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Review Article

Modulatory mechanisms of enterocyte apoptosis by viral, bacterial and parasitic pathogens

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Pages 1-17 | Received 18 Jul 2012, Accepted 02 Nov 2012, Published online: 09 Jan 2013

References

  • Abreu MT, Palladino AA, Arnold ET, et al. (2000). Modulation of barrier function during Fas-mediated apoptosis in human intestinal epithelial cells. Gastroenterology, 119, 1524–36
  • Abreu-Martin MT, Vidrich A, Lynch DH, et al. (1995). Divergent induction of apoptosis and IL-8 secretion in HT-29 cells in response to TNF-alpha and ligation of Fas antigen. J Immunol, 155, 4147–54
  • Abul-Milh M, Wu Y, Lau B, et al. (2001). Induction of epithelial cell death including apoptosis by enteropathogenic Escherichia coli expressing bundle-forming pili. Infect Immun, 69, 7356–64
  • Agarwal B, Halmos B, Feoktistov AS, et al. (2002). Mechanism of lovastatin-induced apoptosis in intestinal epithelial cells. Carcinogenesis, 23, 521–8
  • Amarapal P, Tantivanich S, Balachandra K, et al. (2005). The role of the Tat gene in the pathogenesis of HIV infection. Southeast Asian J Trop Med Public Health, 36, 352–61
  • Ashktorab H, Neapolitano M, Bomma C, et al. (2002). In vivo and in vitro activation of caspase-8 and -3 associated with Helicobacter pylori infection. Microbes Infect, 4, 713–22
  • Bagchi D, Bhattacharya G, Stohs SJ. (1996). Production of reactive oxygen species by gastric cells in association with Helicobacter pylori. Free Radic Res, 24, 439–50
  • Bannerman DD, Eiting KT, Winn RK, et al. (2004). FLICE-like inhibitory protein (FLIP) protects against apoptosis and suppresses NF-kappaB activation induced by bacterial lipopolysaccharide. Am J Pathol, 165, 1423–31
  • Becker SM, Cho KN, Guo X, et al. (2010). Epithelial cell apoptosis facilitates Entamoeba histolytica infection in the gut. Am J Pathol, 176, 1316–22
  • Bhattacharjee RN, Park KS, Uematsu S, et al. (2005). 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, 579, 6604–10
  • Blaser MJ, Atherton JC. (2004). Helicobacter pylori persistence: biology and disease. J Clin Invest, 113, 321–33
  • Blazquez S, Rigothier MC, Huerre M, et al. (2007). Initiation of inflammation and cell death during liver abscess formation by Entamoeba histolytica depends on activity of the galactose/N-acetyl-D-galactosamine lectin. Int J Parasitol, 37, 425–33
  • Boettner DR, Petri WA. (2005). Entamoeba histolytica activates host cell caspases during contact-dependent cell killing. Curr Top Microbiol Immunol, 289, 175–84
  • Bojarski C, Bendfeldt K, Gitter AH, et al. (2000). Apoptosis and intestinal barrier function. Ann NY Acad Sci, 915, 270–4
  • Boshuizen JA, Reimerink JH, Korteland-Van Male AM, et al. (2003). Changes in small intestinal homeostasis, morphology, and gene expression during rotavirus infection of infant mice. J Virol, 77, 13005–16
  • Brenes F, Ruiz B, Correa P, et al. (1993). Helicobacter pylori causes hyperproliferation of the gastric epithelium: pre- and post-eradication indices of proliferating cell nuclear antigen. Am J Gastroenterol, 88, 1870–5
  • Brito GA, Fujji J, Carneiro-Filho BA, et al. (2002). Mechanism of Clostridium difficile toxin A-induced apoptosis in T84 cells. J Infect Dis, 186, 1438–47
  • Buresi MC, Vergnolle N, Sharkey KA, et al. (2005). Activation of proteinase-activated receptor-1 inhibits neurally evoked chloride secretion in the mouse colon in vitro. Am J Physiol Gastrointest Liver Physiol, 288, G337–45
  • Buret AG. (2006). How stress induces intestinal hypersensitivity. Am J Pathol, 168, 3–5
  • Buti L, Spooner E, Van Der Veen AG, et al. (2011). Helicobacter pylori cytotoxin-associated gene A (CagA) subverts the apoptosis-stimulating protein of p53 (ASPP2) tumor suppressor pathway of the host. Proc Natl Acad Sci USA, 108, 9238–43
  • Buret AG, Chin AC, Scott KG. (2003). Infection of human and bovine epithelial cells with Cryptosporidium andersoni induces apoptosis and disrupts tight junctional ZO-1: effects of epidermal growth factor. Int J Parasitol, 33, 1363–71
  • Buret AG, Mitchell K, Muench DG, et al. (2002). Giardia lamblia disrupts tight junctional ZO-1 and increases permeability in non-transformed human small intestinal epithelial monolayers: effects of epidermal growth factor. Parasitology, 125, 11–19
  • Carneiro BA, Fujii J, Brito GA, et al. (2006). Caspase and bid involvement in Clostridium difficile toxin A-induced apoptosis and modulation of toxin A effects by glutamine and alanyl-glutamine in vivo and in vitro. Infect Immun, 74, 81–7
