ACS Publications. Most Trusted. Most Cited. Most Read
My Activity

Heparin and Other Glycosaminoglycans Stimulate the Formation of Amyloid Fibrils from α-Synuclein in Vitro

View Author Information
Department of Chemistry and Biochemistry, University of California, Santa Cruz, California 95064
Cite this: Biochemistry 2002, 41, 5, 1502–1511
Publication Date (Web):January 11, 2002
Copyright © 2002 American Chemical Society

    Article Views





    Other access options


    Parkinson's disease is the second most common neurodegenerative disease and results from loss of dopaminergic neurons in the substantia nigra. The aggregation and fibrillation of α-synuclein have been implicated as a causative factor in the disease. Glycosaminoglycans (GAGs) are routinely found associated with amyloid deposits in most amyloidosis diseases, and there is evidence to support an active role of GAGs in amyloid fibril formation in some cases. In contrast to the extracellular amyloid deposits, the α-synuclein deposits in Lewy body diseases are intracellular, and thus it is less clear whether GAGs may be involved. To determine whether the presence of GAGs does affect the fibrillation of α-synuclein, the kinetics of fibril formation were investigated in the presence of a number of GAGs and other charged polymers. Certain GAGs (heparin, heparan sulfate) and other highly sulfated polymers (dextran sulfate) were found to significantly stimulate the formation of α-synuclein fibrils. Interestingly, the interaction of GAGs with α-synuclein is quite specific, since some GAGs, e.g., keratan sulfate, had negligible effect. Heparin not only increased the rate of fibrillation but also apparently increased the yield of fibrils. The molar ratio of heparin to α-synuclein and the incorporation of fluorescein-labeled heparin into the fibrils demonstrate that the heparin is integrated into the fibrils and is not just a catalyst for fibrillation. The apparent dissociation constant for heparin in stimulating α-synuclein fibrillation was 0.19 μM, indicating a strong affinity. Similar effects of heparin were observed with the A53T and A30P mutants of α-synuclein. Since there is some evidence that Lewy bodies may contain GAGs, these observations may be very relevant in the context of the etiology of Parkinson's disease.

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.


    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

     This research was supported by a grant from the National Institutes of Health (A.L.F.) and a sabbatical leave from California State University, Long Beach (J.A.C.).

     These authors contributed equally to this work.


     To whom correspondence should be addressed. Phone:  (831) 459-2744. Fax:  (831) 459-2935. E-mail:  [email protected].

    Cited By

    This article is cited by 275 publications.

    1. Taniya Bhardwaj, Rajanish Giri. Potential of ADAM 17 Signal Peptide To Form Amyloid Aggregates in Vitro. ACS Chemical Neuroscience 2023, 14 (20) , 3818-3825.
    2. Annemarie Danielsson, Sergey A. Samsonov, Adam Liwo, Adam K. Sieradzan. Extension of the SUGRES-1P Coarse-Grained Model of Polysaccharides to Heparin. Journal of Chemical Theory and Computation 2023, 19 (17) , 6023-6036.
    3. Beenish Khurshid, Ashfaq Ur Rehman, Ray Luo, Alamzeb Khan, Abdul Wadood, Jamshed Anwar. Heparin-Assisted Amyloidogenesis Uncovered through Molecular Dynamics Simulations. ACS Omega 2022, 7 (17) , 15132-15144.
    4. Huayuan Tang, Yunxiang Sun, Feng Ding. Hydrophobic/Hydrophilic Ratio of Amphiphilic Helix Mimetics Determines the Effects on Islet Amyloid Polypeptide Aggregation. Journal of Chemical Information and Modeling 2022, 62 (7) , 1760-1770.
    5. Ishfaq Ahmad Ahanger, Zahoor Ahmad Parray, Khalida Nasreen, Faizan Ahmad, Md. Imtaiyaz Hassan, Asimul Islam, Anurag Sharma. Heparin Accelerates the Protein Aggregation via the Downhill Polymerization Mechanism: Multi-Spectroscopic Studies to Delineate the Implications on Proteinopathies. ACS Omega 2021, 6 (3) , 2328-2339.
    6. David J. Townsend, David A. Middleton, Lorna Ashton. Raman Spectroscopy with 2D Perturbation Correlation Moving Windows for the Characterization of Heparin–Amyloid Interactions. Analytical Chemistry 2020, 92 (20) , 13822-13828.
