Is brain gliosis a characteristic of chronic methamphetamine use in the human?

Neurobiology of Disease

Volumn 67, Issue , 2014, Pages 107-118

  Tong, Junchao ^a   Fitzmaurice, Paul ^b   Furukawa, Yoshiaki ^c   Schmunk, Gregory A ^d   Wickham, Dennis J ^e   Ang, Lee Cyn ^f   Sherwin, Allan ^g   McCluskey, Tina ^a   Boileau, Isabelle ^a   Kish, Stephen J ^a  

^a CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^b MT ALBERT RESEARCH CENTRE   (New Zealand)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d Office of the Polk County Medical Examiner   (United States)

^e Clark Co Off of the Med Examiner   (United States)

^f UNIVERSITY OF WESTERN ONTARIO   (Canada)

^g MCGILL UNIVERSITY   (Canada)

Author keywords

Glial fibrillary acidic protein; Gliosis; Glucose transporter 5; Heat shock protein 27; Human leukocyte antigen; Methamphetamine; Multiple system atrophy; Postmortem human brain; Tolerance; Vimentin

Indexed keywords

4 HYDROXYNONENAL; DOPAMINE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE TRANSPORTER 5; HEAT SHOCK PROTEIN 27; HLA DP ANTIGEN; HLA DQ ANTIGEN; HLA DR ANTIGEN; MALONALDEHYDE; METHAMPHETAMINE; VIMENTIN; CENTRAL STIMULANT AGENT;

ADOLESCENT; ADULT; ARTICLE; ASTROCYTOSIS; AUTOPSY; BRAIN GLIOSIS; CAUDATE NUCLEUS; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; GLIOSIS; HUMAN; HUMAN TISSUE; LIPID PEROXIDATION; MACROGLIA; MALE; METHAMPHETAMINE DEPENDENCE; MICROGLIA; NERVE CELL PLASTICITY; NEUROTOXICITY; PRIORITY JOURNAL; PUTAMEN; RECREATION; TISSUE LEVEL; YOUNG ADULT; BRAIN; CHEMICALLY INDUCED; DRUG EFFECTS; METABOLISM;

ADOLESCENT; ADULT; BRAIN; CENTRAL NERVOUS SYSTEM STIMULANTS; FEMALE; GLIOSIS; HUMANS; MALE; METHAMPHETAMINE; YOUNG ADULT;

EID: 84898995904     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.03.015     Document Type: Article

References (96)

