Lipid rafts and clathrin cooperate in the internalization of PrPC in epithelial FRT cells

PLoS ONE

Volumn 4, Issue 6, 2009, Pages

  Sarnataro, Daniela ^a   Caputo, Anna ^a,b   Casanova, Philippe ^b   Puri, Claudia ^c   Paladino, Simona ^a,d   Tivodar, Simona S ^a   Campana, Vincenza ^a,b   Tacchetti, Carlo ^c,e   Zurzolo, Chiara ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b INSTITUT PASTEUR   (France)

^c FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^d CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^e UNIVERSITY OF GENOA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CHOLESTEROL; CLATHRIN; DYNAMIN II; EPIDERMAL GROWTH FACTOR RECEPTOR PATHWAY SUBSTRATE 15; PRION PROTEIN; PROTEIN CDC42; CALCIUM BINDING PROTEIN; EPS15 PROTEIN, RAT; SIGNAL PEPTIDE;

ANIMAL CELL; ARTICLE; CAVEOLA; CELL LINE; CONTROLLED STUDY; ENDOCYTOSIS; EPITHELIUM CELL; IMMUNOPRECIPITATION; INTERNALIZATION; LIPID RAFT; NONHUMAN; PRION; PROTEIN EXPRESSION; RAT; STRAIN DIFFERENCE; VIRUS REPLICATION; VIRUS VIRULENCE; ANIMAL; CELL MEMBRANE; CHEMISTRY; DOMINANT GENE; FISCHER 344 RAT; METABOLISM; THYROID GLAND;

RATTUS;

ANIMALS; CALCIUM-BINDING PROTEINS; CAVEOLAE; CAVEOLIN 1; CDC42 GTP-BINDING PROTEIN; CHOLESTEROL; CLATHRIN; DYNAMIN II; ENDOCYTOSIS; GENES, DOMINANT; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE MICRODOMAINS; PRIONS; RATS; RATS, INBRED F344; THYROID GLAND;

EID: 67149137755     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005829     Document Type: Article

References (83)

