The Mechanism of Toxicity in HET-S/HET-s Prion Incompatibility

PLoS Biology

Volumn 10, Issue 12, 2012, Pages

  Seuring, Carolin ^a   Greenwald, Jason ^a   Wasmer, Christian ^a,c   Wepf, Roger ^a   Saupe, Sven J ^b   Meier, Beat H ^a   Riek, Roland ^a  

^a ETH ZURICH   (Switzerland)

^b Institut de Biochimie et Genetique Cellulaires   (France)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; GLOBULAR PROTEIN; LIPOSOME; MEMBRANE PROTEIN; PRION PROTEIN; PROTEIN BETA SOLENOID; PROTEIN HELO; PROTEIN HET S; PROTEOLIPOSOME; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; FREEZE FRACTURE; FUNGAL MEMBRANE; LIPID MEMBRANE; MEMBRANE DAMAGE; MEMBRANE STABILIZATION; MOLECULAR MECHANICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OLIGOMERIZATION; PARTICLE SIZE; PODOSPORA ANSERINA; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN UNFOLDING; SOLID STATE; TRANSMISSION ELECTRON MICROSCOPY;

AMINO ACID SEQUENCE; AMYLOID; CELL MEMBRANE; ESCHERICHIA COLI; FREEZE FRACTURING; FUNGAL PROTEINS; LIPOSOMES; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MYCOTOXINS; PHENOTYPE; PHOSPHORYLCHOLINE; PODOSPORA; PRIONS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; THERMODYNAMICS;

FUNGI; HET-S PRION; PODOSPORA ANSERINA; SOLENOIDEA;

EID: 84871682946     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001451     Document Type: Article

References (59)

