Human anti-prion antibodies block prion peptide fibril formation and neurotoxicity

Journal of Biological Chemistry

Volumn 287, Issue 16, 2012, Pages 12858-12866

  Wei, Xing ^a   Roettger, Yvonne ^b   Tan, Bailin ^a   He, Yongzheng ^a   Dodel, Richard ^b   Hampel, Harald ^c   Wei, Gang ^a   Haney, Jillian ^a   Gu, Huiying ^a   Johnstone, Brian H ^e   Liu, Junyi ^d   Farlow, Martin R ^a   Du, Yansheng ^a  

^a INDIANA UNIVERSITY   (United States)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c GOETHE UNIVERSITY   (Germany)

^d PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^e INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID ALANINES; AMINO ACID SEQUENCE; AUTOANTIBODIES; BINDING EPITOPES; BRAIN TISSUE; CELLULAR PRION PROTEINS; CEREBELLAR GRANULE NEURONS; CONFORMATIONAL TRANSFORMATIONS; EFFECTIVE THERAPY; ELISA ASSAY; FIBRIL FORMATION; IMMUNOAFFINITY CHROMATOGRAPHY; N-TERMINALS; NATURALLY OCCURRING; NEURODEGENERATIVE DISORDERS; NEUROTOXICITY; PATHOGENIC EFFECTS; PEPTIDE FIBRILS; PRION DISEASE; PRION PROTEIN; TRANSGENIC MICE; WILD TYPES;

AFFINITY CHROMATOGRAPHY; AMINO ACIDS; ANTIGENS; NEURODEGENERATIVE DISEASES; PLANTS (BOTANY); PURIFICATION;

PEPTIDES;

ALANINE; EPITOPE; IMMUNOGLOBULIN; IMMUNOGLOBULIN G; PRION PROTEIN; PRION PROTEIN ANTIBODY; VALINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; EPITOPE MAPPING; FIBRIL FORMATION; GRANULE CELL; HUMAN; IMMUNOAFFINITY CHROMATOGRAPHY; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RAT;

AMYLOID; ANIMALS; ANTIBODIES, BLOCKING; ANTIBODY SPECIFICITY; AUTOANTIBODIES; CRICETINAE; EPITOPE MAPPING; EPITOPES; HETEROZYGOTE; HUMANS; IMMUNOGLOBULINS, INTRAVENOUS; MICE; MICE, TRANSGENIC; NEUROGLIA; NEURONS; PRIMARY CELL CULTURE; PRION DISEASES; PRPC PROTEINS; PRPSC PROTEINS; RATS; RATS, SPRAGUE-DAWLEY;

CRICETINAE; MUS MUSCULUS; RATTUS;

EID: 84859741481     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.255836     Document Type: Article

References (51)

