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PMID: 10564279 Published · ppublish English Journal Article

Differential roles of syntaxin 7 and syntaxin 8 in endosomal trafficking.

Molecular biology of the cell ·Vol. 10 ·No. 11 ·1999-11-00 ·Pages 3891-908

Prekeris R, Yang B, Oorschot V, Klumperman J, Scheller RH

Abstract

To understand molecular mechanisms that regulate the intricate and dynamic organization of the endosomal compartment, it is important to establish the morphology, molecular composition, and functions of the different organelles involved in endosomal trafficking. Syntaxins and vesicle-associated membrane protein (VAMP) families, also known as soluble N-ethylmaleimide-sensitive factor (NSF) attachment protein receptors (SNAREs), have been implicated in mediating membrane fusion and may play a role in determining the specificity of vesicular trafficking. Although several SNAREs, including VAMP3/cellubrevin, VAMP8/endobrevin, syntaxin 13, and syntaxin 7, have been localized to the endosomal membranes, their precise localization, biochemical interactions, and function remain unclear. Furthermore, little is known about SNAREs involved in lysosomal trafficking. So far, only one SNARE, VAMP7, has been localized to late endosomes (LEs), where it is proposed to mediate trafficking of epidermal growth factor receptor to LEs and lysosomes. Here we characterize the localization and function of two additional endosomal syntaxins, syntaxins 7 and 8, and propose that they mediate distinct steps of endosomal protein trafficking. Both syntaxins are found in SNARE complexes that are dissociated by alpha-soluble NSF attachment protein and NSF. Syntaxin 7 is mainly localized to vacuolar early endosomes (EEs) and may be involved in protein trafficking from the plasma membrane to the EE as well as in homotypic fusion of endocytic organelles. In contrast, syntaxin 8 is likely to function in clathrin-independent vesicular transport and membrane fusion events necessary for protein transport from EEs to LEs.

