Role of the cell cycle in the pathobiology of central nervous system trauma

Cell Cycle

Volumn 4, Issue 9, 2005, Pages 1286-1293

  Cernak, Ibolja ^a   Stoica, Bogdan ^a   Byrnes, Kimberly R ^a   Di Giovanni, Simone ^a   Faden, Alan I ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Astrocyte proliferation; Cell cycle; Flavopiridol; Microglial proliferation; Neuronal injury; Neuroprotection; Traumatic brain injury

Indexed keywords

CELL CYCLE PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR; ETOPOSIDE; FLAVOPIRIDOL; OLOMOUCINE; ROSCOVITINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN INJURY; CELL ACTIVATION; CELL CYCLE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFECT; MICROGLIA; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PATHOPHYSIOLOGY; RAT; UPREGULATION;

ANIMALIA;

EID: 25444457320     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.4.9.1996     Document Type: Article

References (84)

1. Bruns Jr J, Hauser WA. The epidemiology of traumatic brain injury: A review. Epilepsia 2003; 44:2-10.
2. Faden AI. Neuroprotection and traumatic brain injury: Theoretical option or realistic proposition. Curr Opin Neurol 2002; 15:707-12.
3. Okano HJ, Pfaff DW, Gibbs RB. RB and Cdc2 expression in brain: Correlations with 3H-thymidine incorporation and neurogenesis. J Neurosci 1993; 13:2930-8.
4. Nguyen MD, Mushynski WE, Julien JP. Cycling at the interface between neurodevelopment and neurodegeneration. Cell Death Differ 2002; 9:1294-306.
5. Wartiovaara K, Barnabe-Heider F, Miller FD, Kaplan DR. N-myc promotes survival and induces S-phase entry of postmitotic sympathetic neurons. J Neurosci 2002; 22:815-24.
6. 1-phase of the on-going cell cycle. J Cell Biochem 2003; 90:244-252.
7. 1 cyclins. Cell 1993; 73:1059-65.
8. Nishitani H, Lygerou Z. Control of DNA replication licensing in a cell cycle. Genes Cells 2002; 7:523-34.
9. Obaya AJ, Sedivy JM. Regulation of cyclin-Cdk activity in mammalian cells. Cell Mol Life Sci 2002; 59:126-42.
10. Fischer PM, Endicott J, Meijer L. Cyclin-dependent kinase inhibitors. Prog Cell Cycle Res 2003; 5:235-48.
11. Coqueret O. New roles for p21 and p27 cell-cycle inhibitors: A function for each cell compartment? Trends Cell Biol 2003; 13:65-70.
12. Kimelberg HK, Norenberg MD. Astrocytes. Sci Am 1989; 200:66-72, (74,76).
13. McGraw J, Hiebert GW, Steeves JD. Modulating astrogliosis after neurotrauma. J Neurosci Res 2001; 63:109-15.
14. Swanson RA, Ying W, Kauppinen TM. Astrocyte influences on ischemic neuronal death. Curr Mol Med 2004; 4:193-205.
15. Harris FM, Tesseur I, Brecht WJ, Xu Q, Mullendorff K, Chang S, Wyss-Coray T, Mahley RW, Huang Y. Astroglial regulation of apolipoprotein E expression in neuronal cells. Implications for Alzheimer's disease. J Biol Chem 2004; 279:3862-8.
16. Schultz C, Ghebremedhin E, Del Tredici K, Rub U, Braak H. High prevalence of thorn-shaped astrocytes in the aged human medial temporal lobe. Neurobiol Aging 2004; 25:397-405.
17. Silver J, Miller JH. Regeneration beyond the glial scar. Nat Rev Neurosci 2004; 5:146-156.
18. Hoeppner TJ, Morrell F. Control of scar formation in experimentally induced epilepsy. Exp Neurol 1986; 94:519-36.
19. Giulian D, Tapscott MJ. Immunoregulation of cells within the central nervous system. Brain Behav Immun 1988; 2:352-8.
20. Giulian D, Baker TJ. Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 1986; 6:2163-78.
21. Moore S, Thanos S. The concept of microglia in relation to central nervous system disease and regeneration. Prog Neurobiol 1996; 48:441-60.
22. Muessel MJ, Berman NE, Klein RM. Early and specific expression of monocyte chemoattractant protein-1 in the thalamus induced by cortical injury. Brain Res 2000; 870:211-21.
23. Kim SY, Choi YS, Choi JS, Cha JH, Kim ON, Lee SB, Chung JW, Chun MH, Lee MY. Osteopontin in kainic acid-induced microglial reactions in the rat brain. Mol Cells 2002; 13:429-435.
