Abstract
Protein misfolding disorders (PMDs) refer to a group of diseases related to the misfolding of particular proteins that aggregate and deposit in the cells and tissues of humans and other mammals. The mechanisms that trigger protein misfolding and aggregation are still not fully understood. Increasing experimental evidence indicates that abnormal interactions between PMD-related proteins and nucleic acids (NAs) can induce conformational changes. Here, we discuss these protein–NA interactions and address the role of deoxyribonucleic (DNA) and ribonucleic (RNA) acid molecules in the conformational conversion of different proteins that aggregate in PMDs, such as Alzheimer’s, Parkinson’s, and prion diseases. Studies on the affinity, stability, and specificity of proteins involved in neurodegenerative diseases and NAs are specifically addressed. A landscape of reciprocal effects resulting from the binding of prion proteins, amyloid-β peptides, tau proteins, huntingtin, and α-synuclein are presented here to clarify the possible role of NAs, not only as encoders of genetic information but also in triggering PMDs.
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Abbreviations
- AD:
-
Alzheimer’s disease
- α-syn:
-
alpha-synuclein
- HD:
-
Huntington’s disease
- Htt:
-
huntingtin
- PD:
-
Parkinson’s disease
- PrP:
-
prion protein
- PK:
-
proteinase K
- rPrP:
-
recombinant prion protein
- TSE:
-
transmissible spongiform encephalopathy
References
Adams CR, Kamakaka RT (1999) Chromatin assembly: biochemical identities and genetic redundancy. Curr Opin Genet Dev 9:185–190
Adler V, Zeiler B, Kryukov V, Kascsak R, Rubenstein R, Grossman A (2003) Small, highly structured RNAs participate in the conversion of human recombinant PrP(Sen) to PrP(Res) in vitro. J Mol Biol 332:47–57
Ahn BW, Song DU, Jung YD, Chay KO, Chung MA, Yang SY, Shin BA (2000) Detection of beta-amyloid peptide aggregation using DNA electrophoresis. Anal Biochem 284:401–405
Alkhuja S (2013) Parkinson disease: research update and clinical management. South Med J 106(5):334. doi:10.1097/SMJ.0b013e318290f72a
Ano Bom AP, Rangel LP, Costa DC, de Oliveira GA, Sanches D, Braga CA, Gava LM, Ramos CH, Cepeda AO, Stumbo AC, De Moura Gallo CV, Cordeiro Y, Silva JL (2012) Mutant p53 aggregates into prion-like amyloid oligomers and fibrils: implications for cancer. J Biol Chem 287:28152–28162
Antequera F (2003) Structure, function and evolution of CpG island promoters. Cell Mol Life Sci 60:1647–1658
Antony T, Hoyer W, Cherny D, Heim G, Jovin TM, Subramaniam V (2003) Cellular polyamines promote the aggregation of a-synuclein. J Biol Chem 278:3235–3240
Atwood CS, Moir RD, Huang X, Scarpa RC, Bacarra NM, Romano DM, Hartshorn MA, Tanzi RE, Bush AI (1998) Dramatic aggregation of Alzheimer abeta by Cu(II) is induced by conditions representing physiological acidosis. J Biol Chem 273:12817–12826
Barrantes A, Rejas MT, Benıtez MJ, Jimenez JS (2007) Interaction between Alzheimer’s Aβ1-42 peptide and DNA detected by surface plasmon resonance. J Alzheimers Dis 12:345–355
Barrantes A, Camero S, Garcia-Lucas A, Navarro PJ, Benitez MJ, Jiménez JS (2012) Alzheimer’s disease amyloid peptides interact with DNA, as proved by surface plasmon resonance. J Curr Alzheimer Res 9:924–934
Bartels T, Choi JG, Selkoe DJ (2011) alpha-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 477:107–110
Bayer TA, Wirths O, Majtenyi K, Hartmann T, Multhaup G, Beyreuther K, Czech C (2001) Key factors in Alzheimer’s disease: beta-amyloid precursor protein processing, metabolism and intraneuronal transport. Brain Pathol 11:1–11