    7. Pooja Ghosh, Priyadarsi De. Modulation of Amyloid Protein Fibrillation by Synthetic Polymers: Recent Advances in the Context of Neurodegenerative Diseases. ACS Applied Bio Materials 2020, 3 (10) , 6598-6625.
    8. Karan Sharma, Surabhi Mehra, Ajay S. Sawner, Pratap S. Markam, Rajlaxmi Panigrahi, Ambuja Navalkar, Debdeep Chatterjee, Rakesh Kumar, Pradeep Kadu, Komal Patel, Soumik Ray, Ashutosh Kumar, Samir K. Maji. Effect of Disease-Associated P123H and V70M Mutations on β-Synuclein Fibrillation. ACS Chemical Neuroscience 2020, 11 (18) , 2836-2848.
    9. Shashikala Bhute, Deepaneeta Sarmah, Aishika Datta, Pallavi Rane, Amit Shard, Avirag Goswami, Anupom Borah, Kiran Kalia, Kunjan R. Dave, Pallab Bhattacharya. Molecular Pathogenesis and Interventional Strategies for Alzheimer’s Disease: Promises and Pitfalls. ACS Pharmacology & Translational Science 2020, 3 (3) , 472-488.
    10. Giovanni Bellomo, Sara Bologna, Linda Cerofolini, Silvia Paciotti, Leonardo Gatticchi, Enrico Ravera, Lucilla Parnetti, Marco Fragai, Claudio Luchinat. Dissecting the Interactions between Human Serum Albumin and α-Synuclein: New Insights on the Factors Influencing α-Synuclein Aggregation in Biological Fluids. The Journal of Physical Chemistry B 2019, 123 (20) , 4380-4386.
    11. Mathew Sebastiao, Noe Quittot, Isabelle Marcotte, Steve Bourgault. Glycosaminoglycans Induce Amyloid Self-Assembly of a Peptide Hormone by Concerted Secondary and Quaternary Conformational Transitions. Biochemistry 2019, 58 (9) , 1214-1225.
    12. David Townsend, Eleri Hughes, Rohanah Hussain, Giuliano Siligardi, Sarah Baldock, Jillian Madine, and David A. Middleton . Heparin and Methionine Oxidation Promote the Formation of Apolipoprotein A-I Amyloid Comprising α-Helical and β-Sheet Structures. Biochemistry 2017, 56 (11) , 1632-1644.
    13. Nadezhda Nespovitaya, Julia Gath, Konstantin Barylyuk, Carolin Seuring, Beat H. Meier, and Roland Riek . Dynamic Assembly and Disassembly of Functional β-Endorphin Amyloid Fibrils. Journal of the American Chemical Society 2016, 138 (3) , 846-856.
    14. Haiyang Liu, Bimlesh Ojha, Clifford Morris, Mengting Jiang, Ewa P. Wojcikiewicz, Praveen P. N. Rao, and Deguo Du . Positively Charged Chitosan and N-Trimethyl Chitosan Inhibit Aβ40 Fibrillogenesis. Biomacromolecules 2015, 16 (8) , 2363-2373.
    15. Leonid Breydo, Amanda E. Sales, Telma Frege, Mark C. Howell, Boris Y. Zaslavsky, and Vladimir N. Uversky . Effects of Polymer Hydrophobicity on Protein Structure and Aggregation Kinetics in Crowded Milieu. Biochemistry 2015, 54 (19) , 2957-2966.
    16. Dhiman Ghosh, Paulami Dutta, Chanchal Chakraborty, Pradeep K. Singh, A. Anoop, Narendra Nath Jha, Reeba S. Jacob, Mrityunjoy Mondal, Shruti Mankar, Subhadeep Das, Sudip Malik, and Samir K. Maji . Complexation of Amyloid Fibrils with Charged Conjugated Polymers. Langmuir 2014, 30 (13) , 3775-3786.
    17. Jillian Madine, Hannah A. Davies, Eleri Hughes, and David A. Middleton . Heparin Promotes the Rapid Fibrillization of a Peptide with Low Intrinsic Amyloidogenicity. Biochemistry 2013, 52 (50) , 8984-8992.
    18. Narendra Nath Jha, A. Anoop, Srivastav Ranganathan, Ganesh M. Mohite, Ranjith Padinhateeri, and Samir K. Maji . Characterization of Amyloid Formation by Glucagon-Like Peptides: Role of Basic Residues in Heparin-Mediated Aggregation. Biochemistry 2013, 52 (49) , 8800-8810.