  • Ceponis PJ, Riff JD, Sherman PM. (2005). Epithelial cell signaling responses to enterohemorrhagic Escherichia coli infection. Mem Inst Oswaldo Cruz, 100, 199–203
  • Chae S, Eckmann L, Miyamoto Y, et al. (2006). Epithelial cell I kappa B-kinase beta has an important protective role in Clostridium difficile toxin A-induced mucosal injury. J Immunol, 177, 1214–20
  • Chaibi C, Cotte-Laffitte J, Sandre C, et al. (2005). Rotavirus induces apoptosis in fully differentiated human intestinal Caco-2 cells. Virology, 332, 480–90
  • Chandran K, Parker JS, Ehrlich M, et al. (2003). The delta region of outer-capsid protein micro 1 undergoes conformational change and release from reovirus particles during cell entry. J Virol, 77, 13361–75
  • Chen G, Sordillo EM, Ramey WG, et al. (1997). Apoptosis in gastric epithelial cells is induced by Helicobacter pylori and accompanied by increased expression of BAK. Biochem Biophys Res Commun, 239, 626–32
  • Chen XM, Gores GJ, Paya CV, et al. (1999). Cryptosporidium parvum induces apoptosis in biliary epithelia by a Fas/Fas ligand-dependent mechanism. Am J Physiol, 277, G599–608
  • Chen XM, Levine SA, Splinter PL, et al. (2001). Cryptosporidium parvum activates nuclear factor kappaB in biliary epithelia preventing epithelial cell apoptosis. Gastroenterology, 120, 1774–83
  • Cherla RP, Lee SY, Tesh VL. (2003). Shiga toxins and apoptosis. FEMS Microbiol Lett, 228, 159–66
  • Chin AC, Flynn AN, Fedwick JP, et al. (2006). The role of caspase-3 in lipopolysaccharide-mediated disruption of intestinal epithelial tight junctions. Can J Physiol Pharmacol, 84, 1043–50
  • Chin AC, Teoh DA, Scott KG, et al. (2002). Strain-dependent induction of enterocyte apoptosis by Giardia lamblia disrupts epithelial barrier function in a caspase-3-dependent manner. Infect Immun, 70, 3673–80
  • Chin AC, Vergnolle N, Macnaughton WK, et al. (2003). Proteinase-activated receptor 1 activation induces epithelial apoptosis and increases intestinal permeability. Proc Natl Acad Sci USA, 100, 11104–9
  • Ching JC, Jones NL, Ceponis PJ, et al. (2002). Escherichia coli Shiga-like toxins induce apoptosis and cleavage of poly(ADP-ribose) polymerase via in vitro activation of caspases. Infect Immun, 70, 4669–77
  • Cho SJ, Kang NS, Park SY, et al. (2003). Induction of apoptosis and expression of apoptosis related genes in human epithelial carcinoma cells by Helicobacter pylori VacA toxin. Toxicon, 42, 601–11
  • Ciccocioppo R, Di Sabatino A, Luinetti O, et al. (2002). Small bowel enterocyte apoptosis and proliferation are increased in the elderly. Gerontology, 48, 204–8
  • Clark CS, Maurelli AT. (2007). Shigella flexneri inhibits staurosporine-induced apoptosis in epithelial cells. Infect Immun, 75, 2531–9
  • Clarke SC, Haigh RD, Freestone PP, et al. (2003). Virulence of enteropathogenic Escherichia coli, a global pathogen. Clin Microbiol Rev, 16, 365–78
  • Clavel T, Haller D. (2007). Molecular interactions between bacteria, the epithelium, and the mucosal immune system in the intestinal tract: implications for chronic inflammation. Curr Issues Intest Microbiol, 8, 25–43
  • Clayton F, Reka S, Cronin WJ, et al. (1992). Rectal mucosal pathology varies with human immunodeficiency virus antigen content and disease stage. Gastroenterology, 103, 919–33
  • Cliffe LJ, Humphreys NE, Lane TE, et al. (2005). Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science, 308, 1463–5
  • Cliffe LJ, Potten CS, Booth CE, et al. (2007). An increase in epithelial cell apoptosis is associated with chronic intestinal nematode infection. Infect Immun, 75, 1556–64
  • Clyne CA, Eliopoulos GM. (1989). Fever and urticaria in acute giardiasis. Arch Intern Med, 149, 939–40
  • Collier-Hyams LS, Zeng H, Sun J, et al. (2002). Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J Immunol, 169, 2846–50
  • Cotton JA, Beatty JK, Buret AG. (2011). Host parasite interactions and pathophysiology in Giardia infections. Int J Parasitol, 41, 925–33
  • Crane JK, Majumdar S, Pickhardt DF 3rd. (1999). Host cell death due to enteropathogenic Escherichia coli has features of apoptosis. Infect Immun, 67, 2575–84
  • Crane JK, McNamara BP, Donnenberg MS. (2001). Role of EspF in host cell death induced by enteropathogenic Escherichia coli. Cell Microbiol, 3, 197–211
  • Crane JK, Oh JS. (1997). Activation of host cell protein kinase C by enteropathogenic Escherichia coli. Infect Immun, 65, 3277–85
  • D'Anchino M, Orlando D, De Feudis L. (2002). Giardia lamblia infections become clinically evident by eliciting symptoms of irritable bowel syndrome. J Infect, 45, 169–72
