Contribution of in vitro neurotoxicology studies to the elucidation of neurodegenerative processes

Brain Research Bulletin

Volumn 80, Issue 4-5, 2009, Pages 211-216

  Zurich, M G ^a   Monnet Tschudi, F ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Aggregating brain cell cultures; In vitro neurotoxicology; Neurodegeneration

Indexed keywords

ALUMINUM; COPPER; ENVIRONMENTAL CHEMICAL; FUNGICIDE; HEAVY METAL; HERBICIDE; IRON; LEAD; MANGANESE; MERCURY; PESTICIDE; XENOBIOTIC AGENT; ZINC;

ALZHEIMER DISEASE; BRAIN CELL; CELL INTERACTION; CELL TYPE; DEGENERATIVE DISEASE; DISEASE EXACERBATION; DISEASE PREDISPOSITION; ENVIRONMENTAL FACTOR; HEALTH HAZARD; HEREDITY; HUMAN; IN VITRO STUDY; NEUROTOXICOLOGY; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SCREENING; SYMPTOM;

ANIMALS; BRAIN; ENVIRONMENTAL EXPOSURE; HAZARDOUS SUBSTANCES; HUMANS; NEURODEGENERATIVE DISEASES; NEUROTOXINS; RISK FACTORS;

EID: 70349432194     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2009.06.008     Document Type: Review

References (103)

1. Ali S.F., LeBel C.P., and Bondy S.C. Reactive oxygen species formation as a biomarker of methylmercury and trimethyltin neurotoxicity. Neurotoxicology 13 (1992) 637-648
2. Alix P., Winterer J., and Muller W. New illumination technique for IR-video guided patch-clamp recording from neurons in slice cultures on biomembrane. J. Neurosci. Methods 128 (2003) 79-84
3. Anandatheerthavarada H.K., Biswas G., Robin M.A., and Avadhani N.G. Mitochondrial targeting and a novel transmembrane arrest of Alzheimer's amyloid precursor protein impairs mitochondrial function in neuronal cells. J. Cell Biol. 161 (2003) 41-54
4. M.E. Andersen, D. Krewski, E. Mantus, L. Zeise, Toxicity testing in the 21st century, http://www.alttox.org/ttrc/overarching-challenges/way-forward/andersen/, 2008.
5. Anon. National Research Council, Toxicity Testing in the 21st Century: A Vision and Strategy (2007), National Academy Press, Washington, DC
6. Apland J.P., Aroniadou-Anderjaska V., and Braga M.F. Soman induces ictogenesis in the amygdala and interictal activity in the hippocampus that are blocked by a GluR5 kainate receptor antagonist in vitro. Neuroscience 159 (2009) 380-389
7. Aptowicz C.O., Kunkler P.E., and Kraig R.P. Homeostatic plasticity in hippocampal slice cultures involves changes in voltage-gated Na+ channel expression. Brain Res. 998 (2004) 155-163
8. Barker D.J., Winter P.D., Osmond C., Margetts B., and Simmonds S.J. Weight in infancy and death from ischaemic heart disease. Lancet 2 (1989) 577-580
9. Basha M.R., Wei W., Bakheet S.A., Benitez N., Siddiqi H.K., Ge Y.W., Lahiri D.K., and Zawia N.H. The fetal basis of amyloidogenesis: exposure to lead and latent overexpression of amyloid precursor protein and beta-amyloid in the aging brain. J. Neurosci. 25 (2005) 823-829
10. Bence N.F., Sampat R.M., and Kopito R.R. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292 (2001) 1552-1555
11. K. Boekelheide, A paradigm shift in toxicity testing is inevitable, http://www.alttox.org/ttrc/overarching-challenges/way-forward/boekelheide/, 2008.
