Skip to main content
SpringerLink
Log in

Antimutagenic Activity as a Criterion of Potential Probiotic Properties

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

The antimutagenic activity of probiotic strains has been reported over several decades of studying the effects of probiotics. However, this activity is rarely considered an important criterion when choosing strains to produce probiotic preparations and functional food. Meanwhile, the association of antimutagenic activity with the prevention of oncological diseases, as well as with a decrease in the spread of resistant forms in the microbiota, indicates its importance for the selection of probiotics. Besides, an antimutagenic activity can be associated with probiotics’ broader systemic effects, such as geroprotective activity. The main mechanisms of such effects are considered to be the binding of mutagens, the transformation of mutagens, and inhibition of the transformation of promutagens into antimutagens. Besides, we should consider the possibility of interaction of the microbiota with regulatory processes in eukaryotic cells, in particular, through the effect on mitochondria. This work aims to systematize data on the antimutagenic activity of probiotics and emphasize antimutagenic activity as a significant criterion for the selection of probiotic strains.

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

Similar content being viewed by others

Availability of Data and Material

All data generated or analyzed during this study are included in this published article.

References

  1. Mazanko MS, Chistyakov VA, Prazdnova EV et al (2016) Dioxidine induces bacterial resistance to antibiotics. Mol Gen Microbiol Virol 31:227–232. https://doi.org/10.3103/S0891416816040066

    Article  Google Scholar 

  2. Silva MJ, Costa P, Dias A, Valente M, Louro H, Boavida MG (2005) Comparative analysis of the mutagenic activity of oxaliplatin and cisplatin in the Hprt gene of CHO cells. Env Mol Mutagenesis 46(2):104–115. https://doi.org/10.1002/em.20138

    Article  CAS  Google Scholar 

  3. Chistyakov VA, Prazdnova EV, Mazanko MS, Churilov MN, Chmyhalo VK (2018) Increase in bacterial resistance to antibiotics after cancer therapy with platinum-based drugs. Mol Biol (Mosk) 52(2):232–236. https://doi.org/10.1134/S0026893317050077

    Article  CAS  Google Scholar 

  4. Bhattacharya P, Mukherjee S, Mandal SM (2020) Fluoroquinolone antibiotics show genotoxic effect through DNA-binding and oxidative damage. Spectrochim Acta A Mol Biomol Spectrosc 227:117634. https://doi.org/10.1016/j.saa.2019.117634

    Article  CAS  PubMed  Google Scholar 

  5. DeBalsi KL, Hoff KE, Copeland WC (2017) Role of the mitochondrial DNA replication machinery in mitochondrial DNA mutagenesis, aging and age-related diseases. Ageing Res Rev 33:89–104. https://doi.org/10.1016/j.arr.2016.04.006

    Article  CAS  PubMed  Google Scholar 

  6. Giorgi C, Marchi S, Simoes ICM et al (2018) Mitochondria and reactive oxygen species in aging and age-related diseases. Int Rev Cell Mol Biol 340:209–344. https://doi.org/10.1016/bs.ircmb.2018.05.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Zhang L, Vijg J (2018) Somatic mutagenesis in mammals and its implications for human disease and aging. Annu Rev Genet 52:397–419. https://doi.org/10.1146/annurev-genet-120417-031501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Petra AI, Panagiotidou S, Hatziagelaki E et al (2015) Gut-microbiota-brain axis and its effect on neuropsychiatric disorders with suspected immune dysregulation. Clin Ther 37:984–995. https://doi.org/10.1016/j.clinthera.2015.04.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zhou Y, Li S, Pang Q, Miao Z (2020) Bacillus amyloliquefaciens BLCC1-0238 can effectively improve laying performance and egg quality via enhancing immunity and regulating reproductive hormones of laying hens. Probiotics Antimicrob Proteins 12:246–252. https://doi.org/10.1007/s12602-019-9524-1

    Article  CAS  PubMed  Google Scholar 

  10. Li B, Etareri Evivie S, Lu J et al (2018) Lactobacillus helveticus KLDS1.8701 alleviates d -galactose-induced aging by regulating Nrf-2 and gut microbiota in mice. Food Funct 9:6586–6598. https://doi.org/10.1039/C8FO01768A

    Article  CAS  PubMed  Google Scholar 

  11. Vanderhoof J, Mitmesser S (2010) Probiotics in the management of children with allergy and other disorders of intestinal inflammation. Benef Microbes 1:351–356. https://doi.org/10.3920/BM2010.0034

    Article  CAS  PubMed  Google Scholar 

  12. Kanmani P, Satish Kumar R, Yuvaraj N et al (2013) Probiotics and its functionally valuable products-a review. Crit Rev Food Sci Nutr 53:641–658. https://doi.org/10.1080/10408398.2011.553752

    Article  CAS  PubMed  Google Scholar 

  13. Wu J, Zhang Y, Ye L, Wang C (2020) The anti-cancer effects and mechanisms of lactic acid bacteria exopolysaccharides in vitro: a review. Carbohydr Polym. 117308. https://doi.org/10.1016/j.carbpol.2020.117308

  14. Pool-Zobel BL, Neudecker C, Domizlaff I et al (1996) Lactobacillus- and Bifidobacterium-mediated antigenotoxicity in the colon of rats. Nutr Cancer 26:365–380. https://doi.org/10.1080/01635589609514492

