Calpain and caspase: can you tell the difference?

Both necrotic and apoptotic neuronal death are observed in various neurological and neurodegenerative disorders. Calpain is activated in various necrotic and apoptotic conditions, while caspase 3 is only activated in neuronal apoptosis. Despite the difference in cleavage-site specificity, an increasing number of cellular proteins are found to be dually susceptible to these cysteine proteases. These include alpha- and beta-fodrin, calmodulin-dependent protein kinases, ADP-ribosyltransferase (ADPRT/PARP) and tau. Intriguingly, calpastatin is susceptible to caspase-mediated fragmentation. Neurotoxic challenges such as hypoxia-hypoglycemia, excitotoxin treatment or metabolic inhibition of cultured neurons result in activation of both proteases. Calpain inhibitors can protect against necrotic neuronal death and, to a lesser extent, apoptotic death. Caspase inhibitors strongly suppress apoptotic neuronal death. Thus, both protease families might contribute to structural derangement and functional loss in neurons under degenerative conditions.

[1]  Kevin K W Wang,et al.  Evidence for Activation of Caspase‐3‐Like Protease in Excitotoxin‐ and Hypoxia/Hypoglycemia‐Injured Neurons , 1998, Journal of neurochemistry.

[2]  M. Moskowitz,et al.  Attenuation of Delayed Neuronal Death after Mild Focal Ischemia in Mice by Inhibition of the Caspase Family , 1998, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[3]  Y. Lazebnik,et al.  Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE , 1994, Nature.

[4]  Seamus J. Martin,et al.  Proteolysis of Fodrin (Non-erythroid Spectrin) during Apoptosis (*) , 1995, The Journal of Biological Chemistry.

[5]  S. Inoue,et al.  Rapid fragmentation of vimentin in human skin fibroblasts exposed to tamoxifen: a possible involvement of caspase-3. , 1998, Biochemical and biophysical research communications.

[6]  Y. Ben-Ari,et al.  Rapid Communication: Regional Variability in DNA Fragmentation After Global Ischemia Evidenced by Combined Histological and Gel Electrophoresis Observations in the Rat Brain , 1993, Journal of neurochemistry.

[7]  M. Gnegy,et al.  Calcium/Calmodulin-dependent Protein Kinase IV Is Cleaved by Caspase-3 and Calpain in SH-SY5Y Human Neuroblastoma Cells Undergoing Apoptosis* , 1998, The Journal of Biological Chemistry.

[8]  N. Copeland,et al.  Identification and mapping of Casp7, a cysteine protease resembling CPP32β, interleukin-1β converting enzyme, and CED-3 , 1997 .

[9]  G. Robertson,et al.  Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid-beta precursor protein and amyloidogenic A beta peptide formation. , 1999, Cell.

[10]  A. Malkinson,et al.  Calpain activation in apoptosis , 1994, Journal of cellular physiology.

[11]  D. Kufe,et al.  Caspase-3-mediated Cleavage of Protein Kinase C θ in Induction of Apoptosis* , 1997, Journal of Biological Chemistry.

[12]  P. Henkart,et al.  A protease-dependent TCR-induced death pathway in mature lymphocytes. , 1995, Journal of immunology.

[13]  G. Poirier,et al.  Characterization of antibodies specific for the caspase cleavage site on poly(ADP-ribose) polymerase: specific detection of apoptotic fragments and mapping of the necrotic fragments of poly(ADP-ribose) polymerase. , 1997, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[14]  M. Gnegy,et al.  Alterations of Extracellular Calcium Elicit Selective Modes of Cell Death and Protease Activation in SH‐SY5Y Human Neuroblastoma Cells , 1999, Journal of neurochemistry.

[15]  S. Ratnofsky,et al.  Proteolytic Activation of Protein Kinase C ␦ by an Ice/ced 3-like Protease Induces Characteristics of Apoptosis Materials and Methods , 1996 .

[16]  L. Kaczmarek,et al.  DNA fragmentation in rat brain after intraperitoneal administration of kainate , 1994, Neuroreport.

[17]  M. Omary,et al.  Apoptosis Generates Stable Fragments of Human Type I Keratins* , 1997, The Journal of Biological Chemistry.

[18]  K. Wang,et al.  Caspase-mediated fragmentation of calpain inhibitor protein calpastatin during apoptosis. , 1998, Archives of biochemistry and biophysics.

[19]  J. Card,et al.  Proteolytic processing of beta-amyloid precursor by calpain I , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  M. Linnik,et al.  Six-hour window of opportunity for calpain inhibition in focal cerebral ischemia in rats. , 1998, Stroke.

[21]  J. Savill,et al.  Actin is cleaved during constitutive apoptosis. , 1997, The Biochemical journal.

[22]  K. Raser,et al.  Effects of ICE‐like protease and calpain inhibitors on neuronal apoptosis , 1996, Neuroreport.

[23]  A. Spector,et al.  Lens calcium activated proteinase: degradation of vimentin. , 1983, Biochemical and biophysical research communications.

