Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-23T20:30:22.976Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of plant and bacterial myrosinase activity on the metabolic fate of glucosinolates in gnotobiotic rats

Published online by Cambridge University Press:  09 March 2007

Gabrielle Rouzaud ,
Sylvie Rabot ,
Brian Ratcliffe  and
Alan J. Duncan
Gabrielle Rouzaud
Affiliation:
Macaulay Institute, Craigiebuckler, Aberdeen AB15 8QH, UK
Sylvie Rabot
Affiliation:
INRA, Unité d'Ecologie et de Physiologie du Système Digestif, Centre de Recherche de Jouy en Josas, 78 352 Jouy en Josas, France
Brian Ratcliffe
Affiliation:
Robert Gordon University, Queen's Road, Aberdeen AB15 4PH, UK
Alan J. Duncan*
Affiliation:
Macaulay Institute, Craigiebuckler, Aberdeen AB15 8QH, UK
*
*Corresponding author: Dr Alan J. Duncan, fax +44 1224 311556, email [email protected]
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 breakdown of glucosinolates, a group of thioglucoside compounds found in cruciferous plants, is catalysed by dietary or microbial myrosinase. This hydrolysis releases a range of breakdown products among which are the isothiocyanates, which have been implicated in the cancer-protective effects of cruciferous vegetables. The respective involvement of plant myrosinase and gut bacterial myrosinase in the conversion, in vivo, of glucosinolates into isothiocyanates was investigated in sixteen Fischer 344 rats. Glucosinolate hydrolysis in gnotobiotic rats harbouring a whole human faecal flora (Flora+) was compared with that in germ-free rats (Flora−). Rats were offered a diet where plant myrosinase was either active (Myro+) or inactive (Myro−). The conversion of prop-2-enyl glucosinolate and benzyl glucosinolate to their related isothiocyanates, allyl isothiocyanate and benzyl isothiocyanate, was estimated using urinary mercapturic acids, which are endproducts of isothiocyanate metabolism. The highest excretion of urinary mercapturic acids was found when only plant myrosinase was active (Flora−, Myro+ treatment). Lower excretion was observed when both plant and microbial myrosinases were active (Flora+, Myro+ treatment). Excretion of urinary mercapturic acids when only microbial myrosinase was active (Flora+, Myro− treatment) was low and comparable with the levels in the absence of myrosinase (Flora−, Myro− treatment). No intact glucosinolates were detected in the faeces of rats from the Flora+ treatments confirming the strong capacity of the microflora to break down glucosinolates. The results confirm that plant myrosinase can catalyse substantial release of isothiocyanates in vivo. The results also suggest that the human microflora may, in some circumstances, reduce the proportion of isothiocyanates available for intestinal absorption.

Keywords

GlucosinolatesIsothiocyanatesExcretionMyrosinaseHuman colonic microflora
Type
Research Article
Information
British Journal of Nutrition , Volume 90 , Issue 2 , August 2003 , pp. 395 - 404
Copyright
Copyright © The Nutrition Society 2003

