Combination of Copper Ions and Nucleotide Generates Aggregates from Prion Protein Fragments in the N-Terminal Domain

Noriyuki       Shiraishi; Yoshiaki      Hirano
doi:10.2174/0929866527666200225124829
Abstract

Background: It has been previously found that PrP_23-98, which contains four highly conserved octarepeats (residues 60-91) and one partial repeat (residues 92-96), polymerizes into amyloid-like and proteinase K-resistant spherical aggregates in the presence of NADPH plus copper ions.
Objective: We aimed to determine the requirements for the formation of these aggregates.
Methods: In this study, we performed an aggregation experiment using N-acetylated and Camidated PrP fragments of the N-terminal domain, Octa1, Octa2, Octa3, Octa4, PrP₈₄₋₁₁₄, and PrP₇₆₋₁₁₄, in the presence of NADPH with copper ions, and focused on the effect of the number of copper-binding sites on aggregation.
Results: Among these PrP fragments, Octa4, containing four copper-binding sites, was particularly effective in forming aggregates. We also tested the effect of other pyridine nucleotides and adenine nucleotides on the aggregation of Octa4. ATP was equally effective, but NADH, NADP, ADP, and AMP had no effect.
Conclusion: The phosphate group on the adenine-linked ribose moiety of adenine nucleotides and pyridine nucleotides is presumed to be essential for the observed effect on aggregation. Efficient aggregation requires the presence of the four octarepeats. These insights may be helpful in the eventual development of therapeutic agents against prion-related disorders.
Keywords: PrP fragment, Octa4, aggregation, adenine nucleotide, pyridine nucleotide, copper ion.
« Previous Next »
Graphical Abstract

[1] 
Daggett, V. Structure-function aspects of prion proteins. Curr. Opin. Biotechnol.,  1998, 9(4), 359-365.
[http://dx.doi.org/10.1016/S0958-1669(98)80008-6] [PMID:  9720262] 
[2] 
Brown, D.R. Prion and prejudice: Normal protein and the synapse. Trends Neurosci.,  2001, 24(2), 85-90.
[http://dx.doi.org/10.1016/S0166-2236(00)01689-1] [PMID:  11164938] 
[3] 
Aguzzi, A.; Polymenidou, M. Mammalian prion biology: One century of evolving concepts. Cell,  2004, 116(2), 313-327.
[http://dx.doi.org/10.1016/S0092-8674(03)01031-6] [PMID:  14744440] 
[4] 
Sánchez-López, C.; Rossetti, G.; Quintanar, L.; Carloni, P. Structural determinants of the prion protein N-terminus and its adducts with copper ions. Int. J. Mol. Sci.,  2018, 20(1), 18-32.
[http://dx.doi.org/10.3390/ijms20010018] [PMID:  30577569] 
[5] 
Legname, G. Elucidating the function of the prion protein. PLoS Pathog.,  2017, 13(8)e1006458
[http://dx.doi.org/10.1371/journal.ppat.1006458] [PMID:  28859171] 
[6] 
Wulf, M.A.; Senatore, A.; Aguzzi, A. The biological function of the cellular prion protein: An update. BMC Biol.,  2017, 15(1), 34-46.
[http://dx.doi.org/10.1186/s12915-017-0375-5] [PMID:  28464931] 
[7] 
Prusiner, S.B. Molecular biology of prion diseases. Science,  1991, 252(5012), 1515-1522.
[http://dx.doi.org/10.1126/science.1675487] [PMID:  1675487] 
[8] 
Prusiner, S.B. Prions. Proc. Natl. Acad. Sci. USA,  1998, 95(23), 13363-13383.
[http://dx.doi.org/10.1073/pnas.95.23.13363] [PMID:  9811807] 
[9] 
Aguzzi, A.; Calella, A.M. Prions: Protein aggregation and infectious diseases. Physiol. Rev.,  2009, 89(4), 1105-1152.