1. Acarin L., Villapol S., Faiz M., Rohn T.T., Castellano B., Gonzalez B. Caspase-3 activation in astrocytes following postnatal excitotoxic damage correlates with cytoskeletal remodeling but not with cell death or proliferation. Glia 2007, 55:954-965.
2. Adori C., Ando R.D., Kovacs G.G., Bagdy G. Damage of serotonergic axons and immunolocalization of Hsp27, Hsp72, and Hsp90 molecular chaperones after a single dose of MDMA administration in Dark Agouti rat: temporal, spatial, and cellular patterns. J. Comp. Neurol. 2006, 497:251-269.
3. Armstrong V., Reichel C.M., Doti J.F., Crawford C.A., McDougall S.A. Repeated amphetamine treatment causes a persistent elevation of glial fibrillary acidic protein in the caudate-putamen. Eur. J. Pharmacol. 2004, 488:111-115.
4. Barcia C., Sanchez Bahillo A., Fernandez-Villalba E., Bautista V., Poza Y.P.M., Fernandez-Barreiro A., et al. Evidence of active microglia in substantia nigra pars compacta of parkinsonian monkeys 1year after MPTP exposure. Glia 2004, 46:402-409.
5. Buchanan J.B., Sparkman N.L., Johnson R.W. Methamphetamine sensitization attenuates the febrile and neuroinflammatory response to a subsequent peripheral immune stimulus. Brain Behav. Immun. 2010, 24:502-511.
6. Byun Y., Chen F., Chang R., Trivedi M., Green K.J., Cryns V.L. Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis. Cell Death Differ. 2001, 8:443-450.
7. Cadet J.L., Jayanthi S., Deng X. Speed kills: cellular and molecular bases of methamphetamine-induced nerve terminal degeneration and neuronal apoptosis. Faseb J. 2003, 17:1775-1788.
8. Cagnin A., Brooks D.J., Kennedy A.M., Gunn R.N., Myers R., Turkheimer F.E., et al. In-vivo measurement of activated microglia in dementia. Lancet 2001, 358:461-467.
9. Callaghan R.C., Cunningham J.K., Sykes J., Kish S.J. Increased risk of Parkinson's disease in individuals hospitalized with conditions related to the use of methamphetamine or other amphetamine-type drugs. Drug Alcohol Depend. 2012, 120:35-40.
10. Chuang J.Y., Chang W.T., Cherng C.G., Kao G.S., Yu L. Repeated co-administrations of alcohol- and methamphetamine-produced anxiogenic effect could be associated with the neurotoxicity in the dentate gyrus. J. Neural Transm. 2011, 118:1559-1569.
11. Cosenza-Nashat M., Zhao M.L., Suh H.S., Morgan J., Natividad R., Morgello S., et al. Expression of the translocator protein of 18kDa by microglia, macrophages and astrocytes based on immunohistochemical localization in abnormal human brain. Neuropathol. Appl. Neurobiol. 2009, 35:306-328.
12. Dahl D., Rueger D.C., Bignami A., Weber K., Osborn M. Vimentin, the 57000 molecular weight protein of fibroblast filaments, is the major cytoskeletal component in immature glia. Eur. J. Cell Biol. 1981, 24:191-196.
13. Darlington P.J., Podjaski C., Horn K.E., Costantino S., Blain M., Saikali P., et al. Innate immune-mediated neuronal injury consequent to loss of astrocytes. J. Neuropathol. Exp. Neurol. 2008, 67:590-599.
14. David J.P., Ghozali F., Fallet-Bianco C., Wattez A., Delaine S., Boniface B., et al. Glial reaction in the hippocampal formation is highly correlated with aging in human brain. Neurosci. Lett. 1997, 235:53-56.
15. Deininger M.H., Meyermann R., Schluesener H.J. The allograft inflammatory factor-1 family of proteins. FEBS Lett. 2002, 514:115-121.
16. Desai Bradaric B., Patel A., Schneider J.A., Carvey P.M., Hendey B. Evidence for angiogenesis in Parkinson's disease, incidental Lewy body disease, and progressive supranuclear palsy. J. Neural Transm. 2012, 119:59-71.
17. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 1997, 17:5046-5061.
18. Eng L.F. Glial fibrillary acidic protein (GFAP): the major protein of glial intermediate filaments in differentiated astrocytes. J. Neuroimmunol. 1985, 8:203-214.
