Prion metal interaction: Is prion pathogenesis a cause or a consequence of metal imbalance?

Chemico-Biological Interactions

Volumn 181, Issue 3, 2009, Pages 282-291

  Rana, Anshul ^a   Gnaneswari, Divya ^a   Bansal, Saurabh ^a   Kundu, Bishwajit ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY DELHI   (India)

Author keywords

Copper; Neurodegeneration; Prions; Scrapie; Zinc

Indexed keywords

COPPER ION; FERROUS ION; MANGANESE; METAL ION; PRION PROTEIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; ZINC ION;

BETA SHEET; CELL DAMAGE; CELL PROTECTION; CONFORMATIONAL TRANSITION; CYTOTOXICITY; ENDOCYTOSIS; ENZYME ACTIVITY; EXPERIMENTAL STUDY; HOMEOSTASIS; HUMAN; HYPOTHESIS; NONHUMAN; PATHOGENESIS; PRION DISEASE; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVIEW; SCRAPIE;

ANIMALS; CATIONS, DIVALENT; HUMANS; METALS; PRION DISEASES; PROTEIN BINDING; PRPC PROTEINS;

EID: 70249140847     PISSN: 00092797     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbi.2009.07.021     Document Type: Review

References (100)

1. Prusiner S.B. Novel proteinaceous infectious particles cause scrapie. Science 216 (1982) 136-144
2. Prusiner S.B. Prions Nobel lecture: prions. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 13363-13383
3. Legname G., Nguyen H.B., Baskakov I.V., Cohen F.E., DeArmond S.J., and Prusiner S.B. Strain-specified characteristics of mouse synthetic prions. Proc. Natl. Acad. Sci. U.S.A. 102 6 (2004) 2168-2173
4. Pattison I.H., and Jebbett J.N. Histopathological similarities between scrapie and cuprizone toxicity in mice. Nature 230 (1971) 115-117
5. Lehmann S. Metal ions and prion diseases. Curr. Opin. Chem. Biol. 6 (2002) 187-192
6. Kim J., Choi S., Kim N.H., Jin J.K., Choi E., Carp R.I., and Kim Y.S. Oxidative stress and neurodegeneration in prion diseases. Ann. NY Acad. Sci. 928 (2001) 182-186
7. Watt N.T., and Hooper N.M. Reactive oxygen species (ROS)-mediated beta-cleavage of the prion protein in the mechanism of the cellular response to oxidative stress. Biochem. Soc. Trans. Pt 5 (2005) 1123-1125
8. Hill A.F., Antoniou M., and Collinge J. Protease-resistant prion protein produced in-vitro lacks detectable infectivity. J. Gen. Virol. 180 (1999) 11-14
9. Kocisko D.A., Come J.H., Priola S.A., Chesebro B., Raymond G.J., Lansbury P.T., and Caughey B. Cell-free formation of protease-resistant prion protein. Nature 370 (1994) 471-474
10. Supattapone S. Prion protein conversion in-vitro. J. Mol. Med. 82 (2004) 348-356
11. Westergard L., Christensen H.M., and Harris D.A. The cellular prion protein (PrPc): its physiological function and role in disease. Biochem. Biophys. Acta 1772 (2007) 629-644
12. Martins V.R., Linden R., Prado M.A.M., Walz R., Sakamoto A.C., Izquierdo I., and Brentani R.R. Cellular prion protein: on the road for functions. FEBS Lett. 512 1-3 (2002) 25-28
13. Linden R., Martins V.R., Prado M.A.M., Cammarota M., Izquierdo I., and Brentani R.R. Physiology of the prion protein. Physiol. Rev. 88 (2008) 673-728
14. Schmitt-Ulms G., Legname G., Baldwin M.A., Ball H.L., Bradon N., Bosque P.J., Crossin K.L., Edelman G.M., DeArmond S.J., Cohen F.E., and Prusiner S.B. Binding of cellular cell-adhesion molecules (N-CAMs) to the cellular prion protein. J. Mol. Biol. 314 (2001) 1209-1225
