Indirubins deplete striatal monoamines in the Intact and MPTP-treated mouse brain and block kainate-induced striatal astrogliosis

Neurotoxicology and Teratology

Volumn 32, Issue 2, 2010, Pages 212-219

  Magiatis, Prokopios ^a   Polychronopoulos, Panagiotis ^a   Skaltsounis, Alexios Leandros ^a   Lozach, Olivier ^b   Meijer, Laurent ^b   Miller, Diane B ^c   O'Callaghan, James P ^c  

^a UNIVERSITY OF ATHENS   (Greece)

^b Protein Phosphorylation and Human Disease Group   (France)

^c Health Effects Laboratory Division   (United States)

Author keywords

Astrogliosis; Dopamine; Indirubin; Kainate; MPTP; Serotonin

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 5 AMINO 6 BROMOINDIRUBIN; 5 BROMOINDURUBIN 3' OXIME; 6 BROMOINDIRUBIN 3' OXIME; CYCLIN DEPENDENT KINASE; DOPAMINE; GLYCOGEN SYNTHASE KINASE 3; INDIRUBIN; KAINIC ACID; SEROTONIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BROMINATION; CATECHOLAMINE DEPLETION; CHEMICAL ANALYSIS; CONTROLLED STUDY; CORPUS STRIATUM; DIMERIZATION; DOPAMINERGIC TRANSMISSION; DRUG MECHANISM; DRUG SCREENING; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME INHIBITION; FEMALE; HIPPOCAMPUS; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; SEROTONIN METABOLISM;

ANIMALS; ASTROCYTES; BASAL GANGLIA DISEASES; BIOGENIC MONOAMINES; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE; FEMALE; GLIOSIS; INDOLES; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; NEUROTOXINS; OXIMES; PARKINSONIAN DISORDERS; SEROTONIN; TREATMENT OUTCOME;

MUS;

EID: 77949266506     PISSN: 08920362     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ntt.2009.12.005     Document Type: Article

References (35)

