bims-mikwok Biomed News
on Mitochondrial quality control
Issue of 2023–08–27
eleven papers selected by
Gavin McStay, Liverpool John Moores University



  1. Aging Cell. 2023 Aug 23. e13954
      The metabolic consequences of mitophagy alterations due to age-related stress in healthy aging brains versus neurodegeneration remain unknown. Here, we demonstrate that ceramide synthase 1 (CerS1) is transported to the outer mitochondrial membrane by the p17/PERMIT transporter that recognizes mislocalized mitochondrial ribosomes (mitoribosomes) via 39-FLRN-42 residues, inducing ceramide-mediated mitophagy. P17/PERMIT-CerS1-mediated mitophagy attenuated the argininosuccinate/fumarate/malate axis and induced d-glucose and fructose accumulation in neurons in culture and brain tissues (primarily in the cerebellum) of wild-type mice in vivo. These metabolic changes in response to sodium-selenite were nullified in the cerebellum of CerS1to/to (catalytically inactive for C18-ceramide production CerS1 mutant), PARKIN-/- or p17/PERMIT-/- mice that have dysfunctional mitophagy. Whereas sodium selenite induced mitophagy in the cerebellum and improved motor-neuron deficits in aged wild-type mice, exogenous fumarate or malate prevented mitophagy. Attenuating ceramide-mediated mitophagy enhanced damaged mitochondria accumulation and age-dependent sensorimotor abnormalities in p17/PERMIT-/- mice. Reinstituting mitophagy using a ceramide analog drug with selenium conjugate, LCL768, restored mitophagy and reduced malate/fumarate metabolism, improving sensorimotor deficits in old p17/PERMIT-/- mice. Thus, these data describe the metabolic consequences of alterations to p17/PERMIT/ceramide-mediated mitophagy associated with the loss of mitochondrial quality control in neurons and provide therapeutic options to overcome age-dependent sensorimotor deficits and related disorders like amyotrophic lateral sclerosis (ALS).
    Keywords:  CerS1; Drp1; aging; ceramide; mitochondrial metabolism; mitophagy; neurodegeneration; sensorimotor defects
    DOI:  https://doi.org/10.1111/acel.13954
  2. Biomolecules. 2023 Aug 07. pii: 1225. [Epub ahead of print]13(8):
      Mitochondrial network architecture plays a critical role in cellular physiology. Indeed, alterations in the shape of mitochondria upon exposure to cellular stress can cause the dysfunction of these organelles. In this scenario, mitochondrial dynamics proteins and the phospholipid composition of the mitochondrial membrane are key for fine-tuning the modulation of mitochondrial architecture. In addition, several factors including post-translational modifications such as the phosphorylation, acetylation, SUMOylation, and o-GlcNAcylation of mitochondrial dynamics proteins contribute to shaping the plasticity of this architecture. In this regard, several studies have evidenced that, upon metabolic stress, mitochondrial dynamics proteins are post-translationally modified, leading to the alteration of mitochondrial architecture. Interestingly, several proteins that sustain the mitochondrial lipid composition also modulate mitochondrial morphology and organelle communication. In this context, pharmacological studies have revealed that the modulation of mitochondrial shape and function emerges as a potential therapeutic strategy for metabolic diseases. Here, we review the factors that modulate mitochondrial architecture.
    Keywords:  lipids; membrane contact sites (MCSs); metabolic disease; metabolism; mitochondria; mitochondrial dynamics; pharmacology; post-translational modification; tethers
    DOI:  https://doi.org/10.3390/biom13081225
  3. EMBO J. 2023 Aug 25. e113491
      Nix is a membrane-anchored outer mitochondrial protein that induces mitophagy. While Nix has an LC3-interacting (LIR) motif that binds to ATG8 proteins, it also contains a minimal essential region (MER) that induces mitophagy through an unknown mechanism. We used chemically induced dimerization (CID) to probe the mechanism of Nix-mediated mitophagy and found that both the LIR and MER are required for robust mitophagy. We find that the Nix MER interacts with the autophagy effector WIPI2 and recruits WIPI2 to mitochondria. The Nix LIR motif is also required for robust mitophagy and converts a homogeneous WIPI2 distribution on the surface of the mitochondria into puncta, even in the absence of ATG8s. Together, this work reveals unanticipated mechanisms in Nix-induced mitophagy and the elusive role of the MER, while also describing an interesting example of autophagy induction that acts downstream of the canonical initiation complexes.
