Regulation of apoptosis during homeostasis and disease in the intestinal epithelium

Inflammatory Bowel Diseases

Volumn 12, Issue 5, 2006, Pages 413-424

  Edelblum, Karen L ^a   Yan, Fang ^a   Yamaoka, Toshimitsu ^a   Polk, D Brent ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; K RAS PROTEIN; PROSTAGLANDIN RECEPTOR; PROTEIN BCL 2; PROTEIN P53;

APOPTOSIS; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; COLON CANCER; DISEASE PREDISPOSITION; DNA DAMAGE; ENTERITIS; HOMEOSTASIS; HUMAN; INFLAMMATION ASSOCIATED NEOPLASIA; INTESTINE EPITHELIUM CELL; NEOPLASM; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; STOMACH CANCER;

APOPTOSIS; EPITHELIAL CELLS; HOMEOSTASIS; HUMANS; INTESTINAL DISEASES; INTESTINAL MUCOSA;

EID: 33646801637     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/01.MIB.0000217334.30689.3e     Document Type: Review

References (163)

1. Hall PA, Coates PJ, Ansari B, et al. Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J Cell Sci. 1994;107(pt 12):3569-3577.
2. Schreiber AM, Cai L, Brown DD. Remodeling of the intestine during metamorphosis of Xenopus laevis. Proc Natl Acad Sci USA. 2005;102:3720-3725.
3. Mandir N, FitzGerald AJ, Goodlad RA. Differences in the effects of age on intestinal proliferation, crypt fission and apoptosis on the small intestine and the colon of the rat. Int J Exp Pathol. 2005;86:125-130.
4. Xiao ZQ, Moragoda L, Jaszewski R, et al. Aging is associated with increased proliferation and decreased apoptosis in the colonic mucosa. Mech Ageing Dev. 2001;122:1849-1864.
5. Mithani SK, Balch GC, Shiou SR, et al. Smad3 has a critical role in TGF-beta-mediated growth inhibition and apoptosis in colonic epithelial cells. J Surg Res. 2004;117:296-305.
6. Kaiser GC, Yan F, Polk DB. Conversion of TNFa from antiproliferative to proliferative ligand in mouse intestinal epithelial cells by regulating mitogen-activated protein kinase. Exp Cell Res. 1999;249:349-358.
7. Li P, Nijhawan D, Budihardjo I, et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 1997;91:479-489.
8. Zou H, Li Y, Liu X, et al. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem. 1999;274:11549-11556.
9. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer. 2002;2:647-656.
10. Deveraux QL, Stennicke HR, Salvesen GS, et al. Endogenous inhibitors of caspases. J Clin Immunol. 1999;19:388-398.
11. Delhalle S, Duvoix A, Schnekenburger M, et al. An introduction to the molecular mechanisms of apoptosis. Ann NY Acad Sci. 2003;1010:1-8.
12. Ramachandran A, Madesh M, Balasubramanian KA. Apoptosis in the intestinal epithelium: its relevance in normal and pathophysiological conditions. J Gastroenterol Hepatol. 2000;15:109-120.
13. Croitoru K, Zhou P. T-cell-induced mucosal damage in the intestine. Curr Opin Gastroenterol. 2004;20:581-586.
14. Bouma G, Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol. 2003;3:521-533.
15. Koshiji M, Adachi Y, Sogo S, et al. Apoptosis of colorectal adenocarcinoma (COLO 201) by tumour necrosis factor-alpha (TNF-alpha) and/or interferon-gamma (IFN-gamma), resulting from down-modulation of Bcl-2 expression. Clin Exp Immunol. 1998;111:211-218.
16. Novak JM, Collins JT, Donowitz M, et al. Effects of radiation on the human gastrointestinal tract. J Clin Gastroenterol. 1979;1:9-39.
17. Kolesnick R, Fuks Z. Radiation and ceramide-induced apoptosis. Oncogene. 2003;22:5897-5906.
18. Keshavarzian A, Haydek JM, Jacyno M, et al. Modulatory effects of the colonic milieu on neutrophil oxidative burst: a possible pathogenic mechanism of ulcerative colitis. J Lab Clin Med. 1997;130:216-225.
