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Sunde, M.

Publications and source records attributed to Sunde, M..

11 recordsLinked to original sources

A conformational switch governs the dual role of liquid-liquid phase separation in amyloid fibrillization

Biomolecular condensates provide dynamic environments that store and organize proteins, yet the fundamental principles determining whether condensation promotes or suppresses irreversible protein aggregation remain unclear. Here, we show that the receptor-interacting protein kinase 3 (RIPK3) RHIM domain follows distinct self-assembly pathways into condensates or amyloid fibrils depending on its conformational state. We find that predominantly folded proteins undergo liquid-liquid phase separation (LLPS), forming reversible condensates that kinetically suppress fibril formation. Partial unfolding instead promotes direct fibrillization that bypasses LLPS, whereas induced condensate formation via increasing ionic strength or addition of molecular crowder delays amyloid formation. In contrast, when the protein is predominantly unfolded, LLPS accelerates fibrillization through condensate-interface-mediated nucleation. These findings establish protein conformation as a determinant of whether condensates suppress or promote amyloid assembly, revealing a dual role for phase separation in regulating functional amyloid formation and providing a framework that connects condensate dynamics with cellular functions.

biophysics↗

Semaphorin 3G (SEMA3G) is a highly selective marker of cerebral amyloid angiopathy

Biomarkers of cerebral amyloid angiopathy (CAA) are critically needed. We recently identified semaphorin 3G (SEMA3G) as a novel protein selectively enriched in CAA. Here, we aimed to determine if SEMA3G was a selective marker of CAA in a large cohort of human brain tissue spanning multiple neurodegenerative diseases and three brain regions, and to determine if SEMA3G directly interacts with amyloid beta (A{beta}). Multiplexed immunofluorescence showed that SEMA3G significantly accumulated only in CAA+ blood vessels in the brain in all cases. We also showed that SEMA3G preferentially associated with A{beta}40, A{beta}pS8 and A{beta}pE3, but not A{beta}42. Thioflavin T assays and transmission electron microscopy showed that SEMA3G directly interacted with A{beta} and slowed A{beta} aggregation in vitro, and that this effect was more pronounced for A{beta}40 than A{beta}42. Together our results demonstrate that SEMA3G is a highly specific marker of CAA in the brain.

neuroscience↗

De novo Cyclic Peptides Allow Visualisation of the Monomeric and Functional Amyloid Conformations of the Kinase RIPK3

Receptor Interacting Protein Kinase 3 (RIPK3) is a central regulator of necroptosis and a key mediator of inflammatory signaling. Its function is orchestrated through RIP Homotypic Interaction Motif (RHIM)-dependent interactions with other RHIM-containing adapter proteins, forming amyloid-structured necrosomes that trigger kinase activation and subsequently lead to immunogenic cell lysis. Necroptosis eliminates infected or damaged cells and provokes a strong inflammatory response. Dysregulated necroptosis is implicated in chronic inflammatory diseases and associated with ischaemic injury. Despite separate structural elucidation of the isolated RIPK3 kinase domain and the amyloid fibrils formed by the RIPK3 RHIM-containing region, visualizing full-length human RIPK3 in live cells remains challenging due to a lack of specific tools. To address this, we employed Random Non-standard Peptide Integrated Discovery (RaPID) mRNA display to identify cyclic peptides that bind the RHIM-containing region of RIPK3 during its assembly into amyloid fibrils. Three peptides were selected for characterisation and demonstrate utility in visualizing RIPK3 in human cells. These peptides represent promising tools for probing RIPK3 localisation and modulating its function.

biochemistry↗

A One Health study of Klebsiella pneumoniae species complex plasmids shows a highly diverse and ecologically adaptable plasmidome

