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Molecular basis for sterol transport by StART‐like lipid transfer domains

Horenkamp, Florian A, Valverde, Diana P, Nunnari, Jodi, Reinisch, Karin M·2018·The EMBO Journal

Abstract

Lipid transport proteins at membrane contact sites, where two organelles are closely apposed, play key roles in trafficking lipids between cellular compartments while distinct membrane compositions for each organelle are maintained. Understanding the mechanisms underlying non-vesicular lipid trafficking requires characterization of the lipid transporters residing at contact sites. Here, we show that the mammalian proteins in the lipid transfer proteins anchored at a membrane contact site (LAM) family, called GRAMD1a-c, transfer sterols with similar efficiency as the yeast orthologues, which have known roles in sterol transport. Moreover, we have determined the structure of a lipid transfer domain of the yeast LAM protein Ysp2p, both in its apo-bound and sterol-bound forms, at 2.0 Å resolution. It folds into a truncated version of the steroidogenic acute regulatory protein-related lipid transfer (StART) domain, resembling a lidded cup in overall shape. Ergosterol binds within the cup, with its 3-hydroxy group interacting with protein indirectly via a water network at the cup bottom. This ligand binding mode likely is conserved for the other LAM proteins and for StART domains transferring sterols.

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Crossref · 10.15252/embj.201798002

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  • GRAMD1s extract accessible plasma membrane cholesterol for transport to the endoplasmic reticulum via the StART-like domain, which can directly capture and transport sterol across the cytoplasm.

    “GRAMD1s then extract accessible PM cholesterol for transport to the ER via the StART‐like domain, which can directly capture and transport sterol across the cytoplasm (Gatta et al, 2018; Horenkamp et al, 2018; Jentsch et al, 2018; Sandhu et al, 2018; Tong et al, 2018; Khelashvili et al, 2019; Naito et al, 2019).”

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Research works printed but not linked: 51