MeSH Terms
Animals Biological Transport Brefeldin A/pharmacology Carrier Proteins/metabolism Cell Line Cell Membrane/metabolism Endosomes/metabolism,ultrastructure Epidermal Growth Factor/metabolism Fluorescent Antibody Technique Golgi Apparatus/metabolism,ultrastructure Green Fluorescent Proteins Humans Immunohistochemistry Luminescent Proteins/genetics,metabolism Lysosomes/metabolism Membrane Proteins/metabolism Microscopy, Electron Nocodazole/pharmacology Qa-SNARE Proteins SNARE Proteins Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins Transferrin/metabolism Vesicular Transport Proteins
Chemicals
Carrier Proteins Luminescent Proteins Membrane Proteins Qa-SNARE Proteins SNARE Proteins Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins Transferrin Vesicular Transport Proteins Green Fluorescent Proteins Brefeldin A Epidermal Growth Factor Nocodazole
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Prekeris R
Howard Hughes Medical Institute, Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, California 94305-5428, USA.
Yang B
Oorschot V
Klumperman J
Scheller R H
References (47)
47 references, click to expand
  1. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution.
    Nature. 1998 Sep 24;395(6700):347-53 PMID: 9759724
  2. Human syntaxin 7: a Pep12p/Vps6p homologue implicated in vesicle trafficking to lysosomes.
    Gene. 1997 Oct 15;199(1-2):39-48 PMID: 9358037
  3. The syntaxin Tlg1p mediates trafficking of chitin synthase III to polarized growth sites in yeast.
    Mol Biol Cell. 1998 Dec;9(12):3383-97 PMID: 9843576
  4. Three novel proteins of the syntaxin/SNAP-25 family.
    J Biol Chem. 1998 Dec 18;273(51):34171-9 PMID: 9852078
  5. A leucine-based determinant in the epidermal growth factor receptor juxtamembrane domain is required for the efficient transport of ligand-receptor complexes to lysosomes.
    J Biol Chem. 1999 Jan 29;274(5):3141-50 PMID: 9915853
  6. SNARE interactions are not selective. Implications for membrane fusion specificity.
    J Biol Chem. 1999 Feb 26;274(9):5649-53 PMID: 10026182
  7. SNARE membrane trafficking dynamics in vivo.
    J Cell Biol. 1999 Mar 8;144(5):869-81 PMID: 10085287
  8. The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions.
    J Cell Biol. 1999 Apr 5;145(1):123-39 PMID: 10189373
  9. Mixed and non-cognate SNARE complexes. Characterization of assembly and biophysical properties.
    J Biol Chem. 1999 May 28;274(22):15440-6 PMID: 10336434
  10. VAMP-7 mediates vesicular transport from endosomes to lysosomes.
    J Cell Biol. 1999 Aug 23;146(4):765-76 PMID: 10459012
  11. The biogenesis of lysosomes.
    Annu Rev Cell Biol. 1989;5:483-525 PMID: 2557062
  12. Sequential processing of epidermal growth factor in early and late endosomes of rat liver.
    J Biol Chem. 1991 Mar 5;266(7):4348-56 PMID: 1671862
  13. Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat.
    J Cell Biol. 1991 Apr;113(1):123-35 PMID: 2007617
  14. Late endosomes derive from early endosomes by maturation.
    Cell. 1991 May 3;65(3):417-27 PMID: 1850321
  15. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic.
    Cell. 1991 Nov 1;67(3):601-16 PMID: 1682055
  16. Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators.
    Cell. 1992 Apr 3;69(1):129-38 PMID: 1555237
  17. Internalization and processing of transferrin and the transferrin receptor in human carcinoma A431 cells.
    J Cell Biol. 1983 Aug;97(2):508-21 PMID: 6309862
  18. Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells.
    Cell. 1983 Nov;35(1):321-30 PMID: 6313227
  19. Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway.
    Cell. 1984 Jul;37(3):789-800 PMID: 6204769
  20. Two distinct subpopulations of endosomes involved in membrane recycling and transport to lysosomes.
    Cell. 1988 Jan 15;52(1):73-83 PMID: 3345561
  21. Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro.
    J Cell Biol. 1989 Apr;108(4):1301-16 PMID: 2538480
  22. Structural organization of the synaptic exocytosis core complex.
    Neuron. 1997 Nov;19(5):1087-94 PMID: 9390521
  23. Syntaxin 7, a novel syntaxin member associated with the early endosomal compartment.
    J Biol Chem. 1998 Jan 2;273(1):375-80 PMID: 9417091
  24. Two syntaxin homologues in the TGN/endosomal system of yeast.
    EMBO J. 1998 Jan 2;17(1):113-26 PMID: 9427746
  25. Mannose 6-phosphate receptors are sorted from immature secretory granules via adaptor protein AP-1, clathrin, and syntaxin 6-positive vesicles.
    J Cell Biol. 1998 Apr 20;141(2):359-71 PMID: 9548715
  26. Seven novel mammalian SNARE proteins localize to distinct membrane compartments.
    J Biol Chem. 1998 Apr 24;273(17):10317-24 PMID: 9553086
  27. Endobrevin, a novel synaptobrevin/VAMP-like protein preferentially associated with the early endosome.
    Mol Biol Cell. 1998 Jun;9(6):1549-63 PMID: 9614193
  28. The role of endosomes and lysosomes in MHC class II functioning.
    Immunol Today. 1998 Jun;19(6):282-7 PMID: 9639994
  29. A novel synaptobrevin/VAMP homologous protein (VAMP5) is increased during in vitro myogenesis and present in the plasma membrane.
    Mol Biol Cell. 1998 Sep;9(9):2423-37 PMID: 9725904
  30. SNAP receptors implicated in vesicle targeting and fusion.
    Nature. 1993 Mar 25;362(6418):318-24 PMID: 8455717
  31. The molecular machinery for secretion is conserved from yeast to neurons.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2559-63 PMID: 8096639
  32. Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process.
    J Cell Biol. 1993 Jun;121(6):1257-69 PMID: 8509447
  33. Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein.
    Nature. 1993 Jul 22;364(6435):346-9 PMID: 8332193
  34. The syntaxin family of vesicular transport receptors.
    Cell. 1993 Sep 10;74(5):863-73 PMID: 7690687
  35. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion.
    Cell. 1993 Nov 5;75(3):409-18 PMID: 8221884
  36. Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells.
    J Cell Biol. 1994 Jun;125(5):1015-24 PMID: 8195285
  37. Oligomerized transferrin receptors are selectively retained by a lumenal sorting signal in a long-lived endocytic recycling compartment.
    J Cell Biol. 1995 Jun;129(6):1509-22 PMID: 7790351
  38. Membrane transport in the endocytic pathway.
    Curr Opin Cell Biol. 1995 Aug;7(4):552-63 PMID: 7495576
  39. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes.
    J Cell Biol. 1996 Mar;132(6):1011-23 PMID: 8601581
  40. Mammalian vesicle trafficking proteins of the endoplasmic reticulum and Golgi apparatus.
    J Biol Chem. 1996 Mar 8;271(10):5671-9 PMID: 8621431
  41. Novel syntaxin homologue, Pep12p, required for the sorting of lumenal hydrolases to the lysosome-like vacuole in yeast.
    Mol Biol Cell. 1996 Apr;7(4):579-94 PMID: 8730101
  42. Lysosomal targeting of epidermal growth factor receptors via a kinase-dependent pathway is mediated by the receptor carboxyl-terminal residues 1022-1123.
    J Biol Chem. 1996 Nov 29;271(48):30340-6 PMID: 8939994
  43. Endocytosis and molecular sorting.
    Annu Rev Cell Dev Biol. 1996;12:575-625 PMID: 8970738
  44. Protein transport. A fusion of new ideas.
    Nature. 1997 May 8;387(6629):133-5 PMID: 9144278
  45. Syntaxin 6 functions in trans-Golgi network vesicle trafficking.
    Mol Biol Cell. 1997 Jul;8(7):1261-71 PMID: 9243506
  46. Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy.
    Cell. 1997 Aug 8;90(3):523-35 PMID: 9267032
  47. Syntaxin 13 mediates cycling of plasma membrane proteins via tubulovesicular recycling endosomes.
    J Cell Biol. 1998 Nov 16;143(4):957-71 PMID: 9817754
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
1999-11-00
Pages
3891-908
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC25687
Subset
IM
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