Plasmids play a pivotal role in the horizontal gene transfer of antimicrobial resistance (AMR) and virulence determinants among bacteria. Members of the Klebsiella pneumoniae species complex (KpSC) can colonise humans, animals, and various environments, and frequently cause nosocomial and community-acquired infections in humans. While plasmid-borne AMR genes are prevalent in clinical strains, the diversity, distribution, and association of plasmids encoding AMR and virulence across ecological niches remain poorly characterised. Understanding the traits governing successful plasmid transmission within and between ecological niches is critical for developing effective AMR prevention strategies. Here, we characterise the diversity and distribution of KpSC plasmids and identify potential niche associations of AMR, heavy metal resistance, virulence factors, and plasmid clusters. We analysed the plasmidome (i.e. total genetic content attributable to plasmids) of 578 whole-genome sequenced KpSC isolates collected in Norway between 2001-2020 from human (n=453), terrestrial animal (n=102), and marine (n=23) sources. Plasmids from complete hybrid assemblies were annotated and clustered to evaluate the plasmid diversity and content across niches. Additionally, the representativeness of this plasmid collection was determined by clustering with a global collection of 8656 circularised KpSC plasmids. In total, 1415 circularised plasmids were identified and grouped according to rearrangement distance using Pling, resulting in 130 clusters (containing >1 plasmid), of which 36% (n=47) contained plasmids from >1 niche. The plasmids exhibited significant diversity, as 37% (n=524) remained singletons after clustering. AMR and virulence genes existed across diverse clusters and singletons, but predominantly resided on 120-250 kbp conjugative or mobilisable plasmids harbouring various transposable elements. The human niche exhibited a significantly higher prevalence of plasmids with AMR genes compared to animal or marine niches (p<0.001), whereas the animal niche displayed a significantly higher prevalence of virulence-encoding plasmids compared to human or marine niches (p<0.001), which was largely due to an enrichment of iuc3 plasmids in pigs. The high diversity of the KpSC plasmids underscores the dynamic nature of plasmid evolution, driven by horizontal gene transfer, and selective pressures. The presence of variable clusters, marked by high genetic diversity, indicates a dynamic plasmidome capable of rapid adaptation to environmental pressures through the acquisition and rearrangement of accessory genes.

microbiology↗

Structural Studies of an Anti-necroptosis Viral:Human Functional Hetero-amyloid M45:RIPK3 using SSNMR

The formation of RIP-homotypic interaction motif (RHIM)-based heteromeric amyloid assemblies between effector proteins such as RIPK1, ZBP1, or TRIF and the kinase RIPK3 serve as regulating signals for the necroptosis process, a key element of innate immune defense. Murine cytomegalovirus (MCMV) expresses the M45-encoded viral inhibitor of RIP activation (vIRA) which inhibits necroptosis in a RHIM-dependent manner. A pivotal question is how viral M45 forms hetero-amyloids with RIPK3 to effectively create an inhibitory assembly. We report a novel high-resolution structure of the M45:RIPK3 complex where M45 and RIPK3 alternately stack in an amyloid-state structure. Mutagenesis of the residues flanking the IQIG tetrad in M45 results in specific impacts on co-assembly with RIPK3, indicating an extended interface in the heteromeric fibrils. Other key interactions support the formation of stable viral:host fibrils. The M45: RIPK3 hetero-amyloid is likely to act as an anti-necroptotic signal by competing with formation of other pro-necroptotic species and introducing a barrier to RIPK3 autophosphorylation. Significance StatementThis study investigates the structural biology of the necroptotic pathway, an understudied programmed cell death mechanism that plays a crucial role in innate immunity and has implications for infectious diseases, cell cycle regulation, and cancer. We present the high-resolution structure of a cross-species hetero-amyloid in which M45, a murine cytomegalovirus (MCMV) protein, co-assembles with human RIPK3 to inhibit necroptosis by competing with pro-necroptotic amyloids. Using solid-state NMR, cryo-EM, mutagenesis, and biophysical analyses, we uncover a novel structural paradigm for cross-species hetero-amyloids, shedding light on viral strategies to manipulate host immunity and protein interactions.

biophysics↗

A genome-wide One Health study of Klebsiella pneumoniae in Norway reveals overlapping populations but few recent transmission events across reservoirs

Members of the Klebsiella pneumoniae species complex (KpSC) are opportunistic pathogens that cause severe and difficult-to-treat infections. KpSC are common in non-human niches, but the clinical relevance of these populations is disputed. Utilising 3,255 whole-genome sequenced isolates from human, animal and marine sources collected during 2001-2020 in Norway, we showed the KpSC populations in different niches were distinct but overlapping. Notably, human infection isolates showed greatest connectivity with each other, followed by isolates from human carriage, pigs, and bivalves. Nearly 5% of human infection isolates had close relatives ([&le;]22 substitutions) amongst animal and marine isolates, despite temporally and geographically distant sampling of these sources. Infection prevention measures are essential to limit transmission within human clinical settings and reduce disease burden. However, as colonisation often precedes infection, preventing transmission that leads to colonisation, e.g. transmission between animals and humans in the community, and in the food chain, could also be beneficial.

