Skip to main content

Advertisement

SpringerLink
Log in

Anticancer Properties of Probiotic Saccharomyces boulardii Supernatant on Human Breast Cancer Cells

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

Abstract

Saccharomyces boulardii, a variety of S. cerevisiae, is used as a probiotic yeast in food and drug industries. However, S. boulardii is an opportunistic pathogen, and the supernatant of this organism has recently been recommended for its health-promoting benefits. Breast cancer is the most frequent cancer disease in women worldwide. The objective of this study was to investigate the effects of S. boulardii supernatant (SBS) on cell viability, inducing apoptosis and suppression of survivin gene expression in MCF-7 and MCF-7/MX as human non-drug-resistant and multidrug-resistant breast cancer cells respectively. The IC50 value of SBS against MCF-7 was calculated 1037, 542, and 543 µg/mL for 24, 48, and 72 h treatments, respectively. Also, this value against MCF-7/MX cells were measured 1242, 616, and 444 µg/mL after 24, 48, and 72 h respectively. We found that suppression of survivin gene expression should be one of the main molecular antitumor mechanisms which is contributed to apoptosis in breast cancer cells. However, anticancer activity of SBS was observed more efficient against MCF-7 than that against MCF-7/MX cells. SBS is suggested to be considered as one of the prospective anticancer drugs to treat human breast carcinoma. More investigations especially in vivo studies are strongly recommended to be implemented to characterize other antitumor mechanisms of SBS against breast carcinoma.

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

Similar content being viewed by others

Data Availability

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

References

  1. DeSantis C, Ma J, Bryan L, Jemal A (2014) Breast cancer statistics. Cancer J Clin 64(1):52–62. https://doi.org/10.3322/caac.21203

    Article  Google Scholar 

  2. Waks AG, Winer EP (2019) Breast cancer treatment: a review. JAMA 321(3):288–300. https://doi.org/10.1001/jama.2018.19323

    Article  CAS  PubMed  Google Scholar 

  3. Engmann NJ, Golmakani MK, Miglioretti DL, Sprague BL, Kerlikowske K (2017) Population-attributable risk proportion of clinical risk factors for breast cancer. JAMA Oncol 3(9):1228–1236. https://doi.org/10.1001/jamaoncol.2016.6326

    Article  PubMed  PubMed Central  Google Scholar 

  4. Tong CW, Wu M, Cho W, To KK (2018) Recent advances in the treatment of breast cancer. Front Oncol 8:227. https://doi.org/10.3389/fonc.2018.00227

    Article  PubMed  PubMed Central  Google Scholar 

  5. Rayan A, Raiyn J, Falah M (2017) Nature is the best source of anticancer drugs: Indexing natural products for their anticancer bioactivity. PLoS ONE 12(11):e0187925. https://doi.org/10.1371/journal.pone.0187925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Nguyen NNT, Le PN, Nguyen TBT, Nguyen NH, Bach LG, Doan VN, Tran HLB, Le VT, Tran NQ (2018) Synergic activity against MCF-7 breast cancer cell growth of nanocurcumin-encapsulated and cisplatin-complexed nanogels. Molecules 23(12):3347. https://doi.org/10.3390/molecules23123347

    Article  CAS  PubMed Central  Google Scholar 

  7. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S (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(8):506. https://doi.org/10.1038/nrgastro.2014.66

    Article  PubMed  Google Scholar 

  8. O’Toole PW, Marchesi JR, Hill C (2017) Next-generation probiotics: the spectrum from probiotics to live biotherapeutics. Nat Microbiol 2(5):1–6. https://doi.org/10.1038/nmicrobiol.2017.57

    Article  CAS  Google Scholar 

  9. Plaza-Diaz J, Ruiz-Ojeda FJ, Gil-Campos M, Gil A (2019) Mechanisms of action of probiotics. Adv Nutr 10(suppl_1):S49–S66. https://doi.org/10.1093/advances/nmy063

    Article  PubMed  PubMed Central  Google Scholar 

  10. Czerucka D, Piche T, Rampal P (2007) Yeast as probiotics–Saccharomyces boulardii. Pharmacol Ther 26(6):767–778. https://doi.org/10.1111/j.1365-2036.2007.03442.x

    Article  CAS  Google Scholar 

  11. Goldenberg JZ, Yap C, Lytvyn L, Lo CKF, Beardsley J, Mertz D, Johnston BC (2017) Probiotics for the prevention of Clostridium difficile‐associated diarrhea in adults and children. Cochrane Database Syst Rev 12. https://doi.org/10.1002/14651858.CD006095.pub4

