1932

Abstract

The life of eukaryotic cells requires the transport of lipids between membranes, which are separated by the aqueous environment of the cytosol. Vesicle-mediated traffic along the secretory and endocytic pathways and lipid transfer proteins (LTPs) cooperate in this transport. Until recently, known LTPs were shown to carry one or a few lipids at a time and were thought to mediate transport by shuttle-like mechanisms. Over the last few years, a new family of LTPs has been discovered that is defined by a repeating β-groove (RBG) rod-like structure with a hydrophobic channel running along their entire length. This structure and the localization of these proteins at membrane contact sites suggest a bridge-like mechanism of lipid transport. Mutations in some of these proteins result in neurodegenerative and developmental disorders. Here we review the known properties and well-established or putative physiological roles of these proteins, and we highlight the many questions that remain open about their functions.

Keyword(s): ATG2BLTPhobbitSHIP164tweekVPS13
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2023-10-16
2024-04-17
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Literature Cited

  1. Adlakha J, Hong Z, Li P, Reinisch KM. 2022. Structural and biochemical insights into lipid transport by VPS13 proteins. J. Cell Biol. 221:e202202030 https://doi.org/10.1083/jcb.202202030
    [Crossref] [Google Scholar]
  2. Aeschbacher RA, Hauser MT, Feldmann KA, Benfey PN. 1995. The SABRE gene is required for normal cell expansion in Arabidopsis. Genes Dev 9:330–40. https://doi.org/10.1101/gad.9.3.330
    [Crossref] [Google Scholar]
  3. AhYoung AP, Jiang J, Zhang J, Khoi Dang X, Loo JA et al. 2015. Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. PNAS 112:E3179–88. https://doi.org/10.1073/pnas.1422363112
    [Crossref] [Google Scholar]
  4. Anding AL, Wang C, Chang T-K, Sliter DA, Powers CM et al. 2018. Vps13D encodes a ubiquitin-binding protein that is required for the regulation of mitochondrial size and clearance. Curr. Biol. 28:287–95.e6. https://doi.org/10.1016/j.cub.2017.11.064
    [Crossref] [Google Scholar]
  5. Antonny B, Bigay J, Mesmin B. 2018. The oxysterol-binding protein cycle: burning off PI(4)P to transport cholesterol. Annu. Rev. Biochem. 87:809–37. https://doi.org/10.1146/annurev-biochem-061516-044924
    [Crossref] [Google Scholar]
  6. Baldwin HA, Wang C, Kanfer G, Shah HV, Velayos-Baeza A et al. 2021. VPS13D promotes peroxisome biogenesis. J. Cell Biol. 220:e202001188 https://doi.org/10.1083/jcb.202001188
    [Crossref] [Google Scholar]
  7. Bandres-Ciga S, Saez-Atienzar S, Bonet-Ponce L, Billingsley K, Vitale D et al. 2019. The endocytic membrane trafficking pathway plays a major role in the risk of Parkinson's disease. Mov. Disord. 34:460–68. https://doi.org/10.1002/mds.27614
    [Crossref] [Google Scholar]
  8. Bankaitis VA, Johnson LM, Emr SD. 1986. Isolation of yeast mutants defective in protein targeting to the vacuole. PNAS 83:9075–79. https://doi.org/10.1073/pnas.83.23.9075
    [Crossref] [Google Scholar]
  9. Bean BDM, Dziurdzik SK, Kolehmainen KL, Fowler CMS, Kwong WK et al. 2018. Competitive organelle-specific adaptors recruit Vps13 to membrane contact sites. J. Cell Biol. 217:3593–607. https://doi.org/10.1083/jcb.201804111
    [Crossref] [Google Scholar]
  10. Blomen VA, Májek P, Jae LT, Bigenzahn JW, Nieuwenhuis J et al. 2015. Gene essentiality and synthetic lethality in haploid human cells. Science 350:1092–96. https://doi.org/10.1126/science.aac7557
    [Crossref] [Google Scholar]
  11. Bonet-Ponce L, Beilina A, Williamson CD, Lindberg E, Kluss JH et al. 2020. LRRK2 mediates tubulation and vesicle sorting from lysosomes. Sci. Adv. 6:eabb2454 https://doi.org/10.1126/sciadv.abb2454
    [Crossref] [Google Scholar]
  12. Braschi B, Bruford EA, Cavanagh AT, Neuman SD, Bashirullah A. 2022. The bridge-like lipid transfer protein (BLTP) gene group: introducing new nomenclature based on structural homology indicating shared function. Hum. Genom. 16:66 https://doi.org/10.1186/s40246-022-00439-3
    [Crossref] [Google Scholar]
  13. Cai S, Wu Y, Guillén-Samander A, Hancock-Cerutti W, Liu J, De Camilli P. 2022. In situ architecture of the lipid transport protein VPS13C at ER-lysosome membrane contacts. PNAS 119:e2203769119 https://doi.org/10.1073/pnas.2203769119
    [Crossref] [Google Scholar]
  14. Chen JJ, Nathaniel DL, Raghavan P, Nelson M, Tian R et al. 2019. Compromised function of the ESCRT pathway promotes endolysosomal escape of tau seeds and propagation of tau aggregation. J. Biol. Chem. 294:18952–66. https://doi.org/10.1074/jbc.RA119.009432
    [Crossref] [Google Scholar]
  15. Chen S, Mari M, Parashar S, Liu D, Cui Y et al. 2020. Vps13 is required for the packaging of the ER into autophagosomes during ER-phagy. PNAS 117:18530–39. https://doi.org/10.1073/pnas.2008923117
    [Crossref] [Google Scholar]
  16. Cheng X, Bezanilla M. 2021. SABRE populates ER domains essential for cell plate maturation and cell expansion influencing cell and tissue patterning. eLife 10:e65166 https://doi.org/10.7554/eLife.65166
    [Crossref] [Google Scholar]
  17. Chung J, Torta F, Masai K, Lucast L, Czapla H et al. 2015. PI4P/phosphatidylserine countertransport at ORP5- and ORP8-mediated ER-plasma membrane contacts. Science 349:428–32. https://doi.org/10.1126/science.aab1370
    [Crossref] [Google Scholar]
  18. Cohen MM Jr., Hall BD, Smith DW, Graham CB, Lampert KJ 1973. A new syndrome with hypotonia, obesity, mental deficiency, and facial, oral, ocular, and limb anomalies. J. Pediatr. 83:280–84. https://doi.org/10.1016/S0022-3476(73)80493-7
