Cyclin D1, cdk4, and Bim are involved in thrombin-induced apoptosis in cultured cortical neurons

Journal of Neurochemistry

Volumn 101, Issue 2, 2007, Pages 498-505

  Rao, Haripriya Vittal ^a,b   Thirumangalakudi, Lakshmi ^a   Desmond, Paula ^a   Grammas, Paula ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

Author keywords

Alzheimer's disease; Bim; Cyclin D1; Cyclin dependent kinase 4; Neuronal cell death; Thrombin

Indexed keywords

BIM PROTEIN; CYCLIN D1; CYCLIN DEPENDENT KINASE 4; PROTEIN BCL 2; THROMBIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CORTEX; CELL CYCLE REGULATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVATION; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS INHIBITION; RAT;

ALZHEIMER DISEASE; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL CYCLE PROTEINS; CELLS, CULTURED; CEREBRAL CORTEX; CYCLIN D1; CYCLIN-DEPENDENT KINASE 4; DOSE-RESPONSE RELATIONSHIP, DRUG; MEMBRANE PROTEINS; NERVE DEGENERATION; NEURODEGENERATIVE DISEASES; NEURONS; PROTO-ONCOGENE PROTEINS; RATS; RNA, MESSENGER; THROMBIN;

EID: 34047151833     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04389.x     Document Type: Article

References (44)

