Death related ced-3/Nedd2-like protein


EVOLUTIONARY HOMOLOGS part 2/2

Caspase-8/FLICE targets and downstream signaling

The apoptotic signal triggered by ligation of members of the death receptor family is promoted by sequential activation of caspase zymogens. In a purified system, the initiator caspases-8 and -10 directly process the executioner pro-caspase-3. These rates of activation are of sufficient magnitude to indicate direct processing in vivo. Differentially processed forms of caspase-3 that accumulate during caspase-3 activation have similar rates of activation, activities, and specificities. The pattern and rate of caspase-8 induced activation of pro-caspase-3 in cytosolic extracts is the same as in a purified system. Moreover, immunodepletion of pro-caspase-9, a putative intermediary in the pathway to activation, is without consequence. Taken together these data demonstrate that the initiator caspase-8 can directly activate pro-caspase-3 without the requirement for an accelerator. The in vitro data thus help to deconvolute previous in vivo transfection studies that have debated the role of a direct versus indirect transmission of the apoptotic signal generated by ligation of death receptors (Stennicke, 1998).

A cytosolic protein has been purified that induces cytochrome c release from mitochondria in response to caspase-8, the apical caspase activated by cell surface death receptors such as Fas and TNF. Peptide mass fingerprinting identified this protein as Bid, a BH3 domain-containing protein known to interact with both Bcl2 and Bax. Caspase-8 cleaves Bid, and the COOH-terminal part translocates to mitochondria where it triggers cytochrome c release. Immunodepletion of Bid from cell extracts eliminates the cytochrome c releasing activity. The cytochrome c releasing activity of Bid is antagonized by Bcl2. A mutation at the BH3 domain diminishes its cytochrome c releasing activity. Bid, therefore, relays an apoptotic signal from the cell surface to mitochondria (Luo, 1998).

BID, a BH3 domain-containing proapoptotic Bcl2 family member, is a specific proximal substrate of Casp8 in the Fas apoptotic signaling pathway. While full-length BID is localized in cytosol, truncated BID (tBID) translocates to mitochondria and thus transduces apoptotic signals from cytoplasmic membrane to mitochondria. tBID induces first the clustering of mitochondria around the nuclei and release of cytochrome c independent of caspase activity, and then the loss of mitochondrial membrane potential, cell shrinkage, and nuclear condensation in a caspase-dependent fashion. Coexpression of BclxL inhibits all the apoptotic changes induced by tBID. These results indicate that BID is a mediator of mitochondrial damage induced by Casp8 (Li, 1998).

Signaling through the CD95/Fas/APO-1 death receptor plays a critical role in the homeostasis of the immune system. RICK, a novel protein kinase that regulates CD95-mediated apoptosis has been identified and characterized. RICK is composed of an N-terminal serine-threonine kinase catalytic domain and a C-terminal region containing a caspase-recruitment domain. RICK physically interacts with CLARP, a caspase-like molecule known to bind to Fas-associated protein with death domain (FADD) and caspase-8. Expression of RICK promotes the activation of caspase-8 and potentiates apoptosis induced by Fas ligand, FADD, CLARP, and caspase-8. Deletion mutant analysis reveals that both the kinase domain and caspase-recruitment domain are required for RICK to promote apoptosis. A RICK mutant (in which the lysine of the putative ATP-binding site at position 38 is replaced by a methionine) functions as an inhibitor of CD95-mediated apoptosis. Thus, RICK represents a novel kinase that may regulate apoptosis induced by the CD95/Fas receptor pathway (Inohara, 1998).

