Cited by 14Lipid Membrane Structure and BehaviorLipid metabolism and biosynthesisCellular transport and secretion

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Lipid osmosis, membrane tension, and other mechanochemical driving forces of lipid flow

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Zhang, Yongli, Lin, Chenxiang·2024·Current Opinion in Cell Biology

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Abstract

Nonvesicular lipid transport among different membranes or membrane domains plays crucial roles in lipid homeostasis and organelle biogenesis. However, the forces that drive such lipid transport are not well understood. We propose that lipids tend to flow towards the membrane area with a higher membrane protein density in a process termed lipid osmosis. This process lowers the membrane tension in the area, resulting in a membrane tension difference called osmotic membrane tension. We examine the thermodynamic basis and experimental evidence of lipid osmosis and osmotic membrane tension. We predict that lipid osmosis can drive bulk lipid flows between different membrane regions through lipid transfer proteins, scramblases, or similar barriers that selectively pass lipids but not membrane proteins. We also speculate on the biological functions of lipid osmosis. Finally, we explore other driving forces for lipid transfer and describe potential methods and systems to further test our theory.

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Research works printed but not linked: 86

  1. Hanna, 2023, RBG motif bridge-like lipid transport proteins: structure, functions, and open questions, Annu Rev Cell Dev Biol, 39, 409, 10.1146/annurev-cellbio-120420-014634 · DOI
  2. Kumar, 2018, VPS13A and VPS13C are lipid transport proteins differentially localized at ER contact sites, J Cell Biol, 217, 3625, 10.1083/jcb.201807019 · DOI
  3. Reinisch, 2021, Mechanisms of nonvesicular lipid transport, J Cell Biol, 220, 10.1083/jcb.202012058 · DOI
  4. Wong, 2019, Lipid transfer proteins: the lipid commute via shuttles, bridges and tubes, Nat Rev Mol Cell Biol, 20, 85, 10.1038/s41580-018-0071-5 · DOI · Paper page
  5. Cai, 2022, De Camilli P: in situ architecture of the lipid transport protein VPS13C at ER-lysosome membrane contacts, Proc Natl Acad Sci USA, 119
  6. Neuman, 2022, A novel superfamily of bridge-like lipid transfer proteins, Trends Cell Biol, 32, 962, 10.1016/j.tcb.2022.03.011 · DOI
  7. Li, 2020, Cryo-EM reconstruction of a VPS13 fragment reveals a long groove to channel lipids between membranes, J Cell Biol, 219, 10.1083/jcb.202001161 · DOI
  8. Valverde, 2019, ATG2 transports lipids to promote autophagosome biogenesis, J Cell Biol, 218, 1787, 10.1083/jcb.201811139 · DOI
  9. de Saint-Jean, 2011, Osh4p exchanges sterols for phosphatidylinositol 4-phosphate between lipid bilayers, J Cell Biol, 195, 965, 10.1083/jcb.201104062 · DOI
  10. Chung, 2015, PI4P/phosphatidylserine countertransport at ORP5- and ORP8-mediated ER-plasma membrane contacts, Science, 349, 428, 10.1126/science.aab1370 · DOI
  11. Zhang, 2022, Kumar A: quantitative models of lipid transfer and membrane contact formation, Contact, 5, 1, 10.1177/25152564221096024 · DOI
  12. Ghanbarpour, 2021, A model for a partnership of lipid transfer proteins and scramblases in membrane expansion and organelle biogenesis, Proc Natl Acad Sci USA, 118, 10.1073/pnas.2101562118 · DOI
  13. Li, 2021, TMEM41B and VMP1 are scramblases and regulate the distribution of cholesterol and phosphatidylserine, J Cell Biol, 220, 10.1083/jcb.202103105 · DOI
  14. Matoba, 2020, Atg9 is a lipid scramblase that mediates autophagosomal membrane expansion, Nat Struct Mol Biol, 27, 1185, 10.1038/s41594-020-00518-w · DOI · Paper page