    [Crossref] [Google Scholar]
  19. Čopič A, Dorrington M, Pagant S, Barry J, Lee MCS et al. 2009. Genomewide analysis reveals novel pathways affecting endoplasmic reticulum homeostasis, protein modification and quality control. Genetics 182:757–69. https://doi.org/10.1534/genetics.109.101105
    [Crossref] [Google Scholar]
  20. Da Costa R, Bordessoules M, Guilleman M, Carmignac V, Lhussiez V et al. 2020. Vps13b is required for acrosome biogenesis through functions in Golgi dynamic and membrane trafficking. Cell. Mol. Life Sci. 77:511–29. https://doi.org/10.1007/s00018-019-03192-4
    [Crossref] [Google Scholar]
  21. Dabrowski R, Tulli S, Graef M. 2022. Parallel phospholipid transfer by Vps13 and Atg2 determines autophagosome biogenesis dynamics. bioRxiv 2022.11.10.516013. https://doi.org/10.1101/2022.11.10.516013
    [Crossref]
  22. Dall'Armellina F, Stagi M, Swan LE. 2023. In silico modelling human VPS13 proteins associated with donor and target membranes suggests lipid transfer mechanisms. Proteins 91439–55
  23. Darvish H, Bravo P, Tafakhori A, Azcona LJ, Ranji-Burachaloo S et al. 2018. Identification of a large homozygous VPS13C deletion in a patient with early-onset Parkinsonism. Mov. Disord. 33:1968–70. https://doi.org/10.1002/mds.27516
    [Crossref] [Google Scholar]
  24. De M, Oleskie AN, Ayyash M, Dutta S, Mancour L et al. 2017. The Vps13p-Cdc31p complex is directly required for TGN late endosome transport and TGN homotypic fusion. J. Cell Biol. 216:425–39. https://doi.org/10.1083/jcb.201606078
    [Crossref] [Google Scholar]
  25. De Camilli P, Peluchetti D, Meldolesi J. 1976. Dynamic changes of the luminal plasmalemma in stimulated parotid acinar cells. A freeze-fracture study. J. Cell Biol. 70:59–74. https://doi.org/10.1083/jcb.70.1.59
    [Crossref] [Google Scholar]
  26. DeGrella RF, Simoni RD. 1982. Intracellular transport of cholesterol to the plasma membrane. J. Biol. Chem. 257:14256–62. https://doi.org/10.1016/S0021-9258(19)45374-X
    [Crossref] [Google Scholar]
  27. Di Mattia T, Martinet A, Ikhlef S, McEwen AG, Nominé Y et al. 2020. FFAT motif phosphorylation controls formation and lipid transfer function of inter-organelle contacts. EMBO J 39:e104369 https://doi.org/10.15252/embj.2019104369
    [Crossref] [Google Scholar]
  28. Douglass MV, McLean AB, Trent MS. 2022. Absence of YhdP, TamB, and YdbH leads to defects in glycerophospholipid transport and cell morphology in Gram-negative bacteria. PLOS Genet 18:e1010096 https://doi.org/10.1371/journal.pgen.1010096
    [Crossref] [Google Scholar]
  29. Duplomb L, Duvet S, Picot D, Jego G, El Chehadeh-Djebbar S et al. 2014. Cohen syndrome is associated with major glycosylation defects. Hum. Mol. Genet. 23:2391–99. https://doi.org/10.1093/hmg/ddt630
    [Crossref] [Google Scholar]
  30. Dziurdzik SK, Bean BDM, Davey M, Conibear E. 2020. A VPS13D spastic ataxia mutation disrupts the conserved adaptor-binding site in yeast Vps13. Hum. Mol. Genet. 29:635–48. https://doi.org/10.1093/hmg/ddz318
    [Crossref] [Google Scholar]
  31. Dziurdzik SK, Conibear E. 2021. The Vps13 family of lipid transporters and its role at membrane contact sites. Int. J. Mol. Sci. 22:2905 https://doi.org/10.3390/ijms22062905
    [Crossref] [Google Scholar]
  32. Ekiert DC, Bhabha G, Isom GL, Greenan G, Ovchinnikov S et al. 2017. Architectures of lipid transport systems for the bacterial outer membrane. Cell 169:273–85.e17. https://doi.org/10.1016/j.cell.2017.03.019
    [Crossref] [Google Scholar]
  33. Faber AIE, van der Zwaag M, Schepers H, Eggens-Meijer E et al. 2020. Vps13 is required for timely removal of nurse cell corpses. Development 147:dev191759 https://doi.org/10.1242/dev.191759
    [Crossref] [Google Scholar]
  34. Fengsrud M, Erichsen ES, Berg TO, Raiborg C, Seglen PO. 2000. Ultrastructural characterization of the delimiting membranes of isolated autophagosomes and amphisomes by freeze-fracture electron microscopy. Eur. J. Cell Biol. 79:871–82. https://doi.org/10.1078/0171-9335-00125
    [Crossref] [Google Scholar]
  35. Gauthier J, Meijer IA, Lessel D, Mencacci NE, Krainc D et al. 2018. Recessive mutations in VPS13D cause childhood onset movement disorders. Ann. Neurol. 83:1089–95. https://doi.org/10.1002/ana.25204
    [Crossref] [Google Scholar]
  36. Ghanbarpour A, Valverde DP, Melia TJ, Reinisch KM. 2021. A model for a partnership of lipid transfer proteins and scramblases in membrane expansion and organelle biogenesis. PNAS 118:16e2101562118 https://doi.org/10.1073/pnas.2101562118
    [Crossref] [Google Scholar]
  37. Giacometti SI, MacRae MR, Dancel-Manning K, Bhabha G, Ekiert DC. 2022. Lipid transport across bacterial membranes. Annu. Rev. Cell Dev. Biol. 38:125–53. https://doi.org/10.1146/annurev-cellbio-120420-022914
    [Crossref] [Google Scholar]
  38. Gillingham AK, Bertram J, Begum F, Munro S. 2019. In vivo identification of GTPase interactors by mitochondrial relocalization and proximity biotinylation. eLife 8:e45916 https://doi.org/10.7554/eLife.45916
    [Crossref] [Google Scholar]
  39. Goldstein O, Gana-Weisz M, Banfi S, Nigro V, Bar-Shira A et al. 2023. Novel variants in genes related to vesicle-mediated-transport modify Parkinson's disease risk. Mol. Genet. Metab. 139:107608 https://doi.org/10.1016/j.ymgme.2023.107608
    [Crossref] [Google Scholar]
  40. Gómez-Sánchez R, Rose J, Guimarães R, Mari M, Papinski D et al. 2018. Atg9 establishes Atg2-dependent contact sites between the endoplasmic reticulum and phagophores. J. Cell Biol. 217:2743–63. https://doi.org/10.1083/jcb.201710116
