Nuclear envelope dispersion triggered by deregulated Cdk5 precedes neuronal death

Molecular Biology of the Cell

Volumn 22, Issue 9, 2011, Pages 1452-1462

  Chang, Kuei Hua ^a   Multani, Parminder Singh ^a   Sun, Kai Hui ^a   Vincent, Fabien ^a   De Pablo, Yolanda ^a   Ghosh, Soumitra ^a   Gupta, Ritika ^a   Lee, Hyun Pil ^b   Lee, Hyoung Gon ^b   Smith, Mark A ^b   Shah, Kavita ^a  

^a PURDUE UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; CYCLIN DEPENDENT KINASE 5; GLUTAMIC ACID; LAMIN A; LAMIN B1; NUCLEAR PROTEIN; PROTEIN P25; ROSCOVITINE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN CELL; CELL NUCLEUS MEMBRANE; CELL PROLIFERATION; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; MITOSIS; MOUSE; NERVE CELL NECROSIS; NEUROFIBRILLARY TANGLE; NEUROTOXICITY; NONHUMAN; NUCLEAR LAMINA; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CELL DEATH; CYCLIN-DEPENDENT KINASE 5; DISEASE MODELS, ANIMAL; GLUTAMIC ACID; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LAMIN TYPE A; LAMIN TYPE B; MICE; MICE, TRANSGENIC; MUTATION; NERVE TISSUE PROTEINS; NEUROFIBRILLARY TANGLES; NEURONS; NUCLEAR ENVELOPE; NUCLEAR LAMINA; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY;

MUS MUSCULUS;

EID: 79955486290     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-07-0654     Document Type: Article

References (46)

