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Neurological Sciences
Published in: Neurological Sciences 9/2020

Open Access 01-09-2020 | Review Article

Using NMR spectroscopy to investigate the role played by copper in prion diseases

Authors: Rawiah A. Alsiary, Mawadda Alghrably, Abdelhamid Saoudi, Suliman Al-Ghamdi, Lukasz Jaremko, Mariusz Jaremko, Abdul-Hamid Emwas

Published in: Neurological Sciences | Issue 9/2020

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Abstract

Prion diseases are a group of rare neurodegenerative disorders that develop as a result of the conformational conversion of normal prion protein (PrPC) to the disease-associated isoform (PrPSc). The mechanism that actually causes disease remains unclear. However, the mechanism underlying the conformational transformation of prion protein is partially understood—in particular, there is strong evidence that copper ions play a significant functional role in prion proteins and in their conformational conversion. Various models of the interaction of copper ions with prion proteins have been proposed for the Cu (II)-binding, cell-surface glycoprotein known as prion protein (PrP). Changes in the concentration of copper ions in the brain have been associated with prion diseases and there is strong evidence that copper plays a significant functional role in the conformational conversion of PrP. Nevertheless, because copper ions have been shown to have both a positive and negative effect on prion disease onset, the role played by Cu (II) ions in these diseases remains a topic of debate. Because of the unique properties of paramagnetic Cu (II) ions in the magnetic field, their interactions with PrP can be tracked even at single atom resolution using nuclear magnetic resonance (NMR) spectroscopy. Various NMR approaches have been utilized to study the kinetic, thermodynamic, and structural properties of Cu (II)-PrP interactions. Here, we highlight the different models of copper interactions with PrP with particular focus on studies that use NMR spectroscopy to investigate the role played by copper ions in prion diseases.
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Literature
1.
Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D et al (1993) Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci U S A 90(23):10962–10966PubMedPubMedCentral
2.
Shinkai-Ouchi F, Yamakawa Y, Hara H, Tobiume M, Nishijima M, Hanada K et al (2010) Identification and structural analysis of C-terminally truncated collapsin response mediator protein-2 in a murine model of prion diseases. Proteome Sci 8
3.
Kurt TD, Jiang L, Fernández-Borges N, Bett C, Liu J, Yang T et al (2015) Human prion protein sequence elements impede cross-species chronic wasting disease transmission. J Clin Invest 125(4):1485–1496PubMedPubMedCentral
4.
Oliveira-Martins JB, Yusa S-i, Calella AM, Bridel C, Baumann F, Dametto P et al (2010) Unexpected tolerance of α-cleavage of the prion protein to sequence variations. PLoS One 5(2):e9107PubMedPubMedCentral
5.
Schätzl HM, Da Costa M, Taylor L, Cohen FE, Prusiner SB (1995) Prion protein gene variation among primates. J Mol Biol 245(4):362–374PubMed
6.
Collinge J (2001) Prion diseases of humans and animals: their causes and molecular basis. Annu Rev Neurosci 24:519–550PubMed
7.
Morot-Gaudry-Talarmain Y, Rezaei H, Guermonprez L, Treguer E, Grosclaude J (2003) Selective prion protein binding to synaptic components is modulated by oxidative and nitrosative changes induced by copper (II) and peroxynitrite in cholinergic synaptosomes, unveiling a role for calcineurin B and thioredoxin. J Neurochem 87(6):1456–1470PubMed
8.
Suhre MH, Hess S, Golser AV, Scheibel T (2009) Influence of divalent copper, manganese and zinc ions on fibril nucleation and elongation of the amyloid-like yeast prion determinant Sup35p-NM. J Inorg Biochem 103(12):1711–1720PubMed
9.
Huang S, Chen L, Bladen C, Stys PK, Zamponi GW (2018) Differential modulation of NMDA and AMPA receptors by cellular prion protein and copper ions. Mol Brain 11(1):62PubMedPubMedCentral
10.
Bellingham SA, Guo B, Hill AF (2015) The secret life of extracellular vesicles in metal homeostasis and neurodegeneration. Biol Cell 107(11):389–418PubMed
11.
D'Ambrosi N, Rossi L (2015) Copper at synapse: release, binding and modulation of neurotransmission. Neurochem Int 90:36–45PubMed
12.
Gasperini L, Meneghetti E, Pastore B, Benetti F, Legname G (2015) Prion protein and copper cooperatively protect neurons by modulating NMDA receptor through S-nitrosylation. Antioxid Redox Signal 22(9):772–784PubMedPubMedCentral
13.
Manto M (2014) Abnormal copper homeostasis: mechanisms and roles in neurodegeneration. Toxics. 2(2):327–345
14.
Hodgson EK, Fridovich I (1975) Interaction of bovine erythrocyte superoxide dismutase with hydrogen peroxide. Inactivation of the enzyme. Biochemistry 14(24):5294–5299PubMed
15.
Sinet P-M, Garber P (1981) Inactivation of the human CuZn superoxide dismutase during exposure to O2− and H2O2. Arch Biochem Biophys 212(2):411–416PubMed
16.
Blech DM, Borders CL (1983) Hydroperoxide anion, HO2−, is an affinity reagent for the inactivation of yeast Cu,Zn superoxide dismutase: modification of one histidine per subunit. Arch Biochem Biophys 224(2):579–586PubMed
17.
Borders CL, Fridovich I (1985) A comparison of the effects of cyanide, hydrogen peroxide, and phenylglyoxal on eucaryotic and procaryotic Cu,Zn superoxide dismutases. Arch Biochem Biophys 241(2):472–476PubMed
18.
Yim MB, Chock PB, Stadtman ER (1993) Enzyme function of copper, zinc superoxide dismutase as a free radical generator. J Biol Chem 268(6):4099–4105PubMed
19.
Harris ED (1983) Chapter 3 - Copper in human and animal health**. In: Rose J (ed) Acknowledgement: Funding for this review was provided by USPHS Grant AM-26604 from the National Institutes of Health Bethesda, Maryland. Trace Elements in Health, Butterworth-Heinemann, pp 44–73
20.
Tisato F, Marzano C, Porchia M, Pellei M, Santini C (2010) Copper in diseases and treatments, and copper-based anticancer strategies. Med Res Rev 30(4):708–749PubMed
21.
Basun H, Forssell LG, Wetterberg L, Winblad B (1991) Metals and trace elements in plasma and cerebrospinal fluid in normal aging and Alzheimer's disease. J Neural Transm Park Dis Dement Sect 3(4):231–258PubMed
22.
Lutsenko S, Bhattacharjee A, Hubbard AL (2010) Copper handling machinery of the brain. Metallomics. 2(9):596–608PubMed
23.
Hershey CO, Hershey LA, Varnes A, Vibhakar SD, Lavin P, Strain WH (1983) Cerebrospinal fluid trace element content in dementia: clinical, radiologic, and pathologic correlations. Neurology. 33(10):1350–1353PubMed
24.
Nischwitz V, Berthele A, Michalke B (2008) Speciation analysis of selected metals and determination of their total contents in paired serum and cerebrospinal fluid samples: an approach to investigate the permeability of the human blood-cerebrospinal fluid-barrier. Anal Chim Acta 627(2):258–269PubMed
25.
Aguzzi A, Haass C (2003) Games played by rogue proteins in prion disorders and Alzheimer's disease. Science. 302(5646):814–818PubMed
26.
Kneipp J, Miller LM, Joncic M, Kittel M, Lasch P, Beekes M et al (2003) In situ identification of protein structural changes in prion-infected tissue. Biochim Biophys Acta 1639(3):152–158PubMed
27.
Oppenheim C, Zuber M, Galanaud D, Detilleux M, Bolgert F, Mas JL et al (2004) Spectroscopy and serial diffusion MR findings in hGH-Creutzfeldt-Jakob disease. J Neurol Neurosurg Psychiatry 75(7):1066–1069PubMedPubMedCentral
28.
Cordery RJ, MacManus D, Godbolt A, Rossor MN, Waldman AD (2006) Short TE quantitative proton magnetic resonance spectroscopy in variant Creutzfeldt-Jakob disease. Eur Radiol 16(8):1692–1698PubMed
29.
Vidal C, Meric P, Provost F, Herzog C, Lasmezas C, Gillet B et al (2006) Preclinical metabolic changes in mouse prion diseases detected by 1H-nuclear magnetic resonance spectroscopy. Neuroreport. 17(1):89–93PubMed
30.
Macfarlane RG, Wroe SJ, Collinge J, Yousry TA, Jager HR (2007) Neuroimaging findings in human prion disease. J Neurol Neurosurg Psychiatry 78(7):664–670PubMed
31.