    Article  CAS  PubMed  Google Scholar 

  15. Reddy BS, Rivenson A (1993) Inhibitory effect of Bifidobacterium longum on colon, mammary, and liver carcinogenesis induced by 2-amino-3-methylimidazo[4,5-f]quinoline, a food mutagen. Cancer Res 53:3914–3918

    CAS  PubMed  Google Scholar 

  16. Yun S-I (2004) The binding of Bacillus natto isolated from natto to heterocyclic pyrolysates. World J Microbiol Biotechnol 20:469–474. https://doi.org/10.1023/B:WIBI.0000040396.11236.e0

    Article  CAS  Google Scholar 

  17. Hong HA, Duc LH, Cutting SM (2005) The use of bacterial spore formers as probiotics. FEMS Microbiol Rev 29:813–835. https://doi.org/10.1016/j.femsre.2004.12.001

    Article  CAS  PubMed  Google Scholar 

  18. Makarenko MS, Chistyakov VA, Usatov AV et al (2019) The impact of Bacillus subtilis KATMIRA1933 supplementation on telomere length and mitochondrial DNA damage of laying hens. Probiotics Antimicrob Proteins 11:588–593. https://doi.org/10.1007/s12602-018-9440-9

    Article  CAS  PubMed  Google Scholar 

  19. Prazdnova EV, Mazanko MS, Bren AB et al (2019) SOS response inhibitory properties by potential probiotic formulations of Bacillus amyloliquefaciens B-1895 and Bacillus subtilis KATMIRA1933 obtained by solid-state fermentation. Curr Microbiol 76:312–319. https://doi.org/10.1007/s00284-018-01623-2

    Article  CAS  PubMed  Google Scholar 

  20. Sreekumar O, Hosono A (2011) The antimutagenic properties of a polysaccharide produced by Bifidobacterium longum and its cultured milk against some heterocyclic amines. Can J Microbiol 44(11):1029–1036. https://doi.org/10.1139/w98-103

    Article  Google Scholar 

  21. Lo P-R, Yu R-C, Chou C-C, Huang E-C (2004) Determinations of the antimutagenic activities of several probiotic bifidobacteria under acidic and bile conditions against benzo[a]pyrene by a modified Ames test. Int J Food Microbiol 93:249–257. https://doi.org/10.1016/j.ijfoodmicro.2003.11.008

    Article  CAS  PubMed  Google Scholar 

  22. Lankaputhra WEV, Shah NP (1998) Antimutagenic properties of probiotic bacteria and of organic acids. Mutat Res 397:169–182. https://doi.org/10.1016/S0027-5107(97)00208-X

    Article  CAS  PubMed  Google Scholar 

  23. Commane D, Hughes R, Shortt C, Rowland I (2005) The potential mechanisms involved in the anti-carcinogenic action of probiotics. Mutat Res 591:276–289. https://doi.org/10.1016/j.mrfmmm.2005.02.027

    Article  CAS  PubMed  Google Scholar 

  24. Ljungh A, Wadström T (2006) Lactic acid bacteria as probiotics. Curr Issues Intest Microbiol 7:73–89

    CAS  PubMed  Google Scholar 

  25. Nissle A (1918) Die antagonistische behandlung chronischer darmstörungen mit colibakterien. Med Klin 2:29–30

    Google Scholar 

  26. Janosch D, Dubbert S, Eiteljörge K et al (2019) Anti-genotoxic and anti-mutagenic activity of Escherichia coli Nissle 1917 as assessed by in vitro tests. Benef Microbes 10:449–461. https://doi.org/10.3920/BM2018.0113

    Article  CAS  PubMed  Google Scholar 

  27. Bocci A, Sebastiani B, Trotta F, Federici E, Cenci G (2015) In vitro inhibition of 4-nitroquinoline-1-oxide genotoxicity by probiotic Lactobacillus rhamnosus IMC501. J Microbiol Biotechnol 25:1680–1686. https://doi.org/10.4014/jmb.1501.01086

    Article  CAS  PubMed  Google Scholar 

  28. Apás AL, González SN, Arena ME (2014) Potential of goat probiotic to bind mutagens. Anaerobe 28:8–12. https://doi.org/10.1016/j.anaerobe.2014.04.004

    Article  CAS  PubMed  Google Scholar 

  29. Knasmüller S, Steinkellner H, Hirschl AM et al (2001) Impact of bacteria in dairy products and of the intestinal microflora on the genotoxic and carcinogenic effects of heterocyclic aromatic amines. Mutat Res 480–481:129–138. https://doi.org/10.1016/S0027-5107(01)00176-2

    Article  PubMed  Google Scholar 

  30. Chalova VI, Lingbeck JM, Kwon YM, Ricke SC (2008) Extracellular antimutagenic activities of selected probiotic Bifidobacterium and Lactobacillus spp. as a function of growth phase. J Environ Sci Health B 43:193–198. https://doi.org/10.1080/03601230701795262

    Article  CAS  PubMed  Google Scholar 

  31. Hosoda M, Hashimoto H, Morita H et al (1992) Antimutagenicity of milk cultured with lactic acid bacteria against N-methyl-N’-nitro-N-nitrosoguanidine. J Dairy Sci 75:976–981. https://doi.org/10.3168/jds.S0022-0302(92)77839-4

    Article  CAS  PubMed  Google Scholar 

  32. Kim HS, Lee SY, Kang HJ et al (2019) Effects of six different starter cultures on mutagenicity and biogenic amine concentrations in fermented sausages treated with vitamins C and E. Food Sci Anim Resour 39:877–887. https://doi.org/10.5851/kosfa.2019.e66

