OpenLB
Open Library of Bioscience
Advanced Search
Probiotics and antimicrobial proteins
12, 2022;14 (6): 1130-1138.

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

Babak Pakbin, Shaghayegh Pishkhan Dibazar, Samaneh Allahyari, Maryam Javadi, Zahra Amani, Alireza Farasat, Sina Darzi
Author Information
  1. Babak Pakbin: Medical Microbiology Research Center, Qazvin University of Medical Sciences, Qazvin, Iran.
  2. Shaghayegh Pishkhan Dibazar: Department of Immunology, Faculty of Medical Science, Tarbiat Modares University, Tehran, Iran.
  3. Samaneh Allahyari: Department of Food Hygiene and Safety, School of Health, Qazvin University of Medical Sciences, Qazvin, Iran.
  4. Maryam Javadi: 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. Mjavadi@qums.ac.ir.
  5. Zahra Amani: Medical Microbiology Research Center, Qazvin University of Medical Sciences, Qazvin, Iran.
  6. Alireza Farasat: Department of Medical Biotechnology, Qazvin University of Medical Sciences, Qazvin, Iran.
  7. Sina Darzi: Health Products Safety Research Center, Qazvin University of Medical Science, Qazvin, Iran.
PMID: 35094296 DOI: 10.1007/s12602-021-09756-w

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 IC 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.

Keywords

Anticancer properties Breast carcinoma In vitro study Probiotic Saccharomyces boulardii Yeast supernatant

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 [DOI: 10.3322/caac.21203]
  2. Waks AG, Winer EP (2019) Breast cancer treatment: a review. JAMA 321(3):288–300. https://doi.org/10.1001/jama.2018.19323 [DOI: 10.1001/jama.2018.19323]
  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 [DOI: 10.1001/jamaoncol.2016.6326]
  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 [DOI: 10.3389/fonc.2018.00227]
  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 [DOI: 10.1371/journal.pone.0187925]
  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 [DOI: 10.3390/molecules23123347]
  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 [DOI: 10.1038/nrgastro.2014.66]
  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 [DOI: 10.1038/nmicrobiol.2017.57]
  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 [DOI: 10.1093/advances/nmy063]
  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 [DOI: 10.1111/j.1365-2036.2007.03442.x]
  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 [DOI: 10.1016/j.mmcr.2017.07.007]
  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 [DOI: 10.1080/01635581.2018.1380204]
  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 [DOI: 10.1016/j.ijbiomac.2018.06.145]
  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 [DOI: 10.1053/j.gastro.2009.05.050]
  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 [DOI: 10.1111/j.1365-2249.2009.03878.x]
  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 [DOI: 10.1016/j.matlet.2018.11.009]
  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 [DOI: 10.1016/j.pestbp.2017.04.003]
  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 [DOI: 10.1002/cbin.11137]
  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 [DOI: 10.1016/j.ejmech.2016.02.069]
  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 [DOI: 10.1111/jfpp.12704]
  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 [DOI: 10.3390/molecules21010013]
  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 [DOI: 10.3402/fnr.v60.30616]
  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 [DOI: 10.1039/C7FO01964E]
  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 [DOI: 10.1080/01635581.2018.1460672]
  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 [DOI: 10.1002/med.21547]
  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 [DOI: 10.1177/1176935119842576]
  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 [PMID: 30941973]
  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 [DOI: 10.1097/CEJ.0000000000000453]
  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 [DOI: 10.3390/ijms18102074]

MeSH Term

Humans
Female
Saccharomyces boulardii
Saccharomyces cerevisiae
Survivin
Breast Neoplasms
Prospective Studies
Probiotics

Chemicals

Survivin
Journal Article

Word Cloud

Created with Highcharts 10.0.0boulardiiSBScancerbreastcellsSaccharomycesSsupernatantBreastMCF-7MCF-7/MXrespectivelycarcinomaHoweverrecommendedstudyapoptosissuppressionsurvivingeneexpressionhumanvalue244872 honeantitumormechanismsanticancerAnticancerProbioticvarietycerevisiaeusedprobioticyeastfooddrugindustriesopportunisticpathogenorganismrecentlyhealth-promotingbenefitsfrequentdiseasewomenworldwideobjectiveinvestigateeffectscellviabilityinducingnon-drug-resistantmultidrug-resistantICcalculated1037542543 µg/mLtreatmentsAlsomeasured1242616444 µg/mLfoundmainmolecularcontributedactivityobservedefficientsuggestedconsideredprospectivedrugstreatinvestigationsespeciallyvivostudiesstronglyimplementedcharacterizePropertiesSupernatantHumanCancerCellspropertiesvitroYeast

Similar Articles

Cited By