Amyloidogenic Intrinsically Disordered Proteins: New Insights into Their Self-Assembly and Their Interaction with Membranes

. 2020 Aug 08 ; 10 (8) : . [epub] 20200808

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid32784399

Aβ, IAPP, α-synuclein, and prion proteins belong to the amyloidogenic intrinsically disordered proteins' family; indeed, they lack well defined secondary and tertiary structures. It is generally acknowledged that they are involved, respectively, in Alzheimer's, Type II Diabetes Mellitus, Parkinson's, and Creutzfeldt-Jakob's diseases. The molecular mechanism of toxicity is under intense debate, as many hypotheses concerning the involvement of the amyloid and the toxic oligomers have been proposed. However, the main role is represented by the interplay of protein and the cell membrane. Thus, the understanding of the interaction mechanism at the molecular level is crucial to shed light on the dynamics driving this phenomenon. There are plenty of factors influencing the interaction as mentioned above, however, the overall view is made trickier by the apparent irreproducibility and inconsistency of the data reported in the literature. Here, we contextualized this topic in a historical, and even more importantly, in a future perspective. We introduce two novel insights: the chemical equilibrium, always established in the aqueous phase between the free and the membrane phospholipids, as mediators of protein-transport into the core of the bilayer, and the symmetry-breaking of oligomeric aggregates forming an alternating array of partially ordered and disordered monomers.

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Chiti F., Dobson C.M. Protein Misfolding, Functional Amyloid, and Human Disease. Annu. Rev. Biochem. 2006;75:333–366. doi: 10.1146/annurev.biochem.75.101304.123901. PubMed DOI

Sengupta U., Nilson A.N., Kayed R. The Role of Amyloid-β Oligomers in Toxicity, Propagation, and Immunotherapy. EBioMedicine. 2016;6:42–49. doi: 10.1016/j.ebiom.2016.03.035. PubMed DOI PMC

Westermark P., Andersson A., Westermark G.T. Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiol. Rev. 2011;91:795–826. doi: 10.1152/physrev.00042.2009. PubMed DOI

Chiti F., Dobson C.M. Protein Misfolding, Amyloid Formation, and Human Disease: A Summary of Progress over the Last Decade. Annu. Rev. Biochem. 2017;86:27–68. doi: 10.1146/annurev-biochem-061516-045115. PubMed DOI

Scalisi S., Sciacca M.F.M., Zhavnerko G., Grasso D.M., Marletta G., La Rosa C. Self-Assembling Pathway of HiApp Fibrils within Lipid Bilayers. ChemBioChem. 2010;11:1856–1859. doi: 10.1002/cbic.201000090. PubMed DOI

Quist A., Doudevski I., Lin H., Azimova R., Ng D., Frangione B., Kagan B., Ghiso J., Lal R. Amyloid ion channels: A common structural link for protein-misfolding disease. Proc. Natl. Acad. Sci. USA. 2005;102:10427–10432. doi: 10.1073/pnas.0502066102. PubMed DOI PMC

Sciacca M.F.M., Kotler S.A., Brender J.R., Chen J., Lee D., Ramamoorthy A. Two-Step Mechanism of Membrane Disruption by Aβ through Membrane Fragmentation and Pore Formation. Biophys. J. 2012;103:702–710. doi: 10.1016/j.bpj.2012.06.045. PubMed DOI PMC

Finder V.H., Glockshuber R. Amyloid-β Aggregation. Neurodegener. Dis. 2007;4:13–27. doi: 10.1159/000100355. PubMed DOI

Thinakaran G., Koo E.H. Amyloid Precursor Protein Trafficking, Processing, and Function. J. Biol. Chem. 2008;283:29615–29619. doi: 10.1074/jbc.R800019200. PubMed DOI PMC

Goldgaber D., Lerman M.I., Mcbride W., SAFFIoTrI U., Gajdusek D.C. Characterization and Chromosomal Localimtion of a cDNA Encoding Brain Amyloid of Alzheimer’s Disease. Science. 1987;235:877–880. doi: 10.1126/science.3810169. PubMed DOI

Cole S.L., Vassar R. The Role of Amyloid Precursor Protein Processing by BACE1, the β-Secretase, in Alzheimer Disease Pathophysiology. J. Biol. Chem. 2008;283:29621–29625. doi: 10.1074/jbc.R800015200. PubMed DOI PMC

Buoso E., Lanni C., Schettini G., Govoni S., Racchi M. β-Amyloid precursor protein metabolism: Focus on the functions and degradation of its intracellular domain. Pharmacol. Res. 2010;62:308–317. doi: 10.1016/j.phrs.2010.05.002. PubMed DOI

Sisodia S.S. Beta-Amyloid precursor protein cleavage by a membrane-bound protease. Proc. Natl. Acad. Sci. USA. 1992;89:6075–6079. doi: 10.1073/pnas.89.13.6075. PubMed DOI PMC

Riek R., Güntert P., Döbeli H., Wipf B., Wüthrich K. NMR studies in aqueous solution fail to identify significant conformational differences between the monomeric forms of two Alzheimer peptides with widely different plaque-competence, Aβ(1-40) ox and Aβ(1-42) ox: NMR with Alzheimer peptides in aqueous solution. Eur. J. Biochem. 2001;268:5930–5936. doi: 10.1046/j.0014-2956.2001.02537.x. PubMed DOI

Jan A., Gokce O., Luthi-Carter R., Lashuel H.A. The Ratio of Monomeric to Aggregated Forms of Aβ40 and Aβ42 Is an Important Determinant of Amyloid-β Aggregation, Fibrillogenesis, and Toxicity. J. Biol. Chem. 2008;283:28176–28189. doi: 10.1074/jbc.M803159200. PubMed DOI PMC

Amaro M., Šachl R., Aydogan G., Mikhalyov I.I., Vácha R., Hof M. GM 1 Ganglioside Inhibits β-Amyloid Oligomerization Induced by Sphingomyelin. Angew. Chem. Int. Ed. 2016;55:9411–9415. doi: 10.1002/anie.201603178. PubMed DOI PMC

Kowall N.W., Mckee A.C. In Vivo Neurotoxicity of Beta-Amyloid [β(1-40)] and the β(25-35) Fragment. Neurobiol. Aging. 1992;13:537–542. PubMed

Sarkar D., Chakraborty I., Condorelli M., Ghosh B., Mass T., Weingarth M., Mandal A.K., La Rosa C., Subramanian V., Bhunia A. Self-Assembly and Neurotoxicity of β-Amyloid (21–40) Peptide Fragment: The Regulatory Role of GxxxG Motifs. ChemMedChem. 2020;15:293–301. doi: 10.1002/cmdc.201900620. PubMed DOI

Pannuzzo M., Milardi D., Raudino A., Karttunen M., La Rosa C. Analytical model and multiscale simulations of Aβ peptide aggregation in lipid membranes: Towards a unifying description of conformational transitions, oligomerization and membrane damage. Phys. Chem. Chem. Phys. 2013;15:8940–8951. doi: 10.1039/c3cp44539a. PubMed DOI