1. Prusiner, S. B. (1991) Molecular biology of prion diseases. Science 252, 1515-1522
2. Bugiani, O., Giaccone, G., Piccardo, P., Morbin, M., Tagliavini, F., and Ghetti, B. (2000) Neuropathology of Gerstmann-Sträussler-Scheinker disease. Microsc. Res. Tech. 50, 10-15
3. Ghetti, B., Piccardo, P., Frangione, B., Bugiani, O., Giaccone, G., Young, K., Prelli, F., Farlow, M. R., Dlouhy, S. R., and Tagliavini, F. (1996) Prion protein amyloidosis. Brain Pathol. 6, 127-145 (Pubitemid 26161871)
4. Giaccone, G., Verga, L., Bugiani, O., Frangione, B., Serban, D., Prusiner, S. B., Farlow, M. R., Ghetti, B., and Tagliavini, F. (1992) Prion protein preamyloid and amyloid deposits in Gerstmann-Sträussler-Scheinker disease, Indiana kindred. Proc. Natl. Acad. Sci. U.S.A. 89, 9349-9353
5. Kitamoto, T., Tateishi, J., Tashima, T., Takeshita, I., Barry, R. A., DeArmond, S. J., and Prusiner, S. B. (1986) Amyloid plaques in Creutzfeldt- Jakob disease stain with prion protein antibodies. Ann. Neurol. 20, 204-208 (Pubitemid 16050539)
6. Tateishi, J., Kitamoto, T., Hashiguchi, H., and Shii, H. (1988) Gerstmann- Sträussler-Scheinker disease: immunohistological and experimental studies. Ann. Neurol. 24, 35-40
7. Ghetti, B., Tagliavini, F., Masters, C. L., Beyreuther, K., Giaccone, G., Verga, L., Farlow, M. R., Conneally, P. M., Dlouhy, S. R., and Azzarelli, B. (1989) Gerstmann-Sträussler-Scheinker disease. II. Neurofibrillary tangles and plaques with PrP-amyloid coexist in an affected family. Neurology 39, 1453-1461
8. Peretz, D., Williamson, R. A., Kaneko, K., Vergara, J., Leclerc, E., Schmitt- Ulms, G., Mehlhorn, I. R., Legname, G., Wormald, M. R., Rudd, P. M., Dwek, R. A., Burton, D. R., and Prusiner, S. B. (2001) Antibodies inhibit prion propagation and clear cell cultures of prion infectivity. Nature 412, 739-743 (Pubitemid 32771997)
9. Enari, M., Flechsig, E., and Weissmann, C. (2001) Scrapie prion protein accumulation by scrapie-infected neuroblastoma cells abrogated by exposure to a prion protein antibody. Proc. Natl. Acad. Sci. U.S.A. 98, 9295-9299 (Pubitemid 32743910)
10. Heppner, F. L., Musahl, C., Arrighi, I., Klein, M. A., Rülicke, T., Oesch, B., Zinkernagel, R. M., Kalinke, U., and Aguzzi, A. (2001) Prevention of scrapie pathogenesis by transgenic expression of anti-prion protein antibodies. Science 294, 178-182 (Pubitemid 32952973)
11. White, A. R., Enever, P., Tayebi, M., Mushens, R., Linehan, J., Brandner, S., Anstee, D., Collinge, J., and Hawke, S. (2003) Monoclonal antibodies inhibit prion replication and delay the development of prion disease. Nature 422, 80-83 (Pubitemid 36323299)
12. Sigurdsson, E. M., Brown, D. R., Daniels, M., Kascsak, R. J., Kascsak, R., Carp, R., Meeker, H. C., Frangione, B., and Wisniewski, T. (2002) Immunization delays the onset of prion disease in mice. Am. J. Pathol. 161, 13-17 (Pubitemid 34760765)
13. Du, Y., Dodel, R., Hampel, H., Buerger, K., Lin, S., Eastwood, B., Bales, K., Gao, F., Moeller, H. J., Oertel, W., Farlow, M., and Paul, S. (2001) Reduced levels of amyloid beta-peptide antibody in Alzheimer disease. Neurology 57, 801-805 (Pubitemid 32845498)
14. Weksler, M. E., Relkin, N., Turkenich, R., LaRusse, S., Zhou, L., and Szabo, P. (2002) Patients with Alzheimer disease have lower levels of serum antiamyloid peptide antibodies than healthy elderly individuals. Exp. Gerontol. 37, 943-948 (Pubitemid 34665486)
15. Dodel, R., Hampel, H., Depboylu, C., Lin, S., Gao, F., Schock, S., Jäckel, S., Wei, X., Buerger, K., Höft, C., Hemmer, B., Möller, H. J., Farlow, M., Oertel, W. H., Sommer, N., and Du, Y. (2002) Human antibodies against amyloid beta peptide: a potential treatment for Alzheimer's disease. Ann. Neurol. 52, 253-256 (Pubitemid 34810613)
