Stable cell surface expression of GPI-anchored proteins, but not intracellular transport, depends on their fatty acid structure

Traffic

Volumn 15, Issue 12, 2014, Pages 1305-1329

  Jaensch, Nina ^a   Corrêa, Ivan R ^b   Watanabe, Reika ^a,c  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b NEW ENGLAND BIOLABS   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cholesterol; Clathrin independent carrier; Endocytosis; Glycosylphosphatidylinositol anchored proteins; Golgi apparatus; GPI enriched early endosomal compartment; Intracellular protein transport; Lipid rafts; Lipid remodeling; Ordered lipid domains; SNAP tag technology

Indexed keywords

ACTIN; CD59 ANTIGEN; CHOLESTEROL; DYNAMIN; FATTY ACID; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; LIPID LINKED PROTEIN; LOW DENSITY LIPOPROTEIN; PHOSPHATIDYLINOSITOL; SATURATED FATTY ACID; SF CD59; SPHINGOLIPID; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID;

ARTICLE; CELL MEMBRANE; CELL MEMBRANE TRANSPORT; CELL MUTANT; CELL SURFACE; CHO CELL LINE; ENDOCYTOSIS; FLOW CYTOMETRY; INTRACELLULAR TRANSPORT; LIPID COMPOSITION; LIPID TRANSPORT; MEMBRANE POTENTIAL; MEMBRANE TRANSPORT; SECRETORY VESICLE; TRANS GOLGI NETWORK; WILD TYPE; ANIMAL; CHEMISTRY; CRICETULUS; ENDOSOME; HAMSTER; METABOLISM; PROTEIN TRANSPORT;

ANIMALS; CELL MEMBRANE; CHO CELLS; CHOLESTEROL; CRICETINAE; CRICETULUS; ENDOSOMES; FATTY ACIDS; GPI-LINKED PROTEINS; PROTEIN TRANSPORT;

EID: 84911363929     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12224     Document Type: Article

References (72)

