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Retrograde transport pathways utilised by viruses and protein toxins

By Robert A. Spooner, Daniel C. Smith, A. J. (Andrew J.) Easton, L. M. (Lynne M.) Roberts and Mike Lord

Abstract

A model has been presented for retrograde transport of certain toxins and viruses from the cell surface to the ER that suggests an obligatory interaction with a glycolipid receptor at the cell surface. Here we review studies on the ER trafficking cholera toxin, Shiga and Shiga-like toxins, Pseudomonas exotoxin A and ricin, and compare the retrograde routes followed by these protein toxins to those of the ER trafficking SV40 and polyoma viruses. We conclude that there is in fact no obligatory requirement for a glycolipid receptor, nor even with a protein receptor in a lipid-rich environment. Emerging data suggests instead that there is no common pathway utilised for retrograde transport by all of these pathogens, the choice of route being determined by the particular receptor utilised.\u

Topics: QH301
Publisher: BioMed Central Ltd.
Year: 2006
OAI identifier: oai:wrap.warwick.ac.uk:415

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  1. (1991). a 110 kd protein associated with non-clathrin-coated vesicles and the Golgi complex, shows homology to beta-adaptin. Cell doi
  2. (2002). A distinct class of endosome mediates clathrinindependent endocytosis to the Golgi complex. doi
  3. (2003). A: BiP-dependent export of cholera toxin from endoplasmic reticulum-derived microsomes. FEBS Lett doi
  4. (2002). A: Caveolar endocytosis of simian virus 40 is followed by brefeldin A-sensitive transport to the endoplasmic reticulum, where the virus disassembles. doi
  5. A: Toxic lectins and related proteins. doi
  6. (1999). Acheson DW: Shiga toxins stimulate secretion of interleukin8 from intestinal epithelial cells. Infect Immun
  7. (1991). Alpha-toxin of Staphylococcus aureus. Microbiol Rev
  8. (1998). An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells. doi
  9. (1974). Avigad LS: Partial characterization of aerolysin, a lytic exotoxin from Aeromonas hydrophila. Infect Immun
  10. (2001). Caveolae are involved in the trafficking of mouse polyomavirus virions and artificial VP1 pseudocapsids toward cell nuclei. doi
  11. (2002). Characterization of novel Rab6-interacting proteins involved in endosome-to-TGN transport. Traffic doi
  12. (2000). Cholera toxin is exported from microsomesby the Sec61p complex. doi
  13. (1995). Clin MicrobiolRev
  14. (2004). Colombatti M: Reductive activation of ricin and ricin A-chain immunotoxins by protein disulfide isomerase and thioredoxin reductase. Biochem Pharmacol doi
  15. (1994). Cosson P: Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell doi
  16. (1975). D: NAD-dependent inhibition of protein synthesis by Pseudomonas aeruginosa toxin. doi
  17. (2001). DB: Refined crystallographic structure of Pseudomonas aeruginosa exotoxin A and its implications for the molecular mechanism of toxicity. doi
  18. (2004). Deurs B: Pathways followed by protein toxins into cells. doi
  19. (2002). DG: Expression of receptors for verotoxin 1 from Escherichia coli O157 on bovine intestinal epithelium.
  20. (1997). DH: Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation. Nature
  21. (1977). Diphtheria toxin. Annu Rev Biochem doi
  22. (1998). Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of shiga toxin B-fragment transport. doi
  23. (1959). DR: Role of cholera toxin in experimental cholera.
  24. (2002). Early/recycling endosomes-toTGN transport involves two SNARE complexes and a Rab6 isoform. doi
  25. (1999). EH: Rab6 coordinates a novel Golgi to ER retrograde transport pathway in live cells.
  26. (2004). Endosomal ricin transport: involvement of Rab4- and Rab5-positive compartments. Histochem Cell Biol doi
  27. (2001). Endosome to Golgi transport of ricin is independent of clathrin and of the Rab9- and Rab11-GTPases. Mol Biol Cell doi
  28. (2000). Endosome to Golgi transport of ricin is regulated by cholesterol. Mol Biol Cell doi
  29. (1959). Enterotoxicity of bacteria-free culture filtrate of Vibrio cholerae. nature doi
  30. (1980). Formal SB: Cytotoxicity of Shigella dysenteriae 1 for cultured mammalian cells.