16. Dodel, R. C., Du, Y., Depboylu, C., Hampel, H., Frölich, L., Haag, A., Hemmeter, U., Paulsen, S., Teipel, S. J., Brettschneider, S., Spottke, A., Nölker, C., Möller, H. J., Wei, X., Farlow, M., Sommer, N., and Oertel, W. H. (2004) Intravenous immunoglobulins containing antibodies against beta-amyloid for the treatment of Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 75, 1472-1474 (Pubitemid 39279821)
17. Dodel, R., Neff, F., Noelker, C., Pul, R., Du, Y., Bacher, M., and Oertel, W. (2010) Drugs 70, 513-528
18. Du, Y., Wei, X., Dodel, R., Sommer, N., Hampel, H., Gao, F., Ma, Z., Zhao, L., Oertel, W. H., and Farlow, M. (2003) Human anti-beta-amyloid antibodies block beta-amyloid fibril formation and prevent beta-amyloid-induced neurotoxicity. Brain 126, 1935-1939 (Pubitemid 37059433)
19. Beekes, M. (2007) Prions and prion diseases. FEBS J. 274, 575
20. DeArmond, S. J., Yang, S. L., Lee, A., Bowler, R., Taraboulos, A., Groth, D., and Prusiner, S. B. (1993) Three scrapie prion isolates exhibit different accumulation patterns of the prion protein scrapie isoform. Proc. Natl. Acad. Sci. U.S.A. 90, 6449-6453 (Pubitemid 23207230)
21. Wisniewski, T. (2001) Henry M. Wisniewski M.D. Ph.D. J. Alzheimers Dis. 3, 7-22
22. Wisniewski, T., and Sigurdsson, E. M. (2007) Therapeutic approaches for prion and Alzheimer's diseases. FEBS. J. 274, 3784-3798 (Pubitemid 47087675)
23. Brundin, P., Melki, R., and Kopito, R. (2010) Nat. Rev. Mol. Cell Biol. 11, 301-307
24. Hanan, E., Goren, O., Eshkenazy, M., and Solomon, B. (2001) Immunomodulation of the human prion peptide 106-126 aggregation. Biochem. Biophys. Res. Commun. 280, 115-120 (Pubitemid 32917485)
25. Fioriti, L., Quaglio, E., Massignan, T., Colombo, L., Stewart, R. S., Salmona, M., Harris, D. A., Forloni, G., and Chiesa, R. (2005) The neurotoxicity of prion protein (PrP) peptide 106-126 is independent of the expression level of PrP and is not mediated by abnormal PrP species. Mol. Cell Neurosci. 28, 165-176 (Pubitemid 39656020)
26. Tagliavini, F., Forloni, G., D'Ursi, P., Bugiani, O., and Salmona, M. (2001) Studies on peptide fragments of prion proteins. Adv. Protein Chem. 57, 171-201 (Pubitemid 32622684)
27. Forloni, G., Angeretti, N., Chiesa, R., Monzani, E., Salmona, M., Bugiani, O., and Tagliavini, F. (1993) Neurotoxicity of a prion protein fragment. Nature 362, 543-546 (Pubitemid 23113029)
28. Forloni, G., Del Bo, R., Angeretti, N., Chiesa, R., Smiroldo, S., Doni, R., Ghibaudi, E., Salmona, M., Porro, M., and Verga, L. (1994) A neurotoxic prion protein fragment induces rat astroglial proliferation and hypertrophy. Eur. J. Neurosci. 6, 1415-1422 (Pubitemid 24280900)
29. Brown, D. R., Herms, J., and Kretzschmar, H. A. (1994) Mouse cortical cells lacking cellular PrP survive in culture with a neurotoxic PrP fragment. Neuroreport 5, 2057-2060 (Pubitemid 24340069)
30. Brown, D. R., Schmidt, B., and Kretzschmar, H. A. (1996) A neurotoxic prion protein fragment enhances proliferation of microglia but not astrocytes in culture. Glia 18, 59-67 (Pubitemid 26369601)
31. Brown, D. R., Schmidt, B., and Kretzschmar, H. A. (1996) Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature 380, 345-347 (Pubitemid 26097115)
32. Brown, D. R. (1998) Prion protein-overexpressing cells show altered response to a neurotoxic prion protein peptide. J. Neurosci. Res. 54, 331-340
33. Mastrianni, J. A., Curtis, M. T., Oberholtzer, J. C., Da Costa, M. M., DeArmond, S., Prusiner, S. B., and Garbern, J. Y. (1995) Prion disease (PrPA117V) presenting with ataxia instead of dementia. Neurology 45, 2042-2050
34. Tateishi, J. (1990) Slow virus, prion and nervous system Tanpakushitsu Kakusan Koso 35, 1327-1331
35. Hsiao, K. K., Cass, C., Schellenberg, G. D., Bird, T., Devine-Gage, E., Wisniewski, H., and Prusiner, S. B. (1991) A prion protein variant in a family with the telencephalic form of Gerstmann-Sträussler-Scheinker syndrome. Neurology 41, 681-684