[http://dx.doi.org/10.1152/physrev.00006.2009] [PMID:  19789378] 
[10] 
Brandner, S.; Jaunmuktane, Z. Prion disease: Experimental models and reality. Acta Neuropathol.,  2017, 133(2), 197-222.
[http://dx.doi.org/10.1007/s00401-017-1670-5] [PMID:  28084518] 
[11] 
Hornshaw, M.P.; McDermott, J.R.; Candy, J.M.; 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.,  1995, 214(3), 993-999.
[http://dx.doi.org/10.1006/bbrc.1995.2384] [PMID:  7575574] 
[12] 
Viles, J.H.; Cohen, F.E.; Prusiner, S.B.; Goodin, D.B.; Wright, P.E.; Dyson, H.J. Copper binding to the prion protein: Structural implications of four identical cooperative binding sites. Proc. Natl. Acad. Sci. USA,  1999, 96(5), 2042-2047.
[http://dx.doi.org/10.1073/pnas.96.5.2042] [PMID:  10051591] 
[13] 
Aronoff-Spencer, E.; Burns, C.S.; Avdievich, N.I.; Gerfen, G.J.; Peisach, J.; Antholine, W.E.; Ball, H.L.; Cohen, F.E.; Prusiner, S.B.; Millhauser, G.L. Identification of the Cu2+ binding sites in the N-terminal domain of the prion protein by EPR and CD spectroscopy. Biochemistry,  2000, 39(45), 13760-13771.
[http://dx.doi.org/10.1021/bi001472t] [PMID:  11076515] 
[14] 
Bonomo, R.P.; Imperllizzeri, G.; Pappalardo, G.; Rizzarelli, E.; Tabbì, G. Copper(II) binding modes in the prion octapeptide PHGGGWGQ: A spectroscopic and voltammetric study. Chemistry,  2000, 6(22), 4195-4202.
[http://dx.doi.org/10.1002/1521-3765(20001117)6:22<4195:AID-CHEM4195>3.0.CO;2-2] [PMID:  11128284] 
[15] 
Whittal, R.M.; Ball, H.L.; Cohen, F.E.; Burlingame, A.L.; Prusiner, S.B.; Baldwin, M.A. Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry. Protein Sci.,  2000, 9(2), 332-343.
[http://dx.doi.org/10.1110/ps.9.2.332] [PMID:  10716185] 
[16] 
Kramer, M.L.; Kratzin, H.D.; Schmidt, B.; Römer, A.; Windl, O.; Liemann, S.; Hornemann, S.; Kretzschmar, H. Prion protein binds copper within the physiological concentration range. J. Biol. Chem.,  2001, 276(20), 16711-16719.
[http://dx.doi.org/10.1074/jbc.M006554200] [PMID:  11278306] 
[17] 
Jackson, G.S.; Murray, I.; Hosszu, L.L.; Gibbs, N.; Waltho, J.P.; Clarke, A.R.; Collinge, J. Location and properties of metal-binding sites on the human prion protein. Proc. Natl. Acad. Sci. USA,  2001, 98(15), 8531-8535.
[http://dx.doi.org/10.1073/pnas.151038498] [PMID:  11438695] 
[18] 
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.; Millhauser, G.L. Molecular features of the copper binding sites in the octarepeat domain of the prion protein. Biochemistry,  2002, 41(12), 3991-4001.
[http://dx.doi.org/10.1021/bi011922x] [PMID:  11900542] 
[19] 
Lehmann, S. Metal ions and prion diseases. Curr. Opin. Chem. Biol.,  2002, 6(2), 187-192.
[http://dx.doi.org/10.1016/S1367-5931(02)00295-8] [PMID:  12039003] 
[20] 
Burns, C.S.; Aronoff-Spencer, E.; Legname, G.; Prusiner, S.B.; Antholine, W.E.; Gerfen, G.J.; Peisach, J.; Millhauser, G.L. Copper coordination in the full-length, recombinant prion protein. Biochemistry,  2003, 42(22), 6794-6803.