  12. Appel-da-Silva MC, Narvaez GA, Perez LR, Drehmer L, Lewgoy J (2017) Saccharomyces cerevisiae var. boulardii fungemia following probiotic treatment. Med Mycol Case Rep 18:15–17. https://doi.org/10.1016/j.mmcr.2017.07.007

    Article  PubMed  PubMed Central  Google Scholar 

  13. De Marco S, Sichetti M, Muradyan D, Piccioni M, Traina G, Pagiotti R, Pietrella D 2018 Probiotic cell-free supernatants exhibited anti-inflammatory and antioxidant activity on human gut epithelial cells and macrophages stimulated with LPS. Evid Based Complementary Altern Med. https://doi.org/10.1155/2018/1756308

  14. Fortin O, Aguilar-Uscanga B, Vu KD, Salmieri S, Lacroix M (2018) Cancer chemopreventive, antiproliferative, and superoxide anion scavenging properties of Kluyveromyces marxianus and Saccharomyces cerevisiae var. boulardii cell wall components. Nutr Cancer 70(1):8396. https://doi.org/10.1080/01635581.2018.1380204

    Article  CAS  Google Scholar 

  15. Liu Y, Huang G, Lv M (2018) Extraction, characterization and antioxidant activities of mannan from yeast cell wall. Int J Biol Macromol 118:952–956. https://doi.org/10.1016/j.ijbiomac.2018.06.145

    Article  CAS  PubMed  Google Scholar 

  16. Chen X, Fruehauf J, Goldsmith JD, Xu H, Katchar KK, Koon HW, Zhao D, Kokkotou EG, Pothoulakis C, Kelly CP (2009) Saccharomyces boulardii inhibits EGF receptor signaling and intestinal tumor growth in Apcmin mice. Gastroenterology 137(3):914–923. https://doi.org/10.1053/j.gastro.2009.05.050

    Article  CAS  PubMed  Google Scholar 

  17. Fatemi M, Ghandhari F, Karimi N (2019) Effects of the cell debris and supernatant of Saccharomyces boulardii on 7, 12-dimethylbenz (a) anthracene-induced breast cancer in rats. J Kermanshah Uni Med Sci 23(3). https://doi.org/10.5812/jkums

  18. Thomas S, Przesdzing I, Metzke D, Schmitz J, Radbruch A, Baumgart D (2009) Saccharomyces boulardii inhibits lipopolysaccharide-induced activation of human dendritic cells and T cell proliferation. Clin Exp Immunol 156(1):78–87. https://doi.org/10.1111/j.1365-2249.2009.03878.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Rekha S, Anila E (2019) In vitro cytotoxicity studies of surface modified CaS nanoparticles on L929 cell lines using MTT assay. Mater Lett 236:637–639. https://doi.org/10.1016/j.matlet.2018.11.009

    Article  CAS  Google Scholar 

  20. Osakabe M, Imamura T, Nakano R, Kamikawa S, Tadatsu M, Kunimoto Y, Doi M (2017) Combination of restriction endonuclease digestion with the ΔΔCt method in real-time PCR to monitor etoxazole resistance allele frequency in the two-spotted spider mite. Pestic Biochem Physiol 139:1–8. https://doi.org/10.1016/j.pestbp.2017.04.003

    Article  CAS  PubMed  Google Scholar 

  21. D’Arcy MS (2019) Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biol Int 43(6):582–592. https://doi.org/10.1002/cbin.11137

    Article  PubMed  Google Scholar 

  22. Shobeiri N, Rashedi M, Mosaffa F, Zarghi A, Ghandadi M, Ghasemi A, Ghodsi R (2016) Synthesis and biological evaluation of quinoline analogues of flavones as potential anticancer agents and tubulin polymerization inhibitors. Euro J Med Chem 114:14–23. https://doi.org/10.1016/j.ejmech.2016.02.069

    Article  CAS  Google Scholar 

  23. Değirmencioğlu N, Gurbuz O, Şahan Y (2016) The monitoring, via an in vitro digestion system, of the bioactive content of vegetable juice fermented with Saccharomyces cerevisiae and Saccharomyces boulardii. J Food Process Preserv 40(4):798–811. https://doi.org/10.1111/jfpp.12704

    Article  CAS  Google Scholar 

  24. Uifălean A, Schneider S, Ionescu C, Lalk M, Iuga CA (2016) Soy isoflavones and breast cancer cell lines: molecular mechanisms and future perspectives. Molecules 21(1):13. https://doi.org/10.3390/molecules21010013

    Article  CAS  Google Scholar 

  25. Han X, Deng S, Wang N, Liu Y, Yang X (2016) Inhibitory effects and molecular mechanisms of tetrahydrocurcumin against human breast cancer MCF-7 cells. Food Nutr Res 60(1):30616. https://doi.org/10.3402/fnr.v60.30616

