Early onset prion disease from octarepeat expansion correlates with copper binding properties

PLoS Pathogens

Volumn 5, Issue 4, 2009, Pages

  Stevens, Daniel J ^a   Walter, Eric D ^a   Rodríguez, Abel ^b   Draper, David ^b   Davies, Paul ^c   Brown, David R ^c   Millhauser, Glenn L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California Santa Cruz   (United States)

^c University of Bath   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE; COPPER; COPPER ION; HISTIDINE; OCTAPEPTIDE; PRION PROTEIN; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; COPPER BLOOD LEVEL; GENE MUTATION; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; NONHUMAN; OCTAREPEAT EXPANSION; ONSET AGE; PRION DISEASE; PROTEIN DOMAIN; PROTEIN POLYMERIZATION; WILD TYPE; ADULT; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; HAMSTER; HUMAN; METABOLISM; MIDDLE AGED; MOUSE; PHYSIOLOGY; PRION; SYRIAN HAMSTER;

ADULT; AGE OF ONSET; ANIMALS; COPPER; CRICETINAE; HISTIDINE; HUMANS; MESOCRICETUS; MICE; MIDDLE AGED; MODELS, MOLECULAR; PRION DISEASES; PRIONS; PRPSC PROTEINS; REPETITIVE SEQUENCES, AMINO ACID;

EID: 66349096914     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000390     Document Type: Article

References (77)

