Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-24T09:30:20.691Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of caecal microflora and of two dietary protein levels on the adaptation of the exocrine pancreas: comparative study in germ-free and conventional rats

Published online by Cambridge University Press:  09 March 2007

Evelyne F. Lhoste ,
Isabelle Catala ,
Michèle Fiszlewicz ,
A. M. Gueugneau ,
Fran¸oise Popot ,
Pierre Vaissade ,
Tristan Corring  and
Odette Szylit
Evelyne F. Lhoste
Affiliation:
1Laboratoire d'Ecologie et de Physiologie du Système Digestif, INRA, Domaine de Vilvert, F-78350, Jouy-en-Josas, France
Isabelle Catala
Affiliation:
1Laboratoire d'Ecologie et de Physiologie du Système Digestif, INRA, Domaine de Vilvert, F-78350, Jouy-en-Josas, France
Michèle Fiszlewicz
Affiliation:
1Laboratoire d'Ecologie et de Physiologie du Système Digestif, INRA, Domaine de Vilvert, F-78350, Jouy-en-Josas, France
A. M. Gueugneau
Affiliation:
1Laboratoire d'Ecologie et de Physiologie du Système Digestif, INRA, Domaine de Vilvert, F-78350, Jouy-en-Josas, France
Fran¸oise Popot
Affiliation:
1Laboratoire d'Ecologie et de Physiologie du Système Digestif, INRA, Domaine de Vilvert, F-78350, Jouy-en-Josas, France
Pierre Vaissade
Affiliation:
1Laboratoire d'Ecologie et de Physiologie du Système Digestif, INRA, Domaine de Vilvert, F-78350, Jouy-en-Josas, France
Tristan Corring
Affiliation:
1Laboratoire d'Ecologie et de Physiologie du Système Digestif, INRA, Domaine de Vilvert, F-78350, Jouy-en-Josas, France
Odette Szylit
Affiliation:
1Laboratoire d'Ecologie et de Physiologie du Système Digestif, INRA, Domaine de Vilvert, F-78350, Jouy-en-Josas, 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.

Dietary proteins are degraded by both endogenous enzymes and the caecal microflora. In conventional rats the enzyme content of the pancreas depends on the amount of dietary protein. The influence of the caecal microflora on this process is unknown. We report here the effect of the caecal microflora on pancreatic enzymes (proteases, amylase (EC 3.2.1.l), lipase (EC 3.1.1.3)) and on colonic metabolites (NH3, urea, short-chain fatty acids). Germ-free and conventional male Fischer rats were fed for 3 weeks with a diet containing 220 or 450 g protein/kg provided as a mixture of fish concentrate and soyabean isolate. The excretion of NH3, and the pH were specifically increased by the high-protein diet in the germ-free rats. The higher production of isobutyrate, valerate and isovalerate in conventional rats fed on the high-protein diet reflected a high bacterial proteolytic activity since these short-chain fatty acids are specific indicators of this activity. The microflora hydrolysed urea to NH3 and maintained the pH at neutrality whatever the amount of protein in the diet since there were changes in germ-free rats but not in conventional ones. In germ-free rats, amylase, trypsin (EC 3.4.21.4), elastase (EC 3.4.21.36) and carboxypeptidase A (EC 3.4.17.1) specific activities were significantly lower than in conventional rats. The adaptation of the pancreas to the 450 g protein/kg diet was not impaired by the bacterial status except for the specific activity of chymotrypsin (EC 3.4.21.1) which was more increased by this diet in germ-free than in conventional rats. Moreover, the specific activity of lipase increased only in conventional rats fed on the 450g protein/kg diet. In conclusion, we observed a relationship between the enzyme content of the pancreas and the presence or absence of the caecal microflora suggesting that bacterial fermentation influences pancreatic function.

Keywords

Pancreatic enzymesCaecal fermentationGerm-free rat
Type
caecal microflora and pancreatic function
Information
British Journal of Nutrition , Volume 75 , Issue 3 , March 1996 , pp. 433 - 444
Copyright
Copyright © The Nutrition Society 1996

