Cited by 50

The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.

Sterol biosensor reveals LAM-family Ltc1-dependent sterol flow to endosomes upon Arp2/3 inhibition

Marek, Magdalena, Vincenzetti, Vincent, Martin, Sophie G.·2020·Journal of Cell Biology

Published version of a preprint

Abstract

Sterols are crucial components of biological membranes, which are synthetized in the ER and accumulate in the plasma membrane (PM). Here, by applying a genetically encoded sterol biosensor (D4H), we visualize a sterol flow between PM and endosomes in the fission yeast Schizosaccharomyces pombe. Using time-lapse and correlative light-electron microscopy, we found that inhibition of Arp2/3-dependent F-actin assembly promotes the reversible relocalization of D4H from the PM to internal sterol-rich compartments (STRIC) labeled by synaptobrevin Syb1. Retrograde sterol internalization to STRIC is independent of endocytosis or an intact Golgi, but depends on Ltc1, a LAM/StARkin-family protein localized to ER-PM contact sites. The PM in ltc1Δ cells over-accumulates sterols and upon Arp2/3 inhibition forms extended ER-interacting invaginations, indicating that sterol transfer contributes to PM size homeostasis. Anterograde sterol movement from STRIC is independent of canonical vesicular trafficking but requires Arp2/3, suggesting a novel role for this complex. Thus, transfer routes orthogonal to vesicular trafficking govern the flow of sterols in the cell.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1083/jcb.202001147

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Yeast mutants that lack GRAMD1 homologs (Lam/Ltc proteins) are highly susceptible to treatment with the polyene antibiotic Amphotericin B compared to WT cells.

    “Yeast mutants that lack GRAMD1 homologs (Lam/Ltc proteins) are highly susceptible to treatment with the polyene antibiotic, Amphotericin B, compared to WT cells (Gatta et al, 2015; Marek et al, 2020).”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 86