    Article  PubMed  PubMed Central  Google Scholar 

  33. Bodana AR, Rao DR (1990) Antimutagenic activity of milk fermented by Streptococcus thermophilus and Lactobacillus bulgaricus. J Dairy Sci 73:3379–3384. https://doi.org/10.3168/jds.S0022-0302(90)79033-9

    Article  CAS  PubMed  Google Scholar 

  34. Bakalinsky AT, Nadathur SR, Carney JR, Gould SJ (1996) Antimutagenicity of yogurt. Mutat Res 350:199–200. https://doi.org/10.1016/0027-5107(95)00113-1

    Article  PubMed  Google Scholar 

  35. Irecta-Nájera CA, Del Rosario H-López M, Casas-Solís J et al (2017) Protective effect of Lactobacillus casei on DMH-induced colon carcinogenesis in mice. Probiotics Antimicrob Proteins 9:163–171. https://doi.org/10.1007/s12602-017-9253-2

    Article  CAS  PubMed  Google Scholar 

  36. Sharma M, Chandel D, Shukla G (2020) Antigenotoxicity and cytotoxic potentials of metabiotics extracted from isolated probiotic, Lactobacillus rhamnosus MD 14 on Caco-2 and HT-29 human colon cancer cells. Nutr Cancer 72:110–119. https://doi.org/10.1080/01635581.2019.1615514

    Article  CAS  PubMed  Google Scholar 

  37. Ahmadi MA, Ebrahimi MT, Mehrabian S et al (2014) Antimutagenic and anticancer effects of lactic acid bacteria isolated from Tarhana through Ames test and phylogenetic analysis by 16S rDNA. Nutr Cancer 66:1406–1413. https://doi.org/10.1080/01635581.2014.956254

    Article  CAS  PubMed  Google Scholar 

  38. Faridnia F, Hussin A, Saari N et al (2010) In vitro binding of mutagenic heterocyclic aromatic amines by Bifidobacterium pseudocatenulatum G4. Benef Microbes 1:149–154. https://doi.org/10.3920/BM2009.0035

    Article  CAS  PubMed  Google Scholar 

  39. Bolognani F, Rumney CJ, Rowland IR (1997) Influence of carcinogen binding by lactic acid-producing bacteria on tissue distribution and in vivo mutagenicity of dietary carcinogens. Food Chem Toxicol 35:535–545. https://doi.org/10.1016/S0278-6915(97)00029-X

    Article  CAS  PubMed  Google Scholar 

  40. Caldini G, Trotta F, Cenci G (2002) Inhibition of 4-nitroquinoline-1-oxide genotoxicity by Bacillus strains. Res Microbiol 153:165–171. https://doi.org/10.1016/S0923-2508(02)01302-5

    Article  CAS  PubMed  Google Scholar 

  41. Cenci G, Caldini G, Trotta F, Bosi P (2008) In vitro inhibitory activity of probiotic spore-forming bacilli against genotoxins. Lett Appl Microbiol l46:331–337. https://doi.org/10.1111/j.1472-765X.2007.02314.x

  42. Jiang T, Qiao H, Zheng Z et al (2016) Lactic acid production from pretreated hydrolysates of corn stover by a newly developed Bacillus coagulans strain. PLoS ONE 11:e0149101. https://doi.org/10.1371/journal.pone.0149101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Vorob’eva LI, Cherdyntseva TA, Abilev SK, (1995) Antimutagenic action of bacterial culture liquid on mutagenesis induced by 2-nitrofluorene in Salmonella typhimurium strains. Genetika 31:901–907

    Google Scholar 

  44. Belicová A, Križková L, Dobias J et al (2004) Synergic activity of selenium and probiotic bacterium Enterococcus faecium M-74 against selected mutagens in Salmonella assay. Folia Microbiol 49:301–305. https://doi.org/10.1007/BF02931047

    Article  Google Scholar 

  45. Chistyakov VA, Prazdnova EV, Mazanko MS, Bren AB (2018) The use of biosensors to explore the potential of probiotic strains to reduce the SOS response and mutagenesis in bacteria. Biosensors 8:25. https://doi.org/10.3390/bios8010025

    Article  CAS  PubMed Central  Google Scholar 

  46. Verdenelli MC et al (2010) Investigation of the antigenotoxic properties of the probiotic Lactobacillus rhamnosus IMC 501® by gas chromatography-mass spectrometry. Ital J Food Sci 22(4):473–478

    CAS  Google Scholar 

  47. Stidl R, Sontag G, Koller V, Knasmüller S (2008) Binding of heterocyclic aromatic amines by lactic acid bacteria: Results of a comprehensive screening trial. Mol Nutr Food Res 52:322–329. https://doi.org/10.1002/mnfr.200700034

    Article  CAS  PubMed  Google Scholar 

  48. Nadathur SR, Gould SJ, Bakalinsky AT (1994) Antimutagenicity of fermented milk. J Dairy Sci 77:3287–3295. https://doi.org/10.3168/jds.S0022-0302(94)77269-6

    Article  CAS  PubMed  Google Scholar 

  49. Chang JH, Shim YY, Cha SK, Chee KM (2010) Probiotic characteristics of lactic acid bacteria isolated from kimchi. J Appl Microbiol 109(1):220–230. https://doi.org/10.1111/j.1365-2672.2009.04648.x

    Article  CAS  PubMed  Google Scholar 

  50. Kumar A, Singh NK, Sinha PR (2010) Inhibition of 1,2-dimethylhydrazine induced colon genotoxicity in rats by the administration of probiotic curd. Mol Biol Rep 37(3):1373–1376. https://doi.org/10.1007/s11033-009-9519-1