[http://dx.doi.org/10.1021/bi027138+] [PMID:  12779334] 
[21] 
Morante, S.; González-Iglesias, R.; Potrich, C.; Meneghini, C.; Meyer-Klaucke, W.; Menestrina, G.; Gasset, M. Inter- and intra-octarepeat Cu(II) site geometries in the prion protein: Implications in Cu(II) binding cooperativity and Cu(II)-mediated assemblies. J. Biol. Chem.,  2004, 279(12), 11753-11759.
[http://dx.doi.org/10.1074/jbc.M312860200] [PMID:  14703517] 
[22] 
Zahn, R. The octapeptide repeats in mammalian prion protein constitute a pH-dependent folding and aggregation site. J. Mol. Biol.,  2003, 334(3), 477-488.
[http://dx.doi.org/10.1016/j.jmb.2003.09.048] [PMID:  14623188] 
[23] 
Garnett, A.P.; Viles, J.H. Copper binding to the octarepeats of the prion protein. Affinity, specificity, folding, and cooperativity: Insights from circular dichroism. J. Biol. Chem.,  2003, 278(9), 6795-6802.
[http://dx.doi.org/10.1074/jbc.M209280200] [PMID:  12454014] 
[24] 
Jones, C.E.; Abdelraheim, S.R.; Brown, D.R.; Viles, J.H. Preferential Cu2+ coordination by His96 and His111 induces beta-sheet formation in the unstructured amyloidogenic region of the prion protein. J. Biol. Chem.,  2004, 279(31), 32018-32027.
[http://dx.doi.org/10.1074/jbc.M403467200] [PMID:  15145944] 
[25] 
Hureau, C.; Charlet, L.; Dorlet, P.; Gonnet, F.; Spadini, L.; Anxolabéhère-Mallart, E.; Girerd, J.J. A spectroscopic and voltammetric study of the pH-dependent Cu(II) coordination to the peptide GGGTH: Relevance to the fifth Cu(II) site in the prion protein. J. Biol. Inorg. Chem.,  2006, 11(6), 735-744.
[http://dx.doi.org/10.1007/s00775-006-0118-5] [PMID:  16758168] 
[26] 
Klewpatinond, M.; Viles, J.H. Fragment length influences affinity for Cu2+ and Ni2+ binding to His96 or His111 of the prion protein and spectroscopic evidence for a multiple histidine binding only at low pH. Biochem. J.,  2007, 404(3), 393-402.
[http://dx.doi.org/10.1042/BJ20061893] [PMID:  17331076] 
[27] 
Osz, K.; Nagy, Z.; Pappalardo, G.; Di Natale, G.; Sanna, D.; Micera, G.; Rizzarelli, E.; Sóvágó, I. Copper(II) interaction with prion peptide fragments encompassing histidine residues within and outside the octarepeat domain: Speciation, stability constants and binding details. Chemistry,  2007, 13(25), 7129-7143.
[http://dx.doi.org/10.1002/chem.200601568] [PMID:  17566127] 
[28] 
Davies, P.; 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.,  2008, 410(2), 237-244.
[http://dx.doi.org/10.1042/BJ20071477] [PMID:  18254729] 
[29] 
Hureau, C.; Mathé, C.; Faller, P.; Mattioli, T.A.; Dorlet, P. Folding of the prion peptide GGGTHSQW around the copper(II) ion: Identifying the oxygen donor ligand at neutral pH and probing the proximity of the tryptophan residue to the copper ion. J. Biol. Inorg. Chem.,  2008, 13(7), 1055-1064.
[http://dx.doi.org/10.1007/s00775-008-0389-0] [PMID:  18500541] 
[30] 
Shearer, J.; Soh, P.; Lentz, S. Both Met(109) and Met(112) are utilized for Cu(II) coordination by the amyloidogenic fragment of the human prion protein at physiological pH. J. Inorg. Biochem.,  2008, 102(12), 2103-2113.
