Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

An Aqueous Extract of a Bifidobacterium Species Induces Apoptosis and Inhibits Invasiveness of Non-Small Cell Lung Cancer Cells

  • Ahn, Joungjwa (Department of Food Science and Technology, Jungwon University) ;
  • Kim, Hyesung (Institute of Biomedical Science, Apple Tree Dental Hospital) ;
  • Yang, Kyung Mi (Institute of Biomedical Science, Apple Tree Dental Hospital)
  • Received : 2020.01.23
  • Accepted : 2020.03.31
  • Published : 2020.06.28
Download PDF
⟨ Previous Next ⟩

Abstract

Chemotherapy regimens for non-small cell lung cancer (NSCLC) have various adverse effects on the human body. For this reason, probiotics have received attention regarding their potential value as a safe and natural complementary strategy for cancer prevention. This study analyzed the anticancer effects of aqueous extracts of probiotic bacteria Bifidobacterium bifidum (BB), Bifidobacterium longum (BL), Bifidobacterium lactis (BLA), Bifidobacterium infantis 1 (BI1), and Bifidobacterium infantis 2 (BI2) on NSCLC cell lines. When the aqueous extracts of probiotic Bifidobacterium species were applied to the NSCLC cell lines A549, H1299, and HCC827, cell death increased considerably; in particular, the aqueous extracts from BB and BLA markedly reduced cell proliferation. p38 phosphorylation induced by BB aqueous extract increased the expression of cleaved caspase 3 and cleaved poly (ADP-ribose) polymerase (PARP), consequently inducing the apoptosis of A549 and H1299 cells. When the p38 inhibitor SB203580 was applied, phosphorylation of p38 decreased, and the expression of cleaved caspase 3 and cleaved PARP was also inhibited, resulting in a reduction of cell death. In addition, BB aqueous extracts reduced the secretion of MMP-9, leading to inhibition of cancer cell invasion. By contrast, after transfection of short hairpin RNA shMMP-9 (for a knockdown of MMP-9) into cancer cells, BB aqueous extracts treatment failed to suppress the cancer cell invasiveness. According to our results about their anticancer effects on NSCLC, probiotics consisting of Bifidobacterium species may be useful as adjunctive anticancer treatment in the future.

