Cytotoxic activity and apoptosis induction by supernatant of Lentilactobacillus buchneri on HT-29 colon cancer cells
,
Abstract
Background and Objectives: Colorectal cancer (CRC) is the fourth most commonly diagnosed cancer and the third most deadly cancer in the world. According to recent experimental reports, probiotics and their derivatives protect CRC patients from treatment-related side effects. Therefore, the present study aimed to investigate the cytotoxic impact of the cell-free supernatant (CFS) of Lentilactobacillus buchneri on the HT-29 cancer cell line.
Materials and Methods: In the current study, we used the L. buchneri CFS, which was well isolated and identified in our previous investigation from traditional yogurt in the Arak region of Iran. The apoptosis induction in HT-29 cancer cells was assessed by cell cytotoxicity, flow cytometry, and qRT-PCR.
Results: L. buchneri CFS inhibited the proliferation of HT-29 cancer cells in a time- and dose-dependent manner. The apoptotic effect of CFS was further supported by the flow cytometry data, which showed that the maximum incidence of apoptosis was observed in HT-29 cancer cells treated with the IC50 concentration of CFS after 72 hours. CFS of L. buchneri also exerted the up-regulating effect on the expression of pro-apoptotic genes including BAX, CASP9, and CASP3. L. buchneri CFS at an IC50 dose induced cell cycle arrest in the G0/G1 phase in HT-29 cells.
Conclusion: This study indicates that L. buchneri CFS can prevent colorectal cancer (CRC) development in patients by inducing cancer cell apoptosis. This finding suggests that the CFS of L. buchneri could be used as a therapeutic agent for the control of CRC.
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14. Mavromatis P, Stampouli K, Vliora A, Mayilyan A, Samanidou V, Touraki M. Development of an HPLC-DAD method for the extraction and quantification of 5-Fluorouracil, Uracil, and 5-Fluorodeoxyuridin Monophosphate in cells and culture media of lactococcus lactis. Separations 2022; 9: 376.
15. Purdel C, Ungurianu A, Adam-Dima I, Margină D. Exploring the potential impact of probiotic use on drug metabolism and efficacy. Biomed Pharmacother 2023; 161: 114468.
16. Song D, Wang X, Ma Y, Liu N-N, Wang H. Beneficial insights into postbiotics against colorectal cancer. Front Nutr 2023; 10: 1111872.
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18. Mojibi P, Tafvizi F, Bikhof Torbati M. Cell-bound exopolysaccharide extract from indigenous probiotic bacteria induce apoptosis in HT–29 cell-line. Iran J Pathol 2019; 14: 41-51.
19. Escamilla J, Lane MA, Maitin V. Cell-free supernatants from probiotic Lactobacillus casei and Lactobacillus rhamnosus GG decrease colon cancer cell invasion in vitro. Nutr Cancer 2012; 64: 871-878.
20. Chen Z-Y, Hsieh Y-M, Huang C-C, Tsai C-C. Inhibitory effects of probiotic Lactobacillus on the growth of human colonic carcinoma cell line HT-29. Molecules 2017; 22: 107.
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23. Dolati M, Tafvizi F, Salehipour M, Movahed TK, Jafari P. Inhibitory effects of probiotic Bacillus coagulans against MCF7 breast cancer cells. Iran J Microbiol 2021; 13: 839-847.
24. Dolati M, Tafvizi F, Salehipour M, Komeili Movahed T, Jafari P. Antiproliferative potential of Bacillus coagulans supernatant on SKBR3 breast cancer cell line. Iran J Med Microbiol 2022; 16: 383-391.
25. Kvakova M, Kamlarova A, Stofilova J, Benetinova V, Bertkova I. Probiotics and postbiotics in colorectal cancer: Prevention and complementary therapy. World J Gastroenterol 2022; 28: 3370-3382.
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27. Kvakova M, Bertkova I, Stofilova J, Savidge TC. Co-encapsulated synbiotics and immobilized probiotics in human health and gut Microbiota modulation. Foods 2021; 10: 1297.
