Mechanism of Clostridium difficile toxin A-induced apoptosis in T84 cells

Journal of Infectious Diseases

Volumn 186, Issue 10, 2002, Pages 1438-1447

  Brito, Gerly A C ^a   Fujji, Jun ^a   Carneiro Filho, Benedito A ^b   Lima, Aldo A M ^a   Obrig, Tom ^b   Guerrant, Richard L ^b  

^a FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 6; CASPASE 8; CASPASE 9; CASPASE INHIBITOR; CLOSTRIDIUM DIFFICILE TOXIN A; GUANOSINE TRIPHOSPHATASE; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEIN BID; RHO FACTOR; UNCLASSIFIED DRUG; URIDINE 5' DIPHOSPHATE 2',3' DIALDEHYDE; URIDINE DIPHOSPHATE;

APOPTOSIS; ARTICLE; CLOSTRIDIUM DIFFICILE; CONTROLLED STUDY; ENTERITIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME RELEASE; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; MITOCHONDRIAL MEMBRANE; PATHOGENICITY; PRIORITY JOURNAL; TOXICITY;

ANNEXIN A5; ANTIBODIES; APOPTOSIS; BACTERIAL TOXINS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CARRIER PROTEINS; CASPASE 8; CASPASE 9; CASPASES; CELLS, CULTURED; CYTOCHROME C GROUP; DNA FRAGMENTATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENTEROTOXINS; HUMANS; MEMBRANE POTENTIALS; MITOCHONDRIA; RHO GTP-BINDING PROTEINS; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0037111088     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/344729     Document Type: Article

References (62)