1. Harris DA (1999) Cellular biology of prion diseases. Clin Microbiol Rev 12: 429-444.
2. Caughey B, Raymond GJ (1991) The scrapie-associated form of PrP is made from a cell surface precursor that is both protease- and phospholipase-sensitive. J Biol Chem 266: 18217-18223.
3. Campana V, Sarnataro D, Zurzolo C (2005) The highways and byways of prion protein trafficking. Trends Cell Biol 15: 102-111.
4. Prusiner SB (1998) Prions. Proc Natl Acad Sci U S A 95: 13363-13383.
5. Borchelt DR, Taraboulos A, Prusiner SB (1992) Evidence for synthesis of scrapie prion proteins in the endocytic pathway. J Biol Chem 267: 16188-16199.
6. Prado MA, Alves-Silva J, Magalhaes AC, Prado VF, Linden R, et al. (2004) PrPc on the road: trafficking of the cellular prion protein. J Neurochem 88: 769-781.
7. Taraboulos A, Scott M, Semenov A, Avrahami D, Laszlo L, et al. (1995) Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibit formation of the scrapie isoform. J Cell Biol 129: 121-132.
8. Vey M, Pilkuhn S, Wille H, Nixon R, DeArmond SJ, et al. (1996) Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains. Proc Natl Acad Sci U S A 93: 14945-14949.
9. Kaneko K, Vey M, Scott M, Pilkuhn S, Cohen FE, et al. (1997) COOH-terminal sequence of the cellular prion protein directs subcellular trafficking and controls conversion into the scrapie isoform. Proc Natl Acad Sci U S A 94: 2333-2338.
10. Naslavsky N, Stein R, Yanai A, Friedlander G, Taraboulos A (1997) Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform. J Biol Chem 272: 6324-6331.
11. Taylor DR, Hooper NM (2006) The prion protein and lipid rafts. Mol Membr Biol 23: 89-99.
12. Marella M, Lehmann S, Grassi J, Chabry J (2002) Filipin prevents pathological prion protein accumulation by reducing endocytosis and inducing cellular PrP release. J Biol Chem 277: 25457-25464. Epub 2002 May 6.
13. Bonifacino JS, Lippincott-Schwartz J (2003) Coat proteins: shaping membrane transport. Nat Rev Mol Cell Biol 4: 409-414.
14. Lamaze C, Schmid SL (1995) The emergence of clathrin-independent pinocytic pathways. Curr Opin Cell Biol 7: 573-580.
15. Kirkham M, Parton RG (2005) Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. Biochim Biophys Acta 1746: 349-363.
16. Pelkmans L (2005) Secrets of caveolae- and lipid raft-mediated endocytosis revealed by mammalian viruses. Biochim Biophys Acta 1746: 295-304.
17. Damm EM, Pelkmans L, Kartenbeck J, Mezzacasa A, Kurzchalia T, et al. (2005) Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 168: 477-488.
18. Parton RG, Richards AA (2003) Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4: 724-738.
19. Parton RG, Simons K (2007) The multiple faces of caveolae. Nat Rev Mol Cell Biol 8: 185-194.
20. Parton RG, Hanzal-Bayer M, Hancock JF (2006) Biogenesis of caveolae: a structural model for caveolin-induced domain formation. J Cell Sci 119: 787-796.
21. Parton RG, Joggerst B, Simons K (1994) Regulated internalization of caveolae. J Cell Biol 127: 1199-1215.
22. Pelkmans L, Kartenbeck J, Helenius A (2001) Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 3: 473-483.
23. Pelkmans L, Burli T, Zerial M, Helenius A (2004) Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118: 767-780.
24. van der Goot FG, Harder T (2001) Raft membrane domains: from a liquid-ordered membrane phase to a site of pathogen attack. Semin Immunol 13: 89-97.
25. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL (2003) Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 5: 410-421.
26. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, et al. (2005) Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci U S A 102: 270-2765.
27. Deinhardt K, Berninghausen O, Willison HJ, Hopkins CR, Schiavo G (2006) Tetanus toxin is internalized by a sequential clathrin-dependent mechanism initiated within lipid microdomains and independent of epsin1. J Cell Biol 174: 459-471.
28. Orlandi PA, Fishman PH (1998) Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J Cell Biol 141: 905-915.
29. Sabharanjak S, Sharma P, Parton RG, Mayor S (2002) GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2: 411-423.
30. Stoddart A, Dykstra ML, Brown BK, Song W, Pierce SK, et al. (2002) Lipid rafts unite signaling cascades with clathrin to regulate BCR internalization. Immunity 17: 451-462.
31. Torgersen ML, Skretting G, van Deurs B, Sandvig K (2001) Internalization of cholera toxin by different endocytic mechanisms. J Cell Sci 114: 3737-3747.
32. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387: 569-572.