    Keywords:  Autophagy; BNIP3; FIP200; LIR; p62
    DOI:  https://doi.org/10.15252/embj.2023113491
  4. Ageing Res Rev. 2023 Aug 23. pii: S1568-1637(23)00197-6. [Epub ahead of print] 102038
      Intercellular signaling and component conduction are essential for multicellular organisms' homeostasis, and mitochondrial transcellular transport is a key example of such cellular component exchange. In physiological situations, mitochondrial transfer is linked with biological development, energy coordination, and clearance of harmful components, remarkably playing important roles in maintaining mitochondrial quality. Mitochondria are engaged in many critical biological activities, like oxidative metabolism and biomolecular synthesis, and are exclusively prone to malfunction in pathological processes. Importantly, severe mitochondrial damage will further amplify the defects in the mitochondrial quality control system, which will mobilize more active mitochondrial transfer, replenish exogenous healthy mitochondria, and remove endogenous damaged mitochondria to facilitate disease outcomes. This review explores intercellular mitochondrial transport in cells, its role in cellular mitochondrial quality control, and the linking mechanisms in cellular crosstalk. We also describe advances in therapeutic strategies for diseases that target mitochondrial transfer.
    Keywords:  cell crosstalk; intercellular mitochondrial transfer; mitochondrial quality control; therapy
    DOI:  https://doi.org/10.1016/j.arr.2023.102038
  5. Front Cell Dev Biol. 2023 ;11 1196466
      Mitochondria play a critical role in energy metabolism and signal transduction, which is tightly regulated by proteins, metabolites, and ion fluxes. Metabolites and ion homeostasis are mainly mediated by channels and transporters present on mitochondrial membranes. Mitochondria comprise two distinct compartments, the outer mitochondrial membrane (OMM) and the inner mitochondrial membrane (IMM), which have differing permeabilities to ions and metabolites. The OMM is semipermeable due to the presence of non-selective molecular pores, while the IMM is highly selective and impermeable due to the presence of specialized channels and transporters which regulate ion and metabolite fluxes. These channels and transporters are modulated by various post-translational modifications (PTMs), including phosphorylation, oxidative modifications, ions, and metabolites binding, glycosylation, acetylation, and others. Additionally, the mitochondrial protein quality control (MPQC) system plays a crucial role in ensuring efficient molecular flux through the mitochondrial membranes by selectively removing mistargeted or defective proteins. Inefficient functioning of the transporters and channels in mitochondria can disrupt cellular homeostasis, leading to the onset of various pathological conditions. In this review, we provide a comprehensive overview of the current understanding of mitochondrial channels and transporters in terms of their functions, PTMs, and quality control mechanisms.
    Keywords:  MCU; MPQC; MPTP; SLCs; VDAC; mitochondrial channels; mitochondrial transporters; posttranslational modifications
    DOI:  https://doi.org/10.3389/fcell.2023.1196466
  6. Life Metab. 2023 Oct;2(5): load027
      The AMP-activated protein kinase (AMPK) is known to maintain the integrity of cellular mitochondrial networks by (i) promoting fission, (ii) inhibiting fusion, (iii) promoting recycling of damaged components via mitophagy, (iv) enhancing lysosomal biogenesis to support mitophagy, and (v) promoting biogenesis of new mitochondrial components. While the AMPK targets underlying the first three of these effects are known, a recent paper suggests that direct phosphorylation of the folliculin-interacting protein 1 (FNIP1) by AMPK may be involved in the remaining two.