1. Kinoshita T, Fujita M, Maeda Y. Biosynthesis, remodelling and functions of mammalian GPI-anchored proteins: recent progress. J Biochem 2008;144:287-294.
2. Maeda Y, Kinoshita T. Structural remodeling, trafficking and functions of glycosylphosphatidylinositol-anchored proteins. Prog Lipid Res 2011;50:411-424.
3. Fujita M, Kinoshita T. GPI-anchor remodeling: potential functions of GPI-anchors in intracellular trafficking and membrane dynamics. Biochim Biophys Acta 2012;1821:1050-1058.
4. 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.
5. 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.
6. 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.
7. 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.
8. Lisanti MP, Sargiacomo M, Graeve L, Saltiel AR, Rodriguez-Boulan E. Polarized apical distribution of glycosyl-phosphatidylinositol-anchored proteins in a renal epithelial cell line. Proc Natl Acad Sci U S A 1988;85:9557-9561.
9. Benting JH, Rietveld AG, Simons K. N-Glycans mediate the apical sorting of a GPI-anchored, raft-associated protein in Madin-Darby canine kidney cells. J Cell Biol 1999;146:313-320.
10. McGwire GB, Becker RP, Skidgel RA. Carboxypeptidase M, a glycosylphosphatidylinositol-anchored protein, is localized on both the apical and basolateral domains of polarized Madin-Darby canine kidney cells. J Biol Chem 1999;274:31632-31640.
11. Skretting G, Torgersen ML, van Deurs B, Sandvig K. Endocytic mechanisms responsible for uptake of GPI-linked diphtheria toxin receptor. J Cell Sci 1999;112:3899-3909.
12. Ricci V, Galmiche A, Doye A, Necchi V, Solcia E, Boquet P. High cell sensitivity to Helicobacter pylori VacA toxin depends on a GPI-anchored protein and is not blocked by inhibition of the clathrin-mediated pathway of endocytosis. Mol Biol Cell 2000;11:3897-3909.
13. Sabharanjak S, Sharma P, Parton RG, Mayor S. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2002;2:411-423.
14. Sharma P, Sabharanjak S, Mayor S. Endocytosis of lipid rafts: an identity crisis. Semin Cell Dev Biol 2002;13:205-214.
15. Chadda R, Howes MT, Plowman SJ, Hancock JF, Parton RG, Mayor S. Cholesterol-sensitive Cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway. Traffic 2007;8:702-717.
16. Kumari S, Mayor S. ARF1 is directly involved in dynamin-independent endocytosis. Nat Cell Biol 2008;10:30-41.
17. Bonifacino JS, Glick BS. The mechanisms of vesicle budding and fusion. Cell 2004;116:153-166.
18. Fujita M, Watanabe R, Jaensch N, Romanova-Michaelides M, Satoh T, Kato M, Riezman H, Yamaguchi Y, Maeda Y, Kinoshita T. Sorting of GPI-anchored proteins into ER exit sites by p24 proteins is dependent on remodeled GPI. J Cell Biol 2011;194:61-75.
19. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997;387:569-572.
20. Ewers H, Romer W, Smith AE, Bacia K, Dmitrieff S, Chai W, Mancini R, Kartenbeck J, Chambon V, Berland L, Oppenheim A, Schwarzmann G, Feizi T, Schwille P, Sens P, et al. GM1 structure determines SV40-induced membrane invagination and infection. Nat Cell Biol 2010;12:11-18 sup pp 11-12.
21. Chinnapen DJ, Hsieh WT, te Welscher YM, Saslowsky DE, Kaoutzani L, Brandsma E, D'Auria L, Park H, Wagner JS, Drake KR, Kang M, Benjamin T, Ullman MD, Costello CE, Kenworthy AK, et al. Lipid sorting by ceramide structure from plasma membrane to ER for the cholera toxin receptor ganglioside GM1. Dev Cell 2012;23:573-586.
22. 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.
23. Paladino S, Sarnataro D, Pillich R, Tivodar S, Nitsch L, Zurzolo C. Protein oligomerization modulates raft partitioning and apical sorting of GPI-anchored proteins. J Cell Biol 2004;167:699-709.
24. Chang WJ, Rothberg KG, Kamen BA, Anderson RG. Lowering the cholesterol content of MA104 cells inhibits receptor-mediated transport of folate. J Cell Biol 1992;118:63-69.
25. Stevens VL, Tang J. Fumonisin B1-induced sphingolipid depletion inhibits vitamin uptake via the glycosylphosphatidylinositol-anchored folate receptor. J Biol Chem 1997;272:18020-18025.
