Sepiapterin attenuates 1-methyl-4-phenylpyridinium-induced apoptosis in neuroblastoma cells transfected with neuronal NOS: Role of tetrahydrobiopterin, nitric oxide, and proteasome activation

Free Radical Biology and Medicine

Volumn 39, Issue 8, 2005, Pages 1059-1074

  Shang, Tiesong ^a   Kotamraju, Srigiridhar ^a   Zhao, Hongtao ^a   Kalivendi, Shasi V ^a   Hillard, Cecilia J ^b   Kalyanaraman, B ^a  

^a FREE RADICAL RESEARCH CENTER   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Free radicals; Nitric oxide; Parkinson disease; Proteasome; Superoxide; Ubiquitination

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; 1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; NEUROTOXIN; NITRIC OXIDE SYNTHASE; PROTEASOME; PROTEIN; SEPIAPTERIN; SUPEROXIDE; TETRAHYDROBIOPTERIN;

ARTICLE; CELL LINE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; UBIQUITINATION; WILD TYPE;

1-METHYL-4-PHENYLPYRIDINIUM; ACONITATE HYDRATASE; APOPTOSIS; BIOPTERIN; DIMERIZATION; ELECTRON TRANSPORT COMPLEX I; ENZYME ACTIVATION; HUMANS; NEUROBLASTOMA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; PROTEASOME ENDOPEPTIDASE COMPLEX; PTERINS; SUPEROXIDES; TRANSFECTION; TUMOR CELLS, CULTURED;

ANIMALIA;

EID: 25144483746     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2005.05.022     Document Type: Article

References (60)