Genetic studies of the nematode C. elegans have identified several important components of the cell death pathway, most notably CED-3, CED-4, and CED-9. CED-4 directly interacts with the Bcl-2 homolog CED-9 (or the mammalian Bcl-2 family member Bcl-xL) and the caspase CED-3 (or the mammalian caspases ICE and FLICE). This trimolecular complex of CED-4, CED-3, and CED-9 is functional in that CED-9 inhibits CED-4 from activating CED-3 and thereby inhibits apoptosis in heterologous systems. The E1B 19,000-molecular weight protein (E1B 19K) is a potent apoptosis inhibitor and the adenovirus homolog of Bcl-2-related apoptosis inhibitors. Since E1B 19K and Bcl-xL have functional similarity, it was hypothesized that E1B 19K interacts with CED-4 and regulates CED-4-dependent caspase activation. Binding analysis indicates that E1B 19K interacts with CED-4 in a Saccharomyces cerevisiae two-hybrid assay, in vitro, and in mammalian cell lysates. The subcellular localization pattern of CED-4 is dramatically changed by E1B 19K, supporting the theory of a functional interaction between CED-4 and E1B 19K. Whereas expression of CED-4 alone could not induce cell death, coexpression of CED-4 and FLICE augments cell death induction by FLICE, which is blocked by expression of E1B 19K. Even though E1B 19K does not prevent FLICE-induced apoptosis, it does inhibit CED-4-dependent, FLICE-mediated apoptosis, which suggests that CED-4 is required for E1B 19K to block FLICE activation. Thus, E1B 19K functions through interacting with CED-4, and presumably a mammalian homolog of CED-4, to inhibit caspase activation and apoptosis (Han, 1998).

The Bcl-2 family member Bcl-xL has often been correlated with apoptosis resistance. In peripheral human T cells, resistance to CD95-mediated apoptosis is characterized by a lack of caspase-8 recruitment to the CD95 death-inducing signaling complex (DISC) and by increased expression of Bcl-xL. This raises the possibility that Bcl-xL directly prevents caspase-8 activation by the DISC. To test this hypothesis a cell line in which CD95 signaling is inhibited by overexpression of Bcl-xL was used. In these MCF7-Fas-bcl-xL cells Bcl-xL has no effect on the recruitment of caspase-8 to the DISC. It does not affect the activity of the DISC nor the generation of the caspase-8 active subunits p18 and p10. In contrast, cleavage of a typical substrate for caspase-3-like proteases, poly(ADP-ribose) polymerase, is inhibited in comparison with the control-transfected CD95-sensitive MCF7-Fas cells. To test whether Bcl-xL inhibits active caspase-8 subunits in the cytoplasm, a number of immunoprecipitation experiments were performed. Using monoclonal antibodies directed against different domains of caspase-8, anti-Bcl-xL antibodies, or fusion proteins of glutathione S-transferase with different domains of caspase-8, no evidence for a direct or indirect physical interaction between caspase-8 and Bcl-xL was found. Moreover, overexpression of Bcl-xL does not inhibit the activity of the caspase-8 active subunits p18/p10. Therefore, in this cell line that has become resistant to CD95-induced apoptosis due to overexpression of Bcl-xL, Bcl-xL acts independently and downstream of caspase-8 (Medema, 1998).

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).

Apoptosis often involves the release of cytochrome c from mitochondria, leading to caspase activation. However, in apoptosis mediated by CD95 (Fas/APO-1), caspase-8 (FLICE/MACH/Mch5) is immediately activated and, in principle, could process other caspases directly. To investigate whether caspase-8 could also act through mitochondria, active caspase-8 was added to a Xenopus cell-free system requiring these organelles. Caspase-8 rapidly promotes the apoptotic program, culminating in fragmentation of chromatin and the nuclear membrane. In extracts devoid of mitochondria, caspase-8 produces DNA degradation, but leaves nuclear membranes intact. Thus, mitochondria are required for complete engagement of the apoptotic machinery. In the absence of mitochondria, high concentrations of caspase-8 are required to activate downstream caspases. However, when mitochondria are present, the effects of low concentrations of caspase-8 are vastly amplified through cytochrome c-dependent caspase activation. Caspase-8 promotes cytochrome c release indirectly, by cleaving at least one cytosolic substrate. Bcl-2 blocks apoptosis only at the lowest caspase-8 concentrations, potentially explaining why CD95-induced apoptosis can often evade inhibition by Bcl-2 (Kuwana, 1998).

