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Structure–function insights into direct lipid transfer between membranes by Mmm1–Mdm12 of ERMES
Open accessAbstract
The endoplasmic reticulum (ER)–mitochondrial encounter structure (ERMES) physically links the membranes of the ER and mitochondria in yeast. Although the ER and mitochondria cooperate to synthesize glycerophospholipids, whether ERMES directly facilitates the lipid exchange between the two organelles remains controversial. Here, we compared the x-ray structures of an ERMES subunit Mdm12 from Kluyveromyces lactis with that of Mdm12 from Saccharomyces cerevisiae and found that both Mdm12 proteins possess a hydrophobic pocket for phospholipid binding. However in vitro lipid transfer assays showed that Mdm12 alone or an Mmm1 (another ERMES subunit) fusion protein exhibited only a weak lipid transfer activity between liposomes. In contrast, Mdm12 in a complex with Mmm1 mediated efficient lipid transfer between liposomes. Mutations in Mmm1 or Mdm12 impaired the lipid transfer activities of the Mdm12–Mmm1 complex and furthermore caused defective phosphatidylserine transport from the ER to mitochondrial membranes via ERMES in vitro. Therefore, the Mmm1–Mdm12 complex functions as a minimal unit that mediates lipid transfer between membranes.
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“Mdm12, Mdm34, and Mmm1 have synaptotagmin-like mitochondrial-lipid-binding protein (SMP) domains [24], and the ERMES complex mediates lipid transport [25,26].”
From In Candida glabrata, ERMES Component GEM1 Controls Mitochondrial Morphology, mtROS, and Drug Efflux Pump Expression, Resulting in Azole Susceptibility (2023) · cites this paper as [25]
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MethodComparison of simple potential functions for simulating liquid water
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“To monitor lipid transfer between liposomes via the HMmm1s– Mdm12 complex and MBP-HMmm1s, we adopted fluorescent dequenching assays as described previously (Connerth et al., 2012; Watanabe et al., 2015; Miyata et al., 2016).”
Method
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ER: the Silk Road of interorganellar communication
Wang, J., & Dehesh, K. (2018) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2018.07.012 · Cited by 25
“structural and functional analysis of Mmm1-Mdm12 complex supports that ERMES is responsible for not only membrane tethering but also facilitating efficient lipid exchange, such as PE and PS, at ER-mitochondria contact sites in yeast [47].”
BackgroundSpecificity of lipid transfer proteins: An in vitro story
Hamaï, A., & Drin, G. (2024) · Biochimie · doi:10.1016/j.biochi.2024.09.007 · Cited by 24
Maiuolo, J., Gliozzi, M., Musolino, V., Carresi, C., Nucera, S., Scicchitano, M., Scarano, F., Bosco, F., Oppedisano, F., Macrì, R., et al. (2020) · Biomedicines · doi:10.3390/biomedicines8120553 · Cited by 21
“These proteins contain a synaptotagmin-like mitochondrial-lipid binding protein (SMP) domain and it has been shown that, among these, Mmm1 and Mdm12 bind phospholipids in vitro [55,56].”
BackgroundSam, P. N., Calzada, E., Acoba, M. G., Zhao, T., Watanabe, Y., Nejatfard, A., Trinidad, J. C., Shutt, T. E., Neal, S. E., & Claypool, S. M. (2021) · iScience · doi:10.1016/j.isci.2021.102196 · Cited by 23
“Mitochondrial lipid biosynthesis is dependent on the acquisition of phospholipid precursors provided by the endoplasmic reticulum (ER)/vacuole that fuel the generation of phosphatidic acid, phosphatidylglycerol, cardiolipin, and phosphatidylethanolamine (PE) (Elbaz-Alon et al., 2014; Honscher et al., 2014; Kawano et a…”
BackgroundHoribata, Y., Mitsuhashi, S., Shimizu, H., Maejima, S., Sakamoto, H., Aoyama, C., Ando, H., & Sugimoto, H. (2020) · Scientific Reports · doi:10.1038/s41598-020-59444-y · Cited by 21
Multifaceted roles of porin in mitochondrial protein and lipid transport
Endo, T., & Sakaue, H. (2019) · Biochemical Society Transactions · doi:10.1042/bst20190153 · Cited by 22
Kinetics of Atg2-mediated lipid transfer from the ER can account for phagophore expansionPreprint
von Bülow, S., & Hummer, G. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.12.090977 · Cited by 21
New Insights on the Uptake and Trafficking of Coenzyme Q
Guile, M. D., Jain, A., Anderson, K. A., & Clarke, C. F. (2023) · Antioxidants · doi:10.3390/antiox12071391 · Cited by 22
“The Mmm1Mdm12 complex has been shown to mediate phospholipid transfer in vitro and mutations in MMM1 and MDM12 lead to impaired lipid transfer through ERMES in vivo [87].”
