bims-proned Biomed News
on Proteostasis in neurodegeneration
Issue of 2024–08–18
fiveteen papers selected by
Verena Kohler, Umeå University



  1. ACS Chem Neurosci. 2024 Aug 16.
      Early-stage aggregates of amyloid-forming proteins, specifically soluble oligomers, are implicated in neurodegenerative diseases such as Alzheimer's disease, Parkinson's disease, and Huntington's disease. Protein aggregation is typically monitored by fluorescence using the amyloid-binding fluorophore thioflavin T (ThT). Thioflavin T interacts, however, preferentially with fibrillar amyloid structures rather than with soluble, early-stage aggregates. In contrast, the two fluorophores, aminonaphthalene 2-cyanoacrylate-spiropyran (AN-SP) and triazole-containing boron-dipyrromethene (taBODIPY), were reported to bind preferentially to early-stage aggregates of amyloidogenic proteins. The present study compares ThT with AN-SP and taBODIPY with regard to their ability to monitor early stages of aggregation of four different amyloid-forming proteins, including amyloid-β (Aβ), tau protein, amylin, and α-synuclein. The results show that the three fluorophores vary in their suitability to monitor the early aggregation of different amyloid-forming proteins. For instance, in the presence of Aβ and amylin, the fluorescence intensity of AN-SP increased at an earlier stage of aggregation than the fluorescence of ThT, albeit with only a small fluorescence increase in the case of AN-SP. In contrast, in the presence of tau and amylin, the fluorescence intensity of taBODIPY increased at an earlier stage of aggregation than the fluorescence of ThT. Finally, α-synuclein aggregation could only be monitored by ThT fluorescence; neither AN-SP nor taBODIPY showed a significant increase in fluorescence over the course of aggregation of α-synuclein. These results demonstrate the ability of AN-SP and taBODIPY to monitor the formation of early-stage aggregates from specific amyloid-forming proteins at an early stage of aggregation, although moderate increases in fluorescence intensity, relatively large uncertainties in fluorescence values, and limited solubility of both fluorophores limit their usefulness for some amyloid proteins. The capability to monitor early aggregation of some amyloid proteins, such as amylin, might accelerate the discovery of aggregation inhibitors to minimize the formation of toxic oligomeric species for potential therapeutic use.
    Keywords:  AN-SP; amylin; amyloid-beta (Aβ); early stage aggregates; fluorescence; taBODIPY; tau; α-synuclein
    DOI:  https://doi.org/10.1021/acschemneuro.4c00097
  2. Nat Rev Chem. 2024 Aug 12.
      There is an increasing amount of evidence that biomolecular condensates are linked to neurodegenerative diseases associated with protein aggregation, such as Alzheimer's disease and amyotrophic lateral sclerosis, although the mechanisms underlying this link remain elusive. In this Review, we summarize the possible connections between condensates and protein aggregation. We consider both liquid-to-solid transitions of phase-separated proteins and the partitioning of proteins into host condensates. We distinguish five key factors by which the physical and chemical environment of a condensate can influence protein aggregation, and we discuss their relevance in studies of protein aggregation in the presence of biomolecular condensates: increasing the local concentration of proteins, providing a distinct chemical microenvironment, introducing an interface wherein proteins can localize, changing the energy landscape of aggregation pathways, and the presence of chaperones in condensates. Analysing the role of biomolecular condensates in protein aggregation may be essential for a full understanding of amyloid formation and offers a new perspective that can help in developing new therapeutic strategies for the prevention and treatment of neurodegenerative diseases.
