Role of oxidative stress in methamphetamine-induced dopaminergic toxicity mediated by protein kinase Cδ

Behavioural Brain Research

Volumn 232, Issue 1, 2012, Pages 98-113

  Shin, Eun Joo ^a   Duong, Chu Xuan ^a,h   Nguyen, Xuan Khanh Thi ^a   Li, Zhengyi ^a   Bing, Guoying ^b   Bach, Jae Hyung ^a   Park, Dae Hun ^a   Nakayama, Keiichi ^c   Ali, Syed F ^d   Kanthasamy, Anumantha G ^e   Cadet, Jean Lud ^f   Nabeshima, Toshitaka ^g   Kim, Hyoung Chun ^a  

^a Kangwon National University   (South Korea)

^b UNIVERSITY OF KENTUCKY   (United States)

^c KYUSHU UNIVERSITY   (Japan)

^d CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^e IOWA STATE UNIVERSITY   (United States)

^f NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^g MEIJO UNIVERSITY   (Japan)

^h Cantho University of Medicine and Pharmacy   (Viet Nam)

Author keywords

Dopamine; Methamphetamine; Oxidative stress; PKC isozymes; PKC gene deletion; Rottlerin

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; DOPAMINE; DOPAMINE TRANSPORTER; HISPIDIN; METHAMPHETAMINE; PROTEIN KINASE C BETA INHIBITOR; PROTEIN KINASE C DELTA; ROTTLERIN; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; VESICULAR MONOAMINE TRANSPORTER 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; DOPAMINE METABOLISM; DOPAMINERGIC SYSTEM; ENZYME INHIBITION; KNOCKOUT MOUSE; LIPID PEROXIDATION; MALE; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM;

ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; CENTRAL NERVOUS SYSTEM STIMULANTS; DOPAMINE; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INFUSIONS, INTRAVENTRICULAR; ISOENZYMES; MALE; MALONDIALDEHYDE; METHAMPHETAMINE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; OXIDATIVE STRESS; POSTURAL BALANCE; PROTEIN CARBONYLATION; PROTEIN KINASE C-DELTA; PROTEIN KINASE INHIBITORS; SYNAPTOSOMES; TYROSINE 3-MONOOXYGENASE;

EID: 84860218414     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.04.001     Document Type: Article

References (106)

