bims-proarb Biomed News
on Proteostasis in aging and regenerative biology
Issue of 2022–07–17
twelve papers selected by
Rich Giadone, Harvard University



  1. Front Aging. 2022 ;3 854157
      Protein homeostasis (proteostasis) is maintained by a tightly regulated and interconnected network of biological pathways, preventing the accumulation and aggregation of damaged or misfolded proteins. Thus, the proteostasis network is essential to ensure organism longevity and health, while proteostasis failure contributes to the development of aging and age-related diseases that involve protein aggregation. The model organism Caenorhabditis elegans has proved invaluable for the study of proteostasis in the context of aging, longevity and disease, with a number of pivotal discoveries attributable to the use of this organism. In this review, we discuss prominent findings from C. elegans across the many key aspects of the proteostasis network, within the context of aging and disease. These studies collectively highlight numerous promising therapeutic targets, which may 1 day facilitate the development of interventions to delay aging and prevent age-associated diseases.
    Keywords:  C. elegans; autophagy; chaperones; protein aggragation; protein translation; proteostasis; stress responses; ubiquitin-proteasome system
    DOI:  https://doi.org/10.3389/fragi.2022.854157
  2. Front Aging. 2022 ;3 853588
      Temperature is an important environmental condition that determines the physiology and behavior of all organisms. Animals use different response strategies to adapt and survive fluctuations in ambient temperature. The hermaphrodite Caenorhabditis elegans has a well-studied neuronal network consisting of 302 neurons. The bilateral AFD neurons are the primary thermosensory neurons in the nematode. In addition to regulating thermosensitivity, AFD neurons also coordinate cellular stress responses through systemic mechanisms involving neuroendocrine signaling. Recent studies have examined the effects of temperature on altering various signaling pathways through specific gene expression programs that promote stress resistance and longevity. These studies challenge the proposed theories of temperature-dependent regulation of aging as a passive thermodynamic process. Instead, they provide evidence that aging is a well-defined genetic program. Loss of protein homeostasis (proteostasis) is one of the key hallmarks of aging. Indeed, proteostasis pathways, such as the heat shock response and aggregation of metastable proteins, are also controlled by thermosensory neurons in C. elegans. Prolonged heat stress is thought to play a critical role in the development of neurodegenerative protein misfolding diseases in humans. This review presents the latest evidence on how temperature coordinates proteostasis and aging. It also discusses how studies of poikilothermic organisms can be applied to vertebrates and provides new therapeutic strategies for human disease.
    Keywords:  AFD neuron; Caenorhabditis elegans; cell non-autonomous signaling; longevity; protein aggregation; proteostasis; temperature; thermosensation
    DOI:  https://doi.org/10.3389/fragi.2022.853588
  3. Front Aging. 2021 ;2 790702
      Aging is a physiological process defined by decreased cellular and tissue functions. Reduced capacity of protein degradation is one of the important hallmarks of aging that may lead to misfolded protein accumulation and progressive loss of function in organ systems. Recognition of unfolded/misfolded protein aggregates via endoplasmic reticulum (ER) stress sensors activates an adaptive mechanism, the unfolded protein response (UPR). The initial step of UPR is defined by chaperone enhancement, ribosomal translation suppression, and misfolded protein degradation, while prolonged ER stress triggers apoptosis. MicroRNAs (miRNAs) are non-coding RNAs affecting various signaling pathways through degradation or translational inhibition of targeted mRNAs. Therefore, UPR and miRNA impairment in aging and age-related diseases is implicated in various studies. This review will highlight the recent insights in ER stress-miRNAs alterations during aging and age-related diseases, including metabolic, cardiovascular, and neurodegenerative diseases and several cancers.
