Essential Role of Proline Isomerization in Stefin B Tetramer Formation

Journal of Molecular Biology

Volumn 366, Issue 5, 2007, Pages 1569-1579

  Jenko Kokalj, Saša ^a   Gunčar, Gregor ^a   Štern, Igor ^a   Morgan, Gareth ^b   Rabzelj, Sabina ^a   Kenig, Manca ^a   Staniforth, Rosemary A ^b   Waltho, Jonathan P ^b   Žerovnik, Eva ^a   Turk, Dušan ^a  

^a JO EF STEFAN INSTITUTE   (Slovenia)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

amyloid; crystal structure; cystatin; domain swapping; stefin

Indexed keywords

AMYLOID; CYSTATIN; CYSTATIN C; PROLINE; STEFIN B; TETRAMER;

ARTICLE; ISOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; VASCULAR AMYLOIDOSIS;

EID: 33846799138     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.12.025     Document Type: Article

References (41)

1. Conway K.A., Lee S.J., Rochet J.C., Ding T.T., Williamson R.E., and Lansbury Jr. P.T. Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc. Natl Acad. Sci. USA 97 (2000) 571-576
2. Jahn T.R., Parker M.J., Homans S.W., and Radford S.E. Amyloid formation under physiological conditions proceeds via a native-like folding intermediate. Nature Struct. Mol. Biol. 3 (2006) 195-201
3. Silva J.L., Cordeiro Y., and Foguel D. Protein folding and aggregation: two sides of the same coin in the condensation of proteins revealed by pressure studies. Biochim. Biophys. Acta 1764 (2006) 443-451
4. Kameda A., Hoshino M., Higurashi T., Takahashi S., Naiki H., and Goto Y. Nuclear magnetic resonance characterization of the refolding intermediate of beta2-microglobulin trapped by non-native prolyl peptide bond. J. Mol. Biol. 348 (2005) 383-397
5. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., Zurdo J., et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416 (2002) 507-511
6. Bucciantini M., Calloni G., Chiti F., Formigli L., Nosi D., Dobson C.M., and Stefani M. Pre-fibrillar amyloid protein aggregates share common features of cytotoxicity. J. Biol. Chem. 279 (2004) 31374-31382
7. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., and Glabe C.G. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300 (2003) 486-489
8. Glabe C.G. Conformation-dependent antibodies target diseases of protein misfolding. Trends Biochem. Sci. 29 (2004) 542-547
9. Lashuel H.A., and Lansbury P.T. Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins?. Quart. Rev. Biophys. 39 (2006) 167-201
10. Ross C.A., and Poirier M.A. Protein aggregation and neurodegenerative disease. Nature Med. 10 (2004) S10-S17
11. Zerovnik E., Pompe-Novak M., Skarabot M., Ravnikar M., Musevic I., and Turk V. Human stefin B readily forms amyloid fibrils in vitro. Biochim. Biophys. Acta 1594 (2002) 1-5
12. Lomakin A., Teplow D.B., Kirschner D.A., and Benedek G.B. Kinetic theory of fibrillogenesis of amyloid beta-protein. Proc. Natl Acad. Sci. USA 94 (1997) 7942-7947
13. Knaus K.J., Morillas M., Swietnicki W., Malone M., Surewicz W.K., and Yee V.C. Crystal structure of the human prion protein reveals a mechanism for oligomerisation. Nature Struct. Biol. 8 (2001) 770-774
14. Staniforth R.A., Giannini S., Higgins L.D., Conroy M.J., Hounslow A.M., Jerala R., et al. Three-dimensional domain swapping in the folded and molten-globule states of cystatins, an amyloid-forming structural superfamily. EMBO J. 20 (2001) 4774-4781
15. Janowski R., Kozak M., Jankowska E., Grzonka Z., Grubb A., Abrahamson M., and Jaskolski M. Human cystatin C, an amyloidogenic protein, dimerizes through three-dimensional domain swapping. Nature Struct. Biol. 8 (2001) 316-320
16. Guo Z., and Eisenberg D. Runaway domain swapping in amyloid-like fibrils of T7 endonuclease I. Proc. Natl Acad. Sci. USA 103 (2006) 8042-8047
17. Turk B., Turk D., and Salvesen G.S. Regulating cysteine protease activity: essential role of protease inhibitors as guardians and regulators. Curr. Pharm. Des. 8 (2002) 1623-1637
18. Ghiso J., Jenssen O., and Frangione B. Amyloid fibrils in hereditary cerebral hemorrhage with amyloidosis of Icelandic type is a variant of gamma-trace basic protein (cystatin C). Proc. Natl Acad. Sci. USA 83 (1986) 2974-2978