1. Krasnova I.N., Cadet J.L. Methamphetamine toxicity and messengers of death. Brain Research Reviews 2009, 60:379-407.
2. United Nations Office on Drugs and Crime. World drug report. Analysis. Vienna: United Nations Office on Drugs and Crime; 2007.
3. Albertson T.E., Derlet R.W., Van Hoozen B.E. Methamphetamine and the expanding complications of amphetamines. Western Journal of Medicine 1999, 170:214-219.
4. Scott J.C., Woods S.P., Matt G.E., Meyer R.A., Heaton R.K., Atkinson J.H., et al. Neurocognitive effects of methamphetamine: a critical review and meta-analysis. Neuropsychology Review 2007, 17:275-297.
5. Darke S., Kaye S., McKetin R., Duflou J. Major physical and psychological harms of methamphetamine use. Drug and Alcohol Review 2008, 27:253-262.
6. Perez J.A., Arsura E.L., Strategos S. Methamphetamine-related stroke: four cases. Journal of Emergency Medicine 1999, 17:469-471.
7. Kim H.C., Jhoo W.K., Choi D.Y., Im D.H., Shin E.J., Suh J.H., et al. Protection of methamphetamine nigrostriatal toxicity by dietary selenium. Brain Research 1999, 851:76-86.
8. Davidson C., Gow A.J., Lee T.H., Ellinwood E.H. Methamphetamine neurotoxicity: necrotic and apoptotic mechanisms and relevance to human abuse and treatment. Brain Research 2001, 36:1-22.
9. Shin E.J., Duong C.X., Nguyen T.X., Bing G., Bach J.H., Park D.H., et al. PKCδ inhibition enhances tyrosine hydroxylase phosphorylation in mice after methamphetamine treatment. Neurochemistry International 2011, 59:39-50.
10. Gold M.S., Kobeissy F.H., Wang K.K., Merlo L.J., Bruijnzeel A.W., Krasnova I.N., et al. Methamphetamine- and trauma-induced brain injuries: comparative cellular and molecular neurobiological substrates. Biological Psychiatry 2009, 66:118-127.
11. Cadet J.L., Krasnova I.N., Ladenheim B., Cai N.S., McCoy M.T., Atianjoh F.E. Methamphetamine preconditioning: differential protective effects on monoaminergic systems in the rat brain. Neurotoxicity Research 2009, 15:252-259.
12. Thomas D.M., Walker P.D., Benjamins J.A., Geddes T.J., Kuhn D.M. Methamphetamine neurotoxicity in dopamine nerve endings of the striatum is associated with microglial activation. Journal of Pharmacology and Experimental Therapeutics 2004, 311:1-7.
13. Cadet J.L., Krasnova I.N., Jayanthi S., Lyles J. Neurotoxicity of substituted amphetamines: molecular and cellular mechanisms. Neurotoxicity Research 2007, 11:183-202.
14. Kitamura O., Tokunaga I., Gotohda T., Kubo S. Immunohistochemical investigation of dopaminergic terminal markers and caspase-3 activation in the striatum of human methamphetamine users. International Journal of Legal Medicine 2007, 121:163-168.
15. Moszczynska A., Fitzmaurice P., Ang L., Kalasinsky K.S., Schmunk G.A., Peretti F.J., et al. Why is Parkinsonism not a feature of human methamphetamine users. Brain 2004, 127:363-370.
16. Wilson J.M., Kalasinsky K.S., Levey A.I., Bergeron C., Reiber G., Anthony R.M., et al. Striatal dopamine nerve terminal markers in human, chronic methamphetamine users. Nature Medicine 1996, 2:699-703.
17. LaVoie M.J., Hastings T.G. Dopamine quinone formation and protein modification associated with the striatal neurotoxicity of methamphetamine: evidence against a role for extracellular dopamine. Journal of Neuroscience 1999, 19:1484-1491.
18. Gluck M.R., Moy L.Y., Jayatilleke E., Hogan K.A., Manzino L., Sonsalla P.K. Parallel increases in lipid and protein oxidative markers in several mouse brain regions after methamphetamine treatment. Journal of Neurochemistry 2001, 79:152-160.
19. Jayanthi S., Ladenheim B., Cadet J.L. Methamphetamine-induced changes in antioxidant enzymes and lipid peroxidation in copper/zinc-superoxide dismutase transgenic mice. Annals of the New York Academy of Sciences 1998, 844:92-102.
