Cyclin-Dependent Kinase 5 Mediates Neurotoxin-Induced Degradation of the Transcription Factor Myocyte Enhancer Factor 2

Regulation of the process of neuronal death plays a central role both during development of the CNS and in adult brain. The transcription factor myocyte enhancer factor 2 (MEF2) plays a critical role in neuronal survival. Cyclin-dependent kinase 5 (Cdk5) mediates neurotoxic effects by phosphorylating and inhibiting MEF2. How Cdk5-dependent phosphorylation reduces MEF2 transactivation activity remained unknown. Here, we demonstrate a novel mechanism by which Cdk5, in conjunction with caspase, inhibits MEF2. Using primary cerebellar granule neuron as a model, our investigation reveals that neurotoxicity induces destabilization of MEF2s in neurons. Destabilization of MEF2 is caused by an increase in caspase-dependent cleavage of MEF2. This cleavage event requires nuclear activation of Cdk5 activity. Phosphorylation by Cdk5 alone is sufficient to promote degradation of MEF2A and MEF2D by caspase-3. In contrast to MEF2A and MEF2D, MEF2C is not phosphorylated by Cdk5 after glutamate exposure and, therefore, resistant to neurotoxin-induced caspase-dependent degradation. Consistently, blocking Cdk5 or enhancing MEF2 reduced toxin-induced apoptosis. These findings define an important regulatory mechanism that for the first time links prodeath activities of Cdk5 and caspase. The convergence of Cdk5 phosphorylation-dependent caspase-mediated degradation of nuclear survival factors exemplified by MEF2 may represent a general process applicable to the regulation of other survival factors under diverse neurotoxic conditions.

[1]  Jesús Avila,et al.  Glycogen synthase kinase 3: a drug target for CNS therapies , 2004, Journal of neurochemistry.

[2]  G. Johnson,et al.  Cyclin‐dependent kinase‐5 in neurodegeneration , 2004, Journal of neurochemistry.

[3]  David S. Park,et al.  Cyclin-dependent kinase 5 is a mediator of dopaminergic neuron loss in a mouse model of Parkinson's disease , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Li-Huei Tsai,et al.  Aberrant Cdk5 Activation by p25 Triggers Pathological Events Leading to Neurodegeneration and Neurofibrillary Tangles , 2003, Neuron.

[5]  Li-Huei Tsai,et al.  Cyclin-Dependent Kinase 5 and Neuronal Migration in the Neocortex , 2003, Neurosignals.

[6]  E. Marra,et al.  Cytochrome c, released from cerebellar granule cells undergoing apoptosis or excytotoxic death, can generate protonmotive force and drive ATP synthesis in isolated mitochondria , 2003, Journal of neurochemistry.

[7]  Z. Xia,et al.  ERK5 activation of MEF2-mediated gene expression plays a critical role in BDNF-promoted survival of developing but not mature cortical neurons , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Junmin Peng,et al.  Cdk5-Mediated Inhibition of the Protective Effects of Transcription Factor MEF2 in Neurotoxicity-Induced Apoptosis , 2003, Neuron.

[9]  J. Julien,et al.  Cycling at the interface between neurodevelopment and neurodegeneration , 2002, Cell Death and Differentiation.

[10]  Yang Shi,et al.  RNA Interference Reveals a Requirement for Myocyte Enhancer Factor 2A in Activity-dependent Neuronal Survival* , 2002, The Journal of Biological Chemistry.

[11]  P. Davies,et al.  Deregulation of cdk5, Hyperphosphorylation, and Cytoskeletal Pathology in the Niemann–Pick Type C Murine Model , 2002, The Journal of Neuroscience.

[12]  L. Tsai,et al.  A survey of Cdk5 activator p35 and p25 levels in Alzheimer's disease brains , 2002, FEBS letters.

[13]  G. Johnson,et al.  Cdk5 phosphorylates p53 and regulates its activity , 2002, Journal of neurochemistry.

[14]  Jiankun Cui,et al.  Dominant-interfering forms of MEF2 generated by caspase cleavage contribute to NMDA-induced neuronal apoptosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[15]  A. Kulkarni,et al.  Cyclin‐dependent kinase 5 prevents neuronal apoptosis by negative regulation of c‐Jun N‐terminal kinase 3 , 2002, The EMBO journal.

[16]  Li-Huei Tsai,et al.  A decade of CDK5 , 2001, Nature Reviews Molecular Cell Biology.

[17]  L. Tsai,et al.  p35 and p39 Are Essential for Cyclin-Dependent Kinase 5 Function during Neurodevelopment , 2001, The Journal of Neuroscience.

[18]  M. K. Meintzer,et al.  Myocyte Enhancer Factor 2A and 2D Undergo Phosphorylation and Caspase-Mediated Degradation during Apoptosis of Rat Cerebellar Granule Neurons , 2001, The Journal of Neuroscience.

[19]  S. R. Datta,et al.  Transcription-dependent and -independent control of neuronal survival by the PI3K–Akt signaling pathway , 2001, Current Opinion in Neurobiology.

