International Journal of Oral Biology

The Korean Academy of Oral Biology (대한구강생물학회)
권호 표지
DOI QR코드

DOI QR Code

Anti-cancer and -Metastatic Effects of Lactobacillus Rhamnosus GG Extract on Human Malignant Melanoma Cells, A375P and A375SM

  • Lee, Jaehoon (Cellular Reprogramming and Embryo Biotechnology Laboratory, Dental Research Institute, Seoul National University School of Dentistry) ;
  • Park, Sangkyu (Cellular Reprogramming and Embryo Biotechnology Laboratory, Dental Research Institute, Seoul National University School of Dentistry) ;
  • Seo, Jeongmin (Cellular Reprogramming and Embryo Biotechnology Laboratory, Dental Research Institute, Seoul National University School of Dentistry) ;
  • Roh, Sangho (Cellular Reprogramming and Embryo Biotechnology Laboratory, Dental Research Institute, Seoul National University School of Dentistry)
  • Received : 2017.08.06
  • Accepted : 2017.09.02
  • Published : 2017.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Human malignant melanoma is an aggressive skin cancer which has been rising at a greater rate than any other cancers. Although various new therapeutic methods have been developed in previous studies, this disease has properties of high proliferation and metastasis rate which remain obstacles that have lead to a poor prognosis in patients. It has been reported that a specific Lactobacillus extract has anti-cancer and -metastasis effect in vitro and in vivo. However, previous research has not specified precisely what effect the Lactobacillus rhamnosus GG (LGG) extract has had on human malignant melanomas. In this study, we showed that the LGG extract has anti-cancer and -metastasis effects on the human malignant melanoma cell lines, A375P and A375SM. At first, it was found that, while the LGG extract affects human neonatal dermal fibroblasts slightly, it induced the dose-dependent anti-cancer effect on A375P and A375SM by a WST-1 proliferation assay. As a result of a real-time PCR analysis, the expression patterns of several genes related to cell cycle, proliferation, and apoptosis were modulating in a manner that inhibited the growth of both malignant melanoma cell lines after the treatment of the LGG extract. Furthermore, genes related to the epithelial-mesenchymal transition were down-regulated, and migration rates were also decreased significantly by the LGG extract. Our study showed that the LGG extract could be used as a potential therapeutic source.

