Structural similarity between the prion domain of HET-s and a homologue can explain amyloid cross-seeding in spite of limited sequence identity

Journal of Molecular Biology

Volumn 402, Issue 2, 2010, Pages 311-325

  Wasmer, Christian ^a   Zimmer, Agnes ^b   Sabaté, Raimon ^c,d   Soragni, Alice ^a   Saupe, Sven J ^c   Ritter, Christiane ^b   Meier, Beat H ^a  

^a ETH ZURICH   (Switzerland)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c CNRS   (France)

^d UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Amyloid; FgHET s protein; Fibrils; HET s protein; Prion

Indexed keywords

AMYLOID; DEUTERIUM; FUNGAL PROTEIN; HYDROGEN; HET-S PROTEIN, PODOSPORA ANSERINA; MACROMOLECULE; PRION;

AMINO ACID SEQUENCE; ARTICLE; FIBER; FUNGUS; FUSARIUM GRAMINEARUM; GENE LOCUS; IN VITRO STUDY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; PLANT SEED; PODOSPORA ANSERINA; PRION; PRIORITY JOURNAL; PROTEIN DOMAIN; SEQUENCE ALIGNMENT; SOLID STATE; CHEMISTRY; FUSARIUM; GENETICS; MACROMOLECULE; METABOLISM; MOLECULAR GENETICS; PODOSPORA; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; ULTRASTRUCTURE;

FUNGI; GIBBERELLA ZEAE; HET-S PRION; PODOSPORA ANSERINA;

AMINO ACID SEQUENCE; AMYLOID; FUNGAL PROTEINS; FUSARIUM; MACROMOLECULAR SUBSTANCES; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PODOSPORA; PRIONS; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 77956782713     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.06.053     Document Type: Article

References (53)