19. Sanders A., Craven J., Higgins L.D., Giannini S., Conroy M.J., and Hounslow A.M. Cystatin forms a tetramer through structural rearrangement of domain-swapped dimmers prior to amyloidogenesis. J. Mol. Biol. 336 (2004) 165-178
20. Ekiel I., and Abrahamson M. Folding-related dimerization of human cystatin C. J. Biol.Chem. 271 (1996) 1314-1321
21. Jenko S., Škarabot M., Kenig M., Gunèar G., Muševiè I., Turk D., and Žerovnik E. Different propensity to form amyloid fibrils by two homologous proteins-human stefins A and B: searching for an explanation. Proteins: Struct. Funct. Bioinformat. 55 (2004) 417-425
22. Kenig M., Berbić S., Kriješetorac A., Kroon-Žitko L., Tušek M., Pompe-Novak M., and Žerovnik E. Differences in aggregation properties of three site-specific mutants of recombinant human stefin B. Protein Sci. 13 (2004) 63-70
23. Stubbs M.T., Laber B., Bode W., Huber R., Jerala R., Lenarčič B., and Turk V. The refined 2,4 Å X-ray structure of recombinant human stefin B in complex with the cysteine proteinase papain: a novel type of proteinase inhibitor interaction. EMBO J. 9 (1990) 1939-1947
24. Bergdoll M., Remy M.H., Cagnon C., Masson J.M., and Dumas P. Proline-dependent oligomerization with arm exchange. Structure 5 (1997) 391-401
25. Syson K., Thirlway J., Hounslow A.M., Soultanas P., and Waltho J.P. Solution structure of the helicase-interaction domain of the primase DnaG: a model for helicase activation. Structure 13 (2005) 609-616
26. Jerala R., and Žerovnik E. Accessing the global minimum conformation of stefin A dimer by annealing under partially denaturing conditions. J. Mol. Biol. 291 (1999) 1079-1089
27. Janowski R., Grubb A., Abrahamson M., and Jaskolski M. Domain swapping in N-truncated human cystatin C. J. Mol. Biol. 341 (2004) 151-160
28. Janowski R., Kozak M., Abrahamson M., Grubb A., and Jaskolski M. 3D domain-swapped human cystatin C with amyloidlike intermolecular beta-sheets. Proteins: Struct. Funct. Genet. 61 (2005) 570-578
29. Zerovnik E., Jerala R., Kroon-Žitko L., Turk V., and Lohner K. Characterization of the equilibrium intermediates in acid denaturation of human stefin B. Eur. J. Biochem. 245 (1997) 364-372
30. Zerovnik E., Turk V., and Waltho J.P. Amyloid fibril formation by human stefin B: influence of the initial pH-induced intermediate state. Biochem. Soc. Trans. 4 (2002) 543-547
31. Balbach J., and Schmid X. In: Pain R.H. (Ed). Mechanisms of Protein Folding (2000), Oxford University Press, Oxford 212-249
32. Lummis S.C., Beene D.L., Lee L.W., Lester H.A., Broadhurst R.W., and Dougherty D.A. Cis-trans isomerization at a proline opens the pore of a neurotransmitter-gated ion channel. Nature 438 (2005) 248-252
33. Eakin C.M., Berman A.J., and Miranker A.D. A native to amyloidogenic transition regulated by a backbone trigger. Nature Struct. Mol. Biol. 3 (2006) 202-208
34. Ryo A., Togo T., Nakai T., Hirai A., Nishi M., Yamaguchi A., et al. Prolyl-isomerase Pin1 accumulates in lewy bodies of Parkinson disease and facilitates formation of alpha-synuclein inclusions. J. Biol. Chem. 281 (2006) 4117-4125
35. Pastorino L., Sun A., Lu P.J., Zhou X.Z., Balastik M., Finn G., et al. The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-beta production. Nature 440 (2006) 528-534
36. Pedersen J.S., Christensen G., and Otzen D.E. Modulation of S6 fibrillation by unfolding rates and gatekeeper residues. J. Mol. Biol. 341 (2004) 575-588
37. Minor W., and Otwinowski Z. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
38. Navaza J. AMoRe-An automated package for molecular replacement. Acta Crystallog. sect. D 50 (1994) 157-163
39. D. Turk, (1992). Weiterentwicklung eines Programms für Molekülgraphik und Elektrondichte-Manipulation und seine Anwendung auf verschiedene Protein-Strukturaufklärungen. Ph D thesis, Technische Universitaet, München.
40. Sheldrick G., and Schneider T. SHELXL: High-resolution refinement. Methods Enzymol. 277 (1997) 319-343
41. Merritt E.A., and Bacon D.J. Raster3D: photorealistic molecular graphics. Methods Enzymol. 277 (1997) 505-524