36. Brown, D. R. (2000) Altered toxicity of the prion protein peptide PrP106-126 carrying the Ala(117)3Val mutation. Biochem. J. 346, 785-791
37. Molina, F., Laune, D., Gougat, C., Pau, B., and Granier, C. (1996) Improved performances of spot multiple peptide synthesis. Pept. Res. 9, 151-155 (Pubitemid 26369505)
38. Morel, N., Simon, S., Frobert, Y., Volland, H., Mourton-Gilles, C., Negro, A., Sorgato, M. C., Créminon, C., and Grassi, J. (2004) Selective and efficient immunoprecipitation of the disease-associated form of the prion protein can be mediated by nonspecific interactions between monoclonal antibodies and scrapie-associated fibrils. J. Biol. Chem. 279, 30143-30149 (Pubitemid 38937937)
39. Yokoyama, T., Kimura, K. M., Ushiki, Y., Yamada, S., Morooka, A., Nakashiba, T., Sassa, T., and Itohara, S. (2001) In vivo conversion of cellular prion protein to pathogenic isoforms, as monitored by conformationspecific antibodies. J. Biol. Chem. 276, 11265-11271 (Pubitemid 38089314)
40. Du, Y., Bales, K. R., Dodel, R. C., Liu, X., Glinn, M. A., Horn, J. W., Little, S. P., and Paul, S. M. (1998) a2-Macroglobulin attenuates A β(1-40) fibril formation and associated neutrotoxicity of cultured fetal rat cortical neurons. J. Neurochem. 70, 1182-1188 (Pubitemid 28113653)
41. Du, Y., Dodel, R., Bales, K., Hamilton-Byrd, E., and Paul, S. M. (1997) Involvement of a Caspase-3-like cysteine protease in 1-methyl-4-phenylpyridinium (MPP+) mediated apoptosis of cultured cerebellar granule neurons. J. Neurochem. 69, 1382-1388 (Pubitemid 27406938)
42. Resink, A., Hack, N., Boer, G. J., and Balázs, R. (1994) Growth conditions differentially modulate the vulnerability of developing cerebellar granule cells to excitatory amino acids. Brain Res. 655, 222-232 (Pubitemid 24263012)
43. Du, Y., Bales, K. R., Dodel, R. C., Hamilton-Byrd, E., Horn, J. W., Czilli, D. L., Simmons, L. K., Ni, B., and Paul, S. M. (1997) Activation of a caspase 3-related cysteine protease is required for glutamate-mediated apoptosis of cultured cerebellar granule neurons. Proc. Natl. Acad. Sci. U.S.A. 94, 11657-11662 (Pubitemid 27451054)
44. Ciani, E., and Paulsen, R. E. (1995) Activation of a reporter gene responsive to NGFI-B in cultured neurons and astrocytes. J. Mol. Neurosci. 6, 131-139
45. Sparapani, M., Dall'Olio, R., Gandolfi, O., Ciani, E., and Contestabile, A. (1997) Neurotoxicity of polyamines and pharmacological neuroprotection in cultures of rat cerebellar granule cells. Exp. Neurol. 148, 157-166 (Pubitemid 127445123)
46. Kiedrowski, L., Costa, E., and Wroblewski, J. T. (1992) In vitro interaction between cerebellar astrocytes and granule cells: a putative role for nitric oxide. Neurosci. Lett. 135, 59-61
47. Weissmann, C., and Flechsig, E. (2003) PrP knock-out and PrP transgenic mice in prion research. Br. Med. Bull. 66, 43-60 (Pubitemid 37173491)
48. Hegde, R. S., Mastrianni, J. A., Scott, M. R., DeFea, K. A., Tremblay, P., Torchia, M., DeArmond, S. J., Prusiner, S. B., and Lingappa, V. R. (1998) A transmembrane form of the prion protein in neurodegenerative disease. Science 279, 827-834 (Pubitemid 28106269)
49. Flego, M., Ascione, A., Zamboni, S., Dupuis, M. L., Imperiale, V., and Cianfriglia, M. (2007) Generation of human scFvs antibodies recognizing a prion protein epitope expressed on the surface of human lymphoblastoid cells. BMC Biotechnol. 7, 38
50. Weissmann, C., Raeber, A. J., Montrasio, F., Hegyi, I., Frigg, R., Klein, M. A., and Aguzzi, A. (2001) Prions and the lymphoreticular system. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 356, 177-184 (Pubitemid 32241466)
51. Relkin, N. R., Szabo, P., Adamiak, B., Burgut, T., Monthe, C., Lent, R. W., Younkin, S., Younkin, L., Schiff, R., and Weksler, M. E. (2009) 18-Month study of intravenous immunoglobulin for treatment of mild Alzheimer disease. Neurobiol. Aging 30, 1728-1736