Structure, biological functions and applications of the AB5 toxins

Trends in Biochemical Sciences

Volumn 35, Issue 7, 2010, Pages 411-418

  Beddoe, Travis ^a   Paton, Adrienne W ^b   Le Nours, Jérôme ^a   Rossjohn, Jamie ^a   Paton, James C ^b  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AB5 TOXIN; AUTOANTIGEN; BACTERIAL TOXIN; CHOLERA TOXIN; CHOLERA TOXIN B SUBUNIT; CYTOTOXIN; EPIDERMAL GROWTH FACTOR; IMMUNOMODULATING AGENT; SUBTILASE CYTOTOXIN; THAPSIGARGIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; POLYSACCHARIDE;

BORDETELLA PERTUSSIS; BREAST CANCER; ENZYME ACTIVE SITE; EOSINOPHILIA; ESCHERICHIA COLI; HUMAN; IMMUNOMODULATION; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; RECEPTOR BINDING; REVIEW; SHIGELLA DYSENTERIAE; STRUCTURE ANALYSIS; UVEITIS; VIBRIO CHOLERAE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM;

BACTERIAL TOXINS; HUMANS; MOLECULAR STRUCTURE; POLYSACCHARIDES;

BACTERIA (MICROORGANISMS); BORDETELLA PERTUSSIS; ESCHERICHIA COLI; SHIGELLA DYSENTERIAE; VIBRIO CHOLERAE;

EID: 77954316475     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2010.02.003     Document Type: Review

References (72)