  • Dery O, Corvera CU, Steinhoff M, et al. (1998). Proteinase-activated receptors: novel mechanisms of signaling by serine proteases. Am J Physiol, 274, C1429–52
  • Devinney R, Stein M, Reinscheid D, et al. (1999). Enterohemorrhagic Escherichia coli O157:H7 produces Tir, which is translocated to the host cell membrane but is not tyrosine phosphorylated. Infect Immun, 67, 2389–98
  • Di Prisco MC, Hagel I, Lynch NR, et al. (1993). Possible relationship between allergic disease and infection by Giardia lamblia. Ann Allergy, 70, 210–3
  • Ding SZ, Minohara Y, Fan XJ, et al. (2007). Helicobacter pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells. Infect Immun, 75, 4030–9
  • Donnenberg MS, Whittam TS. (2001). Pathogenesis and evolution of virulence in enteropathogenic and enterohemorrhagic Escherichia coli. J Clin Invest, 107, 539–48
  • Eaves-Pyles T, Murthy K, Liaudet L, et al. (2001). Flagellin, a novel mediator of Salmonella-induced epithelial activation and systemic inflammation: I kappa B alpha degradation, induction of nitric oxide synthase, induction of proinflammatory mediators, and cardiovascular dysfunction. J Immunol, 166, 1248–60
  • Eckmann L, Laurent F, Langford TD, et al. (2000). Nitric oxide production by human intestinal epithelial cells and competition for arginine as potential determinants of host defense against the lumen-dwelling pathogen Giardia lamblia. J Immunol, 164, 1478–87
  • Eleouet JF, Slee EA, Saurini F, et al. (2000). The viral nucleocapsid protein of transmissible gastroenteritis coronavirus (TGEV) is cleaved by caspase-6 and -7 during TGEV-induced apoptosis. J Virol, 74, 3975–83
  • Elliott SJ, O'connell CB, Koutsouris A, et al. (2002). A gene from the locus of enterocyte effacement that is required for enteropathogenic Escherichia coli to increase tight-junction permeability encodes a chaperone for EspF. Infect Immun, 70, 2271–7
  • Ernst PB, Gold BD. (2000). The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu Rev Microbiol, 54, 615–40
  • Faherty CS, Maurelli AT. (2009). Spa15 of Shigella flexneri is secreted through the type III secretion system and prevents staurosporine-induced apoptosis. Infect Immun, 77, 5281–90
  • Fan X, Crowe SE, Behar S, et al. (1998). The effect of class II major histocompatibility complex expression on adherence of Helicobacter pylori and induction of apoptosis in gastric epithelial cells: a mechanism for T helper cell type 1-mediated damage. J Exp Med, 187, 1659–69
  • Finlay BB, Cossart P. (1997). Exploitation of mammalian host cell functions by bacterial pathogens. Science, 276, 718–25
  • Fiorentini C, Fabbri A, Falzano L, et al. (1998). Clostridium difficile toxin B induces apoptosis in intestinal cultured cells. Infect Immun, 66, 2660–5
  • Flynn AN, Wang A, McKay DM, et al. (2011). Apoptosis-inducing factor contributes to epithelial cell apoptosis induced by enteropathogenic Escherichia coli. Can J Physiol Pharmacol, 89, 143–8
  • Forney JR, Yang S, Healey MC. (1996). Protease activity associated with excystation of Cryptosporidium parvum oocysts. J Parasitol, 82, 889–92
  • Fujii J, Matsui T, Heatherly DP, et al. (2003). Rapid apoptosis induced by Shiga toxin in HeLa cells. Infect Immun, 71, 2724–35
  • Fullner KJ, Mekalanos JJ. (2000). In vivo covalent cross-linking of cellular actin by the Vibrio cholerae RTX toxin. EMBO J, 19, 5315–23
  • Garcia Rodriguez LA, Ruigomez A, Panes J. (2006). Acute gastroenteritis is followed by an increased risk of inflammatory bowel disease. Gastroenterology, 130, 1588–94
  • Gerhard R, Nottrott S, Schoentaube J, et al. (2008). Glucosylation of Rho GTPases by Clostridium difficile toxin A triggers apoptosis in intestinal epithelial cells. J Med Microbiol, 57, 765–70
  • Gewirtz AT, Simon PO Jr., Schmitt CK, et al. (2001). Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J Clin Invest, 107, 99–109
  • Gewirtz AT, Yu Y, Krishna US, et al. (2004). Helicobacter pylori flagellin evades toll-like receptor 5-mediated innate immunity. J Infect Dis, 189, 1914–20
  • Gitter AH, Bendfeldt K, Schulzke JD, et al. (2000). Leaks in the epithelial barrier caused by spontaneous and TNF-alpha-induced single-cell apoptosis. FASEB J, 14, 1749–53
  • Guttman JA, Samji FN, Li Y, et al. (2006). Evidence that tight junctions are disrupted due to intimate bacterial contact and not inflammation during attaching and effacing pathogen infection in vivo. Infect Immun, 74, 6075–84
  • Hansen KK, Sherman PM, Cellars L, et al. (2005). A major role for proteolytic activity and proteinase-activated receptor-2 in the pathogenesis of infectious colitis. Proc Natl Acad Sci USA, 102, 8363–8