    [Crossref] [Google Scholar]
  41. González Montoro A, Auffarth K, Hönscher C, Bohnert M, Becker T et al. 2018. Vps39 interacts with Tom40 to establish one of two functionally distinct vacuole-mitochondria contact sites. Dev. Cell 45:621–36.e7. https://doi.org/10.1016/j.devcel.2018.05.011
    [Crossref] [Google Scholar]
  42. Grimm J, Shi H, Wang W, Mitchell AM, Wingreen NS et al. 2020. The inner membrane protein YhdP modulates the rate of anterograde phospholipid flow in Escherichia coli. PNAS 117:26907–14. https://doi.org/10.1073/pnas.2015556117
    [Crossref] [Google Scholar]
  43. Guardia CM, Tan X-F, Lian T, Rana MS, Zhou W et al. 2020. Structure of human ATG9A, the only transmembrane protein of the core autophagy machinery. Cell Rep. 31:107837 https://doi.org/10.1016/j.celrep.2020.107837
    [Crossref] [Google Scholar]
  44. Gueneau L, Fish RJ, Shamseldin HE, Voisin N, Mau-Them FT et al. 2018. KIAA1109 variants are associated with a severe disorder of brain development and arthrogryposis. Am. J. Hum. Genet. 102:116–32. https://doi.org/10.1016/j.ajhg.2017.12.002
    [Crossref] [Google Scholar]
  45. Guillén-Samander A, De Camilli P. 2023. Endoplasmic reticulum membrane contact sites, lipid transport, and neurodegeneration. Cold Spring Harb. Perspect. Biol. 15:a041257 https://doi.org/10.1101/cshperspect.a041257
    [Crossref] [Google Scholar]
  46. Guillén-Samander A, Leonzino M, Hanna MG IV, Tang N, Shen H, De Camilli P 2021. VPS13D bridges the ER to mitochondria and peroxisomes via Miro. J. Cell Biol. 220:e202010004 https://doi.org/10.1083/jcb.202010004
    [Crossref] [Google Scholar]
  47. Guillén-Samander A, Wu Y, Pineda SS, García FJ, Eisen JN et al. 2022. A partnership between the lipid scramblase XK and the lipid transfer protein VPS13A at the plasma membrane. PNAS 119:e2205425119 https://doi.org/10.1073/pnas.2205425119
    [Crossref] [Google Scholar]
  48. Hancock-Cerutti W, Wu Z, Xu P, Yadavalli N, Leonzino M et al. 2022. ER-lysosome lipid transfer protein VPS13C/PARK23 prevents aberrant mtDNA-dependent STING signaling. J. Cell Biol. 221:e202106046 https://doi.org/10.1083/jcb.202106046
    [Crossref] [Google Scholar]
  49. Hanna MG, Suen PH, Wu Y, Reinisch KM, De Camilli P. 2022. SHIP164 is a chorein motif lipid transfer protein that controls endosome-Golgi membrane traffic. J. Cell Biol. 221:e202111018 https://doi.org/10.1083/jcb.202111018
    [Crossref] [Google Scholar]
  50. Ho M, Chelly J, Carter N, Danek A, Crocker P, Monaco AP. 1994. Isolation of the gene for McLeod syndrome that encodes a novel membrane transport protein. Cell 77:869–80. https://doi.org/10.1016/0092-8674(94)90136-8
    [Crossref] [Google Scholar]
  51. Huang W-P, Ho H-C. 2006. Role of microtubule-dependent membrane trafficking in acrosomal biogenesis. Cell Tissue Res 323:495–503. https://doi.org/10.1007/s00441-005-0097-9
    [Crossref] [Google Scholar]
  52. Insolera R, Lőrincz P, Wishnie AJ, Juhász G, Collins CA. 2021. Mitochondrial fission, integrity and completion of mitophagy require separable functions of Vps13D in Drosophila neurons. PLOS Genet 17:e1009731 https://doi.org/10.1371/journal.pgen.1009731
    [Crossref] [Google Scholar]
  53. Jansen IE, Ye H, Heetveld S, Lechler MC, Michels H et al. 2017. Discovery and functional prioritization of Parkinson's disease candidate genes from large-scale whole exome sequencing. Genome Biol 18:22 https://doi.org/10.1186/s13059-017-1147-9
    [Crossref] [Google Scholar]
  54. Jeng EE, Bhadkamkar V, Ibe NU, Gause H, Jiang L et al. 2019. Systematic identification of host cell regulators of Legionella pneumophila pathogenesis using a genome-wide CRISPR screen. Cell Host Microbe 26:551–63.e6. https://doi.org/10.1016/j.chom.2019.08.017
    [Crossref] [Google Scholar]
  55. John Peter AT, Herrmann B, Antunes D, Rapaport D, Dimmer KS, Kornmann B 2017. Vps13-Mcp1 interact at vacuole-mitochondria interfaces and bypass ER-mitochondria contact sites. J. Cell Biol. 216:3219–29. https://doi.org/10.1083/jcb.201610055
    [Crossref] [Google Scholar]
  56. John Peter AT, Petrungaro C, Peter M, Kornmann B 2022a. METALIC reveals interorganelle lipid flux in live cells by enzymatic mass tagging. Nat. Cell Biol. 24:996–1004. https://doi.org/10.1038/s41556-022-00917-9
    [Crossref] [Google Scholar]
  57. John Peter AT, van Schie SNS, Cheung NJ, Michel AH, Peter M, Kornmann B 2022b. Rewiring phospholipid biosynthesis reveals resilience to membrane perturbations and uncovers regulators of lipid homeostasis. EMBO J 41:e109998 https://doi.org/10.15252/embj.2021109998
    [Crossref] [Google Scholar]
  58. Jumper J, Evans R, Pritzel A, Green T, Figurnov M et al. 2021. Highly accurate protein structure prediction with AlphaFold. Nature 596:583–89. https://doi.org/10.1038/s41586-021-03819-2
    [Crossref] [Google Scholar]
  59. Jung HH, Danek A, Walker RH. 2011. Neuroacanthocytosis syndromes. Orphanet J. Rare. Dis. 6:68 https://doi.org/10.1186/1750-1172-6-68
    [Crossref] [Google Scholar]
  60. Kaiser SE, Brickner JH, Reilein AR, Fenn TD, Walter P, Brunger AT. 2005. Structural basis of FFAT motif-mediated ER targeting. Structure 13:1035–45. https://doi.org/10.1016/j.str.2005.04.010
    [Crossref] [Google Scholar]
  61. Koh K, Ishiura H, Shimazaki H, Tsutsumiuchi M, Ichinose Y et al. 2020. VPS13D-related disorders presenting as a pure and complicated form of hereditary spastic paraplegia. Mol. Genet. Genom. Med. 8:e1108 https://doi.org/10.1002/mgg3.1108
    [Crossref] [Google Scholar]
