Home LiteratureArticle Details
PMID: 21680708 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The yeast p24 complex regulates GPI-anchored protein transport and quality control by monitoring anchor remodeling.

Molecular biology of the cell ·Vol. 22 ·No. 16 ·2011-08-15 ·Pages 2924-36

Castillon GA, Aguilera-Romero A, Manzano-Lopez J, Epstein S, Kajiwara K, Funato K, Watanabe R, Riezman H, Muñiz M

Abstract

Glycosylphosphatidylinositol (GPI)-anchored proteins are secretory proteins that are attached to the cell surface of eukaryotic cells by a glycolipid moiety. Once GPI anchoring has occurred in the lumen of the endoplasmic reticulum (ER), the structure of the lipid part on the GPI anchor undergoes a remodeling process prior to ER exit. In this study, we provide evidence suggesting that the yeast p24 complex, through binding specifically to GPI-anchored proteins in an anchor-dependent manner, plays a dual role in their selective trafficking. First, the p24 complex promotes efficient ER exit of remodeled GPI-anchored proteins after concentration by connecting them with the COPII coat and thus facilitates their incorporation into vesicles. Second, it retrieves escaped, unremodeled GPI-anchored proteins from the Golgi to the ER in COPI vesicles. Therefore the p24 complex, by sensing the status of the GPI anchor, regulates GPI-anchored protein intracellular transport and coordinates this with correct anchor remodeling.