[http://dx.doi.org/10.1016/j.jinorgbio.2008.07.016] [PMID:  18778855] 
[31] 
Klewpatinond, M.; Davies, P.; Bowen, S.; Brown, D.R.; Viles, J.H. Deconvoluting the Cu2+ binding modes of full-length prion protein. J. Biol. Chem.,  2008, 283(4), 1870-1881.
[http://dx.doi.org/10.1074/jbc.M708472200] [PMID:  18042548] 
[32] 
Gralka, E.; Valensin, D.; Porciatti, E.; Gajda, C.; Gaggelli, E.; Valensin, G.; Kamysz, W.; Nadolny, R.; Guerrini, R.; Bacco, D.; Remelli, M.; Kozlowski, H. CuII binding sites located at His-96 and His-111 of the human prion protein: thermodynamic and spectroscopic studies on model peptides. Dalton Trans.,  2008, 38(38), 5207-5219.
[http://dx.doi.org/10.1039/b806192k] [PMID:  18813375] 
[33] 
Rivillas-Acevedo, L.; Grande-Aztatzi, R.; Lomelí, I.; García, J.E.; Barrios, E.; Teloxa, S.; Vela, A.; Quintanar, L. Spectroscopic and electronic structure studies of copper(II) binding to His111 in the human prion protein fragment 106-115: Evaluating the role of protons and methionine residues. Inorg. Chem.,  2011, 50(5), 1956-1972.
[http://dx.doi.org/10.1021/ic102381j] [PMID:  21261254] 
[34] 
Rivillas-Acevedo, L.; Maciel-Barón, L.; García, J.E.; Juaristi, E.; Quintanar, L. Insertion of beta-alanine in model peptides for copper binding to His96 and His111 of the human prion protein. J. Inorg. Biochem.,  2013, 126, 104-110.
[http://dx.doi.org/10.1016/j.jinorgbio.2013.05.016] [PMID:  23796442] 
[35] 
Qin, K.; Yang, D.S.; Yang, Y.; Chishti, M.A.; Meng, L.J.; Kretzschmar, H.A.; Yip, C.M.; Fraser, P.E.; Westaway, D. Copper(II)-induced conformational changes and protease resistance in recombinant and cellular PrP. Effect of protein age and deamidation. J. Biol. Chem.,  2000, 275(25), 19121-19131.
[http://dx.doi.org/10.1074/jbc.275.25.19121] [PMID:  10858456] 
[36] 
Wong, B.S.; Vénien-Bryan, C.; Williamson, R.A.; Burton, D.R.; Gambetti, P.; Sy, M.S.; Brown, D.R.; Jones, I.M. Copper refolding of prion protein. Biochem. Biophys. Res. Commun.,  2000, 276(3), 1217-1224.
[http://dx.doi.org/10.1006/bbrc.2000.3604] [PMID:  11027613] 
[37] 
Quaglio, E.; Chiesa, R.; Harris, D.A. Copper converts the cellular prion protein into a protease-resistant species that is distinct from the scrapie isoform. J. Biol. Chem.,  2001, 276(14), 11432-11438.
[http://dx.doi.org/10.1074/jbc.M009666200] [PMID:  11278539] 
[38] 
Kuczius, T.; Buschmann, A.; Zhang, W.; Karch, H.; Becker, K.; Peters, G.; Groschup, M.H. Cellular prion protein acquires resistance to proteolytic degradation following copper ion binding. Biol. Chem.,  2004, 385(8), 739-747.
