Microbiota: a mediator to transform glucosinolate precursors in cruciferous vegetables to the active isothiocyanates

Journal of the Science of Food and Agriculture

Volumn 98, Issue 4, 2018, Pages 1255-1260

  Tian, Sicong ^a   Liu, Xiaodong ^a   Lei, Peng ^a   Zhang, Xiaohong ^b   Shan, Yujuan ^a  

^a HARBIN INSTITUTE OF TECHNOLOGY   (China)

^b NINGBO UNIVERSITY   (China)

Author keywords

cruciferous vegetables; glucosinolates; intestinal microflora; isothiocyanates; myrosinase

Indexed keywords

GLUCOSINOLATE; GLYCOSIDASE; ISOTHIOCYANIC ACID DERIVATIVE; THIOGLUCOSIDASE;

ANIMAL; BACTERIUM; BRASSICACEAE; CHEMICAL STRUCTURE; CHEMISTRY; COOKING; ENZYME STABILITY; ENZYMOLOGY; HEAT; HUMAN; INTESTINE; INTESTINE FLORA; METABOLISM; PHYSIOLOGY;

ANIMALS; BACTERIA; BRASSICACEAE; COOKING; ENZYME STABILITY; GASTROINTESTINAL MICROBIOME; GLUCOSINOLATES; GLYCOSIDE HYDROLASES; HOT TEMPERATURE; HUMANS; INTESTINES; ISOTHIOCYANATES; MOLECULAR STRUCTURE;

EID: 85041739786     PISSN: 00225142     EISSN: 10970010     Source Type: Journal    
DOI: 10.1002/jsfa.8654     Document Type: Review

References (46)