MeSH Terms
Binding Sites Endoplasmic Reticulum/metabolism Endoplasmic Reticulum Stress GPI-Linked Proteins/metabolism Gene Knockout Techniques Glycosylphosphatidylinositols/metabolism Golgi Apparatus/metabolism Membrane Proteins/metabolism Multiprotein Complexes/chemistry,genetics,metabolism Protein Binding Protein Transport Saccharomyces cerevisiae/metabolism Saccharomyces cerevisiae Proteins/chemistry,genetics,metabolism Unfolded Protein Response Vesicular Transport Proteins/chemistry,genetics,metabolism
Chemicals
GPI-Linked Proteins Glycosylphosphatidylinositols Membrane Proteins Multiprotein Complexes SFB3 protein, S cerevisiae Saccharomyces cerevisiae Proteins Vesicular Transport Proteins
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Castillon Guillaume A
Department of Biochemistry, Sciences II, University of Geneva, CH-1211 Geneva 4, Switzerland.
Aguilera-Romero Auxiliadora
Manzano-Lopez Javier
Epstein Sharon
Kajiwara Kentaro
Funato Kouichi
Watanabe Reika
Riezman Howard
Muñiz Manuel
References (48)
48 references, click to expand
  1. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae.
    Yeast. 1998 Jul;14(10):953-61 PMID: 9717241
  2. Analysis of the sequence requirements for glycosylphosphatidylinositol anchoring of Saccharomyces cerevisiae Gas1 protein.
    J Biol Chem. 1993 May 15;268(14):10558-63 PMID: 8486709
  3. Ligand-induced redistribution of a human KDEL receptor from the Golgi complex to the endoplasmic reticulum.
    Cell. 1992 Jan 24;68(2):353-64 PMID: 1310258
  4. Interactions between newly synthesized glycoproteins, calnexin and a network of resident chaperones in the endoplasmic reticulum.
    J Cell Biol. 1997 Feb 10;136(3):555-65 PMID: 9024687
  5. An improved cyan fluorescent protein variant useful for FRET.
    Nat Biotechnol. 2004 Apr;22(4):445-9 PMID: 14990965
  6. Distinct roles for the cytoplasmic tail sequences of Emp24p and Erv25p in transport between the endoplasmic reticulum and Golgi complex.
    J Biol Chem. 2001 Nov 16;276(46):43040-8 PMID: 11560939
  7. Mechanisms of COPII vesicle formation and protein sorting.
    FEBS Lett. 2007 May 22;581(11):2076-82 PMID: 17316621
  8. Analysis of ceramides present in glycosylphosphatidylinositol anchored proteins of Saccharomyces cerevisiae.
    Methods Enzymol. 2000;312:506-15 PMID: 11070898
  9. CWH43 is required for the introduction of ceramides into GPI anchors in Saccharomyces cerevisiae.
    Mol Microbiol. 2007 Sep;65(6):1493-502 PMID: 17714445
  10. The Emp24 complex recruits a specific cargo molecule into endoplasmic reticulum-derived vesicles.
    J Cell Biol. 2000 Mar 6;148(5):925-30 PMID: 10704443
  11. Localization and recycling of gp27 (hp24gamma3): complex formation with other p24 family members.
    Mol Biol Cell. 1999 Jun;10(6):1939-55 PMID: 10359607
  12. Sorting of GPI-anchored proteins into ER exit sites by p24 proteins is dependent on remodeled GPI.
    J Cell Biol. 2011 Jul 11;194(1):61-75 PMID: 21727194
  13. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3254-9 PMID: 10716729
  14. Protein sorting receptors in the early secretory pathway.
    Annu Rev Biochem. 2010;79:777-802 PMID: 20533886
  15. Concentration of GPI-anchored proteins upon ER exit in yeast.
    Traffic. 2009 Feb;10(2):186-200 PMID: 19054390
  16. In silicio identification of glycosyl-phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae.
    Yeast. 1997 Dec;13(15):1477-89 PMID: 9434352
  17. Lipid remodeling of GPI-anchored proteins and its function.
    Biochim Biophys Acta. 2008 Mar;1780(3):410-20 PMID: 17913366
  18. Mammalian GPI-anchored proteins require p24 proteins for their efficient transport from the ER to the plasma membrane.
    Biochem J. 2008 Jan 15;409(2):555-62 PMID: 17927562
  19. Protein sorting upon exit from the endoplasmic reticulum.
    Cell. 2001 Jan 26;104(2):313-20 PMID: 11207371
  20. Gpi1, a Saccharomyces cerevisiae protein that participates in the first step in glycosylphosphatidylinositol anchor synthesis.
    J Biol Chem. 1996 Nov 1;271(44):27829-37 PMID: 8910381
  21. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation.
    Cell. 2000 Apr 28;101(3):249-58 PMID: 10847680
  22. Inositol deacylation by Bst1p is required for the quality control of glycosylphosphatidylinositol-anchored proteins.
    Mol Biol Cell. 2006 Feb;17(2):834-50 PMID: 16319176
  23. Protein-O-glycosylation in yeast: protein-specific mannosyltransferases.
    Glycobiology. 1997 Jun;7(4):481-6 PMID: 9184828
  24. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles.
    Cell. 2003 Aug 22;114(4):497-509 PMID: 12941277
  25. PER1 is required for GPI-phospholipase A2 activity and involved in lipid remodeling of GPI-anchored proteins.
    Mol Biol Cell. 2006 Dec;17(12):5253-64 PMID: 17021251
  26. Inositol deacylation of glycosylphosphatidylinositol-anchored proteins is mediated by mammalian PGAP1 and yeast Bst1p.
    J Biol Chem. 2004 Apr 2;279(14):14256-63 PMID: 14734546
  27. Evidence for overlapping and distinct functions in protein transport of coat protein Sec24p family members.
    J Biol Chem. 2000 Apr 14;275(15):11521-8 PMID: 10753972
  28. The yeast p24 complex is required for the formation of COPI retrograde transport vesicles from the Golgi apparatus.
    J Cell Biol. 2008 Feb 25;180(4):713-20 PMID: 18283113
  29. Selective export of human GPI-anchored proteins from the endoplasmic reticulum.
    J Cell Sci. 2010 May 15;123(Pt 10):1705-15 PMID: 20427317
  30. Involvement of the transmembrane protein p23 in biosynthetic protein transport.
    J Cell Biol. 1997 Dec 1;139(5):1119-35 PMID: 9382861
  31. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response.
    Cell. 1996 Nov 1;87(3):391-404 PMID: 8898193
  32. Sphingolipids are required for the stable membrane association of glycosylphosphatidylinositol-anchored proteins in yeast.
    J Biol Chem. 2002 Dec 20;277(51):49538-44 PMID: 12393888
  33. Erv25p, a component of COPII-coated vesicles, forms a complex with Emp24p that is required for efficient endoplasmic reticulum to Golgi transport.
    J Biol Chem. 1996 Oct 25;271(43):26939-46 PMID: 8900179
  34. A major transmembrane protein of Golgi-derived COPI-coated vesicles involved in coatomer binding.
    J Cell Biol. 1996 Dec;135(5):1239-48 PMID: 8947548
  35. Biosynthesis and function of GPI proteins in the yeast Saccharomyces cerevisiae.
    Biochim Biophys Acta. 2007 Mar;1771(3):405-20 PMID: 16859984
  36. Coupling of coat assembly and vesicle budding to packaging of putative cargo receptors.
    Cell. 1999 Feb 19;96(4):495-506 PMID: 10052452
  37. Sorting GPI-anchored proteins.
    Nat Rev Mol Cell Biol. 2004 Feb;5(2):110-20 PMID: 15040444
  38. Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum.
    Science. 2009 Mar 27;323(5922):1693-7 PMID: 19325107
  39. Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum.
    Cell. 1994 Dec 30;79(7):1199-207 PMID: 8001155
  40. Bi-directional protein transport between the ER and Golgi.
    Annu Rev Cell Dev Biol. 2004;20:87-123 PMID: 15473836
  41. The absence of Emp24p, a component of ER-derived COPII-coated vesicles, causes a defect in transport of selected proteins to the Golgi.
    EMBO J. 1995 Apr 3;14(7):1329-39 PMID: 7729411
  42. Live imaging of yeast Golgi cisternal maturation.
    Nature. 2006 Jun 22;441(7096):1007-10 PMID: 16699523
  43. Erp1p and Erp2p, partners for Emp24p and Erv25p in a yeast p24 complex.
    Mol Biol Cell. 1999 Jun;10(6):1923-38 PMID: 10359606
  44. Transport of axl2p depends on erv14p, an ER-vesicle protein related to the Drosophila cornichon gene product.
    J Cell Biol. 1998 Sep 7;142(5):1209-22 PMID: 9732282
  45. The presence of an ER exit signal determines the protein sorting upon ER exit in yeast.
    Biochem J. 2008 Sep 1;414(2):237-45 PMID: 18462190
  46. Thematic review series: lipid posttranslational modifications. GPI anchoring of protein in yeast and mammalian cells, or: how we learned to stop worrying and love glycophospholipids.
    J Lipid Res. 2007 May;48(5):993-1011 PMID: 17361015
  47. An integral membrane component of coatomer-coated transport vesicles defines a family of proteins involved in budding.
    Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):8011-5 PMID: 7644530
  48. Fatty acid remodeling of GPI-anchored proteins is required for their raft association.
    Mol Biol Cell. 2007 Apr;18(4):1497-506 PMID: 17314402
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1939-4586
DOI
10.1091/mbc.E11-04-0294
Published
2011-08-15
Epub
2011-00-16
Pages
2924-36
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC3154887
Subset
IM
External Links
PubMed source DOI: 10.1091/mbc.E11-04-0294 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2