Fascination with bacteria-triggered cell death: The significance of Fas-mediated apoptosis during bacterial infection in vivo

Microbes and Infection

Volumn 5, Issue 12, 2003, Pages 1149-1158

  Menaker, Rena J ^a,b   Jones, Nicola L ^a,b,c  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Apoptosis; Bacteria; Death receptor; Fas; Infections

Indexed keywords

CASPASE 3; CASPASE 6; CASPASE 7; CASPASE 8; CYSTEINE; FAS ANTIBODY; FAS ANTIGEN; FAS LIGAND; INTERLEUKIN 1BETA CONVERTING ENZYME; MEMBRANE PROTEIN; PERFORIN; PROTEIN BCL 2; RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; VEROTOXIN; VIRULENCE FACTOR;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; AMINO TERMINAL SEQUENCE; APOPTOSIS; AUTOIMMUNE DISEASE; AUTOSOMAL RECESSIVE DISORDER; BACTERIAL INFECTION; BACTERIUM; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CELL PROLIFERATION; CYSTIC FIBROSIS; DISEASE COURSE; EPITHELIUM CELL; ESCHERICHIA COLI; GASTRITIS; GENE MUTATION; GENETIC CODE; HELICOBACTER FELIS; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HEMOLYTIC ANEMIA; HOMEOSTASIS; HOST; HOST CELL; HUMAN; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IN VIVO STUDY; INFLAMMATION; LISTERIA MONOCYTOGENES; LUNG TUBERCULOSIS; LYMPHOPROLIFERATIVE DISEASE; MACROPHAGE; MENINGITIS; MOUSE STRAIN; MYCOBACTERIUM TUBERCULOSIS; NATURAL KILLER CELL; NONHUMAN; PEPTIC ULCER; PNEUMONIA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PSEUDOMONAS AERUGINOSA; REVIEW; SEPSIS; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; STOMACH CANCER; T LYMPHOCYTE;

BACTERIA (MICROORGANISMS);

EID: 0141749375     PISSN: 12864579     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micinf.2003.08.001     Document Type: Short Survey

References (102)

1. Meier P., Finch A., Evan G. Apoptosis in development. Nature. 407:2000;796-801.
2. Savill J. Phagocyte recognition of apoptotic cells. Biochem. Soc. Trans. 24:1996;1065-1069.
3. Mysler E., Bini P., Drapp J., Ramos P., Friedman S.M., Krammer P.H., Elkon K.B. The apoptosis-1/Fas protein in human systemic lupus erythematosus. J. Clin. Invest. 93:1994;1029-1034.
4. Galle P.R., Hofmann W.J., Walczak H., Schaller H., Otto G., Stremmel W., Krammer P.H., Runkel L. Involvement of the CD95 (APO-1/Fas) receptor and ligand in liver damage. J. Exp. M. 182:1995;1223-1230.
5. Narula J., Haider N., Virmani R., DiSalvo T.G., Kolodgie F.D., Hajjar R.J., Schmidt U., Semigran M.J., Dec G.W., Khaw B.-A. Apoptosis in myocytes in end stage heart failure. New Engl. J. M. 335:1996;1182-1189.
6. Thompson C.B. Apoptosis in the pathogenesis and treatment of disease. Science. 267:1995;1456-1462.
7. Tanaka J., Asaka M., Imamura M. T-cell co-signalling molecules in graft-versus-host disease. Ann. Haematol. 79:2000;283-290.
8. Ashkenazi A., Dixit V.M. Death receptors: signaling and modulation. Science. 281:1998;1305-1308.
9. Nagata S., Goldstein P. The Fas death factor. Science. 267:1995;1449-1456.
10. Timmer T., de Vries E.G., de Jong S. Fas receptor-mediated apoptosis: a clinical application? J. Pathol. 196:2002;125-134.
11. Itoh N., Nagata S. A novel protein domain required for apoptosis. Mutational analysis of human Fas antigen. J. Biol. Chem. 268:1993;10932-10937.
12. Tanaka M., Suda T., Haze K., Nakamura N., Sato K., Kimura F., Motoyoshi K., Mizuki M., Tagawa S., Ohga S., Hatake K., Drummond A.H., Nagata S. Fas ligand in human serum. Nat. M. 2:1996;317-322.