1. Prusiner SB (1997) Prion diseases and the BSE crisis. Science 278: 245-251.
2. Prusiner SB (1998) Prions. Proc Natl Acad Sci U S A 95: 13363-13383.
3. Prusiner SB (2003) Prion Biology and Diseases. Cold Spring Harbor (New York): Cold Spring Harbor Laboratory Press.
4. Prusiner SB (2001) Shattuck lecture-neurodegenerative diseases and prions. N Engl J Med 344: 1516-1526.
5. Kong Q, Surewicz WK, Petersen RB, Zou W, Chen SG, et al. (2004) Inherited Prion Diseases. In: Prusiner SB, ed. Prion Biology and Diseases. Cold Spring Harbor (New York): Cold Spring Harbor Library Press. pp 673-775.
6. Lehmann S, Harris DA (1996) Two mutant prion proteins expressed in cultured cells acquire biochemical properties reminiscent of the scrapie isoform. Proc Natl Acad Sci U S A 93: 5610-5614.
7. Priola SA, Chesebro B (1998) Abnormal properties of prion protein with insertional mutations in different cell types. J Biol Chem 273: 11980-11985.
8. Ivanova L, Barmada S, Kummer T, Harris DA (2001) Mutant prion proteins are partially retained in the endoplasmic reticulum. J Biol Chem 276: 42409-42421.
9. Lehmann S, Harris DA (1995) A mutant prion protein displays an aberrant membrane association when expressed in cultured cells. J Biol Chem 270: 24589-24597.
10. Chiesa R, Drisaldi B, Quaglio E, Migheli A, Piccardo P, et al. (2000) Accumulation of protease-resistant prion protein (PrP) and apoptosis of cerebellar granule cells in transgenic mice expressing a PrP insertional mutation. Proc Natl Acad Sci U S A 97: 5574-5579.
11. Chiesa R, Piccardo P, Ghetti B, Harris DA (1998) Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron 21: 1339-1351.
12. Chiesa R, Piccardo P, Quaglio E, Drisaldi B, Si-Hoe SL, et al. (2003) Molecular distinction between pathogenic and infectious properties of the prion protein. J Virol 77: 7611-7622.
13. Castilla J, Gutierrez-Adan A, Brun A, Pintado B, Salguero FJ, et al. (2005) Transgenic mice expressing bovine PrP with a four extra repeat octapeptide insert mutation show a spontaneous, non-transmissible, neurodegenerative disease and an expedited course of BSE infection. FEBS Lett 579: 6237-6246.
14. Goldfarb LG, Brown P, McCombie WR, Goldgaber D, Swergold GD, et al. (1991) Transmissible familial Creutzfeldt-Jakob disease associated with five, seven, and eight extra octapeptide coding repeats in the PRNP gene. Proc Natl Acad Sci U S A 88: 10926-10930.
15. Moore RA, Herzog C, Errett J, Kocisko DA, Arnold KM, et al. (2006) Octapeptide repeat insertions increase the rate of protease-resistant prion protein formation. Protein Sci 15: 609-619.
16. Leliveld SR, Dame RT, Wuite GJ, Stitz L, Korth C (2006) The expanded octarepeat domain selectively binds prions and disrupts homomeric prion protein interactions. J Biol Chem 281: 3268-3275.
17. Leliveld SR, Stitz L, Korth C (2008) Expansion of the octarepeat domain alters the misfolding pathway but not the folding pathway of the prion protein. Biochemistry 47: 6267-6278.
18. McKinley MP, Bolton DC, Prusiner SB (1983) A protease-resistant protein is a structural component of the scrapie prion. Cell 35: 57-62.
19. Walter ED, Chattopadhyay M, Millhauser GL (2006) The affinity of copper binding to the prion protein octarepeat domain: evidence for negative cooperativity. Biochemistry 45: 13083-13092.
20. Kramer ML, Kratzin HD, Schmidt B, Romer A, Windl O, et al. (2001) Prion protein binds copper within the physiological concentration range. J Biol Chem 276: 16711-16719.
21. Millhauser GL (2004) Copper binding in the prion protein. Acc Chem Res 37: 79-85.
22. Millhauser GL (2007) Copper and the prion protein: methods, structures, function, and disease. Annu Rev Phys Chem 58: 299-320.
23. Vassallo N, Herms J (2003) Cellular prion protein function in copper homeostasis and redox signalling at the synapse. J Neurochem 86: 538-544.
24. Pauly PC, Harris DA (1998) Copper stimulates endocytosis of the prion protein. J Biol Chem 273: 33107-33110.
25. Perera WS, Hooper NM (2001) Ablation of the metal ion-induced endocytosis of the prion protein by disease-associated mutation of the octarepeat region. Curr Biol 11: 519-523.
26. Chattopadhyay M, Walter ED, Newell DJ, Jackson PJ, Aronoff-Spencer E, et al. (2005) The octarepeat domain of the prion protein binds Cu(II) with three distinct coordination modes at pH 7.4. J Am Chem Soc 127: 12647-12656.
27. Burns CS, Aronoff-Spencer E, Dunham CM, Lario P, Avdievich NI, et al. (2002) Molecular features of the copper binding sites in the octarepeat domain of the prion protein. Biochemistry 41: 3991-4001.
28. Dong J, Bloom JD, Goncharov V, Chattopadhyay M, Millhauser GL, et al. (2007) Probing the role of PrP repeats in conformational conversion and amyloid assembly of chimeric yeast prions. J Biol Chem 282: 34204-34212.
