Retinal cell death induced by TRPV1 activation involves NMDA signaling and upregulation of nitric oxide synthases

Cellular and Molecular Neurobiology

Volumn 33, Issue 3, 2013, Pages 379-392

  Leonelli, Mauro ^a   Martins, Daniel O ^a   Britto, Luiz R G ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Excitotoxicity; Glutamate; Nitric oxide; Nitric oxide synthases; Protein nitration; TRPV1

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4,5 DIAMINOFLUORESCEIN DIACETATE; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; IONOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; NITRIC OXIDE SYNTHASE; VANILLOID RECEPTOR 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; DNA FRAGMENTATION; ENZYME ACTIVITY; ENZYME SYNTHESIS; LIPID PEROXIDATION; NERVE CELL; NITRATION; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN NITRATION; RAT; RETINA BIPOLAR GANGLION CELL; RETINA BLOOD VESSEL; RETINA CELL; SIGNAL TRANSDUCTION; UPREGULATION;

ALDEHYDES; ANIMALS; CELL DEATH; DNA FRAGMENTATION; ION CHANNEL GATING; LIPID PEROXIDATION; MALE; N-METHYLASPARTATE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; NITROSATION; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; RETINA; SIGNAL TRANSDUCTION; TRPV CATION CHANNELS; TYROSINE; UP-REGULATION;

EID: 84876670483     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-012-9904-5     Document Type: Article

References (92)

