High hydrophobic amino acid exposure is responsible of the neurotoxic effects induced by E200K or D202N disease-related mutations of the human prion protein

International Journal of Biochemistry and Cell Biology

Volumn 43, Issue 3, 2011, Pages 372-382

  Corsaro, Alessandro ^a   Thellung, Stefano ^a   Bucciarelli, Tonino ^b   Scotti, Luca ^b   Chiovitti, Katia ^b   Villa, Valentina ^a   D'Arrigo, Cristina ^c   Aceto, Antonio ^b   Florio, Tullio ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF CHIETI   (Italy)

^c CNR   (Italy)

Author keywords

E200K and D202N mutations; Familial TSE; hPrP90 231 wt; Neurotoxicity; Prion protein

Indexed keywords

AMINO ACID; MUTANT PROTEIN; PRION PROTEIN;

ALPHA HELIX; ARTICLE; BETA SHEET; CONTROLLED STUDY; FAMILIAL DISEASE; HUMAN; HUMAN CELL; HYDROPHOBICITY; NEUROTOXICITY; PRION DISEASE; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DENATURATION;

AMINO ACID SUBSTITUTION; AMINO ACIDS; CELL DEATH; CELL LINE, TUMOR; CONGO RED; ENDOCYTOSIS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; IMMUNOBLOTTING; MUTANT PROTEINS; MUTATION; NEUROTOXINS; PEPTIDES; PRION DISEASES; PRIONS; PROTEIN STRUCTURE, QUATERNARY;

EID: 79751525877     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2010.11.007     Document Type: Article

References (56)