  • Hardin JA, Buret AG, Olson ME, et al. (1997). Mast cell hyperplasia and increased macromolecular uptake in an animal model of giardiasis. J Parasitol, 83, 908–12
  • He D, Sougioultzis S, Hagen S, et al. (2002). Clostridium difficile toxin A triggers human colonocyte IL-8 release via mitochondrial oxygen radical generation. Gastroenterology, 122, 1048–57
  • Heczko U, Carthy CM, O'brien BA, et al. (2001). Decreased apoptosis in the ileum and ileal Peyer's patches: a feature after infection with rabbit enteropathogenic Escherichia coli O103. Infect Immun, 69, 4580–9
  • Henning SW, Galandrini R, Hall A, et al. (1997). The GTPase Rho has a critical regulatory role in thymus development. EMBO J, 16, 2397–407
  • Hirota SA, Fines K, Ng J, et al. (2010). Hypoxia-inducible factor signaling provides protection in Clostridium difficile-induced intestinal injury. Gastroenterology, 139, 259–69 e3
  • Huston CD, Boettner DR, Miller-Sims V, et al. (2003). Apoptotic killing and phagocytosis of host cells by the parasite Entamoeba histolytica. Infect Immun, 71, 964–72
  • Huston CD, Houpt ER, Mann BJ, et al. (2000). Caspase 3-dependent killing of host cells by the parasite Entamoeba histolytica. Cell Microbiol, 2, 617–25
  • Islam D, Veress B, Bardhan PK, et al. (1997). In situ characterization of inflammatory responses in the rectal mucosae of patients with shigellosis. Infect Immun, 65, 739–49
  • Ivana Scovassi A, Diederich M. (2004). Modulation of poly(ADP-ribosylation) in apoptotic cells. Biochem Pharmacol, 68, 1041–7
  • Jacobs T, Bruchhaus I, Dandekar T, et al. (1998). Isolation and molecular characterization of a surface-bound proteinase of Entamoeba histolytica. Mol Microbiol, 27, 269–76
  • Jain P, Luo ZQ, Blanke SR. (2011). Helicobacter pylori vacuolating cytotoxin A (VacA) engages the mitochondrial fission machinery to induce host cell death. Proc Natl Acad Sci USA, 108, 16032–7
  • Janssen YM, Van Houten B, Borm PJ, et al. (1993). Cell and tissue responses to oxidative damage. Lab Invest, 69, 261–74
  • Johanesen PA, Dwinell MB. (2006). Flagellin-independent regulation of chemokine host defense in Campylobacter jejuni-infected intestinal epithelium. Infect Immun, 74, 3437–47
  • Jones BA, Gores GJ. (1997). Physiology and pathophysiology of apoptosis in epithelial cells of the liver, pancreas, and intestine. Am J Physiol, 273, G1174–88
  • Jones NL, Day AS, Jennings HA, et al. (1999). Helicobacter pylori induces gastric epithelial cell apoptosis in association with increased Fas receptor expression. Infect Immun, 67, 4237–42
  • Jones NL, Islur A, Haq R, et al. (2000). Escherichia coli Shiga toxins induce apoptosis in epithelial cells that is regulated by the Bcl-2 family. Am J Physiol Gastrointest Liver Physiol, 278, G811–9
  • Jones NL, Shannon PT, Cutz E, et al. (1997). Increase in proliferation and apoptosis of gastric epithelial cells early in the natural history of Helicobacter pylori infection. Am J Pathol, 151, 1695–703
  • Just I, Selzer J, Wilm M, et al. (1995). Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature, 375, 500–3
  • Kalischuk LD, Buret AG. (2010). A role for Campylobacter jejuni-induced enteritis in inflammatory bowel disease?. Am J Physiol Gastrointest Liver Physiol, 298, G1–9
  • Kammanadiminti SJ, Chadee K. (2006). Suppression of NF-kappaB activation by Entamoeba histolytica in intestinal epithelial cells is mediated by heat shock protein 27. J Biol Chem, 281, 26112–20
  • Kaper JB, Morris JG, Jr., Levine MM. (1995). Cholera. Clin Microbiol Rev, 8, 48–86
  • Kaufman SS, Chatterjee NK, et al. (2005). Characteristics of human calicivirus enteritis in intestinal transplant recipients. J Pediatr Gastroenterol Nutr, 40, 328–33
  • Keel MK, Songer JG. (2006). The comparative pathology of Clostridium difficile-associated disease. Vet Pathol, 43, 225–40
  • Kenny B. (2002). Enteropathogenic Escherichia coli (EPEC) – a crafty subversive little bug. Microbiology, 148, 1967–78
  • Kenny B, Jepson M. (2000). Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell Microbiol, 2, 579–90
  • Kim JM, Eckmann L, Savidge TC, et al. (1998). Apoptosis of human intestinal epithelial cells after bacterial invasion. J Clin Invest, 102, 1815–23
  • Knodler LA, Finlay BB, Steele-Mortimer O. (2005). The Salmonella effector protein sopB protects epithelial cells from apoptosis by sustained activation of Akt. J Biol Chem, 280, 9058–64
  • Kominsky DJ, Bickel RJ, Tyler KL. (2002). Reovirus-induced apoptosis requires mitochondrial release of Smac/DIABLO and involves reduction of cellular inhibitor of apoptosis protein levels. J Virol, 76, 11414–24
