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PMID: 26041457 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

ER-endosome contact sites: molecular compositions and functions.

The EMBO journal ·Vol. 34 ·No. 14 ·2015-07-14 ·Pages 1848-58

Raiborg C, Wenzel EM, Stenmark H

Abstract

Recent studies have revealed the existence of numerous contact sites between the endoplasmic reticulum (ER) and endosomes in mammalian cells. Such contacts increase during endosome maturation and play key roles in cholesterol transfer, endosome positioning, receptor dephosphorylation, and endosome fission. At least 7 distinct contact sites between the ER and endosomes have been identified to date, which have diverse molecular compositions. Common to these contact sites is that they impose a close apposition between the ER and endosome membranes, which excludes membrane fusion while allowing the flow of molecular signals between the two membranes, in the form of enzymatic modifications, or ion, lipid, or protein transfer. Thus, ER-endosome contact sites ensure coordination of molecular activities between the two compartments while keeping their general compositions intact. Here, we review the molecular architectures and cellular functions of known ER-endosome contact sites and discuss their implications for human health.

Keywords
endoplasmic reticulum endosome membrane contact sites
MeSH Terms
Animals Cell Membrane/metabolism Cytoskeleton/metabolism Endoplasmic Reticulum/chemistry,metabolism Endosomes/chemistry,metabolism Humans Phosphorylation Protein Tyrosine Phosphatase, Non-Receptor Type 1/metabolism
Chemicals
PTPN1 protein, human Protein Tyrosine Phosphatase, Non-Receptor Type 1
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Raiborg Camilla
Centre for Cancer Biomedicine, Faculty of Medicine, University of Oslo, Oslo, Norway Department of Molecular Cell Biology, Institute for Cancer Research Oslo University Hospital, Oslo, Norway.
Wenzel Eva M
Centre for Cancer Biomedicine, Faculty of Medicine, University of Oslo, Oslo, Norway Department of Molecular Cell Biology, Institute for Cancer Research Oslo University Hospital, Oslo, Norway.
Stenmark Harald
Centre for Cancer Biomedicine, Faculty of Medicine, University of Oslo, Oslo, Norway Department of Molecular Cell Biology, Institute for Cancer Research Oslo University Hospital, Oslo, Norway Centre of Molecular Inflammation Research, Faculty of Medicine, Norwegian University of Science and Technology, Trondheim, Norway [email protected].
References (65)
65 references, click to expand
  1. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11.
    J Cell Biol. 2000 May 15;149(4):901-14 PMID: 10811830
  2. Functional characterization of the MENTAL domain.
    J Biol Chem. 2005 May 6;280(18):17945-52 PMID: 15718238
  3. MLN64 is involved in actin-mediated dynamics of late endocytic organelles.
    Mol Biol Cell. 2005 Aug;16(8):3873-86 PMID: 15930133
  4. Expression of HER2 and the coamplified genes GRB7 and MLN64 in human breast cancer: quantitative real-time reverse transcription-PCR as a diagnostic alternative to immunohistochemistry and fluorescence in situ hybridization.
    Clin Cancer Res. 2005 Dec 1;11(23):8348-57 PMID: 16322295
  5. MLN64 and MENTHO, two mediators of endosomal cholesterol transport.
    Biochem Soc Trans. 2006 Jun;34(Pt 3):343-5 PMID: 16709157
  6. ZFYVE27 (SPG33), a novel spastin-binding protein, is mutated in hereditary spastic paraplegia.
    Am J Hum Genet. 2006 Aug;79(2):351-7 PMID: 16826525
  7. Protrudin induces neurite formation by directional membrane trafficking.
    Science. 2006 Nov 3;314(5800):818-21 PMID: 17082457
  8. Expression of human OSBP-related protein 1L in macrophages enhances atherosclerotic lesion development in LDL receptor-deficient mice.
    Arterioscler Thromb Vasc Biol. 2007 Jul;27(7):1618-24 PMID: 17478758
  9. Overexpression of the cholesterol-binding protein MLN64 induces liver damage in the mouse.
    World J Gastroenterol. 2007 Jun 14;13(22):3071-9 PMID: 17589922
