Death caspase-1


EVOLUTIONARY HOMOLOGS


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Cytokine and transcription factor regulation of the cell death pathways

Hematopoietic cytokines transduce cell survival signals, which are distinct from the signals necessary for the stimulation of DNA synthesis. Recently the Ras and phosphatidylinositol 3-kinase pathways have been shown to play important roles in preventing apoptosis in various cell types (e.g., hematopoietic cells and neuronal cells). Withdrawal of cytokine(s), in turn, results in rapid inactivation of these survival pathways and eventually leads to cell death accompanied by the hallmarks of apoptosis. However, the mechanism of cell death caused by cytokine deprivation has not been fully elucidated. Caspase-3/CPP32, a member of the caspase/interleukin-1beta-converting enzyme family, is activated upon interleukin (IL)-3 deprivation in IL-3-dependent cells as well as IL-2 deprivation in IL-2-dependent cells. In addition, poly(ADP-ribose) polymerase, a cellular substrate for the caspase family proteases, is degraded into apoptotic fragments in both cell lines after cytokine removal. Inhibition of a caspase family protease by synthetic peptides suppresses apoptotic death. These results indicate that the activation of a caspase-like protease(s) is required for the progression of apoptosis following cytokine deprivation. However, readdition of IL-3 does not restore the proliferative potential of the cells that survived in the presence of the peptide inhibitor after IL-3 depletion. Therefore, cellular commitment to apoptosis appears to precede the activation of a caspase-like protease(s) (Ohta, 1997).

Protein tyrosine kinases activate the STAT (signal transducer and activator of transcription) signaling pathway, which can play essential roles in cell differentiation, cell cycle control, and development. However, the potential role of the STAT signaling pathway in the induction of apoptosis remains unexplored. Gamma interferon (IFN-gamma) activates STAT1 and induces apoptosis in both A431 and HeLa cells, whereas epidermal growth factor (EGF) activates STAT proteins and induces apoptosis in A431 but not in HeLa cells. EGF receptor autophosphorylation and mitogen-activated protein kinase activation in response to EGF are similar in both cell lines. The breast cancer cell line MDA-MB-468 exhibits a similar response to A431 cells, i.e., STAT activation and apoptosis correlatively results from EGF or IFN-gamma treatment. In addition, in a mutant A431 cell line in which STAT activation is abolished, no apoptosis is induced by either EGF or IFN-gamma. Both EGF and IFN-gamma induce caspase 1 (interleukin-1beta converting enzyme [ICE]) gene expression in a STAT-dependent manner. IFN-gamma is unable to induce ICE gene expression and apoptosis in either JAK1-deficient HeLa cells (E2A4) or STAT1-deficient cells (U3A). However, ICE gene expression and apoptosis are induced by IFN-gamma in U3A cells into which STAT1 had been reintroduced. Moreover, both EGF-induced apoptosis and IFN-gamma-induced apoptosis are effectively blocked by Z-Val-Ala-Asp-fluoromethylketone (ZVAD) in all the cells tested; studies from ICE-deficient cells indicate that ICE gene expression is necessary for IFN-gamma-induced apoptosis. It is concluded that activation of the STAT signaling pathway can induce apoptosis through the induction of ICE gene expression (Chin, 1997).

Signal transducers and activators of transcription (STATs) enhance transcription of specific genes in response to cytokines and growth factors. STAT1 is also required for efficient constitutive expression of the caspases Ice, Cpp32, and Ich-1 in human fibroblasts. As a consequence, STAT1-null cells are resistant to apoptosis by tumor necrosis factor alpha (TNF-alpha). Reintroduction of STAT1alpha restores both TNF-alpha-induced apoptosis and the expression of Ice, Cpp32, and Ich-1. Variant STAT1 proteins carrying point mutations that inactivate domains required for STAT dimer formation nevertheless restored protease expression and sensitivity to apoptosis, indicating that the functions of STAT1 required for these activities are different from those that mediate induced gene expression. In certain cells IFN-gamma induces apoptosis, and Ice expression is activated by IFN-gamma. This transcriptional induction of the Ice gene is correlated with tyrosine phosphorylation and the DNA binding of STAT1. STAT1 can also act constitutively a monomer independent of IFN-gamma activation (Kumar, 1997).