  • Kurita A, Gotoh H, Eguchi M, et al. (2003). Intracellular expression of the Salmonella plasmid virulence protein, SpvB, causes apoptotic cell death in eukaryotic cells. Microb Pathog, 35, 43–8
  • Kusumoto K, Kawahara T, Kuwano Y, et al. (2005). Ecabet sodium inhibits Helicobacter pylori lipopolysaccharide-induced activation of NADPH oxidase 1 or apoptosis of guinea pig gastric mucosal cells. Am J Physiol Gastrointest Liver Physiol, 288, G300–7
  • Kyne L, Hamel MB, Polavaram R, et al. (2002). Health care costs and mortality associated with nosocomial diarrhea due to Clostridium difficile. Clin Infect Dis, 34, 346–53
  • Laukoetter MG, Bruewer M, Nusrat A. (2006). Regulation of the intestinal epithelial barrier by the apical junctional complex. Curr Opin Gastroenterol, 22, 85–9
  • Ledig S, Wagner S, Manns MP, et al. (2004). Role of the receptor-mediated apoptosis in Helicobacter pylori in gastric epithelial cells. Digestion, 70, 178–86
  • Leroy A, Lauwaet T, De Bruyne G, et al. (2000). Entamoeba histolytica disturbs the tight junction complex in human enteric T84 cell layers. FASEB J, 14, 1139–46
  • Lica M, Schulz F, Schelle I, et al. (2011). Difference in the biological effects of Clostridium difficile toxin B in proliferating and non-proliferating cells. Naunyn Schmiedebergs Arch Pharmacol, 383, 275–83
  • Limaye AP, Turgeon DK, Cookson BT, et al. (2000). Pseudomembranous colitis caused by a toxin A(−) B(+) strain of Clostridium difficile. J Clin Microbiol, 38, 1696–7
  • Lin W, Fullner KJ, Clayton R, et al. (1999). Identification of a vibrio cholerae RTX toxin gene cluster that is tightly linked to the cholera toxin prophage. Proc Natl Acad Sci USA, 96, 1071–6
  • Liu J, Akahoshi T, Sasahana T, et al. (1999). Inhibition of neutrophil apoptosis by verotoxin 2 derived from Escherichia coli O157:H7. Infect Immun, 67, 6203–5
  • Liu J, Enomoto S, Lancto CA, et al. (2008). Inhibition of apoptosis in Cryptosporidium parvum-infected intestinal epithelial cells is dependent on survivin. Infect Immun, 76, 3784–92
  • Liu X, Lu R, Xia Y, et al. (2010). Eukaryotic signaling pathways targeted by Salmonella effector protein AvrA in intestinal infection in vivo. BMC Microbiol, 10, 326
  • Lourbakos A, Chinni C, Thompson P, et al. (1998). Cleavage and activation of proteinase-activated receptor-2 on human neutrophils by gingipain-R from Porphyromonas gingivalis. FEBS Lett, 435, 45–8
  • Lourbakos A, Potempa J, Travis J, et al. (2001). Arginine-specific protease from Porphyromonas gingivalis activates protease-activated receptors on human oral epithelial cells and induces interleukin-6 secretion. Infect Immun, 69, 5121–30
  • Macfarlane SR, Seatter MJ, Kanke T, et al. (2001). Proteinase-activated receptors. Pharmacol Rev, 53, 245–82
  • Madara JL. (1990). Maintenance of the macromolecular barrier at cell extrusion sites in intestinal epithelium: physiological rearrangement of tight junctions. J Membr Biol, 116, 177–84
  • Maeda S, Yoshida H, Mitsuno Y, et al. (2002). Analysis of apoptotic and antiapoptotic signalling pathways induced by Helicobacter pylori. Mol Pathol, 55, 286–93
  • Mahida YR, Makh S, Hyde S, et al. (1996). Effect of Clostridium difficile toxin A on human intestinal epithelial cells: induction of interleukin 8 production and apoptosis after cell detachment. Gut, 38, 337–47
  • Mangan DF, Welch GR, Wahl SM. (1991). Lipopolysaccharide, tumor necrosis factor-alpha, and IL-1 beta prevent programmed cell death (apoptosis) in human peripheral blood monocytes. J Immunol, 146, 1541–6
  • Mannick EE, Bravo LE, Zarama G, et al. (1996). Inducible nitric oxide synthase, nitrotyrosine, and apoptosis in Helicobacter pylori gastritis: effect of antibiotics and antioxidants. Cancer Res, 56, 3238–43
  • Mantis N, Prevost MC, Sansonetti P. (1996). Analysis of epithelial cell stress response during infection by Shigella flexneri. Infect Immun, 64, 2474–82
  • Marshall JK, Thabane M, Garg AX, et al. (2006). Incidence and epidemiology of irritable bowel syndrome after a large waterborne outbreak of bacterial dysentery. Gastroenterology, 131, 445–50; quiz 660
  • Martin-Latil S, Mousson L, Autret A, et al. (2007). Bax is activated during rotavirus-induced apoptosis through the mitochondrial pathway. J Virol, 81, 4457–64
  • Matarrese P, Falzano L, Fabbri A, et al. (2007). Clostridium difficile toxin B causes apoptosis in epithelial cells by thrilling mitochondria. Involvement of ATP-sensitive mitochondrial potassium channels. J Biol Chem, 282, 9029–41
