Delayed treatment with systemic (s)-roscovitine provides neuroprotection and inhibits in vivo CDK5 activity increase in animal stroke models

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Menn, Benedicte ^a   Bach, Stephane ^b   Blevins, Teri L ^c   Campbell, Mark ^c   Meijer, Laurent ^b   Timsit, Serge ^d  

^a Turing Center for Living Systems CENTURI Aix Marseille University   (France)

^b STATION BIOLOGIQUE   (France)

^c MDS Inc   (Canada)

^d FACULTÉ DE MÉDECINE ET DES SCIENCES DE LA SANTÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 5; PROTEIN P25; ROSCOVITINE; NEUROPROTECTIVE AGENT; PURINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL DEATH; CELL PROTECTION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG FORMULATION; DRUG MECHANISM; DRUG PENETRATION; DRUG STRUCTURE; DRUG TARGETING; ENZYME ACTIVITY; IN VIVO STUDY; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; RAT; STEREOISOMERISM; THERAPY DELAY; ANIMAL; BRAIN ISCHEMIA; CHEMISTRY; DISEASE MODEL; DRUG ADMINISTRATION ROUTE; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; HUMAN; INJECTION; METABOLISM; MITOSIS; PATHOLOGY; STROKE; TIME;

ANIMALIA;

ANIMALS; BRAIN ISCHEMIA; CELL DEATH; CHEMISTRY, PHARMACEUTICAL; CYCLIN-DEPENDENT KINASE 5; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION ROUTES; HUMANS; INJECTIONS; MALE; MICE; MITOSIS; NEUROPROTECTIVE AGENTS; PURINES; RATS; STROKE; TIME FACTORS;

EID: 77957860649     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012117     Document Type: Article

References (44)

