Rab12 Localizes to Shiga Toxin-Induced Plasma Membrane Invaginations and Controls Toxin Transport

Traffic

Volumn 15, Issue 7, 2014, Pages 772-787

  Rydell, Gustaf E ^a,b   Renard, Henri François ^a,b   Garcia Castillo, Maria Daniela ^a,b   Dingli, Florent ^a   Loew, Damarys ^a   Lamaze, Christophe ^a,b   Römer, Winfried ^a,b,c   Johannes, Ludger ^a,b  

^a INSTITUT CURIE   (France)

^b CNRS UMR3666   (France)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Clathrin independent endocytosis; Intracellular trafficking; Membrane tubules; RabGTPase; Retrograde transport; Shiga toxin B subunit; STxB

Indexed keywords

CELL MEMBRANE PROTEIN; CLATHRIN; GUANOSINE TRIPHOSPHATASE; PROTEIN RAB12; PROTEIN TGN46; RAB PROTEIN; SHIGA TOXIN; SHIGA TOXIN B; SOMATOMEDIN B RECEPTOR; UNCLASSIFIED DRUG; VEROTOXIN 1; RAB12 PROTEIN, HUMAN;

ARTICLE; CELL MEMBRANE TRANSPORT; CELL PROTECTION; CONTROLLED STUDY; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTERNALIZATION; INTOXICATION; INTRACELLULAR TRANSPORT; ISOTOPE LABELING; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RECEPTOR BINDING; STEADY STATE; TRANS GOLGI NETWORK; CELL MEMBRANE; DRUG EFFECTS; HELA CELL LINE; METABOLISM; PROTEIN TRANSPORT;

CELL MEMBRANE; ENDOCYTOSIS; HELA CELLS; HUMANS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; SHIGA TOXIN;

EID: 84902672939     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12173     Document Type: Article

References (41)