  1. Alvarez, 2007, Sterol-rich plasma membrane domains in fungi, Eukaryot. Cell., 6, 755, 10.1128/EC.00008-07 · DOI
  2. Antonny, 2018, The Oxysterol-Binding Protein Cycle: Burning Off PI(4)P to Transport Cholesterol, Annu. Rev. Biochem., 87, 809, 10.1146/annurev-biochem-061516-044924 · DOI
  3. Baumann, 2005, Transport of newly synthesized sterol to the sterol-enriched plasma membrane occurs via nonvesicular equilibration, Biochemistry., 44, 5816, 10.1021/bi048296z · DOI
  4. Bendezú, 2011, Actin cables and the exocyst form two independent morphogenesis pathways in the fission yeast, Mol. Biol. Cell., 22, 44, 10.1091/mbc.e10-08-0720 · DOI
  5. Bendezú, 2015, Spontaneous Cdc42 polarization independent of GDI-mediated extraction and actin-based trafficking, PLoS Biol., 13, 10.1371/journal.pbio.1002097 · DOI
  6. Besprozvannaya, 2018, GRAM domain proteins specialize functionally distinct ER-PM contact sites in human cells, eLife., 7, 10.7554/eLife.31019 · DOI · Paper page
  7. Carpy, 2014, Absolute proteome and phosphoproteome dynamics during the cell cycle of Schizosaccharomyces pombe (Fission Yeast), Mol. Cell. Proteomics., 13, 1925, 10.1074/mcp.M113.035824 · DOI
  8. Chen, 2013, Actin filament severing by cofilin dismantles actin patches and produces mother filaments for new patches, Curr. Biol., 23, 1154, 10.1016/j.cub.2013.05.005 · DOI
  9. Chugh, 2018, The actin cortex at a glance, J. Cell Sci., 131, 10.1242/jcs.186254 · DOI
  10. Das, 2014, Three pools of plasma membrane cholesterol and their relation to cholesterol homeostasis, eLife., 3, 10.7554/eLife.02882 · DOI · Paper page
  11. Day, 2018, Budding Yeast Has a Minimal Endomembrane System, Dev. Cell., 44, 56, 10.1016/j.devcel.2017.12.014 · DOI
  12. de Saint-Jean, 2011, Osh4p exchanges sterols for phosphatidylinositol 4-phosphate between lipid bilayers, J. Cell Biol., 195, 965, 10.1083/jcb.201104062 · DOI
  13. Dittman, 2017, Speed Limits for Nonvesicular Intracellular Sterol Transport, Trends Biochem. Sci., 42, 90, 10.1016/j.tibs.2016.11.004 · DOI
  14. Doherty, 2009, Mechanisms of endocytosis, Annu. Rev. Biochem., 78, 857, 10.1146/annurev.biochem.78.081307.110540 · DOI · Paper page
  15. Edamatsu, 2003, Fission yeast synaptobrevin is involved in cytokinesis and cell elongation, Biochem. Biophys. Res. Commun., 301, 641, 10.1016/S0006-291X(03)00017-2 · DOI
  16. Eden, 2016, Annexin A1 Tethers Membrane Contact Sites that Mediate ER to Endosome Cholesterol Transport, Dev. Cell., 37, 473, 10.1016/j.devcel.2016.05.005 · DOI
  17. Elbaz-Alon, 2015, Lam6 Regulates the Extent of Contacts between Organelles, Cell Rep., 12, 7, 10.1016/j.celrep.2015.06.022 · DOI
  18. Encinar Del Dedo, 2017, ORP-Mediated ER Contact with Endocytic Sites Facilitates Actin Polymerization, Dev. Cell., 43, 588, 10.1016/j.devcel.2017.10.031 · DOI
  19. Feierbach, 2004, Regulation of a formin complex by the microtubule plus end protein tea1p, J. Cell Biol., 165, 697, 10.1083/jcb.200403090 · DOI
  20. Gachet, 2005, Endocytosis in fission yeast is spatially associated with the actin cytoskeleton during polarised cell growth and cytokinesis, J. Cell Sci., 118, 4231, 10.1242/jcs.02530 · DOI
  21. Galletta, 2009, Actin and endocytosis: mechanisms and phylogeny, Curr. Opin. Cell Biol., 21, 20, 10.1016/j.ceb.2009.01.006 · DOI
  22. Gatta, 2015, A new family of StART domain proteins at membrane contact sites has a role in ER-PM sterol transport, eLife., 4, 10.7554/eLife.07253 · DOI · Paper page
  23. Gatta, 2018, Structural insights into a StART-like domain in Lam4 and its interaction with sterol ligands, Biochem. Biophys. Res. Commun., 495, 2270, 10.1016/j.bbrc.2017.12.109 · DOI · Paper page
