Selective CDK inhibitor limits neuroinflammation and progressive neurodegeneration after brain trauma

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 1, 2012, Pages 137-149

  Kabadi, Shruti V ^a,b   Stoica, Bogdan A ^a,b   Byrnes, Kimberly R ^b,c   Hanscom, Marie ^a   Loane, David J ^a,b   Faden, Alan I ^a,b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

brain trauma; cell cycle; cyclin dependent kinases; microglial activation; neurodegeneration

Indexed keywords

CYCLIN A; CYCLIN D1; FODRIN; ROSCOVITINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; CELL LOSS; CELL STRUCTURE; CELL SURVIVAL; COGNITION; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; MICROGLIA; MOUSE; NERVE DEGENERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; TRAUMATIC BRAIN INJURY;

ANIMALS; APOPTOSIS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; BRAIN INJURIES; CARRIER PROTEINS; CELL CYCLE; CYCLIN A; CYCLIN D1; CYCLIN-DEPENDENT KINASES; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICROFILAMENT PROTEINS; MICROGLIA; MOTOR ACTIVITY; NEURONS; NEUROPROTECTIVE AGENTS; PURINES; TIME FACTORS;

EID: 84855360054     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2011.117     Document Type: Article

References (47)

1. Arendt T (2003) Synaptic plasticity and cell cycle activation in neurons are alternative effector pathways: the 'Dr Jekyll and Mr Hyde concept' of Alzheimer's disease or disease or the yin and yang of neuroplasticity. Prog Neurobiol 71:83-248 (Pubitemid 38004483)
2. Bach S, Knockaert M, Reinhardt J, Lozach O, Schmitt S, Baratte B, Koken M, Coburn S, Tang L, Jiang T, Liang D, Galons H, Dierick J, Pinna L, Meggio F, Totzke F, Schächtele C, Lerman A, Carnero A, Wan Y, Gray N, Meijer L (2005) Roscovitine targets, protein kinases and pyridoxal kinase. J Biol Chem 280:31208-19 (Pubitemid 41291858)
3. Bain J, Plater L, Elliott M, Shapiro N, Hastie C, McLauchlan H, Klevernic I, Arthur J, Alessi D, Cohen P (2007) The selectivity of protein kinase inhibitors: a further update. Biochem J 408:297-315
4. Bramlett H, Dietrich W (2007) Progressive damage after brain and spinal cord injury: pathomechanisms and treatment strategies. Prog Brain Res 161:125-41 (Pubitemid 47017402)
5. Byrnes K, Faden A (2007) Role of cell cycle proteins in CNS injury. Neurochem Res 32:1799-807 (Pubitemid 47428847)
6. Byrnes K, Stoica B, Fricke S, Di Giovanni S, Faden A (2007) Cell cycle activation contributes to post-mitotic cell death and secondary damage after spinal cord injury. Brain 130:2977-92 (Pubitemid 350033958)
7. Cernak I (2005) Animal models of head trauma. NeuroRx 2:410-22 (Pubitemid 41444875)
8. Cernak I, Stoica B, Byrnes K, Di Giovanni S, Faden A (2005) Role of the cell cycle in the pathophysiology of central nervous system trauma. Cell Cycle 4:1286-93 (Pubitemid 41365402)
9. Davis E, Foster T, Thomas W (1994) Cellular forms and functions of brain microglia. Brain Res Bull 34:73-8 (Pubitemid 24099729)
10. Dixon C, Clifton G, Lighthall J, Yaghmai A, Hayes R (1991) A controlled cortical impact model of traumatic brain injury in the rat. J Neurosci Methods 39:253-62
11. Dutton R, Stansbury L, Leone S, Kramer E, Hess J, Scalea T (2010) Trauma mortality in mature trauma systems: are we doing better? An analysis trauma mortality patterns, 1997-2008. J Trauma 69:620-6