19. Jabs T. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol. 1999;57:231-245.
20. Ruemmele FM, Dionne S, Qureshi I, et al. Butyrate mediates Caco-2 cell apoptosis via up-regulation of pro-apoptotic BAK and inducing caspase-3 mediated cleavage of poly-(ADP-ribose) polymerase (PARP). Cell Death Differ 1999;6:729-735.
21. Ruemmele FM, Schwartz S, Seidman EG, et al. Butyrate induced Caco-2 cell apoptosis is mediated via the mitochondrial pathway. Gut. 2003;52:94-100.
22. Jones SA, Butler RN, Sanderson IR, et al. The effect of specific caspase inhibitors on TNF-alpha and butyrate-induced apoptosis of intestinal epithelial cells. Exp Cell Res. 2004;292:29-39.
23. Pritchard DM, Potten CS, Korsmeyer SJ, et al. Damage-induced apoptosis in intestinal epithelia from bcl-2-null and bax-null mice: investigations of the mechanistic determinants of epithelial apoptosis in vivo. Oncogene. 1999;18:7287-7293.
24. Merritt AJ, Potten CS, Watson AJ, et al. Differential expression of bcl-2 in intestinal epithelia: correlation with attenuation of apoptosis in colonic crypts and the incidence of colonic neoplasia. J Cell Sci. 1995;108(pt 6):2261-2271.
25. el-Deiry WS, Tokino T, Velculescu VE, et al. WAF1, a potential mediator of p53 tumor suppression. Cell. 1993;75:817-825.
26. Harper JW, Adami GR, Wei N, et al. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell. 1993;75:805-816.
27. Clarke AR, Gledhill S, Hooper ML, et al. p53 dependence of early apoptotic and proliferative responses within the mouse intestinal epithelium following gamma-irradiation. Oncogene. 1994;9:1767-1773.
28. Merritt AJ, Potten CS, Kemp CJ, et al. The role of p53 in spontaneous and radiation-induced apoptosis in the gastrointestinal tract of normal and p53-deficient mice. Cancer Res. 1994;54:614-617.
29. Pritchard DM, Potten CS, Hickman JA. The relationships between p53-dependent apoptosis, inhibition of proliferation, and 5-fluorouracil-induced histopathology in murine intestinal epithelia. Cancer Res. 1998;58:5453-5465.
30. Merritt AJ, Allen TD, Potten CS, et al. Apoptosis in small intestinal epithelial from p53-null mice: evidence for a delayed, p53-independent G2/M-associated cell death after gamma-irradiation. Oncogene. 1997;14:2759-2766.
31. Hendry JH, Cai WB, Roberts SA, et al. p53 deficiency sensitizes clonogenic cells to irradiation in the large but not the small intestine. Radiat Res. 1997;148:254-259.
32. Inagaki-Ohara K, Yada S, Takamura N, et al. p53-dependent radiation-induced crypt intestinal epithelial cells apoptosis is mediated in part through TNF-TNFR1 system. Oncogene. 2001;20:812-818.
33. Wu GS, Burns TF, McDonald ER 3rd, et al. KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat Genet. 1997;17:141-143.
34. Reinke V, Lozano G. The p53 targets mdm2 and Fas are not required as mediators of apoptosis in vivo. Oncogene. 1997;15:1527-1534.
35. Sheikh MS, Burns TF, Huang Y, et al. p53-dependent and -independent regulation of the death receptor KILLER/DR5 gene expression in response to genotoxic stress and tumor necrosis factor alpha. Cancer Res. 1998;58:1593-1598.
36. Bennett M, Macdonald K, Chan S-W, et al. Cell surface trafficking of Fas: a rapid mechanism of p53-mediated apoptosis. Science. 1998;282:290-293.
37. Ruemmele FM, Russo P, Beaulieu J, et al. Susceptibility to FAS-induced apoptosis in human nontumoral enterocytes: role of costimulatory factors. J Cell Physiol. 1999;181:45-54.
38. Strater J, Wellisch I, Riedl S, et al. CD95 (APO-1/Fas)-mediated apoptosis in colon epithelial cells: a possible role in ulcerative colitis. Gastroenterology. 1997;113:160-167.
