Colonic epithelial cell turnover: possible implications for ulcerative colitis and cancer initiation

References

• Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972;26:239–57.
   Google Scholar
• Green DR. Apoptotic pathways: the roads to ruin. Cell 1998;94: 695–8.
   PubMed Web of Science ®Google Scholar
• Strater J, Wellisch I, Riedl S, Walczak H, Koretz K, Tandara A, et al. CD95 (APO-1/Fas)-mediated apoptosis in colon epithelial cells: a possible role in ulcerative colitis. Gastroenterology 1997; 113:160–7.
   PubMed Web of Science ®Google Scholar
• Strater J, Walczak H, Pukrop T, Von Muller L, Hasel C, Kornmann M, et al. TRAIL and its receptors in the colonic epithelium: a putative role in the defense of viral infections. Gastroenterology 2002;122:659–66.
   Google Scholar
• Muzio M, Stockwell BR, Stennicke HR, Salvesen GS, Dixit VM. An induced proximity model for caspase-8 activation. J Biol Chem 1998;273: 2926–930.
   Google Scholar
• Ravagnan L, Roumier T, Kroemer G. Mitochondria, the killer organelles and their weapons. J Cell Physiol 2002;192:131–7.
   PubMed Web of Science ®Google Scholar
• Potten CS. Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Phil Trans R Soc Lond B Biol Sci 1998;353:821–30.
   PubMed Web of Science ®Google Scholar
• Merritt AJ, Potten CS, Kemp CJ, Hickman JA, Balmain A, Lane DP, 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;54:614–7.
   PubMed Web of Science ®Google Scholar
• Bortner CD, Cidlowski JA. Cellular mechanisms for the repression of apoptosis. Annu Rev Pharmacol Toxicol 2002;42: 259–81.
   PubMed Web of Science ®Google Scholar
• Potten CS, Loeffler M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 1990;110:1001–20.
   Google Scholar
• Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, et al. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ ephrinB. Cell 2002;111:251–63.
   Google Scholar
• Ko TC, Pan F, Sheng H, Brown DB, Thompson EA, Beauchamp RD. Cyclin D3 is essential for intestinal epithelial cell proliferation. World J Surg 2002;26:812–8.
   PubMed Web of Science ®Google Scholar
• Wodarz A, Nusse R. Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol 1998;14:59–88.
   PubMed Web of Science ®Google Scholar
• van de Wetering, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A, et al. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 2002; 111:241–50.
   Google Scholar
• Craven PA, Pfanstiel J, Saito R, DeRubertis FR. Actions of sulfasalazine and 5-aminosalicylic acid as reactive oxygen scavengers in the suppression of bile acid-induced increases in colonic epithelial cell loss and proliferative activity. Gastroenterology 1987;92:1998–2008.
   PubMed Web of Science ®Google Scholar
• Skraastad O, Reichelt KL. Further studies on the biological characteristics of an endogenous colon mitosis inhibitor: comparison with some structurally related peptides. Virchows Arch B Cell Pathol Incl Mol Pathol 1989;56:321–5.
   PubMedGoogle Scholar
• Bartram HP, Kasper K, Dusel G, Liebscher E, Gostner A, Loges C, et al. Effects of calcium and deoxycholic acid on human colonic cell proliferation in vitro. Ann Nutr Metab 1997;41:315–23.
   PubMed Web of Science ®Google Scholar
• Nobre-Leitao C, Chaves P, Fidalgo P, Cravo M, Gouveia-Oliveira A, Ferra MA, et al. Calcium regulation of colonic crypt cell kinetics: evidence for a direct effect in mice. Gastroenterology 1995;109:498–504.
   Google Scholar
• Potten CS. Epithelial cell growth and differentiation. II. Intestinal apoptosis. Am J Physiol 1997;273:G253–7.
   Google Scholar
• Frisch SM, Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 1994;124:619–26.
   PubMed Web of Science ®Google Scholar
• Strater J, Wedding U, Barth TF, Koretz K, Elsing C, Moller P. Rapid onset of apoptosis in vitro follows disruption of beta 1- integrin/matrix interactions in human colonic crypt cells. Gastroenterology 1996;110:1776–84.
   PubMed Web of Science ®Google Scholar
• Grossmann J, Walther K, Artinger M, Kiessling S, Scholmerich J. Apoptotic signaling during initiation of detachment-induced apoptosis (‘anoikis’) of primary human intestinal epithelial cells. Cell Growth Differ 2001;12:147–55.
   Google Scholar
• Hall PA, Coates PJ, Ansari B, Hopwood D. Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J Cell Sci 1994;107 (Pt 12)3569–77.