1. Ankarcrona M, Zhivotovsky B, Holmstrom T, Diana A, Eriksson JE, Orrenius S, Nicotera P (1996). Lamin and β-tubulin fragmentation precede chromatin degradation in glutamate-induced neuronal apoptosis. Neuroreport 7, 2659-2664. (Pubitemid 26403035)
2. Behrens MM, Strasser U, Koh JY, Gwag BJ, Choi DW (1999). Prevention of neuronal apoptosis by phorbol ester-induced activation of protein kinase C: blockade of p38 mitogen-activated protein kinase. Neuroscience 94, 917-927. (Pubitemid 29474981)
3. Cenni V et al. (2008). Lamin A Ser404 is a nuclear target of Akt phosphorylation in C2C12 cells. J Proteome Res 7, 4727-4735.
4. Chang KH, de Pablo Y, Lee HP, Lee HG, Smith MA, Shah K (2010). Cdk5 is a major regulator of p38 cascade: relevance to neurotoxicity in Alzheimer's disease. J Neurochem 113, 1221-1229.
5. Cruz JC, Tseng HC, Goldman JA, Shih H, Tsai LH (2003). Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron 40, 471-483. (Pubitemid 37494698)
6. Dechat T, Adam SA, Goldman RD (2009). Nuclear lamins and chromatin: when structure meets function. Adv Enzyme Regul 49, 157-166.
7. Friedlander RM (2003). Apoptosis and caspases in neurodegenerative diseases. N Engl J Med 348, 1365-1375.
8. Fu X, Choi YK, Qu D, Yu Y, Cheung NS, Qi RZ (2006). Identification of nuclear import mechanisms for the neuronal Cdk5 activator. J Biol Chem 281, 39014-39021. (Pubitemid 46041860)
9. Heald R, McKeon F (1990). Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61, 579-589.
10. Hocevar BA, Burns DJ, Fields AP (1993). Identification of protein kinase C (PKC) phosphorylation sites on human lamin BPotential role of PKC in nuclear lamina structural dynamics. J Biol Chem 268, 7545-7552. (Pubitemid 23105656)
11. Huang E, Qu D, Zhang Y, Venderova K, Haque ME, Rousseaux MW, Slack RS, Woulfe JM, Park DS (2010). The role of Cdk5-mediated apurinic/apyrimidinic endonuclease 1 phosphorylation in neuronal death. Nat Cell Biol 12, 563-571.
12. Ino H, Chiba T (1996). Intracellular localization of cyclin-dependent kinase 5 (CDK5) in mouse neuron: CDK5 is located in both nucleus and cytoplasm. Brain Res 732, 179-185. (Pubitemid 26305303)
13. Kim D et al. (2008). Deregulation of HDAC1 by p25/Cdk5 in neurotoxicity. Neuron 60, 803-817.
14. Kim S, Shah K (2007). Dissecting yeast Hog1 MAP kinase pathway using a chemical genetic approach. FEBS Lett 581, 1209-1216. (Pubitemid 46385943)
15. Klementiev B, Novikova T, Novitskaya V, Walmod PS, Dmytriyeva O, Pakkenberg B, Berezin V, Bock E (2007). A neural cell adhesion molecule-derived peptide reduces neuropathological signs and cognitive impairment induced by Aβ25-35. Neuroscience 145, 209-224. (Pubitemid 46227730)
16. Lee HG, Ueda M, Miyamoto Y, Yoneda Y, Perry G, Smith MA, Zhu X (2006a). Aberrant localization of importin α1 in hippocampal neurons in Alzheimer disease. Brain Res 1124, 1-4. (Pubitemid 44779563)
17. Lee HG, Ueda M, Zhu X, Perry G, Smith MA (2006b). Ectopic expression of phospho-Smad2 in Alzheimer's disease: uncoupling of the transforming growth factor-β pathway? J Neurosci Res 84, 1856-1861. (Pubitemid 44892619)
18. Lee JH, Kim KT (2007). Regulation of cyclin-dependent kinase 5 and p53 by ERK1/2 pathway in the DNA damage-induced neuronal death. J Cell Physiol 210, 784-797.
19. Lee KY, Clark AW, Rosales JL, Chapman K, Fung T, Johnston RN (1999). Elevated neuronal Cdc2-like kinase activity in the Alzheimer disease brain. Neurosci Res 34, 21-29. (Pubitemid 29245996)
20. Lin H, Lin TY, Juang JL (2007). Abl deregulates Cdk5 kinase activity and subcellular localization in Drosophila neurodegeneration. Cell Death Differ 14, 607-615.
21. Maestre C, Delgado-Esteban M, Gomez-Sanchez JC, Bolanos JP, Almeida A (2008). Cdk5 phosphorylates Cdh1 and modulates cyclin B1 stability in excitotoxicity. EMBO J 27, 2736-2745.
22. Moffat et al. (2006). A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124, 1283-1298.
23. Oberhammer FA, Hochegger K, Froschl G, Tiefenbacher R, Pavelka M (1994). Chromatin condensation during apoptosis is accompanied by degradation of lamin A+B, without enhanced activation of cdc2 kinase. J Cell Biol 126, 827-837. (Pubitemid 24252132)
24. O'Hare MJ, Kushwaha N, Zhang Y, Aleyasin H, Callaghan SM, Slack RS, Albert PR, Vincent I, Park DS (2005). Differential roles of nuclear and cytoplasmic cyclin-dependent kinase 5 in apoptotic and excitotoxic neuronal death. J Neurosci 25, 8954-8966. (Pubitemid 41384464)
