Skip to main content
SpringerLink
Log in

Methionine augments endogenous antioxidant capacity of rice protein through stimulating MSR antioxidant system and activating Nrf2-ARE pathway in growing and adult rats

  • Original Paper
  • Published:
European Food Research and Technology Aims and scope Submit manuscript

Abstract

To elucidate the influence of methionine on the endogenous antioxidant activity of rice protein (RP), growing and adult rats were fed with RP and methionine-supplemented RP (RM). After 2 weeks feeding, hepatic contents of ROS were significantly reduced by RP and RM. The endogenous antioxidant responses were induced by RP and increased by RM, in which methionine sulfoxide reductases (MsrA, MsrB2, MsrB3) expression and glutathione synthesis were uniformly stimulated and up-regulated with increasing consumption of methionine. With the intake of RP and RM, Nrf2 was activated through depressing Keap1 and Cul3, resulting in the up-regulation of antioxidant-responsive element (ARE)-driven antioxidant expressions (GCLC, GCLM, CAT, SOD, HO-1, NQO1) with increasing dietary level of methionine. The present study demonstrates that methionine can augment the endogenous antioxidant activity of rice protein, which is primarily attributed to stimulating methionine sulfoxide reductases expression and enhancing glutathione synthesis via Nrf2-ARE pathway. Results suggest that the methionine availability might play a key role in inducing and augmenting the endogenous antioxidant response exerted by rice protein, which is independent of age.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Zhang J, Zhang H, Wang L, Guo X, Wang X, Yao H (2009) Antioxidant activities of the rice endosperm protein hydrolysate: identification of the active peptide. Eur Food Res Technol 229:709–719

    Article  CAS  Google Scholar 

  2. Adebiyi AP, Adebiyi AO, Hasegawa Y, Ogawa T, Muramoto K (2009) Isolation and characterization of protein fractions from deoiled rice bran. Eur Food Res Technol 228:391–401

    Article  CAS  Google Scholar 

  3. Adebiyi AP, Adebiyi AO, Yamashita J, Ogawa T, Muramoto K (2009) Purification and characterization of antioxidative peptides derived from rice bran protein hydrolysates. Eur Food Res Technol 228:553–563

    Article  CAS  Google Scholar 

  4. Li H, Yang L, Yang H, Sun S, Liu H, Wu Q, Chen J, Zhuang T (2014) Rice protein regulates HDL metabolism-related gene expression and enzyme activity in adult rats. Food Biosci 8:1–7

    Article  CAS  Google Scholar 

  5. Yang L, Chen JH, Zhang H, Qiu W, Liu QH, Peng X, Li YN, Yang HK (2012) Alkali treatment affects in vitro digestibility and bile acid binding activity of rice protein due to varying its ratio of arginine to lysine. Food Chem 132:925–930

    Article  CAS  Google Scholar 

  6. Yang L, Chen JH, Xu T, Nie MH, Yang HK (2013) Hypocholesterolemic effect of rice protein is due to regulating hepatic cholesterol metabolism in adult rats. Gene 512:470–476

    Article  CAS  PubMed  Google Scholar 

  7. Yang L, Chen JH, Xu T, Zhou AS, Yang HK (2012) Rice protein improves oxidative stress by regulating glutathione metabolism and attenuating oxidative damage to lipids and proteins in rats. Life Sci 91:389–394

    Article  CAS  PubMed  Google Scholar 

  8. Cai J, Yang L, He HJ, Xu T, Liu HB, Wu Q, Ma Y, Liu QH, Nie MH (2014) Antioxidant capacity responsible for a hypocholesterolemia is independent of dietary cholesterol in adult rats fed rice protein. Gene 533:57–66

    Article  CAS  PubMed  Google Scholar 

  9. Métayer S, Seiliez I, Collin A, Duchêne S, Mercier Y, Geraert P-A, Tesseraud S (2008) Mechanisms through which sulfur amino acids control protein metabolism and oxidative status. J Nutr Biochem 19:207–215

    Article  PubMed  CAS  Google Scholar 

  10. Lu SC (2013) Glutathione synthesis. Biochim Biophys Acta 1830:3143–3153

    Article  CAS  PubMed  Google Scholar 

  11. Lu SC (2009) Regulation of glutathione synthesis. Mol Asp Med 30:42–59

    Article  CAS  Google Scholar 

  12. Lee BC, Gladyshev VN (2011) The biological significance of methionine sulfoxide stereochemistry. Free Radic Biol Med 50:271–277