Sciacca M.F.M., Monaco I., La Rosa C., Milardi D. The active role of Ca 2+ ions in Aβ-mediated membrane damage. Chem. Commun. 2018;54:3629–3631. doi: 10.1039/C8CC01132J. PubMed DOI

Clark A., Nilsson M.R. Islet amyloid: A complication of islet dysfunction or an aetiological factor in Type 2 diabetes? Diabetologia. 2004;47:157–169. doi: 10.1007/s00125-003-1304-4. PubMed DOI

Hull R.L., Westermark G.T., Westermark P., Kahn S.E. Islet Amyloid: A Critical Entity in the Pathogenesis of Type 2 Diabetes. J. Clin. Endocrinol. Metab. 2004;89:3629–3643. doi: 10.1210/jc.2004-0405. PubMed DOI

Haataja L., Gurlo T., Huang C.J., Butler P.C. Islet Amyloid in Type 2 Diabetes, and the Toxic Oligomer Hypothesis. Endocr. Rev. 2008;29:303–316. doi: 10.1210/er.2007-0037. PubMed DOI PMC

Marzban L. Islet amyloid polypeptide and type 2 diabetes. Exp. Gerontol. 2003;38:347–351. doi: 10.1016/S0531-5565(03)00004-4. PubMed DOI

Cooper G.J., Willis A.C., Clark A., Turner R.C., Sim R.B., Reid K.B. Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients. Proc. Natl. Acad. Sci. USA. 1987;84:8628–8632. doi: 10.1073/pnas.84.23.8628. PubMed DOI PMC

Westermark P., Wernstedt C., Wilander E., Hayden D.W., O’Brien T.D., Johnson K.H. Amyloid fibrils in human insulinoma and islets of Langerhans of the diabetic cat are derived from a neuropeptide-like protein also present in normal islet cells. Proc. Natl. Acad. Sci. USA. 1987;84:3881–3885. doi: 10.1073/pnas.84.11.3881. PubMed DOI PMC

Milardi D., Pappalardo M., Pannuzzo M., Grasso D.M., Rosa C.L. The role of the Cys2-Cys7 disulfide bridge in the early steps of Islet amyloid polypeptide aggregation: A molecular dynamics study. Chem. Phys. Lett. 2008;463:396–399. doi: 10.1016/j.cplett.2008.07.110. DOI

Cooper G.J., Leighton B., Dimitriadis G.D., Parry-Billings M., Kowalchuk J.M., Howland K., Rothbard J.B., Willis A.C., Reid K.B. Amylin found in amyloid deposits in human type 2 diabetes mellitus may be a hormone that regulates glycogen metabolism in skeletal muscle. Proc. Natl. Acad. Sci. USA. 1988;85:7763–7766. doi: 10.1073/pnas.85.20.7763. PubMed DOI PMC

Cluck M.W., Chan C.Y., Adrian T.E. The Regulation of Amylin and Insulin Gene Expression and Secretion. Prancreas. 2005;30:1–14. PubMed

Gurlo T., Ryazantsev S., Huang C., Yeh M.W., Reber H.A., Hines O.J., O’Brien T.D., Glabe C.G., Butler P.C. Evidence for Proteotoxicity in β Cells in Type 2 Diabetes. Am. J. Pathol. 2010;176:861–869. doi: 10.2353/ajpath.2010.090532. PubMed DOI PMC

Milardi D., Sciacca M.F.M., Pappalardo M., Grasso D.M., La Rosa C. The role of aromatic side-chains in amyloid growth and membrane interaction of the islet amyloid polypeptide fragment LANFLVH. Eur. Biophys. J. 2011;40:1–12. doi: 10.1007/s00249-010-0623-x. PubMed DOI

Sciacca M.F., Pappalardo M., Attanasio F., Milardi D., La Rosa C., Grasso D.M. Are fibril growth and membrane damage linked processes? An experimental and computational study of IAPP 12–18 and IAPP 21–27 peptides. New J. Chem. 2010;34:200–207. doi: 10.1039/B9NJ00253G. DOI

Pannuzzo M., Raudino A., Milardi D., La Rosa C., Karttunen M. α-helical structures drive early stages of self-assembly of amyloidogenic amyloid polypeptide aggregate formation in membranes. Sci. Rep. 2013;3:2781. doi: 10.1038/srep02781. PubMed DOI PMC

Abedini A., Raleigh D.P. Destabilization of Human IAPP Amyloid Fibrils by Proline Mutations Outside of the Putative Amyloidogenic Domain: Is There a Critical Amyloidogenic Domain in Human IAPP? J. Mol. Biol. 2006;355:274–281. doi: 10.1016/j.jmb.2005.10.052. PubMed DOI

Pappalardo G., Milardi D., Magrì A., Attanasio F., Impellizzeri G., La Rosa C., Grasso D., Rizzarelli E. Environmental Factors Differently Affect Human and Rat IAPP: Conformational Preferences and Membrane Interactions of IAPP17–29 Peptide Derivatives. Chem. A Eur. J. 2007;13:10204–10215. doi: 10.1002/chem.200700576. PubMed DOI

Owen M.C., Gnutt D., Gao M., Wärmländer S.K.T.S., Jarvet J., Gräslund A., Winter R., Ebbinghaus S., Strodel B. Effects of in vivo conditions on amyloid aggregation. Chem. Soc. Rev. 2019;48:3946–3996. doi: 10.1039/C8CS00034D. PubMed DOI

Susa A.C., Wu C., Bernstein S.L., Dupuis N.F., Wang H., Raleigh D.P., Shea J.-E., Bowers M.T. Defining the Molecular Basis of Amyloid Inhibitors: Human Islet Amyloid Polypeptide–Insulin Interactions. J. Am. Chem. Soc. 2014;136:12912–12919. doi: 10.1021/ja504031d. PubMed DOI PMC

Jaikaran E.T.A.S., Nilsson M.R., Clark A. Pancreatic β-cell granule peptides form heteromolecular complexes which inhibit islet amyloid polypeptide fibril formation. Biochem. J. 2004;377:709–716. doi: 10.1042/bj20030852. PubMed DOI PMC

Knight J.D., Williamson J.A., Miranker A.D. Interaction of membrane-bound islet amyloid polypeptide with soluble and crystalline insulin. Protein Sci. 2008;17:1850–1856. doi: 10.1110/ps.036350.108. PubMed DOI PMC

Knight J.D., Miranker A.D. Phospholipid Catalysis of Diabetic Amyloid Assembly. J. Mol. Biol. 2004;341:1175–1187. doi: 10.1016/j.jmb.2004.06.086. PubMed DOI