39. Martin DA, Siegel RM, Zheng L, et al. Membrane oligomerization and cleavage activates the caspase-8 (FLICE/MACHalpha1) death signal. J Biol Chem. 1998;273:4345-4349.
40. Via C, Nguyen P, Shustov A, et al. A major role for the Fas pathway in acute graft-versus-host disease. JImmunol. 1996;157:5387-5393.
41. Yada S, Takamura N, Inagaki-Ohara K, et al. The role of p53 and Fas in a model of acute murine graft-versus-host disease. J Immunol. 2005;174:1291-1297.
42. Thanos D, Maniatis T. NF-κB: a lesson in family values. Cell. 1995;80:529-532.
43. Kasibhatla S, Brunner T, Genestier L, et al. DNA damaging agents induce expression of Fas ligand and subsequent apoptosis in T lymphocytes via the activation of NF-kappa B and AP-1. Mol Cell. 1998;1:543-551.
44. Neurath MF, Becker C, Barbulescu K. Role of NF-κB in immune and inflammatory responses in the gut. Gut. 1998;43:856-860.
45. Schmid RM, Adler G. NF-κB/Rel/IκB: implications in gastrointestinal diseases. Gastroenterology. 2000;118:1208-1228.
46. Rogler G, Brand K, Vogl D, et al. Nuclear factor κB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology. 1998;115:357-369.
47. Russo SM, Tepper JE, Baldwin AS Jr. Enhancement of radiosensitivity by proteasome inhibition: implications for a role of NF-kappaB. Int J Radiat Oncol Biol Phys. 2001;50:183-193.
48. Egan LJ, Eckmann L, Greten FR, et al. IκB-kinaseβ-dependent NF-κB activation provides radioprotection to the intestinal epithelium. Proc Natl Acad Sci U S A. 2004;101:2452-2457.
49. Chen LW, Egan L, Li ZW, et al. The two faces of IKK and NF-κB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion. Nat Med. 2003;9:575-581.
50. Polk DB, Lozano J, Kolesnick RN. Kinase suppressor of Ras as a ceramide-activated protein kinase. In: Futerman AH, ed. Ceramide Signaling. Georgetown, Tex: Landes Bioscience/Eurekah.com; 2002.
51. Zhang Y, Yao B, Delikat S, et al. Kinase suppressor of Ras is ceramide-activated protein kinase. Cell. 1997;89:63-72.
52. Yan F, John SK, Polk DB. Kinase suppressor of Ras determines survival of intestinal cells exposed to tumor necrosis factor. Cancer Res. 2001;61:8668-8675.
53. Yan F, Polk DB. Kinase suppressor of Ras is necessary for tumor necrosis factor a activation of extracellular signal-regulated kinase/mitogen-activated protein kinase in intestinal epithelial cells. Cancer Res. 2001;61:963-969.
54. Yan F, John SK, Wilson G, et al. Kinase suppressor of Ras-1 protects intestinal epithelium from cytokine-mediated apoptosis during inflammation. J Clin Invest. 2004;114:1272-1280.
55. Kuhn R, Lohler J, Rennick D, et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75:263-274.
56. Kennedy RJ, Hoper M, Deodhar K, et al. Interleukin 10-deficient colitis: new similarities to human inflammatory bowel disease. Br J Surg. 2000;87:1346-1351.
57. Xing HR, Kolesnick R. Kinase suppressor of Ras signals through Thr269 of c-Raf-1. J Biol Chem. 2001;276:9733-9741.
58. Zhong J, Troppmair J, Rapp UR. Independent control of cell survival by Raf-1 and Bcl-2 at the mitochondria. Oncogene. 2001;20:4807-4816.
59. Wang HG, Reed JC. Bcl-2, Raf-1 and mitochondrial regulation of apoptosis. Biofactors. 1998;8:13-16.
60. Jin S, Zhuo Y, Guo W, et al. p21-Activated Kinase 1 (PAK1)-dependent phosphorylation of Raf-1 regulates its mitochondrial localization, phosphorylation of BAD, and Bcl-2 association. J Biol Chem. 2005;280:24698- 24705.
