Proteomic profiling of PrP27-30-enriched preparations extracted from the brain of hamsters with experimental scrapie

Proteomics

Volumn 9, Issue 15, 2009, Pages 3802-3814

  Giorgi, Alessandra ^a   Di Francesco, Laura ^a   Principe, Serena ^b   Mignogna, Giuseppina ^a   Sennels, Lau ^c   Mancone, Carmine ^d   Alonzi, Tonino ^d   Sbriccoli, Marco ^b   De Pascalis, Angela ^b   Rappsilber, Juri ^c   Cardone, Franco ^b   Pocchiari, Maurizio ^b   Maras, Bruno ^a   Schinina, M Eugenia ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

Author keywords

FT ICR; MALDI TOF TOF; Prion protein; PrP27 30; Transmissible spongiform encephalopathies

Indexed keywords

ACTIN; APOLIPOPROTEIN E; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; COFILIN; FERRITIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEAT SHOCK PROTEIN 90; HISTONE; PRION PROTEIN; PROTEIN PRP27; PROTEIN PRP30; TUBULIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; PROTEIN PURIFICATION; PROTEOMICS; SCRAPIE;

ANIMALS; APOLIPOPROTEINS E; BLOTTING, WESTERN; BRAIN; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CRICETINAE; PROTEINS; PROTEOMICS; PRP 27-30 PROTEIN; SCRAPIE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

CRICETINAE;

EID: 68549096430     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200900085     Document Type: Article

References (65)

