Skip to main content

Advertisement

SpringerLink
Log in

A Newly Characterized Potentially Probiotic Strain, Lactobacillus brevis MK05, and the Toxicity Effects of its Secretory Proteins Against MCF-7 Breast Cancer Cells

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

Abstract

Among seven strains of lactic acid bacteria (LAB) isolated from traditional dairy products, a Lactobacillus strain was identified through 16S rRNA gene sequencing and tentatively designated as Lactobacillus brevis MK05. This strain demonstrated the highest probiotic potential through biochemical analysis, including acid and bile salt resistance, as well as antibacterial activity. The collected cell-free supernatant (CFC) of L. brevis MK05 culture, compared with MRS broth with pH equal to the pH for CFC, revealed antimicrobial activity against Escherichia coli (ATCC 25922) and Staphylococcus aureus subsp. aureus (ATCC 25923), possibly due to the presence of antibacterial metabolites other than organic acids. This strain was, therefore, selected to assess the biological activity of its partially purified secretory proteins against MCF-7 cancer cells and normal fibroblast cells via the MTT assay. The partially purified cell-secreted proteins of this strain (hereafter referred to as Lb-PPSPs) showed a time and dose-dependent anti-cancer and apoptosis induction function. There was a remarkable decline in the survival rate of MCF-7 cells at doses equal to and higher than 0.5 mg/mL after 48 h. The changes in expression of the three genes involved in the apoptosis pathway (BAX, BCL-2, and BCL2L11) in MCF-7 cells treated with the Lb-PPSPs confirm its cytotoxic activity and apoptosis induction.

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
Fig. 8

Similar content being viewed by others

Data Availability

The data is defined as the minimal dataset that would be necessary to interpret, replicate, and build upon the findings reported in the article.

References

  1. Stefanovic E, Fitzgerald G, McAuliffe O (2017) Advances in the genomics and metabolomics of dairy lactobacilli: a review. Food Microbiol 61:33–49. https://doi.org/10.1016/j.fm.2016.08.009

    Article  CAS  PubMed  Google Scholar 

  2. Shehata M, El Sohaimy S, El-Sahn MA, Youssef M (2016) Screening of isolated potential probiotic lactic acid bacteria for cholesterol lowering property and bile salt hydrolase activity. Ann Agric Sci 61(1):65–75. https://doi.org/10.1016/j.aoas.2016.03.001

    Article  Google Scholar 

  3. Xia AN, Meng XS, Tang XJ, Zhang YZ, Lei SM, Liu YG (2021) Probiotic and related properties of a novel lactic acid bacteria strain isolated from fermented rose jam. LWT 136:110327. https://doi.org/10.1016/j.lwt.2020.110327

    Article  CAS  Google Scholar 

  4. Kerry RG, Patra JK, Gouda S, Park Y, Shin HS, Das G (2018) Benefaction of probiotics for human health: a review. J Food Drug Anal 26(3):927–939. https://doi.org/10.1016/j.jfda.2018.01.002

    Article  CAS  Google Scholar 

  5. Azad M, Kalam A, Sarker M, Li T, Yin J (2018) Probiotic species in the modulation of gut microbiota: an overview. Biomed Res Int 2018. https://doi.org/10.1155/2018/9478630

  6. Van den Nieuwboer M, Van De Burgwal L, Claassen E (2016) A quantitative key-opinion-leader analysis of innovation barriers in probiotic research and development: valorisation and improving the tech transfer cycle. PharmaNutrition 4(1):9–18. https://doi.org/10.1016/j.phanu.2015.09.003

  7. Kumar R, Dhanda S (2017) Mechanistic insight of probiotics derived anticancer pharmaceuticals: a road forward for cancer therapeutics. Nutr Cancer 69(3):375–380. https://doi.org/10.1080/01635581.2017.1267773

    Article  PubMed  Google Scholar 

  8. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: Cancer J Clin 68(6):394–424. https://doi.org/10.3322/caac.21492

  9. Siegel RL, Miller KD, Jemal A (2020) Cancer statistics, 2020. CA: Cancer J Clin 70(1):7–30. https://doi.org/10.3322/caac.21590

  10. Nazir Y, Hussain SA, Abdul Hamid A, Song Y (2018) Probiotics and their potential preventive and therapeutic role for cancer high serum cholesterol and allergic and HIV diseases. Biomed Res Int, 2018. https://doi.org/10.1155/2018/342843711

  11. Alvarez-Olmos MI, Oberhelman RA (2001) Probiotic agents and infectious diseases: a modern perspective on a traditional therapy. Clin Infect Dis 32(11):1567–1576. https://doi.org/10.1086/320518