1. Powolny AA and Singh SV, Differential response of normal (PrEC) and cancerous human prostate cells (PC-3) to phenethyl isothiocyanate-mediated changes in expression of antioxidant defense genes. Pharm Res 27:2766–2775 (2010).
2. Wang XT, Di Pasqua AJ, Govind S, McCracken E, Hong C, Mi LX et al., Selective depletion of mutant p53 by cancer chemopreventive isothiocyanates and their structure–activity relationships. J Med Chem 54:809–816 (2011).
3. Li D, Wu K, Howie AF, Beckett GJ, Wang W and Bao YP, Synergy between broccoli sprout extract and selenium in the upregulation of thioredoxin reductase in human hepatocytes. Food Chem 110:193–198 (2008).
4. Mukherjee S, Gangopadhyay H and Das DK, Broccoli: a unique vegetable that protects mammalian hearts through the redox cycling of the thioredoxin superfamily (retracted article: see 2012, vol. 60:2768). J Agric Food Chem 56:609–617 (2008).
5. Khalaj L, Nejad SC, Mohammadi M, Zadeh SS, Pour MH, Ashabi G et al., Assessing competence of broccoli consumption on inflammatory and antioxidant pathways in restraint-induced models: estimation in rat hippocampus and prefrontal cortex. Biomed Res Int; doi:https://doi.org/10.1155/2013/590379 (2013).
6. Fahey JW, Haristoy X, Dolan PM, Kensler TW, Scholtus I, Stephenson KK et al., Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of Helicobacter pylori and prevents benzo[a]pyrene-induced stomach tumors. Proc Natl Acad Sci USA 99:7610–7615 (2002).
7. Zheng HT, Whitman SA, Wu W, Wondrak GT, Wong PK, Fang DY et al., Therapeutic potential of Nrf2 activators in streptozotocin-induced diabetic nephropathy. Diabetes 60:3055–3066 (2011).
8. Jazwa A, Rojo AI, Innamorato NG, Hesse M, Fernandez-Ruiz J and Cuadrado A, Pharmacological targeting of the transcription factor Nrf2 at the basal ganglia provides disease modifying therapy for experimental parkinsonism. Antioxid Redox Sign 14:2347–2360 (2011).
9. Poulton EJ, Levy L, Lampe JW, Shen DD, Tracy J, Shuhart MC et al., Sulforaphane is not an effective antagonist of the human pregnane X-receptor in vivo. Toxicol Appl Pharm 266:122–131 (2013).
10. Bheemreddy RM and Jeffery EH, The metabolic fate of purified glucoraphanin in F344 rats. J Agric Food Chem 55:2861–2866 (2007).
11. Dinkova-Kostova AT and Kostov RV, Glucosinolates and isothiocyanates in health and disease. Trends Mol Med 18:337–347 (2012).
12. Kelly P, Bones A and Rossiter J, Sub-cellular immunolocalization of the glucosinolate sinigrin in seedlings of Brassica juncea. Planta 206:370–377 (1998).
13. Bones AM and Rossiter JT, The myrosinase–glucosinolate system, its organisation and biochemistry. Physiol Plant 97:194–208 (1996).
14. Fahey JW, Zalcmann AT and Talalay P, The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51 (2001).
15. Halkier BA and Gershenzon J, Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333 (2006).
16. Winde I and Wittstock U, Insect herbivore counteradaptations to the plant glucosinolate–myrosinase system. Phytochemistry 72:1566–1575 (2011).
17. Sathishkumar N, Senthil KT, Jong P, Mi C and Ill-Sup N, Molecular modeling of myrosinase from Brassica oleracea: a structural investigation of sinigrin interaction. Genes (Basel) 6:1315–1329 (2015).
18. Van Eylen D, Indrawati, Hendrickx M and Van Loey A, Temperature and pressure stability of mustard seed (Sinapis alba L.) myrosinase. Food Chem 97:263–271 (2006).
19. Rungapamestry V, Duncan AJ, Fuller Z and Ratcliffe B, Changes in glucosinolate concentrations, myrosinase activity, and production of metabolites of glucosinolates in cabbage (Brassica oleracea var. capitata) cooked for different durations. J Agric Food Chem 54:7628–7634 (2006).
20. Chen SX and Halkier BA, Functional expression and characterization of the myrosinase MYR1 from Brassica napus in Saccharomyces cerevisiae. Protein Expres Purif 17:414–420 (1999).
21. Ludikhuyze L, Ooms V, Weemaes C and Hendrickx M, 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 (1999).
22. Rouzaud G, Young SA and Duncan AJ, Hydrolysis of glucosinolates to isothiocyanates after ingestion of raw or microwaved cabbage by human volunteers. Cancer Epidemiol, Biomarkers Prev 13:125–131 (2004).
23. Kellingray L, Saha S, Doleman J, Narbad A and Mithen R, Investigating the metabolism of glucoraphanin by the human gut microbiota using ex vivo culturing methods. Proc Nutr Soc 73:E34–E34 (2014).
24. Angelino D and Jeffery E, Glucosinolate hydrolysis and bioavailability of resulting isothiocyanates: focus on glucoraphanin. J Funct Foods 7:67–76 (2014).