[http://dx.doi.org/10.1515/BC.2004.090] [PMID:  15449710] 
[39] 
Yen, C.F.; Harischandra, D.S.; Kanthasamy, A.; Sivasankar, S. Copper-induced structural conversion templates prion protein oligomerization and neurotoxicity. Sci. Adv.,  2016, 2(7)e1600014
[http://dx.doi.org/10.1126/sciadv.1600014] [PMID:  27419232] 
[40] 
Lu, B.; Zhao, L.; Qin, K. Copper induces structural changes in N-terminus of human prion protein. Biochem. Biophys. Res. Commun.,  2018, 499(3), 470-474.
[http://dx.doi.org/10.1016/j.bbrc.2018.03.171] [PMID:  29580990] 
[41] 
Charco, J.M.; Eraña, H.; Venegas, V.; García-Martínez, S.; López-Moreno, R.; González-Miranda, E.; Pérez-Castro, M.Á.; Castilla, J. Recombinant PrP and its contribution to research on transmissible spongiform encephalopathies. Pathogens,  2017, 6(4), 67-86.
[http://dx.doi.org/10.3390/pathogens6040067] [PMID:  29240682] 
[42] 
Goldfarb, L.G.; Brown, P.; McCombie, W.R.; Goldgaber, D.; Swergold, G.D.; Wills, P.R.; Cervenakova, L.; Baron, H.; Gibbs, C.J. Jr.; Gajdusek, D.C. Transmissible familial Creutzfeldt-Jakob disease associated with five, seven, and eight extra octapeptide coding repeats in the PRNP gene. Proc. Natl. Acad. Sci. USA,  1991, 88(23), 10926-10930.
[http://dx.doi.org/10.1073/pnas.88.23.10926] [PMID:  1683708] 
[43] 
Campbell, T.A.; Palmer, M.S.; Will, R.G.; Gibb, W.R.; Luthert, P.J.; Collinge, J. A prion disease with a novel 96-base pair insertional mutation in the prion protein gene. Neurology,  1996, 46(3), 761-766.
[http://dx.doi.org/10.1212/WNL.46.3.761] [PMID:  8618679] 
[44] 
Chiesa, R.; Piccardo, P.; Ghetti, B.; Harris, D.A. Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron,  1998, 21(6), 1339-1351.
[http://dx.doi.org/10.1016/S0896-6273(00)80653-4] [PMID:  9883727] 
[45] 
Chiesa, R.; Drisaldi, B.; Quaglio, E.; Migheli, A.; Piccardo, P.; Ghetti, B.; Harris, D.A. 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. USA,  2000, 97(10), 5574-5579.
[http://dx.doi.org/10.1073/pnas.97.10.5574] [PMID:  10805813] 
[46] 
Kundu, B.; Maiti, N.R.; Jones, E.M.; Surewicz, K.A.; Vanik, D.L.; Surewicz, W.K. Nucleation-dependent conformational conversion of the Y145Stop variant of human prion protein: Structural clues for prion propagation. Proc. Natl. Acad. Sci. USA,  2003, 100(21), 12069-12074.
[http://dx.doi.org/10.1073/pnas.2033281100] [PMID:  14519851] 
[47] 
Vanik, D.L.; Surewicz, K.A.; Surewicz, W.K. Molecular basis of barriers for interspecies transmissibility of mammalian prions. Mol. Cell,  2004, 14(1), 139-145.
[http://dx.doi.org/10.1016/S1097-2765(04)00155-8] [PMID:  15068810] 
[48] 
Jones, E.M.; Surewicz, W.K. Fibril conformation as the basis of species- and strain-dependent seeding specificity of mammalian prion amyloids. Cell,  2005, 121(1), 63-72.
[http://dx.doi.org/10.1016/j.cell.2005.01.034] [PMID:  15820679] 
[49] 
Abdallah, A.; Wang, P.; Richt, J.A.; Sreevatsan, S. Y145Stop is sufficient to induce de novo generation prions using protein misfolding cyclic amplification. Prion,  2012, 6(1), 81-88.