15. 27-30 is a normal soluble prion protein fragment released by human platelets. Biochem. Biophys. Res. Commun. 223 (1996) 572-577
16. Gatti J.L., Metayer S., Moudjou M., Andreoletti O., Lantier F., Dacheux J.L., and Sarradin P. Prion protein is secreted in soluble forms in the epididymal fluid and proteolytically processed and transported in the seminal plasma. Biol. Reprod. 67 (2002) 393-400
17. Rudd P.M., Merry A.H., Wormald M.R., and Dwek R.A. Glycosylation and prion protein. Curr. Opin. Struct. Biol. 12 (2002) 578-586
18. Prusiner S.B., Cohen E.F., Fletterick R.J., Huang Z., Mehlhorn I., Groth D., Serban A., Gasset M., Nguyen J., Baldwin M., and Pan K.M. Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 10962-10966
19. Zahn R., Liu A., Lührs T., Riek R., vonSchroetter C., López García F., Billeter M., Calzolai L., Wider G., and Wüthrich K. NMR solution structure of the human prion protein. Proc. Natl. Acad. Sci. U.S.A. 97 1 (2000) 145-150
20. Lysek D.A., Schorn C., Nivon L.G., Esteve-Moya V., Christen B., Calzolai L., vonSchroetter C., Fiorito F., Herrmann T., Güntert P., and Wüthrich K. Prion protein NMR structures of cats dogs pigs and sheep. Proc. Natl. Acad. Sci. U.S.A. 102 3 (2005) 640-645
21. 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 oligomerization. Nat. Struct. Biol. 9 (2001) 770-774
22. Leliveld S.R., Dame R.T., Wuite G.J.L., Stitz L., and Korth C. The expanded octarepeat domain selectively binds prions and disrupts homomeric prion protein interactions. J. Biol. Chem. 281 (2006) 3268-3275
23. Goldfarb L.G., Brown P., McCombie W.R., Goldgaber D., Swergold G.D., Willis P.R., Cervenakova L., Barron H., Gibbs C., and Gajdusek D.C. Transmissible familial Creutzfeld-Jakob disease associated with 5,7 and 8 extra octapeptide coding repeats in the PrnP gene. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 10926-10930
24. Grover A., Dugar D., and Kundu B. Predicting alternate structure attainment and amyloidogenesis: a nonlinear signal analysis approach. Biochem. Biophys. Res. Commun. 338 (2005) 1410-1416
25. Kundu B., Maiti N.R., Jones E.M., Surewicz K.A., Vanik D.L., and Surewicz W.K. Nucleation-dependent conformational conversion of the Y145Stop variant of human prion protein: structural clues for prion propagation. Proc. Natl. Acad. Sci. U.S.A. 100 21 (2003) 12069-12074
26. Büeler H., Fischer M., Lang Y., Bluethman H., Lipp H.P., DeArmond S.J., Prusiner S.B., Aguet M., and Weissman C. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356 (1992) 577-582
27. Manson J.C., Clarke A.R., Hooper M.L., Aitchison L., McConnell I., and Hope J. 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol. Neurobiol. 8 (1994) 121-127
28. Weissmann C., and Flechsig E. PrP knock-out and PrP transgenic mice in prion research. Br. Med. Bull. 66 (2003) 43-60
29. Whittington M.A., Sidle K.C.L., Gowland I., Meads J., Hill A.F., Palmer M.S., Jefferys J.G.R., and Collinge J. Rescue of neurophysiological phenotype seen in PrP null mice by transgene encoding human prion protein. Nat. Genet. 9 (1995) 197-201
30. Brown D.R., Qin K., Herms J.W., Madlung A., Manson J., Strome R., Fraser P.E., Kruck T., vanBohlen A., Schulz-Schaefer W., Giese A., Westaway D., and Kretzschmar H. The cellular prion protein binds copper in-vivo. Nature 390 (1997) 18-25
31. Watt N.T., and Hooper N.M. The prion protein and neuronal zinc homeostasis. Trends Biochem. Sci. 8 (2003) 406-410
