4rik › Citations

Structure of the toxic core of α-synuclein from invisible crystals.

Rodriguez JA, Ivanova MI, Sawaya MR, Cascio D, Reyes FE, Shi D, Sangwan S, Guenther EL, Johnson LM, Zhang M, Jiang L, Arbing MA, Nannenga BL, Hattne J, Whitelegge J, Brewster AS, Messerschmidt M, Boutet S, Sauter NK, Gonen T, Eisenberg DS
Nature 525 486-90 (2015)
Related entries: 4ril, 4znn

Cited: 313 times
EuropePMC logo PMID: 26352473

Abstract

The protein α-synuclein is the main component of Lewy bodies, the neuron-associated aggregates seen in Parkinson disease and other neurodegenerative pathologies. An 11-residue segment, which we term NACore, appears to be responsible for amyloid formation and cytotoxicity of human α-synuclein. Here we describe crystals of NACore that have dimensions smaller than the wavelength of visible light and thus are invisible by optical microscopy. As the crystals are thousands of times too small for structure determination by synchrotron X-ray diffraction, we use micro-electron diffraction to determine the structure at atomic resolution. The 1.4 Å resolution structure demonstrates that this method can determine previously unknown protein structures and here yields, to our knowledge, the highest resolution achieved by any cryo-electron microscopy method to date. The structure exhibits protofibrils built of pairs of face-to-face β-sheets. X-ray fibre diffraction patterns show the similarity of NACore to toxic fibrils of full-length α-synuclein. The NACore structure, together with that of a second segment, inspires a model for most of the ordered portion of the toxic, full-length α-synuclein fibril, presenting opportunities for the design of inhibitors of α-synuclein fibrils.

Articles - 4rik mentioned but not cited (6)

  1. Structure of the toxic core of α-synuclein from invisible crystals. Rodriguez JA, Ivanova MI, Sawaya MR, Cascio D, Reyes FE, Shi D, Sangwan S, Guenther EL, Johnson LM, Zhang M, Jiang L, Arbing MA, Nannenga BL, Hattne J, Whitelegge J, Brewster AS, Messerschmidt M, Boutet S, Sauter NK, Gonen T, Eisenberg DS. Nature 525 486-490 (2015)
  2. Cryo-EM structure of alpha-synuclein fibrils. Guerrero-Ferreira R, Taylor NM, Mona D, Ringler P, Lauer ME, Riek R, Britschgi M, Stahlberg H. Elife 7 e36402 (2018)
  3. Two new polymorphic structures of human full-length alpha-synuclein fibrils solved by cryo-electron microscopy. Guerrero-Ferreira R, Taylor NM, Arteni AA, Kumari P, Mona D, Ringler P, Britschgi M, Lauer ME, Makky A, Verasdonck J, Riek R, Melki R, Meier BH, Böckmann A, Bousset L, Stahlberg H. Elife 8 e48907 (2019)
  4. Evidence for Intramolecular Antiparallel Beta-Sheet Structure in Alpha-Synuclein Fibrils from a Combination of Two-Dimensional Infrared Spectroscopy and Atomic Force Microscopy. Roeters SJ, Iyer A, Pletikapić G, Kogan V, Subramaniam V, Woutersen S. Sci Rep 7 41051 (2017)
  5. Nano-particle mediated inhibition of Parkinson's disease using computational biology approach. Kaushik AC, Bharadwaj S, Kumar S, Wei DQ. Sci Rep 8 9169 (2018)
  6. Conformational Search for the Building Block of Proteins Based on the Gradient Gravitational Search Algorithm (ConfGGS) Using Force Fields: CHARMM, AMBER, and OPLS-AA. Pradhan R, Panigrahi S, Sahu PK. J Chem Inf Model 63 670-690 (2023)


Reviews citing this publication (128)

  1. Protein Misfolding, Amyloid Formation, and Human Disease: A Summary of Progress Over the Last Decade. Chiti F, Dobson CM. Annu Rev Biochem 86 27-68 (2017)