20. Kobeissy F.H., Warren M.W., Ottens A.K., Sadasivan S., Zhang Z., Gold M.S., et al. Psychoproteomic analysis of rat cortex following acute methamphetamine exposure. Journal of Proteome Research 2008, 7:1971-1983.
21. Li X., Wang H., Qiu P., Luo H. Proteomic profiling of proteins associated with methamphetamine-induced neurotoxicity in different regions of rat brain. Neurochemistry International 2008, 52:256-264.
22. Dempsey E.C., Newton A.C., Mochly-Rosen D., Fields A.P., Reyland M.E., Insel P.A., et al. Protein kinase C isozymes and the regulation of diverse cell responses. American Journal of Physiology. Lung Cellular and Molecular Physiology 2000, 279:L429-L438.
23. Gschwendt M. Protein kinase C delta. European Journal of Biochemistry 1999, 259:555-564.
24. Gopalakrishna R., Gundimeda U. Protein kinase C as a molecular target for cancer prevention by selenocompounds. Nutrition and Cancer 2001, 40:55-63.
25. Gopalakrishna R., Jaken S. Protein kinase C signaling and oxidative stress. Free Radical Biology and Medicine 2000, 28:1349-1361.
26. Chiarpotto E., Domenicotti C., Paola D., Vitali A., Nitti M., Pronzato M.A., et al. Regulation of rat hepatocyte protein kinase C beta isoenzymes by the lipid peroxidation product 4-hydroxy-2,3-nonenal: a signaling pathway to modulate vesicular transport of glycoproteins. Hepatology 1999, 29:1565-1572.
27. Nitti M., d'Abramo C., Traverso N., Verzola D., Garibotto G., Poggi A., et al. Central role of PKCdelta in glycoxidation-dependent apoptosis of human neurons. Free Radical Biology and Medicine 2005, 38:846-856.
28. Domenicotti C., Paola D., Vitali A., Nitti M., d'Abramo C., Cottalasso D., et al. Glutathione depletion induces apoptosis of rat hepatocytes through activation of protein kinase C novel isoforms and dependent increase in AP-1 nuclear binding. Free Radical Biology and Medicine 2000, 29:1280-1290.
29. Pubill D., Chipana C., Camins A., Pallas M., Camarasa J., Escubedo E. Free radical production induced by methamphetamine in rat striatal synaptosomes. Toxicology and Applied Pharmacology 2005, 204:57-68.
30. Cowell R.M., Kantor L., Hewlett G.H., Frey K.A., Gnegy M.E. Dopamine transporter antagonists block phorbol ester-induced dopamine release and dopamine transporter phosphorylation in striatal synaptosomes. European Journal of Pharmacology 2000, 389:59-65.
31. Kantor L., Gnegy M.E. Protein kinase C inhibitors block amphetamine-mediated dopamine release in rat striatal slices. Journal of Pharmacology and Experimental Therapeutics 1998, 284:592-598.
32. Kantor L., Hewlett G.H., Park Y.H., Richardson-Burns S.M., Mellon M.J., Gnegy M.E. Protein kinase C and intracellular calcium are required for amphetamine-mediated dopamine release via the norepinephrine transporter in undifferentiated PC12 cells. Journal of Pharmacology and Experimental Therapeutics 2001, 297:1016-1024.
33. Miyamoto A., Nakayama K., Imaki H., Hirose S., Jiang Y., Abe M., et al. Increased proliferation of B cells and auto-immunity in mice lacking protein kinase Cdelta. Nature 2002, 416:865-869.
34. Franklin K.B.J., Paxinos G. The mouse brain in stereotaxic coordinates 2008, Academic Press, San Diego. 3rd ed.
35. Shin E.J., Chae J.S., Park S.J., Kim S.C., Koo K.H., Yamada K., et al. Growth hormone-releaser diet attenuates beta-amyloid(1-42)-induced cognitive impairment via stimulation of the insulin-like growth factor (IGF)-1 receptor in mice. Journal of Pharmacological Sciences 2009, 109:139-143.
36. Smith F.L., Gabra B.H., Smith P.A., Redwood M.C., Dewey W.L. Determination of the role of conventional, novel and atypical PKC isoforms in the expression of morphine tolerance in mice. Pain 2007, 127:129-139.