Upon activation, cell surface death receptors, Fas/APO-1/CD95 and tumor necrosis factor receptor-1 (TNFR-1), are attached to cytosolic adaptor proteins, which in turn recruit caspase-8 (MACH/FLICE/Mch5) to activate the interleukin-1 beta-converting enzyme (ICE)/CED-3 family protease (caspase) cascade. However, it remains unknown whether these apoptotic proteases are generally involved in apoptosis triggered by other stimuli, such as Myc and p53. This study suggests that a death protease cascade consisting of caspases and serine proteases plays an essential role in Myc-mediated apoptosis. When Rat-1 fibroblasts stably expressing either s-Myc or c-Myc are induced to undergo apoptosis by serum deprivation, a caspase-3 (CPP32)-like protease activity that cleaves a specific peptide substrate (Ac-DEVD-MCA) appears in the cell lysates. Induction of s-Myc- and c-Myc-mediated apoptotic cell death is effectively prevented by caspase inhibitors such as Z-Asp-CH2-DCB and Ac-DEVD-CHO. Exposing the cells to a serine protease inhibitor also significantly inhibits s-Myc- and c-Myc-mediated apoptosis and the appearance of the caspase-3-like protease activity in vivo. However, the inhibitor does not directly inhibit caspase-3-like protease activity in the apoptotic cell lysates in vitro. Together, these results indicate that caspase-3-like proteases play a critical role in both s-Myc- and c-Myc-mediated apoptosis and that caspase-3-like proteases function downstream of the protease-sensitive step in the signaling pathway of Myc-mediated apoptosis (Kagaya, 1997).

Both caspase-1- and caspase-3-like activities are required for Fas-mediated apoptosis. However, the role of caspase-1 and caspase-3 in mediating Fas-induced cell death is not clear. The contributions of these caspases to Fas signaling in hepatocyte cell death in vitro were assessed. Although wild-type, caspase-1(-/-), and caspase-3(-/-) hepatocytes are killed at a similar rate when cocultured with FasL expressing NIH 3T3 cells, caspase-3(-/-) hepatocytes displays drastically different morphological changes as well as significantly delayed DNA fragmentation. For both wild-type and caspase-1(-/-) apoptotic hepatocytes, typical apoptotic features such as cytoplasmic blebbing and nuclear fragmentation are seen within 6 hr, but neither event is observed for caspase-3(-/-) hepatocytes. These studies were extended to thymocytes and it was found that apoptotic caspase-3(-/-) thymocytes exhibit similar 'abnormal' morphological changes and delayed DNA fragmentation observed in hepatocytes. Furthermore, the cleavage of various caspase substrates implicated in mediating apoptotic events, including gelsolin, fodrin, laminB, and DFF45/ICAD, is delayed or absent. The altered cleavage of these key substrates is likely responsible for the aberrant apoptosis observed in both hepatocytes and thymocytes deficient in caspase-3 (Zheng, 1998).

Pim-1 oncoprotein is a serine/threonine kinase that can closely cooperate with c-Myc in lymphomagenesis, as does Bcl-2. Although the molecular mechanism of this cooperative transformation remains unknown, it is speculated that (similar to Bcl-2) Pim-1 contributes to transformation by inhibiting apoptosis. In this study, therefore, the effect of Pim-1 expression was examined on c-Myc-mediated apoptosis of Rat-1 fibroblasts triggered by serum deprivation. Rather than inhibiting apoptosis, Pim-1 expression stimulates c-Myc-mediated apoptosis in Rat-1 fibroblasts. Pim-1 stimulates c-Myc-mediated apoptosis through an enhancement of the c-Myc-mediated activation of caspase-3 (CPP32)-like proteases, since the suppression of this activity by a specific caspase inhibitor abolishes the apoptosis stimulation by Pim-1. A kinase-defective Pim-1 mutant fails to stimulate c-Myc-mediated apoptosis; Pim-1 expression alone, in the absence of c-Myc overexpression, does not induce apoptosis of serum-deprived Rat-1 cells, indicating that the kinase activity of Pim-1 and the activated c-Myc signaling pathway are required for apoptosis stimulation by Pim-1. Together, these results suggest that Pim-1 oncoprotein stimulates as a serine/threonine kinase the death signaling elicited by c-Myc at a step upstream of caspase-3-like protease activation in Rat-1 fibroblasts. These results also suggest that Pim-1 kinase might function cooperatively with c-Myc through the phosphorylation of a factor(s) that regulates the common signaling pathway involved in c-Myc-mediated apoptosis and transformation (Mochizuki, 1997).

