Lipids as targeting signals: Lipid rafts and intracellular trafficking

Traffic

Volumn 5, Issue 4, 2004, Pages 247-254

  Helms, J Bernd ^a   Zurzolo, Chiara ^b,c  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c INSTITUT PASTEUR   (France)

Author keywords

Caveolae; Detergent resistant microdomains (DRMs); GPI anchored proteins; Lipid shells; Rafts; Sorting mechanisms

Indexed keywords

CHOLESTEROL; MEMBRANE LIPID; MEMBRANE PROTEIN; SIGNAL PEPTIDE; SPHINGOLIPID;

CHEMICAL COMPOSITION; CHEMICAL INTERACTION; CYTOSKELETON; DIFFUSION; HYPOTHESIS; INTRACELLULAR TRANSPORT; LIPID TRANSPORT; MEMBRANE COMPONENT; MEMBRANE MODEL; MEMBRANE RAFT; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; THERMODYNAMICS; THERMOSTABILITY;

ANIMALS; CAVEOLAE; ENDOPLASMIC RETICULUM; ENDOSOMES; GOLGI APPARATUS; HUMANS; LYSOSOMES; MEMBRANE MICRODOMAINS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 1842588906     PISSN: 13989219     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2004.0181.x     Document Type: Review

References (80)