    Article  CAS  PubMed  Google Scholar 

  12. Sharma M, Shukla G (2016) Metabiotics: one step ahead of probiotics; an insight into mechanism involved in anticancerous effect in colorectal cancer. Front Microbiol 7:1940. https://doi.org/10.3389/fmicb.2016.01940

    Article  PubMed  PubMed Central  Google Scholar 

  13. Mendoza L (2019) Potential effect of probiotics in the treatment of breast cancer. Oncol Rev 13(2). https://doi.org/10.4081/2Foncol.2019.422

  14. Shenderov BA (2013) Metabiotics: novel idea or natural development of probiotic conception. Microb Ecol Health Dis 24(1):20399. https://www.tandfonline.com/doi/full/10.3402/mehe/doi/full/10.3402/mehd.v24i0.20399

  15. Nataraj BH, Ali SA, Behare PV, Yadav H (2020) Postbiotics-parabiotics: the new horizons in microbial biotherapy and functional foods. Microb Cell Fact 19(1):1–22. https://doi.org/10.1186/s12934-020-01426-w

    Article  CAS  Google Scholar 

  16. Chuah LO, Foo HL, Loh TC, Alitheen NBM, Yeap SK, Mutalib NEA, Rahim RA, Yusoff K (2019) Postbiotic metabolites produced by Lactobacillus plantarum strains exert selective cytotoxicity effects on cancer cells. BMC Complement Altern Med 19(1):114. https://doi.org/10.1186/s12906-019-2528-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Orlando A, Refolo M, Messa C, Amati L, Lavermicocca P, Guerra V, Russo F (2012) Antiproliferative and proapoptotic effects of viable or heat-killed Lactobacillus paracasei IMPC2. 1 and Lactobacillus rhamnosus GG in HGC-27 gastric and DLD-1 colon cell lines. Nutr Cancer 64(7):1103–1111. https://doi.org/10.1080/01635581.2012.717676

  18. Nambiar S, Hegde V (2016) Apoptosis in cancer therapy. J med radiol pathol surg 3(5):10–14. https://doi.org/10.15713/ins.jmrps.68

    Article  Google Scholar 

  19. Thomas CM, Versalovic J (2010) Probiotics-host communication: modulation of signaling parthways in the intestine. Gut microbes 1(3):148–163. https://doi.org/10.4161/gmic.1.3.11712

    Article  PubMed  PubMed Central  Google Scholar 

  20. Luang-In et al. (2020) Cytotoxicity of Lactobacillus plantarum KK518 Isolated from Pak-Sian Dong (Thai Fermented Gynandropsis pentaphylla DC.) Against HepG2, MCF-7 and HeLa Cancer Cells. Pharmacogn J 12(5). https://doi.org/10.4314/tjpr.v19i11.20

  21. Charteris W, Kelly P, Morelli L, Collins J (1998) Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J Appl Microbiol 84 (5):759–768. https://sfamjournals.onlinelibrary.wiley.com/doi/pdfdirect/10.1046/j.1365-2.1998.00407.x

  22. Parente E, Ricciardi A, Addario G (1994) Influence of pH on growth and bacteriocin production by Lactococcus lactis subsp. lactis 14ONWC during batch fermentation. Appl Microbiol Biotechnol 41(4):388–394. https://doi.org/10.1007/BF01982525

  23. Mirmalek SA, Azizi MA, Jangholi E, Yadollah-Damavandi S, Javidi MA, Parsa Y, Parsa T, Salimi-Tabatabaee SA, Alizadeh-Navaei R (2015) Cytotoxic and apoptogenic effect of hypericin the bioactive component of Hypericum perforatum on the MCF-7 human breast cancer cell line. Cancer Cell Int 16(1):1–9. https://doi.org/10.1186/s12935-016-0279-4

    Article  CAS  Google Scholar 

  24. Kumar BV, Vijayendra SVN, Reddy OVS (2015) Trends in dairy and non-dairy probiotic products-a review. J Food Sci Technol 52(10):6112–6124. https://doi.org/10.1007/s13197-015-1795-2

    Article  CAS  Google Scholar 

  25. Fernández MF, Boris S, Barbes C (2003) Probiotic properties of human lactobacilli strains to be used in the gastrointestinal tract. J Appl Microbiol 94(3):449–455. https://doi.org/10.1080/2F01926230701320337

  26. So SS, Wan ML, El-Nezami H (2017) Probiotics-mediated suppression of cancer. Curr Opin Oncol 29(1):62–72. https://doi.org/10.1097/CCO.0000000000000342