  10. Increased metastatic lymph node 64 and CYP17 expression are associated with high stage prostate cancer.
    J Endocrinol. 2007 Jul;194(1):55-61 PMID: 17592021
  11. Glycosphingolipid synthesis requires FAPP2 transfer of glucosylceramide.
    Nature. 2007 Sep 6;449(7158):62-7 PMID: 17687330
  12. Cellular cholesterol trafficking and compartmentalization.
    Nat Rev Mol Cell Biol. 2008 Feb;9(2):125-38 PMID: 18216769
  13. Intracellular transport and kinesin superfamily proteins, KIFs: structure, function, and dynamics.
    Physiol Rev. 2008 Jul;88(3):1089-118 PMID: 18626067
  14. Oxysterol binding protein-related protein-5 is related to invasion and poor prognosis in pancreatic cancer.
    Cancer Sci. 2008 Dec;99(12):2387-94 PMID: 19032366
  15. DCTN1 mutations in Perry syndrome.
    Nat Genet. 2009 Feb;41(2):163-5 PMID: 19136952
  16. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins.
    Nature. 2009 Mar 26;458(7237):445-52 PMID: 19325624
  17. Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILP-p150 Glued and late endosome positioning.
    J Cell Biol. 2009 Jun 29;185(7):1209-25 PMID: 19564404
  18. Rab GTPases as coordinators of vesicle traffic.
    Nat Rev Mol Cell Biol. 2009 Aug;10(8):513-25 PMID: 19603039
  19. Cell signaling by receptor tyrosine kinases.
    Cell. 2000 Oct 13;103(2):211-25 PMID: 11057895
  20. Regulation of receptor tyrosine kinase signaling by protein tyrosine phosphatases.
    Trends Cell Biol. 2001 Jun;11(6):258-66 PMID: 11356362
  21. Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and -independent components.
    Curr Biol. 2002 Apr 30;12(9):695-704 PMID: 12007412
  22. Mutations in the small GTP-ase late endosomal protein RAB7 cause Charcot-Marie-Tooth type 2B neuropathy.
    Am J Hum Genet. 2003 Mar;72(3):722-7 PMID: 12545426
  23. Regulated portals of entry into the cell.
    Nature. 2003 Mar 6;422(6927):37-44 PMID: 12621426
  24. Mutant dynactin in motor neuron disease.
    Nat Genet. 2003 Apr;33(4):455-6 PMID: 12627231
  25. Molecular machinery for non-vesicular trafficking of ceramide.
    Nature. 2003 Dec 18;426(6968):803-9 PMID: 14685229
  26. Lipid and cholesterol trafficking in NPC.
    Biochim Biophys Acta. 2004 Oct 11;1685(1-3):28-37 PMID: 15465424
  27. Intracellular trafficking of cholesterol monitored with a cyclodextrin.
    J Biol Chem. 1996 Aug 30;271(35):21604-13 PMID: 8702948
  28. Steroidogenic acute regulatory protein (StAR) is a sterol transfer protein.
    J Biol Chem. 1998 Oct 9;273(41):26285-8 PMID: 9756854
  29. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene.
    Science. 1999 Mar 5;283(5407):1544-8 PMID: 10066179
  30. A new locus for autosomal dominant "pure" hereditary spastic paraplegia mapping to chromosome 12q13, and evidence for further genetic heterogeneity.
    Am J Hum Genet. 1999 Sep;65(3):757-63 PMID: 10441583
  31. Endocytosis and signalling: intertwining molecular networks.
    Nat Rev Mol Cell Biol. 2009 Sep;10(9):609-22 PMID: 19696798
  32. Twenty bone-mineral-density loci identified by large-scale meta-analysis of genome-wide association studies.
    Nat Genet. 2009 Nov;41(11):1199-206 PMID: 19801982
  33. The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex.
    Dev Cell. 2009 Nov;17(5):712-23 PMID: 19922875
  34. FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport.
    J Cell Biol. 2010 Jan 25;188(2):253-69 PMID: 20100911
  35. Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction.
    Nat Cell Biol. 2010 Mar;12(3):267-72 PMID: 20118922
  36. Microautophagy of the nucleus coincides with a vacuolar diffusion barrier at nuclear-vacuolar junctions.
    Mol Biol Cell. 2010 Dec;21(23):4173-83 PMID: 20943953
  37. A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking.
    J Cell Biol. 2011 Jan 10;192(1):121-35 PMID: 21220512
  38. PI(4,5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins.
    Cell. 2013 Jun 20;153(7):1494-509 PMID: 23791178
  39. Cholesterol-binding molecules MLN64 and ORP1L mark distinct late endosomes with transporters ABCA3 and NPC1.
    J Lipid Res. 2013 Aug;54(8):2153-65 PMID: 23709693
