Clostridium difficile binary toxin CDT induces clustering of the lipolysis-stimulated lipoprotein receptor into lipid rafts

mBio

Volumn 4, Issue 3, 2013, Pages

  Papatheodorou, Panagiotis ^a   Hornuss, Daniel ^a   Nölke, Thilo ^a   Hemmasi, Sarah ^a,b   Castonguay, Jan ^a   Picchianti, Monica ^c,d   Aktories, Klaus ^a,b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^d UNIVERSITY OF SIENA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; CELL MARKER; CELL PROTEIN; CLOSTRIDIUM DIFFICILE TRANSFERASE B TOXIN; LIPOLYSIS STIMULATED LIPOPROTEIN RECEPTOR; LIPOPROTEIN RECEPTOR; METHYL BETA CYCLODEXTRIN; UNCLASSIFIED DRUG; ACTIN-SPECIFIC ADP-RIBOSYLTRANSFERASE, CLOSTRIDIUM; BACTERIAL PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ARTICLE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELL STRAIN CACO 2; CELL SURFACE; CHOLESTEROL DEPLETION; CONTROLLED STUDY; DEPLETION; DETERGENT RESISTANT MEMBRANE; FLUORESCENCE MICROSCOPY; HELA CELL; LIPID RAFT; LIPOLYSIS; MOLECULAR MODEL; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR BINDING; SUCROSE GRADIENT; CACO 2 CELL LINE; CHEMISTRY; DRUG EFFECTS; HELA CELL LINE; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE; PEPTOCLOSTRIDIUM DIFFICILE; PROTEIN TERTIARY STRUCTURE;

CLOSTRIDIUM DIFFICILE;

ADP RIBOSE TRANSFERASES; BACTERIAL PROTEINS; CACO-2 CELLS; CELL MEMBRANE; CLOSTRIDIUM DIFFICILE; DNA MUTATIONAL ANALYSIS; HELA CELLS; HUMANS; MEMBRANE MICRODOMAINS; MICROSCOPY, FLUORESCENCE; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, LIPOPROTEIN;

EID: 84879571965     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00244-13     Document Type: Article

References (37)

