Escherichia coli subtilase cytotoxin

Toxins

Volumn 2, Issue 2, 2010, Pages 215-228

  Paton, Adrienne W ^a   Paton, James C ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

AB 5 toxin; BiP GRP78; Endoplasmic reticulum stress; Shiga toxigenic escherichia coli; Subtilase cytotoxin

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; BACTERIAL VACCINE; CELL ENZYME; EPIDERMAL GROWTH FACTOR RECEPTOR SUBTILASE CYTOTOXIN SUBUNIT A FUSION PROTEIN; GLUCOSE REGULATED PROTEIN 78; GLYCAN; HYBRID PROTEIN; INOSITOL; N GLYCOLOYLNEURAMINIC ACID; PROTEIN KINASE R LIKE ENDOPLASMIC RETICULUM KINASE; SIALIC ACID; SUBTILASE CYTOTOXIN; THAPSIGARGIN; UNCLASSIFIED DRUG;

ALPHA CHAIN; APOPTOSIS; ARTHRITIS; BACTERIAL GENE; BETA CHAIN; BREAST CANCER; CELL FUNCTION; CYTOTOXICITY; DISEASE ASSOCIATION; DOSE RESPONSE; DRUG EFFICACY; DRUG POTENTIATION; ENDOPLASMIC RETICULUM STRESS; ESCHERICHIA COLI INFECTION; EUKARYOTIC CELL; GENE FREQUENCY; GENE TARGETING; GENETIC ANALYSIS; GLIOMA; HEMOLYTIC UREMIC SYNDROME; HUMAN; INTRACELLULAR TRANSPORT; NONHUMAN; PROSTATE CANCER; PROTEIN CLEAVAGE; PROTEIN FUNCTION; RECEPTOR SENSITIVITY; REVIEW; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; SIGNAL TRANSDUCTION; STRAIN IDENTIFICATION; STRUCTURE ANALYSIS; TOXIN ANALYSIS; TOXIN STRUCTURE; UPREGULATION;

ESCHERICHIA COLI; EUKARYOTA; MUS;

EID: 79952066988     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins2020215     Document Type: Review

References (63)