  51. Ambalam P, Dave JM, Nair BM, Vyas BR (2011) In vitro mutagen binding and antimutagenic activity of human Lactobacillus rhamnosus 231. Anaerobe 17(5):217–222. https://doi.org/10.1016/j.anaerobe.2011.07.001

    Article  CAS  PubMed  Google Scholar 

  52. Chooruk A, Piwat S, Teanpaisan R (2017) Antioxidant activity of various oral Lactobacillus strains. J Appl Microbiol 123:271–279. https://doi.org/10.1111/jam.13482

    Article  CAS  PubMed  Google Scholar 

  53. Li Z, Teng J, Lyu Y et al (2019) Enhanced antioxidant activity for apple juice fermented with Lactobacillus plantarum ATCC14917. Molecules 24:51. https://doi.org/10.3390/molecules24010051

    Article  CAS  Google Scholar 

  54. Song MW, Jang HJ, Paik K-TK, H-D, (2019) Probiotic and antioxidant properties of novel Lactobacillus brevis KCCM 12203P isolated from kimchi and evaluation of immune-stimulating activities of its heat-killed cells in RAW 264.7 cells. J Microbiol Biotechnol 29:1894–1903. https://doi.org/10.4014/jmb.1907.07081

    Article  CAS  PubMed  Google Scholar 

  55. Huang G, Pan H, Zhu Z, Li Q (2020) The complete genome sequence of Bifidobacterium longum LTBL16, a potential probiotic strain from healthy centenarians with strong antioxidant activity. Genomics 112:769–773. https://doi.org/10.1016/j.ygeno.2019.05.015

    Article  CAS  PubMed  Google Scholar 

  56. Bernini LJ, Simão ANC, de Souza CHB et al (2018) Effect of Bifidobacterium lactis HN019 on inflammatory markers and oxidative stress in subjects with and without the metabolic syndrome. Br J Nutr 120:645–652. https://doi.org/10.1017/S0007114518001861

    Article  CAS  PubMed  Google Scholar 

  57. Wang B, Xu H, Xu F et al (2015) Efficacy of oral Bifidobacterium bifidum ATCC 29521 on microflora and antioxidant in mice. Can J Microbiol 62(3):249–262. https://doi.org/10.1139/cjm-2015-0685

    Article  CAS  PubMed  Google Scholar 

  58. Pieniz S, Andreazza R, Okeke BC et al (2015) Antimicrobial and antioxidant activities of Enterococcus species isolated from meat and dairy products. Braz J Biol 75:923–931. https://doi.org/10.1590/1519-6984.02814

    Article  CAS  PubMed  Google Scholar 

  59. Riane K, Ouled-Haddar H, Alyane M et al (2019) Assessment of Streptococcus salivarius sp thermophilus antioxidant efficiency and its role in reducing paracetamol hepatotoxicity. Iran J Biotechnol 17:58–66. https://doi.org/10.30498/ijb.2019.91761

  60. Rahman MdS, Hee Choi Y, Seok Choi Y et al (2018) A novel antioxidant peptide, purified from Bacillus amyloliquefaciens, showed strong antioxidant potential via Nrf-2 mediated heme oxygenase-1 expression. Food Chem 239:502–510. https://doi.org/10.1016/j.foodchem.2017.06.106

    Article  CAS  PubMed  Google Scholar 

  61. Wang Y, Wu Y, Wang Y et al (2017) Bacillus amyloliquefaciens SC06 alleviates the oxidative stress of IPEC-1 via modulating Nrf2/Keap1 signaling pathway and decreasing ROS production. Appl Microbiol Biotechnol 101:3015–3026. https://doi.org/10.1007/s00253-016-8032-4

    Article  CAS  PubMed  Google Scholar 

  62. Ton AMM, Campagnaro BP, Alves GA et al (2020) Oxidative stress and dementia in Alzheimer’s patients: effects of synbiotic supplementation. Oxid Med Cell Longev 2020:2638703. https://doi.org/10.1155/2020/2638703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Morotomi M, Mutal M (1986) In vitro binding of potent mutagenic pyrolyzates to intestinal bacteria. J Natl Cancer Inst 77:195–201. https://doi.org/10.1093/jnci/77.1.195

    Article  CAS  PubMed  Google Scholar 

  64. Zhang XB, Ohta Y (1991) Binding of mutagens by fractions of the cell wall skeleton of lactic acid bacteria on mutagens. J Dairy Sci 74:1477–1481. https://doi.org/10.3168/jds.S0022-0302(91)78306-9

    Article  CAS  PubMed  Google Scholar 

  65. Zhang XB, Ohta Y (1993) Antimutagenicity of cell fractions of microorganisms on potent mutagenic pyrolysates. Mutat Res Genet Toxicol Environ Mutagen 298:247–253. https://doi.org/10.1016/0165-1218(93)90003-V

    Article  CAS  Google Scholar 

  66. Zhang XB, Ohta Y, Hosono A (1990) Antimutagenicity and binding of lactic acid bacteria from a Chinese cheese to mutagenic pyrolyzates. J Dairy Sci 73:2702–2710. https://doi.org/10.3168/jds.S0022-0302(90)78955-2

    Article  CAS  PubMed  Google Scholar 

  67. Cummings J (1983) Fermentation in the human large intestine: evidence and implications for health. Lancet 321:1206–1209. https://doi.org/10.1016/S0140-6736(83)92478-9