1. Rupnik M, Wilcox MH, Gerding DN. 2009. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 7:526-536.
2. Aktories K. 2011. Bacterial protein toxins that modify host regulatory GTPases. Nat. Rev. Microbiol. 9:487-498.
3. McDonald LC, Killgore GE, Thompson A, Owens RC, Jr, Kazakova SV, Sambol SP, Johnson S, Gerding DN. 2005. An epidemic, toxin genevariant strain of Clostridium difficile. N. Engl. J. Med. 353:2433-2441.
4. Barth H, Aktories K, Popoff MR, Stiles BG. 2004. Binary bacterial toxins: biochemistry, biology, and applications of common Clostridium and Bacillus proteins. Microbiol. Mol. Biol. Rev. 68:373-402.
5. Aktories K, Bärmann M, Ohishi I, Tsuyama S, Jakobs KH, Habermann E. 1986. Botulinum C2 toxin ADP-ribosylates actin. Nature 322:390-392.
6. Aktories K, Schwan C, Papatheodorou P, Lang AE. 2012. Bidirectional attack on the actin cytoskeleton. Bacterial protein toxins causing polymerization or depolymerization of actin. Toxicon 60:572-581.
7. Schwan C, Stecher B, Tzivelekidis T, van Ham M, Rohde M, Hardt WD, Wehland J, Aktories K. 2009. Clostridium difficile toxin CDT induces formation of microtubule-based protrusions and increases adherence of bacteria. PLoS Pathog. 5:e1000626.
8. Blöcker D, Behlke J, Aktories K, Barth H. 2001. Cellular uptake of the Clostridium perfringens binary iota-toxin. Infect. Immun. 69:2980-2987.
9. Nagahama M, Umezaki M, Tashiro R, Oda M, Kobayashi K, Shibutani M, Takagishi T, Ishidoh K, Fukuda M, Sakurai J. 2012. Intracellular trafficking of Clostridium perfringens iota-toxin b. Infect. Immun. 80: 3410-3416.
10. Kaiser E, Kroll C, Ernst K, Schwan C, Popoff M, Fischer G, Buchner J, Aktories K, Barth H. 2011. Membrane translocation of binary actinADP-ribosylating toxins from Clostridium difficile and Clostridium perfringens is facilitated by cyclophilin A and Hsp90. Infect. Immun. 79: 3913-3921.
11. Papatheodorou P, Carette JE, Bell GW, Schwan C, Guttenberg G, Brummelkamp TR, Aktories K. 2011. Lipolysis-stimulated lipoprotein receptor (LSR) is the host receptor for the binary toxin Clostridium difficile transferase (CDT). Proc. Natl. Acad. Sci. U. S. A. 108:16422-16427.
12. Papatheodorou P, Wilczek C, Nölke T, Guttenberg G, Hornuss D, Schwan C, Aktories K. 2012. Identification of the cellular receptor of Clostridium spiroforme toxin. Infect. Immun. 80:1418-1423.
13. Yen FT, Masson M, Clossais-Besnard N, André P, Grosset JM, Bougueleret L, Dumas JB, Guerassimenko O, Bihain BE. 1999. Molecular cloning of a lipolysis-stimulated remnant receptor expressed in the liver. J. Biol. Chem. 274:13390-13398.
14. Mesli S, Javorschi S, Bérard AM, Landry M, Priddle H, Kivlichan D, Smith AJ, Yen FT, Bihain BE, Darmon M. 2004. Distribution of the lipolysis stimulated receptor in adult and embryonic murine tissues and lethality of LSR-/embryos at 12.5 to 14.5 days of gestation. Eur. J. Biochem. 271:3103-3114.
15. Bihain BE, Yen FT. 1998. The lipolysis stimulated receptor: a gene at last. Curr. Opin. Lipidol. 9:221-224.
16. Masuda S, Oda Y, Sasaki H, Ikenouchi J, Higashi T, Akashi M, Nishi E, Furuse M. 2011. LSR defines cell corners for tricellular tight junction formation in epithelial cells. J. Cell Sci. 124:548-555.
17. Nagahama M, Yamaguchi A, Hagiyama T, Ohkubo N, Kobayashi K, Sakurai J. 2004. Binding and internalization of Clostridium perfringens iota-toxin in lipid rafts. Infect. Immun. 72:3267-3275.
18. Hale ML, Marvaud JC, Popoff MR, Stiles BG. 2004. Detergent-resistant membrane microdomains facilitate Ib oligomer formation and biological activity of Clostridium perfringens iota-toxin. Infect. Immun. 72: 2186-2193.
19. Brown DA, Rose JK. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533-544.
20. Marvaud JC, Smith T, Hale ML, Popoff MR, Smith LA, Stiles BG. 2001. Clostridium perfringens iota-toxin: mapping of receptor binding and Ia docking domains on Ib. Infect. Immun. 69:2435-2441.
21. Stiles BG, Hale ML, Marvaud JC, Popoff MR. 2000. Clostridium perfringens iota toxin: binding studies and characterization of cell surface receptor by fluorescence-activated cytometry. Infect. Immun. 68:3475-3484.
22. Nagahama M, Nagayasu K, Kobayashi K, Sakurai J. 2002. Binding component of Clostridium perfringens iota-toxin induces endocytosis in Vero cells. Infect. Immun. 70:1909-1914.
23. Stiles BG, Hale ML, Marvaud JC, Popoff MR. 2002. Clostridium perfringens iota toxin: characterization of the cell-associated iota B complex. Biochem. J. 367:801-808.
24. Gibert M, Monier MN, Ruez R, Hale ML, Stiles BG, Benmerah A, Johannes L, Lamaze C, Popoff MR. 2011. Endocytosis and toxicity of clostridial binary toxins depend on a clathrin-independent pathway regulated by Rho-GDI. Cell. Microbiol. 13:154-170.
25. Lamaze C, Dujeancourt A, Baba T, Lo CG, Benmerah A, Dautry-Varsat A. 2001. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol. Cell 7:661-671.
26. Jiao X, Zhang N, Xu X, Oppenheim JJ, Jin T. 2005. Ligand-induced partitioning of human CXCR1 chemokine receptors with lipid raft microenvironments facilitates G-protein-dependent signaling. Mol. Cell. Biol. 25:5752-5762.
27. Xue M, Vines CM, Buranda T, Cimino DF, Bennett TA, Prossnitz ER. 2004. N-formyl peptide receptors cluster in an active raft-associated state prior to phosphorylation. J. Biol. Chem. 279:45175-45184.
28. Igarashi J, Michel T. 2000. Agonist-modulated targeting of the EDG-1 receptor to plasmalemmal caveolae. eNOS activation by sphingosine 1-phosphate and the role of caveolin-1 in sphingolipid signal transduction. J. Biol. Chem. 275:32363-32370.
29. Feron O, Smith TW, Michel T, Kelly RA. 1997. Dynamic targeting of the agonist-stimulated m2 muscarinic acetylcholine receptor to caveolae in cardiac myocytes. J. Biol. Chem. 272:17744-17748.
30. Lasley RD, Narayan P, Uittenbogaard A, Smart EJ. 2000. Activated cardiac adenosine A(1) receptors translocate out of caveolae. J. Biol. Chem. 275:4417-4421.
31. Nakayama M, Hisatsune J, Yamasaki E, Nishi Y, Wada A, Kurazono H, Sap J, Yahiro K, Moss J, Hirayama T. 2006. Clustering of Helicobacter pylori VacA in lipid rafts, mediated by its receptor, receptor-like protein tyrosine phosphatase beta, is required for intoxication in AZ-521 cells. Infect. Immun. 74:6571-6580.
32. 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.
33. Wigelsworth DJ, Ruthel G, Schnell L, Herrlich P, Blonder J, Veenstra TD, Carman RJ, Wilkins TD, Van Nhieu GT, Pauillac S, Gibert M, Sauvonnet N, Stiles BG, Popoff MR, Barth H. 2012. CD44 promotes intoxication by the clostridial iota-family toxins. PLoS One 7:e51356.
34. Blonder J, Hale ML, Chan KC, Yu LR, Lucas DA, Conrads TP, Zhou M, Popoff MR, Issaq HJ, Stiles BG, Veenstra TD. 2005. Quantitative profiling of the detergent-resistant membrane proteome of iota-b toxin induced vero cells. J. Proteome Res. 4:523-531.
35. Schwan C, Nölke T, Kruppke AS, Schubert DM, Lang AE, Aktories K. 2011. Cholesterol and sphingolipid-rich microdomains are essential for microtubule-based membrane protrusions induced by Clostridium difficile transferase (CDT). J. Biol. Chem. 286:29356-29365.
36. Barth H, Blocker D, Behlke J, Bergsma-Schutter W, Brisson A, Benz R, Aktories K. 2000. Cellular uptake of Clostridium botulinum C2 toxin requires oligomerization and acidification. J. Biol. Chem. 275: 18704-18711.
37. Sterthoff C, Lang AE, Schwan C, Tauch A, Aktories K. 2010. Functional characterization of an extended binding component of the actin-ADPribosylating C2 toxin detected in Clostridium botulinum strain (C). Infect. Immun. 2300:78: 1468-1474.