TRAIL induces necroptosis involving RIPK1/RIPK3-dependent PARP-1 activation

Jouan-Lanhouet, Sandrine; Arshad, Muhammad; Piquet‐Pellorce, Claire; Martin-Chouly, Corinne; Moigne-Muller, Gwénaëlle Le; Herreweghe, Franky Van; Takahashi, Nozomi; Sergent, Odile; Lagadic‐Gossmann, Dominique; Vandenabeele, Peter; Samson, Michel; Dimanche‐Boitrel, Marie‐Thérèse

doi:10.1038/cdd.2012.90

Cited by 313 publications

(242 citation statements)

References 40 publications

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“…49 Primary Ripk3 þ / þ and Ripk3 À / À MEFs were isolated from E12.5 littermate embryos following standard protocol. The Tak1 þ / þ and Tak1 À / À MEFs were kindly provided by Dr. Takeuchi.…”

Section: Cell Lines Sv40 Large T-immortalizedmentioning

confidence: 99%

RIPK3 contributes to TNFR1-mediated RIPK1 kinase-dependent apoptosis in conditions of cIAP1/2 depletion or TAK1 kinase inhibition

et al. 2013

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Receptor-interacting protein kinase (RIPK) 1 and RIPK3 have emerged as essential kinases mediating a regulated form of necrosis, known as necroptosis, that can be induced by tumor necrosis factor (TNF) signaling. As a consequence, inhibiting RIPK1 kinase activity and repressing RIPK3 expression levels have become commonly used approaches to estimate the contribution of necroptosis to specific phenotypes. Here, we report that RIPK1 kinase activity and RIPK3 also contribute to TNFinduced apoptosis in conditions of cellular inhibitor of apoptosis 1 and 2 (cIAP1/2) depletion or TGF-b-activated kinase 1 (TAK1) kinase inhibition, implying that inhibition of RIPK1 kinase activity or depletion of RIPK3 under cell death conditions is not always a prerequisite to conclude on the involvement of necroptosis. Moreover, we found that, contrary to cIAP1/2 depletion, TAK1 kinase inhibition induces assembly of the cytosolic RIPK1/Fas-associated protein with death domain/caspase-8 apoptotic TNF receptor 1 (TNFR1) complex IIb without affecting the RIPK1 ubiquitylation status at the level of TNFR1 complex I. These results indicate that the recruitment of TAK1 to the ubiquitin (Ub) chains, and not the Ub chains per se, regulates the contribution of RIPK1 to the apoptotic death trigger. In line with this, we found that cylindromatosis repression only provided protection to TNFmediated RIPK1-dependent apoptosis in condition of reduced RIPK1 ubiquitylation obtained by cIAP1/2 depletion but not upon TAK1 kinase inhibition, again arguing for a role of TAK1 in preventing RIPK1-dependent apoptosis downstream of RIPK1 ubiquitylation. Importantly, we found that this function of TAK1 was independent of its known role in canonical nuclear factor-jB (NF-jB) activation. Our study therefore reports a new function of TAK1 in regulating an early NF-jB-independent cell death checkpoint in the TNFR1 apoptotic pathway. In both TNF-induced RIPK1 kinase-dependent apoptotic models, we found that RIPK3 contributes to full caspase-8 activation independently of its kinase activity or intact RHIM domain. In contrast, RIPK3 participates in caspase-8 activation by acting downstream of the cytosolic death complex assembly, possibly via reactive oxygen species generation. Tumor necrosis factor (TNF) is a pleiotropic cytokine that controls a variety of cellular responses, including proliferation, differentiation, inflammatory cytokine production, survival and death. 1 TNF signals by binding and activating two cell surface receptors, TNF receptor (TNFR) 1 and TNFR2, 2 but most of its biological activities have been associated with TNFR1. 3 In most cell types, TNFR1 activation does not induce cell death but instead leads to the transcriptional upregulation of genes encoding pro-survival and pro-inflammatory molecules. 4 This function is mediated by the assembly of a plasma membranebound multiprotein signaling complex, referred to as TNFR1 complex I, 5 that contains TNF receptor-associated death domain (TRADD), receptor-interacting protein kinase 1 (RIPK1, also know...

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Section: Cell Lines Sv40 Large T-immortalizedmentioning

confidence: 99%

RIPK3 contributes to TNFR1-mediated RIPK1 kinase-dependent apoptosis in conditions of cIAP1/2 depletion or TAK1 kinase inhibition

et al. 2013

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“…Necroptosis mediated by TNF was previously described to be independent of and distinct from PARP-1 activation (11). On the contrary, TRAIL was previously described to induce necroptosis dependent on PARP-1 under acidic-pH conditions (31). Three PARP-1 inhibitors, PJ-34, 3-AB, and olaparib, rescued cells from the formation of TRAIL-zVAD-mediated PAR chains in a concentration-dependent manner (Fig.…”