   Google Scholar
• Marshall CJ. Ras effectors. Curr Opin Cell Biol 1996;8:197–204.
   PubMed Web of Science ®Google Scholar
• Giancotti FG, Ruoslahti E. Integrin signaling. Science 1999;285: 1028–32.
   PubMed Web of Science ®Google Scholar
• Frisch SM, Screaton RA. Anoikis mechanisms. Curr Opin Cell Biol 2001;13:555–62.
   PubMed Web of Science ®Google Scholar
• Rosen K, Rak J, Leung T, Dean NM, Kerbel RS, Filmus J. Activated Ras prevents downregulation of Bcl-X(L) triggered by detachment from the extracellular matrix. A mechanism of Rasinduced resistance to anoikis in intestinal epithelial cells. J Cell Biol 2000;149:447–56.
   Google Scholar
• Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, Stanbridge E, et al. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998;282:1318–2l.
   Google Scholar
• Datta sR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997;91:231–41.
   Google Scholar
• Probstmeier R, Martini R, Tacke R, Schachner M. Expression of the adhesion molecules L1, N-CAM and J1/tenascin during development of the murine small intestine. Differentiation 1990; 44:42–55.
   Google Scholar
• Probstmeier R, Martini R, Schachner M. Expression of J1/ tenascin in the crypt-villus unit of adult mouse small intestine: implications for its role in epithelial cell shedding. Development 1990;109: 313–21.
   Google Scholar
• Grossmann J, Mohr S, Lapentina EG, Fiocchi C, Levine AD. Sequential and rapid activation of select caspases during apoptosis of normal intestinal epithelial cells. Am J Physiol 1998;274:G1117–24.
   Google Scholar
• Ilic D, Almeida EA, Schlaepfer DD, Dazin P, Aizawa S, Damsky CH. Extracellular matrix survival signals transduced by focal adhesion kinase suppress p53-mediated apoptosis. J Cell Biol 1998;143:547–60.
   PubMed Web of Science ®Google Scholar
• Grossmann J, Artinger M, Grasso AW, Kung HJ, Scholmerich J, Fiocchi C, et al. Hierarchical cleavage of focal adhesion kinase by caspases alters signal transduction during apoptosis of intestinal epithelial cells. Gastroenterology 2001;120:79–88.
   PubMed Web of Science ®Google Scholar
• Merritt AJ, Potten CS, Watson AJ, Loh DY, Nakayama K, Nakayama K, 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)2261–71.
   Google Scholar
• Potten CS, Wilson JW, Booth C. Regulation and significance of apoptosis in the stem cells of the gastrointestinal epithelium. Stem Cells 1997;15:82–93.
   Google Scholar
• Grossmann J, Walther K, Artinger M, Rummele P, Woenckhaus M, Scholmerich J. Induction of apoptosis before shedding of human intestinal epithelial cells. Am J Gastroenterol 2002; 97: 1421–8.
   PubMed Web of Science ®Google Scholar
• Hall PA, Coates PJ, Ansari B, Hopwood D. Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J Cell Sci 1994;107 (Pt 12)3569–77.
   Google Scholar
• Hermiston ML, Gordon JI. Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science 1995;270:1203–7.
   PubMed Web of Science ®Google Scholar
• Weng Z, Xin M, Pablo L, Grueneberg D, Hagel M, Bain G, et al. Protection against anoikis and down-regulation of cadherin expression by a regulatable beta-catenin protein. J Biol Chem 2002;277:18677–86.
   PubMed Web of Science ®Google Scholar
• Cai WB, Roberts SA, Bowley E, Hendry JH, Potten CS. Differential survival of murine small and large intestinal crypts following ionizing radiation. Int J Radiat Biol 1997;71:145–55.
   Google Scholar
• Bleiberg H, Mainguet P, Galand P, Chretien J, Dupont-Mairesse N. Cell renewal in the human rectum. In vitro autoradiographic study on active ulcerative colitis. Gastroenterology 1970; 58: 851–5.
   Google Scholar
• Serafini EP, Kirk AP, Chambers TJ. Rate and pattern ofepithelial cell proliferation in ulcerative colitis. Gut 1981;22:648–52.
   Google Scholar
• Noffsinger AE, Miller MA, Cusi MV, Fenoglio-Preiser CM. The pattern of cell proliferation in neoplastic and nonneoplastic lesions of ulcerative colitis. Cancer 1996;78:2307–12.
   Google Scholar
• Withers HR, Elkind MM. Microcolony survival assay for cells of mouse intestinal mucosa exposed to radiation. Int J Radiat Biol Relat Stud Phys Chem Med 1970;17:261–7.