1. Fan, E.; Merritt, E.A.; Verlinde, C.L.M.J.; Hol, W.G.J. AB(5) toxins: Structures and inhibitor design. Curr. Opin. Struct. Biol. 2000, 10, 680-686.
2. Paton, A.W.; Srimanote, P.; Talbot, U.M.; Wang, H.; Paton, J.C. A new family of potent AB5 cytotoxins produced by Shiga toxigenic Escherichia coli. J. Exp. Med. 2004, 200, 35-46.
3. Paton, A.W.; Woodrow, M.C.; Doyle, R.M.; Lanser, J.A.; Paton, J.C. Molecular characterization of a Shiga-toxigenic Escherichia coli O113:H21 strain lacking eae responsible for a cluster of cases of hemolytic-uremic syndrome. J. Clin. Microbiol. 1999, 37, 3357-3361.
4. Paton, J.C.; Paton, A.W. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev. 1998, 11, 450-479.
5. Karmali, M.A.; Petric, M.; Lim, C.; Fleming, P.C.; Arbus, G.S.; Lior, H. The asociation between idiopathic hemolytic uremic syndrome and infection by Verotoxin-producing Escherichia coli. J. Infect. Dis. 1985, 151, 775-782.
6. Siezen, R.J.; Leunissen, J.A.M. Subtilases: The superfamily of subtilisin-like serine proteases. Protein Sci. 1997, 6, 501-523.
7. Noda, M.; Yutsudo, T.; Nakabayashi, N.; Hirayama, T.; Takeda, Y. Purification and some properties of Shiga-like toxin from Escherichia coli O157:H7 that is immunologically identical to Shiga toxin. Microb. Pathog. 1987, 2, 339-349.
8. Yutsudo, T.; Nakabayashi, N.; Hirayama, T.; Takeda, Y. Purification and some properties of a Vero toxin from Escherichia coli O157:H7 that is immunologically unrelated to Shiga toxin. Microb. Pathog. 1987, 3, 21-30.
9. Richardson, S.E.; Rotman, T.A.; Jay, V.; Smith, C.R.; Becker, L.E.; Petric, M.; Olivieri, N.F.; Karmali, M.A. Experimental verocytotoxemia in rabbits. Infect. Immun. 1992, 60, 4154-4167.
10. Lindgren, S.W.; Samuel, J.E.; Schmitt, C.K.; O'Brien, A.D. The specific activities of Shiga-like toxin type II (SLT-II) and SLT-II-related toxins of enterohemorrhagic Escherichia coli differ when measured by Vero cell cytotoxicity but not by mouse lethality. Infect. Immun. 1994, 62, 623-631.
11. Fujii, J.; Matsui, T.; Heatherly, D.P.; Schlegel, K.H.; Lobo, P.I.; Yutsudo, T.; Ciraolo, G.M.; Morris, R.E.; Obrig, T. Rapid apoptosis induced by Shiga toxin in HeLa cells. Infect. Immun. 2003, 71, 2724-2735.
12. Morinaga, N.; Yahiro, K.; Matsuura, G.; Watanabe, M.; Nomura, F.; Moss, J.; Noda, M. Two distinct cytotoxic activities of subtilase cytotoxin produced by Shiga-toxigenic Escherichia coli. Infect. Immun. 2007, 75, 488-496.
13. Lass, A.; Kujawa, M.; McConnell, E.; Paton, A.W.; Paton, J.C.; Wójcik, C. Decreased ER-associated degradation of α-TCR induced by Grp78 depletion with the SubAB cytotoxin. Int. J. Biochem. Cell Biol. 2008, 40, 2865-2879.
14. Paton, A.W.; Beddoe, T.; Thorpe, C.M.; Whisstock, J.C.; Wilce, M.C.J.; Rossjohn, J.; Talbot, U.M.; Paton J.C. AB5 subtilase cytotoxin inactivates the endoplasmic reticulum chaperone BiP. Nature 2006, 443, 548-552.
15. Gething, M.J. Role and regulation of the ER charperone BiP. Cell Devel. Biol. 1999, 10, 465-472.
16. L.M. The ER chaperone BiP is a master regulator of ER function. Mt. Sinai J. Med. 2004, 71, 289-297.
17. Boyce, M.; Yuan, J. Cellular response to endoplasmic reticulum stress: A matter of life or death. Cell Death Differ. 2006, 13, 363-373.
18. Szegezdi, E.; Logue, S.E.; Gorman, A.M.; Samali, A. Mediators of endoplasmic reticulum stressinduced apoptosis. EMBO Reports 2006, 7, 880-885.
19. Wolfson, J.; Thorpe, C.M.; May, K.L.; Paton, J.C.; Jandhyala, D.M.; Paton, A.W. Subtilase cytotoxin activates PERK, ATF6 and IRE1 endoplasmic reticulum stress-signaling pathways. Cell. Microbiol. 2008, 10, 795-806.
