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Bifidobacterium animalis sup F1-7 Acts as an Effective Activator to Regulate Immune Response Via Casepase-3 and Bak of FAS/CD95 Pathway

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Abstract

Intestinal microecology was closely related to immune regulation, but the related mechanism was still unclear. This study aimed to reveal how microorganisms improved immune response via casepase-3 and Bak of FAS/CD95 pathway. Bifidobacterium animalis F1-7 inhibited the melanoma B16-F10 cells in vitro effectively; had a potent anticancer effect of lung cancer mice; effectively improved the spleen immune index and CD3+ (75.8%) and CD8+ (19.8%) expression level; strengthened the phagocytosis of macrophages; inhibited the overexpression of inflammatory factors IL-6 (319.10 ± 2.46 pg/mL), IL-8 (383.05 ± 9.87 pg/mL), and TNF-α (2003.40 ± 11.42 pg/mL); and promoted the expression of anti-inflammatory factor IL-10 (406.00 ± 3.59 pg/mL). This process was achieved by promoting caspase-8/3 and BH3-interacting domain death agonist (Bid), Bak genes, and protein expression. This study confirmed the B. animalis F1-7 could act as an effective activator to regulate immune response by promoting the expression of caspase-8/3, Bid and Bak genes, and proteins and by activating the FAS/CD95 pathway. Our study provided a data support for the application of potentially beneficial microorganisms of B. animalis F1-7 as an effective activator to improve immunity.

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Data Availability Statement

Data are included as electronic supplementary material.

Abbreviations

Bak:

Bcl-2 homologous antagonist killer

Bid:

BH3-interacting domain death agonist

Caspase-3:

Cysteinyl aspartate–specific proteinase-3

DMEM:

Dulbecco’s modified Eagle’s medium

ELISA:

Enzyme-linked immunosorbent assay

FADD:

FAS-associated death domain protein

FBS:

Fetal bovine serum

References

  1. Mohme M, Riethdorf S, Pantel K (2017) Circulating and disseminated tumour cells - mechanisms of immune surveillance and escape. Nat Rev Clin Oncol 14(3):155–167. https://doi.org/10.1038/nrclinonc.2016.144

    Article  CAS  PubMed  Google Scholar 

  2. Jordan KR, Loman BR, Bailey MT et al (2018) Gut microbiota-immune-brain interactions in chemotherapy-associated behavioral comorbidities. Cancer 124(20):3990–3999. https://doi.org/10.1002/cncr.31584

    Article  PubMed  Google Scholar 

  3. Santoni A, Arcuri E (2020) The ambiguity of opioids revealed by immunology is changing the knowledge and the therapeutic approach in cancer and non-cancer pain: a narrative review. Immunol Lett 226:12–21. https://doi.org/10.1016/j.imlet.2020.06.011

    Article  CAS  PubMed  Google Scholar 

  4. Yarchoan M, Johnson BA, Lutz ER et al (2017) Targeting neoantigens to augment antitumour immunity. Nat Rev Cancer 17(4):209–222. https://doi.org/10.1038/nrc.2016.154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Rashidi A, Kaiser T, Graiziger C et al (2020) Specific gut microbiota changes heralding bloodstream infection and neutropenic fever during intensive chemotherapy. Leukemia 34(1):312–316. https://doi.org/10.1038/s41375-019-0547-0

    Article  PubMed  Google Scholar 

  6. Biagio Ricciuti ARN, Naidoo J, Sehgal K, Miller A, Kehl K, Venkatraman D, Sands J, Lamberti G, Recondo G, Zhang J, Macherla S, Baig S, Walker P, Rangachari D, Gainor JF, Costa DB, Rizvi N, Sholl LM, Nishino M, Henick B, Farago AF, Awad MM (2020) Association between immune-related adverse events and clinical outcomes to PD-1/PD-L1 blockade in small cell lung cancer. JTO Clin Res Rep. https://doi.org/10.1016/j.jtocrr.2020.100092