1. Prusiner S.B., Scott M.R., DeArmond S.J., Cohen F.E. Prion protein biology. Cell 1998, 93:337-348.
2. Wickner R.B., Edskes H.K., Shewmaker F., Nakayashiki T. Prions of fungi: inherited structures and biological roles. Nat. Rev. Microbiol. 2007, 5:611-618.
3. Coustou V., Deleu C., Saupe S., Begueret J. The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog. Proc. Natl Acad. Sci. USA 1997, 94:9773-9778.
4. Balguerie A., Dos Reis S., Ritter C., Chaignepain S., Coulary-Salin B., Forge V., et al. Domain organization and structure-function relationship of the HET-s prion protein of Podospora anserina. EMBO J. 2003, 22:2071-2081.
5. Wasmer C., Lange A., Van Melckebeke H., Siemer A.B., Riek R., Meier B.H. Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 2008, 319:1523-1526.
6. Kajava A.V., Steven A.C. Beta-rolls, beta-helices, and other beta-solenoid proteins. Adv. Protein Chem. 2006, 73:55-96.
7. Siemer A.B., Arnold A.A., Ritter C., Westfeld T., Ernst M., Riek R., Meier B.H. Observation of highly flexible residues in amyloid fibrils of the HET-s prion. J. Am. Chem. Soc. 2006, 128:13224-13228.
8. Lange A., Gattin Z., Van Melckebeke H., Wasmer C., Soragni A., van Gunsteren W.F., Meier B.H. A combined solid-state NMR and MD characterization of the stability and dynamics of the HET-s(218-289) prion in its amyloid conformation. ChemBioChem 2009, 10:1657-1665.
9. Wasmer C., Schütz A., Loquet A., Buhtz C., Greenwald J., Riek R., et al. The molecular organization of the fungal prion HET-s in its amyloid form. J. Mol. Biol. 2009, 394:119-127.
10. Parry D., Jenkinson P., McLeod L. Fusarium ear blight (scab) in small grain cereals-a review. Plant Pathol. 1995, 44:207-238.
11. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
12. Moreno-Hagelsieb G., Latimer K. Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics 2008, 24:319-324.
13. Sabate R., Baxa U., Benkemoun L., Sanchez de Groot N., Coulary-Salin B., Maddelein M., et al. Prion and non-prion amyloids of the HET-s prion forming domain. J. Mol. Biol. 2007, 370:768-783.
14. Ritter C., Maddelein M.L., Siemer A.B., Luhrs T., Ernst M., Meier B.H., et al. Correlation of structural elements and infectivity of the HET-s prion. Nature 2005, 435:844-848.
15. Luhrs T., Ritter C., Adrian M., Riek-Loher D., Bohrmann B., Dobeli H., et al. 3D structure of Alzheimer's amyloid-beta(1-42) fibrils. Proc. Natl Acad. Sci. USA 2005, 102:17342-17347.
16. Vilar M., Chou H.T., Luhrs T., Maji S.K., Riek-Loher D., Verel R., et al. The fold of alpha-synuclein fibrils. Proc. Natl Acad. Sci. USA 2008, 105:8637-8642.
17. Toyama B.H., Kelly M.J.S., Gross J.D., Weissman J.S. The structural basis of yeast prion strain variants. Nature 2007, 449:233-237.
18. Hoshino M., Katou H., Hagihara Y., Hasegawa K., Naiki H., Goto Y. Mapping the core of the beta(2)-microglobulin amyloid fibril by H/D exchange. Nat. Struct. Biol. 2002, 9:332-336.
19. Cornilescu G., Delaglio F., Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 1999, 13:289-302.
20. Spera S., Bax A. Empirical correlation between protein backbone conformation and C.alpha. and C.beta. 13C nuclear magnetic resonance chemical shifts. J. Am. Chem. Soc. 1991, 113:5490-5492.
21. Pines A., Gibby M., Waugh J. Proton-enhanced NMR of dilute spins in solids. J. Chem. Phys. 1973, 59:569-590.
22. Hediger S., Meier B.H., Ernst R.R. Adiabatic passage Hartmann-Hahn cross polarization in NMR under magic angle sample spinning. Chem. Phys. Lett. 1995, 240:449-456.
23. Takegoshi K., Nakamura S., Terao T. C-13-H-1 dipolar-assisted rotational resonance in magic-angle spinning NMR. Chem. Phys. Lett. 2001, 344:631-637.
24. Scholz I., Huber M., Manolikas T., Meier B.H., Ernst M. MIRROR recoupling and its application to spin diffusion under fast magic-angle spinning. Chem. Phys. Lett. 2008, 460:278-283.
25. Detken A., Hardy E.H., Ernst M., Kainosho M., Kawakami T., Aimoto S., Meier B.H. Methods for sequential resonance assignment in solid, uniformly 13C, 15N labelled peptides: quantification and application to antamanide. J. Biomol. NMR 2001, 20:203-221.
26. Straus S.K., Bremi T., Ernst R.R. Experiments and strategies for the assignment of fully 13C/15N-labelled polypeptides by solid state NMR. J. Biomol. NMR 1998, 12:39-50.