  1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse‐Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) PHENIX: a comprehensive Python‐based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213–221 · DOI · Paper page
  2. Alpy F, Tomasetto C (2014) START ships lipids across interorganelle space. Biochimie 96: 85–95 · DOI
  3. Ashkenazy H, Abadi S, Martz E, Chay O, Mayrose I, Pupko T, Ben‐Tal N (2016) ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucleic Acids Res 44: W344–W350 · DOI · Paper page
  4. Bigay J, Antonny B (2012) Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev Cell 23: 886–895 · DOI
  5. Bose HS, Baldwin MA, Miller WL (2000) Evidence that StAR and MLN64 act on the outer mitochondrial membrane as molten globules. Endocr Res 26: 629–637 · DOI
  6. Budisa N, Steipe B, Demange P, Eckerskorn C, Kellermann J, Huber R (1995) High‐level biosynthetic substitution of methionine in proteins by its analogs 2‐aminohexanoic acid, selenomethionine, telluromethionine and ethionine in Escherichia coli. Eur J Biochem 230: 788–796 · DOI
  7. Chung J, Torta F, Masai K, Lucast L, Czapla H, Tanner LB, Narayanaswamy P, Wenk MR, Nakatsu F, De Camilli P (2015) INTRACELLULAR TRANSPORT. PI4P/phosphatidylserine countertransport at ORP5‐ and ORP8‐mediated ER‐plasma membrane contacts. Science 349: 428–432 · DOI
  8. Clark BJ (2012) The mammalian START domain protein family in lipid transport in health and disease. J Endocrinol 212: 257–275 · DOI
  9. Drin G, Moser von Filseck J, Copic A (2016) New molecular mechanisms of inter‐organelle lipid transport. Biochem Soc Trans 44: 486–492 · DOI
  10. Ejsing CS, Sampaio JL, Surendranath V, Duchoslav E, Ekroos K, Klemm RW, Simons K, Shevchenko A (2009) Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proc Natl Acad Sci USA 106: 2136–2141 · DOI
  11. Elbaz‐Alon Y, Eisenberg‐Bord M, Shinder V, Stiller SB, Shimoni E, Wiedemann N, Geiger T, Schuldiner M (2015) Lam6 regulates the extent of contacts between organelles. Cell Rep 12: 7–14 · DOI
  12. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486–501 · DOI · Paper page
  13. Gatta AT, Wong LH, Sere YY, Calderon‐Norena DM, Cockcroft S, Menon AK, Levine TP (2015) A new family of StART domain proteins at membrane contact sites has a role in ER‐PM sterol transport. Elife 4: e07253 · DOI · Paper page
  14. Ghai R, Du X, Wang H, Dong J, Ferguson C, Brown AJ, Parton RG, Wu JW, Yang H (2017) ORP5 and ORP8 bind phosphatidylinositol‐4, 5‐biphosphate (PtdIns(4,5)P 2) and regulate its level at the plasma membrane. Nat Commun 8: 757 · DOI
  15. Hendrickson WA (1991) Determination of macromolecular structures from anomalous diffraction of synchrotron radiation. Science 254: 51–58 · DOI
  16. Horvath MP, George EW, Tran QT, Baumgardner K, Zharov G, Lee S, Sharifzadeh H, Shihab S, Mattinson T, Li B, Bernstein PS (2016) Structure of the lutein‐binding domain of human StARD3 at 1.74 A resolution and model of a complex with lutein. Acta Crystallogr F Struct Biol Commun 72: 609–618 · DOI
  17. Iaea DB, Dikiy I, Kiburu I, Eliezer D, Maxfield FR (2015) STARD4 membrane interactions and sterol binding. Biochemistry 54: 4623–4636 · DOI
  18. Im YJ, Raychaudhuri S, Prinz WA, Hurley JH (2005) Structural mechanism for sterol sensing and transport by OSBP‐related proteins. Nature 437: 154–158 · DOI
  19. John K, Kubelt J, Muller P, Wustner D, Herrmann A (2002) Rapid transbilayer movement of the fluorescent sterol dehydroergosterol in lipid membranes. Biophys J 83: 1525–1534 · DOI
  20. Kabsch W (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Crystallogr 26: 795–800 · DOI
  21. Kentala H, Weber‐Boyvat M, Olkkonen VM (2016) OSBP‐related protein family: mediators of lipid transport and signaling at membrane contact sites. Int Rev Cell Mol Biol 321: 299–340 · DOI
  22. Koag MC, Cheun Y, Kou Y, Ouzon‐Shubeita H, Min K, Monzingo AF, Lee S (2013) Synthesis and structure of 16,22‐diketocholesterol bound to oxysterol‐binding protein Osh4. Steroids 78: 938–944 · DOI
  23. Kudo N, Kumagai K, Tomishige N, Yamaji T, Wakatsuki S, Nishijima M, Hanada K, Kato R (2008) Structural basis for specific lipid recognition by CERT responsible for nonvesicular trafficking of ceramide. Proc Natl Acad Sci USA 105: 488–493 · DOI
  24. Lahiri S, Toulmay A, Prinz WA (2015) Membrane contact sites, gateways for lipid homeostasis. Curr Opin Cell Biol 33: 82–87 · DOI
  25. Landau M, Mayrose I, Rosenberg Y, Glaser F, Martz E, Pupko T, Ben‐Tal N (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res 33: W299–W302 · DOI
  26. Lavigne P, Najmanivich R, Lehoux JG (2010) Mammalian StAR‐related lipid transfer (START) domains with specificity for cholesterol: structural conservation and mechanism of reversible binding. Subcell Biochem 51: 425–437 · DOI
  27. Lees JA, Messa M, Sun EW, Wheeler H, Torta F, Wenk MR, De Camilli P, Reinisch KM (2017) Lipid transport by TMEM24 at ER‐plasma membrane contacts regulates pulsatile insulin secretion. Science 355: eaah6171 · DOI
  28. Letourneau D, Lefebvre A, Lavigne P, LeHoux JG (2015) The binding site specificity of STARD4 subfamily: breaking the cholesterol paradigm. Mol Cell Endocrinol 408: 53–61 · DOI