    Article  PubMed  PubMed Central  Google Scholar 

  7. Zhou J, Peng H, Li K et al (2019) Liver-resident NK cells control antiviral activity of hepatic T cells via the PD-1-PD-L1 axis. Immunity 50(2):403–417. https://doi.org/10.1016/j.immuni.2018.12.024

    Article  CAS  PubMed  Google Scholar 

  8. Eslami M, Yousefi B, Kokhaei P et al (2019) Importance of probiotics in the prevention and treatment of colorectal cancer. J Cell Physiol 234(10):17127–17143. https://doi.org/10.1002/jcp.28473

    Article  CAS  PubMed  Google Scholar 

  9. Liao Y, Yang ZH, Huang JT et al (2018) Nuclear receptor binding protein 1 correlates with better prognosis and induces caspase-dependent intrinsic apoptosis through the JNK signalling pathway in colorectal cancer. Cell Death Dis 9(4):436. https://doi.org/10.1038/s41419-018-0402-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Noh DO, Gilliland SE (1993) Influence of bile on cellular integrity and beta-galactosidase activity of Lactobacillus acidophilus. J Dairy Sci 76(5):1253–1259. https://doi.org/10.3168/jds.S0022-0302(93)77454-8

    Article  CAS  PubMed  Google Scholar 

  11. Chen TT, Zhao XX, Ren YM et al (2019) Triptolide modulates tumour-colonisation and anti-tumour effect of attenuated Salmonella encoding DNase I. Appl Microbiol Biot 103(2):929–939. https://doi.org/10.1007/s00253-018-9481-8

    Article  CAS  Google Scholar 

  12. Tewary P, AaL G, Sayers TJ (2017) Using natural products to promote caspase-8-dependent cancer cell death. Cancer Immunol Immun 66(2):223–231. https://doi.org/10.1007/s00262-016-1855-0

    Article  CAS  Google Scholar 

  13. Li SY, Jiang ZX, Chai WJ et al (2019) Autophagy activation alleviates nonylphenol-induced apoptosis in cultured cortical neurons. Neurochem Int 122:73–84. https://doi.org/10.1016/j.neuint.2018.11.009

    Article  CAS  PubMed  Google Scholar 

  14. Larsen BD, Sorensen CS (2017) The caspase-activated DNase: apoptosis and beyond. FEBS J 284(8):1160–1170. https://doi.org/10.1111/febs.13970

    Article  CAS  PubMed  Google Scholar 

  15. Lu Y, Yu Z, Zhang Z et al (2021) Bifidobacterium animalis F1–7 in combination with konjac glucomannan improves constipation in mice via humoral transport. Food Function 12(2):791–801. https://doi.org/10.1039/d0fo02227f

    Article  CAS  PubMed  Google Scholar 

  16. Jiang SP, Shi FL, Lin H et al (2020) Inonotus obliquus polysaccharides induces apoptosis of lung cancer cells and alters energy metabolism via the LKB1/AMPK axis. Int J Biol Macromol 151:1277–1286. https://doi.org/10.1016/j.ijbiomac.2019.10.174

    Article  CAS  PubMed  Google Scholar 

  17. Lee KHLDW, Kang BC (2020) The ‘R’ principles in laboratory animal experiments. Lab Anim Res 36:45. https://doi.org/10.1186/s42826-020-00078-6

    Article  PubMed  PubMed Central  Google Scholar 

  18. Teng Y, Ren Y, Sayed M et al (2018) Plant-derived exosomal microRNAs shape the gut microbiota. Cell Host Microbe 24(5):637–652. https://doi.org/10.1016/j.chom.2018.10.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Behera B, Devi KS, Mishra D et al (2014) Biochemical analysis and antitumour effect of Abrus precatorius agglutinin derived peptides in Ehrlich’s ascites and B16 melanoma mice tumour model. Environ Toxicol Pharmacol 38(1):288–296. https://doi.org/10.1016/j.etap.2014.06.006

    Article  CAS  PubMed  Google Scholar 

  20. Xing R, Yang H, Wang X et al (2020) Effects of calcium source and calcium level on growth performance, immune organ indexes, serum components, intestinal microbiota, and intestinal morphology of broiler chickens. J Appl Poultry Res 29(1):106–120. https://doi.org/10.3382/japr/pfz033