13. Hohlbaum A.M., Gregory M.S., Ju S.T., Marshak-Rothstein A. Fas ligand engagement of resident peritoneal macrophages in vivo induces apoptosis and the production of neutrophil chemotactic factors. J. Immunol. 167:2001;6217-6224.
14. Seino K., Iwabuchi K., Kayagaki N., Miyata R., Nagaoka I., Matsuzawa A., Fukao K., Yagita H., Okumura K. Chemotactic activity of soluble Fas ligand against phagocytes. J. Immunol. 161:1998;4484-4488.
15. Ottonello L., Tortolina G., Amelotti M., Dallegri F. Soluble Fas ligand is chemotactic for human neutrophilic polymorphonuclear leukocytes. J. Immunol. 162:1999;3601-3606.
16. Miwa K., Asano M., Horai R., Iwakura Y., Nagata S., Suda T. Caspase 1-independent IL-1β release and inflammation induced by the apoptosis inducer Fas ligand. Nat. M. 4:1998;1287-1292.
17. Hohlbaum A.M., Moe S., Marshak-Rothstein A. Opposing effects of transmembrane and soluble Fas-ligand on inflammation and tumor cell survival. J. Exp. M. 191:2000;1209-1220.
18. Varadhachary A.S., Salgame P. CD95 mediated T cell apoptosis and its relevance to immune deviation. Oncogene. 17:1998;3271-3276.
19. Nagata S. Apoptosis by death factor. Cell. 88:1997;355-365.
20. Kischkel F.C., Hellbardt S., Behrmann I., Germer M., Pawlita M., Krammer P.H., Peter M.E. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J. 14:1995;5579-5588.
21. Scaffidi C., Fulda S., Srinivasan A., Friesen C., Li F., Tomaselli K.J., Debatin K.-M., Krammer P.H., Peter M.E. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17:1998;1675-1687.
22. Boldin M.P., Goncharov T.M., Goltseve Y.V., Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell. 85:1996;803-815.
23. Cohen G.M. Caspases: the executioners of apoptosis. Biochem. J. 326:1997;1-16.
24. Enari M., Sakahira H., Yokoyama H., Okawa K., Iwamatsu A., Nagata S. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature. 391:1998;43-50.
25. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/Caspase-9 complex initiates an apoptotic protease cascade. Cell. 91:1997;479-489.
26. Krammer P.H. CD95's deadly mission in the immune system. Nature. 407:2000;789-795.
27. Harris M.H., Thompson C.B. The role of the Bcl-2 family in the regulation of outer mitochondrial membrane permeability. Cell Death Differ. 7:2000;1182-1191.
28. Shimizu S., Narita M., Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature. 399:1999;483-487.
29. Siegel R.M., Chan F.K.-M., Chun H.J., Lenardo M.J. The multifaceted role of Fas signaling in immune cell homeostasis and autoimmunity. Nat. Immunol. 1:2000;469-474.
30. Golstein P. Signal transduction. FasL binds preassembled Fas. Science. 288:2000;2328-2329.
31. Siegel R.M., Frederiksen J.K., Zacharias D.A., Chan F.K., Johnson M., Lynch D., Tsien R.Y., Lenardo M.J. Fas preassociation required for apoptosis signaling and dominant inhibition by pathogenic mutations. Science. 288:2000;2354-2357.
32. Fisher G.H., Rosenberg F.J., Straus S.E., Dale J.K., Middleton L.A., Lin A.Y., Strober W., Lenardo M.J., Puck J.M. Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell. 81:1995;935-946.
33. Takahashi T., Tanaka M., Brannan C.I., Jenkins N.A., Copeland N.G., Suda T., Nagata S. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell. 76:1994;969-976.
34. Watanabe-Fukunaga R., Brannan C.I., Copeland N.G., Jenkins N.A., Nagata S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature. 356:1992;314-317.
35. Trune D.R., Kempton J.B. Female MRL.MpJ-Fas(lpr) autoimmune mice have greater hearing loss than males. Hear Res. 167:2002;170-174.