32. Pauly P.C., and Harris D.A. Copper stimulates endocytosis of the prion protein. J. Biol. Chem. 273 50 (1998) 33107-33110
33. White A.R., Collins S.J., Maher F., Jobling M.F., Stewart L.R., Thyer J.M., Beyreuther K., Masters C.L., and Cappai R. Prion protein deficient neurons reveal lower glutathione reductase activity and increased susceptibility to hydrogen peroxide toxicity. Am. J. Pathol. 155 (1999) 1723-1730
34. Brown D.R., Schmidt B., and Kretzschmar H.A. Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature 380 (1996) 345-347
35. Brown L.R., and Harris D.A. Copper and zinc cause delivery of the prion protein from the plasma membrane to a subset of early endosomes and the Golgi. J. Neurochem. 87 2 (2003) 353-363
36. Whittal R.M., Ball H.L., Cohen F.E., Burlingame A.L., Prusiner S.B., and Baldwin M.A. Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry. Protein Sci. 2 (2000) 332-343
37. Perera W.S.S., and Hooper N.M. Ablation of the metal ion-induced endocytosis of the prion protein by disease-associated mutation of the octarepeat region. Curr. Biol. 11 7 (2001) 519-523
38. Kuwahara C., Takeuchi A.M., Nishimura T., Haraguchi K., Kubosaki A., Matsumoto Y., Saeki K., Matsumoto Y., Yokoyama T., Itohara S., and Onodera T. Prions prevents neuronal cell-line death. Nature 400 (1999) 225-226
39. Wong B.S., Pan T., Liu T., Li R., Petersen R.B., Jones I.M., Gambetti P., Brown D.R., and Sy M.S. Prion disease: a loss of antioxidant function?. Biochem. Biophys. Res. Commun. 275 (2000) 249-252
40. Pushie M.J., Ross A.R.S., and Vogel H.J. Mass spectrometric determination of the coordination geometry of potential copper (II) surrogates for the mammalian prion protein octarepeat region. Anal. Chem. 79 (2007) 5659-5667
41. Pan K.M., Stahl N., and Prusiner S.B. Purification and properties of the cellular prion protein from Syrian hamster brain. Protein Sci. 10 (1992) 1343-1352
42. Choi C.J., Kanthasamy A., Anantharam V., and Kanthasamy A.G. Interaction of metals with prion protein: possible role of divalent cations in the pathogenesis of prion diseases. Neurotoxicology 27 (2006) 777-787
43. Basu S., Moha M.L., Luo X., Kundu B., Kong Q., and Singh N. 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 18 (2007) 3302-3312
44. Leach S.P., Salman M.D., and Hamar D. Trace elements and prion diseases: a review of the interactions of copper manganese & zinc with the prion protein. Anim. Health Res. Rev. 7 1-2 (2006) 97-105
45. Thackray A.M., Knight R., Haswell S.J., Bujdoso R., and Brown D.R. Metal imbalance and compromised antioxidant function are early changes in prion disease. Biochem. J. 362 (2002) 253-258
46. Sigurdsson E.M., Brown D.R., Alim M.A., Scholtzova H., Carp R., Meeker H.C., Prelli F., Frangione B., and Wisniewski T. Copper chelation delays the onset of prion disease. J. Biol. Chem. 278 47 (2003) 46199-46202
47. Imrie C.E., Korre A., and Munoz-Melendez G. Spatial correlation between the prevalence of transmissible spongiform diseases and British soil geochemistry. Environ. Geochem. Health 31 (2009) 133-145
48. Ragnarsdottir K.V., and Hawkins D.P. Bioavailable copper and manganese in soils from Iceland and their relationship to scrapie occurrence in sheep. J. Geochem. Explor. 88 (2006) 228-234
49. 2+ binding modes of full-length prion protein. J. Biol. Chem. 283 4 (2008) 1870-1881
