Exit of GPI-anchored proteins from the ER differs in yeast and mammalian cells

Traffic

Volumn 11, Issue 8, 2010, Pages 1017-1033

  Rivier, Anne Sophie ^a   Castillon, Guillaume A ^a   Michon, Laetitia ^a   Fukasawa, Masayoshi ^b   Romanova Michaelides, Maria ^a   Jaensch, Nina ^a   Hanada, Kentaro ^b   Watanabe, Reika ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

Copii; Detergent resistantmembrane; ER exit site; GPI anchored protein; Lipid raft; Protein sorting; Sar1 protein; Sphingolipid

Indexed keywords

COAT PROTEIN COMPLEX II; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; SECRETORY PROTEIN; SPHINGOLIPID; FUNGAL PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL; MEMBRANE PROTEIN; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; PHOSPHOLIPID; SAR1A PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; LIPID RAFT; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; PROTEIN TRANSPORT; YEAST CELL; ANIMAL; CHEMISTRY; CHO CELL; COATED VESICLE; CRICETULUS; CYTOLOGY; GENETICS; HAMSTER; HUMAN; METABOLISM; MICROSOME; PHYSIOLOGY; ULTRASTRUCTURE; YEAST;

ANIMALS; CHO CELLS; COP-COATED VESICLES; CRICETINAE; CRICETULUS; ENDOPLASMIC RETICULUM; FUNGAL PROTEINS; GLYCOSYLPHOSPHATIDYLINOSITOLS; GOLGI APPARATUS; HUMANS; MEMBRANE PROTEINS; MICROSOMES; MONOMERIC GTP-BINDING PROTEINS; PHOSPHOLIPIDS; PROTEIN TRANSPORT; SPHINGOLIPIDS; YEASTS;

EID: 77958114881     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2010.01081.x     Document Type: Article

References (76)

