Abstract
Double-strand breaks in the DNA of the small intestine in male Wistar rats were studied using a neutral comet assay after 7 days of feeding with a single strain probiotic formulation Narine (Vitamax-E, Armenia), containing Lactobacillus acidophilus strain Er-2317/402 Narine, and putative probiotics L. rhamnosus Vahe and L. delbrueckii IAHAHI. Type 0 (undamaged DNA), type 1 (head diameter 13.18–17.08 μm), and type 2 (14.15-μm head diameter) damaged DNA comets were studied in control and lactobacilli-fed rats using the neutral comet assay. Lactobacilli-fed rats were shown to carry only type 0 (undamaged) DNA.
Thus, the effects of probiotic Lactobacillus acidophilus strain INMIA 9602 Er 317/402 and putative probiotic lactobacilli on DNA damage in the small intestine of Wistar rats in vivo was shown, and the neutral comet assay is suggested as a potential tool for the in vivo selection of putative probiotics with DNA-protective activity.
Similar content being viewed by others
References
Cannan WJ, Pederson DS (2016) Mechanisms and consequences of double-strand DNA break formation in chromatin. J Cell Physiol 231(1):3–14. https://doi.org/10.1002/jcp.25048
Schipler A, Iliakis G (2013) DNA double-strand–break complexity levels and their possible contributions to the probability for error-prone processing and repair pathway choice. Nucleic Acids Res 41(16):7589–7605. https://doi.org/10.1093/nar/gkt556
White RR, Vijg J (2016) Do DNA double-strand breaks drive aging? Mol Cell 63(5):729–738. https://doi.org/10.1016/j.molcel.2016.08.004
Nougayrède JP, Homburg S, Taieb F et al (2006) Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313:848–851. https://doi.org/10.1126/science.1127059
Cuevas-Ramos G, Petit CR, Marcq I, Boury M, Oswald E, Nougayrede JP (2010) Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci U S A 107(25):11537–11542. https://doi.org/10.1073/pnas.1001261107
Wei W, Ba Z, Gao M, Wu Y, Ma Y, Amiard S, White CI, Rendtlew Danielsen JM, Yang YG, Qi Y (2012) A role for small RNAs in DNA double-strand break repair. Cell 149(1):101–112. https://doi.org/10.1016/j.cell.2012.03.002
Chang HHY, Pannunzio NR, Adachi N, Lieber MR (2017) Non-homologous DNA end joining and alternative pathways to double-strand break repair. Nat Rev Mol Cell Biol 18:495–506. https://doi.org/10.1038/nrm.2017.48
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B et al (2014) Expert consensus document: the international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11:506–514
Kechagia M, Basoulis D, Konstantopoulou S, Dimitriadi D, Gyftopoulou K, Skarmoutsou N, Fakiri EM (2013) Health benefits of probiotics: a review. ISRN Nutr 2013:481651–481657. https://doi.org/10.5402/2013/481651
Kelesidis T, Pothoulakis C (2012) Efficacy and safety of the probiotic Saccharomyces boulardii for the prevention and therapy of gastrointestinal disorders. Therap Adv Gastroenterol 5(2):111–125. https://doi.org/10.1177/1756283X11428502
Balayan M, Manvelyan A, Marutyan S et al (2015) Impact of lactobacillus acidophilus INMIA 9602 Er-2 and Escherichia coli M-17 on some clinical blood characteristics of familial Mediterranean fever disease patients from the Armenian cohort. Int J Probiotics Prebiotics 10:91–95
Bagherpour G, Ghasemi H, Zand B, Zarei N, Roohvand F, Ardakani EM, Azizi M, Khalaj V (2018) Oral administration of recombinant Saccharomyces boulardii expressing ovalbumin-CPE fusion protein induces antibody response in mice. Front Microbiol 9:723. https://doi.org/10.3389/fmicb.2018.00723