1. Chiti F, Dobson CM, (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75: 333-366.
2. Fowler DM, Koulov AV, Balch WE, Kelly JW, (2007) Functional amyloid-from bacteria to humans. Trends Biochem Sci 32: 217-224.
3. Glass NL, Jacobson DJ, Shiu PK, (2000) The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annu Rev Genet 34: 165-186.
4. Saupe SJ, (2000) Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiol Mol Biol Rev 64: 489-502.
5. Hartl DL, Dempster ER, Brown SW, (1975) Adaptive significance of vegetative incompatibility in Neurospora crassa. Genetics 81: 553-569.
6. Aanen DK, Debets AJM, Glass NL, Saupe SJ (2010) Biology and genetics of vegetative incompatibility in fungi. Borkovich KA, Ebbole DJ, editors. Washington (D.C.): ASM Press. 274-288 p.
7. Choi GH, Dawe AL, Churbanov A, Smith ML, Milgroom MG, et al. (2012) Molecular characterization of vegetative incompatibility genes that restrict hypovirus transmission in the chestnut blight fungus Cryphonectria parasitica. Genetics 190: 113-127.
8. Pinan-Lucarre B, Paoletti M, Clave C, (2007) Cell death by incompatibility in the fungus Podospora. Semin Cancer Biol 17: 101-111.
9. Coustou V, Deleu C, Saupe S, Begueret J, (1997) The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog. Proc Natl Acad Sci U S A 94: 9773-9778.
10. Balguerie A, Dos Reis S, Ritter C, Chaignepain S, Coulary-Salin B, et al. (2003) Domain organization and structure-function relationship of the HET-s prion protein of Podospora anserina. EMBO J 22: 2071-2081.
11. Maddelein ML, Dos Reis S, Duvezin-Caubet S, Coulary-Salin B, Saupe SJ, (2002) Amyloid aggregates of the HET-s prion protein are infectious. Proc Natl Acad Sci U S A 99: 7402-7407.
12. Mathur V, Seuring C, Riek R, Saupe SJ, Liebman SW, (2011) 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: 139-153.
13. Turcq B, Deleu C, Denayrolles M, Begueret J, (1991) Two allelic genes responsible for vegetative incompatibility in the fungus Podospora anserina are not essential for cell viability. Mol Gen Genet 228: 265-269.
14. Greenwald J, Buhtz C, Ritter C, Kwiatkowski W, Choe S, et al. (2010) The mechanism of prion inhibition by HET-S. Mol Cell 38: 889-899.
15. Beisson-Schecroun J, (1962) Incompatibilité cellulaire et interactions nucléocytoplamsiques dans les phénomènes de barrage chez le Podospora anserina. Ann Genet 4: 3-50.
16. Ritter C, Maddelein ML, Siemer AB, Luhrs T, Ernst M, et al. (2005) Correlation of structural elements and infectivity of the HET-s prion. Nature 435: 844-848.
17. Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R, et al. (2008) Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319: 1523-1526.
18. Van Melckebeke H, Wasmer C, Lange A, Ab E, Loquet A, et al. (2010) Atomic-resolution three-dimensional structure of HET-s(218-289) amyloid fibrils by solid-state NMR spectroscopy. J Am Chem Soc 132: 13765-13775.
19. Wasmer C, Schutz A, Loquet A, Buhtz C, Greenwald J, et al. (2009) The molecular organization of the fungal prion HET-s in its amyloid form. J Mol Biol 394: 119-127.
20. Dos Reis S, Coulary-Salin B, Forge V, Lascu I, Begueret J, et al. (2002) The HET-s prion protein of the filamentous fungus Podospora anserina aggregates in vitro into amyloid-like fibrils. J Biol Chem 277: 5703-5706.
21. Coustou V, Deleu C, Saupe SJ, Begueret J, (1999) Mutational analysis of the [Het-s] prion analog of Podospora anserina. A short N-terminal peptide allows prion propagation. Genetics 153: 1629-1640.
22. Kayalar C, Duzgunes N, (1986) Membrane action of colicin E1: detection by the release of carboxyfluorescein and calcein from liposomes. Biochim Biophys Acta 860: 51-56.
23. Osborn MJ, Munson R, (1974) Separation of the inner (cytoplasmic) and outer membranes of Gram-negative bacteria. Methods Enzymol 31: 642-653.
24. Deleu C, Clave C, Begueret J, (1993) A single amino acid difference is sufficient to elicit vegetative incompatibility in the fungus Podospora anserina. Genetics 135: 45-52.
25. Siemer AB, Ritter C, Steinmetz MO, Ernst M, Riek R, et al. (2006) 13C, 15N resonance assignment of parts of the HET-s prion protein in its amyloid form. J Biomol NMR 34: 75-87.
26. Schuetz A, Wasmer C, Habenstein B, Verel R, Greenwald J, et al. (2010) Protocols for the sequential solid-state NMR spectroscopic assignment of a uniformly labeled 25 kDa protein: HET-s(1-227). Chembiochem 11: 1543-1551.
27. Lewandowski JR, De Paepe G, Griffin RG, (2007) Proton assisted insensitive nuclei cross polarization. J Am Chem Soc 129: 728-729.
28. De Paepe G, Lewandowski JR, Loquet A, Eddy M, Megy S, et al. (2011) Heteronuclear proton assisted recoupling. J Chem Phys 134: 095101.