1. Brettle RP. Wallace E. Clostridium difficile-associated diarrhea. J Infect 1984; 8:123-8.
2. George WL, Rolfe RD, Harding GK, Klein R, Putnam CW, Finegold SM. Clostridium difficile and cytotoxin in feces of patients with antimicrobial agent-associated pseudomembranous colitis. Infection 1982; 10:205-8.
3. Gilligan PH, McCarthy LR, Genta VM. Relative frequency of Clostridium difficile in patients with diarrheal disease. J Clin Microbiol 1981; 14:26-31.
4. Price AB, Davies DR, Pseudomembranous colitis. J Clin Pathol 1977;30:1-12.
5. Thielman NM, Guerrant RL. Clostridium difficile and its toxins. In: Iglewski B, Moss J, Tu AT, Vaughn M, eds. Handbook of Natural Toxins. New York: Marcel Dekker, 1995:327-66.
6. Bartlett JG, Taylor NS, Chang T, Dzink J. Clinical and laboratory observations in Clostridium difficile colitis. Am J Clin Nutr 1980; 33:2521-6.
7. Humphrey CD, Condon CW, Cantey JR, Pittman FE. Partial purification of a toxin found in hamsters with antibiotic-associated colitis: Reversible binding of the toxin by cholestyramine. Gastroenterology 1979; 76:468-76.
8. Lima AA, Innes DJ Jr, Chadee K, Lyerly DM, Wilkins TD, Guerrant RL, Clostridium difficile toxin A: Interactions with mucus and early sequential histopathologic effects in rabbit small intestine. Lab Invest 1989; 61:419-25.
9. Lima AAM, Lyerly DM, Wilkins TD, Innes DJ, Guerrant RL. Effects of Clostridium difficile toxins A and B in rabbit small and large intestine in vivo and on cultured cells in vitro. Infect Immun 1988; 56:582-8.
10. Lyerly DM, Lockwood DE, Richardson SH, Wilkins TD. Biological activities of toxins A and B of Clostridium difficile. Infect Immun 1982; 35:1147-50.
11. Lyerly DM, Krivan HC, Wilkins TD. Clostridium difficile: Its disease and toxins [review]. Clin Microbiol Rev 1988; 1:1-18.
12. Rehg JE, Cecal toxin(s) from guinea pigs with clindamycin-associated colitis, neutralized by Clostridium sordellii antitoxin. Infect Immun 1980; 27:387-90.
13. Just I, Wilm M, Seizer J, et al. The enterotoxin from Clostridium difficile (ToxA) monoglucosylates the p proteins. J Biol Chem 1995;270:13932-6.
14. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998;279:509-14.
15. Potten CS, Epithelial cell growth and differentiation. II. Intestinal apoptosis. Am J Physiol 1997;273:G253-7.
16. Cryns V, Yuan J. The cutting edge: Caspases in apoptosis and disease. In: Lockshin R, Zakeri Z, Tilly J, eds. When Cells Die. New York: Wiley-Liss. 1998:177-210.
17. Wolf BB, Green DR, Suicidal tendencies: Apoptotic cell death by caspase family proteinases. J Biol Chem 1999;274:20049-52.
18. Raff M. Cell suicide for beginners. Nuture 1998;396:119-22.
19. Ashkenazi A, Dixit VM. Death receptors: Signaling and modulation. Science 1998;281:1305-8.
20. Nunez G, Benedict MA, Hu Y. Inohara N. Caspases: The proteases of the apoptotic pathway. Oncogene 1998;17:3237-45.
21. Rokhlin OW, Glover RA, Cohen MB. Fas-mediated apoptosis in human prostatic carcinoma cell lines occurs via activation of caspase-8 and caspase-7. Cancer Res 1998;58:5870-5.
22. Green DR, Reed JC. Mitochondria and apoptosis. Science 1998;281:1309-12.
23. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: A primary site for Bcl-2 regulation ofapoptosis. Science 1997;275:1132-6.
24. Saleh A, Srinivasula SM, Acharya S, Fishel R, Alnemri ES. Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation. J Biol Chem 1999;274:17941-5.
25. Kang JJ, Schaber MD, Srinivasula SM, et al. Cascades of mammalian caspase activation in the yeast Saccharomyces cerevisiae. J Biol Chem 1999;274:3189-98.
26. Stennicke HR, Jurgensmeier JM, Shin H, et al. Pro-caspase-3 is a major physiologic target of caspase-8. J Biol Chem 1998;273:27084-90.
27. Lazebnik YA, Takahashi A, Moir RD, et al. Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc Natl Acad Sci USA 1995;92:9042-6.
28. Orth K, Chinnaiyan AM, Garg M, Froelich CJ, Dixit VM. The CED-3/ICE-like protease Mch2 is activated during apoptosis and cleaves the death substrate lamin A. J Biol Chem 1996; 271:16443-6.
29. Mashima T, Naito M, Noguchi K, Miller DK, Nicholson DW, Tsuruo T. Actin cleavage by CPP-32/apopain during the development of apoptosis. Oncogene 1997; 14:1007-12.
30. Liu X, Zou H, Slaughter C, Wang X, DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 1997; 89:175-84.
31. Sakahira H, Enari M, Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 1998;391:96-9.
32. Zamzami N, El Hamel C, Maisse C, et al. Bid acts on the permeability transition pore complex to induce apoptosis. Oncogene 2000;19:6342-50.
33. Pothoulakis C. LaMont JT. Microbes and microbial toxins: Paradigms for microbial-mucosal interactions. II. The integrated response of the intestine to Clostridium difficile toxins. Am J Physiol Gastrointest Liver Physiol 2001;280:G178-83.