50. 2+ to the C-terminal domain of the murine prion protein. Biophys. J. 81 1 (2001) 516-525
51. Viles J.H., Cohen F.E., Prusiner S.B., Goodin D.B., Wright P.E., and Dyson H.J. Copper binding to the prion protein: structural implications of four identical cooperative binding sites. Proc. Natl. Acad. Sci. U.S.A. 96 5 (1999) 2042-2047
52. Millhauser G.L. Copper and the prion protein: methods structures function and disease. Ann. Rev. Phys. Chem. 58 (1999) 299-320
53. Davies P., and Brown D.R. The chemistry of copper binding to PrP: is there sufficient evidence to elucidate a role for copper in protein function?. Biochem. J. 410 2 (2008) 237-244
54. Miura T., Hori A., Mototani H., and Takeuchi H. Raman spectroscopic study on the copper (II) binding mode of prion octapeptide and its pH dependence. Biochemistry 38 35 (1999) 11560-11569
55. Kramer M.L., Kratzin H.D., Schmidt B., Romer A., Windl O., Liemann S., Hornemann S., and Kretzschmar H. Prion protein binds copper within the physiological concentration range. J. Biol. Chem. 276 20 (2001) 16711-16719
56. Jackson G.S., Murray I., Hosszu L.L., Gibbs N., Waltho J.P., Clarke A.R., and Collinge J. Location and properties of metal-binding sites on the human prion protein. Proc. Natl. Acad. Sci. U.S.A. 98 15 (2001) 8531-8535
57. Pushie M.J., and Rauk A. Computational studies of Cu (II) peptide binding motifs: Cu[HGGG] and Cu[HG] as models for Cu(II) binding to the prion protein octarepeat region. J. Biol. Inorg. Chem. 8 (2003) 53-65
58. Walter E.D., Chattopadhyay M., and Millhauser G.L. The affinity of copper binding to the prion protein octarepeat domain: evidence for negative cooperativity. Biochemistry 45 43 (2006) 3083-3092
59. Inanami O., Hashida S., Iizuka D., Horiuchi M., Hiraoka W., Shimoyama Y., Nakamura H., Inagaki F., and Kuwabara M. Conformational change in full-length mouse prion: a site-directed spin-labeling study. Biochem. Biophys. Res. Commun. 335 3 (2005) 785-792
60. Gustiananda M., Haris P.I., Milburn P.J., and Gready J.E. Copper-induced conformational change in a marsupial prion protein repeat peptide probed using FTIR spectroscopy. FEBS Lett. 512 1-3 (2002) 38-42
61. Qin K., Yang D.S., Yang Y., Chishti M.A., Meng L.J., Kretzschmar H.A., Yip C.M., Fraser P.E., and Westaway D. Copper (II)-induced conformational changes and protease resistance in recombinant and cellular PrP. J. Biol. Chem. 275 25 (2000) 19121-19131
62. 2+: a novel ionic mediator of neural injury in brain disease. Trends Pharmacol. Sci. 21 10 (2000) 395-401
63. Howell G.A., Welch M.G., and Frederickson C.J. Simulation induced neuronal uptake and release of zinc in hippocampal slices. Nature 308 (1984) 736-738
64. 2+ from brain tissue during activity. Nature 308 (1984) 734-736
65. Frederickson C.J. Neurobiology of zinc and zinc-containing neurons. Int. Rev. Neurobiol. 31 (1989) 145-238
66. Colvin R.A., Davis N., Nipper R.W., and Carter P.A. Zinc transport in the brain: routes of zinc influx and efflux in neurons. J. Nutr. 130 5S Suppl. (2000) 1484S-1487S
67. 2+ coordination modes. J. Am. Chem. Soc. 129 (2007) 15440-15444
68. Brown D.R., Hafiz F., Glassmith L.L., Wong B., Jones I.M., Clive C., and Haswell S.J. Consequences of manganese replacement of copper for prion protein function and proteinase resistance. EMBO J. 19 6 (2000) 1180-1186