  31. (2001). Fouet A: Anthrax. Annu Rev Microbiol doi
  32. (1999). FR: Chimeric forms of furin and TGN38 are transported with the plasma membrane in the transGolgi network via distinct endosomal pathways. doi
  33. (1998). Getting through the Golgi complex. Trends Cell Biol doi
  34. (1988). Griffiths G: Estimation of the amount of internalized ricin that reaches the trans-Golgi network. doi
  35. (2000). Hammerling GJ, Momburg F: Export of antigenic peptides from the endoplasmic reticulum intersects with retrograde protein translocation through the Sec61p channel. Immunity doi
  36. (1999). Harter C: Mechanisms of vesicle formation: insights from the COP system. Curr Opin Cell Biol doi
  37. (2005). Haslam DB: Shiga toxin is transported from the endoplasmic reticulum following interaction with the luminal chaperone HEDJ/ERdj3. Infection and Immunity doi
  38. (2001). Helenius A: Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol doi
  39. (2004). Helenius A: Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell doi
  40. (2005). Helenius A: Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. doi
  41. (2002). Helenius A: Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science doi
  42. (2002). Holmes RK: Inhibition of endoplasmic reticulum-associated degradation in CHO cells resistant to cholera toxin, Pseudomonas aeruginosa exotoxin A, and ricin. Infect Immun doi
  43. (2004). Hong W: Autoantigen Golgin-97, an effector of Arl1 GTPase, participates in traffic from the endosome to the trans-golgi network. Mol Biol Cell doi
  44. (2004). Hong W: Participation of the syntaxin5/Ykt6/GS28/GS15 SNARE complex in transport from the early/recycling endosomes to the trans-Golgi network. Mol Biol Cell doi
  45. (1987). Identification of the carbohydrate receptor for Shiga toxin produced by Shigella dysenteriae type 1.
  46. (1988). Igarashi K: Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. doi
  47. (2002). Iversen TG: Pathways followed by ricin and Shiga toxin into cells. Histochem Cell Biol doi
  48. (1995). JE: The capacity to retrieve escaped ER proteins extends to the trans-most cisterna of rthe Golgi stack. doi
  49. (2005). JL: E-Cadherin Transport from the trans-Golgi Network in Tubulovesicular Carriers is Selectively Regulated by Golgin-97. Traffic doi
  50. (2001). JM: An interaction between ricin and calreticulin that may have implications for toxin trafficking. doi
  51. (2002). JM: Binding of ricin A-chain to negatively charged phospholipid vesicles leads to protein structural changes and destabilizes the lipid bilayer. Biochemistry doi
  52. (2000). JM: CD40 ligand, Bcl-2, and Bcl-xL spare group I Burkitt lymphoma cells from CD77-directed killing via Verotoxin-1 B chain but fail to protect against the holotoxin. Cell Death Differ doi
  53. (1989). JM: Recombinant proricin binds galactose but does not depurinate 28 S ribosomal RNA. FEBS Lett doi
  54. (1986). Keusch GT: Pathogenesis of shigella diarrhea. XI. Isolation of a shigella toxin-binding glycolipid from rabbit jejunum and HeLa cells and its identification as globotriaosylceramide. J Exp Med doi
  55. (2005). Kuksin D: The caveolae-mediated sv40 entry pathway bypasses the golgi complex en route to the endoplasmic reticulum. Virol J
  56. (2001). L: Targeting of Shiga toxin B-subunit to retrograde transport route in association with detergentresistant membranes. Mol Biol Cell doi
  57. (1996). LC: Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol Biol Cell doi
  58. (2003). Lencer WI: Gangliosides that associate with lipid rafts mediate transport of cholera and related toxins from the plasma membrane to endoplasmic reticulm. Mol Biol Cell doi
  59. (2004). Lencer WI: Retrograde transport of cholera toxin from the plasma membrane to the endoplasmic reticulum requires the transGolgi network but not the Golgi apparatus in Exo2-treated cells. EMBO Rep doi
  60. (2005). Lencer WI: Role of p97 AAA-ATPase in the retrotranslocation of the cholera toxin A1 chain, a non-ubiquitinated substrate. doi
  61. (2002). Lencer WI: Role of ubiquitination in retro-translocation of cholera toxin and escape of cytosolic degradation. EMBO Rep doi
  62. (1997). Letourner F: Coatomer (COP1)-coated vesicles: role in intracellular transport and protein sorting. Curr Opin Cell Biol doi
  63. (1990). Lingwood CA: Induction of verotoxin sensitivity in receptor-deficient cell lines using the receptor glycolipid globotriosylceramide. doi
  64. (2006). LM: Protein disulphide isomerase reducesVirology Journal
  65. (1985). London E: Effect of pH on the conformation of diphtheria toxin and its implications for membrane penetration. Biochemistry doi
  66. (1977). Mechanism of action of choleragen: evidence for ADP-ribosyltransferase activity with arginine as an acceptor.