26. Mayor S, Sabharanjak S, Maxfield FR. Cholesterol-dependent retention of GPI-anchored proteins in endosomes. EMBO J 1998;17:4626-4638.
27. Chatterjee S, Smith ER, Hanada K, Stevens VL, Mayor S. GPI anchoring leads to sphingolipid-dependent retention of endocytosed proteins in the recycling endosomal compartment. EMBO J 2001;20:1583-1592.
28. Mayinger P. Phosphoinositides and vesicular membrane traffic. Biochim Biophys Acta 2012;1821:1104-1113.
29. Kwik J, Boyle S, Fooksman D, Margolis L, Sheetz MP, Edidin M. Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4, 5-bisphosphate-dependent organization of cell actin. Proc Natl Acad Sci U S A 2003;100:13964-13969.
30. Lu D, Sun HQ, Wang H, Barylko B, Fukata Y, Fukata M, Albanesi JP, Yin HL. Phosphatidylinositol 4-kinase IIalpha is palmitoylated by Golgi-localized palmitoyltransferases in cholesterol-dependent manner. J Biol Chem 2012;287:21856-21865.
31. Howard MF, Murakami Y, Pagnamenta AT, Daumer-Haas C, Fischer B, Hecht J, Keays DA, Knight SJ, Kolsch U, Kruger U, Leiz S, Maeda Y, Mitchell D, Mundlos S, Phillips JA III, et al. Mutations in PGAP3 impair GPI-anchor maturation, causing a subtype of hyperphosphatasia with mental retardation. Am J Hum Genet 2014;94:278-287.
32. Murakami H, Wang Y, Hasuwa H, Maeda Y, Kinoshita T, Murakami Y. Enhanced response of T lymphocytes from Pgap3 knockout mouse: insight into roles of fatty acid remodeling of GPI anchored proteins. Biochem Biophys Res Commun 2012;417:1235-1241.
33. Wang Y, Murakami Y, Yasui T, Wakana S, Kikutani H, Kinoshita T, Maeda Y. Significance of glycosylphosphatidylinositol-anchored protein enrichment in lipid rafts for the control of autoimmunity. J Biol Chem 2013;288:25490-25499.
34. Gautier A, Juillerat A, Heinis C, Correa IR Jr, Kindermann M, Beaufils F, Johnsson K. An engineered protein tag for multiprotein labeling in living cells. Chem Biol 2008;15:128-136.
35. Seong J, Wang Y, Kinoshita T, Maeda Y. Implication of lipid moiety in oligomerization and immunoreactivities of GPI-anchored proteins. J Lipid Res 2013;54:1077-1091.
36. Munro S. Lipid rafts: elusive or illusive? Cell 2003;115:377-388.
37. Schroeder R, London E, Brown D. Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior. Proc Natl Acad Sci U S A 1994;91:12130-12134.
38. Wang Y, Thiele C, Huttner WB. Cholesterol is required for the formation of regulated and constitutive secretory vesicles from the trans-Golgi network. Traffic 2000;1:952-962.
39. Stuven E, Porat A, Shimron F, Fass E, Kaloyanova D, Brugger B, Wieland FT, Elazar Z, Helms JB. Intra-Golgi protein transport depends on a cholesterol balance in the lipid membrane. J Biol Chem 2003;278:53112-53122.
40. Ridsdale A, Denis M, Gougeon PY, Ngsee JK, Presley JF, Zha X. Cholesterol is required for efficient endoplasmic reticulum-to-Golgi transport of secretory membrane proteins. Mol Biol Cell 2006;17:1593-1605.
41. Bonnon C, Wendeler MW, Paccaud JP, Hauri HP. Selective export of human GPI-anchored proteins from the endoplasmic reticulum. J Cell Sci 2010;123:1705-1715.
42. Castillon GA, Michon L, Watanabe R. Apical sorting of lysoGPI-anchored proteins occurs independent of association with detergent-resistant membranes but dependent on their N-glycosylation. Mol Biol Cell 2013;24:2021-2033.
43. Cole NB, Donaldson JG. Releasable SNAP-tag probes for studying endocytosis and recycling. ACS Chem Biol 2012;7:464-469.
44. Harper CB, Martin S, Nguyen TH, Daniels SJ, Lavidis NA, Popoff MR, Hadzic G, Mariana A, Chau N, McCluskey A, Robinson PJ, Meunier FA. Dynamin inhibition blocks botulinum neurotoxin type A endocytosis in neurons and delays botulism. J Biol Chem 2011;286:35966-35976.
45. Bhagatji P, Leventis R, Comeau J, Refaei M, Silvius JR. Steric and not structure-specific factors dictate the endocytic mechanism of glycosylphosphatidylinositol-anchored proteins. J Cell Biol 2009;186:615-628.
46. Nonnenmacher M, Weber T. Adeno-associated virus 2 infection requires endocytosis through the CLIC/GEEC pathway. Cell Host Microbe 2011;10:563-576.