   PubMed Web of Science ®Google Scholar
• Cai WB, Roberts SA, Potten CS. The number of clonogenic cells in crypts in three regions of murine large intestine. Int J Radiat Biol 1997;71:573–9.
   Google Scholar
• Dignass AU. Mechanisms and modulation of intestinal epithelial repair. Inflamm Bowel Dis 2001;7:68–77.
   PubMed Web of Science ®Google Scholar
• Al Nafussi AI, Wright NA. The effect of epidermal growth factor (EGF) on cell proliferation of the gastrointestinal mucosa in rodents. Virchows Arch B Cell Pathol Incl Mol Pathol 1982;40: 63–9.
   PubMedGoogle Scholar
• Ruifrok AC, Mason KA, Lozano G, Thames HD. Spatial and temporal patterns of expression of epidermal growth factor, transforming growth factor alpha and transforming growth factor beta 1–3 and their receptors in mouse jejunum after radiation treatment. Radiat Res 1997;147:1–12.
   PubMed Web of Science ®Google Scholar
• Thomas DM, Nasim MM, Gullick WJ, Alison MR. Immuno-reactivity of transforming growth factor alpha in the normal adult gastrointestinal tract. Gut 1992;33:628–31.
   PubMed Web of Science ®Google Scholar
• Babyatsky MW, Rossiter G, Podolsky DK. Expression of transforming growth factors alpha and beta in colonic mucosa in inflammatory bowel disease. Gastroenterology 1996; 110:975–84.
   Google Scholar
• Chowdhury A, Fukuda R, Fukumoto S. Growth factor mRNA expression in normal colorectal mucosa and in uninvolved mucosa from ulcerative colitis patients. J Gastroenterol 1996;31: 353–60.
   Google Scholar
• Malecka-Panas E, Kordek R, Biernat W, Tureaud J, Liberski PP, Majumdar AP. 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;44:435–40.
   Google Scholar
• Brauchle M, Madlener M, Wagner AD, Angermeyer K, Lauer U, Hofschneider PH, et al. Keratinocyte growth factor is highly overexpressed in inflammatory bowel disease. Am J Pathol 1996; 149:521–9.
   PubMed Web of Science ®Google Scholar
• Potten CS, O’Shea JA, Farrell CL, Rex K, Booth C. The effects of repeated doses of keratinocyte growth factor on cell proliferation in the cellular hierarchy of the crypts of the murine small intestine. Cell Growth Differ 2001;12:265–75.
   PubMedGoogle Scholar
• Monteleone I, Vavassori P, Biancone L, Monteleone G, Pallone F. Immunoregulation in the gut: success and failures in human disease. Gut 2002;50 Suppl 3:III60–III64.
   Google Scholar
• Seidelin JB, Horn T, Nielsen OH. A simple and efficient method for the isolation and cultivation of endoscopically obtained human colonocytes. Am J Physiol Gastrointest Liver Physiol 2003 In press.
   Google Scholar
• Schorkhuber M, Karner-Hanusch J, Sedivy R, Ellinger A, Armbruster C, Schulte-Hermann R, et al. Survival of normal colonic epithelial cells from both rats and humans is prolonged by coculture with rat embryo colonic fibroblasts. Cell Biol Toxicol 1998;14:211–23.
   PubMed Web of Science ®Google Scholar
• Iwamoto M, Koji T, Makiyama K, Kobayashi N, Nakane PK. Apoptosis of crypt epithelial cells in ulcerative colitis. J Pathol 1996;180:152–9.
   Google Scholar
• Arai N, Mitomi H, Ohtani Y, Igarashi M, Kakita A, Okayasu I. Enhanced epithelial cell turnover associated with p53 accumulation and high p21WAF1/CIP1 expression in ulcerative colitis. Mod Pathol 1999;12:604–11.
   PubMed Web of Science ®Google Scholar
• Madara JL, Stafford J. Interferon-gamma directly affects barrier function of cultured intestinal epithelial monolayers. J Clin Invest 1989;83:724–7.
   PubMed Web of Science ®Google Scholar
• Gitter AH, Wullstein F, Fromm M, Schulzke JD. Epithelial barrier defects in ulcerative colitis: characterization and quantification by electrophysiological imaging. Gastroenterology 2001;121:1320–8.
   PubMed Web of Science ®Google Scholar
• Heyman M, Desjeux JF. Cytokine-induced alteration of the epithelial barrier to food antigens in disease. Ann NY Acad Sci 2000;915:304–11.