  2. α-synuclein toxicity in neurodegeneration: mechanism and therapeutic strategies. Wong YC, Krainc D. Nat Med 23 1-13 (2017)
  3. A new era for understanding amyloid structures and disease. Iadanza MG, Jackson MP, Hewitt EW, Ranson NA, Radford SE. Nat Rev Mol Cell Biol 19 755-773 (2018)
  4. The Synucleinopathies: Twenty Years On. Goedert M, Jakes R, Spillantini MG. J Parkinsons Dis 7 S51-S69 (2017)
  5. Structural Studies of Amyloid Proteins at the Molecular Level. Eisenberg DS, Sawaya MR. Annu Rev Biochem 86 69-95 (2017)
  6. The activities of amyloids from a structural perspective. Riek R, Eisenberg DS. Nature 539 227-235 (2016)
  7. Review: Sporadic Parkinson's disease: development and distribution of α-synuclein pathology. Del Tredici K, Braak H. Neuropathol Appl Neurobiol 42 33-50 (2016)
  8. Like prions: the propagation of aggregated tau and α-synuclein in neurodegeneration. Goedert M, Masuda-Suzukake M, Falcon B. Brain 140 266-278 (2017)
  9. Mechanisms of α-Synuclein Induced Synaptopathy in Parkinson's Disease. Bridi JC, Hirth F. Front Neurosci 12 80 (2018)
  10. Half a century of amyloids: past, present and future. Ke PC, Zhou R, Serpell LC, Riek R, Knowles TPJ, Lashuel HA, Gazit E, Hamley IW, Davis TP, Fändrich M, Otzen DE, Chapman MR, Dobson CM, Eisenberg DS, Mezzenga R. Chem Soc Rev 49 5473-5509 (2020)
  11. Secondary nucleation in amyloid formation. Törnquist M, Michaels TCT, Sanagavarapu K, Yang X, Meisl G, Cohen SIA, Knowles TPJ, Linse S. Chem Commun (Camb) 54 8667-8684 (2018)
  12. Alpha-synuclein structure, functions, and interactions. Emamzadeh FN. J Res Med Sci 21 29 (2016)
  13. Implications of peptide assemblies in amyloid diseases. Ke PC, Sani MA, Ding F, Kakinen A, Javed I, Separovic F, Davis TP, Mezzenga R. Chem Soc Rev 46 6492-6531 (2017)
  14. 3D Electron Diffraction: The Nanocrystallography Revolution. Gemmi M, Mugnaioli E, Gorelik TE, Kolb U, Palatinus L, Boullay P, Hovmöller S, Abrahams JP. ACS Cent Sci 5 1315-1329 (2019)
  15. Cellular and Molecular Basis of Neurodegeneration in Parkinson Disease. Zeng XS, Geng WS, Jia JJ, Chen L, Zhang PP. Front Aging Neurosci 10 109 (2018)
  16. Alpha-Synuclein in Parkinson's Disease: From Pathogenetic Dysfunction to Potential Clinical Application. Xu L, Pu J. Parkinsons Dis 2016 1720621 (2016)
  17. The expanding amyloid family: Structure, stability, function, and pathogenesis. Sawaya MR, Hughes MP, Rodriguez JA, Riek R, Eisenberg DS. Cell 184 4857-4873 (2021)
  18. The cryo-EM method microcrystal electron diffraction (MicroED). Nannenga BL, Gonen T. Nat Methods 16 369-379 (2019)
  19. Amyloid Polymorphism in the Protein Folding and Aggregation Energy Landscape. Adamcik J, Mezzenga R. Angew Chem Int Ed Engl 57 8370-8382 (2018)
  20. Amyloid assembly and disassembly. Chuang E, Hori AM, Hesketh CD, Shorter J. J Cell Sci 131 jcs189928 (2018)
  21. How can rAAV-α-synuclein and the fibril α-synuclein models advance our understanding of Parkinson's disease? Volpicelli-Daley LA, Kirik D, Stoyka LE, Standaert DG, Harms AS. J Neurochem 139 Suppl 1 131-155 (2016)
  22. ɑ-Synuclein strains and seeding in Parkinson's disease, incidental Lewy body disease, dementia with Lewy bodies and multiple system atrophy: similarities and differences. Peelaerts W, Bousset L, Baekelandt V, Melki R. Cell Tissue Res 373 195-212 (2018)
  23. Small-molecule PET Tracers for Imaging Proteinopathies. Mathis CA, Lopresti BJ, Ikonomovic MD, Klunk WE. Semin Nucl Med 47 553-575 (2017)