12. Bossy-Wetzel E., Schwarzenbacher R., and Lipton S.A. Molecular pathways to neurodegeneration. Nat. Med. Suppl. 10 (2004) S2-S9
13. Brown R.C., Lockwood A.H., and Sonawane B.R. Neurodegenerative diseases: an overview of environmental risk factors. Environ. Health Perspect. 113 (2005) 1250-1256
14. Bueler H. Impaired mitochondrial dynamics and function in the pathogenesis of Parkinson's disease. Exp. Neurol. (2009)
15. Cagnon L., and Braissant O. CNTF protects oligodendrocytes from ammonia toxicity: intracellular signaling pathways involved. Neurobiol. Dis. 33 (2009) 133-142
16. Cho S., Wood A., and Bowlby M.R. Brain slices as models for neurodegenerative disease and screening platforms to identify novel therapeutics. Curr. Neuropharmacol. 5 (2007) 19-33
17. Chou A.P., Maidment N., Klintenberg R., Casida J.E., Li S., Fitzmaurice A.G., Fernagut P.O., Mortazavi F., Chesselet M.F., and Bronstein J.M. Ziram causes dopaminergic cell damage by inhibiting E1 ligase of the proteasome. J. Biol. Chem. 283 (2008) 34696-34703
18. Coppede F., Mancuso M., Siciliano G., Migliore L., and Murri L. Genes and the environment in neurodegeneration. Biosci. Rep. 26 (2006) 341-367
19. Davey F.D., and Breen K.C. The interaction between chronic low-level lead and the amyloid beta precursor protein. Amyloid 5 (1998) 90-98
20. De Silva R.H.A., Khan N.L., and Wood N.W. The genetics of Parkinson's disease. Curr. Opin. Genet. Dev. (2000) 292-298
21. Devi L., Raghavendran V., Prabhu B.M., Avadhani N.G., and Anandatheerthavarada H.K. Mitochondrial import and accumulation of alpha-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. J. Biol. Chem. 283 (2008) 9089-9100
22. Domico L.M., Cooper K.R., Bernard L.P., and Zeevalk G.D. Reactive oxygen species generation by the ethylene-bis-dithiocarbamate (EBDC) fungicide mancozeb and its contribution to neuronal toxicity in mesencephalic cells. Neurotoxicology 28 (2007) 1079-1091
23. Dringen R., and Hirrlinger J. Glutathione pathways in the brain. Biol. Chem. 384 (2003) 505-516
24. Eskes C., Honegger P., Jones-Lepp T., Varner K., Matthieu J.-M., and Monnet-Tschudi F. Neurotoxicity of dibutyltin in aggregating brain cell cultures. Toxicol. In Vitro 13 (1999) 555-560
25. Eskes C., Honegger P., Juillerat-Jeanneret L., and Monnet-Tschudi F. Microglial reaction induced by noncytotoxic methylmercury treatment leads to neuroprotection via interactions with astrocytes and IL-6 release. Glia 37 (2002) 43-52
26. Eskes C., Juillerat-Jeanneret L., Leuba G., Honegger P., and Monnet-Tschudi F. Involvement of microglia-neuron interactions in the tumor necrosis factor-alpha release, microglial activation, and neurodegeneration induced by trimethyltin. J. Neurosci. Res. 71 (2003) 583-590
27. Finley M., Fairman D., Liu D., Li P., Wood A., and Cho S. Functional validation of adult hippocampal organotypic cultures as an in vitro model of brain injury. Brain Res. 1001 (2004) 125-132
28. Gahwiler B.H. Organotypic slice cultures: a model for interdisciplinary studies. Prog. Clin. Biol. Res. 253 (1987) 13-18
29. Gao X., and Hu H. Quality control of the proteins associated with neurodegenerative diseases. Acta Biochim. Biophys. Sin. (Shanghai) 40 (2008) 612-618
30. Gerlach M., Riederer P., Przuntek H., and Youdim M.B. MPTP mechanisms of neurotoxicity and their implications for Parkinson's disease. Eur. J. Pharmacol. 208 (1991) 273-286
31. Giordano G., Afsharinejad Z., Guizzetti M., Vitalone A., Kavanagh T.J., and Costa L.G. Organophosphorus insecticides chlorpyrifos and diazinon and oxidative stress in neuronal cells in a genetic model of glutathione deficiency. Toxicol. Appl. Pharmacol. 219 (2007) 181-189