  24. Georgiev, 2011, Osh proteins regulate membrane sterol organization but are not required for sterol movement between the ER and PM, Traffic., 12, 1341, 10.1111/j.1600-0854.2011.01234.x · DOI
  25. Goode, 2015, Actin and endocytosis in budding yeast, Genetics., 199, 315, 10.1534/genetics.112.145540 · DOI
  26. Grebe, 2003, Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes, Curr. Biol., 13, 1378, 10.1016/S0960-9822(03)00538-4 · DOI
  27. Grossmann, 2007, Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast, EMBO J., 26, 1, 10.1038/sj.emboj.7601466 · DOI
  28. Heider, 2012, Exorcising the exocyst complex, Traffic., 13, 898, 10.1111/j.1600-0854.2012.01353.x · DOI
  29. Heino, 2000, Dissecting the role of the golgi complex and lipid rafts in biosynthetic transport of cholesterol to the cell surface, Proc. Natl. Acad. Sci. USA., 97, 8375, 10.1073/pnas.140218797 · DOI
  30. Hoffmann, 2019, Tricalbins Contribute to Cellular Lipid Flux and Form Curved ER-PM Contacts that Are Bridged by Rod-Shaped Structures, Dev. Cell., 51, 488, 10.1016/j.devcel.2019.09.019 · DOI
  31. Hofsäss, 2003, Molecular dynamics simulations of phospholipid bilayers with cholesterol, Biophys. J., 84, 2192, 10.1016/S0006-3495(03)75025-5 · DOI
  32. Horenkamp, 2018, Molecular basis for sterol transport by StART-like lipid transfer domains, EMBO J., 37, 10.15252/embj.201798002 · DOI · Paper page
  33. Hoya, 2017, Traffic Through the Trans-Golgi Network and the Endosomal System Requires Collaboration Between Exomer and Clathrin Adaptors in Fission Yeast, Genetics., 205, 673, 10.1534/genetics.116.193458 · DOI
  34. Im, 2005, Structural mechanism for sterol sensing and transport by OSBP-related proteins, Nature., 437, 154, 10.1038/nature03923 · DOI
  35. Iwaki, 2004, Characterization of end4+, a gene required for endocytosis in Schizosaccharomyces pombe, Yeast., 21, 867, 10.1002/yea.1134 · DOI
  36. Jacquier, 2012, Mechanisms of sterol uptake and transport in yeast, J. Steroid Biochem. Mol. Biol., 129, 70, 10.1016/j.jsbmb.2010.11.014 · DOI
  37. Jentsch, 2018, Structural basis of sterol binding and transport by a yeast StARkin domain, J. Biol. Chem., 293, 5522, 10.1074/jbc.RA118.001881 · DOI · Paper page
  38. Johnson, 2012, Modifications in perfringolysin O domain 4 alter the cholesterol concentration threshold required for binding, Biochemistry., 51, 3373, 10.1021/bi3003132 · DOI
  39. Kabeche, 2011, The filament-forming protein Pil1 assembles linear eisosomes in fission yeast, Mol. Biol. Cell., 22, 4059, 10.1091/mbc.e11-07-0605 · DOI
  40. Kabeche, 2015, Eisosomes provide membrane reservoirs for rapid expansion of the yeast plasma membrane, J. Cell Sci., 128, 4057, 10.1242/jcs.176867 · DOI
  41. Kabeche, 2015, Pil1 cytoplasmic rods contain bundles of crosslinked tubules, Commun. Integr. Biol., 8, 10.4161/19420889.2014.990848 · DOI
  42. Kanerva, 2013, LDL cholesterol recycles to the plasma membrane via a Rab8a-Myosin5b-actin-dependent membrane transport route, Dev. Cell., 27, 249, 10.1016/j.devcel.2013.09.016 · DOI
  43. Khafif, 2014, Identification and phylogenetic analyses of VASt, an uncharacterized protein domain associated with lipid-binding domains in Eukaryotes, BMC Bioinformatics., 15, 222, 10.1186/1471-2105-15-222 · DOI
  44. Kita, 2004, Loss of Apm1, the micro1 subunit of the clathrin-associated adaptor-protein-1 complex, causes distinct phenotypes and synthetic lethality with calcineurin deletion in fission yeast, Mol. Biol. Cell., 15, 2920, 10.1091/mbc.e03-09-0659 · DOI