  24. Neurodegeneration and the ordered assembly of α-synuclein. Spillantini MG, Goedert M. Cell Tissue Res 373 137-148 (2018)
  25. Monomer-dependent secondary nucleation in amyloid formation. Linse S. Biophys Rev 9 329-338 (2017)
  26. Lipids at the Crossroad of α-Synuclein Function and Dysfunction: Biological and Pathological Implications. Alza NP, Iglesias González PA, Conde MA, Uranga RM, Salvador GA. Front Cell Neurosci 13 175 (2019)
  27. Potential Modes of Intercellular α-Synuclein Transmission. Valdinocci D, Radford RA, Siow SM, Chung RS, Pountney DL. Int J Mol Sci 18 E469 (2017)
  28. Versatile Structures of α-Synuclein. Wang C, Zhao C, Li D, Tian Z, Lai Y, Diao J, Liu C. Front Mol Neurosci 9 48 (2016)
  29. α-synuclein aggregation and its modulation. Ghosh D, Mehra S, Sahay S, Singh PK, Maji SK. Int J Biol Macromol 100 37-54 (2017)
  30. Designer protein disaggregases to counter neurodegenerative disease. Shorter J. Curr Opin Genet Dev 44 1-8 (2017)
  31. Review: Spreading the word: precise animal models and validated methods are vital when evaluating prion-like behaviour of alpha-synuclein. Rey NL, George S, Brundin P. Neuropathol Appl Neurobiol 42 51-76 (2016)
  32. New Perspectives on Roles of Alpha-Synuclein in Parkinson's Disease. Zhang G, Xia Y, Wan F, Ma K, Guo X, Kou L, Yin S, Han C, Liu L, Huang J, Xiong N, Wang T. Front Aging Neurosci 10 370 (2018)
  33. Prion-like propagation of pathology in Parkinson disease. Volpicelli-Daley L, Brundin P. Handb Clin Neurol 153 321-335 (2018)
  34. Evidence of distinct α-synuclein strains underlying disease heterogeneity. Holec SAM, Woerman AL. Acta Neuropathol 142 73-86 (2021)
  35. Towards correlative super-resolution fluorescence and electron cryo-microscopy. Wolff G, Hagen C, Grünewald K, Kaufmann R. Biol Cell 108 245-258 (2016)
  36. Biophysical processes underlying cross-seeding in amyloid aggregation and implications in amyloid pathology. Ivanova MI, Lin Y, Lee YH, Zheng J, Ramamoorthy A. Biophys Chem 269 106507 (2021)
  37. Proteopathic Strains and the Heterogeneity of Neurodegenerative Diseases. Walker LC. Annu Rev Genet 50 329-346 (2016)
  38. Alpha Synuclein Connects the Gut-Brain Axis in Parkinson's Disease Patients - A View on Clinical Aspects, Cellular Pathology and Analytical Methodology. Schaeffer E, Kluge A, Böttner M, Zunke F, Cossais F, Berg D, Arnold P. Front Cell Dev Biol 8 573696 (2020)
  39. Dynamic structural flexibility of α-synuclein. Mor DE, Ugras SE, Daniels MJ, Ischiropoulos H. Neurobiol Dis 88 66-74 (2016)
  40. Genetics of Parkinson's disease and related disorders. Zhang PL, Chen Y, Zhang CH, Wang YX, Fernandez-Funez P. J Med Genet 55 73-80 (2018)
  41. The elusive tau molecular structures: can we translate the recent breakthroughs into new targets for intervention? Fichou Y, Al-Hilaly YK, Devred F, Smet-Nocca C, Tsvetkov PO, Verelst J, Winderickx J, Geukens N, Vanmechelen E, Perrotin A, Serpell L, Hanseeuw BJ, Medina M, Buée L, Landrieu I. Acta Neuropathol Commun 7 31 (2019)
  42. Effects of oligomer toxicity, fibril toxicity and fibril spreading in synucleinopathies. Cascella R, Bigi A, Cremades N, Cecchi C. Cell Mol Life Sci 79 174 (2022)
  43. The Promise and Challenges of Developing miRNA-Based Therapeutics for Parkinson's Disease. Titze-de-Almeida SS, Soto-Sánchez C, Fernandez E, Koprich JB, Brotchie JM, Titze-de-Almeida R. Cells 9 E841 (2020)