32. Goate A., Chartier-Harlin M.C., Mullan M., Brown J., Crawford F., Fidani L., Giuffra L., Haynes A., Irving N., James L., et al. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349 (1991) 704-706
33. Green C.R., and Nicholson L.F. Interrupting the inflammatory cycle in chronic diseases-do gap junctions provide the answer?. Cell. Biol. Int. 32 (2008) 1578-1583
34. Guentert-Lauber B., Monnet-Tschudi F., Omlin F.X., Favrod P., and Honegger P. Serum-free aggregate cultures of rat CNS glial cells: biochemical, immunocytochemical and morphological characterization. Dev. Neurosci. 7 (1985) 33-44
35. Hakkoum D., muller D., and Stoppini L. Electrophysiological monitoring of hippocampal slice cultures using MEA on porous membrane. In: Takeni M., and Baudry M. (Eds). Advances in Network Electrophysiology using Multi-Electrode Array (2006), Springer 116-130
36. Harrer M.D., von Budingen H.C., Stoppini L., Alliod C., Pouly S., Fischer K., and Goebels N. Live imaging of remyelination after antibody-mediated demyelination in an ex-vivo model for immune mediated CNS damage. Exp. Neurol. (2009)
37. Harry G.J., and Kraft A.D. Neuroinflammation and microglia: considerations and approaches for neurotoxicity assessment. Expert Opin. Drug Metab. Toxicol. 4 (2008) 1265-1277
38. Hawkins R.A., Peterson D.R., and Vina J.R. The complementary membranes forming the blood-brain barrier. IUBMB Life 54 (2002) 101-107
39. Hirai K., Aliev G., Nunomura A., Fujioka H., Russell R.L., Atwood C.S., Johnson A.B., Kress Y., Vinters H.V., Tabaton M., Shimohama S., Cash A.D., Siedlak S.L., Harris P.L., Jones P.K., Petersen R.B., Perry G., and Smith M.A. Mitochondrial abnormalities in Alzheimer's disease. J. Neurosci. 21 (2001) 3017-3023
40. Holopainen I.E. Organotypic hippocampal slice cultures: a model system to study basic cellular and molecular mechanisms of neuronal cell death, neuroprotection, and synaptic plasticity. Neurochem. Res. 30 (2005) 1521-1528
41. Honegger P., and Matthieu J.-M. Selective toxicity of the general anesthetic propofol for GABAergic neurons in rat brain cell cultures. J. Neurosci. Res. 45 (1996) 631-636
42. Honegger P., Pardo B., and Monnet-Tschudi F. Muscimol-induced death of GABAergic neurons in rat brain aggregating cell cultures. Dev. Brain Res. 105 (1998) 219-225
43. Honegger P., and Richelson E. Biochemical differentiation of aggregating cell cultures of different fetal rat brain regions. Brain Res. 133 (1977) 329-339
44. Jenkins S.M., and Barone S. The neurotoxicant trimethyltin induces apoptosis via caspase activation, p38 protein kinase, and oxidative stress in PC12 cells. Toxicol. Lett. 147 (2004) 63-72
45. Johansen M.L., Bak L.K., Schousboe A., Iversen P., Sorensen M., Keiding S., Vilstrup H., Gjedde A., Ott P., and Waagepetersen H.S. The metabolic role of isoleucine in detoxification of ammonia in cultured mouse neurons and astrocytes. Neurochem. Int. 50 (2007) 1042-1051
46. Kanthasamy A.G., Kitazawa M., Yang Y., Anantharam V., and Kanthasamy A. Environmental neurotoxin dieldrin induces apoptosis via caspase-3-dependent proteolytic activation of protein kinase C delta (PKCdelta): Implications for neurodegeneration in Parkinson's disease. Mol. Brain 1 (2008) 12
47. Kaur P., Aschner M., and Syversen T. Glutathione modulation influences methyl mercury induced neurotoxicity in primary cell cultures of neurons and astrocytes. Neurotoxicology 27 (2006) 492-500
48. Keller J.N., Schmitt F.A., Scheff S.W., Ding Q., Chen Q., Butterfield D.A., and Markesbery W.R. Evidence of increased oxidative damage in subjects with mild cognitive impairment. Neurology 64 (2005) 1152-1156