References

Beecher, CWW (1994) Cancer preventive properties of varieties of Brassica oleracea: a review. Am J Clin Nutr 59, Suppl., 1166S–1170S.CrossRefGoogle ScholarPubMed
Coates, ME (1968) The Germ-free Animal in Research. London: Academic Press.Google Scholar
Combourieu, B, Elfoul, L, Delort, AM & Rabot, S (2001) Identification of new derivatives of sinigrin and glucotropaeolin produced by the human digestive microflora using (1)H NMR spectroscopy analysis of in vitro incubations. Drug Metab Dispos 29, 1440–1445.Google ScholarPubMed
Conaway, CC, Yang, YM & Chung, FL (2002) Isothiocyanates as cancer chemopreventive agents: Their biological activities and metabolism in rodents and humans. Curr Drug Metab 3, 233–255.CrossRefGoogle Scholar
Debure, A, Colombel, JF, Flourie, B, Rautureau, M & Rambaud, JC (1989) Comparaison de l'implantation et de l'activité métabolique d'une flore fécale de rat et d'une flore fécale humaine, inoculée chez le rat axénique (Comparison of the composition and metabolic activities of a rat and a human faecal flora inoculated into germ-free rats). Gastroenterol Clin Biol 13, 25–31.Google Scholar
Dekker, M, Verkerk, R & Jongen, WMF (2000) Predictive modelling of health aspects in the food production chain: a case study on glucosinolates in cabbage. Trends Food Sci Technol 11, 174–181.CrossRefGoogle Scholar
Duncan, AJ, Rabot, S & Nugon-Baudon, L (1995) Urinary mercapturic acids as markers for the estimation of isothiocyanate release from parent glucosinolates in the digestive tract of rats. In Proceedings of the 9th International Rapeseed Congress, Rapeseed Today and Tomorrow, pp. 928–929 [Murphy, D, editor] Cambridge, UK: Royal Society of Chemistry.Google Scholar
Duncan, AJ, Rabot, S & Nugon-Baudon, L (1997) Urinary mercapturic acids as markers for the determination of isothiocyanate release from glucosinolates in rats fed a cauliflower diet. J Sci Food Agric 73, 214–220.3.0.CO;2-#>CrossRefGoogle Scholar
Elfoul, L (1999) Bioconversion de la Sinigrine, Microconstitutant des Légumes Crucifères, par une Souche Colique Humaine de Bacteroides Thetaiotaomicron (Bioconversion of Sinigrin, a Microconstituent of Brassica Vegetables, by a Human Colonic Strain of Bacteroides Thetaiotatomicron). PhD thesis. Orsay, France: Université de Paris-SudGoogle Scholar
Elfoul, L, Rabot, S, Khelifa, N, Quinsac, A, Duguay, A & Rimbault, A (2001) Formation of allyl isothiocyanate from sinigrin in the digestive tract of rats monoassociated with a human colonic strain of Bacteroides thetaiotaomicron. FEMS Microbiol Lett 197, 99–103.CrossRefGoogle ScholarPubMed
Fenwick, GR, Heaney, RK & Mullin, WJ (1983) Glucosinolates and their breakdown products in food and food plants. CRC Critical Rev Food Sci Nutr 18, 123–201.CrossRefGoogle ScholarPubMed
Getahun, SM & Chung, F-L (1999) Conversion of glucosinolates to isothiocyanates in humans after ingestion of cooked watercress. Cancer Epidemiol Biomarkers Prev 8, 447–451.Google ScholarPubMed
Hecht, SS (1999) Chemoprevention of cancer by isothiocyanates, modifiers of carcinogen metabolism. J Nutr 129, 768S–774S.CrossRefGoogle ScholarPubMed
Johnson, IT, Williamson, G & Musk, SRR (1994) Anticarcinogenic factors in plant foods: a new class of nutrients? Nutr Res Rev 7, 175–204.CrossRefGoogle Scholar
Krul, C, Humblot, C & Philippe, C (2002) Metabolism of sinigrin (2-propenyl glucosinolate) by the human colonic microflora in a dynamic in vitro large intestinal model. Carcinogenesis 23, 1009–1016.CrossRefGoogle Scholar
Ludikhuyze, L, Ooms, V, Weemaes, C & Hendrickx, M (1999) Kinetic study of the irreversible thermal and pressure inactivation of myrosinase from broccoli (Brassica oleracea L-Cv. Italica). J Agric Food Chem 47, 1794–1800.CrossRefGoogle ScholarPubMed
Mallett, AK, Bearne, CA, Rowland, IR, Farthing, MJG, Cole, CB & Fuller, R (1987) The use of rats associated with a human fecal flora as a model for studying the effects of diet on the human gut microflora. J Appl Bacteriol 63, 39–45.CrossRefGoogle Scholar
Mennicke, WH, Görler, K & Krumbiegel, G (1983) Metabolism of some naturally occurring isothiocyanates in the rat. Xenobiotica 13, 203–207.CrossRefGoogle ScholarPubMed
Mennicke, WH, Kral, T, Krumbiegel, G & Rittmann, N (1987) Determination of N-acetyl-S-(N-alkylthiocarbamoyl)-L-cysteine, a principal metabolite of alkyl isothiocyanates, in rat urine. J Chromatogr 414, 19–24.CrossRefGoogle ScholarPubMed
Meselhy, MR, Nakamura, N & Hattori, M (1997) Biotransformation of (-)epicatechin 3-O-gallate by human intestinal bacteria. Chem Pharm Bull 45, 888–893.CrossRefGoogle ScholarPubMed
Michaelsen, S, Otte, J, Simonsen, L-O & Sørensen, H (1994) Absorption and degradation of individual intact glucosinolates in the digestive tract of rodents. Acta Agric Scand 44A, 25–37.Google Scholar
Minchinton, IR, Sang, JP, Burke, D & Truscott, RJW (1982) Separation of desulphoglucosinolates by reversed-phase high-performance liquid chromatography. J Chromatogr 247, 141–148.CrossRefGoogle Scholar
Rabot, S, Guerin, C, Nugon-Baudon, L & Szylit, O (1995) Glucosinolate degradation by bacterial strains isolated from a human intestinal microflora. In Proceedings of the 9th International Rapeseed Congress, Rapeseed Today and Tomorrow, pp. 212–214 [Murphy, D, editor] Cambridge, UK: Royal Society of Chemistry.Google Scholar
Rumney, CJ, Rowland, IR & O'Neil, IK (1993) Conversion of IQ to 7OHIQ by gut microflora. Nutr Cancer 27, 250–255.Google Scholar
Shapiro, TA, Fahey, JW, Wade, KL, Stephenson, KK & Talalay, P (1998) Human metabolism and excretion of cancer chemoprotective glucosinolates and isothiocyanates of cruciferous vegetables. Cancer Epidemiol Biomarkers Prev 7, 1091–1100.Google ScholarPubMed
Shapiro, TA, Fahey, JW, Wade, KL, Stephenson, KK & Talalay, P (2001) Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts: metabolism and excretion in humans. Cancer Epidemiol Biomarkers Prev 10, 501–508.Google ScholarPubMed
Smith, TK, Lund, EK, Musk, SRR & Johnson, IT (1998) Inhibition of DMH induced aberrant crypt foci and induction of apoptosis in rat colon, following oral administration of a naturally occurring glucosinolate. Carcinogenesis 19, 967–973.CrossRefGoogle Scholar
Spinks, EA, Sones, K & Fenwick, GR (1984) The quantitative analysis of glucosinolates in cruciferous vegetables, oilseeds and forage crops using high performance liquid chromatography. Fette Seifen Anstr 6, 228–231.CrossRefGoogle Scholar
Steinmetz, KA & Potter, JD (1991) Vegetables, fruit, and cancer. I. Epidemiology. Cancer Causes Control 2, 325–357.CrossRefGoogle ScholarPubMed
Watson, SH & Kohlmeier, L (1999) Crucifera, glucosinolates and colon cancer. FASEB J 13, A919Google Scholar
Zhang, Y & Talalay, P (1994) Anticarcinogenic activities of organic isothiocyanates: chemistry and mechanisms. Cancer Res 54, Suppl., 1976s–1981s.Google ScholarPubMed