Home LiteratureArticle Details
PMID: 20210553 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

Induction of apoptosis by Shiga toxins.

Future microbiology ·Vol. 5 ·No. 3 ·2010-03-00 ·Pages 431-53

Tesh VL

Abstract

Shiga toxins comprise a family of structurally and functionally related protein toxins expressed by Shigella dysenteriae serotype 1 and multiple serotypes of Escherichia coli. While the capacity of Shiga toxins to inhibit protein synthesis by catalytic inactivation of eukaryotic ribosomes has been well described, it is also apparent that Shiga toxins trigger apoptosis in many cell types. This review presents evidence that Shiga toxins induce apoptosis of epithelial, endothelial, leukocytic, lymphoid and neuronal cells. Apoptotic signaling pathways activated by the toxins are reviewed with an emphasis on signaling mechanisms that are shared among different cell types. Data suggesting that Shiga toxins induce apoptosis through the endoplasmic reticulum stress response and clinical evidence demonstrating apoptosis in humans infected with Shiga toxin-producing bacteria are briefly discussed. The potential for use of Shiga toxins to induce apoptosis in cancer cells is briefly reviewed.

MeSH Terms
Apoptosis Endothelial Cells/microbiology Epithelial Cells/microbiology Escherichia coli/pathogenicity Humans Leukocytes/microbiology Neurons/microbiology Shiga Toxins/biosynthesis,toxicity Shigella dysenteriae/pathogenicity
Chemicals
Shiga Toxins
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Tesh Vernon L
Department of Microbial & Molecular Pathogenesis, College of Medicine, Texas A&M University System Health Science Center, 407 Reynolds Medical Building, College Station, TX 77843-1114, USA. tesh@medicine.tamhsc.edu
References (141)
141 references, click to expand
  1. Shiga toxin 1-induced activation of c-Jun NH(2)-terminal kinase and p38 in the human monocytic cell line THP-1: possible involvement in the production of TNF-alpha.
    J Leukoc Biol. 2002 Jan;71(1):107-14 PMID: 11781386
  2. Activation of Shiga toxin type 2d (Stx2d) by elastase involves cleavage of the C-terminal two amino acids of the A2 peptide in the context of the appropriate B pentamer.
    Mol Microbiol. 2002 Jan;43(1):207-15 PMID: 11849548
  3. Damage to nuclear DNA induced by Shiga toxin 1 and ricin in human endothelial cells.
    FASEB J. 2002 Mar;16(3):365-72 PMID: 11874985
  4. Identification, characterization, and distribution of a Shiga toxin 1 gene variant (stx(1c)) in Escherichia coli strains isolated from humans.
    J Clin Microbiol. 2002 Apr;40(4):1441-6 PMID: 11923370
  5. The treatment of malignant meningioma with verotoxin.
    Neoplasia. 2002 Jul-Aug;4(4):304-11 PMID: 12082546
  6. c-FLIP(L) is a dual function regulator for caspase-8 activation and CD95-mediated apoptosis.
    EMBO J. 2002 Jul 15;21(14):3704-14 PMID: 12110583
  7. Bacteriophage control of bacterial virulence.
    Infect Immun. 2002 Aug;70(8):3985-93 PMID: 12117903
  8. Escherichia coli shiga-like toxins induce apoptosis and cleavage of poly(ADP-ribose) polymerase via in vitro activation of caspases.
    Infect Immun. 2002 Aug;70(8):4669-77 PMID: 12117981
  9. Molecular basis for up-regulation by inflammatory cytokines of Shiga toxin 1 cytotoxicity and globotriaosylceramide expression.
    J Infect Dis. 2002 Oct 1;186(7):976-82 PMID: 12232838
  10. Shiga toxin receptor glycolipid binding. Pathology and utility.
    Methods Mol Med. 2003;73:165-86 PMID: 12375428
  11. Detection of Shiga toxin-mediated programmed cell death and delineation of death-signaling pathways.
    Methods Mol Med. 2003;73:229-41 PMID: 12375433
  12. Shiga-like toxin inhibition of FLICE-like inhibitory protein expression sensitizes endothelial cells to bacterial lipopolysaccharide-induced apoptosis.