25. Palop ML, Smiths JP and Tenbrink B, Degradation of sinigrin by Lactobacillus agilis strain R16. Int J Food Microbiol 26:219–229 (1995).
26. Li F, Hullar MAJ, Beresford SAA and Lampe JW, Variation of glucoraphanin metabolism in vivo and ex vivo by human gut bacteria. Br J Nutr 106:408–416 (2011).
27. Elfoul L, Rabot S, Khelifa N, Quinsac A, Duguay A and Rimbault A, 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 (2001).
28. Mullaney JA, Kelly WJ, McGhie TK, Ansell J and Heyes JA, Lactic acid bacteria convert glucosinolates to nitriles efficiently yet differently from Enterobacteriaceae. J Agric Food Chem 61:3039–3046 (2013).
29. Ohtsuru MTI and Hata T, The production and stability of intracellular myrosinase from Aspergillus niger. Agric Biol Chem 37:967–971 (1973).
30. Clarke JD, Hsu A, Riedl K, Bella D, Schwartz SJ, Stevens JF et al., Bioavailability and inter-conversion of sulforaphane and erucin in human subjects consuming broccoli sprouts or broccoli supplement in a cross-over study design. Pharmacol Res 64:456–463 (2011).
31. Mahn A, Angulo A and Cabanas F, Purification and characterization of broccoli (Brassica oleracea var. italica) myrosinase (beta-thioglucosidase glucohydrolase). J Agric Food Chem 62:11666–11671 (2014).
32. Jones AME, Bridges M, Bones AM, Cole R and Rossiter JT, Purification and characterisation of a non-plant myrosinase from the cabbage aphid Brevicoryne brassicae (L.). Insect Biochem Mol 31:1–5 (2001).
33. Lai RH, Miller MJ and Jeffery E, Glucoraphanin hydrolysis by microbiota in the rat cecum results in sulforaphane absorption. Food Funct 1:161–166 (2010).
34. Birgit H and Gary W, A critical review of the bioavailability of glucosinolates and related compounds. Nat Prod Rep 21:425–447 (2004).
35. Platz S, Piberger AL, Budnowski J, Herz C, Schreiner M, Blaut M et al., Bioavailability and biotransformation of sulforaphane and erucin metabolites in different biological matrices determined by LC-MS-MS. Anal Bioanal Chem 407:1819–1829 (2015).
36. Francisco JB, Nooshin N, Shahin R, Anissa K, Zhu ZZ and Mohamed K, Bioavailability of glucosinolates and their breakdown products: impact of processing. Front Nutr doi:https://doi.org/10.3389/fnut.2016.00024(2016).
37. Luang-In V, Narbad A, Nueno-Palop C, Mithen R, Bennett M and Rossiter JT, The metabolism of methylsulfinylalkyl- and methylthioalkyl-glucosinolates by a selection of human gut bacteria. Mol Nutr Food Res 58:875–883 (2014).
38. Petroski RJ and Kwolek WF, Interactions of a fungal thioglucoside glucohydrolase and cruciferous plant epithiospecifier protein to form 1-cyanoepithioalkanes - implications of an allosteric mechanism. Phytochemistry 24:213–216 (1985).
39. Rakariyatham N and Sakorn P, Biodegradation of glucosinolates in brown mustard seed meal (Brassica juncea) by Aspergillus sp NR-4201 in liquid and solid-state cultures. Biodegradation 13:395–399 (2002).
40. Rakariyatham N, Butrindr B, Niamsup H and Shank L, Screening of filamentous fungi for production of myrosinase. Braz J Microbiol 36:242–245 (2005).
41. Rabot S, Nugonbaudon L, Raibaud P and Szylit O, Rapeseed meal toxicity in gnotobiotic-rats - influence of a whole human fecal flora or single human strains of Escherichia coli and Bacteroides vulgatus. Br J Nutr 70:323–331 (1993).
42. Tani N, Ohtsuru M and Hata T, Purification and general characteristics of bacterial myrosinase produced by Enterobacter cloacae. Agric Biol Chem 38:1623–1630 (1974).
43. Luciano FB, Belland J and Holley RA, Microbial and chemical origins of the bactericidal activity of thermally treated yellow mustard powder toward Escherichia coli O157:H7 during dry sausage ripening. Int J Food Microbiol 145:69–76 (2011).
44. Albaser A, Kazana E, Bennett MH, Cebeci F, Luang-In V, Spanu PD et al., Discovery of a bacterial glycoside hydrolase family 3 (GH3) beta-glucosidase with myrosinase activity from a Citrobacter strain isolated from soil. J Agric Food Chem 64:1520–1527 (2016).
45. Nugon-Baudon L, Rabot S, Wal J-M and Szylit O, Interactions of the intestinal microflora with glucosinolates in rapeseed meal toxicity: first evidence of an intestinal Lactobacillus possessing a myrosinase-like activity in vivo. J Sci Food Agric 52:547–559 (1990).
46. Dolara P, Luceri C, De Filippo C, Femia AP, Giovannelli L, Caderni G et al., Red wine polyphenols influence carcinogenesis, intestinal microflora, oxidative damage and gene expression profiles of colonic mucosa in F344 rats. Mutat Res 591:237–246 (2005).