37. Smith F.L., Javed R.R., Smith P.A., Dewey W.L., Gabra B.H. PKC and PKA inhibitors reinstate morphine-induced behaviors in morphine tolerant mice. Pharmacological Research 2006, 54:474-480.
38. Shin E.J., Nguyen T.X.K., Nguyen T.P.K., Mai A.T., Park S.J., Bach J.H., et al. Attenuation of methamphetamine-induced nigrostriatal dopaminergic toxicity by pharmacological and genetic inhibition of protein kinase Cδ. Spring international convention of the pharmaceutical society of Korea 2010, 1-96. Pharmaceutical Society of Korea, Daegu EXCO.
39. Jung B.D., Shin E.J., Nguyen X.K., Jin C.H., Bach J.H., Park S.J., et al. Potentiation of methamphetamine neurotoxicity by intrastriatal lipopolysaccharide administration. Neurochemistry International 2010, 56:229-244.
40. Choi D.Y., Liu M., Hunter R.L., Cass W.A., Pandya J.D., Sullivan P.G., et al. Striatal neuroinflammation promotes Parkinsonism in rats. PLoS One 2009, 4:e5482.
41. Hunter R.L., Dragicevic N., Seifert K., Choi D.Y., Liu M., Kim H.C., et al. Inflammation induces mitochondrial dysfunction and dopaminergic neurodegeneration in the nigrostriatal system. Journal of Neurochemistry 2007, 100:1375-1386.
42. Li Z., Choi D.Y., Shin E.J., Hunter R.L., Jin C.H., Wie M.B., et al. Phenidone protects the nigral dopaminergic neurons from LPS-induced neurotoxicity. Neuroscience Letters 2008, 445:1-6.
43. Liu M., Hunter R., Nguyen X.V., Kim H.C., Bing G. Microsomal epoxide hydrolase deletion enhances tyrosine hydroxylase phosphorylation in mice after MPTP treatment. Journal of Neuroscience Research 2008, 86:2792-2801.
44. Kwon Y.S., Ann H.S., Nabeshima T., Shin E.J., Kim W.K., Jhoo J.H., et al. Selegiline potentiates the effects of EGb 761 in response to ischemic brain injury. Neurochemistry International 2004, 45:157-170.
45. Eyerman D.J., Yamaoto B.K. A rapid oxidation and persistent decrease in the vesicular monoamine transporter 2 after methamphetamine. Journal of Neurochemistry 2007, 103:1219-1227.
46. Nguyen X.V., Liu M., Kim H.C., Bing G. Effects of prodynorphin deletion on striatal dopamine in mice during normal aging and in response to MPTP. Experimental Neurology 2009, 219:228-238.
47. Liu M., Choi D.Y., Hunter R.L., Pandya J.D., Cass W.A., Sullivan P.G., et al. Trichloroethylene induces dopaminergic neurodegeneration in Fisher 344 rats. Journal of Neurochemistry 2010, 112:773-783.
48. Nakajima A., Yamada K., Nagai T., Uchiyama T., Miyamoto Y., Mamiya T., et al. Role of tumor necrosis factor-alpha in methamphetamine-induced drug dependence and neurotoxicity. Journal of Neuroscience 2004, 24:2212-2225.
49. Nagatsu T., Oka K., Kato T. Highly sensitive assay for tyrosine hydroxylase activity by high-performance liquid chromatography. Journal of Chromatography 1979, 163:247-252.
50. Jareno E.J., Bosch-Morell F., Fernandez-Delgado R., Donat J., Romero F.J. Serum malondialdehyde in HIV seropositive children. Free Radical Biology and Medicine 1998, 24:503-506.
51. Kim H.C., Jhoo W.K., Shin E.J., Bing G. Selenium deficiency potentiates methamphetamine-induced nigral neuronal loss; comparison with MPTP model. Brain Research 2000, 862:247-252.
52. Oliver C.N., Ahn B.W., Moerman E.J., Goldstein S., Stadtman E.R. Age-related changes in oxidized proteins. Journal of Biological Chemistry 1987, 262:5488-5491.
53. Benedetti A., Comporti M., Esterbauer H. Identification of 4-hydroxynonenal as a cytotoxic product originating from the peroxidation of liver microsomal lipids. Biochimica et Biophysica Acta 1980, 620:281-296.
54. Tran H.Y., Shin E.J., Saito K., Nguyen X.K., Chung Y.H., Jeong J.H., et al. Protective potential of IL-6 against trimethyltin-induced neurotoxicity in vivo. Free Radical Biology and Medicine 2012, 52:1159-1174.