    19. Francesca Brambilla, Francesca Lavatelli, Dario Di Silvestre, Veronica Valentini, Giovanni Palladini, Giampaolo Merlini, and Pierluigi Mauri . Shotgun Protein Profile of Human Adipose Tissue and Its Changes in Relation to Systemic Amyloidoses. Journal of Proteome Research 2013, 12 (12) , 5642-5655.
    20. Bimlesh Ojha, Haiyang Liu, Samrat Dutta, Praveen P. N. Rao, Ewa P. Wojcikiewicz, and Deguo Du . Poly(4-styrenesulfonate) as an Inhibitor of Aβ40 Amyloid Fibril Formation. The Journal of Physical Chemistry B 2013, 117 (45) , 13975-13984.
    21. Christian Bleiholder, Thanh D. Do, Chun Wu, Nicholas J. Economou, Summer S. Bernstein, Steven K. Buratto, Joan-Emma Shea, and Michael T. Bowers . Ion Mobility Spectrometry Reveals the Mechanism of Amyloid Formation of Aβ(25–35) and Its Modulation by Inhibitors at the Molecular Level: Epigallocatechin Gallate and Scyllo-inositol. Journal of the American Chemical Society 2013, 135 (45) , 16926-16937.
    22. Joan Camunas-Soler, Silvia Frutos, Cristiano V. Bizarro, Sara de Lorenzo, Maria Eugenia Fuentes-Perez, Roland Ramsch, Susana Vilchez, Conxita Solans, Fernando Moreno-Herrero, Fernando Albericio, Ramón Eritja, Ernest Giralt, Sukhendu B. Dev, and Felix Ritort . Electrostatic Binding and Hydrophobic Collapse of Peptide–Nucleic Acid Aggregates Quantified Using Force Spectroscopy. ACS Nano 2013, 7 (6) , 5102-5113.
    23. David C. DeWitt and Elizabeth Rhoades . α-Synuclein Can Inhibit SNARE-Mediated Vesicle Fusion through Direct Interactions with Lipid Bilayers. Biochemistry 2013, 52 (14) , 2385-2387.
    24. Yisheng Xu, Daniel Seeman, Yunfeng Yan, Lianhong Sun, Jared Post, and Paul L. Dubin . Effect of Heparin on Protein Aggregation: Inhibition versus Promotion. Biomacromolecules 2012, 13 (5) , 1642-1651.
    25. Sharadrao M. Patil, Andrew Mehta, Suman Jha, and Andrei T. Alexandrescu . Heterogeneous Amylin Fibril Growth Mechanisms Imaged by Total Internal Reflection Fluorescence Microscopy. Biochemistry 2011, 50 (14) , 2808-2819.
    26. Steve Bourgault, James P. Solomon, Natàlia Reixach, and Jeffery W. Kelly . Sulfated Glycosaminoglycans Accelerate Transthyretin Amyloidogenesis by Quaternary Structural Conversion. Biochemistry 2011, 50 (6) , 1001-1015.
    27. Jessika Meuvis, Melanie Gerard, Linda Desender, Veerle Baekelandt, and Yves Engelborghs . The Conformation and the Aggregation Kinetics of α-Synuclein Depend on the Proline Residues in Its C-Terminal Region. Biochemistry 2010, 49 (43) , 9345-9352.
    28. Natalya I. Topilina, Vitali Sikirzhytsky, Seiichiro Higashiya, Vladimir V. Ermolenkov, Igor K. Lednev and John T. Welch. Charge Distribution and Amyloid Fibril Formation: Insights from Genetically Engineered Model Systems. Biomacromolecules 2010, 11 (7) , 1721-1726.
    29. Xiaoyun Meng, Larissa A. Munishkina, Anthony L. Fink and Vladimir N. Uversky . Molecular Mechanisms Underlying the Flavonoid-Induced Inhibition of α-Synuclein Fibrillation. Biochemistry 2009, 48 (34) , 8206-8224.
    30. Katie Giger, Ram P. Vanam, Emek Seyrek and Paul L. Dubin. Suppression of Insulin Aggregation by Heparin. Biomacromolecules 2008, 9 (9) , 2338-2344.
    31. Hongbo Xie,, Slobodan Vucetic,, Lilia M. Iakoucheva,, Christopher J. Oldfield,, A. Keith Dunker,, Zoran Obradovic, and, Vladimir N. Uversky. Functional Anthology of Intrinsic Disorder. 3. Ligands, Post-Translational Modifications, and Diseases Associated with Intrinsically Disordered Proteins. Journal of Proteome Research 2007, 6 (5) , 1917-1932.