   PubMed Web of Science ®Google Scholar
• Ueyama H, Kiyohara T, Sawada N, Isozaki K, Kitamura S, Kondo S, et al. High Fas ligand expression on lymphocytes in lesions of ulcerative colitis. Gut 1998;43:48–55.
   PubMed Web of Science ®Google Scholar
• Ruemmele FM, Russo P, Beaulieu J, Dionne S, Levy E, Lentze MJ, et al. Susceptibility to FAS-induced apoptosis in human nontumoral enterocytes: role of costimulatory factors. J Cell Physiol 1999;181:45–54.
   PubMed Web of Science ®Google Scholar
• Ossina NK, Cannas A, Powers VC, Fitzpatrick PA, Knight JD, Gilbert JR, et al. Interferon-gamma modulates a p53-independent apoptotic pathway and apoptosis-related gene expression. J Biol Chem 1997;272:16351–7.
   PubMed Web of Science ®Google Scholar
• O’Connell J, Bennett MW, Nally K, O’Sullivan GC, Collins JK, Shanahan F. Interferon-gamma sensitizes colonic epithelial cell lines to physiological and therapeutic inducers of colonocyte apoptosis. J Cell Physiol 2000;185:331–8.
   Google Scholar
• Xu X, Fu XY, Plate J, Chong. AS. IFN-gamma induces cell growth inhibition by Fas-mediated apoptosis: requirement of STAT1 protein for up-regulation of Fas and FasL expression. Cancer Res 1998;58:2832–7.
   PubMed Web of Science ®Google Scholar
• Naujokat C, Sezer O, Possinger K. Tumor necrosis factor-alpha and interferon-gamma induce expression of functional Fas ligand on HT29 and MCF7 adenocarcinoma cells. Biochem Biophys Res Commun 1999;264: 813–9.
   Google Scholar
• Koshiji M, Adachi Y, Sogo S, Taketani S, Oyaizu N, Than S, et al. Apoptosis of colorectal adenocarcinoma (COLO 201) by tumour necrosis factor-alpha (TNF-alpha) and/or interferongamma (IFN-gamma), resulting from down-modulation of Bcl-2 expression. Clin Exp Immunol 1998;111:211–8.
   PubMed Web of Science ®Google Scholar
• Sveinbjornsson B, Rushfeldt C, Olsen R, Smedsrod B, Seljelid R. Cytotoxic effect of cytokines on murine colon carcinoma cells involves TNF-mediated apoptosis. Biochem Biophys Res Commun 1997;233:270–5.
   Google Scholar
• Iimura M, Nakamura T, Shinozaki S, Iizuka B, Inoue Y, Suzuki S, et al. Bax is downregulated in inflamed colonic mucosa of ulcerative colitis. Gut 2000;47:228–35.
   PubMed Web of Science ®Google Scholar
• Ludwig D, Stahl M, Ibrahim ET, Wenzel BE, Drabicki D, Wecke A, et al. Enhanced intestinal expression of heat shock protein 70 in patients with inflammatory bowel diseases. Dig Dis Sci 1999; 44:1440–7.
   PubMed Web of Science ®Google Scholar
• Martinon F, Burns K, Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 2002;10:417–26.
   Google Scholar
• Vainer B, Seidelin JB, Nielsen OH, Horn T. Expression of ICAM-1 in inflammatory bowel disease and colon cancer cell lines. Virchows Archiv 2003 In press.
   Google Scholar
• Pedersen G, Saermark T, Horn T, Giese B, Bendtzen K, Brynskov J. Cytokine-induced impairment of short-chain fatty acid oxidation and viability in human colonic epithelial cells. Cytokine 2000;12:1400–4.
   PubMed Web of Science ®Google Scholar
• Inoue S, Matsumoto T, Iida M, Mizuno M, Kuroki F, Hoshika K, et al. Characterization of cytokine expression in the rectal mucosa of ulcerative colitis: correlation with disease activity. Am J Gastroenterol 1999;94:2441–6.
   PubMed Web of Science ®Google Scholar
• Fuss IJ, Neurath M, Boirivant M, Klein JS, de la MC, Strong SA, et al. Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn’s disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J Immunol 1996;157: 1261–70.
   Google Scholar
• Proskuryakov SY, Konoplyannikov AG, Gabai VL. Necrosis: a specific form of programmed cell death? Exp Cell Res 2003/283: 1–16.
   Google Scholar
• Riddell RH, Path FRC. Pathology of idiopathic inflammatory bowel disease. In: Kirsner JB, editor. Inflammatory bowel disease. Philadelphia, Saunders 2000. p. 427–50.