1. T.M. Dawson, and V.L. Dawson Molecular pathways of neurodegeneration in Parkinson's disease Science 302 2003 819 822
2. R.S. Burns, C.C. Chiueh, S.P. Markey, M.H.E. Ebert, D.M. Jacobowitz, and I.J. Kopin A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine Proc. Natl. Acad. Sci. USA 80 1984 4546 4550
3. J.A. Javitch, R.J. D'Amato, S.M. Strittmatter, and S.H. Snyder Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine: uptake of the metabolite N-methyl-4-phenylpyridine by dopamine neurons explains selective toxicity Proc. Natl. Acad. Sci. USA 82 1985 2173 2177
4. H. Mochizuki, H. Imai, K. Endo, K. Yokomizo, Y. Murata, N. Hattori, and Y. Mizuno Iron accumulation in the substantia nigra of 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine (MPTP)-induced hemiparkinsonian monkeys Neurosci. Lett. 168 1994 251 253
5. J. Lan, and D.H. Jiang Excessive iron accumulation in the brain: a possible potential risk of neurodegeneration in Parkinson's disease J. Neural Transm. 104 1997 649 660
6. P. Rauhala, A.M. Lin, and C.C. Chiueh Neuroprotection by S-nitrosoglutathione of brain dopamine neurons from oxidative stress FASEB J. 12 1998 165 173
7. S. Kotamraju, C.R. Chitambar, S.V. Kalivendi, J. Joseph, and B. Kalyanaraman Transferrin receptor-dependent iron uptake is responsible for doxorubicin-mediated apoptosis in endothelial cells: role of oxidant-induced iron signaling in apoptosis J. Biol. Chem. 277 2002 17179 17187
8. Z.M. Qian, Y.M. Pu, P.L. Tang, and Q. Wang Transferrin-bound iron uptake by the cultured cerebellar granule cells Neurosci. Lett. 251 1998 9 12
9. +)-induced apoptosis and mitochondrial oxidant generation: role of transferrin-receptor-dependent iron and hydrogen peroxide Biochem. J. 371 2003 151 164
10. D. Kaur, F. Yantiri, S. Rajagopalan, J. Kumar, J.Q. Mo, R. Boonplueang, V. Viswanath, R. Jacobs, L. Yang, M.F. Beal, D. DiMonte, I. Volitaskis, L. Ellerby, R.A. Cherny, A.I. Bush, and J.K. Andersen Genetic or pharmacological iron chelation prevents MPTP-induced neurotoxicity in vivo: a novel therapy for Parkinson's disease Neuron 37 2003 899 909
11. S. Przedborski, V. Jackson-Lewis, R. Yokoyama, T. Shibata, V.L. Dawson, and T.M. Dawson Role of neuronal nitric oxide in 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine (MPTP)-induced dopaminergic neurotoxicity Proc. Natl. Acad. Sci. USA 93 1996 4565 4571
12. G.M. Mackenzie, M.J. Jackson, P. Jenner, and C.D. Marsden Nitric oxide synthase inhibition and MPTP-induced toxicity in the common marmoset Synapse 26 1997 301 316
13. +-treated rat was not prevented by treatments with nitric oxide synthase or poly(ADP-ribose) polymerase inhibitors Neurosci. Lett. 314 2001 82 86
14. K.P. Mohanakumar, B. Thomas, S.M. Sharma, D. Muralikrishnan, R. Chowdhury, and C.C. Chiueh Nitric oxide: an antioxidant and neuroprotector Ann. N. Y. Acad. Sci. 962 2002 389 401
15. M.A. Tayeh, and M.A. Marletta Macrophage oxidation of l-arginine to nitric oxide, nitrite, and nitrate: tetrahydrobiopterin is required as a cofactor J. Biol. Chem. 264 1989 19654 19658
16. J. Vasquez-Vivar, N. Hogg, P. Martasek, H. Karoui, K.A. Pritchard Jr., and B. Kalyanaraman Tetrahydrobiopterin-dependent inhibition of superoxide generation from neuronal nitric oxide synthase J. Biol. Chem. 274 1999 26736 26742
17. M.A. Kuiper, J.J. Visser, P.L. Bergmans, P. Scheltens, and E.C. Wolters Decreased cerebrospinal fluid nitrate levels in Parkinson's disease, Alzheimer's disease and multiple system atrophy patients J. Neurol. Sci. 121 1994 46 49
18. W. Lovenberg, R.A. Levine, D.S. Robinson, M. Ebert, A.C. Williams, and D.B. Calne Hydroxylase cofactor activity in cerebrospinal fluid of normal subjects and patients with Parkinson's disease Science 204 1979 624 626
19. T. Shang, S. Kotamraju, S.V. Kalivendi, C.J. Hillard, and B. Kalyanaraman 1-Methyl-4-phenylpyridinium-induced apoptosis in cerebellar granule neurons is mediated by transferrin receptor iron-dependent depletion of tetrahydrobiopterin and neuronal nitric-oxide synthase-derived superoxide J. Biol. Chem. 279 2004 19099 19112
20. A.M. Lin Recovery by NO of the iron-attenuated dopamine dynamics in nigrostriatal system of rat brain Neurosci. Res. 34 1999 133 139