55. Giambalvo C.T. Protein kinase C and dopamine release-II. Effect of dopamine acting drugs in vivo. Biochemical Pharmacology 1988, 37:4009-4017.
56. Giambalvo C.T. Protein kinase C and dopamine release-III. Effect of dopamine depleting drugs. Biochemical Pharmacology 1989, 38:4445-4454.
57. Fornai F., Battaglia G., Gesi M., Orzi F., Nicoletti F., Ruggieri S. Dose-dependent protective effects of apomorphine against methamphetamine-induced nigrostriatal damage. Brain Research 2001, 898:27-35.
58. Wilson J.M., Kalasinski K.S., Levey A.I., Bergeron C., Reiber G., Anthony R.T., et al. Striatal dopamine nerve terminal markers in human, chronic methamphetamine users. Nature Medicine 1996, 2:699-703.
59. Fumagalli F., Gainetdinov R.R., Valenzano K.J., Caron M.G. Role of dopamine transporter in methamphetamine-induced neurotoxicity: evidence from mice lacking the transporter. Journal of Neuroscience 1998, 18:4861-4869.
60. Ferrer I., Friguls B., Dalfó E., Justicia C., Planas A.M. Caspase-dependent and caspase-independent signalling of apoptosis in the penumbra following middle cerebral artery occlusion in the adult rat. Neuropathology and Applied Neurobiology 2003, 29:472-481.
61. Spalding K.L., Dharmarajan A.M., Harvey A.R. Caspase-independent retinal ganglion cell death after target ablation in the neonatal rat. European Journal of Neuroscience 2005, 21:33-45.
62. Zhu J.P., Xu W., Angulo J.A. Methamphetamine-induced cell death: selective vulnerability in neuronal subpopulations of the striatum in mice. Neuroscience 2006, 140:607-622.
63. Zhu J.P., Xu W., Angulo J.A. Disparity in the temporal appearance of methamphetamine-induced apoptosis and depletion of dopamine terminal markers in the striatum of mice. Brain Research 2005, 1049:171-181.
64. Conricode K.M., Brewer K.A., Exton J.H. Activation of phospholipase D by protein kinase C. Evidence for a phosphorylation-independent mechanism. Journal of Biological Chemistry 1992, 267:7199-7202.
65. Gerlach M., Riederer P. Animal models of Parkinson's disease: an empirical comparison with the phenomenology of the disease in man. Journal of Neural Transmission 1996, 103:987-1041.
66. Lenard L.G., Beer B. Relationship of brain levels of norepinephrine and dopamine to avoidance behavior in rats after intraventricular administration of 6-hydoxydopamine. Pharmacology, Biochemistry and Behavior 1975, 3:895-899.
67. Neill D.B., Boggan W.O., Grossman S.P. Impairment of avoidance performance by intrastriatal administration of 6-hydroxydopamine. Pharmacology, Biochemistry and Behavior 1974, 2:97-103.
68. Kanthasamy A., Jin H., Mehrotra S., Mishra R., Kanthasamy A., Rana A. Novel cell death signaling pathways in neurotoxicity models of dopaminergic degeneration: relevance to oxidative stress and neuroinflammation in Parkinson's disease. NeuroToxicology 2010, 31:555-561.
69. Domenicotti C., Marengo B., Verzola D., Garibotto G., Traverso N., Patriarca S., et al. Role of PKC-delta activity in glutathione-depleted neuroblastoma cells. Free Radical Biology and Medicine 2003, 35:504-516.
70. Cubells J.F., Rayport S., Rajendran G., Sulzer D. Methamphetamine neurotoxicity involves vacuolation of endocytic organelles and dopamine-dependent intracellular oxidative stress. Journal of Neuroscience 1994, 14:2260-2271.
71. De Vito M.J., Wagner G.C. Methamphetamine-induced neuronal damage: a possible role for free radicals. Neuropharmacology 1989, 28:1145-1150.
72. Graham D.G., Tiffany S.M., Bell W.R., Gutknecht W.F. Autoxidation versus covalent binding of quinones as the mechanism of toxicity of dopamine, 6-hydroxydopamine, and related compounds toward C1300 neuroblastoma cells in vitro. Molecular Pharmacology 1978, 14:644-653.