Goedert M., Jakes R., Crowther R.A., Spillantini M.G. Parkinson’s Disease, Dementia with Lewy Bodies, and Multiple System Atrophy as α-Synucleinopathies. [(accessed on 7 August 2020)]; Available online: https://link.springer.com/protocol/10.1385/1-59259-142-6:33. DOI

Galvagnion C. The Role of Lipids Interacting with α-Synuclein in the Pathogenesis of Parkinson’s Disease. JPD. 2017;7:433–450. doi: 10.3233/JPD-171103. PubMed DOI

Shahmoradian S.H., Lewis A.J., Genoud C., Hench J., Moors T.E., Navarro P.P., Castaño-Díez D., Schweighauser G., Graff-Meyer A., Goldie K.N., et al. Lewy pathology in Parkinson’s disease consists of crowded organelles and lipid membranes. Nat. Neurosci. 2019;22:1099–1109. doi: 10.1038/s41593-019-0423-2. PubMed DOI

Lashuel H.A. Do Lewy bodies contain alpha-synuclein fibrils? and Does it matter? A brief history and critical analysis of recent reports. Neurobiol. Dis. 2020;141:104876. doi: 10.1016/j.nbd.2020.104876. PubMed DOI

Maroteaux L., Campanelli J., Scheller R. Synuclein: A neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J. Neurosci. 1988;8:2804–2815. doi: 10.1523/JNEUROSCI.08-08-02804.1988. PubMed DOI PMC

Shtilerman M.D., Ding T.T., Lansbury P.T. Molecular Crowding Accelerates Fibrillization of α-Synuclein: Could an Increase in the Cytoplasmic Protein Concentration Induce Parkinson’s Disease? Biochemistry. 2002;41:3855–3860. doi: 10.1021/bi0120906. PubMed DOI

Iwai A., Masliah E., Yoshimoto M., Ge N., Fianagan L., Kittei A., Saitoh T. The Precursor Protein of Non-Ap Component of Alzheimer’s Disease Amyloid Is a Presynaptic Protein of the Central Nervous System. Neuron. 1995;14:467–475. doi: 10.1016/0896-6273(95)90302-X. PubMed DOI

Cooper A.A. α-Synuclein Blocks ER-Golgi Traffic and Rab1 Rescues Neuron Loss in Parkinson’s Models. Science. 2006;313:324–328. doi: 10.1126/science.1129462. PubMed DOI PMC

Burré J. The Synaptic Function of α-Synuclein. JPD. 2015;5:699–713. doi: 10.3233/JPD-150642. PubMed DOI PMC

Burré J., Sharma M., Tsetsenis T., Buchman V., Etherton M.R., Südhof T.C. α-Synuclein Promotes SNARE-Complex Assembly in Vivo and in Vitro. Science. 2010;329:5. doi: 10.1126/science.1195227. PubMed DOI PMC

El-Agnaf O.M.A., Irvine G.B. Review: Formation and Properties of Amyloid-like Fibrils Derived from α-Synuclein and Related Proteins. J. Struct. Biol. 2000;130:300–309. doi: 10.1006/jsbi.2000.4262. PubMed DOI

Aarsland D., Marsh L., Schrag A. Neuropsychiatric symptoms in Parkinson’s disease. Mov. Disord. 2009;24:2175–2186. doi: 10.1002/mds.22589. PubMed DOI PMC

Aarsland D., Larsen J.P., Lim N.G., Janvin C., Karlsen K., Tandberg E., Cummings J.L. Range of neuropsychiatric disturbances in patients with Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry. 1999;67:492–496. doi: 10.1136/jnnp.67.4.492. PubMed DOI PMC

Lin Chua C.E., Tang B.L. α—synuclein and Parkinson’s disease: The first roadblock. J. Cell. Mol. Med. 2006;10:828–837. doi: 10.2755/jcmm010.004.04. PubMed DOI

George J.M., Jin H., Woods W.S., Clayton D.F. Characterization of a novel protein regulated during the critical period for song learning in the zebra finch. Neuron. 1995;15:361–372. doi: 10.1016/0896-6273(95)90040-3. PubMed DOI

Beyer K. Mechanistic aspects of Parkinson’s disease: α-synuclein and the biomembrane. Cell Biochem. Biophys. 2007;47:285–299. doi: 10.1007/s12013-007-0014-9. PubMed DOI

Fusco G., De Simone A., Gopinath T., Vostrikov V., Vendruscolo M., Dobson C.M., Veglia G. Direct observation of the three regions in α-synuclein that determine its membrane-bound behaviour. Nat. Commun. 2014;5:3827. doi: 10.1038/ncomms4827. PubMed DOI PMC

Bodner C.R., Dobson C.M., Bax A. Multiple Tight Phospholipid-Binding Modes of α-Synuclein Revealed by Solution NMR Spectroscopy. J. Mol. Biol. 2009;390:775–790. doi: 10.1016/j.jmb.2009.05.066. PubMed DOI PMC

Jang H., Connelly L., Teran Arce F., Ramachandran S., Kagan B.L., Lal R., Nussinov R. Mechanisms for the Insertion of Toxic, Fibril-like β-Amyloid Oligomers into the Membrane. J. Chem. Theory Comput. 2013;9:822–833. doi: 10.1021/ct300916f. PubMed DOI PMC

O’Leary E.I., Lee J.C. Interplay between α-synuclein amyloid formation and membrane structure. Biochim. Biophys. Acta (BBA) Proteins Proteom. 2019;1867:483–491. doi: 10.1016/j.bbapap.2018.09.012. PubMed DOI PMC

Conway K.A., Lee S.-J., Rochet J.-C., Ding T.T., Williamson R.E., Lansbury P.T. Acceleration of oligomerization, not fibrillization, is a shared property of both α-synuclein mutations linked to early-onset Parkinson’s disease: Implications for pathogenesis and therapy. Proc. Natl. Acad. Sci. USA. 2000;97:571–576. doi: 10.1073/pnas.97.2.571. PubMed DOI PMC

Conway K.A., Harper J.D., Lansbury P.T. Accelerated in vitro fibril formation by a mutant α-synuclein linked to early-onset Parkinson disease. Nat. Med. 1998;4:1318–1320. doi: 10.1038/3311. PubMed DOI

Nussbaum R.L., Polymeropoulos M.H. Genetics of Parkinson’s disease. Cold Spring Harb. Perspect. Med. 1997;6:1687–1691. doi: 10.1093/hmg/6.10.1687. PubMed DOI

Shimura H. Ubiquitination of a New Form of alpha-Synuclein by Parkin from Human Brain: Implications for Parkinson’s Disease. Science. 2001;293:263–269. doi: 10.1126/science.1060627. PubMed DOI

Minton A.P. Implications of macromolecular crowding for protein assembly. Curr. Opin. Struct. Biol. 2000;10:34–39. doi: 10.1016/S0959-440X(99)00045-7. PubMed DOI

Ellis R.J. Macromolecular crowding: An important but neglected aspect of the intracellular environment. Curr. Opin. Struct. Biol. 2001;11:114–119. doi: 10.1016/S0959-440X(00)00172-X. PubMed DOI

