bims-proarb Biomed News
on Proteostasis in aging and regenerative biology
Issue of 2022‒07‒31
fourteen papers selected by
Rich Giadone
Harvard University


  1. Front Aging. 2022 ;3 861686
      Discoveries made in the nematode Caenorhabditis elegans revealed that aging is under genetic control. Since these transformative initial studies, C. elegans has become a premier model system for aging research. Critically, the genes, pathways, and processes that have fundamental roles in organismal aging are deeply conserved throughout evolution. This conservation has led to a wealth of knowledge regarding both the processes that influence aging and the identification of molecular and cellular hallmarks that play a causative role in the physiological decline of organisms. One key feature of age-associated decline is the failure of mechanisms that maintain proper function of the proteome (proteostasis). Here we highlight components of the proteostatic network that act to maintain the proteome and how this network integrates into major longevity signaling pathways. We focus in depth on the heat shock transcription factor 1 (HSF1), the central regulator of gene expression for proteins that maintain the cytosolic and nuclear proteomes, and a key effector of longevity signals.
    Keywords:  Caenorhabditis elegans (C. elegans); HSF-1 = heat-shock factor-1; aging; cell stress and aging; genetics; longevity; proteostasis
    DOI:  https://doi.org/10.3389/fragi.2022.861686
  2. Front Mol Biosci. 2022 ;9 915307
      Protein aggregation, or the uncontrolled self-assembly of partially folded proteins, is an ever-present danger for living organisms. Unimpeded, protein aggregation can result in severe cellular dysfunction and disease. A group of proteins known as molecular chaperones is responsible for dismantling protein aggregates. However, how protein aggregates are recognized and disassembled remains poorly understood. Here we employ a single particle fluorescence technique known as Burst Analysis Spectroscopy (BAS), in combination with two structurally distinct aggregate types grown from the same starting protein, to examine the mechanism of chaperone-mediated protein disaggregation. Using the core bi-chaperone disaggregase system from Escherichia coli as a model, we demonstrate that, in contrast to prevailing models, the overall size of an aggregate particle has, at most, a minor influence on the progression of aggregate disassembly. Rather, we show that changes in internal structure, which have no observable impact on aggregate particle size or molecular chaperone binding, can dramatically limit the ability of the bi-chaperone system to take aggregates apart. In addition, these structural alterations progress with surprising speed, rendering aggregates resistant to disassembly within minutes. Thus, while protein aggregate structure is generally poorly defined and is often obscured by heterogeneous and complex particle distributions, it can have a determinative impact on the ability of cellular quality control systems to process protein aggregates.
    Keywords:  molecular chaperone; protein aggregate detection; protein aggregation; protein disaggregase; single particle fluorescence
    DOI:  https://doi.org/10.3389/fmolb.2022.915307
  3. J Mol Biol. 2022 Jul 26. pii: S0022-2836(22)00364-3. [Epub ahead of print] 167762
      Hsp90 and Hsp70 are highly conserved molecular chaperones that promote the proper folding and activation of substrate proteins that are often referred to as clients. The two chaperones functionally collaborate to fold specific clients in an ATP-dependent manner. In eukaryotic cytosol, initial client folding is done by Hsp70 and its co-chaperones, followed by a direct transfer of client refolding intermediates to Hsp90 for final client processing. However, the mechanistic details of collaboration of organelle specific Hsp70 and Hsp90 are lacking. This work investigates the collaboration of the endoplasmic reticulum (ER) Hsp70 and Hsp90, BiP and Grp94 respectively, in protein remodeling using in vitro refolding assays. We show that under milder denaturation conditions, BiP collaborates with its co-chaperones to refold misfolded proteins in an ATP-dependent manner. Grp94 does not play a major role in this refolding reaction. However, under stronger denaturation conditions that favor aggregation, Grp94 works in an ATP-independent manner to bind and hold misfolded clients in a folding competent state for subsequent remodeling by the BiP system. We also show that the collaboration of Grp94 and BiP is not simply a reversal of the eukaryotic refolding mechanism since a direct interaction of Grp94 and BiP is not required for client transfer. Instead, ATP binding but not hydrolysis by Grp94 facilitates the release of the bound client, which is then picked up by the BiP system for subsequent refolding in a Grp94-independent manner.