1. Prusiner, S. B., Prions. Proc. Natl. Acad. Sci. USA 1998, 95, 13363-13383.
2. Stahl, N., Baldwin, M. A., Teplow, D. B., Hood, L. et al., Structural studies of the scrapie prion protein using mass spectrometry and amino acid sequencing. Biochemistry 1993, 32, 1991-2002.
3. Caughey, B. W., Dong, A., Bhat, K. S., Ernst, D. et al., Secondary structure analysis of the scrapie-associated protein PrP27-30 in water by infrared spectroscopy. Biochemistry 1991, 30, 7672-7680.
4. Safar, J., Roller, P. P., Gajdusek, D. C., Gibbs, C. J., jr., Conformational transitions, dissociation, and unfolding of scrapie amyloid (prion) protein. J. Biol. Chem. 1993, 268, 20276-20284.
5. Pan, K. M., Baldwin, M., Nguyen, J., Gasset, M. et al., Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. USA 1993, 90, 10962-10966.
6. Turk, E., Teplow, D. B., Hood, L. E., Prusiner, S. B., Purification and properties of the cellular and scrapie hamster prion proteins. Eur. J. Biochem. 1988, 176, 21-30.
7. Schmitt-Ulms, G., Legname, G., Baldwin, M. A., Ball, H. L. et al., Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein. J. Mol. Biol. 2001, 314, 1209-1225.
8. Satoh, J., Onoue, H., Arima, K., Yamamura, T., The 14-3-3 protein forms a molecular complex with heat shock protein Hsp60 and cellular prion protein. J. Neuropathol. Exp. Neurol. 2005, 64, 858-868.
9. Petrakis, S., Sklaviadis, T., Identification of proteins with high affinity for refolded and native PrPC. Proteomics 2006, 6, 6476-6484.
10. Zomosa-Signoret, V., Arnaud, J. D., Fontes, P., Alvarez-Martinez, M. T., Liautard, J. P., Physiological role of the cellular prion protein. Vet. Res. 2008, 39, 9.
11. Kellings, K., Meyer, N.,Mirenda, C., Prusiner, S. B., Riesner, D., Further analysis of nucleic acids in purified scrapie prion preparations by improved return refocusing gel electrophoresis. J. Gen. Virol. 1992, 73, 1025-1029.
12. Diringer, H., Beekes, M., Ozel, M., Simon, D. et al., Highly infectious purified preparations of disease-specific amyloid of transmissible spongiform encephalopathies are not devoid of nucleic acids of viral size. Intervirology 1997, 40, 238-246.
13. Kellings, K., Meyer, N., Mirenda, C., Prusiner, S. B., Riesner, D., Analysis of nucleic acids in purified scrapie prion preparations. Arch. Virol. Suppl. 1993, 7, 215-225.
14. Berardi, V. A., Cardone, F., Valanzano, A., Lu, M., Pocchiari, M., Preparation of soluble infectious samples from scrapie-infected brain: a new tool to study the clearance of transmissible spongiform encephalopathy agents during plasma fractionation. Transfusion 2006, 46, 652-658.
15. Pocchiari, M., Schmittinger, S., Masullo, C., Amphotericin B delays the incubation period of scrapie in intracerebrally inoculated hamsters. J. Gen. Virol. 1987, 68, 219-223.
16. Silvestrini, M. C., Cardone, F., Maras, B., Pucci, P. et al., Identification of the prion protein allotypes which accumulate in the brain of sporadic and familial Creutzfeldt-Jakob disease patients. Nat. Med. 1997, 3, 521-525.
17. Pappin, D. J., Peptide mass fingerprinting using MALDI-TOF mass spectrometry. Methods Mol. Biol. 2003, 211, 211-219.
18. Rappsilber, J., Ishihama, Y., Mann, M., Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 2003, 75, 663-670.
19. Ishihama, Y., Rappsilber, J., Andersen, J. S., Mann, M., Microcolumns with self-assembled particle frits for proteomics. J. Chromatogr. A 2002, 979, 233-239.
20. Zanusso, G., Righetti, P. G., Ferrari, S., Terrin, L. et al., Two-dimensional mapping of three phenotype-associated isoforms of the prion protein in sporadic Creutzfeldt-Jakob disease. Electrophoresis 2002, 23, 347-355.
21. Castagna, A., Campostrini, N., Farinazzo, A., Zanusso, G. et al., Comparative two-dimensional mapping of prion protein isoforms in human cerebrospinal fluid and central nervous system. Electrophoresis 2002, 23, 339-346.
22. Swanson, S. K., Washburn, M. P., The continuing evolution of shotgun proteomics. Drug Discov. Today 2005, 10, 719-725.
23. Bogdanov, B., Smith, R. D., Proteomics by FTICR mass spectrometry: top down and bottom up. Mass Spectrom. Rev. 2005, 24, 168-200.