  • Matte I, Lane D, Cote E, et al. (2009). Antiapoptotic proteins Bcl-2 and Bcl-XL inhibit Clostridium difficile toxin A-induced cell death in human epithelial cells. Infect Immun, 77, 5400–10
  • McCole DF, Eckmann L, Laurent F, et al. (2000). Intestinal epithelial cell apoptosis following Cryptosporidium parvum infection. Infect Immun, 68, 1710–3
  • McCormick BA. (2003). Salmonella spp.: masters of inflammation. Washington DC, USA: ASM Press
  • McDermott PF, Ciacci-Woolwine F, Snipes JA, et al. (2000). High-affinity interaction between gram-negative flagellin and a cell surface polypeptide results in human monocyte activation. Infect Immun, 68, 5525–9
  • Mele R, Gomez Morales MA, Tosini F, et al. (2004). Cryptosporidium parvum at different developmental stages modulates host cell apoptosis in vitro. Infect Immun, 72, 6061–7
  • Mellies JL, Barron AM, Carmona AM. (2007). Enteropathogenic and enterohemorrhagic Escherichia coli virulence gene regulation. Infect Immun, 75, 4199–210
  • Moriez R, Salvador-Cartier C, Theodorou V, et al. (2005). Myosin light chain kinase is involved in lipopolysaccharide-induced disruption of colonic epithelial barrier and bacterial translocation in rats. Am J Pathol, 167, 1071–9
  • Moss SF, Calam J, Agarwal B, et al. (1996). Induction of gastric epithelial apoptosis by Helicobacter pylori. Gut, 38, 498–501
  • Mukherjee G, Biswas A, Banerjee KK, et al. (2008). Vibrio cholerae hemolysin is apoptogenic to peritoneal B-1a cells but its oligomer shepherd the cells for IgA response. Mol Immunol, 45, 266–70
  • Nagai T, Abe A, Sasakawa C. (2005). Targeting of enteropathogenic Escherichia coli EspF to host mitochondria is essential for bacterial pathogenesis: critical role of the 16th leucine residue in EspF. J Biol Chem, 280, 2998–3011
  • Nagata K, Yu H, Nishikawa M, et al. (1998). Helicobacter pylori generates superoxide radicals and modulates nitric oxide metabolism. J Biol Chem, 273, 14071–3
  • Nasirudeen AM. (2005). Cell death and human intestinal protozoa: a brief overview. Curr Issues Intest Microbiol, 6, 77–82
  • Nataro JP, Kaper JB. (1998). Diarrheagenic Escherichia coli. Clin Microbiol Rev, 11, 142–201
  • Ogura K, Yahiro K, Tsutsuki H, et al. (2011). Characterization of Cholix toxin-induced apoptosis in HeLa cells. J Biol Chem, 286, 37207–15
  • O'hara SP, Small AJ, Nelson JB, et al. (2007). The human immunodeficiency virus type 1 tat protein enhances Cryptosporidium parvum-induced apoptosis in cholangiocytes via a Fas ligand-dependent mechanism. Infect Immun, 75, 684–96
  • Ojcius DM, Perfettini JL, Bonnin A, et al. (1999). Caspase-dependent apoptosis during infection with Cryptosporidium parvum. Microbes Infect, 1, 1163–8
  • O'Loughlin EV, Robins-Browne RM. (2001). Effect of Shiga toxin and Shiga-like toxins on eukaryotic cells. Microbes Infect, 3, 493–507
  • Olson MF, Ashworth A, Hall A. (1995). An essential role for Rho, Rac, and Cdc42 GTPases in cell cycle progression through G1. Science, 269, 1270–2
  • Paesold G, Guiney DG, Eckmann L, et al. (2002). Genes in the Salmonella pathogenicity island 2 and the Salmonella virulence plasmid are essential for Salmonella-induced apoptosis in intestinal epithelial cells. Cell Microbiol, 4, 771–81
  • Panaro MA, Cianciulli A, Mitolo V, et al. (2007). Caspase-dependent apoptosis of the HCT-8 epithelial cell line induced by the parasite Giardia intestinalis. FEMS Immunol Med Microbiol, 51, 302–9
  • Panesar NS. (2003). Lymphopenia in SARS. Lancet, 361, 1985
  • Parashar UD, Gibson CJ, Bresee JS, et al. (2006). Rotavirus and severe childhood diarrhea. Emerg Infect Dis, 12, 304–6
  • Peek RM, Jr., Moss SF, Tham KT, et al. (1997). Helicobacter pylori cagA+ strains and dissociation of gastric epithelial cell proliferation from apoptosis. J Natl Cancer Inst, 89, 863–8
  • Potoka DA, Upperman JS, Zhang XR, et al. (2003). Peroxynitrite inhibits enterocyte proliferation and modulates Src kinase activity in vitro. Am J Physiol Gastrointest Liver Physiol, 285, G861–9
  • Potten CS. (1998). Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos Trans R Soc Lond B Biol Sci, 353, 821–30
  • Qi W, Ebbert KV, Craig AW, et al. (2005). Absence of Fer protein tyrosine kinase exacerbates endotoxin induced intestinal epithelial barrier dysfunction in vivo. Gut, 54, 1091–7
  • Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, et al. (2004). Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell, 118, 229–41
  • Raupach B, Zychlinsky, A. (2003). Apoptosis and enteric bacterial infections. Washington DC, USA: ASM Press
  • Ravdin JI, Guerrant RL. (1981). Role of adherence in cytopathogenic mechanisms of Entamoeba histolytica. Study with mammalian tissue culture cells and human erythrocytes. J Clin Invest, 68, 1305–13