33. Brown CM, Petersen NO (1998) An image correlation analysis of the distribution of clathrin associated adaptor protein (AP-2) at the plasma membrane. J Cell Sci 111 (Pt 2): 271-281.
34. Puri C, Tosoni D, Comai R, Rabellino A, Segat D, et al. (2005) Relationships between EGFR signaling-competent and endocytosis-competent membrane microdomains. Mol Biol Cell 16: 2704-2718.
35. Shogomori H, Futerman AH (2001) Cholera toxin is found in detergent-insoluble rafts/domains at the cell surface of hippocampal neurons but is internalized via a raft-independent mechanism. J Biol Chem 276: 9182-9188.
36. Mayor S, Rothberg KG, Maxfield FR (1994) Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science 264: 1948-1951.
37. Mayor S, Riezman H (2004) Sorting GPI-anchored proteins. Nat Rev Mol Cell Biol 5: 110-120.
38. Taylor DR, Hooper NM (2007) The low-density lipoprotein receptor-related protein 1 (LRP1) mediates the endocytosis of the cellular prion protein. Biochem J 402: 17-23.
39. Taylor DR, Watt NT, Perera WS, Hooper NM (2005) Assigning functions to distinct regions of the N-terminus of the prion protein that are involved in its copper-stimulated, clathrin-dependent endocytosis. J Cell Sci 118: 5141-5153.
40. Sunyach C, Jen A, Deng J, Fitzgerald KT, Frobert Y, et al. (2003) The mechanism of internalization of glycosylphosphatidylinositol-anchored prion protein. Embo J 22: 3591-3601.
41. Shyng SL, Heuser JE, Harris DA (1994) A glycolipid-anchored prion protein is endocytosed via clathrin-coated pits. J Cell Biol 125: 1239-1250.
42. Galvan C, Camoletto PG, Dotti CG, Aguzzi A, Ledesma MD (2005) Proper axonal distribution of PrP(C) depends on cholesterol-sphingomyelin-enriched membrane domains and is developmentally regulated in hippocampal neurons. Mol Cell Neurosci 30: 304-315.
43. Peters PJ, Mironov A Jr., Peretz D, van Donselaar E, Leclerc E, et al. (2003) Trafficking of prion proteins through a caveolae-mediated endosomal pathway. J Cell Biol 162: 703-717.
44. Morris RJ, Parkyn CJ, Jen A (2006) Traffic of prion protein between different compartments on the neuronal surface, and the propagation of prion disease. FEBS Lett 580: 5565-5571.
45. Lipardi C, Mora R, Colomer V, Paladino S, Nitsch L, et al. (1998) Caveolin transfection results in caveolae formation but not apical sorting of glycosylphosphatidylinositol (GPI)-anchored proteins in epithelial cells. J Cell Biol 140: 617-626.
46. Sarnataro D, Paladino S, Campana V, Grassi J, Nitsch L, et al. (2002) PrPC is sorted to the basolateral membrane of epithelial cells independently of its association with rafts. Traffic 3: 810-821.
47. Sarnataro D, Campana V, Paladino S, Stornaiuolo M, Nitsch L, et al. (2004) PrPC Association with Lipid Rafts in the Early Secretory Pathway Stabilizes Its Cellular Conformation. Mol Biol Cell 15: 4031-4042.
48. Campana V, Sarnataro D, Fasano C, Casanova P, Paladino S, et al. (2006) Detergent-resistant membrane domains but not the proteasome are involved in the misfolding of a PrP mutant retained in the endoplasmic reticulum. J Cell Sci 119: 433-442.
49. Hommelgaard AM, Roepstorff K, Vilhardt F, Torgersen ML, Sandvig K, et al. (2005) Caveolae: stable membrane domains with a potential for internalization. Traffic 6: 720-724.
50. Paladino S, Sarnataro D, Pillich R, Tivodar S, Nitsch L, et al. (2004) Protein oligomerization modulates raft partitioning and apical sorting of GPI-anchored proteins. J Cell Biol 167: 699-709.
51. Keller P, Simons K (1998) Cholesterol is required for surface transport of influenza virus hemagglutinin. J Cell Biol 140: 1357-1367.
52. Madore N, Smith KL, Graham CH, Jen A, Brady K, et al. (1999) Functionally different GPI proteins are organized in different domains on the neuronal surface. Embo J 18: 6917-6926.
53. Zurzolo C, Lisanti MP, Caras IW, Nitsch L, Rodriguez-Boulan E (1993) Glycosylphosphatidylinositol-anchored proteins are preferentially targeted to the basolateral surface in Fischer rat thyroid epithelial cells. J Cell Biol 121: 1031-1039.
54. Subtil A, Gaidarov I, Kobylarz K, Lampson MA, Keen JH, et al. (1999) Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc Natl Acad Sci U S A 96: 6775-6780.
55. Rodal SK, Skretting G, Garred O, Vilhardt F, van Deurs B, et al. (1999) Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 10: 961-974.
56. Parkyn CJ, Vermeulen EG, Mootoosamy RC, Sunyach C, Jacobsen C, et al. (2008) LRP1 controls biosynthetic and endocytic trafficking of neuronal prion protein. J Cell Sci 121: 773-783.
57. Tkachenko E, Lutgens E, Stan RV, Simons M (2004) Fibroblast growth factor 2 endocytosis in endothelial cells proceed via syndecan-4-dependent activation of Rac1 and a Cdc42-dependent macropinocytic pathway. J Cell Sci 117: 3189-3199.