21. N.V. Gorbunov, J.C. Yalowich, A. Gaddam, P. Thampatty, V.B. Ritov, E.R. Kisin, N.M. Elsayed, and V.E. Kagan Nitric oxide prevents oxidative damage produced by tert-butyl hydroperoxide in erythroleukemia cells via nitrosylation of heme and non-heme iron: electron paramagnetic resonance evidence J. Biol. Chem. 272 1997 12328 12341
22. 2-induced transferrin receptor-dependent apoptosis in endothelial cells: role of ubiquitin-proteasome pathway Proc. Natl. Acad. Sci. USA 100 2003 10653 10658
23. S.Y. Ryu, K.S. Jeong, B.N. Kang, S.J. Park, W.K. Yoon, S.H. Kim, and T.H. Kim Modulation of transferrin synthesis, transferrin receptor expression, iNOS expression and NO production in mouse macrophages by cytokines, either alone or in combination Anticancer Res. 20 2000 3331 3338
24. C.J. Hillard, S. Muthian, and C.S. Kearn Effects of CB(1) cannabinoid receptor activation on cerebellar granule cell nitric oxide synthase activity FEBS Lett. 459 1999 277 281
25. M.C. Kennedy, M.H. Emptage, J.L. Dreyer, and H. Beinert The role of iron in the activation-inactivation of aconitase J. Biol. Chem. 258 1983 11098 11105
26. H.C. Yen, T.D. Oberley, C.G. Gairola, L.I. Szweda, and D.K. St. Clair Manganese superoxide dismutase protects mitochondrial complex I against adriamycin-induced cardiomyopathy in transgenic mice Arch. Biochem. Biophys. 362 1999 59 66
27. P. Klatt, K. Schmidt, D. Lehner, O. Glatter, H.P. Bachinger, and B. Mayer Structural analysis of porcine brain nitric oxide synthase reveals a role for tetrahydrobiopterin and l-arginine in the formation of an SDS-resistant dimer EMBO J. 14 1995 3687 3695
28. H. Zhao, S. Kalivendi, H. Zhang, J. Joseph, K. Nithipatikom, J. Vasquez-Vivar, and B. Kalyanaraman Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide Free Radic. Biol. Med. 34 2003 1359 1368
29. J. Vasquez-Vivar, J. Whitsett, P. Martasek, N. Hogg, and B. Kalyanaraman Reaction of tetrahydrobiopterin with superoxide: EPR-kinetic analysis and characterization of the pteridine radical Free Radic. Biol. Med. 31 2001 975 985
30. E. Ciani, S. Guidi, R. Bartesaghi, and A. Contestabile Nitric oxide regulates cGMP-dependent cAMP-responsive element binding protein phosphorylation and Bcl-2 expression in cerebellar neurons: implication for a survival role of nitric oxide J. Neurochem. 82 2002 1282 1289
31. +-induced apoptosis in neuroblastoma cells: intermediacy of transferrin receptor iron and hydrogen peroxide J. Biol. Chem. 279 2004 15240 15247
32. G.U. Hoglinger, G. Carrard, P.P. Michel, F. Medja, A. Lombes, M. Ruberg, B. Friguet, and E.C. Hirsch Dysfunction of mitochondrial complex I and the proteasome: interactions between two biochemical deficits in a cellular model of Parkinson's disease J. Neurochem. 86 2003 1297 1307
33. H.J. Rideout, and L. Stefanis Proteasomal inhibition-induced inclusion formation and death in cortical neurons require transcription and ubiquitination Mol. Cell. Neurosci. 21 2002 223 238
34. M.H. Zou, C. Shi, and R.A. Cohen Oxidation of the zinc-thiolate complex and uncoupling of endothelial nitric oxide synthase by peroxynitrite J. Clin. Invest. 109 2002 817 826
35. B. Thony, G. Auerbach, and N. Blau Tetrahydrobiopterin biosynthesis, regeneration and functions Biochem. J. 347 2000 1 16
36. A. Reif, L.G. Frohlich, P. Kotsonis, A. Frey, H.M. Bommel, D.A. Wink, W. Pfleiderer, and H.H. Schmidt Tetrahydrobiopterin inhibits monomerization and is consumed during catalysis in neuronal NO synthase J. Biol. Chem. 274 1999 24921 24929
37. C.P. Tiefenbacher, W.M. Chilian, M. Mitchell, and D.V. DeFily Restoration of endothelium-dependent vasodilation after reperfusion injury by tetrahydrobiopterin Circulation 94 1996 1423 1429
38. S. Cho, B.T. Volpe, Y. Bae, O. Hwang, H.J. Choi, J. Gal, L.C. Park, C.K. Chu, J. Du, and T.H. Joh Blockade of tetrahydrobiopterin synthesis protects neurons after transient forebrain ischemia in rat: a novel role for the cofactor J. Neurosci. 19 1999 878 889
39. S.M. Day, D. Duquaine, L.V. Mundada, R.G. Menon, B.V. Khan, S. Rajagopalan, and W.P. Fay Chronic iron administration increases vascular oxidative stress and accelerates arterial thrombosis Circulation 107 2003 2601 2606
40. M. Pannirselvam, S. Verma, T.J. Anderson, and C.R. Triggle Cellular basis of endothelial dysfunction in small mesenteric arteries from spontaneously diabetic (db/db -/-) mice: role of decreased tetrahydrobiopterin bioavailability Br. J. Pharmacol. 136 2002 255 263
