdala in a model of arthritic pain: differential roles of metabotropic glutamate receptors 1 and 5. J Neurosci 23:52-63.
61. Neugebauer V, Li W, Bird GC, Han JS (2004) The amygdala and persistent pain. Neuroscientist 10:221-234.
62. Neugebauer V, Han JS, Adwanikar H, Fu Y, Ji G (2007) Techniques for assessing knee joint pain in arthritis. Mol Pain 3:8-20.
63. Neugebauer V, Galhardo V, Maione S, Mackey SC (2009) Forebrain pain mechanisms. Brain Res Rev 60:226-242.
64. 3 receptor, attenuates the increase in cytosolic calcium level and degranulation that is induced by antigen in RBL-2H3 mast cells. Br J Pharmacol 135:1959-1966.
65. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. New York: Academic.
66. PedersenLH,Scheel-Krüger J, Blackburn-MunroG (2007) Amygdala GABA-A receptor involvement in mediating sensory-discriminative and affectivemotivational pain responses in a rat model of peripheral nerve injury. Pain 127:17-26.
67. Pernía-Andrade AJ, Kato A, Witschi R, Nyilas R, Katona I, Freund TF, Watanabe M, Filitz J, Koppert W, Schüttler J, Ji G, Neugebauer V, Marsicano G, Lutz B, Vanegas H, Zeilhofer HU (2009) Spinal endocannabinoids and CB1 receptors mediate C-fiber-induced heterosynaptic pain sensitization. Science 325:760-764.
68. Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175-187.
69. Robinson KM, Janes MS, Beckman JS (2008) The selective detection of mitochondrial superoxide by live cell imaging. Nat Protoc 3:941-947.
70. Rudy JW, Matus-Amat P (2009) DHPG activation of group 1 mGluRs in BLA enhances fear conditioning. Learn Mem 16:421-425.
71. Schwaber JS, Sternini C, Brecha NC, Rogers WT, Card JP (1988) Neurons containing calcitonin gene-related peptide in the parabrachial nucleus project to the central nucleus of the amygdala. J Comp Neurol 270: 416-426.
72. Schwartz ES, Lee I, Chung K, Chung JM (2008) Oxidative stress in the spinal cord is an important contributor in capsaicin-induced mechanical secondary hyperalgesia in mice. Pain 138:514-524.
73. Schwartz ES, Kim HY, Wang J, Lee I, Klann E, Chung JM, Chung K (2009) Persistent pain is dependent on spinal mitochondrial antioxidant levels. J Neurosci 29:159-168.
74. Seymour B, Dolan R (2008) Emotion, decision making, and the amygdala. Neuron 58:662-671.
75. Steinmann C, Landsverk ML, Barral JM, Boehning D (2008) Requirement of inositol 1,4,5-trisphosphate receptors for tumor-mediated lymphocyte apoptosis. J Biol Chem 283:13506-13509.
76. TalM (1996) A novel antioxidant alleviates heat hyperalgesia in rats with an experimental painful peripheral neuropathy. Neuroreport 7:1382-1384.
77. Twining CM, Sloane EM, Milligan ED, Chacur M, Martin D, Poole S, Marsh H, Maier SF, Watkins LR (2004) Peri-sciatic proinflammatory cytokines, reactive oxygen species, and complement induce mirror-image neuropathic pain in rats. Pain 110:299-309.
78. Varney MA, Gereau RW 4th (2002) Metabotropic glutamate receptor involvement in models of acute and persistent pain: prospects for the development of novel analgesics. Curr Drug Targets CNS Neurol Disord 1:283-296.
79. Wang ZQ, Porreca F, Cuzzocrea S, Galen K, Lightfoot R, Masini E, Muscoli C, Mollace V, Ndengele M, Ischiropoulos H, Salvemini D (2004) A newly identified role for superoxide in inflammatory pain. J Pharmacol Exp Ther 309:869-878.
80. 2+ release enhances neuroprotection by increasing astrocyte mitochondrial metabolism during aging. J Neurosci 27:6510-6520.
81. + channels in hippocampus involves a mitogen-activated protein kinase pathway. J Neurosci 22:4860-4868.