References

Bieth, J., Metais, P. & Warter, J. (1966). Etude des protéases pancréatiques I. Dosage de la trypsine par la benzoylarginine-P-nitroanilide et ses applications. (Study of pancreatic proteases. The assay of trypsin by benzoyl-P-nitroanilide and its applications). Annales Biologie Clinique 24, 787–803.Google Scholar
Bieth, J., Metais, P. & Warter, J. (1968). Etude des protéases pancréatiques II. Dosage de la chymotrypsine par la succinyl-phénylalanine-P-nitroanilide et ses applications. (Study of pancreatic proteases. The assay of chymotrypsin by succinyl-phenylalanine-P-nitroanilide and its applications). Annales Biologie Clinique 26,143–158.Google Scholar
Borgström, B., Dahlqvist, A., Gustafsson, B. E., Lundh, G. & Malmquist, J. (1959). Trypsin, invertase and amylase contents of faeces of germfree rats. Proceedings of the Sociery for Experimental Biology and Medicine 102, 154–155.CrossRefGoogle ScholarPubMed
Brannon, P. M. (1990). Adaptation of the exocrine pancreas to diet. Annual Review of Nutrition 10, 85–105.CrossRefGoogle ScholarPubMed
Coates, M. E. (1968). Nutrition and metabolism. In The Germ-free Animal in Research, pp. 161–179 [Coates, M. E., Gordon, H. A. & Wostmann, B. S., editors]. New York: Academic Press.Google Scholar
Coates, M. E. (1973). Gnotobiotic animals in nutrition research. Proceedings of the Nutrition Society 32, 53–58.CrossRefGoogle ScholarPubMed
Combe, E., Demarne, Y., Gueguen, L., Ivorec-Szylit, O., Meslin, J. C. & Sacquet, E. (1976). Some aspects of the relationships between gastro-intestinal flora and host nutrition. World Review of Nutrition and Dietetics 24, 1–57.CrossRefGoogle Scholar
Combe, E., Penot, E., Charlier, H. & Sacquet, E. (1965). Métabolisme du rat “gem-free”. Teneurs des contenus digestifs en certains composés azotés, en sodium et en potassium. Teneurs de quelques tissus en acides nucléiques (Metabolism of the germ-free rat. Some nitrogenous compounds, sodium and potassium contents of the intestine. The nuclei acid content of some tissues). Annales de Biologie Animale, Biochimie, Biophysique 5, 189–206.CrossRefGoogle Scholar
Combe, E., Pion, R. & Sacquet, E. (1970). Influence de la nature et du taux des protéines alimentaires sur la composition en acides aminés du contenu du caecum du rat axénique (Influence of the nature and amount of dietary proteins on the amino acid coiltents of the caecum of axenic rats). Annales de Biologie Animale, Biochimie, Biophysique 10, 697–702.CrossRefGoogle Scholar
Committee on Diet and Health (1989). Dier and Health, Implications of Reducing Chronic Diseases Risk. Washington, DC: National Academy Press.Google Scholar
Corring, T., Juste, C. & Lhoste, E. F. (1989).Nutritional regulation of pancreatic and biliary Secretions. Nutrition Research Reviews 2, 161–180.CrossRefGoogle ScholarPubMed
Corring, T., Moreau, C. & Ducluzeau, R. (1979). Comparative apparent digestibility of casein in holoxenic, axenic, and Clostridium bifermentans monoassociated rats. American Journal of Clinical Nutrition 32, 1231–1237.CrossRefGoogle ScholarPubMed
Cuber, J. C., Vilas, F., Charles, N., Bernard, C. & Chayvialle, J. A. (1989). Bombesin and nutrients stimulate release of CCK through distinct pathways in the rat. American Journal of Physiology 256, G989–G996.Google ScholarPubMed
Cummings, J. H. & Bingham, S. A. (1987). Dietary fibre, fermentation and large bowel cancer. Cancer Surveys 6, 601–614.Google ScholarPubMed
Demigné, C. & Remesy, C. (1979). Urea cycling and ammonia absorption in vivo in the digestive tract of the rat. Annales de Biologie Animale, Biochimie, Biophysique 19, 929–935.CrossRefGoogle Scholar
Dropsy, G. & Boy, J. (1961). Détermination de l'ammoniémie, méthode automatique par dialyse (Assay of ammoniaemia: an automatic method using dialysis). Annales Biologie Clinique Paris 19, 313–317.Google Scholar
Dufour, C. (1989). Impacts de la microflore digestive sur les effets nutritionnels et physiologiques des fibres alimentaires chez le rat hétéroxénique à flore humaine (Influence of a human microflora on the effects of dietary fibres on nutritional and physiological parameters in the heteroxenic rat). Thesis, Institut National Agronomique, Paris-Grignon.Google Scholar
Genell, S., Gustafsson, B. E. & Ohlsson, K. (1976).Quantification of active pancreatic endopeptidases in the intestinal contents of germfree and conventional rats. Scandinavian Journal of Gastroenterology 11, 757–762.CrossRefGoogle Scholar