73. Slivka A., Cohen G. Hydroxyl radical attack on dopamine. Journal of Biological Chemistry 1985, 260:15466-15472.
74. Riddle E.L., Fleckenstein A.E., Hanson G.R. Role of monoamine transporters in mediating psychostimulant effects. AAPS Journal 2005, 7:E847-E851.
75. Fleckenstein A.E., Metzger R.R., Wilkins D.G., Gibb J.W., Hanson G.R. Rapid and reversible effects of methamphetamine on dopamine transporters. Journal of Pharmacology and Experimental Therapeutics 1997, 282:834-838.
76. Vergo S., Johansen J.L., Leist M., Lotharius J. Vesicular monoamine transporter 2 regulates the sensitivity of rat dopaminergic neurons to disturbed cytosolic dopamine levels. Brain Research 2007, 1185:18-32.
77. Guillot T.S., Richardson J.R., Wang M.Z., Li Y.J., Taylor T.N., Ciliax B.J., et al. PACAP38 increases vesicular monoamine transporter 2 (VMAT2) expression and attenuates methamphetamine toxicity. Neuropeptides 2008, 42:423-434.
78. Granado N., Lastres-Becker I., Ares-Santos S., Oliva I., Martin E., Cuadrado A., et al. Nrf2 deficiency potentiates methamphetamine-induced dopaminergic axonal damage and gliosis in the striatum. Glia 2011, 59:1850-1863.
79. Miyazaki I., Asanuma M., Kikkawa Y., Takeshima M., Murakami S., Miyoshi K., et al. Astrocyte-derived metallothionein protects dopaminergic neurons from dopamine quinone toxicity. Glia 2011, 59:435-451.
80. Zhang W., Shin E.J., Wang T., Lee P.H., Pang H., Wie M.B., et al. 3-Hydroxymorphinan, a metabolite of dextromethorphan, protects nigrostriatal pathway against MPTP-elicited damage both in vivo and in vitro. FASEB Journal 2006, 20:2496-2511.
81. Deng X., Cai N.S., McCoy M.T., Chen W., Trush M.A., Cadet J.L. Methamphetamine induces apoptosis in an immortalized rat striatal cell line by activating the mitochondrial cell death pathway. Neuropharmacology 2002, 42:837-845.
82. Jayanthi S., Deng X., Noailles P.A., Ladenheim B., Cadet J.L. Methamphetamine induces neuronal apoptosis via cross-talks between endoplasmic reticulum and mitochondria-dependent death cascades. FASEB Journal 2004, 18:238-251.
83. Warren M.W., Kobeissy F.H., Liu M.C., Hayes R.L., Gold M.S., Wang K.K. Concurrent calpain and caspase-3 mediated proteolysis of alpha II-spectrin and tau in rat brain after methamphetamine exposure: a similar profile to traumatic brain injury. Life Sciences 2005, 78:301-309.
84. Wallace T.L., Vorhees C.V., Zemlan F.P., Gudelsky G.A. Methamphetamine enhances the cleavage of the cytoskeletal protein tau in the rat brain. Neuroscience 2003, 116:1063-1068.
85. Nath R., Raser K.J., Stafford D., Hajimohammadreza I., Posner A., Allen H., et al. Non-erythroid alpha-spectrin breakdown by calpain and interleukin 1 beta-converting-enzyme-like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis. Biochemical Journal 1996, 319:683-690.
86. Stumm G., Schlegel J., Schafer T., Wurz C., Mennel H.D., Krieg J.C., et al. Amphetamines induce apoptosis and regulation of bcl-x splice variants in neocortical neurons. FASEB Journal 1999, 13:1065-1072.
87. Deng X., Cadet J.L. Methamphetamine-induced apoptosis is attenuated in the striata of copper-zinc superoxide dismutase transgenic mice. Brain Research. Molecular Brain Research 2000, 83:121-124.
88. Deng X., Wang Y., Chou J., Cadet J.L. Methamphetamine causes widespread apoptosis in the mouse brain: evidence from using an improved TUNEL histochemical method. Brain Research. Molecular Brain Research 2001, 93:64-69.
89. Cadet J.L., Jayanthi S., Deng X. Speed kills: cellular and molecular bases of methamphetamine-induced nerve terminal degeneration and neuronal apoptosis. FASEB Journal 2003, 17:1775-1788.
90. Loonam T.M., Noailles P.A., Yu J., Zhu J.P., Angulo J.A. Substance P and cholecystokinin regulate neurochemical responses to cocaine and methamphetamine in the striatum. Life Sciences 2003, 73:727-739.
