Hostname: page-component-7c8c6479df-p566r Total loading time: 0 Render date: 2024-03-29T10:17:52.227Z Has data issue: false hasContentIssue false

Effects of galacto-oligosaccharide and bacterial status on mucin distribution in mucosa and on large intestine fermentation in rats

Published online by Cambridge University Press:  09 March 2007

J. C. Meslin
Affiliation:
Laboratoire de Nutrition et Sécurité Alimentaire, Centre de Recherches de Jouy, 78352 Jouy-en-Josas Cédex, France
C. Andrieux
Affiliation:
Laboratoire ď Ecologie et de Physiologie du Systéme Digestif INRA, Centre de Recherches de Jouy, 78352 Jouy-en-Josas Cédex, France
T. Sakata
Affiliation:
Ishinomaki Senshu University, Minamizakai Shinmito 1, Ishinomaki 986, Japan
P. Beaumatin
Affiliation:
Laboratoire de Nutrition et Sécurité Alimentaire, Centre de Recherches de Jouy, 78352 Jouy-en-Josas Cédex, France
M. Bensaada
Affiliation:
Laboratoire ď Ecologie et de Physiologie du Systéme Digestif INRA, Centre de Recherches de Jouy, 78352 Jouy-en-Josas Cédex, France
F. Popot
Affiliation:
Laboratoire ď Ecologie et de Physiologie du Systéme Digestif INRA, Centre de Recherches de Jouy, 78352 Jouy-en-Josas Cédex, France
O. Szylit
Affiliation:
Laboratoire ď Ecologie et de Physiologie du Systéme Digestif INRA, Centre de Recherches de Jouy, 78352 Jouy-en-Josas Cédex, France
M. Durand
Affiliation:
Laboratoire de Nutrition et Sécurité Alimentaire, Centre de Recherches de Jouy, 78352 Jouy-en-Josas Cédex, France
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The purpose of the present paper was to study the effects of a dietary undigestible carbohydrate and intestinal microflora on mucin distribution (neutral, acid, sulphonated), glycolytic activities: η-D-galactosidase (EC 3.2.1.23), N-acetyl-η-D-galactosaminidase ( Ec 3.2.1.43), N-acetyl-η-D-gluco-saminidase (EC 3.2.1.30), β-L-fucosidase (EC 3.2.1.51) and bacterial metabolism (gas production, short-chain fatty acids (SCFA) and lactic acid caecal concentration) in germ-free (GF), conventional (CV) and heteroxenic (HE) rats (GF rats associated with a human flora). Rats were fed on either a control diet or a diet containing 40 g trans-galactosylated oligosaccharide (TOS)/kg. In GF rats fed on the control diet caecal pH was almost neutral and glycolytic activities negligible. The number of mucus- containing cells increased from the caecum to the colon for the three types of mucin. TOS had no effect in the caecum but it modified mucin cell repartition in the colon. In CV and HE rats fed on the control diet caecal pH was similar (6.8), but caecal SCFA and lactic acid concentrations (μmol/g) and gas production (m1/24 h) were higher in CV (70, 5.9 and 2.3 respectively) than in HE rats (32, 4.6 and 0.4 respectively). In CV, as in HE rats, acid-mucin-containing cells increased from the caecum to the colon and glycolytic activities were similar. TOS reduced acid-mucin-containing cells in the caecum of CV rats by twofold but had no effect in either the caecum or the colon of HE rats. TOS strongly increased η- galactosidase activity and slightly modified the other glycolytic activities. Its effect on bacterial metabolites depended on bacterial status. However, comparison between CV and HE rats showed no evident relationship between the number of mucus-containing cells and measured bacterial metabolites. Differences between CV and HE rats might be due to bacterial microflora specificity. TOS had an intrinsic effect on mucus cell distribution in the colon of GF rats. In CV and HE rats the presence of the flora abolished this effect.