1. Lee MC, Miller EA, Goldberg J, Orci L, Schekman R. Bi-directional protein transport between the ER and Golgi. Annu Rev Cell Dev Biol 2004;20:87-123.
2. Leidich SD, Drapp DA, Orlean P. A conditionally lethal yeast mutant blocked at the first step in glycosyl phosphatidylinositol anchor synthesis. J Biol Chem 1994;269:10193-10196.
3. Kawagoe K, Kitamura D, Okabe M, Taniuchi I, Ikawa M, Watanabe T, Kinoshita T, Takeda J. Glycosylphosphatidylinositol-anchor-deficient mice: implications for clonal dominance of mutant cells in paroxysmal nocturnal hemoglobinuria. Blood 1996;87:3600-3606.
4. Pittet M, Conzelmann A. Biosynthesis and function of GPI proteins in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 2007;1771:405-420.
5. Kinoshita T, Fujita M, Maeda Y. Biosynthesis, remodelling and functions of mammalian GPI-anchored proteins: recent progress. J Biochem 2008;144:287-294.
6. Moran P, Caras IW. Proteins containing an uncleaved signal for glycophosphatidylinositol membrane anchor attachment are retained in a post-ER compartment. J Cell Biol 1992;119:763-772.
7. Delahunty MD, Stafford FJ, Yuan LC, Shaz D, Bonifacino JS. Uncleaved signals for glycosylphosphatidylinositol anchoring cause retention of precursor proteins in the endoplasmic reticulum. J Biol Chem 1993;268:12017-12027.
8. Field MC, Moran P, Li W, Keller GA, Caras IW. Retention and degradation of proteins containing an uncleaved glycosylphosphatidylinositol signal. J Biol Chem 1994;269:10830-10837.
9. Bosson R, Jaquenoud M, Conzelmann A. GUP1 of Saccharomyces cerevisiae encodes an O-acyltransferase involved in remodeling of the GPI anchor. Mol Biol Cell 2006;17:2636-2645.
10. Fujita M, Umemura M, Yoko-o T, Jigami Y. PER1 is required for GPI-phospholipase A2 activity and involved in lipid remodeling of GPI-anchored proteins. Mol Biol Cell 2006;17:5253-5264.
11. Tashima Y, Taguchi R, Murata C, Ashida H, Kinoshita T, Maeda Y. PGAP2 is essential for correct processing and stable expression of GPI-anchored proteins. Mol Biol Cell 2006;17:1410-1420.12.
12. Maeda Y, Tashima Y, Houjou T, Fujita M, Yoko-o T, Jigami Y, Taguchi R, Kinoshita T. Fatty acid remodeling of GPI-anchored proteins is required for their raft association. Mol Biol Cell 2007;18:1497-1506.
13. Fujita M, Jigami Y. Lipid remodeling of GPI-anchored proteins and its function. Biochim Biophys Acta 2008;1780:410-420.
14. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997;387:569-572.
15. Muniz M, Morsomme P, Riezman H. Protein sorting upon exit from the endoplasmic reticulum. Cell 2001;104:313-320.
16. Morsomme P, Riezman H. The Rab GTPase Ypt1p and tethering factors couple protein sorting at the ER to vesicle targeting to the Golgi apparatus. Dev Cell 2002;2:307-317.
17. Morsomme P, Prescianotto-Baschong C, Riezman H. The ER v-SNAREs are required for GPI-anchored protein sorting from other secretory proteins upon exit from the ER. J Cell Biol 2003;162:403-412.
18. Castillon GA, Watanabe R, Taylor M, Schwabe TM, Riezman H. Concentration of GPI-anchored proteins upon ER exit in yeast. Traffic 2009;10:186-200.
19. Horvath A, Sutterlin C, Manning-Krieg U, Movva NR, Riezman H. Ceramide synthesis enhances transport of GPI-anchored proteins to the Golgi apparatus in yeast. Embo J 1994;13:3687-3695.
20. Sutterlin C, Doering TL, Schimmoller F, Schroder S, Riezman H. Specific requirements for the ER to Golgi transport of GPI-anchored proteins in yeast. J Cell Sci 1997;110:2703-2714.
21. Watanabe R, Funato K, Venkataraman K, Futerman AH, Riezman H. Sphingolipids are required for the stable membrane association of glycosylphosphatidylinositol-anchored proteins in yeast. J Biol Chem 2002;277:49538-49544.
22. Hanada K, Hara T, Fukasawa M, Yamaji A, Umeda M, Nishijima M. Mammalian cell mutants resistant to a sphingomyelin-directed cytolysin. Genetic and biochemical evidence for complex formation of the LCB1 protein with the LCB2 protein for serine palmitoyltransferase. J Biol Chem 1998;273:33787-33794.
23. Kornfeld R, Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem 1985;54:631-664.
24. Hanada K, Nishijima M, Fujita T, Kobayashi S. Specificity of inhibitors of serine palmitoyltransferase (SPT), a key enzyme in sphingolipid biosynthesis, in intact cells. A novel evaluation system using an SPT-defective mammalian cell mutant. Biochem Pharmacol 2000;59:1211-1216.
25. Hidari K, Ichikawa S, Fujita T, Sakiyama H, Hirabayashi Y. Complete removal of sphingolipids from the plasma membrane disrupts cell to substratum adhesion of mouse melanoma cells. J Biol Chem 1996;271:14636-14641.
26. Sutterwala SS, Creswell CH, Sanyal S, Menon AK, Bangs JD. De novo sphingolipid synthesis is essential for viability, but not for transport of glycosylphosphatidylinositol-anchored proteins, in African trypanosomes. Eukaryot Cell 2007;6:454-464.