28. Cano-Garrido O, Seras-Franzoso J, Garcia-Fruitós E. Lactic acid bacteria: reviewing the potential of a promising delivery live vector for biomedical purposes. Microb Cell Fact 2015; 14: 137.
29. Orlando A, Refolo M, Messa C, Amati L, Lavermicocca P, Guerra V, et al. 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 2012; 64: 1103-1111.
30. Gamallat Y, Meyiah A, Kuugbee ED, Hago AM, Chiwala G, Awadasseid A, et al. Lactobacillus rhamnosus induced epithelial cell apoptosis, ameliorates inflammation and prevents colon cancer development in an animal model. Biomed Pharmacother 2016; 83: 536-541.
31. Tiptiri-Kourpeti A, Spyridopoulou K, Santarmaki V, Aindelis G, Tompoulidou E, Lamprianidou EE, et al. Lactobacillus casei exerts anti-proliferative effects accompanied by apoptotic cell death and up-regulation of TRAIL in colon carcinoma cells. PLoS One 2016; 11(2): e0147960.
32. Guo Y, Zhang T, Gao J, Jiang X, Tao M, Zeng X, et al. Lactobacillus acidophilus CICC 6074 inhibits growth and induces apoptosis in colorectal cancer cells in vitro and in HT-29 cells induced-mouse model. J Funct Foods 2020; 75: 104290.
33. Hiraishi N, Kanmura S, Oda K, Arima S, Kumagai K, Mawatari S, et al. Extract of Lactobacillus plantarum strain 06CC2 induces JNK/p38 MAPK pathway-mediated apoptosis through endoplasmic reticulum stress in Caco2 colorectal cancer cells. Biochem Biophys Rep 2019; 20: 100691.
34. Azam R, Ghafouri-Fard S, Tabrizi M, Modarressi M-H, Ebrahimzadeh-Vesal R, Daneshvar M, et al. Lactobacillus acidophilus and Lactobacillus crispatus culture supernatants downregulate expression of cancer-testis genes in the MDA-MB-231 cell line. Asian Pac J Cancer Prev 2014; 15: 4255-4259.
35. Riaz Rajoka MS, Zhao H, Mehwish HM, Li N, Lu Y, Lian Z, et al. Anti-tumor potential of cell free culture supernatant of Lactobacillus rhamnosus strains isolated from human breast milk. Food Res Int 2019; 123: 286-297.
36. Abdoli M, Fathi Rezaei P, Mansouri K. Exploring the anticancer efficacy of mixture of local probiotics on MDA-MB-231 and MCF-7 breast cell lines. J Cell Mol Res 2021; 13: 54-64.
37. Fan T-J, Han L-H, Cong R-S, Liang J. Caspase family proteases and apoptosis. Acta Biochim Biophys Sin (Shanghai) 2005; 37: 719-727.
38. Brentnall M, Rodriguez-Menocal L, De Guevara RL, Cepero E, Boise LH. Caspase-9, caspase-3 and caspase-7 have distinct roles during intrinsic apoptosis. BMC Cell Biol 2013; 14: 32.
2. Ding C, Tang W, Fan X, Wu G. Intestinal microbiota: a novel perspective in colorectal cancer biotherapeutics. Onco Targets Ther 2018; 11: 4797-4810.
3. Lee J-E, Lee J, Kim JH, Cho N, Lee SH, Park SB, et al. Characterization of the anti-cancer activity of the probiotic bacterium Lactobacillus fermentum using 2D vs. 3D culture in colorectal cancer cells. Biomolecules 2019; 9: 557.
4. Sullivan Å, Nord CE, Evengård B. Effect of supplement with lactic-acid producing bacteria on fatigue and physical activity in patients with chronic fatigue syndrome. Nutr J 2009; 8: 4.
5. Soerjomataram I, Bray F. Planning for tomorrow: global cancer incidence and the role of prevention 2020–2070. Nat Rev Clin Oncol 2021; 18: 663-672.
6. Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut 2017; 66: 683-691.