1. Brown DA, London E. Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 1998;14:111-136.
2. Silvius JR. Role of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim Biophys Acta 2003;1610:174-183.
3. Heerklotz H. Triton promotes domain formation in lipid raft mixtures. Biophys J 2002;83:2693-2701.
4. Heerklotz H, Szadkowska H, Anderson T, Seelig J. The sensitivity of lipid domains to small perturbations demonstrated by the effect of Triton. J Mol Biol 2003;329:793-799.
5. Edidin M. The state of lipid rafts: From model membranes to cells. Annu Rev Biophys Biomol Struct 2003;32:257-283.
6. Devaux PF, Morris R. Transmembrane asymmetry and lateral domains in biological membranes. Traffic 2004;5:241-246.
7. Mayor S, Rao M. Rafts: Scale dependent, active lipid organization at the cell surface. Traffic 2004;5:231-240.
8. Dietrich C, Bagatolli LA, Volovyk ZN, Thompson NL, Levi M, Jacobson K, Gratton E. Lipid rafts reconstituted in model membranes. Biophys J 2001;80:1417-1428.
9. Anderson RG, Jacobson K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 2002;296:1821-1825.
10. Parton RG. Caveolae - from ultrastructure to molecular mechanisms. Nat Rev Mol Cell Biol 2003;4:162-167.
11. Cheong KH, Zacchetti D, Schneeberger EE, Simons K. VIP17/MAL, a lipid raft-associated protein, is involved in apical transport in MDCK cells. Proc Natl Acad Sci U S A 1999;96:6241-6248.
12. Martin-Belmonte F, Puertollano R, Millan J, Alonso MA, de Marco MC, Albar JP. The MAL proteolipid is necessary for the overall apical delivery of membrane proteins in the polarized epithelial Madin-Darby canine kidney and fischer rat thyroid cell lines The MAL proteolipid is necessary for normal apical transport and accurate sorting of the influenza virus hemagglutinin in Madin-Darby canine kidney cells. Mol Biol Cell 2000;11:2033-2045.
13. Bickel PE, Scherer PE, Schnitzer JE, Oh P, Lisanti MP, Lodish HF. Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J Biol Chem 1997;272:13793-13802.
14. Salzer U, Prohaska R. Stomatin, flotillin-1, and flotillin-2 are major integral proteins of erythrocyte lipid rafts. Blood 2001;97:1141-1143.
15. Scheiffele P, Roth MG, Simons K. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J 1997;16:5501-5508.
16. 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.
17. Bagnat M, Keranen S, Shevchenko A, Simons K. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc Natl Acad Sci U S A 2000;97:3254-3259.
18. Muniz M, Morsomme P, Riezman H. Protein sorting upon exit from the endoplasmic reticulum. Cell 2001;104:313-320.
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. 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.
21. Mayor S, Riezman H. Sorting of GPI-anchored proteins. Nat Rev Mol Cell Biol 2004;5:110-120.
22. Prusiner SB. Genetic and infectious prion diseases. Arch Neurol 1993;50:1129-1153.
23. Simons K, van Meer G. Lipid sorting in epithelial cells. Biochemistry 1988;27:6197-6202.
24. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997;387:569-572.
25. Brown DA, Rose JK. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 1992;68:533-544.
26. Zurzolo C, van't Hof W, van Meer G, Rodriguez-Boulan E. VIP21/caveolin, glycosphingolipid clusters and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells. EMBO J 1994;13:42-53.
27. Lipardi C, Nitsch L, Zurzolo C, Detergent-Insoluble GPI-anchored proteins are apically sorted in fischer rat thyroid cells, but interference with cholesterol or sphingolipids differentially affects detergent insolubility and apical sorting. Mol Biol Cell 2000;11:531-542.
28. 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.
29. 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.
30. Jacob R, Naim HY. Apical membrane proteins are transported in distinct vesicular carriers. Curr Biol 2001;11:1444-1450.
31. Lisanti MP, Caras IW, Davitz MA, Rodriguez-Boulan E. A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells. J Cell Biol 1989;109:2145-2156.
32. Brown DA, Crise B, Rose JK. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science 1989;245:1499-1501.
33. Scheiffele P, Peranen J, Simons K. N-glycans as apical sorting signals in epithelial cells. Nature 1995;378:96-98.
34. Rodriguez-Boulan E, Gonzalez A. Glycans in post-Golgi apical targeting: Sorting signals or structural props? Trends Cell Biol 1999;9:291-294.
35. 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.
36. Lindwasser OW, Rash MD. Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains. J Virol 2001;75:7913-7924.
37. Cerneus DP, Ueffing E, Posthuma G, Strous GJ, van der Ende A. Detergent insolubility of alkaline phosphatase during biosynthetic transport and endocytosis. Role of cholesterol. J Biol Chem 1993;268:3150-3155.
38. van Meer G. Lipid traffic in animal cells. Annu Rev Cell Biol 1989;5:247-275.
39. Eberle HB, Serrano RL, Fullekrug J, Schlosser A, Lehmann WD, Lottspeich F, Kaloyanova D, Wieland FT, Helms JB. Identification and characterization of a novel human plant pathogenesis-related protein that localizes to lipid-enriched microdomains in the Golgi complex. J Cell Sci 2002;115:827-838.
40. Gkantiragas I, Brugger B, Stuven E, Kaloyanova D, Li XY, Lohr K, Lottspeich F, Wieland FT, Helms JB. Sphingomyelin-enriched microdomains at the Golgi complex. Mol Biol Cell 2001;12:1819-1833.
41. Brügger B, Sandhoff R, Wegehingel S, Gorgas K, Malsam J, Helms JB, Lehmann W, Nickel W, Wieland FT. Evidence for segregation of sphingomyelin and cholesterol during formation of COPI-coated vesicles. J Cell Biol 2000;151:507-518.
42. Hansen GH, Niels-Christiansen LL, Thorsen E, Immerdal L, Danielsen EM. Cholesterol depletion of enterocytes. Effect on the Golgi complex and apical membrane trafficking. J Biol Chem 2000;275:5136-5142.