  62. Koizumi K, Gallagher KL. 2013. Identification of SHRUBBY, a SHORT-ROOT and SCARECROW interacting protein that controls root growth and radial patterning. Development 140:1292–300. https://doi.org/10.1242/dev.090761
    [Crossref] [Google Scholar]
  63. Kolehmainen J, Black GCM, Saarinen A, Chandler K, Clayton-Smith J et al. 2003. Cohen syndrome is caused by mutations in a novel gene, COH1, encoding a transmembrane protein with a presumed role in vesicle-mediated sorting and intracellular protein transport. Am. J. Hum. Genet. 72:1359–69. https://doi.org/10.1086/375454
    [Crossref] [Google Scholar]
  64. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J et al. 2009. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325:477–81. https://doi.org/10.1126/science.1175088
    [Crossref] [Google Scholar]
  65. Kotani T, Kirisako H, Koizumi M, Ohsumi Y, Nakatogawa H. 2018. The Atg2-Atg18 complex tethers pre-autophagosomal membranes to the endoplasmic reticulum for autophagosome formation. PNAS 115:10363–68. https://doi.org/10.1073/pnas.1806727115
    [Crossref] [Google Scholar]
  66. Kumar N, Leonzino M, Hancock-Cerutti W, Horenkamp FA, Li P et al. 2018. VPS13A and VPS13C are lipid transport proteins differentially localized at ER contact sites. J. Cell Biol. 217:3625–39. https://doi.org/10.1083/jcb.201807019
    [Crossref] [Google Scholar]
  67. Lang AB, Peter ATJ, Walter P, Kornmann B. 2015. ER-mitochondrial junctions can be bypassed by dominant mutations in the endosomal protein Vps13. J. Cell Biol. 210:883–90. https://doi.org/10.1083/jcb.201502105
    [Crossref] [Google Scholar]
  68. Lee JS, Yoo T, Lee M, Lee Y, Jeon E et al. 2020. Genetic heterogeneity in Leigh syndrome: highlighting treatable and novel genetic causes. Clin. Genet. 97:586–94. https://doi.org/10.1111/cge.13713
    [Crossref] [Google Scholar]
  69. Lees JA, Reinisch KM. 2020. Inter-organelle lipid transfer: a channel model for Vps13 and chorein-N motif proteins. Curr. Opin. Cell Biol. 65:66–71. https://doi.org/10.1016/j.ceb.2020.02.008
    [Crossref] [Google Scholar]
  70. Leonzino M, Reinisch KM, De Camilli P. 2021. Insights into VPS13 properties and function reveal a new mechanism of eukaryotic lipid transport. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1866:159003 https://doi.org/10.1016/j.bbalip.2021.159003
    [Crossref] [Google Scholar]
  71. Lesage S, Drouet V, Majounie E, Deramecourt V, Jacoupy M et al. 2016. Loss of VPS13C function in autosomal-recessive parkinsonism causes mitochondrial dysfunction and increases PINK1/Parkin-dependent mitophagy. Am. J. Hum. Genet. 98:500–13. https://doi.org/10.1016/j.ajhg.2016.01.014
    [Crossref] [Google Scholar]
  72. Levine TP. 2019. Remote homology searches identify bacterial homologues of eukaryotic lipid transfer proteins, including Chorein-N domains in TamB and AsmA and Mdm31p. BMC Mol. Cell Biol. 20:43 https://doi.org/10.1186/s12860-019-0226-z
    [Crossref] [Google Scholar]
  73. Levine TP. 2022. Sequence analysis and structural predictions of lipid transfer bridges in the repeating beta groove (RBG) superfamily reveal past and present domain variations affecting form, function and interactions of VPS13, ATG2, SHIP164, Hobbit and Tweek. Contact 5: https://doi.org/10.1177/25152564221134328
    [Crossref] [Google Scholar]
  74. Levin-Konigsberg R, Grinstein S. 2020. Phagosome-endoplasmic reticulum contacts: kissing and not running. Traffic 21:172–80. https://doi.org/10.1111/tra.12708
    [Crossref] [Google Scholar]
  75. Li P, Lees JA, Lusk CP, Reinisch KM. 2020. Cryo-EM reconstruction of a VPS13 fragment reveals a long groove to channel lipids between membranes. J. Cell Biol. 219:e202001161 https://doi.org/10.1083/jcb.202001161
    [Crossref] [Google Scholar]
  76. Li YE, Wang Y, Du X, Zhang T, Mak HY et al. 2021. TMEM41B and VMP1 are scramblases and regulate the distribution of cholesterol and phosphatidylserine. J. Cell Biol. 220:e202103105 https://doi.org/10.1083/jcb.202103105
    [Crossref] [Google Scholar]
  77. Maeda S, Otomo C, Otomo T. 2019. The autophagic membrane tether ATG2A transfers lipids between membranes. eLife 8:e45777 https://doi.org/10.7554/eLife.45777
    [Crossref] [Google Scholar]
  78. Maeda S, Yamamoto H, Kinch LN, Garza CM, Takahashi S et al. 2020. Structure, lipid scrambling activity and role in autophagosome formation of ATG9A. Nat. Struct. Mol. Biol. 27:1194–201. https://doi.org/10.1038/s41594-020-00520-2
    [Crossref] [Google Scholar]
  79. Mailler E, Guardia CM, Bai X, Jarnik M, Williamson CD et al. 2021. The autophagy protein ATG9A enables lipid mobilization from lipid droplets. Nat. Commun. 12:6750 https://doi.org/10.1038/s41467-021-26999-x
    [Crossref] [Google Scholar]
  80. Matoba K, Kotani T, Tsutsumi A, Tsuji T, Mori T et al. 2020. Atg9 is a lipid scramblase that mediates autophagosomal membrane expansion. Nat. Struct. Mol. Biol. 27:1185–93. https://doi.org/10.1038/s41594-020-00518-w
    [Crossref] [Google Scholar]
  81. McKay RM, McKay JP, Avery L, Graff JM. 2003. C. elegans: a model for exploring the genetics of fat storage. Dev. Cell 4:131–42. https://doi.org/10.1016/S1534-5807(02)00411-2
    [Crossref] [Google Scholar]
  82. Melia TJ, Lystad AH, Simonsen A. 2020. Autophagosome biogenesis: from membrane growth to closure. J. Cell Biol. 219:e202002085 https://doi.org/10.1083/jcb.202002085
    [Crossref] [Google Scholar]
  83. Melia TJ, Reinisch KM. 2022. A possible role for VPS13-family proteins in bulk lipid transfer, membrane expansion and organelle biogenesis. J. Cell Sci. 135:jcs259357 https://doi.org/10.1242/jcs.259357
    [Crossref] [Google Scholar]