Type
Mineral Metabolism
Copyright
Copyright © The Nutrition Society 1993

References

Allen, A. (1981). Structure and function of gastrointestinal mucus. In Physiology of the Gastrointestinal Tract, pp. 617639 [Johnson, L. R., editor]. New York: Raven Press.Google Scholar
Andrieux, C., Lory, S., Dufour-Lescoat, C., de Baynast, R. & Szylit, O. (1991). Physiological effects of inulin in germ-free rats and in heteroxenic rats inoculated with a human flora. Food Hydrocolloids 5, 4956.Google Scholar
Andrieux, C. & Sacquet, E. (1986). Effects of amylomaize starch on mineral metabolism in the adult rat: role of the microflora. Journal of Nutrition 116, 991998.Google Scholar
Cassidy, M. M., Lightfoot, F. G., Grau, L. E., Story, J. A., Kritchevsky, D. & Vahouny, G. V. (1981). Effect of chronic intake of dietary fibers on the ultrastructural topography of rat jejunum and colon: a scanning electron microscope study. American Journal of Clinical Nutrition 34, 218228.Google Scholar
Combe, E., Demarne, Y., Gueguen, L., Ivorec-Szylit, O., Mesin, J. C. & Sacquet, E. (1976). Some aspects of the relationship between gastrointestinal flora and host nutrition. World Review of Nutrition and Dietetics 24, 157.Google Scholar
Debure, A., Colombel, J. F., Flourie, B., Rautureau, M. & Rambaud, J. C. (1989). Comparaison de I'implantation et de l'activité métabolique ďune flore féale de rat et ďune flore fécale humaine inoculée chez le rat axenique (Implantation and metabolic activity of rat and human faecal bacterial flora administered to germ-free rats). Gastrorntirologie Clinique et Biologique 13, 2531.Google Scholar
Filipe, I. (1979). Mucins in the human gastrointestinal epithelium: a review. Investigation in Cell Pathology 2, 195216.Google Scholar
Gibson, G. R., Cummings, J. H. & Macfarlane, G. T. (1988). Use of a three-stage continuous culture system to study the effect of mucin on dissimilatory sulfate reduction and methanogenesis by mixed populations of human gut bacteria. Applied and Environmental Microbiology 54, 27502755.CrossRefGoogle Scholar
Heneghan, J. B. (1979). Enterocyte kinetics, mucosal surface area and mucus in gnotobiotes. In Clinical and Experimental Gnotobiotics. Proceedings of the VI International Symposium on Gnotobiology, pp. 1927 [liedner, T. M., Heit, H., Niethammer, D. and Pflieger, H., editors]. Stuttgart: Gustav Fischer Verlag.Google Scholar
Heneghan, J. B., Gordon, H. A. & Miniats, O. P. (1979). Intestinal mucosal surface area and goblet cells in germfree and conventional piglets. In Clinical and Experimental Gnotobiotics. Proceedings of the VI International Symposium on Gnotobiology, pp. 109111 [Fliedner, T. M.Heit, H.Niethammer, D. and Pflieger, H., editors]. Stuttgart: Gustav Fischer Verlag.Google Scholar
Hill, R. R. & Cowley, H. M. (1990). The influence of colonizing micro-organisms on development of crypt architecture in the neonatal mouse colon. Actu Anatoniica 137, 137140.CrossRefGoogle ScholarPubMed
Hoskins, L. C. & Boulding, E. T. (1981). Mucus degradation in human colon ecosystems. Journal of Clinical Investigation 67, 163172.Google Scholar
Ishikawa, K., Satoh, Y., Oomori, Y., Yamano, M., Matsuda, M. & Ono, K. (1989). Influence of conventionalization on cecal wall structure of germfree Wistar rats: quantitative light and qualitative electron microscopic observations. Anatomy and Embryology 180, 191198.Google Scholar
Ishikawa, K., Satoh, Y., Tanaka, H. & Ono, K. (1986). Influence of conventionalization on small intestinal mucosa of germfree Wistar rats: quantitative light microscopic observations. Acta Anatomicu 128, 296302.Google Scholar
Ito, M., Deguchi, Y., Miyamori, A., Matsumoto, K., Kikuchi, H., Kobayashi, Y., Yajima, T. & Kan, T. (1990). Effects of administration of galacto-ohgosaccharides on the human fecal microflora, stool weight and abdominal sensation. Microbial Ecology in Health and Disease 3, 285292.Google Scholar
Le Coz, Y., Morel, M. T., Bousseboua, H., Dufour, C. & Szylit, O. (1989). Mise au pointďune chambre. respiratoire connectée sur isolateur pour la mesure in vivo des gaz de fermentation chez I'animal gnotoxenique (Development of a respiratory chamber and its connection with an isolator: a method to measure the in vivo production of fermentation gas by gnotobiotic animals). Science et Techniques des Animaux de Laboratoire 14, 3539.Google Scholar