1. Doherty GJ, McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem 2009;78:857-902.
2. Howes MT, Mayor S, Parton RG. Molecules, mechanisms, and cellular roles of clathrin-independent endocytosis. Curr Opin Cell Biol 2010;22:519-527.
3. Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, Sharma DK, Pagano RE, Hancock JF, Mayor S, Parton RG. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 2005;168:465-476.
4. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007;8:603-612.
5. 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.
6. Romer W, Berland L, Chambon V, Gaus K, Windschiegl B, Tenza D, Aly MR, Fraisier V, Florent JC, Perrais D, Lamaze C, Raposo G, Steinem C, Sens P, Bassereau P, et al. Shiga toxin induces tubular membrane invaginations for its uptake into cells. Nature 2007;450:670-675.
7. 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;12:11-12.
8. Romer W, Pontani LL, Sorre B, Rentero C, Berland L, Chambon V, Lamaze C, Bassereau P, Sykes C, Gaus K, Johannes L. Actin dynamics drive membrane reorganization and scission in clathrin-independent endocytosis. Cell 2010;140:540-553.
9. Rydell GE, Svensson L, Larson G, Johannes L, Römer W. Human GII.4 norovirus VLP induces membrane invaginations on giant unilamellar vesicles containing secretor gene dependent α1, 2-fucosylated glycosphingolipids. Biochim Biophys Acta 2013;1828:1840-1845.
10. Johannes L, Mayor S. Induced domain formation in endocytic invagination, lipid sorting, and scission. Cell 2010;142:507-510.
11. Watkins EB, Miller CE, Majewski J, Kuhl TL. Membrane texture induced by specific protein binding and receptor clustering: active roles for lipids in cellular function. Proc Natl Acad Sci USA 2011;108:6975-6980.
12. Eierhoff T, Stechmann B, Römer W. Pathogen and toxin entry - how pathogens and toxins induce and harness endocytotic mechanisms. In: Ceresa B, editor. Molecular Regulation of Endocytosis. Rijeka: InTech; 2012.
13. Johannes L, Popoff V. Tracing the retrograde route in protein trafficking. Cell 2008;135:1175-1187.
14. Johannes L, Wunder C. Retrograde transport: two (or more) roads diverged in an endosomal tree? Traffic 2011;12:956-962.
15. Sandvig K, Torgersen ML, Engedal N, Skotland T, Iversen T-G. Protein toxins from plants and bacteria: probes for intracellular transport and tools in medicine. FEBS Lett 2010;584:2626-2634.
16. Spooner RA, Lord JM. How ricin and Shiga toxin reach the cytosol of target cells: retrotranslocation from the endoplasmic reticulum. Curr Top Microbiol Immunol 2012;357:19-40.
17. Karch H, Denamur E, Dobrindt U, Finlay BB, Hengge R, Johannes L, Ron EZ, Tønjum T, Sansonetti PJ, Vicente M. The enemy within us: lessons from the 2011 European Escherichia coli O104:H4 outbreak. EMBO Mol Med 2012;4:841-848.
18. Johannes L, Römer W. Shiga toxins - from cell biology to biomedical applications. Nat Rev Microbiol 2010;8:105-116.
19. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009;10:513-525.
20. Iida H, Noda M, Kaneko T, Doiguchi M, Mori T. Identification of rab12 as a vesicle-associated small GTPase highly expressed in Sertoli cells of rat testis. Mol Reprod Dev 2005;71:178-185.
21. Matsui T, Itoh T, Fukuda M. Small GTPase Rab12 regulates constitutive degradation of transferrin receptor. Traffic 2011;12:1432-1443.
22. Matsui T, Fukuda M. Rab12 regulates mTORC1 activity and autophagy through controlling the degradation of amino-acid transporter PAT4. EMBO Rep 2013;14:450-457.
23. Amessou M, Popoff V, Yelamos B, Saint-Pol A, Johannes L. Measuring retrograde transport to the trans-Golgi network. Curr Protoc Cell Biol 2006; Chapter 15:Unit 15.10.
24. Matsui T, Fukuda M. Small GTPase Rab12 regulates transferrin receptor degradation. Cell Logist 2011:155-158.
25. Amessou M, Fradagrada A, Falguières T, Lord JM, Smith DC, Roberts LM, Lamaze C, Johannes L. Syntaxin 16 and syntaxin 5 are required for efficient retrograde transport of several exogenous and endogenous cargo proteins. J Cell Sci 2007;120:1457-1468.
26. Holmgren J, Lönnroth I, Svennerholm L. Tissue receptor for cholera exotoxin: postulated structure from studies with GM1 ganglioside and related glycolipids. Infect Immun 1973;8:208-214.
27. Banting G, Maile R, Roquemore EP. The steady state distribution of humTGN46 is not significantly altered in cells defective in clathrin-mediated endocytosis. J Cell Sci 1998;111(Pt 2):3451-3458.
28. Wiley HS, Burke PM. Regulation of receptor tyrosine kinase signaling by endocytic trafficking. Traffic 2001;2:12-18.
29. Boncompain G, Divoux S, Gareil N, de Forges H, Lescure A, Latreche L, Mercanti V, Jollivet F, Raposo G, Perez F. Synchronization of secretory protein traffic in populations of cells. Nat Methods 2012;9:493-498.
30. Spang A. On the fate of early endosomes. Biol Chem 2009;390:753-759.
31. Snider MD, Rogers OC. Intracellular movement of cell surface receptors after endocytosis: resialylation of asialo-transferrin receptor in human erythroleukemia cells. J Cell Biol 1985;100:826-834.
32. Shi G, Azoulay M, Dingli F, Lamaze C, Loew D, Florent J-C, Johannes L. SNAP-tag based proteomics approach for the study of the retrograde route. Traffic 2012;13:914-925.
33. Uemura T, Nakano A. Plant TGNs: dynamics and physiological functions. Histochem Cell Biol 2013;140:341-345.
34. Richter S, Voss U, Jürgens G. Post-Golgi traffic in plants. Traffic 2009;10:819-828.
35. Huotari J, Helenius A. Endosome maturation. EMBO J 2011;30:3481-3500.
36. Popoff V, Mardones GA, Tenza D, Rojas R, Lamaze C, Bonifacino JS, Raposo G, Johannes L. The retromer complex and clathrin define an early endosomal retrograde exit site. J Cell Sci 2007;120:2022-2031.
37. 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.
38. Mallard F, Johannes L. Shiga toxin B-subunit as a tool to study retrograde transport. Methods Mol Med 2003;73:209-220.
39. Bolte S, Cordelières FP. A guided tour into subcellular colocalization analysis in light. J Microsc 2006;224:213-232.
40. Dieckmann-Schuppert A, Schnittler HJ. A simple assay for quantification of protein in tissue sections, cell cultures, and cell homogenates, and of protein immobilized on solid surfaces. Cell Tissue Res 1997;288:119-126.
41. Jordan M, Schallhorn A, Wurm FM. Transfecting mammalian cells: optimization of critical parameters affecting calcium-phosphate precipitate formation. Nucleic Acids Res 1996;24:596-601.