Antimutagenic activity of Aspergillus awamori-fermented black soybean response to simulated digestive juice treatments and its antimutagenic mechanisms

https://doi.org/10.1016/j.lwt.2008.06.001Get rights and content

Abstract

Aspergillus awamori-fermented black soybeans, a potential healthy food ingredient, possess antimutagenicity against 4-nitroquinoline-N-oxide (4-NQO); a direct mutagen and benzo[a]pyrene (B[a]P; an indirect mutagen). Results of this study revealed that antimutagenic, desmutagenic, and blocking effects all contributed to the antimutagenicity of the methanol of fermented black soybean. However, the desmutagenic effect of the fermented black soybean extract on B[a]P is not caused by the interaction of intact B[a]P or S9 mixture with the extract. Instead, it is due to the interaction of B[a]P metabolites with the antimutagenic factors in the extract. Exposure to simulated gastric juice (pH 1.2) for 30 min or intestinal juice for 2 h resulted in a reduced antimutagenicity of fermented black soybean extract. Nevertheless, the simulated gastric juice treated-fermented black soybean extracts and the simulated intestinal juice treated-fermented black soybean extracts still possessed a considerable antimutagenic effect against 4-NQO and B[a]P.

Introduction

The black soybean (Glycine max (L.) Merr.) is a nutritionally rich food. Certain components of black soybeans such as isoflavone, sopponin, anthocyanin, and vitamin E have been shown to exert biological activity (Aparicio-Fernández et al., 2005, Cardador-Martinez et al., 2002, Miyazawa et al., 1999, Rao and Sung, 1995). In China, black soybeans were used to prepare traditional fermented products such as in-yu black soybeans, and in-si or tou si, the dried by-product of the mash black soybean sauce. The beneficial effects of black soybean were described in Ben-Tsao Gong Mu, an ancient Chinese Botanical Encyclopedia as early as the 16th century (Li, 1990).

Recently, researchers have also demonstrated that black soybeans inhibit low density lipoprotein oxidation (Takahashi et al., 2005) and reduce the incidence of DNA damage by cyclophosphamide (Ribeiro & Salvadori, 2003). Moreover, using Rhizopus azygosporus-fermented black soybean with rice has also been suggested as a way to develop a nutritious weaning food (Rodriguez-Bűrger, Mason, & Nielsen, 1998).

In the past few years, a series of studies of black soybean have been conducted in our laboratory in an attempt to develop healthy food that possesses beneficial properties. It was found that fermentation by filamentous fungi enhanced the antioxidative activity (Lee, Hung, & Chou, 2007) and the content of the bioactive isoflavone, aglycone, which has been linked to health benefits and well being (Lee & Chou, 2006). Additionally, fermentation was also found to enhance the antimutagenic effect of black soybeans against 4-NQO and B[a]P (Hung, Huang, & Chou, 2007). Further, it was also noted that the antimutagenicity of the fermented black soybean varied with the starter organism, mutagen, and the test strain of Salmonella typhimurium. These observations further support the suggestion of using fermented black soybean as an ingredient for the formulation of healthy food.

Dietary components, after ingestion, are exposure to gastric and intestinal juices. The chemical structure and properties of the dietary components may change in the presence of gastric juice, with its low pH, bile acid, and digestive enzymes, thus altering their functional properties. For example, it has been observed that the antimutagenicity of onion changes after exposure to stimulated gastric juice (pH 1.2) or intestinal juice, with increases or decreases in antimutagenicity depending on the kinds of onion, mutagen and the test strain of S. typhimurium. Lo, Yu, Chou, and Tsai (2002) also reported that the antimutagenic activity of probiotics changed after bile and acid treatments. Moreover, the exposure of lactic fermented soymilk to acid (pH 2.0) or bile salt has been reported to reduce antimutagenicity (Hsieh & Chou, 2006). Additionally, Vis, Plinck, Alink, and van Boekel (1998) observed that bile acid was a strong comutagenic to N-methyl-N-nitro-N-nitrosoguanidine (MNNG). In the present study, the possible mechanism of the antimutagenic effect of methanol extract of the Aspergillus awamori-fermented black soybean, which exhibited the most significant enhancement in antimutagenicity compared to the unfermented black soybean (Hung et al., 2007), was further explored. Finally, the antimutagenicity of the fermented black soybean extract in the presence of simulated gastric and intestinal juices was also examined.

Section snippets

Microorganisms and chemicals

In the present study, S. typhimurium TA98 and TA100, obtained from the Bioresources Collection and Research Center (BCRC), Hsinchu, Taiwan, were used as the test organisms. S. typhimurium TA100 results from the substitution of a leucine (GAG/CTC) by a proline (GGG/CCC). Mutagens that cause base-pair substitution mutations primarily at one of the GC pairs will revert this mutant to the wild-type state. In contrast to S. typhimurium TA100, S. typhimurium TA98 is a −1 frameshift mutation which

Bio-antimutagenic effect

It was reported that antimutagens may exert a bio-antimutagenic effect by modulating cellular mutagenic processes, i.e., by acting on DNA replication and repair processes after DNA is damaged by the mutagen (Chen and Yen, 1997, Kada et al., 1985). Previously, Kada et al. (1985) reported that epigallo–catechin–gallate, isolated from Japanese green tea (leaves of Camellia sinensis) exerted bio-antimutagenic effect by altering DNA-polymerase III in a mutator strain of Bacillus subtilis. Using

Conclusion

Based on the data obtained from the present study, it is concluded that bio-antimutagenic, desmutagenic, and blocking effects all contributed to the antimutagenicity of the methanol of fermented black soybean against 4-NQO and B[a]P in both S. typhimurium TA98 and TA100. On the other hand, exposure to simulated gastric juice (pH 1.2) for 30 min or intestinal juice for 2 h resulted in a reduced antimutagenicity of fermented black soybean extract. Nevertheless, these treated-fermented black soybean

Acknowledgement

This research was financially supported by The National Science Council, ROC (Taiwan) (NSC 95-2313-B-002-017).