[http://dx.doi.org/10.4161/pri.6.1.18493] [PMID:  22453182] 
[50] 
Choi, J.K.; Cali, I.; Surewicz, K.; Kong, Q.; Gambetti, P.; Surewicz, W.K. Amyloid fibrils from the N-terminal prion protein fragment are infectious. Proc. Natl. Acad. Sci. USA,  2016, 113(48), 13851-13856.
[http://dx.doi.org/10.1073/pnas.1610716113] [PMID:  27849581] 
[51] 
Shiraishi, N.; Utsunomiya, H.; Nishikimi, M. Combination of NADPH and copper ions generates proteinase K-resistant aggregates from recombinant prion protein. J. Biol. Chem.,  2006, 281(46), 34880-34887.
[http://dx.doi.org/10.1074/jbc.M606581200] [PMID:  16990274] 
[52] 
Shiraishi, N.; Inai, Y.; Ihara, Y. Proteinase K-resistant aggregates of recombinant prion protein PrP-(23-98) are toxic to cultured cells. Protein Pept. Lett.,  2009, 16(1), 91-96.
[http://dx.doi.org/10.2174/092986609787049475] [PMID:  19149680] 
[53] 
Shiraishi, N.; Nishikimi, M. Carbonyl formation on a copper-bound prion protein fragment, PrP23-98, associated with its dopamine oxidase activity. FEBS Lett.,  2002, 511(1-3), 118-122.
[http://dx.doi.org/10.1016/S0014-5793(01)03324-5] [PMID:  11821060] 
[54] 
ProtParam. ExPaSy SIB Bioinformatics., https://www.expasy.org/tools/
[55] 
Klunk, W.E.; Jacob, R.F.; Mason, R.P. Quantifying amyloid by congo red spectral shift assay. Methods Enzymol.,  1999, 309, 285-305.
[http://dx.doi.org/10.1016/S0076-6879(99)09021-7] [PMID:  10507031] 
[56] 
Stathopulos, P.B.; Scholz, G.A.; Hwang, Y.M.; Rumfeldt, J.A.; Lepock, J.R.; Meiering, E.M. Sonication of proteins causes formation of aggregates that resemble amyloid. Protein Sci.,  2004, 13(11), 3017-3027.
[http://dx.doi.org/10.1110/ps.04831804] [PMID:  15459333] 
[57] 
Frid, P.; Anisimov, S.V.; Popovic, N. Congo red and protein aggregation in neurodegenerative diseases. Brain Res. Rev.,  2007, 53(1), 135-160.
[http://dx.doi.org/10.1016/j.brainresrev.2006.08.001] [PMID:  16959325] 
[58] 
Baskakov, I.V.; Bocharova, O.V. In vitro conversion of mammalian prion protein into amyloid fibrils displays unusual features. Biochemistry,  2005, 44(7), 2339-2348.
[http://dx.doi.org/10.1021/bi048322t] [PMID:  15709746] 
[59] 
Lührs, T.; Zahn, R.; Wüthrich, K. Amyloid formation by recombinant full-length prion proteins in phospholipid bicelle solutions. J. Mol. Biol.,  2006, 357(3), 833-841.
[http://dx.doi.org/10.1016/j.jmb.2006.01.016] [PMID:  16466741] 
[60] 
El Moustaine, D.; Perrier, V.; Smeller, L.; Lange, R.; Torrent, J. Full-length prion protein aggregates to amyloid fibrils and spherical particles by distinct pathways. FEBS J.,  2008, 275(9), 2021-2031.
[http://dx.doi.org/10.1111/j.1742-4658.2008.06356.x] [PMID:  18355314] 
[61] 
Giannopoulos, P.N.; Robertson, C.; Jodoin, J.; Paudel, H.; Booth, S.A.; LeBlanc, A.C. Phosphorylation of prion protein at serine 43 induces prion protein conformational change. J. Neurosci.,  2009, 29(27), 8743-8751.