36. Nose M., Nishihara M., Kamogawa J., Terada M., Nakatsuru S. Genetic basis of autoimmune disease in MRL/lpr mice: dissection of the complex pathological manifestations and their susceptibility loci. Rev. Immunogenet. 2:2000;154-164.
37. Toda I., Sullivan B.D., Wickham L.A., Sullivan D.A. Gender- and androgen-related influence on the expression of proto-oncogene and apoptotic factor mRNAs in lacrimal glands of autoimmune and non-autoimmune mice. J. Steroid Biochem. Mol. Biol. 71:1999;49-61.
38. Zychlinksy A., Sansonetti P. Perspectives series: host/pathogen interactions. Apoptosis in bacterial pathogenesis. J. Clin. Invest. 100:1997;493-495.
39. Braun J.S., Novak R., Herzog K.-H., Bodner S.M., Cleveland J.L., Tuomanen E.I. Neuroprotection by a caspase inhibitor in acute bacterial meningitis. Nat. M. 5:1999;298-302.
40. Leib S.L., Kim Y.S., Chow L.L., Sheldon R.A., Tauber M.G. Reactive oxygen intermediates contribute to necrotic and apoptotic neuronal injury in an infant rat model of bacterial meningitis due to group B streptococci. J. Clin. Invest. 98:1996;2632-2639.
41. Zychlinksy A. Apoptosis as a proinflammatory event: what can we learn from bacterial-induced cell death? Trends Microbiol. 5:1997;201-204.
42. Sly L.M., Hingley-Wilson S.M., Reiner N.E., McMaster W.R. Survival of Mycobacterium tuberculosis in host macrophages involves resistance to apoptosis dependent upon induction of antiapoptotic Bcl-2 family member Mcl-1. J. Immunol. 170:2003;430-437.
43. Covacci A., Telford J.L., Giudice G.D., Parsonnet J., Rappuoli R. Helicobacter pylori virulence and genetic geography. Science. 284:1999;1328-1333.
44. Peek R.M. Jr, Blaser M.J. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer. 2:2002;28-37.
45. Jones N.L., Day A.S., Jennings H.A., Sherman P.M. Helicobacter pylori induces gastric epithelial cell apoptosis in association with increased Fas receptor expression. Infect. Immun. 67:1999;4237-4242.
46. Hofman V., Ricci V., Mograbi B., Brest P., Luciano F., Boquet P., Rossi B., Auberger P., Hofman P. Helicobacter pylori lipopolysaccharide hinders polymorphonuclear leukocyte apoptosis. Lab. Invest. 81:2001;375-384.
47. Wang J., Brooks E.G., Bamford K.B., Denning T.L., Pappo J., Ernst P.B. Negative selection of T cells by Helicobacter pylori as a model for bacterial strain selection by immune evasion. J. Immunol. 167:2001;926-934.
48. Moss S.F. The carcinogenic effect of H. pylori on the gastric epithelial cell. J. Physiol. Pharmacol. 50:1999;847-856.
49. Moss S.F., Calam J., Agarwal B., Wang S., Holt P.R. Induction of gastric epithelial apoptosis by Helicobacter pylori. Gut. 38:1996;498-501.
50. Kohda K., Tanaka K., Aiba Y., Yasuda M., Miwa T., Koga Y. Role of apoptosis induced by Helicobacter pylori infection in the development of duodenal ulcer. Gut. 44:1999;456-462.
51. Scotiniotis I.A., Rokkas T., Furth E.E., Rigas B., Shiff S.J. Altered gastric epithelial cell kinetics in Helicobacter pylori-associated intestinal metaplasia: implications for gastric carcinogenesis. Int. J. Cancer. 85:2000;192-200.
52. Houghton J., Korah R.M., Condon M.R., Kim K.H. Apoptosis in Helicobacter pylori-associated gastric and duodenal ulcer disease is mediated via the Fas antigen pathway. Dig. Dis. Sci. 44:1999;465-478.
53. Jones N.L., Day A.S., Jennings H., Shannon P.T., Galindo-Mata E., Sherman P.M. Enhanced disease severity in Helicobacter pylori-infected mice deficient in Fas signaling. Infect. Immun. 70:2002;2591-2597.