    DOI:  https://doi.org/10.1038/s41570-024-00635-w
  3. bioRxiv. 2024 Jul 30. pii: 2024.07.30.605873. [Epub ahead of print]
      I.Protein misfolding is a widespread phenomenon that can result in the formation of protein aggregates, which are markers of various disease states, including Alzheimer's disease (AD). In AD, amyloid beta (Aβ) peptides, particularly Aβ40 and Aβ42, are key players in the disease's progression, as they aggregate to form amyloid plaques and contribute to neuronal toxicity. Recent research has shifted attention from solely Aβ fibrils to also include Aβ protofibrils and oligomers as potentially critical pathogenic agents. Particularly, oligomers demonstrate greater toxicity compared to other Aβ specie. Hence, there is an increased interest in studying the correlation between toxicity and their structure and aggregation pathway. The present study investigates the aggregation of a 150 kDa Aβ42 oligomer that does not lead to fibril formation over time. Using negative stain transmission electron microscopy (TEM), size exclusion chromatography (SEC), dynamic light scattering (DLS), and cryo-electron microscopy (cryo-EM), we demonstrate that 150 kDa Aβ42 oligomers form higher-order string-like assemblies over time. The strings are unique from the classical Aβ fibril structures. The significance of our work lies in elucidating molecular behavior of a novel non-fibrillar form of Aβ42 aggregate.
    DOI:  https://doi.org/10.1101/2024.07.30.605873
  4. J Biochem Mol Toxicol. 2024 Aug;38(8): e23800
      Pyroglutamate (pE)-modified amyloid-β (Aβ) peptides play a crucial role in the development of Alzheimer's disease. pEAβ3-42 can rapidly form oligomers that gradually elongate hydrophobic segments to form β-sheet-rich amyloid intermediates, ultimately resulting in the formation of mature amyloid fibrils. pEAβ3-42 can also catalyze the aggregation of Aβ species and subsequently accelerate the formation of amyloid senile plaques. Considering the recent clinical success of the pEAβ3-42-targeting antibody donanemab, molecules that strongly bind pEAβ3-42 and prevent its aggregation and catalytic effect on Aβs may also provide potential therapeutic options for Alzheimer's disease. Here, we demonstrate that the natural antibiotic cyclopeptide tyrocidine A (TA) not only strongly inhibits the aggregation of Aβ1-42 as previously reported, but also interacts with the hydrophobic C-terminus and middle domain of pEAβ3-42 to maintain an unordered conformation, effectively impeding the formation of initial oligomers and subsequently halting the aggregation of pEAβ3-42. Furthermore, TA can disrupt the "catalytic effect" of pEAβ3-42 on amyloid aggregates, effectively suppressing Aβ aggregation and ultimately preventing the pathological events induced by Aβs.
    Keywords:  Alzheimer's disease; amyloid‐β; catalytic effect; pyroglutamate‐modified amyloid‐β; tyrocidine A
    DOI:  https://doi.org/10.1002/jbt.23800
  5. Ecotoxicol Environ Saf. 2024 Aug 10. pii: S0147-6513(24)00917-5. [Epub ahead of print]283 116841
      Lewy body disease (LBD), one of the most common neurodegenerative diseases (NDDs), is characterized by excessive accumulation of α-synuclein (α-syn) in neurons. In recent years, environmental factors such as exposure to herbicides and pesticides have been attributed to the development of this condition. While majority of the studies on neurotoxic effects of paraquat (PQ) have focused on α-syn-mediated neuronal damage in the early stages of α-syn accumulation in neurons, efforts to explore the key target for α-syn degradation are limited. Recent research has suggested that histone deacetylase 6 (HDAC6) might possibly regulate amyloid clearance, and that the metabolism of compounds in neurons is also directly affected by axonal transport in neurons. Dynein predominantly mediates reverse transportation of metabolites and uptake of signal molecules and other compounds at the end of axons, which is conducive to the reuse of cell components. However, the role of interaction of dynein with HDAC6 in metabolites transport is still unclear. Therefore, this study aimed to investigate the role of HDAC6 in α-syn accumulation/clearance in neurons and the associated possible influencing factors. The results revealed that HDAC6 could transport ubiquitinated α-syn, bind to dynein, form an aggresome, and relocate to the center of the microtubule tissue, ultimately reducing abnormal accumulation of α-syn. However, PQ treatment resulted in HDAC6 upregulation, causing abnormal aggregation of α-syn. Taken together, these findings indicated that PQ exposure caused abnormal accumulation of α-syn and decreased effective degradation of α-syn by HDAC6-mediated aggresome-autophagy-lysosome pathway.