  67. (1990). Mekada E: The cytotoxic action of diphtheria toxin and its degradation in intact Vero cells are inhibited by bafilomycin A1, a specific inhibitor of vacuolartype H(+)-ATPase.
  68. (2005). MJ: Rab5 and Rab7, but not ARF6, govern the early events of HIV-1 infection in polarized human placental cells. doi
  69. (1995). Molecular genetics of clostridial neurotoxins. doi
  70. (2003). Mouse polyomavirus utilizes recycling endosomes for a traffic pathway independent of COPI vesicle transport. doi
  71. (2003). Nabi IR: Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. doi
  72. (2001). Ohno K: Accumulation of cholera toxin and GM1 ganglioside in the early endosome of Niemann-Pick C1-deficient cells. doi
  73. (1999). Olsnes S: Dependence of ricin toxicity on translocation of the toxin A-chain from the endoplasmic reticulum to the cytosol. doi
  74. (1992). Orci L: Molecular dissection of the secretory pathway. Nature doi
  75. (2004). PA: Mammalian GRIP domain proteins differ in their membrane binding properties and are recruited to distinct domains of the TGN. doi
  76. (2003). Pagano RE: Selective caveolin-1-dependent endocytosis of glycosphingolipids. Mol Biol Cell
  77. (2005). Paschal BM: Retrotranslocation of the chaperone calreticulin from the endoplasmic reticulum lumen to the cytosol. Mol Cell Biol doi
  78. (1995). Pastan I: Importance of the glutamate residue of the KDEL in increasing the cytotoxicity of Pseudomonas exotoxinderivatives and for increased binding to the KDEL receptor.
  79. (1991). Pastan I: Increased cytotoxic activity of Pseudomonas exotoxin and two chimeric toxins ending in KDEL.
  80. (1990). Pastan I: Pseudomonas exotoxin contains a specific sequence at the carboxyl terminus that is required for cytotoxicity. Proc Natl Acad Sci USA doi
  81. (1999). Pepperkok R: Evidence for a COP-I-independent transport route from the Golgi complex to the endoplasmic reticulum. Nat Cell Biol
  82. (1996). Ploegh HL: Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature doi
  83. (1996). Ploegh HL: The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell doi
  84. (1997). Protein-disulfide isomerase-mediated reduction of the A subunit of cholera toxin in a human intestinal cell line.