  15. Guillén-Samander, 2022, A partnership between the lipid scramblase XK and the lipid transfer protein VPS13A at the plasma membrane, Proc Natl Acad Sci USA, 119, 10.1073/pnas.2205425119 · DOI
  16. Falzone, 2022, TMEM16 scramblases thin the membrane to enable lipid scrambling, Nat Commun, 13, 2604, 10.1038/s41467-022-30300-z · DOI
  17. Sakuragi, 2023, Regulation of phospholipid distribution in the lipid bilayer by flippases and scramblases, Nat Rev Mol Cell Biol, 24, 576, 10.1038/s41580-023-00604-z · DOI
  18. van Vliet, 2022, ATG9A and ATG2A form a heteromeric complex essential for autophagosome formation, Mol Cell, 82, 4324, 10.1016/j.molcel.2022.10.017 · DOI
  19. Mi, 2017, Structural basis of MsbA-mediated lipopolysaccharide transport, Nature, 549, 233, 10.1038/nature23649 · DOI
  20. Grimm, 2020, The inner membrane protein YhdP modulates the rate of anterograde phospholipid flow in Escherichia coli, Proc Natl Acad Sci USA, 117, 26907, 10.1073/pnas.2015556117 · DOI
  21. Cooper, 2023, Isom GL: phospholipid transport to the bacterial outer membrane through an envelope-spanning bridge, bioRxiv preprint
  22. Trimble, 2015, Barriers to the free diffusion of proteins and lipids in the plasma membrane, J Cell Biol, 208, 259, 10.1083/jcb.201410071 · DOI
  23. Cohen, 2020, Do cell membranes flow like honey or jiggle like jello?, Bioessays, 42, 10.1002/bies.201900142 · DOI
  24. Winckler, 1999, A diffusion barrier maintains distribution of membrane proteins in polarized neurons, Nature, 397, 698, 10.1038/17806 · DOI
  25. Albrecht, 2016, Nanoscopic compartmentalization of membrane protein motion at the axon initial segment, J Cell Biol, 215, 37, 10.1083/jcb.201603108 · DOI
  26. Xu, 2013, Form a periodic cytoskeletal structure in axons, Science, 339, 452, 10.1126/science.1232251 · DOI
  27. Hu, 2010, A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution, Science, 329, 436, 10.1126/science.1191054 · DOI
  28. Tada, 2007, Role of septin cytoskeleton in spine morphogenesis and dendrite development in neurons, Curr Biol, 17, 1752, 10.1016/j.cub.2007.09.039 · DOI
  29. Caudron, 2009, Septins and the lateral compartmentalization of eukaryotic membranes, Dev Cell, 16, 493, 10.1016/j.devcel.2009.04.003 · DOI
  30. De Belly, 2023, Cell protrusions and contractions generate long-range membrane tension propagation, Cell, 186, 3049, 10.1016/j.cell.2023.05.014 · DOI
  31. Kusumi, 2005, Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules, Annu Rev Biophys Biomol Struct, 34, 351, 10.1146/annurev.biophys.34.040204.144637 · DOI
  32. Pánek, 2020, Returning to the fold for lessons in mitochondrial crista diversity and evolution, Curr Biol, 30, R575, 10.1016/j.cub.2020.02.053 · DOI
  33. Friedman, 2022, Mitochondria from the outside in: the relationship between inter-organelle crosstalk and mitochondrial internal organization, Contact, 5
  34. Bragulat-Teixidor, 2023, The junctions connecting the endoplasmic reticulum to the nuclear envelope are constricted and remodelled during the cell cycle, BioRxiv Preprint
  35. Sawa-Makarska, 2020, Reconstitution of autophagosome nucleation defines Atg9 vesicles as seeds for membrane formation, Science, 369, 10.1126/science.aaz7714 · DOI
  36. Kory, 2015, Protein crowding is a determinant of lipid droplet protein composition, Dev Cell, 34, 351, 10.1016/j.devcel.2015.06.007 · DOI
  37. Perez, 2022, Rapid propagation of membrane tension at retinal bipolar neuron presynaptic terminals, Sci Adv, 8
  38. Dai, 1999, Membrane tether formation from blebbing cells, Biophys J, 77, 3363, 10.1016/S0006-3495(99)77168-7 · DOI
  39. Shi, 2022, Membrane tension propagation couples axon growth and collateral branching, Sci Adv, 8, 10.1126/sciadv.abo1297 · DOI
  40. Marbach, 2019, Osmosis, from molecular insights to large-scale applications, Chem Soc Rev, 48, 3102, 10.1039/C8CS00420J · DOI
  41. Phillips, 2012, Physical biology of the cell edn 2nd, Garland Science