41. F. Coria, I. Rubio, and C. Bayon Alzheimer's disease, beta-amyloidosis, and aging Rev. Neurosci. 5 1994 275 292
42. P.A. Temussi, L. Masino, and A. Pastore From Alzheimer to Huntington: why is a structural understanding so difficult? EMBO J. 22 2003 355 361
43. T. Kitada, S. Asakawa, N. Hattori, H. Matsumine, Y. Yamamura, S. Minoshima, M. Yokochi, Y. Mizuno, and N. Shimizu Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism Nature 392 1998 605 608
44. G.G. Mason, K.B. Hendil, and A.J. Rivett Phosphorylation of proteasomes in mammalian cells: identification of two phosphorylated subunits and the effect of phosphorylation on activity Eur. J. Biochem. 238 1996 453 462
45. J.C. de la Torre, and G.B. Stefano Evidence that Alzheimer's disease is a microvascular disorder: the role of constitutive nitric oxide Brain Res. Brain Res. Rev. 34 2000 119 136
46. G. Venturini, M. Colasanti, T. Persichini, E. Fioravanti, P. Ascenzi, L. Palomba, O. Cantoni, and G. Musci Beta-amyloid inhibits NOS activity by subtracting NADPH availability FASEB J. 16 2002 1970 1972
47. F. Tao, Y.X. Tao, C. Zhao, S. Dore, W.J. Liaw, S.N. Raja, and R.A. Johns Differential roles of neuronal and endothelial nitric oxide synthases during carrageenan-induced inflammatory hyperalgesia Neuroscience 128 2004 421 430
48. T.J. O'Dell, P.L. Huang, T.M. Dawson, J.L. Dinerman, S.H. Snyder, E.R. Kandel, and M.C. Fishman Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS Science 265 1994 542 546
49. S.A. Khan, K. Lee, K.M. Minhas, D.R. Gonzalez, S.V. Raju, A.D. Tejani, D. Li, D.E. Berkowitz, and J.M. Hare Neuronal nitric oxide synthase negatively regulates xanthine oxidoreductase inhibition of cardiac excitation-contraction coupling Proc. Natl. Acad. Sci. USA 101 2004 15944 15948
50. R. Bockelmann, G. Wolf, G. Ransmayr, and P. Riederer NADPH-diaphorase/ nitric oxide synthase containing neurons in normal and Parkinson's disease putamen J. Neural Transm. Parkinson Dis. Dement. Sect. 7 1994 115 121
51. G. Sancesario, M. Morello, A. Reiner, P. Giacomini, R. Massa, S. Schoen, and G. Bernardi Nitrergic neurons make synapses on dual-input dendritic spines of neurons in the cerebral cortex and the striatum of the rat: implication for a postsynaptic action of nitric oxide Neuroscience 99 2000 627 642
52. A.R. West, and A.A. Grace The nitric oxide-guanylyl cyclase signaling pathway modulates membrane activity states and electrophysiological properties of striatal medium spiny neurons recorded in vivo J. Neurosci. 24 2004 1924 1935
53. M.S. Starr, and B.S. Starr Do NMDA receptor-mediated changes in motor behaviour involve nitric oxide? Eur. J. Pharmacol. 272 1995 211 217
54. H.L. Klawans, R.W. Stein, C.M. Tanner, and C.G. Goetz A pure parkinsonian syndrome following acute carbon monoxide intoxication Arch. Neurol. 39 1982 302 304
55. V.S. Sharma, and D. Magde Activation of soluble guanylate cyclase by carbon monoxide and nitric oxide: a mechanistic model Methods 19 1999 494 505
56. M. Hernandez-Viadel, A.F. Castoldi, T. Coccini, L. Manzo, S. Erceg, and V. Felipo In vivo exposure to carbon monoxide causes delayed impairment of activation of soluble guanylate cyclase by nitric oxide in rat brain cortex and cerebellum J. Neurochem. 89 2004 1157 1165
57. J.B. Gramsbergen, M. Sandberg, A. Moller Dall, B. Kornblit, and J. Zimmer Glutathione depletion in nigrostriatal slice cultures: GABA loss, dopamine resistance and protection by the tetrahydrobiopterin precursor sepiapterin Brain Res. 935 2002 47 58
58. K. Nakamura, D.A. Wright, T. Wiatr, D. Kowlessur, S. Milstien, X.G. Lei, and U.J. Kang Preferential resistance of dopaminergic neurons to the toxicity of glutathione depletion is independent of cellular glutathione peroxidase and is mediated by tetrahydrobiopterin J. Neurochem. 74 2000 2305 2314
59. S. Kikuchi, K. Shinpo, S. Tsuji, M. Takeuchi, S. Yamagishi, Z. Makita, M. Niino, I. Yabe, and K. Tashiro Effect of proteasome inhibitor on cultured mesencephalic dopaminergic neurons Brain Res. 964 2003 228 236
60. J.T. Madsen, P. Jansen, C. Hesslinger, M. Meyer, J. Zimmer, and J.B. Gramsbergen Tetrahydrobiopterin precursor sepiapterin provides protection against neurotoxicity of 1-methyl-4-phenylpyridinium in nigral slice cultures J. Neurochem. 85 2003 214 223