BackgroundMembrane contact sites and cytoskeleton‐membrane interactions in autophagy
Duckney, P. J., Wang, P., & Hussey, P. J. (2022) · FEBS Letters · doi:10.1002/1873-3468.14414 · Cited by 20
Mitochondrial Control of Fungal Cell Walls: Models and Relevance in Fungal Pathogens
Koch, B., & Traven, A. (2019) · Current Topics in Microbiology and Immunology · doi:10.1007/82_2019_183 · Cited by 19
Mitochondrial junctions with cellular organelles: Ca2+ signalling perspective
Tepikin, A. V. (2018) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-018-2179-z · Cited by 19
Organelle zones in mitochondria
Shimizu, S. (2018) · The Journal of Biochemistry · doi:10.1093/jb/mvy068 · Cited by 18
Dissociation of ERMES clusters plays a key role in attenuating the endoplasmic reticulum stress
Kakimoto, Y., Kojima, R., Shiino, H., Shinmyo, M., Kurokawa, K., Nakano, A., Endo, T., & Tamura, Y. (2022) · iScience · doi:10.1016/j.isci.2022.105362 · Cited by 16
“…transport between the ER and mitochondria is known to be mediated by the ER-mitochondria encounter structure (ERMES) in yeast, which also functions as the molecular tether between these organelles (Jeong et al., 2016,2017; Kawano et al., 2018; Kojima et al., 2016; Kornmann et al., 2009).”
InfluentialMembrane tethering by the autophagy ATG2A-WIPI4 complex
Graef, M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1814759115 · Cited by 17
MITOL regulates phosphatidic acid-binding activity of RMDN3/PTPIP51
Ito, N., Takahashi, T., Shiiba, I., Nagashima, S., Inatome, R., & Yanagi, S. (2021) · The Journal of Biochemistry · doi:10.1093/jb/mvab153 · Cited by 16
Navigating the landscape of mitochondrial-ER communication in health and disease
Ronayne, C. T., & Latorre‐Muro, P. (2024) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2024.1356500 · Cited by 16
“In yeast, the ERMES system facilitates the transport of PS and PC to mitochondria (Kawano et al., 2018).”
BackgroundImaging and proteomics toolkits for studying organelle contact sites
Gamuyao, R., & Chang, C. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1466915 · Cited by 17
“The ERMES is vital for the ef fi cient transfer of phospholipids between these organelles (Kornmann et al., 2009; Voss et al., 2012; AhYoung et al., 2015; Kawano et al., 2018).”
BackgroundVps39 is required for ethanolamine-stimulated elevation in mitochondrial phosphatidylethanolamine
Iadarola, D. M., Ball, W. B., Trivedi, P. P., Fu, G., Nan, B., & Gohil, V. M. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2020.158655 · Cited by 16
Regulation of mitochondrial cristae organization by Myo19, Miro1 and Miro2, and metaxin 3
Shembekar, S., Nikolaus, P., Honnert, U., Höring, M., Attia, A., Topp, K., Lohmann, B., Liebisch, G., & Bähler, M. (2025) · Journal of Cell Science · doi:10.1242/jcs.263637 · Cited by 14
Mitochondrial phospholipid transport: Role of contact sites and lipid transport proteins
Mavuduru, V. A., Vadupu, L., Ghosh, K. K., Chakrabortty, S., Gulyás, B. Z., Padmanabhan, P., & Ball, W. B. (2024) · Progress in Lipid Research · doi:10.1016/j.plipres.2024.101268 · Cited by 15
Contribution of ERMES subunits to mature peroxisome abundance
Esposito, M., Denmat, S. H., & Delahodde, A. (2019) · PLoS ONE · doi:10.1371/journal.pone.0214287 · Cited by 14
Amino Acids Promote Mitochondrial-Derived Compartment Formation in Mammalian CellsPreprint
Schuler, M.-H., English, A. M., VanderMeer, L., Shaw, J. M., & Hughes, A. L. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.23.424218 · Cited by 14
Friedman, J. R. (2022) · Contact · doi:10.1177/25152564221133267 · Cited by 11
“In vitro work demonstrates the ability of such SMP proteins to bind and transport lipids, and consistent with this, cells deficient in the ERMES complex have altered mitochondria phospholipid composition (AhYoung et al., 2017; Jeong et al., 2017; Kawano et al., 2018).”
BackgroundMitochondrial protein import machinery conveys stress signals to the cytosol and beyond
Lionaki, E., Gkikas, I., & Tavernarakis, N. (2023) · BioEssays · doi:10.1002/bies.202200160 · Cited by 13
Okamoto, M., Nakano, K., Takahashi-Nakaguchi, A., Sasamoto, K., Yamaguchi, M., Teixeira, M. C., & Chibana, H. (2023) · Journal of Fungi · doi:10.3390/jof9020240 · Cited by 11
“Mdm12, Mdm34, and Mmm1 have synaptotagmin-like mitochondrial-lipid-binding protein (SMP) domains [24], and the ERMES complex mediates lipid transport [25,26].”