  84. Menon AK, Stevens VL. 1992. Phosphatidylethanolamine is the donor of the ethanolamine residue linking a glycosylphosphatidylinositol anchor to protein. J. Biol. Chem. 267:15277–80. https://doi.org/10.1016/S0021-9258(19)49529-X
    [Crossref] [Google Scholar]
  85. Mesmin B, Bigay J, Moser von Filseck J, Lacas-Gervais S, Drin G, Antonny B. 2013. A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER-Golgi tether OSBP. Cell 155:830–43. https://doi.org/10.1016/j.cell.2013.09.056
    [Crossref] [Google Scholar]
  86. Moretti F, Bergman P, Dodgson S, Marcellin D, Claerr I et al. 2018. TMEM41B is a novel regulator of autophagy and lipid mobilization. EMBO Rep 19:e45889 https://doi.org/10.15252/embr.201845889
    [Crossref] [Google Scholar]
  87. Morita K, Hama Y, Izume T, Tamura N, Ueno T et al. 2018. Genome-wide CRISPR screen identifies TMEM41B as a gene required for autophagosome formation. J. Cell Biol. 217:3817–28. https://doi.org/10.1083/jcb.201804132
    [Crossref] [Google Scholar]
  88. Mulder E, Van Deenen LLM. 1965. Metabolism of red-cell lipids: III. Pathways for phospholipid renewal. Biochim. Biophys. Acta Lipids Lipid Metab. 106:348–56. https://doi.org/10.1016/0005-2760(65)90043-3
    [Crossref] [Google Scholar]
  89. Muñoz-Braceras S, Calvo R, Escalante R. 2015. TipC and the chorea-acanthocytosis protein VPS13A regulate autophagy in Dictyostelium and human HeLa cells. Autophagy 11:918–27. https://doi.org/10.1080/15548627.2015.1034413
    [Crossref] [Google Scholar]
  90. Murphy SE, Levine TP. 2016. VAP, a versatile access point for the endoplasmic reticulum: review and analysis of FFAT-like motifs in the VAPome. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1861:952–61. https://doi.org/10.1016/j.bbalip.2016.02.009
    [Crossref] [Google Scholar]
  91. Nagata O, Nakamura M, Sakimoto H, Urata Y, Sasaki N et al. 2018. Mouse model of chorea-acanthocytosis exhibits male infertility caused by impaired sperm motility as a result of ultrastructural morphological abnormalities in the mitochondrial sheath in the sperm midpiece. Biochem. Biophys. Res. Commun. 503:915–20. https://doi.org/10.1016/j.bbrc.2018.06.096
    [Crossref] [Google Scholar]
  92. Nagata S, Suzuki J, Segawa K, Fujii T. 2016. Exposure of phosphatidylserine on the cell surface. Cell Death Differ 23:952–61. https://doi.org/10.1038/cdd.2016.7
    [Crossref] [Google Scholar]
  93. Nakamura TS, Suda Y, Muneshige K, Fujieda Y, Okumura Y et al. 2021. Suppression of Vps13 adaptor protein mutants reveals a central role for PI4P in regulating prospore membrane extension. PLOS Genet 17:e1009727 https://doi.org/10.1371/journal.pgen.1009727
    [Crossref] [Google Scholar]
  94. Neuman SD, Bashirullah A. 2018. Hobbit regulates intracellular trafficking to drive insulin-dependent growth during Drosophila development. Development 145:dev161356 https://doi.org/10.1242/dev.161356
    [Crossref] [Google Scholar]
  95. Neuman SD, Jorgensen JR, Cavanagh AT, Smyth JT, Selegue JE et al. 2021. The Hob proteins are novel and conserved lipid-binding proteins at ER-PM contact sites. J. Cell Sci. 135:jcs259086 https://doi.org/10.1242/jcs.259086
    [Crossref] [Google Scholar]
  96. Neuman SD, Levine TP, Bashirullah A. 2022. A novel superfamily of bridge-like lipid transfer proteins. Trends Cell Biol 32:962–74. https://doi.org/10.1016/j.tcb.2022.03.011
    [Crossref] [Google Scholar]
  97. Noda NN. 2021. Atg2 and Atg9: intermembrane and interleaflet lipid transporters driving autophagy. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1866:158956 https://doi.org/10.1016/j.bbalip.2021.158956
    [Crossref] [Google Scholar]
  98. Obara K, Sekito T, Niimi K, Ohsumi Y. 2008. The Atg18-Atg2 complex is recruited to autophagic membranes via phosphatidylinositol 3-phosphate and exerts an essential function. J. Biol. Chem. 283:23972–80. https://doi.org/10.1074/jbc.M803180200
    [Crossref] [Google Scholar]
  99. Okumura Y, Nakamura TS, Tanaka T, Inoue I, Suda Y et al. 2015. The dysferlin domain-only protein, Spo73, is required for prospore membrane extension in Saccharomyces cerevisiae. mSphere 1:e00038-15. https://doi.org/10.1128/mSphere.00038-15
    [Crossref] [Google Scholar]
  100. Olivas TJ, Wu Y, Yu S, Luan L, Choi P et al. 2022. ATG9 vesicles comprise the seed membrane of mammalian autophagosomes. bioRxiv 2022.08.16.504143. https://doi.org/10.1101/2022.08.16.504143
    [Crossref]
  101. Osawa T, Kotani T, Kawaoka T, Hirata E, Suzuki K et al. 2019. Atg2 mediates direct lipid transfer between membranes for autophagosome formation. Nat. Struct. Mol. Biol. 26:281–88. https://doi.org/10.1038/s41594-019-0203-4
    [Crossref] [Google Scholar]
  102. Otto GP, Razi M, Morvan J, Stenner F, Tooze SA. 2010. A novel syntaxin 6-interacting protein, SHIP164, regulates syntaxin 6-dependent sorting from early endosomes. Traffic 11:688–705. https://doi.org/10.1111/j.1600-0854.2010.01049.x
    [Crossref] [Google Scholar]
  103. Palade G. 1975. Intracellular aspects of the process of protein synthesis. Science 189:347–58. https://doi.org/10.1126/science.1096303
    [Crossref] [Google Scholar]
  104. Park J-S, Hu Y, Hollingsworth NM, Miltenberger-Miltenyi G, Neiman AM. 2022. Interaction between VPS13A and the XK scramblase is important for VPS13A function in humans. J. Cell Sci. 135:jcs260227 https://doi.org/10.1242/jcs.260227
    [Crossref] [Google Scholar]
  105. Park J-S, Neiman AM. 2012. VPS13 regulates membrane morphogenesis during sporulation in Saccharomyces cerevisiae. J. Cell Sci. 125:3004–11. https://doi.org/10.1242/jcs.105114
    [Crossref] [Google Scholar]