20. Shen, J.; Snapp, E.L.; Lippincott-Schwartz, J.; Prywes, R. Stable binding of ATF6 to BiP in the endoplasmic reticulum stress response. Mol. Cell. Biol. 2005, 25, 921-932.
21. Wang, H.; Paton, J.C.; Paton, A.W. 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.
22. N.; Yahiro, K.; Matsuura, G.; Moss, J.; Noda, M. Subtilase cytotoxin, produced by Shiga-toxigenic Escherichia coli, transiently inhibits protein synthesis of Vero cells via degradation of BiP and induces cell cycle arrest at G1 by downregulation of cyclin D1. Cell. Microbiol. 2008, 10, 921-929.
23. Matsuura, G.; Morinaga, N.; Yahiro, K.; Komine, R.; Moss, J.; Yoshida, H.; Noda, M. Novel subtilase cytotoxin produced by Shiga-toxigenic Escherichia coli induces apoptosis in vero cells via mitochondrial membrane damage. Infect. Immun. 2009, 77, 2919-2924.
24. Chong, D.C.; Paton, J.C.; Thorpe, C.M.; Paton, A.W. Clathrin-dependent trafficking of subtilase cytotoxin, a novel AB5 toxin that targets the endoplasmic reticulum chaperone BiP. Cell. Microbiol. 2008, 10, 795-806.
25. Smith, R.D.; Willett, R.; Kudlyk, T.; Pokrovskaya, I.; Paton, A.W.; Paton, J.C.; Lupashin, V.V. The COG comples, Rab6 and COPI define a novel Golgi retrograde trafficking pathway that is exploited by SubAB toxin. Traffic 2009, 10, 1502-1517.
26. Lencer, W.I.; Tsai, B. The intracellular voyage of cholera toxin: Going retro. Trends Biochem. Sci. 2003, 28, 639-645.
27. Yu, M.; Haslam, D.B. Shiga toxin is transported from the endoplasmic reticulum following interaction with the luminal chaperone HEDJ/ERdj3. Infect. Immun. 2005, 73, 2524-2532.
28. Stein, P.E.; Boodhoo, A.; Armstrong, G.D.; Heerze, L.D.; Cockle, S.A.; Klein, M.H.; Read, R.J. Structure of a pertussis toxin-sugar complex as a model for receptor binding. Nature Struct. Biol. 1994, 1, 591-596.
29. Yahiro, K.; Morinaga, N.; Satoh, M.; Matsuura, G.; Tomonaga, T.; Nomura, F.; Moss, J.; Noda, M. Identification and characterization of receptors for vacuolating activity of subtilase cytotoxin. Mol. Microbiol. 2006, 62, 480-490.
30. Kondo, Y.; Tokuda, N.; Fan, X.; Yamashita, T.; Honke, K.; Takematsu, H.; Togayachi, A.; Ohta, M.; Kotzusumi, Y.; Narimatsu, H.; Tajima, O.; Furukawa, K.; Furukawa K. Glycosphingolipids are not pivotal receptors for Subtilase cytotoxin in vivo: Sensitivity analysis with glycosylationdefective mutant mice. Biochem. Biophys. Res. Commun. 2009, 378, 179-181.
31. Byres, E.; Paton, A.W.; Paton, J.C.; Löfling, J.C.; Smith, D.F.; Wilce, M.C.J.; Talbot, U.M.; Chong, D.C.; Yu, H.; Huang, S.; Chen, X.; Varki, N.M.; Varki, A.; Rossjohn, J.; Beddoe, T. Incorporation of a non-human glycan mediates human susceptibility to a bacterial toxin. Nature 2008, 456, 648-652.
32. Merritt, E.A.; Sarfarty, S.; Jobling, M.G.; Chang, T.; Holmes, R.K.; Hirst, T.R.; Hol, W.G. Structural studies of receptor binding by cholera toxin mutants. Protein Sci. 1997, 6, 1516-1528.
33. Merritt, E.A.; Sixma, T.K.; Kalk, K.H.;, van Zanten, B.A.; Hol, W.G. Galactose-binding site in Escherichia coli heat-labile enterotoxin (LT) and cholera toxin (CT). Mol. Microbiol. 1994, 13, 745-753.
34. Ling, H.; Bast, D.; Brunton, J.L.; Read, R.J. Structure of the Shiga-like toxin I B-pentamer complexed with an analogue of its receptor Gb3. Biochemistry 1998, 37, 1777-1788.
35. Paton, A.W.; Paton, J.C. Multiplex PCR for direct detection of Shiga toxigenic Escherichia coli producing the novel subtilase cytotoxin. J. Clin. Microbiol. 2005, 43, 2944-2947.
