Hydroxylated phenylacetamides derived from bioactive benzoxazinoids are bioavailable in humans after habitual consumption of whole grain sourdough rye bread

Molecular Nutrition and Food Research

Volumn 57, Issue 10, 2013, Pages 1859-1873

  Beckmann, Manfred ^a   Lloyd, Amanda J ^a   Haldar, Sumanto ^b   Seal, Chris ^b   Brandt, Kirsten ^b   Draper, John ^a  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Benzoxazinoids; Bioactive; Metabolomics; Multivariate data analysis; Whole grain sourdough rye bread

Indexed keywords

2 HYDROXY 1,4 BENZOXAZIN 3 ONE; 2-HYDROXY-1,4-BENZOXAZIN-3-ONE; ACETANILIDE DERIVATIVE; BENZOXAZINE DERIVATIVE;

ARTICLE; BENZOXAZINOIDS; BIOACTIVE; BREAD; CHEMISTRY; DIET; FEMALE; FERMENTATION; HUMAN; HYDROXYLATION; MALE; MASS SPECTROMETRY; METABOLOMICS; MIDDLE AGED; MULTIVARIATE ANALYSIS; MULTIVARIATE DATA ANALYSIS; REPRODUCIBILITY; RYE; URINE; WHOLE GRAIN SOURDOUGH RYE BREAD;

BENZOXAZINOIDS; BIOACTIVE; METABOLOMICS; MULTIVARIATE DATA ANALYSIS; WHOLE GRAIN SOURDOUGH RYE BREAD;

ACETANILIDES; BENZOXAZINES; BREAD; DIET; FEMALE; FERMENTATION; HUMANS; HYDROXYLATION; MALE; MASS SPECTROMETRY; MIDDLE AGED; MULTIVARIATE ANALYSIS; REPRODUCIBILITY OF RESULTS; SECALE CEREALE;

EID: 84884965446     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200777     Document Type: Article

References (58)