    Keywords:  Aggresome; Autophagy; Dynein; Histone deacetylase 6; Paraquat; α-Synuclein
    DOI:  https://doi.org/10.1016/j.ecoenv.2024.116841
  6. Protein Sci. 2024 Sep;33(9): e5099
      The microtubule associated protein, tau, is implicated in a multitude of neurodegenerative disorders that are collectively termed as tauopathies. These disorders are characterized by the presence of tau aggregates within the brain of afflicted individuals. Mutations within the MAPT gene that encodes the tau protein form the genetic backdrop for familial forms of tauopathies, such as frontotemporal dementia (FTD), but the molecular consequences of such alterations and their pathological effects are unclear. We sought to investigate the conformational properties of the aggregates of three tau mutants: A152T, P301L, and R406W, all implicated within FTD, and compare them to those of the native form (WT-Tau 2N4R). Our immunochemical analysis reveals that mutants and WT tau oligomers exhibit similar affinity for conformation-specific antibodies but have distinct morphology and secondary structure. Additionally, these oligomers possess different dye-binding properties and varying sensitivity to proteolytic processing. These results point to conformational variety among them. We then tested the ability of the mutant oligomers to cross-seed the aggregation of WT tau monomer. Using similar array of experiments, we found that cross-seeding with mutant aggregates leads to the formation of conformationally unique WT oligomers. The results discussed in this paper provide a novel perspective on the structural properties of oligomeric forms of WT tau 2N4R and its mutant, along with shedding some light on their cross-seeding behavior.
    Keywords:  MAPT; conformation; cross‐seeding; frontotemporal dementia; oligomers; tauopathy
    DOI:  https://doi.org/10.1002/pro.5099
  7. Proc Natl Acad Sci U S A. 2024 Aug 20. 121(34): e2315006121
      Amyloid formation by α-synuclein (αSyn) occurs in Parkinson's disease, multiple system atrophy, and dementia with Lewy bodies. Deciphering the residues that regulate αSyn amyloid fibril formation will not only provide mechanistic insight but may also reveal targets to prevent and treat disease. Previous investigations have identified several regions of αSyn to be important in the regulation of amyloid formation, including the non-amyloid-β component (NAC), P1 region (residues 36 to 42), and residues in the C-terminal domain. Recent studies have also indicated the importance of the N-terminal region of αSyn for both its physiological and pathological roles. Here, the role of residues 2 to 7 in the N-terminal region of αSyn is investigated in terms of their ability to regulate amyloid fibril formation in vitro and in vivo. Deletion of these residues (αSynΔN7) slows the rate of fibril formation in vitro and reduces the capacity of the protein to be recruited by wild-type (αSynWT) fibril seeds, despite cryo-EM showing a fibril structure consistent with those of full-length αSyn. Strikingly, fibril formation of αSynΔN7 is not induced by liposomes, despite the protein binding to liposomes with similar affinity to αSynWT. A Caenorhabditis elegans model also showed that αSynΔN7::YFP forms few puncta and lacks motility and lifespan defects typified by expression of αSynWT::YFP. Together, the results demonstrate the involvement of residues 2 to 7 of αSyn in amyloid formation, revealing a target for the design of amyloid inhibitors that may leave the functional role of the protein in membrane binding unperturbed.
