Abstract
We hypothesized that dietary hydrolyzable tannins would not act as digestibility reducing substances but would be excreted in the feces if the tannin were ingested by rats producing salivary proline-rich proteins (PRPs). To test that hypothesis we used two groups of Sprague–Dawley rats: tannin-naïve rats that were secreting basal levels of salivary PRPs and tannin-habituated rats that were secreting elevated levels of PRPs. The animals were fed for 10–18 d on diets containing 3% (w/w) purified hydrolyzable tannin [pentagalloyl glucose (PGG)] that was periodically spiked with chemically synthesized, radiolabeled 1,2,3,4,6-penta-O-galloyl-[U-14 C]-d-glucopyranose (1 μCi per gram diet). The PGG-habituated rats excreted three times more of the consumed 14 C in their feces than did the PGG-naïve rats (11.4% for PGG-habituated rats vs. 3.5% for PGG-naïve rats, P < 0.05). The addition of 3% PGG to the diet of the PGG-naïve rats had no significant effect on apparent dry matter or nitrogen digestibility (P > 0.05). However, dry matter digestibility and nitrogen digestibility were significantly decreased by PGG in the diets of the PGG-habituated rats (7 and 25%, P < 0.001, respectively). Production of PRPs increased the amount of PGG excreted intact in the feces but at the cost of diminishing apparent dry matter and nitrogen digestibility.
Similar content being viewed by others
REFERENCES
American Institute Of Nutrition. 1977. Report of the American Institute of Nutrition ad hoc committee on stand ards for nutritional studies. J. Nutr.107:1340–1348.
Austin, P. J., Suchar, L. A., Robbins, C. T., and Hagerman, A. E. 1989. Tannin-binding proteins in saliva of deer and their absence in saliva of sheep and cattle. J. Chem. Ecol. 15:1335–1347.
Bernays, E. A., Driver, C., and Bilgener, M. 1989. Herbivores and Plant Tannins, pp. 263–302, in M. Begon, A. H. Fitter, and E. D. Ford (eds.). Advances in Ecological Research, Vol. 19. Academic Press, New York.
Booth, A. N., Masri, M. S., Robbins, D. J., Emerson, O. H., Jones, F. T., and Deeds, F. 1959. The metabolic fate of gallic acid and related compounds. J. Biol. Chem.234:3014–3016.
Bravo, L., Abia, R., Eastwood, M. A., and Saura-Calixto, F. 1994. Degradation of polyphenols (catechin and tannic acid) in the rat intestinal tract. Effect on colonic fermentation and faecal output. Br.J.Nutr.71:933–946.
Chen, Y., Hagerman, A. E., and Minto, R. E. 2003. Preparation of 1, 2, 3, 4, 6-penta-O-galloyl-[U-14C-D-glucopyranose. J. Labelled Compd. Radiopharm.46:99–105.
Deplancke, B. and Gaskins, H. R. 2001. Microbial modulation of innate defense: Goblet cells and the intestinal mucus layer. Am.J.Clin.Nutr.73:1131S–1141S.
Feeney, P. 1968. Effect of oak leaf tannins on larval growth of the winter moth Operophtera brumata. J. Insect Physiol.14:805–817.
Glick, Z. and Joslyn, M. A. 1969. Effect of tannic acid and related compounds on the absorption and utilization of proteins in the rat. J. Nutr.100:516–520.
Hagerman, A., Zhao, Y., and Johanson, Y. 1997. Methods for determination of condensed and hydrolysable tannins, pp. 209–222, in F. Shahadi (ed.). Phytochemicals in Foods. American Chemical Society, Washington, DC.
Hagerman, A. E. and Butler, L. G. 1981. The specificity of proanthocyanidin-protein interactions. J. Biol. Chem.256:4494–4497.
Hagerman, A. E. and Butler, L. G. 1989. Choosing appropriate methods and stand ards for assaying tannin. J. Chem. Ecol.15:1795–1810.
Hagerman, A. E., Rice, M. E., and Ritchard, N. T. 1998. Mechanisms of protein precipitation for two tannins, pentagalloyl glucose and epicatechin16 (4→8)catechin (procyanidin). J. Agric. Food Chem.46:2590–2595.
Hagerman, A. E., Robbins, C. T., Weerasuriya, Y., Wilson, T. C., and Mcarthur, C. 1992. Tannin chemistry in relation to digestion. J. Range Manage.45:57–62.
Hanley, T. A., Robbins, C. T., Hagerman, A. E., and Mcarthur, C. 1992. Predicting digestible protein and digestible dry matter in tannin-containing forages consumed by ruminants. Ecology 73:537–541.
Haslam, E. 1989. Plant Polyphenols. Cambridge University Press, Cambridge, UK.
Horigome, T., Kumar, R., and Okamoto, K. 1988. Effects of condensed tannins prepared from leaves of fodder plants on digestive enzymes in vitro and in the intestine of rats. Br.J.Nutr. 60:275–285.
Iason, G. R.and Murray, A. H. 1996. The energy costs of ingestion of naturally occurring nontannin plant phenolics by sheep. Physiol. Zool. 69:532–546.
Illius, A. W. and Jessop, N. S. 1995. Modeling metabolic costs of allelochemical ingestion by foraging herbivores. J. Chem. Ecol. 21:693–719.
Jansman, A. J., Frohlich, A. A., and Marquardt, R. R. 1994. Production of proline-rich proteins by the parotid gland s of rats is enhanced by feeding diets containing tannins from faba beans(Vicia faba L.). J. Nutr. 124:249–258.
Jansman, A. J., Verstegen, M. W., Huisman, J., and Van Den Berg, J. W. 1995. Effects of hulls of faba beans (Vicia faba L.) with a low or high content of condensed tannins on the apparent ileal and fecal digestibility of nutrients and the excretion of endogenous protein in ileal digesta and feces of pigs. J. Anim. Sci. 73:118–127.