19. Escubedo E., Guitart L., Sureda F.X., Jimenez A., Pubill D., Pallas M., et al. Microgliosis and down-regulation of adenosine transporter induced by methamphetamine in rats. Brain Res. 1998, 814:120-126.
20. Fellner L., Jellinger K.A., Wenning G.K., Stefanova N. Glial dysfunction in the pathogenesis of alpha-synucleinopathies: emerging concepts. Acta Neuropathol. 2011, 121:675-693.
21. Fitzmaurice P.S., Tong J., Yazdanpanah M., Liu P.P., Kalasinsky K.S., Kish S.J. Levels of 4-hydroxynonenal and malondialdehyde are increased in brain of human chronic users of methamphetamine. J. Pharmacol. Exp. Ther. 2006, 319:703-709.
22. Franke H., Kittner H., Grosche J., Illes P. Enhanced P2Y1 receptor expression in the brain after sensitisation with d-amphetamine. Psychopharmacology (Berl.) 2003, 167:187-194.
23. Friend D.M., Keefe K.A. Glial reactivity in resistance to methamphetamine-induced neurotoxicity. J. Neurochem. 2013, 125:566-574.
24. Gerhard A., Banati R.B., Goerres G.B., Cagnin A., Myers R., Gunn R.N., et al. [11C](R)-PK11195 PET imaging of microglial activation in multiple system atrophy. Neurology 2003, 61:686-689.
25. Gilman S., Wenning G.K., Low P.A., Brooks D.J., Mathias C.J., Trojanowski J.Q., et al. Second consensus statement on the diagnosis of multiple system atrophy. Neurology 2008, 71:670-676.
26. 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.
27. 18F-PBR111 in healthy humans: a genetic polymorphism effect on in vivo binding. J. Nucl. Med. 2013, 54:1915-1923.
28. Harpin M.L., Delaere P., Javoy-Agid F., Bock E., Jacque C., Delpech B., et al. Glial fibrillary acidic protein and beta A4 protein deposits in temporal lobe of aging brain and senile dementia of the Alzheimer type: relation with the cognitive state and with quantitative studies of senile plaques and neurofibrillary tangles. J. Neurosci. Res. 1990, 27:587-594.
29. Hashimoto M., Inoue S., Ogawa S., Conrad C., Muramatsu M., Shackelford D., et al. Rapid fragmentation of vimentin in human skin fibroblasts exposed to tamoxifen: a possible involvement of caspase-3. Biochem. Biophys. Res. Commun. 1998, 247:401-406.
30. Head M.W., Corbin E., Goldman J.E. Overexpression and abnormal modification of the stress proteins alpha B-crystallin and HSP27 in Alexander disease. Am. J. Pathol. 1993, 143:1743-1753.
31. Hess A., Desiderio C., McAuliffe W.G. Acute neuropathological changes in the caudate nucleus caused by MPTP and methamphetamine: immunohistochemical studies. J. Neurocytol. 1990, 19:338-342.
32. Horikoshi Y., Sasaki A., Taguchi N., Maeda M., Tsukagoshi H., Sato K., et al. Human GLUT5 immunolabeling is useful for evaluating microglial status in neuropathological study using paraffin sections. Acta Neuropathol. 2003, 105:157-162.
33. Imamura K., Hishikawa N., Sawada M., Nagatsu T., Yoshida M., Hashizume Y. Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson's disease brains. Acta Neuropathol. 2003, 106:518-526.
34. Ingelsson M., Fukumoto H., Newell K.L., Growdon J.H., Hedley-Whyte E.T., Frosch M.P., et al. Early Abeta accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain. Neurology 2004, 62:925-931.
35. Ishizawa K., Komori T., Sasaki S., Arai N., Mizutani T., Hirose T. Microglial activation parallels system degeneration in multiple system atrophy. J. Neuropathol. Exp. Neurol. 2004, 63:43-52.
36. Ishizawa K., Komori T., Arai N., Mizutani T., Hirose T. Glial cytoplasmic inclusions and tissue injury in multiple system atrophy: a quantitative study in white matter (olivopontocerebellar system) and gray matter (nigrostriatal system). Neuropathology 2008, 28:249-257.
37. 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 J. 2004, 18:238-251.