91. Bowyer J.F., Tank A.W., Newport G.D., Slikker W., Ali S.F., Holson R.R. The influence of environmental temperature on the transient effects of methamphetamine on dopamine levels and dopamine release in striatum. Journal of Pharmacology and Experimental Therapeutics 1992, 260:817-824.
92. Bowyer J.F., Davies D.L., Schmued L., Broening H.W., Newport G.D., Slikker W., et al. Further studies of the role of hyperthermia in methamphetamine neurotoxicity. Journal of Pharmacology and Experimental Therapeutics 1994, 268:1571-1580.
93. Albers D.S., Sonsalla P.K. Methamphetamine-induced hyperthermia and dopaminergic neurotoxicity in mice: pharmacological profile of protective and nonprotective agents. Journal of Pharmacology and Experimental Therapeutics 1995, 275:1104-1114.
94. Ricaurte G.A., Fuller R.W., Perry K.W., Seiden L.S., Schuster C.R. Fluoxetine increases long-lasting neostriatal dopamine depletion after administration of d-methamphetamine and d-amphetamine. Neuropharmacology 1983, 22:1165-1169.
95. Wagner G.C., Lucot J.B., Schuster C.R., Seiden L.S. α-Methyltyrosine attenuates and reserpine increases methamphetamine-induced neuronal changes. Brain Research 1983, 270:285-288.
96. Fornstedt B., Carlsson A. A marked rise in 5-S-cysteinyl-dopamine levels in guinea pig striatum following reserpine treatment. Journal of neural transmission 1989, 76:155-161.
97. Fumagalli F., Gainetdinov R.R., Wang Y.M., Valenzano K.J., Miller G.W., Caron M.G. Increased methamphetamine neurotoxicity in heterozygous vesicular monoamine transporter 2 knock-out mice. Journal of Neuroscience 1999, 19:2424-2431.
98. Zhang D., Anantharam V., Kanthasamy A., Kanthasamy A.G. Neuroprotective effect of protein kinase C delta inhibitor rottlerin in cell culture and animal models of Parkinson's disease. Journal of Pharmacology and Experimental Therapeutics 2007, 322:913-922.
99. Bourque M., Dluzen D.E., Di Paolo T. Neuroprotective actions of sex steroids in Parkinson's disease. Frontiers in Neuroendocrinology 2009, 30:142-157.
100. Gschwendt M., Muller H.J., Kielbassa K., Zang R., Kittstein W., Rincke G., et al. Rottlerin, a novel protein kinase inhibitor. Biochemical and Biophysical Research Communications 1994, 199:93-98.
101. Li C., Chen X., Williams J.A. Regulation of CCK-induced amylase release by PKC-delta in rat pancreatic acinar cells. American Journal of Physiology. Gastrointestinal and Liver Physiology 2004, 287:G764-G771.
102. Yokoyama G., Fujii T., Tayama K., Yamana H., Kuwano M., Shirouzu K. PKCdelta and MAPK mediate G(1) arrest induced by PMA in SKBR-3 breast cancer cells. Biochemical and Biophysical Research Communications 2005, 327:720-726.
103. Zhang D., Kanthasamy A., Yang Y., Anantharam V. Protein kinase C delta negatively regulates tyrosine hydroxylase activity and dopamine synthesis by enhancing protein phosphatase-2A activity in dopaminergic neurons. Journal of Neuroscience 2007, 27:5349-5362.
104. Soltoff S.P. Rottlerin: an inappropriate and ineffective inhibitor of PKCdelta. Trends in Pharmacological Sciences 2007, 28:453-458.
105. Susarla B.T., Robinson M.B. Rottlerin, an inhibitor of protein kinase Cdelta (PKCdelta), inhibits astrocytic glutamate transport activity and reduces GLAST immunoreactivity by a mechanism that appears to be PKCdelta-independent. Journal of Neurochemistry 2003, 86:635-645.
106. Tapia J.A., Jensen R.T., Garcia-Marin L.J. Rottlerin inhibits stimulated enzymatic secretion and several intracellular signaling transduction pathways in pancreatic acinar cells by a non-PKC-delta-dependent mechanism. Biochimica et Biophysica Acta 2006, 1763:25-38.