  106. Park J-S, Neiman AM. 2020. XK is a partner for VPS13A: a molecular link between Chorea-Acanthocytosis and McLeod Syndrome. Mol. Biol. Cell 31:2425–36. https://doi.org/10.1091/mbc.E19-08-0439-T
    [Crossref] [Google Scholar]
  107. Park J-S, Okumura Y, Tachikawa H, Neiman AM. 2013. SPO71 encodes a developmental stage-specific partner for Vps13 in Saccharomyces cerevisiae. Eukaryot. Cell 12:1530–37. https://doi.org/10.1128/EC.00239-13
    [Crossref] [Google Scholar]
  108. Park J-S, Thorsness MK, Policastro R, McGoldrick LL, Hollingsworth NM et al. 2016. Yeast Vps13 promotes mitochondrial function and is localized at membrane contact sites. Mol. Biol. Cell 27:2435–49. https://doi.org/10.1091/mbc.E16-02-0112
    [Crossref] [Google Scholar]
  109. Prinz WA, Toulmay A, Balla T. 2020. The functional universe of membrane contact sites. Nat. Rev. Mol. Cell Biol. 21:7–24. https://doi.org/10.1038/s41580-019-0180-9
    [Crossref] [Google Scholar]
  110. Procissi A, Guyon A, Pierson ES, Giritch A, Knuiman B et al. 2003. KINKY POLLEN encodes a SABRE-like protein required for tip growth in Arabidopsis and conserved among eukaryotes. Plant J 36:894–904. https://doi.org/10.1046/j.1365-313X.2003.01933.x
    [Crossref] [Google Scholar]
  111. Rampoldi L, Dobson-Stone C, Rubio JP, Danek A, Chalmers RM et al. 2001. A conserved sorting-associated protein is mutant in chorea-acanthocytosis. Nat. Genet 28:119–20. https://doi.org/10.1038/88821
    [Crossref] [Google Scholar]
  112. Ramseyer VD, Kimler VA, Granneman JG. 2018. Vacuolar protein sorting 13C is a novel lipid droplet protein that inhibits lipolysis in brown adipocytes. Mol. Metab. 7:57–70. https://doi.org/10.1016/j.molmet.2017.10.014
    [Crossref] [Google Scholar]
  113. Reinisch KM, Prinz WA. 2021. Mechanisms of nonvesicular lipid transport. J. Cell Biol. 220:e202012058 https://doi.org/10.1083/jcb.202012058
    [Crossref] [Google Scholar]
  114. Roczniak-Ferguson A, Petit CS, Froehlich F, Qian S, Ky J et al. 2012. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci. Signal. 5:ra42 https://doi.org/10.1126/scisignal.2002790
    [Crossref] [Google Scholar]
  115. Ropolo A, Grasso D, Pardo R, Sacchetti ML, Archange C et al. 2007. The pancreatitis-induced vacuole membrane protein 1 triggers autophagy in mammalian cells. J. Biol. Chem. 282:37124–33. https://doi.org/10.1074/jbc.M706956200
    [Crossref] [Google Scholar]
  116. Rothman JH, Stevens TH. 1986. Protein sorting in yeast: Mutants defective in vacuole biogenesis mislocalize vacuolar proteins into the late secretory pathway. Cell 47:1041–51. https://doi.org/10.1016/0092-8674(86)90819-6
    [Crossref] [Google Scholar]
  117. Ruiz N, Davis RM, Kumar S. 2021. YhdP, TamB, and YdbH are redundant but essential for growth and lipid homeostasis of the gram-negative outer membrane. mBio 12:e02714-21. https://doi.org/10.1128/mBio.02714-21
    [Crossref] [Google Scholar]
  118. Ryoden Y, Segawa K, Nagata S. 2022. Requirement of Xk and Vps13a for the P2X7-mediated phospholipid scrambling and cell lysis in mouse T cells. PNAS 119:e2119286119 https://doi.org/10.1073/pnas.2119286119
    [Crossref] [Google Scholar]
  119. Saheki Y, De Camilli P. 2017. Endoplasmic reticulum-plasma membrane contact sites. Annu. Rev. Biochem. 86:659–84. https://doi.org/10.1146/annurev-biochem-061516-044932
    [Crossref] [Google Scholar]
  120. Sakimoto H, Nakamura M, Nagata O, Yokoyama I, Sano A. 2016. Phenotypic abnormalities in a chorea-acanthocytosis mouse model are modulated by strain background. Biochem. Biophys. Res. Commun. 472:118–24. https://doi.org/10.1016/j.bbrc.2016.02.077
    [Crossref] [Google Scholar]
  121. Sawa-Makarska J, Baumann V, Coudevylle N, von Bülow S, Nogellova V et al. 2020. Reconstitution of autophagosome nucleation defines Atg9 vesicles as seeds for membrane formation. Science 369:eaaz7714 https://doi.org/10.1126/science.aaz7714
    [Crossref] [Google Scholar]
  122. Schormair B, Kemlink D, Mollenhauer B, Fiala O, Machetanz G et al. 2018. Diagnostic exome sequencing in early-onset Parkinson's disease confirms VPS13C as a rare cause of autosomal-recessive Parkinson's disease. Clin. Genet. 93:603–12. https://doi.org/10.1111/cge.13124
    [Crossref] [Google Scholar]
  123. Schütter M, Giavalisco P, Brodesser S, Graef M. 2020. Local fatty acid channeling into phospholipid synthesis drives phagophore expansion during autophagy. Cell 180:135–49.e14. https://doi.org/10.1016/j.cell.2019.12.005
    [Crossref] [Google Scholar]
  124. Scott-Hewitt N, Perrucci F, Morini R, Erreni M, Mahoney M et al. 2020. Local externalization of phosphatidylserine mediates developmental synaptic pruning by microglia. EMBO J 39:e105380 https://doi.org/10.15252/embj.2020105380
    [Crossref] [Google Scholar]
  125. Segawa K, Nagata S. 2015. An apoptotic ‘eat me’ signal: phosphatidylserine exposure. Trends Cell Biol 25:639–50. https://doi.org/10.1016/j.tcb.2015.08.003
    [Crossref] [Google Scholar]
  126. Seifert W, Kühnisch J, Maritzen T, Horn D, Haucke V, Hennies HC. 2011. Cohen syndrome-associated protein, COH1, is a novel, giant Golgi matrix protein required for Golgi integrity. J. Biol. Chem. 286:37665–75. https://doi.org/10.1074/jbc.M111.267971
    [Crossref] [Google Scholar]
  127. Seifert W, Kühnisch J, Maritzen T, Lommatzsch S, Hennies HC et al. 2015. Cohen syndrome-associated protein COH1 physically and functionally interacts with the small GTPase RAB6 at the Golgi complex and directs neurite outgrowth. J. Biol. Chem. 290:3349–58. https://doi.org/10.1074/jbc.M114.608174
    [Crossref] [Google Scholar]