Galanaud D, Haik S, Linguraru MG, Ranjeva JP, Faucheux B, Kaphan E et al (2010) Combined diffusion imaging and MR spectroscopy in the diagnosis of human prion diseases. AJNR Am J Neuroradiol 31(7):1311–1318PubMed
32.
Krasnoslobodtsev AV, Portillo AM, Deckert-Gaudig T, Deckert V, Lyubchenko YL (2010) Nanoimaging for prion related diseases. Prion. 4(4):265–274PubMedPubMedCentral
33.
Lyubchenko YL, Kim BH, Krasnoslobodtsev AV, Yu J (2010) Nanoimaging for protein misfolding diseases. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2(5):526–543PubMed
34.
Letourneau-Guillon L, Wada R, Kucharczyk W (2012) Imaging of prion diseases. J Magn Reson Imaging 35(5):998–1012PubMed
35.
McDade EM, Boeve BF, Fields JA, Kumar N, Rademakers R, Baker MC et al (2013) MRS in early and presymptomatic carriers of a novel octapeptide repeat insertion in the prion protein gene. J Neuroimaging 23(3):409–413PubMed
36.
Ortega-Cubero S, Luquin MR, Dominguez I, Arbizu J, Pagola I, Carmona-Abellan MM et al (2013) Structural and functional neuroimaging in human prion diseases. Neurologia. 28(5):299–308PubMed
37.
Riek R, Hornemann S, Wider G, Billeter M, Glockshuber R, Wuthrich K (1996) NMR structure of the mouse prion protein domain PrP(121-231). Nature. 382(6587):180–182PubMed
38.
Zahn R, Liu A, Luhrs T, Riek R, von Schroetter C, Lopez Garcia F et al (2000) NMR solution structure of the human prion protein. Proc Natl Acad Sci U S A 97(1):145–150PubMedPubMedCentral
39.
Sigurdsson EM, Brown DR, Alim MA, Scholtzova H, Carp R, Meeker HC et al (2003) Copper chelation delays the onset of prion disease. J Biol Chem 278(47):46199–46202PubMed
40.
Meloni G, Faller P, Vašák M (2007) Redox silencing of copper in metal-linked neurodegenerative disorders reaction of Zn7metallothionein-3 with Cu2+ ions. J Biol Chem 282(22):16068–16078PubMed
41.
Alghrably M, Czaban I, Jaremko Ł, Jaremko M (2019) Interaction of amylin species with transition metals and membranes. J Inorg Biochem 191:69–76PubMed
42.
Dong X, Svantesson T, Sholts SB, Wallin C, Jarvet J, Gräslund A et al (2019) Copper ions induce dityrosine-linked dimers in human but not in murine islet amyloid polypeptide (IAPP/amylin). Biochem Biophys Res Commun 510(4):520–524
43.
Nishida Y (2011) The chemical process of oxidative stress by copper (II) and iron (III) ions in several neurodegenerative disorders. Monatshefte für Chemie-Chemical Monthly 142(4):375–384
44.
Dudzik CG, Walter ED, Millhauser GL (2011) Coordination features and affinity of the Cu2+ site in the α-synuclein protein of Parkinson’s disease. Biochemistry. 50(11):1771–1777PubMedPubMedCentral
45.
Spencer WA, Jeyabalan J, Kichambre S, Gupta RC (2011) Oxidatively generated DNA damage after Cu (II) catalysis of dopamine and related catecholamine neurotransmitters and neurotoxins: role of reactive oxygen species. Free Radic Biol Med 50(1):139–147PubMed
46.
Chan T, Chow AM, Tang DW, Li Q, Wang X, Brown IR et al (2010) Interaction of baicalein and copper with α-synuclein: electrochemical approach to Parkinson’s disease. J Electroanal Chem 648(2):151–155
47.
Lin C-J, Huang H-C, Jiang Z-F (2010) Cu (II) interaction with amyloid-β peptide: a review of neuroactive mechanisms in AD brains. Brain Res Bull 82(5–6):235–242PubMed
48.
Multhaup G (1997) Amyloid precursor protein, copper and Alzheimer's disease. Biomed Pharmacother 51(3):105–111PubMed
49.
Qin K, Yang D-S, Yang Y, Chishti MA, Meng L-J, Kretzschmar HA et al (2000) Copper (II)-induced conformational changes and protease resistance in recombinant and cellular PrP effect of protein age and deamidation. J Biol Chem 275(25):19121–19131PubMed
50.
Lech T, Sadlik J (2007) Copper concentration in body tissues and fluids in normal subjects of southern Poland. Biol Trace Elem Res 118(1):10–15PubMed
51.
Gybina AA, Tkac I, Prohaska JR (2009) Copper deficiency alters the neurochemical profile of developing rat brain. Nutr Neurosci 12(3):114–122PubMedPubMedCentral
52.
Emwas AHM, Al-Talla ZA, Guo X, Al-Ghamdi S, Al-Masri HT (2013) Utilizing NMR and EPR spectroscopy to probe the role of copper in prion diseases. Magn Reson Chem 51(5):255–268PubMed
53.
Uriu-Adams JY, Scherr RE, Lanoue L, Keen CL (2010) Influence of copper on early development: prenatal and postnatal considerations. Biofactors. 36(2):136–152PubMed
54.
Sorrentino G, Bonavita V (2007) Neurodegeneration and Alzheimer's disease: the lesson from tauopathies. Neurol Sci 28(2):63–71PubMed
55.
Kodaka M (2004) Interpretation of concentration-dependence in aggregation kinetics. Biophys Chem 109(2):325–332PubMed
56.
Hedberg YS, Dobryden I, Chaudhary H, Wei Z, Claesson PM, Lendel C (2019) Synergistic effects of metal-induced aggregation of human serum albumin. Colloids Surf B: Biointerfaces 173:751–758PubMed
57.
Yuan Y, Niu F, Liu Y, Lu N (2014) Zinc and its effects on oxidative stress in Alzheimer's disease. Neurol Sci 35(6):923–928PubMed
58.
Tsukita K, Sakamaki-Tsukita H, Tanaka K, Suenaga T, Takahashi R (2019) Value of in vivo alpha-synuclein deposits in Parkinson's disease: a systematic review and meta-analysis. Mov Disord 34(10):1452–1463PubMed
59.
Bernabeu-Zornoza A, Coronel R, Palmer C, Monteagudo M, Zambrano A, Liste I (2019) Physiological and pathological effects of amyloid-beta species in neural stem cell biology. Neural Regen Res 14(12):2035–2042PubMedPubMedCentral
60.
Scheltens P, Blennow K, Breteler MM, de Strooper B, Frisoni GB, Salloway S et al (2016) Alzheimer's disease. Lancet. 388(10043):505–517PubMed
61.
Lippens G, Sillen A, Landrieu I, Amniai L, Sibille N, Barbier P et al (2007) Tau aggregation in Alzheimer's disease: what role for phosphorylation? Prion. 1(1):21–25PubMedPubMedCentral
62.
Alonso AD, Cohen LS, Corbo C, Morozova V, ElIdrissi A, Phillips G et al (2018) Hyperphosphorylation of tau associates with changes in its function beyond microtubule stability. Front Cell Neurosci 12(338)
63.
Zhu Y, Wang J (2015) Wogonin increases β-amyloid clearance and inhibits tau phosphorylation via inhibition of mammalian target of rapamycin: potential drug to treat Alzheimer’s disease. Neurol Sci 36(7):1181–1188PubMed
64.
Crouch PJ, Hung LW, Adlard PA, Cortes M, Lal V, Filiz G et al (2009) Increasing cu bioavailability inhibits Abeta oligomers and tau phosphorylation. Proc Natl Acad Sci U S A 106(2):381–386PubMedPubMedCentral
65.
Zhou LX, Du JT, Zeng ZY, Wu WH, Zhao YF, Kanazawa K et al (2007) Copper (II) modulates in vitro aggregation of a tau peptide. Peptides. 28(11):2229–2234PubMed
66.
Ma Q, Li Y, Du J, Liu H, Kanazawa K, Nemoto T et al (2006) Copper binding properties of a tau peptide associated with Alzheimer's disease studied by CD, NMR, and MALDI-TOF MS. Peptides. 27(4):841–849PubMed
67.
Soragni A, Zambelli B, Mukrasch MD, Biernat J, Jeganathan S, Griesinger C et al (2008) Structural characterization of binding of Cu (II) to tau protein. Biochemistry. 47(41):10841–10851PubMed
68.