Keywords

References

  1. Chen Z, Fillmore CM, Hammerman PS, Kim CF, Wong KK. 2014. Non-small-cell lung cancers: a heterogeneous set of diseases. Nat. Rev. Cancer 14: 535-546. https://doi.org/10.1038/nrc3775
  2. Schuurbiers OCJ, Kaanders JHAM, van der Heijden HFM, Dekhuijzen RPN, Oyen WJG, Bussink J. 2009. The PI3-K/AKT-Pathway and radiation resistance mechanisms in non-small cell lung cancer. J. Thorac. Oncol. 4: 761-767. https://doi.org/10.1097/JTO.0b013e3181a1084f
  3. Min J, Li X, Huang KN, Tang H, Ding XY, Qi C, et al. 2015. Phloretin induces apoptosis of non-small cell lung carcinoma A549 cells via JNK1/2 and p38 MAPK pathways. Oncol. Rep. 34: 2871-2879. https://doi.org/10.3892/or.2015.4325
  4. Lee KH. 2010. Discovery and development of natural product-derived chemotherapeutic agents based on a medicinal chemistry approach. J. Nat. Prod. 73: 500-516. https://doi.org/10.1021/np900821e
  5. Uccello M, Malaguarnera G, Basile F, D'agata V, Malaguarnera M, Bertino G, et al. 2012. Potential role of probiotics on colorectal cancer prevention. BMC Surg. 12 Suppl 1(Suppl 1): S35. https://doi.org/10.1186/1471-2482-12-S1-S35
  6. Ishaque SM, Khosruzzaman SM, Ahmed DS, Sah MP. 2018. A randomized placebo-controlled clinical trial of a multi-strain probiotic formulation (Bio-Kult(R) in the management of diarrhea-predominant irritable bowel syndrome. BMC Gastroenterol. 18: 71. https://doi.org/10.1186/s12876-018-0788-9
  7. Amer M, Nadeem M, Nazir SUR, Fakhar M, Abid F, Ain QU, et al. 2018. Probiotics and their use in inflammatory bowel disease. Altern. Ther. Health Med. 24: 16-23.
  8. Chui CH, Cheng GYM, Ke B, Lau FY, Wong RSM, Kok SHL, et al. 2004. Growth inhibitory potential of effective microorganism fermentation extract (EM-X) on cancer cells. Int. J. Mol. Med. 14: 925-929.
  9. Chui CH, Hau DKP, Lau FY, Cheng GYM, Wong RSM, Gambari R, et al. 2006. Apoptotic potential of the concentrated effective microorganism fermentation extract on human cancer cells. Int. J. Mol. Med. 17: 279-284.
  10. Campana R, van Hemert S, Baffone W. 2017. Strain-specific probiotic properties of lactic acid bacteria and their interference with human intestinal pathogens invasion. Gut Pathog. 9: 12. doi: 10.1186/s13099-017-0162-4.
  11. Zhong L, Zhang XF, Covasa M. 2014. Emerging roles of lactic acid bacteria in protection against colorectal cancer. World J. Gastroenterol. 20: 7878-7886. https://doi.org/10.3748/wjg.v20.i24.7878
  12. del Carmen S, de LeBlanc AD, Levit R, Azevedo V, Langella P, Bermudez-Humaran LG, et al. 2017. Anti-cancer effect of lactic acid bacteria expressing antioxidant enzymes or IL-10 in a colorectal cancer mouse model. Int. Immunopharmacol. 42: 122-129. https://doi.org/10.1016/j.intimp.2016.11.017
  13. Shyu PT, Oyong GG, Cabrera EC. 2014. Cytotoxicity of probiotics from philippine commercial dairy products on cancer cells and the effect on expression of cfos and cjun early apoptotic-promoting genes and interleukin-1 beta and tumor necrosis factor-alpha proinflammatory cytokine genes. Biomed. Res. Int. 2014:491740.
  14. Tang W, He YF, Zhou SC, Ma YP, Liu GL. 2009. A novel Bifidobacterium infantis-mediated TK/GCV suicide gene therapy system exhibits antitumor activity in a rat model of bladder cancer. J. Exp. Clin. Canc. Res. 28(1): 155. https://doi.org/10.1186/1756-9966-28-155
  15. Sharma A, Viswanath B, Park YS. 2018. Role of probiotics in the management of lung cancer and related diseases: An update. J. Funct. Foods 40: 625-633. https://doi.org/10.1016/j.jff.2017.11.050
  16. Mortaz E, Adcock IM, Folkerts G, Barnes PJ, Vos AP, Garssen J. 2013. Probiotics in the management of lung diseases. Mediators Inflamm. 2013: 751068.
  17. Ahn J, Chung YW, Park JB, Yang KM. 2018. -hydroxyundec-9-enoic acid induces apoptosis by ROS mediated JNK and p38 phosphorylation in breast cancer cell lines. J. Cell. Biochem. 119: 998-1007. https://doi.org/10.1002/jcb.26267
  18. Yoon JW, Lee JS, Kim BM, Ahn J, Yang KM. 2014. Catechin-7-O-xyloside induces apoptosis via endoplasmic reticulum stress and mitochondrial dysfunction in human non-small cell lung carcinoma H1299 cells. Oncol. Rep. 31: 314-320. https://doi.org/10.3892/or.2013.2840
  19. O'Callaghan A, van Sinderen D. 2016. Bifidobacteria and their role as members of the human gut microbiota. Front. Microbiol. 7: 925.
  20. Ray D, Alpini G, Glaser S. 2014. Probiotic Bifidobacterium species: potential beneficial effects in diarrheal disorders. Focus on "Probiotic Bifidobacterium species stimulate human SLC26A3 gene function and expression in intestinal epithelial cells". Am. J. Physiol. Cell Physiol. 307: C1081-C1083. https://doi.org/10.1152/ajpcell.00300.2014