    DOI:  https://doi.org/10.1093/lifemeta/load027
  7. Nature. 2023 Aug 23.
      Distinct morphologies of the mitochondrial network support divergent metabolic and regulatory processes that determine cell function and fate1-3. The mechanochemical GTPase optic atrophy 1 (OPA1) influences the architecture of cristae and catalyses the fusion of the mitochondrial inner membrane4,5. Despite its fundamental importance, the molecular mechanisms by which OPA1 modulates mitochondrial morphology are unclear. Here, using a combination of cellular and structural analyses, we illuminate the molecular mechanisms that are key to OPA1-dependent membrane remodelling and fusion. Human OPA1 embeds itself into cardiolipin-containing membranes through a lipid-binding paddle domain. A conserved loop within the paddle domain inserts deeply into the bilayer, further stabilizing the interactions with cardiolipin-enriched membranes. OPA1 dimerization through the paddle domain promotes the helical assembly of a flexible OPA1 lattice on the membrane, which drives mitochondrial fusion in cells. Moreover, the membrane-bending OPA1 oligomer undergoes conformational changes that pull the membrane-inserting loop out of the outer leaflet and contribute to the mechanics of membrane remodelling. Our findings provide a structural framework for understanding how human OPA1 shapes mitochondrial morphology and show us how human disease mutations compromise OPA1 functions.
    DOI:  https://doi.org/10.1038/s41586-023-06441-6
  8. Biomed Rep. 2023 Sep;19(3): 64
      The mitochondrial genome or mitochondrial DNA (mtDNA) is released as a response to cellular stress. In mitochondrial biogenesis, active communication between the mitochondria genome and nucleus is associated with the mtDNA profile that affects the mitochondrial quality. The present review aimed to assess the molecular mechanism and potential roles of mitochondria in neuro-aging, including the importance of evaluating the health status of mtDNA via mitochondrial dynamics. The normal condition of mitochondria, defined as mitochondrial dynamics, includes persistent changes in morphology due to fission and fusion events and autophagy-mitophagy in the mitochondrial quality control process. The calculated copy number of mtDNA in the mitochondria genome represents cellular health, which can be affected by a long-term imbalance between the production and accumulation of reactive oxygen species in the neuroendocrine system, which leads to an abnormal function of mitochondria and mtDNA damage. Mitochondria health is a new approach to discovering a potential indicator for the health status of the nervous system and several types of neurodegenerative disorders. Mitochondrial dynamics is a key contributor to predicting neuro-aging development, which affects the self-renewal and differentiation of neurons in cell metabolism. Neuro-aging is associated with uncontrolled mitochondrial dynamics, which generates age-associated diseases via various mechanisms and signaling routes that lead to the mtDNA damage that has been associated with neurodegeneration. Future studies on the strategic positioning of mtDNA health profile are needed to detect early neurodegenerative disorders.
    Keywords:  cellular health; mitochondrial DNA; mitochondrial dynamics; neuro-aging
    DOI:  https://doi.org/10.3892/br.2023.1646
  9. Curr Med Chem. 2023 Aug 22.
      Mitochondria are the energy factories of cells, and their functions are closely related to cell homeostasis. The mitochondrial unfolded protein response (mtUPR) is a newly discovered mechanism for regulating mitochondrial homeostasis. When unfolded/misfolded proteins accumulate in mitochondria, the mitochondria release signals that regulate the transcription of certain proteins in the nucleus, thereby inducing the correct folding or degradation of proteins in mitochondria. Many studies have also shown that an abnormality of mtUPR is closely related to the occurrence and development of diseases. Here, we summarized the pathways regulating mtUPR signaling and reviewed the research progress on mtUPR in diseases. Finally, we summarized the currently identified agonists and inhibitors of the mtUPR and discussed the potential of the mtUPR as a therapeutic target for diseases.