61. Ogura Y, Bonen DK, Inohara N, et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature. 2001;411:603-606.
62. Hugot J, Laurent-Puig P, Gower-Rousseau C, et al. Mapping of a susceptibility locus for Crohn's disease on chromosome 16. Nature. 1996;379:821-823.
63. Gutierrez O, Pipaon C, Inohara N, et al. Induction of Nod2 in myelomonocytic and intestinal epithelial cells via nuclear factor-kB activation. J Biol Chem. 2002;277:41701-41705.
64. Girardin SE, Boneca IG, Viala J, et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem. 2003;278:8869-8872.
65. Kobayashi KS, Chamaillard M, Ogura Y, et al. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science. 2005;307:731-734.
66. Hugot JP, Chamaillard M, Zouali H, et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature. 2001;411:599-603.
67. Abbott DW, Wilkins A, Asara JM, et al. The Crohn's disease protein, NOD2, requires RIP2 in order to induce ubiquitinylation of a novel site on NEMO. Curr Biol. 2004;14:2217-2227.
68. Barnich N, Aguirre JE, Reinecker HC, et al. Membrane recruitment of NOD2 in intestinal epithelial cells is essential for nuclear factor-κB activation in muramyl dipeptide recognition. J Cell Biol. 2005;170:21-26.
69. Maeda S, Hsu LC, Liu H, et al. Nod2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing. Science. 2005;307:734-738.
70. Boughton-Smith NK, Hawkey CJ, Whittle BJ. Biosynthesis of lipoxygenase and cyclo-oxygenase products from [14C]-arachidonic acid by human colonic mucosa. Gut. 1983;24:1176-1182.
71. Houchen CW, Sturmoski MA, Anant S, et al. Prosurvival and antiapoptotic effects of PGE2 in radiation injury are mediated by EP2 receptor in intestine. Am J Physiol Gastrointest Liver Physiol. 2003;284:0490-0498.
72. Tessner TG, Muhale F, Riehl TE, et al. Prostaglandin E2 reduces radiation-induced epithelial apoptosis through a mechanism involving AKT activation and bax translocation. J Clin Invest. 2004;114:1676-1685.
73. Kabashima K, Saji T, Murata T, et al. The prostaglandin receptor EP4 suppresses colitis, mucosal damage and CD4 cell activation in the gut. J Clin Invest. 2002;109:883-893.
74. Abreu MT, Palladino AA, Arnold ET, et al. Modulation of barrier function during Fas-mediated apoptosis in human intestinal epithelial cells. Gastroenterology. 2000;119:1524-1536.
75. Watson AJ, Chu S, Sieck L, et al. Epithelial barrier function in vivo is sustained despite gaps in epithelial layers. Gastroenterology. 2005;129:902-912.
76. Colgan SP, Resnick MB, Parkos CA, et al. IL-4 directly modulates function of a model human intestinal epithelium. J Immunol. 1994;153:2122-2129.
77. Madara JL, Stafford J. Interferon-gamma directly affects barrier function of cultured intestinal epithelial monolayers. J Clin Invest. 1989;83:724-727.
78. Ma TY, Iwamoto GK, Hoa NT, et al. TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol. 2004;286:G367-G376.
79. Schmitz H, Barmeyer C, Fromm M, et al. Altered tight junction structure contributes to the impaired epithelial barrier function in ulcerative colitis. Gastroenterology. 1999;116:301-309.
80. Potten CS, Owen G, Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci. 2002;115:2381-2388.
81. Wong MH, Huelsken J, Birchmeier W, et al. Selection of multipotent stem cells during morphogenesis of small intestinal crypts of Lieberkuhn is perturbed by stimulation of Lef-1/beta-catenin signaling. 2002;277:15843-15850.
82. Booth C, Potten CS. Gut instincts: thoughts on intestinal epithelial stem cells. J Clin Invest. 2000;105:1493-1499.
83. Iwamoto M, Koji T, Makiyama K, et al. Apoptosis of crypt epithelial cells in ulcerative colitis. J Pathol. 1996;180:152-159.