38. Kalasinsky K.S., Bosy T.Z., Schmunk G.A., Reiber G., Anthony R.M., Furukawa Y., et al. Regional distribution of methamphetamine in autopsied brain of chronic human methamphetamine users. Forensic Sci. Int. 2001, 116:163-169.
39. Kayano T., Burant C.F., Fukumoto H., Gould G.W., Fan Y.S., Eddy R.L., et al. Human facilitative glucose transporters. Isolation, functional characterization, and gene localization of cDNAs encoding an isoform (GLUT5) expressed in small intestine, kidney, muscle, and adipose tissue and an unusual glucose transporter pseudogene-like sequence (GLUT6). J. Biol. Chem. 1990, 265:13276-13282.
40. Kish S.J. Chapter 08: The Pathology of Methamphetamine Use in the Human Brain 2014, Elsevier Inc.
41. Kish S.J., Fitzmaurice P.S., Boileau I., Schmunk G.A., Ang L.C., Furukawa Y., et al. Brain serotonin transporter in human methamphetamine users. Psychopharmacology (Berl.) 2009, 202:649-661.
42. 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. Int. J. Legal Med. 2007, 121:163-168.
43. Kitamura O., Takeichi T., Wang E.L., Tokunaga I., Ishigami A., Kubo S. Microglial and astrocytic changes in the striatum of methamphetamine abusers. Leg. Med. (Tokyo) 2010, 12:57-62.
44. Krasnova I.N., Justinova Z., Ladenheim B., Jayanthi S., McCoy M.T., Barnes C., et al. Methamphetamine self-administration is associated with persistent biochemical alterations in striatal and cortical dopaminergic terminals in the rat. PLoS One 2010, 5:e8790.
45. Kreisl W.C., Lyoo C.H., McGwier M., Snow J., Jenko K.J., Kimura N., et al. In vivo radioligand binding to translocator protein correlates with severity of Alzheimer's disease. Brain 2013, 136:2228-2238.
46. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996, 19:312-318.
47. Krueger-Naug A.M., Hopkins D.A., Armstrong J.N., Plumier J.C., Currie R.W. Hyperthermic induction of the 27-kDa heat shock protein (Hsp27) in neuroglia and neurons of the rat central nervous system. J. Comp. Neurol. 2000, 428:495-510.
48. Lavisse S., Guillermier M., Herard A.S., Petit F., Delahaye M., Van Camp N., et al. Reactive astrocytes overexpress TSPO and are detected by TSPO positron emission tomography imaging. J. Neurosci. 2012, 32:10809-10818.
49. Mandyam C.D., Wee S., Eisch A.J., Richardson H.N., Koob G.F. Methamphetamine self-administration and voluntary exercise have opposing effects on medial prefrontal cortex gliogenesis. J. Neurosci. 2007, 27:11442-11450.
50. Mandyam C.D., Wee S., Crawford E.F., Eisch A.J., Richardson H.N., Koob G.F. Varied access to intravenous methamphetamine self-administration differentially alters adult hippocampal neurogenesis. Biol. Psychiatry 2008, 64:958-965.
51. Mao L., Wang J.Q. Gliogenesis in the striatum of the adult rat: alteration in neural progenitor population after psychostimulant exposure. Brain Res. Dev. Brain Res. 2001, 130:41-51.
52. McFadden L.M., Hadlock G.C., Allen S.C., Vieira-Brock P.L., Stout K.A., Ellis J.D., et al. Methamphetamine self-administration causes persistent striatal dopaminergic alterations and mitigates the deficits caused by a subsequent methamphetamine exposure. J. Pharmacol. Exp. Ther. 2012, 340:295-303.
53. McGeer P.L., Schwab C., Parent A., Doudet D. Presence of reactive microglia in monkey substantia nigra years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine administration. Ann. Neurol. 2003, 54:599-604.
54. Miller D.B., O'Callaghan J.P., Johnson E.A. Prior exposure to a behaviorally sensitizing regimen of d-methamphetamine does not alter the striatal dopaminergic damage induced by a neurotoxic regimen. Addict. Biol. 2000, 5:361-367.
55. Mirza B., Hadberg H., Thomsen P., Moos T. The absence of reactive astrocytosis is indicative of a unique inflammatory process in Parkinson's disease. Neuroscience 2000, 95:425-432.