1. Adachi J., Mori Y., Matsui S., Takigami H., Fujino J., Kitagawa H., Miller III C.A., Kato T., Saeki K., and Matsuda T. Indirubin and indigo are potent aryl hydrocarbon receptor ligands present in human urine. J. Biol. Chem (2001) 27631475-27631478
2. Beauchard A., Ferandin Y., Frere S., Lozach O., Blairvacq M., Meijer L., Thierya V., and Besson T. Synthesis of novel 5-substituted indirubins as protein kinases inhibitors. Bioorg. Med. Chem. 14 (2006) 6434-6443
3. Benkovic S.A., O'Callaghan J.P., and Miller D.B. Sensitive indicators of injury reveal hippocampal damage in C57BL/6 J mice treated with kainic acid in the absence of tonic-clonic seizures. Brain Res. 1024 (2004) 59-76
4. Benkovic S.A., O'Callaghan J.P., and Miller D.B. Regional neuropathology following kainic acid intoxication in adult and aged C57Bl/6 J mice. Brain Res. 1070 (2006) 215-231
5. Cruz J.C., Tseng H.-C., Goldman J.A., Shiih H., and Tsai L.-H. Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron 40 (2003) 471-483
6. O. Engmann, K.P Giese, Crosstalk between Cdk5 and GSK3β: implications for Alzheimer's Disease. Front Mol Neurosci 2009;2:2 (in press), doi:10.3389/neuro.02.002.2009.
7. Guengerich P.F., Martin M.V., McCormick W.A., Nguyen L.P., Glover E., and Bradfield C.A. Aryl hydrocarbon receptor response to indigoids in vitro and in vivo. Arch. Biochem. Biophys. 423 (2004) 309-316
8. Jnaneshwar G.K., and Deshpande V.H. Synthesis of convolutamydine A from isatin. J. Chem.Res. (1999) 632-633 S
9. Hoessel R., Leclerc S., Endicott J., Noble M., Lawrie A., Tunnah P., Leost M., Damiens E., Marie D., Marko D., Niederberger E., Tang W., Eisenbrand G., and Meijer L. Indirubin, the active constituent of a Chinese antileukaemia medicine, inhibits cyclin-dependent kinases. Nat. Cell Biol. 1 (1999) 60-67
10. Kajta M., Domin H., Grynkiewicz G., and Lason W. Genistein inhibits glutamate-induced apoptoci process in primary neuronal cell cultures: an involvement of aryl hydrocarbon receptor and estrogen receptor/glycogen synthase kinase-3beta intracellular signaling pathway. Neuroscience 145 (2007) 592-604
11. Kim D., Frank C.L., Dobbin M.M., Tsunemoto R.K., Tu W., Peng P.L., Guan J.-S., Lee B.-H., Moy L.Y., Giusti P., Broodie N., Mazitschek R., Delalle I., Haggarty S.J., Neve R.L., and Tsai L.-H. Deregulation of HDAC1 by p25/Cdk5 in neurotoxicit. Neuron 60 (2008) 803-817
12. Kosmopoulou M.N., Leonidas D.D., Chysina E.D., Bischler N., Eisenbrand G., Sakarellos C.E., Pauptit R., and Oikonomakos N.G. Binding of the potential antitumour agent indirubin-5-sulphonate at the inhibitor site of rabbit muscle glycogen phosphorylase b. Comparison with ligand binding to pCDK2-cyclin A complex. Eur. J. Biochem. 271 (2004) 2280-2290
13. Knockaert M., Blondel M., Bach S., Leost M., Elbi C., Hager G., Naggy S.R., Ham D., Denison M., Ffrench M., Ryan X.P., Magiatis P., Polychronopoulos P., Greengard P., Skaltsounis L., and Meijer L. Independent actions on cyclin-dependent kinases and aryl hydrocarbon receptor mediate the anti-proliferative effects of indirubins. Oncogene 23 (2004) 4400-4412
14. Kurschner V.C., Petruzzi R.L., Golden G.T., Berrettini W.H., and Ferraro T.N. Kainate and AMPA receptor binding in seizure-prone and seizure-resistant inbred mouse strains. Brain Res. 780 (1998) 1-8
15. Leclerc S., Garnier M., Hoessel R., Marko D., Bibb J.A., Snyder G.L., Greengard P., Biernat J., Mandelkow E.-M., Eisenbrand G., and Meijer L. Indirubins inhibit glycogen synthase kinase-3β and CDK5/p25, two kinases involved in abnormal tau phosphorylation in Alzheimer's disease - a property common to most CDK inhibitors ?. J. Biol. Chem. 276 (2001) 251-260
16. Luellen B.A., Miller D.B., Chisnell A.C., Murphy D.L., O'Callaghan J.P., and Andrews A.M. Neuronal and astroglial responses to the serotonin and norepinephrine neurotoxin: 1-methyl-4-(2′-aminophenyl)-1,2,3,6-tetrahydro-pyridine. J. Pharmacol. Exp. Ther. 307 (2003) 923931
17. Meijer L., Skaltsounis A.L., Magiatis P., Polychonopoulos P., Knockaert M., Leost M., Ryan X.P., Vonica C.D., Brivanlou A., Dajani R., Tarricone A., Musacchio A., Roe S.M., Pearl L., and Greengard P. GSK-3 selective inhibitors derived from Tyrian purple indirubins. Chem. & Biol. 10 (2003) 1255-1266
