TY - JOUR
T1 - The Lck inhibitor, AMG-47a, blocks necroptosis and implicates RIPK1 in signalling downstream of MLKL
AU - Jacobsen, Annette V.
AU - Pierotti, Catia L.
AU - Lowes, Kym N.
AU - Au, Amanda E.
AU - Zhang, Ying
AU - Etemadi, Nima
AU - Fitzgibbon, Cheree
AU - Kersten, Wilhelmus J.A.
AU - Samson, André L.
AU - van Delft, Mark F.
AU - Huang, David C.S.
AU - Sabroux, Hélène Jousset
AU - Lessene, Guillaume
AU - Silke, John
AU - Murphy, James M.
N1 - Funding Information:
We thank the following people for technical assistance: Sam Young (cloning), Anne Hempel (CETSA), and Wil Lehmann (Western blots). Thanks also to Vishva Dixit for Ripk3−/− mice, Grant Dewson for supplying Bax−/− Bak−/− and wild-type MEFs, and Jean-Marc Garnier for coordinating DiscoverX analyses. We acknowledge Compounds Australia (www.compoundsaustralia.com) for their provision of specialised compound management and logistics services to the project.
Funding Information:
This work was funded by Australian National Health and Medical Research Council (NHMRC) grants (1046984, 1067289, 1105023, 1124735, 1124737 and 2002965) and fellowships (JMM: 1105754, 1172929; JS: 1058190,1107149; GL: 1117089; DCSH: 1156024); Anaxis Pharma Pty Ltd for funding support; and was made possible through Victorian State Government Operational Infrastructure Support, NHMRC IRIISS grant (9000719) and Australian Cancer Research Foundation funding. AVJ and CLP were supported by an Australian Government Research Training Program Stipend Scholarship. WEHI’s screening facility is supported by Therapeutic Innovation Australia (TIA). TIA is supported by the Australian Government through the National Collaborative Research Infrastructure Strategy (NCRIS) program.
Publisher Copyright:
© 2022, The Author(s).
PY - 2022/4
Y1 - 2022/4
N2 - Necroptosis is a form of caspase-independent programmed cell death that arises from disruption of cell membranes by the mixed lineage kinase domain-like (MLKL) pseudokinase after its activation by the upstream kinases, receptor interacting protein kinase (RIPK)-1 and RIPK3, within a complex known as the necrosome. Dysregulated necroptosis has been implicated in numerous inflammatory pathologies. As such, new small molecule necroptosis inhibitors are of great interest, particularly ones that operate downstream of MLKL activation, where the pathway is less well defined. To better understand the mechanisms involved in necroptosis downstream of MLKL activation, and potentially uncover new targets for inhibition, we screened known kinase inhibitors against an activated mouse MLKL mutant, leading us to identify the lymphocyte-specific protein tyrosine kinase (Lck) inhibitor AMG-47a as an inhibitor of necroptosis. We show that AMG-47a interacts with both RIPK1 and RIPK3, that its ability to protect from cell death is dependent on the strength of the necroptotic stimulus, and that it blocks necroptosis most effectively in human cells. Moreover, in human cell lines, we demonstrate that AMG-47a can protect against cell death caused by forced dimerisation of MLKL truncation mutants in the absence of any upstream signalling, validating that it targets a process downstream of MLKL activation. Surprisingly, however, we also found that the cell death driven by activated MLKL in this model was completely dependent on the presence of RIPK1, and to a lesser extent RIPK3, although it was not affected by known inhibitors of these kinases. Together, these results suggest an additional role for RIPK1, or the necrosome, in mediating human necroptosis after MLKL is phosphorylated by RIPK3 and provide further insight into reported differences in the progression of necroptosis between mouse and human cells.
AB - Necroptosis is a form of caspase-independent programmed cell death that arises from disruption of cell membranes by the mixed lineage kinase domain-like (MLKL) pseudokinase after its activation by the upstream kinases, receptor interacting protein kinase (RIPK)-1 and RIPK3, within a complex known as the necrosome. Dysregulated necroptosis has been implicated in numerous inflammatory pathologies. As such, new small molecule necroptosis inhibitors are of great interest, particularly ones that operate downstream of MLKL activation, where the pathway is less well defined. To better understand the mechanisms involved in necroptosis downstream of MLKL activation, and potentially uncover new targets for inhibition, we screened known kinase inhibitors against an activated mouse MLKL mutant, leading us to identify the lymphocyte-specific protein tyrosine kinase (Lck) inhibitor AMG-47a as an inhibitor of necroptosis. We show that AMG-47a interacts with both RIPK1 and RIPK3, that its ability to protect from cell death is dependent on the strength of the necroptotic stimulus, and that it blocks necroptosis most effectively in human cells. Moreover, in human cell lines, we demonstrate that AMG-47a can protect against cell death caused by forced dimerisation of MLKL truncation mutants in the absence of any upstream signalling, validating that it targets a process downstream of MLKL activation. Surprisingly, however, we also found that the cell death driven by activated MLKL in this model was completely dependent on the presence of RIPK1, and to a lesser extent RIPK3, although it was not affected by known inhibitors of these kinases. Together, these results suggest an additional role for RIPK1, or the necrosome, in mediating human necroptosis after MLKL is phosphorylated by RIPK3 and provide further insight into reported differences in the progression of necroptosis between mouse and human cells.
UR - https://www.scopus.com/pages/publications/85127528550
U2 - 10.1038/s41419-022-04740-w
DO - 10.1038/s41419-022-04740-w
M3 - Article
C2 - 35365636
AN - SCOPUS:85127528550
SN - 2041-4889
VL - 13
JO - Cell Death and Disease
JF - Cell Death and Disease
IS - 4
M1 - 291
ER -