24. Boyles, J. K., Pitas, R.E., Wilson, E., Mahley, R.W. et al., Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J. Clin. Invest. 1985, 76, 1501-1513.
25. Hudmon, A., Schulman, H., Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem. J. 2002, 364, 593-611.
26. Mahley, R. W., Weisgraber, K. H., Huang, Y., Apolipoprotein E4: a causative factor and therapeutic target in neuropathology, including Alzheimer's disease. Proc. Natl. Acad. Sci. USA 2006, 103, 5644-5651.
27. Van Everbroeck, B., Croes, E. A., Pals, P., Dermaut, B. et al., Influence of the prion protein and the apolipoprotein E genotype on the Creutzfeldt-Jakob Disease phenotype. Neurosci. Lett. 2001, 313, 69-72.
28. Ampuero, I., Ros, R., Royuela, A., Abraira, V. et al., Risk factors for dementia of Alzheimer type and aging-associated cognitive decline in a Spanish population based sample, and in brains with pathology confirmed Alzheimer's disease. J. Alzheimers Dis. 2008, 14, 179-191.
29. Brouwers, N., Sleegers, K., Van Broeckhoven, C., Molecular genetics of Alzheimer's disease: an update. Ann. Med. 2008, 40, 562-583.
30. Baumann, M. H., Kallijarvi, J., Lankinen, H., Soto, C., Haltia, M., Apolipoprotein E includes a binding site which is recognized by several amyloidogenic polypeptides. Biochem. J. 2000, 349, 77-84.
31. Armstrong, R. A., Lantos, P. L., Cairns, N. J., What determines the molecular composition of abnormal protein aggregates in neurodegenerative disease? Neuropathology 2008, 28, 351-365.
32. Namba, Y., Tomonaga,M., Kawasaki, H., Otomo, E., Ikeda, K., Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer's disease and kuru plaque amyloid in Creutzfeldt-Jakob disease. Brain Res. 1991, 541, 163-166.
33. Nakamura, S., Ono, F., Hamano, M., Odagiri, K. et al., Immunohistochemical detection of apolipoprotein E within prion-associated lesions in squirrel monkey brains. Acta Neuropathol. (Berl). 2000, 100, 365-370.
34. Gao, C., Lei, Y. J., Han, J., Shi, Q. et al., Recombinant neural protein PrP can bind with both recombinant and native apolipoprotein E in vitro. Acta Biochim. Biophys. Sin. (Shanghai) 2006, 38, 593-601.
35. Diedrich, J. F., Minnigan, H., Carp, R. I., Whitaker, J. N. et al., Neuropathological changes in scrapie and Alzheimer's disease are associated with increased expression of apolipoprotein E and cathepsin D in astrocytes. J. Virol. 1991, 65, 4759-4768.
36. Castano, E. M., Prelli, F., Wisniewski, T., Golabek, A. et al., Fibrillogenesis in Alzheimer's disease of amyloid beta peptides and apolipoprotein E. Biochem. J. 1995, 306, 599-604.
37. Charge, S. B., Esiri, M. M., Bethune, C. A., Hansen, B. C., Clark, A., Apolipoprotein E is associated with islet amyloid and other amyloidoses: implications for Alzheimer's disease. J. Pathol. 1996, 179, 443-447.
38. Soto, C., Castano, E. M., Prelli, F., Kumar, R. A., Baumann, M., Apolipoprotein E increases the fibrillogenic potential of synthetic peptides derived from Alzheimer's, Gelsolin and AA amyloids. FEBS Lett. 1995, 371, 110-114.
39. Jin, J. K., Choi, J. K., Lee, H. G., Kim, Y. S. et al., Increased expression of CaM kinase II alpha in the brains of scrapie-infected mice. Neurosci. Lett. 1999, 273, 37-40.
40. Cosseddu, G. M., Andreoletti, O., Maestrale, C., Robert, B. et al., Gene expression profiling on sheep brain reveals differential transcripts in scrapie-affected/not-affected animals. Brain Res. 2007, 1142, 217-222.
41. Mishra, R. S., Basu, S., Gu, Y., Luo, X. et al., Protease-resistant human prion protein and ferritin are cotransported across caco-2 epithelial cells: implications for species barrier in prion uptake from the intestine. J. Neurosci. 2004, 24, 11280-11290.
42. Cho, H. J., Greig, A. S., Isolation of 14-nm virus-like particles from mouse brain infected with scrapie agent. Nature 1975, 257, 685-686.
43. Cho, H. J., Greig, A. S., Corp, C. R., Kimberlin, R. H. et al., Virus-like particles from both control and scrapie-affected mouse brain. Nature 1977, 267, 459-460.