36. Izumiya, H.; Iyoda, S.; Terajima, J.; Ohnishi, M.; Yamasaki, S.; Watanabe, H. Distribution of the subA gene among LEE-negative STEC isolates in Japan. Abstracts of the Sixth International Symposium on Shiga toxin (Verocytotoxin) -Producing Escherichia coli Infections (VTEC2006), Melbourne, Australia, 29 October-1 November 2006; Abstract P07.2.11, pp. 84-85.
37. Khaitan, A.; Jandhyala, D.M.; Thorpe, C.M.; Ritchie, J.M.; Paton, A.W. 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.
38. Cergole-Novella, M.C.; Nishimura, L.S.; dos Santos, L.F.; Irino, K.; Vaz, T.M.I.; Bergamini, A.M.M.; Guth, B.E.C. 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. 2008, 274, 329-334.
39. Wolfson, J.J.; Jandhyala, D.M.; Gorczyca, L.A.; Qadeer, Z.; Manning, S.D.; Hadler, J.; Rudrik, J.T.; Thorpe, C.M. Prevalence of the operon encoding subtilase cytotoxin in non-O157 Shiga toxin-producing Escherichia coli isolated from humans in the United States. J. Clin. Microbiol. 2009, 47, 3058-3059.
40. Slanec, T.; Fruth, A.; Creuzburg, K.; Schmidt, H. Molecular analysis of virulence profiles and Shiga toxin genes in food-borne Shiga toxin-producing Escherichia coli. Appl. Environ. Microbiol. 2009, 75, 6187-6197.
41. Karama, M.; Johnson, R.P.; Holtslander, R.; McEwen, S.A.; Gyles, C.L. Prevalence and characterization of verotoxin-producing Escherichia coli (VTEC) in cattle from an Ontario abattoir. Can. J. Vet. Res. 2008, 72, 297-302.
42. Irino, K.; Vieira, M.A.M.; Gomes, T.A.T.; Naves, Z.V.F.; Guth, B.E.C.; Oliveira, M.G.; Timm, C.D.; Pigatto, C.P.; Farah, S.M.S.S.; Vaz, T.M.I. The subAB operon encoding the subtilase cytotoxin (SubAB) is present only among Shiga toxin-producing Escherichia coli. In Abstracts of the Seventh International Symposium on Shiga toxin (Verocytotoxin)-Producing Escherichia coli Infections (VTEC2009), Buenos Aires, Argentina, 10-13 May 2009; Abstract P02.4.7, p. 95.
43. Gerhardt, E.; Miliwebsky, E.; Rivas, M.; Ibarra, C. Detection of subtilase cytotoxin (SubAB) in Shiga toxin-producing Escherichia coli strains associated with hemolytic uremic syndrome in Argentine children. In Abstracts of the Seventh International Symposium on Shiga toxin(Verocytotoxin)-Producing Escherichia coli Infections (VTEC2009), Buenos Aires, Argentina, 10-13 May 2009; Abstract P04.4.3, p. 101.
44. Tozzoli, R.; Caprioli, A.; Cappannella, S.; Michelacci, V.; Marziano, M.L.; Morabito, S. Production of the subtilase AB5 cytotoxin by Shiga toxin-negative Escherichia coli. J. Clin. Microbiol. 2010, 48, 178-183.
45. Srimanote, P.; Paton A.W.; Paton, J.C. Characterization of a novel type IV pilus locus carried on the large plasmid of human-virulent strains of locus of enterocyte effacement-negative Shigatoxigenic Escherichia coli. Infect. Immun. 2002, 70, 3094-3100.
46. Talbot, U.M.; Paton, J.C.; Paton, A.W. Protective immunization of mice with an active site mutant of subtilase cytotoxin of Shiga toxigenic Escherichia coli. Infect. Immun. 2005, 73, 4432-4436.
47. Hu, C.A.; Dougan, S.K.; Winter, S.V.; Paton, A.W.; Paton, J.C.; Ploegh, H.L. Subtilase cytotoxin cleaves newly synthesised BiP and blocks antibody secretion in B lymphocytes. J. Exp. Med. 2009, 206, 2429-2440.
48. Yamazaki, H.; Hiramatsu, N.; Hayakawa, K.; Okamura, M.; Huang, T.; Nakajima, S.; Yao, J.; Paton, A.W.; Paton, J.C.; Kitamura, M. Activation of the Akt-NF-κB pathway by subtilase cytotoxin through the ATF6 branch of the unfolded protein response. J. Immunol. 2009, 183, 1480-1487.