Voss K, Harris C, Ralle M, Duffy M, Murchison C, Quinn JF (2014) Modulation of tau phosphorylation by environmental copper. Transl Neurodegener 3(1):24PubMedPubMedCentral
69.
Poulson BG, Szczepski K, Lachowicz JI, Jaremko L, Emwas A-H, Jaremko M (2020) Aggregation of biologically important peptides and proteins: inhibition or acceleration depending on protein and metal ion concentrations. RSC Adv 10(1):215–227
70.
Ueda K, Fukushima H, Masliah E, Xia Y, Iwai A, Yoshimoto M et al (1993) Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc Natl Acad Sci U S A 90(23):11282–11286PubMedPubMedCentral
71.
72.
Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M (1997) Alpha-synuclein in Lewy bodies. Nature. 388(6645):839–840PubMed
73.
Spillantini MG, Crowther RA, Jakes R, Hasegawa M, Goedert M (1998) Alpha-synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with lewy bodies. Proc Natl Acad Sci U S A 95(11):6469–6473PubMedPubMedCentral
74.
Bougea A, Stefanis L, Paraskevas GP, Emmanouilidou E, Vekrelis K, Kapaki E (2019) Plasma alpha-synuclein levels in patients with Parkinson's disease: a systematic review and meta-analysis. Neurol Sci 40(5):929–938PubMed
75.
Ghosh D, Mehra S, Sahay S, Singh PK, Maji SK (2017) Alpha-synuclein aggregation and its modulation. Int J Biol Macromol 100:37–54PubMed
76.
Breydo L, Wu JW, Uversky VN (2012) Alpha-synuclein misfolding and Parkinson's disease. Biochim Biophys Acta 1822(2):261–285PubMed
77.
Pall HS, Williams AC, Blake DR, Lunec J, Gutteridge JM, Hall M et al (1987) Raised cerebrospinal-fluid copper concentration in Parkinson's disease. Lancet. 2(8553):238–241PubMed
78.
Rasia RM, Bertoncini CW, Marsh D, Hoyer W, Cherny D, Zweckstetter M et al (2005) Structural characterization of copper (II) binding to alpha-synuclein: insights into the bioinorganic chemistry of Parkinson's disease. Proc Natl Acad Sci U S A 102(12):4294–4299PubMedPubMedCentral
79.
Valensin D, Dell'Acqua S, Kozlowski H, Casella L (2016) Coordination and redox properties of copper interaction with alpha-synuclein. J Inorg Biochem 163:292–300PubMed
80.
Bloch DN, Kolkowska P, Tessari I, Baratto MC, Sinicropi A, Bubacco L et al (2019) Fibrils of alpha-Synuclein abolish the affinity of Cu(2+)-binding site to His50 and induce hopping of Cu(2+) ions in the termini. Inorg Chem 58(16):10920–10927PubMed
81.
Koppenol WH (2001) The Haber-Weiss cycle–70 years later. Redox Rep 6(4):229–234PubMed
82.
Barb W, Baxendale J, George P, Hargrave K (1951) Reactions of ferrous and ferric ions with hydrogen peroxide. Part I.—the ferrous ion reaction. Trans Faraday Soc 47:462–500
83.
Baruch-Suchodolsky R, Fischer B (2009) Aβ40, either soluble or aggregated, is a remarkably potent antioxidant in cell-free oxidative systems. Biochemistry. 48(20):4354–4370PubMed
84.
Halliwell B, Gutteridge JM (1990) Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol. 186: Elsevier; p. 1–85
85.
Sanchez-Lopez C, Rossetti G, Quintanar L, Carloni P (2018) Structural determinants of the prion protein N-terminus and its adducts with copper ions. Int J Mol Sci 20(1)
86.
Bertini I, Mangani S, Viezzoli M, Sykes A (1998) Advanced inorganic chemistry. Academic, San Diego, pp 127–250
87.
Quintanar L, Rivillas-Acevedo L, Grande-Aztatzi R, Gómez-Castro CZ, Arcos-López T, Vela A (2013) Copper coordination to the prion protein: insights from theoretical studies. Coord Chem Rev 257(2):429–444
88.
Ling Y, Khade RL, Zhang Y (2011) Structural, EPR superhyperfine, and NMR hyperfine properties of the u−octarepeat binding site in the prion protein. J Phys Chem B 115(11):2663–2670PubMed
89.
dos Santos NV, Silva AF, Oliveira VX Jr, Homem-de-Mello P, Cerchiaro G (2012) Copper (II) complexation to 1-octarepeat peptide from a prion protein: insights from theoretical and experimental UV-visible studies. J Inorg Biochem 114:1–7PubMed
90.
Viles JH (2012) Metal ions and amyloid fiber formation in neurodegenerative diseases. Copper, zinc and iron in Alzheimer's, Parkinson's and prion diseases. Coord Chem Rev 256(19–20):2271–2284
91.
Sánchez-López C, Rossetti G, Quintanar L, Carloni P (2019) Structural determinants of the prion protein N-terminus and its adducts with copper ions. Int J Mol Sci 20(1):18
92.
McCord JM, Fridovich I (1969) Superoxide dismutase. J Biol Chem 244(22):6049–6055PubMed
93.
Fee JA, Gaber BP (1972) Anion binding to bovine erythrocyte superoxide dismutase. J Biol Chem 247(1):60–65PubMed
94.
White AR, Multhaup G, Maher F, Bellingham S, Camakaris J, Zheng H et al (1999) The Alzheimer's disease amyloid precursor protein modulates copper-induced toxicity and oxidative stress in primary neuronal cultures. J Neurosci 19(21):9170–9179PubMedPubMedCentral
95.
Bush AI, Pettingell W, De Paradis M, Tanzi RE, Wasco W (1994) The amyloid beta-protein precursor and its mammalian homologues. Evidence for a zinc-modulated heparin-binding superfamily. J Biol Chem 269(43):26618–26621PubMed
96.
Simons A, Ruppert T, Schmidt C, Schlicksupp A, Pipkorn R, Reed J et al (2002) Evidence for a copper-binding superfamily of the amyloid precursor protein. Biochemistry. 41(30):9310–9320PubMed
97.
Requena JR, Groth D, Legname G, Stadtman ER, Prusiner SB, Levine RL (2001) Copper-catalyzed oxidation of the recombinant SHa (29–231) prion protein. Proc Natl Acad Sci 98(13):7170–7175PubMed
98.
Hornshaw M, McDermott J, Candy J, Lakey J (1995) 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):993–999PubMed
99.
Brown DR, Qin K, Herms JW, Madlung A, Manson J, Strome R et al (1997) The cellular prion protein binds copper in vivo. Nature. 390(6661):684PubMed
100.
Hornshaw M, McDermott J, Candy J (1995) Copper binding to the N-terminal tandem repeat regions of mammalian and avian prion protein. Biochem Biophys Res Commun 207(2):621–629PubMed
101.
Serra A, Manno D, Filippo E, Buccolieri A, Urso E, Rizzello A et al (2011) SERS based optical sensor to detect prion protein in neurodegenerate living cells. Sensors Actuators B Chem 156(1):479–485
102.
Kállay C, Turi I, Timári S, Nagy Z, Sanna D, Pappalardo G et al (2011) The effect of point mutations on copper (II) complexes with peptide fragments encompassing the 106–114 region of human prion protein. Monatshefte für Chemie-Chemical Monthly 142(4):411–419
103.
Hong L, Simon JD (2011) Insights into the thermodynamics of copper association with amyloid-β, α-synuclein and prion proteins. Metallomics. 3(3):262–266PubMed
104.
Chaves JA, Sanchez-López C, Gomes MP, Sisnande T, Macedo B, de Oliveira VE et al (2014) Biophysical and morphological studies on the dual interaction of non-octarepeat prion protein peptides with copper and nucleic acids. JBIC J Biol Inorg Chem 19(6):839–851PubMed
105.
Evans EGB (2015) Copper and zinc drive inter-domain structure in the cellular prion protein: UC Santa Cruz
106.
Cereghetti GM, Negro A, Vinck E, Massimino ML, Sorgato MC, Van Doorslaer S (2004) Copper (II) binding to the human Doppel protein may mark its functional diversity from the prion protein. J Biol Chem 279(35):36497–36503PubMed
107.
Giese A, Buchholz M, Herms J, Kretzschmar HA (2005) Mouse brain synaptosomes accumulate copper-67 efficiently by two distinct processes independent of cellular prion protein. J Mol Neurosci 27(3):347–354PubMed
108.
Hijazi N, Shaked Y, Rosenmann H, Ben-Hur T, Gabizon R (2003) Copper binding to PrPC may inhibit prion disease propagation. Brain Res 993(1–2):192–200PubMed
109.