    Article  Google Scholar 

  68. Aguilar-Toalá JE, Santiago-López L, Peres CM et al (2017) Assessment of multifunctional activity of bioactive peptides derived from fermented milk by specific Lactobacillus plantarum strains. J Dairy Sci 100:65–75. https://doi.org/10.3168/jds.2016-11846

    Article  CAS  PubMed  Google Scholar 

  69. Hsieh M-L, Chou C-C (2006) Mutagenicity and antimutagenic effect of soymilk fermented with lactic acid bacteria and bifidobacteria. Int J Food Microbiol 111:43–47. https://doi.org/10.1016/j.ijfoodmicro.2006.04.034

    Article  CAS  PubMed  Google Scholar 

  70. Hsieh M-L, Fang SW, Yu R-C, Chou C-C (2007) Possible mechanisms of antimutagenicity in fermented soymilk prepared with a coculture of Streptococcus infantis and Bifidobacterium infantis. J Food Prot 70:1025–1028. https://doi.org/10.4315/0362-028X-70.4.1025

    Article  CAS  PubMed  Google Scholar 

  71. Sah BNP, Vasiljevic T, McKechnie S, Donkor ON (2014) Effect of probiotics on antioxidant and antimutagenic activities of crude peptide extract from yogurt. Food Chem 156:264–270. https://doi.org/10.1016/j.foodchem.2014.01.105

    Article  CAS  PubMed  Google Scholar 

  72. Rhee C-H, Park H-D (2001) Three glycoproteins with antimutagenic activity identified in Lactobacillus plantarum KLAB21. Appl Environ Microbiol 67:3445–3449. https://doi.org/10.1128/AEM.67.8.3445-3449.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Nakagawa H, Shiozaki T, Kobatake E et al (2016) Effects and mechanisms of prolongevity induced by Lactobacillus gasseri SBT2055 in Caenorhabditis elegans. Aging Cell 15:227–236. https://doi.org/10.1111/acel.12431

    Article  CAS  PubMed  Google Scholar 

  74. Savustyanenko AV (2016) Mechanisms of action of probiotics based on Bacillus subtilis. Actual Infectology [RU] 2(11):35–44. https://doi.org/10.22141/2312-413x.2.11.2016.77529

  75. Ahire JJ, Mokashe NU, Patil HJ, Chaudhari BL (2013) Antioxidative potential of folate producing probiotic Lactobacillus helveticus CD6. J Food Sci Technol 50:26–34. https://doi.org/10.1007/s13197-011-0244-0

    Article  CAS  PubMed  Google Scholar 

  76. Landis GN, Tower J (2005) Superoxide dismutase evolution and life span regulation. Mech Ageing Dev 126:365–379. https://doi.org/10.1016/j.mad.2004.08.012

    Article  CAS  PubMed  Google Scholar 

  77. Kullisaar T, Zilmer M, Mikelsaar M et al (2002) Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol 72:215–224. https://doi.org/10.1016/S0168-1605(01)00674-2

    Article  CAS  PubMed  Google Scholar 

  78. Kim HS, Chae HS, Jeong SG et al (2005) In vitro antioxidative properties of lactobacilli. Asian-australas J Anim Sci 19:262–265.

  79. LeBlanc JG, del Carmen S, Miyoshi A et al (2011) Use of superoxide dismutase and catalase producing lactic acid bacteria in TNBS induced Crohn’s disease in mice. J Biotechnol 151:287–293. https://doi.org/10.1016/j.jbiotec.2010.11.008

    Article  CAS  PubMed  Google Scholar 

  80. Zulueta A, Maurizi A, Frígola A et al (2009) Antioxidant capacity of cow milk, whey and deproteinized milk. Int Dairy J 19:380–385. https://doi.org/10.1016/j.idairyj.2009.02.003

    Article  CAS  Google Scholar 

  81. Power O, Jakeman P, FitzGerald RJ (2013) Antioxidative peptides: enzymatic production, in vitro and in vivo antioxidant activity and potential applications of milk-derived antioxidative peptides. Amino Acids 44:797–820. https://doi.org/10.1007/s00726-012-1393-9

    Article  CAS  PubMed  Google Scholar 

  82. Gjorgievski N, Tomovska J, Dimitrovska G et al (2014) Determination of the antioxidant activity in yogurt. J HygEng Des 8:88–92

    Google Scholar 

  83. Solieri L, Rutella GS, Tagliazucchi D (2015) Impact of non-starter lactobacilli on release of peptides with angiotensin-converting enzyme inhibitory and antioxidant activities during bovine milk fermentation. Food Microbiol 51:108–116. https://doi.org/10.1016/j.fm.2015.05.012

    Article  CAS  PubMed  Google Scholar 

  84. Gagnon M, Savard P, Rivière A et al (2015) Bioaccessible antioxidants in milk fermented by Bifidobacterium longum subsp. longum strains. Bio Med Res Int 2015:16938. https://doi.org/10.1155/2015/169381

  85. Kullisaar T, Songisepp E, Aunapuu M et al (2010) Complete glutathione system in probiotic Lactobacillus fermentum ME-3. Appl Biochem Microbiol 46:481–486. https://doi.org/10.1134/S0003683810050030

    Article  CAS  Google Scholar 

  86. BerniCanani R, Sangwan N, Stefka AT et al (2016) Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants. ISME J10:742–750. https://doi.org/10.1038/ismej.2015.151