  128. Seong E, Insolera R, Dulovic M, Kamsteeg E-J, Trinh J et al. 2018. Mutations in VPS13D lead to a new recessive ataxia with spasticity and mitochondrial defects. Ann. Neurol. 83:1075–88. https://doi.org/10.1002/ana.25220
    [Crossref] [Google Scholar]
  129. Sheetz MP, Singer SJ. 1974. Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. PNAS 71:4457–61. https://doi.org/10.1073/pnas.71.11.4457
    [Crossref] [Google Scholar]
  130. Shen JL, Fortier TM, Zhao YG, Wang R, Burmeister M, Baehrecke EH. 2021. Vmp1, Vps13D, and Marf/Mfn2 function in a conserved pathway to regulate mitochondria and ER contact in development and disease. Curr. Biol. 31:3028–39.e7. https://doi.org/10.1016/j.cub.2021.04.062
    [Crossref] [Google Scholar]
  131. Sherman DJ, Xie R, Taylor RJ, George AH, Okuda S et al. 2018. Lipopolysaccharide is transported to the cell surface by a membrane-to-membrane protein bridge. Science 359:798–801. https://doi.org/10.1126/science.aar1886
    [Crossref] [Google Scholar]
  132. Shoemaker CJ, Huang TQ, Weir NR, Polyakov NJ, Schultz SW, Denic V. 2019. CRISPR screening using an expanded toolkit of autophagy reporters identifies TMEM41B as a novel autophagy factor. PLOS Biol 17:e2007044 https://doi.org/10.1371/journal.pbio.2007044
    [Crossref] [Google Scholar]
  133. Subra M, Dezi M, Bigay J, Lacas-Gervais S, Di Cicco A et al. 2023. VAP-A intrinsically disordered regions enable versatile tethering at membrane contact sites. Dev. Cell 58:121–38.e9. https://doi.org/10.1016/j.devcel.2022.12.010
    [Crossref] [Google Scholar]
  134. Suzuki H, Osawa T, Fujioka Y, Noda NN. 2017. Structural biology of the core autophagy machinery. Curr. Opin. Struct. Biol. 43:10–17. https://doi.org/10.1016/j.sbi.2016.09.010
    [Crossref] [Google Scholar]
  135. Swanson MS, Isberg RR. 1995. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63:3609–20. https://doi.org/10.1128/iai.63.9.3609-3620.1995
    [Crossref] [Google Scholar]
  136. Tábara L-C, Escalante R. 2016. VMP1 establishes ER-microdomains that regulate membrane contact sites and autophagy. PLOS ONE 11:e0166499 https://doi.org/10.1371/journal.pone.0166499
    [Crossref] [Google Scholar]
  137. Tamura N, Nishimura T, Sakamaki Y, Koyama-Honda I, Yamamoto H, Mizushima N. 2017. Differential requirement for ATG2A domains for localization to autophagic membranes and lipid droplets. FEBS Lett 591:3819–30. https://doi.org/10.1002/1873-3468.12901
    [Crossref] [Google Scholar]
  138. Tan JX, Finkel T. 2022. A phosphoinositide signalling pathway mediates rapid lysosomal repair. Nature 609:815–21. https://doi.org/10.1038/s41586-022-05164-4
    [Crossref] [Google Scholar]
  139. Tangpranomkorn S, Igarashi M, Ishizuna F, Kato Y, Suzuki T, Fujii S, Takayama S. 2022. A land plant specific VPS13 mediates polarized vesicle trafficking in germinating pollen. bioRxiv 2022.11.01.514778. https://doi.org/10.1101/2022.11.01.514778
    [Crossref]
  140. Tatzer V, Zellnig G, Kohlwein SD, Schneiter R. 2002. Lipid-dependent subcellular relocalization of the acyl chain desaturase in yeast. Mol. Biol. Cell 13:4429–42. https://doi.org/10.1091/mbc.e02-04-0196
    [Crossref] [Google Scholar]
  141. Tokai M, Kawasaki H, Kikuchi Y, Ouchi K. 2000. Cloning and characterization of the CSF1 gene of Saccharomyces cerevisiae, which is required for nutrient uptake at low temperature. J. Bacteriol. 182:2865–68. https://doi.org/10.1128/JB.182.10.2865-2868.2000
    [Crossref] [Google Scholar]
  142. Tornero-Écija A, Zapata-del-Baño A, Antón-Esteban L, Vincent O, Escalante R. 2023. The association of lipid transfer protein VPS13A with endosomes is mediated by sorting nexin SNX5. Life Sci. Alliance 6:e202201852 https://doi.org/10.26508/lsa.202201852 .
    [Crossref] [Google Scholar]
  143. Toulmay A, Whittle FB, Yang J, Bai X, Diarra J et al. 2022. Vps13-like proteins provide phosphatidylethanolamine for GPI anchor synthesis in the ER. J. Cell Biol. 221:e202111095 https://doi.org/10.1083/jcb.202111095
    [Crossref] [Google Scholar]
  144. Tsukada M, Ohsumi Y. 1993. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333:169–74. https://doi.org/10.1016/0014-5793(93)80398-E
    [Crossref] [Google Scholar]
  145. Tung TT, Nagaosa K, Fujita Y, Kita A, Mori H et al. 2013. Phosphatidylserine recognition and induction of apoptotic cell clearance by Drosophila engulfment receptor Draper. J. Biochem. 153:483–91. https://doi.org/10.1093/jb/mvt014
    [Crossref] [Google Scholar]
  146. Ueno S, Maruki Y, Nakamura M, Tomemori Y, Kamae K et al. 2001. The gene encoding a newly discovered protein, chorein, is mutated in chorea-acanthocytosis. Nat. Genet. 28:121–22. https://doi.org/10.1038/88825
    [Crossref] [Google Scholar]
  147. Ugur B, Hancock-Cerutti W, Leonzino M, De Camilli P. 2020. Role of VPS13, a protein with similarity to ATG2, in physiology and disease. Curr. Opin. Genet. Dev. 65:61–68. https://doi.org/10.1016/j.gde.2020.05.027
    [Crossref] [Google Scholar]
  148. Urata Y, Nakamura M, Sasaki N, Shiokawa N, Nishida Y et al. 2019. Novel pathogenic XK mutations in McLeod syndrome and interaction between XK protein and chorein. Neurol. Genet. 5:e328 https://doi.org/10.1212/NXG.0000000000000328
    [Crossref] [Google Scholar]
  149. Vaccaro MI, Ropolo A, Grasso D, Iovanna JL. 2008. A novel mammalian trans-membrane protein reveals an alternative initiation pathway for autophagy. Autophagy 4:388–90. https://doi.org/10.4161/auto.5656
    [Crossref] [Google Scholar]
  150. Valverde DP, Yu S, Boggavarapu V, Kumar N, Lees JA et al. 2019. ATG2 transports lipids to promote autophagosome biogenesis. J. Cell Biol. 14:jcb.201811139 https://doi.org/10.1083/jcb.201811139
    [Crossref] [Google Scholar]