29. Tusnady GE, Simon I, (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17: 849-850.
30. von Heijne G, (1992) Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225: 487-494.
31. Hofmann K, Stoffel W, (1993) TMbase- A database of membrane spanning proteins segments. Biol Chem Hoppe-Seyler 374.
32. Krogh A, Larsson B, von Heijne G, Sonnhammer EL, (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
33. Maslennikov I, Krupa M, Dickson C, Esquivies L, Blain K, et al. (2009) Characterization of protein detergent complexes by NMR, light scattering, and analytical ultracentrifugation. J Struct Funct Genomics 10: 25-35.
34. Maji SK, Perrin MH, Sawaya MR, Jessberger S, Vadodaria K, et al. (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325: 328-332.
35. Greenwald J, Riek R, (2010) Biology of amyloid: structure, function, and regulation. Structure 18: 1244-1260.
36. Loquet A, Bousset L, Gardiennet C, Sourigues Y, Wasmer C, et al. (2009) Prion fibrils of Ure2p assembled under physiological conditions contain highly ordered, natively folded modules. J Mol Biol 394: 108-118.
37. Hegde RS, Mastrianni JA, Scott MR, DeFea KA, Tremblay P, et al. (1998) A transmembrane form of the prion protein in neurodegenerative disease. Science 279: 827-834.
38. Kagan BL, Hirakura Y, Azimov R, Azimova R, Lin MC, (2002) The channel hypothesis of Alzheimer's disease: current status. Peptides 23: 1311-1315.
39. Arispe N, Rojas E, Pollard HB, (1993) Alzheimer disease amyloid beta protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc Natl Acad Sci U S A 90: 567-571.
40. Stefani M, Dobson CM, (2003) Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J Mol Med (Berl) 81: 678-699.
41. Mueller M, Ban N, (2010) Enhanced SnapShot: pore-forming toxins. Cell 142: 334, 334 e331.
42. Mueller M, Grauschopf U, Maier T, Glockshuber R, Ban N, (2009) The structure of a cytolytic alpha-helical toxin pore reveals its assembly mechanism. Nature 459: 726-730.
43. Parker MW, Buckley JT, Postma JP, Tucker AD, Leonard K, et al. (1994) Structure of the Aeromonas toxin proaerolysin in its water-soluble and membrane-channel states. Nature 367: 292-295.
44. Young JA, Collier RJ, (2007) Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu Rev Biochem 76: 243-265.
45. Pilpa RM, Bayrhuber M, Marlett JM, Riek R, Young JA, (2011) A receptor-based switch that regulates anthrax toxin pore formation. PLoS Pathog 7: e1002354 doi:10.1371/journal.ppat.1002354.
46. Bischofberger M, Iacovache I, Gisou van der Goot F, (2012) Pathogenic pore-forming proteins: function and host response. Cell Host Microbe 12: 266-275.
47. Li N, Erman M, Pangborn W, Duax WL, Park CM, et al. (1999) Structure of Ustilago maydis killer toxin KP6 alpha-subunit. A multimeric assembly with a central pore. J Biol Chem 274: 20425-20431.
48. Tomita T, Noguchi K, Mimuro H, Ukaji F, Ito K, et al. (2004) Pleurotolysin, a novel sphingomyelin-specific two-component cytolysin from the edible mushroom Pleurotus ostreatus, assembles into a transmembrane pore complex. J Biol Chem 279: 26975-26982.
49. Ottmann C, Luberacki B, Kufner I, Koch W, Brunner F, et al. (2009) A common toxin fold mediates microbial attack and plant defense. Proc Natl Acad Sci U S A 106: 10359-10364.
50. Szczesny P, Iacovache I, Muszewska A, Ginalski K, van der Goot FG, et al. (2011) Extending the aerolysin family: from bacteria to vertebrates. PLoS One 6: e20349 doi:10.1371/journal.pone.0020349.
51. Paoletti M, Saupe SJ, (2009) Fungal incompatibility: evolutionary origin in pathogen defense? Bioessays 31: 1201-1210.
52. 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: e34854 doi:10.1371/journal.pone.0034854.
53. Paoletti M, Clave C, (2007) The fungus-specific HET domain mediates programmed cell death in Podospora anserina. Eukaryot Cell 6: 2001-2008.
54. Mestre P, Baulcombe DC, (2006) Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18: 491-501.
55. Riedl SJ, Salvesen GS, (2007) The apoptosome: signalling platform of cell death. Nat Rev Mol Cell Biol 8: 405-413.
56. Saleh M, (2011) The machinery of Nod-like receptors: refining the paths to immunity and cell death. Immunol Rev 243: 235-246.
57. Heger A, Wilton CA, Sivakumar A, Holm L, (2005) ADDA: a domain database with global coverage of the protein universe. Nucleic Acids Res 33: D188-191.
58. Bockmann A, Gardiennet C, Verel R, Hunkeler A, Loquet A, et al. (2009) Characterization of different water pools in solid-state NMR protein samples. J Biomol NMR 45: 319-327.
59. Verel R, Ernst M, Meier BH, (2001) Adiabatic dipolar recoupling in solid-state NMR: the DREAM scheme. J Magn Reson 150: 81-99.