  29. Maeda K, Anand K, Chiapparino A, Kumar A, Poletto M, Kaksonen M, Gavin AC (2013) Interactome map uncovers phosphatidylserine transport by oxysterol‐binding proteins. Nature 501: 257–261 · DOI
  30. Mathieu AP, Fleury A, Ducharme L, Lavigne P, LeHoux JG (2002) Insights into steroidogenic acute regulatory protein (StAR)‐dependent cholesterol transfer in mitochondria: evidence from molecular modeling and structure‐based thermodynamics supporting the existence of partially unfolded states of StAR. J Mol Endocrinol 29: 327–345 · DOI · Paper page
  31. Mesmin B, Pipalia NH, Lund FW, Ramlall TF, Sokolov A, Eliezer D, Maxfield FR (2011) STARD4 abundance regulates sterol transport and sensing. Mol Biol Cell 22: 4004–4015 · DOI
  32. Moser von Filseck J, Copic A, Delfosse V, Vanni S, Jackson CL, Bourguet W, Drin G (2015a) INTRACELLULAR TRANSPORT. Phosphatidylserine transport by ORP/Osh proteins is driven by phosphatidylinositol 4‐phosphate. Science 349: 432–436 · DOI
  33. Moser von Filseck J, Vanni S, Mesmin B, Antonny B, Drin G (2015b) A phosphatidylinositol‐4‐phosphate powered exchange mechanism to create a lipid gradient between membranes. Nat Commun 6: 6671 · DOI
  34. Murcia M, Faraldo‐Gomez JD, Maxfield FR, Roux B (2006) Modeling the structure of the StART domains of MLN64 and StAR proteins in complex with cholesterol. J Lipid Res 47: 2614–2630 · DOI · Paper page
  35. Murley A, Sarsam RD, Toulmay A, Yamada J, Prinz WA, Nunnari J (2015) Ltc1 is an ER‐localized sterol transporter and a component of ER‐mitochondria and ER‐vacuole contacts. J Cell Biol 209: 539–548 · DOI
  36. Murley A, Yamada J, Niles BJ, Toulmay A, Prinz WA, Powers T, Nunnari J (2017) Sterol transporters at membrane contact sites regulate TORC1 and TORC2 signaling. J Cell Biol 216: 2697–2689 · DOI
  37. Pei J, Grishin NV (2014) PROMALS3D: multiple protein sequence alignment enhanced with evolutionary and three‐dimensional structural information. Methods Mol Biol 1079: 263–271 · DOI
  38. Raychaudhuri S, Im YJ, Hurley JH, Prinz WA (2006) Nonvesicular sterol movement from plasma membrane to ER requires oxysterol‐binding protein‐related proteins and phosphoinositides. J Cell Biol 173: 107–119 · DOI
  39. Reinisch KM, De Camilli P (2016) SMP‐domain proteins at membrane contact sites: structure and function. Biochim Biophys Acta 1861: 924–927 · DOI
  40. Roderick SL, Chan WW, Agate DS, Olsen LR, Vetting MW, Rajashankar KR, Cohen DE (2002) Structure of human phosphatidylcholine transfer protein in complex with its ligand. Nat Struct Biol 9: 507–511
  41. Roostaee A, Barbar E, Lavigne P, LeHoux JG (2009) The mechanism of specific binding of free cholesterol by the steroidogenic acute regulatory protein: evidence for a role of the C‐terminal alpha‐helix in the gating of the binding site. Biosci Rep 29: 89–101 · DOI
  42. Saheki Y, Bian X, Schauder CM, Sawaki Y, Surma MA, Klose C, Pincet F, Reinisch KM, De Camilli P (2016) Control of plasma membrane lipid homeostasis by the extended synaptotagmins. Nat Cell Biol 18: 504–515 · DOI
  43. de Saint‐Jean M, Delfosse V, Douguet D, Chicanne G, Payrastre B, Bourguet W, Antonny B, Drin G (2011) Osh4p exchanges sterols for phosphatidylinositol 4‐phosphate between lipid bilayers. J Cell Biol 195: 965–978 · DOI
  44. Schauder CM, Wu X, Saheki Y, Narayanaswamy P, Torta F, Wenk MR, De Camilli P, Reinisch KM (2014) Structure of a lipid‐bound extended synaptotagmin indicates a role in lipid transfer. Nature 510: 552–555 · DOI
  45. Steck TL, Ye J, Lange Y (2002) Probing red cell membrane cholesterol movement with cyclodextrin. Biophys J 83: 2118–2125 · DOI
  46. Thorsell AG, Lee WH, Persson C, Siponen MI, Nilsson M, Busam RD, Kotenyova T, Schuler H, Lehtio L (2011) Comparative structural analysis of lipid binding START domains. PLoS ONE 6: e19521 · DOI
  47. Tilley SJ, Skippen A, Murray‐Rust J, Swigart PM, Stewart A, Morgan CP, Cockcroft S, McDonald NQ (2004) Structure‐function analysis of human [corrected] phosphatidylinositol transfer protein alpha bound to phosphatidylinositol. Structure 12: 317–326 · DOI
  48. Tsujishita Y, Hurley JH (2000) Structure and lipid transport mechanism of a StAR‐related domain. Nat Struct Biol 7: 408–414 · DOI
  49. Vordtriede PB, Doan CN, Tremblay JM, Helmkamp GM Jr, Yoder MD (2005) Structure of PITPbeta in complex with phosphatidylcholine: comparison of structure and lipid transfer to other PITP isoforms. Biochemistry 44: 14760–14771 · DOI
  50. Wong LH, Copic A, Levine TP (2017) Advances on the transfer of lipids by lipid transfer proteins. Trends Biochem Sci 42: 516–530 · DOI
  51. Yeung T, Gilbert GE, Shi J, Silvius J, Kapus A, Grinstein S (2008) Membrane phosphatidylserine regulates surface charge and protein localization. Science 319: 210–213 · DOI

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Metadata

Authors
Horenkamp, F. A., Valverde, D. P., Nunnari, J., & Reinisch, K. M.
Venue
The EMBO Journal
Published
2018-02-21
Volume
37
Issue
6
ISSN
  • 0261-4189
  • 1460-2075
Cited by
113
References
2
Language
en
Funders
  • HHS | National Institutes of Health (R01GM80616, R37GM097432, R01GM106019)
  • National Institute of General Medical Sciences (P41 GM103403)
  • NSF Graduate Research Fellowship

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