  85. (1981). Purification and some properties of the hemolytic toxin aerolysin. doi
  86. (2001). Rapid cycling of lipid raft markers between the cell surface and Golgi complex. doi
  87. (1991). RD: Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell doi
  88. (2000). Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem
  89. (2002). RG: Inhibitors of COPmediated transport and cholera toxin action inhibit simian virus 40 infection. Mol Biol Cell doi
  90. (1997). RG: Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol Biol Cell doi
  91. (2003). Richards AA: Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic doi
  92. (1974). Ricin: the toxic protein of castor oil seeds. Toxicology doi
  93. (1997). RJ: Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells. Biochemistry doi
  94. (2003). RK: A class of mutant CHO cells resistant to cholera toxin rapidly degrades the catalytic polypeptide of cholera toxin and exhibits increased endoplasmic reticulum-associated degradation. Traffic doi
  95. (2003). RK: Evidence that the transport of ricin to the cytoplasm is independent of both Rab6A and COPI. doi
  96. (2005). RK: p97 s in a complex with cholera toxin and influences the transport of cholera toxin and related toxins to the cytoplasm. doi
  97. (1987). RK: Shiga and the Shiga-like toxins. Microbiol Rev
  98. (1987). RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. doi
  99. (2006). Roberts LM: Internalised Pseudomonas exotoxin A can exploit multiple pathways to reach the endoplasmic reticulum. Traffic doi
  100. (1998). Roberts LM: Toxin entry: retrograde transport through the secretory pathway. doi
  101. (2001). Role of lipid rafts in Shiga toxin 1 interaction with the apical surface of Caco-2 cells.
  102. (2003). Role of lipids in the retrograde pathway of ricin intoxication. Traffic doi
  103. (1997). Romisch K: Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation. Embo J doi
  104. (1992). Saelinger CB: The alpha2-macroglobulin receptor/low de3nsity lipoprotein-related protein binds and internalizes Pseudomonas exotoxin A.
  105. (1999). Sandvig K: Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell doi
  106. (2003). Sandvig K: Induction of direct endosome to endoplasmic reticulum transport in Chinese Hamster Ovary (CHO) cells (LdlF) with a temperaturesensitive defect in {epsilon}-coatomer protein ({epsilon}-COP). doi
  107. (2004). Shiga toxin binding to globotriaosyl ceramide induces intracellular signals that mediate cytoskeleton remodeling in human renal carcinoma-derived cells. doi
  108. (1993). SR: Rab9 functions in transport between late endosomes and the trans Golgi network. Embo J
  109. (2003). Src regulates Golgi structure and KDEL receptor-dependent retrograde transport to the endoplasmic reticulum. doi
  110. (1998). Surfing on a retrograde wave: how does Shiga toxin reach the endoplasmic reticulum? Trends Cell Biol doi
  111. (1973). Swennerholm I: Fixation and inactivation of cholera toxin by GM1 gangliosides.
  112. (1973). Swennerholm I: Tissue receptor for cholera exotoxin: postulated structure from studies with GM1 ganglioside and related glycolipids. Infect Immun
  113. (2003). TA: Gangliosides are receptors for murine polyoma virus and SV40. Embo J
  114. (2001). TA: Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell doi
  115. (2004). TA: Structural insight into the protein translocation channel. Curr Opin Struct Biol doi
  116. (2002). TA: Unfolded cholera toxin is transferred to the ER membrane and released from protein disulfide isomerase upon oxidation by Ero1. doi
  117. (2004). TA: X-ray structure of a protein-conducting channel. nature doi
  118. (1995). Terasawa K: Inhibitory effect of bafilomycin A1, a specific inhibitor of vacuolar-type proton pump, on the growth of influenza A and B viruses in MDCK cells. Antiviral Res doi
  119. (2004). The endoplasmic reticulum membrane is permeable to small molecules. Mol Biol Cell doi
  120. (2003). The intracellular voyage of cholera toxin: going retro. Trends Biochem Sci doi
  121. The KDEL retrieval system is exploited by Pseudomonas exotoxin A, but not by Shiga-like toxin-1, during retrograde transport from the Golgi complex to the endoplasmic reticulum.
  122. (2002). The low lysine content of ricin A chain reduces the risk of proteolytic degradation after translocation from the endoplasmic reticulum to the cytosol. Biochemistry doi
  123. (2003). TL: Cell penetration and trafficking of polyomavirus. doi
  124. (2000). TL: Early steps of polyomavirus entry into cells. doi
  125. (2005). Tsai B: ERp29 triggers a conformational change in polyomavirus to stimulate membrane binding. Mol Cell doi
  126. Two distinct Gb3/CD77 signaling pathways leading to apoptosis are triggered by anti-Gb3/CD77 mAb and verotoxin-1. doi

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