Inhibitory effects of postbiotic consisting sonication-killed Bifidobacterium bifidum on experimental triple negative breast neoplasm in mice: a preliminary study
,
Abstract
Background and Objectives: Breast cancer is the second leading cause of death and one of the most common malignancies among women in the world. The aim of this study was to investigate the preventive effects of postbiotic consisting of sonicated Bifidobacterium bifidum cells on triple negative breast cancer.
Materials and Methods: Thirty-six female BALB/c mice aged 5-7 weeks were randomly divided into 3 groups (n=12): Ctrl-, healthy mice; Ctrl+, mice with breast cancer with no treatment; and Postbiotic, mice with orally gavage postbiotic before and after 4T1 cell line transplantation. Cancer progress and the effects of postbiotic were assayed by histological, immunohistochemical and gene expression quantification.
Results: The histological results showed that administration postbiotic consisting of B. bifidum significantly decreased carcinogenesis in terms of tumor incidence, multiplicity and volume. The tumor progress was suppressed by oral intake of B. bifidum as showed by p53 and Ki-67 expression. Furthermore, Oral intake of postbiotic resulted in extended survival of mice and inhibited sever weigh loss.
Conclusion: Pretreatment with sonication killed B. bifidum, as a postbiotic, inhibited breast cancer progress and malignancy.
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4. Zendehdel M, Niakan B, Keshtkar A, Rafiei E, Salamat F. Subtypes of benign breast disease as a risk factor for breast cancer: a systematic review and meta-analysis protocol. Iran J Med Sci 2018; 43: 1-8.
5. Allred DC. Ductal carcinoma in situ: terminology, classification, and natural history. J Natl Cancer Inst Monogr 2010; 2010: 134-138.
6. Bao L, Haque A, Jackson K, Hazari S, Moroz K, Jetly R, et al. Increased expression of P-glycoprotein is associated with doxorubicin chemoresistance in the metastatic 4T1 breast cancer model. Am J Pathol 2011; 178: 838-852.
7. Aad G, Abbott B, Abdallah J, Abdelalim AA, Abdesselam A, Abdinov O, et al. Electron performance measurements with the ATLAS detector using the 2010 LHC proton-proton collision data. Eur Phys J Cancer 2012; 72: 1909.
8. Baker KJ, Houston A, Brint E. IL-1 family members in cancer; two sides to every story. Front Immunol 2019; 10: 1197.
9. Ren G, Zheng X, Bmmarito M, Metzger S, Walia Y, Letson J, et al. Reduced Basal Nitric oxide production Induces precancerous Mammary Lesions via ERBB2 and tGFβ. Sci Rep 2019; 9: 6688.
10. Berrueta L, Bergholz J, Munoz D, Muskaj L, Badger GJ, Shukla A, et al. Stretching reduces tumor growth in a mouse breast cancer model. Sci Rep 2018; 8: 7864.
11. Marzo F, Jauregui P, Barrenetxe J, Martínez Peñuela A, Ibañez FC, Milagro FI. Effect of a diet supplemented with sphingomyelin and probiotics on colon cancer development in mice. Probiotics Antimicrob Proteins 2022; 14: 407-414.
12. Maroof H, Mohammad Hassan Z, Mohabati Mobarez A, Azimi Mohamadabadi M. Lactobacillus acidophilus could modulate the immune response against breast cancer in murine model. J Clin Immunol 2012; 32: 1353-1359.
13. Cai W, Kesavan DK, Wan J, Abdelaziz MH, Su Z, Xu H. Bacterial outer membrane vesicles, a potential vaccine candidate in interactions with host cells based. Diagn Pathol 2018; 13: 95.
14. Molska M, Reguła J. Potential mechanisms of probiotics action in the prevention and treatment of colorectal cancer. Nutrients 2019; 11: 2453.
15. Jadidi-Niaragh F, Atybi F, Rastegari A, Kheshtchin N, Arab S, Hassannia H, et al. CD73 specific siRNA loaded chitosan lactate nanoparticles potentiate the antitumor effect of a dendritic cell vaccine in 4T1 breast cancer bearing mice. J Control Release 2017; 246: 46-59.
16. Tao K , Fang M, Alroy J, Sahagian GG. Imagable 4T1 model for the study of late stage breast cancer. BMC Cancer 2008; 8: 228.
17. DuPre SA, Redelman D, Hunter KW Jr. The mouse mammary carcinoma 4T1: characterization of the cellular landscape of primary tumours and metastatic tumour foci. Int J Exp Pathol 2007; 88: 351-360.
18. Abd-Alhaseeb MM, Zaitone SA, Abou-El-Ela SH, Moustafa YM. Olmesartan potentiates the anti-angiogenic effect of sorafenib in mice bearing Ehrlich's ascites carcinoma: role of angiotensin (1-7). PLoS One 2014; 9(1): e85891.