  151. van Vliet AR, Chiduza GN, Maslen SL, Pye VE, Joshi D et al. 2022. ATG9A and ATG2A form a heteromeric complex essential for autophagosome formation. Mol. Cell 82:4324–39.e8. https://doi.org/10.1016/j.molcel.2022.10.017
    [Crossref] [Google Scholar]
  152. Vance JE. 1990. Phospholipid synthesis in a membrane fraction associated with mitochondria. J. Biol. Chem. 265:7248–56. https://doi.org/10.1016/S0021-9258(19)39106-9
    [Crossref] [Google Scholar]
  153. Velayos-Baeza A, Vettori A, Copley RR, Dobson-Stone C, Monaco AP. 2004. Analysis of the human VPS13 gene family. Genomics 84:536–49. https://doi.org/10.1016/j.ygeno.2004.04.012
    [Crossref] [Google Scholar]
  154. Velikkakath AKG, Nishimura T, Oita E, Ishihara N, Mizushima N. 2012. Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Mol. Biol. Cell 23:896–909. https://doi.org/10.1091/mbc.e11-09-0785
    [Crossref] [Google Scholar]
  155. Verstreken P, Ohyama T, Haueter C, Habets RLP, Lin YQ et al. 2009. Tweek, an evolutionarily conserved protein, is required for synaptic vesicle recycling. Neuron 63:203–15. https://doi.org/10.1016/j.neuron.2009.06.017
    [Crossref] [Google Scholar]
  156. Vidyadhara DJ, Lee JE, Chandra SS. 2019. Role of the endolysosomal system in Parkinson's disease. J. Neurochem. 150:487–506. https://doi.org/10.1111/jnc.14820
    [Crossref] [Google Scholar]
  157. Vonk JJ, Yeshaw WM, Pinto F, Faber AIE, Lahaye LL et al. 2017. Drosophila Vps13 is required for protein homeostasis in the brain. PLOS ONE 12:e0170106 https://doi.org/10.1371/journal.pone.0170106
    [Crossref] [Google Scholar]
  158. Wang C, Wang B, Pandey T, Long Y, Zhang J et al. 2022. A conserved megaprotein-based molecular bridge critical for lipid trafficking and cold resilience. Nat. Commun. 13:6805 https://doi.org/10.1038/s41467-022-34450-y
    [Crossref] [Google Scholar]
  159. Wang C-W, Kim J, Huang W-P, Abeliovich H, Stromhaug PE et al. 2001. Apg2 is a novel protein required for the cytoplasm to vacuole targeting, autophagy, and pexophagy pathways. J. Biol. Chem. 276:30442–51. https://doi.org/10.1074/jbc.M102342200
    [Crossref] [Google Scholar]
  160. Wang J, Chu Q, Chang W, Deng L, Ji W-K. 2022. A complex containing RhoBTB3-SHIP164-Vps26B promotes the biogenesis of early endosome buds at Golgi-endosome contacts. bioRxiv 2022.09.30.510409. https://doi.org/10.1101/2022.09.30.510409
    [Crossref]
  161. Wang J, Fang N, Xiong J, Du Y, Cao Y, Ji W-K. 2021. An ESCRT-dependent step in fatty acid transfer from lipid droplets to mitochondria through VPS13D−TSG101 interactions. Nat. Commun. 12:1252 https://doi.org/10.1038/s41467-021-21525-5
    [Crossref] [Google Scholar]
  162. Wang R, Miao G, Shen JL, Fortier TM, Baehrecke EH. 2022. ESCRT dysfunction compromises endoplasmic reticulum maturation and autophagosome biogenesis in Drosophila. Curr. Biol. 32:1262–74.e4. https://doi.org/10.1016/j.cub.2022.01.040
    [Crossref] [Google Scholar]
  163. Wang T, Birsoy K, Hughes NW, Krupczak KM, Post Y et al. 2015. Identification and characterization of essential genes in the human genome. Science 350:1096–101. https://doi.org/10.1126/science.aac7041
    [Crossref] [Google Scholar]
  164. Wideman JG, Gawryluk RMR, Gray MW, Dacks JB. 2013. The ancient and widespread nature of the ER-mitochondria encounter structure. Mol. Biol. Evol. 30:2044–49. https://doi.org/10.1093/molbev/mst120
    [Crossref] [Google Scholar]
  165. Wirtz KWA. 1991. Phospholipid transfer proteins: from lipid monolayers to cells. Klin. Wochenschr. 69:105–11. https://doi.org/10.1007/BF01795953
    [Crossref] [Google Scholar]
  166. Wong LH, Gatta AT, Levine TP. 2019. Lipid transfer proteins: the lipid commute via shuttles, bridges and tubes. Nat. Rev. Mol. Cell Biol. 20:85–101. https://doi.org/10.1038/s41580-018-0071-5
    [Crossref] [Google Scholar]
  167. Wozny MR, Di Luca A, Morado DR, Picco A, Khaddaj R et al. 2023. In situ architecture of the ER–mitochondria encounter structure. Nature 618:188–92. https://doi.org/10.1038/s41586-023-06050-3
    [Crossref] [Google Scholar]
  168. Xu Z, Dooner HK. 2006. The maize aberrant pollen transmission 1 gene is a SABRE/KIP homolog required for pollen tube growth. Genetics 172:1251–61. https://doi.org/10.1534/genetics.105.050237
    [Crossref] [Google Scholar]
  169. Yang J, Anishchenko I, Park H, Peng Z, Ovchinnikov S, Baker D. 2020. Improved protein structure prediction using predicted interresidue orientations. PNAS 117:1496–503. https://doi.org/10.1073/pnas.1914677117
    [Crossref] [Google Scholar]
  170. Yeshaw WM, van der Zwaag M, Pinto F, Lahaye LL, Faber AI et al. 2019. Human VPS13A is associated with multiple organelles and influences mitochondrial morphology and lipid droplet motility. eLife 8:e43561 https://doi.org/10.7554/eLife.43561
    [Crossref] [Google Scholar]
  171. Yuan W, Akşit A, de Boer R, Krikken AM, van der Klei IJ. 2022. Yeast Vps13 is crucial for peroxisome expansion in cells with reduced peroxisome-ER contact sites. Front. Cell Dev. Biol. 10: https://doi.org/10.3389/fcell.2022.842285
    [Crossref] [Google Scholar]
  172. Zhang Y, Ge J, Bian X, Kumar A. 2022. Quantitative models of lipid transfer and membrane contact formation. Contact 5:25152564221096024 https://doi.org/10.1177/25152564221096024
    [Crossref] [Google Scholar]
  173. Zhang Y, Wang H, Kage-Nakadai E, Mitani S, Wang X. 2012. C.elegans secreted lipid-binding protein NRF-5 mediates PS appearance on phagocytes for cell corpse engulfment. Curr. Biol. 22:1276–84. https://doi.org/10.1016/j.cub.2012.06.004
    [Crossref] [Google Scholar]
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