Structural and functional characterization of pronyl-lysine, a novel protein modification in bread crust melanoidins showing in vitro antioxidative and phase I/II enzyme modulating activity
Abstract
Application of an in vitro antioxidant assay to solvent fractions isolated from bread crust, bread crumb, and flour, respectively, revealed the highest antioxidative potential for the dark brown, ethanol solubles of the crust, whereas corresponding crumb and flour fractions showed only minor activities. To investigate whether these browning products may also act as antioxidants in biological systems, their modulating activity on detoxification enzymes was investigated as a functional parameter in intestinal Caco-2 cells. The bread crust and, in particular, the intensely brown, ethanolic crust fraction induced a significantly elevated glutathione S-transferase (GST) activity and a decreased phase I NADPH-cytochrome c reductase (CCR) activity compared to crumb-exposed cells. Antioxidant screening of Maillard-type model mixtures, followed by structure determination, revealed the pyrrolinone reductones 1 and 2 as the key antioxidants formed from the hexose-derived acetylformoin and N(alpha)-acetyl-L-lysine methyl ester or glycine methyl ester, chosen as model substances to mimic nonenzymatic browning reactions with the lysine side chain or the N terminus of proteins, respectively. Quantitation of protein-bound pyrrolinone reductonyl-lysine, abbreviated pronyl-lysine, revealed high amounts in the bread crust (62.2 mg/kg), low amounts in the crumb (8.0 mg/kg), and the absence of this compound in untreated flour. Exposing Caco-2 cells for 48 h to either synthetically pronylated albumin or purified pronyl-glycine (3) significantly increased phase II GST activity by 12 or 34%, respectively, thus demonstrating for the first time that "pronylated" proteins as part of bread crust melanoidins act as monofunctional inducers of GST, serving as a functional parameter of an antioxidant, chemopreventive activity in vitro.
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Increased intake of long-chain n-3 PUFA results in increased proportions of those fatty acids in inflammatory cell phospholipids.
“Increased intake of long-chain n-3 PUFA results in increased proportions of those fatty acids in inflammatory cell phospholipids (610 -614) .”
From Dietary factors and low-grade inflammation in relation to overweight and obesity (2011) · cites this paper as [614]
Cites
PROTEIN MEASUREMENT WITH THE FOLIN PHENOL REAGENT
Lowry, O. H., Rosebrough, N., Farr, A. L., & Randall, R. (1951) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52451-6 · Cited by 315,771 · see citing works
Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)42083-8 · Cited by 18,394 · see citing works
Schmiedlin‐Ren, P., Thummel, K. E., Fisher, J. M., Paine, M. F., Lown, K. S., & Watkins, P. B. (1997) · Molecular Pharmacology · doi:10.1124/mol.51.5.741 · Cited by 325 · see citing works
Loss and/or formation of antioxidants during food processing and storage
Nicoli, M. C., Anese, M., Parpinel, M. T., Franceschi, S., & Lerici, C. R. (1997) · Cancer Letters · doi:10.1016/s0304-3835(97)04628-4 · Cited by 305 · see citing works
Antioxidant Properties of Coffee Brews in Relation to the Roasting Degree
Nicoli, M. C., Anese, M., Manzocco, L., & Lerici, C. R. (1997) · LWT - Food Science and Technology · doi:10.1006/fstl.1996.0181 · Cited by 299 · see citing works
Detoxication Enzymes and Chemoprevention
Wilkinson, J. C., & Clapper, M. L. (1997) · Experimental Biology and Medicine · doi:10.3181/00379727-216-44169 · Cited by 199 · see citing works
Hofmann, T. F., & Schieberle, P. (2001) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf010823n · Cited by 131 · see citing works
Self-citationStability of antioxidants formed from histidine and glucose by the Maillard reaction
Lingnert, H., & Waller, G. R. (1983) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf00115a007 · Cited by 66 · see citing works
Isolation and characterization of melanoidins from beer
KUNTCHEVA, M. J., & OBRETENOV, T. D. (1996) · European Food Research and Technology · doi:10.1007/bf01263547 · Cited by 42 · see citing works
Effect of Heat-Treated Proteins on Selected Parameters of the Biotransformation System in the Rat
Wenzel, E., Tasto, S., Erbersdobler, H. F., & Faist, V. (2002) · Annals of Nutrition and Metabolism · doi:10.1159/000046747 · Cited by 36 · see citing works