  40. Organization and function of membrane contact sites.
    Biochim Biophys Acta. 2013 Nov;1833(11):2526-41 PMID: 23380708
  41. Late endosomal transport and tethering are coupled processes controlled by RILP and the cholesterol sensor ORP1L.
    J Cell Sci. 2013 Aug 1;126(Pt 15):3462-74 PMID: 23729732
  42. Protrudin binds atlastins and endoplasmic reticulum-shaping proteins and regulates network formation.
    Proc Natl Acad Sci U S A. 2013 Sep 10;110(37):14954-9 PMID: 23969831
  43. Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites.
    Cell. 2011 Feb 4;144(3):389-401 PMID: 21295699
  44. Endosome maturation.
    EMBO J. 2011 Aug 31;30(17):3481-500 PMID: 21878991
  45. ER tubules mark sites of mitochondrial division.
    Science. 2011 Oct 21;334(6054):358-62 PMID: 21885730
  46. Staying in touch: the molecular era of organelle contact sites.
    Trends Biochem Sci. 2011 Nov;36(11):616-23 PMID: 21958688
  47. Peroxiredoxin-controlled G-CSF signalling at the endoplasmic reticulum-early endosome interface.
    J Cell Sci. 2011 Nov 1;124(Pt 21):3695-705 PMID: 22045733
  48. The fusion of early endosomes induces molecular-motor-driven tubule formation and fission.
    J Cell Sci. 2012 Apr 15;125(Pt 8):1910-9 PMID: 22357949
  49. Endoplasmic reticulum-mitochondria contacts: function of the junction.
    Nat Rev Mol Cell Biol. 2012 Oct;13(10):607-25 PMID: 22992592
  50. Endosomal cholesterol trafficking: protein factors at a glance.
    Acta Biochim Biophys Sin (Shanghai). 2013 Jan;45(1):11-7 PMID: 23165745
  51. Autophagosomes form at ER-mitochondria contact sites.
    Nature. 2013 Mar 21;495(7441):389-93 PMID: 23455425
  52. Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature.
    Mol Biol Cell. 2013 Apr;24(7):1030-40 PMID: 23389631
  53. Interactome map uncovers phosphatidylserine transport by oxysterol-binding proteins.
    Nature. 2013 Sep 12;501(7466):257-61 PMID: 23934110
  54. PTP1B: a simple enzyme for a complex world.
    Crit Rev Biochem Mol Biol. 2013 Sep-Oct;48(5):430-45 PMID: 23879520
  55. A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER-Golgi tether OSBP.
    Cell. 2013 Nov 7;155(4):830-43 PMID: 24209621
  56. Oxysterol-binding proteins: sterol and phosphoinositide sensors coordinating transport, signaling and metabolism.
    Prog Lipid Res. 2013 Oct;52(4):529-38 PMID: 23830809
  57. STARD3 or STARD3NL and VAP form a novel molecular tether between late endosomes and the ER.
    J Cell Sci. 2013 Dec 1;126(Pt 23):5500-12 PMID: 24105263
  58. Small regulators, major consequences - Ca²⁺ and cholesterol at the endosome-ER interface.
    J Cell Sci. 2014 Mar 1;127(Pt 5):929-38 PMID: 24554437
  59. Control of lipid droplet size in budding yeast requires the collaboration between Fld1 and Ldb16.
    J Cell Sci. 2014 Mar 15;127(Pt 6):1214-28 PMID: 24434579
  60. Protrudin regulates endoplasmic reticulum morphology and function associated with the pathogenesis of hereditary spastic paraplegia.
    J Biol Chem. 2014 May 9;289(19):12946-61 PMID: 24668814
  61. A close-up view of membrane contact sites between the endoplasmic reticulum and the endolysosomal system: from yeast to man.
    Crit Rev Biochem Mol Biol. 2014 May-Jun;49(3):262-8 PMID: 24382115
  62. ER contact sites define the position and timing of endosome fission.
    Cell. 2014 Nov 20;159(5):1027-41 PMID: 25416943
  63. PTP1B promotes cell proliferation and metastasis through activating src and ERK1/2 in non-small cell lung cancer.
    Cancer Lett. 2015 Apr 10;359(2):218-25 PMID: 25617799
  64. Repeated ER-endosome contacts promote endosome translocation and neurite outgrowth.
    Nature. 2015 Apr 9;520(7546):234-8 PMID: 25855459
  65. Cholesterol transport through lysosome-peroxisome membrane contacts.
    Cell. 2015 Apr 9;161(2):291-306 PMID: 25860611
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
1460-2075
Published
2015-07-14
Epub
2015-00-03
Pages
1848-58
Language
English
Region
England
NLM ID
8208664
PMCID
PMC4547891
Subset
IM
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