[24]  E. Alnemri,et al.  Activation of the CED3/ICE-Related Protease CPP32 in Cerebellar Granule Neurons Undergoing Apoptosis But Not Necrosis , 1997, The Journal of Neuroscience.

[25]  B. Pike,et al.  Temporal relationships between de novo protein synthesis, calpain and caspase 3‐like protease activation, and DNA fragmentation during apoptosis in septo‐hippocampal cultures , 1998, Journal of neuroscience research.

[26]  A. Malkinson,et al.  Calpain and calpastatin regulate neutrophil apoptosis , 1999, Journal of cellular physiology.

[27]  E. Preston,et al.  Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain , 1993, Neuroscience Letters.

[28]  M. Luskin,et al.  Strategies utilized by migrating neurons of the postnatal vertebrate forebrain , 1998, Trends in Neurosciences.

[29]  K. Raser,et al.  Neuronal Nitric Oxide Synthase and Calmodulin‐Dependent Protein Kinase IIα Undergo Neurotoxin‐Induced Proteolysis , 1997, Journal of neurochemistry.

[30]  E. Kun,et al.  Isolation and identification of a proteinase from calf thymus that cleaves poly(ADP-ribose) polymerase and histone H1. , 1997, Biochimica et biophysica acta.

[31]  E. Cheng,et al.  Conversion of Bcl-2 to a Bax-like death effector by caspases. , 1997, Science.

[32]  M. Linnik,et al.  Evidence Supporting a Role for Programmed Cell Death in Focal Cerebral Ischemia in Rats , 1993, Stroke.

[33]  C. Mitchell,et al.  Focal adhesion kinase (pp125FAK) cleavage and regulation by calpain. , 1996, The Biochemical journal.

[34]  J C Reed,et al.  IAP family proteins--suppressors of apoptosis. , 1999, Genes & development.

[35]  M. Weller,et al.  Potassium Deprivation-Induced Apoptosis of Cerebellar Granule Neurons: A Sequential Requirement for New mRNA and Protein Synthesis, ICE-Like Protease Activity, and Reactive Oxygen Species , 1996, The Journal of Neuroscience.

[36]  L Manzo,et al.  Neuronal cell death: a demise with different shapes. , 1999, Trends in pharmacological sciences.

[37]  K. Wang,et al.  Calmodulin-binding proteins as calpain substrates. , 1989, The Biochemical journal.

[38]  A. Srinivasan,et al.  Apoptosis after traumatic human spinal cord injury. , 1998, Journal of neurosurgery.

[39]  Patrick Ng,et al.  Caspase-3 Is Required for α-Fodrin Cleavage but Dispensable for Cleavage of Other Death Substrates in Apoptosis* , 1998, The Journal of Biological Chemistry.

[40]  John Calvin Reed,et al.  Bax cleavage is mediated by calpain during drug-induced apoptosis , 1998, Oncogene.

[41]  S. Adam‐Klages,et al.  Caspase-mediated inhibition of human cytosolic phospholipase A2 during apoptosis. , 1998, Journal of immunology.

[42]  R. Talanian,et al.  Simultaneous Degradation of αII- and βII-Spectrin by Caspase 3 (CPP32) in Apoptotic Cells* , 1998, The Journal of Biological Chemistry.

[43]  G. Poirier,et al.  Different cleavage pattern for poly(ADP-ribose) polymerase during necrosis and apoptosis in HL-60 cells. , 1996, Biochemical and biophysical research communications.

[44]  S. Lipton,et al.  Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[45]  G. Majno,et al.  Apoptosis, oncosis, and necrosis. An overview of cell death. , 1995, The American journal of pathology.

[46]  A. Yakovlev,et al.  Activation of CPP32-Like Caspases Contributes to Neuronal Apoptosis and Neurological Dysfunction after Traumatic Brain Injury , 1997, The Journal of Neuroscience.

[47]  C. Moorehead All rights reserved , 1997 .

[48]  S. Nakashima,et al.  Endogenous Cleavage of Phospholipase C-β3 by Agonist-induced Activation of Calpain in Human Platelets (*) , 1995, The Journal of Biological Chemistry.

[49]  M. Paskind,et al.  Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. , 1995, Cell.

[50]  B. Pike,et al.  Regional calpain and caspase‐3 proteolysis of α‐spectrin after traumatic brain injury , 1998, Neuroreport.

[51]  G. Johnson,et al.  Phosphorylation of τ In Situ: Inhibition of Calcium‐Dependent Proteolysis , 1995, Journal of neurochemistry.

[52]  J. Savill,et al.  Constitutive Apoptosis in Human Neutrophils Requires Synergy between Calpains and the Proteasome Downstream of Caspases* , 1998, The Journal of Biological Chemistry.

[53]  Y. Nishizuka,et al.  Limited proteolysis of protein kinase C subspecies by calcium-dependent neutral protease (calpain). , 1989, The Journal of biological chemistry.

