The toxicity of antiprion antibodies is mediated by the flexible tail of the prion protein

Nature

Volumn 501, Issue 7465, 2013, Pages 102-106

  Sonati, Tiziana ^a   Reimann, Regina R ^a   Falsig, Jeppe ^a   Baral, Pravas Kumar ^b   O'Connor, Tracy ^a   Hornemann, Simone ^a   Yaganoglu, Sine ^a   Li, Bei ^a   Herrmann, Uli S ^a   Wieland, Barbara ^b   Swayampakula, Mridula ^b   Rahman, Muhammad Hafizur ^b   Das, Dipankar ^b   Kav, Nat ^b   Riek, Roland ^c   Liberski, Pawel P ^d   James, Michael N G ^b   Aguzzi, Adriano ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF ALBERTA   (Canada)

^c ETH ZURICH   (Switzerland)

^d MEDICAL UNIVERSITY OF LODZ   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CALPASTATIN; MONOCLONAL ANTIBODY; OCTAPEPTIDE; PRION PROTEIN; PRION PROTEIN ANTIBODY; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2;

ANTIBODY; CREUTZFELDT JAKOB DISEASE; ENZYME; LIGAND; OXYGEN; PROTEIN; TOXICITY;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; BRAIN SLICE; FAMILIAL CREUTZFELDT JAKOB DISEASE; GENE OVEREXPRESSION; MOUSE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRION DISEASE; PRIORITY JOURNAL; TISSUE CULTURE;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; ANTIBODIES, MONOCLONAL; BINDING SITES, ANTIBODY; CALPAIN; CEREBELLUM; CREUTZFELDT-JAKOB SYNDROME; CROSS-LINKING REAGENTS; EPITOPE MAPPING; FEMALE; IMMUNOGLOBULIN FAB FRAGMENTS; LIGANDS; MALE; MEMBRANE GLYCOPROTEINS; MICE; MOLECULAR SEQUENCE DATA; NADPH OXIDASE; NEURODEGENERATIVE DISEASES; OXIDATIVE STRESS; PLIABILITY; PRIONS; PRPC PROTEINS; REACTIVE OXYGEN SPECIES; SEQUENCE DELETION; SINGLE-CHAIN ANTIBODIES;

MUS;

EID: 84883742582     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12402     Document Type: Article

References (55)