Hashimoto M., Rockenstein E., Mante M., Mallory M., Masliah E. beta-Synuclein inhibits alpha-synuclein aggregation: A possible role as an anti-parkinsonian factor. Neuron. 2001;32:213–223. doi: 10.1016/S0896-6273(01)00462-7. PubMed DOI

Uversky V.N., Li J., Souillac P., Millett I.S., Doniach S., Jakes R., Goedert M., Fink A.L. Biophysical Properties of the Synucleins and Their Propensities to Fibrillate: INHIBITION OF α-SYNUCLEIN ASSEMBLY BY β- AND γ-SYNUCLEINS. J. Biol. Chem. 2002;277:11970–11978. doi: 10.1074/jbc.M109541200. PubMed DOI

Tsigelny I.F., Bar-On P., Sharikov Y., Crews L., Hashimoto M., Miller M.A., Keller S.H., Platoshyn O., Yuan J.X.-J., Masliah E. Dynamics of α-synuclein aggregation and inhibition of pore-like oligomer development by β-synuclein: Modeling of α-syn oligomer formation. FEBS J. 2007;274:1862–1877. doi: 10.1111/j.1742-4658.2007.05733.x. PubMed DOI

Sung Y., Eliezer D. Residual Structure, Backbone Dynamics, and Interactions within the Synuclein Family. J. Mol. Biol. 2007;372:689–707. doi: 10.1016/j.jmb.2007.07.008. PubMed DOI PMC

Sode K., Ochiai S., Kobayashi N., Usuzaka E. Effect of Reparation of Repeat Sequences in the Human α-Synuclein on Fibrillation Ability. Int. J. Biol. Sci. 2007;3:1–7. doi: 10.7150/ijbs.3.1. PubMed DOI PMC

Prusiner S.B. Molecular Biology of Prion Diseases. Science. 1991;252:8. doi: 10.1126/science.1675487. PubMed DOI

Cohen F.E., Prusiner S.B. Pathologic Conformations of Prion Proteins. Annu. Rev. Biochem. 1998;67:793–819. doi: 10.1146/annurev.biochem.67.1.793. PubMed DOI

Colby D.W., Prusiner S.B. Prions. Cold Spring Harb. Perspect. Biol. 2011;3:a006833. doi: 10.1101/cshperspect.a006833. PubMed DOI PMC

Abskharon R., Wang F., Wohlkonig A., Ruan J., Soror S., Giachin G., Pardon E., Zou W., Legname G., Ma J., et al. Structural evidence for the critical role of the prion protein hydrophobic region in forming an infectious prion. PLoS Pathog. 2019;15:e1008139. doi: 10.1371/journal.ppat.1008139. PubMed DOI PMC

Pan K.-M., Baldwin M., Nguyen J., Gasset M., Mehlhorn I., Huang Z., Fletterick R.J., Cohenu F.E., Prusiner S.B. Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. USA. 1993;90:10962–10966. doi: 10.1073/pnas.90.23.10962. PubMed DOI PMC

Zhang J., Zhang Y. Molecular dynamics studies on 3D structures of the hydrophobic region PrP (109–136) Acta Biochim. Biophys. Sin. 2013;45:509–519. doi: 10.1093/abbs/gmt031. PubMed DOI

Garnier J., Osguthorpe D.J., Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J. Mol. Biol. 1978;120:97–120. doi: 10.1016/0022-2836(78)90297-8. PubMed DOI

Riek R., Wider G., Billeter M., Hornemann S., Glockshuber R., Wuthrich K. Prion protein NMR structure and familial human spongiform encephalopathies. Proc. Natl. Acad. Sci. USA. 1998;95:11667–11672. doi: 10.1073/pnas.95.20.11667. PubMed DOI PMC

Donne D.G., Viles J.H., Groth D., Mehlhorn I., James T.L., Cohen F.E., Prusiner S.B., Wright P.E., Dyson H.J. Structure of the recombinant full-length hamster prion protein PrP(29-231): The N terminus is highly flexible. Proc. Natl. Acad. Sci. USA. 1997;94:13452–13457. doi: 10.1073/pnas.94.25.13452. PubMed DOI PMC

Liu H., Farr-Jones S., Ulyanov N.B., Llinas M., Marqusee S., Groth D., Cohen F.E., Prusiner S.B., James T.L. Solution Structure of Syrian Hamster Prion Protein rPrP(90−231) Biochemistry. 1999;38:5362–5377. doi: 10.1021/bi982878x. PubMed DOI

Riek R., Hornemann S., Wider G., Glockshuber R., Wüthrich K. NMR characterization of the full-length recombinant murine prion protein, m PrP(23-231) FEBS Lett. 1997;413:282–288. doi: 10.1016/S0014-5793(97)00920-4. PubMed DOI

Zahn R., Liu A., Luhrs T., Riek R., von Schroetter C., Lopez Garcia F., Billeter M., Calzolai L., Wider G., Wuthrich K. NMR solution structure of the human prion protein. Proc. Natl. Acad. Sci. USA. 2000;97:145–150. doi: 10.1073/pnas.97.1.145. PubMed DOI PMC

Cho K.R., Huang Y., Yu S., Yin S., Plomp M., Qiu S.R., Lakshminarayanan R., Moradian-Oldak J., Sy M.-S., De Yoreo J.J. A Multistage Pathway for Human Prion Protein Aggregation in Vitro: From Multimeric Seeds to β-Oligomers and Nonfibrillar Structures. J. Am. Chem. Soc. 2011;133:8586–8593. doi: 10.1021/ja1117446. PubMed DOI PMC

Bocharova O.V., Breydo L., Parfenov A.S., Salnikov V.V., Baskakov I.V. In vitro Conversion of Full-length Mammalian Prion Protein Produces Amyloid Form with Physical Properties of PrPSc. J. Mol. Biol. 2005;346:645–659. doi: 10.1016/j.jmb.2004.11.068. PubMed DOI

Baskakov I.V., Bocharova O.V. In Vitro Conversion of Mammalian Prion Protein into Amyloid Fibrils Displays Unusual Features. Biochemistry. 2005;44:2339–2348. doi: 10.1021/bi048322t. PubMed DOI

Safar J., Wille H., Itri V., Groth D., Serban H., Torchia M., Cohen F.E., Prusiner S.B. Eight prion strains have PrPSc molecules with different conformations. Nat. Med. 1998;4:1157–1165. doi: 10.1038/2654. PubMed DOI

Prusiner S.B., McKinley M.P., Bowman K.A., Bolton D.C., Bendheim P.E., Groth D.F., Glenner G.G. Scrapie prions aggregate to form amyloid-like birefringent rods. Cell. 1983;35:349–358. doi: 10.1016/0092-8674(83)90168-X. PubMed DOI