69. Wong B., Chen S.G., Colucci M., Xie Z., Pan T., Liu T., Li R., Gambetti P., Sy M.S., and Brown D.R. Aberrant metal binding by prion protein in human prion disease. J. Neurochem. 78 (2001) 1400-1408
70. Hesketh S., Sassoon J., Knight R., Hopkins J., and Brown D.R. Elevated manganese levels in blood and central nervous system occur before onset of clinical signs in scrapie and bovine spongiform encephalopathy. J. Anim. Sci. 85 6 (2007) 1596-1609
71. Hesketh S., Sassoon J., Knight R., and Brown D.R. Elevated manganese levels in blood and CNS in human prion disease. Mol. Cell. Neurosci. 37 3 (2008) 590-598
72. Tsenkova R.N., Iordanova I.K., Toyoda K., and Brown D.R. Prion protein fate governed by metal binding. Biochem. Biophys. Res. Commun. 325 (2004) 1005-1012
73. Choi C.J., Anantharam V., Saetveit N.J., Houk R.S., Kanthasamy A., and Kanthasamy A.G. Normal cellular prion protein protects against manganese-induced oxidative stress and apoptotic cell death. Toxicol. Sci. 98 2 (2007) 495-509
74. Brazier M.W., Davies P., Player E., Marken F., Viles J.H., and Brown D.R. Manganese binding to the prion protein. J. Biol. Chem. 283 19 (2008) 12831-12839
75. Mishra R.S., Basu S., Gu Y., Luo X., Zou W.Q., Mishra R., Li R., Chen S.G., Gambetti P., Fujioka H., and Singh N. 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. 24 50 (2004) 11280-11290
76. Kim N., Park S., Jin J., Kwon M., Choi E., Carp R.I., and Kim Y. Increased ferric iron content and iron-induced oxidative stress in the brains of scrapie-infected mice. Brain Res. 884 (2000) 98-103
77. Fernaeus S., Halldin J., Bedecs K., and Land T. Changed iron regulation in scrapie-infected neuroblastoma cells. Mol. Brain. Res. 133 (2005) 266-273
78. Hornshaw M.P., McDermott J.R., Candy J.M., and Lakey J.H. Copper binding to the N-terminal tandem repeat region of mammalian and avian prion protein: structural studies using synthetic peptides. Biochem. Biophys. Res. Commun. 214 3 (1995) 993-999
79. Bull P.C., Thomas G.R., Rommens J.M., Forbes J.R., and Cox D.W. The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat. Genet. 5 4 (1993) 327-337
80. Chelly J., Tümer Z., Tønnesen T., Petterson A., Ishikawa-Brush Y., Tommerup N., Horn N., and Monaco A.P. Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nat. Genet. 3 1 (1993) 14-19
81. Stöckel J., Safar J., Wallace A.C., Cohen F.E., and Prusiner S.B. Prion protein selectively binds copper(II) ions. Biochemistry 37 20 (1998) 7185-7193
82. Quaglio E., Chiesa R., and Harris D.A. Copper converts the cellular prion protein into a protease-resistant species that is distinct from the scrapie isoform. J. Biol. Chem. 276 14 (2001) 11432-11438
83. McKenzie D., Bartz J., Mirwald J., Olander D., Marsh R., and Aiken J. Reversibility of scrapie inactivation is enhanced by copper. J. Biol. Chem. 273 40 (1998) 25545-25547
84. Shaked Y., Rosenmann H., Hijazi N., Halimi M., and Gabizon R. Copper binding to the PrP isoforms: a putative marker of their conformation and function. J. Virol. 75 17 (2001) 7872-7874
85. Yang S., Thackray A.M., Fitzmaurice T.J., and Bujdoso R. Copper-induced structural changes in the ovine prion protein are influenced by a polymorphism at codon 112. Biochim. Biophys. Acta 1784 (2008) 683-692