    Keywords:  DnaJB11; Grp170; Hsp70; Hsp90; molecular chaperones
    DOI:  https://doi.org/10.1016/j.jmb.2022.167762
  4. Ann Neurosci. 2022 Jan;29(1): 71-82
      Background: Human neurodegenerative diseases occur as a result of various factors. Regardless of the variety in the etiology of development, many of these diseases are characterized by the accumulation of pathological, misfolded proteins; hence, such diseases are considered as proteinopathies. While plenty of research study has been conducted in order to identify the pathophysiology of these proteinopathies, there is still a lack of understanding in terms of potential therapeutic targets.Summary: Molecular chaperones present the main workforce for cellular protection and stress response. Therefore, considering these functions, molecular chaperones present a promising target for research within the field of conformational diseases that arise from proteinopathies. Since the association between neurodegenerative disorders and their long-term consequences is well documented, the need for the development of new therapeutic strategies becomes even more critical.
    Key message: In this review, we summarized the molecular function of heat shock proteins and recent progress on their role, involvement, and other mechanisms related to neurodegeneration caused by different etiological factors. Based on the relevant scientific data, we will highlight the functional classification of heat shock proteins, regulation, and their therapeutic potential for neurodegenerative disorders.
    Keywords:  Alzheimer disease; Guillain–Barré syndrome; HSP27; HSP70; HSP90; Heat shock protein; Neurodegeneration; Parkinson disease
    DOI:  https://doi.org/10.1177/09727531211070528
  5. STAR Protoc. 2022 Sep 16. 3(3): 101571
      The loss of protein homeostasis results in cytotoxic protein aggregates, a common hallmark of aging and neurological diseases. Here, we present an adjusted filter-trapping assay protocol to detect global aggregated proteins in human cell lines, via a high-sensitive protein staining method. This protocol also details an alternative approach to monitor specific protein aggregates trapped in the filter membrane, by subsequent immunoblotting of ectopically expressed and endogenous proteins. For complete details on the use and execution of this protocol, please refer to Chhipi-Shrestha et al. (2022).
    Keywords:  Molecular Biology; Protein Biochemistry; Protein expression and purification
    DOI:  https://doi.org/10.1016/j.xpro.2022.101571
  6. Int J Mol Sci. 2022 Jul 14. pii: 7760. [Epub ahead of print]23(14):
      As the organelle of photosynthesis and other important metabolic pathways, chloroplasts contain up to 70% of leaf proteins with uniquely complex processes in synthesis, import, assembly, and turnover. Maintaining functional protein homeostasis in chloroplasts is vitally important for the fitness and survival of plants. Research over the past several decades has revealed a multitude of mechanisms that play important roles in chloroplast protein quality control and turnover under normal and stress conditions. These mechanisms include: (i) endosymbiotically-derived proteases and associated proteins that play a vital role in maintaining protein homeostasis inside the chloroplasts, (ii) the ubiquitin-dependent turnover of unimported chloroplast precursor proteins to prevent their accumulation in the cytosol, (iii) chloroplast-associated degradation of the chloroplast outer-membrane translocon proteins for the regulation of chloroplast protein import, (iv) chloroplast unfolded protein response triggered by accumulated unfolded and misfolded proteins inside the chloroplasts, and (v) vesicle-mediated degradation of chloroplast components in the vacuole. Here, we provide a comprehensive review of these diverse mechanisms of chloroplast protein quality control and turnover and discuss important questions that remain to be addressed in order to better understand and improve important chloroplast functions.