    Article  CAS  Google Scholar 

  21. Liu N, Dong ZH, Zhu XS et al (2018) Characterization and protective effect of Polygonatum sibiricum polysaccharide against cyclophosphamide-induced immunosuppression in Balb/c mice. Int J Biol Macromol 107:796–802. https://doi.org/10.1016/j.ijbiomac.2017.09.051

    Article  CAS  PubMed  Google Scholar 

  22. Gao ZZ, Zhang C, Jing LR et al (2020) The structural characterization and immune modulation activitives comparison of Codonopsis pilosula polysaccharide (CPPS) and selenizing CPPS (sCPPS) on mouse in vitro and vivo. Int J Biol Macromol 160:814–822. https://doi.org/10.1016/j.ijbiomac.2020.05.149

    Article  CAS  PubMed  Google Scholar 

  23. Patel BA, Fidalgo S, Wang C et al (2017) The TNF-α antagonist etanercept reverses age-related decreases in colonic SERT expression and faecal output in mice. Sci Rep-Uk 7:42754

    Article  CAS  Google Scholar 

  24. Wan YY, Luo HS, Yang M et al (2020) miR-324-5p contributes to cell proliferation and apoptosis in pancreatic cancer by targeting KLF3. Mol Ther-Oncolytics 18:432–442. https://doi.org/10.1016/j.omto.2020.07.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Le Noci V, Guglielmetti S, Arioli S et al (2018) Modulation of pulmonary microbiota by antibiotic or probiotic aerosol therapy: a strategy to promote immunosurveillance against lung metastases. Cell Rep 24(13):3528–3538. https://doi.org/10.1016/j.celrep.2018.08.090

    Article  CAS  PubMed  Google Scholar 

  26. Longhi G, Van Sinderen D, Ventura M et al (2020) Microbiota and cancer: the emerging beneficial role of bifidobacteria in cancer immunotherapy. Front Microbiol. https://doi.org/10.1016/j.jconrel.2020.04.037

    Article  PubMed  PubMed Central  Google Scholar 

  27. Callstrom MR, Woodrum DA, Nichols FC et al (2020) Multicenter Study of Metastatic Lung Tumors Targeted by Interventional Cryoablation Evaluation (SOLSTICE). J Thorac Oncol 15(7):1200–1209. https://doi.org/10.1016/j.jtho.2020.02.022

    Article  PubMed  PubMed Central  Google Scholar 

  28. Limond J, Thomas S, Bull KS et al (2020) Quality of survival assessment in European childhood brain tumour trials, for children below the age of 5 years. Eur J Paediatr Neuro 25:59–67. https://doi.org/10.1016/j.ejpn.2019.10.002

    Article  CAS  Google Scholar 

  29. Amit Kumar GS, Nagar RK, Chauhan N, Gupta N, Kaul A, Zabeer Ahmed PL, Sangwan PS, Kumar GY (2021) Evaluation of the immunomodulatory and anti-inflammatory activity of Bakuchiol using RAW 264.7 macrophage cell lines and in animal models stimulated by lipopolysaccharide (LPS). Int Immunopharmacol 91:107264. https://doi.org/10.1016/j.intimp.2020.107264

    Article  CAS  PubMed  Google Scholar 

  30. Jiang Z, Chi J, Li H et al (2021) Effect of chitosan oligosaccharide-conjugated selenium on improving immune function and blocking gastric cancer growth. Eur J Pharmacol 891:173673. https://doi.org/10.1016/j.ejphar.2020.173673

    Article  CAS  PubMed  Google Scholar 

  31. Li H, Somiya M, Kuroda S (2020) Enhancing antibody-dependent cellular phagocytosis by re-education of tumor-associated macrophages with resiquimod-encapsulated liposomes. Biomaterials 268:120601. https://doi.org/10.1016/j.biomaterials.2020.120601