1. De Munter, J. S. L., Hu, F. B., Spiegelman, D., Franz, M. et al., Whole grain, bran, and germ intake and risk of type 2 diabetes: A prospective cohort study and systematic review. PLOS Medicine 2007, 4, e261. doi:10.1371/journal.pmed.0040261.
2. Seal, C. J., Brownlee, I. A., Whole grains and health: evidence from observational and intervention studies. Cereal Chem. 2010, 87, 167-174.
3. Mellen, P. B., Walsh, T. F., Herrington, D. M., Whole grain intake and cardiovascular disease: a meta-analysis. Nutr. Metab. Cardiovasc. Dis. 2008, 18, 283-290.
4. Aune, D., Chan, D. S. M., Lau, R., Vieir, R. et al., Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose-response meta-analysis of prospective studies. Br. Med. J. 2011, 343, d6617.
5. Jones, J. M., Engleson, J., Whole grains: benefits and challenges. Annu. Rev. Food Sci. Technol. 2010, 1, 19-40.
6. Kyrø, C., Skeie, G., Dragsted, L. O., Christensen, J. et al., Intake of whole grain in Scandinavia: intake, sources and compliance with new national recommendations. Scand. J. Public Health 2012, 40, 76-84.
7. United States Department of Agriculture, Centre for Nutrition Policy and Promotion. 2011. Available from: http://www.cnpp.usda.gov/dgas2010-policydocument.htm.
8. Brandt, K., Christensen, L. P., Hansen-Møller, J., Hansen, S. L. et al., Health promoting compounds in vegetables and fruits: a systematic approach for identifying plant components with impact on human health. Trends Food Sci. Technol. 2004, 15, 384-393.
9. Ross, A. B., Kamal-Eldin, A., Åman, P., Dietary alkylresorcinols: absorption, bioactivities, and possible use as biomarkers of whole-grain wheat- and rye-rich foods. Nutr. Rev. 2004, 62, 81-95.
10. Aubertin-Leheudre, M., Koskela, A., Samaletdin, A., Adlercreutz, H., Plasma alkylresorcinol metabolites as potential biomarkers of whole-grain wheat and rye cereal fibre intakes in women. Br. J. Nutr. 2010, 103, 339-343.
11. Ross, A. B., Bourgeois, A., Macharia, H. N., Kochhar, S. et al., Plasma alkylresorcinols as a biomarker of whole-grain food consumption in a large population: results from the WHOLEheart Intervention Study. Am. J. Clin. Nutr. 2012, 95, 204-211.
12. Landberg, R., Townsend, M. K., Neelakantan, N., Sun, Q. et al., Alkylresorcinol metabolite concentrations in spot urine samples correlated with whole grain and cereal fiber intake but showed low to modest reproducibility over one to three years in U.S. women. J. Nutr. 2012, 142, 872-877.
13. Guyman, L. A., Adlercreutz, H., Koskela, A., Li, L. et al., Urinary 3-(3, 5-dihydroxyphenyl)-1-propanoic acid, an alkylresorcinol metabolite, is a potential biomarker of whole-grain intake in a US population. J. Nutr. 2008, 138, 1957-1962.
14. Sicker, D., Frey, M., Schulz, M., Gierl, A., Role of natural benzoxazinoes in the survival strategy of plants. Int. Rev. Cytol. 2000, 198, 319-346.
15. Villagrasa, M., Guillamon, M., Labandeira, A., Taberner, A., Benzoxazinoid allelochemicals in wheat: distribution among foliage, roots, and seeds. J. Agric. Food Chem. 2006, 54, 1009-1015.
16. Carlsen, S. C. K., Kudsk, P., Laursen, B., Mathiassen, S. K. et al., Allelochemicals in rye (Secale cereale L.): cultivar and tissue differences in the production of benzoxazinoids and phenolic acids. Nat. Prod. Commun. 2009, 4, 199-208.
17. Prinz, S., Schauberger, D., Bauer, I. M., Knasmueller, S. et al., Aneugenic 2, 4-dihydroxyl-7-methoxy-1, 4-benzoxazin-3-one (DIMBOA) and 2, 4-dihydroxyl-1, 4-benzoxazin-3-one (DIBOA) in sprouts of Triticum aestivum cultivars - a 'safety health food'? Food Chem. 2010, 121, 973-979.
18. Macias, F. A., Marin, D., Oliveros-Bastidas, A., Molinillo, J. M. G., Rediscovering the bioactivity and ecological role of 1, 4-benzoxazinones. Nat. Prod. Rep. 2009, 26, 478-489.
19. Niemeyer, H. M., Hydroxamic acids derived from 2-hydroxy-2H-1, 4-benzoxazin-3(4H)-one: key defense chemicals of cereals. J. Agri. Food Chem. 2009, 57, 1677-1696.
20. Fomsgaard, I. S., Mortensen, A. G., Carlsen, S. C. K., Microbial transformation products of benzoxazolinone and benzoxazinone allelochemicals - a review. Chemosphere 2004, 54, 1025-1038.