Section: Atg5 But Not Atg16l1 or Receptor Internalization Promotes Trmentioning

confidence: 79%

“…1C), which are known to downregulate the protein level of RIPK1 (30). Furthermore, the main role of RIPK1 during necroptosis was confirmed for all analyzed cell lines (L929Ts, NIH 3T3, Jurkat, and HT-29), as Nec-1s (analogue of Nec-1, a specific and stable RIPK1 inhibitor, but lacking the targeting effect on the immunomodulatory enzyme indoleamine 2,3-dioxygenase [IDO] [31]) prevented the execution of TRAIL-mediated necroptosis (Fig. 1D).…”

Section: Resultsmentioning

confidence: 98%

Differences and Similarities in TRAIL- and Tumor Necrosis Factor-Mediated Necroptotic Signaling in Cancer Cells

Sosna

Philipp

Chico

et al. 2016

Molecular and Cellular Biology

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e Recently, a type of regulated necrosis (RN) called necroptosis was identified to be involved in many pathophysiological processes and emerged as an alternative method to eliminate cancer cells. However, only a few studies have elucidated components of TRAIL-mediated necroptosis useful for anticancer therapy. Therefore, we have compared this type of cell death to tumor necrosis factor (TNF)-mediated necroptosis and found similar signaling through acid and neutral sphingomyelinases, the mitochondrial serine protease HtrA2/Omi, Atg5, and vacuolar H ؉ -ATPase. Notably, executive mechanisms of both TRAIL-and TNF-mediated necroptosis are independent of poly(ADP-ribose) polymerase 1 (PARP-1), and depletion of p38␣ increases the levels of both types of cell death. Moreover, we found differences in signaling between TNF-and TRAIL-mediated necroptosis, e.g., a lack of involvement of ubiquitin carboxyl hydrolase L1 (UCH-L1) and Atg16L1 in executive mechanisms of TRAIL-mediated necroptosis. Furthermore, we discovered indications of an altered involvement of mitochondrial components, since overexpression of the mitochondrial protein Bcl-2 protected Jurkat cells from TRAIL-and TNF-mediated necroptosis, and overexpression of Bcl-XL diminished only TRAIL-induced necroptosis in Colo357 cells. Furthermore, TRAIL does not require receptor internalization and endosome-lysosome acidification to mediate necroptosis. Taken together, pathways described for TRAIL-mediated necroptosis and differences from those for TNF-mediated necroptosis might be unique targets to increase or modify necroptotic signaling and eliminate tumor cells more specifically in future anticancer approaches.

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“…44,45 However, genetic ablation or pharmacological inhibition of RIPK1 failed to block PARP1-mediated cell death induced by DNA alkylating agents. 46 Our data also showed that the kinase activity of RIPK1 did not affect PARP1-dependent necrosis in response to H 2 O 2 .…”

Section: Discussionmentioning

confidence: 99%

FAF1 mediates regulated necrosis through PARP1 activation upon oxidative stress leading to dopaminergic neurodegeneration

Kim

2016

Cell Death Differ

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Cumulative damage caused by oxidative stress results in diverse pathological conditions. Therefore, elucidating the molecular mechanisms underlying cell death following oxidative stress is important. Here, we describe a novel role for Fas-associated factor 1 (FAF1) as a crucial regulator of necrotic cell death elicited by hydrogen peroxide. Upon oxidative insult, FAF1 translocated from the cytoplasm to the nucleus and promoted the catalytic activation of poly(ADP-ribose) polymerase 1 (PARP1) through physical interaction. Moreover, FAF1 depletion prevented PARP1-linked downstream events involved in the triggering of cell death, including energetic collapse, mitochondrial depolarization and nuclear translocation of apoptosis-inducing factor (AIF), implying that FAF1 has a key role in PARP1-dependent necrosis in response to oxidative stress. We further investigated whether FAF1 might contribute to the pathogenesis of Parkinson's disease through excessive PARP1 activation. Indeed, the overexpression of FAF1 using a recombinant adeno-associated virus system in the mouse ventral midbrain promoted PARP1 activation and dopaminergic neurodegeneration in a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) mouse model of Parkinson's disease. Collectively, our data demonstrate the presence of an FAF1-PARP1 axis that is involved in oxidative stress-induced necrosis and in the pathology of Parkinson's disease.

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TRAIL induces necroptosis involving RIPK1/RIPK3-dependent PARP-1 activation

Cited by 313 publications

References 40 publications

RIPK3 contributes to TNFR1-mediated RIPK1 kinase-dependent apoptosis in conditions of cIAP1/2 depletion or TAK1 kinase inhibition

RIPK3 contributes to TNFR1-mediated RIPK1 kinase-dependent apoptosis in conditions of cIAP1/2 depletion or TAK1 kinase inhibition

Differences and Similarities in TRAIL- and Tumor Necrosis Factor-Mediated Necroptotic Signaling in Cancer Cells

FAF1 mediates regulated necrosis through PARP1 activation upon oxidative stress leading to dopaminergic neurodegeneration

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