7. Rawla P, Sunkara T, Barsouk A. Epidemiology of colorectal cancer: incidence, mortality, survival, and risk factors. Prz Gastroenterol 2019; 14: 89-103.
8. Edwards BK, Ward E, Kohler BA, Eheman C, Zauber AG, Anderson RN, et al. Annual report to the nation on the status of cancer, 1975-2006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates. Cancer 2010; 116: 544-573.
9. Tanis PJ, Tuynman JB. Long-term safety of laparoscopic rectal cancer resection. Lancet Gastroenterol Hepatol 2021; 6: 516-518.
10. Huang F, Li S, Chen W, Han Y, Yao Y, Yang L, et al. Postoperative probiotics administration attenuates gastrointestinal complications and gut microbiota dysbiosis caused by chemotherapy in colorectal cancer patients. Nutrients 2023; 15: 356.
11. Garbacz K. Anticancer activity of lactic acid bacteria. Semin Cancer Biol 2022; 86: 356-366.
12. Lu K, Dong S, Wu X, Jin R, Chen H. Probiotics in cancer. Front Oncol 2021; 11: 638148.
13. Dicks LM, Vermeulen W. Do bacteria provide an alternative to cancer treatment and what role does lactic acid bacteria play? Microorganisms 2022; 10: 1733.
14. Mavromatis P, Stampouli K, Vliora A, Mayilyan A, Samanidou V, Touraki M. Development of an HPLC-DAD method for the extraction and quantification of 5-Fluorouracil, Uracil, and 5-Fluorodeoxyuridin Monophosphate in cells and culture media of lactococcus lactis. Separations 2022; 9: 376.
15. Purdel C, Ungurianu A, Adam-Dima I, Margină D. Exploring the potential impact of probiotic use on drug metabolism and efficacy. Biomed Pharmacother 2023; 161: 114468.
16. Song D, Wang X, Ma Y, Liu N-N, Wang H. Beneficial insights into postbiotics against colorectal cancer. Front Nutr 2023; 10: 1111872.
17. Thoda C, Touraki M. Probiotic-derived bioactive compounds in colorectal cancer treatment.
Microorganisms 2023; 11: 1898.
18. Mojibi P, Tafvizi F, Bikhof Torbati M. Cell-bound exopolysaccharide extract from indigenous probiotic bacteria induce apoptosis in HT–29 cell-line. Iran J Pathol 2019; 14: 41-51.
19. Escamilla J, Lane MA, Maitin V. Cell-free supernatants from probiotic Lactobacillus casei and Lactobacillus rhamnosus GG decrease colon cancer cell invasion in vitro. Nutr Cancer 2012; 64: 871-878.
20. Chen Z-Y, Hsieh Y-M, Huang C-C, Tsai C-C. Inhibitory effects of probiotic Lactobacillus on the growth of human colonic carcinoma cell line HT-29. Molecules 2017; 22: 107.
21. Chuah L-O, Foo HL, Loh TC, Mohammed Alitheen NB, Yeap SK, Abdul Mutalib NE, et al. Postbiotic metabolites produced by Lactobacillus plantarum strains exert selective cytotoxicity effects on cancer cells. BMC Complement Altern Med 2019; 19: 114.
22. Abedi A, Tafvizi F, Akbari N, Jafari P. Cell-Free Supernatant of L. buchneri probiotic bacteria enhancing apoptosis activity in AGS gastric cancer cells. Iran J Sci 2023; 47: 1071-1079.
23. Dolati M, Tafvizi F, Salehipour M, Movahed TK, Jafari P. Inhibitory effects of probiotic Bacillus coagulans against MCF7 breast cancer cells. Iran J Microbiol 2021; 13: 839-847.
24. Dolati M, Tafvizi F, Salehipour M, Komeili Movahed T, Jafari P. Antiproliferative potential of Bacillus coagulans supernatant on SKBR3 breast cancer cell line. Iran J Med Microbiol 2022; 16: 383-391.
25. Kvakova M, Kamlarova A, Stofilova J, Benetinova V, Bertkova I. Probiotics and postbiotics in colorectal cancer: Prevention and complementary therapy. World J Gastroenterol 2022; 28: 3370-3382.