43. Ying M, Grimmer S, Iversen TG, Van Deurs B, Sandvig K. Cholesterol loading induces a block in the exit of VSVG from the TGN. Traffic 2003;4:772-784.
44. 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.
45. Sharma DK, Choudhury A, Singh RD, Wheatley CL, Marks DL, Pagano RE. Glycosphingolipids internalized via caveolar-related endocytosis rapidly merge with the clathrin pathway in early endosomes and form microdomains for recycling. J Biol Chem 2003;278:7564-7572.
46. Pagano RE. Endocytic trafficking of glycosphingolipids in sphingolipid storage diseases. Philos Trans R Soc Lond B Biol Sci 2003;358:885-891.
47. Anderson RG. The caveolae membrane system. Annu Rev Biochem 1998;67:199-225.
48. Parton RG, Joggerst B, Simons K. Regulated internalization of caveolae. J Cell Biol 1994;127:1199-1215.
49. Fujimoto T. GPI-anchored proteins, glycosphingolipids, and sphingomyelin are sequestered to caveolae only after crosslinking. J Histochem Cytochem 1996;44:929-941.
50. Mayor S, Rothberg KG, Maxfield FR. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science 1994;264:1948-1951.
51. Nabi IR, Le PU. Caveolae/raft-dependent endocytosis. J Cell Biol 2003;161:673-677.
52. Sunyach C, Jen A, Deng J, Fitzgerald KT, Frobert Y, Grassi J, McCaffrey MW, Morris R. The mechanism of internalization of glycosylphosphatidylinositol-anchored prion protein Conformal irradiation for pure and mixed oligodendroglioma: The experience of Centre Leon Berard Lyon. EMBO J 2003;22:3591-3601.
53. Conese M, Nykjaer A, Petersen CM, Cremona O, Pardi R, Andreasen PA, Gliemann J, Christensen EI, Blasi F. α-2 Macroglobulin receptor/Ldl receptor-related protein (Lrp)-dependent internalization of the urokinase receptor. J Cell Biol 1995;131:1609-1622.
54. Triantafilou K, Triantafilou M, Dedrick RL. A CD14-independent LPS receptor cluster. Nat Immunol 2001;2:338-345.
55. 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.
56. Puri V, Watanabe R, Singh RD, Dominguez M, Brown JC, Wheatley CL, Marks DL, Pagano RE. Clathrin-dependent and -independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways. J Cell Biol 2001;154:535-547.
57. Lamaze C, Dujeancourt A, Baba T, Lo CG, Benmerah A, Dautry-Varsat A. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol Cell 2001;7: 661-671.
58. Chatterjee S, Mayor S. The GPI-anchor and protein sorting. Cell Mol Life Sci 2001;58:1969-1987.
59. Abrami L, Liu S, Cosson P, Leppla SH, van der Goot FG. Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process. J Cell Biol 2003;160:321-328.
60. Ghosh RN, Mallet WG, Soe TT, McGraw TE, Maxfield FR. An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells. J Cell Biol 1998;142:923-936.
61. Mallard F, Tang BL, Galli T, Tenza D, Saint-Pol A, Yue X, Antony C, Hong W, Goud B, Johannes L. Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J Cell Biol 2002;156:653-664.
62. Gagescu R, Demaurex N, Parton RG, Hunziker W, Huber LA, Gruenberg J. The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol Biol Cell 2000;11:2775-2791.
63. Kobayashi T, Stang E, Fang KS, de Moerloose P, Parton RG, Gruenberg J. A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 1998;392:193-197.
64. Simons K, Gruenberg J. Jamming the endosomal system: Lipid rafts and lysosomal storage diseases. Trends Cell Biol 2000;10:459-462.
65. Mobius W, van Donselaar E, Ohno-Iwashita Y, Shimada Y, Heijnen HF, Slot JW, Gauze HJ. Recycling compartments and the internal vesicles of multivesicular bodies harbor most of the cholesterol found in the endocytic pathway. Traffic 2003;4:222-231.
66. Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, Mobius W, Hoernschemeyer J, Slot JW, Geuze HJ, Stoorvogel W. Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem 2003:278:10963-10972.
67. Gould SJ, Booth AM, Hildreth JE. The Trojan exosome hypothesis. Proc Natl Acad Sci U S A 2003;100:10592-10597.
68. Kurzchalia TV, Dupree P, Parton RG, Kellner R, Virta H, Lehnert M et al. VIP21, a 21-kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles. J Cell Biol 1992;118:1003-1014.
69. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell 1992;68:673-682.
70. Lipardi C, Mora R, Colomer V, Paladino S, Nitsch L, Rodriguez-Boulan E at al. Caveolin transfection results in caveolae formation but not apical sorting of glycosylphosphatidylinositol (GPI) -anchored proteins in epithelial cells. J Cell Biol 1998;140:617-626.
71. Fra AM, Williamson E, Simons K, Parton RG. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci U S A 1995;92:8655-8659.
72. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B et al. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001;293:2449-2452.
73. Schubert W, Frank PG, Razani B, Park DS, Chow CW, Lisanti MP. Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo. J Biol Chem 2001;276:48619-48622.
74. Thomsen P, Roepstorff K, Stahlhut M, van Deurs B. Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol Biol Cell 2002;13:238-250.
75. Pelkmans L, Puntener D, Helenius A. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 2002;296:535-539.
76. Pelkmans L, Kartenbeck J, Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 2001;3:473-483.
77. Torgersen ML, Skretting G, van Deurs B, Sandvig K. Internalization of cholera toxin by different endocytic mechanisms. J Cell Sci 2001;114:3737-3747.
78. Nichols BJ. A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat Cell Biol 2002;4:374-378.
79. Schnitzer JE, Liu J, Oh P. Endothelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP, NSF, SNAP, annexins, and GTPases. J Biol Chem 1995;270:14399-14404.
80. Norkin LC, Anderson HA, Wolfrom SA, Oppenheim A. Caveolar endocytosis of simian virus 40 is followed by brefeldin A-sensitive transport to the endoplasmic reticulum, where the virus disassembles. J Virol 2002;76:5156-5166.