Beaudoin S, Vanderperre B, Grenier C, Tremblay I, Leduc F, Roucou X (2009) A large ribonucleoprotein particle induced by cytoplasmic PrP shares striking similarities with the chromatoid body, an RNA granule predicted to function in posttranscriptional gene regulation. Biochim Biophys Acta 1793:335–345
Benn CL, Landles C, Li H, Strand AD, Woodman B, Sathasivam K, Li SH, Ghazi-Noori S, Hockly E, Faruque SM, Cha JH, Sharpe PT, Olson JM, Li XJ, Bates GP (2005) Contribution of nuclear and extranuclear polyQ to neurological phenotypes in mouse models of Huntington’s disease. Hum Mol Genet 14:3065–3078
Benn CL, Sun T, SadriVakili G, McFarland KN, DiRocco DP, Yohrling GJ, Clark TW, Bouzou B, Cha JJ (2008) Huntingtin modulates transcription, occupies gene promoters In Vivo, and binds directly to DNA in a polyglutamine dependent manner. J Neurosci 28:10720–10733
Bera A, Nandi PK (2007) Biological polyamines inhibit nucleic-acid-induced polymerisation of prion protein. Arch Virol 152:655–668
Binder LI, Frankfurter A, Rebhun LI (1985) The distribution of tau in the mammalian central nervous system. J Cell Biol 101:1371–1378
Bisaglia M, Mammi S, Bubacco L (2009) Structural insights on physiological functions and pathological effects of alphasynuclein. FASEB J 23:329–340
Bonini NM (2002) Chaperoning brain degeneration. Proc Natl Acad Sci USA 99:16407–16411
Brady RM, Zinkowski RP, Binder LI (1995) Presence of tau in isolated nuclei from human brain. Neurobiol Aging 16:479–486
Brignull HR, Morley JF, Morimoto RI (2007) The stress of misfolded proteins: C. elegans models for neurodegenerative disease and aging. Adv Exp Med Biol 594:167–189
Buckig A, Tikkanen R, Herzog V, Schmitz A (2002) Cytosolic and nuclear aggregation of the amyloid-peptide following its expression in the endoplasmic reticulum. Histochem Cell Biol 118:353–360
Buee L, Bussiere T, Buée-Scherrer V, Delacourte A, Hof PR (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev 33:95–130
Camero S, Benítez MJ, Jiménez JS (2013a) Anomalous Protein-DNA Interactions Behind Neurological Disorders. Adv Protein Chem Struct Biol 91:37–63
Camero S, Ayuso JM, Barrantes A, Benítez MJ, Jiménez JS (2013b) Specific binding of DNA to aggregated forms of Alzheimer’s disease amyloid peptides. Int J Biol Macromol 55:201–206
Cavaliere P, Pagano B, Granata V, Prigent S, Rezaei H, Giancola C, Zagari A (2013) Cross-talk between prion protein and quadruplex-forming nucleic acids: a dynamic complex formation. Nucleic Acids Res 41:327–339. The authors show by diverse techniques, such as isothermal titration calorimetry, surface plasmon resonance, and circular dichroism that PrP binds quadruplex nucleic acids and that both PrP and the nucleic acid conformation is altered upon this interaction
Chandra S, Gallardo G, Fernandez-Chacon R, Schlüter OM, Südhof TC (2005) Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 123:383–396
Chastain M, Tinoco I Jr (1991) Structural elements in RNA. Prog Nucleic Acid Res Mol Biol 41:131–177
Cherny D, Hoyer W, Subramaniam V, Jovin TM (2004) Double-stranded DNA stimulates the fibrillation of alpha-synuclein in vitro and is associated with the mature fibrils: an electron microscopy study. J Mol Biol 344:929–938
Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333–366
Citron M, Diehl TS, Gordon G, Biere AL, Seubert P, Selkoe DJ (1996) Evidence that the 42- and 40-amino acid forms of amyloid beta protein are generated from the beta-amyloid precursor protein by different protease activities. Proc Natl Acad Sci USA 93:13170–13175
Cohen FE, Prusiner SB (1998) Pathologic conformations of prion proteins. Annu Rev Biochem 67:793–819
Cohlberg JA, Li J, Uversky VN, Fink AL (2002) Heparin and other glycosaminoglycans stimulate the formation of amyloid fibrils from a-synuclein in vitro. Biochemistry 41:1502–1511