    Article  CAS  PubMed  Google Scholar 

  26. Wu Q, Needs PW, Lu Y, Kroon PA, Ren D, Yang X (2018) Different antitumor effects of quercetin, quercetin-3′-sulfate and quercetin-3-glucuronide in human breast cancer MCF-7 cells. Food Funct 9(3):1736–1746. https://doi.org/10.1039/C7FO01964E

    Article  CAS  PubMed  Google Scholar 

  27. Fortin O, Aguilar-Uscanga BR, Vu KD, Salmieri S, Lacroix M (2018b) Effect of Saccharomyces boulardii cell wall extracts on colon cancer prevention in male F344 rats treated with 1, 2-dimethylhydrazine. Nutr Cancer 70(4):632–642. https://doi.org/10.1080/01635581.2018.1460672

    Article  CAS  PubMed  Google Scholar 

  28. Bonyadi F, Nejati V, Tukmechi A, Hasanzadeh S, Mokarizadeh A (2017) An investigation of the complex effects of a Saccharomyces cerevisiae cytoplasmic extract on apoptosis in K562 cells. Iran Red Crescent Med J 19(1) https://doi.org/10.5812/ircmj.28773

  29. Martínez-García D, Manero-Rupérez N, Quesada R, Korrodi-Gregório L, Soto-Cerrato V (2019) Therapeutic strategies involving survivin inhibition in cancer. Med Res Rev 39(3):887–909. https://doi.org/10.1002/med.21547

    Article  CAS  PubMed  Google Scholar 

  30. Purnamasari R, Winarni D, Permanasari AA, Agustina E, Hayaza S, Darmanto W (2019) Anticancer activity of methanol extract of Ficus carica leaves and fruits against proliferation, apoptosis, and necrosis in Huh7it cells. Cancer Inform 18:1176935119842576. https://doi.org/10.1177/F1176935119842576

    Article  PubMed  PubMed Central  Google Scholar 

  31. Fang W, Ma Y, Wang J, Yang X, Gu Y, Li Y (2019) In vitro and in vivo antitumor activity of neochlorogenic acid in human gastric carcinoma cells are complemented with ROS generation, loss of mitochondrial membrane potential and apoptosis induction. J BUON 24:221–226

    PubMed  Google Scholar 

  32. Shojaei F, Yazdani-Nafchi F, Banitalebi-Dehkordi M, Chehelgerdi M, Khorramian-Ghahfarokhi M (2019) Trace of survivin in cancer. Eur J Cancer Prev 28(4):365–372. https://doi.org/10.1097/CEJ.0000000000000453

    Article  CAS  PubMed  Google Scholar 

  33. Oh T-I, Lee Y-M, Nam T-J, Ko Y-S, Mah S, Kim J, Kim Y, Reddy RH, Kim YJ, Hong S (2017) Fascaplysin exerts anti-cancer effects through the downregulation of survivin and HIF-1α and inhibition of VEGFR2 and TRKA. Int J Molecul Sci 18(10):2074. https://doi.org/10.3390/ijms18102074

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Medical Microbiology Research Center, Qazvin University of Medical Sciences, Qazvin, Iran

    Babak Pakbin & Zahra Amani

  2. Department of Immunology, Faculty of Medical Science, Tarbiat Modares University, Tehran, Iran

    Shaghayegh Pishkhan Dibazar

  3. Department of Food Hygiene and Safety, School of Health, Qazvin University of Medical Sciences, Qazvin, Iran

    Samaneh Allahyari

  4. Children Growth and Development Research Center, Research Institute for Prevention of Non- Communicable Disease, Qazvin University of Medical Sciences, P.O. Box: 34185-754, Bahonar Blvd., Qazvin, Iran

    Maryam Javadi

  5. Department of Medical Biotechnology, Qazvin University of Medical Sciences, Qazvin, Iran

    Alireza Farasat

  6. Health Products Safety Research Center, Qazvin University of Medical Science, Qazvin, Iran

    Sina Darzi

Authors
  1. Babak Pakbin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shaghayegh Pishkhan Dibazar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Samaneh Allahyari
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maryam Javadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zahra Amani
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alireza Farasat
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sina Darzi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maryam Javadi.

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

Pakbin, B., Dibazar, S.P., Allahyari, S. et al. Anticancer Properties of Probiotic Saccharomyces boulardii Supernatant on Human Breast Cancer Cells. Probiotics & Antimicro. Prot. 14, 1130–1138 (2022). https://doi.org/10.1007/s12602-021-09756-w

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-021-09756-w

Keywords

Search

Navigation