    32. Anthony L. Fink. The Aggregation and Fibrillation of α-Synuclein. Accounts of Chemical Research 2006, 39 (9) , 628-634.
    33. Dong-Pyo Hong,, Atta Ahmad, and, Anthony L. Fink. Fibrillation of Human Insulin A and B Chains. Biochemistry 2006, 45 (30) , 9342-9353.
    34. Elena Gaggelli,, Henryk Kozlowski,, Daniela Valensin, and, Gianni Valensin. Copper Homeostasis and Neurodegenerative Disorders (Alzheimer's, Prion, and Parkinson's Diseases and Amyotrophic Lateral Sclerosis). Chemical Reviews 2006, 106 (6) , 1995-2044.
    35. Ghiam Yamin,, Larissa A. Munishkina,, Mikhail A. Karymov,, Yuri L. Lyubchenko,, Vladimir N. Uversky, and, Anthony L. Fink. Forcing Nonamyloidogenic β-Synuclein To Fibrillate. Biochemistry 2005, 44 (25) , 9096-9107.
    36. Olga V. Bocharova,, Leonid Breydo,, Vadim V. Salnikov, and, Ilia V. Baskakov. Copper(II) Inhibits in Vitro Conversion of Prion Protein into Amyloid Fibrils. Biochemistry 2005, 44 (18) , 6776-6787.
    37. Bakthisaran Raman,, Eri Chatani,, Miho Kihara,, Tadato Ban,, Miyo Sakai,, Kazuhiro Hasegawa,, Hironobu Naiki,, Ch Mohan Rao, and, Yuji Goto. Critical Balance of Electrostatic and Hydrophobic Interactions Is Required for β2-Microglobulin Amyloid Fibril Growth and Stability. Biochemistry 2005, 44 (4) , 1288-1299.
    38. Takashi Ohgita, Hiroki Kono, Izumi Morita, Hiroyuki Oyama, Toshinori Shimanouchi, Norihiro Kobayashi, Hiroyuki Saito. Intramolecular interaction kinetically regulates fibril formation by human and mouse α-synuclein. Scientific Reports 2023, 13 (1)
    39. Ilaria Piccialli, Francesca Greco, Giovanni Roviello, Maria Josè Sisalli, Valentina Tedeschi, Antonia di Mola, Nicola Borbone, Giorgia Oliviero, Vincenzo De Feo, Agnese Secondo, Antonio Massa, Anna Pannaccione. The 3-(3-oxoisoindolin-1-yl)pentane-2,4-dione (ISOAC1) as a new molecule able to inhibit Amyloid β aggregation and neurotoxicity. Biomedicine & Pharmacotherapy 2023, 168 , 115745.
    40. Jakob Rupert, Michele Monti, Elsa Zacco, Gian Gaetano Tartaglia. RNA sequestration driven by amyloid formation: the alpha synuclein case. Nucleic Acids Research 2023, 51 (21) , 11466-11478.
    41. Dan Li, Cong Liu. Molecular rules governing the structural polymorphism of amyloid fibrils in neurodegenerative diseases. Structure 2023, 31 (11) , 1335-1347.
    42. Olga N. Makshakova, Liliya R. Bogdanova, Dzhigangir A. Faizullin, Elena A. Ermakova, Yuriy F. Zuev. Sulfated Polysaccharides as a Fighter with Protein Non-Physiological Aggregation: The Role of Polysaccharide Flexibility and Charge Density. International Journal of Molecular Sciences 2023, 24 (22) , 16223.
    43. Patricia Aguilar-Calvo, Adela Malik, Daniel R. Sandoval, Christopher Barback, Christina D. Orrù, Heidi G. Standke, Olivia R. Thomas, Chrissa A. Dwyer, Donald P. Pizzo, Jaidev Bapat, Katrin Soldau, Ryotaro Ogawa, Mckenzie B. Riley, K. Peter R. Nilsson, Allison Kraus, Byron Caughey, Jeffrey J. Iliff, David R. Vera, Jeffrey D. Esko, Christina J. Sigurdson, . Neuronal Ndst1 depletion accelerates prion protein clearance and slows neurodegeneration in prion infection. PLOS Pathogens 2023, 19 (9) , e1011487.