29. Walter ED, Stevens DJ, Visconte MP, Millhauser GL (2007) The prion protein is a combined zinc and copper binding protein: Zn2+ alters the distribution of Cu2+ coordination modes. J Am Chem Soc 129: 15440-15441.
30. Shtyrlin V, Zyavkina Y, Ilakin V, Garipov R, Zakharov A (2005) Structure, stability, and ligand exchange of copper (II) complexes with oxidized glutathione. J Inorg Biochem 99: 1335-1346.
31. Várnagy K, SzabóJ, SóvágóI, Malandrinos G, Hadjiliadis N, et al. (2000) Equilibrium and structural studies on copper (II) complexes of tetra-, penta-, and hexa-peptides containing histidyl residues at the C-termini. J Chem Soc Dalton Trans 2000: 467-472.
32. Croes EA, Theuns J, Houwing-Duistermaat JJ, Dermaut B, Sleegers K, et al. (2004) Octapeptide repeat insertions in the prion protein gene and early onset dementia. J Neurol Neurosurg Psychiatry 75: 1166-1170.
33. Altman DG (1991) Practical Statistics for Medical Research. London: Chapman and Hall.
34. Breiman L, Friedman J, Stone CJ, Olshen RA (1984) Classification and Regression Trees. New York: Chapman and Hall (Wadsworth, Inc.).
35. Boesenberg C, Schulz-Schaeffer WJ, Meissner B, Kallenberg K, Bartl M, et al. (2005) Clinical course in young patients with sporadic Creutzfeldt-Jakob disease. Ann Neurol 58: 533-543.
36. Hopt A, Korte S, Fink H, Panne U, Niessner R, et al. (2003) Methods for studying synaptosomal copper release. J Neurosci Methods 128: 159-172.
37. Kardos J, Kovacs I, Hajos F, Kalman M, Simonyi M (1989) Nerve endings from rat brain tissue release copper upon depolarization. A possible role in regulating neuronal excitability. Neurosci Lett 103: 139-144.
38. Li A, Christensen HM, Stewart LR, Roth KA, Chiesa R, et al. (2007) Neonatal lethality in transgenic mice expressing prion protein with a deletion of residues 105-125. EMBO J 26: 548-558.
39. Baumann F, Tolnay M, Brabeck C, Pahnke J, Kloz U, et al. (2007) Lethal recessive myelin toxicity of prion protein lacking its central domain. EMBO J 26: 538-547.
40. Taylor DR, Hooper NM (2007) The low-density lipoprotein receptor-related protein 1 (LRP1) mediates the endocytosis of the cellular prion protein. Biochem J 402: 17-23.
41. Bocharova OV, Breydo L, Salnikov VV, Baskakov IV (2005) Copper(II) inhibits in vitro conversion of prion protein into amyloid fibrils. Biochemistry 44: 6776-6787.
42. Aronoff-Spencer E, Burns CS, Avdievich NI, Gerfen GJ, Peisach J, et al. (2000) Identification of the Cu2+ binding sites in the N-terminal domain of the prion protein by EPR and CD spectroscopy. Biochemistry 39: 13760-13771.
43. Abdelraheim SR, Kralovicova S, Brown DR (2006) Hydrogen peroxide cleavage of the prion protein generates a fragment able to initiate polymerisation of full length prion protein. Int J Biochem Cell Biol 38: 1429-1440.
44. Thompsett AR, Abdelraheim SR, Daniels M, Brown DR (2005) High affinity binding between copper and full-length prion protein identified by two different techniques. J Biol Chem 280: 42750-42758.
45. Herrmann T, Guntert P, Wuthrich K (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319: 209-227.
46. Liu H, Farr-Jones S, Ulyanov NB, Llinas M, Marqusee S, et al. (1999) Solution structure of Syrian hamster prion protein rPrP(90-231). Biochemistry 38: 5362-5377.
47. Laplanche JL, Delasnerie-Laupretre N, Brandel JP, Dussaucy M, Chatelain J, et al. (1995) Two novel insertions in the prion protein gene in patients with lateonset dementia. Hum Mol Genet 4: 1109-1111.
48. Pietrini V, Puoti G, Limido L, Rossi G, Di Fede G, et al. (2003) Creutzfeldt- Jakob disease with a novel extra-repeat insertional mutation in the PRNP gene. Neurology 61: 1288-1291.
49. van Harten B, van Gool WA, Van Langen IM, Deekman JM, Meijerink PH, et al. (2000) A new mutation in the prion protein gene: a patient with dementia and white matter changes. Neurology 55: 1055-1057.
50. Grasbon-Frodl E, Schmalzbauer R, Weber P, Krebs B, Windl O, et al. (2004) A novel three extra-repeat insertion in the prion protein gene (PRNP) in a patient with Creutzfeldt-Jakob disease. Neurogenetics 5: 249-250.
51. Nishida Y, Sodeyama N, Toru Y, Toru S, Kitamoto T, et al. (2004) Creutzfeldt- Jakob disease with a novel insertion and codon 219 Lys/Lys polymorphism in PRNP. Neurology 63: 1978-1979.
52. Isozaki EMK, Kagamihara Y, Hirose K, Tanabe H, Uchihara TOM, Nagashima T (1994) CJD presenting as frontal lobe dementia associated with a 96 base pair insertion in the prion protein gene (in Japanese). Dementia 8: 363-371.
53. Campbell TA, Palmer MS, Will RG, Gibb WR, Luthert PJ, et al. (1996) A prion disease with a novel 96-base pair insertional mutation in the prion protein gene. Neurology 46: 761-766.