The transcription factor NFkappaB is an important regulator of gene expression during immune and inflammatory responses, and can also protect against apoptosis. Endothelial cells undergo apoptosis when deprived of growth factors. Surviving viable cells exhibit increased activity of NFkappaB, whereas apoptotic cells show caspase-mediated cleavage of the NFkappaB p65/RelA subunit. This cleavage leads to loss of carboxy-terminal transactivation domains and a transcriptionally inactive p65 molecule. The truncated p65 acts as a dominant-negative inhibitor of NFkappaB, promoting apoptosis, whereas an uncleavable, caspase-resistant p65 protects the cells from apoptosis. The generation of a dominant-negative fragment of p65 during apoptosis may be an efficient pro-apoptotic feedback mechanism between caspase activation and NF-kappaB inactivation (Levkau, 1999).

The maintenance of NF-kappaB activity by endothelial cells is required for cell survival, because overexpression of a transcriptionally active p65 clearly prevents apoptosis in this system. the results presented here are consistent with several reports that show that NF-kappaB protects cells from a number of apoptotic stimuli, such as TNF-alpha, ionizing radiation and chemotherapeutic agents, and mediates anti-apoptotic signals from the matrix through integrin alphavbeta3. Transcriptional activation of survival genes is believed to be the mechanism by which NF-kappaB provides protection from apoptosis. However, an absolute requirement for NF-kappaB as a transcription factor that universally prevents cell death is far from established (Levkau, 1999).

Other results indicate that NF-kappaB's transcriptional activity may be involved in glutamate-induced toxicity in neuronal cells, and can accelerate growth-factor-deprivation-induced apoptosis in certain transformed cell lines. Although classic NF-kappaB activators, such as TNF-alpha, do not induce apoptosis unless NF-kappaB is blocked, other apoptotic stimuli, such as ligation of the cell-surface-located receptor Fas, induce cell death independent of their ability to activate NF-kappaB. Therefore, growth-factor deprivation in endothelial cells may be an apoptotic stimulus that activates NF-kappaB as an initial protective reaction. NF-kappaB's persistence in the viable population is at least responsible for the cells' resistance to apoptosis. In contrast, cells committed to apoptosis appear to repress NF-kappaB. These results indicate that, as long as cells are capable of maintaining transcriptionally active NF-kappaB, they can resist apoptosis induced by growth-factor deprivation (Levkau, 1999 and references therein).

Mitochondria and the activation of caspases

In a cell-free system based on Xenopus egg extracts, Bcl-2 blocks apoptotic activity by preventing cytochrome c release from mitochondria. Cytochrome c plays a crucial role in this system. The mitochondrial fraction, when incubated with cytosol, releases cytochrome c. In turn, cytochrome c induces the activation of a protease(s) resembling caspase-3 (CPP32), leading to downstream apoptotic events, including the cleavage of fodrin and lamin B1. CPP32-like protease activity plays an essential role in this system, since the caspase inhibitor (Ac-DEVD-CHO) strongly inhibits fodrin and lamin B1 cleavage, as well as nuclear morphology changes. Cytochrome c preparations from various vertebrate species, but not from Saccharomyces cerevisiae, are able to initiate all signs of apoptosis. By itself, cytochrome c is unable to process the precursor form of CPP32; the presence of cytosol is required. The electron transport activity of cytochrome c is not required for its pro-apoptotic function; Cu- and Zn-substituted cytochrome c have strong pro-apoptotic activity, despite being redox-inactive. However, certain structural features of the molecule are required for this activity. Thus, in the Xenopus cell-free system, cytosol-dependent mitochondrial release of cytochrome c induces apoptosis by activating CPP32-like caspases, via unknown cytosolic factors (Kluck, 1997).

Two cell types have been identified, each using almost exclusively one of two different CD95 (APO-1/Fas) signaling pathways. In type I cells, caspase-8 is activated within seconds and caspase-3 within 30 min of receptor engagement, whereas in type II cells, cleavage of both caspases is delayed for approximately 60 min. However, both type I and type II cells show similar kinetics of CD95-mediated apoptosis and loss of mitochondrial transmembrane potential (DeltaPsim). Upon CD95 triggering, all mitochondrial apoptogenic activities are blocked by Bcl-2 or Bcl-xL overexpression in both cell types. However, in type II but not type I cells, overexpression of Bcl-2 or Bcl-xL blocks caspase-8 and caspase-3 activation as well as apoptosis. In type I cells, induction of apoptosis is accompanied by activation of large amounts of caspase-8 by the death-inducing signaling complex (DISC), whereas in type II cells DISC formation is strongly reduced and activation of caspase-8 and caspase-3 occurs following the loss of DeltaPsim. Overexpression of caspase-3 in the caspase-3-negative cell line MCF7-Fas, normally resistant to CD95-mediated apoptosis by overexpression of Bcl-xL, converts these cells into true type I cells in which apoptosis is no longer inhibited by Bcl-xL. In summary, in the presence of caspase-3 the amount of active caspase-8 generated at the DISC determines whether a mitochondria-independent apoptosis pathway is used (type I cells) or not (type II cells) (Scaffidi, 1998).