    Keywords:  amyloid; liposome; membrane; synuclein
    DOI:  https://doi.org/10.1073/pnas.2315006121
  8. Biomark Res. 2024 Aug 13. 12(1): 81
      Tissue-resident macrophages and recruited macrophages play pivotal roles in innate immunity and the maintenance of brain homeostasis. Investigating the involvement of these macrophage populations in eliciting pathological changes associated with neurodegenerative diseases has been a focal point of research. Dysregulated states of macrophages can compromise clearance mechanisms for pathological proteins such as amyloid-β (Aβ) in Alzheimer's disease (AD) and TDP-43 in Amyotrophic lateral sclerosis (ALS). Additionally, recent evidence suggests that abnormalities in the peripheral clearance of pathological proteins are implicated in the pathogenesis and progression of neurodegenerative diseases. Furthermore, numerous genome-wide association studies have linked genetic risk factors, which alter the functionality of various immune cells, to the accumulation of pathological proteins. This review aims to unravel the intricacies of macrophage biology in both homeostatic conditions and neurodegenerative disorders. To this end, we initially provide an overview of the modifications in receptor and gene expression observed in diverse macrophage subsets throughout development. Subsequently, we outlined the roles of resident macrophages and recruited macrophages in neurodegenerative diseases and the progress of targeted therapy. Finally, we describe the latest advances in macrophage imaging methods and measurement of inflammation, which may provide information and related treatment strategies that hold promise for informing the design of future investigations and therapeutic interventions.
    Keywords:  Gene expression; Imaging methodologies; Immune cells; Macrophages; Neurodegenerative disease
    DOI:  https://doi.org/10.1186/s40364-024-00624-7
  9. SciBase Neurol. 2024 ;pii: 1017. [Epub ahead of print]2(2):
      This study investigates the role of histone tail modifications in Parkinson's disease (PD), emphasizing the epigenetic regulation of genes associated with the disease. PD primarily manifests in individuals over 60, suggesting that PD-causal genes remain dormant until later in life, influenced by environmental factors and epigenetic modifications. Histone modifications such as methylation, acetylation, phosphorylation, and ubiquitylation play crucial roles in gene expression regulation by altering chromatin structure or interacting with gene regulatory regions. Specifically, modifications on histones H2A, H2AX, H3, and H4 have been linked to PD. For instance, α-synuclein (α-SYN) aggregation, a hallmark of PD, is regulated by histone modifications like H3K27ac and H3K4me3, which enhance α-SYN expression and contribute to PD progression. Conversely, repressive marks like H3K9ac and H3K27me3 can mitigate PD risk by reducing α-SYN levels. Therapeutic strategies targeting these histone modifications, such as the use of GSK-J4 or vitamin C-treated neural stem cells, show potential in alleviating PD symptoms by modulating histone marks and gene expression. Understanding these epigenetic mechanisms offers promising avenues for developing novel treatments for PD.
    Keywords:  Parkinson’s disease; acetylation; epigenetic regulation; gene expression; histone modification; histone tail; methylation
  10. Neuroscience. 2024 Aug 09. pii: S0306-4522(24)00386-5. [Epub ahead of print]557 1-11
      Previous studies have shown that α-synuclein (α-Syn) aggregates derived from the brains of patients with Parkinson's disease (PD) and multiple system atrophy (MSA) exhibit different phosphorylation, cytotoxicity, and seeding activity. However, the mechanism underlying the differences remains poorly understood. Here, recombinant human α-Syn was incubated in the plasma of patients with PD and MSA, and the oligomers formed in the plasma (PD-O-α-Syn and MSA-O-α-Syn) were purified and analyzed for their phosphorylation, cytotoxicity and seeding activity. In vitro assays revealed that both PD-O-α-Syn and MSA-O-α-Syn were phosphorylated at serine 129. However, the phosphorylation degree of MSA-O-α-Syn was significantly higher than that of PD-O-α-Syn. In addition, MSA-O-α-Syn exhibited stronger cytotoxicity and seeding activity compared with PD-O-α-Syn. In vivo experiments showed that mice receiving intrastriatal inoculation of MSA-O-α-Syn developed more severe motor dysfunction and dopaminergic degeneration than mice receiving intrastriatal inoculation of PD-O-α-Syn. Compared with the mice inoculated with PD-O-α-Syn, the mice inoculated with MSA-O-α-Syn accumulated more phosphorylated and oligomerized α-Syn in the striatum and brain regions (substantia nigra, hippocampus and prefrontal cortex) away from the inoculated site. The results obtained suggest that α-Syn oligomers formed in PD and MSA plasma are different in phosphorylation, cytotoxicity, and seeding activity.