Self-citationMarko, D., Kemény, M., Bernady, E., et al. (2002) · Food and Chemical Toxicology · doi:10.1016/s0278-6915(01)00093-x · Cited by 29 · see citing works
Zur Isolierung und Charakterisierung der braunen Kaffeer�ststoffe II Mitteilung
Maier, H. G., & Buttle, H. (1973) · European Food Research and Technology · doi:10.1007/bf01356789 · Cited by 24 · see citing works
Effect of oat constituents on aggregation behavior of Oryzaephilus surinamensis (L)
Mikolajczak, K. L., Freedman, B., Zilkowski, B. W., Smith, C. R., & Burkholder, W. E. (1983) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf00115a008 · Cited by 24 · see citing works
ISOLATION AND CHARACTERIZATION OF MELANOIDINES FROM MALT AND MALT ROOTS
OBRETENOV, T. D., KUNTCHEVA, M. J., MANTCHEV, S. C., et al. (1991) · Journal of Food Biochemistry · doi:10.1111/j.1745-4514.1991.tb00162.x · Cited by 23 · see citing works
Description of the Flavour of Comté Cheese
Bérodier, F., Stèvenot, C., & Schlich, P. (1997) · LWT · doi:10.1006/fstl.1996.0180 · Cited by 22 · see citing works
Bildung von Pyrrolinonreduktonen beim Erhitzen von Hexosen mit Aminosauren
Ledl, F., & Fritsch, G. (1984) · European Food Research and Technology · doi:10.1007/bf01042312 · Cited by 21 · see citing works
Hiramoto, K., Ishihara, A., Sakui, N., et al. (1998) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.21.102 · Cited by 9 · see citing works
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Calder, P. C., Ahluwalia, N., Brouns, F., Buetler, T., Clement, K., Cunningham, K., Esposito, K., Jönsson, L. S., Kolb, H., Lansink, M., et al. (2011) · British Journal of Nutrition · doi:10.1017/s0007114511005460 · Cited by 1,098 · see citing works
Melanoidins produced by the Maillard reaction: Structure and biological activity
Wang, H.-Y., Qian, H., & Yao, W.-R. (2011) · Food Chemistry · doi:10.1016/j.foodchem.2011.03.075 · Cited by 719 · see citing works
Metabolism of Maillard reaction products by the human gut microbiota – implications for health
Tuohy, K. M., Hinton, D. J. S., Davies, S. J., Crabbe, M. J. C., Gibson, G. R., & Ames, J. M. (2006) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.200500126 · Cited by 186 · see citing works
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Šebeková, K., & Somoza, V. (2007) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.200700035 · Cited by 148 · see citing works
Role of Hydroxycinnamates in Coffee Melanoidin Formation
Nunes, F. M., & Coimbra, M. A. (2010) · Phytochemistry Reviews · doi:10.1007/s11101-009-9151-7 · Cited by 82 · see citing works
Zhu, Z., Zhang, Y., Wang, W., Huang, Z., Wang, J., Li, X., & Sun, S. (2021) · International Journal of Food Science & Technology · doi:10.1111/ijfs.14881 · Cited by 14 · see citing works
- Authors
- Lindenmeier, M., Faist, V., & Hofmann, T.
- Affiliations
- Leibniz-Institute for Food Systems Biology at the Technical University of Munich (DE)
- Corresponding author
- Hofmann, Thomas
- ORCID
- Hofmann, Thomas
- Venue
- Journal of Agricultural and Food Chemistry
- Publisher
- American Chemical Society (ACS)
- Published
- 2002-10-16
- Volume
- 50
- Issue
- 24
- Pages
- 6997-7006
- ISSN
- 0021-8561 (ISSN-L)
- 1520-5118
- OpenAlex
- W2053542354
- Cited by
- 191
- References
- 17
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 5 · 2023: 4 · 2022: 10 · 2021: 12 · 2020: 8 · 2019: 9 · 2018: 8 · 2017: 6 · 2016: 6 · 2015: 11 · 2014: 7 · 2013: 6 · 2012: 10
- FWCI
- 11.88
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Agricultural and Food Chemistry (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Potato Plant Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Advanced Glycation End Products research
- Health Sciences › Medicine › Biochemistry › Phytochemicals and Antioxidant Activities
- Keywords
- Maillard reaction, non-enzymatic browning, glutathione S-transferase induction, phase II enzymes, NADPH-cytochrome c reductase, antioxidant activity, Caco-2 cells, chemoprevention, bread crumb
- MeSH terms
- Antioxidants, Bread, Chromatography, High Pressure Liquid, Glutathione Transferase, Humans, Lysine, Malondialdehyde, Gas Chromatography-Mass Spectrometry, NADPH-Ferrihemoprotein Reductase, Magnetic Resonance Spectroscopy, Polymers, Proteins, Pyrroles, Maillard Reaction, Caco-2 Cells
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