    Article  CAS  PubMed  Google Scholar 

  32. Young Ji Ko JWL, Kim H, Cho E, Yang Y, Kim IS, Kim SH, Kwon IC (2020) Versatile activatable vSIRPα-probe for cancer-targeted imaging and macrophage-mediated phagocytosis of cancer cells. J Control Release 323:376–386. https://doi.org/10.1016/j.jconrel.2020.04.037

    Article  CAS  PubMed  Google Scholar 

  33. Hendriks JJ, Slaets H, Carmans S et al (2008) Leukemia inhibitory factor modulates production of inflammatory mediators and myelin phagocytosis by macrophages. J Neuroimmunol 204(1–2):52–57. https://doi.org/10.1016/j.jneuroim.2008.07.015

    Article  CAS  PubMed  Google Scholar 

  34. Dang AT, Marsland BJ (2019) Microbes, metabolites, and the gut-lung axis. Mucosal Immunol 12(4):843–850. https://doi.org/10.1038/s41385-019-0160-6

    Article  CAS  PubMed  Google Scholar 

  35. Yonehara SIA, Yonehara M (1989) A cell killing monoclonal antibody (anti-Fas) to a cell surface antigen co-down regulated with the receptor of tumor necrosis factor. J Exp Med 169(1):1747–1756. https://doi.org/10.1016/0192-0561(88)90288-3

    Article  CAS  PubMed  Google Scholar 

  36. Vaishnaw a K OJR, Chu J L. (1999) The molecular basis for apoptotic defects in patients with CD95 (Fas/Apo1) mutations. J Clin Investig 103(7):1099. https://doi.org/10.1172/JCI5121

    Article  Google Scholar 

  37. Strasser ANK (1999) FADD/MORT1, a signal transducer that can promote cell death or cell growth. Int J Biochem Cell Biol 31(5):533–537. https://doi.org/10.1016/S1357-2725(99)00003-5

    Article  CAS  PubMed  Google Scholar 

  38. Cohen GM (1997) Caspases: the executioners of apoptosis. Biochem J 326:1–16. https://doi.org/10.1042/bj3260001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Billen LP, Shamas-Din A, Andrews DW (2008) Bid: a Bax-like BH3 protein. Oncogene 27:S93–S104. https://doi.org/10.1038/onc.2009.47

    Article  CAS  PubMed  Google Scholar 

  40. Schwabe RF, Greten TF (2020) Gut microbiome in HCC - mechanisms, diagnosis and therapy. J Hepatol 72(2):230–238. https://doi.org/10.1016/j.jhep.2019.08.016

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Thanks to Dr. Yeting Wu for the technical guidance.

Funding

This work was financially supported by the National Key R&D of China (grant number 2017YFC13092003) and Heilongjiang Province Key Sci. & Techn. Plan (grant number GA16B201-2).

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Authors and Affiliations

  1. College of Food Science and Technology; Key Laboratory of Environment Correlative Dietology, Ministry of Education, Huazhong Agricultural University, Wuhan, 430070, China

    Youyou Lu

  2. College of Food Science and Engineering, Ocean University of China, Qingdao, 266000, China

    Xi Liang, Yeting Wu, Ruiqi Wang, Tongjie Liu, Huaxi Yi, Zhe Zhang, Pimin Gong & Lanwei Zhang

  3. Affiliated Hospital of Qingdao University, Qingdao, 266042, China

    Zhuang Yu

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Contributions

Youyou Lu: writing of the original draft; Xi Liang: conceptualization; Zhe Zhang: data curation; Yeting Wu: formal analysis; Ruiqi Wang: investigation; Tongjie Liu: methodology; Huaxi Yi: project administration; Zhuang Yu: visualization; Pimin Gong: resources; Lanwei Zhang: writing including review and editing. All authors have read and approved the final manuscript.

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Lu, Y., Liang, X., Wu, Y. et al. Bifidobacterium animalis sup F1-7 Acts as an Effective Activator to Regulate Immune Response Via Casepase-3 and Bak of FAS/CD95 Pathway. Probiotics & Antimicro. Prot. 15, 1234–1249 (2023). https://doi.org/10.1007/s12602-022-09975-9

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