    Keywords:  aging; cancer; cardiovascular diseases; endoplasmic reticulum stress; metabolic disorders; microRNA; neurodegenerative diseases
    DOI:  https://doi.org/10.3389/fragi.2021.790702
  4. Neuronal Signal. 2022 Jun;6(2): NS20210063
      Synapses maintain their molecular composition, plasticity and function through the concerted action of protein synthesis and removal. The complex and polarized neuronal architecture poses specific challenges to the logistics of protein and organelle turnover since protein synthesis and degradation mainly happen in the cell soma. In addition, post-mitotic neurons accumulate damage over a lifetime, challenging neuronal degradative pathways and making them particularly susceptible to the effects of aging. This review will summarize the current knowledge on neuronal protein turnover mechanisms with a particular focus on the presynapse, including the proteasome, autophagy and the endolysosomal route and their roles in regulating presynaptic proteostasis and function. In addition, the author will discuss how physiological brain aging, which entails a progressive decline in cognitive functions, affects synapses and the degradative machinery.
    Keywords:  aging; autophagy; endolysosome; presynapse; proteostasis; ubiquitin proteasome system
    DOI:  https://doi.org/10.1042/NS20210063
  5. Front Aging. 2022 ;3 860404
      Organisms are constantly exposed to stress both from the external environment and internally within the cell. To maintain cellular homeostasis under different environmental and physiological conditions, cell have adapted various stress response signaling pathways, such as the heat shock response (HSR), unfolded protein responses of the mitochondria (UPRMT), and the unfolded protein response of the endoplasmic reticulum (UPRER). As cells grow older, all cellular stress responses have been shown to deteriorate, which is a major cause for the physiological consequences of aging and the development of numerous age-associated diseases. In contrast, elevated stress responses are often associated with lifespan extension and amelioration of degenerative diseases in different model organisms, including C. elegans. Activating cellular stress response pathways could be considered as an effective intervention to alleviate the burden of aging by restoring function of essential damage-clearing machinery, including the ubiquitin-proteosome system, chaperones, and autophagy. Here, we provide an overview of newly emerging concepts of these stress response pathways in healthy aging and longevity with a focus on the model organism, C. elegans.
    Keywords:  C. elegans; aging; endoplasmic reticulum; heat-shock; mitochondria; stress
    DOI:  https://doi.org/10.3389/fragi.2022.860404
  6. Methods Mol Biol. 2022 ;2473 349-366
      Protein misfolding poses a significant threat to the fitness of eukaryotic cells, particularly for neurons facing environmental stress. To effectively triage and remove defective and unwanted proteins, cells have evolved diverse protein quality control (PQC) mechanisms relying on proteasome- and endolysosome-mediated degradation systems. Defects in PQC functions are linked to various human diseases including many aging-associated neurodegenerative diseases. Misfolding-associated protein secretion (MAPS) is a recently reported PQC mechanism that eliminates misfolded cytosolic proteins by an unconventional secretory pathway using an endo-vesiclular network. This process implicates DNAJC5, a chaperone that escorts misfolded cargos to intracellular vesicles to facilitate their secretion. Cargos of DNAJC5 include Parkinson's and Alzheimer's disease-associated proteins known to undergo cell-to-cell transmission during disease progression. Thus, elucidating how these proteins are secreted may reveal novel therapeutic targets for these diseases. Here we describe a collection of methods used to detect either the basal or induced secretion of misfolded proteins from cell lines and cultured primary neurons.
    Keywords:  Alzheimer’s disease; DNAJC5/CLN4/CSPα; Misfolding-associated protein secretion (MAPS); Parkinson’s disease; Primary murine hippocampal neurons; Protein quality control (PQC); Tau; Unconventional protein secretion (UPS); α-Synuclein; β-Galactosidase/LacZ assay
    DOI:  https://doi.org/10.1007/978-1-0716-2209-4_22
  7. Front Cell Dev Biol. 2022 ;10 912470
      What lies at the basis of the mechanisms that regulate the maintenance and self-renewal of pluripotent stem cells is still an open question. The control of stemness derives from a fine regulation between transcriptional and metabolic factors. In the last years, an emerging topic has concerned the involvement of Chaperone-Mediated Autophagy (CMA) as a key mechanism in stem cell pluripotency control acting as a bridge between epigenetic, transcriptional and differentiation regulation. This review aims to clarify this new and not yet well-explored horizon discussing the recent studies regarding the CMA impact on embryonic, mesenchymal, and haematopoietic stem cells. The review will discuss how CMA influences embryonic stem cell activity promoting self-renewal or differentiation, its involvement in maintaining haematopoietic stem cell function by increasing their functionality during the normal ageing process and its effects on mesenchymal stem cells, in which modulation of CMA regulates immunosuppressive and differentiation properties. Finally, the importance of these new discoveries and their relevance for regenerative medicine applications, from transplantation to cell rejuvenation, will be addressed.