    Keywords:  ATFS-1; aging; kidney diseases; mitochondria; mtUPR
    DOI:  https://doi.org/10.2174/0929867331666230822095924
  10. Biomolecules. 2023 Jul 31. pii: 1198. [Epub ahead of print]13(8):
      Mitochondria are often referred to as the "powerhouse" of the cell. However, this organelle has many more functions than simply satisfying the cells' metabolic needs. Mitochondria are involved in calcium homeostasis and lipid metabolism, and they also regulate apoptotic processes. Many of these functions require contact with the ER, which is mediated by several tether proteins located on the respective organellar surfaces, enabling the formation of mitochondria-ER contact sites (MERCS). Upon damage, mitochondria produce reactive oxygen species (ROS) that can harm the surrounding cell. To circumvent toxicity and to maintain a functional pool of healthy organelles, damaged and excess mitochondria can be targeted for degradation via mitophagy, a form of selective autophagy. Defects in mitochondria-ER tethers and the accumulation of damaged mitochondria are found in several neurodegenerative diseases, including Parkinson's disease and amyotrophic lateral sclerosis, which argues that the interplay between the two organelles is vital for neuronal health. This review provides an overview of the different mechanisms of mitochondrial quality control that are implicated with the different mitochondria-ER tether proteins, and also provides a novel perspective on how MERCS are involved in mediating mitophagy upon mitochondrial damage.
    Keywords:  mitochondria; mitophagy; organellar contact sites
    DOI:  https://doi.org/10.3390/biom13081198
  11. Eur J Med Chem. 2023 Aug 18. pii: S0223-5234(23)00695-5. [Epub ahead of print]260 115728
      The mitochondria have been identified as key targets in nonalcoholic fatty liver disease (NAFLD), one of the most prevalent chronic liver damage diseases globally. Meanwhile, the biological information analysis in this study revealed that SIRT1, PPARG, PPARA, and PPARGC1A (mitochondrial biogenesis-related proteins) were NAFLD therapeutic targets. Therefore, the design and synthesis of targeted drugs that promote mitochondrial biogenesis and improve mitochondrial function are particularly important for NAFLD treatment. Recently, we introduced butyls, hydroxyls, and halogens to benzophenone and synthesized a series of NAFLD-related 4-butylpolyhydroxybenzophenone compounds, aiming at investigating the hepatoprotective activity from the aspect of mitochondrial biogenesis. The structure-activity relationship demonstrated that hydroxyl and ketone groups were active groups interacting with mitochondrial biogenesis proteins (SIRT1 and PGC1α), and the activity was stronger when the o-hydroxyl group was present on the benzene ring. In contrast, the activity was little affected by the presence of the p-hydroxyl group, m-hydroxyl group, butyl group type, or halogen. In addition, in vitro studies confirmed that these compounds could directly bind to SIRT1 and PGC1α, markedly promote their interaction, significantly increase the expression of proteins and genes related to mitochondrial biogenesis (SIRT1, PGC1α, NRF1, TFAM, COX1, and ND6) and subsequently ameliorate mitochondria dysfunction, which was evidenced by the decreased ROS, upregulated ATP production, increased MMP, and enhanced mitochondrial number. According to the outcomes of our in vitro and in vivo experiments, 4-butyl-polyhydroxybenzophenone compounds could also effectively reduce the formation of lipid droplets and liver injury index (ALT, AST, LDH, AKP, γ-GT, and GDH) and improve the level of antioxidant enzymes (GSH and SOD). Particularly, the treatment of these compounds after a high-fat diet could significantly reduce body weight, decrease liver coefficient, attenuate liver damage, and ameliorate lipid accumulation in rat liver, demonstrating their therapeutic effects on NAFLD. Mechanistically, 4-butyl-polyhydroxybenzophenone compounds promoted mitochondrial biogenesis and eventually prevented NAFLD liver injury by activating the PGC1α signaling pathway in a SIRT1-dependent manner, which was strongly supported by SIRT1 inhibitor EX527.
    Keywords:  4-Butyl-polyhydroxybenzophenone compounds; Mitochondrial biogenesis; NAFLD; PGC1α; SIRT1
    DOI:  https://doi.org/10.1016/j.ejmech.2023.115728