    Article  PubMed  Google Scholar 

  27. Sun M, Liu W, Song Y, Tuo Y, Mu G, Ma F (2020) The effects of Lactobacillus plantarum-12 crude exopolysaccharides on the cell proliferation and apoptosis of human colon cancer (HT-29) cells. Probiotics Antimicrob Proteins. 1–9 https://doi.org/10.1007/s12602-020-09699-8

  28. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516. https://doi.org/10.1080/2F01926230701320337

  29. Malik SS, Saeed A, Baig M, Asif N, Masood N, Yasmin A (2018) Anticarcinogenecity of microbiota and probiotics in breast cancer. Int J Food Prop 21(1):655–666. https://doi.org/10.1080/10942912.2018.1448994

    Article  CAS  Google Scholar 

  30. Park KB, Oh CH, Oh SH (2015) Anti-proliferative and Apoptosis Inducing Activity of Lactobacillus brevis OPK-3 Isolated from Kimchi on Leukemia Cell Lines. Current Topics in Lactic Acid Bacteria and Probiotics 3(1):1–7. https://doi.org/10.35732/ctlabp.2015.3.1.1

  31. Z Nasiri H Montazeri N Akbari SS Mirfazli P Tarighi 2020 Synergistic cytotoxic and apoptotic effects of local probiotic Lactobacillus brevis isolated from regional dairy products in combination with tamoxifen Nutr Cancer 1–10. https://doi.org/10.1080/01635581.2020.1743871

  32. Groussard C, Morel I, Chevanne M, Monnier M, Cillard J, Delamarche A (2000) Free radical scavenging and antioxidant effects of lactate ion: an in vitro study. J Appl Physiol 89(1):169–175. https://doi.org/10.1152/jappl.2000.89.1.169

    Article  CAS  PubMed  Google Scholar 

  33. Ouyang L, Shi Z, Zhao S, Wang FT, Zhou TT, Liu B, Bao JK (2012) Programmed cell death pathways in cancer: a review of apoptosis, autophagy and programmed necrosis. Cell Prolif 5(6):487–498. https://doi.org/10.1111/j.1365-2184.2012.00845.x

    Article  CAS  Google Scholar 

  34. Goldar S, Khaniani MS, Derakhshan SM, Baradaran B (2015) Molecular mechanisms of apoptosis and roles in cancer development and treatment. Asian Pac J Cancer Prev 16(6):2129–2144. https://doi.org/10.7314/APJCP.2015.16.6.2129

    Article  PubMed  Google Scholar 

  35. Lopez J, Tait S (2015) Mitochondrial apoptosis: killing cancer using the enemy within. Br J Cancer 112(6):957–962. https://doi.org/10.1038/bjc.2015.85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kadirareddy RH, Vemuri SG, Palempalli UMD (2016) Probiotic conjugated linoleic acid mediated apoptosis in breast cancer cells by down regulation of NFB. Asian Pac J Cancer Prev 17(7):3395–3403. http://journal.waocp.org/article_32528_75300b29de2566a96f39824c57150730

Download references

Author information

Authors and Affiliations

  1. Department of Energy & Environmental Biotechnology, National Institute of Genetic Engineering and Biotechnology (NIGEB), Tehran, Iran

    Mona Pourbaferani, Sima Modiri, Amir Norouzy, Venus Derakhshan, Hossein Shahbani Zahiri & Kambiz Akbari Noghabi

  2. Department of Microbiology and Microbial Biotechnology, Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, Tehran, Iran

    Hadi Maleki

  3. Dental Implant Research Center, Tehran University of Medical Sciences, Tehran, Iran

    Mohadeseh Heidari

  4. Guilan University of Medical Sciences (GUMS), Rasht, Iran

    Leila Alidoust

Authors
  1. Mona Pourbaferani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sima Modiri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amir Norouzy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hadi Maleki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohadeseh Heidari
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Leila Alidoust
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Venus Derakhshan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hossein Shahbani Zahiri
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Kambiz Akbari Noghabi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kambiz Akbari Noghabi.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pourbaferani, M., Modiri, S., Norouzy, A. et al. A Newly Characterized Potentially Probiotic Strain, Lactobacillus brevis MK05, and the Toxicity Effects of its Secretory Proteins Against MCF-7 Breast Cancer Cells. Probiotics & Antimicro. Prot. 13, 982–992 (2021). https://doi.org/10.1007/s12602-021-09766-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-021-09766-8

Keywords

Search

Navigation