   Google Scholar
• Waterhouse CC, Joseph RR, Stadnyk AW. Endogenous IL-1 and type II IL-1 receptor expression modulate anoikis in intestinal epithelial cells. Exp Cell Res 2001;269: 109–16.
   Google Scholar
• Zeng Q, Chen S, You Z, Yang F, Carey TE, Saims D, et al. Hepatocyte growth factor inhibits anoikis in head and neck squamous cell carcinoma cells by activation of ERK and Akt signaling independent of NFkappa B. J Biol Chem 2002; 277: 25203–8.
   PubMed Web of Science ®Google Scholar
• Michelassi F, Leuthner S, Lubienski M, Bostwick D, Rodgers J, Handcock M, et al. Ras oncogene p21 levels parallel malignant potential of different human colonic benign conditions. Arch Surg 1987;122:1414–6.
   PubMedGoogle Scholar
• Eaden JA, Abrams KR, Mayberry JF. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 2001;48:526–35.
   Google Scholar
• Heinen CD, Noffsinger AE, Belli J, Straughen J, Fischer J, Groden J, et al. Regenerative lesions in ulcerative colitis are characterized by microsatellite mutation. Genes Chromosomes Cancer 1997;19:170–5.
   PubMed Web of Science ®Google Scholar
• Brentnall TA, Crispin DA, Bronner MP, Cherian SP, Hueffed M, Rabinovitch PS, et al. Microsatellite instability in nonneoplastic mucosa from patients with chronic ulcerative colitis. Cancer Res 1996;56:1237–40.
   PubMed Web of Science ®Google Scholar
• Lang SM, Stratakis DF, Heinzlmann M, Heldwein W, Wiebecke B, Loeschke K. Molecular screening of patients with long standing extensive ulcerative colitis: detection of p53 and Ki-ras mutations by single strand conformation polymorphism analysis and differential hybridisation in colonic lavage fluid. Gut 1999; 44:822–5.
   PubMed Web of Science ®Google Scholar
• Cawkwell L, Sutherland F, Murgatroyd H, Jarvis P, Gray S, Cross D, et al. Defective hMSH2/hMLH1 protein expression is seen infrequently in ulcerative colitis associated colorectal cancers. Gut 2000;46:367–9.
   PubMed Web of Science ®Google Scholar
• Noffsinger AE, Belli JM, Fogt F, Fischer J, Goldman H, Fenoglio-Preiser CM. A germline hMSH2 alteration is unrelated to colonic microsatellite instability in patients with ulcerative colitis. Hum Pathol 1999;30: 8–12.
   Google Scholar
• Linn SC, Morelli PJ, Edry I, Cottongim SE, Szabo C, Salzman AL. Transcriptional regulation of human inducible nitric oxide synthase gene in an intestinal epithelial cell line. Am J Physiol 1997;272:G1499–508.
   PubMedGoogle Scholar
• Singer II, Kawka DW, Scott S, Weidner JR, Mumford RA, Riehl TE, et al. Expression of inducible nitric oxide synthase and nitrotyrosine in colonic epithelium in inflammatory bowel disease. Gastroenterology 1996;111:871–85.
   PubMed Web of Science ®Google Scholar
• Lundberg JO, Hellstrom PM, Lundberg JM, Alving K. Greatly increased luminal nitric oxide in ulcerative colitis. Lancet 1994; 344:1673–4.
   PubMed Web of Science ®Google Scholar
• Kubes P. Inducible nitric oxide synthase: a little bit of good in all of us. Gut 2000;47:6–9.
   PubMed Web of Science ®Google Scholar
• Tamir S, Tannenbaum SR. The role of nitric oxide (NO) in the carcinogenic process. Biochim Biophys Acta 1996;1288:F31–6.
   PubMed Web of Science ®Google Scholar
• Evan GI, Vousden KH. Proliferation, cell cycle and apoptosis in cancer. Nature 2001;411:342–8.
   PubMed Web of Science ®Google Scholar
• Walworth NC. Cell-cycle checkpoint kinases: checking in on the cell cycle. Curr Opin Cell Biol 2000;12:697–704.
   PubMed Web of Science ®Google Scholar
• Schuler M, Green DR. Mechanisms of p53-dependent apoptosis. Biochem Soc Trans 2001;29:684–8.
   PubMed Web of Science ®Google Scholar
• Fleisher AS, Esteller M, Harpaz N, Leytin A, Rashid A, Xu Y, et al. Microsatellite instability in inflammatory bowel disease- associated neoplastic lesions is associated with hypermethylation and diminished expression of the DNA mismatch repair gene, hMLH1. Cancer Res 2000;60:4864–8.
   PubMed Web of Science ®Google Scholar