86. Liu M., Li Y., Zhou X., and Zhao D. Copper (II) inhibits in-vitro conformational conversion of Ovine prion protein triggered by low pH. J. Biochem. 143 (2008) 333-337
87. Wadsworth J.D.F., Hill A.F., Joiner S., Jackson G.S., Clarke A.R., and Collinge J. Strain-specific prion-protein conformation determined by metal ions. Nat. Cell. Biol. 1 (1999) 55-59
88. Burns C.S., Aronoff-Spencer E., Dunham C.M., Lario P., Avdievich N.I., Antholine W.E., Olmstead M.M., Vrielink A., Gerfen G.J., Peisach J., Scott W.G., and Millhauser G.L. Molecular features of the copper binding sites in the octarepeat domain of the prion protein. Biochemistry 41 (2002) 3991-4001
89. Balvay D.T., Simon S., Creminon C., Grassi J., Srikrishnan T., and Vijayalakshmi M.A. Copper binding to prion octarepeat peptides a combined metal chelate affinity and immunochemical approaches. J. Chromatogr. B 818 (2005) 75-82
90. Cereghetti G.M., Schweiger A., Glockshuber R., and Doorslaer S.V. Stability and Cu(II) binding of prion protein variants related to inherited human prion disease. Biophys. J. 84 (2003) 1985-1997
91. Bocharova O.V., Breydo L., Salnikov V.V., and Baskakov I.V. Copper (II) inhibits in-vitro conversion of prion protein in to amyloid fibrils. Biochemistry 44 (2005) 6776-6787
92. Jobling M.F., Huang X., Stewart L.R., Barnham K.J., Curtain C., Volitakis I., Perugini M., White A.R., Cherny R.A., Masters C.L., Barrow C.J., Collins S.J., Bush A.I., and Cappai R. Copper and zinc binding modulates the aggregation and neurotoxic properties of the prion peptide PrP106-126. Biochemistry 40 27 (2001) 8073-8084
93. Kenward A.G., Bartolotti L.J., and Burns C.S. Copper and zinc promote interactions between membrane-anchored peptides of the metal binding domain of the prion protein. Biochemistry 46 14 (2007) 4261-4271
94. Varela-Nallar L., Toledo E.M., Larrondo L.F., Cabral A.L.B., Martins V.L., and Inestrosa N.C. Induction of cellular prion protein gene expression by copper in neurons. Am. J. Physiol. Cell Physiol. 290 (2006) C271-C281
95. Rachidi W., Vilette D., Guiraud P., Arlotto M., Riondel J., Laude H., Lehmann S., and Favier A. Expression of prion protein increases cellular copper binding and antioxidant enzyme activities but not copper delivery. J. Biol. Chem. 278 11 (2003) 9064-9072
96. Maynard C.J., Cappai R., Volitakis I., Cherny R.A., White A.R., Beyreuther K., Masters C.L., Bush A.I., and Li Q.X. Overexpression of Alzheimer's disease amyloid-beta opposes the age-dependent elevations of brain copper and iron. J. Biol. Chem. 277 47 (2002) 44670-44676
97. Hegde R.S., Tremblay P., Groth D., DeArmond S.J., Prusiner S.B., and Lingappa V.R. Transmissible and genetic prion diseases share a common pathway of neurodegeneration. Nature 402 6763 (1999) 822-826
98. Armendariz A.D., Gonzalez M., Loguinov A.V., and Vulpe C.D. Gene expression profiling in chronic copper overload reveals upregulation of PrnP and App. Physiol. Genomics 20 (2004) 45-54
99. Toni M., Massimino M.L., Griffoni C., Salvato B., Tomasi V., and Spisni E. Extracellular copper ions regulate cellular prion protein (PrPc) expression and metabolism in neuronal cells. FEBS Lett. 579 (2005) 741-744
100. Lewis P.A., Tattum M.H., Jones S., Bhelt D., Batchelor M., Clarke A.R., Collinge J., and Jackson G.S. Codon 129 polymorphism of the human prion protein influences the kinetics of amyloid formation. J. Gen. Virol. 87 (2006) 2443-2449