1. K. Abid, and C. Soto The intriguing prion disorders Cell Mol Life Sci 63 2006 2342 2351 (Pubitemid 44653044)
2. A. Aceto, P. Sacchetta, T. Bucciarelli, B. Dragani, S. Angelucci, and G.L. Radatti Structural and functional properties of the 34-kDa fragment produced by the N-terminal chymotryptic cleavage of glutathione transferase P1-1 Arch Biochem Biophys 316 1995 873 878
3. A. Aguzzi Prion diseases of humans and farm animals: epidemiology, genetics, and pathogenesis J Neurochem 97 2006 1726 1739 (Pubitemid 43873663)
4. A. Aguzzi, and M. Polymenidou Mammalian prion biology: one century of evolving concepts Cell 116 2004 313 327 (Pubitemid 38167320)
5. I.V. Baskakov, G. Legname, M.A. Baldwin, S.B. Prusiner, and F.E. Cohen Pathway complexity of prion protein assembly into amyloid J Biol Chem 277 2002 21140 21148 (Pubitemid 34952249)
6. P. Brown, C.J. Gibbs Jr., P. Rodgers-Johnson, D.M. Asher, M.P. Sulima, and A. Bacote Human spongiform encephalopathy: the National Institutes of Health series of 300 cases of experimentally transmitted disease Ann Neurol 35 1994 513 529 (Pubitemid 24153834)
7. M. Bucciantini, G. Calloni, F. Chiti, L. Formigli, D. Nosi, and C.M. Dobson Prefibrillar amyloid protein aggregates share common features of cytotoxicity J Biol Chem 279 2004 31374 31382 (Pubitemid 39037804)
8. S. Capellari, P. Parchi, C.M. Russo, J. Sanford, M.S. Sy, and P. Gambetti Effect of the E200K mutation on prion protein metabolism. Comparative study of a cell model and human brain Am J Pathol 157 2000 613 622 (Pubitemid 30626920)
9. J. Chapman, P. Brown, J.M. Rabey, L.G. Goldfarb, R. Inzelberg, and C.J. Gibbs Jr. Transmission of spongiform encephalopathy from a familial Creutzfeldt-Jakob disease patient of Jewish Libyan origin carrying the PRNP codon 200 mutation Neurology 42 1992 1249 1250
10. K. Chiovitti, A. Corsaro, S. Thellung, V. Villa, D. Paludi, and C. D'Arrigo Intracellular accumulation of a mild-denatured monomer of the human PrP fragment 90-231, as possible mechanism of its neurotoxic effects J Neurochem 103 2007 2597 2609
11. F.E. Cohen, and S.B. Prusiner Pathologic conformations of prion proteins Annu Rev Biochem 67 1998 793 819 (Pubitemid 28411145)
12. J. Collinge Human prion diseases and bovine spongiform encephalopathy (BSE) Hum Mol Genet 6 1997 1699 1705 (Pubitemid 27401613)
13. J. Collinge Prion diseases of humans and animals: their causes and molecular basis Annu Rev Neurosci 24 2001 519 550 (Pubitemid 32695238)
14. L. Colucci-D'Amato, C. Perrone-Capano, and U. di Porzio Chronic activation of ERK and neurodegenerative diseases Bioessays 25 2003 1085 1095 (Pubitemid 37411768)
15. A. Corsaro, C. Anselmi, M. Polano, A. Aceto, T. Florio, and M. De Nobili The interaction of humic substances with the human prion protein fragment 90-231 affects its protease K resistance and cell internalization J Biol Regul Homeost Agents 24 2010 27 39
16. A. Corsaro, D. Paludi, V. Villa, C. D'Arrigo, K. Chiovitti, and S. Thellung Conformation dependent pro-apoptotic activity of the recombinant human prion protein fragment 90-231 Int J Immunopathol Pharmacol 19 2006 339 356 (Pubitemid 44181957)
17. A. Corsaro, S. Thellung, K. Chiovitti, V. Villa, A. Simi, and F. Raggi Dual modulation of ERK1/2 and p38 MAP kinase activities induced by minocycline reverses the neurotoxic effects of the prion protein fragment 90-231 Neurotox Res 15 2009 138 154
18. A. Corsaro, S. Thellung, C. Russo, V. Villa, S. Arena, and M.C. D'Adamo Expression in E. coli and purification of recombinant fragments of wild type and mutant human prion protein Neurochem Int 41 2002 55 63 (Pubitemid 34251406)
19. A. Corsaro, S. Thellung, V. Villa, D.R. Principe, D. Paludi, and S. Arena Prion protein fragment 106-126 induces a p38 MAP kinase-dependent apoptosis in SH-SY5Y neuroblastoma cells independently from the amyloid fibril formation Ann N Y Acad Sci 1010 2003 610 622 (Pubitemid 38265055)
20. V.V. Daggett Structure-function aspects of prion proteins Curr Opin Biotechnol 9 1998 549
21. K.A. Dill The meaning of hydrophobicity Science 250 1990 297 298
22. T. Florio, D. Paludi, V. Villa, D.R. Principe, A. Corsaro, and E. Millo Contribution of two conserved glycine residues to fibrillogenesis of the 106-126 prion protein fragment. Evidence that a soluble variant of the 106-126 peptide is neurotoxic J Neurochem 85 2003 62 72 (Pubitemid 36389695)
23. T. Florio, S. Thellung, C. Amico, M. Robello, M. Salmona, and O. Bugiani Prion protein fragment 106-126 induces apoptotic cell death and impairment of L-type voltage-sensitive calcium channel activity in the GH3 cell line J Neurosci Res 54 1998 341 352 (Pubitemid 28493944)
24. M. Gallo, D. Paludi, D.O. Cicero, K. Chiovitti, E. Millo, and A. Salis Identification of a conserved N-capping box important for the structural autonomy of the prion alpha 3-helix: the disease associated D202N mutation destabilizes the helical conformation Int J Immunopathol Pharmacol 18 2005 95 112 (Pubitemid 40343463)
25. K. Hasegawa, S. Mohri, and T. Yokoyama Fragment molecular orbital calculations reveal that the E200K mutation markedly alters local structural stability in the human prion protein Prion 4 2010 38 44
26. G.S. Jackson, A.F. Hill, C. Joseph, L. Hosszu, A. Power, and J.P. Waltho Multiple folding pathways for heterologously expressed human prion protein Biochim Biophys Acta 1431 1999 1 13 (Pubitemid 29182716)
27. M.F. Jobling, L.R. Stewart, A.R. White, C. McLean, A. Friedhuber, and F. Maher The hydrophobic core sequence modulates the neurotoxic and secondary structure properties of the prion peptide 106-126 J Neurochem 73 1999 1557 1565 (Pubitemid 29440157)