Syngai GG, Gopi R, Bharali R, Dey S, Lakshmanan GMA, Ahmed G (2016) Probiotics - the versatile functional food ingredients. J Food Sci Technol 53(2):921–933. https://doi.org/10.1007/s13197-015-2011-0
Chelule PK, Mokgatle MM, Zungu LI, Chaponda A (2014) Caregivers’ knowledge and use of fermented foods for infant and young children feeding in a rural community of odi, Gauteng province, South Africa. Health Promot Perspect 4(1):54–60. https://doi.org/10.5681/hpp.2014.007 eCollection 2014
Suez J, Zmora N, Zilberman-Schapira G, Mor U, Dori-Bachash M, Bashiardes S, Zur M, Regev-Lehavi D, Ben-Zeev Brik R, Federici S, Horn M, Cohen Y, Moor AE, Zeevi D, Korem T, Kotler E, Harmelin A, Itzkovitz S, Maharshak N, Shibolet O, Pevsner-Fischer M, Shapiro H, Sharon I, Halpern Z, Segal E, Elinav E (2018) Post-antibiotic gut mucosal microbiome reconstitution is impaired by probiotics and improved by autologous FMT. Cell 174(6):1406–1423. https://doi.org/10.1016/j.cell.2018.08.047
Zmora N, Zilberman-Schapira G, Suez J et al (2018) Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell 174(6):1388–1405. e21. https://doi.org/10.1016/j.cell.2018.08.041
Pepoyan A, Harutyunyan N, Grigoryan A et al (2015) Some clinical blood characteristics of patients with familial Mediterranean fever disease from an Armenian cohort. Klin Lab Diagn 60:46–47
Pepoyan A, Balayan M, Manvelyan A et al (2018) Probiotic Lactobacillus acidophilus strain INMIA 9602 Er 317/402 administration reduces the numbers of Candida albicans and abundance of enterobacteria in the gut microbiota of familial Mediterranean fever patients. Front Immunol 9:1426. https://doi.org/10.3389/fimmu.2018.01426
Pepoyan AZ, Balayan MH, Manvelyan AM, Mamikonyan V, Isajanyan M, Tsaturyan VV, Kamiya S, Netrebov V, Chikindas ML (2017) Lactobacillus acidophilus INMIA 9602 Er-2 strain 317/402 probiotic regulates growth of commensal Escherichia coli in gut microbiota of familial Mediterranean fever disease subjects. Lett Appl Microbiol 64:254–260. https://doi.org/10.1111/lam.12722
Pepoyan AZ, Balayan M, Manvelyan A et al (2018) Radioprotective effects of lactobacilli with antagonistic activities against human pathogens. Biophys J 114(3):665a. https://doi.org/10.1016/j.bpj.2017.11.3586
Jayakumar S, Bhilwade HN, Pandey BN, Sandur SK, Chaubey RC (2012) The potential value of the neutral comet assay and the expression of genes associated with DNA damage in assessing the radiosensitivity of tumor cells. Mutat Res 748(1–2):52–59. https://doi.org/10.1016/j.mrgentox.2012.06.008
Bocker W, Bauch T, Muller WU, Streffer C (1997) Technical report image analysis of comet assay measurements. Int J Radiat Biol 72(4):449–460. https://doi.org/10.1080/095530097143220
Sykora P, Witt KL, Revanna P, Smith-Roe SL, Dismukes J, Lloyd DG, Engelward BP, Sobol RW (2018) Next generation high throughput DNA damage detection platform for genotoxic compound screening. Sci Rep 8:2771. https://doi.org/10.1038/s41598-018-20995-w
Wojewódzka M, Buraczewska I, Kruszewski M (2002) A modified neutral comet assay: elimination of lysis at high temperature and validation of the assay with anti-single-stranded DNA antibody. Mutat Res 518(1):9–20
Cortes-Gutierrez EI, Hernandez-Garza F, Garcia Perez JO et al (2012) Evaluation of DNA single and double strand breaks in women with cervical neoplasia based on alkaline and neutral comet assay techniques. J Biomed Biotechnol 2012:385245–385247. https://doi.org/10.1155/2012/385245