Cordeiro Y, Silva JL (2005) The hypothesis of the catalytic action of nucleic acid on the conversion of prion protein. Protein Pept Lett 12:251–255
Cordeiro Y, Machado F, Juliano L, Juliano MA, Brentani RR, Foguel D, Silva JL (2001) DNA converts cellular prion protein into the beta-sheet conformation and inhibits prion peptide aggregation. J Biol Chem 276:49400–49409. This work reported that recombinant PrP was converted into a scrapie-like, beta-sheet-rich conformation upon binding to nucleic acids, proposing that nucleic acids act as catalysts in the conversion process
Costa FF (2007) Non-coding RNAs: lost in translation? Gene 386:1–10
Cummings JL (2004) Alzheimer’s disease. N Engl J Med 351:56–67
De Felice FG, Vieira MN, Saraiva LM, Figueroa-Villar JD, Garcia-Abreu J, Liu R, Chang L, Klein WL, Ferreira ST (2004) Targeting the neurotoxic species in Alzheimer’s disease: inhibitors of Abeta oligomerization. FASEB J 18:1366–1372
Deleault NR, Lucassen RW, Supattapone S (2003) RNA molecules stimulate prion protein conversion. Nature 425:717–720
Di Domizio J, Zhang R, Stagg LJ, Gagea M, Zhuo M, Ladbury JE, Cao W (2012) Binding with nucleic acids or glycosaminoglycans converts soluble protein oligomers to amyloid. J Biol Chem 287:736–747
DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, Aronin N (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277:1990–1993
Dinger ME, Mercer TR, Mattick JS (2008) RNAs as extracellular signaling molecules. J Mol Endocrinol 40:151–159
Dobson CM (2001) Protein folding and its links with human disease. Biochem Soc Symp 68:1–26
Dorsman JC, Smoor MA, Maat-Schieman ML, Bout M, Siesling S, van Duinen SG, Verschuuren JJ, den Dunnen JT, Roos RA, van Ommen GJ (1999) Analysis of the subcellular localization of huntingtin with a set of rabbit polyclonal antibodies in cultured mammalian cells of neuronal origin: comparison with the distribution of huntingtin in Huntington’s disease autopsy brain. Philos Trans R Soc Lond B 354:1061–1067
Draper DE, Reynaldo LP (1999) RNA binding strategies of ribosomal proteins. Nucleic Acids Res 27:381–388
Dyer RB, McMurray CT (2001) Mutant protein in Huntington disease is resistant to proteolysis in affected brain. Nat Genet 29:270–278
Ecroyd H, Carver JA (2008) Unraveling the mysteries of protein folding and misfolding. IUBMB Life 60:769–774
Eisenberg D, Jucker M (2012) The amyloid state of proteins in human diseases. Cell 148:1188–1203
Gabus C, Derrington E, Leblanc P, Chnaiderman J, Dormont D, Swietnicki W, Morillas M, Surewicz WK, Marc D, Nandi P, Darlix JL (2001) The prion protein has RNA binding and chaperoning properties characteristic of nucleocapsid protein NCP7 of HIV-1. J Biol Chem 276:19301–19309
Giraldo R (2007) Defined DNA sequences promote the assembly of a bacterial protein into distinct amyloid nanostructures. Proc Natl Acad Sci USA 104:17388–17393
Goedert M (2001) a-synuclein and neurodegenerative diseases. Nature Rev Neurosci 2:492–501
Goedert M, Klug A, Crowther RA (2006) Tau protein, the paired helical filament and Alzheimer’s disease. J Alzheimers Dis 9:195–207
Goers J, Manning-Bog AB, McCormack AL, Millett IS, Doniach S, Di Monte DA, Uversky VN, Fink AL (2003) Nuclear localization of a-synuclein and its interaction with histones. Biochemistry 42:8465–8471