84. Di Sabatino A, Ciccocioppo R, Luinetti O, et al. Increased enterocyte apoptosis in inflamed areas of Crohn's disease. Dis Colon Rectum. 2003;46:1498-1507.
85. Hagiwara C, Tanaka M, Kudo H. Increase in colorectal epithelial apoptotic cells in patients with ulcerative colitis ultimately requiring surgery. J Gastroenterol Hepatol. 2002;17:758-764.
86. Sartor RB. Current concepts of the etiology and pathogenesis of ulcerative colitis and Crohn's disease. Gastroenterol Clin North Am. 1995;24:475-507.
87. Marini M, Bamias G, Rivera-Nieves J, TNF-a neutralization ameliorates the severity of murine Crohn's-like ileitis by abrogation of intestinal epithelial cell apoptosis. Proc Natl Acad Sci USA. 2003;100:8366-8371.
88. Weber CK, Liptay S, Wirth T, et al. Suppression of NF-kappaB activity by sulfasalazine is mediated by direct inhibition of IkappaB kinases alpha and beta. Gastroenterology. 2000;119:1209-1218.
89. Kaiser GC, Yan F, Polk DB. Mesalamine blocks tumor necrosis factor growth inhibition and nuclear factor κB activation in mouse colonocytes. Gastroenterology. 1999;116:602-609.
90. Yan F, Polk DB. Aminosalicylic acid inhibits IκB kinase a phosphorylation of IκBa in mouse intestinal epithelial cells. J Biol Chem. 1999;274:36631-36636.
91. Jobin C, Sartor RB. The IκB/NF-κB system: a key determinant of mucosal inflammation and protection. Am J Physiol Cell Physiol. 2000;278:C451-C462.
92. Waetzig GH, Seegert D, Rosenstiel P, et al. p38 mitogen-activated protein kinase is activated and linked to TNF-α signaling in inflammatory bowel disease. J Immunol. 2002;168:5342-5351.
93. Hollenbach E, Vieth M, Roessner A, et al. Inhibition of RICK/nuclear factor-kappaB and p38 signaling attenuates the inflammatory response in a murine model of Crohn disease. J Biol Chem. 2005;280:14981-14988.
94. ten Hove T, van den Blink B, Pronk I, et al. Dichotomal role of inhibition of p38 MAPK with SB 203580 in experimental colitis. Gut. 2002;50:507-512.
95. Evans ME, Jones DP, Ziegler TR. Glutamine inhibits cytokine-induced apoptosis in human colonic epithelial cells via the pyrimidine pathway. Am J Physiol Gastrointest Liver Physiol. 2005;289:G388-G396.
96. Paesold G, Guiney DG, Eckmann L, et al. Genes in the Salmonella pathogenicity island 2 and the Salmonella virulence plasmid are essential for Salmonella-induced apoptosis in intestinal epithelial cells. Cell Microbiol. 2002;4:771-781.
97. Knodler LA, Finlay BB, Steele-Mortimer O. The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J Biol Chem. 2005;280:9058-9064.
98. Abul-Milh M, Wu Y, Lau B, et al. Induction of epithelial cell death including apoptosis by enteropathogenic Escherichia coli expressing bundle-forming pili. Infect Immun. 2001;69:7356-7364.
99. Boshuizen JA, Reimerink JH, Kortel-van Male AM, et al. Changes in small intestinal homeostasis, morphology, and gene expression during rotavirus infection of infant mice. J Virol. 2003;77:13005-13016.
100. Fleeton MN, Contractor N, Leon F, et al. Peyer's patch dendritic cells process viral antigen from apoptotic epithelial cells in the intestine of reovirus-infected mice. J Exp Med. 2004;200:235-245.
101. Cover TL, Krishna US, Israel DA, et al. Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin. Cancer Res. 2003;63:951-957.
102. Le'Negrate G, Ricci V, Hofman V, et al. Epithelial intestinal cell apoptosis induced by Helicobacter pylori depends on expression of the cag pathogenicity island phenotype. Infect Immun. 2001;69:5001-5009.
103. Gupta RA, Polk DB, Krishna U, et al. Activation of peroxisome proliferator-activated receptor g suppresses nuclear factor κB-mediated apoptosis induced by helicobacter pylori in gastric epithelial cells. J Biol Chem. 2001;276:31059-31066.
