Prevention of the degeneration of human dopaminergic neurons in an astrocyte co-culture system allowing endogenous drug metabolism

British Journal of Pharmacology

Volumn 172, Issue 16, 2015, Pages 4119-4132

  Efremova, Liudmila ^a   Schildknecht, Stefan ^a   Adam, Martina ^a   Pape, Regina ^a   Gutbier, Simon ^a   Hanf, Benjamin ^a   Bürkle, Alexander ^a   Leist, Marcel ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; 1'5 ISOQUINOLINEDIOL; 1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; 7 NITROINDAZOLE; ASCORBIC ACID; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE INHIBITOR; CEP 1347; DEFEROXAMINE; DOPAMINE TRANSPORTER; FASUDIL; GLUTATHIONE DISULFIDE; MINOCYCLINE; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; N(G) METHYLARGININE; NEUROPROTECTIVE AGENT; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; POLY(ADENOSINE DIPHOSPHATE RIBOSE); RASAGILINE; RHO KINASE INHIBITOR; SELEGILINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VANOXERINE; VELIPARIB; 1,5-DIHYDROXYISOQUINOLINE; ISOQUINOLINE DERIVATIVE; NEUROTOXIN;

ANIMAL CELL; ARTICLE; ASTROCYTE CULTURE; BRAIN TISSUE; CELL VIABILITY; COCULTURE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG METABOLISM; ENZYME ACTIVATION; FEMALE; FETUS; GLIA CELL; HUMAN; HUMAN CELL; IMAGING; MONOCULTURE; MOUSE; MOUSE MODEL; NERVE CELL DEGENERATION; NERVE CELL NETWORK; NEURITE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; ANIMAL; CELL CULTURE; CELL LINE; DRUG EFFECTS; GLIA; METABOLISM; MPTP POISONING; RAT;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; 1-METHYL-4-PHENYLPYRIDINIUM; ANIMALS; CELL LINE; CELLS, CULTURED; COCULTURE TECHNIQUES; DOPAMINERGIC NEURONS; HUMANS; ISOQUINOLINES; MICE; MPTP POISONING; NEUROGLIA; NEUROPROTECTIVE AGENTS; NEUROTOXINS; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; RATS;

EID: 84937513010     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13193     Document Type: Article

References (69)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: Transporters. Br J Pharmacol 170: 1706-1796.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Enzymes. Br J Pharmacol 170: 1797-1867.
3. Allen NJ, Barres BA, (2009). Neuroscience: glia-more than just brain glue. Nature 457: 675-677.
4. 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.
5. Burke RE, O'Malley K, (2013). Axon degeneration in Parkinson's disease. Exp Neurol 246: 72-83.
6. Cacci E, Ajmone-Cat MA, Anelli T, Biagioni S, Minghetti L, (2008). In vitro neuronal and glial differentiation from embryonic or adult neural precursor cells are differently affected by chronic or acute activation of microglia. Glia 56: 412-425.
7. Caudle WM, Guillot TS, Lazo CR, Miller GW, (2012). Industrial toxicants and Parkinson's disease. Neurotoxicology 33: 178-188.
8. Chong CM, Shen M, Zhou ZY, Pan P, Hoi PM, Li S, et al. (2014). Discovery of a benzofuran derivative (MBPTA) as a novel ROCK inhibitor that protects against MPP(+)-induced oxidative stress and cell death in SH-SY5Y cells. Free Radic Biol Med 74: 283-293.
9. Dauer W, Przedborski S, (2003). Parkinson's disease: mechanisms and models. Neuron 39: 889-909.
10. Falsig J, Latta M, Leist M, (2004a). Defined inflammatory states in astrocyte cultures: correlation with susceptibility towards CD95-driven apoptosis. J Neurochem 88: 181-193.
11. Falsig J, Porzgen P, Lotharius J, Leist M, (2004b). Specific modulation of astrocyte inflammation by inhibition of mixed lineage kinases with CEP-1347. J Immunol 173: 2762-2770.
12. Fischer JM, Popp O, Gebhard D, Veith S, Fischbach A, Beneke S, et al. (2014). Poly(ADP-ribose)-mediated interplay of XPA and PARP1 leads to reciprocal regulation of protein function. FEBS J 281: 3625-3641.