1. Abu El-Asrar AM, Desmet S, Meersschaert A et al (2001) Expression of the inducible isoform of nitric oxide synthase in the retinas of human subjects with diabetes mellitus. Am J Ophthalmol 132:551-556
2. Akerman S, Kaube H, Goadsby PJ (2004) Anandamide acts as a vasodilator of dural blood vessels in vivo by activating TRPV1 receptors. Br J Pharmacol 142:1354-1360
3. Alawi K, Keeble J (2010) The paradoxical role of the transient receptor potential vanilloid 1 receptor in inflammation. Pharmacol Ther 125:181-195
4. Amantini C, Mosca M, Nabissi M et al (2007) Capsaicin-induced apoptosis of glioma cells is mediated by TRPV1 vanilloid receptor and requires p38 MAPK activation. J Neurochem 102:977-990
5. Arundine M, Tymianski M (2003) Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 34:325-337
6. Aslan M, Cort A, Yucel I (2008) Oxidative and nitrative stress markers in glaucoma. Free Radic Biol Med 45:367-376
7. Bal-Price A, Brown GC (2001) Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J Neurosci 21:6480-6491
8. Bal-Price A, Matthias A, Brown GC (2002) Stimulation of the NADPH oxidase in activated rat microglia removes nitric oxide but induces peroxynitrite production. J Neurochem 80:73-80
9. Bandyopadhyay A, Chakder S, Rattan S (1997) Regulation of inducible and neuronal nitric oxide synthase gene expression by interferon-gamma and VIP. Am J Physiol 272:C1790-C1797
10. Beal MF (1992) Mechanisms of excitotoxicity in neurologic diseases. FASEB J 6:3338-3344
11. Beckman JS, Beckman TW, Chen J et al (1990) Apparent hydroxyl radical production by peroxynitrite - implications for endothelial injury from nitric-oxide and superoxide. Proc Natl Acad Sci USA 87:1620-1624
12. Bisset GW, Lewis GP (1962) A spectrum of pharmacological activity in some biologically active peptides. Br J Pharmacol Chemother 19:168-182
13. Blute TA, Lee MR, Eldred WD (2000) Direct imaging of NMDA-stimulated nitric oxide production in the retina. Vis Neurosci 17:557-566
14. Bredt DS, Hwang PM, Snyder SH (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347:768-770
15. Brown GC, Cooper CE (1994) Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett 356:295-298
16. Brown GC, Neher JJ (2010) Inflammatory neurodegeneration and mechanisms of microglial killing of neurons. Mol Neurobiol 41:242-247
17. Caterina MJ, Schumacher MA, Tominaga M et al (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824
18. Chakravarthy U, Stitt AW, McNally J et al (1995) Nitric oxide synthase activity and expression in retinal capillary endothelial cells and pericytes. Curr Eye Res 14:285-294
19. Chu CJ, Huang SM, De Petrocellis L et al (2003) N-Oleoyldopamine, a novel endogenous capsaicin-like lipid that produces hyperalgesia. J Biol Chem 278:13633-13639
20. Corradin SB, Mauel J, Donini SD et al (1993) Inducible nitric oxide synthase activity of cloned murine microglial cells. Glia 7:255-262
21. Dedov VN, Roufogalis BD (2000) Mitochondrial calcium accumulation following activation of vanilloid (VR1) receptors by capsaicin in dorsal root ganglion neurons. Neuroscience 95:183-188
22. del Zoppo GJ (2006) Stroke and neurovascular protection. N Engl J Med 354:553-555
23. Du Y, Hirooka K, Miyamoto O et al (2008) Both amacrine and bipolar cells release glutamate in the rat retina after ischemia/reperfusion insult in vitro. Curr Eye Res 33:782-788
24. El-Remessy AB, Khalil IE, Matragoon S et al (2003) Neuroprotective effect of (-)Delta9-tetrahydrocannabinol and cannabidiol in N-methyl-d-aspartate- induced retinal neurotoxicity: involvement of peroxynitrite. Am J Pathol 163:1997-2008
25. Forder JP, Tymianski M (2009) Postsynaptic mechanisms of excitotoxicity: involvement of postsynaptic density proteins, radicals, and oxidant molecules. Neuroscience 158:293-300
26. Garthwaite J (2008) Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci 27:2783-2802
27. Garthwaite J, Charles SL, Chess-Williams R (1988) Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336:385-388
28. Gaspar MN, Ribeiro CA, Cunha-Vaz JG et al (2004) Effects of neuropeptides on the sumatriptan-disturbed circulation in the optic nerve head of rabbits. Pharmacology 70:152-159
29. Geller DA, Billiar TR (1998) Molecular biology of nitric oxide synthases. Cancer Metastasis Rev 17:7-23
30. Geppetti P, Trevisani M (2004) Activation and sensitisation of the vanilloid receptor: role in gastrointestinal inflammation and function. Br J Pharmacol 141:1313-1320
31. Hardingham GE, Bading H (2010) Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 11:682-696
32. Haverkamp S, Wassle H (2000) Immunocytochemical analysis of the mouse retina. J Comp Neurol 424:1-23
33. Huang SM, Bisogno T, Trevisani M et al (2002) An endogenous capsaicin-like substance with high potency at recombinant and native vanilloid VR1 receptors. Proc Natl Acad Sci USA 99:8400-8405
34. Ientile R, Picciurro V, Pedale S et al (1996) Nitric oxide enhances amino acid release from immature chick embryo retina. Neurosci Lett 219:79-82