58. Gauthier NC, Monzo P, Kaddai V, Doye A, Ricci V, et al. (2005) Helicobacter pylori VacA cytotoxin: a probe for a clathrin-independent and Cdc42-dependent pinocytic pathway routed to late endosomes. Mol Biol Cell 16: 4852-4866.
59. Lamaze C, Chuang TH, Terlecky LJ, Bokoch GM, Schmid SL (1996) Regulation of receptor-mediated endocytosis by Rho and Rac. Nature 382: 177-179.
60. Nabi IR, Le PU (2003) Caveolae/raft-dependent endocytosis. J Cell Biol 161: 673-677.
61. Sauvonnet N, Dujeancourt A, Dautry-Varsat A (2005) Cortactin and dynamin are required for the clathrin-independent endocytosis of gammac cytokine receptor. J Cell Biol 168: 155-163.
62. Damke H, Baba T, Warnock DE, Schmid SL (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127: 915-934.
63. McNiven MA, Cao H, Pitts KR, Yoon Y (2000) The dynamin family of mechanoenzymes: pinching in new places. Trends Biochem Sci 25: 115-120.
64. Cao H, Garcia F, McNiven MA (1998) Differential distribution of dynamin isoforms in mammalian cells. Mol Biol Cell 9: 2595-2609.
65. Lamaze C, Dujeancourt A, Baba T, Lo CG, Benmerah A, et al. (2001) Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol Cell 7: 661-671.
66. Benmerah A, Poupon V, Cerf-Bensussan N, Dautry-Varsat A (2000) Mapping of Eps15 domains involved in its targeting to clathrin-coated pits. J Biol Chem 275: 3288-3295.
67. Motley A, Bright NA, Seaman MN, Robinson MS (2003) Clathrin-mediated endocytosis in AP-2-depleted cells. J Cell Biol 162: 909-918.
68. Heuser JE, Anderson RG (1989) Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 108: 389-400.
69. Schatzl HM, Laszlo L, Holtzman DM, Tatzelt J, DeArmond SJ, et al. (1997) A hypothalamic neuronal cell line persistently infected with scrapie prions exhibits apoptosis. J Virol 71: 8821-8831.
70. Deinhardt K, Reversi A, Berninghausen O, Hopkins CR, Schiavo G (2007) Neurotrophins Redirect p75NTR from a clathrin-independent to a clathrin-dependent endocytic pathway coupled to axonal transport. Traffic 8: 1736-1749.
71. Mahal SP, Baker CA, Demczyk CA, Smith EW, Julius C, et al. (2007) Prion strain discrimination in cell culture: the cell panel assay. Proc Natl Acad Sci U S A 104: 20908-20913.
72. Paladino S, Sarnataro D, Tivodar S, Zurzolo C (2007) Oligomerization is a specific requirement for apical sorting of glycosyl-phosphatidylinositol-anchored proteins but not for non-raft-associated apical proteins. Traffic 8: 251-258.
73. Pimpinelli F, Lehmann S, Maridonneau-Parini I (2005) The scrapie prion protein is present in flotillin-1-positive vesicles in central- but not peripheral-derived neuronal cell lines. Eur J Neurosci 21: 2063-2072.
74. Benmerah A, Bayrou M, Cerf-Bensussan N, Dautry-Varsat A (1999) Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J Cell Sci 112 (Pt 9): 1303-1311.
75. Westergard L, Christensen HM, Harris DA (2007) The cellular prion protein (PrP(C)): its physiological function and role in disease. Biochim Biophys Acta 1772: 629-644.
76. Steer CJ, Bisher M, Blumenthal R, Steven AC (1984) Detection of membrane cholesterol by filipin in isolated rat liver coated vesicles is dependent upon removal of the clathrin coat. J Cell Biol 99: 315-319.
77. Abrami L, Liu S, Cosson P, Leppla SH, van der Goot FG (2003) Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process. J Cell Biol 160: 321-328.
78. Nathke IS, Heuser J, Lupas A, Stock J, Turck CW, et al. (1992) Folding and trimerization of clathrin subunits at the triskelion hub. Cell 68: 899-910.
79. Zurzolo C, Le Bivic A, Rodriguez-Boulan E (1994) Cell surface Biotynilation techniques Cell Biology. Handbook AL, ed. Academic Press. Inc. pp 185-192.
80. Sarnataro D, Grimaldi C, Pisanti S, Gazzerro P, Laezza C, et al. (2005) Plasma membrane and lysosomal localization of CB1 cannabinoid receptor are dependent on lipid rafts and regulated by anandamide in human breast cancer cells. FEBS Lett 579: 6343-6349.
81. Broquet AH, Thomas G, Masliah J, Trugnan G, Bachelet M (2003) Expression of the molecular chaperone Hsp70 in detergent-resistant microdomains correlates with its membrane delivery and release. J Biol Chem 278: 21601-21606.
82. Stuermer CA, Lang DM, Kirsch F, Wiechers M, Deininger SO, et al. (2001) Glycosylphosphatidyl inositol-anchored proteins and fyn kinase assemble in noncaveolar plasma membrane microdomains defined by reggie-1 and -2. Mol Biol Cell 12: 3031-3045.
83. Galli T, Chilcote T, Mundigl O, Binz T, Niemann H, et al. (1994) Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells. J Cell Biol 125: 1015-1024.