  • Reijasse D, Patey-Mariaud De Serre N, Canioni D, et al. (2001). Cytotoxic T cells in AIDS colonic cryptosporidiosis. J Clin Pathol, 54, 298–303
  • Rosenshine I, Donnenberg MS, Kaper JB, et al. (1992). Signal transduction between enteropathogenic Escherichia coli (EPEC) and epithelial cells: EPEC induces tyrosine phosphorylation of host cell proteins to initiate cytoskeletal rearrangement and bacterial uptake. EMBO J, 11, 3551–60
  • Rosenthal PJ. (1999). Proteases of protozoan parasites. Adv Parasitol, 43, 105–59
  • Roxstrom-Lindquist K, Ringqvist E, Palm D, et al. (2005). Giardia lamblia-induced changes in gene expression in differentiated Caco-2 human intestinal epithelial cells. Infect Immun, 73, 8204–8
  • Rudi J, Kuck D, Strand S, et al. (1998). Involvement of the CD95 (APO-1/Fas) receptor and ligand system in Helicobacter pylori-induced gastric epithelial apoptosis. J Clin Invest, 102, 1506–14
  • Saka HA, Bidinost C, Sola C, et al. (2008). Vibrio cholerae cytolysin is essential for high enterotoxicity and apoptosis induction produced by a cholera toxin gene-negative V. cholerae non-O1, non-O139 strain. Microb Pathog, 44, 118–28
  • Samba-Louaka A, Nougayrede JP, Watrin C, et al. (2009). The enteropathogenic Escherichia coli effector Cif induces delayed apoptosis in epithelial cells. Infect Immun, 77, 5471–7
  • Sandoval M, Liu X, Oliver PD, et al. (1995). Nitric oxide induces apoptosis in a human colonic epithelial cell line, T84. Mediators Inflamm, 4, 248–50
  • Sansonetti PJ. (2004). War and peace at mucosal surfaces. Nat Rev Immunol, 4, 953–64
  • Santos RL, Tsolis RM, Zhang S, et al. (2001). Salmonella-induced cell death is not required for enteritis in calves. Infect Immun, 69, 4610–7
  • Sasahara T, Maruyama H, Aoki M, et al. (2003). Apoptosis of intestinal crypt epithelium after Cryptosporidium parvum infection. J Infect Chemother, 9, 278–81
  • Savioli L, Smith H, Thompson A. (2006). Giardia and Cryptosporidium join the ‘Neglected Diseases Initiative’. Trends Parasitol, 22, 203–8
  • Schauser K, Olsen JE, Larsson LI. (2005). Salmonella typhimurium infection in the porcine intestine: evidence for caspase-3-dependent and -independent programmed cell death. Histochem Cell Biol, 123, 43–50
  • Scott KG, Meddings JB, Kirk DR, et al. (2002). Intestinal infection with Giardia spp. reduces epithelial barrier function in a myosin light chain kinase-dependent fashion. Gastroenterology, 123, 1179–90
  • Seydel KB, Li E, Zhang Z, et al. (1998). Epithelial cell-initiated inflammation plays a crucial role in early tissue damage in amebic infection of human intestine. Gastroenterology, 115, 1446–53
  • Seydel KB, Stanley SL, Jr. (1998). Entamoeba histolytica induces host cell death in amebic liver abscess by a non-Fas-dependent, non-tumor necrosis factor alpha-dependent pathway of apoptosis. Infect Immun, 66, 2980–3
  • Shen L, Black ED, Witkowski ED, et al. (2006). Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J Cell Sci, 119, 2095–106
  • Shibayama K, Doi Y, Shibata N, et al. (2001). Apoptotic signaling pathway activated by Helicobacter pylori infection and increase of apoptosis-inducing activity under serum-starved conditions. Infect Immun, 69, 3181–9
  • Shirin H, Moss SF. (1998). Helicobacter pylori induced apoptosis. Gut, 43, 592–4
  • Sim S, Kim KA, Yong TS, et al. (2004). Ultrastructural observation of human neutrophils during apoptotic cell death triggered by Entamoeba histolytica. Korean J Parasitol, 42, 205–8
  • Sirinarumitr T, Kluge JP, Paul PS. (1998). Transmissible gastroenteritis virus induced apoptosis in swine testes cell cultures. Arch Virol, 143, 2471–85
  • Stecher B, Hapfelmeier S, Muller C, et al. (2004). Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun, 72, 4138–50
  • Steiner TS. (2007). How flagellin and toll-like receptor 5 contribute to enteric infection. Infect Immun, 75, 545–52
  • Steiner TS, Nataro JP, Poteet-Smith CE, et al. (2000). Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells. J Clin Invest, 105, 1769–77
  • Stoicov C, Cai X, Li H, et al. (2005). Major histocompatibility complex class II inhibits fas antigen-mediated gastric mucosal cell apoptosis through actin-dependent inhibition of receptor aggregation. Infect Immun, 73, 6311–21
  • Strober W. (2004). Epithelial cells pay a Toll for protection. Nat Med, 10, 898–900
  • Sun Z, Wang X, Wallen R, et al. (1998). The influence of apoptosis on intestinal barrier integrity in rats. Scand J Gastroenterol, 33, 415–22