  21. Gratz SW, Mykkanen H, El-Nezami HS. 2010. Probiotics and gut health: A special focus on liver diseases. World J. Gastroenterol. 16: 403-410. https://doi.org/10.3748/wjg.v16.i4.403
  22. Riedel CU, Foata F, Philippe D, Adolfsson O, Eikmanns BJ, Blum S. 2006. Anti-inflammatory effects of bifidobacteria by inhibition of LPS-induced NF-kappa B activation. World J. Gastroenterol. 12: 3729-3735. https://doi.org/10.3748/wjg.v12.i23.3729
  23. van Beek AA, Sovran B, Hugenholtz F, Meijer B, Hoogerland JA, Mihailova V, et al. 2016. Supplementation with Lactobacillus plantarum WCFS1 prevents decline of mucus barrier in colon of accelerated aging Ercc1(-/Delta7) mice. Front. Immunol. 7: 408. https://doi.org/10.3389/fimmu.2016.00408
  24. Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, et al. 2011. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am. J. Respir. Crit. Care Med. 184: 957-963. https://doi.org/10.1164/rccm.201104-0655OC
  25. Erb-Downward JR, Thompson DL, Han MK, Freeman CM, McCloskey L, Schmidt LA, et al. 2011. Analysis of the lung microbiome in the "Healthy" Smoker and in COPD. PLoS One 6: e16384 . https://doi.org/10.1371/journal.pone.0016384
  26. Mao QX, Jiang F, Yin R, Wang J, Xia WJ, Dong GC, et al. 2018. Interplay between the lung microbiome and lung cancer. Cancer Lett. 415: 40-48. https://doi.org/10.1016/j.canlet.2017.11.036
  27. Iyer C, Kosters A, Sethi G, Kunnumakkara AB, Aggarwal BB, Versalovic J. 2008. Probiotic Lactobacillus reuteri promotes TNFinduced apoptosis in human myeloid leukemia-derived cells by modulation of NF-kappa B and MAPK signalling. Cell. Microbiol. 10: 1442-1452. https://doi.org/10.1111/j.1462-5822.2008.01137.x
  28. Lee DK, Jang S, Kim MJ, Kim JH, Chung MJ, Kim KJ, et al. 2008. Anti-proliferative effects of Bifidobacterium adolescentis SPM0212 extract on human colon cancer cell lines. BMC Cancer. 8: 310. https://doi.org/10.1186/1471-2407-8-310
  29. Hwang JW, Baek YM, Yang KE, Yoo HS, Cho CK, Lee YW, et al. 2013. Lactobacillus casei extract induces apoptosis in gastric cancer by Inhibiting NF-kappa B and mTOR-Mediated Signaling. Integr. Cancer Ther. 12: 165-173. https://doi.org/10.1177/1534735412442380
  30. Dallal MMS, Mojarrad M, Baghbani F, Raoofian R, Mardaneh J, Salehipour Z. 2015. Effects of Probiotic Lactobacillus acidophilus and Lactobacillus casei on colorectal tumor cells activity (CaCo-2). Arch. Iran Med. 18: 167-172.
  31. Escamilla J, Lane MA, Maitin V. 2012. Cell-Free supernatants from probiotic Lactobacillus casei and Lactobacillus rhamnosus GG decrease colon cancer cell invasion in vitro. Nutr. Cancer. 64: 871-878. https://doi.org/10.1080/01635581.2012.700758
  32. Stuelten CH, Parent CA, Montell DJ. 2018. Cell motility in cancer invasion and metastasis: insights from simple model organisms. Nat. Rev. Cancer 18: 296-312. https://doi.org/10.1038/nrc.2018.15
  33. Peng WJ, Yan JW, Wan YN, Wang BX, Tao JH, Yang GJ, et al. 2012. Matrix metalloproteinases: A review of their structure and role in systemic sclerosis. J. Clin. Immunol. 32: 1409-1414. https://doi.org/10.1007/s10875-012-9735-7
  34. Nouri Z, Karami F, Neyazi N, Modarressi MH, Karimi R, Khorramizadeh MR, et al. 2016. Dual anti-metastatic and anti-proliferative activity assessment of two probiotics on HeLa and HT-29 cell lines. Cell J. 18: 127-134.
  35. Maghsood F, Mirshafiey A, Farahani MM, Modarressi MH, Jafari P, Motevaseli E. 2018. Dual effects of cell free supernatants from Lactobacillus acidophilus and Lactobacillus rhamnosus GG in regulation of MMP-9 by Up-Regulating TIMP-1 and down-regulating CD147 in PMA-Differentiated THP-1 cells. Cell J. 19: 559-568.
  36. Yao M, Brummer G, Acevedo D, Cheng N. 2016. Cytokine regulation of metastasis and tumorigenicity. Adv. Cancer Res. 132: 265-367. https://doi.org/10.1016/bs.acr.2016.05.005
  37. He F, Morita H, Ouwehand AC, Hosoda M, Hiramatsu M, Kurisaki J, et al. 2002. Stimulation of the secretion of pro-inflammatory cytokines by Bifidobacterium strains. Microbiol. Immunol. 46: 781-785. https://doi.org/10.1111/j.1348-0421.2002.tb02765.x
  38. Medina M, De Palma G, Ribes-Koninckx C, Calabuig M, Sanz Y. 2008. Bifidobacterium strains suppress in vitro the proinflammatory milieu triggered by the large intestinal microbiota of coeliac patients. J. Inflamm. 5: 19. https://doi.org/10.1186/1476-9255-5-19

Cited by

  1. Lactobacillus acidophilus and Bifidobacterium longum exhibit antiproliferation, anti-angiogenesis of gastric and bladder cancer: Impact of COX2 inhibition vol.14, 2020, https://doi.org/10.1016/j.phanu.2020.100219