54. Houghton J.M., Bloch L.M., Goldstein M., Von Hagen S., Korah R.M. In vivo disruption of the Fas pathway abrogates gastric growth alterations secondary to Helicobacter infection. J. Infect. Dis. 182:2000;856-864.
55. Mohammadi M., Redline R., Nedrud J., Czinn S. Role of the host in pathogenesis of Helicobacter-associated gastritis: H. felis infection of inbred and congenic mouse strains. Infect. Immun. 64:1996;238-245.
56. Fox J.G., Rogers A.B., Ihrig M., Taylor N.S., Whary M.T., Dockray G., Varro A., Wang T.C. Helicobacter pylori-associated gastric cancer in INS-GAS mice is gender specific. Cancer Res. 63:2003;942-950.
57. Adachi M., Watanabe-Fukunaga R., Nagata S. Aberrant transcription caused by the insertion of an early transposable element in an intron of the Fas antigen gene of lpr mice. Proc. Natl. Acad. Sci. USA. 90:1993;1756-1760.
58. Ayala A., Herndon C., Lehman D., Ayala C.A., Chaudry I.H. Differential induction of apoptosis in lymphoid tissues during sepsis: variation in onset, frequency, and the nature of the mediators. Blood. 87:1996;4261-4275.
59. Hotchkiss R.S., Swanson P.E., Cobb J.P., Jacobson A., Buchman T.G., Karl I.E. Apoptosis in lymphoid and parenchymal cells during sepsis: findings in normal and T- and B-cell-deficient mice. Crit. Care M. 25:1997;1298-1307.
60. Chung C., Ying X.X., Wang W., Chaudry I.H., Ayala A. Is Fas ligand or endotoxin responsible for mucosal lymphocyte apoptosis in sepsis? Arch. Surg. 133:1998;1213-1220.
61. Hotchkiss R.S., Swanson P.E., Knudson C.M., Chang K.C., Cobb J.P., Osborne D.F., Zollner K.M., Buchman T.G., Korsmeyer S.J., Karl I.E. Overexpression of Bcl-2 in transgenic mice decreases apoptosis and improves survival in sepsis. J. Immunol. 162:1999;4148-4156.
62. Hotchkiss R.S., Tinsley K.W., Swanson P.E., Chang K.C., Cobb J.P., Buchman T.G., Korsmeyer S.J., Karl I.E. Prevention of lymphocyte cell death in sepsis improves survival in mice. Proc. Natl. Acad. Sci. USA. 96:1999;14541-14546.
63. Grobmyer S.R., Armstrong R.C., Nicholson S.C., Gabay C., Arend W.P., Potter S.H., Melchior M., Fritz L.C., Nathan C.F. Peptidomimetic fluoromethylketone rescues mice from lethal endotoxic shock. Mol. M. 5:1999;585-594.
64. Nicholson D.W. From bench to clinic with apoptosis-based therapeutic agents. Nature. 407:2000;810-816.
65. Jendrossek V., Grassmé H., Mueller I., Lang F., Gulbins E. Pseudomonas aeruginosa-induced apoptosis involves mitochondria and stress-activated protein kinases. Infect. Immun. 69:2001;2675-2683.
66. Verheij M., Bose R., Lin X.H., Yao B., Jarvis W.D., Grant S., Birrer M.J., Szabo E., Zon L.I., Kyriakis J.M., Haimowitz-Friedman A., Fuks Z., Kolesnick R.N. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature. 380:1996;75-79.
67. L in response to DNA-damage. J. Biol. Chem. 275:2000;322-327.
68. Grassmé H., Kirschnek S., Riethmueller J., Riehle A., von Kürthy G., Lang F., Weller M., Gulbins E. CD95/CD95 ligand interactions on epithelial cells in host defense to Pseudomonas aeruginosa. Science. 290:2000;527-530.
69. Hotchkiss R.S., Dunne W.M., Swanson P.E., Davis C.G., Tinsley K.W., Chang K.C., Buchman T.G., Karl I.E. Role of apoptosis in Pseudomonas aeruginosa pneumonia. Science. 294:2001;1783a.