    J Biol Chem. 2002 Oct 25;277(43):40567-74 PMID: 12189147
  13. DEDD and DEDD2 associate with caspase-8/10 and signal cell death.
    Oncogene. 2003 Jan 16;22(2):291-7 PMID: 12527898
  14. Insights into the regulatory mechanism for caspase-8 activation.
    Mol Cell. 2003 Feb;11(2):543-9 PMID: 12620240
  15. Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol.
    J Cell Biol. 2003 Mar 31;160(7):1115-27 PMID: 12668660
  16. Paclitaxel-induced apoptosis in BJAB cells proceeds via a death receptor-independent, caspases-3/-8-driven mitochondrial amplification loop.
    Oncogene. 2003 Apr 17;22(15):2236-47 PMID: 12700660
  17. Rapid apoptosis induced by Shiga toxin in HeLa cells.
    Infect Immun. 2003 May;71(5):2724-35 PMID: 12704147
  18. Identification and characterization of a new variant of Shiga toxin 1 in Escherichia coli ONT:H19 of bovine origin.
    J Clin Microbiol. 2003 May;41(5):2106-12 PMID: 12734256
  19. Molecular and functional analysis of Shiga toxin-induced response patterns in human vascular endothelial cells.
    Blood. 2003 Aug 15;102(4):1323-32 PMID: 12702508
  20. Shiga toxin induces decreased expression of the anti-apoptotic protein Mcl-1 concomitant with the onset of endothelial apoptosis.
    Microb Pathog. 2003 Aug;35(2):87-93 PMID: 12901848
  21. Shiga toxin-producing Escherichia coli in Montana: bacterial genotypes and clinical profiles.
    J Infect Dis. 2003 Sep 1;188(5):719-29 PMID: 12934188
  22. A multimeric model for murine anti-apoptotic protein Bcl-2 and structural insights for its regulation by post-translational modification.
    J Mol Model. 2003 Oct;9(5):298-303 PMID: 14517609
  23. Association of genomic O island 122 of Escherichia coli EDL 933 with verocytotoxin-producing Escherichia coli seropathotypes that are linked to epidemic and/or serious disease.
    J Clin Microbiol. 2003 Nov;41(11):4930-40 PMID: 14605120
  24. Two distinct Gb3/CD77 signaling pathways leading to apoptosis are triggered by anti-Gb3/CD77 mAb and verotoxin-1.
    J Biol Chem. 2003 Nov 14;278(46):45200-8 PMID: 12944404
  25. Shiga toxins and apoptosis.
    FEMS Microbiol Lett. 2003 Nov 21;228(2):159-66 PMID: 14638419
  26. Interaction of Shiga toxin from Escherichia coli with human intestinal epithelial cell lines and explants: Stx2 induces epithelial damage in organ culture.
    Cell Microbiol. 2004 Mar;6(3):289-301 PMID: 14764112
  27. Mitogen-activated protein kinases in apoptosis regulation.
    Oncogene. 2004 Apr 12;23(16):2838-49 PMID: 15077147
  28. Structure of shiga toxin type 2 (Stx2) from Escherichia coli O157:H7.
    J Biol Chem. 2004 Jun 25;279(26):27511-7 PMID: 15075327
  29. Brefeldin A and filipin distinguish two globotriaosyl ceramide/verotoxin-1 intracellular trafficking pathways involved in Vero cell cytotoxicity.
    Glycobiology. 2004 Aug;14(8):701-12 PMID: 15102715
  30. Association of active caspase 8 with the mitochondrial membrane during apoptosis: potential roles in cleaving BAP31 and caspase 3 and mediating mitochondrion-endoplasmic reticulum cross talk in etoposide-induced cell death.
    Mol Cell Biol. 2004 Aug;24(15):6592-607 PMID: 15254227
  31. Shiga toxin-encoding bacteriophages--genomes in motion.
    Int J Med Microbiol. 2004 Sep;294(2-3):115-21 PMID: 15493821
  32. Glycosphingolipids of the globo-series are associated with the monocytic lineage of human myeloid cells.
    Eur J Biochem. 1985 May 15;149(1):187-91 PMID: 3858098
  33. 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.
    Eur J Biochem. 1988 Jan 15;171(1-2):45-50 PMID: 3276522
  34. Cloning and sequencing of the genes for Shiga toxin from Shigella dysenteriae type 1.
    J Bacteriol. 1988 Mar;170(3):1116-22 PMID: 2830229
  35. Role of Shiga toxin in the pathogenesis of bacillary dysentery, studied by using a Tox- mutant of Shigella dysenteriae 1.