Although the molecular mechanisms of TNF signaling have been largely elucidated, the principle that regulates the balance of life and death is still unknown. The death domain kinase RIP, a key component of the TNF signaling complex, is cleaved by Caspase-8 in TNF-induced apoptosis. The cleavage site maps to the aspartic acid at position 324 of RIP. The cleavage of RIP results in the blockage of TNF-induced NFkappa-B activation. RIPc, one of the cleavage products, enhances interaction between TRADD and FADD/MORT1 and increases cell sensitivity to TNF. Most importantly, the Caspase-8 resistant RIP mutants protect cells against TNF-induced apopotosis. These results suggest that cleavage of RIP is an important process in TNF-induced apoptosis. Furthermore, RIP cleavage is also detected in other death receptor-mediated apoptosis. Therefore, this study provides a potential mechanism to convert cells from life to death in death receptor-mediated apoptosis (Lin, 1999).

Caspase-8/FLICE interaction with CED-3/Apaf-1

Previous genetic studies of the nematode C. elegans have identified three important components of cell death machinery. CED-3 and CED-4 (Drosophila homolog: Apaf-1-related-killer) function to kill cells, whereas CED-9 protects cells from death. Both CED-9 and its mammalian homolog Bcl-xL (a member of the Bcl-2 family of cell death regulators) interact with and inhibit the function of CED-4. In addition, CED-4 can simultaneously interact with CED-3 and its mammalian counterparts interleukin-1beta-converting enzyme (ICE) and FLICE. Thus, CED-4 plays a central role in the cell death pathway, biochemically linking CED-9 and the Bcl-2 family to CED-3 and the ICE family of pro-apoptotic cysteine proteases (Chinnaiyan, 1997).

Miscellaneous Caspase-8/FLICE interacting proteins

The CD95 signaling pathway comprises proteins that contain one or two death effector domains (DED), such as FADD/Mort1 or caspase-8. A novel 37 kDa protein, DEDD, is described that contains an N-terminal DED. DEDD is highly conserved between human and mouse (98. 7% identity) and is ubiquitously expressed. Overexpression of DEDD in 293T cells induces weak apoptosis, mainly through its DED by which it interacts with FADD and caspase-8. Endogenous DEDD is found in the cytoplasm and translocates into the nucleus upon stimulation of CD95. Immunocytological studies reveal that overexpressed DEDD directly translocates into the nucleus, where it co-localizes in the nucleolus with UBF, a basal factor required for RNA polymerase I transcription. Consistent with its nuclear localization, DEDD contains two nuclear localization signals and the C-terminal part shares sequence homology with histones. Recombinant DEDD binds to both DNA and reconstituted mononucleosomes and inhibits transcription in a reconstituted in vitro system. The results suggest that DEDD is a final target of a chain of events by which the CD95-induced apoptotic signal is transferred into the nucleolus to shut off cellular biosynthetic activities (Stegh, 1998).

Adenovirus type 5 encodes a 14.7-kDa protein that protects infected cells from tumor necrosis factor-induced cytolysis by an unknown mechanism. Infection of cells with an adenovirus vector expressing Fas ligand induces rapid apoptosis that is blocked by coinfection with a virus expressing the 14.7-kDa protein. Moreover, FasL promotes the rapid activation of DEVD-specific caspases, and caspase activation is blocked by coinfection with Adenovirus coding for the 14.7-kDa protein. Cell death induced by the overexpression of Fas ligand, Fas-associated death domain-containing protein (FADD)/MORT1, or FADD-like interleukin-1beta-converting enzyme (FLICE)/caspase-8 in a virus-free system is efficiently blocked by 14.7K expression. Moreover, 14.7K is shown to interact with FLICE. These results support the idea that FLICE is a cellular target for the 14.7-kDa protein (Chen, 1998a).