Gomes MP, Millen TA, Ferreira PS, e Silva NL, Vieira TC, Almeida MS, Silva JL, Cordeiro Y (2008a) Prion protein complexed to N2a cellular RNAs through its N-terminal domain forms aggregates and is toxic to murine neuroblastoma cells. J Biol Chem 283:19616–19625. The authors showed that PrP interacts with RNA extracted from neuroblastoma cells (N2aRNA) with nanomolar affinity and produces aggregates that are partially resistant to proteolysis upon this interaction. Only the N2aRNA extract induced PrP-RNA aggregates that reduced the viability of cultured cells; interaction with small RNAs did not result in toxic oligomers. Thus, it was proposed that the catalytic effect of RNA on PrP conversion depends on the RNA sequence/conformation
Gomes MP, Cordeiro Y, Silva JL (2008b) The peculiar interaction between mammalian prion protein and RNA. Prion 2:64–66
Gomes MP, Vieira TC, Cordeiro Y, Silva JL (2012) The role of RNA in mammalian prion protein conversion. WIREs RNA 3:415–428
Greenwood JA, Johnson GV (1995) Localization and in situ phosphorylation state of nuclear tau. Exp Cell Res 220:332–337
Grundke-Iqbal I, Iqbal K, Quinlan M, Tung YC, Zaidi MS, Wisniewski HM (1986) Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J Biol Chem 261:6084–6089
Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer’s amyloid beta-peptide. Nat Rev Mol Cell Biol 8:101–112
Harper JD, Lansbury PT Jr (1997) Models of amyloid seeding in Alzheimer’s disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu Rev Biochem 66:385–407
Harper JD, Lieber CM, Lansbury PT Jr. (1997) Atomic force microscopic imaging of seeded fibril formation and fibril branching by the Alzheimer’s disease amyloid-beta protein. Chem Biol 4951-4959
Hegde ML, Rao KS (2007) DNA induces folding in synuclein: Understanding the mechanism using chaperone properties of osmolites. Arch Biochem Biophys 464:57–69
Hegde ML, Anitha S, Latha KS, Mustak MS, Stein R, Ravid R, Rao KS (2003) First evidence for helical transitions in supercoiled DNA by amyloid-peptide (1-42) and aluminium. J Mol Neurosci 22:19–31
Ho LW, Carmichael J, Swartz J, Wyttenbach A, Rankin J, Rubinsztein DC (2001) The molecular biology of huntington’s disease. Psychol Med 31:3–14
Hua Q, He RQ (2002) Effect of phosphorylation and aggregation on tau binding to DNA Protein. Pept Lett 9:349–357
Hua Q, He RQ (2003) Tau could protect DNA double helix structure. Biochim Biophys Acta 1645:205–211
Ishimaru D, Andrade LR, Teixeira LS, Quesado PA, Maiolino LM, Lopez PM, Cordeiro Y, Costa LT, Heckl WM, Weissmüller G, Foguel D, Silva JL (2003) Fibrillar aggregates of the tumor suppressor p53 core domain. Biochemistry 42:9022–9027
Ishimaru D, Ano Bom AP, Lima LM, Quesado PA, Oyama MF, de Moura Gallo CV, Cordeiro Y, Silva JL (2009) Cognate DNA stabilizes the tumor suppressor p53 and prevents misfolding and aggregation. Biochemistry 48:6126–6135
Ivanyi-Nagy R, Davidovic L, Khandjian EW, Darlix JL (2005) Disordered RNA chaperone proteins: from functions to disease. Cell Mol Life Sci 62:1409–1417
Jaumot J, Eritja R, Navea S, Gargallo R (2009) Classification of nucleic acids structures by means of the chemometric analysis of circular dichroism spectra. Anal Chim Acta 642:117–126
Jiménez JS (2010) Protein-DNA interaction at the origin of neurological diseases: a hypothesis. J Alzheimers Dis 22:375–391
Johnstone EM, Bebbey LE, Stephenson D, Paul DC, Santerre RF, Clemens JA, Williams DC, Little SP (1996) Nuclear and cytoplasmic localization of the beta-amyloid peptide (1-43) in transfected 293 cells. Biochem Biophys Res Commun 220:710–718
Kalia LV, Kalia SK, McLean PJ, Lozano AM, Lang AE (2013) α-Synuclein oligomers and clinical implications for Parkinson disease. Ann Neurol 73:155–169
Kampers T, Friedhoff P, Biernat J, Mandelkow EM, Mandelkow E (1996) RNA stimulates aggregation of microtubule-associated protein tau into Alzheimer-like paired helical filaments. FEBS Lett 399:344–349
Kaplan B, Ratner V, Haas E (2003) Alpha-synuclein: its biological function and role in neurodegenerative diseases. J Mol Neurosci 20:83–92