13. Frakes AE, Ferraiuolo L, Haidet-Phillips AM, Schmelzer L, Braun L, Miranda CJ, et al. (2014). Microglia induce motor neuron death via the classical NF-kappaB pathway in amyotrophic lateral sclerosis. Neuron 81: 1009-1023.
14. Giordano G, Costa LG, (2012). Morphological assessment of neurite outgrowth in hippocampal neuron-astrocyte co-cultures. Curr Protoc Toxicol 11: Unit 11.16.
15. Grunewald T, Beal MF, (1999). NOS knockouts and neuroprotection. Nat Med 5: 1354-1355.
16. Hirt UA, Gantner F, Leist M, (2000). Phagocytosis of nonapoptotic cells dying by caspase-independent mechanisms. J Immunol 164: 6520-6529.
17. Kaneko M, Saito Y, Saito H, Matsumoto T, Matsuda Y, Vaught JL, et al. (1997). Neurotrophic 3,9-bis[(alkylthio)methyl]-and-bis(alkoxymethyl)-K-252a derivatives. J Med Chem 40: 1863-1869.
18. Kawamitsu H, Hoshino H, Okada H, Miwa M, Momoi H, Sugimura T, (1984). Monoclonal antibodies to poly(adenosine diphosphate ribose) recognize different structures. Biochemistry 23: 3771-3777.
19. Kincses ZT, Vecsei L, (2011). Pharmacological therapy in Parkinson's disease: focus on neuroprotection. CNS Neurosci Ther 17: 345-367.
20. Kingham PJ, Pocock JM, (2001). Microglial secreted cathepsin B induces neuronal apoptosis. J Neurochem 76: 1475-1484.
21. Krug AK, Balmer NV, Matt F, Schonenberger F, Merhof D, Leist M, (2013). Evaluation of a human neurite growth assay as specific screen for developmental neurotoxicants. Arch Toxicol 87: 2215-2231.
22. Krug AK, Gutbier S, Zhao L, Poltl D, Kullmann C, Ivanova V, et al. (2014). Transcriptional and metabolic adaptation of human neurons to the mitochondrial toxicant MPP. Cell Death Dis 5: e1222.
23. Langston JW, Langston EB, Irwin I, (1984). MPTP-induced parkinsonism in human and non-human primates-clinical and experimental aspects. Acta Neurol Scand Suppl 100: 49-54.
24. Lee M, McGeer E, McGeer PL, (2015). Activated human microglia stimulate neuroblastoma cells to upregulate production of beta amyloid protein and tau: implications for Alzheimer's disease pathogenesis. Neurobiol Aging 36: 42-52.
25. Lee Y, Karuppagounder SS, Shin JH, Lee YI, Ko HS, Swing D, et al. (2013). Parthanatos mediates AIMP2-activated age-dependent dopaminergic neuronal loss. Nat Neurosci 16: 1392-1400.
26. Lee Y, Kang HC, Lee BD, Lee YI, Kim YP, Shin JH, (2014). Poly (ADP-ribose) in the pathogenesis of Parkinson's disease. BMB Rep 47: 424-432.
27. Leist M, Volbracht C, Fava E, Nicotera P, (1998). 1-Methyl-4-phenylpyridinium induces autocrine excitotoxicity, protease activation, and neuronal apoptosis. Mol Pharmacol 54: 789-801.
28. Liu S, Tian Z, Yin F, Zhao Q, Fan M, (2009). Generation of dopaminergic neurons from human fetal mesencephalic progenitors after co-culture with striatal-conditioned media and exposure to lowered oxygen. Brain Res Bull 80: 62-68.
29. Lotharius J, Falsig J, van Beek J, Payne S, Dringen R, Brundin P, et al. (2005). Progressive degeneration of human mesencephalic neuron-derived cells triggered by dopamine-dependent oxidative stress is dependent on the mixed-lineage kinase pathway. J Neurosci 25: 6329-6342.
30. Malchiodi-Albedi F, Domenici MR, Paradisi S, Bernardo A, Ajmone-Cat MA, Minghetti L, (2001). Astrocytes contribute to neuronal impairment in beta A toxicity increasing apoptosis in rat hippocampal neurons. Glia 34: 68-72.
31. Mandir AS, Przedborski S, Jackson-Lewis V, Wang ZQ, Simbulan-Rosenthal CM, Smulson ME, et al. (1999). Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1, 2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism. Proc Natl Acad Sci U S A 96: 5774-5779.