1. Akiyama H., Ikeda K., Kondo H. et al. (1992) Thrombin accumulation in brains of patients with Alzheimer's disease. Neurosci. Lett. 146, 152-154.
2. Becker E. B. and Bonni A. (2004) Beyond proliferation - cell cycle control of neuronal survival and differentiation in the developing mammalian brain. Semin. Cell Dev. Biol. 16, 439-448.
3. Biswas S. C., Liu D. X. and Greene L. A. (2005) Bim is a direct target of a neuronal E2F-dependent apoptotic pathway. J. Neurosci. 25, 8349-8358.
4. Boutillier A. L., Trinh E. and Loeffler J. P. (2000) Caspase-dependent cleavage of the retinoblastoma protein is an early step in neuronal apoptosis. Oncogene 19, 2171-2178.
5. Busser J., Geldmacher D. S. and Herrup K. (1998) Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J. Neurosci. 18, 2801-2807.
6. de Castro Ribeiro M., Badaut J., Price M. et al. (2006) Thrombin in ischemic neuronal death. Exp. Neurol. 198, 199-203.
7. Chalmers C. J., Balmanno K., Hadfield K. et al. (2003) Thrombin inhibits Bim (Bcl-2-interacting mediator of cell death) expression and prevents serum-withdrawal-induced apoptosis via protease-activated receptor 1. Biochem. J. 375, 99-109.
8. Di Giovanni S., Movsesyan V., Ahmed F. et al. (2005) Cell cycle inhibition provides neuroprotection and reduces glial proliferation and scar formation after traumatic brain injury. Proc. Natl Acad. Sci. USA 102, 8333-8338.
9. Dobashi Y., Kudoh T., Toyoshima K. and Akiyama T. (1996) Persistent activation of CDK4 during neuronal differentiation of rat pheochromocytoma PC12 cells. Biochem. Biophys. Res. Commun. 221, 351-355.
10. Dobashi Y., Shoji M., Kondo E. et al. (1998) CDK4, a possible critical regulator of apoptosis in rat pheochromocytoma PC12 cells. Biochem. Biophys. Res. Commun. 253, 609-613.
11. Donovan F. M., Pike C. J., Cotman C. W. et al. (1997) Thrombin induces apoptosis in cultured neurons and astrocytes via a pathway requiring tyrosine kinase and RhoA activities. J. Neurosci. 17, 5316-5326.
12. Freeman R. S., Estus S. and Johnson E. M. Jr (1994) Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of cyclin D1 during programmed cell death. Neuron 12, 343-355.
13. Grammas P., Moore P. and Weigel P. H. (1999) Microvessels from Alzheimer's disease brains kill neurons in vitro. Am. J. Pathol. 154, 337-342.
14. Grammas P., Ottman T., Reimann-Philipp U. et al. (2004) Injured brain endothelial cells release neurotoxic thrombin. J. Alzheimers Dis. 6, 275-281.
15. Grammas P., Samany P. G. and Thirumangalakudi L. (2006) Thrombin and inflammatory proteins are elevated in Alzheimer's disease microvessels: implications for disease pathogenesis. J. Alzheimers Dis. 9, 51-58.
16. Herrup K., Neve R., Ackerman S. L. et al. (2004) Divide and die: cell cycle events as triggers of nerve cell death. J. Neurosci. 24, 9232-9239.
17. Hsu S. Y., Lin P. and Hsueh A. J. (1998) BOD (Bcl-2-related ovarian death gene) is an ovarian BH3 domain-containing proapoptotic Bcl-2 protein capable of dimerization with diverse antiapoptotic Bcl-2 members. Mol. Endocrinol. 12, 1432-1440.
18. Kranenburg O., van der Eb A. J. and Zantema A. (1996) Cyclin D1 is an essential mediator of apoptotic neuronal cell death. EMBO J 15, 46-54.
19. Lim A. C., Qu D. and Qi R. Z. (2003) Protein-protein interactions in Cdk5 regulation and function. Neurosignals 12, 230-238.
20. McGeer P. L., Klegeris A., Walker D. G. et al. (1994) Pathological proteins in senile plaques. Tohoku J. Exp. Med. 174, 269-277.
21. Mhatre M., Nguyen A., Kashani S. et al. (2004) Thrombin, a mediator of neurotoxicity and memory impairment. Neurobiol. Aging 25, 783-793.
22. O'Connor L., Strasser A., O'Reilly L. A. et al. (1998) Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 17, 384-395.
23. Ogawa O., Zhu X., Lee H. G. et al. (2003) Ectopic localization of phosphorylated histone H3 in Alzheimer's disease: a mitotic catastrophe Acta Neuropathol. (Berl.) 105, 524-528.
24. Padmanabhan J., Park D. S., Greene L. A. et al. (1999) Role of cell cycle regulatory proteins in cerebellar granule neuron apoptosis. J. Neurosci. 19, 8747-8756.
25. Park D. S., Morris E. J., Bremner R. et al. (2000) Involvement of retinoblastoma family members and E2F/DP complexes in the death of neurons evoked by DNA damage. J. Neurosci. 20, 3104-3114.
26. Putcha G. V., Moulder K. L., Golden J. P. et al. (2001) Induction of BIM, a proapoptotic BH3-only BCL-2 family member, is critical for neuronal apoptosis. Neuron 29, 615-628.
27. Puthalakath H. and Strasser A. (2002) Keeping killers on a tight leash: transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins. Cell Death Differ. 9, 505-512.
28. Rashidian J., Iyirhiaro G., Aleyasin H. et al. (2005) Multiple cyclin-dependent kinases signals are critical mediators of ischemia/hypoxic neuronal death in vitro and in vivo. Proc. Natl Acad. Sci. USA 102, 14 080-14 085.
29. Reimann-Philipp U., Ovase R., Weigel P. H. et al. (2001) Mechanisms of cell death in primary cortical neurons and PC12 cells. J. Neurosci. Res. 64, 654-660.
30. Rohatgi T., Sedehizade F. and Reymann K. G. (2004) Protease-activated receptors in neuronal development, neurodegeneration, and neuroprotection: thrombin as signaling molecule in the brain. Neuroscientist 10, 501-512.
31. Shirvan A., Ziv I., Zilkha-Falb R. et al. (1998) Expression of cell cycle-related genes during neuronal apoptosis: is there a distinct pattern Neurochem. Res. 23, 767-777.
32. Smirnova I. V., Zhang S. X., Citron B. A. et al. (1998) Thrombin is an extracellular signal that activates intracellular death protease pathways inducing apoptosis in model motor neurons. J. Neurobiol. 36, 64-80.
33. (2 +) mobilization, and apoptosis. J. Neurobiol. 48, 87-100.
34. Suo Z., Wu M., Citron B. A. et al. (2003) Rapid tau aggregation and delayed hippocampal neuronal death induced by persistent thrombin signaling. J. Biol. Chem. 278, 37 681-37 689.
35. Tagliati F., Bottoni A., Bosetti A. et al. (2005) Utilization of luminescent technology to develop a kinase assay: cdk4 as a model system. J. Pharm. Biomed. Anal. 39, 811-814.
36. Turgeon V. L., Lloyd E. D., Wang S. et al. (1998) Thrombin perturbs neurite outgrowth and induces apoptotic cell death in enriched chick spinal motoneuron cultures through caspase activation. J. Neurosci. 18, 6882-6891.
37. Turgeon V. L., Milligan C. E. and Houenou L. J. (1999) Activation of the protease-activated thrombin receptor (PAR)-1 induces motoneuron degeneration in the developing avian embryo. J. Neuropathol. Exp. Neurol. 58, 499-504.
38. Vincent I., Jicha G., Rosado M. et al. (1997) Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer's disease brain. J. Neurosci. 17, 3588-3598.
39. Wang Q. S., Sabourin C. L., Wang H. et al. (1996) Overexpression of cyclin D1 and cyclin E in N-nitrosomethylbenzylamine-induced rat esophageal tumorigenesis. Carcinogenesis 17, 1583-1588.
40. Wen Y., Yang S., Liu R. et al. (2005) Cell-cycle regulators are involved in transient cerebral ischemia induced neuronal apoptosis in female rats. FEBS Lett. 579, 4591-4599.
41. Whitfield J., Neame S. J., Paquet L. et al. (2001) Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 29, 629-643.
42. Yang E., Zha J., Jockel J. et al. (1995) Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 8, 285-291.
43. Yang Y., Varvel N. H., Lamb B. T. et al. (2006) Ectopic cell cycle events link human Alzheimer's disease and amyloid precursor protein transgenic mouse models. J. Neurosci. 26, 775-784.
44. Zhu X., McShea A., Harris P. L. et al. (2004) Elevated expression of a regulator of the G2/M phase of the cell cycle, neuronal CIP-1-associated regulator of cyclin B, in Alzheimer's disease. J. Neurosci. Res. 75, 698-703.