[http://dx.doi.org/10.1523/JNEUROSCI.2294-09.2009] [PMID:  19587281] 
[62] 
El Moustaine, D.; Perrier, V.; Acquatella-Tran Van Ba, I.; Meersman, F.; Ostapchenko, V.G.; Baskakov, I.V.; Lange, R.; Torrent, J. Amyloid features and neuronal toxicity of mature prion fibrils are highly sensitive to high pressure. J. Biol. Chem.,  2011, 286(15), 13448-13459.
[http://dx.doi.org/10.1074/jbc.M110.192872] [PMID:  21357423] 
[63] 
Saverioni, D.; Notari, S.; Capellari, S.; Poggiolini, I.; Giese, A.; Kretzschmar, H.A.; Parchi, P. Analyses of protease resistance and aggregation state of abnormal prion protein across the spectrum of human prions. J. Biol. Chem.,  2013, 288(39), 27972-27985.
[http://dx.doi.org/10.1074/jbc.M113.477547] [PMID:  23897825] 
[64] 
Shiraishi, N.; Hirano, Y. Aggregates produced from PrP-(23-98) in the presence of nucleotide plus copper ions are toxic to cultured cells. Bulletin of Tokai Gakuen University,  2017, 21, 14-22.
[65] 
Cohn, M.; Hughes, T.R. Jr. Nuclear magnetic resonance spectra of adenosine di- and triphosphate. II. Effect of complexing with divalent metal ions. J. Biol. Chem.,  1962, 237, 176-181.
[PMID:  13880359] 
[66] 
Naumann, C.F.; Prijs, B.; Sigel, H. Adenosine and inosine 5′-triphosphates. Protonation, metal-ion coordination, and charge-transfer interaction between two ligands within ternary complexes. Eur. J. Biochem.,  1974, 41(2), 209-216.
[http://dx.doi.org/10.1111/j.1432-1033.1974.tb03262.x] [PMID:  4816894] 
[67] 
Fazakerley, G.V.; Reid, D.G. Determination of the interaction of ADP and dADP with copper(II), manganese(II) and lanthanide(III) ions by nuclear-magnetic-resonance spectroscopy. Eur. J. Biochem.,  1979, 93(3), 535-543.
[http://dx.doi.org/10.1111/j.1432-1033.1979.tb12852.x] [PMID:  33807] 
[68] 
Gasowska, A. Interaction centres of purine nucleotides: Adenosine-5′-diphosphate and adenosine-5′-triphosphate in their reactions with tetramines and Cu(II) ions. J. Inorg. Biochem.,  2003, 96(2-3), 346-356.
[http://dx.doi.org/10.1016/S0162-0134(03)00150-8] [PMID:  12888270] 
[69] 
Jastrzab, R. Phosphoserine and specific types of its coordination in copper(II) and adenosine nucleotides systems - potentiometric and spectroscopic studies. J. Inorg. Biochem.,  2009, 103(5), 766-773.
[http://dx.doi.org/10.1016/j.jinorgbio.2009.01.012] [PMID:  19230980] 
[70] 
Bregier-Jarzebowska, R.; Gasowska, A.; Hoffmann, S.K.; Lomozik, L. Interactions of diamines with adenosine-5′-triphosphate (ATP) in the systems including copper(II) ions. J. Inorg. Biochem.,  2016, 162, 73-82.
[http://dx.doi.org/10.1016/j.jinorgbio.2016.06.007] [PMID:  27289347] 
[71] 
Hoffmann, S.K.; Goslar, J.; Bregier-Jarzebowska, R.; Gasowska, A.; Zalewska, A.; Lomozik, L. Copper(II) ions interactions in the systems with triamines and ATP. Potentiometric and spectroscopic studies. J. Inorg. Biochem.,  2017, 177, 89-100.