Keefe AD, Pai S, Ellington A (2010) Aptamers as therapeutics. Nat Rev Drug Discov 9:537–550
Kegel KB, Meloni AR, Yi Y, Kim YJ, Doyle E, Cuiffo BG, Sapp E, Wang Y, Qin Z, Chen JD, Nevins JR, Aronin N, Figlia M (2002) Huntingtin is present in the nucleus, interacts with the transcriptional corepressor C-terminal binding protein, and represses transcription. J Biol Chem 277:7466–7476
King DJ, Safar JG, Legname G, Prusiner SB (2007) Thioaptamer interactions with prion proteins: sequence-specific and non-specific binding sites. J Mol Biol 369:1001–1014
Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95:6448–6453
Lima LM, Cordeiro Y, Tinoco LW, Marques AF, Oliveira CL, Sampath S, Kodali R, Choi G, Foguel D, Torriani I, Caughey B, Silva JL (2006) Structural insights into the interaction between prion protein and nucleic acid. Biochemistry 45:9180–9187. Interaction of a DNA sequence with recombinant PrP was characterized by NMR and SAXS, revealing that although direct binding seems to occur through the PrP C-terminal domain, the N-terminal region is also affected and loses flexibility
Liu C, Zhang Y (2011) Nucleic acid-mediated protein aggregation and assembly. Adv Protein Chem Struct Biol 84:1–40
Liu ML, Yu S, Yang J, Yin X, Zhao D (2007) RNA and CuCl2 induced conformational changes of the recombinant ovine prion protein. Mol Cell Biochem 294:197–203
Liu ML, Wen JJ, Xu XF, Zhao DM (2011) Neurotoxic effect of the complex of the ovine prion protein (OvPrP(C)) and RNA on the cultured rat cortical neurons. Neurochem Res 36:1863–1869
Luscombe NM, Laskowski RA, Thornton JM (2001) Amino acid-base interactions: a three-dimensional analysis of protein-DNA interactions at an atomic level. Nucleic Acids Res 29:2860–2874
Luthi-Carter R, Cha JH (2003) Mechanisms of transcriptional dysregulation in Huntington’s disease. Clin Neurosci Res 3:165–177
Ma J (2012) The role of cofactors in prion propagation and infectivity. PLoS Pathog 8:e1002589
Macedo B, Millen TA, Braga CA, Gomes MP, Ferreira PS, Kraineva J, Winter R, Silva JL, Cordeiro Y (2012) Nonspecific prion protein-nucleic acid interactions lead to different aggregates and cytotoxic species. Biochemistry 51:5402–5413
Maloney B, Lahiri DK (2011) The Alzheimer’s amyloid β-peptide (Aβ) binds a specific DNA Aβ-interacting domain (AβID) in the APP, BACE1, and APOE promoters in a sequence-specific manner: characterizing a new regulatory motif. Gene 488:1–12
Maroteaux L, Campanelli JT, Scheller RH (1988) Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J Neurosci 8:2804–2815
Martindale D, Hackam A, Wieczorek A, Ellerby L, Wellington C, McCutcheon K, Singaraja R, Kazemi-Esfarjani P, Devon R, Kim SU, Bredesen DE, Tufaro F, Hayden MR (1998) Length of huntingtin and its polyglutamine tract influences localization and frequency of intracellular aggregates. Nat Genet 18:150–154
Mashima T, Matsugami A, Nishikawa F, Nishikawa S, Katahira M (2009) Unique quadruplex structure and interaction of an RNA aptamer against bovine prion protein. Nucleic Acids Res 37:6249–6258
Mashima T, Nishikawa F, Kamatari YO, Fujiwara H, Saimura M, Nagata T, Kodaki T, Nishikawa S, Kuwata K, Katahira M (2013) Anti-prion activity of an RNA aptamer and its structural basis. Nucleic Acids Res 41:1355–1362
Nagai K (1996) RNA-protein complexes. Curr Opin Struct Biol 6:53–61
Nandi PK (1997) Interaction of prion peptide HuPrP106-126 with nucleic acid. Arch Virol 142:2537–2545
Nandi PK (1998) Polymerization of human prion peptide HuPrP 106-126 to amyloid in nucleic acid solution. Arch Virol 143:1251–1263
Nandi PK, Leclerc E (1999) Polymerization of murine recombinant prion protein in nucleic acid solution. Arch Virol 144:1751–1763