Wille H., Michelitsch M.D., Guénebaut V., Supattapone S., Serban A., Cohen F.E., Agard D.A., Prusiner S.B. Structural studies of the scrapie prion protein by electron crystallography. Proc. Natl. Acad. Sci. USA. 2002;99:3563–3568. doi: 10.1073/pnas.052703499. PubMed DOI PMC

Chesebro B., Trifilo M., Race R., Meade-White K., Teng C., Lacasse R., Raymond L., Favara C., Baron G., Priola S., et al. Anchorless Prion Protein Results in Infectious Amyloid Disease Without Clinical Scrapie. Science. 2005;308:1435–1439. doi: 10.1126/science.1110837. PubMed DOI

Pappalardo M., Milardi D., Grasso D., La Rosa C. Steered molecular dynamics studies reveal different unfolding pathways of prions from mammalian and non-mammalian species. New J. Chem. 2007;31:901–905. doi: 10.1039/b700764g. DOI

Lashuel H.A., Lansbury P.T. Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins? Q. Rev. Biophys. 2006;39:167–201. doi: 10.1017/S0033583506004422. PubMed DOI

Hebda J.A., Miranker A.D. The Interplay of Catalysis and Toxicity by Amyloid Intermediates on Lipid Bilayers: Insights from Type II Diabetes. Annu. Rev. Biophys. 2009;38:125–152. doi: 10.1146/annurev.biophys.050708.133622. PubMed DOI

Hirakura Y., Yiu W.W., Yamamoto A., Kagan B.L. Amyloid peptide channels: Blockade by zinc and inhibition by Congo red (amyloid channel block) Amyloid. 2000;7:194–199. doi: 10.3109/13506120009146834. PubMed DOI

Sciacca M.F.M., Milardi D., Messina G.M.L., Marletta G., Brender J.R., Ramamoorthy A., La Rosa C. Cations as Switches of Amyloid-Mediated Membrane Disruption Mechanisms: Calcium and IAPP. Biophys. J. 2013;104:173–184. doi: 10.1016/j.bpj.2012.11.3811. PubMed DOI PMC

Sciacca M.F.M., Brender J.R., Lee D.-K., Ramamoorthy A. Phosphatidylethanolamine Enhances Amyloid Fiber-Dependent Membrane Fragmentation. Biochemistry. 2012;51:7676–7684. doi: 10.1021/bi3009888. PubMed DOI PMC

Engel M.F.M., Khemtemourian L., Kleijer C.C., Meeldijk H.J.D., Jacobs J., Verkleij A.J., de Kruijff B., Killian J.A., Hoppener J.W.M. Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane. Proc. Natl. Acad. Sci. USA. 2008;105:6033–6038. doi: 10.1073/pnas.0708354105. PubMed DOI PMC

Zhu M., Li J., Fink A.L. The Association of α-Synuclein with Membranes Affects Bilayer Structure, Stability, and Fibril Formation. J. Biol. Chem. 2003;278:40186–40197. doi: 10.1074/jbc.M305326200. PubMed DOI

Sanghera N., Pinheiro T.J.T. Binding of prion protein to lipid membranes and implications for prion conversion. J. Mol. Biol. 2002;315:1241–1256. doi: 10.1006/jmbi.2001.5322. PubMed DOI

Terzi E., Holzemann G. Alzheimer, & Amyloid Peptide 25-35: Electrostatic Interactions with Phospholipid Membranest. Biochemistry. 1994;33:7434–7441. PubMed

Hane F., Drolle E., Gaikwad R., Faught E., Leonenko Z. Amyloid-β Aggregation on Model Lipid Membranes: An Atomic Force Microscopy Study. JAD. 2011;26:485–494. doi: 10.3233/JAD-2011-102112. PubMed DOI

Terzi E., Hölzemann G., Seelig J. Interaction of Alzheimer β-Amyloid Peptide(1−40) with Lipid Membranes. Biochemistry. 1997;36:14845–14852. doi: 10.1021/bi971843e. PubMed DOI

Sciacca M.F., Pappalardo M., Milardi D., Grasso D.M., La Rosa C. Calcium-activated membrane interaction of the islet amyloid polypeptide: Implications in the pathogenesis of type II diabetes mellitus. Arch. Biochem. Biophys. 2008;477:291–298. doi: 10.1016/j.abb.2008.06.018. PubMed DOI

Brender J.R., Krishnamoorthy J., Messina G.M.L., Deb A., Vivekanandan S., Rosa C.L., Penner-Hahn J.E., Ramamoorthy A. Zinc stabilization of prefibrillar oligomers of human islet amyloid polypeptide. Chem. Commun. 2013;49:3339–3341. doi: 10.1039/c3cc40383a. PubMed DOI

Ahyayauch H., de la Arada I., Masserini M.E., Arrondo J.L.R., Goñi F.M., Alonso A. The Binding of Aβ42 Peptide Monomers to Sphingomyelin/Cholesterol/Ganglioside Bilayers Assayed by Density Gradient Ultracentrifugation. Int. J. Mol. Sci. 2020;21:1674. doi: 10.3390/ijms21051674. PubMed DOI PMC

Wakabayashi M., Matsuzaki K. Ganglioside-induced amyloid formation by human islet amyloid polypeptide in lipid rafts. FEBS Lett. 2009;583:2854–2858. doi: 10.1016/j.febslet.2009.07.044. PubMed DOI

Hoshino T., Mahmood M.I., Mori K., Matsuzaki K. Binding and Aggregation Mechanism of Amyloid β-Peptides onto the GM1 Ganglioside-Containing Lipid Membrane. J. Phys. Chem. B. 2013;117:8085–8094. doi: 10.1021/jp4029062. PubMed DOI

Wakabayashi M., Okada T., Kozutsumi Y., Matsuzaki K. GM1 ganglioside-mediated accumulation of amyloid β-protein on cell membranes. Biochem. Biophys. Res. Commun. 2005;328:1019–1023. doi: 10.1016/j.bbrc.2005.01.060. PubMed DOI

Di Scala C., Troadec J.-D., Lelièvre C., Garmy N., Fantini J., Chahinian H. Mechanism of cholesterol-assisted oligomeric channel formation by a short Alzheimer β-amyloid peptide. J. Neurochem. 2014;128:186–195. doi: 10.1111/jnc.12390. PubMed DOI

Sciacca M.F.M., Lolicato F., Di Mauro G., Milardi D., D’Urso L., Satriano C., Ramamoorthy A., La Rosa C. The Role of Cholesterol in Driving IAPP-Membrane Interactions. Biophys. J. 2016;111:140–151. doi: 10.1016/j.bpj.2016.05.050. PubMed DOI PMC

Yu X., Zheng J. Cholesterol Promotes the Interaction of Alzheimer β-Amyloid Monomer with Lipid Bilayer. J. Mol. Biol. 2012;421:561–571. doi: 10.1016/j.jmb.2011.11.006. PubMed DOI