49. Landrigan P.J., Sonawane B., Butler R.N., Trasande L., Callan R., and Droller D. Early environmental origins of neurodegenerative disease in later life. Environ. Health Perspect. 113 (2005) 1230-1233
50. Langston J.W., Forno L.S., Tetrud J., Reeves A.G., Kaplan J.A., and Karluk D. Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure. Ann. Neurol. 46 (1999) 598-605
51. Leist M., Hartung T., and Nicotera P. The dawning of a new age of toxicology. ALTEX 25 (2008) 103-114
52. Leutgeb J.K., Frey J.U., and Behnisch T. LTP in cultured hippocampal-entorhinal cortex slices from young adult (P25-30) rats. J. Neurosci. Methods 130 (2003) 19-32
53. Mancini J.D., Autio D.M., and Atchison W.D. Continuous exposure to low concentrations of methylmercury impairs cerebellar granule cell migration in organotypic slice culture. Neurotoxicology 30 (2009) 203-208
54. Maruoka N., Murata T., Omata N., Takashima Y., Fujibayashi Y., and Wada Y. Biphasic mechanism of the toxicity induced by 1-methyl-4-phenylpyridinium ion (MPP+) as revealed by dynamic changes in glucose metabolism in rat brain slices. Neurotoxicology 28 (2007) 672-678
55. Mattson M.P., Gleichmann M., and Cheng A. Mitochondria in neuroplasticity and neurological disorders. Neuron 60 (2008) 748-766
56. McGeer P.L., and McGeer E.G. Glial reactions in Parkinson's disease. Mov. Disord. 23 (2008) 474-483
57. McGeer P.L., and McGeer E.G. Innate immunity, local inflammation, and degenerative disease. Sci. Aging Knowl. Environ. 2002 (2002) re3
58. Mena M.A., and Garcia de Yebenes J. Glial cells as players in parkinsonism: the "good," the "bad," and the "mysterious" glia. Neuroscientist 14 (2008) 544-560
59. Migliore L., Fontana I., Trippi F., Colognato R., Coppede F., Tognoni G., Nucciarone B., and Siciliano G. Oxidative DNA damage in peripheral leukocytes of mild cognitive impairment and AD patients. Neurobiol. Aging 26 (2005) 567-573
60. Miller R.L., Sun G.Y., and Sun A.Y. Cytotoxicity of paraquat in microglial cells: involvement of PKCdelta- and ERK1/2-dependent NADPH oxidase. Brain Res. 1167 (2007) 129-139
61. Monnet-Tschudi F., Hazekamp A., Perret N., Zurich M.G., Mangin P., Giroud C., and Honegger P. Delta-9-tetrahydrocannabinol accumulation, metabolism and cell-type-specific adverse effects in aggregating brain cell cultures. Toxicol. Appl. Pharmacol. 228 (2008) 8-16
62. Monnet-Tschudi F., Zurich M.G., Boschat C., Corbaz A., and Honegger P. Involvement of environmental mercury and lead in the etiology of neurodegenerative diseases. Rev. Environ. Health 21 (2006) 105-117
63. Monnet-Tschudi F., Zurich M.-G., and Honegger P. Evaluation of the toxicity of different metal compounds in the developing brain using aggregating cell cultures as a model. Toxicol. In Vitro 7 (1993) 335-339
64. Monnet-Tschudi F., Zurich M.-G., and Honegger P. Comparison of the developmental effects of two mercury compounds on glial cells and neurons in aggregate cultures of rat telencephalon. Brain Res. 741 (1996) 52-59
65. Monnet-Tschudi F., Zurich M.G., and Honegger P. Neurotoxicant-induced inflammatory response in three-dimensional brain cell cultures. Hum. Exp. Toxicol. 26 (2007) 339-346
66. Monnet-Tschudi F., Zurich M.-G., Pithon E., van Melle G., and Honegger P. Microglial responsiveness as a sensitive marker for trimethyltin (TMT) neurotoxicity. Brain Res. 690 (1995) 8-14
67. Monnet-Tschudi F., Zurich M.-G., Riederer B.M., and Honegger P. Effects of trimethyltin (TMT) on glial and neuronal cells in aggregate cultures: dependence on the developmental stage. Neurotoxicology 16 (1995) 97-104