19. Yang G, Xiog Y, Wang G, Li W, Tang T, Sun J, et al. miR‑374c‑5p regulates PTTG1 and inhibits cell growth and metastasis in hepatocellular carcinoma by regulating epithelial‑mesenchymal transition. Mol Med Rep 2022; 25: 148.
20. Mahmoud MA, Okda TM, Omran GA, Abd-Alhaseeb MM. Rosmarinic acid suppresses inflammation, angiogenesis, and improves paclitaxel induced apoptosis in a breast cancer model via NF3 κB-p53-caspase-3 pathways modulation. J Appl Biomed 2021; 19: 202-209.
21. Zamberi NR , Abu N, Mohamed NE, Nordin N, Keong YS, Beh BK, et al. The antimetastatic and antiangiogenesis effects of kefir water on murine breast cancer cells. Integr Cancer Ther 2016; 15: NP53-NP66.
22. Kerry RG, Patra J, Gouda S, Park y, Shin H-S, Das G. Benefaction of probiotics for human health: A review. J Food Drug Anal 2018; 26: 927-939.
23. Chiba Y, Shida K, Nagata S, Wada M, Bian L, Wang C, et al. Well‐controlled proinflammatory cytokine responses of Peyer’s patch cells to probiotic Lactobacillus casei. Immunology 2010; 130: 352-362.
24. Azam F, Mehta S, Harris AL. Mechanisms of resistance to antiangiogenesis therapy. Eur J Cancer 2010; 46: 1323-1332.
25. Homayouni Rad A, Aghebati Maleki L, Samadi Kafil H, Fathi Zavoshti H, Abbasi A. Postbiotics as promising tools for cancer adjuvant therapy. Adv Pharm Bull 2021; 11: 1-5.
26. You HJ, Oh D-K, Ji GE. Anticancerogenic effect of a novel chiroinositol-containing polysaccharide from Bifidobacterium bifidum BGN4. FEMS Microbiol Lett 2004; 240: 131-136.
27. Rybinska I, Agresti R, Trapani A, Tagliabue E, Triulzi T. Adipocytes in breast cancer, the thick and the thin. Cells 2020; 9: 560.
28. Han Y-H, Mun J-G, Jeon HD, Yoon DH, Choi B-M, Kee j-y, et al. The extract of Arctium lappa L. fruit (Arctii Fructus) improves cancer-induced cachexia by inhibiting weight loss of skeletal muscle and adipose tissue. Nutrients 2020; 12: 3195.
29. Vaghef-Mehrabany E, Alipour B, Homayouni-Rad A, Sharif S-K, Asghari-Jafarabadi M, Zavvari S. Probiotic supplementation improves inflammatory status in patients with rheumatoid arthritis. Nutrition 2014; 30: 430-435.
30. Ubachs J, Ziemons J, Soons Z, Aarnoutse R, Van Dijk DPJ, Penders J, et al. Gut microbiota and short‐chain fatty acid alterations in cachectic cancer patients. J Cachexia Sarcopenia Muscle 2021; 12: 2007-2021.
31. O'Callaghan A, Van Sinderen D. Bifidobacteria and their role as members of the human gut microbiota. Front Microbiol 2016; 7: 925.
32. Kim MJ, Ku S, Kim SY, Lee HH, Jin H, Kang S, et al. Safety Evaluations of Bifidobacterium bifidum BGN4 and Bifidobacterium longum BORI. Int J Mol Sci 2018; 19: 1422.
33. Zhan C, Lu W. Peptide activators of the p53 tumor suppressor. Curr Pharm Des 2011; 17: 603-609.
34. Pan Y, Yuan Y, Liu G, Wei Y. P53 and Ki-67 as prognostic markers in triple-negative breast cancer patients. PLoS One 2017; 12(2): e0172324.
35. Menendez JA, Lupu R. RNA interference-mediated silencing of the p53 tumor-suppressor protein drastically increases apoptosis after inhibition of endogenous fatty acid metabolism in breast cancer cells. Int J Mol Med 2005; 15: 33-40.
36. Liang Y, Besch-Williford C, Benakanakere I, Thorpe PE, Hyder SM. Targeting mutant p53 protein and the tumor vasculature: an effective combination therapy for advanced breast tumors. Breast Cancer Res Treat 2011; 125: 407-420.
37. Hofseth LJ, Hussain SP, Harris CC. p53: 25 years after its discovery. Trends Pharmacol Sci 2004; 25: 177-181.
38. Hafner A, Bulyk ML, Jambhekar A, Lahav G. The multiple mechanisms that regulate p53 activity and cell fate. Nat Rev Mol Cell Biol 2019; 20: 199-210.