Kourie J, Kenna B, Tew D, Jobling MF, Curtain C, Masters C et al (2003) Copper modulation of ion channels of PrP [106–126] mutant prion peptide fragments. J Membr Biol 193(1):35–45PubMed
110.
Li A, Dong J, Harris DA (2004) Cell surface expression of the prion protein in yeast does not alter copper utilization phenotypes. J Biol Chem 279(28):29469–29477PubMed
111.
112.
Rachidi W, Mangé A, Senator A, Guiraud P, Riondel J, Benboubetra M et al (2003) Prion infection impairs copper binding of cultured cells. J Biol Chem 278(17):14595–14598PubMed
113.
Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A et al (1997) Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science 276(5321):2045–2047PubMed
114.
Miura T, Hori-i A, Takeuchi H (1996) Metal-dependent [alpha]-helix formation promoted by the glycine-rich octapeptide region of prion protein. FEBS Lett 396(2–3):248–252PubMed
115.
Stöckel J, Safar J, Wallace AC, Cohen FE, Prusiner SB (1998) Prion protein selectively binds copper (II) ions. Biochemistry. 37(20):7185–7193PubMed
116.
Zheng Z, Zhang M, Wang Y, Ma R, Guo C, Feng L et al (2018) Structural basis for the complete resistance of the human prion protein mutant G127V to prion disease. Sci Rep 8(1):13211PubMedPubMedCentral
117.
Alahmari F, Dey S, Emwas A-H, Davaasuren B, Rothenberger A (2019) Layered copper thioaluminate K2Cu3AlS4: synthesis, crystal structure, characterization and solid-state 27Al and 39K NMR studies. J Alloys Compd 776:1041–1047
118.
Alahmari F, Davaasuren B, Emwas A-H, Costa PMFJ, Rothenberger A (2019) Tris (ethylenediamine) nickel (II) thio-hydroxogermanate monohydrate: synthesis, crystal structure, 1H NMR, EPR, optical and magnetic properties. Inorg Chim Acta 488:145–151
119.
Brown DR (2001) Copper and prion disease. Brain Res Bull 55(2):165–173PubMed
120.
Davaasuren B, Emwas A-H, Rothenberger A (2017) MAu2GeS4-Chalcogel (M = Co, Ni): heterogeneous intra- and intermolecular hydroamination catalysts. Inorg Chem 56(16):9609–9616PubMed
121.
Emwas A-H, Roy R, McKay RT, Tenori L, Saccenti E, Gowda GAN et al (2019) NMR spectroscopy for metabolomics research. Metabolites. 9(7):123PubMedCentral
122.
Toni M, Massimino ML, Griffoni C, Salvato B, Tomasi V, Spisni E (2005) Extracellular copper ions regulate cellular prion protein (PrPC) expression and metabolism in neuronal cells. FEBS Lett 579(3):741–744PubMed
123.
Mattar SM, Emwas AH, Calhoun LA (2004) Spectroscopic studies of the intermediates in the conversion of 1, 4, 11, 12-tetrahydro-9, 10-anthraquinone to 9, 10-anthraquinone by reaction with oxygen under basic conditions. J Phys Chem A 108(52):11545–11553
124.
Ellegood J, McKay RT, Hanstock CC, Beaulieu C (2007) Anisotropic diffusion of metabolites in peripheral nerve using diffusion weighted magnetic resonance spectroscopy at ultra-high field. J Magn Reson 184(1):20–28PubMed
125.
McKay RT, Saltibus LF, Li MX, Sykes BD (2000) Energetics of the induced structural change in a Ca2+ regulatory protein: Ca2+ and troponin I peptide binding to the E41A mutant of the N-domain of skeletal troponin C. Biochemistry. 39(41):12731–12738PubMed
126.
Amniai L, Barbier P, Sillen A, Wieruszeski J-M, Peyrot V, Lippens G et al (2009) Alzheimer disease specific phosphoepitopes of tau interfere with assembly of tubulin but not binding to microtubules. FASEB J 23(4):1146–1152PubMed
127.
Giustiniani J, Guillemeau K, Dounane O, Sardin E, Huvent I, Schmitt A et al (2015) The FK506-binding protein FKBP52 in vitro induces aggregation of truncated tau forms with prion-like behavior. FASEB J 29(8):3171–3181PubMed
128.
Abdul Jameel AG, Van Oudenhoven V, Emwas A-H, Sarathy SM (2018) Predicting octane number using nuclear magnetic resonance spectroscopy and artificial neural networks. Energy Fuel 32(5):6309–6329
129.
Alahmari F, Davaasuren B, Emwas A-H, Rothenberger A (2018) Thioaluminogermanate M (AlS2)(GeS2) 4 (M= Na, Ag, Cu): synthesis, crystal structures, characterization, ion-exchange and solid-state 27Al and 23Na NMR spectroscopy. Inorg Chem 57(7):3713–3719PubMed
130.
Batool F, Parveen S, Emwas A-H, Sioud S, Gao X, Munawar MA et al (2015) Synthesis of fluoroalkoxy substituted arylboronic esters by iridium-catalyzed aromatic C-H borylation. Org Lett 17(17):4256–4259PubMed
131.
Alahmari F, Dey S, Emwas A-H, Davaasuren B, Rothenberger A (2019) Ultra-low thermal conductivity in Na/Sb chalcobismuthates: synthesis, crystal structures, optical properties and 23Na NMR spectroscopy. New J Chem 43(27):10814–10820
132.
Medina SC, Farinha ASF, Emwas A-H, Tabatabai A, Leiknes T (2020) A fundamental study of adsorption kinetics of surfactants onto metal oxides using quartz crystal microbalance with dissipation (QCM-D). Colloids Surf A Physicochem Eng Asp 586:124237
133.
Alkordi MH, Haikal RR, Hassan YS, Emwas A-H, Belmabkhout Y (2015) Poly-functional porous-organic polymers to access functionality–CO 2 sorption energetic relationships. J Mater Chem A 3(45):22584–22590
134.
Atiqullah M, Al-Harthi MA, Anantawaraskul S, Emwas A-HM (2015) Ethylene homo-and copolymerization chain-transfers: a perspective from supported (nBuCp) 2ZrCl2 catalyst active Centre distribution. J Chem Sci 127(4):717–728
135.
Chisca S, Duong P, Emwas A-H, Sougrat R, Nunes SP (2015) Crosslinked copolyazoles with a zwitterionic structure for organic solvent resistant membranes. Polym Chem 6(4):543–554
136.
Bahuleyan BK, De Kumar S, Sarath PU, Furquan SA, Masihullah JK, Emwas AH et al (2012) Effect of aluminium nitride on the properties of polyethylene obtained by in situ polymerization using Ni (II) diimine complex. Macromol Res 20(7):772–775
137.
Liu Z, Dong X, Zhu Y, Emwas A-H, Zhang D, Tian Q et al (2015) Investigating the influence of mesoporosity in zeolite beta on its catalytic performance for the conversion of methanol to hydrocarbons. ACS Catal 5(10):5837–5845
138.
Alezi D, Belmabkhout Y, Suyetin M, Bhatt PM, Weseliński ŁJ, Solovyeva V et al (2015) MOF crystal chemistry paving the way to gas storage needs: aluminum-based soc-MOF for CH4, O2, and CO2 storage. J Am Chem Soc 137(41):13308–13318PubMedPubMedCentral
139.
Al-Bloushi M, Davaasuren B, Emwas AH, Rothenberger A (2015) Synthesis and characterization of the quaternary thioaluminogermanates A (AlS2)(GeS2)(A= Na, K). Z Anorg Allg Chem 641(7):1352–1356
140.
Caro JA, Wand AJ (2018) Practical aspects of high-pressure NMR spectroscopy and its applications in protein biophysics and structural biology. Methods. 148:67–80PubMedPubMedCentral
141.
Matlahov I, van der Wel PCA (2018) Hidden motions and motion-induced invisibility: dynamics-based spectral editing in solid-state NMR. Methods 148:123–135
142.
Quinn CM, Polenova T (2017) Structural biology of supramolecular assemblies by magic-angle spinning NMR spectroscopy. Q Rev Biophys 50
143.
Yadav DK, Lukavsky PJ (2016) NMR solution structure determination of large RNA-protein complexes. Prog Nucl Magn Reson Spectrosc 97:57–81PubMed
144.
Bechmann M, Mueller N (2017) Nonlinear effects in NMR. Annual Reports on NMR Spectroscopy. 92: Elsevier; p. 199–226
145.
Bian J, Jiang M, Cui J, Liu X, Chen B, Ji Y et al (2017) Universal quantum control in zero-field nuclear magnetic resonance. Phys Rev A 95(5):052342
146.