    Infect Immun. 1988 Dec;56(12):3099-109 PMID: 3053452
  36. Verotoxin-resistant cell clones are deficient in the glycolipid globotriosylceramide: differential basis of phenotype.
    Arch Biochem Biophys. 1991 May 1;286(2):448-52 PMID: 1910293
  37. Retrograde transport of endocytosed Shiga toxin to the endoplasmic reticulum.
    Nature. 1992 Aug 6;358(6386):510-2 PMID: 1641040
  38. Impairment by verotoxin of tubular function contributes to the renal damage seen in haemolytic uraemic syndrome.
    J Infect. 1993 Nov;27(3):339-41 PMID: 8308331
  39. Direct evidence of neuron impairment by oral infection with verotoxin-producing Escherichia coli O157:H- in mitomycin-treated mice.
    Infect Immun. 1994 Aug;62(8):3447-53 PMID: 8039916
  40. Role of processing and intracellular transport for optimal toxicity of Shiga toxin and toxin mutants.
    Exp Cell Res. 1995 May;218(1):39-49 PMID: 7737376
  41. Furin-induced cleavage and activation of Shiga toxin.
    J Biol Chem. 1995 May 5;270(18):10817-21 PMID: 7738018
  42. Crystal structure of the holotoxin from Shigella dysenteriae at 2.5 A resolution.
    Nat Struct Biol. 1994 Jan;1(1):59-64 PMID: 7656009
  43. Verocytotoxin-1 induces apoptosis in vero cells.
    J Infect. 1995 May;30(3):213-8 PMID: 7673744
  44. Interaction of cytokines and growth factor in the regulation of verotoxin-induced apoptosis in cultured human endothelial cells.
    Br J Haematol. 2001 Jun;113(4):891-7 PMID: 11442480
  45. Differentiation-associated toxin receptor modulation, cytokine production, and sensitivity to Shiga-like toxins in human monocytes and monocytic cell lines.
    Infect Immun. 1996 Apr;64(4):1173-80 PMID: 8606075
  46. Neuronal and vascular pathology produced by verocytotoxin 2 in the rabbit central nervous system.
    Acta Neuropathol. 1996;91(3):254-62 PMID: 8834537
  47. Magnetic resonance imaging and histopathological study of brain lesions in rabbits given intravenous verotoxin 2.
    Infect Immun. 1996 Dec;64(12):5053-60 PMID: 8945546
  48. Two distinct binding sites for globotriaosyl ceramide on verotoxins: identification by molecular modelling and confirmation using deoxy analogues and a new glycolipid receptor for all verotoxins.
    Chem Biol. 1996 Apr;3(4):263-75 PMID: 8807854
  49. Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the alpha-sarcin/ricin loop in the 28S rRNA.
    Mol Cell Biol. 1997 Jun;17(6):3373-81 PMID: 9154836
  50. Translocation of verotoxin-1 across T84 monolayers: mechanism of bacterial toxin penetration of epithelium.
    Am J Physiol. 1997 Dec;273(6 Pt 1):G1349-58 PMID: 9435561
  51. Apoptosis of renal cortical cells in the hemolytic-uremic syndrome: in vivo and in vitro studies.
    Infect Immun. 1998 Feb;66(2):636-44 PMID: 9453620
  52. Crystal structure of the ribosomal RNA domain essential for binding elongation factors.
    Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13436-41 PMID: 9811818
  53. Intracellular targeting of the endoplasmic reticulum/nuclear envelope by retrograde transport may determine cell hypersensitivity to verotoxin via globotriaosyl ceramide fatty acid isoform traffic.
    J Cell Physiol. 1998 Dec;177(4):646-60 PMID: 10092217
  54. Localization of verotoxin receptors in nervous system.
    Brain Res. 1999 Apr 17;825(1-2):183-8 PMID: 10216186
  55. The identification of three biologically relevant globotriaosyl ceramide receptor binding sites on the Verotoxin 1 B subunit.
    Mol Microbiol. 1999 Jun;32(5):953-60 PMID: 10361298
  56. Regulated expression of the Shiga toxin B gene induces apoptosis in mammalian fibroblastic cells.
    Mol Microbiol. 1999 Sep;33(6):1190-9 PMID: 10510233
  57. Food-related illness and death in the United States.
    Emerg Infect Dis. 1999 Sep-Oct;5(5):607-25 PMID: 10511517
  58. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies.
