Identification of a novel cell death-inducing domain reveals that fungal amyloid-controlled programmed cell death is related to necroptosis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 10, 2016, Pages 2720-2725

  Daskalov, Asen ^a,d   Habenstein, Birgit ^a   Sabaté, Raimon ^b   Berbon, Mélanie ^a   Martinez, Denis ^a   Chaignepain, Stéphane ^a   Coulary Salin, Bénédicte ^a   Hofmann, Kay ^c   Loquet, Antoine ^a   Saupe, Sven J ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF COLOGNE   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amyloid; Incompatibility; Necroptosis; Prion; Programmed cell death

Indexed keywords

AMYLOID; HELLP PROTEIN; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PROTEIN; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; FUNGAL PROTEIN; PHOTOPROTEIN; PRION;

APOPTOSIS; ARTICLE; CHAETOMIUM GLOBOSUM; CONTROLLED STUDY; GENE CLUSTER; HOST RESISTANCE; NECROPTOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; SOLID STATE; X RAY DIFFRACTION; AMINO ACID SEQUENCE; CELL DEATH; CELL MEMBRANE; CHEMISTRY; GENETICS; INFRARED SPECTROSCOPY; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PODOSPORA; PRION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMYLOID; CELL DEATH; CELL MEMBRANE; FUNGAL PROTEINS; LUMINESCENT PROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PODOSPORA; PRIONS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; X-RAY DIFFRACTION;

EID: 84960406547     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1522361113     Document Type: Article

References (31)

1. Dickman MB, Fluhr R (2013) Centrality of host cell death in plant-microbe interactions. Annu Rev Phytopathol 51:543-570.
2. Blander JM (2014) A long-awaited merger of the pathways mediating host defence and programmed cell death. Nat Rev Immunol 14(9):601-618.
3. Pinan-Lucarré B, Paoletti M, Clavé C (2007) Cell death by incompatibility in the fungus Podospora. Semin Cancer Biol 17(2):101-111.
4. Makarova KS, Anantharaman V, Aravind L, Koonin EV (2012) Live virus-free or die: Coupling of antivirus immunity and programmed suicide or dormancy in prokaryotes. Biol Direct 7:40.
5. van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62(14):4749-4761.
6. Wasmer C, et al. (2008) Amyloid fibrils of the HET-s (218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319(5869):1523-1526.
7. Balguerie A, et al. (2003) Domain organization and structure-function relationship of the HET-s prion protein of Podospora anserina. EMBO J 22(9):2071-2081.
8. Greenwald J, et al. (2010) The mechanism of prion inhibition by HET-S. Mol Cell 38(6):889-899.
9. Seuring C, et al. (2012) The mechanism of toxicity in HET-S/HET-s prion incompatibility. PLoS Biol 10(12):e1001451.
10. Mathur V, Seuring C, Riek R, Saupe SJ, Liebman SW (2012) Localization of HET-S to the cell periphery, not to [Het-s] aggregates, is associated with [Het-s]-HET-S toxicity. Mol Cell Biol 32(1):139-153.
11. Daskalov A, et al. (2015) Signal transduction by a fungal NOD-like receptor based on propagation of a prion amyloid fold. PLoS Biol 13(2):e1002059.
12. Daskalov A, Paoletti M, Ness F, Saupe SJ (2012) Genomic clustering and homology between HET-S and the NWD2 STAND protein in various fungal genomes. PLoS One 7(4):e34854.
13. Cai X, et al. (2014) Prion-like polymerization underlies signal transduction in antiviral immune defense and inflammasome activation. Cell 156(6):1207-1222.
14. Wu H (2013) Higher-order assemblies in a new paradigm of signal transduction. Cell 153(2):287-292.
15. Li J, et al. (2012) The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell 150(2):339-350.
16. Sun L, et al. (2012) Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148(1-2):213-227.
17. Daskalov A, Dyrka W, Saupe SJ (2015) Theme and variations: Evolutionary diversification of the HET-s functional amyloid motif. Sci Rep 5:12494.
18. Graziani S, Silar P, Daboussi MJ (2004) Bistability and hysteresis of the "Secteur" differentiation are controlled by a two-gene locus in Nectria haematococca. BMC Biol 2:18.
19. Dyrka W, et al. (2014) Diversity and variability of NOD-like receptors in fungi. Genome Biol Evol 6(12):3137-3158.
20. Kajava AV, Klopffleisch K, Chen S, Hofmann K (2014) Evolutionary link between metazoan RHIM motif and prion-forming domain of fungal heterokaryon incompatibility factor HET-s/HET-s. Sci Rep 4:17436.
21. Mueller BK, Subramaniam S, Senes A (2014) A frequent, GxxxG-mediated, transmembrane association motif is optimized for the formation of interhelical Ca-H hydrogen bonds. Proc Natl Acad Sci USA 111(10):E888-E895.
22. Sabaté R, et al. (2007) Prion and non-prion amyloids of the HET-s prion forming domain. J Mol Biol 370(4):768-783.
23. Murphy JM, et al. (2013) The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39(3):443-453.
24. Cai Z, et al. (2014) Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat Cell Biol 16(1):55-65.
25. Chen X, et al. (2014) Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res 24(1):105-121.
26. Su L, et al. (2014) A plug release mechanism for membrane permeation by MLKL. Structure 22(10):1489-1500.
27. Collier SM, Hamel LP, Moffett P (2011) Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein. Mol Plant Microbe Interact 24(8):918-931.
28. Böckmann A, et al. (2009) Characterization of different water pools in solid-state NMR protein samples. J Biomol NMR 45(3):319-327.
29. Fung BM, Khitrin AK, Ermolaev K (2000) An improved broadband decoupling sequence for liquid crystals and solids. J Magn Reson 142(1):97-101.
30. Wang Y, Jardetzky O (2002) Probability-based protein secondary structure identification using combined NMR chemical-shift data. Protein Sci 11(4):852-861.
31. Vranken WF, et al. (2005) The CCPN data model for NMR spectroscopy: Development of a software pipeline. Proteins 59(4):687-696.