68. Monnet-Tschudi F., Zurich M.-G., Schilter B., Costa L.G., and Honegger P. Maturation-dependent effects of chlorpyrifos and parathion and their oxygen analogs on acetylcholinesterase and neuronal and glial markers in aggregating brain cell cultures. Toxicol. Appl. Pharm. 165 (2000) 175-183
69. Monnet-Tschudi F., Zurich M.-G., Sorg O., Matthieu J.-M., Honegger P., and Schilter B. The naturally occuring food mycotoxin fumonisin B1 impairs myelin formation in aggregating brain cell culture. Neurotoxicology 20 (1999) 41-48
70. Muchowski P.J., and Wacker J.L. Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 6 (2005) 11-22
71. Murray J., and Capaldi R.A. Screening for the metabolic basis of neurodegeneration: developing a focused proteomic approach. Ann. NY Acad. Sci. 1147 (2008) 348-357
72. Nakamura T., and Lipton S.A. Cell death: protein misfolding and neurodegenerative diseases. Apoptosis (2009)
73. Olivieri G., Brack C., Muller-Spahn F., Stahelin H.B., Herrmann M., Renard P., Brockhaus M., and Hock C. Mercury induces cell cytotoxicity and oxidative stress and increases beta-amyloid secretion and tau phosphorylation in SHSY5Y neuroblastoma cells. J. Neurochem. 74 (2000) 231-236
74. Olmos C., Sandoval R., Rozas C., Navarro S., Wyneken U., Zeise M., Morales B., and Pancetti F. Effect of short-term exposure to dichlorvos on synaptic plasticity of rat hippocampal slices: involvement of acylpeptide hydrolase and alpha(7) nicotinic receptors. Toxicol. Appl. Pharmacol. 238 (2009) 37-46
75. Pardo B., and Honegger P. High sensitivity of immature GABAergic neurons to blockers of voltage-gated calcium channels. Dev. Brain Res. 115 (1999) 9-16
76. Pouly S., Storch M.K., Matthieu J.-M., Lassman H., Monnet-Tschudi F., and Honegger P. Demyelination induced by protein kinase C-activating tumor promoters in aggregating brain cell cultures. J. Neurosci. Res. 49 (1997) 121-132
77. Rock R.B., and Peterson P.K. Microglia as a pharmacological target in infectious and inflammatory diseases of the brain. J. Neuroimmune Pharmacol. 1 (2006) 117-126
78. Rosenberg R.N. The molecular and genetic basis of Alzheimer's diseases: the end of the beginning. Neurology 54 (2000) 2045-2054
79. Roy S., Zhang B., Lee V.M., and Trojanowski J.Q. Axonal transport defects: a common theme in neurodegenerative diseases. Acta Neuropathol. 109 (2005) 5-13
80. Sas K., Robotka H., Toldi J., and Vecsei L. Mitochondria, metabolic disturbances, oxidative stress and the kynurenine system, with focus on neurodegenerative disorders. J. Neurol. Sci. 257 (2007) 221-239
81. 2+. FEBS J. 272 (2005) 3593-3601
82. Schousboe A., Bak L.K., Sickmann H.M., Sonnewald U., and Waagepetersen H.S. Energy substrates to support glutamatergic and GABAergic synaptic function: role of glycogen, glucose and lactate. Neurotoxicol. Res. 12 (2007) 263-268
83. Schuh R.A., Kristian T., Gupta R.K., Flaws J.A., and Fiskum G. Methoxychlor inhibits brain mitochondrial respiration and increases hydrogen peroxide production and CREB phosphorylation. Toxicol. Sci. 88 (2005) 495-504
84. Sherer T.B., Betarbet R., Testa C.M., Seo B.B., Richardson J.R., Kim J.H., Miller G.W., Yagi T., Matsuno-Yagi A., and Greenamyre J.T. Mechanism of toxicity in rotenone models of Parkinson's disease. J. Neurosci. 23 (2003) 10756-10764
85. Sorg O., Schilter B., Honegger P., and Monnet-Tschudi F. Increased vulnerability of neurones and glial cells to low concentrations of methylmercury in a prooxidant situation. Acta Neuropathol. 96 (1998) 621-627
