Journal of Cell Science, Vol 107, Issue 12 3569-3577, Copyright © 1994 by Company of Biologists

JOURNAL ARTICLES

Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis

PA Hall, PJ Coates, B Ansari and D Hopwood
Department of Pathology, University of Dundee, UK.

The regulation of cell number in adult tissues is determined by the balance of cell production and cell loss. In the gastrointestinal tract, where there are well defined zones of proliferation and migration of both epithelial cells and associated fibroblasts, it is widely held that cell loss occurs by shedding into the gut lumen. Since the evidence for this is not compelling, we investigated the distribution and amount of apoptosis in the normal mammalian gut. In the stomach, small intestine and colon of rodents and man, there is a small number of apoptotic bodies in the epithelium and in the immediate sub-epithelial connective tissue. Engulfment by adjacent epithelial cells and sub-epithelial macrophages accounts for the removal of apoptotic bodies. Apoptotic bodies are not randomly distributed but are found towards the distal end of the known cellular migration routes of both epithelial and mesenchymal cells. Furthermore, consideration of the absolute numbers of apoptotic bodies, their rapid clearance and the dimensions of the small intestinal villi and colonic crypts indicates that the cell loss in the normal murine intestine can largely be explained on the basis of the observed apoptosis. Despite being inconspicuous in histological material, apoptosis probably accounts for the bulk of cell loss in the gut and is a central feature of the regulation of cell number in adult tissues.
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				A. Danilkovitch, S. Donley, A. Skeel, and E. J. Leonard Two Independent Signaling Pathways Mediate the Antiapoptotic Action of Macrophage-Stimulating Protein on Epithelial Cells Mol. Cell. Biol., March 15, 2000; 20(6): 2218 - 2227. [Abstract] [Full Text]

				D. A. Swartz-Basile, D. C. Rubin, and M. S. Levin Vitamin A Status Modulates Intestinal Adaptation After Partial Small Bowel Resection JPEN J Parenter Enteral Nutr, March 1, 2000; 24(2): 81 - 88. [Abstract] [PDF]

				C. Bai, B. Connolly, M. L. Metzker, C. A. Hilliard, X. Liu, V. Sandig, A. Soderman, S. M. Galloway, Q. Liu, C. P. Austin, et al. Overexpression of M68/DcR3 in human gastrointestinal tract tumors independent of gene amplification and its location in a four-gene cluster PNAS, February 1, 2000; 97(3): 1230 - 1235. [Abstract] [Full Text] [PDF]

				F. Sanvito, F. Vivoli, S. Gambini, G. Santambrogio, M. Catena, E. Viale, F. Veglia, A. Donadini, S. Biffo, and P. C. Marchisio Expression of a Highly Conserved Protein, p27BBP, during the Progression of Human Colorectal Cancer Cancer Res., February 1, 2000; 60(3): 510 - 516. [Abstract] [Full Text]

				T. Stappenbeck and J. Gordon Rac1 mutations produce aberrant epithelial differentiation in the developing and adult mouse small intestine Development, January 6, 2000; 127(12): 2629 - 2642. [Abstract] [PDF]

				K. Sonoyama, S. Rutatip, and T. Kasai Gene expression of activin, activin receptors, and follistatin in intestinal epithelial cells Am J Physiol Gastrointest Liver Physiol, January 1, 2000; 278(1): G89 - G97. [Abstract] [Full Text] [PDF]

				J J Keller, G J A Offerhaus, M Polak, S N Goodman, M L Zahurak, L M Hylind, S R Hamilton, and F M Giardiello Rectal epithelial apoptosis in familial adenomatous polyposis patients treated with sulindac Gut, December 1, 1999; 45(6): 822 - 828. [Abstract] [Full Text] [PDF]

				M. Campbell-Thompson, G. Y. Lauwers, K. K. Reyher, J. Cromwell, and K. T. Shiverick 17{beta}-Estradiol Modulates Gastroduodenal Preneoplastic Alterations in Rats Exposed to the Carcinogen N-Methyl-N'-Nitro-Nitrosoguanidine Endocrinology, October 1, 1999; 140(10): 4886 - 4894. [Abstract] [Full Text]

				M. C. Willingham Cytochemical Methods for the Detection of Apoptosis J. Histochem. Cytochem., September 1, 1999; 47(9): 1101 - 1110. [Abstract] [Full Text]