35. Jin YH, Bailey TW, Li BY et al (2004) Purinergic and vanilloid receptor activation releases glutamate from separate cranial afferent terminals in nucleus tractus solitarius. J Neurosci 24:4709-4717
36. Johnson TV, Martin KR (2008) Development and characterization of an adult retinal explant organotypic tissue culture system as an in vitro intraocular stem cell transplantation model. Invest Ophthalmol Vis Sci 49:3503-3512
37. Jung JE, Kim GS, Narasimhan P et al (2009) Regulation of Mn-superoxide dismutase activity and neuroprotection by STAT3 in mice after cerebral ischemia. J Neurosci 29:7003-7014
38. Kermer P, Klocker N, Weishaupt JH et al (2001) Transection of the optic nerve in rats: studying neuronal death and survival in vivo. Brain Res Brain Res Protoc 7:255-260
39. Kim SR, Kim SU, Oh U et al (2006) Transient receptor potential vanilloid subtype 1 mediates microglial cell death in vivo and in vitro via Ca2+-mediated mitochondrial damage and cytochrome c release. J Immunol 177:4322-4329
40. Koeberle PD, Ball AK (1999) Nitric oxide synthase inhibition delays axonal degeneration and promotes the survival of axotomized retinal ganglion cells. Exp Neurol 158:366-381
41. Kojima H, Nakatsubo N, Kikuchi K et al (1998) Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Anal Chem 70:2446-2453
42. Leonelli M, Martins DO, Kihara AH et al (2009) Ontogenetic expression of the vanilloid receptors TRPV1 and TRPV2 in the rat retina. Int J Dev Neurosci 27:709-718
43. Leonelli M, Martins DO, Britto LR (2010) TRPV1 receptors are involved in protein nitration and Muller cell reaction in the acutely axotomized rat retina. Exp Eye Res 91:755-768
44. Leonelli M, Martins DO, Britto LR (2011) TRPV1 receptors modulate retinal development. Int J Dev Neurosci 29:405-413
45. Li DP, Chen SR, Pan HL (2004) VR1 receptor activation induces glutamate release and postsynaptic firing in the paraventricular nucleus. J Neurophysiol 92:1807-1816
46. Lilja J, Lindegren H, Forsby A (2007) Surfactant-induced TRPV1 activity-a novel mechanism for eye irritation? Toxicol Sci 99:174-180
47. Liu B, Neufeld AH (2000) Expression of nitric oxide synthase-2 (NOS-2) in reactive astrocytes of the human glaucomatous optic nerve head. Glia 30:178-186
48. Maccarrone M, Rossi S, Bari M et al (2008) Anandamide inhibits metabolism and physiological actions of 2-arachidonoylglycerol in the striatum. Nat Neurosci 11:152-159
49. Macho A, Calzado MA, Munoz-Blanco J et al (1999) Selective induction of apoptosis by capsaicin in transformed cells: the role of reactive oxygen species and calcium. Cell Death Differ 6:155-165
50. Marella M, Chabry J (2004) Neurons and astrocytes respond to prion infection by inducing microglia recruitment. J Neurosci 24:620-627
51. Marinelli S, Di Marzo V, Berretta N et al (2003) Presynaptic facilitation of glutamatergic synapses to dopaminergic neurons of the rat substantia nigra by endogenous stimulation of vanilloid receptors. J Neurosci 23:3136-3144
52. Medvedeva YV, Kim MS, Usachev YM (2008) Mechanisms of prolonged presynaptic Ca2+ signaling and glutamate release induced by TRPV1 activation in rat sensory neurons. J Neurosci 28:5295-5311
53. Metea MR, Newman EA (2007) Signalling within the neurovascular unit in the mammalian retina. Exp Physiol 92:635-640
54. Morgans CW, Zhang J, Jeffrey BG et al (2009) TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells. Proc Natl Acad Sci USA 106:19174-19178
55. Mozaffarieh M, Grieshaber MC, Flammer J (2008) Oxygen and blood flow: players in the pathogenesis of glaucoma. Mol Vis 14:224-233
56. Murphy TH, Miyamoto M, Sastre A et al (1989) Glutamate toxicity in a neuronal cell line involves inhibition of cystine transport leading to oxidative stress. Neuron 2:1547-1558
57. Musella A, De Chiara V, Rossi S et al (2009) TRPV1 channels facilitate glutamate transmission in the striatum. Mol Cell Neurosci 40:89-97
58. Neufeld AH, Sawada A, Becker B (1999) Inhibition of nitric-oxide synthase 2 by aminoguanidine provides neuroprotection of retinal ganglion cells in a rat model of chronic glaucoma. Proc Natl Acad Sci USA 96:9944-9948
59. Nguyen D, Alavi MV, Kim KY et al (2011) A new vicious cycle involving glutamate excitotoxicity, oxidative stress and mitochondrial dynamics. Cell Death Dis 2:e240
60. Nucci C, Gasperi V, Tartaglione R et al (2007) Involvement of the endocannabinoid system in retinal damage after high intraocular pressure-induced ischemia in rats. Invest Ophthalmol Vis Sci 48:2997-3004
61. Palazzo E, de Novellis V, Marabese I et al (2002) Interaction between vanilloid and glutamate receptors in the central modulation of nociception. Eur J Pharmacol 439:69-75
62. Poblete IM, Orliac ML, Briones R et al (2005) Anandamide elicits an acute release of nitric oxide through endothelial TRPV1 receptor activation in the rat arterial mesenteric bed. J Physiol 568:539-551