  45. Kukulski, 2012, Precise, correlated fluorescence microscopy and electron tomography of lowicryl sections using fluorescent fiducial markers, Methods Cell Biol., 111, 235, 10.1016/B978-0-12-416026-2.00013-3 · DOI
  46. Lacy, 2018, Molecular mechanisms of force production in clathrin-mediated endocytosis, FEBS Lett., 592, 3586, 10.1002/1873-3468.13192 · DOI
  47. Lee, 2000, Fission yeast myosin-I, Myo1p, stimulates actin assembly by Arp2/3 complex and shares functions with WASp, J. Cell Biol., 151, 789, 10.1083/jcb.151.4.789 · DOI
  48. Luo, 2017, Routes and mechanisms of post-endosomal cholesterol trafficking: A story that never ends, Traffic., 18, 209, 10.1111/tra.12471 · DOI
  49. Luo, 2019, Intracellular Cholesterol Transport by Sterol Transfer Proteins at Membrane Contact Sites, Trends Biochem. Sci., 44, 273, 10.1016/j.tibs.2018.10.001 · DOI
  50. Maekawa, 2015, Complementary probes reveal that phosphatidylserine is required for the proper transbilayer distribution of cholesterol, J. Cell Sci., 128, 1422, 10.1242/jcs.164715 · DOI
  51. Maekawa, 2016, Perfringolysin O Theta Toxin as a Tool to Monitor the Distribution and Inhomogeneity of Cholesterol in Cellular Membranes, Toxins (Basel)., 8, 67, 10.3390/toxins8030067 · DOI
  52. Makushok, 2016, Sterol-Rich Membrane Domains Define Fission Yeast Cell Polarity, Cell., 165, 1182, 10.1016/j.cell.2016.04.037 · DOI
  53. Marek, 2014, Serum albumin promotes ATP-binding cassette transporter-dependent sterol uptake in yeast, FEMS Yeast Res., 14, 1223, 10.1111/1567-1364.12219 · DOI
  54. Mastronarde, 2017, Automated tilt series alignment and tomographic reconstruction in IMOD, J. Struct. Biol., 197, 102, 10.1016/j.jsb.2016.07.011 · DOI
  55. Maxfield, 2010, Cholesterol, the central lipid of mammalian cells, Curr. Opin. Cell Biol., 22, 422, 10.1016/j.ceb.2010.05.004 · DOI · Paper page
  56. Moser von Filseck, 2015, A phosphatidylinositol-4-phosphate powered exchange mechanism to create a lipid gradient between membranes, Nat. Commun., 6, 6671, 10.1038/ncomms7671 · DOI
  57. Murley, 2015, Ltc1 is an ER-localized sterol transporter and a component of ER-mitochondria and ER-vacuole contacts, J. Cell Biol., 209, 539, 10.1083/jcb.201502033 · DOI
  58. Ng, 2020, Plasma Membrane Furrows Control Plasticity of ER-PM Contacts, Cell Rep., 30, 1434, 10.1016/j.celrep.2019.12.098 · DOI
  59. Nolen, 2009, Characterization of two classes of small molecule inhibitors of Arp2/3 complex, Nature., 460, 1031, 10.1038/nature08231 · DOI
  60. Postma, 2019, PlotsOfData-A web app for visualizing data together with their summaries, PLoS Biol., 17, 10.1371/journal.pbio.3000202 · DOI
  61. Quon, 2018, Endoplasmic reticulum-plasma membrane contact sites integrate sterol and phospholipid regulation, PLoS Biol., 16, 10.1371/journal.pbio.2003864 · DOI
  62. Raiborg, 2015, ER-endosome contact sites: molecular compositions and functions, EMBO J., 34, 1848, 10.15252/embj.201591481 · DOI
  63. Raychaudhuri, 2006, Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein-related proteins and phosphoinositides, J. Cell Biol., 173, 107, 10.1083/jcb.200510084 · DOI
  64. Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods., 9, 676, 10.1038/nmeth.2019 · DOI · Paper page
  65. Schulz, 2009, Lipid-regulated sterol transfer between closely apposed membranes by oxysterol-binding protein homologues, J. Cell Biol., 187, 889, 10.1083/jcb.200905007 · DOI
  66. Scott, 2002, Modeling the lipid component of membranes, Curr. Opin. Struct. Biol., 12, 495, 10.1016/S0959-440X(02)00353-6 · DOI
  67. Sezgin, 2016, A comparative study on fluorescent cholesterol analogs as versatile cellular reporters, J. Lipid Res., 57, 299, 10.1194/jlr.M065326 · DOI