    44. Ishfaq Ahmad Ahanger, Zahoor Ahmad Parray, Neha Raina, Sania Bashir, Faizan Ahmad, Md. Imtaiyaz Hassan, Mohammad Shahid, Anurag Sharma, Asimul Islam. Counteraction of the cetyltrimethylammonium bromide-induced protein aggregation by heparin: Potential impact on protein aggregation and neurodegenerative diseases using biophysical approaches. Journal of Molecular Structure 2023, 1276 , 134714.
    45. Olga Makshakova, Liliya Bogdanova, Dzhigangir Faizullin, Diliara Khaibrakhmanova, Sufia Ziganshina, Elena Ermakova, Yuriy Zuev, Igor Sedov. The Ability of Some Polysaccharides to Disaggregate Lysozyme Amyloid Fibrils and Renature the Protein. Pharmaceutics 2023, 15 (2) , 624.
    46. Munishwar Nath Gupta, Vladimir N. Uversky. Macromolecular crowding: how it affects protein structure, disorder, and catalysis. 2023, 353-376.
    47. Youqi Tao, Yunpeng Sun, Shiran Lv, Wencheng Xia, Kun Zhao, Qianhui Xu, Qinyue Zhao, Lin He, Weidong Le, Yong Wang, Cong Liu, Dan Li. Heparin induces α-synuclein to form new fibril polymorphs with attenuated neuropathology. Nature Communications 2022, 13 (1)
    48. Takashi Ohgita, Norihiro Namba, Hiroki Kono, Toshinori Shimanouchi, Hiroyuki Saito. Mechanisms of enhanced aggregation and fibril formation of Parkinson’s disease-related variants of α-synuclein. Scientific Reports 2022, 12 (1)
    49. Tatsuya Karaki, Hisao Haniu, Yoshikazu Matsuda, Tamotsu Tsukahara. Lysophospholipids: A Potential Drug Candidates for Neurodegenerative Disorders. Biomedicines 2022, 10 (12) , 3126.
    50. Amrita Basu, Neil G. Patel, Elijah D. Nicholson, Ryan J. Weiss. Spatiotemporal diversity and regulation of glycosaminoglycans in cell homeostasis and human disease. American Journal of Physiology-Cell Physiology 2022, 322 (5) , C849-C864.
    51. Olga N. Makshakova, Yuriy F. Zuev. Interaction-Induced Structural Transformations in Polysaccharide and Protein-Polysaccharide Gels as Functional Basis for Novel Soft-Matter: A Case of Carrageenans. Gels 2022, 8 (5) , 287.
    52. Edoardo Moretto, Skye Stuart, Sunaina Surana, Jose Norberto S. Vargas, Giampietro Schiavo. The Role of Extracellular Matrix Components in the Spreading of Pathological Protein Aggregates. Frontiers in Cellular Neuroscience 2022, 16
    53. Kariem Ezzat, Andrea Sturchio, Alberto J. Espay. Proteins Do Not Replicate, They Precipitate: Phase Transition and Loss of Function Toxicity in Amyloid Pathologies. Biology 2022, 11 (4) , 535.
    54. Francesca De Giorgi, Vladimir N. Uversky, François Ichas. α-Synuclein Fibrils as Penrose Machines: A Chameleon in the Gear. Biomolecules 2022, 12 (4) , 494.
    55. Pavel Semenyuk, Diana Evstafyeva, Vladimir Izumrudov, Vladimir Muronetz. Synthetic Sulfated Polymers Control Amyloid Aggregation of Ovine Prion Protein and Decrease Its Toxicity. Polymers 2022, 14 (7) , 1478.
    56. Vladimir I. Muronetz, Sofia S. Kudryavtseva, Evgeniia V. Leisi, Lidia P. Kurochkina, Kseniya V. Barinova, Elena V. Schmalhausen. Regulation by Different Types of Chaperones of Amyloid Transformation of Proteins Involved in the Development of Neurodegenerative Diseases. International Journal of Molecular Sciences 2022, 23 (5) , 2747.
    57. Nicholas J. Fiore, Yosif M. Ganat, Kapil Devkota, Rebecca Batorsky, Ming Lei, Kyongbum Lee, Lenore J. Cowen, Gist Croft, Scott A. Noggle, Thomas J. F. Nieland, David L. Kaplan. Bioengineered models of Parkinson’s disease using patient-derived dopaminergic neurons exhibit distinct biological profiles in a 3D microenvironment. Cellular and Molecular Life Sciences 2022, 79 (2)
    58. Inka Brockhausen, John Schutzbach, Jiabei Wang, Beth Fishwick, Jennifer Brockhausen. Glycoconjugate journal special issue on: the glycobiology of Parkinson’s disease. Glycoconjugate Journal 2022, 39 (1) , 55-74.