    Bull World Health Organ. 1999;77(8):651-66 PMID: 10516787
  59. Comparative evaluation of apoptosis induced by Shiga toxin 1 and/or lipopolysaccharides in human monocytic and macrophage-like cells.
    Microb Pathog. 2005 Feb-Mar;38(2-3):63-76 PMID: 15748808
  60. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome.
    Lancet. 2005 Mar 19-25;365(9464):1073-86 PMID: 15781103
  61. Shiga toxin is transported from the endoplasmic reticulum following interaction with the luminal chaperone HEDJ/ERdj3.
    Infect Immun. 2005 Apr;73(4):2524-32 PMID: 15784599
  62. A role for the protease-sensitive loop region of Shiga-like toxin 1 in the retrotranslocation of its A1 domain from the endoplasmic reticulum lumen.
    J Biol Chem. 2005 Jun 17;280(24):23310-8 PMID: 15817449
  63. Shiga toxin 1 induces apoptosis in the human myelogenous leukemia cell line THP-1 by a caspase-8-dependent, tumor necrosis factor receptor-independent mechanism.
    Infect Immun. 2005 Aug;73(8):5115-26 PMID: 16041028
  64. Induction of competing apoptotic and survival signaling pathways in the macrophage by the ribotoxic trichothecene deoxynivalenol.
    Toxicol Sci. 2005 Sep;87(1):113-22 PMID: 15976193
  65. The A-subunit of surface-bound Shiga toxin stimulates clathrin-dependent uptake of the toxin.
    FEBS J. 2005 Aug;272(16):4103-13 PMID: 16098193
  66. Silencing of Bak ameliorates apoptosis of human proximal tubular epithelial cells by Escherichia coli-derived Shiga toxin 2.
    Infection. 2005 Oct;33(5-6):362-7 PMID: 16258868
  67. Escherichia coli verotoxin 1 mediates apoptosis in human HCT116 colon cancer cells by inducing overexpression of the GADD family of genes and S phase arrest.
    FEBS Lett. 2005 Dec 5;579(29):6604-10 PMID: 16297916
  68. Shiga toxin B-subunit binds to the chaperone BiP and the nucleolar protein B23.
    Biol Cell. 2006 Feb;98(2):125-34 PMID: 15853775
  69. Shiga toxin 1-induced cytokine production is mediated by MAP kinase pathways and translation initiation factor eIF4E in the macrophage-like THP-1 cell line.
    J Leukoc Biol. 2006 Feb;79(2):397-407 PMID: 16301326
  70. Shiga toxins present in the gut and in the polymorphonuclear leukocytes circulating in the blood of children with hemolytic-uremic syndrome.
    J Clin Microbiol. 2006 Feb;44(2):313-7 PMID: 16455876
  71. Shiga toxin regulates its entry in a Syk-dependent manner.
    Mol Biol Cell. 2006 Mar;17(3):1096-109 PMID: 16371508
  72. The association of Shiga-like toxin with detergent-resistant membranes is modulated by glucosylceramide and is an essential requirement in the endoplasmic reticulum for a cytotoxic effect.
    Mol Biol Cell. 2006 Mar;17(3):1375-87 PMID: 16381816
  73. Entry of protein toxins into mammalian cells by crossing the endoplasmic reticulum membrane: co-opting basic mechanisms of endoplasmic reticulum-associated degradation.
    Curr Top Microbiol Immunol. 2005;300:149-68 PMID: 16573240
  74. Targeted disruption of Gb3/CD77 synthase gene resulted in the complete deletion of globo-series glycosphingolipids and loss of sensitivity to verotoxins.
    J Biol Chem. 2006 Apr 14;281(15):10230-5 PMID: 16476743
  75. Thrombin induces neurodegeneration and microglial activation in the cortex in vivo and in vitro: proteolytic and non-proteolytic actions.