63. Premkumar LS, Ahern GP (2000) Induction of vanilloid receptor channel activity by protein kinase C. Nature 408:985-990
64. Qiao S, Li W, Tsubouchi R et al (2005) Involvement of peroxynitrite in capsaicin-induced apoptosis of C6 glioma cells. Neurosci Res 51:175-183
65. Rego AC, Oliveira CR (2003) Mitochondrial dysfunction and reactive oxygen species in excitotoxicity and apoptosis: implications for the pathogenesis of neurodegenerative diseases. Neurochem Res 28:1563-1574
66. Ritter S, Dinh TT (1990) Capsaicin-induced neuronal degeneration in the brain and retina of preweanling rats. J Comp Neurol 296:447-461
67. Ryskamp DA, Witkovsky P, Barabas P et al (2012) The polymodal ion channel transient receptor potential vanilloid 4 modulates calcium flux, spiking rate, and apoptosis of mouse retinal ganglion cells. J Neurosci 31:7089-7101
68. Sappington RM, Calkins DJ (2008) Contribution of TRPV1 to microglia-derived IL-6 and NFkappaB translocation with elevated hydrostatic pressure. Invest Ophthalmol Vis Sci 49:3004-3017
69. Sappington RM, Sidorova T, Long DJ et al (2009) TRPV1: contribution to retinal ganglion cell apoptosis and increased intracellular Ca2+ with exposure to hydrostatic pressure. Invest Ophthalmol Vis Sci 50:717-728
70. Schilling T, Eder C (2009) Importance of the non-selective cation channel TRPV1 for microglial reactive oxygen species generation. J Neuroimmunol 216(1-2):118-121
71. Shen Y, Heimel JA, Kamermans M et al (2009) A transient receptor potential-like channel mediates synaptic transmission in rod bipolar cells. J Neurosci 29:6088-6093
72. Shirakawa H, Yamaoka T, Sanpei K et al (2008) TRPV1 stimulation triggers apoptotic cell death of rat cortical neurons. Biochem Biophys Res Commun 377:1211-1215
73. Sikand P, Premkumar LS (2007) Potentiation of glutamatergic synaptic transmission by protein kinase C-mediated sensitization of TRPV1 at the first sensory synapse. J Physiol 581:631-647
74. Smart D, Gunthorpe MJ, Jerman JC et al (2000) The endogenous lipid anandamide is a full agonist at the human vanilloid receptor (hVR1). Br J Pharmacol 129:227-230
75. Starowicz K, Maione S, Cristino L et al (2007) Tonic endovanilloid facilitation of glutamate release in brainstem descending antinociceptive pathways. J Neurosci 27:13739-13749
76. Szallasi A, Blumberg PM (1990) Resiniferatoxin and its analogs provide novel insights into the pharmacology of the vanilloid (capsaicin) receptor. Life Sci 47:1399-1408
77. Szolcsanyi J (2004) Forty years in capsaicin research for sensory pharmacology and physiology. Neuropeptides 38:377-384
78. Thomas KC, Sabnis AS, Johansen ME et al (2007) Transient receptor potential vanilloid 1 agonists cause endoplasmic reticulum stress and cell death in human lung cells. J Pharmacol Exp Ther 321:830-838
79. Thomas KC, Roberts JK, Deering-Rice CE et al (2012) Contributions of TRPV1, endovanilloids, and endoplasmic reticulum stress in lung cell death in vitro and lung injury. Am J Physiol Lung Cell Mol Physiol 302:L111-L119
80. Thoreson WB, Witkovsky P (1999) Glutamate receptors and circuits in the vertebrate retina. Prog Retin Eye Res 18:765-810
81. Tominaga M, Caterina MJ (2004) Thermosensation and pain. J Neurobiol 61:3-12
82. Toth A, Boczan J, Kedei N et al (2005) Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res Mol Brain Res 135:162-168
83. Vellani V, Mapplebeck S, Moriondo A et al (2001) Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. J Physiol 534:813-825
84. Venturini CM, Knowles RG, Palmer RM et al (1991) Synthesis of nitric oxide in the bovine retina. Biochem Biophys Res Commun 180:920-925
85. Vidal L, Diaz F, Villena A et al (2006) Nitric oxide synthase in retina and optic nerve head of rat with increased intraocular pressure and effect of timolol. Brain Res Bull 70:406-413
86. Vriens J, Appendino G, Nilius B (2009) Pharmacology of vanilloid transient receptor potential cation channels. Mol Pharmacol 75:1262-1279
87. Westlund KN, Kochukov MY, Lu Y et al (2010) Impact of central and peripheral TRPV1 and ROS levels on proinflammatory mediators and nociceptive behavior. Mol Pain 6:46
88. Ye XD, Laties AM, Stone RA (1990) Peptidergic innervation of the retinal vasculature and optic nerve head. Invest Ophthalmol Vis Sci 31:1731-1737
89. Zeevalk GD, Nicklas WJ (1994) Nitric oxide in retina: relation to excitatory amino acids and excitotoxicity. Exp Eye Res 58:343-350
90. Zeevalk GD, Schoepp D, Nicklas WJ (1995) Excitotoxicity at both NMDA and non-NMDA glutamate receptors is antagonized by aurintricarboxylic acid: evidence for differing mechanisms of action. J Neurochem 64:1749-1758
91. Zschenderlein C, Gebhardt C, von Bohlen Und Halbach O et al (2011) Capsaicin-induced changes in LTP in the lateral amygdala are mediated by TRPV1. PLoS One 6:e16116
92. Zygmunt PM, Petersson J, Andersson DA et al (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400:452-457