  • Superti F, Ammendolia MG, Tinari A, et al. (1996). Induction of apoptosis in HT-29 cells infected with SA-11 rotavirus. J Med Virol, 50, 325–34
  • Teoh DA, Kamieniecki D, Pang G, et al. (2000). Giardia lamblia rearranges F-actin and alpha-actinin in human colonic and duodenal monolayers and reduces transepithelial electrical resistance. J Parasitol, 86, 800–6
  • Thornley JP, Jenkins D, Neal K, et al. (2001). Relationship of Campylobacter toxigenicity in vitro to the development of postinfectious irritable bowel syndrome. J Infect Dis, 184, 606–9
  • Tonna I, Welsby PD. (2005). Pathogenesis and treatment of Clostridium difficile infection. Postgrad Med J, 81, 367–9
  • Troeger H, Epple HJ, Schneider T, et al. (2007). Effect of chronic Giardia lamblia infection on epithelial transport and barrier function in human duodenum. Gut, 56, 328–35
  • Troeger H, Loddenkemper C, Schneider T, et al. (2009). Structural and functional changes of the duodenum in human norovirus infection. Gut, 58, 1070–7
  • Vijay-Kumar M, Wu H, Jones R, et al. (2006). Flagellin suppresses epithelial apoptosis and limits disease during enteric infection. Am J Pathol, 169, 1686–700
  • Voth DE, Ballard JD. (2005). Clostridium difficile toxins: mechanism of action and role in disease. Clin Microbiol Rev, 18, 247–63
  • Vu TK, Hung DT, Wheaton VI, et al. (1991). Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell, 64, 1057–68
  • Wagner S, Beil W, Westermann J, et al. (1997). Regulation of gastric epithelial cell growth by Helicobacter pylori: offdence for a major role of apoptosis. Gastroenterology, 113, 1836–47
  • Watanabe S, Takagi A, Koga Y, et al. (2000). Helicobacter pylori induces apoptosis in gastric epithelial cells through inducible nitric oxide. J Gastroenterol Hepatol, 15, 168–74
  • Weber P, Koch M, Heizmann WR, et al. (1992). Microbic superinfection in relapse of inflammatory bowel disease. J Clin Gastroenterol, 14, 302–8
  • Wei J, O'brien D, Vilgelm A, et al. (2008). Interaction of Helicobacter pylori with gastric epithelial cells is mediated by the p53 protein family. Gastroenterology, 134, 1412–23
  • Wensaas KA, Langeland N, Hanevik K, et al. (2012). Irritable bowel syndrome and chronic fatigue 3 years after acute giardiasis: historic cohort study. Gut, 61, 214–19
  • Widmer G, Corey EA, Stein B, et al. (2000). Host cell apoptosis impairs Cryptosporidium parvum development in vitro. J Parasitol, 86, 922–8
  • Williams AG, Coombs GH. (1995). Multiple protease activities in Giardia intestinalis trophozoites. Int J Parasitol, 25, 771–8
  • Wu H, Jones RM, Neish AS. (2012). The Salmonella effector AvrA mediates bacterial intracellular survival during infection in vivo. Cell Microbiol, 14, 28–39
  • Xia HH, Talley NJ. (2001). Apoptosis in gastric epithelium induced by Helicobacter pylori infection: implications in gastric carcinogenesis. Am J Gastroenterol, 96, 16–26
  • Yan L, Stanley SL, Jr. (2001). Blockade of caspases inhibits amebic liver abscess formation in a mouse model of disease. Infect Immun, 69, 7911–14
  • Yoshida T, Fukada M, Koide N, et al. (1999). Primary cultures of human endothelial cells are susceptible to low doses of Shiga toxins and undergo apoptosis. J Infect Dis, 180, 2048–52
  • Yu LC, Flynn AN, Turner JR, et al. (2005). SGLT-1-mediated glucose uptake protects intestinal epithelial cells against LPS-induced apoptosis and barrier defects: a novel cellular rescue mechanism?. FASEB J, 19, 1822–35
  • Yu LC, Huang CY, Kuo WT, et al. (2008). SGLT-1-mediated glucose uptake protects human intestinal epithelial cells against Giardia duodenalis-induced apoptosis. Int J Parasitol, 38, 923–34
  • Yu LC, Turner JR, Buret AG. (2006). LPS/CD14 activation triggers SGLT-1-mediated glucose uptake and cell rescue in intestinal epithelial cells via early apoptotic signals upstream of caspase-3. Exp Cell Res, 312, 3276–86
  • Yuan JP, Li T, Chen HB, et al. (2004). Analysis of gene expression profile in gastric cancer cells stimulated with Helicobacter pylori isogenic strains. J Med Microbiol, 53, 965–74
  • Zimmermann KC, Green DR. (2001). How cells die: apoptosis pathways. J Allergy Clin Immunol, 108, S99–103
  • Zychlinsky A, Prevost MC, Sansonetti PJ. (1992). Shigella flexneri induces apoptosis in infected macrophages. Nature, 358, 167–9
  • Zychlinsky A, Sansonetti P. (1997). Perspectives series: host/pathogen interactions. Apoptosis in bacterial pathogenesis. J Clin Invest, 100, 493–5
  • Zychlinsky A, Thirumalai K, Arondel J, et al. (1996). In vivo apoptosis in Shigella flexneri infections. Infect Immun, 64, 5357–65

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