Keywords

References

  1. Lee JE. Factors associated with melanoma incidence and prognosis. Semin Surg Oncol. 1996;12:379-385. https://doi.org/10.1002/(SICI)1098-2388(199611/12)12:6<379::AID-SSU2>3.0.CO;2-7
  2. Parker SL, Tong T, Bolden S, Wingo PA. Cancer statistics. CA Cancer J Clin. 1996;6:5-27.
  3. Jemal A, Murray T, Samuels A, Ghafoor A, Ward E, Thun MJ. Cancer statistics. CA Cancer J Clin. 2003;53:5-26. https://doi.org/10.3322/canjclin.53.1.5
  4. Rigel, DS, J Russak, R Friedman. The evolution of melanoma diagnosis: 25 years beyond the ABCDs. CA Cancer J Clin. 2010;60:301-316. doi:10.3322/caac.20074.
  5. Faiao-Flores F, Coelho P, Arruda-Neto J, Maria DA. Boron neutron capture therapy induces cell cycle arrest and DNA fragmentation in murine melanoma cells. Appl Radiat Isot. 2011;69:1741-1744. doi:10.1016/j.apradiso.2011.03.005.
  6. Dimitrakopoulos I, Lazaridis N, Skordalaki A. Primary malignant melanoma of the oral cavity. Report of an unusual case. Aust Dent J. 1998;43:379-381.
  7. Pliskin ME, Mastrangelo MJ, Brown AM, Custer RP. Metastatic melanoma of the maxilla presenting as a gingival swelling. Oral Surg Oral Med Oral Pathol. 1976;41:101-104. https://doi.org/10.1016/0030-4220(76)90257-7
  8. Chiu NT, Weinstock MA. Melanoma of oronasal mucosa. Population-based analysis of occurrence and mortality. Arch Otolaryngol Head Neck Surg. 1996;122:985-988. https://doi.org/10.1001/archotol.1996.01890210057013
  9. Gonzalez-Garcia R, Naval-Gias L, Martos PL, Nam-Cha SH, Rodriguez-Campo FJ, Munoz-Guerra MF, Sastre-Perez J. Melanoma of the oral mucosa. Clinical cases and review of the literature. Med Oral Patol Oral Cir Bucal. 2005;10: 264-271.
  10. Lee B, Mukhi N, Liu D. Current management and novel agents for malignant melanoma. J Hematol Oncol.2012; 5:3. doi:10.1186/1756-8722-5-3.
  11. Kirjavainen PV, El-Nezami HS, Salminen SJ, Ahokas JT, Wright PF. The effect of orally administered viable probiotic and dairy lactobacilli on mouse lymphocyte proliferation. FEMS Immunol Med Microbiol. 1999;26:131-135. https://doi.org/10.1111/j.1574-695X.1999.tb01380.x
  12. Pessi T, Sutas Y, Hurme M, Isolauri E. Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GG. Clinical and experimental allergy. J Br Soc Allergy Clin Immunol. 2000;30:1804-1808. https://doi.org/10.1046/j.1365-2222.2000.00948.x
  13. Hemarajata P, Versalovic J. Effects of probiotics on gut microbiota: mechanisms of intestinal immunomodulation and neuromodulation. Therap Adv Gastroenterol. 2013;6:39-51. doi:10.1177/1756283X12459294.
  14. Hwang JW, Baek YM, Yang KE, Yoo HS, Cho CK, Lee YW, Park J, Eom CY, Lee ZW, Choi JS, Jang IS. Lactobacillus casei extract induces apoptosis in gastric cancer by inhibiting $NF-{\kappa}B$ and mTOR-mediated signaling. Integr Cancer Ther. 2013;12:165-173. doi:10.1177/1534735412442380.
  15. Khan I, Kang SC. Apoptotic activity of Lactobacillus plantarum DGK-17-fermented soybean seed extract in human colon cancer cells via ROS-JNK signaling pathway. J Food Sci. 2017;82:1475-1483. doi:10.1111/1750-3841.13732.
  16. Matsuzaki T, Yokokura T, Azuma I. Antimetastatic effect of Lactobacillus casei YIT9018 (LC 9018) on a highly metastatic variant of B16 melanoma in C57BL/6J mice. Cancer Immunol Immunother. 1987;24:99-105.
  17. Gamallat Y, Meyiah A, Kuugbee ED, Hago AM, Chiwala G, Awadasseid A, Bamba D, Zhang X, Shang X, Luo F, Xin Y. Lactobacillus rhamnosus induced epithelial cell apoptosis, ameliorates inflammation and prevents colon cancer development in an animal model. Biomed Pharmacother. 2016;83:536-541. doi:10.1016/j.biopha.2016.07.001.
  18. Riedl S, Rinner B, Schaider H, Liegl-Atzwanger B, Meditz K, Preishuber-Pflugl J, Grissenberger S, Lohner K, Zweytick D. In vitro and in vivo cytotoxic activity of human lactoferricin derived antitumor peptide R-DIM-P-LF11-334 on human malignant melanoma. Oncotarget. 2017. doi:10.18632/oncotarget.17823.
  19. Peterson M, Albertini MR, Remington P. Incidence, survival, and mortality of malignant cutaneous melanoma in wisconsin, 1995-2011. W M J. 2015;114:196-201.
  20. Zehavi L, Schayek H, Jacob-Hirsch J, Sidi Y, Leibowitz- Amit R, Avni D. MiR-377 targets E2F3 and alters the $NF-{\kappa}B$ signaling pathway through MAP3K7 in malignant melanoma. Mol Cancer. 2015;14:68. doi:10.1186/s12943-015-0338-9.