Choo-Smith L.-P., Garzon-Rodriguez W., Glabe C.G., Surewicz W.K. Acceleration of Amyloid Fibril Formation by Specific Binding of Aβ-(1–40) Peptide to Ganglioside-containing Membrane Vesicles. J. Biol. Chem. 1997;272:22987–22990. doi: 10.1074/jbc.272.37.22987. PubMed DOI

Ji S.-R., Wu Y., Sui S. Cholesterol Is an Important Factor Affecting the Membrane Insertion of β-Amyloid Peptide (Aβ1–40), Which May Potentially Inhibit the Fibril Formation. J. Biol. Chem. 2002;277:6273–6279. doi: 10.1074/jbc.M104146200. PubMed DOI

Dias C.L., Jalali S., Yang Y., Cruz L. Role of Cholesterol on Binding of Amyloid Fibrils to Lipid Bilayers. J. Phys. Chem. B. 2020;124:3036–3042. doi: 10.1021/acs.jpcb.0c00485. PubMed DOI

Chi E.Y., Ege C., Winans A., Majewski J., Wu G., Kjaer K., Lee K.Y.C. Lipid membrane templates the ordering and induces the fibrillogenesis of Alzheimer’s disease amyloid-β peptide: Lipid Membrane Templates Aβ Fibrillogenesis. Proteins. 2008;72:1–24. doi: 10.1002/prot.21887. PubMed DOI

Soong R., Brender J.R., Macdonald P.M., Ramamoorthy A. Association of Highly Compact Type II Diabetes Related Islet Amyloid Polypeptide Intermediate Species at Physiological Temperature Revealed by Diffusion NMR Spectroscopy. J. Am. Chem. Soc. 2009;131:7079–7085. doi: 10.1021/ja900285z. PubMed DOI

Brender J.R., Lee E.L., Cavitt M.A., Gafni A., Steel D.G., Ramamoorthy A. Amyloid Fiber Formation and Membrane Disruption are Separate Processes Localized in Two Distinct Regions of IAPP, the Type-2-Diabetes-Related Peptide. J. Am. Chem. Soc. 2008;130:6424–6429. doi: 10.1021/ja710484d. PubMed DOI PMC

Terzi E. Self-association of β-Amyloid Peptide (1–40) in Solution and Binding to Lipid Membranes. J. Mol. Biol. 1998;252:633–642. doi: 10.1006/jmbi.1995.0525. PubMed DOI

Morillas M., Swietnicki W., Gambetti P., Surewicz W.K. Membrane Environment Alters the Conformational Structure of the Recombinant Human Prion Protein. J. Biol. Chem. 1999;274:36859–36865. doi: 10.1074/jbc.274.52.36859. PubMed DOI

Domanov Y.A., Kinnunen P.K.J. Islet Amyloid Polypeptide Forms Rigid Lipid–Protein Amyloid Fibrils on Supported Phospholipid Bilayers. J. Mol. Biol. 2008;376:42–54. doi: 10.1016/j.jmb.2007.11.077. PubMed DOI

Jayasinghe S.A., Langen R. Lipid Membranes Modulate the Structure of Islet Amyloid Polypeptide. Biochemistry. 2005;44:12113–12119. doi: 10.1021/bi050840w. PubMed DOI

Sparr E., Engel M.F.M., Sakharov D.V., Sprong M., Jacobs J., de Kruijff B., Höppener J.W.M., Antoinette Killian J. Islet amyloid polypeptide-induced membrane leakage involves uptake of lipids by forming amyloid fibers. FEBS Lett. 2004;577:117–120. doi: 10.1016/j.febslet.2004.09.075. PubMed DOI

Bucciantini M., Cecchi C. Biological Membranes as Protein Aggregation Matrices and Targets of Amyloid Toxicity. In: Bross P., Gregersen N., editors. Protein Misfolding and Cellular Stress in Disease and Aging. Volume 648. Humana Press; Totowa, NJ, USA: 2010. pp. 231–243. Methods in Molecular Biology. PubMed

Sciacca M.F.M., Tempra C., Scollo F., Milardi D., La Rosa C. Amyloid growth and membrane damage: Current themes and emerging perspectives from theory and experiments on Aβ and hIAPP. Biochim. Biophys. Acta (BBA) Biomembr. 2018;1860:1625–1638. doi: 10.1016/j.bbamem.2018.02.022. PubMed DOI

Bokvist M., Lindström F., Watts A., Gröbner G. Two Types of Alzheimer’s β-Amyloid (1–40) Peptide Membrane Interactions: Aggregation Preventing Transmembrane Anchoring Versus Accelerated Surface Fibril Formation. J. Mol. Biol. 2004;335:1039–1049. doi: 10.1016/j.jmb.2003.11.046. PubMed DOI

Fink A.L. The Aggregation and Fibrillation of α-Synuclein. Acc. Chem. Res. 2006;39:628–634. doi: 10.1021/ar050073t. PubMed DOI

Ambadi Thody S., Mathew M.K., Udgaonkar J.B. Mechanism of aggregation and membrane interactions of mammalian prion protein. Biochim. Biophys. Acta (BBA) Biomembr. 2018;1860:1927–1935. doi: 10.1016/j.bbamem.2018.02.031. PubMed DOI

Scollo F., Tempra C., Lolicato F., Sciacca M.F.M., Raudino A., Milardi D., La Rosa C. Phospholipids Critical Micellar Concentrations Trigger Different Mechanisms of Intrinsically Disordered Proteins Interaction with Model Membranes. J. Phys. Chem. Lett. 2018;9:5125–5129. doi: 10.1021/acs.jpclett.8b02241. PubMed DOI

La Rosa C., Scalisi S., Lolicato F., Pannuzzo M., Raudino A. Lipid-assisted protein transport: A diffusion-reaction model supported by kinetic experiments and molecular dynamics simulations. J. Chem. Phys. 2016;144:184901. doi: 10.1063/1.4948323. PubMed DOI

Milardi D., Sciacca M.F.M., Randazzo L., Raudino A., La Rosa C. The Role of Calcium, Lipid Membranes and Islet Amyloid Polypeptide in the Onset of Type 2 Diabetes: Innocent Bystanders or Partners in a Crime? Front. Endocrinol. 2014;5 doi: 10.3389/fendo.2014.00216. PubMed DOI PMC

Brender J.R., Hartman K., Nanga R.P.R., Popovych N., de la Salud Bea R., Vivekanandan S., Marsh E.N.G., Ramamoorthy A. Role of Zinc in Human Islet Amyloid Polypeptide Aggregation. J. Am. Chem. Soc. 2010;132:8973–8983. doi: 10.1021/ja1007867. PubMed DOI PMC

Hindo S.S., Mancino A.M., Braymer J.J., Liu Y., Vivekanandan S., Ramamoorthy A., Lim M.H. Small Molecule Modulators of Copper-Induced Aβ Aggregation. J. Am. Chem. Soc. 2009;131:16663–16665. doi: 10.1021/ja907045h. PubMed DOI PMC