Negritto MC (2010) Repairing double-strand DNA breaks. Nature Education 3(9):26
Paul W, O’Toole PW, Jeffery IB (2015) Gut microbiota and aging. Science 350(6265):1214–1215. https://doi.org/10.1126/science.aac8469
Bok E, Mazurek J, Myc A, Stosik M, Wojciech M, Baldy-Chudzik K (2018) Comparison of commensal Escherichia coli isolates from adults and young children in Lubuskie Province, Poland: virulence potential, phylogeny and antimicrobial resistance. Int J Environ Res Public Health 15(4):617. https://doi.org/10.3390/ijerph15040617
Sengupta P (2013) The laboratory rat relating its age with humans. Int J Prev Med 4(6):624–630
Quiles JL, Ochoa JJ, Huertas JR, Mataix J et al (2004) Coenzyme Q supplementation protects from age-related DNA double-strand breaks and increases lifespan in rats fed on a PUFA-rich diet. Exp Gerontol 39(2):189–194
Rosenfeldt V, Benfeldt E, Valerius NH, Pærregaard A, Michaelsen KF (2004) Effect of probiotics on gastrointestinal symptoms and small intestinal permeability in children with atopic dermatitis. J Pediatr 145:612–616. https://doi.org/10.1016/j.jpeds.2004.06.068
Mishra DK, Verma AK, Agarwal N et al (2016) Effect of probiotics on blood biochemical profile, immunity and small intestine morphology in growing finishing pigs. Agric Res 5:407–412. https://doi.org/10.1007/s40003-016-0231-9
Ghoshal UC, Shukla R, Ghoshal U (2017) Small intestinal bacterial overgrowth and irritable bowel syndrome: a bridge between functional organic dichotomy. Gut Liver 11(2):196–208. https://doi.org/10.5009/gnl16126
Ki Y, Kim W, Cho H, Ahn K, Choi Y, Kim D (2014) The effect of probiotics for preventing radiation-induced morphological changes in intestinal mucosa of rats. J Korean Med Sci 29(10):1372–1378. https://doi.org/10.3346/jkms.2014.29.10.1372
Ding C, Tang W, Fan X, Wu G (2018) Intestinal microbiota: a novel perspective in colorectal cancer biotherapeutics. Onco Targets Ther 11:4797–4810. https://doi.org/10.2147/OTT.S170626
Lorenzo Y, Costa S, Collins AR, Azqueta A (2013) The comet assay, DNA damage, DNA repair and cytotoxicity: hedgehogs are not always dead. Mutagenesis 28(4):427–432. https://doi.org/10.1093/mutage/get018
Wollowski I, Ji ST, Bakalinsky AT, Neudecker C, Pool-Zobel BL (1999) Bacteria used for the production of yogurt inactivate carcinogens and prevent DNA damage in the colon of rats. J Nutr 129(1):77–82. https://doi.org/10.1093/jn/129.1.77
Mkrtchyan H, Gibbons S, Heidelberger S, Zloh M, Limaki HK (2010) Purification, characterization and identification of acidocin LCHV, an antimicrobial peptide produced by Lactobacillus acidophilus n.v. Er 317/402 strain Narine. Int J Antimicrob Agents 35(3):255–260. https://doi.org/10.1016/j.ijantimicag.2009.11.017
Funding
This study was supported by a grant for the International Science and Technology Center (A-2134) and the “CANDLE” Synchrotron Research Institute foundation (17A-1F010).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Pepoyan, A.Z., Balayan, M.H., Malkhasyan, L. et al. Effects of Probiotic Lactobacillus acidophilus Strain INMIA 9602 Er 317/402 and Putative Probiotic Lactobacilli on DNA Damages in the Small Intestine of Wistar Rats In Vivo. Probiotics & Antimicro. Prot. 11, 905–909 (2019). https://doi.org/10.1007/s12602-018-9491-y
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12602-018-9491-y