  21. Balch CM, Gershenwald JE, Soong S-j, Thompson JF, Atkins MB, Byrd DR, Buzaid AC, Cochran AJ, Coit DG, Ding S, Eggermont AM, Flaherty KT, Gimotty PA, Kirkwood JM, McMasters KM, Mihm MC Jr, Morton DL, Ross MI, Sober AJ, Sondak VK. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol. 2009;27:6199-6206. doi:10.1200/JCO.2009.23.4799.
  22. Howlader N, Noone A, Krapcho M, Miller D, Bishop K, Kosary C, Yu M, Ruhl J, Tatalovich Z, Mariotto A, Lewis D, Chen H, Feuer E. SEER Cancer Statistics Review, 1975-2014. National Cancer Institute. https://seer.cancer.gov/csr/1975_2014/, based on November 2016 SEER data submission, posted to the SEER web site.
  23. Hegedus L, Padanyi R, Molnar J, Paszty K, Varga K3, Kenessey I, Sarkozy E, Wolf M, Grusch M, Hegyi Z, Homolya L, Aigner C, Garay T, Hegedus B, Timar J, Kallay E, Enyedi A. Histone Deacetylase Inhibitor treatment increases the expression of the plasma membrane $Ca^{2+}$ pump PMCA4b and inhibits the migration of melanoma cells independent of ERK. Front Oncol. 2017;7:95. doi:10.3389/fonc.2017.00095.
  24. Forestier C, Champs CD, Vatoux C, Joly B. Probiotic activities of Lactobacillus casei rhamnosus: in vitro adherence to intestinal cells and antimicrobial properties. Res Microbiol. 2001;152:167-173. https://doi.org/10.1016/S0923-2508(01)01188-3
  25. Lilly DM, Stillwell RH. Probiotics: growth-promoting factors produced by microorganisms. Science. 1965;147:747-748. https://doi.org/10.1126/science.147.3659.747
  26. Zhang Z, Zhou Z, Li Y, Zhou L, Ding Q, Xu L. Isolated exopolysaccharides from Lactobacillus rhamnosus GG alleviated adipogenesis mediated by TLR2 in mice. Sci Rep. 2016;6:36083. doi:10.1038/srep36083.
  27. Al-Ghazzewi FH, Tester RF. Impact of prebiotics and probiotics on skin health. Benef Microbes. 2014;5:99-107. doi:10.3920/BM2013.0040.
  28. Miller DM, Thomas SD, Islam A, Muench D, Sedoris K. c-Myc and cancer metabolism. Clin Cancer Res. 2012; 18:5546-5553. doi:10.1158/1078-0432.CCR-12-0977.
  29. Yalcin SE, Ocal I, Yalcin Y, Selim HS, Caltekin MD, Aydogmus H, Kelekci S. Evaluation of the Ki-67 proliferation index and urocortin expression in women with ovarian endometriomas. Eurasian J Med. 2017;49:107-112. doi: 10.5152/eurasianjmed.2017.17070.
  30. Huisman MA, De Heer E, Grote JJ. Cholesteatoma epithelium is characterized by increased expression of Ki-67, p53 and p21, with minimal apoptosis. Acta Otolaryngol. 2003;123:377-382. https://doi.org/10.1080/00016480310001376
  31. Da Silva GN, Filoni LT, Salvadori MC, Salvadori DMF. Gemcitabine/Cisplatin treatment induces concomitant SERTAD1, CDKN2B and GADD45A modulation and cellular changes in bladder cancer cells regardless of the site of TP53 mutation. Pathol Oncol Res. 2017. doi:10.1007/s12253-017-0255-x.
  32. Matsuzaki T, Yokokura T, Azuma I. Antitumor activity of Lactobacillus casei on Lewis lung carcinoma and Line-10 hepatoma in syngeneic mice and guinea pigs. Cancer Immunol Immunother. 1985;20:18-22.
  33. Matsuzaki T, Yokokura T. Inhibition of tumor metastasis of Lewis lung carcinoma in C57BL/6 mice by intrapleural administration of Lactobacillus casei. Cancer Immunol Immunother. 1987;25:100-104.
  34. Cho IH, Jang EH, Hong D, Jung B, Park MJ, Kim JH. Suppression of LPS-induced epithelial-mesenchymal transition by aqueous extracts of Prunella vulgaris through inhibition of the $NF-{\kappa}B$/Snail signaling pathway and regulation of EMTrelated protein expression. Oncol Rep. 2015; 34:2445-2450. doi: 10.3892/or.2015.4218.
  35. Hsieh CC, Huang YS. Aspirin Breaks the Crosstalk between 3T3-L1 Adipocytes and 4T1 Breast Cancer Cells by Regulating Cytokine Production. PLoS One. 2016; 11:e0147161. doi: 10.1371/journal.pone.0147161
  36. Wu S, Singh S, Varney ML, Kindle S, Singh RK. Modulation of CXCL-8 expression in human melanoma cells regulates tumor growth, angiogenesis, invasion, and metastasis. Cancer Med. 2012;1:306-317. doi:10.1002/cam4.28.
  37. Varney ML, Li A, Dave BJ, Bucana CD, Johansson SL, Singh RK. Expression of CXCR1 and CXCR2 receptors in malignant melanoma with different metastatic potential and their role in interleukin-8 (CXCL-8)-mediated modulation of metastatic phenotype. Clin Exp Metastasis. 2003;20:723-731. https://doi.org/10.1023/B:CLIN.0000006814.48627.bd