    Keywords:  autophagy; chloroplast associated protein degradation; chloroplast proteases; chloroplast protein quality control; chloroplast unfolded protein responses; ubiquitin proteasome system; vesicle-mediated protein degradation
    DOI:  https://doi.org/10.3390/ijms23147760
  7. Biomedicines. 2022 Jul 06. pii: 1611. [Epub ahead of print]10(7):
      Mitochondrial dysfunction is a key hub that is common to many diseases. Mitochondria's role in energy production, calcium homeostasis, and ROS balance makes them essential for cell survival and fitness. However, there are no effective treatments for most mitochondrial and related diseases to this day. Therefore, new therapeutic approaches, such as activation of the mitochondrial unfolded protein response (UPRmt), are being examined. UPRmt englobes several compensation processes related to proteostasis and antioxidant mechanisms. UPRmt activation, through an hormetic response, promotes cell homeostasis and improves lifespan and disease conditions in biological models of neurodegenerative diseases, cardiopathies, and mitochondrial diseases. Although UPRmt activation is a promising therapeutic option for many conditions, its overactivation could lead to non-desired side effects, such as increased heteroplasmy of mitochondrial DNA mutations or cancer progression in oncologic patients. In this review, we present the most recent UPRmt activation therapeutic strategies, UPRmt's role in diseases, and its possible negative consequences in particular pathological conditions.
    Keywords:  aging; heart diseases; homeostasis; lifespan; mitochondria; mitochondrial diseases; neurodegeneration; proteostasis; therapeutic target; unfolded protein response
    DOI:  https://doi.org/10.3390/biomedicines10071611
  8. Exp Gerontol. 2022 Jul 20. pii: S0531-5565(22)00204-2. [Epub ahead of print]167 111896
      BACKGROUND AND AIMS: Ageing is a multifactorial degenerative process which causes a decrease in the cellular capacity for repair and adaptation to external stressors. In this way, it is important to maintain the proper balance of the proteome. Heat shock proteins (HSP) will intervene in this balance, which are responsible for the correct assembly, folding and translocation of other proteins when cells are subjected to stressors. This type of protein is overexpressed in human tumor cells, while its deficit, both in function and quantity, contributes to ageing processes. The present work aims to analyze the response of cells from studies carried out in normal and tumor cells that are subjected to stressors.METHODS AND RESULTS: A PubMed search was performed using the keywords "cell ageing, cell longevity, resistance, HSP, heat shock proteins, thermal shock proteins". This search generated 212 articles. Subsequently, a series of inclusion and exclusion criteria were applied to select the articles of interest to be evaluated. Normal cells subjected to external stressors at low doses increase the number of HSP, causing them to become more resistant. In addition, tumor cells expressing high levels of HSP show greater resistance to treatment and increased cell replication. HSP intervene in the cellular resistance of both normal and tumor cells.
    CONCLUSIONS: In the case of normal cells, the increase in HSP levels makes them respond effectively to an external stressor, increasing their resistance and not causing cell death. In the case of tumor cells, there is an increase in resistance to treatment.
    Keywords:  Ageing; Cancer; Drug resistance; HSP; Heat shock proteins; Longevity; Ubiquitin-proteasome system (UPS)
    DOI:  https://doi.org/10.1016/j.exger.2022.111896
  9. Front Mol Neurosci. 2022 ;15 921908
      Mitochondria provide neurons not only energy as ATP to keep them growing, proliferating and developing, but they also control apoptosis. Due to their high bioenergetic demand, neurons which are highly specific terminally differentiated cells, essentially depend on mitochondria. Defective mitochondrial function is thus related to numerous age-linked neurodegenerative ailments like Alzheimer's disease (AD), in which the build-up of impaired and malfunctioning mitochondria has been identified as a primary sign, paying to disease development. Mitophagy, selective autophagy, is a key mitochondrial quality control system that helps neurons to stay healthy and functional by removing undesired and damaged mitochondria. Dysfunctional mitochondria and dysregulated mitophagy have been closely associated with the onset of ADs. Various proteins associated with mitophagy were found to be altered in AD. Therapeutic strategies focusing on the restoration of mitophagy capabilities could be utilized to strike the development of AD pathogenesis. We summarize the mechanism and role of mitophagy in the onset and advancement of AD, in the quality control mechanism of mitochondria, the consequences of dysfunctional mitophagy in AD, and potential therapeutic approaches involving mitophagy modulation in AD. To develop new therapeutic methods, a better knowledge of the function of mitophagy in the pathophysiology of AD is required.