47. Yahara N, Ueda T, Sato K, Nakano A. Multiple roles of Arf1 GTPase in the yeast exocytic and endocytic pathways. Mol Biol Cell 2001;12:221-238.
48. Volpicelli-Daley LA, Li Y, Zhang CJ, Kahn RA. Isoform-selective effects of the depletion of ADP-ribosylation factors 1-5 on membrane traffic. Mol Biol Cell 2005;16:4495-4508.
49. Bordier C. Phase separation of integral membrane proteins in Triton X-114 solution. J Biol Chem 1981;256:1604-1607.
50. Loizides-Mangold U, David FP, Nesatyy VJ, Kinoshita T, Riezman H. Glycosylphosphatidylinositol anchors regulate glycosphingolipid levels. J Lipid Res 2012;53:1522-1534.
51. Zurzolo C, Le Bivic A, Quaroni A, Nitsch L, Rodriguez-Boulan E. Modulation of transcytotic and direct targeting pathways in a polarized thyroid cell line. EMBO J 1992;11:2337-2344.
52. Mayor S, Rothberg KG, Maxfield FR. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science 1994;264:1948-1951.
53. Howes MT, Kirkham M, Riches J, Cortese K, Walser PJ, Simpson F, Hill MM, Jones A, Lundmark R, Lindsay MR, Hernandez-Deviez DJ, Hadzic G, McCluskey A, Bashir R, Liu L, et al. Clathrin-independent carriers form a high capacity endocytic sorting system at the leading edge of migrating cells. J Cell Biol 2010;190:675-691.
54. Fujita M, Kinoshita T. Structural remodeling of GPI anchors during biosynthesis and after attachment to proteins. FEBS Lett 2010;584:1670-1677.
55. 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.
56. 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.
57. Castillon GA, Watanabe R, Taylor M, Schwabe TME, Riezman H. Concentration of GPI-anchored proteins upon ER exit in yeast. Traffic 2009;10:186-200.
58. Hanzal-Bayer MF, Hancock JF. Lipid rafts and membrane traffic. FEBS Lett 2007;581:2098-2104.
59. Kraft ML. Plasma membrane organization and function: moving past lipid rafts. Mol Biol Cell 2013;24:2765-2768.
60. 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.
61. Goswami D, Gowrishankar K, Bilgrami S, Ghosh S, Raghupathy R, Chadda R, Vishwakarma R, Rao M, Mayor S. Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 2008;135:1085-1097.
62. van Zanten TS, Cambi A, Koopman M, Joosten B, Figdor CG, Garcia-Parajo MF. Hotspots of GPI-anchored proteins and integrin nanoclusters function as nucleation sites for cell adhesion. Proc Natl Acad Sci U S A 2009;106:18557-18562.
63. Suzuki KG, Kasai RS, Hirosawa KM, Nemoto YL, Ishibashi M, Miwa Y, Fujiwara TK, Kusumi A. Transient GPI-anchored protein homodimers are units for raft organization and function. Nat Chem Biol 2012;8:774-783.
64. 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.
65. Paladino S, Lebreton S, Tivodar S, Formiggini F, Ossato G, Gratton E, Tramier M, Coppey-Moisan M, Zurzolo C. Golgi sorting regulates organization and activity of GPI proteins at apical membranes. Nat Chem Biol 2014;10:350-357.
66. Refaei M, Leventis R, Silvius JR. Assessment of the roles of ordered lipid microdomains in post-endocytic trafficking of glycosyl-phosphatidylinositol-anchored proteins in mammalian fibroblasts. Traffic 2011;12:1012-1024.
67. Nichols B. Endocytosis of lipid-anchored proteins: excluding GEECs from the crowd. J Cell Biol 2009;186:457-459.
68. Fivaz M, Vilbois F, Thurnheer S, Pasquali C, Abrami L, Bickel PE, Parton RG, van der Goot FG. Differential sorting and fate of endocytosed GPI-anchored proteins. EMBO J 2002;21:3989-4000.
69. 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.
70. O'Brien JS, Rouser G. The fatty acid composition of brain sphingolipids: sphingomyelin, ceramide, cerebroside, and cerebroside sulfate. J Lipid Res 1964;5:339-342.
71. Ries J, Kaplan C, Platonova E, Eghlidi H, Ewers H. A simple, versatile method for GFP-based super-resolution microscopy via nanobodies. Nat Methods 2012;9:582-584.
72. Schuck S, Honsho M, Ekroos K, Shevchenko A, Simons K. Resistance of cell membranes to different detergents. Proc Natl Acad Sci U S A 2003;100:5795-5800.