28. C. Korth, B.C. May, F.E. Cohen, and S.B. Prusiner Acridine and phenothiazine derivatives as pharmacotherapeutics for prion disease Proc Natl Acad Sci USA 98 2001 9836 9841 (Pubitemid 32769390)
29. A.Y. Lee, S. Zhang, P. Kongsaeree, J. Clardy, B. Ganem, and J.W. Erickson Thermodynamics of a transition state analogue inhibitor binding to Escherichia coli chorismate mutase: probing the charge state of an active site residue and its role in inhibitor binding and catalysis Biochemistry 37 1998 9052 9057 (Pubitemid 28299677)
30. H. LeVine 3rd Thioflavine T interaction with synthetic Alzheimer's disease beta-amyloid peptides: detection of amyloid aggregation in solution Protein Sci 2 1993 404 410
31. P.P. Liberski, and H. Budka Gerstmann-Straussler-Scheinker disease. I. Human diseases Folia Neuropathol 42 Suppl. B 2004 120 140
32. S. Liemann, and R. Glockshuber Influence of amino acid substitutions related to inherited human prion diseases on the thermodynamic stability of the cellular prion protein Biochemistry 38 1999 3258 3267
33. A. Lorenzo, and B.A. Yankner Beta-amyloid neurotoxicity requires fibril formation and is inhibited by congo red Proc Natl Acad Sci USA 91 1994 12243 12247 (Pubitemid 24368641)
34. J.A. Mastrianni The genetics of prion diseases Genet Med 12 2010 187 195
35. C. Masullo, A. Bizzarro, V. Guglielmi, E. Iannaccone, G. Minicuci, and M.G. Vita An atypical phenotype of CJD associated with the E200K mutation in the prion protein gene Neurol Sci 2010
36. S. Mead Prion disease genetics Eur J Hum Genet 14 2006 273 281
37. D. Paludi, S. Thellung, K. Chiovitti, A. Corsaro, V. Villa, and C. Russo Different structural stability and toxicity of PrP(ARR) and PrP(ARQ) sheep prion protein variants J Neurochem 103 2007 2291 2300 (Pubitemid 350173570)
38. P. Piccardo, S.R. Dlouhy, P.M. Lievens, K. Young, T.D. Bird, and D. Nochlin Phenotypic variability of Gerstmann-Straussler-Scheinker disease is associated with prion protein heterogeneity J Neuropathol Exp Neurol 57 1998 979 988 (Pubitemid 28478008)
39. P.L. Privalov, and S.J. Gill Stability of protein structure and hydrophobic interaction Adv Protein Chem 39 1988 191 234
40. S.B. Prusiner Prions Proc Natl Acad Sci USA 95 1998 13363 13383 (Pubitemid 28525623)
41. S.B. Prusiner Shattuck lecture - neurodegenerative diseases and prions N Engl J Med 344 2001 1516 1526 (Pubitemid 32429212)
42. H. Rosenmann, G. Talmor, M. Halimi, A. Yanai, R. Gabizon, and Z. Meiner Prion protein with an E200K mutation displays properties similar to those of the cellular isoform PrP(C) J Neurochem 76 2001 1654 1662 (Pubitemid 32221105)
43. W. Swietnicki, M. Morillas, S.G. Chen, P. Gambetti, and W.K. Surewicz Aggregation and fibrillization of the recombinant human prion protein huPrP90-231 Biochemistry 39 2000 424 431 (Pubitemid 30056478)
44. W. Swietnicki, R.B. Petersen, P. Gambetti, and W.K. Surewicz Familial mutations and the thermodynamic stability of the recombinant human prion protein J Biol Chem 273 1998 31048 31052
45. S. Thellung, T. Florio, A. Corsaro, S. Arena, M. Merlino, and M. Salmona Intracellular mechanisms mediating the neuronal death and astrogliosis induced by the prion protein fragment 106-126 Int J Dev Neurosci 18 2000 481 492 (Pubitemid 30243078)
46. S. Thellung, V. Villa, A. Corsaro, S. Arena, E. Millo, and G. Damonte G. p38 MAP kinase mediates the cell death induced by PrP106-126 in the SH-SY5Y neuroblastoma cells Neurobiol Dis 9 2002 69 81 (Pubitemid 34174566)
47. S. Thellung, V. Villa, A. Corsaro, F. Pellistri, V. Venezia, and C. Russo ERK1/2 and p38 MAP kinases control prion protein fragment 90-231-induced astrocyte proliferation and microglia activation Glia 55 2007 1469 1485 (Pubitemid 47461162)
48. M. Toni, E. Spisni, C. Griffoni, S. Santi, M. Riccio, and P. Lenaz Cellular prion protein and caveolin-1 interaction in a neuronal cell line precedes Fyn/Erk 1/2 signal transduction J Biomed Biotechnol 2006 2006 69469
49. M.W. van der Kamp, and V. Daggett The consequences of pathogenic mutations to the human prion protein Protein Eng Des Sel 22 2009 461 468
50. M. Vey, S. Pilkuhn, H. Wille, R. Nixon, S.J. DeArmond, and E.J. Smart Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains Proc Natl Acad Sci USA 93 1996 14945 14949 (Pubitemid 26419075)
51. V. Villa, A. Corsaro, S. Thellung, D. Paludi, K. Chiovitti, and V. Venezia Characterization of the proapoptotic intracellular mechanisms induced by a toxic conformer of the recombinant human prion protein fragment 90-231 Ann N Y Acad Sci 1090 2006 276 291 (Pubitemid 47092132)
52. V. Villa, M. Tonelli, S. Thellung, A. Corsaro, B. Tasso, and F. Novelli Efficacy of novel acridine derivatives in the inhibition of hPrP90-231 prion protein fragment toxicity Neurotox Res 2010 10.1007/s12640-010-9189-8
53. Z. Xia, M. Dickens, J. Raingeaud, R.J. Davis, and M.E. Greenberg Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis Science 270 1995 1326 1331
54. J.T. Yang, C.S. Wu, and H.M. Martinez Calculation of protein conformation from circular dichroism Methods Enzymol 130 1986 208 269
55. S. Yin, N. Pham, S. Yu, C. Li, P. Wong, and B. Chang Human prion proteins with pathogenic mutations share common conformational changes resulting in enhanced binding to glycosaminoglycans Proc Natl Acad Sci USA 104 2007 7546 7551 (Pubitemid 47185943)
56. Y. Zhang, W. Swietnicki, M.G. Zagorski, W.K. Surewicz, and F.D. Sonnichsen Solution structure of the E200K variant of human prion protein. Implications for the mechanism of pathogenesis in familial prion diseases J Biol Chem 275 2000 33650 33654