  44. The formation, function and regulation of amyloids: insights from structural biology. Landreh M, Sawaya MR, Hipp MS, Eisenberg DS, Wüthrich K, Hartl FU. J Intern Med 280 164-176 (2016)
  45. Is Lewy pathology in the human nervous system chiefly an indicator of neuronal protection or of toxicity? Chartier S, Duyckaerts C. Cell Tissue Res 373 149-160 (2018)
  46. Looking Beyond the Core: The Role of Flanking Regions in the Aggregation of Amyloidogenic Peptides and Proteins. Ulamec SM, Brockwell DJ, Radford SE. Front Neurosci 14 611285 (2020)
  47. Molecular Mechanisms and Regulation of Mammalian Mitophagy. Choubey V, Zeb A, Kaasik A. Cells 11 38 (2021)
  48. Protein aggregation, misfolding and consequential human neurodegenerative diseases. Sami N, Rahman S, Kumar V, Zaidi S, Islam A, Ali S, Ahmad F, Hassan MI. Int J Neurosci 127 1047-1057 (2017)
  49. Ecology and Biogenesis of Functional Amyloids in Pseudomonas. Rouse SL, Matthews SJ, Dueholm MS. J Mol Biol 430 3685-3695 (2018)
  50. MicroED opens a new era for biological structure determination. Nannenga BL, Gonen T. Curr Opin Struct Biol 40 128-135 (2016)
  51. A critical review of the prion hypothesis of human synucleinopathies. Tamgüney G, Korczyn AD. Cell Tissue Res 373 213-220 (2018)
  52. Databases and Archiving for CryoEM. Patwardhan A, Lawson CL. Methods Enzymol 579 393-412 (2016)
  53. Interaction of Alpha-Synuclein With Lipids: Mitochondrial Cardiolipin as a Critical Player in the Pathogenesis of Parkinson's Disease. Gilmozzi V, Gentile G, Castelo Rueda MP, Hicks AA, Pramstaller PP, Zanon A, Lévesque M, Pichler I. Front Neurosci 14 578993 (2020)
  54. Alpha-Synuclein Aggregation Pathway in Parkinson's Disease: Current Status and Novel Therapeutic Approaches. Vidović M, Rikalovic MG. Cells 11 1732 (2022)
  55. Extracellular Interactions of Alpha-Synuclein in Multiple System Atrophy. Valdinocci D, Radford RAW, Goulding M, Hayashi J, Chung RS, Pountney DL. Int J Mol Sci 19 E4129 (2018)
  56. Membrane interactions of intrinsically disordered proteins: The example of alpha-synuclein. Das T, Eliezer D. Biochim Biophys Acta Proteins Proteom 1867 879-889 (2019)
  57. Alpha-synuclein and iron: two keys unlocking Parkinson's disease. Lingor P, Carboni E, Koch JC. J Neural Transm (Vienna) 124 973-981 (2017)
  58. Membranes as modulators of amyloid protein misfolding and target of toxicity. Rawat A, Langen R, Varkey J. Biochim Biophys Acta Biomembr 1860 1863-1875 (2018)
  59. MicroED in natural product and small molecule research. Danelius E, Halaby S, van der Donk WA, Gonen T. Nat Prod Rep 38 423-431 (2021)
  60. Neurons and Glia Interplay in α-Synucleinopathies. Mavroeidi P, Xilouri M. Int J Mol Sci 22 4994 (2021)
  61. Amyloid-Like Aggregation in Diseases and Biomaterials: Osmosis of Structural Information. Balasco N, Diaferia C, Morelli G, Vitagliano L, Accardo A. Front Bioeng Biotechnol 9 641372 (2021)
  62. Circular RNAs in Embryogenesis and Cell Differentiation With a Focus on Cancer Development. Di Agostino S, Riccioli A, De Cesaris P, Fontemaggi G, Blandino G, Filippini A, Fazi F. Front Cell Dev Biol 8 389 (2020)
  63. Mechanisms of Neurodegeneration in Various Forms of Parkinsonism-Similarities and Differences. Koziorowski D, Figura M, Milanowski ŁM, Szlufik S, Alster P, Madetko N, Friedman A. Cells 10 656 (2021)
  64. An Update on the Critical Role of α-Synuclein in Parkinson's Disease and Other Synucleinopathies: from Tissue to Cellular and Molecular Levels. Serratos IN, Hernández-Pérez E, Campos C, Aschner M, Santamaría A. Mol Neurobiol 59 620-642 (2022)