    Biochem Biophys Res Commun. 2006 Aug 4;346(3):727-38 PMID: 16777064
  76. Targeting of Shiga toxin B-subunit to retrograde transport route in association with detergent-resistant membranes.
    Mol Biol Cell. 2001 Aug;12(8):2453-68 PMID: 11514628
  77. Shiga toxins.
    Toxicon. 2001 Nov;39(11):1629-35 PMID: 11595626
  78. Bcl-2 Phosphorylation by p38 MAPK: identification of target sites and biologic consequences.
    J Biol Chem. 2006 Jul 28;281(30):21353-61 PMID: 16714293
  79. Mediators of endoplasmic reticulum stress-induced apoptosis.
    EMBO Rep. 2006 Sep;7(9):880-5 PMID: 16953201
  80. The functional state of neutrophils correlates with the severity of renal dysfunction in children with hemolytic uremic syndrome.
    Pediatr Res. 2007 Jan;61(1):123-8 PMID: 17211153
  81. Mitochondrial membrane permeabilization in cell death.
    Physiol Rev. 2007 Jan;87(1):99-163 PMID: 17237344
  82. Comparative analysis of the abilities of Shiga toxins 1 and 2 to bind to and influence neutrophil apoptosis.
    Infect Immun. 2007 Feb;75(2):760-5 PMID: 17101648
  83. Shiga toxin binding in normal and inflamed human intestinal mucosa.
    Microbes Infect. 2007 Jan;9(1):35-9 PMID: 17208032
  84. Simultaneous induction of apoptotic and survival signaling pathways in macrophage-like THP-1 cells by Shiga toxin 1.
    Infect Immun. 2007 Mar;75(3):1291-302 PMID: 17194804
  85. Shiga toxin-producing Escherichia coli: an overview.
    J Anim Sci. 2007 Mar;85(13 Suppl):E45-62 PMID: 17085726
  86. Protein kinase Cdelta is activated by Shiga toxin and regulates its transport.
    J Biol Chem. 2007 Jun 1;282(22):16317-28 PMID: 17403690
  87. Apoptosis: a review of programmed cell death.
    Toxicol Pathol. 2007 Jun;35(4):495-516 PMID: 17562483
  88. Specific Rab GTPase-activating proteins define the Shiga toxin and epidermal growth factor uptake pathways.
    J Cell Biol. 2007 Jun 18;177(6):1133-43 PMID: 17562788
  89. Stx-phages: drivers and mediators of the evolution of STEC and STEC-like pathogens.
    Future Microbiol. 2007 Apr;2(2):165-74 PMID: 17661653
  90. Membrane cytosolic translocation of verotoxin A1 subunit in target cells.
    Microbiology. 2007 Aug;153(Pt 8):2700-10 PMID: 17660434
  91. Identification and characterization of small molecules that inhibit intracellular toxin transport.
    Infect Immun. 2007 Sep;75(9):4552-61 PMID: 17576758
  92. Differential binding of Shiga toxin 2 to human and murine neutrophils.
    J Med Microbiol. 2007 Nov;56(Pt 11):1423-30 PMID: 17965340
  93. Polyunsaturated fatty acids regulate Shiga toxin transport.
    Biochem Biophys Res Commun. 2007 Dec 14;364(2):283-8 PMID: 17942073
  94. The Shiga toxin genotype rather than the amount of Shiga toxin or the cytotoxicity of Shiga toxin in vitro correlates with the appearance of the hemolytic uremic syndrome.
    Diagn Microbiol Infect Dis. 2007 Nov;59(3):235-42 PMID: 17931818
  95. Shiga toxin induces tubular membrane invaginations for its uptake into cells.
    Nature. 2007 Nov 29;450(7170):670-5 PMID: 18046403
  96. The Mitogen-activated protein kinase p38 links Shiga Toxin-dependent signaling and trafficking.
    Mol Biol Cell. 2008 Jan;19(1):95-104 PMID: 17959827
  97. Molecular pathogenesis of Shigella spp.: controlling host cell signaling, invasion, and death by type III secretion.
    Clin Microbiol Rev. 2008 Jan;21(1):134-56 PMID: 18202440
  98. Shiga toxin 1 induces apoptosis through the endoplasmic reticulum stress response in human monocytic cells.
    Cell Microbiol. 2008 Mar;10(3):770-80 PMID: 18005243
  99. Retrograde traffic in the biosynthetic-secretory route.
    Histochem Cell Biol. 2008 Mar;129(3):277-88 PMID: 18270728
  100. Glycosphingolipids in vascular endothelial cells: relationship of heterogeneity in Gb3Cer/CD77 receptor expression with differential Shiga toxin 1 cytotoxicity.