microbiology↗

Two-color coincidence single-molecule pull-down for the specific detection of disease-associated protein aggregates

The misfolding and aggregation of protein is a characteristic of many neurodegenerative disorders, including Alzheimers and Parkinsons disease. The wide range of sizes and structures of oligomers and fibrils generated have previously been studied using single-molecule and super-resolution microscopy. These methods, however, tend to rely on the use of either directly labeled protein, or on the addition of non-specific amyloid stains, such as thioflavin-T. This has prevented the characterization of protein aggregate composition in complex biological samples. Here, we have developed a single-molecule two-color aggregate pull-down (STAPull) assay to overcome this challenge by probing immobilized proteins using orthogonally labeled antibodies targeting the same epitope. By looking at colocalized signals, we can eliminate monomeric protein, and specifically quantify aggregated proteins. Using the aggregation-prone alpha-synuclein protein as a model, we demonstrate that this approach can specifically detect aggregates with a limit of detection of 5 pM. Furthermore, we show that STAPull can be used in a range of samples, including in human biofluids. STAPull is generally applicable to protein aggregates from a variety of disorders, and will aid in the identification of biomarkers that are crucial in the effort to diagnose these diseases.

neuroscience↗

iPSC-Derived PSEN2 (N141I) Astrocytes and Microglia Exhibit a Primed Inflammatory Phenotype

BackgroundWidescale evidence points to the involvement of glia and immune pathways in the progression of Alzheimers disease (AD). AD-associated iPSC-derived glial cells show a diverse range of AD-related phenotypic states encompassing cytokine/chemokine release, phagocytosis and morphological profiles, but to date studies are limited to cells derived from PSEN1, APOE and APP mutations or sporadic patients. The aim of the current study was to successfully differentiate iPSC-derived microglia and astrocytes from patients harbouring an AD-causative PSEN2 (N141I) mutation and characterise the inflammatory and morphological profile of these cells. MethodsiPSCs from three healthy control individuals and three familial AD patients harbouring a heterozygous PSEN2 (N141I) mutation were used to derive astrocytes and microglia-like cells and cell identity and morphology were characterised through immunofluorescent microscopy. Cellular characterisation involved the stimulation of these cells by LPS and A{beta}42 and analysis of cytokine/chemokine release was conducted through ELISAs and multi-cytokine arrays. The phagocytic capacity of these cells was then indexed by the uptake of fluorescently labelled fibrillar A{beta}42. ResultsAD-derived astrocytes and microglia-like cells exhibited an atrophied and less complex morphological appearance than healthy controls. AD-derived astrocytes showed increased basal expression of GFAP, S100{beta} and increased secretion and phagocytosis of A{beta}42 while AD-derived microglia-like cells showed decreased IL-8 secretion compared to healthy controls. Upon immunological challenge AD-derived astrocytes and microglia-like cells show exaggerated secretion of the pro-inflammatory IL-6, CXCL1, ICAM-1 and IL-8 from astrocytes and IL-18 and MIF from microglia. ConclusionOur study showed, for the first time, the differentiation and characterisation of iPSC-derived astrocytes and microglia-like cells harbouring a PSEN2 (N141I) mutation. PSEN2 (N141I)-mutant astrocytes and microglia-like cells presented with a primed phenotype characterised by reduced morphological complexity, exaggerated pro-inflammatory cytokine secretion and altered A{beta}42 production and phagocytosis.

neuroscience↗

Perphenazine-macrocycle conjugates divert Aβ42 towards non-toxic aggregates by monomer sequestration.