[http://dx.doi.org/10.1016/j.jinorgbio.2017.09.004] [PMID:  28941402] 
[72] 
Gasowska, A. Interaction centres of pyrimidine nucleotides: Cytidine-5′-diphosphate (CDP) and cytidine-5′-triphosphate (CTP) in their reactions with tetramines and Cu(II) ions. J. Inorg. Biochem.,  2005, 99(8), 1698-1707.
[http://dx.doi.org/10.1016/j.jinorgbio.2005.05.005] [PMID:  15993946] 
[73] 
Hoffmann, S.K.; Goslar, J.; Lijewski, S.; Basiński, K.; Gąsowska, A.; Łomozik, L. EPR and potentiometric studies of copper(II) binding to nicotinamide adenine dinucleotide (NAD+) in water solution. J. Inorg. Biochem.,  2012, 111, 18-24.
[http://dx.doi.org/10.1016/j.jinorgbio.2012.02.028] [PMID:  22484248] 
[74] 
Green, M.K.; Kotowycz, G. The stoichiometry and stability of the NADP complexes with manganese(II) ions as studied by electron paramagnetic resonance. Can. J. Biochem.,  1979, 57(7), 995-999.
[http://dx.doi.org/10.1139/o79-123] [PMID:  39671] 
[75] 
Fink, A.L. Protein aggregation: Folding aggregates, inclusion bodies and amyloid. Fold. Des.,  1998, 3(1), R9-R23.
[http://dx.doi.org/10.1016/S1359-0278(98)00002-9] [PMID:  9502314] 
[76] 
Roberts, C.J. Protein aggregation and its impact on product quality. Curr. Opin. Biotechnol.,  2014, 30, 211-217.
[http://dx.doi.org/10.1016/j.copbio.2014.08.001] [PMID:  25173826] 
[77] 
Alam, P.; Siddiqi, K.; Chturvedi, S.K.; Khan, R.H. Protein aggregation: From background to inhibition strategies. Int. J. Biol. Macromol.,  2017, 103, 208-219.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.05.048] [PMID:  28522393] 
[78] 
Wang, W.; Roberts, C.J. Protein aggregation - mechanisms, detection, and control. Int. J. Pharm.,  2018, 550(1-2), 251-268.
[http://dx.doi.org/10.1016/j.ijpharm.2018.08.043] [PMID:  30145245] 
[79] 
Chandel, T.I.; Zaman, M.; Khan, M.V.; Ali, M.; Rabbani, G.; Ishtikhar, M.; Khan, R.H. A mechanistic insight into protein-ligand interaction, folding, misfolding, aggregation and inhibition of protein aggregates: An overview. Int. J. Biol. Macromol.,  2018, 106, 1115-1129.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.07.185] [PMID:  28890370] 
[80] 
Zaman, M.; Khan, A.N. Wahiduzzaman; Zakariya, S.M.; Khan, R.H. Protein misfolding, aggregation and mechanism of amyloid cytotoxicity: An overview and therapeutic strategies to inhibit aggregation. Int. J. Biol. Macromol.,  2019, 134, 1022-1037.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.05.109] [PMID:  31128177] 
[81] 
Westaway, D.; Goodman, P.A.; Mirenda, C.A.; McKinley, M.P.; Carlson, G.A.; Prusiner, S.B. Mouse (with short incubation period) prion protein (PRNP) gene, complete cds GenBank: M18070.1, 1987.
Rights & Permissions Print Cite
Article Metrics
17
1
Journal Information
For Authors
For Editors
For Reviewers
Explore Articles
Open Access
Open Access Articles
For Visitors
DOI https://dx.doi.org/10.2174/0929866527666200225124829	Print ISSN 0929-8665
Publisher Name Bentham Science Publisher	Online ISSN 1875-5305
Protein & Peptide Letters

Combination of Copper Ions and Nucleotide Generates Aggregates from Prion Protein Fragments in the N-Terminal Domain

Abstract Play Pause

Graphical Abstract

Related Journals

Related Books

Abstract