70. Guilbault C., Stotland P., Lachance C., Tam M., Keller A., Thompson-Snipes L., Cowley E., Hamilton T.A., Eidelman D.H., Stevenson M.M., Radzioch D. Influence of gender and interleukin-10 deficiency on the inflammatory response during lung infection with Pseudomonas aeruginosa in mice. Immunology. 107:2002;297-305.
71. Dye C., Scheele S., Dolin P., Pathania V., Raviglione M.C. Consensus statement: global burden of tuberculosis: estimated incidence, prevalence and mortality by country. WHO Global Surveillance and Monitoring Project. J. Am. Med. Assoc. 282:1999;677-686.
72. Pathan A.A., Wilkinson K.A., Klenerman P., McShane H., Davidson R.N., Pasvol G., Hill A.V., Lalvani A. Direct ex vivo analysis of antigen-specific IFN-gamma-secreting CD4 T cells in Mycobacterium tuberculosis-infected individuals: associations with clinical disease state and effect of treatment. J. Immunol. 167:2001;5217-5225.
73. Stenger S., Hanson D.A., Teitelbaum R., Dewan P., Niazi K.R., Froelich C.J., Ganz T., Thoma-Uszynski S., Melian A., Bogdna C., Porcelli S.A., Bloom B.R., Krensky A.M., Modlin R.L. The antimicrobial activity of cytolytic T cells is mediated by granulysin. Science. 282:1998;121-125.
74. Trapani J.A., Smyth M.J. Functional significance of the perforin/ granzyme cell death pathway. Nat. Rev. Immunol. 2:2002;735-747.
75. Turner J., D'Souza C.D., Pearl J.E., Marietta P., Noel M., Frank A.A., Appelberg R., Orme I.M., Cooper A.M. CD8- and CD95/95L-dependent mechanisms of resistance in mice with chronic pulmonary tuberculosis. Am. J. Respir. Cell Mol. Biol. 24:2001;203-209.
76. Oddo M., Renno T., Attinger A., Bakker T., MacDonald H.R., Meylan P.R.A. Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. J. Immunol. 160:1998;5448-5454.
77. Balcewicz-Sablinska M.K., Keane J., Kornfeld H., Remold H.G. Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-α J. Immunol. 161:1998;2636-2641.
78. Keane J., Balcewicz-Sablinska M.K., Remold H.G., Chupp G.L., Meek B.B., Fenton M.J., Kornfeld H. Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect. Immun. 65:1997;298-304.
79. Mustafa T., Bjune G., Jonsson R., Pando R.H., Nilsen R. Increased expression of Fas ligand in human tuberculosis and leprosy lesions: a potential novel mechanism of immune evasion in Mycobacterial infection. Scand. J. Immunol. 54:2001;630-639.
80. Dockrell D.H., Badley A.D., Villacian J.S., Heppelmann C.J., Algeciras A., Ziesmer S., Yagita H., Lynch D.H., Roche P.C., Leibson P.J., Paya C.V. The expression of Fas ligand by macrophages and its upregulation by human immunodeficiency virus infection. J. Clin. Invest. 101:1998;2394-2405.
81. Mustafa T., Phyu S., Nilsen R., Bjune G., Jonsson R. Increased expression of Fas ligand on Mycobacterium tuberculosis infected macrophages: a potential novel mechanism of immune evasion by Mycobacterium tuberculosis? Inflammation. 23:1999;507-521.
82. Wing E.J., Gregory S.H. Listeria monocytogenes: clinical and experimental update. J. Infect. Dis. 185:2002;S18-S24.
83. Jensen E.R., Glass A.A., Clark W.R., Wing E.J., Miller J.F., Gregory S.H. Fas (CD95)-dependent cell-mediated immunity to Listeria monocytogenes. Infect. Immun. 66:1998;4143-4150.
84. Gregory S.H., Sagnimeni A.J., Wing E.J. Bacteria in the bloodstream are trapped in the liver and killed by immigrating neutrophils. J. Immunol. 157:1996;2514-2520.
85. Rogers H.W., Callery M.P., Deck B., Unanue E.R. Listeria monocytogenes induces apoptosis of infected hepatocytes. J. Immunol. 156:1996;679-684.