24. Akiyama H, Itagaki S, McGeer PL. Major histocompatibility complex antigen expression on rat microglia following epidural kainic acid lesions. J Neurosci Res 1988; 20:147-57.
25. Zhang Z, Chopp M, Powers C. Temporal profile of microglial response following transient (2 h) middle cerebral artery occlusion. Brain Res 1997; 744:189-98.
26. Bellander BM, Bendel O, Von Euler G, Ohlsson M, Svensson M. Activation of microglial cells and complement following traumatic injury in rat entorhinal-hippocampal slice cultures. J Neurotrauma 2004; 21:605-15.
27. Lynch NJ, Willis CL, Nolan CC, Roscher S, Fowler MJ, Weihe E, Ray DE, Schwaeble WJ. Microglial activation and increased synthesis of complement component C1q precedes blood-brain barrier dysfunction in rats. Mol Immunol 2004; 40:709-16.
28. Wiessner C, Brink I, Lorenz P, Neumann-Haefelin T, Vogel P, Yamashita K. Cyclin D1 messenger RNA is induced in microglia rather than neurons following transient forebrain ischaemia. Neuroscience 1996; 72:947-58.
29. Kato H, Takahaski A, Itoyama Y. Cell cycle protein expression in proliferating microglia and astrocytes following transient global cerebral ischemia in the rat. Brain Res Bull 2003; 60:215-221.
30. Di Giovanni S, Knoblach SM, Brandoli C, Aden SA, Hoffman EP, Faden AI. Gene profiling in spinal cord injury shows role of cell cycle in neuronal death. Ann Neurol 2003; 53:454-68.
31. Natale JE, Ahmed F, Cernak I, Stoica B, Faden AI. Gene expression profile changes are commonly modulated across models and species after traumatic brain injury. J Neurotrauma 2003; 20:907-27.
32. Gallo V, Armstrong RC. Developmental and growth factor-induced regulation of nestin in oligodendrocyte lineage cells. J Neurosci 1995; 15:394-406.
33. Sugita Y, Becerra SP, Chader GJ, Schwartz JP. Pigment epithelium-derived factor (PEDF) has direct effects on the metabolism and proliferation of microglia and indirect effects on astrocytes. J Neurosci Res 1997; 49:710-8.
34. Mukhin AG, Ivanova SA, Knoblach SM, Faden AI. New in vitro model of traumatic neuronal injury: Evaluation of secondary injury and glutamate receptor-mediated neurotoxicity. J Neurotrauma 1997; 14:651-63.
35. Faden AI, Knoblach SM, Cernak I, Fan L, Vink R, Araldi GL, Fricke ST, Roth BL, Kozikowski AP. Novel diketopiperazine enhances motor and cognitive recovery after traumatic brain injury in rats and shows neuroprotection in vitro and in vivo. J Cereb Blood Flow Metab 2003; 23:342-54.
36. Hanstock CC, Faden AI, Bendall MR, Vink R. Diffusion-weighted imaging differentiates ischemic tissue from traumatized tissue. Stroke 1994; 25:843-8.
37. Albensi BC, Knoblach SM, Chew BG, O'Reilly MP, Faden AI, Pekar JJ. Diffusion and high resolution MRI of traumatic brain injury in rats: Time course and correlation with histology. Exp Neurol 2000; 162:61-72.
38. Yakovlev AG, Knoblach SM, Fan L, Fox GB, Goodnight R, Faden AI. Activation of CPP32-like caspases contributes to neuronal apoptosis and neurological dysfunction after traumatic brain injury. J Neurosci 1997; 17:7415-724.
39. Swanton C. Cell-cycle targeted therapies. Lancet Oncol 2004; 5:27-36.
40. Dai Y, Grant S. Small molecule inhibitors targeting cyclin-dependent kinases as anticancer agents. Curr Oncol Rep 2004; 6:123-30.
41. Meijer L, Raymond E. Roscovitine and other purines as kinase inhibitors. From starfish oocytes to clinical trials. Acc Chem Res 2003; 36:417-25.
42. Abraham RT, Acquarone M, Andersen A, Asensi A, Belle R, Berger F, Bergounioux C, Brunn G, Buquet-Fagot C, Fagot D, et al. Cellular effects of olomoucine, an inhibitor of cyclin-dependent kinases. Biol Cell 1995; 83:105-20.
43. Movsesyan VA, Yakovlev AG, Fan L, Faden AI. Effect of serine protease inhibitors on post-traumatic brain injury and neuronal apoptosis. Exp Neurol 2001; 167:366-75.
44. Sinensky MC, Leiser AL, Babich H. Oxidative stress aspects of the cytotoxicity of carbamide peroxide: In vitro studies. Toxicol Lett 1995; 75:101-9.