25. Patrick GN, Zhou P, Kwon YT, Howley PM, Tsai LH (1998). p35, the neuronal-specific activator of cyclin-dependent kinase 5 (Cdk5) is degraded by the ubiquitin-proteasome pathway. J Biol Chem 273, 24057-24064. (Pubitemid 28435748)
26. Pike CJ, Walencewicz-Wasserman AJ, Kosmoski J, Cribbs DH, Glabe CG, Cotman CW (1995). Structure-activity analyses of β-amyloid peptides: contributions of the β25-35 region to aggregation and neurotoxicity. J Neurochem 64, 253-265.
27. Sahlgren CM, Pallari HM, He T, Chou YH, Goldman RD, Eriksson JE (2006). A nestin scaffold links Cdk5/p35 signaling to oxidant-induced cell death. EMBO J 25, 4808-4819. (Pubitemid 44607026)
28. Saito T, Konno T, Hosokawa T, Asada A, Ishiguro K, Hisanaga S (2007). p25/cyclin-dependent kinase 5 promotes the progression of cell death in nucleus of endoplasmic reticulum-stressed neurons. J Neurochem 102, 133-140. (Pubitemid 46906270)
29. Shah K, Liu Y, Deirmengian C, Shokat KM (1997). Engineering unnatural nucleotide specificity for Rous sarcoma virus tyrosine kinase to uniquely label its direct substrates. Proc Natl Acad Sci USA 94, 3565-3570. (Pubitemid 27180412)
30. Shah K, Shokat KM (2002). A chemical genetic screen for direct v-Src substrates reveals ordered assembly of a retrograde signaling pathway. Chem Biol 9, 35-47. (Pubitemid 34155863)
31. Shah K, Shokat KM (2003). A chemical genetic approach for the identification of direct substrates of protein kinases. Methods Mol Biol 233, 253-271.
32. Shah K, Vincent F (2005). Divergent roles of c-Src in controlling platelet-derived growth factor-dependent signaling in fibroblasts. Mol Biol Cell 16, 5418-5432. (Pubitemid 41566850)
33. Shea TB, Yabe JT, Ortiz D, Pimenta A, Loomis P, Goldman RD, Amin N, Pant HC (2004b). Cdk5 regulates axonal transport and phosphorylation of neurofilaments in cultured neurons. J Cell Sci 117, 933-941. (Pubitemid 38386950)
34. Shea TB, Zheng YL, Ortiz D, Pant HC (2004a). Cyclin-dependent kinase 5 increases perikaryal neurofilament phosphorylation and inhibits neurofilament axonal transport in response to oxidative stress. J Neurosci Res 76, 795-800. (Pubitemid 38720686)
35. Sheffield LG, Miskiewicz HB, Tannenbaum LB, Mirra SS (2006). Nuclear pore complex proteins in Alzheimer disease. J Neuropathol Exp Neurol 65, 45-54.
36. Shimizu T, Cao CX, Shao RG, Pommier Y (1998). Lamin B phosphorylation by protein kinase cα and proteolysis during apoptosis in human leukemia HL60 cells. J Biol Chem 273, 8669-8674. (Pubitemid 28176143)
37. Stewart CL, Roux KJ, Burke B (2007). Blurring the boundary: the nuclear envelope extends its reach. Science 318, 1408-1412. (Pubitemid 350208920)
38. Su JH, Anderson AJ, Cummings BJ, Cotman CW (1994). Immunohistochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 5, 2529-2533.
39. Sun KH, de Pablo Y, Vincent F, Johnson EO, Chavers AK, Shah K (2008a). Novel genetic tools reveal Cdk5's major role in Golgi fragmentation in Alzheimer's disease. Mol Biol Cell 19, 3052-3069.
40. Sun KH, de Pablo Y, Vincent F, Shah K (2008b). Deregulated Cdk5 promotes oxidative stress and mitochondrial dysfunction. J Neurochem 107, 265-278.
41. Sun KH, Lee HG, Smith MA, Shah K (2009). Direct and indirect roles of cyclin-dependent kinase 5 as an upstream regulator in the c-Jun NH2-terminal kinase cascade: relevance to neurotoxic insults in Alzheimer's disease. Mol Biol Cell 20, 4611-4619.
42. Tang X, Wang X, Gong X, Tong M, Park D, Xia Z, Mao Z (2005). Cyclin-dependent kinase 5 mediates neurotoxin-induced degradation of the transcription factor myocyte enhancer factor 2. J Neurosci 25, 4823-4834. (Pubitemid 40664130)
43. Tian B, Yang Q, Mao Z (2009). Phosphorylation of ATM by Cdk5 mediates DNA damage signalling and regulates neuronal death. Nat Cell Biol 11, 211-218.
44. Wen Y et al. (2008). Transcriptional regulation of β-secretase by p25/cdk5 leads to enhanced amyloidogenic processing. Neuron 57, 680-690. (Pubitemid 351335351)
45. Zhang J, Li H, Herrup K (2010). Cdk5 nuclear localization is p27-dependent in nerve cells: implications for cell cycle suppression and caspase-3 activation. J Biol Chem 285, 14052-14061.
46. Zhang Y, McLaughlin R, Goodyer C, LeBlanc A (2002). Selective cytotoxicity of intracellular amyloid β peptide1-42 through p53 and Bax in cultured primary human neurons. J Cell Biol 156, 519-529. (Pubitemid 34839899)