  42. Bieber, 2022, In situ structural analysis reveals membrane shape transitions during autophagosome formation, Proc Natl Acad Sci USA, 119, 10.1073/pnas.2209823119 · DOI
  43. Rangamani, 2022, The many faces of membrane tension: challenges across systems and scales, Biochim Biophys Acta Biomembr, 1864, 183897, 10.1016/j.bbamem.2022.183897 · DOI
  44. Deserno, 2015, Fluid lipid membranes: from differential geometry to curvature stresses, Chem Phys Lipids, 185, 11, 10.1016/j.chemphyslip.2014.05.001 · DOI
  45. Seifert, 1995, The concept of effective tension for fluctuating vesicles, Z Phys B Con Mat, 97, 299, 10.1007/BF01307480 · DOI
  46. Jahnig, 1984, Lipid exchange between membranes, Biophys J, 46, 687, 10.1016/S0006-3495(84)84067-9 · DOI
  47. Klier, 2022, Fluorescent indicators for imaging membrane potential of organelles, Curr Opin Chem Biol, 71, 102203, 10.1016/j.cbpa.2022.102203 · DOI
  48. Feng, 2023, Identification of a drug binding pocket in TMEM16F calcium-activated ion channel and lipid scramblase, Nat Commun, 14, 4874, 10.1038/s41467-023-40410-x · DOI
  49. Feng, 2019, Cryo-EM studies of TMEM16F calcium-activated ion channel suggest features important for lipid scrambling, Cell Rep, 28, 567, 10.1016/j.celrep.2019.06.023 · DOI
  50. Moser von Filseck, 2015, Drin G: a phosphatidylinositol-4-phosphate powered exchange mechanism to create a lipid gradient between membranes, Nat Commun, 6, 6671, 10.1038/ncomms7671 · DOI
  51. Melia, 2023, Growing thin-How bulk lipid transport drives expansion of the autophagosome membrane but not of its lumen, Curr Opin Cell Biol, 83
  52. Kavokine, 2021, Fluids at the nanoscale: from continuum to subcontinuum transport, Annu Rev Fluid Mech, 53, 377, 10.1146/annurev-fluid-071320-095958 · DOI
  53. Gravelle, 2013, Optimizing water permeability through the hourglass shape of aquaporins, Proc Natl Acad Sci USA, 110, 16367, 10.1073/pnas.1306447110 · DOI
  54. Barnoy, 2023, Mechanism of tension propagation in cell membranes, bioRxiv preprint
  55. Leonzino, 2021, Insights into VPS13 properties and function reveal a new mechanism of eukaryotic lipid transport, Bba-Mol Cell Biol L, 1866, 159003
  56. Xie, 2008, Atg8 controls phagophore expansion during autophagosome formation, Mol Biol Cell, 19, 3290, 10.1091/mbc.e07-12-1292 · DOI · Paper page
  57. Royes, 2020, Inducible intracellular membranes: molecular aspects and emerging applications, Microb Cell Factories, 19, 176, 10.1186/s12934-020-01433-x · DOI
  58. Wright, 1988, Increased amounts of HMG-CoA reductase induce "Karmellae" - a proliferation of stacked membrane pairs surrounding the yeast nucleus, J Cell Biol, 107, 101, 10.1083/jcb.107.1.101 · DOI
  59. Tinevez, 2009, Role of cortical tension in bleb growth, Proc Natl Acad Sci USA, 106, 18581, 10.1073/pnas.0903353106 · DOI
  60. Sakai, 2020, Modeling membrane morphological change during autophagosome formation, iScience, 23, 101466, 10.1016/j.isci.2020.101466 · DOI
  61. Melia, 2020, Autophagosome biogenesis: from membrane growth to closure, J Cell Biol, 219, 10.1083/jcb.202002085 · DOI
  62. Maeda, 2019, The autophagic membrane tether ATG2A transfers lipids between membranes, Elife, 8, 10.7554/eLife.45777 · DOI
  63. Osawa, 2019, Atg2 mediates direct lipid transfer between membranes for autophagosome formation, Nat Struct Mol Biol, 26, 281, 10.1038/s41594-019-0203-4 · DOI
  64. Shen, 2020, Engineering lipid membranes with programmable DNA nanostructures, Adv Biosyst, 4, 1900215, 10.1002/adbi.201900215 · DOI
  65. Wang, 2021, Single-molecule manipulation of macromolecules on GUV or SUV membranes using optical tweezers, Biophys J, 120, 5454, 10.1016/j.bpj.2021.11.2884 · DOI
  66. Ge, 2022, Stepwise membrane binding of extended synaptotagmins revealed by optical tweezers, Nat Chem Biol, 18, 313, 10.1038/s41589-021-00914-3 · DOI