    Glycoconj J. 2008 May;25(4):291-304 PMID: 18176841
  101. The catalytic subunit of shiga-like toxin 1 interacts with ribosomal stalk proteins and is inhibited by their conserved C-terminal domain.
    J Mol Biol. 2008 Apr 25;378(2):375-86 PMID: 18358491
  102. Neuronal apoptosis and inflammatory responses in the central nervous system of a rabbit treated with Shiga toxin-2.
    J Neuroinflammation. 2008;5:11 PMID: 18355415
  103. ZAK: a MAP3Kinase that transduces Shiga toxin- and ricin-induced proinflammatory cytokine expression.
    Cell Microbiol. 2008 Jul;10(7):1468-77 PMID: 18331592
  104. Shiga toxin 2 causes apoptosis in human brain microvascular endothelial cells via C/EBP homologous protein.
    Infect Immun. 2008 Aug;76(8):3679-89 PMID: 18541659
  105. Regulation of TNFR1 and CD95 signalling by receptor compartmentalization.
    Nat Rev Mol Cell Biol. 2008 Aug;9(8):655-62 PMID: 18545270
  106. Treatment and outcome of Shiga-toxin-associated hemolytic uremic syndrome (HUS).
    Pediatr Nephrol. 2008 Oct;23(10):1749-60 PMID: 18704506
  107. Use of flow cytometry in an apoptosis assay to determine pH and temperature stability of shiga-like toxin 1.
    J Microbiol Methods. 2008 Oct;75(2):167-71 PMID: 18710788
  108. Subtilase cytotoxin activates PERK, IRE1 and ATF6 endoplasmic reticulum stress-signalling pathways.
    Cell Microbiol. 2008 Sep;10(9):1775-86 PMID: 18433465
  109. Interactions between Shiga toxins and human polymorphonuclear leukocytes.
    J Leukoc Biol. 2008 Oct;84(4):1019-27 PMID: 18625912
  110. Shiga toxin 2 affects the central nervous system through receptor globotriaosylceramide localized to neurons.
    J Infect Dis. 2008 Nov 1;198(9):1398-406 PMID: 18754742
  111. Lysosomal membrane permeabilization in cell death.
    Oncogene. 2008 Oct 27;27(50):6434-51 PMID: 18955971
  112. Macropinocytosis in Shiga toxin 1 uptake by human intestinal epithelial cells and transcellular transcytosis.
    Am J Physiol Gastrointest Liver Physiol. 2009 Jan;296(1):G78-92 PMID: 18974311
  113. In vivo tumor targeting by the B-subunit of shiga toxin.
    Mol Imaging. 2008 Nov-Dec;7(6):239-47 PMID: 19123994
  114. Shiga toxins, glycosphingolipid diversity, and endothelial cell injury.
    Thromb Haemost. 2009 Feb;101(2):252-64 PMID: 19190807
  115. Death effector domain-containing proteins.
    Cell Mol Life Sci. 2009 Mar;66(5):814-30 PMID: 18989622
  116. Expression of verotoxin-1 receptor Gb3 in breast cancer tissue and verotoxin-1 signal transduction to apoptosis.
    BMC Cancer. 2009;9:67 PMID: 19245689
  117. Passage through the Golgi is necessary for Shiga toxin B subunit to reach the endoplasmic reticulum.
    FEBS J. 2009 Mar;276(6):1581-95 PMID: 19220458
  118. Bcl-2 family on guard at the ER.
    Am J Physiol Cell Physiol. 2009 May;296(5):C941-53 PMID: 19279228
  119. Caspase-8 in cancer biology and therapy.
    Cancer Lett. 2009 Aug 28;281(2):128-33 PMID: 19111387
  120. Apoptosis and autophagy: Regulation of caspase-9 by phosphorylation.
    FEBS J. 2009 Nov;276(21):6063-73 PMID: 19788417
  121. Bcl-2 regulates the onset of shiga toxin 1-induced apoptosis in THP-1 cells.
    Infect Immun. 2009 Dec;77(12):5233-44 PMID: 19752028
  122. Inhibition of neutrophil apoptosis by verotoxin 2 derived from Escherichia coli O157:H7.
    Infect Immun. 1999 Nov;67(11):6203-5 PMID: 10531291
  123. Shiga toxins 1 and 2 translocate differently across polarized intestinal epithelial cells.
    Infect Immun. 1999 Dec;67(12):6670-7 PMID: 10569789
  124. Activation of Src family kinase yes induced by Shiga toxin binding to globotriaosyl ceramide (Gb3/CD77) in low density, detergent-insoluble microdomains.