1. Ginsberg MA (2008) Neuroprotection for ischemic stroke: Past, present and future. Neuropharm 55: 363-389.
2. Sacco RL, Chong J, Prabhakaran S, Elkind MS (2007) Experimental treatments for acute ischemic stroke. Lancet 369: 331-341.
3. Chavez JC, Hurko O, Baronne FC, Feuerstein GZ (2009) Pharmacologic interventions for stroke: Looking beyond the thrombolysis time window into the penumbra with biomarkers, not a stopwatch. Stroke 40: e558-563.
4. Phan TG, Wright P, Markus R, Howells DW, Davis SM, et al. (2002) Salvaging the ischaemic penumbra: more than just reperfusion? Clin Exp Pharmacol Physiol 29: 1-10.
5. O'Collins VE, MacLeod M, Donnan GA, Horky LL, van der Worp BH, et al. (2006) 1,026 experimental treatments in acute stroke. Ann Neurol 59: 467-477.
6. Faden AI, Stoica B (2007) Neuroprotection: challenges and opportunities. Arch Neurol 64: 794-800.
7. Fischer M, Feuerstein G, Howells DW, Hurn PD, Kent TA, et al. (2009) Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 40: 2244-2250.
8. STAIR Stroke Therapy Academic Industry Roundtable (1999) Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 30: 2752-2758.
9. Knockaert M, Greengard P, Meijer L (2002) Pharmacological inhibitors of cyclin-dependent kinases. Trends Pharmacol Sci 23: 417-425.
10. Rashidian J, Iyirhiaro G, Park DS (2007) Cell cycle machinery and stroke. Biochem Biophys Acta 1772: 484-493.
11. Timsit S, Menn B (2007) Cerebral ischemia, cell cycle elements and Cdk5. Biotechnol J 2: 958-966.
12. Dhavan R, Tsai LH (2001) A decade of CDK5. Nat Rev Mol Cell Biol 2: 749-759.
13. Cheung ZH, Fu AK, Ip NY (2006) Synaptic roles of Cdk5: implications in higher cognitive functions and neurodegenerative diseases. Neuron 50: 13-18.
14. Byrnes KB, Faden A (2007) Role of the cell cycle proteins in CNS injury. Neurochem Res 32: 1799-1807.
15. Katchanov J, Harms C, Gertz K, Hauck L, Waeber C, et al. (2001) Mild cerebral ischemia induces loss of cyclin-dependent kinase inhibitors and activation of cell cycle machinery before delayed neuronal death. J Neurosci 21: 5045-5053.
16. Kato H, Takahashi A, Itoyama Y (2003) Cell cycle protein expression in proliferating microglia and astrocytes following transient global cerebral ischemia in the rat. Brain Res Bull 60: 215-221.
17. Timsit S, Rivera S, Ouaghi P, Guishard F, Tremblay E, et al. (1999) Increased cyclin D1 expression in dying neurons after ischemia provides a link between in vivo programmed cell death and cell cycle. Eur J Neurosci 11: 263-278.
18. Smith PD, Crocker S, Jackson-Lewis V, Jordan-Sciutto KL, Hayley S, et al. (2003) 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: 13650-13655.
19. Wang J, Lui S, Fu YP, Wang JH, Lu YM (2003) Cdk5 activation induces hippocampal CA1 cell death by directly phosphorylating NMDA receptors. Nat Neurosci 6: 1039-1047.
20. Zhang M, Li J, Chakrabarty P, Bu B, Vincent I (2004) Cyclin-dependent kinase inhibitors attenuate protein hyperphosphorylation, cytoskeletal lesion formation, and motor defects in Niemann-Pick Type C mice. Am J Pathol 165: 843-853.
21. Wen Y, Yang S, Liu R, Perez EJ, Brun-Zinkernagel AM, et al. (2006) Cdk5 is involved in NFT-like tauopathy induced by transient cerebral ischemia in female rats. Biochim Biophys Acta 1772: 473-483.
22. Zhang Q, Chen C, Lu J, Xie M, Pan D, et al. (2009) Cell cycle inhibition attenuates microglial proliferation and production of IL-b, MIP-1a, and NO after focal cerebral ischemia in the rat. Glia 57: 908-920.
23. Hilton GD, Stoica B, Byrnes KR, Faden AI (2008) Roscovitine reduces neuronal loss, glial activation, and neurologic deficits after brain trauma. J Cereb Flow Met 28: 1845-1859.
24. Sallam H, Jimenez P, Song H, Vita M, Cedazo-Minguez A, et al. (2008) Age-dependent pharmacokinetics and effect of roscovitine on Cdk5 and Erk1/2 in the rat brain. Pharmacol Res 58: 32-37.
25. Vita M, Abdel-Rehim M, Olofsson S, Hassan Z, Meurling L, et al. (2005) Tissue distribution, pharmacokinetics and identification of roscovitine metabolites in rat. Eur J Pharm Sci 25: 91-103.
26. Guegan C, Ceballos-Picot I, Nicole A, Kato H, Onteniente B, et al. (1998) Recruitment of several neuroprotective pathways after permanent focal ischemia in mice. Exp Neurol 154: 371-380.
27. Tamura A, Graham D, McCulloch J, Teasdale GM (1981) Focal cerebral ischemia in the rat: 1. Description of technique and early neuropathological consequences following middle cerebral artery occlusion. J Cereb Flow Met 1: 53-60.
28. Strickley RG (2004) Solubilizing excipients in oral and injectable formulations. Pharm Res 21: 201-230.
29. Portera-Cailliau C, Price DJ, Martin LJ (1997) Non-NMDA and NMDA receptor-mediated excitotoxic neuronal deaths in the adult brain are morphologically distinct: Further evidence for an apoptosis- necrosis continuum. J Comp Neurol 372: 88-104.
30. Bach S, Knockaert M, Reinhardt J, Lozach O, Schmitt S, et al. (2005) Roscovitine targets, protein kinases and pyridoxal kinase. J Biol Chem 280: 31208-31219.
31. Tang L, Li MH, Cao P, Wang F, Chang WR, et al. (2005) Crystal structure of pyridoxal kinase in complex with roscovitine and derivatives. J Biol Chem 280: 31220-31229.
32. Padmanabhan J, Park DS, Greene LA, Shelanski ML (1999) Role of cell cycle regulatory proteins in cerebellar granule neuron apoptosis. J Neurosci 19: 8747-8756.
33. Frade JM (2000) Unscheduled re-entry into the cell cycle induced by NGF precedes cell death in nascent retinal neurons. J Cell Sci 113: 1139-1148.
34. Padmanabhan J, Brown K, Shelanski ML (2007) Cell cycle inhibition and retinoblastoma protein overexpression prevent Purkinje cell death in organo-typic slice cultures. Dev Neurobiol 67: 818-826.
35. Calabrese EJ (2008) Drug therapies for stroke and traumatic brain injury often display U-shaped dose responses: occurrence, mechanisms, and clinical implications. Crit Rev Toxicol 38: 557-577.
36. Lee MS, Kwon Y, Li M, Peng J, Friedlander RM, et al. (2000) Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405: 360-364.
37. Meijer L, Borgne A, Mulner O, Chong JP, Blow JJ, et al. (1997) Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem 243: 527-536.
38. Chu CT, Levinthal D, Kulich SM, Chalovich EM, DeFranco DB (2004) Oxidative neuronal injury. The dark side of ERK1/2. Eur J Biochem 271: 2060-2066.
39. Osuga H, Osuga S, Wang F, Fetni R, Hogan MJ, et al. (2000) Cyclin-dependent kinases as a therapeutic target for stroke. Proc Natl Acad Sci USA 97: 10254-10259.
40. Wang F, Corbett D, Osuga H, Osuga S, Ikeda JE, et al. (2002) Inhibition of cyclin-dependent kinases improves CA1 neuronal survival and behavioral performance after global ischemia in the rat. J Cereb Blood Flow Metab 22: 171-182.
41. Leclerc S, Garnier M, Hoessel R, Marko D, Bibb JA, et al. (2001) Indirubins inhibit glycogen synthase kinase-3 beta and CDK5/p25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer's disease. A property common to most cyclin-dependent kinase inhibitors? J Biol Chem 276: 251-260.
42. Aldoss IT, Tashi T, Ganti AK (2009) Seliciclib in malignancies. Expert Opin Investig Drugs 18: 1957-1965.
43. Zea-Longa E, Weinstein P, Carlson S, Cummins R (1989) Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20: 84-91.
44. Buerli T, Pellegrino C, Baer K, Lardi-Studler B, Chudotvorova I, et al. (2007) Efficient transfection of DNA or shRNA vectors into neurons using magnetofection. Nat Protoc 2: 3090-3101.