12. Eikelenboom P, Bate C, Van Gool W, Hoozemans J, Rozemuller J, Veerhuis R, Williams A (2002) Neuroin-flammation in Alzheimer's disease and prion disease. Glia 40:232-9
13. Faden AI, Fox GB, Di X, Knoblach SM, Cernak I, Mullins P, Nikolaeva M, Kozikowski AP (2003) Neuroprotective and nootropic actions of a novel cyclized dipeptide after controlled cortical impact injury in mice. J Cereb Blood Flow Metab 23:355-63 (Pubitemid 36307579)
14. Faul M, Xu L, Wald M, Coronado V (2010) Traumatic brain injury in the United States: emergency department visits, hospitalizations and deaths 2002-2006. Atlanta (GA): Centers for Disease Control and Prevention, National Center for Injury Prevention and Control
15. Fox GB, Fan L, Levasseur RA, Faden AI (1998) Sustained sensory/motor and cognitive deficits with neuronal apoptosis following controlled cortical impact brain injury in the mouse. J Neurotrauma 15:599-614 (Pubitemid 28413053)
16. Freeman RS, Estus S, Johnson Jr EM (1994) Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of Cyclin D1 during programmed cell death. Neuron 12:343-55 (Pubitemid 24071299)
17. Gilbert PE, Brushfield AM (2009) The role of the CA3 hippocampal subregion in spatial memory: a process oriented behavioral assessment. Prog Neuropsychophar-macol Biol Psychiatry 33:774-81
18. Giovanni SD, Movsesyan V, Ahmed F, Cernak I, Schinelli S, Stoica B, Faden A (2005) Cell cycle inhibition provides neuroprotection and reduces glial proliferation and scar formation after traumatic brain injury. Proc Natl Acad Sci USA 102:8333-8 (Pubitemid 40800089)
19. Goldstein LB (2003) Model of recovery of locomotor ability after sensorimotor cortex injury in rats. ILAR J 44:125-9 (Pubitemid 36410966)
20. Greene L, Biswas S, Liu D (2004) Cell cycle molecules and vertebrate neuron death: E2F at the hub. Cell Death Differ 11:49-60 (Pubitemid 38111372)
21. Hall ED, Sullivan PG, Gibson TR, Pavel KM, Thompson BM, Scheff SW (2005) Spatial and temporal characteristics of neurodegeneration after controlled cortical impact in mice: more than a focal brain injury. J Neurotrauma 22:252-65 (Pubitemid 40333519)
22. Herrup K, Yang Y (2007) Cell cycle regulation in the postmitotic neuron: oxymoron or new biology? Nat Rev Neurosci 8:368-78 (Pubitemid 46652467)
23. Hilton G, Stoica B, Byrnes K, Faden A (2008) Roscovitine reduces neuronal cell loss, glial activation, and neurological deficits after brain trauma. J Cereb Blood Flow Metab 28:1845-59
24. Iizuka H, Sakatani K, Young W (1990) Neural damage in the rat thalamus after cortical infarcts. Stroke 21:790-4 (Pubitemid 20180805)
25. Kranenburg O, vanderEb A, Zantema A (1996) Cyclin D1 is an essential mediator of apoptotic neuronal cell death. EMBO J 15:46-54 (Pubitemid 26020387)
26. Lee I, Kesner R (2004) Encoding versus retrieval of spatial memory: double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus 14:66-76 (Pubitemid 38351173)
27. Lee I, Hunsaker MR, Kesner RP (2005) The role of hippocampal subregions in detecting spatial novelty. Behav Neurosci 119:145-53 (Pubitemid 40279505)
28. Loane DJ, Pocivavsek A, Moussa CE, Thompson R, Matsuoka Y, Faden AI, Rebeck GW, Burns MP (2009) Amyloid precursor protein secretases as therapeutic targets for traumatic brain injury. Nat Med 15:377-9