Fundo JF, Galvis-Sanchez A, Madureira AR, Carvalho A, Feio G, Silva CL et al (2016) NMR water transverse relaxation time approach to understand storage stability of fresh-cut ‘Rocha’pear. LWT. 74:280–285
147.
Ilc G, Giachin G, Jaremko M, Jaremko L, Benetti F, Plavec J et al (2010) NMR structure of the human prion protein with the pathological Q212P mutation reveals unique structural features. PLoS One 5(7):e11715PubMedPubMedCentral
148.
Larda ST, Simonetti K, Al-Abdul-Wahid MS, Sharpe S, Prosser RS (2013) Dynamic equilibria between monomeric and oligomeric misfolded states of the mammalian prion protein measured by 19F NMR. J Am Chem Soc 135(28):10533–10541PubMed
149.
Mead S (2019) Prion diseases and possible treatments. J Neurol Sci 405:70
150.
Fremuntova Z, Mosko T, Soukup J, Kucerova J, Kostelanska M, Hanusova ZB et al (2020) Changes in cellular prion protein expression, processing and localisation during differentiation of the neuronal cell line CAD 5. Biol Cell 112(1):1–21PubMed
151.
Geissen M, Krasemann S, Matschke J, Glatzel M (2007) Understanding the natural variability of prion diseases. Vaccine. 25(30):5631–5636PubMed
152.
Fernandez-Borges N, Erana H, Venegas V, Elezgarai SR, Harrathi C, Castilla J (2015) Animal models for prion-like diseases. Virus Res 207:5–24PubMed
153.
Geschwind MD (2015) Prion diseases. Continuum (Minneapolis, Minn) 21(6 Neuroinfectious Disease):1612–1638
154.
Huang WJ, Chen WW, Zhang X (2015) Prions mediated neurodegenerative disorders. Eur Rev Med Pharmacol Sci 19(21):4028–4034PubMed
155.
Lukic A, Uphill J, Brown CA, Beck J, Poulter M, Campbell T et al (2015) Rare structural genetic variation in human prion diseases. Neurobiol Aging 36(5):2004.e1–2004.e8
156.
Nhat Tran Thanh L, Narkiewicz J, Aulic S, Salzano G, Hoa Thanh T, Scaini D et al (2015) Synthetic prions and other human neurodegenerative proteinopathies. Virus Res 207:25–37
157.
Marandi Y, Farahi N, Sadeghi A, Sadeghi-Hashjin G (2012) Prion diseases - current theories and potential therapies: a brief review. Folia Neuropathol 50(1):46–49PubMed
158.
Norrby E (2011) Prions and protein-folding diseases. J Intern Med 270(1):1–14PubMed
159.
Sikorska B, Liberski PP (2012) Human prion diseases: from Kuru to variant Creutzfeldt-Jakob disease. Subcell Biochem 65:457–496PubMed
160.
Solomon IH, Biasini E, Harris DA (2012) Ion channels induced by the prion protein mediators of neurotoxicity. Prion. 6(1):40–45PubMedPubMedCentral
161.
Syed M, Nourizadeh-Lillabadi R, Press CM, Alestrom P (2011) Prion protein function and the disturbance of early embryonic development in zebrafish. Prion. 5(2):88–92PubMedPubMedCentral
162.
Akhvlediani T, Gochitashvili N, Tsertsvadze T (2007) Prion diseases--mysterious persistent infections. Georgian Med News 146:38–42
163.
Fornai F, Ferrucci M, Gesi M, di Poggio AB, Giorgi FS, Biagioni F et al (2006) A hypothesis on prion disorders: are infectious, inherited, and sporadic causes so distinct? Brain Res Bull 69(2):95–100PubMed
164.
Ironside JW. Human prion diseases: biology and transmission by blood. In: Mayr WR, editor. Isbt Science Series, Vol 1, No 1: State of the Art Presentations. ISBT Science Series. 12006. p. 15–20
165.
Ironside JW, Ritchie DL, Head MW (2005) Phenotypic variability in human prion diseases. Neuropathol Appl Neurobiol 31(6):565–579PubMed
166.
Rachidi W, Riondel J, McMahon HM, Favier A (2005) Prion protein and copper: a mysterious relationship. Pathol Biol 53(4):244–250PubMed
167.
Sakudo A, Onodera T (2011) Tissue- and cell type-specific modification of prion protein (PrP)-like protein Doppel, which affects PrP endoproteolysis. Biochem Biophys Res Commun 404(1):523–527PubMed
168.
Figini M, Alexander DC, Redaelli V, Fasano F, Grisoli M, Baselli G et al (2015) Mathematical models for the diffusion magnetic resonance signal abnormality in patients with prion diseases. NeuroImage Clinical 7:142–154PubMed
169.
Krakauer DC, Zanotto PMD, Pagel M (1998) Prion's progress: patterns and rates of molecular evolution in relation to spongiform disease. J Mol Evol 47(2):133–145PubMed
170.
Lodi R, Parchi P, Tonon C, Manners D, Capellari S, Strammiello R et al (2009) Magnetic resonance diagnostic markers in clinically sporadic prion disease: a combined brain magnetic resonance imaging and spectroscopy study. Brain. 132:2669–2679PubMedPubMedCentral
171.
Tranchant C, Geranton L, Guiraud-Chaumeil C, Mohr M, Warter JM (1999) Basis of phenotypic variability in sporadic Creutzfeldt-Jakob disease. Neurology. 52(6):1244–1249PubMed
172.
Collins SJ, Lawson VA, Masters CL (2004) Transmissible spongiform encephalopathies. Lancet. 363(9402):51–61PubMed
173.
Edskes HK, Wickner RB (2004) Transmissible spongiform encephalopathies - prion proof in progress. Nature. 430(7003):977–979PubMed
174.
Basset-Leobon C, Uro-Coste E, Peoc'h K, Haik S, Sazdovitch V, Rigal M et al (2006) Familial Creutzfeldt-Jakob disease with an R208H-129V haplotype and Kuru plaques. Arch Neurol 63(3):449–452PubMed
175.
Giles K, Olson SH, Prusiner SB (2017) Developing therapeutics for PrP prion diseases. Cold Spring Harbor perspectives in medicine 7(4):a023747PubMedPubMedCentral
176.
Mead S, Whitfield J, Poulter M, Shah P, Uphill J, Campbell T et al (2009) A novel protective prion protein variant that colocalizes with Kuru exposure. N Engl J Med 361(21):2056–2065PubMed
177.
Stewart LA, Rydzewska LH, Keogh GF, Knight RS (2008) Systematic review of therapeutic interventions in human prion disease. Neurology. 70(15):1272–1281PubMed
178.
Mancuso M, Siciliano G, Capellari S, Orsucci D, Moretti P, Di Fede G et al (2009) Creutzfeldt-Jakob disease with E200K PRNP mutation: a case report and revision of the literature. Neurol Sci 30(5):417–420PubMed
179.
Bilandžić N, Đokić M, Sedak M, Varenina I, Kolanović BS, Oraić D et al (2012) Determination of copper in food of animal origin and fish in Croatia. Food Control 27(2):284–288
180.
Bandmann O, Weiss KH, Kaler SG (2015) Wilson's disease and other neurological copper disorders. Lancet Neurol 14(1):103–113PubMedPubMedCentral
181.
Zheng W, Monnot AD (2012) Regulation of brain iron and copper homeostasis by brain barrier systems: implication in neurodegenerative diseases. Pharmacol Ther 133(2):177–188PubMed
182.
Hart E, Steenbock H, Waddell J, Elvehjem C, Van Donk E, Riising BM (2001) Iron in nutrition: VII. Copper as a supplement to iron for hemoglobin building in the rat (Reprinted from Journal of Biological Chemistry, vol 77, pg 797-812, 1928). J Trace Elem Exp Med 14(2):195–206
183.
Kozlowski H, Luczkowski M, Remelli M, Valensin D (2012) Copper, zinc and iron in neurodegenerative diseases (Alzheimer's, Parkinson's and prion diseases). Coord Chem Rev 256(19–20):2129–2141
184.
Prohaska JR, Bailey WR (1994) Regional specificity in alterations of rat brain copper and catecholamines following perinatal copper deficiency. J Neurochem 63(4):1551–1557PubMed
185.
Singh N, Das D, Singh A, Mohan ML (2010) Prion protein and metal interaction: physiological and pathological implications. Curr Issues Mol Biol 12(2):99PubMed
186.