    Keywords:  Chaperone-Mediated Autophagy (CMA); adult stem cells; aging; embryonic stem cells; haematopoietic stem cells; mesenchymal stromal cells (MSC); pluripotent stem cell; rejuvenation
    DOI:  https://doi.org/10.3389/fcell.2022.912470
  8. J Cachexia Sarcopenia Muscle. 2022 Jul 12.
       BACKGROUND: Cell assays are important for investigating the mechanisms of ageing, including losses in protein homeostasis and 'proteostasis collapse'. We used novel isotopic labelling and proteomic methods to investigate protein turnover in replicatively aged (>140 population doublings) murine C2C12 myoblasts that exhibit impaired differentiation and serve as a model for age-related declines in muscle homeostasis.
    METHODS: The Absolute Dynamic Profiling Technique for Proteomics (Proteo-ADPT) was used to investigate proteostasis in young (passage 6-10) and replicatively aged (passage 48-50) C2C12 myoblast cultures supplemented with deuterium oxide (D2 O) during early (0-24 h) or late (72-96 h) periods of differentiation. Peptide mass spectrometry was used to quantify the absolute rates of abundance change, synthesis and degradation of individual proteins.
    RESULTS: Young cells exhibited a consistent ~25% rise in protein accretion over the 96-h experimental period. In aged cells, protein accretion increased by 32% (P < 0.05) during early differentiation, but then fell back to baseline levels by 96-h. Proteo-ADPT encompassed 116 proteins and 74 proteins exhibited significantly (P < 0.05, FDR < 5% interaction between age × differentiation stage) different changes in abundance between young and aged cells at early and later periods of differentiation, including proteins associated with translation, glycolysis, cell-cell adhesion, ribosomal biogenesis, and the regulation of cell shape. During early differentiation, heat shock and ribosomal protein abundances increased in aged cells due to suppressed degradation rather than heightened synthesis. For instance, HS90A increased at a rate of 10.62 ± 1.60 ng/well/h in aged which was significantly greater than the rate of accretion (1.86 ± 0.49 ng/well/h) in young cells. HS90A synthesis was similar in young (21.23 ± 3.40 ng/well/h) and aged (23.69 ± 1.13 ng/well/h), but HS90A degradation was significantly (P = 0.05) greater in young (19.37 ± 2.93 ng/well/h) versus aged (13.06 ± 0.76 ng/well/h) cells. During later differentiation the HS90A degradation (8.94 ± 0.38 ng/well/h) and synthesis (7.89 ± 1.28 ng/well/h) declined and were significantly less than the positive net balance between synthesis and degradation (synthesis = 28.14 ± 3.70 ng/well/h vs. degradation = 21.49 ± 3.13 ng/well/h) in young cells.
    CONCLUSIONS: Our results suggest a loss of proteome quality as a precursor to the lack of fusion of aged myoblasts. The quality of key chaperone proteins, including HS90A, HS90B and HSP7C was reduced in aged cells and may account for the disruption to cell signalling required for the later stages of differentiation and fusion.