Ladiwala A.R.A., Lin J.C., Bale S.S., Marcelino-Cruz A.M., Bhattacharya M., Dordick J.S., Tessier P.M. Resveratrol Selectively Remodels Soluble Oligomers and Fibrils of Amyloid Aβ into Off-pathway Conformers. J. Biol. Chem. 2010;285:24228–24237. doi: 10.1074/jbc.M110.133108. PubMed DOI PMC

Bieschke J., Herbst M., Wiglenda T., Friedrich R.P., Boeddrich A., Schiele F., Kleckers D., Lopez del Amo J.M., Grüning B.A., Wang Q., et al. Small-molecule conversion of toxic oligomers to nontoxic β-sheet–rich amyloid fibrils. Nat. Chem. Biol. 2012;8:93–101. doi: 10.1038/nchembio.719. PubMed DOI

Wärmländer S., Tiiman A., Abelein A., Luo J., Jarvet J., Söderberg K.L., Danielsson J., Gräslund A. Biophysical Studies of the Amyloid β-Peptide: Interactions with Metal Ions and Small Molecules. ChemBioChem. 2013;14:1692–1704. doi: 10.1002/cbic.201300262. PubMed DOI

Yoo S.I., Yang M., Brender J.R., Subramanian V., Sun K., Joo N.E., Jeong S.-H., Ramamoorthy A., Kotov N.A. Inhibition of Amyloid Peptide Fibrillation by Inorganic Nanoparticles: Functional Similarities with Proteins. Angew. Chem. Int. Ed. 2011;50:5110–5115. doi: 10.1002/anie.201007824. PubMed DOI PMC

D’Urso L., Condorelli M., Puglisi O., Tempra C., Lolicato F., Compagnini G., Rosa C.L. Detection and characterization at nM concentration of oligomers formed by hIAPP, Aβ(1–40) and their equimolar mixture using SERS and MD simulations. Phys. Chem. Chem. Phys. 2018;20:20588–20596. doi: 10.1039/C7CP08552D. PubMed DOI

Sciacca M.F.M., Romanucci V., Zarrelli A., Monaco I., Lolicato F., Spinella N., Galati C., Grasso G., D’Urso L., Romeo M., et al. Inhibition of Aβ Amyloid Growth and Toxicity by Silybins: The Crucial Role of Stereochemistry. ACS Chem. Neurosci. 2017;8:1767–1778. doi: 10.1021/acschemneuro.7b00110. PubMed DOI

Hyung S.-J., DeToma A.S., Brender J.R., Lee S., Vivekanandan S., Kochi A., Choi J.-S., Ramamoorthy A., Ruotolo B.T., Lim M.H. Insights into antiamyloidogenic properties of the green tea extract (-)-epigallocatechin-3-gallate toward metal-associated amyloid- species. Proc. Natl. Acad. Sci. USA. 2013;110:3743–3748. doi: 10.1073/pnas.1220326110. PubMed DOI PMC

Sciacca M.F., Chillemi R., Sciuto S., Pappalardo M., Rosa C.L., Grasso D., Milardi D. Interactions of two O-phosphorylresveratrol derivatives with model membranes. Arch. Biochem. Biophys. 2012;521:111–116. doi: 10.1016/j.abb.2012.03.022. PubMed DOI

Sciacca M.F.M., Chillemi R., Sciuto S., Greco V., Messineo C., Kotler S.A., Lee D.-K., Brender J.R., Ramamoorthy A., La Rosa C., et al. A blend of two resveratrol derivatives abolishes hIAPP amyloid growth and membrane damage. Biochim. Biophys. Acta (BBA) Biomembr. 2018;1860:1793–1802. doi: 10.1016/j.bbamem.2018.03.012. PubMed DOI

Marsh D. Handbook of Lipid Bilayer. 2nd ed. CRC Press; Boca Raton, FL, USA: 2013.

Korshavn K.J., Satriano C., Lin Y., Zhang R., Dulchavsky M., Bhunia A., Ivanova M.I., Lee Y.-H., La Rosa C., Lim M.H., et al. Reduced Lipid Bilayer Thickness Regulates the Aggregation and Cytotoxicity of Amyloid-β. J. Biol. Chem. 2017;292:4638–4650. doi: 10.1074/jbc.M116.764092. PubMed DOI PMC

Sunde M., Blake C. Advances in Protein Chemistry. Volume 50. Elsevier; Amsterdam, The Netherlands: 1997. The Structure of Amyloid Fibrils by Electron Microscopy and X-Ray Diffraction; pp. 123–159. PubMed

Fändrich M. Oligomeric Intermediates in Amyloid Formation: Structure Determination and Mechanisms of Toxicity. J. Mol. Biol. 2012;421:427–440. doi: 10.1016/j.jmb.2012.01.006. PubMed DOI

Tuttle M.D., Comellas G., Nieuwkoop A.J., Covell D.J., Berthold D.A., Kloepper K.D., Courtney J.M., Kim J.K., Barclay A.M., Kendall A., et al. Solid-state NMR structure of a pathogenic fibril of full-length human α-synuclein. Nat. Struct. Mol. Biol. 2016;23:409–415. doi: 10.1038/nsmb.3194. PubMed DOI PMC

Vilar M., Chou H.-T., Luhrs T., Maji S.K., Riek-Loher D., Verel R., Manning G., Stahlberg H., Riek R. The fold of -synuclein fibrils. Proc. Natl. Acad. Sci. USA. 2008;105:8637–8642. doi: 10.1073/pnas.0712179105. PubMed DOI PMC

Luhrs T., Ritter C., Adrian M., Riek-Loher D., Bohrmann B., Dobeli H., Schubert D., Riek R. 3D structure of Alzheimer’s amyloid- (1-42) fibrils. Proc. Natl. Acad. Sci. USA. 2005;102:17342–17347. doi: 10.1073/pnas.0506723102. PubMed DOI PMC

Kollmer M., Close W., Funk L., Rasmussen J., Bsoul A., Schierhorn A., Schmidt M., Sigurdson C.J., Jucker M., Fändrich M. Cryo-EM structure and polymorphism of Aβ amyloid fibrils purified from Alzheimer’s brain tissue. Nat. Commun. 2019;10:4760. doi: 10.1038/s41467-019-12683-8. PubMed DOI PMC

Guerrero-Ferreira R., Taylor N.M., Arteni A.-A., Kumari P., Mona D., Ringler P., Britschgi M., Lauer M.E., Makky A., Verasdonck J., et al. Two new polymorphic structures of human full-length alpha-synuclein fibrils solved by cryo-electron microscopy. eLife. 2019;8:e48907. doi: 10.7554/eLife.48907. PubMed DOI PMC

Guerrero-Ferreira R., Taylor N.M., Mona D., Ringler P., Lauer M.E., Riek R., Britschgi M., Stahlberg H. Cryo-EM structure of alpha-synuclein fibrils. eLife. 2018;7:e36402. doi: 10.7554/eLife.36402. PubMed DOI PMC