Kawabata, A., Kinoshita, M., Nishikawa, H., Kuroda, R., Nishida, M., Araki, H., Arizono, N., Oda, Y., and Kakehi, K. 2001. The protease-activated receptor-2 agonist induces gastric mucus secretion and mucosal cytoprotection. J. Clin. Invest. 107:1443–1450.
Lindroth, R. L. and Batzli, G. O. 1983. Detoxification of some naturally occurring phenolics by prairie voles: A rapid assay of glucuronidation metabolism. Biochem. Syst. Ecol. 11:405–409.
Long, L. H., Clement, M. V., and Halliwell, B. 2000. Artifacts in cell culture: Rapid generation of hydrogen peroxide on addition of (–)-epigallocatechin, (–)-epigallocatechin gallate, (+)-catechin, and quercetin to commonly used cell culture media. Biochem. Biophys. Res. Commun. 273:50–53.
Lowry, J. B., Mcsweeney, C. S., and Palmer, B. 1996. Changing perceptions of the effect of plant phenolics on nutrient supply in the ruminant. Aust. J. Agric. Res. 47:829–842.
Magne, C. and Larher, F. 1992. High sugar content of extracts interferes with colorimetric determi-nation of amino acids and free praline. Anal. Biochem. 200:115–118.
Mcarthur, C., Sanson, G. D., and Beal, A. M. 1995. Salivary proline-rich proteins in mammals: Roles in oral homeostasis and counteracting dietary tannin. J. Chem. Ecol. 21:663–689.
Mehansho, H., Asquith, T. M., Butler, L. G., Rogler, J., and Carlson, D. M. 1992. Tannin-mediated induction of proline-rich protein synthesis. J. Agric. Food Chem. 40:93–97.
Mehansho, H., Hagerman, A., Clements, S., Butler, L., Rogler, J., and Carlson, D. M. 1983. Modulation of proline-rich protein biosynthesis in rat parotid gland s by sorghums with high tannin levels. Proc. Nat. Acad. Sci. U. S. A. 80:3948–3952.
Meyer, M. W. and Richardson, C. 1993. The effects of chronic tannic acid intake on prairie vole(Microtus ochrogaster) reproduction. J. Chem. Ecol. 19:1577–1585.
Mitjavila, S., Lacombe, C., Carrera, G., and Derache, R. 1977. Tannic acid and oxidized tannic acid on the functional state of rat intestinal epithelium. J. Nutr. 107:2113–2121.
Mole, S., Rogler, J., and Butler, L. 1993. Growth reduction by dietary tannins: Different effects due to different tannins. Biochem. Syst. Ecol. 21:667–677.
Mole, S., Rogler, J., Morell, C. J., and Butler, L. G. 1990. Herbivore growth reduction by tannins: Use of Waldbauer ratio techniques and manipulation of salivary protein production to elucidate mechanisms of action. Biochem. Syst. Ecol. 18:183–197.
Mueller-Harvey, I. 2001. Analysis of hydrolysable tannins. Anim. Feed Sci. Technol. 91:3–20.
Murdiati, T. B., McSweeney, C. S., and Lowry, J. B. 1991. Complexing of toxic hydrolysable tannins of yellow-wood (Terminalia oblongata) and harendong (Clidemia hirta) with reactive substances: An approach to preventing toxicity. J. Appl. Toxicol. 11:333–338.
National Research Council. 1995. Nutrient Requirements of Laboratory Animals, 4th edn. rev. National Academy Press, Washington, DC.
Niho, N., Shibutani, M., Tamura, T., Toyoda, K., Uneyama, C., Takahashi, N., and Hirose, M. 2001. Subchronic toxicity study of gallic acid by oral administration in F344 rats. Food Chem. Toxicol. 39:1063–1070.
Ortiz, L. T., Alzueta, C., Trevino, J., and Castano, M. 1994. Effects of faba bean tannins on the growth and histological structure of the intestinal tract and liver of chicks and rats. Br. Poult. Sci. 35:743–754.
Robbins, C. T., Hagerman, A. E., Austin, P. J., Mcarthur, C., and Hanley, T. A. 1991. Variation in mammalian physiological responses to a condensed tannin and its ecological implications. J. Mammal. 72:480–486.
Robbins, C. T., Hanley, T. A., and Hagerman, A. 1987. Role of tannins in defending plants against ruminants: Reduction in dry matter digestion? Ecology 68:1606–1615.
Thomas, D. W., Samson, C., and Bergeron, J. 1988. Metabolic costs associated with the ingestion of plant phenolics by Microtus Pennsylvanicus. J. Mammal. 69:512–515.
Weatherburn, M. W. 1967. Phenol-hypochlorite reaction for determination of ammonia. Anal. Chem. 39:971–974.
Wilkinson, L. and Coward, M. 2000. SYSTAT® 10 Statistics 1. SPSS, Chicago, IL.
Zong, L., Inoue, M., Nose, M., Kojima, K., Sakaguchi, N., Isuzugawa, K., Takeda, T., and Ogihara, Y. 1999. Metabolic fate of gallic acid orally administered to rats. Biol. Pharm. Bull. 22:326–329.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Skopec, M.M., Hagerman, A.E. & Karasov, W.H. Do Salivary Proline-Rich Proteins Counteract Dietary Hydrolyzable Tannin in Laboratory Rats?. J Chem Ecol 30, 1679–1692 (2004). https://doi.org/10.1023/B:JOEC.0000042395.31307.be
Issue Date:
DOI: https://doi.org/10.1023/B:JOEC.0000042395.31307.be