[54]  D. H. Burgess,et al.  Protease Involvement in Fodrin Cleavage and Phosphatidylserine Exposure in Apoptosis* , 1996, The Journal of Biological Chemistry.

[55]  R. Gilbertsen,et al.  Non-erythroid alpha-spectrin breakdown by calpain and interleukin 1 beta-converting-enzyme-like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis. , 1996, The Biochemical journal.

[56]  G. Rosen,et al.  Cleavage of Focal Adhesion Kinase by Caspases during Apoptosis* , 1997, The Journal of Biological Chemistry.

[57]  G. Poirier,et al.  Involvement of caspase-dependent activation of cytosolic phospholipase A2 in tumor necrosis factor-induced apoptosis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[58]  T. Murachi,et al.  Degradation of actin and vimentin by calpain II, a Ca2+‐dependent cysteine proteinase, in bovine lens , 1984, FEBS letters.

[59]  C. Barbato,et al.  Tau Cleavage and Dephosphorylation in Cerebellar Granule Neurons Undergoing Apoptosis , 1998, The Journal of Neuroscience.

[60]  M. Kuettel,et al.  Apoptosis-associated proteolysis of vimentin in human prostate epithelial tumor cells. , 1998, Biochemical and biophysical research communications.

[61]  R. Kannagi,et al.  Purification and characterization of calpains from pig epidermis and their action on epidermal keratin. , 1988, The Journal of investigative dermatology.

[62]  B. Berger,et al.  Transient expression of tyrosine hydroxylase immunoreactivity in some neurons of the rat neocortex during postnatal development. , 1985, Brain research.

[63]  Sten Orrenius,et al.  Cleavage of the calpain inhibitor, calpastatin, during apoptosis , 1998, Cell Death and Differentiation.

[64]  R. Kamen,et al.  Mice deficient in IL-1β-converting enzyme are defective in production of mature IL-1β and resistant to endotoxic shock , 1995, Cell.

[65]  T. Tsuruo,et al.  Identification of actin as a substrate of ICE and an ICE-like protease and involvement of an ICE-like protease but not ICE in VP-16-induced U937 apoptosis. , 1995, Biochemical and biophysical research communications.

[66]  M. Molinari,et al.  Calpain: a protease in search of a function? , 1998, Biochemical and biophysical research communications.

[67]  J. Trojanowski,et al.  Evidence of apoptotic cell death after experimental traumatic brain injury in the rat. , 1995, The American journal of pathology.

[68]  Development, Brain, and Behavior. , 1987 .

[69]  N. Thornberry,et al.  Caspases: killer proteases. , 1997, Trends in biochemical sciences.

[70]  K. Wang,et al.  CALPAIN INHIBITORS : NOVEL NEUROPROTECTANTS AND POTENTIAL ANTI CATARACT AGENTS , 1998 .

[71]  J. Geddes,et al.  Mechanisms of Cell Death Induced by the Mitochondrial Toxin 3-Nitropropionic Acid: Acute Excitotoxic Necrosis and Delayed Apoptosis , 1997, The Journal of Neuroscience.

[72]  R. Mechoulam,et al.  Ontogenetic development of the response to anandamide and Δ9-tetrahydrocannabinol in mice , 1996 .

[73]  R. Gilbertsen,et al.  Characterization of CPP32‐Like Protease Activity Following Apoptotic Challenge in SH‐SY5Y Neuroblastoma Cells , 1997, Journal of neurochemistry.

[74]  M. Herkenham,et al.  The cannabinoid receptor: biochemical, anatomical and behavioral characterization , 1990, Trends in Neurosciences.

[75]  Keisuke Kuida,et al.  Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice , 1996, Nature.

[76]  S. Lipton,et al.  Cytoskeletal Breakdown and Apoptosis Elicited by NO Donors in Cerebellar Granule Cells Require NMDA Receptor Activation , 1996, Journal of neurochemistry.

[77]  R. Oppenheim,et al.  Increased Production of Amyloid Precursor Protein Provides a Substrate for Caspase-3 in Dying Motoneurons , 1998, The Journal of Neuroscience.

[78]  K. Wang,et al.  Procaspase-3 and poly(ADP)ribose polymerase (PARP) are calpain substrates. , 1999, Biochemical and biophysical research communications.

[79]  H. Kawasaki,et al.  Identification of calcium-activated neutral protease as a processing enzyme of human interleukin 1 alpha. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[80]  T. Yamauchi,et al.  Purification and characterization of active fragment of Ca2+/calmodulin-dependent protein kinase II from the post-synaptic density in the rat forebrain. , 1996, Journal of biochemistry.

[81]  M. Gnegy,et al.  Endogenous Bax Translocation in Sh-sy5y Human Neuroblastoma Cells and Cerebellar Granule Neurons Undergoing Apoptosis , 2022 .

[82]  H. Vinters,et al.  Antibody to caspase-cleaved actin detects apoptosis in differentiated neuroblastoma and plaque-associated neurons and microglia in Alzheimer's disease. , 1998, The American journal of pathology.