Yen C-F, Harischandra DS, Kanthasamy A, Sivasankar S (2016) Copper-induced structural conversion templates prion protein oligomerization and neurotoxicity. Sci Adv 2(7):e1600014PubMedPubMedCentral
187.
Scheiber IF, Mercer JF, Dringen R (2014) Metabolism and functions of copper in brain. Prog Neurobiol 116:33–57PubMed
188.
Brazier MW, Volitakis I, Kvasnicka M, White AR, Underwood JR, Green JE et al (2010) Manganese chelation therapy extends survival in a mouse model of M1000 prion disease. J Neurochem 114(2):440–451PubMed
189.
De Gregorio G, Biasotto F, Hecel A, Luczkowski M, Kozlowski H, Valensin D (2019) Structural analysis of copper (I) interaction with amyloid β peptide. J Inorg Biochem
190.
Strausak D, Mercer JF, Dieter HH, Stremmel W, Multhaup G (2001) Copper in disorders with neurological symptoms: Alzheimer’s, Menkes, and Wilson diseases. Brain Res Bull 55(2):175–185PubMed
191.
Rivera-Mancía S, Pérez-Neri I, Ríos C, Tristán-López L, Rivera-Espinosa L, Montes S (2010) The transition metals copper and iron in neurodegenerative diseases. Chem Biol Interact 186(2):184–199PubMed
192.
Bolognin S, Drago D, Messori L, Zatta P (2009) Chelation therapy for neurodegenerative diseases. Med Res Rev 29(4):547–570PubMed
193.
Slivarichová D, Mitrová E, Ursínyová M, Uhnáková I, Koscová S, Wsólová L (2011) Geographic accumulation of Creutzfeldt-Jakob disease in Slovakia-environmental metal imbalance as a possible cofactor. Cent Eur J Public Health 19(3):158PubMed
194.
Mitteregger G, Korte S, Shakarami M, Herms J, Kretzschmar HA (2009) Role of copper and manganese in prion disease progression. Brain Res 1292:155–164PubMed
195.
Hodak M, Chisnell R, Lu W, Bernholc J (2009) Functional implications of multistage copper binding to the prion protein. Proc Natl Acad Sci 106(28):11576–11581PubMed
196.
Desai V, Kaler SG (2008) Role of copper in human neurological disorders. Am J Clin Nutr 88(3):855S–858SPubMed
197.
Viles JH, Klewpatinond M, Nadal RC (2008) Copper and the structural biology of the prion protein. Portland Press Limited
198.
Varela-Nallar L, González A, Inestrosa NC (2006) Role of copper in prion diseases: deleterious or beneficial? Curr Pharm Des 12(20):2587–2595PubMed
199.
Quaglio E, Chiesa R, Harris DA (2001) Copper converts the cellular prion protein into a protease-resistant species that is distinct from the scrapie isoform. J Biol Chem 276(14):11432–11438PubMed
200.
Prince RC, Gunson DE (1998) Prions are copper-binding proteins. Trends Biochem Sci 23(6):197–198PubMed
201.
Yamamoto N, Kuwata K (2009) Difference in redox behaviors between copper-binding octarepeat and nonoctarepeat sites in prion protein. JBIC J Biol Inorg Chem 14(8):1209–1218PubMed
202.
Giachin G, Mai PT, Tran TH, Salzano G, Benetti F, Migliorati V et al (2015) The non-octarepeat copper binding site of the prion protein is a key regulator of prion conversion. Sci Rep 5:15253PubMedPubMedCentral
203.
O'Sullivan J, Comerford E, Rachidi W, Scott M, Hooper NM, McMahon HE (2015) The effects of the cellular and infectious prion protein on the neuronal adaptor protein X11α. Biochim Biophys Acta Gen Subj 1850(11):2213–2221
204.
Bocharova OV, Breydo L, Salnikov VV, Baskakov IV (2005) Copper (II) inhibits in vitro conversion of prion protein into amyloid fibrils. Biochemistry. 44(18):6776–6787PubMed
205.
Giese A, Levin J, Bertsch U, Kretzschmar H (2004) Effect of metal ions on de novo aggregation of full-length prion protein. Biochem Biophys Res Commun 320(4):1240–1246PubMed
206.
Kjaergaard CH, Jones SM, Gounel SB, Mano N, Solomon EI (2015) Two-electron reduction versus one-electron oxidation of the type 3 pair in the multicopper oxidases. J Am Chem Soc 137(27):8783–8794PubMedPubMedCentral
207.
Serrano-Plana J, Garcia-Bosch I, Company A, Costas M (2015) Structural and reactivity models for copper oxygenases: cooperative effects and novel reactivities. Acc Chem Res 48(8):2397–2406PubMed
208.
Arnesano F, Banci L, Bertini I, Mangani S, Thompsett AR (2003) A redox switch in CopC: an intriguing copper trafficking protein that binds copper (I) and copper (II) at different sites. Proc Natl Acad Sci 100(7):3814–3819PubMed
209.
Artés JM, López-Martínez M, Díez-Pérez I, Sanz F, Gorostiza P (2014) Conductance switching in single wired redox proteins. Small. 10(13):2537–2541PubMed
210.
Hepel M, Stobiecka M, Peachey J, Miller J (2012) Intervention of glutathione in pre-mutagenic catechol-mediated DNA damage in the presence of copper (II) ions. Mutat Res Fundam Mol Mech Mutagen 735(1–2):1–11
211.
Gutiérrez AGP, Zeitouny J, Gomila A, Douziech B, Cosquer N, Conan F et al (2014) Insights into water coordination associated with the Cu II/Cu I electron transfer at a biomimetic Cu centre. Dalton Trans 43(17):6436–6445
212.
K-i S, Maeshima H, Yoshida H, Satsuma A, Hattori T (2000) Spectroscopic characterisation of Cu–Al 2 O 3 catalysts for selective catalytic reduction of NO with propene. Phys Chem Chem Phys 2(10):2435–2439
213.
Collery P, Maymard I, Theophanides T, Khassanova L, Collery T, Collery P, et al. Metal ions in biology and medicine, Vol 10. Metal Ions in Biology and Medicine, Vol 10. Metal Ions in Biology and Medicine. 102008
214.
Roat-Malone RM, Roat-Malone RM. Bioinorganic chemistry: a short course2002. i-xvii, 1–348 p
215.
Brewer GJ (2009) Risks of copper and iron toxicity during aging in humans. Chem Res Toxicol 23(2):319–326
216.
Abuhijleh AL, Ali HA, Emwas A-H (2009) Synthesis, spectral and structural characterization of dinuclear rhodium (II) complexes of the anticonvulsant drug valproate with theophylline and caffeine. J Organomet Chem 694(22):3590–3596
217.
Nageeb A, Al-Tawashi A, Mohammad Emwas A-H, Abdel-Halim Al-Talla Z, Al-Rifai N (2013) Comparison of artemisia annua bioactivities between traditional medicine and chemical extracts. Curr Bioact Compd 9(4):324–332PubMedPubMedCentral
218.
Al-Talla Z, Akrawi SH, Emwas A (2011) Solid state NMR and bioequivalence comparison of the pharmacokinetic parameters of two formulations of clindamycin. Int J Clin Pharmacol Ther 49(7):469–476PubMed
219.
Chu S, Maltsev S, Emwas A-H, Lorigan GA (2010) Solid-state NMR paramagnetic relaxation enhancement immersion depth studies in phospholipid bilayers. J Magn Reson 207(1):89–94PubMedPubMedCentral
220.
Jackson MD, Chae SR, Mulcahy SR, Meral C, Taylor R, Li P et al (2013) Unlocking the secrets of Al-tobermorite in Roman seawater concrete. Am Mineral 98(10):1669–1687
221.
Jackson MD, Moon J, Gotti E, Taylor R, Chae SR, Kunz M et al (2013) Material and elastic properties of Al-tobermorite in ancient Roman seawater concrete. J Am Ceram Soc 96(8):2598–2606
222.
Mroue KH, Emwas A-HM, Power WP (2010) Solid-state 27Al nuclear magnetic resonance investigation of three aluminum-centered dyes. Can J Chem 88(2):111–123
223.
Bouhrara M, Ranga C, Fihri A, Shaikh RR, Sarawade P, Emwas A-H et al (2013) Nitridated fibrous silica (KCC-1) as a sustainable solid base nanocatalyst. ACS Sustain Chem Eng 1(9):1192–1199
224.
Sahloul N, Emwas A, Power W, Penlidis A (2005) Ethyl acrylate-hydroxyethyl acrylate and hydroxyethyl acrylate-methacrylic acid: reactivity ratio estimation from cross-linked polymer using high resolution magic angle spinning spectroscopy. J Macromol Sci Pure Appl Chem A42(10):1369–1385
225.