Goodlad, R. A., Ratcliffe, B., Fordham, J. P., Ghatei, M. A., Domin, J., Bloom, S. R. & Wright, N. A. (1989). Plasma enteroglucagon, gastrin and peptide YY in conventional and germ-free rats refed with a fibre-free or fibre-supplemented diet. Quarterly Journal of Experimental Physiology 74, 437–442.CrossRefGoogle ScholarPubMed
Le Huérou-Luron, I., Lhoste, E., Wicker-Planquart, C., Dakka, N., Toullec, R., Corring, T., Guilloteau, P. & Puigserver, A. (1993). Molecular aspects of enzyme synthesis in the exocrine pancreas with emphasis on development and nutritional regulation. Proceedings of the Nutrition Society 52, 301–313.CrossRefGoogle ScholarPubMed
Lepkovsky, S., Furuta, F., Ozone, K. & Koike, T. (1966). The proteases, amylase and lipase of the pancreas and intestinal contents of germ-free and conventional rats. British Journal of Nutrition 20, 257–261.CrossRefGoogle ScholarPubMed
Levenson, S. M., Crowley, L. V., Horowitz, R. E. & Malm, O. J. (1959). The metabolism of carbon-labeled urea in the germfree rat. Journal of Biological Chemistry 234, 2061–2062.CrossRefGoogle Scholar
Lhoste, E. F., Fiszlewicz, M., Gueugneau, A. M., Wicker-Planquart, C., Puigserver, A. & Corring, T. (1993). Effects of dietary proteins on some pancreatic mRNAs encoding digestive enzymes in the pig. Journal of Nutritional Biochemistry 4, 143–152.CrossRefGoogle Scholar
Lin, H. C. & Visek, W. J. (1991). Large intestinal pH and ammonia in rats: dietary fat and protein interactions. Journal of Nutrition 121, 832–843.CrossRefGoogle ScholarPubMed
Lupton, J. R. & Marchand, L. J. (1989). Independent effects of fiber and protein on colonic luminal ammonia concentration. Journal of Nutrition 119, 235–241.CrossRefGoogle ScholarPubMed
Marsh, W. H., Fingerhut, B. & Miller, H. (1965). Automated and manual direct methods for the determination of blood urea. Clinical Chemistry 11, 624–627.CrossRefGoogle ScholarPubMed
McBurney, M. I., Van Soest, P. J. & Jeraci, J. L. (1987). Colinic carcinogenesis: the microbial feast or famine mechanism. Nutrition and Cancer 10, 23–28.CrossRefGoogle ScholarPubMed
McNeil, N. I. (1988). Nutritional implications of human and mammalian large intestinal function. World Review of Nutrition and Dietetics 56, 1–42.CrossRefGoogle ScholarPubMed
Meslin, J. C., Andrieux, C., Sakata, T., Beaumatin, P., Bensaada, M., Popot, F., Szylit, O. & Durand, M. (1993). Effects of galacto-oligosaccharide and bacterial status on mucin distribution in mucosa and on large intestine fermentation in rats. British Journal of Nutrition 69, 903–912.CrossRefGoogle ScholarPubMed
Ohbo, M., Katoh, K. & Sasaki, Y. (1989). Effects of short-, medium-, and long-chain fatty acids on amylase release from pancreatic segments of rats. Australian Journal of Applied Sciences 2, 193–194.Google Scholar
Ottensheim, O. M. & Bartley, D. A. (1971). Improved gas chromatography separation of free acids C2-C5 in dilute solution. Analytical Chemistry 43, 952–955.CrossRefGoogle Scholar
Reddy, B. S., Pleasants, J. R. & Wostmann, B. S. (1969). Pancreatic enzymes in germfree and conventional rats fed chemically defined, water soluble diet free from natural substances. Journal of Nutrition 97, 327–334.CrossRefGoogle Scholar
Rérat, A. (1978). Digestion and absorption of carbohydrates and nitrogenous matters in the hindgut of the omnivorous nonruminant animal. Journal of Animal Science 46, 1808–1837.CrossRefGoogle ScholarPubMed
Salter, D. N. (1973). Influence of gut micro-organisms on utilization of dietary protein. Proceedings of the Nutrition Society 32, 65–71.CrossRefGoogle ScholarPubMed
Visek, W. J. (1978). The mode of growth promotion by antibiotics. Journal of Animal Science 46, 1147–1169.CrossRefGoogle Scholar
Von Juhr, N. C. (1980). Intestinale Enzymeaktivität bei keimfreien und konventionellen Ratten und Mäusen (Intestinal enzyme activities in germ-free and conventional rats and mice). Zeitschrift fuer Versuchstierkunde 22,197–203.Google Scholar
Wiech, N. L., Hamilton, J. G. & Miller, O. N. (1967). Absorption and metabolism of dietary triglycerides in germfree and conventional rats. Journal of Nutrition 93, 324–330.CrossRefGoogle ScholarPubMed
Yamasaki, M., Brown, J. R., Cox, D. J., Greenshields, R. N., Wade, R. D. & Neurath, H. (1963). Procarboxypeptidase A-S6. Further studies of its isolation and properties. Biochemistry 2, 859–866.CrossRefGoogle Scholar
Yanagida, K., Takahashi, M., Honma, C., Kametaka, M. & Yamanaka, M. (1985). Ammonia in intestinal contents from germfree rats. Experimetal Animals 34, 463–465.CrossRefGoogle ScholarPubMed
Zarling, E. J. & Ruchim, M. A. (1987). Protein origin of the volatile fatty acids isobutyrate and isovalerate in human stool. Journal of Laboratory and Clinical Medicine 109, 566–570.Google ScholarPubMed