BackgroundShapiro, I. M., Risbud, M. V., & Landis, W. J. (2024) · Bone · doi:10.1016/j.bone.2024.117112 · Cited by 12
Fujimoto, S., Tashiro, S., & Tamura, Y. (2023) · Contact · doi:10.1177/25152564231153621 · Cited by 11
“Furthermore, in vitro assays using membrane fractions or the puri fi ed Mmm1-Mdm12 complex revealed that the ERMES directly facilitates phospholipid transport between the ER and mitochondria (Kawano et al., 2018; Kojima et al., 2016).”
BackgroundStructural basis for interorganelle phospholipid transport mediated by VAT-1
Watanabe, Y., Tamura, Y., Kakuta, C., Watanabe, S., & Endo, T. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.011019 · Cited by 11
“In yeast, the best-characterized interorganelle contact site is formed by the ER–mitochondrial encounter structure (ERMES), a protein complex consisting of the integral ER membrane protein Mmm1, integral mitochondrial OM proteins Mdm10 and Mdm34, and the peripheral mitochondrial OM protein Mdm12 (14).”
BackgroundInfluentialMitochondria–plasma membrane contact sites regulate the ER–mitochondria encounter structure
Casler, J. C., Harper, C. S., & Lackner, L. L. (2025) · Journal of Cell Science · doi:10.1242/jcs.263685 · Cited by 10
Mizuike, A., Kobayashi, S., Rikukawa, T., Ohta, A., Horiuchi, H., & Fukuda, R. (2019) · PLoS ONE · doi:10.1371/journal.pone.0215009 · Cited by 10
Role of the small protein Mco6 in the mitochondrial sorting and assembly machinery
Busto, J. V., Ganesan, I., Mathar, H., Steiert, C., Schneider, E. F., Straub, S. P., Ellenrieder, L., Song, J., Stiller, S. B., Lübbert, P., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113805 · Cited by 12
Uncovering the principles coordinating systems-level organelle biogenesis with cellular growth
Wang, S., Kailash, D., & Mukherji, S. (2025) · Cell Systems · doi:10.1016/j.cels.2025.101267 · Cited by 9
Supramolecular architecture of the ER-mitochondria encounter structure in its native environmentPreprint
Wozny, M. R., Luca, A. D., Morado, D. R., Picco, A., Hoffmann, P. C., Miller, E. A., Vanni, S., & Kukulski, W. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.12.488000 · Cited by 9
“ERMES mediates the transport of phospholipids between ER and mitochondria (8, 9), possibly underpinning its roles in mitochondrial function.”
BackgroundChemical inhibition of phosphatidylcholine biogenesis reveals its role in mitochondrial division
Shiino, H., Tashiro, S., Hashimoto, M., Sakata, Y., Hosoya, T., Endo, T., Kojima, H., & Tamura, Y. (2024) · iScience · doi:10.1016/j.isci.2024.109189 · Cited by 8
The Endoplasmic Reticulum-Mitochondria Encounter Structure and its Regulatory Proteins
Cheema, J. Y., He, J., Wei, W., & Fu, C. (2021) · Contact · doi:10.1177/25152564211064491 · Cited by 9
Metadata
- Authors
- Kawano, S., Tamura, Y., Kojima, R., Bala, S., Asai, E., Michel, A. H., Kornmann, B., Riezman, I., Riezman, H., Sakae, Y., Okamoto, Y., & Endo, T.
- Affiliations
- Kyoto Sangyo University (JP)
- Yamagata University (JP)
- Nagoya University (JP)
- ETH Zurich (CH)
- Institute of Biochemistry, ETH Zürich, Zürich, Switzerland 9
- University of Geneva (CH)
- Corresponding author
- Endo, Toshiya
- ORCID
- Venue
- Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 2017-12-26
- Volume
- 217
- Issue
- 3
- Pages
- 959-974
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC5839780
- OpenAlex
- W2777157902
- Cited by
- 148
- References
- 58
- Citations by year
- 2026: 12 · 2025: 11 · 2024: 20 · 2023: 11 · 2022: 14 · 2021: 17 · 2020: 23 · 2019: 26 · 2018: 14
- FWCI
- 8.72
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The Journal of Cell Biology (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion, other-oa)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by-nc-sa)
- ETH Zürich Research Collection
- Funders
- Japan Society of the Promotion of Science (25840020, 17K18230, 15H05595, 15H05705, 2222703)
- Japan Science and Technology Agency
- Core Research for Evolutional Science and Technology (JPMJCR12M1)
- Swiss National Science Foundation
- National Centre of Competence in Research
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- ERMES, lipid transfer, endoplasmic reticulum-mitochondria contacts, phosphatidylserine transport, glycerophospholipid biosynthesis, Kluyveromyces lactis, Saccharomyces cerevisiae, protein structure, membrane lipid exchange
- MeSH terms
- Biological Transport, Active, Endoplasmic Reticulum, Kluyveromyces, Membrane Proteins, Phospholipids, Saccharomyces cerevisiae, Structure-Activity Relationship, Mitochondrial Proteins, Saccharomyces cerevisiae Proteins, Multiprotein Complexes, Mitochondrial Membranes
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