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PMID: 9843576 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The syntaxin Tlg1p mediates trafficking of chitin synthase III to polarized growth sites in yeast.

Molecular biology of the cell ·Vol. 9 ·No. 12 ·1998-12-00 ·Pages 3383-97

Holthuis JC, Nichols BJ, Pelham HR

Abstract

Tlg1p and Tlg2p, members of the syntaxin family of SNAREs in yeast, have been implicated in both endocytosis and the retention of late Golgi markers. We have investigated the functions of these and the other endocytic syntaxins Pep12p and Vam3p. Remarkably, growth is possible in the absence of all four proteins. In the absence of the others, Pep12p and Tlg1p can each create endosomes accessible to the endocytic tracer dye FM4-64. However, although Pep12p is required for the ligand-induced internalization of the alpha factor receptor and its passage via Pep12p-containing membranes to the vacuole, Tlg1p is not. In contrast, Tlg1p is required for the efficient localization of the catalytic subunit of chitin synthase III (Chs3p) to the bud neck, a process that involves endocytosis and polarized delivery of Chs3p. In wild-type cells, internalized Chs3p cofractionates with Tlg1p and Tlg2p, and in a strain lacking the other endocytic syntaxins, either Tlg1p or Tlg2p is sufficient for correct localization of the enzyme. Pep12p is neither necessary nor sufficient for this process. We conclude that there are two endocytic routes in yeast that can operate independently and that Tlg1p is located at the junction of one of these with the polarized exocytic pathway.