  65. Protein Quality Control Pathways at the Crossroad of Synucleinopathies. De Mattos EP, Wentink A, Nussbaum-Krammer C, Hansen C, Bergink S, Melki R, Kampinga HH. J Parkinsons Dis 10 369-382 (2020)
  66. Taking the measure of MicroED. Rodriguez JA, Eisenberg DS, Gonen T. Curr Opin Struct Biol 46 79-86 (2017)
  67. Understanding amyloid fibril formation using protein fragments: structural investigations via vibrational spectroscopy and solid-state NMR. Martial B, Lefèvre T, Auger M. Biophys Rev 10 1133-1149 (2018)
  68. Vertebrate food products as a potential source of prion-like α-synuclein. Killinger BA, Labrie V. NPJ Parkinsons Dis 3 33 (2017)
  69. The Proteome Folding Problem and Cellular Proteostasis. Powers ET, Gierasch LM. J Mol Biol 433 167197 (2021)
  70. Lipids as Trans-Acting Effectors for α-Synuclein in the Pathogenesis of Parkinson's Disease. Ikenaka K, Suzuki M, Mochizuki H, Nagai Y. Front Neurosci 13 693 (2019)
  71. Toward the Atomic Structure of PrPSc. Rodriguez JA, Jiang L, Eisenberg DS. Cold Spring Harb Perspect Biol 9 a031336 (2017)
  72. Navigating the dynamic landscape of alpha-synuclein morphology: a review of the physiologically relevant tetrameric conformation. Lucas HR, Fernández RD. Neural Regen Res 15 407-415 (2020)
  73. Targeting alpha-synuclein via the immune system in Parkinson's disease: Current vaccine therapies. Fleming SM, Davis A, Simons E. Neuropharmacology 202 108870 (2022)
  74. The complementarity of serial femtosecond crystallography and MicroED for structure determination from microcrystals. Zatsepin NA, Li C, Colasurd P, Nannenga BL. Curr Opin Struct Biol 58 286-293 (2019)
  75. Advances in methods for atomic resolution macromolecular structure determination. Thompson MC, Yeates TO, Rodriguez JA. F1000Res 9 F1000 Faculty Rev-667 (2020)
  76. Atomic resolution structure determination by the cryo-EM method MicroED. Liu S, Hattne J, Reyes FE, Sanchez-Martinez S, Jason de la Cruz M, Shi D, Gonen T. Protein Sci 26 8-15 (2017)
  77. Beyond protein structure determination with MicroED. Nguyen C, Gonen T. Curr Opin Struct Biol 64 51-58 (2020)
  78. Delivering the Promise of Gene Therapy with Nanomedicines in Treating Central Nervous System Diseases. Luo M, Lee LKC, Peng B, Choi CHJ, Tong WY, Voelcker NH. Adv Sci (Weinh) 9 e2201740 (2022)
  79. In Search of Effective Treatments Targeting α-Synuclein Toxicity in Synucleinopathies: Pros and Cons. Fouka M, Mavroeidi P, Tsaka G, Xilouri M. Front Cell Dev Biol 8 559791 (2020)
  80. The Neuroprotective Role of Protein Quality Control in Halting the Development of Alpha-Synuclein Pathology. Manecka DL, Vanderperre B, Fon EA, Durcan TM. Front Mol Neurosci 10 311 (2017)
  81. Alpha-Synuclein and Cognitive Decline in Parkinson Disease. Fan TS, Liu SC, Wu RM. Life (Basel) 11 1239 (2021)
  82. Consequences of variability in α-synuclein fibril structure on strain biology. Holec SAM, Liu SL, Woerman AL. Acta Neuropathol 143 311-330 (2022)
  83. Electron Diffraction of 3D Molecular Crystals. Saha A, Nia SS, Rodríguez JA. Chem Rev 122 13883-13914 (2022)
  84. Formation of Heterotypic Amyloids: α-Synuclein in Co-Aggregation. Bhasne K, Mukhopadhyay S. Proteomics 18 e1800059 (2018)
  85. Molecular pathology of neurodegenerative diseases by cryo-EM of amyloids. Scheres SHW, Ryskeldi-Falcon B, Goedert M. Nature 621 701-710 (2023)