45. McIntosh TK, Vink R, Noble L, Yamakami I, Fernyak S, Soares H, Faden AI. Traumatic brain injury in the rat: Characterization of a lateral fluid - Percussion model. Neuroscience 1989; 28:233-44.
46. Faden AI, Demediuk P, Panter SS, Vink R. The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 1989; 244:798-800.
47. Vink R, McIntosh TK, Demediuk P, Weiner MW, Faden AI. Decline in intracellular free Mg2+ is associated with irreversible tissue injury after brain trauma. J Biol Chem 1988; 263:757-61.
48. Osuga H, Osuga S, Wang F, Fetni R, Hogan MJ, Slack RS, Hakim AM, Ikeda JE, Park DS. Cyclin-dependent kinases as a therapeutic target for stroke. Proc Natl Acad Sci USA 2000; 97:10254-9.
49. Wang F, Corbett D, Osuga H, Osuga S, Ikeda JE, Slack RS, Hogan MJ, Hakim AM, Park DS. Inhibition of cyclin-dependent kinases improves CA1 neuronal survival and behavioral performance after global ischemia in the rat. J Cereb Blood Flow Metab 2002; 22:171-82.
50. Di Giovanni S, Movsesyan V, Ahmed F, Cernak I, Schinelli S, Stoica B, Faden AI. Cell cycle inhibition provides neuroprotection and reduces glial proliferation and scar formation after traumatic brain injury. Proc Natl Acad Sci USA 2005; 102:8333-8, (Epub 2005 May 8327).
51. Tsan MF, Clark RN, Goyert SM, White JE. Induction of TNF-alpha and MnSOD by endotoxin: Role of membrane CD14 and Toll-like receptor-4. Am J Physiol Cell Physiol 2001; 280:C1422-30.
52. Akundi RS, Candelario-Jalil E, Hess S, Hull M, Lieb K, Gebicke-Haerter PJ, Fiebich BL. Signal transduction pathways regulating cyclooxygenase-2 in lipopolysaccharide-activated primary rat microglia. Glia 2005; In press.
53. Waetzig V, Czeloth K, Hidding U, Mielke K, Kanzow M, Brecht S, Goetz M, Lucius R, Herdegen T, Hanisch UK. c-Jun N-terminal kinases (JNKs) mediate pro-inflammatory actions of microglia. Glia 2005; 50:235-46.
54. Gao HM, Jiang J, Wilson B, Zhang W, Hong JS, Liu B. Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: Relevance to Parkinson's disease. J Neurochem 2002; 81:1285-97.
55. Shaked I, Tchoresh D, Gersner R, Meiri G, Mordechai S, Xiao X, Hart RP, Schwartz M. Protective autoimmunity: Interferon-gamma enables microglia to remove glutamate without evoking inflammatory mediators. J Neurochem 2005; 92:997-1009.
56. Brar SS, Kennedy TP, Sturrock AB, Huecksteadt TP, Quinn MT, Murphy TM, Chitano P, Hoidal JR. NADPH oxidase promotes NF-kappaB activation and proliferation in human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2002; 282:L782-95.
57. Kim HR, Lin HM, Biliran H, Raz A. Cell cycle arrest and inhibition of anoikis by galectin-3 in human breast epithelial cells. Cancer Res 1999; 59:4148-54.
58. Blamire AM, Anthony DC, Rajagopalan B, Sibson NR, Perry VH, Styles P. Interleukin-1beta -induced changes in blood-brain barrier permeability, apparent diffusion coefficient, and cerebral blood volume in the rat brain: A magnetic resonance study. J Neurosci 2000; 20:8153-9.
59. Quagliarello VJ, Wispelwey B, Long Jr WJ, Scheld WM. Recombinant human interleukin-1 induces meningitis and blood-brain barrier injury in the rat. Characterization and comparison with tumor necrosis factor. J Clin Invest 1991; 87:1360-6.
60. Bonmann E, Suschek C, Spranger M, Kolb-Bachofen V. The dominant role of exogenous or endogenous interleukin-1 beta on expression and activity of inducible nitric oxide synthase in rat microvascular brain endothelial cells. Neurosci Lett 1997; 230:109-12.
61. Fitch MT, Silver J. Activated macrophages and the blood-brain barrier: Inflammation after CNS injury leads to increases in putative inhibitory molecules. Exp Neurol 1997; 148:587-603.
62. Grewal RP, Morgan TE, Finch CE. C1qB and clusterin mRNA increase in association with neurodegeneration in sporadic amyotrophic lateral sclerosis. Neurosci Lett 1999; 271:65-7.