44. Dale, C. J., Walker, S. G., Lyddiatt, A. Scale-up and intensification of the abnormal PrP present in bovine brain infected with spongiform encephalopathy. in: Pyle, D. L., (Ed.), Separations for Biotechnology, vol. 3, SCI, 1994, pp. 141-146.
45. Walker, S. G., Dale, C., Lyddiatt, A., Aqueous two-phase partition of complex protein feedstocks derived from brain tissue homogenates. J. Chromatogr. B, 1996, 680, 91-96.
46. Ozel, M., Xi, Y. G., Baldauf, E., Diringer, H., Pocchiari, M., Small virus-like structure in brains from cases of sporadic and familial Creutzfeldt-Jakob disease. Lancet 1994, 344, 923-924.
47. Ozel, M., Diringer, H., Small virus-like structure in fractions from scrapie hamster brain. Lancet 1994, 343, 894-895.
48. Kim, B. H., Jun, Y. C., Jin, J. K., Kim, J. I. et al., Alteration of iron regulatory proteins (IRP1 and IRP2) and ferritin in the brains of scrapie-infected mice. Neurosci. Lett. 2007, 422, 158-163.
49. Basu, S., Mohan, M. L., Luo, X., Kundu, B. et al., Modulation of proteinase K-resistant prion protein in cells and infectious brain homogenate by redox iron: implications for prion replication and disease pathogenesis. Mol. Biol. Cell 2007, 18, 3302-3312.
50. Saunders, G. C., Horigan, V., Tout, A. C., Windl, O., Identification of a proteinase K-resistant protein for use as an internal positive control marker in PrP Western blotting. Res. Vet. Sci. 2007, 83, 157-164.
51. Atkinson, B. G ., Dean, R. L ., Tomlinson, J ., Blaker, T. W ., Rapid purification of ferritin from lysates of red blood cells using proteinase-K. Biochem. Cell Bio. 1989, 67, 52-57.
52. Keshet, G. I., Bar-Peled, O., Yaffe, D., Nudel, U., Gabizon, R., The cellular prion protein colocalizes with the dystroglycan complex in the brain. J. Neurochem. 2000, 75, 1889-1897.
53. Hachiya, N. S., Watanabe, K., Sakasegawa, Y., Kaneko, K., Anterograde and retrograde intracellular trafficking of fluorescent cellular prion protein. Biochem. Biophys. Res. Commun. 2004, 313, 818-823.
54. Dong, C. F., Shi, S., Wang, X. F., An, R. et al., The N-terminus of PrP is responsible for interacting with tubulin and fCJD related PrP mutants possess stronger inhibitive effect on microtubule assembly in vitro. Arch. Biochem. Biophys. 2008, 470, 83-92.
55. Mange, A., Crozet, C., Lehmann, S., Beranger, F., Scrapie-like prion protein is translocated to the nuclei of infected cells independently of proteasome inhibition and interacts with chromatin. J. Cell Sci. 2004, 117, 2411-2416.
56. Borchelt, D. R., Koliatsos, V. E., Guarnieri, M., Pardo, C. A. et al., Rapid anterograde axonal transport of the cellular prion glycoprotein in the peripheral and central nervous systems. J. Biol. Chem. 1994, 269, 14711-14714.
57. Moya, K. L., Hassig, R., Creminon, C., Laffont, I., Di Giamberardino, L., Enhanced detection and retrograde axonal transport of PrPc in peripheral nerve. J. Neurochem. 2004, 88, 155-160.
58. Nieznanski, K., Nieznanska, H., Skowronek, K. J., Osiecka, K. M., Stepkowski, D., Direct interaction between prion protein and tubulin. Biochem. Biophys. Res. Commun. 2005, 334, 403-411.
59. Nieznanski, K., Podlubnaya, Z. A., Nieznanska, H., Prion protein inhibits microtubule assembly by inducing tubulin oligomerization. Biochem. Biophys. Res. Commun. 2006, 349, 391-399.
60. Minamide, L. S., Striegl, A. M., Boyle, J. A., Meberg, P. J., Bamburg, J. R., Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function. Nat. Cell. Biol. 2000, 2, 628-636.
61. Schoenenberger, C. A., Bischler, N., Fahrenkrog, B., Aebi, U., Actin's propensity for dynamic filament patterning. FEBS Lett. 2002, 529, 27-33.
62. Andrianantoandro, E., Pollard, T. D., Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol. Cell. 2006, 24, 13-23.
63. Kovacs, G. G., Kurucz, I., Budka, H., Adori, C. et al., Prominent stress response of Purkinje cells in Creutzfeldt-Jakob disease. Neurobiol. Dis. 2001, 8, 881-889.
64. Castilla, J., Saa, P., Hetz, C., Soto, C., In vitro generation of infectious scrapie prions. Cell 2005, 121, 195-206.
65. Deleault, N. R., Harris, B. T., Rees, J. R., Supattapone, S., Formation of native prions from minimal components in vitro. Proc. Natl. Acad. Sci. USA 2007, 104, 9741-9746.