MeSH Terms
Biological Transport, Active Cell Polarity Chitin Synthase/metabolism Endocytosis Endosomes/metabolism Exocytosis Fungal Proteins/metabolism Golgi Apparatus/metabolism Membrane Fusion Membrane Proteins/metabolism Microscopy, Electron Qa-SNARE Proteins SNARE Proteins Saccharomyces cerevisiae/cytology,growth & development,metabolism Vesicular Transport Proteins
Chemicals
Fungal Proteins Membrane Proteins Qa-SNARE Proteins SNARE Proteins Vesicular Transport Proteins Chitin Synthase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Holthuis J C
Medical Research Council Laboratory of Molecular Biology, Cambridge CB2 2QH, United Kingdom.
Nichols B J
Pelham H R
References (49)
49 references, click to expand
  1. Yeast syntaxins Sso1p and Sso2p belong to a family of related membrane proteins that function in vesicular transport.
    EMBO J. 1993 Nov;12(11):4095-104 PMID: 8223426
  2. The Sec1p homologue Vps45p binds to the syntaxin Tlg2p.
    Eur J Cell Biol. 1998 Dec;77(4):263-8 PMID: 9930650
  3. Mechanisms of intracellular protein transport.
    Nature. 1994 Nov 3;372(6501):55-63 PMID: 7969419
  4. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast.
    J Cell Biol. 1995 Mar;128(5):779-92 PMID: 7533169
  5. A SNARE-like protein required for traffic through the Golgi complex.
    Nature. 1995 Jun 29;375(6534):806-9 PMID: 7596416
  6. Membrane transport in the endocytic pathway.
    Curr Opin Cell Biol. 1995 Aug;7(4):552-63 PMID: 7495576
  7. Parallel secretory pathways to the cell surface in yeast.
    J Cell Biol. 1995 Oct;131(2):297-310 PMID: 7593160
  8. SNARE-mediated retrograde traffic from the Golgi complex to the endoplasmic reticulum.
    Cell. 1996 Apr 19;85(2):205-15 PMID: 8612273
  9. Receptor-mediated protein sorting to the vacuole in yeast: roles for a protein kinase, a lipid kinase and GTP-binding proteins.
    Annu Rev Cell Dev Biol. 1995;11:1-33 PMID: 8689553
  10. 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
  11. Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p.
    J Cell Biol. 1996 Nov;135(3):597-610 PMID: 8909536
  12. Chs1p and Chs3p, two proteins involved in chitin synthesis, populate a compartment of the Saccharomyces cerevisiae endocytic pathway.
    Mol Biol Cell. 1996 Dec;7(12):1909-19 PMID: 8970154
  13. Targeting of chitin synthase 3 to polarized growth sites in yeast requires Chs5p and Myo2p.
    J Cell Biol. 1997 Jan 13;136(1):95-110 PMID: 9008706
  14. Two separate signals act independently to localize a yeast late Golgi membrane protein through a combination of retrieval and retention.
    J Cell Biol. 1997 Jan 27;136(2):287-97 PMID: 9015300
  15. Transport through the yeast endocytic pathway occurs through morphologically distinct compartments and requires an active secretory pathway and Sec18p/N-ethylmaleimide-sensitive fusion protein.
    Mol Biol Cell. 1997 Jan;8(1):13-31 PMID: 9017592
  16. A conserved domain is present in different families of vesicular fusion proteins: a new superfamily.
    Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3046-51 PMID: 9096343
  17. Homotypic vacuolar fusion mediated by t- and v-SNAREs.
    Nature. 1997 May 8;387(6629):199-202 PMID: 9144293
  18. Novel Golgi to vacuole delivery pathway in yeast: identification of a sorting determinant and required transport component.
    EMBO J. 1997 May 15;16(10):2769-82 PMID: 9184222
  19. Sec2p mediates nucleotide exchange on Sec4p and is involved in polarized delivery of post-Golgi vesicles.
    J Cell Biol. 1997 Jun 30;137(7):1495-509 PMID: 9199166
  20. The yeast v-SNARE Vti1p mediates two vesicle transport pathways through interactions with the t-SNAREs Sed5p and Pep12p.
    J Cell Biol. 1997 Jun 30;137(7):1511-24 PMID: 9199167
  21. Vam3p, a new member of syntaxin related protein, is required for vacuolar assembly in the yeast Saccharomyces cerevisiae.
    J Cell Sci. 1997 Jun;110 ( Pt 11):1299-306 PMID: 9202390
  22. Syntaxin 6 functions in trans-Golgi network vesicle trafficking.
    Mol Biol Cell. 1997 Jul;8(7):1261-71 PMID: 9243506
  23. High expression of the yeast syntaxin-related Vam3 protein suppresses the protein transport defects of a pep12 null mutant.
    FEBS Lett. 1997 Jul 7;411(1):48-52 PMID: 9247140
  24. A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole.
    J Cell Biol. 1997 Aug 11;138(3):517-29 PMID: 9245783
  25. The membrane protein alkaline phosphatase is delivered to the vacuole by a route that is distinct from the VPS-dependent pathway.
    J Cell Biol. 1997 Aug 11;138(3):531-45 PMID: 9245784
  26. Yeast actin cytoskeleton mutants accumulate a new class of Golgi-derived secretary vesicle.
    Mol Biol Cell. 1997 Aug;8(8):1481-99 PMID: 9285820
  27. A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall.
    J Cell Biol. 1997 Oct 6;139(1):75-93 PMID: 9314530
  28. The yeast adaptor protein complex, AP-3, is essential for the efficient delivery of alkaline phosphatase by the alternate pathway to the vacuole.
    J Cell Biol. 1997 Dec 29;139(7):1761-74 PMID: 9412470
  29. Two syntaxin homologues in the TGN/endosomal system of yeast.
    EMBO J. 1998 Jan 2;17(1):113-26 PMID: 9427746
  30. Morphology of the yeast endocytic pathway.
    Mol Biol Cell. 1998 Jan;9(1):173-89 PMID: 9436999
  31. 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
  32. Tlg2p, a yeast syntaxin homolog that resides on the Golgi and endocytic structures.
    J Biol Chem. 1998 May 8;273(19):11719-27 PMID: 9565594
  33. Syntaxin-16, a putative Golgi t-SNARE.
    Eur J Cell Biol. 1998 Mar;75(3):223-31 PMID: 9587053
  34. Functional expression of the cre-lox site-specific recombination system in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1987 Jun;7(6):2087-96 PMID: 3037344
  35. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  36. Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway.
    Cell. 1990 May 18;61(4):723-33 PMID: 2188733
  37. The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle.
    J Cell Biol. 1991 Jul;114(1):111-23 PMID: 2050738
  38. A simple and efficient procedure for transformation of yeasts.
    Biotechniques. 1992 Jul;13(1):18-20 PMID: 1503765
  39. SED5 encodes a 39-kD integral membrane protein required for vesicular transport between the ER and the Golgi complex.
    J Cell Biol. 1992 Nov;119(3):513-21 PMID: 1400588
  40. end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae.
    J Cell Biol. 1993 Jan;120(1):55-65 PMID: 8380177
  41. 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
  42. Partial purification and characterization of early and late endosomes from yeast. Identification of four novel proteins.
    J Biol Chem. 1993 Jul 5;268(19):14376-86 PMID: 8314797
  43. Homologs of the synaptobrevin/VAMP family of synaptic vesicle proteins function on the late secretory pathway in S. cerevisiae.
    Cell. 1993 Sep 10;74(5):855-61 PMID: 8374953
  44. Chs6p-dependent anterograde transport of Chs3p from the chitosome to the plasma membrane in Saccharomyces cerevisiae.
    Mol Biol Cell. 1998 Jun;9(6):1565-76 PMID: 9614194
  45. Traffic into the prevacuolar/endosomal compartment of Saccharomyces cerevisiae: a VPS45-dependent intracellular route and a VPS45-independent, endocytic route.
    Eur J Cell Biol. 1998 May;76(1):43-52 PMID: 9650782
  46. Getting through the Golgi complex.
    Trends Cell Biol. 1998 Jan;8(1):45-9 PMID: 9695808
  47. SNAREs and membrane fusion in the Golgi apparatus.
    Biochim Biophys Acta. 1998 Aug 14;1404(1-2):9-31 PMID: 9714710
  48. The dynamics of golgi protein traffic visualized in living yeast cells.
    Mol Biol Cell. 1998 Sep;9(9):2667-80 PMID: 9725919
  49. Direct evidence for ligand-induced internalization of the yeast alpha-factor pheromone receptor.
    Mol Cell Biol. 1994 Nov;14(11):7245-55 PMID: 7935439
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
1998-12-00
Pages
3383-97
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC25643
Subset
IM
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