  68. Sezgin, 2017, The mystery of membrane organization: composition, regulation and roles of lipid rafts, Nat. Rev. Mol. Cell Biol., 18, 361, 10.1038/nrm.2017.16 · DOI · Paper page
  69. Shimada, 2002, The C-terminal domain of perfringolysin O is an essential cholesterol-binding unit targeting to cholesterol-rich microdomains, Eur. J. Biochem., 269, 6195, 10.1046/j.1432-1033.2002.03338.x · DOI
  70. Simonetti, 2019, Actin-dependent endosomal receptor recycling, Curr. Opin. Cell Biol., 56, 22, 10.1016/j.ceb.2018.08.006 · DOI · Paper page
  71. Sirotkin, 2005, Interactions of WASp, myosin-I, and verprolin with Arp2/3 complex during actin patch assembly in fission yeast, J. Cell Biol., 170, 637, 10.1083/jcb.200502053 · DOI
  72. Skau, 2010, Fimbrin and tropomyosin competition regulates endocytosis and cytokinesis kinetics in fission yeast, Curr. Biol., 20, 1415, 10.1016/j.cub.2010.06.020 · DOI
  73. Solanko, 2018, Ergosterol is mainly located in the cytoplasmic leaflet of the yeast plasma membrane, Traffic., 19, 198, 10.1111/tra.12545 · DOI
  74. TerBush, 1996, The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae, EMBO J., 15, 6483, 10.1002/j.1460-2075.1996.tb01039.x · DOI
  75. Tong, 2018, Structural basis of sterol recognition and nonvesicular transport by lipid transfer proteins anchored at membrane contact sites, Proc. Natl. Acad. Sci. USA., 115, E856, 10.1073/pnas.1719709115 · DOI
  76. Turi, 1994, Brefeldin A sensitivity and resistance in Schizosaccharomyces pombe. Isolation of multiple genes conferring resistance, J. Biol. Chem., 269, 24229, 10.1016/S0021-9258(19)51072-9 · DOI
  77. Urbani, 1990, Cholesterol and vesicular stomatitis virus G protein take separate routes from the endoplasmic reticulum to the plasma membrane, J. Biol. Chem., 265, 1919, 10.1016/S0021-9258(19)39918-1 · DOI
  78. Vjestica, 2019, A toolbox of Stable Integration Vectors (SIV) in the fission yeast Schizosaccharomyces pombe, J. Cell Sci.
  79. Wachtler, 2003, Sterol-rich plasma membrane domains in the fission yeast Schizosaccharomyces pombe, J. Cell Sci., 116, 867, 10.1242/jcs.00299 · DOI
  80. Wang, 2002, The multiprotein exocyst complex is essential for cell separation in Schizosaccharomyces pombe, Mol. Biol. Cell., 13, 515, 10.1091/mbc.01-11-0542 · DOI
  81. Weill, 2018, Toolbox: Creating a systematic database of secretory pathway proteins uncovers new cargo for COPI, Traffic., 19, 370, 10.1111/tra.12560 · DOI
  82. West, 2011, A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature, J. Cell Biol., 193, 333, 10.1083/jcb.201011039 · DOI
  83. Wilhelm, 2017, STARD3 mediates endoplasmic reticulum-to-endosome cholesterol transport at membrane contact sites, EMBO J., 36, 1412, 10.15252/embj.201695917 · DOI
  84. Wong, 2016, Lipid transfer proteins do their thing anchored at membrane contact sites… but what is their thing?, Biochem. Soc. Trans., 44, 517, 10.1042/BST20150275 · DOI
  85. Wong, 2017, Advances on the Transfer of Lipids by Lipid Transfer Proteins, Trends Biochem. Sci., 42, 516, 10.1016/j.tibs.2017.05.001 · DOI
  86. Zhang, 2012, Plasma membrane tethering of the cortical ER necessitates its finely reticulated architecture, Curr. Biol., 22, 2048, 10.1016/j.cub.2012.08.047 · DOI

Cited by

Sorted by citations

Metadata

Authors
Marek, M., Vincenzetti, V., & Martin, S. G.
Venue
Journal of Cell Biology
Published
2020-04-22
Volume
219
Issue
6
ISSN
  • 0021-9525
  • 1540-8140
Cited by
50
References
2
Language
en
Funders
  • European Research Council
  • Swiss National Science Foundation (310030B_176396)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review