    59. Laxmikant Gadhe, Arunima Sakunthala, Semanti Mukherjee, Nitisha Gahlot, Riya Bera, Ajay Singh Sawner, Pradeep Kadu, Samir K. Maji. Intermediates of α-synuclein aggregation: Implications in Parkinson's disease pathogenesis. Biophysical Chemistry 2022, 281 , 106736.
    60. Anindita Roy, Akila V. Chalapathi, Kuberan Balagurunathan. Investigating the Roles of Heparan Sulfate Structures in Alpha-Synuclein Aggregation in Cell Culture Models. 2022, 807-820.
    61. Maria Ennemoser, Alexandra Pum, Andreas Kungl. Disease-specific glycosaminoglycan patterns in the extracellular matrix of human lung and brain. Carbohydrate Research 2022, 511 , 108480.
    62. Anita Pras, Bert Houben, Francesco A Aprile, Renée Seinstra, Rodrigo Gallardo, Leen Janssen, Wytse Hogewerf, Christian Gallrein, Matthias De Vleeschouwer, Alejandro Mata‐Cabana, Mandy Koopman, Esther Stroo, Minke de Vries, Samantha Louise Edwards, Janine Kirstein, Michele Vendruscolo, Salvatore Fabio Falsone, Frederic Rousseau, Joost Schymkowitz, Ellen A A Nollen. The cellular modifier MOAG‐4/SERF drives amyloid formation through charge complementation. The EMBO Journal 2021, 40 (21)
    63. Surabhi Mehra, Laxmikant Gadhe, Riya Bera, Ajay Singh Sawner, Samir K. Maji. Structural and Functional Insights into α-Synuclein Fibril Polymorphism. Biomolecules 2021, 11 (10) , 1419.
    64. Zahra Najarzadeh, Masihuz Zaman, Vita Sereikaite, Kristian Strømgaard, Maria Andreasen, Daniel E. Otzen. Heparin promotes fibrillation of most phenol-soluble modulin virulence peptides from Staphylococcus aureus. Journal of Biological Chemistry 2021, 297 (2) , 100953.
    65. Asad Jan, Nádia Pereira Gonçalves, Christian Bjerggaard Vaegter, Poul Henning Jensen, Nelson Ferreira. The Prion-Like Spreading of Alpha-Synuclein in Parkinson’s Disease: Update on Models and Hypotheses. International Journal of Molecular Sciences 2021, 22 (15) , 8338.
    66. Ana Freitas, Miguel Aroso, Sara Rocha, Rita Ferreira, Rui Vitorino, Maria Gomez‐Lazaro. Bioinformatic analysis of the human brain extracellular matrix proteome in neurodegenerative disorders. European Journal of Neuroscience 2021, 53 (12) , 4016-4033.
    67. Amy Brown, Marianna Török. Functional amyloids in the human body. Bioorganic & Medicinal Chemistry Letters 2021, 40 , 127914.
    68. Panagiota Mavroeidi, Maria Xilouri. Neurons and Glia Interplay in α-Synucleinopathies. International Journal of Molecular Sciences 2021, 22 (9) , 4994.
    69. Daniel Erskine, David Koss, Viktor I. Korolchuk, Tiago F. Outeiro, Johannes Attems, Ian McKeith. Lipids, lysosomes and mitochondria: insights into Lewy body formation from rare monogenic disorders. Acta Neuropathologica 2021, 141 (4) , 511-526.
    70. Anita Pras, Ellen A. A. Nollen. Regulation of Age-Related Protein Toxicity. Frontiers in Cell and Developmental Biology 2021, 9
    71. Monika Holubová, Petr Štěpánek, Martin Hrubý. Polymer materials as promoters/inhibitors of amyloid fibril formation. Colloid and Polymer Science 2021, 299 (3) , 343-362.
    72. Dan Li, Cong Liu. Hierarchical chemical determination of amyloid polymorphs in neurodegenerative disease. Nature Chemical Biology 2021, 17 (3) , 237-245.