39. Fischer M. Census and evaluation of p53 target genes. Oncogene 2017; 36: 3943-3956.
40. Sun X, Kaufman PD. Ki-67: more than a proliferation marker. Chromosoma 2018; 127: 175-186.
2. Bettaieb A, Paul C, Plenchette S, Shan J, Chouchane L, Ghiringhelli F. Precision medicine in breast cancer: reality or utopia? J Transl Med 2017; 15: 139.
3. Zhang L, Long X. Association of three SNPs in TOX3 and breast cancer risk: Evidence from 97275 cases and 128686 controls. Sci Rep 2015; 5: 12773.
4. Zendehdel M, Niakan B, Keshtkar A, Rafiei E, Salamat F. Subtypes of benign breast disease as a risk factor for breast cancer: a systematic review and meta-analysis protocol. Iran J Med Sci 2018; 43: 1-8.
5. Allred DC. Ductal carcinoma in situ: terminology, classification, and natural history. J Natl Cancer Inst Monogr 2010; 2010: 134-138.
6. Bao L, Haque A, Jackson K, Hazari S, Moroz K, Jetly R, et al. Increased expression of P-glycoprotein is associated with doxorubicin chemoresistance in the metastatic 4T1 breast cancer model. Am J Pathol 2011; 178: 838-852.
7. Aad G, Abbott B, Abdallah J, Abdelalim AA, Abdesselam A, Abdinov O, et al. Electron performance measurements with the ATLAS detector using the 2010 LHC proton-proton collision data. Eur Phys J Cancer 2012; 72: 1909.
8. Baker KJ, Houston A, Brint E. IL-1 family members in cancer; two sides to every story. Front Immunol 2019; 10: 1197.
9. Ren G, Zheng X, Bmmarito M, Metzger S, Walia Y, Letson J, et al. Reduced Basal Nitric oxide production Induces precancerous Mammary Lesions via ERBB2 and tGFβ. Sci Rep 2019; 9: 6688.
10. Berrueta L, Bergholz J, Munoz D, Muskaj L, Badger GJ, Shukla A, et al. Stretching reduces tumor growth in a mouse breast cancer model. Sci Rep 2018; 8: 7864.
11. Marzo F, Jauregui P, Barrenetxe J, Martínez Peñuela A, Ibañez FC, Milagro FI. Effect of a diet supplemented with sphingomyelin and probiotics on colon cancer development in mice. Probiotics Antimicrob Proteins 2022; 14: 407-414.
12. Maroof H, Mohammad Hassan Z, Mohabati Mobarez A, Azimi Mohamadabadi M. Lactobacillus acidophilus could modulate the immune response against breast cancer in murine model. J Clin Immunol 2012; 32: 1353-1359.
13. Cai W, Kesavan DK, Wan J, Abdelaziz MH, Su Z, Xu H. Bacterial outer membrane vesicles, a potential vaccine candidate in interactions with host cells based. Diagn Pathol 2018; 13: 95.
14. Molska M, Reguła J. Potential mechanisms of probiotics action in the prevention and treatment of colorectal cancer. Nutrients 2019; 11: 2453.
15. Jadidi-Niaragh F, Atybi F, Rastegari A, Kheshtchin N, Arab S, Hassannia H, et al. CD73 specific siRNA loaded chitosan lactate nanoparticles potentiate the antitumor effect of a dendritic cell vaccine in 4T1 breast cancer bearing mice. J Control Release 2017; 246: 46-59.
16. Tao K , Fang M, Alroy J, Sahagian GG. Imagable 4T1 model for the study of late stage breast cancer. BMC Cancer 2008; 8: 228.
17. DuPre SA, Redelman D, Hunter KW Jr. The mouse mammary carcinoma 4T1: characterization of the cellular landscape of primary tumours and metastatic tumour foci. Int J Exp Pathol 2007; 88: 351-360.
18. Abd-Alhaseeb MM, Zaitone SA, Abou-El-Ela SH, Moustafa YM. Olmesartan potentiates the anti-angiogenic effect of sorafenib in mice bearing Ehrlich's ascites carcinoma: role of angiotensin (1-7). PLoS One 2014; 9(1): e85891.
19. Yang G, Xiog Y, Wang G, Li W, Tang T, Sun J, et al. miR‑374c‑5p regulates PTTG1 and inhibits cell growth and metastasis in hepatocellular carcinoma by regulating epithelial‑mesenchymal transition. Mol Med Rep 2022; 25: 148.
20. Mahmoud MA, Okda TM, Omran GA, Abd-Alhaseeb MM. Rosmarinic acid suppresses inflammation, angiogenesis, and improves paclitaxel induced apoptosis in a breast cancer model via NF3 κB-p53-caspase-3 pathways modulation. J Appl Biomed 2021; 19: 202-209.