BH3-only proapoptotic proteins of the Bcl-2 family such as Bad, Bid, Bim, or Bik transduce death stimuli from the cell surface to the central death machinery. Following apoptosis stimulation, these molecules translocate from the cytosol to mitochondria where they bind to membrane-based Bcl-2 family members. Bid plays an essential role in Fas-mediated apoptosis of the so-called type II cells. In type II cells, such as Jurkat cells or hepatocytes, death-inducing signaling complex (DISC) formation is strongly reduced compared to type I cells in which activation of large amounts of caspase 8 by the DISC enables direct activation of downstream caspases leading to irreversible cell damage. In type II cells, following cleavage by caspase 8, the C-terminal fragment of Bid translocates to mitochondria and triggers the release of apoptogenic factors, thereby inducing cell death. Bid is phosphorylated by casein kinase I (CKI) and casein kinase II (CKII). Inhibition of CKI and CKII accelerates Fas-mediated apoptosis and Bid cleavage, whereas hyperactivity of the kinases delays apoptosis. When phosphorylated, Bid is insensitive to caspase 8 cleavage in vitro. Moreover, a mutant of Bid that cannot be phosphorylated was found to be more toxic than wild-type Bid. Together, these data indicate that phosphorylation of Bid represents a new mechanism whereby cells control apoptosis (Desagher, 2001).

Caspase-8/FLICE deficiency

Fas (APO-1/CD95) is a member of the tumor necrosis factor receptor (TNF-R) family and induces apoptosis when crosslinked with either Fas ligand or agonistic antibody (Fas antibody). The Fas-Fas ligand system has an important role in the immune system, where it is involved in the downregulation of immune responses and the deletion of peripheral autoreactive T lymphocytes. The intracellular domain of Fas interacts with several proteins including FADD (MORT-1), DAXX, RIP, FAF-1, FAP-1 and Sentrin. The adaptor protein FADD can, in turn, interact with the cysteine protease caspase-8 (FLICE/MACH/Mch5). In a genetic screen for essential components of the Fas-mediated apoptotic cascade, a Jurkat T lymphocyte cell line deficient in caspase-8 has been isolated that was completely resistant to Fas-induced apoptosis. Complementation of this cell line with wild-type caspase-8 restores Fas-mediated apoptosis. Fas activation of multiple caspases and of the stress kinase p38 and c-Jun NH2-terminial kinase (JNK) is completely blocked in the caspase-8-deficient cell line. Furthermore, the cell line is severely deficient in cell death induced by TNF-alpha and is partially deficient in cell death induced by ultraviolet irradiation, adriamycin and etoposide. This study provides the first genetic evidence that caspase-8 occupies an essential and apical position in the Fas signaling pathway and suggests that caspase-8 may participate broadly in multiple apoptotic pathways (Juo, 1998).

Regulation of Caspase-8/FLICE

Inhibitor of apoptosis (IAP) gene products play an evolutionarily conserved role in regulating programmed cell death in diverse species ranging from insects to humans. Human XIAP, cIAP1 and cIAP2 are direct inhibitors of at least two members of the caspase family of cell death proteases: caspase-3 and caspase-7. The mechanism by which IAPs interfere with activation of caspase-3 and other effector caspases was compared in cytosolic extracts where caspase activation was initiated by caspase-8, a proximal protease activated by ligation of TNF-family receptors, or by cytochrome c, which is released from mitochondria into the cytosol during apoptosis. These studies demonstrate that XIAP, cIAP1 and cIAP2 can prevent the proteolytic processing of pro-caspases -3, -6 and -7 by blocking the cytochrome c-induced activation of pro-caspase-9. In contrast, these IAP family proteins do not prevent the caspase-8-induced proteolytic activation of pro-caspase-3; however, they subsequently inhibit active caspase-3 directly, thus blocking downstream apoptotic events such as further activation of caspases. These findings demonstrate that IAPs can suppress different apoptotic pathways by inhibiting distinct caspases and identify pro-caspase-9 as a new target for IAP-mediated inhibition of apoptosis (Deveraux, 1998).