26. Fong W, Li Q, Yu J. Gut microbiota modulation: a novel strategy for prevention and treatment of colorectal cancer. Oncogene 2020; 39: 4925-4943.
27. Kvakova M, Bertkova I, Stofilova J, Savidge TC. Co-encapsulated synbiotics and immobilized probiotics in human health and gut Microbiota modulation. Foods 2021; 10: 1297.
28. Cano-Garrido O, Seras-Franzoso J, Garcia-Fruitós E. Lactic acid bacteria: reviewing the potential of a promising delivery live vector for biomedical purposes. Microb Cell Fact 2015; 14: 137.
29. Orlando A, Refolo M, Messa C, Amati L, Lavermicocca P, Guerra V, et al. 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 2012; 64: 1103-1111.
30. Gamallat Y, Meyiah A, Kuugbee ED, Hago AM, Chiwala G, Awadasseid A, et al. Lactobacillus rhamnosus induced epithelial cell apoptosis, ameliorates inflammation and prevents colon cancer development in an animal model. Biomed Pharmacother 2016; 83: 536-541.
31. Tiptiri-Kourpeti A, Spyridopoulou K, Santarmaki V, Aindelis G, Tompoulidou E, Lamprianidou EE, et al. Lactobacillus casei exerts anti-proliferative effects accompanied by apoptotic cell death and up-regulation of TRAIL in colon carcinoma cells. PLoS One 2016; 11(2): e0147960.
32. Guo Y, Zhang T, Gao J, Jiang X, Tao M, Zeng X, et al. Lactobacillus acidophilus CICC 6074 inhibits growth and induces apoptosis in colorectal cancer cells in vitro and in HT-29 cells induced-mouse model. J Funct Foods 2020; 75: 104290.
33. Hiraishi N, Kanmura S, Oda K, Arima S, Kumagai K, Mawatari S, et al. Extract of Lactobacillus plantarum strain 06CC2 induces JNK/p38 MAPK pathway-mediated apoptosis through endoplasmic reticulum stress in Caco2 colorectal cancer cells. Biochem Biophys Rep 2019; 20: 100691.
34. Azam R, Ghafouri-Fard S, Tabrizi M, Modarressi M-H, Ebrahimzadeh-Vesal R, Daneshvar M, et al. Lactobacillus acidophilus and Lactobacillus crispatus culture supernatants downregulate expression of cancer-testis genes in the MDA-MB-231 cell line. Asian Pac J Cancer Prev 2014; 15: 4255-4259.
35. Riaz Rajoka MS, Zhao H, Mehwish HM, Li N, Lu Y, Lian Z, et al. Anti-tumor potential of cell free culture supernatant of Lactobacillus rhamnosus strains isolated from human breast milk. Food Res Int 2019; 123: 286-297.
36. Abdoli M, Fathi Rezaei P, Mansouri K. Exploring the anticancer efficacy of mixture of local probiotics on MDA-MB-231 and MCF-7 breast cell lines. J Cell Mol Res 2021; 13: 54-64.
37. Fan T-J, Han L-H, Cong R-S, Liang J. Caspase family proteases and apoptosis. Acta Biochim Biophys Sin (Shanghai) 2005; 37: 719-727.
38. Brentnall M, Rodriguez-Menocal L, De Guevara RL, Cepero E, Boise LH. Caspase-9, caspase-3 and caspase-7 have distinct roles during intrinsic apoptosis. BMC Cell Biol 2013; 14: 32.
| Files | ||
| Issue | Vol 16 No 2 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i2.15355 | |
| Keywords | ||
| Colorectal cancer; Cell free-supernatant; Probiotic; Lentilactobacillus buchneri; Apoptosis; Cell cycle arrest | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Abedi A, Tafvizi F, Akbari N, Jafari P. Cytotoxic activity and apoptosis induction by supernatant of Lentilactobacillus buchneri on HT-29 colon cancer cells. Iran J Microbiol. 2024;16(2):219-226.