34. Fiorentini C, Arancia G, Paradisi S, et al. Effects of Clostridium difficile toxins A and B on cytoskeleton organization in HEp-2 cells: A comparative morphological study. Toxicon 1989; 27:1209-18.
35. Mahida YR, Makh S, Hyde S, Gray T, Borriello SP. Effect of Clostridium difficile toxin A on human intestinal epithelial cells: Induction of interleukin 8 production and apoptosis after cell detachment. Gut 1996; 38:337-47.
36. Mahida YR, Galvin A, Makh S, et al. Effect of Clostridium difficile toxin A on human colonic lamina propria cells: Early loss of macrophages followed by T-cell apoptosis. Infect Immun 1998;66:5462-9.
37. Calderon GM, Torres-Lopez J, Lin TJ, et al. Effects of toxin A from Clostridium difficile on mast cell activation and survival. Infect Immun 1998; 66:2755-61.
38. Genth H, Selzer J, Busch C, et al. New method to generate enzymatically deficient Clostridium difficile toxin B as an antigen for immunization. Infect Immun 2000; 68:1094-101.
39. Sellins KS, Cohen JJ. Gene induction by gamma-irradiation leads to DNA fragmentation in lymphocytes. J Immunol 1987; 139:3199-206.
40. Heibein JA, Goping IS, Barry M, et al. Granzyme B-mediated cytochrome c release is regulated by the Bcl-2 family members Bid and Bax. J Exp Med 2000; 192:1391-402.
41. Bitko V, Barik S. Persistent activation of RelA by respiratory syncytial virus involves protein kinase C, underphosphorylated IκBβ, and sequestration of protein phosphatase 2A by the viral phosphoprotein. J Virol 1998;72: 5610-8.
42. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis: Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein-labelled Annexin V. J Immunol Methods 1995:184:39-51.
43. Bobak D, Moorman J, Guanzon A. Gilmer L, Hahn C. Inactivation of the small GTPase Rho disrupts cellular attachment and induces adhesion-dependent and adhesion-independent apoptosis. Oncogene 1997;15:2179-89.
44. Petit PX, Susin SA, Zamzami N, Mignotte B, Kroemer G. Mitochondria and programmed cell death: Back to the future. FEBS Lett 1996;396:7-13.
45. Susin SA, Lorenzo HK, Zamzami N, et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999;397:441-6.
46. Cai J, Jones DP. Superoxide in apoptosis: Mitochondrial generation triggered by cytochrome c loss. J Biol Chem 1998;273:11401-4.
47. Abastado JP. Apoptosis: Function and regulation of cell death [review]. Res Immunol 1996;147:443-56.
48. Thornberry NA, Lazebnik Y. Caspases: Enemies within [review]. Science 1998:281:1312-6.
49. He D, Hagen SJ, Pothoulakis C, et al. Clostridium difficile toxin A causes early damage to mitochondria in cultured cells. Gastroenterology 2000: 119:139-50.
50. Adams JM, Cory S. The Bcl-2 Protein Family: Arbiters of Cell Survival [Review] 1998:281:1322-6.
51. Desagher S, Osen-Sand A, Nichols A, et al. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 1999:144:891-901.
52. Rocha MF, Maia ME, Bezerra LR, et al. Clostridium difficile toxin A induces the release of neutrophil chemotactic factors from rat peritoneal macrophages: Role of interleukin-1β, tumor necrosis factor-α, and leukotrienes. Infect Immun 1997:65:2740-6.
53. Jung HC, Eckmann L, Yang SK, et al. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest 1995:95:55-65.
54. Taylor CT, Dzus AL, Colgan SP. Autocrine regulation of epithelial permeability by hypoxia: Role for polarized release of tumor necrosis factor-α. Gastroenterology 1998:114:657-68.
55. Le'Negrate G, Selva E, Auberger P, Rossi B, Hofman P. Sustained polymorphonuclear leukocyte transmigration induces apoptosis in T84 intestinal epithelial cells. J Cell Biol 2000;150:1479-88.
56. Moorman JP, Bobak DA, Hahn CS. Inactivation of the small GTP binding protein Rho induces multinucleate cell formation and apoptosis in murine T lymphoma EL4. J Immunol 1996:156:4146-53.
57. Nishida K, Kaziro Y, Satoh T. Anti-apoptotic function of Rac in hematopoietic cells. Oncogene 1999:18:407-15.
58. Gomez J, Martinez C, Giry M, Garcia A, Rebollo A. Rho prevents apoptosis through Bcl-2 expression: Implications for interleukin-2 receptor signal transduction. Eur J Immunol 1997;27:2793-9.
59. Fiorentini C, Matarrese P, Straface E, et al. Toxin-induced activation of Rho GTP-binding protein increases Bcl-2 expression and influences mitochondrial homeostasis. Exp Cell Res 1998:242:341-50.
60. Bobak D, Moorman J, Guanzon A, Gilmer L, Hahn C. Inactivation of the small GTPase Rho disrupts cellular attachment and induces adhesion-dependent and adhesion-independent apoptosis. Oncogene 1997:15:2179-89.
61. Jimenez B, Arends M, Esteve P, et al. Induction of apoptosis in N1H3T3 cells after serum deprivation by overexpression of rho-p21, a GTPase protein of the ras superfamily. Oncogene 1995:10:811-6.
62. Esteve P, Embade N, Perona R, et al. Rho-regulated signals induce apoptosis in vitro and in vivo by a p53-independent, but Bcl2-dependent pathway. Oncogene 1998:17:1855-69.