  86. Understanding and controlling amyloid aggregation with chirality. Foley AR, Raskatov JA. Curr Opin Chem Biol 64 1-9 (2021)
  87. Adeno-Associated Virus Expression of α-Synuclein as a Tool to Model Parkinson's Disease: Current Understanding and Knowledge Gaps. Huntington TE, Srinivasan R. Aging Dis 12 1120-1137 (2021)
  88. Alpha-synuclein Immunization Strategies for Synucleinopathies in Clinical Studies: A Biological Perspective. Knecht L, Folke J, Dodel R, Ross JA, Albus A. Neurotherapeutics 19 1489-1502 (2022)
  89. Roles, Characteristics, and Analysis of Intrinsically Disordered Proteins: A Minireview. Lermyte F. Life (Basel) 10 E320 (2020)
  90. Comparing the Folds of Prions and Other Pathogenic Amyloids. Flores-Fernández JM, Rathod V, Wille H. Pathogens 7 E50 (2018)
  91. High-Resolution Macromolecular Structure Determination by MicroED, a cryo-EM Method. Rodriguez JA, Gonen T. Methods Enzymol 579 369-392 (2016)
  92. α-Synuclein-mediated neurodegeneration in Dementia with Lewy bodies: the pathobiology of a paradox. Simon C, Soga T, Okano HJ, Parhar I. Cell Biosci 11 196 (2021)
  93. An Overview of Microcrystal Electron Diffraction (MicroED). Mu X, Gillman C, Nguyen C, Gonen T. Annu Rev Biochem 90 431-450 (2021)
  94. MicroED: conception, practice and future opportunities. Clabbers MTB, Shiriaeva A, Gonen T. IUCrJ 9 169-179 (2022)
  95. Monitoring α-synuclein aggregation. Estaun-Panzano J, Arotcarena ML, Bezard E. Neurobiol Dis 176 105966 (2023)
  96. Bacterial Protein Homeostasis Disruption as a Therapeutic Intervention. Khodaparast L, Wu G, Khodaparast L, Schmidt BZ, Rousseau F, Schymkowitz J. Front Mol Biosci 8 681855 (2021)
  97. Electron cryomicroscopy as a powerful tool in biomedical research. Quentin D, Raunser S. J Mol Med (Berl) 96 483-493 (2018)
  98. Macromolecular crystallography using microcrystal electron diffraction. Clabbers MTB, Xu H. Acta Crystallogr D Struct Biol 77 313-324 (2021)
  99. Mechanisms Underlying Neurodegenerative Disorders and Potential Neuroprotective Activity of Agrifood By-Products. Angeloni C, Malaguti M, Prata C, Freschi M, Barbalace MC, Hrelia S. Antioxidants (Basel) 12 94 (2022)
  100. Target Enzymes Considered for the Treatment of Alzheimer's Disease and Parkinson's Disease. Kim N, Lee HJ. Biomed Res Int 2020 2010728 (2020)
  101. The Evolution and the Advantages of MicroED. Nannenga BL, Bu G, Shi D. Front Mol Biosci 5 114 (2018)
  102. Development of Small Molecules Targeting α-Synuclein Aggregation: A Promising Strategy to Treat Parkinson's Disease. Peña-Díaz S, García-Pardo J, Ventura S. Pharmaceutics 15 839 (2023)
  103. Diffraction Techniques in Structural Biology. Egli M. Curr Protoc Nucleic Acid Chem 65 7.13.1-7.13.41 (2016)
  104. Examining the Toxicity of α-Synuclein in Neurodegenerative Disorders. Shan FY, Fung KM, Zieneldien T, Kim J, Cao C, Huang JH. Life (Basel) 11 1126 (2021)
  105. Growing and making nano- and microcrystals. Shoeman RL, Hartmann E, Schlichting I. Nat Protoc 18 854-882 (2023)
  106. Macromolecular Nanocrystal Structural Analysis with Electron and X-Rays: A Comparative Review. Khakurel KP, Angelov B, Andreasson J. Molecules 24 E3490 (2019)
  107. MicroED for the study of protein-ligand interactions and the potential for drug discovery. Clark LJ, Bu G, Nannenga BL, Gonen T. Nat Rev Chem 5 853-858 (2021)
  108. MicroED in drug discovery. Danelius E, Patel K, Gonzalez B, Gonen T. Curr Opin Struct Biol 79 102549 (2023)