56. 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.
57. Motbey C.P., Clemens K.J., Apetz N., Winstock A.R., Ramsey J., Li K.M., et al. High levels of intravenous mephedrone (4-methylmethcathinone) self-administration in rats: neural consequences and comparison with methamphetamine. J. Psychopharmacol. 2013, 27:823-836.
58. Nakanishi K., Maruyama M., Shibata T., Morishima N. Identification of a caspase-9 substrate and detection of its cleavage in programmed cell death during mouse development. J. Biol. Chem. 2001, 276:41237-41244.
59. +-activated proteinase specific for these intermediate filament proteins. Mol. Cell. Biol. 1983, 3:1146-1156.
60. O'Callaghan J.P. Assessment of neurotoxicity: use of glial fibrillary acidic protein as a biomarker. Biomed. Environ. Sci. 1991, 4:197-206.
61. O'Callaghan J.P. Quantification of glial fibrillary acidic protein: comparison of slot-immunobinding assays with a novel sandwich ELISA. Neurotoxicol. Teratol. 1991, 13:275-281.
62. O'Callaghan J.P., Miller D.B. Neurotoxicity profiles of substituted amphetamines in the C57BL/6J mouse. J. Pharmacol. Exp. Ther. 1994, 270:741-751.
63. O'Callaghan J.P., Sriram K. Glial fibrillary acidic protein and related glial proteins as biomarkers of neurotoxicity. Expert Opin. Drug Saf. 2005, 4:433-442.
64. O'Callaghan J.P., Sriram K., Miller D.B. Defining "neuroinflammation". Ann. N. Y. Acad. Sci. 2008, 1139:318-330.
65. Ouchi Y., Yoshikawa E., Sekine Y., Futatsubashi M., Kanno T., Ogusu T., et al. Microglial activation and dopamine terminal loss in early Parkinson's disease. Ann. Neurol. 2005, 57:168-175.
66. Papadopoulos V., Baraldi M., Guilarte T.R., Knudsen T.B., Lacapere J.J., Lindemann P., et al. Translocator protein (18kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol. Sci. 2006, 27:402-409.
67. Peleg-Raibstein D., Knuesel I., Feldon J. Amphetamine sensitization in rats as an animal model of schizophrenia. Behav. Brain Res. 2008, 191:190-201.
68. Probst-Cousin S., Rickert C.H., Schmid K.W., Gullotta F. Cell death mechanisms in multiple system atrophy. J. Neuropathol. Exp. Neurol. 1998, 57:814-821.
69. Pubill D., Canudas A.M., Pallas M., Camins A., Camarasa J., Escubedo E. Different glial response to methamphetamine- and methylenedioxymethamphetamine-induced neurotoxicity. Naunyn Schmiedeberg's Arch. Pharmacol. 2003, 367:490-499.
70. Renkawek K., Bosman G.J., Gaestel M. Increased expression of heat-shock protein 27kDa in Alzheimer disease: a preliminary study. Neuroreport 1993, 5:14-16.
71. Ricaurte G.A., Mechan A.O., Yuan J., Hatzidimitriou G., Xie T., Mayne A.H., et al. Amphetamine treatment similar to that used in the treatment of adult attention-deficit/hyperactivity disorder damages dopaminergic nerve endings in the striatum of adult nonhuman primates. J. Pharmacol. Exp. Ther. 2005, 315:91-98.
72. Ridet J.L., Malhotra S.K., Privat A., Gage F.H. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 1997, 20:570-577.
73. Ross G.W., O'Callaghan J.P., Sharp D.S., Petrovitch H., Miller D.B., Abbott R.D., et al. Quantification of regional glial fibrillary acidic protein levels in Alzheimer's disease. Acta Neurol. Scand. 2003, 107:318-323.
74. 18F]-FEPPA and positron emission tomography. J. Cereb. Blood Flow Metab. 2011, 31:1807-1816.
75. Schwendt M., Rocha A., See R.E., Pacchioni A.M., McGinty J.F., Kalivas P.W. Extended methamphetamine self-administration in rats results in a selective reduction of dopamine transporter levels in the prefrontal cortex and dorsal striatum not accompanied by marked monoaminergic depletion. J. Pharmacol. Exp. Ther. 2009, 331:555-562.
76. Schwob J.E., Farber N.B., Gottlieb D.I. Neurons of the olfactory epithelium in adult rats contain vimentin. J. Neurosci. 1986, 6:208-217.