86. Mannering S.I., Zhong J., Cheers C. T-cell activation, proliferation and apoptosis in primary Listeria monocytogenes infection. J. Immunol. 106:2002;87-95.
87. Mueller N.J., Wilkinson R.A., Fishman J.A. Listeria monocytogenes infection in caspase-11-deficient mice. Infect. Immun. 70:2002;2657-2664.
88. Fuse Y., Nishimura H., Maeda K., Yoshikai Y. CD95 (Fas) may control the expansion of activated T cells after elimination of bacteria in murine listeriosis. Infect. Immun. 65:1997;1883-1891.
89. Mukasa A., Lahn M., Fleming S., Freiberg B., Pflum E., Vollmer M., Kupfer A., O'Brien R., Born W. Extensive and preferential Fas/Fas ligand-dependent death of γδ T cells following infection with Listeria monocytogenes. Scand. J. Immunol. 56:2002;223-247.
90. Ferrick D.A., Schrenzel M.D., Mulvania T., Hsieh B., Ferlin W.G., Lepper H. Differential production of interferon-γ and interleukin-4 in response to Th1 and Th2-stimulating pathogens by γδ T cells in vivo. Nature. 373:1995;255-257.
91. Fu Y.X., Roark C.E., Kelly K., Drevets D., Campbell P., O'Brien R., Born W. Immune protection and control of inflammatory tissue necrosis by γδ T cells. J. Immunol. 153:1994;3101-3115.
92. Nataro J.P., Kaper J.B. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:1998;142-201.
93. Lingwood C.A. Role of verotoxin receptors in pathogenesis. Trends Microbiol. 4:1996;147-153.
94. Lingwood C.A., Law H., Richardson S.E., Petric M., Brunton J.L., de Grandis S., Karmali M.A. Glycolipid binding of purified and recombinant Escherichia coli produced verotoxin in vitro. J. Biol. Chem. 262:1987;8834-8839.
95. Jones N.L., Islur A., Haq R., Mascarenhas M., Karmali M.A., Perdue M.H., Zanke B.W., Sherman P.M. Escherichia coli Shiga toxins induce apoptosis in epithelial cells that is regulated by the Bcl-2 family. Am. J. Physiol. Gastrointest. Liver Physiol. 278:2000;811-819.
96. Ching J.C.Y., Jones N.L., Ceponis P.J.M., Karmali M.A., Sherman P.M. Escherichia coli Shiga-like toxins induce apoptosis and cleavage of poly(ADP-Ribose) polymerase via in vitro activation of caspases. Infect. Immun. 70:2002;4669-4677.
97. Karpman D., Hakansson A., Perez M.T., Isaksson C., Carlemalm E., Caprioli A., Svanborg C. Apoptosis of renal cortical cells in the hemolytic-uremic syndrome: in vivo and in vitro studies. Infect. Immun. 66:1998;636-644.
98. Masri C., Proulx F., Toledano B., Clermont M.-J., Mariscalco M.M., Seidman E.G., Carillo J. Soluble Fas and soluble Fas-ligand in children with Escherichia coli O157:H7-associated hemolytic uremic syndrome. Am. J. Kidney Dis. 36:2000;687-694.
99. Esen M., Schreiner B., Jendrossek V., Lang F., Fassbender K., Grassmé H., Gulbins E. Mechanisms of Staphylococcus aureus induced apoptosis of human endothelial cells. Apoptosis. 6:2001;431-439.
100. Menzies B.E., Kourteva I. Internalization of Staphylococcus aureus by endothelial cells induces apoptosis. Infect. Immun. 66:1998;5994-5998.
101. Wesson C.A., Deringer J., Liou L.E., Bayles K.W., Bohach G.A., Trumble W.R. Apoptosis induced by Staphylococcus aureus in epithelial cells utilizes a mechanism involving caspases 8 and 3. Infect. Immun. 68:2000;2998-3001.
102. Nalbant A., Zadeh H.H. Actinobacillus actinomycetemcomitans induces apoptosis of T lymphocytes by the Fas and Fas ligand pathway. Oral Microbiol. Immunol. 17:2002;277-284.