104. Lehmann FS, Terracciano L, Carena I, et al. In situ correlation of cytokine secretion and apoptosis in Helicobacter pylori-associated gastritis. Am J Physiol Gastrointest Liver Physiol. 2002;283:G481-G488.
105. Genesca M, Sola A, Miquel R, et al. Role of changes in tissular nucleotides on the development of apoptosis during ischemia/reperfusion in rat small bowel. Am J Pathol. 2002;161:1839-1847.
106. Jilling T, Lu J, Jackson M, et al. Intestinal epithelial apoptosis initiates gross bowel necrosis in an experimental rat model of neonatal necrotizing enterocolitis. Pediatr Res. 2004;55:622-629.
107. Ozen S, Akisu M, Baka M, et al. Insulin-like growth factor attenuates apoptosis and mucosal damage in hypoxia/reoxygenation-induced intestinal injury. Biol Neonate. 2005;87:91-96.
108. Clark JA, Lane RH, Maclennan NK, et al. Epidermal growth factor reduces intestinal apoptosis in an experimental model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol. 2005;288:G755-G762.
109. Moss SF, Attia L, Scholes JV, et al. Increased small intestinal apoptosis in coeliac disease. Gut. 1996;39:811-817.
110. Ciccocioppo R, Di Sabatino A, Parroni R, et al. Increased enterocyte apoptosis and Fas-Fas ligand system in celiac disease. Am J Clin Pathol. 2001;115:494-503.
111. Maiuri L, Ciacci C, Raia V, et al. FAS engagement drives apoptosis of enterocytes of coeliac patients. Gut. 2001;48:418-424.
112. Giovannini C, Matarrese P, Scazzocchio B, et al. Wheat gliadin induces apoptosis of intestinal cells via an autocrine mechanism involving Fas-Fas ligand pathway. FEBS Lett. 2003;540:117-124.
113. Ciccocioppo R, Di Sabatino A, Parroni R, et al. Cytolytic mechanisms of intraepithelial lymphocytes in coeliac disease (CoD). Clin Exp Immunol. 2000;120:235-240.
114. Zicha D, Dunn G, Jones G. Analyzing chemotaxis using the Dunn direct-viewing chamber. In: Pollard JW, Walker JM, eds. Basic Cell Culture Protocols. 2nd ed. Totowa, NJ: Humana Press; 1997:449.
115. Schotte P, Van Loo G, Carpentier I, et al. Lithium sensitizes tumor cells in an NF-kappa B-independent way to caspase activation and apoptosis induced by tumor necrosis factor (TNF): evidence for a role of the TNF receptor-associated death domain protein. J Biol Chem. 2001;276:25939-25945.
116. Laudanna C, Mochly-Rosen D, Liron T, et al. Evidence of z protein kinase C involvement in polymorphonuclear neutrophil integrin-dependent adhesion and chemotaxis. J Biol Chem. 1998;273:30306-30315.
117. Shirasawa S, Furuse M, Yokoyama N, et al. Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science. 1993;260:85-88.
118. Peek RM Jr, Moss SF, Tham KT, et al. Helicobacter pylori cagA+ strains and dissociation of gastric epithelial cell proliferation from apoptosis. J Natl Cancer Inst. 1997;89:863-868.
119. Rokkas T, Ladas S, Liatsos C, et al. Relationship of Helicobacter pylori CagA status to gastric cell proliferation and apoptosis. Dig Dis Sci. 1999;44:487-493.
120. Moss SF, Sordillo EM, Abdalla AM, et al. Increased gastric epithelial cell apoptosis associated with colonization with cagA+ Helicobacter pylori strains. Cancer Res. 2001;61:1406-1411.
121. Peek RM Jr. Orchestration of aberrant epithelial signaling by Helicobacter pylori CagA. Sci STKE. 2005;2005:e14.
122. Peek RM Jr. Events at the host-microbial interface of the gastrointestinal tract, IV: the pathogenesis of Helicobacter pylori persistence. Am J Physiol Gastrointest Liver Physiol. 2005;289:G8-G12.