    Google Scholar 

  13. Lee BC, Dikiy A, Kim HY, Gladyshev VN (2009) Functions and evolution of selenoprotein methionine sulfoxide reductases. Biochim Biophys Acta 1790:1471–1477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Liu Y, Wang Z, Li H, Liang M, Yang L (2016) In vitro antioxidant activity of rice protein affected by alkaline degree and gastrointestinal protease digestion. J Sci Food Agric 96:4940–4950

    Article  CAS  PubMed  Google Scholar 

  15. Wang Z, Liu Y, Li H, Yang L (2016) Rice proteins, extracted by alkali and α-amylase, differently affect in vitro antioxidant activity. Food Chem 206:137–145

    Article  CAS  PubMed  Google Scholar 

  16. Wang Z, Li H, Liang M, Yang L (2016) Glutelin and prolamin, different components of rice protein, exert differently in vitro antioxidant activities. J Cereal Sci 72:108–116

    Article  CAS  Google Scholar 

  17. Li H, He H, Wang Z, Cai J, Sun B, Wu Q, Zhang Y, Zhou G, Yang L (2016) Rice protein suppresses ROS generation and stimulates antioxidant gene expression via Nrf2 activation in adult rats. Gene 585:256–264

    Article  CAS  PubMed  Google Scholar 

  18. Nguyen T, Nioi P, Pickett CB (2009) The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 284:13291–13295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Atmaca G (2004) Antioxidant effects of sulfur-containing amino acids. Yonsei Med J 45:776–788

    Article  CAS  PubMed  Google Scholar 

  20. Yang L, Kadowaki M (2011) Addition of methionine to rice protein affects hepatic cholesterol output inducing hypocholesterolemia in rats fed cholesterol-free diets. J Med Food 14:445–453

    Article  CAS  PubMed  Google Scholar 

  21. Balkan J, Doğru-Abbasoğlu S, Çevikbaş U, Aykaç-Toker G, Uysal M (2004) Methionine supplementation did not augment oxidative stress, atherosclerotic changes and hepatotoxicity induced by high cholesterol diet in C57BL/6J mice. J Nutr Sci Vitaminol 50:258–264

    Article  CAS  PubMed  Google Scholar 

  22. Moundras C, Rémésy C, Levrat MA, Demigné C (1995) Methionine deficiency in rats fed soy protein induces hypercholesterolemia and potentiates lipoprotein susceptibility to peroxidation. Metabolism 44:1146–1152

    Article  CAS  PubMed  Google Scholar 

  23. Li H, Wang Z, Liang M, Cai L, Yang L (2018) Methionine augments antioxidant acitivity of rice protein during gastrointestinal digestion. Int J Mol Sci 20:868

    Article  CAS  Google Scholar 

  24. Zhang Y, Xu S, Jin H, Wang R, Peng Z (2015) Influence of selenium and methionine intake of the female chicken on lipid oxidation in the thigh muscles of progeny. Eur Food Res Technol 240:83–91

    Article  CAS  Google Scholar 

  25. Brosnan JT, Brosnan ME (1640S) The sulfur-containing amino acids: An overview. J Nutr 136:1636S–1640S

    Article  CAS  PubMed  Google Scholar 

  26. Brosnan JT, Brosnan ME, Bertolo RFP, Brunton JA (2007) Methionine: A metabolically unique amino acid. Livest Sci 112:2–7

    Article  Google Scholar 

  27. Martinov MV, Vitvitsky VM, Banerjee R, Ataullakhanov FI (2010) The logic of the hepatic methionine metabolic cycle. Biochim Biophys Acta 1804:89–96

    Article  CAS  PubMed  Google Scholar 

  28. McBean GJ (2012) The transsulfuration pathway: a source of cysteine for glutathione in astrocytes. Amino Acids 42:199–205

    Article  CAS  PubMed  Google Scholar 

  29. Wang Z, Liang M, Li H, Cai L, He H, Wu Q, Yang L (2019) l-Methionine activates Nrf2-ARE pathway to induce endogenous antioxidant activity for depressing ROS-derived oxidative stress in growing rats. J Sci Food Agric 99:4849–4862

    Article  CAS  PubMed  Google Scholar 

  30. Cadenas E, Davies KJA (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29:222–230

    Article  CAS  PubMed  Google Scholar 

  31. Reeves PG, Nielsen FH, Fahey GC (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN-76A rodent diet. J Nutr 123:1939–1951