Netrins activate caspase in a p38 dependent manner

Axon guidance cues trigger rapid changes in protein dynamics in retinal growth cones: netrin-1 stimulates both protein synthesis and degradation, while Sema3A elicits synthesis, and LPA induces degradation. What signaling pathways are involved? These studies confirm that p42/44 MAPK mediates netrin-1 responses and further show that inhibiting its activity blocks cue-induced protein synthesis. Unexpectedly, p38 MAPK is also activated by netrin-1 in retinal growth cones and is required for chemotropic responses and translation. Sema3A- and LPA-induced responses, by contrast, require a single MAPK, p42/p44 and p38, respectively. In addition, caspase-3, an apoptotic protease, is rapidly activated by netrin-1 and LPA in a proteasome- and p38-dependent manner and is required for chemotropic responses. These findings suggest that the apoptotic pathway may be used locally to control protein levels in growth cones and that the differential activation of MAPK pathways may underlie cue-directed migration (Campbell, 2003).

These data provide evidence for the presence of caspases in growth cones and identify caspase-3 as a potential target of p38 signaling for mediating both netrin-1-induced turning and LPA-induced growth cone collapse. This suggests that, in addition to their roles in apoptosis, caspase-induced protein degradation may play a role in growth cone guidance. Previous studies identified the netrin receptor DCC in regulating cell survival via the activation of caspase-3 by caspase-9 in the absence of netrin-1 in human embryonic kidney 293T cells. By contrast, in Xenopus retinal growth cones, netrin-1 and LPA induce the rapid activation of caspase-3 independent of caspase-9 via the MAPK- and proteasome-mediated proteolysis pathways. The activation of caspase-3 in the confined cellular compartment of the growth cone might not lead to activation of the full apoptotic cascade and cell death but rather to transient, localized changes in specific proteins. The p42/p44 and PI-3 kinase pathways identified in netrin-1 signaling are known to play roles in mediating cell survival and may ensure tight regulation of caspase activity in the growth cone. A role has been identified for caspases in synaptic plasticity independent of their roles in cell death (Campbell, 2003 and references therein).

Since caspases are proteases, a key question asks which proteins do caspases degrade? Candidate proteins include known caspase substrates, such as actin, actin binding proteins, and signal transduction pathway components. For example, gelsolin, an actin severing protein, is present in growth cones and is activated by caspase-3-mediated cleavage. Netrin-1 and LPA stimulate the rapid caspase-3-dependent cleavage of PARP. In addition to its role in maintaining genomic stability, PARP is able to interact with and activate proteasome-mediated proteolysis. Cleavage of PARP may inactivate itself, providing a possible mechanism by which proteasome-mediated proteolysis may be regulated in the case of netrin-1 and LPA. The netrin-1 receptor DCC is itself a substrate of caspase-3, and caspase-mediated cleavage of DCC may potentially be involved in mediating netrin-1-induced chemotropic responses. During apoptosis, caspase-3 is also able to cleave eukaryotic initiation factor 4G (eIF-4G), a crucial protein required for binding cellular mRNA to ribosomes. This may decrease the rate of translation and provide a possible mechanism for negative regulation of netrin-1-stimulated protein synthesis in growth cones. Since the chemotropic responses of growth cones elicited by netrin-1 and LPA are essentially blocked by inhibition of caspase-3, it is likely that of the caspases, caspase-3 plays a major role in these processes (Campbell, 2003 and references therein).

The ubiquitin-proteasome system is critically involved in apoptosis and in mediating chemotropic responses of growth cones. In neuronal cells, proteasome inhibitors protect against apoptosis by acting upstream of caspase activation. These results have revealed a parallel in retinal growth cones where the activation or cleavage of caspase-3 in response to netrin-1 and LPA requires proteasome function, suggesting that caspase-mediated protein degradation lies downstream of proteasome/ubiquitin-mediated proteolysis. Candidate proteins to undergo proteasome/ubiquitin-mediated proteolysis include the inhibitor of apoptosis (IAP) family of proteins, degradation of which can result in caspase activation. IAPs can also target caspase-3 itself for proteasome/ubiquitin-mediated proteolysis, suggesting a possible mechanism for the transient and localized nature of caspase-3 activation in growth cones (Campbell, 2003 and references therein).


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Death caspase-1: Biological Overview | Developmental Biology | Effects of Mutation | References

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