    Article  CAS  Google Scholar 

  87. Canani RB, Filippis FD, Nocerino R et al (2017) Specific signatures of the gut microbiota and increased levels of butyrate in children treated with fermented cow’s milk containing heat-killed Lactobacillus paracasei CBA L74. Appl Environ Microbiol 83(19):e01206-e1217. https://doi.org/10.1128/AEM.01206-17

    Article  CAS  Google Scholar 

  88. Endo H, Niioka M, Kobayashi N et al (2013) Butyrate-producing probiotics reduce nonalcoholic fatty liver disease progression in rats: new insight into the probiotics for the gut-liver axis. PLoS One 8:e63388. https://doi.org/10.1371/journal.pone.0063388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Lutgendorff F, Nijmeijer RM, Sandström PA et al (2009) Probiotics prevent intestinal barrier dysfunction in acute pancreatitis in rats via induction of ileal mucosal glutathione biosynthesis. PLoS One 4:e4512. https://doi.org/10.1371/journal.pone.0004512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Yang H, Li X, Li X et al (2015) Identification of lipopeptide isoforms by MALDI-TOF-MS/MS based on the simultaneous purification of iturin, fengycin, and surfactin by RP-HPLC. Anal Bioanal Chem 407:2529–2542. https://doi.org/10.1007/s00216-015-8486-8

    Article  CAS  PubMed  Google Scholar 

  91. Vasilchenko AS, Rogozhin EA (2019) Sub-inhibitory effects of antimicrobial peptides. Front Microbiol 10:1160. https://doi.org/10.3389/fmicb.2019.01160

    Article  PubMed  PubMed Central  Google Scholar 

  92. Kozina LS (2007) Effects of bioactive tetrapeptides on free-radical processes. Bull Exp Biol Med 143:744–746. https://doi.org/10.1007/s10517-007-0230-8

    Article  CAS  PubMed  Google Scholar 

  93. Christen S, Peterhans E, Stocker R (1990) Antioxidant activities of some tryptophan metabolites: possible implication for inflammatory diseases. Proc Natl Acad Sci U S A 87:2506–2510. https://doi.org/10.1073/pnas.87.7.2506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Chalisova NI, Lopatina NG, Kamishev NG et al (2012) Effect of tripeptide lys-glu-asp on physiological activity of neuroimmunoendocrine system cells. Bull Exp Biol Med 153:569–572. https://doi.org/10.1007/s10517-012-1768-7

    Article  CAS  PubMed  Google Scholar 

  95. Ashapkin V, Khavinson V, Shilovsky G et al (2020) Gene expression in human mesenchymal stem cell aging cultures: modulation by short peptides. Mol Biol Rep 47:4323–4329. https://doi.org/10.1007/s11033-020-05506-3

    Article  CAS  PubMed  Google Scholar 

  96. Jones RM, Desai C, Darby TM et al (2015) Lactobacilli modulate epithelial cytoprotection through the Nrf2 pathway. Cell Rep 12:1217–1225. https://doi.org/10.1016/j.celrep.2015.07.042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Diao Y, Xin Y, Zhou Y et al (2014) Extracellular polysaccharide from Bacillus sp. strain LBP32 prevents LPS-induced inflammation in RAW 264.7 macrophages by inhibiting NF-κB and MAPKs activation and ROS production. Int Immunopharmacol 18:12–19. https://doi.org/10.1016/j.intimp.2013.10.021

    Article  CAS  PubMed  Google Scholar 

  98. Seth A, Yan F, Polk DB, Rao RK (2008) Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism. Am J Physiol Gastrointest Liver Physiol 294:G1060–G1069. https://doi.org/10.1152/ajpgi.00202.2007

    Article  CAS  PubMed  Google Scholar 

  99. Mazzoli A, Donadio G, Lanzilli M et al (2019) Bacillus megaterium SF185 spores exert protective effects against oxidative stress in vivo and in vitro. Sci Rep 9:12082. https://doi.org/10.1038/s41598-019-48531-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Shen Q, Shang N, Li P (2011) In vitro and in vivo antioxidant activity of Bifidobacterium animalis 01 isolated from centenarians. Curr Microbiol 62:1097–1103. https://doi.org/10.1007/s00284-010-9827-7

    Article  CAS  PubMed  Google Scholar 

  101. Achuthan AA, Duary RK, Madathil A et al (2012) Antioxidative potential of lactobacilli isolated from the gut of Indian people. Mol Biol Rep 39:7887–7897. https://doi.org/10.1007/s11033-012-1633-9

    Article  CAS  PubMed  Google Scholar 

  102. Wegh CAM, Geerlings SY, Knol J et al (2019) Postbiotics and their potential applications in early life nutrition and beyond. Int J Mol Sci 20:4673. https://doi.org/10.3390/ijms20194673

    Article  CAS  PubMed Central  Google Scholar 

  103. Hoarau C, Lagaraine C, Martin L et al (2006) Supernatant of Bifidobacterium breve induces dendritic cell maturation, activation, and survival through a toll-like receptor 2 pathway. J Allergy Clin Immunol 117:696–702. https://doi.org/10.1016/j.jaci.2005.10.043

    Article  CAS  PubMed  Google Scholar 

  104. Ménard S, Laharie D, Asensio C et al (2005) Bifidobacterium breve and Streptococcus thermophilus secretion products enhance T helper 1 immune response and intestinal barrier in mice. Exp Biol Med (Maywood) 230:749–756. https://doi.org/10.1177/153537020523001008