    73. Sen Li, Yushan Yi, Ke Cui, Yanqiu Zhang, Yange Chen, Dou Han, Ling Sun, Xiaohui Zhang, Fei Chen, Yixin Zhang, Yufeng Yang, . A Single-Chain Variable Fragment Antibody Inhibits Aggregation of Phosphorylated Tau and Ameliorates Tau Toxicity in vitro and in vivo. Journal of Alzheimer's Disease 2021, 79 (4) , 1613-1629.
    74. Weihua Jin, Fuming Zhang, Robert J. Linhardt. Glycosaminoglycans in Neurodegenerative Diseases. 2021, 189-204.
    75. Keiichi Yamaguchi, Masatomo So, César Aguirre, Kensuke Ikenaka, Hideki Mochizuki, Yasushi Kawata, Yuji Goto. Polyphosphates induce amyloid fibril formation of α-synuclein in concentration-dependent distinct manners. Journal of Biological Chemistry 2021, 296 , 100510.
    76. Valentina Greco, Irina Naletova, Ikhlas M. M. Ahmed, Susanna Vaccaro, Luciano Messina, Diego La Mendola, Francesco Bellia, Sebastiano Sciuto, Cristina Satriano, Enrico Rizzarelli. Hyaluronan-carnosine conjugates inhibit Aβ aggregation and toxicity. Scientific Reports 2020, 10 (1)
    77. Stephanie J. Guiney, Paul A. Adlard, Peng Lei, Celeste H. Mawal, Ashley I. Bush, David I. Finkelstein, Scott Ayton. Fibrillar α-synuclein toxicity depends on functional lysosomes. Journal of Biological Chemistry 2020, 295 (51) , 17497-17513.
    78. Niccolo Candelise, Matthias Schmitz, Katrin Thüne, Maria Cramm, Alberto Rabano, Saima Zafar, Erik Stoops, Hugo Vanderstichele, Anna Villar-Pique, Franc Llorens, Inga Zerr. Effect of the micro-environment on α-synuclein conversion and implication in seeded conversion assays. Translational Neurodegeneration 2020, 9 (1)
    79. Stefanie Smolders, Christine Van Broeckhoven. Genetic perspective on the synergistic connection between vesicular transport, lysosomal and mitochondrial pathways associated with Parkinson’s disease pathogenesis. Acta Neuropathologica Communications 2020, 8 (1)
    80. Yu-Mi Jeon, Younghwi Kwon, Myungjin Jo, Shinrye Lee, Seyeon Kim, Hyung-Jun Kim. The Role of Glial Mitochondria in α-Synuclein Toxicity. Frontiers in Cell and Developmental Biology 2020, 8
    81. Lars Lewejohann, Srinivas R. Pallerla, Rebecca S. Schreiber, Joanna Gerula, Kay Grobe. Cerebellar Morphology and Behavioral Profiles in Mice Lacking Heparan Sulfate Ndst Gene Function. Journal of Developmental Biology 2020, 8 (3) , 13.
    82. Line K. Skaanning, Angelo Santoro, Thomas Skamris, Jacob Hertz Martinsen, Anna Maria D’Ursi, Saskia Bucciarelli, Bente Vestergaard, Katrine Bugge, Annette Eva Langkilde, Birthe B. Kragelund. The Non-Fibrillating N-Terminal of α-Synuclein Binds and Co-Fibrillates with Heparin. Biomolecules 2020, 10 (8) , 1192.
    83. Patricia Aguilar-Calvo, Alejandro M. Sevillano, Jaidev Bapat, Katrin Soldau, Daniel R. Sandoval, Hermann C. Altmeppen, Luise Linsenmeier, Donald P. Pizzo, Michael D. Geschwind, Henry Sanchez, Brian S. Appleby, Mark L. Cohen, Jiri G. Safar, Steven D. Edland, Markus Glatzel, K. Peter R. Nilsson, Jeffrey D. Esko, Christina J. Sigurdson. Shortening heparan sulfate chains prolongs survival and reduces parenchymal plaques in prion disease caused by mobile, ADAM10-cleaved prions. Acta Neuropathologica 2020, 139 (3) , 527-546.
    84. Pavel Semenyuk, Lidia Kurochkina, Kseniya Barinova, Vladimir Muronetz. Alpha-Synuclein Amyloid Aggregation Is Inhibited by Sulfated Aromatic Polymers and Pyridinium Polycation. Polymers 2020, 12 (3) , 517.
    85. Magisetty Obulesu. α-Synuclein-targeted nanoparticles. 2020, 103-114.
    86. Jia Wang, He Zhu, Huizhu Gan, Qin Meng, Guangguang Du, Yang An, Jihua Liu. The effect of heparan sulfate on promoting amyloid fibril formation by β-casein and their binding research with multi-spectroscopic approaches. Journal of Photochemistry and Photobiology B: Biology 2020, 202 , 111671.