27. Rienstra C., Hohwy M., Hong M., Griffin R. 2D and 3D N-15-C-13-C-13 NMR chemical shift correlation spectroscopy of solids: assignment of MAS spectra of peptides. J. Am. Chem. Soc. 2000, 122:10979-10990.
28. Hong M. Resonance assignment of 13C/15N labeled solid proteins by two- and three-dimensional magic-angle-spinning NMR. J. Biomol. NMR 1999, 15:1-14.
29. Siemer A.B., Ritter C., Steinmetz M.O., Ernst M., Riek R., Meier B.H. 13C, 15N resonance assignment of parts of the HET-s prion protein in its amyloid form. J. Biomol. NMR 2006, 34:75-87.
30. Wishart D.S., Bigam C.G., Holm A., Hodges R.S., Sykes B.D. 1H, 13C and 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR 1995, 5:67-81.
31. Morris G.A., Freeman R. Enhancement of nuclear magnetic resonance signals by polarization transfer. J. Am. Chem. Soc. 1979, 101:760-762.
32. Burum D.P., Ernst R.R. Net polarization transfer via a J-ordered state for signal enhancement of low-sensitivity nuclei. J. Magn. Reson. 1980, 39:163-168.
33. Andronesi O.C., Becker S., Seidel K., Heise H., Young H.S., Baldus M. Determination of membrane protein structure and dynamics by magic-angle-spinning solid-state NMR spectroscopy. J. Am. Chem. Soc. 2005, 127:12965-12974.
34. Lange A., Meier B.H. Fungal prion proteins studied by solid-state NMR. C. R. Chim. 2008, 11:332-339.
35. Baldus M., Iuliucci R., Meier B.H. Probing through-bond connectivities and through-space distances in solids by magic-angle-spinning nuclear magnetic resonance. J. Am. Chem. Soc. 1997, 119:1121-1124.
36. Hardy E.H., Verel R., Meier B.H. Fast MAS total through-bond correlation spectroscopy. J. Magn. Reson. 2001, 148:459-464.
37. Ulrich E.L., Akutsu H., Doreleijers J.F., Harano Y., Ioannidis Y.E., Lin J., et al. BioMagResBank. Nucleic Acids Res. 2008, 36:D402-D408.
38. Hennetin J., Jullian B., Steven A.C., Kajava A.V. Standard conformations of beta-arches in beta-solenoid proteins. J. Mol. Biol. 2006, 358:1094-1105.
39. Wishart D.S., Nip A.M. Protein chemical shift analysis: a practical guide. Biochem. Cell Biol. 1998, 76:153-163.
40. Krebs M.R.H., Bromley E.H.C., Donald A.M. The binding of thioflavin-T to amyloid fibrils: localisation and implications. J. Struct. Biol. 2005, 149:30-37.
41. Chothia C., Lesk A.M. The relation between the divergence of sequence and structure in proteins. EMBO J. 1986, 5:823-826.
42. Ginalski K. Comparative modeling for protein structure prediction. Curr. Opin. Struct. Biol. 2006, 16:172-177.
43. Tycko R., Sciarretta K., Orgel J., Meredith S. Evidence for novel β-sheet structures in Iowa mutant β-amyloid fibrils. Biochemistry 2009, 48:6072-6084.
44. Dos Reis S., Coulary-Salin B., Forge V., Lascu I., Begueret J., Saupe S.J. The HET-s prion protein of the filamentous fungus Podospora anserina aggregates in vitro into amyloid-like fibrils. J. Biol. Chem. 2002, 277:5703-5706.
45. Santoro M., Bolen D. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl β-chymotrypsin using different denaturants. Biochemistry 1988, 27:8063-8068.
46. Pace C., Hebert E., Shaw K., Schell D., Both V., Krajcikova D., et al. Conformational stability and thermodynamics of folding of ribonucleases Sa, Sa2 and Sa3. J. Mol. Biol. 1998, 279:271-286.
47. Koditz J., Ulbrich-Hofmann R., Arnold U. Probing the unfolding region of ribonuclease A by site-directed mutagenesis. Eur. J. Biochem. 2004, 271:4147-4156.
48. Li R., Woodward C. The hydrogen exchange core and protein folding. Protein Sci. 1999, 8:1571-1590.
49. Wittekind M., Mueller L. HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resonances in proteins. J. Magn. Reson. Ser. B 1993, 101:201-205.
50. Diercks T., Coles M., Kessler H. An efficient strategy for assignment of cross-peaks in 3D heteronuclear NOESY experiments. J. Biomol. NMR 1999, 15:177-180.
51. Guntert P., Dotsch V., Wider G., Wuthrich K. Processing of multi-dimensional NMR data with the new software PROSA. J. Biomol. NMR 1992, 2:619-629.
52. Keller R. The Computer Aided Resonance Assignment Tutorial 2004, CANTINA Verlag, Goldau, Switzerland.
53. Böckmann A., Gardiennet C., Verel R., Hunkeler A., Loquet A., Pintacuda G., et al. Characterization of different water pools in solid-state NMR protein samples. J. Biomol. NMR 2009, 45:319-327.