Alzheimers disease is imposing a growing social and economic burden worldwide and effective therapies are required. Strategies aimed at the removal of fibrillar plaques formed by the amyloid-{beta} peptide have not proved therapeutic and the focus has shifted to approaches that target the cytotoxic oligomeric amyloid-{beta} species that are populated before fibrils are deposited. We have designed and synthesized perphenazine-cyclam conjugates that specifically and rapidly bind to the monomeric form of A{beta}42, reducing the production of both cytotoxic oligomers and amyloid fibrils. We have applied detailed kinetic analysis and NMR spectroscopy to show that the perphenazine-cyclam conjugates divert the A{beta}42 monomer into amorphous aggregates that are not toxic to differentiated SH-SY5Y cells in vitro. Unlike most other amyloid inhibitors studied to date, these conjugates inhibit oligomer and fibril assembly even in the presence of pre-formed fibrillar seeds, demonstrating that they act through a monomer sequestration mechanism. These modular, three-dimensional conjugates therefore effectively prevent monomer-dependent secondary nucleation, the autocatalytic process that generates the majority of toxic oligomers.

biophysics↗

Varicella zoster virus encodes a viral decoy RHIM to inhibit cell death

Herpesviruses are known to encode a number of inhibitors of host cell death, including Rip Homotypic Interaction Motif (RHIM)-containing proteins. Varicella zoster virus (VZV) is a member of the alphaherpesvirus subfamily and is responsible for causing chickenpox and shingles. We have identified a novel viral RHIM in the VZV capsid triplex protein open reading frame (ORF) 20 that acts as a host cell death inhibitor. Like the human cellular RHIMs in RIPK1 and RIPK3 that stabilise the necrosome in TNF-induced necroptosis, and the viral RHIM in M45 from murine cytomegalovirus that inhibits cell death, the ORF20 RHIM is capable of forming fibrillar functional amyloid complexes. Notably, the ORF20 RHIM forms hybrid amyloid complexes with human ZBP1, a cytoplasmic sensor of viral nucleic acid. Although VZV can inhibit TNF-induced necroptosis, the ORF20 RHIM does not appear to be responsible for this inhibition. In contrast, the ZBP1 pathway is identified as important for VZV infection. Mutation of the ORF20 RHIM renders the virus incapable of efficient spread in ZBP1-expressing HT-29 cells, an effect which can be reversed by the inhibition of caspases. Therefore we conclude that the VZV ORF20 RHIM is important for preventing ZBP1-driven apoptosis during VZV infection, and propose that it mediates this effect by sequestering ZBP1 into decoy amyloid assemblies. Author SummaryRip homotypic interaction motifs (RHIMs) are found in host proteins that can signal for programmed cell death and in viral proteins that can prevent it. Complexes stabilized by intermolecular interactions involving RHIMs have a fibrillar amyloid structure. We have identified a novel RHIM within the ORF20 protein expressed by Varicella zoster virus (VZV) that forms amyloid-based complexes with human cellular RHIMs. Whereas other herpesvirus RHIMs inhibit TNF-driven necroptosis, this new VZV RHIM targets the host RHIM-containing protein ZBP1 to inhibit apoptosis during infection. This is the first study to demonstrate the importance of the ZBP1 pathway in VZV infection and to identify the role of a viral RHIM in apoptosis inhibition. It broadens our understanding of host defense pathways and demonstrates how a decoy amyloid strategy is employed by pathogens to circumvent the host response.

microbiology↗

The RHIM within the M45 protein from murine cytomegalovirus forms heteromeric functional amyloid fibrils with RIPK1 and RIPK3

The M45 protein from murine cytomegalovirus protects infected murine cells from death by necroptosis and can protect human cells from necroptosis induced by TNFR activation, when heterologously expressed. We show that the N-terminal 90 residues of the M45 protein, which contain a RIP Homotypic Interaction Motif (RHIM), are sufficient to confer protection against TNFR-induced necroptosis. This N-terminal region of M45 drives rapid self-assembly into homo-oligomeric amyloid fibrils and interacts with the RHIMs of human RIPK1 and RIPK3 kinases to form heteromeric amyloid fibrils in vitro. An intact RHIM core tetrad is required for the inhibition of cell death by M45 and we show that mutation of those key tetrad residues abolishes homo- and hetero-amyloid assembly by M45 in vitro, suggesting that the amyloidogenic nature of the M45 RHIM underlies its biological activity. Our results indicate that M45 mimics the interactions made by RIPK1 with RIPK3 in forming heteromeric amyloid structures.

biophysics↗