63. Daly Jt, Kotwal GJ. Pro-inflammatory complement activation by the A beta peptide of Alzheimer's disease is biologically significant and can be blocked by vaccinia virus complement control protein. Neurobiol Aging 1998; 19:619-27.
64. McGeer PL, McGeer EG. Inflammation and the degenerative diseases of aging. Ann New York Acad Sci 2004; 1035:104-16.
65. Eikelenboom P, Bate C, Van Gool WA, Hoozemans JJ, Rozemuller JM, Veerhuis R, Williams A. Neuroinflammation in Alzheimer's disease and prion disease. Glia 2002; 40:232-9.
66. Hunot S, Hirsch EC. Neuroinflammatory processes in Parkinson's disease. Ann Neurol 2003; 53:S49-58, (discussion S58-60).
67. Xu J, Qu ZX, Hogan EL, Perot Jr PL. Protective effect of methylprednisolone on vascular injury in rat spinal cord injury. J Neurotrauma 1992; 9:245-53.
68. Lee SM, Yune TY, Kim SJ, Park do W, Lee YK, Kim YC, Oh YJ, Markelonis GJ, Oh TH. Minocycline reduces cell death and improves functional recovery after traumatic spinal cord injury in the rat. J Neurotrauma 2003; 20:1017-27.
69. Hains BC, Yucra JA, Hulsebosch CE. Reduction of pathological and behavioral deficits following spinal cord contusion injury with the selective cyclooxygenase-2 inhibitor NS-398. J Neurotrauma 2001; 18:409-23.
70. Prewitt CM, Niesman IR, Kane CJ, Houle JD. Activated macrophage/ microglial cells can promote the regeneration of sensory axons into the injured spinal cord. Exp Neurol 1997; 148:433-443.
71. Rabchevsky AG, Streit WJ. Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J Neurosci Res 1997; 47:34-48.
72. Rapalino O, Lazarov-Spiegler O, Agranov E, Velan GJ, Yoles E, Fraidakis M, Solomon A, Gepstein R, Katz A, Belkin M, Hadani M, Schwartz M. Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 1998; 4:814-21.
73. Schwartz M, Lazarov-Spiegler O, Rapalino O, Agranov I, Velan G, Hadani M. Potential repair of rat spinal cord injuries using stimulated homologous macrophages. Neurosurgery 1999; 44:1041-5, (discussion 1045-6).
74. Hashimoto M, Nitta A, Fukumitsu H, Nomoto H, Shen L, Furukawa S. Inflammation-induced GDNF improves locomotor function after spinal cord injury. Neuroreport 2005; 16:99-102.
75. Vink R, Van Den Heuvel C. Recent advances in the development of multifactorial therapies for the treatment of traumatic brain injury. Expert Opin Investig Drugs 2004; 13:1263-74.
76. Tolias CM, Bullock MR. Critical appraisal of neuroprotection trials in head injury: What have we learned? Neurorx 2004; 1:71-9.
77. Fitch MT, Doller C, Combs CK, Landreth GE, Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation: In vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J Neurosci 1999; 19:8182-98.
78. Dusart I, Schwab ME. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci 1994; 6:712-24.
79. Allan SM, Rothwell NJ. Inflammation in central nervous system injury. Philos Trans R Soc Lond B Biol Sci 2003; 358:1669-77.
80. Blagosklonny MV. Flavopiridol, an inhibitor of transcription: Implications, problems and solutions. Cell Cycle 2004; 3:1537-42.
81. Verdaguer E, Garcia-Jorda E, Canudas AM, Dominguez E, Jimenez A, Pubill D, Escubedo E, Pallas JC, Camins A. Kainic acid-induced apoptosis in cerebellar granule neurons: An attempt at cell cycle reentry. Neuroreport 2002; 13:413-6.
82. Shapiro GI, Supko JG, Patterson A, Lynch C, Lucca J, Zacarola PF, Muzikansky A, Wright JJ, Lynch Jr TJ, Rollins BJ. A phase II trial of the cyclin-dependent kinase inhibitor flavopiridol in patients with previously untreated stage IV nonsmall cell lung cancer. Clin Cancer Res 2001; 7:1590-9.
83. Schwartz GK, Ilson D, Saltz L, O'Reilly E, Tong W, Maslak P, Werner J, Perkins P, Stoltz M, Kelsen D. Phase II study of the cyclin-dependent kinase inhibitor flavopiridol administered to patients with advanced gastric carcinoma. J Clin Oncol 2001; 19:1985-92.
84. Senderowicz AM. Small-molecule cyclin-dependent kinase modulators. Oncogene 2003; 22:6609-20.