Loesche, W. J. (1968). Accumulation of endogenous protein in the caecum of the germfree rat. Proceedings of the Society for Experimental Biology and Medicine 129, 380384.Google Scholar
McManus, J. F. A. (1946). Histological and histochemical use of periodic acid. Stain Technology 23, 99108.Google Scholar
Mallett, A. K., Bearne, C. A., Rowland, I. R., Farthing, M. J. G., Cole, C. B. & Fuller, R. (1987). The use of rats associated with a human faecal flora as a model for studying the effects of diet on the human gut microflora. Journal of Applied Bacteriology 63, 3945.Google Scholar
Moré, J., Fioramonti, F., Benazet, F. & Bueno, L. (1987). Histochemical characterization of glycoproteins present in jejunal and colonic goblet cells of pigs on different diets. A biopsy study using chemical methods and peroxidase-labelled lectins. Histochemistry 87, 189194.Google Scholar
Mowry, R. W. & Winkler, C. H. (1956). The coloration of acid carbohydrate of bacteria and fungi in the tissue sections with special reference to capsules of Cryptococcus neoformis, Pneumocorci and Staphylococci. American Journal of Pathology 32, 628629.Google Scholar
Rémésy, C. & Demignt, C. (1976). Partition and absorption of volatile fatty acids in the alimentary canal of the rat. Annales de Recherches VPthrinaires 7, 3955.Google ScholarPubMed
Rhodes, J. M. (1989). Colonic mucus and mucosal glycoproteins: the key to colitis and cancer? Gut 30, 16601666.Google Scholar
Rhodes, J. M., Gallimore, R., Elias, E.. Allan, R. N. & Kennedy, J. F. (1985 a). Faecal mucus degrading glycosidases in ulcerative colitis and Crohn's disease. Gut 26, 761765.Google Scholar
Rhodes, J. M., Gallimore, R., Elias, E. & Kennedy, J. F. (1985 b). Faecal sulphatase in health and in inflammatory bowel disease. Gut 26, 466469.CrossRefGoogle ScholarPubMed
Sakata, T. & Von Engelhardt, W. (1981 a). Influence of short-chain fatty acids and osmolality on mucin release in the rat colon. Cell and Tissue Research 219, 371377.Google Scholar
Sakata, T. & Von Engelhardt, W. (1981 b). Luminal mucin in the large intestine of mice, rats and guinea pigs. Cell and Tissue Research 219, 629635.Google Scholar
Salyers, A. A., Vercellotti, J. R., West, S. E. H. & Wilkins, T. D. (1977). Fermentation of mucus and plant polysaccharides by strains of Bacteroides from the human colon. Applied Environmental Microbiology 33, 319322.Google Scholar
Schneeman, B. O., Rechter, B. D. &Jacobs, L. R. (1982). Response to dietary wheat bran in the exocrine pancreas and intestine of rats. Journal of Nutrition 112, 283286.Google Scholar
Smith, A. C. & Podolsky, D. K. (1986). Colonic mucin glycoproteins in health and disease. Clinics in Gastroenterology 15, 815837.Google Scholar
Spicer, S. S. (1965). Diamine methods for differentiating mucosubstances histochemically. Journal of Histochemistry and Cytochemistry 13, 211231.Google Scholar
Sprinz, H., Kundel, D. W., Dammin, G. J., Horowitz, R. E., Scheiner, H. & Formal, S. B. (1961). The response of the germfree guinea pig to oral bacterial challenge with Escherichia coli and Shigella Jlexneri. American Journal of Pathology 39, 681695.Google Scholar
Staley, T. E., Corley, L. D. & Jones, E. W. (1970). Early pathogenesis of colitis in neonatal pigs monocontaminated with Esrherichiu coli. Fine structural changes in the colonic epithelium. American Journal of Digestive Diseases 15, 923935.Google Scholar
Szylit, O., Dabard, J., Durand, M., Dumay, C., Bensaada, M. & Raibaud, P. (1988). Production of volatile fatty acids as a result of bacterial interactions in the cecum of gnotobiotic rats and chickens fed a lactose-containing diet. Reproducrion, Nutrition, Dveloepement 28, 14551464.Google Scholar
Tanaka, R., Takayama, H., Morotomi, M., Kuroschima, T., Ueyama, S., Matsumoto, K., Kuroda, A. & Mutai, M. (1983). Effects of administration of TOS and Bifidobacterium breve 4006 on the human fecal flora. Bijidobacteria Microflora 2, 1724.CrossRefGoogle Scholar
Vahouny, G. W., Le, T., Satchithanandam, S. & Cassidy, M. M. (1985). Stimulation of intestinal cytokinetics and mucin turnover in rats fed wheat bran or cellulose. American Journal of Clinical Nutrition 41, 895900.Google Scholar