1. Sack D.A., et al. Cholera. Lancet 2004, 363:223-233.
2. Nataro J.P., Kaper J.B. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 1998, 11:142-201.
3. Paton J.C., Paton A.W. Pathogenesis and diagnosis of shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev. 1998, 11:450-479.
4. Tarr P.I., et al. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 2005, 365:1073-1086.
5. Griffin, P.M. et al. (2000) Shiga toxin-producing Escherichia coli infections in the United States. In 4th International Symposium and Workshop on Shiga Toxin-producing Escherichia coli Infections, Kyoto, Japan, 31.
6. Fan E., et al. AB(5) toxins: structures and inhibitor design. Curr. Opin. Struct. Biol. 2000, 10:680-686.
7. O'Neal C.J., et al. Crystal structures of an intrinsically active cholera toxin mutant yield insight into the toxin activation mechanism. Biochemistry 2004, 43:3772-3782.
8. van den Akker F., et al. Crystal structure of a new heat-labile enterotoxin, LT-IIb. Structure 1996, 4:665-678.
9. Paton A.W., Paton J.C. Detection and characterization of Shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E. coli hlyA, rfbO111, and rfbO157. J. Clin. Microbiol. 1998, 36:598-602.
10. Fraser M.E., et al. Structure of shiga toxin type 2 (Stx2) from Escherichia coli O157:H7. J. Biol. Chem. 2004, 279:27511-27517.
11. Siegler R.L., et al. Response to Shiga toxin 1 and 2 in a baboon model of hemolytic uremic syndrome. Pediatr. Nephrol. 2003, 18:92-96.
12. Paton A.W., et al. A new family of potent AB(5) cytotoxins produced by Shiga toxigenic Escherichia coli. J. Exp. Med. 2004, 200:35-46.
13. Paton A.W., et al. AB5 subtilase cytotoxin inactivates the endoplasmic reticulum chaperone BiP. Nature 2006, 443:548-552.
14. Cergole-Novella M.C., et al. Distribution of virulence profiles related to new toxins and putative adhesins in Shiga toxin-producing Escherichia coli isolated from diverse sources in Brazil. FEMS Microbiol. Lett. 2007, 274:329-334.
15. Khaitan A., et al. The operon encoding SubAB, a novel cytotoxin, is present in shiga toxin-producing Escherichia coli isolates from the United States. J. Clin. Microbiol. 2007, 45:1374-1375.
16. Wang H., et al. Pathologic changes in mice induced by subtilase cytotoxin, a potent new Escherichia coli AB5 toxin that targets the endoplasmic reticulum. J. Infect. Dis. 2007, 196:1093-1101.
17. Hendershot L.M. The ER function BiP is a master regulator of ER function. Mt Sinai J. Med. 2004, 71:289-297.
18. Plaut R.D., Carbonetti N.H. Retrograde transport of pertussis toxin in the mammalian cell. Cell Microbiol. 2008, 10:1130-1139.
19. Tsai B., et al. Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell 2001, 104:937-948.
20. Matlack K.E., et al. Protein translocation: tunnel vision. Cell 1998, 92:381-390.
21. Bernardi K.M., et al. Derlin-1 facilitates the retro-translocation of cholera toxin. Mol. Biol. Cell 2008, 19:877-884.
22. Bernardi K.M., et al. The E3 ubiquitin ligases Hrd1 and gp78 bind to and promote cholera toxin retro-translocation. Mol. Biol. Cell 2010, 21:140-151.
23. Dixit G., et al. Cholera toxin up-regulates endoplasmic reticulum proteins that correlate with sensitivity to the toxin. Exp. Biol. Med. 2008, 233:163-175.
24. Tarrago-Trani M.T., et al. Shiga-like toxin subunit B (SLTB)-enhanced delivery of chlorin e6 (Ce6) improves cell killing. Photochem. Photobiol. 2006, 82:527-537.
25. Chong D.C., et al. Clathrin-dependent trafficking of subtilase cytotoxin, a novel AB5 toxin that targets the endoplasmic reticulum chaperone BiP. Cell Microbiol. 2008, 10:795-806.
26. Smith R.D., et al. The COG complex, Rab6 and COPI define a novel Golgi retrograde trafficking pathway that is exploited by SubAB toxin. Traffic 2009, 10:1502-1517.
27. Kitov P.I., et al. In vivo supramolecular templating enhances the activity of multivalent ligands: a potential therapeutic against the Escherichia coli O157 AB5 toxins. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16837-16842.
28. Kitov P.I., et al. Shiga-like toxins are neutralized by tailored multivalent carbohydrate ligands. Nature 2000, 403:669-672.
29. Merritt E.A., et al. Crystal structure of cholera toxin B-pentamer bound to receptor GM1 pentasaccharide. Protein Sci. 1994, 3:166-175.
30. Fukuta S., et al. Comparison of the carbohydrate-binding specificities of cholera toxin and Escherichia coli heat-labile enterotoxins LTh-I, LT-IIa, and LT-IIb. Infect. Immun. 1988, 56:1748-1753.
31. Byres E., et al. Incorporation of a non-human glycan mediates human susceptibility to a bacterial toxin. Nature 2008, 456:648-652.
32. Soltyk A.M., et al. A mutational analysis of the globotriaosylceramide-binding sites of verotoxin VT1. J. Biol. Chem. 2002, 277:5351-5359.
33. Merritt E.A., et al. Galactose-binding site in Escherichia coli heat-labile enterotoxin (LT) and cholera toxin (CT). Mol. Microbiol. 1994, 13:745-753.
34. MacKenzie C.R., et al. Quantitative analysis of bacterial toxin affinity and specificity for glycolipid receptors by surface plasmon resonance. J. Biol. Chem. 1997, 272:5533-5538.
35. Karlsson K.A., et al. Unexpected carbohydrate cross-binding by Escherichia coli heat-labile enterotoxin. Recognition of human and rabbit target cell glycoconjugates in comparison with cholera toxin. Bioorg. Med. Chem. 1996, 4:1919-1928.
36. Galvan E.M., et al. Functional interaction of Escherichia coli heat-labile enterotoxin with blood group A-active glycoconjugates from differentiated HT29 cells. FEBS J. 2006, 273:3444-3453.
37. Holmner A., et al. Novel binding site identified in a hybrid between cholera toxin and heat-labile enterotoxin: 1.9Å crystal structure reveals the details. Structure 2004, 12:1655-1667.