Atiqullah M, Winston M, Bercaw J, Hussain I, Fazal A, Al-Harthi M et al (2012) Effects of a vanadium post-metallocene catalyst-induced polymer backbone inhomogeneity on UV oxidative degradation of the resulting polyethylene film. Polym Degrad Stab 97(7):1164–1177
226.
Karbach FF, Macko T, Duchateau R (2016) Preparation of ethylene/1-hexene copolymers from ethylene using a fully silica-supported tandem catalyst system. Macromolecules. 49(4):1229–1241
227.
Kirchheim A, Dal Molin D, Fischer P, Emwas A-H, Provis JL, Monteiro PJM (2011) Real-time high-resolution X-ray imaging and nuclear magnetic resonance study of the hydration of pure and Na-doped C3A in the presence of sulfates. Inorg Chem 50(4):1203–1212PubMed
228.
Emwas A-H, Luchinat C, Turano P, Tenori L, Roy R, Salek RM et al (2015) Standardizing the experimental conditions for using urine in NMR-based metabolomic studies with a particular focus on diagnostic studies: a review. Metabolomics. 11(4):872–894PubMed
229.
Asghar S, Shahzadi T, Alazmi M, Gao X, Emwas A-H, Saleem RS et al (2018) Iridium-catalyzed regioselective borylation of substituted biaryls. Synthesis. 50(11):2211–2220
230.
Jameel AGA, Naser N, Issayev G, Touitou J, Ghosh MK, Emwas A-H et al (2018) A minimalist functional group (MFG) approach for surrogate fuel formulation. Combust Flame 192:250–271
231.
Fine M, Cinar M, Voolstra CR, Safa A, Rinkevich B, Laffoley D et al (2019) Coral reefs of the Red Sea—challenges and potential solutions. Reg Stud Mar Sci 25:100498
232.
Omar H, Moosa B, Alamoudi K, Anjum DH, Emwas A-H, El Tall O et al (2018) Impact of pore–walls ligand assembly on the biodegradation of mesoporous Organosilica nanoparticles for controlled drug delivery. ACS Omega 3(5):5195–5201PubMedPubMedCentral
233.
Yang P, Alsufyani M, Emwas AH, Chen C, Khashab NM (2018) Lewis acid guests in a {P8W48} archetypal polyoxotungstate host: enhanced proton conductivity via metal-oxo cluster within cluster assemblies. Angew Chem Int Ed 57(40):13046–13051
234.
Li S, Winters H, Jeong S, Emwas A-H, Vigneswaran S, Amy GL (2016) Marine bacterial transparent exopolymer particles (TEP) and TEP precursors: characterization and RO fouling potential. Desalination. 379:68–74
235.
Li S, Winters H, Villacorte L, Ekowati Y, Emwas A-H, Kennedy M et al (2015) Compositional similarities and differences between transparent exopolymer particles (TEPs) from two marine bacteria and two marine algae: significance to surface biofouling. Mar Chem 174:131–140
236.
Linenberger KJ, Emwas A-H, Peat I, Lorigan GA, Bretz SL, editors. Using NMR to determine the structure of a peptide: an inquiry approach for an upper level undergraduate laboratory. ABSTRACTS OF PAPERS OF THE AMERICAN CHEMICAL SOCIETY; 2009: AMER CHEMICAL SOC 1155 16TH ST, NW, WASHINGTON, DC 20036 USA
237.
Das SK, Xu S, Emwas A-H, Lu YY, Srivastava S, Archer LA (2012) High energy lithium–oxygen batteries–transport barriers and thermodynamics. Energy Environ Sci 5(10):8927–8931
238.
Decken A, Mattar S, Emwas A (2005) 1, 4, 11, 12-Tetrahydro-9, 10-anthraquinone. Acta Crystallogr Sect E: Struct Rep Online 61(3):o641–o6o2
239.
Elbaz AM, Gani A, Hourani N, Emwas A-H, Sarathy SM, Roberts W (2015) TG/DTG, FT-ICR mass spectrometry, and NMR spectroscopy study of heavy fuel oil. Energy Fuel 29(12):7825–7835
240.
Emwas A-HM, Merzaban JS, Serrai H (2015) Theory and applications of NMR-based metabolomics in human disease diagnosis. Applications of NMR Spectroscopy: Elsevier, pp 93–130
241.
Emwas A-HM, Antakly T, Saoudi A-H, Al-Ghamdi S, Serrai H (2015) Magnetic resonance spectroscopy and imaging in breast cancer prognosis and diagnosis. applications of NMR spectroscopy: Volume 3: Elsevier; p. 4–35
242.
Emwas A-H, Saunders M, Ludwig C, Günther U (2008) Determinants for optimal enhancement in ex situ DNP experiments. Appl Magn Reson 34(3–4):483–494
243.
Chiliveri SC, Deshmukh MV (2016) Recent excitements in protein NMR: large proteins and biologically relevant dynamics. J Biosci 41(4):787–803PubMed
244.
Wang Y, Xu J, Wang L, Zhang B, Du W (2010) Interaction of the human prion protein PrP106–126 with metal complexes: potential therapeutic agents against prion disease. Chem Eur J 16(45):13339–13342PubMed
245.
Frederick KK, Michaelis VK, Corzilius B, Ong T-C, Jacavone AC, Griffin RG et al (2015) Sensitivity-enhanced NMR reveals alterations in protein structure by cellular milieus. Cell. 163(3):620–628PubMedPubMedCentral
246.
Wang X, He L, Zhao C, Du W, Lin J (2013) Gold complexes inhibit the aggregation of prion neuropeptides. JBIC J Biol Inorg Chem. 18(7):767–778PubMed
247.
Hecel A, Valensin D, Kozłowski H (2019) How copper ions and membrane environment influence the structure of the human and chicken tandem repeats domain? J Inorg Biochem 191:143–153PubMed
248.
Sandusky P, Raftery D (2005) Use of selective TOCSY NMR experiments for quantifying minor components in complex mixtures: application to the metabonomics of amino acids in honey. Anal Chem 77(8):2455–2463PubMed
249.
Banci L, Bertini I, Cantini F, Felli IC, Gonnelli L, Hadjiliadis N et al (2006) The Atx1-Ccc2 complex is a metal-mediated protein-protein interaction. Nat Chem Biol 2(7):367PubMed
250.
Féraud B, Govaerts B, Verleysen M, De Tullio P (2015) Statistical treatment of 2D NMR COSY spectra in metabolomics: data preparation, clustering-based evaluation of the metabolomic informative content and comparison with 1 H-NMR. Metabolomics. 11(6):1756–1768
251.
Guennec AL, Giraudeau P, Caldarelli S (2014) Evaluation of fast 2D NMR for metabolomics. Anal Chem 86(12):5946–5954PubMed
252.
Tompa P, Fuxreiter M (2008) Fuzzy complexes: polymorphism and structural disorder in protein–protein interactions. Trends Biochem Sci 33(1):2–8PubMed
253.
Becker W, Bhattiprolu KC, Gubensäk N, Zangger K (2018) Investigating protein–ligand interactions by solution nuclear magnetic resonance spectroscopy. ChemPhysChem. 19(8):895–906PubMedPubMedCentral
254.
Skinner AL, Laurence JS (2008) High-field solution NMR spectroscopy as a tool for assessing protein interactions with small molecule ligands. J Pharm Sci 97(11):4670–4695PubMedPubMedCentral
255.
Larsen E, Olivieri C, Walker C, Manu VS, Gao J, Bernlohr D et al (2018) Probing protein-protein interactions using asymmetric labeling and carbonyl-carbon selective heteronuclear NMR spectroscopy. Molecules 23(8):1937PubMedCentral
256.
Cobine PA, McKay RT, Zangger K, Dameron CT, Armitage IM (2004) Solution structure of Cu6 metallothionein from the fungus Neurospora crassa. Eur J Biochem 271(21):4213–4221PubMed
257.
Maret W (2011) Metals on the move: zinc ions in cellular regulation and in the coordination dynamics of zinc proteins. Biometals 24(3):411–418PubMed
258.
Chong LX, Ash M-R, Maher MJ, Hinds MG, Xiao Z, Wedd AG (2009) Unprecedented binding cooperativity between CuI and CuII in the copper resistance protein CopK from Cupriavidus metallidurans CH34: implications from structural studies by NMR spectroscopy and X-ray crystallography. J Am Chem Soc 131(10):3549–3564PubMed
259.