    Keywords:  Cytotoxicity; Multiple system atrophy; Parkinson’s disease; Phosphorylation; Seeding activity; α-synuclein
    DOI:  https://doi.org/10.1016/j.neuroscience.2024.08.006
  11. J Biol Chem. 2024 Aug 09. pii: S0021-9258(24)02161-6. [Epub ahead of print] 107660
      Protein aggregation is a common feature of many neurodegenerative diseases. In Huntington's disease, mutant huntingtin is the primary aggregating protein, but the aggregation of other proteins, such as TDP43, is likely to further contribute to toxicity. Moreover, mutant huntingtin is also a risk factor for TDP pathology in ALS. Despite this co-pathology of huntingtin and TDP43, it remains unknown whether these amyloidogenic proteins directly interact with each other. Using a combination of biophysical methods, we show that the aggregation prone regions of both proteins, huntingtin exon-1 (Httex1) and the TDP43 low complexity domain (TDP43-LCD), interact in a conformationally specific manner. This interaction significantly slows Httex1 aggregation, while it accelerates TDP43-LCD aggregation. A key intermediate responsible for both effects is a complex formed by liquid TDP43-LCD condensates and Httex1 fibrils. This complex shields seeding competent surfaces of Httex1 fibrils from Httex1 monomers, which are excluded from the condensates. In contrast, TDP43-LCD condensates undergo an accelerated liquid-to-solid transition upon exposure to Httex1 fibrils. Cellular studies show co-aggregation of untagged Httex1 with TDP43. This interaction causes mislocalization of TDP43, which has been linked to TDP43 toxicity. The protection from Httex1 aggregation in lieu of TDP43-LCD aggregation is interesting, as it mirrors what has been found in disease models, namely that TDP43 can protect from huntingtin toxicity, while mutant huntingtin can promote TDP43 pathology. These results suggest that direct protein interaction could, at least in part, be responsible for the linked pathologies of both proteins.
    Keywords:  ALS; Huntington’s disease; TDP43; coaggregation; condensates; electron paramagnetic resonance; huntingtin exon-1; protein aggregation
    DOI:  https://doi.org/10.1016/j.jbc.2024.107660
  12. ACS Chem Neurosci. 2024 Aug 10.
      Alzheimer's disease (AD) stands as one of the most prevalent neurodegenerative conditions, leading to cognitive impairment, with no cure and preventive measures. Misfolding and aberrant aggregation of amyloid-β (Aβ) peptides are believed to be the underlying cause of AD. These amyloid aggregates culminate in the development of toxic Aβ oligomers and subsequent accumulation of β-amyloid plaques amidst neuronal cells in the brain, marking the hallmarks of AD. Drug development for the potentially curative treatment of Alzheimer's is, therefore, a tremendous challenge for the scientific community. In this study, we investigate the potency of Whitlock's caffeine-armed molecular tweezer in combating the deleterious effects of Aβ aggregation, with special emphasis on the seven residue Aβ16-22 fragment. Extensive all-atom molecular dynamics simulations are conducted to probe the various structural and conformational transitions of the peptides in an aqueous medium in both the presence and absence of tweezers. To explore the specifics of peptide-tweezer interactions, radial distribution functions, contact number calculations, binding free energies, and 2-D kernel density plots depicting the variation of distance-angle between the aromatic planes of the peptide-tweezer pair are computed. The central hydrophobic core, particularly the aromatic Phe residues, is crucial in the development of harmful amyloid oligomers. Notably, all analyses indicate reduced interpeptide interactions in the presence of the tweezer, which is attributed to the tweezer-Phe aromatic interaction. Upon increasing the tweezer concentration, the residues of the peptide are further encased in a hydrophobic environment created by the self-aggregating tweezer cluster, leading to the segregation of the peptide residues. This is further aided by the weakening of interstrand hydrogen bonding between the peptides, thereby impeding their self-aggregation and preventing the formation of neurotoxic β-amyloid. Furthermore, the study also highlights the efficacy of the molecular tweezer in destabilizing preformed amyloid fibrils as well as hindering the aggregation of the full-length Aβ1-42 peptide.