				C. E. Shin, R. A. Falcone Jr., C. J. Kemp, C. R. Erwin, D. A. Litvak, B. M. Evers, and B. W. Warner Intestinal adaptation and enterocyte apoptosis following small bowel resection is p53 independent Am J Physiol Gastrointest Liver Physiol, September 1, 1999; 277(3): G717 - G724. [Abstract] [Full Text] [PDF]

				D. W. Powell, R. C. Mifflin, J. D. Valentich, S. E. Crowe, J. I. Saada, and A. B. West Myofibroblasts. II. Intestinal subepithelial myofibroblasts Am J Physiol Cell Physiol, August 1, 1999; 277(2): C183 - C201. [Abstract] [Full Text] [PDF]

				Y.-Y. Fan, J. Zhang, R. Barhoumi, R. C. Burghardt, N. D. Turner, J. R. Lupton, and R. S. Chapkin Antagonism of CD95 signaling blocks butyrate induction of apoptosis in young adult mouse colonic cells Am J Physiol Cell Physiol, August 1, 1999; 277(2): C310 - C319. [Abstract] [Full Text] [PDF]

				D. W. Powell, R. C. Mifflin, J. D. Valentich, S. E. Crowe, J. I. Saada, and A. B. West Myofibroblasts. I. Paracrine cells important in health and disease Am J Physiol Cell Physiol, July 1, 1999; 277(1): C1 - C19. [Abstract] [Full Text] [PDF]

				F. A. Sinicrope, J. Hart, H.-A. Hsu, M. Lemoine, F. Michelassi, and L. C. Stephens Apoptotic and Mitotic Indices Predict Survival Rates in Lymph Node-negative Colon Carcinomas Clin. Cancer Res., July 1, 1999; 5(7): 1793 - 1804. [Abstract] [Full Text] [PDF]

				N. R. Murray, L. A. Davidson, R. S. Chapkin, W. Clay Gustafson, D. G. Schattenberg, and A. P. Fields Overexpression of Protein Kinase C {beta}II Induces Colonic Hyperproliferation and Increased Sensitivity to Colon Carcinogenesis J. Cell Biol., May 17, 1999; 145(4): 699 - 711. [Abstract] [Full Text] [PDF]

				J. K. Crane, S. Majumdar, and D. F. Pickhardt III Host Cell Death due to Enteropathogenic Escherichia coli Has Features of Apoptosis Infect. Immun., May 1, 1999; 67(5): 2575 - 2584. [Abstract] [Full Text] [PDF]

				M.-L. Kuo, S.-G. Shiah, C.-J. Wang, and S.-E. Chuang Suppression of Apoptosis by Bcl-2 to Enhance Benzene Metabolites-Induced Oxidative DNA Damage and Mutagenesis: A Possible Mechanism of Carcinogenesis Mol. Pharmacol., May 1, 1999; 55(5): 894 - 901. [Abstract] [Full Text]

				K Kohda, K Tanaka, Y Aiba, M Yasuda, T Miwa, and Y Koga Role of apoptosis induced by Helicobacter pylori infection in the development of duodenal ulcer Gut, April 1, 1999; 44(4): 456 - 462. [Abstract] [Full Text] [PDF]

				D. Pinto, S. Robine, F. Jaisser, F. E. Marjou, and D. Louvard Regulatory Sequences of the Mouse Villin Gene That Efficiently Drive Transgenic Expression in Immature and Differentiated Epithelial Cells of Small and Large Intestines J. Biol. Chem., March 5, 1999; 274(10): 6476 - 6482. [Abstract] [Full Text] [PDF]

				C. M. Coopersmith, D. O'Donnell, and J. I. Gordon Bcl-2 inhibits ischemia-reperfusion-induced apoptosis in the intestinal epithelium of transgenic mice Am J Physiol Gastrointest Liver Physiol, March 1, 1999; 276(3): G677 - G686. [Abstract] [Full Text] [PDF]

				T. Kawamori, R. Lubet, V. E. Steele, G. J. Kelloff, R. B. Kaskey, and C. V. Rao Chemopreventive Effect of Curcumin, a Naturally Occurring Anti-Inflammatory Agent, during the Promotion/Progression Stages of Colon Cancer Cancer Res., February 1, 1999; 59(3): 597 - 601. [Abstract] [Full Text] [PDF]

				E. Slorach, F. Campbell, and J. Dorin A mouse model of intestinal stem cell function and regeneration J. Cell Sci., January 9, 1999; 112(18): 3029 - 3038. [Abstract] [PDF]