27. Hong Y, Ohishi K, Inoue N, Kang JY, Shime H, Horiguchi Y, van der Goot FG, Sugimoto N, Kinoshita T. Requirement of N-glycan on GPIanchored proteins for efficient binding of aerolysin but not Clostridium septicum alpha-toxin. EMBO J 2002;21:5047-5056.
28. Plutner H, Davidson HW, Saraste J, Balch WE. Morphological analysis of protein transport from the ER to Golgi membranes in digitoninpermeabilized cells: role of the P58 containing compartment. J Cell Biol 1992;119:1097-1116.
29. Saito K, Chen M, Bard F, Chen S, Zhou H, Woodley D, Polischuk R, Schekman R, Malhotra V. TANGO1 facilitates cargo loading at endoplasmic reticulum exit sites. Cell 2009;136:891-902.
30. Bonifacino JS, Glick BS. The mechanisms of vesicle budding and fusion. Cell 2004;116:153-166.
31. Bielli A, Haney CJ, Gabreski G, Watkins SC, Bannykh SI, Aridor M. Regulation of Sar1 NH2 terminus by GTP binding and hydrolysis promotes membrane deformation to control COPII vesicle fission. J Cell Biol 2005;171:919-924.
32. Watanabe R, Castillon GA, Meury A, Riezman H. The presence of an ER exit signal determines the protein sorting upon ER exit in yeast. Biochem J 2008;414:237-245.
33. Nakano A, Otsuka H, Yamagishi M, Yamamoto E, Kimura K, Nishikawa S, Oka T. Mutational analysis of the Sar1 protein, a small GTPase which is essential for vesicular transport from the endoplasmic reticulum. J Biochem (Tokyo) 1994;116:243-247.
34. Yamanushi T, Hirata A, Oka T, Nakano A. Characterization of yeast sar1 temperature-sensitive mutants, which are defective in protein transport from the endoplasmic reticulum. J Biochem (Tokyo) 1996;120:452-458.
35. Kirk SJ, Ward TH. COPII under the microscope. Semin Cell Dev Biol 2007;18:435-447.
36. Paulhe F, Imhof BA, Wehrle-Haller B. A specific endoplasmic reticulum export signal drives transport of stem cell factor (Kitl) to the cell surface. J Biol Chem 2004;279:55545-55555.
37. Nakamura N, Inoue N, Watanabe R, Takahashi M, Takeda J, Stevens VL, Kinoshita T. Expression cloning of PIG-L, a candidate N-acetylglucosaminyl-phosphatidylinositol deacetylase. J Biol Chem 1997;272:15834-15840.
38. Tatu U, Braakman I, Helenius A. Membrane glycoprotein folding, oligomerization and intracellular transport: effects of dithiothreitol in living cells. EMBO J 1993;12:2151-2157.
39. Lodish HF, Kong N. The secretory pathway is normal in dithiothreitoltreated cells, but disulfide-bonded proteins are reduced and reversibly retained in the endoplasmic reticulum. J Biol Chem 1993;268:20598-20605.
40. Martinez-Menarguez JA, Geuze HJ, Slot JW, Klumperman J. Vesicular tubular clusters between the ER and Golgi mediate concentration of soluble secretory proteins by exclusion from COPI-coated vesicles. Cell 1999;98:81-90.
41. Stephens DJ, Lin-Marq N, Pagano A, Pepperkok R, Paccaud JP. COPI-coated ER-to-Golgi transport complexes segregate from COPII in close proximity to ER exit sites. J Cell Sci 2000;113:2177-2185.
42. Mezzacasa A, Helenius A. The transitional ER defines a boundary for quality control in the secretion of tsO45 VSV glycoprotein. Traffic 2002;3:833-849.
43. Kreis TE. Microinjected antibodies against the cytoplasmic domain of vesicular stomatitis virus glycoprotein block its transport to the cell surface. EMBO J 1986;5:931-941.
44. Xu D, Hay JC. Reconstitution of COPII vesicle fusion to generate a pre-Golgi intermediate compartment. J Cell Biol 2004;167: 997-1003.
45. Bentley M, Liang Y, Mullen K, Xu D, Sztul E, Hay JC. SNARE status regulates tether recruitment and function in homotypic COPII vesicle fusion. J Biol Chem 2006;281:38825-38833.
46. Oka T, Nakano A. Inhibition of GTP hydrolysis by Sar1p causes accumulation of vesicles that are a functional intermediate of the ER-to-Golgi transport in yeast. J Cell Biol 1994;124:425-434.
47. Doering TL, Schekman R. GPI anchor attachment is required for Gas1p transport from the endoplasmic reticulum in COP II vesicles. EMBO J 1996;15:182-191.
48. Tanaka S, Maeda Y, Tashima Y, Kinoshita T. Inositol deacylation of glycosylphosphatidylinositol-anchored proteins is mediated by mammalian PGAP1 and yeast Bst1p. J Biol Chem 2004;279:14256-14263.
49. Haass FA, Jonikas M, Walter P, Weissman JS, Jan YN, Jan LY, Schuldiner M. Identification of yeast proteins necessary for cellsurface function of a potassium channel. Proc Natl Acad Sci U S A 2007;104:18079-18084.
50. Fujita M, Maeda Y, Ra M, Yamaguchi Y, Taguchi R, Kinoshita T. GPI glycan remodeling by PGAP5 regulates transport of GPI-anchored proteins from the ER to the Golgi. Cell 2009;139:352-365.