    Article  CAS  PubMed  Google Scholar 

  32. Liang M, Wang Z, Li H, Cai L, Pan J, He H, Wu Q, Tang Y, Ma J, Yang L (2018) l-Arginine induces antioxidant response to prevent oxidative stress via stimulation of glutathione synthesis and activation of Nrf2 pathway. Food Chem Toxicol 115:315–328

    Article  CAS  PubMed  Google Scholar 

  33. Zielińska-Dawidziak M, Dwiecki K, Lewko K (2018) Modification of soybean and lupine sprouting conditions: influence on yield, ROS generation, and antioxidative systems. Eur Food Res Technol 244:1945–1952

    Article  CAS  Google Scholar 

  34. Karawita R, Siriwardhana N, Lee K, Heo M, Yeo I, Lee Y, Jeon Y (2005) Reactive oxygen species scavenging, metal chelation, reducing power and lipid peroxidation inhibition properties of different solvent fractions from Hizikia fusiformis. Eur Food Res Technol 220:363–371

    Article  CAS  Google Scholar 

  35. Kantorow M, Hawse JR, Cowell TL, Benhamed S, Pizarro GO, Reddy VN, Hejtmancik JF (2004) Methionine sulfoxide reductase A is important for lens cell viability and resistance to oxidative stress. Proc Natl Acad Sci USA 101:9654–9659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zhang H, Davies KJA, Forman HJ (2015) Oxidative stress response and Nrf2 signaling in aging. Free Radic Biol Med 88:314–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Lee BC, Kaya A, Gladyshev VN (2016) Methionine restriction and lifespan control. Ann N Y Acad Sci 1363:116–124

    Article  CAS  PubMed  Google Scholar 

  38. Perrone CE, Malloy VL, Orentreich DS, Orntreich N (2013) Metabolic adaptations to methionine restriction that benefit health and lifespan in rodents. Exp Gerontol 48:654–660

    Article  CAS  PubMed  Google Scholar 

  39. Cabreiro F, Picot CR, Friguet B, Petropoulos I (2006) Methionine sulfoxide reductases: Relevance to aging and protection against oxidative stress. Ann N Y Acad Sci 1067:37–44

    Article  CAS  PubMed  Google Scholar 

  40. Schöneich C (2005) Methionine oxidation by reactive oxygen species: reaction mechanisms and relevance to Alzheimer’s disease. Biochim Biophys Acta 1703:111–119

    Article  PubMed  CAS  Google Scholar 

  41. Landis GN, Tower J (2005) Superoxide dismutase evolution and life span regulation. Mech Ageing Dev 126:365–379

    Article  CAS  PubMed  Google Scholar 

  42. Prasad KN (2016) Simultaneous activation of Nrf2 and elevation of antioxidant compounds for reducing oxidative stress and chronic inflammation in human Alzheimer's disease. Mech Ageing Dev 153:41–47

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to the National Natural Science Foundation of China (31371755) for supporting this work. Also, we thank the Rice Research Institute of Heilongjiang Academy of Agricultural Science for providing rice grains.

Author information

Author notes

  1. Hui Li and Liang Cai have contributed equally to this article as first authors.

Authors and Affiliations

  1. Department of Food Science and Engineering, School of Chemistry and Chemical Engineering, Harbin Institute of Technology, 92 West Dazhi Street, Harbin, 150001, China

    Hui Li, Liang Cai, Mingcai Liang, Zhengxuan Wang & Lin Yang

  2. School of Life Science and Biotechnology, Harbin Institute of Technology, Harbin, 150001, China

    Yan Zhang & Qiong Wu

Authors
  1. Hui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liang Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mingcai Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhengxuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qiong Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lin Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lin Yang.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Compliance with ethics requirements

The animal study used in this study was approved and performed in conformity with the Guidelines of the Committee for the Experimental Animals of Harbin Institute of Technology. There were no human participants in this study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

SDS-PAGE analysis of rice protein and rice flour. M, marker; RF, rice flour; RP, rice protein. (PDF 141 kb)

Supplementary file2 (PDF 41 kb)

Supplementary file3 (PDF 45 kb)

Supplementary file4 (PDF 47 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, H., Cai, L., Liang, M. et al. Methionine augments endogenous antioxidant capacity of rice protein through stimulating MSR antioxidant system and activating Nrf2-ARE pathway in growing and adult rats. Eur Food Res Technol 246, 1051–1063 (2020). https://doi.org/10.1007/s00217-020-03464-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00217-020-03464-5

Keywords

Search

Navigation