21. Zamberi NR , Abu N, Mohamed NE, Nordin N, Keong YS, Beh BK, et al. The antimetastatic and antiangiogenesis effects of kefir water on murine breast cancer cells. Integr Cancer Ther 2016; 15: NP53-NP66.
22. Kerry RG, Patra J, Gouda S, Park y, Shin H-S, Das G. Benefaction of probiotics for human health: A review. J Food Drug Anal 2018; 26: 927-939.
23. Chiba Y, Shida K, Nagata S, Wada M, Bian L, Wang C, et al. Well‐controlled proinflammatory cytokine responses of Peyer’s patch cells to probiotic Lactobacillus casei. Immunology 2010; 130: 352-362.
24. Azam F, Mehta S, Harris AL. Mechanisms of resistance to antiangiogenesis therapy. Eur J Cancer 2010; 46: 1323-1332.
25. Homayouni Rad A, Aghebati Maleki L, Samadi Kafil H, Fathi Zavoshti H, Abbasi A. Postbiotics as promising tools for cancer adjuvant therapy. Adv Pharm Bull 2021; 11: 1-5.
26. You HJ, Oh D-K, Ji GE. Anticancerogenic effect of a novel chiroinositol-containing polysaccharide from Bifidobacterium bifidum BGN4. FEMS Microbiol Lett 2004; 240: 131-136.
27. Rybinska I, Agresti R, Trapani A, Tagliabue E, Triulzi T. Adipocytes in breast cancer, the thick and the thin. Cells 2020; 9: 560.
28. Han Y-H, Mun J-G, Jeon HD, Yoon DH, Choi B-M, Kee j-y, et al. The extract of Arctium lappa L. fruit (Arctii Fructus) improves cancer-induced cachexia by inhibiting weight loss of skeletal muscle and adipose tissue. Nutrients 2020; 12: 3195.
29. Vaghef-Mehrabany E, Alipour B, Homayouni-Rad A, Sharif S-K, Asghari-Jafarabadi M, Zavvari S. Probiotic supplementation improves inflammatory status in patients with rheumatoid arthritis. Nutrition 2014; 30: 430-435.
30. Ubachs J, Ziemons J, Soons Z, Aarnoutse R, Van Dijk DPJ, Penders J, et al. Gut microbiota and short‐chain fatty acid alterations in cachectic cancer patients. J Cachexia Sarcopenia Muscle 2021; 12: 2007-2021.
31. O'Callaghan A, Van Sinderen D. Bifidobacteria and their role as members of the human gut microbiota. Front Microbiol 2016; 7: 925.
32. Kim MJ, Ku S, Kim SY, Lee HH, Jin H, Kang S, et al. Safety Evaluations of Bifidobacterium bifidum BGN4 and Bifidobacterium longum BORI. Int J Mol Sci 2018; 19: 1422.
33. Zhan C, Lu W. Peptide activators of the p53 tumor suppressor. Curr Pharm Des 2011; 17: 603-609.
34. Pan Y, Yuan Y, Liu G, Wei Y. P53 and Ki-67 as prognostic markers in triple-negative breast cancer patients. PLoS One 2017; 12(2): e0172324.
35. Menendez JA, Lupu R. RNA interference-mediated silencing of the p53 tumor-suppressor protein drastically increases apoptosis after inhibition of endogenous fatty acid metabolism in breast cancer cells. Int J Mol Med 2005; 15: 33-40.
36. Liang Y, Besch-Williford C, Benakanakere I, Thorpe PE, Hyder SM. Targeting mutant p53 protein and the tumor vasculature: an effective combination therapy for advanced breast tumors. Breast Cancer Res Treat 2011; 125: 407-420.
37. Hofseth LJ, Hussain SP, Harris CC. p53: 25 years after its discovery. Trends Pharmacol Sci 2004; 25: 177-181.
38. Hafner A, Bulyk ML, Jambhekar A, Lahav G. The multiple mechanisms that regulate p53 activity and cell fate. Nat Rev Mol Cell Biol 2019; 20: 199-210.
39. Fischer M. Census and evaluation of p53 target genes. Oncogene 2017; 36: 3943-3956.
40. Sun X, Kaufman PD. Ki-67: more than a proliferation marker. Chromosoma 2018; 127: 175-186.
| Files | ||
| Issue | Vol 14 No 5 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i5.10964 | |
| Keywords | ||
| Triple negative breast neoplasm; Bifidobacterium bifidum; Ki67 antigen; Tumor suppressor protein p53 | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Nazari F, Jafari P, Nomanpour B, Varmira K, Raissi F. Inhibitory effects of postbiotic consisting sonication-killed Bifidobacterium bifidum on experimental triple negative breast neoplasm in mice: a preliminary study. Iran J Microbiol. 2022;14(5):689-697.