21. Hanhineva, K., Rogachev, I., Aura, A.-M., Aharoni, A. et al., Qualitative characterization of benzoxazinoid derivatives in whole grain rye and wheat by LC-MS metabolite profiling. J. Agri. Food Chem. 2011, 59, 921-927.
22. Pedersen, H. A., Laursen, B., Mortensen, A., Fomsgaard, I. S., Bread from common cereal cultivars contains an important array of neglected bioactive benzoxazinoids. Food Chem. 2011, 127, 1814-1820.
23. Cambier, V., Hance, T., de Hoffmann, E., Non-injured maize contains several 1, 4-benzoxazin-3-one related compounds but only as glucoconjugates. Phytochem. Analysis 1999, 10, 119-126.
24. Krogh, S. S., Mensz, S. J. M., Nielsen, S. T., Mortensen, A. G. et al., Fate of benzoxazinone allelochemicals in soil after incorporation of wheat and rye sprouts. J. Agri. Food Chem. 2006, 54, 1064-1074.
25. Villagrasa, M., Guillamon, M., Navarro, A., Eljarrat, E. et al., Development of a pressurized liquid extraction-solid-phase extraction followed by liquid chromatography-electrospray ionization tandem mass spectrometry method for the quantitative determination of benzoxazolinones and their degradation products in agricultural soil. J. Chromatogr. A 2008, 1179, 190-197.
26. Zikmundova, M., Drandarov, K., Bigler, L., Hesse, A. et al., Biotransformation of 2-benzoxazolinone and 2-hydroxy-1, 4-benzoxazin-3-one by endophytic fungi isolated from Aphelandra tetragona. Appl. Environ. Microbiol. 2002, 68, 4863-4870.
27. Zikmundova, M., Drandarov, K., Hesse, M., Werner, C., Hydroxylated 2-amino-3H-phenoxazin-3-one derivatives as products of 2-hydroxy-1, 4-benzoxazin-3-one (HBOA) biotransformation by Chaetosphaeria sp., an endophytic fungus from Aphelandra tetragona. Z. Naturforsch. C 2002, 57, 660-665.
28. Poupaert, J., Carato, P., Colacillo, E., 2(3H)-benzoxazolone and bioisosters as "privileged scaffold" in the design of pharmacological probes. Curr. Med. Chem. 2005, 12, 877-885.
29. Adhikari, K. B., Laursen, B. B., Lærke, H. N., Fomsgaard, I. S., Bioactive benzoxazinoids in rye bread are absorbed and metabolized in pigs. J. Agri. Food Chem. 2012, 60, 2497-2506.
30. Brownlee, I. A., Moore, C., Chatfield, M., Richardson, D. P. et al., Markers of cardiovascular risk are not changed by increased whole grain-intake. The WHOLEheart study: a randomised, controlled dietary intervention. Br. J. Nutr. 2011, 104, 125-134.
31. Bingham, S. A., Gill, C., Welch, A., Cassidy, A. et al., Validation of dietary assessment methods in the UK arm of EPIC using weighed records, and 24-hour urinary nitrogen and potassium and serum vitamin C and carotenoids as biomarkers. Int. J. Epidemiol. 1997, 26, S137-S151.
32. Favé, G., Beckmann, M., Lloyd, A. J., Zhou, S., Development and validation of a standardized protocol to monitor human dietary exposure by metabolite fingerprinting of urine samples. Metabolomics 2011, 7, 469-484.
33. Lloyd, A. J., Beckmann, M., Favé, G., Mathers, J. C. et al., Proline betaine and its biotransformation products in fasting urine samples are potential biomarkers of habitual citrus fruit consumption. Br. J. Nutr. 2011, 106, 812-824.
34. Lloyd, A. J., Favé, G., Beckmann, M., Lin, W. et al., Use of mass spectrometry fingerprinting to identify urinary metabolites after consumption of specific foods. Am. J. Clin. Nutr. 2011, 94, 981-991.
35. Lloyd, A. J., Beckmann, M., Halder, S., Seal, C. et al., Data driven strategy for the discovery of potential urinary biomarkers of habitual dietary exposure. Am. J. Clin. Nutr. 2013, 97, 377-389.
36. Assfalg, M., Bertini, I., Colangiuli, D., Luchinat, C. et al., Evidence of different metabolic phenotypes in humans. Proc. Natl. Acad. Sci. USA 2008, 105, 1420-1424.
37. Holmes, E., Loo, R. L., Stamler, J., Bictash, M. et al., Human metabolic phenotype diversity and its association with diet and blood pressure. Nature 2008, 453, 396-401.
38. O'Sullivan, A., Gibney, M. J., Brennan, L., Dietary intake patterns are reflected in metabolomic profiles: potential role in dietary assessment studies. Am. J. Clin. Nutr. 2011, 93, 314-321.