54. Rossi G, Giaccone G, Giampaolo L, Iussich S, Puoti G, et al. (2000) Creutzfeldt- Jakob disease with a novel four extra-repeat insertional mutation in the PrP gene. Neurology 55: 405-410.
55. Yanagihara C, Yasuda M, Maeda K, Miyoshi K, Nishimura Y (2002) Rapidly progressive dementia syndrome associated with a novel four extra repeat mutation in the prion protein gene. J Neurol Neurosurg Psychiatry 72: 788-791.
56. Cochran EJ, Bennett DA, Cervenakova L, Kenney K, Bernard B, et al. (1996) Familial Creutzfeldt-Jakob disease with a five-repeat octapeptide insert mutation. Neurology 47: 727-733.
57. Skworc KH, Windl O, Schulz-Schaeffer WJ, Giese A, Bergk J, et al. (1999) Familial Creutzfeldt-Jakob disease with a novel 120-bp insertion in the prion protein gene. Ann Neurol 46: 693-700.
58. Beck G, Kawano T, Naba I, Nishimura T, Sawada J, et al. (2005) A case with a 120 base pair insertional mutation in the prion protein gene: the first case in Japan. J Neurol Neurosurg Psychiatry 76: 756-757.
59. Mead S, Webb TE, Campbell TA, Beck J, Linehan JM, et al. (2007) Inherited prion disease with 5-OPRI: phenotype modification by repeat length and codon 129. Neurology 69: 730-738.
60. Oda T, Kitamoto T, Tateishi J, Mitsuhashi T, Iwabuchi K, et al. (1995) Prion disease with 144 base pair insertion in a Japanese family line. Acta Neuropathol 90: 80-86.
61. Capellari S, Vital C, Parchi P, Petersen RB, Ferrer X, et al. (1997) Familial prion disease with a novel 144-bp insertion in the prion protein gene in a Basque family. Neurology 49: 133-141.
62. King A, Doey L, Rossor M, Mead S, Collinge J, et al. (2003) Phenotypic variability in the brains of a family with a prion disease characterized by a 144- base pair insertion in the prion protein gene. Neuropathol Appl Neurobiol 29: 98-105.
63. Gelpi E, Kovacs GG, Strobel T, Koperek O, Voigtlander T, et al. (2005) Prion disease with a 144 base pair insertion: unusual cerebellar prion protein immunoreactivity. Acta Neuropathol 110: 513-519.
64. Kovacs T, Beck JA, Papp MI, Lantos PL, Aranyi Z, et al. (2007) Familial prion disease in a Hungarian family with a novel 144-base pair insertion in the prion protein gene. J Neurol Neurosurg Psychiatry 78: 321-323.
65. Collinge J, Brown J, Hardy J, Mullan M, Rossor MN, et al. (1992) Inherited prion disease with 144 base pair gene insertion. 2. Clinical and pathological features. Brain 115(Pt 3): 687-710.
66. Owen F, Poulter M, Lofthouse R, Collinge J, Crow TJ, et al. (1989) Insertion in prion protein gene in familial Creutzfeldt-Jakob disease. Lancet 1: 51-52.
67. Mizushima S, Ishii K, Nishimaru T (1994) A case of presenile dementia with a 168 base pair insertion in prion protein gene (in Japanese). Dementia 8: 380-390.
68. Dermaut B, Cruts M, Backhovens H, Lubke U, Van Everbroeck B, et al. (2000) Familial Creutzfeldt-Jakob disease in a patient carrying both a presenilin 1 missense substitution and a prion protein gene insertion. J Neurol 247: 364-368.
69. Lewis V, Collins S, Hill AF, Boyd A, McLean CA, et al. (2003) Novel prion protein insert mutation associated with prolonged neurodegenerative illness. Neurology 60: 1620-1624.
70. Wang XF, Guo YJ, Zhang BY, Zhao WQ, Gao JM, et al. (2007) Creutzfeldt- Jakob disease in a Chinese patient with a novel seven extra-repeat insertion in PRNP. J Neurol Neurosurg Psychiatry 78: 201-203.
71. Goldfarb LG, Brown P, Vrbovska A, Baron H, McCombie WR, et al. (1992) An insert mutation in the chromosome 20 amyloid precursor gene in a Gerstmann- Straussler-Scheinker family. J Neurol Sci 111: 189-194.
72. van Gool WA, Hensels GW, Hoogerwaard EM, Wiezer JH, Wesseling P, et al. (1995) Hypokinesia and presenile dementia in a Dutch family with a novel insertion in the prion protein gene. Brain 118(Pt 6): 1565-1571.
73. Stam FC, Wigboldus JM, Grosveld FM (1968) A peculiar type of presenile dementia. Psychiatr Neurol Neurochir 71: 337-350.
74. Laplanche JL, Hachimi KH, Durieux I, Thuillet P, Defebvre L, et al. (1999) Prominent psychiatric features and early onset in an inherited prion disease with a new insertional mutation in the prion protein gene. Brain 122(Pt 12): 2375-2386.
75. Owen F, Poulter M, Collinge J, Leach M, Lofthouse R, et al. (1992) A dementing illness associated with a novel insertion in the prion protein gene. Brain Res Mol Brain Res 13: 155-157.
76. Duchen LW, Poulter M, Harding AE (1993) Dementia associated with a 216 base pair insertion in the prion protein gene. Clinical and neuropathological features. Brain 116(Pt 3): 555-567.
77. Krasemann S, Zerr I, Weber T, Poser S, Kretzschmar H, et al. (1995) Prion disease associated with a novel nine octapeptide repeat insertion in the PRNP gene. Brain Res Mol Brain Res 34: 173-176.