  109. Pre-structured hydrophobic peptide β-strands: A universal amyloid trap? Sivanesam K, Andersen N. Arch Biochem Biophys 664 51-61 (2019)
  110. Advances in protein misfolding, amyloidosis and its correlation with human diseases. Kundu D, Prerna K, Chaurasia R, Bharty MK, Dubey VK. 3 Biotech 10 193 (2020)
  111. Amyloidogenicity at a Distance: How Distal Protein Regions Modulate Aggregation in Disease. Lucato CM, Lupton CJ, Halls ML, Ellisdon AM. J Mol Biol 429 1289-1304 (2017)
  112. Challenges with osmolytes as inhibitors of protein aggregation: Can nucleic acid aptamers provide an answer? Patel KA, Sethi R, Dhara AR, Roy I. Int J Biol Macromol 100 75-88 (2017)
  113. Current status and future prospects for enabling chemistry technology in the drug discovery process. Djuric SW, Hutchins CW, Talaty NN. F1000Res 5 2426 (2016)
  114. The young person's guide to the PDB. Minor W, Dauter Z, Jaskolski M. Postepy Biochem 62 242-249 (2016)
  115. Analysis and comparison of electron radiation damage assessments in Cryo-EM by single particle analysis and micro-crystal electron diffraction. Shi D, Huang R. Front Mol Biosci 9 988928 (2022)
  116. Light, Water, and Melatonin: The Synergistic Regulation of Phase Separation in Dementia. Loh D, Reiter RJ. Int J Mol Sci 24 5835 (2023)
  117. Multifaceted interactions mediated by intrinsically disordered regions play key roles in alpha synuclein aggregation. Khare SD, Chinchilla P, Baum J. Curr Opin Struct Biol 80 102579 (2023)
  118. Peptide-based approaches to directly target alpha-synuclein in Parkinson's disease. Allen SG, Meade RM, White Stenner LL, Mason JM. Mol Neurodegener 18 80 (2023)
  119. Targeting α-Synuclein in Parkinson's Disease by Induced Pluripotent Stem Cell Models. Spathopoulou A, Edenhofer F, Fellner L. Front Neurol 12 786835 (2021)
  120. The Synucleins and the Astrocyte. Myers AJ, Brahimi A, Jenkins IJ, Koob AO. Biology (Basel) 12 155 (2023)
  121. Advancements in Genetic and Biochemical Insights: Unraveling the Etiopathogenesis of Neurodegeneration in Parkinson's Disease. Ratan Y, Rajput A, Pareek A, Pareek A, Jain V, Sonia S, Farooqui Z, Kaur R, Singh G. Biomolecules 14 73 (2024)
  122. Alpha-Synuclein Contribution to Neuronal and Glial Damage in Parkinson's Disease. Saramowicz K, Siwecka N, Galita G, Kucharska-Lusina A, Rozpędek-Kamińska W, Majsterek I. Int J Mol Sci 25 360 (2023)
  123. Brain clearance of protein aggregates: a close-up on astrocytes. Giusti V, Kaur G, Giusto E, Civiero L. Mol Neurodegener 19 5 (2024)
  124. Energetics of cosolvent effect on peptide aggregation. Matubayasi N, Masutani K. Biophys Physicobiol 16 185-195 (2019)
  125. Extension of research data repository system to support direct compute access to biomedical datasets: enhancing Dataverse to support large datasets. McKinney B, Meyer PA, Crosas M, Sliz P. Ann N Y Acad Sci 1387 95-104 (2017)
  126. Interactions of amyloidogenic proteins with mitochondrial protein import machinery in aging-related neurodegenerative diseases. Reed AL, Mitchell W, Alexandrescu AT, Alder NN. Front Physiol 14 1263420 (2023)
  127. The Bidirectional Interplay of α-Synuclein with Lipids in the Central Nervous System and Its Implications for the Pathogenesis of Parkinson's Disease. Battis K, Xiang W, Winkler J. Int J Mol Sci 24 13270 (2023)
  128. Update on Nonhuman Primate Models of Brain Disease and Related Research Tools. Qiao N, Ma L, Zhang Y, Wang L. Biomedicines 11 2516 (2023)

Articles citing this publication (179)



Quick links