39. Beckmann, M., Enot, D. P., Overy, D. P., Scott, I. M. et al., Metabolite fingerprinting of urine suggests breed-specific dietary metabolism differences in domestic dogs. Br. J. Nutr. 2010, 103, 1127-1138.
40. Beckmann, M., Parker, D., Enot, D. P., Duval, E. et al., High-throughput, nontargeted metabolite fingerprinting using nominal mass flow injection electrospray mass spectrometry. Nat. Protoc. 2008, 3, 486-504.
41. Enot, D. P., Lin, W., Beckmann, M., Parker, D. et al., Preprocessing, classification modeling and feature selection using flow injection electrospray mass spectrometry metabolite fingerprint data. Nat. Protoc. 2008, 3, 446-470.
42. Draper, J., Enot, D. P., Parker, D., Beckmann, M. et al., Metabolite signal identification in accurate mass metabolomics data with MZedDB, an interactive m/z annotation tool utilising predicted ionisation behaviour 'rules'. BMC Bioinform. 2009, 10, 227.
43. Levsen, K., Schiebel, H. M., Behnke, B., Dotzer, R. et al., Structure elucidation of phase II metabolites by tandem mass spectrometry: an overview. J. Chromatogr. A 2005, 1067, 55-72.
44. Laryea, M. D., Herebian, D., Meissner, T., Mayatepek, E., Simultaneous LC-MS/MS determination of phenylbutyrate, phenylacetate benzoate and their corresponding metabolites phenylacetylglutamine and hippurate in blood and urine. J. Inherit. Metab. Dis. 2010, DOI 10.1007/s10545-010-9172-9.
45. Vogelmanna, S. A., Hertel, C., Impact of ecological factors on the stability of microbial associations in sourdough fermentation. Food Microbiol. 2011, 28, 583-589.
46. Katina, K., Liukkonen, K.-H., Kaukovirta-Norja, H., Adlercreutz, H. et al., Fermentation-induced changes in the nutritional value of native or germinated rye. J. Cereal Sci. 2007, 46, 348-355.
47. Hanhineva, K., Aura, A.-M., Rogachev, I., Matero S. et al., In vitro microbiotic fermentation causes an extensive metabolite turnover of rye bran phytochemicals. PLoS One 2012, 7, e39322.
48. Adhikari, K. B., Lærke, H. N., Mortensen, A. G., Fomsgaard, I. S., Plasma and urine concentrations of bioactive dietary benzoxazinoids and their glucuronidated conjugates in rats fed a rye bread-based diet. J. Agri. Food Chem. 2012, 60, 11518-11524.
49. Bondia-Pons, I., Barri, T., Hanhineva, K., Juntunen, K. et al., UPLC-QTOF/MS metabolic profiling unveils urinary changes in humans after a whole grain rye versus refined wheat bread intervention. Mol. Nutr. Food Res. 2013, 57, 412-422.
50. Brandt, K., Christensen, L. P., Hansen, S. L., Young, J. F. et al., Functions of bioactive plant compounds and effect on humans. Innov. Food Tech. 2001, 10, 60-62.
51. Katina, K., Arendt, E., Liukkonen, K.-H., Autio, K. et al., Potential of sourdough for healthier cereal products. Trends Food Sci. Technol. 2005, 16, 104-112.
52. Bondia-Pons, I., Nordlund, E., Mattila, I., Katina, K. et al., Postprandial differences in the plasma metabolome of healthy Finnish subjects after intake of a sourdough fermented endosperm rye bread versus white wheat bread. Nutr. J. 2011, 10, 116.
53. Rondini, L., Peyrat-Maillard, M. N., Marsset-Baglieri, A., Fromentin, G. et al., Bound ferulic acid from bran is more bioavailable than the free compound in rat. J. Agri. Food Chem. 2004, 52, 4338-4343.
54. Fardet, A., Rock, E., Remesy, C., Is the in vitro antioxidant potential of whole-grain cereals and cereal products well reflected in vivo? J. Cereal Sci. 2008, 48, 258-276.
55. Kern, S. M., Bennett, R. N., Mellon, F. A., Kroon, P. A. et al., Absorption of hydroxycinnamates in humans after high-bran cereal consumption. J. Agri. Food Chem. 2003, 51, 6050-6055.
56. Zhao, Z., Egashira, Y., Sanada, H., Digestion and absorption of ferulic acid sugar esters in rat gastrointestinal tract. J. Agri. Food Chem. 2003, 51, 5534-5539.
57. Zhao, Z., Egashira, Y., Sanada, H., Ferulic acid sugar esters are recovered in rat plasma and urine mainly as the sulfoglucuronide of ferulic acid. J. Nutr. 2003, 133, 1355-1361.
58. Zhao, Z., Egashira, Y., Sanada, H., Ferulic acid is quickly absorbed from rat stomach as the free form and then conjugated mainly in liver. J. Nutr. 2004, 134, 3083-3088.