    Keywords:  Ageing; Deuterium oxide; Heavy water; Muscle regeneration; Myoblast differentiation; Protein degradation; Protein synthesis; Proteomics; Proteostasis
    DOI:  https://doi.org/10.1002/jcsm.13034
  9. Front Aging. 2022 ;3 897741
      In multicellular organisms such as Caenorhabditis elegans, cellular stress stimuli and responses are communicated between tissues to promote organismal health- and lifespan. The nervous system is the predominant regulator of cell nonautonomous proteostasis that orchestrates systemic stress responses to integrate both internal and external stimuli. This review highlights the role of the intestine in mediating cell nonautonomous stress responses and explores recent findings that suggest a central role for the intestine to regulate organismal proteostasis. As a tissue that receives and further transduces signals from the nervous system in response to dietary restriction, heat- and oxidative stress, and hypoxia, we explore evidence suggesting the intestine is a key regulatory organ itself. From the perspective of naturally occurring stressors such as dietary restriction and pathogen infection we highlight how the intestine can function as a key regulator of organismal proteostasis by integrating insulin/IGF-like signaling, miRNA-, neuropeptide- and metabolic signaling to alter distal tissue functions in promoting survival, health- and lifespan.
    Keywords:  C. elegans; cell-nonautonomous; intercellular signaling; intestine; neurons; organismal aging; proteostasis; stress
    DOI:  https://doi.org/10.3389/fragi.2022.897741
  10. Biochim Biophys Acta Mol Basis Dis. 2022 Jul 12. pii: S0925-4439(22)00156-9. [Epub ahead of print] 166485
      Amyloid oligomers and fibrils are protein aggregates that cause an onset and progression of many neurodegenerative diseases, diabetes type 2 and systemic amyloidosis. Although a growing body of evidence shows that oligomers and fibrils trigger mitochondrial dysfunction simultaneously enhancing production of reactive oxygen species, exact mechanisms by which these protein aggregates exert their toxicities remain unclear. In this study, we used advanced microscopic and spectroscopic methods to examine topography and structure of insulin aggregates grown in the lipid-free environment, as well as in the presence of major classes of phospho- and sphingolipids. We also employed a set of molecular markers to determine the extent to which insulin aggregates induce a damage of cell endoplasmic reticulum (ER), an important cell organelle used for calcium storage, protein synthesis and folding. Our results show that insulin aggregates activate the expression of Activating Transcription Factor 6 (ATF6), a transmembrane protein that is involved in unfolded protein response (UPR) of the stressed ER. At the same time, two other ER transmembrane proteins, Inositol Requiring 1 (IRE1α) and eLF2a, the product of PKR-like ER kinase (PERK), exhibited very low expression levels. Furthermore, amyloid aggregates trigger an expression of the 78-kDa glucose-regulated protein GRP78, which is also involved in the UPR. We also observed UPR-induced expression of a proapoptotic transcription factor CHOP, which, in turn, regulates expression of caspase 3 kinase and BCL2 protein family members, including the ER localized Bax. These findings show that insulin oligomers and fibrils induce UPR-associated ER stress and ultimately fatal changes in cell homeostasis.
    Keywords:  AFM-IR; Amyloids; Endoplasmic reticulum; Lipids; Unfolded protein response
    DOI:  https://doi.org/10.1016/j.bbadis.2022.166485
  11. Life Sci Alliance. 2022 Nov;pii: e202201531. [Epub ahead of print]5(11):
      Mitochondria-ER contact sites (MERCs) orchestrate many important cellular functions including regulating mitochondrial quality control through mitophagy and mediating mitochondrial calcium uptake. Here, we identify and functionally characterize the Drosophila ortholog of the recently identified mammalian MERC protein, Pdzd8. We find that reducing pdzd8-mediated MERCs in neurons slows age-associated decline in locomotor activity and increases lifespan in Drosophila. The protective effects of pdzd8 knockdown in neurons correlate with an increase in mitophagy, suggesting that increased mitochondrial turnover may support healthy aging of neurons. In contrast, increasing MERCs by expressing a constitutive, synthetic ER-mitochondria tether disrupts mitochondrial transport and synapse formation, accelerates age-related decline in locomotion, and reduces lifespan. Although depletion of pdzd8 prolongs the survival of flies fed with mitochondrial toxins, it is also sufficient to rescue locomotor defects of a fly model of Alzheimer's disease expressing Amyloid β42 (Aβ42). Together, our results provide the first in vivo evidence that MERCs mediated by the tethering protein pdzd8 play a critical role in the regulation of mitochondrial quality control and neuronal homeostasis.
    DOI:  https://doi.org/10.26508/lsa.202201531