References (30)

  • T. Sato et al.

    Mechanism of the desmutagenic effect of humic acid

    Mutation Research

    (1987)
  • M.Y. Shon et al.

    Antimutagenic, antioxidant and free radical scavenging activity of ethyl acetate extracts from white, yellow and red onions

    Food and Chemical Toxicology

    (2004)
  • G.C. Yen et al.

    Antimutagenicity of a partially fractionated Maillard reaction-product

    Food Chemistry

    (1993)
  • X. Aparicio-Fernández et al.

    Comparison of antimutagenic activity of phenolic compounds in newly harvested and stored common beans Phaseolus vulgaris against aflatoxin B1

    Journal of Food Science

    (2005)
  • A. Cardador-Martinez et al.

    Antimutagenic activity of natural phenolic compounds present in the common bean (Phaseolus vulgaris) against aflatoxin B1

    Food Additives and Contaminants

    (2002)
  • Cited by (15)

    • Therapeutic effects of polyphenols in fermented soybean and black soybean products

      2021, Journal of Functional Foods
      Citation Excerpt :

      Thus SSF can influence the enhancement of anti-cancer effects of soybean extract by converting glucoside isoflavones to aglycones (Hung, Huang, & Chou, 2007). An anti-mutagen material can act in two different ways by both modulating and inactivating mutagens or avoid the action of their precursors by blocking the activity of related enzymes (Hung, Wang, & Chou, 2009). Several studies investigated the antimutagenic activity of various fermented soybean and black soybean products and all of them revealed that fermentation causes a significant increase in the antimutagenic and anticancer activity of soybean (Chen, Inaba, Abe, & Hirota, 2003; Kiriakidis et al., 2005).

    • Inhibition of DNA oxidative damage and antimutagenic activity by dichloromethane extract of Brassica rapa var. rapa L. seeds

      2015, Industrial Crops and Products
      Citation Excerpt :

      So, diet rich in antioxidants and nutrients can helps in suppressing these genetic alterations through, prevention of mutations and helps in overcoming the oxidative stress which can boost the effective DNA repair. On the basis of mode of action, natural inhibitors of mutagenesis can be bioantimutagenic and desmutagenic (Hung et al., 2009). Bioantimutagen stops the mutation, after damage of genes by mutagen and desmutagen stops mutation before the mutagen’s effects on genes.

    • Antioxidant and antimutagenic activity of Curcuma caesia Roxb. rhizome extracts

      2015, Toxicology Reports
      Citation Excerpt :

      The inhibition of mutagenesis are grouped into two namely desmutagens and bioantimutagens. It has been hypothesised that bioantimutagens act as second stage inhibitors that blocks the mutagen before they could attack the DNA [46] and bioantimutagenic effect of phytochemicals is determined in co incubation method [47]. The different extracts of C. caesia Roxb.

    • Production of nigragillin and dihydrophaseic acid by biotransformation of litchi pericarp with Aspergillus awamori and their antioxidant activities

      2014, Journal of Functional Foods
      Citation Excerpt :

      It has been used in food preparation since ancient time and is generally recognised as safe (Schuster, Dunn-Coleman, Frisvad, & van Dijck, 2002). Enhancement in antioxidant (Chen, Huang, Lin, Hsu, & Chung, 2013) and antimutagenicity (Hung, Wang, & Chou, 2009) were observed after fermentation with A. awamori on several phenolics-enriched plant materials, and increased total phenolics content is generally considered as a key factor for bioactivity improvement. This viewpoint is supported by our previous study when litchi pericarp was employed as the substrate (Lin et al., 2012).

    • Production of quercetin, kaempferol and their glycosidic derivatives from the aqueous-organic extracted residue of litchi pericarp with Aspergillus awamori

      2014, Food Chemistry
      Citation Excerpt :

      Gottschalk, Oliveira, and Bon (2010) reported that Aspergillus awamori can produce many kinds of phenolic-related metabolic enzymes and hydrolytic enzymes which make it possible to be used as a new resource to transform the bioactive pheonolic compounds. Hung, Wang, and Chou (2009) have found that the antimutagenic activity of black bean can be increased after the A. awamori fermentation, which resulted in increased polyphenol contents. Thus, A. awamori exhibits a potential to be used as a resource to increase or transform the phenolic compounds present in plant waste.

    • Storage effects on the content of anthocyanin, mutagenicity and antimutagenicity of black soybean koji

      2010, LWT
      Citation Excerpt :

      The contents of anthocyanin and isoflavone were reported to be associated with the antimutagenicity of beans (Miyazawa, Sakano, Nakamura, & Kosaka, 1999; Azevedo et al., 2003; Lee & Chou, 2006). In the present study, we also found that reduction of antimutagenicity of black soybean koji during storage (Tables 4 and 5) was generally associated with a decrease in anthocyanin content (Table 1) and isoflavone content (Hung, Hwang, & Chou, 2009). Additionally, black soybean koji stored with both deoxidant and deoxidant was found to contain a higher isoflavone residual than those stored under other packaging conditions (Huang & Chou, 2009).

    View all citing articles on Scopus
    View full text