[20]  J. Julien,et al.  Deregulation of Cdk5 in a Mouse Model of ALS Toxicity Alleviated by Perikaryal Neurofilament Inclusions , 2001, Neuron.

[21]  H. Pant,et al.  Cyclin-dependent protein kinase 5 (Cdk5) and the regulation of neurofilament metabolism. , 2001, European journal of biochemistry.

[22]  R. Maccioni,et al.  The protein kinase Cdk5 , 2001 .

[23]  R. Maccioni,et al.  The protein kinase Cdk5. Structural aspects, roles in neurogenesis and involvement in Alzheimer's pathology. , 2001, European journal of biochemistry.

[24]  Veeranna,et al.  Neuronal Cyclin-Dependent Kinase 5 Activity Is Critical for Survival , 2001, The Journal of Neuroscience.

[25]  Mark P. Mattson,et al.  Apoptosis in neurodegenerative disorders , 2000, Nature Reviews Molecular Cell Biology.

[26]  Junying Yuan,et al.  Apoptosis in the nervous system , 2000, Nature.

[27]  S. Lipton,et al.  Antiapoptotic role of the p38 mitogen-activated protein kinase-myocyte enhancer factor 2 transcription factor pathway during neuronal differentiation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[28]  K. Ishiguro,et al.  Calpain-dependent Proteolytic Cleavage of the p35 Cyclin-dependent Kinase 5 Activator to p25* , 2000, The Journal of Biological Chemistry.

[29]  L. Tsai,et al.  Neurotoxicity induces cleavage of p35 to p25 by calpain , 2000, Nature.

[30]  L. Tsai,et al.  Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration , 1999, Nature.

[31]  Z. Mao,et al.  Calcineurin Enhances MEF2 DNA Binding Activity in Calcium-dependent Survival of Cerebellar Granule Neurons* , 1999, The Journal of Biological Chemistry.

[32]  M E Greenberg,et al.  Neuronal activity-dependent cell survival mediated by transcription factor MEF2. , 1999, Science.

[33]  P. J. Steinbach,et al.  Identification of Substrate Binding Site of Cyclin-dependent Kinase 5* , 1999, The Journal of Biological Chemistry.

[34]  D. Kaplan,et al.  Akt-Dependent Potentiation of L Channels by Insulin-Like Growth Factor-1 Is Required for Neuronal Survival , 1999, The Journal of Neuroscience.

[35]  S. Al-Sarraj,et al.  Cyclin-dependent kinase-5 is associated with lipofuscin in motor neurones in amyotrophic lateral sclerosis , 1998, Neuroscience Letters.

[36]  R. Johnston,et al.  Neuronal Cdc2-like Kinase (Nclk) Binds and Phosphorylates the Retinoblastoma Protein* , 1997, The Journal of Biological Chemistry.

[37]  O. Ornatsky,et al.  MEF2 Protein Expression, DNA Binding Specificity and Complex Composition, and Transcriptional Activity in Muscle and Non-muscle Cells* , 1996, The Journal of Biological Chemistry.

[38]  J. Martín,et al.  Mutational analysis of the DNA binding, dimerization, and transcriptional activation domains of MEF2C , 1996, Molecular and cellular biology.

[39]  S. Imai,et al.  Expression of a MADS box gene, MEF2D, in neurons of the mouse central nervous system: implication of its binary function in myogenic and neurogenic cell lineages , 1995, Neuroscience Letters.

[40]  J. Brion,et al.  Cortical and brainstem-type Lewy bodies are immunoreactive for the cyclin-dependent kinase 5. , 1995, The American journal of pathology.

[41]  G. Lyons,et al.  Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  N. Copeland,et al.  A Mef2 gene that generates a muscle-specific isoform via alternative mRNA splicing , 1994, Molecular and cellular biology.

[43]  B. Nadal-Ginard,et al.  A fourth human MEF2 transcription factor, hMEF2D, is an early marker of the myogenic lineage. , 1993, Development.

[44]  S. Lipton,et al.  hMEF2C gene encodes skeletal muscle- and brain-specific transcription factors , 1993, Molecular and cellular biology.

[45]  S. Lipton,et al.  MEF2C, a MADS/MEF2-family transcription factor expressed in a laminar distribution in cerebral cortex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[46]  B. Nadal-Ginard,et al.  Human myocyte-specific enhancer factor 2 comprises a group of tissue-restricted MADS box transcription factors. , 1992, Genes & development.

[47]  S. Paul,et al.  N-methyl-D-aspartate exposure blocks glutamate toxicity in cultured cerebellar granule cells. , 1992, Molecular pharmacology.

[48]  A. Schousboe,et al.  Development of excitatory amino acid induced cytotoxicity in cultured neurons , 1990, International Journal of Developmental Neuroscience.

[49]  S H Kaufmann,et al.  Mammalian caspases: structure, activation, substrates, and functions during apoptosis. , 1999, Annual review of biochemistry.

[50]  K. Kinzler,et al.  A simplified system for generating recombinant adenoviruses. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[51]  B. Black,et al.  Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. , 1998, Annual review of cell and developmental biology.

[52]  Y. Barde,et al.  Physiology of the neurotrophins. , 1996, Annual review of neuroscience.