Nandi PK, Leclerc E, Nicole JC, Takahashi M (2002) DNA-induced partial unfolding of prion protein leads to its polymerisation to amyloid. J Mol Biol 322:153–161
Necula M, Chirita CN, Kuret J (2003) Rapid anionic micelle-mediated a-synuclein fibrillization in vitro. J Biol Chem 278:46674–46680
Ohyagi Y, Asahara H, Chui DH, Tsuruta Y, Sakae N, Miyoshi K, Yamada T, Kikuchi H, Taniwaki T, Murai H, Ikezoe K, Furuya H, Kawarabayashi T, Shoji M, Checler F, Iwaki T, Makifuchi T, Takeda K, Kira J, Tabira T (2005) Intracellular Abeta42 activates p53 promoter: a pathway to neurodegeneration in Alzheimer’s disease. FASEB J 19:255–257
Prusiner SB (1998) Prions. Proc Natl Acad Sci USA 95:13363–13383
Qu MH, Li H, Tian R, Nie CL, Liu Y, Han BS, He RQ (2004) Neuronal tau induces DNA conformational changes observed by atomic force microscopy. Neuroreport 15:2723–2727
Rega S, Stiewe T, Chang D-I, Pollmeier B, Esche H, Bardenheuer W, Marquitan G, Putzer BM (2001) Identification of the full-length huntingtin- interacting protein p231HBP/HYPB as a DNA-binding factor. Mol Cell Neurosci 18:68–79
Rhie A, Kirby L, Sayer N, Wellesley R, Disterer P, Sylvester I, Gill A, Hope J, James W, Tahiri-Alaoui A (2003) Characterization of 2′-fluoro-RNA aptamers that bind preferentially to disease-associated conformations of prion protein and inhibit conversion. J Biol Chem 278:39697–39705
Riek R, Hornemann S, Wider G, Billeter M, Glockshuber R, Wutrich K (1996) NMR structure of the mouse prion protein domain PrP(121-321). Nature 382:180–182
Rohs R, Jin X, West SM, Joshi R, Honig B, Mann RS (2010) Origins of specificity in protein-DNA recognition. Annu Rev Biochem 79:233–269
Ross CA, Poirier MA (2004) Protein aggregation and neurodegenerative disease. Nat Med 10:S10–17
Sayer NM, Cubin M, Rhie A, Bullock M, Tahiri-Alaoui A, James W (2004) Structural determinants of conformationally selective, prion-binding aptamers. J Biol Chem 279:13102–13109
Schilling G, Savonenko AV, Klevytska A, Morton JL, Tucker SM, Poirier M, Gale A, Chan N, Gonzales V, Slunt HH, Coonfield ML, Jenkins NA, Copeland NG, Ross CA, Borchelt DR (2004) Nuclear-targeting of mutant huntingtin fragments produces Huntington’s disease-like phenotypes in transgenic mice. Hum Mol Genet 13:1599–1610
Selkoe DJ (1997) Alzheimer’s disease: genotypes, phenotypes, and treatments. Science 275:630–631
Silva JL, Lima LM, Foguel D, Cordeiro Y (2008) Intriguing nucleic-acid-binding features of mammalian prion protein. Trends Biochem Sci 33:132–140
Silva JL, Vieira TC, Gomes MP, Bom AP, Lima LM, Freitas MS, Ishimaru D, Cordeiro Y, Foguel D (2010a) Ligand Binding and Hydration in Protein Misfolding: Insights from Studies of Prion and p53 Tumor Suppressor Proteins. Acc Chem Res 43:271–279
Silva JL, Gomes MP, Vieira TC, Cordeiro Y (2010b) PrP interactions with nucleic acids and glycosaminoglycans in function and disease. Front Biosci 15:132–150
Silva JL, Rangel LP, Costa DC, Cordeiro Y, De Moura Gallo CV (2013) Expanding the Prion Concept to Cancer Biology: Dominant-Negative Effect of Aggregates of Mutant p53 Tumor Suppressor. Biosci Rep. doi:10.1042/BSR20130065
Sipe JD, Benson MD, Buxbaum JN, Ikeda S, Merlini G, Saraiva MJ, Westermark P (2012) Amyloid fibril protein nomenclature: 2012 recommendations from the Nomenclature Committee of the International Society of Amyloidosis. Amyloid 19:167–170
Steffan JS, Kazantsev A, Spasic-Boskovic O, Greenwald M, Zhu Y-Z, Gohler H, Wanker EE, Bates GP, Housman DE, Thompson LM (2000) The Huntington’s disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc Natl Acad Sci USA 97:6763–6768