49. Harama, D.; Koyama, K.; Mukai, M.; Shimokawa, N.; Miyata, M.; Nakamura, Y.; Ohnuma, Y.; Ogawa, H.; Matsuoka, S.; Paton, A.W.; Paton, J.C.; Kitamura, M.; Nakao, A. A sub-cytotoxic dose of subtilase cytotoxin prevents LPS-induced inflammatory responses, depending on its capacity to induce the unfolded protein response. J. Immunol. 2009, 183, 1368-1374.
50. Varki, A. Loss of N-glycolylneuraminic acid in humans: Mechanisms, consequences, and implications for hominid evolution. Am. J. Phys. Anthropol. 2001, Suppl. 33, 54-69.
51. Tangvoranuntakul, P.; Gagneux, P.; Diaz, S.; Bardor, M.; Varki, N.; Varki, A.; Muchmore, E. Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc. Natl. Acad. Sci. USA 2003, 100, 12045-12050.
52. Takano, Y.; Hiramatsu, N.; Okamura, M.; Hayakawa, K.; Shimada, T.; Kasai, A.; Yokouchi, M.; Shitamura, A.; Yao, J.; Paton, A.W.; Paton, J.C.; Kitamura, M. Suppression of cytokine responses by GATA inhibitor K-7174: Implication for unfolded protein response. Biochem. Biophys. Res. Comm. 2007, 360, 470-475.
53. Hayakawa, K.; Hiramatsu, N.; Okamura, M.; Yao, J.; Paton, A.W.; Paton, J.C.; Kitamura, M. Blunted activation of NF-κB and NF-κB-dependent gene expression by geranylgeranylacetone: Involvement of unfolded protein response. Biochem. Biophys. Res. Comm. 2008, 365, 47-53.
54. Hayakawa, K.; Hiramatsu, N.; Okamura, M.; Yamazaki, H.; Nakajima, S.; Yao, J.; Paton, A.W.; Paton, J.C.; Kitamura, M. Acquisition of anergy to proinflammatory cytokines in nonimmune cells through endoplasmic reticulum stress response: A mechanism for subsidence of inflammation. J. Immunol. 2009, 182, 1182-1191.
55. Du, S.; Hiramatsu, N.; Hayakawa, K.; Kasai, A.; Okamura, M.; Huang, T.; Yao, J.; Takeda, M.; Araki, I.; Sawada, N.; Paton, A.W.; Paton, J.C.; Kitamura, M. Suppression of NF-κB by cyclosporin A and tacrolimus (FK506) via induction of the C/EBP family: Implication for unfolded protein response. J. Immunol. 2009, 182, 7201-7211.
56. Okamura, M.; Takano, Y.; Hiramatsu, N.; Hayakawa, K.; Yao, J.; Paton, A.W.; Paton, J.C.; Kitamura, M. Suppression of cytokine responses by indomethacin in podocytes: A mechanism through induction of unfolded protein response. Am. J. Physiol. Renal Physiol. 2009, 295, F1495-F1503.
57. Huang, T.; Wan, Y.; Zhu, Y.; Fang, X.; Hiramatsu, N.; Hayakawa, K.; Paton, A.W.; Paton, J.C.; Kitamura, M.; Yao, J. Downregulation of gap junction expression and function by endoplasmic reticulum stress. J. Cell Biochem. 2009, 107, 973-983.
58. Buchkovich, N.J.; Maguire, T.G.; Yu, Y.; Paton, A.W.; Paton, J.C.; Alwine, J.C. 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.
59. Buchkovich, N.J.; Maguire, T.G.; Paton, A.W.; Paton, J.C.; Alwine, J.C. The endoplasmic reticulum chaperone BiP/GRP78 is important in the structure and function of the HCMV assembly compartment. J. Virol. 2009, 83, 11421-11428.
60. Wati, S.; Soo, M.L.; Zilm, P.; Li, P.; Paton, A.W.; Burrell, C.J.; Beard, M.; Carr, J. M. Dengue virus infection induces GRP78 which acts to chaperone viral antigen production. J. Virol. 2009, 83, 12871-12880.
61. Macario, A.J.L.; Conway de Macario, E. Sick chaperones, cellular stress and disease. N. Engl. J. Med. 2005, 353, 1489-1501.
62. Li, J.; Lee, A.S. Stress induction of GRP78/BiP and its role in cancer. Curr. Mol. Med. 2006, 6, 45-54.
63. Backer, J.M.; Krivoshein, A.; Hamby, C.V.; Pizzonia, J.; Gilbert, K.; Ray, Y.S.; Brand, H.; Paton, A.W.; Paton, J.C.; Backer, M.V. Chaperone-targeting cytotoxin and ER stress-inducing drug synergize to kill cancer cells. Neoplasia 2009, 11, 1165-1173.