123. Fan X, Crowe SE, Behar S, et al. 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. 1998;187:1659-1669.
124. Peek RM Jr, Blaser MJ, Mays DJ, et al. Helicobacter pylori strain-specific genotypes and modulation of the gastric epithelial cell cycle. Cancer Res. 1999;59:6124-6131.
125. Kennedy SG, Wagner AJ, Conzen SD, et al. The PI 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes Dev. 1997;11:701-713.
126. Ireland H, Kemp R, Houghton C, et al. Inducible Cre-mediated control of gene expression in the murine gastrointestinal tract: effect of loss of beta-catenin. Gastroenterology. 2004;126:1236-1246.
127. Jones NL, Day AS, Jennings HA, et al. Helicobacter pylori induces gastric epithelial cell apoptosis in association with increased Fas receptor expression. Infect Immun. 1999;67:4237-4242.
128. Schutze S, Potthoff K, Machleidt T, et al. TNF activates NFκB by phosphatidylcholine-specific phospholipase C-induced "acidic" sphinomyelin breakdown. Cell. 1992;71:765-776.
129. Nagasako T, Sugiyama T, Mizushima T, et al. Up-regulated Smad5 mediates apoptosis of gastric epithelial cells induced by Helicobacter pylori infection. J Biol Chem. 2003;278:4821-4825.
130. Gupta RA, Polk DB, Krishna U, et al. Activation of peroxisome proliferator-activated receptor gamma suppresses nuclear factor kappa B-mediated apoptosis induced by Helicobacter pylori in gastric epithelial cells. J Biol Chem. 2001;276:31059-31066.
131. Kanai M, Konda Y, Nakajima T, et al. TGF-alpha Inhibits apoptosis of murine gastric pit cells through an NF-κB-dependent pathway. Gastroenterology. 2001;121:56-67.
132. Su CG, Wen X, Bailey ST, et al. A novel therapy for colitis utilizing PPAR-gamma ligands to inhibit the epithelial inflammatory response. J Clin Invest 1999;104:383-389.
133. Fu S, Ramanujam KS, Wong A, et al. Increased expression and cellular localization of inducible nitric oxide synthase and cyclooxygenase 2 in Helicobacter pylori gastritis. Gastroenterology. 1999;116:1319-1329.
134. McDermott MF, Aksentijevich I, Galon J, et al. Germline mutations in the extracellular domains of the 55 κDa TNF receptor, TNFR1, define a family of dominantly inherited autoinflammatory syndromes. Cell. 1999;97:133-144.
135. Ristimaki A, Honkanen N, Jankala H, et al. Expression of cyclooxygenase-2 in human gastric carcinoma. Cancer Res. 1997;57:1276-1280.
136. Sawaoka H, Tsuji S, Tsujii M, et al. Involvement of cyclooxygenase-2 in proliferation and morphogenesis induced by transforming growth factor alpha in gastric epithelial cells. Prostaglandins Leukot Essent Fatty Acids. 1999;61:315-322.
137. Sung JJ, Leung WK, Go MY, et al. Cyclooxygenase-2 expression in Helicobacter pylori-associated premalignant and malignant gastric lesions. Am J Pathol. 2000;157:729-735.
138. Tatsuguchi A, Sakamoto C, Wada K, et al. Localisation of cyclooxygenase 1 and cyclooxygenase 2 in Helicobacter pylori related gastritis and gastric ulcer tissues in humans. Gut. 2000;46:782-789.
139. Uefuji K, Ichikura T, Mochizuki H, et al. Expression of cyclooxygenase-2 proteinin gastric adenocarcinoma. J Surg Oncol. 1998;69:168-272.
140. Peek RM Jr, Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer. 2002;2:28-37.
141. Eaden JA, Abrams KR, Mayberry JF. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut. 2001;48:526-535.
142. Ekbom A, Helmick C, Zack M, et al. Ulcerative colitis and colorectal cancer: a population-based study. N Engl J Med. 1990;323:1228-1233.
143. Vagefi PA, Longo WE. Colorectal cancer in patients with inflammatory bowel disease. Clin Colorectal Cancer. 2005;4:313-319.