    J Biol Chem. 1999 Dec 3;274(49):35278-82 PMID: 10575015
  125. A new Shiga toxin 2 variant (Stx2f) from Escherichia coli isolated from pigeons.
    Appl Environ Microbiol. 2000 Mar;66(3):1205-8 PMID: 10698793
  126. Escherichia coli Shiga toxins induce apoptosis in epithelial cells that is regulated by the Bcl-2 family.
    Am J Physiol Gastrointest Liver Physiol. 2000 May;278(5):G811-9 PMID: 10801274
  127. Binding and transfer of verocytotoxin by polymorphonuclear leukocytes in hemolytic uremic syndrome.
    Blood. 2000 Jun 1;95(11):3396-402 PMID: 10828021
  128. Bcl-2 antiapoptotic protein mediates verotoxin II-induced cell death: possible association between bcl-2 and tissue failure by E. coli O157:H7.
    Genes Dev. 2000 Jul 15;14(14):1734-40 PMID: 10898788
  129. The B subunit of Shiga toxin fused to a tumor antigen elicits CTL and targets dendritic cells to allow MHC class I-restricted presentation of peptides derived from exogenous antigens.
    J Immunol. 2000 Sep 15;165(6):3301-8 PMID: 10975847
  130. 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. 2000 Sep;7(9):785-94 PMID: 11042673
  131. Globotriaosyl ceramide (CD77/Gb3) in the glycolipid-enriched membrane domain participates in B-cell receptor-mediated apoptosis by regulating lyn kinase activity in human B cells.
    Exp Hematol. 2000 Nov;28(11):1260-8 PMID: 11063874
  132. Caspase-3 activation and apoptosis induction coupled with the retrograde transport of shiga toxin: inhibition by brefeldin A.
    FEMS Immunol Med Microbiol. 2000 Dec;29(4):275-81 PMID: 11118908
  133. Activation of the caspase cascade during Stx1-induced apoptosis in Burkitt's lymphoma cells.
    J Cell Biochem. 2001;81(1):128-42 PMID: 11180403
  134. Detection of apoptosis in kidney biopsies of patients with D+ hemolytic uremic syndrome.
    Pediatr Res. 2001 Mar;49(3):413-6 PMID: 11228269
  135. Detection of verocytotoxin bound to circulating polymorphonuclear leukocytes of patients with hemolytic uremic syndrome.
    J Am Soc Nephrol. 2001 Apr;12(4):800-6 PMID: 11274241
  136. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation.
    Physiol Rev. 2001 Apr;81(2):807-69 PMID: 11274345
  137. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions.
    Endocr Rev. 2001 Apr;22(2):153-83 PMID: 11294822
  138. Cytoprotective effect of curcumin in human proximal tubule epithelial cells exposed to shiga toxin.
    Biochem Biophys Res Commun. 2001 Apr 27;283(1):36-41 PMID: 11322764
  139. Novel role for JNK as a stress-activated Bcl2 kinase.
    J Biol Chem. 2001 Jun 29;276(26):23681-8 PMID: 11323415
  140. Verotoxin 1 binding to intestinal crypt epithelial cells results in localization to lysosomes and abrogation of toxicity.
    Cell Microbiol. 2003 Feb;5(2):85-97 PMID: 12580945
  141. Shiga toxin 1 triggers a ribotoxic stress response leading to p38 and JNK activation and induction of apoptosis in intestinal epithelial cells.
    Infect Immun. 2003 Mar;71(3):1497-504 PMID: 12595468
Article Info
Journal
Future microbiology
Abbr.
Future Microbiol
ISSN
1746-0921
DOI
10.2217/fmb.10.4
Email
tesh@medicine.tamhsc.edu
Published
2010-03-00
Pages
431-53
Language
English
Region
England
NLM ID
101278120
PMCID
PMC2855686
Subset
IM
Grants
NIAID NIH HHS · R01 AI034530 · United States
NIAID NIH HHS · R01 AI034530-12 · United States
NIAID NIH HHS · R01 AI34530-12 · United States
External Links
PubMed source DOI: 10.2217/fmb.10.4 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2