Sugars KL, Rubinsztein DC (2003) Transcriptional abnormalities in Huntington’s disease. Trends Genet 19:233–238
Suram A, Rao KS, Latha KS, Viswamitra MA (2002) First evidence to show the topological change of DNA from B-DNA to Z-DNA conformation in the hippocampus of Alzheimer’s brain. Neuromolecular Med 2:289–297
Syrjanen S, Heinonen O, Miettinen R, Paljarvi L, Syrjanen K, Riekkinen P (1991) Short biotinylated oligonucleotides bind non-specifically to senile plaques of Alzheimer’s disease. Neurosci Lett 130:89–91
Takahashi T, Tada K, Mihara H (2009) RNA aptamers selected against amyloid β-peptide (Aβ) inhibit the aggregation of Aβ. Mol Biosyst 5:986–991
Thayanidhi N, Helm JR, Nycz DC, Bentley M, Liang Y, Hay JC (2010) Alpha-synuclein delays endoplasmic reticulum (ER)-to-Golgi transport in mammalian cells by antagonizing ER/Golgi SNAREs. Mol Biol Cell 21:1850–1863
The Huntington’s Disease Collaboration Research Group (1993) A novel gene containing a trinucleotide repeats that is expanded and unstable on Huntington’s disease chromosomes. Cell 72:971–983
Thurston VC, Zinkowski RP, Binder LI (1996) Tau as a nucleolar protein in human nonneural cells in vitro and in vivo. Chromosoma 105:20–30
Uversky VN (2010) Mysterious oligomerization of the amyloidogenic proteins. FEBS J 277:2940–2953
Uversky VN, Li J, Fink AL (2001) Metal-triggered structural transformations, aggregation, and fibrillation of human a-synuclein. A possible molecular link between Parkinson’s disease and heavy metal exposure. J Biol Chem 276:44284–44296
Vasudevaraju P, Guerrero E, Hegde ML, Collen TB, Britton GB, Rao KS (2012) New evidence on α-synuclein and Tau binding to conformation and sequence specific GC* rich DNA: Relevance to neurological disorders. J Pharm Bioallied Sci 4:112–117
Vieira TC, Reynaldo DP, Gomes MP, Almeida MS, Cordeiro Y, Silva JL (2011) Heparin binding by murine recombinant prion protein leads to transient aggregation and formation of RNA-resistant species. J Am Chem Soc 133:334–344
Wang W, Perovic I, Chittuluru J, Kaganovich A, Nguyen LT, Liao J, Auclair JR, Johnson D, Landeru A, Simorellis AK, Ju S, Cookson MR, Asturias FJ, Agar JN, Webb BN, Kang C, Ringe D, Petsko GA, Pochapsky TC, Hoang QQ (2011) A soluble alpha-synuclein construct forms a dynamic tetramer. Proc Natl Acad Sci USA 108:17797–17802
Wei Y, Qu MH, Wang XS, Chen L, Wang DL, Liu Y, Hua Q, He RQ (2008) Binding to the minor groove of the double-strand, tau protein prevents DNA from damage by peroxidation. PLoS ONE 3:e2600
Weingarten MD, Lockwood AH, Hwo SY, Kirschner MW (1975) A protein factor essential for microtubule assembly. Proc Natl Acad Sci USA 72:1858–1862
Yin J, Chen R, Liu C (2009) Nucleic acid induced protein aggregation and its role in biology and pathology. Front Biosci 14:5084–5106
Yu H, Ren J, Qu X (2007) Time-dependent DNA condensation induced by amyloid beta-peptide. Biophys J 92:185–191
Acknowledgments
The laboratory work of Y.C. and J.L.S. was supported by grants from the Conselho Nacional de Desenvolvimento Cientifíco e Tecnológico (CNPq), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Financiadora de Estudos e Projetos (FINEP) of Brazil.
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Authors Yraima Cordeiro, Bruno Macedo, Jerson L. Silva and Mariana P. B. Gomes declare that they have no conflict of interest.
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Cordeiro, Y., Macedo, B., Silva, J.L. et al. Pathological implications of nucleic acid interactions with proteins associated with neurodegenerative diseases. Biophys Rev 6, 97–110 (2014). https://doi.org/10.1007/s12551-013-0132-0
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DOI: https://doi.org/10.1007/s12551-013-0132-0