38. Holmner A., et al. Blood group antigen recognition by Escherichia coli heat-labile enterotoxin. J. Mol. Biol. 2007, 371:754-764.
39. Obara Y., et al. Betagamma subunits of G(i/o) suppress EGF-induced ERK5 phosphorylation, whereas ERK1/2 phosphorylation is enhanced. Cell Signal. 2008, 20:1275-1283.
40. Nakamura K., et al. G(i)-coupled GPCR signaling controls the formation and organization of human pluripotent colonies. PLoS One 2009, 4:e7780.
41. Regard J.B., et al. Probing cell type-specific functions of Gi in vivo identifies GPCR regulators of insulin secretion. J. Clin. Invest. 2007, 117:4034-4043.
42. Sanchez J., Holmgren J. Cholera toxin structure, gene regulation and pathophysiological and immunological aspects. Cell Mol. Life Sci. 2008, 65:1347-1360.
43. Vanden Broeck D., et al. Vibrio cholerae: cholera toxin. Int. J. Biochem. Cell Biol. 2007, 39:1771-1775.
44. Boyaka P.N., et al. Chimeras of labile toxin one and cholera toxin retain mucosal adjuvanticity and direct Th cell subsets via their B subunit. J. Immunol. 2003, 170:454-462.
45. Stanford M., et al. Oral tolerization with peptide 336-351 linked to cholera toxin B subunit in preventing relapses of uveitis in Behcet's disease. Clin. Exp. Immunol. 2004, 137:201-208.
46. Smits H.H., et al. Cholera toxin B suppresses allergic inflammation through induction of secretory IgA. Mucosal Immunol. 2009, 2:331-339.
47. Tarrago-Trani M.T., Storrie B. Alternate routes for drug delivery to the cell interior: pathways to the Golgi apparatus and endoplasmic reticulum. Adv. Drug Deliv. Rev. 2007, 59:782-797.
48. Lass A., et al. Decreased ER-associated degradation of alpha-TCR induced by Grp78 depletion with the SubAB cytotoxin. Int. J. Biochem. Cell Biol. 2008, 40:2865-2879.
49. Huang T., et al. Downregulation of gap junction expression and function by endoplasmic reticulum stress. J. Cell Biochem. 2009, 107:973-983.
50. Buchkovich N.J., et al. Human cytomegalovirus specifically controls the levels of the endoplasmic reticulum chaperone BiP/GRP78, which is required for virion assembly. J. Virol. 2008, 82:31-39.
51. Wati S., et al. Dengue virus infection induces upregulation of GRP78, which acts to chaperone viral antigen production. J. Virol. 2009, 83:12871-12880.
52. Du S., et al. Suppression of NF-kappaB by cyclosporin a and tacrolimus (FK506) via induction of the C/EBP family: implication for unfolded protein response. J. Immunol. 2009, 182:7201-7211.
53. Hayakawa K., et al. Blunted activation of NF-kappaB and NF-kappaB-dependent gene expression by geranylgeranylacetone: involvement of unfolded protein response. Biochem. Biophys. Res. Commun. 2008, 365:47-53.
54. Hu C.C., et al. Subtilase cytotoxin cleaves newly synthesized BiP and blocks antibody secretion in B lymphocytes. J. Exp. Med. 2009, 206:2429-2440.
55. Yamazaki H., et al. Activation of the Akt-NF-kappaB pathway by subtilase cytotoxin through the ATF6 branch of the unfolded protein response. J. Immunol. 2009, 183:1480-1487.
56. Harama D., et al. A subcytotoxic dose of subtilase cytotoxin prevents lipopolysaccharide-induced inflammatory responses, depending on its capacity to induce the unfolded protein response. J. Immunol. 2009, 183:1368-1374.
57. Distler U., et al. Shiga toxin receptor Gb3Cer/CD77: tumor-association and promising therapeutic target in pancreas and colon cancer. PLoS One 2009, 4:e6813.
58. Falguieres T., et al. Human colorectal tumors and metastases express Gb3 and can be targeted by an intestinal pathogen-based delivery tool. Mol. Cancer Ther. 2008, 7:2498-2508.
59. Johansson D., et al. Expression of verotoxin-1 receptor Gb3 in breast cancer tissue and verotoxin-1 signal transduction to apoptosis. BMC Cancer 2009, 9:67.
60. Ishitoya S., et al. Verotoxin induces rapid elimination of human renal tumor xenografts in SCID mice. J. Urol. 2004, 171:1309-1313.
61. Janssen K.P., et al. In vivo tumor targeting using a novel intestinal pathogen-based delivery approach. Cancer Res. 2006, 66:7230-7236.
62. Amessou M., et al. Retrograde delivery of photosensitizer (TPPp-O-beta-GluOH)3 selectively potentiates its photodynamic activity. Bioconjug. Chem. 2008, 19:532-538.
63. El Alaoui A., et al. Shiga toxin-mediated retrograde delivery of a topoisomerase I inhibitor prodrug. Angew. Chem. Int. Ed. Engl. 2007, 46:6469-6472.
64. Li J., Lee A.S. Stress induction of GRP78/BiP and its role in cancer. Curr. Mol. Med. 2006, 6:45-54.
65. Hedlund M., et al. Evidence for a human-specific mechanism for diet and antibody-mediated inflammation in carcinoma progression. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:18936-18941.
66. Backer J.M., et al. Chaperone-targeting cytotoxin and endoplasmic reticulum stress-inducing drug synergize to kill cancer cells. Neoplasia 2009, 11:1165-1173.
67. Schwarzkopf M., et al. Sialylation is essential for early development in mice. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:5267-5270.
68. Varki N.M., Varki A. Diversity in cell surface sialic acid presentations: implications for biology and disease. Lab. Invest. 2007, 87:851-857.
69. Chou H.H., et al. A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:11751-11756.
70. Muchmore E.A., et al. A structural difference between the cell surfaces of humans and the great apes. Am. J. Phys. Anthropol. 1998, 107:187-198.
71. Martin M.J., et al. Evolution of human-chimpanzee differences in malaria susceptibility: relationship to human genetic loss of N-glycolylneuraminic acid. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12819-12824.
72. Rich S.M., et al. The origin of malignant malaria. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14902-14907.