1. Brandner, S. et al. Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 379, 339-343 (1996).
2. Riek, R. et al. NMR structure of the mouse prion protein domain PrP (121-231). Nature 382, 180-182 (1996).
3. Polymenidou, M. et al. The POM monoclonals: a comprehensive set of antibodies to non-overlapping prion protein epitopes. PLoS ONE 3, e3872 (2008).
4. Falsig, J. et al. Prion pathogenesisisfaithfully reproducedin cerebellar organotypic slice cultures. PLoS Pathog. 8, e1002985 (2012).
5. Fischer, M. et al. Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 15, 1255-1264 (1996).
6. Mallucci, G. et al. Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302, 871-874 (2003).
7. Baumann, F. et al. Lethal recessive myelin toxicity of prion protein lacking its central domain. EMBO J. 26, 538-547 (2007).
8. Aguzzi, A. & Calella, A. M. Prions: protein aggregation and infectious diseases. Physiol. Rev. 89, 1105-1152 (2009).
9. Falsig, J. & Aguzzi, A. The prion organotypic slice culture assay-POSCA. Nature Protocols 3, 555-562 (2008).
10. Riek, R., Hornemann, S., Wider, G., Glockshuber, R. & Wüthrich, K. NMR characterization of the full-length recombinant murine prion protein, mPrP (23-231). FEBS Lett. 413, 282-288 (1997).
11. Solforosi, L. et al. Cross-linking cellular prion protein triggers neuronal apoptosis in vivo. Science 303, 1514-1516 (2004).
12. Büeler, H. et al. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356, 577-582 (1992).
13. Zahn, R. et al. NMR solution structure of the human prion protein. Proc. Natl Acad. Sci. USA 97, 145-150 (2000).
14. Wüthrich, K. & Riek, R. Three-dimensional structures ofprion proteins. Adv. Protein Chem. 57, 55-82 (2001).
15. Flechsig, E. et al. Prion protein devoid of the octapeptide repeat region restores susceptibility to scrapie in PrP knockout mice. Neuron 27, 399-408 (2000).
16. Bremer, J. et al. Axonal prion protein is required for peripheral myelin maintenance. Nature Neurosci. 13, 310-318 (2010)
17. Wang, K. K. Calpain and caspase: can you tell the difference? Trends Neurosci. 23, 20-26 (2000).
18. Fatokun, A. A., Stone, T. W. & Smith, R. A. Oxidative stressinneurodegeneration and available means of protection. Front. Biosci. 13, 3288-3311 (2008).
19. Sorce, S. & Krause, K. H. NOX enzymes in the central nervous system: from signaling to disease. Antioxid. Redox Signal. 11, 2481-2504 (2009).
20. Silva, A. C., Lee, J. H., Aoki, I. & Koretsky, A. P. Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed. 17, 532-543 (2004).
21. Granados-Principal, S., Quiles, J. L., Ramirez-Tortosa, C. L., Sanchez-Rovira, P. & Ramirez-Tortosa, M. C. Hydroxytyrosol: from laboratory investigations to future clinical trials. Nutr. Rev. 68, 191-206 (2010).
22. Pollock, J. D. et al. Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nature Genet. 9, 202-209 (1995).
23. Yamaguchi, Y. et al. Biological and biochemical characterization of mice expressing prion protein devoid of the octapeptide repeat region after infection with prions. PLoS ONE 7, e43540 (2012).
24. Chiesa, R., Piccardo, P., Ghetti, B. & Harris, D. A. Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron 21, 1339-1351 (1998).
25. Krasemann, S. et al. Prion disease associated with a novel nine octapeptide repeat insertion in the PRNP gene. Brain Res. Mol. Brain Res. 34, 173-176 (1995).
26. Mead, S. et al. Inherited prion disease with six octapeptide repeat insertional mutation-molecular analysisofphenotypic heterogeneity. Brain 129, 2297-2317 (2006).
27. Vital, C., Gray, F., Vital, A., Ferrer, X. & Julien, J. Prion disease with octapeptide repeat insertion. Clin. Exp. Pathol. 47, 153-159 (1999).
28. Sc in vivo and antagonizes prion disease. Cell 113, 49-60 (2003).
29. Zahn, R., von Schroetter, C. & Wüthrich, K. Human prion proteins expressed in Escherichia coli and purified by high-affinity column refolding. FEBS Lett. 417, 400-404 (1997).
30. Lysek, D. A. & Wuthrich, K. Prion protein interaction with the C-terminal SH3 domain of Grb2 studied using NMR and optical spectroscopy. Biochemistry 43, 10393-10399 (2004).
31. Aller, M. I. et al. Cerebellar granule cell Cre recombinase expression. Genesis 36, 97-103 (2003).
32. Mallucci, G. R. et al. Post-natal knockout of prion protein alters hippocampal CA1 properties, but does not result in neurodegeneration. EMBO J. 21, 202-210 (2002).
33. C. J. Neurosci. 25, 4879-4888 (2005).
34. Prinz, M. et al. Intrinsic resistance of oligodendrocytes to prion infection. J. Neurosci. 24, 5974-5981 (2004).
35. Heppner, F. L. et al. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nature Med. 11, 146-152 (2005).
36. Levites, Y. et al. Intracranial adeno-associated virus-mediated delivery of anti-pan amyloid b, amyloid b40, and amyloid b42 single-chain variable fragments attenuates plaque pathology in amyloid precursor protein mice. J. Neurosci. 26, 11923-11928 (2006).
37. Grünecker, B. et al. Fractionated manganese injections: effects on MRI contrast enhancement and physiological measures in C57BL/6 mice. NMR Biomed. 23, 913-921 (2010).
38. Faas, H. et al. Context-dependent perturbation of neural systems in transgenic mice expressing a cytosolic prion protein. Neuroimage 49, 2607-2617 (2010).
39. Falsig, J. et al. A versatile prion replication assay in organotypic brain slices. Nature Neurosci. 11, 109-117 (2008).
40. 6-Cys scFv. Protein Expr. Purif. 39, 199-208 (2005).
41. Baudino, L. et al. IgM and IgA anti-erythrocyte autoantibodies induce anemia in a mouse model through multivalency-dependent hemagglutination but not through complement activation. Blood 109, 5355-5362 (2007).
42. Hornemann, S., Christen, B., von Schroetter, C., Perez, D. R. & Wuthrich, K. Prion protein library of recombinant constructs for structural biology. FEBS J. 276, 2359-2367 (2009).
43. Pervushin, K., Riek, R., Wider, G. & Wuthrich, K. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl Acad. Sci. USA 94, 12366-12371 (1997).
44. Keller, R. L. J. The Computer-aided Resonance Assignment Tutorial CARA (Cantina Verlag 2004) (2004).
45. Riek, R. NMR of the mouse prion protein, PhD thesis, ETH Zürich (1998).
46. Baral, P. K. et al. Crystallization and preliminary X-ray diffraction analysis of prion protein bound to the Fab fragment of the POM1 antibody. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67, 1211-1213 (2011).
47. Cohen, A. E., Ellis, P. J., Miller, M. D., Deacon, A. M. & Phizackerley, R. P. An automated system to mount cryo-cooled protein crystals on a synchrotron beamline, using compact sample cassettes and a small-scale robot. J. Appl. Crystallogr. 35, 720-726 (2002).
48. González, A. et al. Web-Ice: integrated data collection and analysis for macromolecular crystallography. J. Appl. Crystallogr. 41, 176-184 (2008).
49. McPhillips, T. M. et al. Blu-Ice and the Distributed Control System: software for data acquisitionandinstrumentcontrolatmacromolecularcrystallography beamlines. J. Synchrotron Radiat. 9, 401-406 (2002).
50. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
51. Vagin, A. & Teplyakov, A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025 (1997).
52. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235-242 (2011).
53. Echols, N. et al. Graphical tools for macromolecular crystallography in PHENIX. J. Appl. Crystallogr. 45, 581-586 (2012).
54. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
55. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12-21 (2010).