77. Sekine Y., Ouchi Y., Sugihara G., Takei N., Yoshikawa E., Nakamura K., et al. Methamphetamine causes microglial activation in the brains of human abusers. J. Neurosci. 2008, 28:5756-5761.
78. Simoes P.F., Silva A.P., Pereira F.C., Marques E., Grade S., Milhazes N., et al. Methamphetamine induces alterations on hippocampal NMDA and AMPA receptor subunit levels and impairs spatial working memory. Neuroscience 2007, 150:433-441.
79. Simpson I.A., Chundu K.R., Davies-Hill T., Honer W.G., Davies P. Decreased concentrations of GLUT1 and GLUT3 glucose transporters in the brains of patients with Alzheimer's disease. Ann. Neurol. 1994, 35:546-551.
80. Sofroniew M.V., Vinters H.V. Astrocytes: biology and pathology. Acta Neuropathol. 2010, 119:7-35.
81. Song Y.J., Halliday G.M., Holton J.L., Lashley T., O'Sullivan S.S., McCann H., et al. Degeneration in different parkinsonian syndromes relates to astrocyte type and astrocyte protein expression. J. Neuropathol. Exp. Neurol. 2009, 68:1073-1083.
82. Staszewski R.D., Yamamoto B.K. Methamphetamine-induced spectrin proteolysis in the rat striatum. J. Neurochem. 2006, 96:1267-1276.
83. Stetler R.A., Gao Y., Signore A.P., Cao G., Chen J. HSP27: mechanisms of cellular protection against neuronal injury. Curr. Mol. Med. 2009, 9:863-872.
84. Streit W.J. Microglial activation and neuroinflammation in Alzheimer's disease: a critical examination of recent history. Front. Aging Neurosci. 2010, 2:22.
85. Thomas D.M., Kuhn D.M. Attenuated microglial activation mediates tolerance to the neurotoxic effects of methamphetamine. J. Neurochem. 2005, 92:790-797.
86. 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. J. Pharmacol. Exp. Ther. 2004, 311:1-7.
87. Tong J., Fitzmaurice P.S., Ang L.C., Furukawa Y., Guttman M., Kish S.J. Brain dopamine-stimulated adenylyl cyclase activity in Parkinson's disease, multiple system atrophy, and progressive supranuclear palsy. Ann. Neurol. 2004, 55:125-129.
88. Tong J., Wong H., Guttman M., Ang L.C., Forno L.S., Shimadzu M., et al. Brain alpha-synuclein accumulation in multiple system atrophy, Parkinson's disease and progressive supranuclear palsy: a comparative investigation. Brain 2010, 133:172-188.
89. Tong J., Furukawa Y., Sherwin A., Hornykiewicz O., Kish S.J. Heterogeneous intrastriatal pattern of proteins regulating axon growth in normal adult human brain. Neurobiol. Dis. 2011, 41:458-468.
90. Warren M.W., Larner S.F., Kobeissy F.H., Brezing C.A., Jeung J.A., Hayes R.L., et al. Calpain and caspase proteolytic markers co-localize with rat cortical neurons after exposure to methamphetamine and MDMA. Acta Neuropathol. 2007, 114:277-286.
91. Wharton S.B., O'Callaghan J.P., Savva G.M., Nicoll J.A., Matthews F., Simpson J.E., et al. Population variation in glial fibrillary acidic protein levels in brain ageing: relationship to Alzheimer-type pathology and dementia. Dement. Geriatr. Cogn. Disord. 2009, 27:465-473.
92. 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. Nat. Med. 1996, 2:699-703.
93. Yamada T., Kawamata T., Walker D.G., McGeer P.L. Vimentin immunoreactivity in normal and pathological human brain tissue. Acta Neuropathol. 1992, 84:157-162.
94. Yamamoto B.K., Moszczynska A., Gudelsky G.A. Amphetamine toxicities: classical and emerging mechanisms. Ann. N. Y. Acad. Sci. 2010, 1187:101-121.
95. Yokoyama N., Iwaki T., Goldman J.E., Tateishi J., Fukui M. Small heat-shock protein is expressed in meningiomas and in granulofilamentous inclusion bodies. Acta Neuropathol. 1993, 85:248-255.
96. Zhang D., Hu X., Qian L., O'Callaghan J.P., Hong J.S. Astrogliosis in CNS pathologies: is there a role for microglia?. Mol. Neurobiol. 2010, 41:232-241.