Van den Akker C.C., Deckert-Gaudig T., Schleeger M., Velikov K.P., Deckert V., Bonn M., Koenderink G.H. Nanoscale Heterogeneity of the Molecular Structure of Individual hIAPP Amyloid Fibrils Revealed with Tip-Enhanced Raman Spectroscopy. Small. 2015;11:4131–4139. doi: 10.1002/smll.201500562. PubMed DOI

La Rosa C., Condorelli M., Compagnini G., Lolicato F., Milardi D., Do T.N., Karttunen M., Pannuzzo M., Ramamoorthy A., Fraternali F., et al. Symmetry-breaking transitions in the early steps of protein self-assembly. Eur. Biophys. J. 2020;49:1–17. doi: 10.1007/s00249-020-01424-1. PubMed DOI

Iljina M., Garcia G.A., Dear A.J., Flint J., Narayan P., Michaels T.C.T., Dobson C.M., Frenkel D., Knowles T.P.J., Klenerman D. Quantitative analysis of co-oligomer formation by amyloid-beta peptide isoforms. Sci. Rep. 2016;6:28658. doi: 10.1038/srep28658. PubMed DOI PMC

Milardi D., La Rosa C., Grasso D., Guzzi R., Sportelli L., Fini C. Thermodynamics and kinetics of the thermal unfolding of plastocyanin. Eur. Biophys. J. 1998;27:273–282. doi: 10.1007/s002490050134. DOI

La Rosa C., Milardi D., Grasso D.M., Verbeet M.P., Canters G.W., Sportelli L., Guzzi R. A model for the thermal unfolding of amicyanin. Eur. Biophys. J. 2002;30:559–570. doi: 10.1007/s00249-001-0193-z. PubMed DOI

Manetto G.D., Grasso D.M., Milardi D., Pappalardo M., Guzzi R., Sportelli L., Verbeet M.P., Canters G.W., La Rosa C. The Role Played by the α-Helix in the Unfolding Pathway and Stability of Azurin: Switching Between Hierarchic and Nonhierarchic Folding. ChemBioChem. 2007;8:1941–1949. doi: 10.1002/cbic.200700214. PubMed DOI

Pappalardo M., Sciacca M., Milardi D., Grasso D., La Rosa C. Thermodynamics of azurin folding: The role of copper ion. J. Therm. Anal. Calorim. 2008;93:575–581. doi: 10.1007/s10973-007-8422-z. DOI

La Rosa C., Milardi D., Amato E., Pappalardo M., Grasso D. Molecular mechanism of the inhibition of cytochrome c aggregation by Phe-Gly. Arch. Biochem. Biophys. 2005;435:182–189. doi: 10.1016/j.abb.2004.12.006. PubMed DOI

Sciacca M., Milardi D., Pappalardo M., La Rosa C., Grasso D. Role of electrostatics in the thermal stability of ubiquitin: A combined DSC and MM study. J. Therm. Anal. Calorim. 2006;86:311–314. doi: 10.1007/s10973-005-7467-0. DOI

Manetto G., La Rosa C., Grasso D., Milardi D. Evaluation of thermodynamic properties of irreversible protein thermal unfolding measured by DSC. J. Therm. Anal. Calorim. 2005;80:263–270. doi: 10.1007/s10973-005-0646-1. DOI

Romanucci V., Milardi D., Campagna T., Gaglione M., Messere A., D’Urso A., Crisafi E., La Rosa C., Zarrelli A., Balzarini J., et al. Synthesis, biophysical characterization and anti-HIV activity of d (TG 3 AG) quadruplexes bearing hydrophobic tails at the 5′-end. Bioorg. Med. Chem. 2014;22:960–966. doi: 10.1016/j.bmc.2013.12.051. PubMed DOI

Khare S.D., Caplow M., Dokholyan N.V. The rate and equilibrium constants for a multistep reaction sequence for the aggregation of superoxide dismutase in amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA. 2004;101:15094–15099. doi: 10.1073/pnas.0406650101. PubMed DOI PMC

Stathopulos P.B., Rumfeldt J.A.O., Karbassi F., Siddall C.A., Lepock J.R., Meiering E.M. Calorimetric Analysis of Thermodynamic Stability and Aggregation for Apo and Holo Amyotrophic Lateral Sclerosis-associated Gly-93 Mutants of Superoxide Dismutase. J. Biol. Chem. 2006;281:6184–6193. doi: 10.1074/jbc.M509496200. PubMed DOI

Milardi D., Pappalardo M., Grasso D.M., La Rosa C. Unveiling the unfolding pathway of FALS associated G37R SOD1 mutant: A computational study. Mol. BioSyst. 2010;6:1032–1039. doi: 10.1039/b918662j. PubMed DOI

Lella M., Mahalakshmi R. Metamorphic Proteins: Emergence of Dual Protein Folds from One Primary Sequence. Biochemistry. 2017;56:2971–2984. doi: 10.1021/acs.biochem.7b00375. PubMed DOI

Brender J.R., Krishnamoorthy J., Sciacca M.F.M., Vivekanandan S., D’Urso L., Chen J., La Rosa C., Ramamoorthy A. Probing the Sources of the Apparent Irreproducibility of Amyloid Formation: Drastic Changes in Kinetics and a Switch in Mechanism Due to Micellelike Oligomer Formation at Critical Concentrations of IAPP. J. Phys. Chem. B. 2015;119:2886–2896. doi: 10.1021/jp511758w. PubMed DOI

Cao P., Abedini A., Wang H., Tu L.-H., Zhang X., Schmidt A.M., Raleigh D.P. Islet amyloid polypeptide toxicity and membrane interactions. Proc. Natl. Acad. Sci. USA. 2013;110:19279–19284. doi: 10.1073/pnas.1305517110. PubMed DOI PMC

Tomasello M.F., Sinopoli A., Attanasio F., Giuffrida M.L., Campagna T., Milardi D., Pappalardo G. Molecular and cytotoxic properties of hIAPP17–29 and rIAPP17–29 fragments: A comparative study with the respective full-length parent polypeptides. Eur. J. Med. Chem. 2014;81:442–455. doi: 10.1016/j.ejmech.2014.05.038. PubMed DOI

La Rosa C. Intrinsically Disordered Proteins Share a Common Molecular Mechanism in Membranes Damages: Lipid-Chaperone Hypothesis. [(accessed on 7 August 2020)]; Available online: https://www.morressier.com/article/intrinsically-disordered-proteins-share-common-molecular-mechanism-membranes-damages-lipidchaperone-hypothesis/5e736588cde2b641284ab645.

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Lipid-Chaperone Hypothesis: A Common Molecular Mechanism of Membrane Disruption by Intrinsically Disordered Proteins

. 2020 Dec 16 ; 11 (24) : 4336-4350. [epub] 20201203

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