    Keywords:  Alzheimer’s disease; mitochondrial dynamics; mitochondrial dysfunction; mitochondrial quality control; mitophagy; targeting mitophagy
    DOI:  https://doi.org/10.3389/fnmol.2022.921908
  10. Plant Direct. 2022 Jul;6(7): e431
      The endoplasmic reticulum (ER) houses sensors that respond to environmental stress and underly plants' adaptative responses. These sensors transduce signals that lead to changes in nuclear gene expression. The ER to nuclear signaling pathways are primarily attributed to the unfolded protein response (UPR) and are also integrated with a wide range of development, hormone, immune, and stress signaling pathways. Understanding the role of the UPR in signaling network mechanisms that associate with particular phenotypes is crucially important. While UPR-associated genes are the subject of ongoing investigations in a few model plant systems, most remain poorly annotated, hindering the identification of candidates across plant species. This open-source curated database provides a centralized resource of peer reviewed knowledge of ER to nuclear signaling pathways for the plant community. We provide a UPRome interactive viewer for users to navigate through the pathways and to access annotated information. The plant ER UPRome website is located at http://uprome.tamu.edu. We welcome contributions from the researchers studying the ER UPR to incorporate additional genes into the database through the "contact us" page.
    Keywords:  curated database; plant protein interaction maps; plant signal transduction; unfolded protein response
    DOI:  https://doi.org/10.1002/pld3.431
  11. Mol Neurobiol. 2022 Jul 29.
      Alzheimer's disease (AD) is the most common neurodegenerative disorder characterized by the accumulation of amyloid-β (Aβ) aggregates in the brain. Clusterin (CLU), also known as apolipoprotein J, is a potent risk factor associated with AD pathogenesis, in which Aβ aggregation is essentially involved. We observed close colocalization of CLU and Aβ(1-42) (Aβ42) in parenchymal amyloid plaques or vascular amyloid deposits in the brains of human amyloid precursor protein (hAPP)-transgenic Tg2576 mice. Therefore, to elucidate the binding interaction between CLU and Aβ42 and its impact on amyloid aggregation and toxicity, the two synthetic proteins were incubated together under physiological conditions, and their structural and morphological variations were investigated using biochemical, biophysical, and microscopic analyses. Synthetic CLU spontaneously bound to different possible variants of Aβ42 aggregates with very high affinity (Kd = 2.647 nM) in vitro to form solid CLU-Aβ42 complexes. This CLU binding prevented further aggregation of Aβ42 into larger oligomers or fibrils, enriching the population of smaller Aβ42 oligomers and protofibrils and monomers. CLU either alleviated or augmented Aβ42-induced cytotoxicity and apoptosis in the neuroblastoma-derived SH-SY5Y and N2a cells, depending on the incubation period and the molar ratio of CLU:Aβ42 involved in the reaction before addition to the cells. Thus, the effects of CLU on Aβ42-induced cytotoxicity were likely determined by the extent to which it bound and sequestered toxic Aβ42 oligomers or protofibrils. These findings suggest that CLU could influence amyloid neurotoxicity and pathogenesis by modulating Aβ aggregation.