29. Loane DJ, Byrnes KR (2010) Role of microglia in neuro-trauma. Neurotherapeutics 7:366-77
30. Loane DJ, Faden AI (2010) Neuroprotection for traumatic brain injury: translational challenges and emerging therapeutic strategies. Trends Pharmacol Sci 31: 596-604
31. Lundberg A, Weinberg R (1998) Functional inactivation of the retinoblastoma protein requires sequential modification by at least two distinct cyclin-CDK complexes. Mol Cell Biol 23:1044-53
32. Martin JH (ed). (1996) Neuroanatomy, Text and Atlas. Appleton & Lange: Stamford, CT
33. Meijer L, Borgne A, Mulner O, Chong JP, Blow JJ, Inagaki N, Inagaki M, Delcros JG, Moulinoux JP (1997) Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem 243:527-36 (Pubitemid 27060443)
34. Menn B, Bach S, Blevins TL, Campbell M, Meijer L, Timsit S (2010) Delayed treatment with systemic (S)-roscovitine provides neuroprotection and inhibits in vivo CDK5 activity increase in animal stroke models. PLoS One 5:e12117
35. Mori T, Kawamata T, Katayama Y, Maeda T, Aoyama N, Kikuchi T, Uwahodo Y (1998) Antioxidant, OPC-14117, attenuates edema formation, and subsequent tissue damage following cortical contusion in rats. Acta Neurochir Suppl 71:120-2 (Pubitemid 128444375)
36. Nandoe R (2002) Head trauma and Alzheimer's disease. J Alzheimer's Dis 4:303-8
37. Nauta WJH, Feirtag M (eds). (1986) Fundamental Neuroa-natomy. New York: WH Freeman and Company
38. Nguyen M, Boudreau M, Kriz J, Couillard-Despres S, Kaplan D, Julien J (2003) Cell cycle regulators in the neuron death pathway of amyotrophic lateral sclerosis caused by mutant superoxide dismutase. J Neurosci 23:2131-40 (Pubitemid 36368901)
39. Nutley BP, Raynaud FI, Wilson SC, Fischer PM, Hayes A, Goddard PM, McClue SJ, Jarman M, Lane DP, Workman P (2005) Metabolism and pharmacokinetics of the cyclin-dependent kinase inhibitor R-roscovitine in the mouse. Mol Cancer Ther 4:125-39 (Pubitemid 40276782)
40. Panter SS, Faden AI (1992) Pretreatment with NMDA antagonists limits release of excitatory amino acids following traumatic brain injury. Neurosci Lett 136:165-8
41. Redish AD, Touretzky DS (1998) The role of the hippocampus in solving the Morris water maze. Neural Comput 10:73-111 (Pubitemid 128463654)
42. Saatman KE, Creed J, Raghupathi R (2010) Calpain as a therapeutic target in traumatic brain injury. Neurother-apeutics 7:31-42
43. Siman R, Baudry M, Lynch G (1984) Brain fodrin: substrate for calpain I, an endogenous calcium-activated protease. Proc Natl Acad Sci USA 81:3572-6 (Pubitemid 14122716)
44. Siman R, McIntosh TK, Soltesz KM, Chen Z, Neumar RW, Roberts VL (2004) Proteins released from degenerating neurons are surrogate markers for acute brain damage. Neurobiol Dis 16:311-20 (Pubitemid 38757313)
45. Soltys Z, Ziaja M, Pawlinski R, Setkowicz Z, Janeczko K (2001) Morphology of reactive microglia in the injured cerebral cortex. Fractal analysis and complementary quantitative methods. J Neurosci Res 63:90-7 (Pubitemid 32039799)
46. Stoica BA, Byrnes KR, Faden AI (2009) Cell cycle activation and CNS injury. Neurotox Res 16:221-37
47. Zhan X, Kim C, Sharp F (2008) Very brief focal ischemia simulating transient ischemic attacks TIAs) can injure brain and induce Hsp70 protein. Brain Res 1234:184-97