    Keywords:  amyloid-β peptide; aromatic stacking; molecular tweezer; neurodegenerative disease; peptide aggregation; peptide inhibitor
    DOI:  https://doi.org/10.1021/acschemneuro.4c00387
  13. ACS Chem Neurosci. 2024 Aug 15.
      Various oligomeric species of amyloid-beta have been proposed to play different immunogenic roles in the cellular pathology of Alzheimer's Disease. The dynamic interconversion between various amyloid oligomers and fibrillar assemblies makes it difficult to elucidate the role each potential aggregation state may play in driving neuroinflammatory and neurodegenerative pathology. The ability to identify the amyloid species that are key and essential drivers of these pathological hallmarks of Alzheimer's Disease is of fundamental importance for also understanding downstream events including tauopathies that mediate neuroinflammation with neurologic deficits. Here, we report the design and construction of a quantum dot mimetic for larger spherical oligomeric amyloid species as an "endogenously" fluorescent proxy for this cytotoxic assembly of amyloid to investigate its role in inducing inflammatory and stress response states in neuronal and glial cell types. The design parameters and construction protocol developed here may be adapted for developing quantum dot nano-bio assemblies for other biological systems of interest, particularly neurodegenerative diseases involving other protein aggregates.
    Keywords:  Alzheimer’s; amyloid; biomimetic; fluorescence microscopy; neuronal imaging; neurotoxic oligomers; quantum dots
    DOI:  https://doi.org/10.1021/acschemneuro.4c00183
  14. J Phys Chem Lett. 2024 Aug 14. 8577-8583
      A progressive aggregation of Tau proteins in the brain is linked to both Alzheimer's disease (AD) and various Tauopathies. This pathological process can be enhanced by several substances, including heparin. However, very little if anything is known about molecules that can inhibit the aggregation of Tau isoforms. In this study, we examined the effect of phosphatidylserines (PSs) with various lengths and saturations of fatty acids (FAs) on the aggregation properties of Tau isoforms with one (1N4R) and two (2N4R) N-terminal inserts that enhance binding of Tau to tubulin. We found that PS with unsaturated and short-length FAs inhibited Tau aggregation and drastically lowered the toxicity of Tau oligomers that were formed in the presence of such phospholipids. Such an effect was not observed for PS with fully saturated long-chain FAs. These results suggest that a short-chain irreversible disbalance between saturated and unsaturated lipids in the brain could be the trigger of Tau aggregation.
    DOI:  https://doi.org/10.1021/acs.jpclett.4c01718
  15. Database (Oxford). 2024 Aug 08. 2024 0
      A structural alteration in copper/zinc superoxide dismutase (SOD1) is one of the common features caused by amyotrophic lateral sclerosis (ALS)-linked mutations. Although a large number of SOD1 variants have been reported in ALS patients, the detailed structural properties of each variant are not well summarized. We present SoDCoD, a database of superoxide dismutase conformational diversity, collecting our comprehensive biochemical analyses of the structural changes in SOD1 caused by ALS-linked gene mutations and other perturbations. SoDCoD version 1.0 contains information about the properties of 188 types of SOD1 mutants, including structural changes and their binding to Derlin-1, as well as a set of genes contributing to the proteostasis of mutant-like wild-type SOD1. This database provides valuable insights into the diagnosis and treatment of ALS, particularly by targeting conformational alterations in SOD1. Database URL: https://fujisawagroup.github.io/SoDCoDweb/.
    DOI:  https://doi.org/10.1093/database/baae064