32. Maroney AC, Finn JP, Bozyczko-Coyne D, O'Kane TM, Neff NT, Tolkovsky AM, et al. (1999). CEP-1347 (KT7515), an inhibitor of JNK activation, rescues sympathetic neurons and neuronally differentiated PC12 cells from death evoked by three distinct insults. J Neurochem 73: 1901-1912.
33. McGeer PL, McGeer EG, (2008). Glial reactions in Parkinson's disease. Mov Disord 23: 474-483.
34. McNaught KS, Jenner P, (1999). Altered glial function causes neuronal death and increases neuronal susceptibility to 1-methyl-4-phenylpyridinium- and 6-hydroxydopamine-induced / toxicity in astrocytic ventral mesencephalic co-cultures. J Neurochem 73: 2469-2476.
35. Meissner WG, Frasier M, Gasser T, Goetz CG, Lozano A, Piccini P, et al. (2011). Priorities in Parkinson's disease research. Nat Rev Drug Discov 10: 377-393.
36. Miller JD, Ganat YM, Kishinevsky S, Bowman RL, Liu B, Tu EY, et al. (2013). Human iPSC-based modeling of late-onset disease via progerin-induced aging. Cell Stem Cell 13: 691-705.
37. Morizane A, Darsalia V, Guloglu MO, Hjalt T, Carta M, Li JY, et al. (2010). A simple method for large-scale generation of dopamine neurons from human embryonic stem cells. J Neurosci Res 88: 3467-3478.
38. Olanow CW, Kordower JH, (2009). Modeling Parkinson's disease. Ann Neurol 66: 432-436.
39. Pan-Montojo F, Schwarz M, Winkler C, Arnhold M, O'Sullivan GA, Pal A, et al. (2012). Environmental toxins trigger PD-like progression via increased alpha-synuclein release from enteric neurons in mice. Sci Rep 2: 898.
40. Parkinson Study Group PI (2007). Mixed lineage kinase inhibitor CEP-1347 fails to delay disability in early Parkinson disease. Neurology 69: 1480-1490.
41. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al.; NC-IUPHAR (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledge base of drug targets and their ligands. Nucl Acids Res 42 (Database Issue): D1098-1106.
42. Peng J, Liu Q, Rao MS, Zeng X, (2013). Using human pluripotent stem cell-derived dopaminergic neurons to evaluate candidate Parkinson's disease therapeutic agents in MPP+ and rotenone models. J Biomol Screen 18: 522-533.
43. Perrier AL, Tabar V, Barberi T, Rubio ME, Bruses J, Topf N, et al. (2004). Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci U S A 101: 12543-12548.
44. Piani D, Spranger M, Frei K, Schaffner A, Fontana A, (1992). Macrophage-induced cytotoxicity of N-methyl-D-aspartate receptor positive neurons involves excitatory amino acids rather than reactive oxygen intermediates and cytokines. Eur J Immunol 22: 2429-2436.
45. Pizzurro DM, Dao K, Costa LG, (2014). Astrocytes protect against diazinon- and diazoxon-induced inhibition of neurite outgrowth by regulating neuronal glutathione. Toxicology 318: 59-68.
46. Poltl D, Schildknecht S, Karreman C, Leist M, (2012). Uncoupling of ATP-depletion and cell death in human dopaminergic neurons. Neurotoxicology 33: 769-779.
47. Reinhardt P, Glatza M, Hemmer K, Tsytsyura Y, Thiel CS, Hoing S, et al. (2013). Derivation and expansion using only small molecules of human neural progenitors for neurodegenerative disease modeling. PLoS ONE 8: e59252.
48. Sanchez-Danes A, Richaud-Patin Y, Carballo-Carbajal I, Jimenez-Delgado S, Caig C, Mora S, et al. (2012). Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson's disease. EMBO Mol Med 4: 380-395.
49. Schapira A, Bate G, Kirkpatrick P, (2005). Rasagiline. Nat Rev Drug Discov 4: 625-626.
50. Schildknecht S, Poltl D, Nagel DM, Matt F, Scholz D, Lotharius J, et al. (2009). Requirement of a dopaminergic neuronal phenotype for toxicity of low concentrations of 1-methyl-4-phenylpyridinium to human cells. Toxicol Appl Pharmacol 241: 23-35.
51. Schildknecht S, Kirner S, Henn A, Gasparic K, Pape R, Efremova L, et al. (2012). Characterization of mouse cell line IMA 2.1 as a potential model system to study astrocyte functions. ALTEX 29: 261-274.