51. Muniz M, Nuoffer C, Hauri HP, Riezman H. The Emp24 complex recruits a specific cargo molecule into endoplasmic reticulum-derived vesicles. J Cell Biol 2000;148:925-930.
52. Takida S, Maeda Y, Kinoshita T. Mammalian GPI-anchored proteins require p24 proteins for their efficient transport from the ER to the plasma membrane. Biochem J 2008;409:555-562.
53. Muniz M, Riezman H. Intracellular transport of GPI-anchored proteins. EMBO J 2000;19:10-15.
54. Strating JR, Martens GJ. The p24 family and selective transport processes at the ER-Golgi interface. Biol Cell 2009;101:495-509.
55. Aridor M, Fish KN, Bannykh S, Weissman J, Roberts TH, Lippincott-Schwartz J, Balch WE. The Sar1 GTPase coordinates biosynthetic cargo selection with endoplasmic reticulum export site assembly. J Cell Biol 2001;152:213-229.56.
56. Sato K, Nakano A. Dissection of COPII subunit-cargo assembly and disassembly kinetics during Sar1p-GTP hydrolysis. Nat Struct Mol Biol 2005;12:167-174.
57. Lee MC, Orci L, Hamamoto S, Futai E, Ravazzola M, Schekman R. Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 2005;122:605-617.
58. Keller P, Toomre D, Diaz E, White J, Simons K. Multicolour imaging of post-Golgi sorting and trafficking in live cells. Nat Cell Biol 2001;3:140-149.
59. Brown DA, Rose JK. Sorting of GPI-anchored proteins to glycolipidenriched membrane subdomains during transport to the apical cell surface. Cell 1992;68:533-544.
60. Mays RW, Siemers KA, Fritz BA, Lowe AW, van Meer G, Nelson WJ. Hierarchy of mechanisms involved in generating Na/K-ATPase polarity in MDCK epithelial cells. J Cell Biol 1995;130:1105-1115.
61. Puoti A, Desponds C, Conzelmann A. Biosynthesis of mannosylinositolphosphoceramide in Saccharomyces cerevisiae is dependent on genes controlling the flow of secretory vesicles from the endoplasmic reticulum to the Golgi. J Cell Biol 1991;113:515-525.
62. Reggiori F, Conzelmann A. Biosynthesis of inositol phosphoceramides and remodeling of glycosylphosphatidylinositol anchors in Saccharomyces cerevisiae are mediated by different enzymes. J Biol Chem 1998;273:30550-30559.
63. Funato K, Riezman H. Vesicular and nonvesicular transport of ceramide from ER to the Golgi apparatus in yeast. J Cell Biol 2001;155:949-959.
64. Kajiwara K, Watanabe R, Pichler H, Ihara K, Murakami S, Riezman H, Funato K. Yeast ARV1 is required for efficient delivery of an early GPI intermediate to the first mannosyltransferase during GPI assembly and controls lipid flow from the endoplasmic reticulum. Mol Biol Cell 2008;19:2069-2082.
65. Fukasawa M, Nishijima M, Hanada K. Genetic evidence for ATPdependent endoplasmic reticulum-to-Golgi apparatus trafficking of ceramide for sphingomyelin synthesis in Chinese hamster ovary cells. J Cell Biol 1999;144:673-685.
66. Hanada K, Kumagai K, Yasuda S, Miura Y, Kawano M, Fukasawa M, Nishijima M. Molecular machinery for non-vesicular trafficking of ceramide. Nature 2003;426:803-809.
67. Kumagai K, Yasuda S, Okemoto K, Nishijima M, Kobayashi S, Hanada K. CERT mediates intermembrane transfer of various molecular species of ceramides. J Biol Chem 2005;280:6488-6495.
68. Prydz K, Dick G, Tveit H. How many ways through the Golgi maze? Traffic 2008;9:299-304.
69. Glick BS, Nakano A. Membrane traffic within the golgi stack. Annu Rev Cell Dev Biol 2009; 25: 113-132.
70. Rossanese OW, Soderholm J, Bevis BJ, Sears IB, O'Connor J, Williamson EK, Glick BS. Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J Cell Biol 1999;145:69-81.
71. Yano H, Yamamoto-Hino M, Abe M, Kuwahara R, Haraguchi S, Kusaka I, Awano W, Kinoshita-Toyoda A, Toyoda H, Goto S. Distinct functional units of the Golgi complex in Drosophila cells. Proc Natl Acad Sci U S A 2005;102:13467-13472.
72. Fujita T, Inoue K, Yamamoto S, Ikumoto T, Sasaki S, Toyama R, Chiba K, Hoshino Y, Okumoto T. Fungalmetabolites. Part 11. A potent immunosuppressive activity found in Isaria sinclairii metabolite. J Antibiot (Tokyo) 1994;47:208-215.
73. Wilson R, Allen AJ, Oliver J, Brookman JL, High S, Bulleid NJ. The translocation, folding, assembly and redox-dependent degradation of secretory and membrane proteins in semi-permeabilized mammalian cells. Biochem J 1995;307:679-687.
74. Aniento F, Roche E, Cuervo AM, Knecht E. Uptake and degradation of glyceraldehyde-3-phosphate dehydrogenase by rat liver lysosomes. J Biol Chem 1993;268:10463-10470.
75. Kim J, Hamamoto S, Ravazzola M, Orci L, Schekman R. Uncoupled packaging of amyloid precursor protein and presenilin 1 into coat protein complex II vesicles. J Biol Chem 2005;280:7758-7768.
76. Rowe T, Aridor M, McCaffery JM, Plutner H, Nuoffer C, Balch WE. COPII vesicles derived from mammalian endoplasmic reticulum microsomes recruit COPI. J Cell Biol 1996;135:895-911.