144. Weitzman SA, Gordon LI. Inflammation and cancer: role of phagocyte-generated oxidants in carcinogenesis. Blood. 1990;76:655-663.
145. Burmer GC, Rabinovitch PS, Haggitt RC, et al. Neoplastic progression in ulcerative colitis: histology, DNA content, and loss of a p53 allele. Gastroenterology. 1992;103:1602-1610.
146. Kerneis S, Bernet MF, Coconnier MH, et al. Adhesion of human enterotoxigenic Escherichia coli to human mucus secreting HT-29 cell subpopulations in culture. Gut. 1994;35:1449-1454.
147. Levine DS, Rabinovitch PS, Haggitt RC, et al. Distribution of aneuploid cell populations in ulcerative colitis with dysplasia or cancer. Gastroenterology. 1991;101:1198-1210.
148. Willenbucher RF, Zelman SJ, Ferrell LD, et al. Chromosomal alterations in ulcerative colitis-related neoplastic progression. Gastroenterology. 1997;113:791-801.
149. Redston MS, Papadopoulos N, Caldas C, et al. Common occurrence of APC and K-ras gene mutations in the spectrum of colitis-associated neoplasias. Gastroenterology. 1995;108:383-392.
150. Tarmin L, Yin J, Harpaz N, et al. Adenomatous polyposis coli gene mutations in ulcerative colitis-associated dysplasias and cancers versus sporadic colon neoplasms. Cancer Res. 1995;55:2035-2038.
151. Holmgren L, O'Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med. 1995;1:149-153.
152. Kulkarni N, Zang E, Kelloff G, et al. Effect of the chemopreventive agents piroxicam and D,L-alpha-difluoromethylornithine on intermediate biomarkers of colon carcinogenesis. Carcinogenesis. 1992;13:995-1000.
153. Sinicrope FA, Roddey G, McDonnell TJ, et al. Increased apoptosis accompanies neoplastic development in the human colorectum. Clin Cancer Res. 1996;2:1999-2006.
154. Langlois NE, Lamb J, Eremin O, et al. Apoptosis in colorectal carcinoma occurring in patients aged 45 years and under: relationship to prognosis, mitosis, and immunohistochemical demonstration of p53, c-myc and bcl-2 protein products. J Pathol. 1997;182:392-397.
155. Sugamura K, Makino M, Kaibara N. Apoptosis as a prognostic factor in colorectal carcinoma. Surg Today. 1998;28:145-150.
156. Reinacher-Schick A, Gumbiner BM. Apical membrane localization of the adenomatous polyposis coli tumor suppressor protein and subcellular distribution of the b-catenin destruction complex in polarized epithelial cells. J Cell Biol. 2001;152:491-502.
157. Rodenburg RJ, Ganga A, van Lent PL, et al. The antiinflammatory drug sulfasalazine inhibits tumor necrosis factor alpha expression in macrophages by inducing apoptosis. Arthritis Rheum. 2000;43:1941-1950.
158. Sinha A, Nightingale J, West KP, et al. Epidermal growth factor enemas with oral mesalamine for mild-to-moderate left-sided ulcerative colitis or proctitis. N Engl J Med. 2003;349:350-357.
159. Ciardiello F, Kim N, Saeki T, et al. Differential expression of epidermal growth factor-related proteins in human colorectal tumors. Proc Natl Acad Sci USA. 1991;88:7792-7796.
160. Malecka-Panas E, Kordek R, Biernat W, et al. Differential activation of total and EGF receptor (EGF-R) tyrosine kinase (tyr-k) in the rectal mucosa in patients with adenomatous polyps, ulcerative colitis and colon cancer. Hepatogastroenterology. 1997;44:435-440.
161. Chu F-F, Esworthy RS, Chu PG, et al. Bacteria-induced intestinal cancer in mice with disrupted Gpx1 and Gpx2 genes. Cancer Res. 2004;64:962-968.
162. O'Mahony L, Feeney M, O'Halloran S, et al. Probiotic impact on microbial flora, inflammation and tumour development in IL-10 knockout mice. Aliment Pharmacol Ther. 2001;15:1219-1225.
163. Yan F, Polk DB. Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem. 2002;277:50959-50965.