Ou M-H, Chen Y-M, Chang Y-H, Lu W-K, Liu G-C, Wang Y-M (2007) Synthesis, complexation and water exchange properties of Gd (iii)–TTDA-mono and bis (amide) derivatives and their binding affinity to human serum albumin. Dalton Trans 26:2749–2759
260.
Evans EG, Pushie MJ, Markham KA, Lee H-W, Millhauser GL (2016) Interaction between prion protein's copper-bound octarepeat domain and a charged C-terminal pocket suggests a mechanism for N-terminal regulation. Structure. 24(7):1057–1067PubMedPubMedCentral
261.
Narayanan SP, Nair DG, Schaal D, De Aguiar MB, Wenzel S, Kremer W et al (2016) Structural transitions in full-length human prion protein detected by xenon as probe and spin labeling of the N-terminal domain. Sci Rep 6:28419PubMedPubMedCentral
262.
De Ricco R, Potocki S, Kozlowski H, Valensin D (2014) NMR investigations of metal interactions with unstructured soluble protein domains. Coord Chem Rev 269:1–12
263.
O'sullivan DB, Jones CE, Abdelraheim SR, Brazier MW, Toms H, Brown DR et al (2009) Dynamics of a truncated prion protein, PrP (113–231), from 15N NMR relaxation: order parameters calculated and slow conformational fluctuations localized to a distinct region. Protein Sci 18(2):410–423PubMedPubMedCentral
264.
Guantieri V, Venzo A, Di Marco V, Acampora M, Biondi B (2007) Potentiometric and NMR studies on Cd2+ coordination with the histidine-containing Ac184–188NH2 prion protein fragment. Inorg Chim Acta 360(14):4051–4057
265.
Wells MA, Jackson GS, Jones S, Hosszu LL, Craven CJ, Clarke AR et al (2006) A reassessment of copper (II) binding in the full-length prion protein. Biochem J 399(3):435–444PubMedPubMedCentral
266.
Gaggelli E, Bernardi F, Molteni E, Pogni R, Valensin D, Valensin G et al (2005) Interaction of the human prion PrP (106− 126) sequence with copper (II), manganese (II), and zinc (II): NMR and EPR studies. J Am Chem Soc 127(3):996–1006PubMed
267.
Wissler J, Laub M, Jennissen H, editors. 3D-Rapid prototyping molecular image models of cellular prion proteins [PrPC] based on NMR data: metalloregulated interactions with copper-structured RNA biaptamers and relation to RNA chaperones. FASEB JOURNAL; 2003: FEDERATION AMER SOC EXP BIOL 9650 ROCKVILLE PIKE, BETHESDA, MD 20814–3998 USA
268.
Banci L, Bertini I, Ciofi-Baffoni S, Gonnelli L, Su X-C (2003) Structural basis for the function of the N-terminal domain of the ATPase CopA from Bacillus subtilis. J Biol Chem 278(50):50506–50513PubMed
269.
Banci L, Bertini I, Ciofi-Baffoni S, Su X-C, Borrelly GP, Robinson NJ (2004) Solution structures of a cyanobacterial metallochaperone INSIGHT INTO AN ATYPICAL COPPER-BINDING MOTIF. J Biol Chem 279(26):27502–27510PubMed
270.
Myari A, Hadjiliadis N, Fatemi N, Sarkar B (2004) Copper (I) interaction with model peptides of WD6 and TM6 domains of Wilson ATPase: regulatory and mechanistic implications. J Inorg Biochem 98(9):1483–1494PubMed
271.
Abajian C, Yatsunyk LA, Ramirez BE, Rosenzweig AC (2004) Yeast Cox17 solution structure and copper (I) binding. J Biol Chem 279(51):53584–53592PubMed
272.
Wernimont AK, Huffman DL, Finney LA, Demeler B, O'Halloran TV, Rosenzweig AC (2003) Crystal structure and dimerization equilibria of PcoC, a methionine-rich copper resistance protein from Escherichia coli. JBIC J Biol Inorg Chem 8(1–2):185–194PubMed
273.
Cobine PA, George GN, Jones CE, Wickramasinghe WA, Solioz M, Dameron CT (2002) Copper transfer from the Cu (I) chaperone, CopZ, to the repressor, Zn (II) CopY: metal coordination environments and protein interactions. Biochemistry 41(18):5822–5829PubMed
274.
Bonomo RP, Pappalardo G, Rizzarelli E, Tabbì G, Vagliasindi LI (2008) Studies of nitric oxide interaction with mono-and dinuclear copper (II) complexes of prion protein bis-octarepeat fragments. Dalton Trans 29:3805–3816
275.
Martic S, Rains MK, Kraatz H-B (2013) Probing copper/tau protein interactions electrochemically. Anal Biochem 442(2):130–137PubMed
276.
Viles JH, Cohen FE, Prusiner SB, Goodin DB, Wright PE, Dyson HJ (1999) Copper binding to the prion protein: structural implications of four identical cooperative binding sites. Proc Natl Acad Sci 96(5):2042–2047PubMed
277.
Gaggelli E, Kozlowski H, Valensin D, Valensin G (2006) Copper homeostasis and neurodegenerative disorders (Alzheimer's, prion, and Parkinson's diseases and amyotrophic lateral sclerosis). Chem Rev 106(6):1995–2044PubMed
278.
Migliorini C, Sinicropi A, Kozlowski H, Luczkowski M, Valensin D (2014) Copper-induced structural propensities of the amyloidogenic region of human prion protein. JBIC J Biol Inorg Chem 19(4–5):635–645PubMed
279.
Berti F, Gaggelli E, Guerrini R, Janicka A, Kozlowski H, Legowska A et al (2007) Structural and dynamic characterization of copper (II) binding of the human prion protein outside the octarepeat region. Chem Eur J 13(7):1991–2001PubMed
280.
Hecel A, Migliorini C, Valensin D, Luczkowski M, Kozlowski H (2015) Impact of SDS surfactant on the interactions of Cu2+ ions with the amyloidogenic region of human prion protein. Dalton Trans 44(29):13125–13132PubMed
281.
Cox DL, Pan J, Singh RR (2006) A mechanism for copper inhibition of infectious prion conversion. Biophys J 91(2):L11–LL3PubMedPubMedCentral
282.
Viles JH (2012) Metal ions and amyloid fiber formation in neurodegenerative diseases. Copper, zinc and iron in Alzheimer's, Parkinson's and prion disease. Coord Chem Rev 256:2271–2284
283.
Sarell CJ, Syme CD, Rigby SEJ, Viles JH (2009) Copper (II) binding to amyloid-β fibrils of Alzheimer’s disease reveals a picomolar affinity: stoichiometry and coordination geometry are independent of Aβ oligomeric form. Biochemistry 48(20):4388–4402PubMed
284.
Burns CS, Aronoff-Spencer E, Legname G, Prusiner SB, Antholine WE, Gerfen GJ et al (2003) Copper coordination in the full-length, recombinant prion protein. Biochemistry 42(22):6794–6803PubMedPubMedCentral
285.
Whittal RM, Ball HL, Cohen FE, Burlingame AL, Prusiner SB, Baldwin MA (2000) Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry. Protein Sci 9(2):332–343PubMedPubMedCentral
286.
Kramer ML, Kratzin HD, Schmidt B, Römer A, Windl O, Liemann S et al (2001) Prion protein binds copper within the physiological concentration range. J Biol Chem 276(20):16711–16719PubMed
287.
Qin K, Yang Y, Mastrangelo P, Westaway D (2002) Mapping Cu (II) binding sites in prion proteins by diethyl pyrocarbonate modification and matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometric footprinting. J Biol Chem 277(3):1981–1990PubMed
288.
Klewpatinond M, Davies P, Bowen S, Brown DR, Viles JH (2008) Deconvoluting the Cu2+ binding modes of full-length prion protein. J Biol Chem 283(4):1870–1881PubMed
289.
Viles JH, Klewpatinond M, Nadal RC (2008) Copper and the structural biology of the prion protein. Biochem Soc Trans 36(Pt 6):1288–1292PubMed
290.
Younan ND, Klewpatinond M, Davies P, Ruban AV, Brown DR, Viles JH (2011) Copper (II) induced secondary structure changes and reduced folding stability of the prion protein. J Mol Biol 410:369–382PubMed
Metadata
Title
Using NMR spectroscopy to investigate the role played by copper in prion diseases
Authors
Rawiah A. Alsiary
Mawadda Alghrably
Abdelhamid Saoudi
Suliman Al-Ghamdi
Lukasz Jaremko
Mariusz Jaremko
Abdul-Hamid Emwas
Publication date
01-09-2020
Publisher
Springer International Publishing
Published in
Neurological Sciences / Issue 9/2020
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-020-04321-9

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