    Article  Google Scholar 

  105. Corsello G, Carta M, Marinello R et al (2017) Preventive effect of cow’s milk fermented with Lactobacillus paracasei CBA L74 on common infectious diseases in children: a multicenter randomized controlled trial. Nutrients 9:669. https://doi.org/10.3390/nu9070669

    Article  CAS  PubMed Central  Google Scholar 

  106. De Marco S, Sichetti M, Muradyan D et al (2018) Probiotic cell-free supernatants exhibited anti-inflammatory and antioxidant activity on human gut epithelial cells and macrophages stimulated with LPS. Evid Based Complement Alternat Med 2018:1756308. https://doi.org/10.1155/2018/1756308

    Article  PubMed  PubMed Central  Google Scholar 

  107. Wang K, Li W, Rui X et al (2014) Characterization of a novel exopolysaccharide with antitumor activity from Lactobacillus plantarum 70810. Int J Biol Macromol 63:133–139. https://doi.org/10.1016/j.ijbiomac.2013.10.036

    Article  CAS  PubMed  Google Scholar 

  108. Li W, Ji J, Chen X et al (2014) Structural elucidation and antioxidant activities of exopolysaccharides from Lactobacillus helveticus MB2-1. CarbohydrPolym 102:351–359. https://doi.org/10.1016/j.carbpol.2013.11.053

    Article  CAS  Google Scholar 

  109. Khalil ES, Abd Manap MY, Mustafa S et al (2018) Probiotic properties of exopolysaccharide-producing Lactobacillus strains isolated from tempoyak. Molecules 23:398. https://doi.org/10.3390/molecules23020398

    Article  CAS  PubMed Central  Google Scholar 

  110. Skulachev VP (2010) How to cancel the program of body aging? Russ J Gen Chem 80:1523–1541. https://doi.org/10.1134/S1070363210070492

    Article  CAS  Google Scholar 

  111. Skulachev VP (2011) Aging as a particular case of phenoptosis, the programmed death of an organism (A response to Kirkwood and Melov “On the programmed/non-programmed nature of ageing within the life history”). Aging 3:1120–1123. https://doi.org/10.18632/aging.100403

  112. Anisimov VN, Egorov MV, Krasilshchikova MS et al (2011) Effects of the mitochondria-targeted antioxidant SkQ1 on lifespan of rodents. Aging 3:1110–1119. https://doi.org/10.18632/aging.100404

  113. Chae S, Ahn BY, Byun K et al (2013) A systems approach for decoding mitochondrial retrograde signaling pathways. Sci Signal 6(264):rs4. https://doi.org/10.1126/scisignal.2003266

  114. Shinjo S, Jiang S, Nameta M et al (2017) Disruption of the mitochondria-associated ER membrane (MAM) plays a central role in palmitic acid–induced insulin resistance. Exp Cell Res 359:86–93. https://doi.org/10.1016/j.yexcr.2017.08.006

    Article  CAS  PubMed  Google Scholar 

  115. Bajpai P, Darra A, Agrawal A (2018) Microbe-mitochondrion crosstalk and health: an emerging paradigm. Mitochondrion 39:20–25. https://doi.org/10.1016/j.mito.2017.08.008

    Article  CAS  PubMed  Google Scholar 

  116. Zolotukhin P, Kozlova Y, Dovzhik A et al (2013) Oxidative status interactome map: towards novel approaches in experiment planning, data analysis, diagnostics and therapy. Mol Biosyst 9:2085–2096. https://doi.org/10.1039/C3MB70096H

    Article  CAS  PubMed  Google Scholar 

  117. Lo S-C, Hannink M (2008) PGAM5 tethers a ternary complex containing Keap1 and Nrf2 to mitochondria. Exp Cell Res 314:1789–1803. https://doi.org/10.1016/j.yexcr.2008.02.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Niture SK, Jain AK, Shelton PM, Jaiswal AK (2011) Src subfamily kinases regulate nuclear export and degradation of transcription factor Nrf2 to switch off Nrf2-mediated antioxidant activation of cytoprotective gene expression. J Biol Chem 286:28821–28832. https://doi.org/10.1074/jbc.M111.255042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Zolotukhin PV, Belanova AA, Prazdnova EV et al (2016) Mitochondria as a signaling Hub and target for phenoptosis shutdown. Biochemistry 81:329–337. https://doi.org/10.1134/S0006297916040039

    Article  CAS  PubMed  Google Scholar 

  120. Stefanaki C, Bacopoulou F, Michos A (2018) The impact of probiotics’ administration on glycemic control, body composition, gut microbiome, mitochondria, and other hormonal signals in adolescents with prediabetes – a randomized, controlled trial study protocol. Contemp Clin Trials Commun 11:55–62. https://doi.org/10.1016/j.conctc.2018.06.002

    Article  PubMed  PubMed Central  Google Scholar 

  121. Zorov DB, Plotnikov EY, Silachev DN et al (2014) Microbiota and mitobiota. Putting an equal sign between mitochondria and bacteria. Biochemistry 79:1017–1031. https://doi.org/10.1134/S0006297914100046

    Article  CAS  PubMed  Google Scholar 

  122. Saint-Georges-Chaumet Y, Attaf D, Pelletier E, Edeas M (2015) Targeting microbiota-mitochondria inter-talk: microbiota control mitochondria metabolism. Cell Mol Biol (Noisy-le-grand) 61:121–124

  123. Edeas M, Weissig V (2013) Targeting mitochondria: strategies, innovations and challenges: the future of medicine will come through mitochondria. Mitochondrion 13:389–390. https://doi.org/10.1016/j.mito.2013.03.009