18. In: Meijer L., Guyard N., Skaltsounis L.A., and Eisenbrand G. (Eds). Indirubin, the red shade of indigo. Editions «Life in Progress» (2006), Station Biologique, Roscoff. 9-782951-802902 27 chapters, 297. pp
19. Meyer D.A., Richer E., Benkovic S.A., Hayashi K., Tansy J.W., Hale C.F., Moy L.Y., Kim Y., O'Callaghan J.P., Tsai L.H., Greengard P., Nairn A.C., Cowan C.W., Miller D.B., Antich P., and Bibb J.A. Striatal dysregulation of Cdk5 alters locomotor responses to cocaine, motor learning, and dendritic morphology. PNAS 105 (2008) 18561-18566
20. Miller D.B., and O'Callaghan J.P. Environment-, drug- and stress-induced alterations in body temperature affect the neurotoxicity of substituted amphetamines in the C57Bl/6 J mouse. J. Pharmacol. Exp. Ther. 270 (1994) 752-760
21. O'Callaghan J.P., Miller D.B., and Reinhard Jr. J.F. Characterization of the origins of astrocyte response to injury using the dopaminergic neurotoxicant, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Brain Res (1990) 73-80
22. O'Callaghan J.P. Quantification of glial fibrillary acidic protein: comparison of slot-immunobinding assays with a novel sandwich ELISA. Neurotoxicol. Teratol. 13 (1991) 275-281
23. O'Callaghan J.P. Quantitative features of reactive gliosis following toxicant-induced damage of the CNS. Ann. NY Acad. Sci. 679 (1993) 195-210
24. O'Callaghan J.P. Measurement of glial fibrillary acidic protein. In: Costa L.G. (Ed). Current Protocols in Toxicology (2002), John Wiley & Sons, New York 12.81.1-12.8.12
25. O'Callaghan J.P., and Sriram K. Focused microwave irradiation of the brain preserves in vivo protein phosphorylation: comparison with other methods of sacrifice and analysis of multiple phosphoproteins. J. Neurosci. Methods 135 (2004) 159-168
26. O'Callaghan J.P., and Sriram K. GFAP and other glial proteins as biomarkers of neurotoxicity. Expert Opinion in Drug Safety 4 (2005) 433-442
27. Polychronopoulos P., Magiatis P., Skaltsounis L., Myrianthopoulos V., Mikros E., Tarricone A., Musacchio A., Roe S.M., Pearl L., Leost M., Greengard P., and Meijer L. Structural basis for the synthesis of indirubins as potent and selective inhibitors of glycogen synthase kinase-3 and cyclin-dependent kinases. J. Med. Chem. 47 (2004) 935-946
28. Primot A., Baratte B., Gompel M., Borgne A., Liabeuf S., Romette J.L., Costantini F., and Meijer L. Purification of GSK-3 by affinity chromatography on immobilised axin. Protein Expr. & Purif. 3 (2000) 394-404
29. Qu D., Rashidian J., Mount M.P., Aleyasin H., Parsanejad M., Lira A., Haque E., Zhang Y., Callaghan S., Daigle M., Rousseaux M.W.C., Slack R.S., Albert P.R., Voincent I., Woulfe J.M., and Park D.S. Role of Cdk5-mediated phosphorylation of Prx2 in MPTP toxicity and Parkinson's disease. Neuron 55 (2007) 37-52
30. Ribas J., Bettayeb K., Ferandin Y., Knockaert M., Totzke F., Schächtele C., Mester J., Polychronopoulos P., Magiatis P., Skaltsounis A.L., Boix J., and Meijer L. 7-bromo-indirubins induce caspase-independent cell death. Oncogene 25 (2006) 6304-6318
31. Smith P.D., Crocker S.J., Jackson-Lewis V., Jordan-Sciutto K.L., Hayley S., Mount M.P., O'Hare M.J., Callaghan S., Slack R.S., Przedborski S., Anisman H., and Park D.S. Cyclin-dependent kinase 5 is a mediator of dopaminergic neuron loss in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. USA 100 (2003) 13650-13655
32. Sriram K., Benkovic S.A., Hebert M.A., Miller D.B., and O'Callaghan J.P. Activation of the gp130-JAK/STAT3 pathway in astrocytes precedes the induction of GFAP in the MPTP model of dopaminergic neurodegeneration: key signaling pathway for astrogliosis?. J. Biol. Chem. 279 (2004) 19936-19947
33. Sriram K., Miller D.B., and O'Callaghan J.P. Minocycline attenuates microglial activation but fails to mitigate striatal dopaminergic neurotoxicity : role of tumor necrosis factor-α. J. Neurochem. 96 (2006) 706-718
34. Wang W., Yang Y., Ying C., Li W., Ruan H., Zhu X., You Y., Han Y., Chen R., Wang Y., and Li M. Inhibition of glycogen synthase kinase-3beta protect dopaminergic neurons from MPTP toxicity. Neuropharmacology 52 (2007) 1678-1684
35. Wei F.-Y., Tomizawa K., Ohshima T., Asada A., Saito T., Nguyen C., Bibb J.A., Ishiguro K., Kulkarni A.B., Pant H.C., Mikoshiba K., Matsui H., and Hisanaga S.J. Control of cyclin-dependent kinase 5 (Cdk5) activity by glutamatergtic regulation of p35 stability. Neurochem. 93 (2005) 502-512