  67. Ma, 2017, Single-molecule force spectroscopy of protein-membrane interactions, Elife, 6, 10.7554/eLife.30493 · DOI
  68. Ramakrishnan, 2022, Suspended lipid bilayer: a versatile platform for nextgen drug discovery and biomedical applications, Acc Mater Res, 3, 996, 10.1021/accountsmr.2c00157 · DOI
  69. Colom, 2018, Dal Molin M, Sakai N, Gonzalez-Gaitan M, Matile S, Roux A: a fluorescent membrane tension probe, Nat Chem, 10, 1118, 10.1038/s41557-018-0127-3 · DOI
  70. Derenyi, 2002, Formation and interaction of membrane tubes, Phys Rev Lett, 88, 238101, 10.1103/PhysRevLett.88.238101 · DOI
  71. Yang, 2016, Self-assembly of size-controlled liposomes on DNA nanotemplates, Nat Chem, 8, 476, 10.1038/nchem.2472 · DOI
  72. Yang, 2021, Sorting sub-150-nm liposomes of distinct sizes by DNA-brick-assisted centrifugation, Nat Chem, 13, 335, 10.1038/s41557-021-00667-5 · DOI
  73. Chung, 2013, Formation and analysis of topographical domains between lipid membranes tethered by DNA hybrids of different lengths, Faraday Discuss, 161, 333, 10.1039/C2FD20108A · DOI
  74. Bian, 2019, A programmable DNA-origami platform for studying lipid transfer between bilayers, Nat Chem Biol, 15, 830, 10.1038/s41589-019-0325-3 · DOI
  75. Zhang, 2023, Functionalization and higher-order organization of liposomes with DNA nanostructures, Nat Commun, 14, 5256, 10.1038/s41467-023-41013-2 · DOI
  76. Litschel, 2021, Reconstitution of contractile actomyosin rings in vesicles, Nat Commun, 12, 2254, 10.1038/s41467-021-22422-7 · DOI
  77. Simon, 2019, Actin dynamics drive cell-like membrane deformation, Nat Phys, 15, 602, 10.1038/s41567-019-0464-1 · DOI
  78. Jahnke, 2023, Engineering DNA-based cytoskeletons for synthetic cells, Interface Focus, 13, 20230028, 10.1098/rsfs.2023.0028 · DOI
  79. Grome, 2018, Vesicle tubulation with self-assembling DNA nanosprings, Angew Chem, Int Ed, 57, 5330, 10.1002/anie.201800141 · DOI
  80. Franquelim, 2021, Reversible membrane deformations by straight DNA origami filaments, Soft Matter, 17, 276, 10.1039/D0SM00150C · DOI
  81. Franquelim, 2018, Membrane sculpting by curved DNA origami scaffolds, Nat Commun, 9, 811, 10.1038/s41467-018-03198-9 · DOI
  82. Jahnke, 2021, Proton gradients from light-harvesting control DNA assemblies for synthetic cells, Nat Commun, 12, 3967, 10.1038/s41467-021-24103-x · DOI
  83. Jahnke, 2022, Bottom-up assembly of synthetic cells with a DNA cytoskeleton, ACS Nano, 16, 7233, 10.1021/acsnano.1c10703 · DOI
  84. Liu, 2022, Actuating tension-loaded DNA clamps drives membrane tubulation, Sci Adv, 8
  85. Zheng, 2023, A membrane tension-responsive mechanosensitive DNA nanomachine, Angew Chem, Int Ed, 62, 10.1002/anie.202305896 · DOI
  86. Ohmann, 2018, Al Nahas K, Baumann KN, Gopfrich K, Yoo J, Keyser UF, Aksimentiev A: a synthetic enzyme built from DNA flips 107 lipids per second in biological membranes, Nat Commun, 9, 2426, 10.1038/s41467-018-04821-5 · DOI

Metadata

Authors
Zhang, Y., & Lin, C.
Affiliations
Yale University (US)
Corresponding author
  • Zhang, Yongli
  • Lin, Chenxiang
Venue
Current Opinion in Cell Biology
Publisher
Elsevier BV
Published
2024-06
Volume
88
Pages
102377
ISSN
0955-0674 (ISSN-L)
OpenAlex
W4399239987
Cited by
14
References
2
Citations by year
2026: 7 · 2025: 6 · 2024: 1
FWCI
0.57
Type
journal article
Language
en
Open access
Locations
  • Current Opinion in Cell Biology (acceptedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
Funders
  • National Institutes of Health
  • NIGMS (R35 GM131714, R35GM149264)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
  • 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
Keywords
membrane tension, lipid flow, lipid transfer proteins, scramblase, lipid homeostasis, organelle biogenesis, membrane domains

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