    Article  CAS  PubMed  Google Scholar 

  124. Prasun P (2019) Mitochondrial Medicine. In: Prasun P (ed) Chapter 1 - functions of mitochondria. Academic Press, pp 1–3

  125. Xu C, Qiao L, Ma L et al (2019) Biogenic selenium nanoparticles synthesized by Lactobacillus casei ATCC 393 alleviate intestinal epithelial barrier dysfunction caused by oxidative stress via Nrf2 signaling-mediated mitochondrial pathway. Iran J Neonatol 14:4491–4502. https://doi.org/10.2147/IJN.S199193

    Article  CAS  Google Scholar 

  126. Pallen MJ (2011) Time to recognise that mitochondria are bacteria? Trends Microbiol 19:58–64. https://doi.org/10.1016/j.tim.2010.11.001

    Article  CAS  PubMed  Google Scholar 

  127. Lobet E, Letesson J-J, Arnould T (2015) Mitochondria: a target for bacteria. Biochem Pharmacol 94:173–185. https://doi.org/10.1016/j.bcp.2015.02.007

    Article  CAS  PubMed  Google Scholar 

  128. Hosoi T, Ametani A, Kiuchi K, Kaminogawa S (2011) Improved growth and viability of lactobacilli in the presence of Bacillus subtilis (natto), catalase, or subtilisin. Can J Microbiol 46(10):892–897. https://doi.org/10.1139/w00-070

    Article  Google Scholar 

  129. Zhang Y-R, Xiong H-R, Guo X-H (2014) Enhanced viability of Lactobacillus reuteri for probiotics production in mixed solid-state fermentation in the presence of Bacillus subtilis. Folia Microbiol 59:31–36. https://doi.org/10.1007/s12223-013-0264-4

    Article  CAS  Google Scholar 

  130. Papadimitriou K, Zoumpopoulou G, Foligné B et al (2015) Discovering probiotic microorganisms: in vitro, in vivo, genetic and omics approaches. Front Microbiol 6:58. https://doi.org/10.3389/fmicb.2015.00058

    Article  PubMed  PubMed Central  Google Scholar 

  131. Zeiger E (2019) The test that changed the world: the Ames test and the regulation of chemicals. Mutat Res 841:43–48. https://doi.org/10.1016/j.mrgentox.2019.05.007

    Article  CAS  Google Scholar 

  132. Ragavan ML, Das N (2020) In vitro studies on therapeutic potential of probiotic yeasts isolated from various sources. Curr Microbiol 77(10):2821–2830. https://doi.org/10.1007/s00284-020-02100-5

    Article  CAS  PubMed  Google Scholar 

  133. Lee SB, Cosmas B, Park HD (2020) the antimutagenic and antioxidant activity of fermented milk supplemented with Cudrania tricuspidata powder. Foods 9(12):1762. https://doi.org/10.3390/foods9121762

    Article  CAS  PubMed Central  Google Scholar 

Download references

Funding

EVP, MSM, VAC, AAB, AGR, and EYK were financially supported by the Ministry of Science and Higher Education of the Russian Federation within the framework of the state task in the field of scientific activity (Southern Federal University, no. 0852–2020-0029). VAC and MLC acknowledge the support of the Government of the Russian Federation (contract No. 075–15-2019–1880).

Author information

Authors and Affiliations

  1. Academy of Biology and Biotechnologies, Southern Federal University, Prospect Stachki, 194/1, Rostov-on-Don, Russia

    Evgeniya V. Prazdnova, Maria S. Mazanko, Vladimir A. Chistyakov & Evgeniya Y. Kharchenko

  2. Center for Agrobiotechnology, Don State Technical University, Rostov-on-Don, Russia

    Evgeniya V. Prazdnova, Maria S. Mazanko, Vladimir A. Chistyakov & Michael L. Chikindas

  3. Evolutionary Biomedicine Laboratory, SCAMT Institute, ITMO University, Saint Petersburg, Russia

    Anna A. Bogdanova

  4. Cell Biophysics Laboratory, SCAMT Institute, ITMO University, Saint Petersburg, Russia

    Aleksandr G. Refeld

  5. Health Promoting Naturals Laboratory, School of Environmental and Biological Sciences, Rutgers State University, New Brunswick, NJ, USA

    Michael L. Chikindas

  6. I.M. Sechenov First Moscow State Medical University, Moscow, Russia

    Michael L. Chikindas

Authors
  1. Evgeniya V. Prazdnova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria S. Mazanko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vladimir A. Chistyakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anna A. Bogdanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aleksandr G. Refeld
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Evgeniya Y. Kharchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michael L. Chikindas
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Evgeniya V. Prazdnova conceived the original idea and performed the overall analysis. Maria S. Mazanko performed the analysis on antioxidant activity of probiotics. Vladimir A. Chistyakov supervised the project. Anna A. Bogdanova prepared figures and schemes and systematized the list of references. Aleksandr G.Refeld performed the analyses of recent reviews. Evgeniya Y.Kharchenko performed meta-analysis. Michael L. Chikindas was in charge of the overall direction and planning.

Corresponding author

Correspondence to Evgeniya V. Prazdnova.

Ethics declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prazdnova, E.V., Mazanko, M.S., Chistyakov, V.A. et al. Antimutagenic Activity as a Criterion of Potential Probiotic Properties. Probiotics & Antimicro. Prot. 14, 1094–1109 (2022). https://doi.org/10.1007/s12602-021-09870-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-021-09870-9

Keywords

Search

Navigation