52. Schildknecht S, Karreman C, Poltl D, Efremova L, Kullmann C, Gutbier S, et al. (2013). Generation of genetically-modified human differentiated cells for toxicological tests and the study of neurodegenerative diseases. ALTEX 30: 427-444.
53. Scholz D, Poltl D, Genewsky A, Weng M, Waldmann T, Schildknecht S, et al. (2011). Rapid, complete and large-scale generation of post-mitotic neurons from the human LUHMES cell line. J Neurochem 119: 957-971.
54. Schule B, Pera RA, Langston JW, (2009). Can cellular models revolutionize drug discovery in Parkinson's disease? Biochim Biophys Acta 1792: 1043-1051.
55. Schulz JB, Matthews RT, Muqit MM, Browne SE, Beal MF, (1995). Inhibition of neuronal nitric oxide synthase by 7-nitroindazole protects against MPTP-induced neurotoxicity in mice. J Neurochem 64: 936-939.
56. Schulz TC, Noggle SA, Palmarini GM, Weiler DA, Lyons IG, Pensa KA, et al. (2004). Differentiation of human embryonic stem cells to dopaminergic neurons in serum-free suspension culture. Stem Cells 22: 1218-1238.
57. Smeyne M, Goloubeva O, Smeyne RJ, (2001). Strain-dependent susceptibility to MPTP and MPP(+)-induced parkinsonism is determined by glia. Glia 34: 73-80.
58. Sofroniew MV, Vinters HV, (2010). Astrocytes: biology and pathology. Acta Neuropathol 119: 7-35.
59. Sun X, Liu J, Crary JF, Malagelada C, Sulzer D, Greene LA, et al. (2013). ATF4 protects against neuronal death in cellular Parkinson's disease models by maintaining levels of parkin. J Neurosci 33: 2398-2407.
60. Tonges L, Frank T, Tatenhorst L, Saal KA, Koch JC, Szego EM, et al. (2012). Inhibition of rho kinase enhances survival of dopaminergic neurons and attenuates axonal loss in a mouse model of Parkinson's disease. Brain 135: 3355-3370.
61. Tower DB, Young OM, (1973). The activities of butyrylcholinesterase and carbonic anhydrase, the rate of anaerobic glycolysis, and the question of a constant density of glial cells in cerebral cortices of various mammalian species from mouse to whale. J Neurochem 20: 269-278.
62. Volbracht C, Leist M, Nicotera P, (1999). ATP controls neuronal apoptosis triggered by microtubule breakdown or potassium deprivation. Mol Med 5: 477-489.
63. Weidele K, Kunzmann A, Schmitz M, Beneke S, Burkle A, (2010). Ex vivo supplementation with nicotinic acid enhances cellular poly(ADP-ribosyl)ation and improves cell viability in human peripheral blood mononuclear cells. Biochem Pharmacol 80: 1103-1112.
64. Yacoubian TA, Standaert DG, (2009). Targets for neuroprotection in Parkinson's disease. Biochim Biophys Acta 1792: 676-687.
65. Youdim MB, (2010). Why do we need multifunctional neuroprotective and neurorestorative drugs for Parkinson's and Alzheimer's diseases as disease modifying agents. Exp Neurobiol 19: 1-14.
66. Zeng X, Chen J, Deng X, Liu Y, Rao MS, Cadet JL, et al. (2006). An in vitro model of human dopaminergic neurons derived from embryonic stem cells: MPP+ toxicity and GDNF neuroprotection. Neuropsychopharmacology 31: 2708-2715.
67. Zhang Y, Pak C, Han Y, Ahlenius H, Zhang Z, Chanda S, et al. (2013). Rapid single-step induction of functional neurons from human pluripotent stem cells. Neuron 78: 785-798.
68. Zhao X, Zhai S, An MS, Wang YH, Yang YF, Ge HQ, et al. (2013). Neuroprotective effects of protocatechuic aldehyde against neurotoxin-induced cellular and animal models of Parkinson's disease. PLoS ONE 8: e78220.
69. Zimmer B, Kuegler PB, Baudis B, Genewsky A, Tanavde V, Koh W, et al. (2011). Coordinated waves of gene expression during neuronal differentiation of embryonic stem cells as basis for novel approaches to developmental neurotoxicity testing. Cell Death Differ 18: 383-395.