    Keywords:  Alzheimer’s disease; Amyloid pathogenesis; Apolipoprotein J; Aβ oligomers; Chaperone protein; Cytotoxicity; Protein–protein interaction
    DOI:  https://doi.org/10.1007/s12035-022-02973-6
  12. Nat Metab. 2022 Jul 28.
      ABSTACT: Ageing is the largest risk factor for many chronic diseases. Studies of heterochronic parabiosis, substantiated by blood exchange and old plasma dilution, show that old-age-related factors are systemically propagated and have pro-geronic effects in young mice. However, the underlying mechanisms how bloodborne factors promote ageing remain largely unknown. Here, using heterochronic blood exchange in male mice, we show that aged mouse blood induces cell and tissue senescence in young animals after one single exchange. This induction of senescence is abrogated if old animals are treated with senolytic drugs before blood exchange, therefore attenuating the pro-geronic influence of old blood on young mice. Hence, cellular senescence is neither simply a response to stress and damage that increases with age, nor a chronological cell-intrinsic phenomenon. Instead, senescence quickly and robustly spreads to young mice from old blood. Clearing senescence cells that accumulate with age rejuvenates old circulating blood and improves the health of multiple tissues.
    DOI:  https://doi.org/10.1038/s42255-022-00609-6
  13. Cells. 2022 Jul 20. pii: 2250. [Epub ahead of print]11(14):
      Chaperone-mediated autophagy (CMA) is a protein degradation mechanism through lysosomes. By targeting the KFERQ motif of the substrate, CMA is responsible for the degradation of about 30% of cytosolic proteins, including a series of proteins associated with neurodegenerative diseases (NDs). The fact that decreased activity of CMA is observed in NDs, and ND-associated mutant proteins, including alpha-synuclein and Tau, directly impair CMA activity reveals a possible vicious cycle of CMA impairment and pathogenic protein accumulation in ND development. Given the intrinsic connection between CMA dysfunction and ND, enhancement of CMA has been regarded as a strategy to counteract ND. Indeed, genetic and pharmacological approaches to modulate CMA have been shown to promote the degradation of ND-associated proteins and alleviate ND phenotypes in multiple ND models. This review summarizes the current knowledge on the mechanism of CMA with a focus on its relationship with NDs and discusses the therapeutic potential of CMA modulation for ND.
    Keywords:  Alzheimer’s disease; HSC70; Huntington’s disease; LAMP2A; Parkinson’s disease; autophagy; chaperone-mediated autophagy; neurodegenerative disease; small molecule; α-synuclein
    DOI:  https://doi.org/10.3390/cells11142250
  14. Neuron. 2022 Jul 21. pii: S0896-6273(22)00600-6. [Epub ahead of print]
      Tau aggregation in neurofibrillary tangles (NFTs) is closely associated with neurodegeneration and cognitive decline in Alzheimer's disease (AD). However, the molecular signatures that distinguish between aggregation-prone and aggregation-resistant cell states are unknown. We developed methods for the high-throughput isolation and transcriptome profiling of single somas with NFTs from the human AD brain, quantified the susceptibility of 20 neocortical subtypes for NFT formation and death, and identified both shared and cell-type-specific signatures. NFT-bearing neurons shared a marked upregulation of synaptic transmission-related genes, including a core set of 63 genes enriched for synaptic vesicle cycling. Oxidative phosphorylation and mitochondrial dysfunction were highly cell-type dependent. Apoptosis was only modestly enriched, and the susceptibilities of NFT-bearing and NFT-free neurons for death were highly similar. Our analysis suggests that NFTs represent cell-type-specific responses to stress and synaptic dysfunction. We provide a resource for biomarker discovery and the investigation of tau-dependent and tau-independent mechanisms of neurodegeneration.
    Keywords:  amyloid; biomarkers; dementia; neurodegeneration; neuropathology; selective vulnerability; single-cell RNA-seq; single-nucleus RNA-seq; tauopathies; transcriptomics
    DOI:  https://doi.org/10.1016/j.neuron.2022.06.021