    87. Serena Singh, Mari L DeMarco. In Vitro Conversion Assays Diagnostic for Neurodegenerative Proteinopathies. The Journal of Applied Laboratory Medicine 2020, 5 (1) , 142-157.
    88. Anett Hudák, Erzsébet Kusz, Ildikó Domonkos, Katalin Jósvay, Alpha Tom Kodamullil, László Szilák, Martin Hofmann-Apitius, Tamás Letoha. Contribution of syndecans to cellular uptake and fibrillation of α-synuclein and tau. Scientific Reports 2019, 9 (1)
    89. Ben A. Meinen, Varun V. Gadkari, Frederick Stull, Brandon T. Ruotolo, James C. A. Bardwell. SERF engages in a fuzzy complex that accelerates primary nucleation of amyloid proteins. Proceedings of the National Academy of Sciences 2019, 116 (46) , 23040-23049.
    90. Surabhi Mehra, Shruti Sahay, Samir K. Maji. α-Synuclein misfolding and aggregation: Implications in Parkinson’s disease pathogenesis. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 2019, 1867 (10) , 890-908.
    91. Justine Lempart, Eric Tse, James A Lauer, Magdalena I Ivanova, Alexandra Sutter, Nicholas Yoo, Philipp Huettemann, Daniel Southworth, Ursula Jakob. Mechanistic insights into the protective roles of polyphosphate against amyloid cytotoxicity. Life Science Alliance 2019, 2 (5) , e201900486.
    92. Amir Tayaranian Marvian, David J. Koss, Farhang Aliakbari, Dina Morshedi, Tiago Fleming Outeiro. In vitro models of synucleinopathies: informing on molecular mechanisms and protective strategies. Journal of Neurochemistry 2019, 150 (5) , 535-565.
    93. Michael C. Owen, David Gnutt, Mimi Gao, Sebastian K. T. S. Wärmländer, Jüri Jarvet, Astrid Gräslund, Roland Winter, Simon Ebbinghaus, Birgit Strodel. Effects of in vivo conditions on amyloid aggregation. Chemical Society Reviews 2019, 48 (14) , 3946-3996.
    94. Daniel Ysselstein, Joshua M. Shulman, Dimitri Krainc. Emerging links between pediatric lysosomal storage diseases and adult parkinsonism. Movement Disorders 2019, 34 (5) , 614-624.
    95. Clara Iannuzzi, Margherita Borriello, Antonella D’Agostino, Donatella Cimini, Chiara Schiraldi, Ivana Sirangelo. Protective effect of extractive and biotechnological chondroitin in insulin amyloid and advanced glycation end product‐induced toxicity. Journal of Cellular Physiology 2019, 234 (4) , 3814-3828.
    96. Valentina Oliveri. Toward the discovery and development of effective modulators of α-synuclein amyloid aggregation. European Journal of Medicinal Chemistry 2019, 167 , 10-36.
    97. Jie Sheng, Nick K. Olrichs, Willie J. Geerts, Xueyi Li, Ashfaq Ur Rehman, Barend M. Gadella, Dora V. Kaloyanova, J. Bernd Helms. Zinc binding regulates amyloid-like aggregation of GAPR-1. Bioscience Reports 2019, 39 (2)
    98. Auriane Maïza, Sandrine Chantepie, Cecilia Vera, Alexandre Fifre, Minh Bao Huynh, Olivier Stettler, Mohand Ouidir Ouidja, Dulce Papy‐Garcia. The role of heparan sulfates in protein aggregation and their potential impact on neurodegeneration. FEBS Letters 2018, 592 (23) , 3806-3818.
    99. Federica Boraldi, Pasquale Moscarelli, Brigida Bochicchio, Antonietta Pepe, Anna M. Salvi, Daniela Quaglino. Heparan sulfates facilitate harmless amyloidogenic fibril formation interacting with elastin-like peptides. Scientific Reports 2018, 8 (1)
    100. Sinjan Choudhary, Shreyada N. Save, Sirisha L. Vavilala. Unravelling the inhibitory activity of Chlamydomonas reinhardtii sulfated polysaccharides against α-Synuclein fibrillation. Scientific Reports 2018, 8 (1)
    Load more citations

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Your Mendeley pairing has expired. Please reconnect