Tumor necrosis factor alpha (TNF-alpha) binding to the TNF receptor (TNFR) potentially initiates apoptosis and activates the transcription factor nuclear factor kappa B (NF-kappaB), which suppresses apoptosis by an unknown mechanism. The activation of NF-kappaB blocks the activation of caspase-8. TRAF1 (TNFR-associated factor 1), TRAF2, and the inhibitor-of-apoptosis (IAP) proteins c-IAP1 and c-IAP2 have been identified as gene targets of NF-kappaB transcriptional activity. In cells in which NF-kappaB is inactive, all of these proteins are required to fully suppress TNF-induced apoptosis, whereas c-IAP1 and c-IAP2 are sufficient to suppress etoposide-induced apoptosis. Thus, NF-kappaB activates a group of gene products that function cooperatively at the earliest checkpoint to suppress TNF-alpha-mediated apoptosis and that function more distally to suppress genotoxic agent-mediated apoptosis (Wang, 1998).

Cells of the monocyte/macrophage lineage play a central role in both innate and acquired immunity of the host. However, the acquisition of functional competence and the ability to respond to a variety of activating or modulating signals require maturation and differentiation of circulating monocytes and entails alterations in both the biochemical and phenotypic profiles of the cells. The process of activation also confers survival signals essential for the functional integrity of monocytes enabling the cells to remain viable in microenvironments of immune or inflammatory lesions that are rich in cytotoxic inflammatory mediators and reactive free-radical species. However, the molecular mechanisms of activation-induced survival signals in monocytes remain obscure. To define the mechanistic basis of activation-induced resistance to apoptosis in human monocytes at the molecular level, the modulation of expression profiles of genes associated with the cellular apoptotic pathways upon activation was evaluated and the following three results have been demonstrated: (1) activation results in selective resistance to apoptosis particularly to that induced by signaling via death receptors and DNA damage; (2) concurrent with activation, the most apical protease in the death receptor pathway, caspase-8/FLICE is rapidly down-regulated at the mRNA level representing a novel regulatory mechanism; and (3) activation of monocytes also leads to dramatic induction of the Bfl-1 gene, an anti apoptotic member of the Bcl-2 family. These findings thus provide a potential mechanistic basis for the activation-induced resistance to apoptosis in human monocytes (Perera, 1998).

Caspase-8/FLICE and Sphingomyelinase activation

Sphingomyelinase (SMase) activation and ceramide generation have emerged as an important signaling pathway transducing diverse biological effects of cytokine receptors like p55 tumor necrosis factor (TNF) receptor or Fas. The TNF-dependent activation of acid SMase (A-SMase) through the p55 TNF receptor-associated proteins TRADD and FADD is described. Overexpression of TRADD and FADD in 293 cells does not change the basal activity of A-SMase but enhances TNF-induced stimulation of A-SMase. Other TNF R55-associated proteins like TRAF2 and RIP, which have been reported to mediate TNF R55-mediated activation of nuclear factor kappaB, do not affect activation of A-SMase. Caspase inhibitors markedly reduce A-SMase activity, suggesting the involvement of an ICE-like protease in TRADD/FADD-mediated activation of A-SMase. Overexpression of caspase-8/a (FLICE/MACH) or caspase-10/b (FLICE2) does not change A-SMase activity, suggesting that TRADD/FADD-mediated activation of A-SMase involves a yet to be defined caspase-like protease distinct from caspase-8/a or -10/b (Schwandner, 1998).

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Death related ced-3/Nedd2-like protein: Biological Overview | Developmental Biology | Effects of Mutation | References

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