86. Stoppini L., Duport S., and Correges P. A new extracellular multirecording system for electrophysiological studies: application to hippocampal organotypic cultures. J. Neurosci. Methods 72 (1997) 23-33
87. Streit W.J. Microglial senescence: does the brain's immune system have an expiration date?. Trends Neurosci. 29 (2006) 506-510
88. Suh E.C., Jung Y.J., Kim Y.A., Park E.M., and Lee K.E. A beta 25-35 induces presynaptic changes in organotypic hippocampal slice cultures. Neurotoxicology 29 (2008) 691-699
89. Terzioglu M., and Larsson N.G. Mitochondrial dysfunction in mammalian ageing. Novartis Found. Symp. 287 (2007) 197-208 discussion 208-213
90. Thomas M.P., Davis M.I., Monaghan D.T., and Morrisett R.A. Organotypic brain slice cultures for functional analysis of alcohol-related disorders: novel versus conventional preparations. Alcohol Clin. Exp. Res. 22 (1998) 51-59
91. Uversky V.N., Li J., and Fink A.L. Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular NK between Parkinson's disease and heavy metal exposure. J. Biol. Chem. 276 (2001) 44284-44296
92. Uversky V.N., Li J., and Fink A.L. Pesticides directly accelerate the rate of alpha-synuclein fibril formation: a possible factor in Parkinson's disease. FEBS Lett. 500 (2001) 105-108
93. van Vliet E., Stoppini L., Balestrino M., Eskes C., Griesinger C., Sobanski T., Whelan M., Hartung T., and Coecke S. Electrophysiological recording of re-aggregating brain cell cultures on multi-electrode arrays to detect acute neurotoxic effects. Neurotoxicology 28 (2007) 1136-1146
94. 2+ on muscarinic modulation of glutamatergic synaptic transmission in rat hippocampal CA1 area. Neurotoxicology 28 (2007) 499-507
95. White L.D., Cory-Slechta D.A., Gilbert M.E., Tiffany-Castiglioni E., Zawia N.H., Virgolini M., Rossi-George A., Lasley S.M., Qian Y.C., and Basha M.R. New and evolving concepts in the neurotoxicology of lead. Toxicol. Appl. Pharmacol. 225 (2007) 1-27
96. Wu Y.N., and Johnson S.W. Rotenone reduces Mg(2+)-dependent block of NMDA currents in substantia nigra dopamine neurons. Neurotoxicology 30 (2009) 320-325
97. Zurich M.-G., Eskes C., Honegger P., Bérode M., and Monnet-Tschudi F. Maturation-dependent neurotoxicity of lead acetate in vitro: implication of glial reactions. J. Neurosci. Res. 70 (2002) 108-116
98. Zurich M.-G., Honegger P., Schilter B., Costa L.G., and Monnet-Tschudi F. Use of aggregating brain cell cultures to study developmental effects of organophosphorus insecticides. Neurotoxicology 21 (2000) 599-606
99. Zurich M.G., Honegger P., Schilter B., Costa L.G., and Monnet-Tschudi F. Involvement of glial cells in the neurotoxicity of parathion and chlorpyrifos. Toxicol. Appl. Pharmacol. 201 (2004) 97-104
100. Zurich M.G., Lengacher S., Braissant O., Monnet-Tschudi F., Pellerin L., and Honegger P. Unusual astrocyte reactivity caused by the food mycotoxin ochratoxin A in aggregating rat brain cell cultures. Neuroscience 134 (2005) 771-782
101. Zurich M.-G., Monnet-Tschudi F., Bérode M., and Honegger P. Lead acetate toxicity in vitro: dependence of the cell composition of the cultures. Toxicol. In Vitro 12 (1998) 191-196
102. Zurich M.-G., Monnet-Tschudi F., Costa L.G., Schilter B., and Honegger P. Aggregating brain cell cultures for neurotoxicological studies. In: Tiffany-Castiglioni E. (Ed). Methods in Pharmacology and Toxicology: In vitro Neurotoxicology: Principles and challenges (2004), Humana Press Inc., Totowa, NJ 243-266
103. Zurich M.-G., Monnet-Tschudi F., and Honegger P. Long-term treatment of aggregating brain cell cultures with low concentrations of lead acetate. Neurotoxicology 15 3 (1994) 715-720