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Research Paper

The biotherapeutic Clostridium butyricum MIYAIRI 588 strain potentiates enterotropism of Rorγt+Treg and PD-1 blockade efficacy

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Article: 2315631 | Received 20 Sep 2023, Accepted 02 Feb 2024, Published online: 22 Feb 2024

References

  • Paz-Ares L, Luft A, Vicente D, Tafreshi A, Gumus M, Mazieres J, Hermes B, Çay Şenler F, Csőszi T, Fülöp A. et al. Pembrolizumab plus chemotherapy for squamous non–small-Cell lung cancer. N Engl J Med. 2018;379(21):2040–17. doi:10.1056/NEJMoa1810865.
  • Reck M, Rodriguez-Abreu D, Robinson AG, Hui R, Csoszi T, Fulop A, Gottfried M, Peled N, Tafreshi A, Cuffe S. et al. Pembrolizumab versus chemotherapy for PD-L1–positive non–small-Cell lung cancer. N Engl J Med. 2016;375(19):1823–1833. doi:10.1056/NEJMoa1606774.
  • Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, Chow LQ, Vokes EE, Felip E, Holgado E. et al. Nivolumab versus docetaxel in advanced nonsquamous non–small-Cell lung cancer. N Engl J Med. 2015;373(17):1627–1639. doi:10.1056/NEJMoa1507643.
  • Brahmer J, Reckamp KL, Baas P, Crino L, Eberhardt WE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E. et al. Nivolumab versus Docetaxel in Advanced Squamous-Cell Non–Small-Cell Lung Cancer. N Engl J Med. 2015;373(2):123–135. doi:10.1056/NEJMoa1504627.
  • Ellis PM, Vella ET, Ung YC. Immune checkpoint inhibitors for patients with advanced non–small-Cell lung cancer: a systematic review. Clin Lung Cancer. 2017;18(5):444–459.e1. doi:10.1016/j.cllc.2017.02.001.
  • Borghaei H, Brahmer J. Nivolumab in Nonsquamous Non-Small-Cell Lung Cancer. N Engl J Med. 2016;374:493–494.
  • Lurienne L, Cervesi J, Duhalde L, de Gunzburg J, Andremont A, Zalcman G, Buffet R, Bandinelli P-A. NSCLC immunotherapy efficacy and antibiotic use: a systematic review and meta-analysis. J Thorac Oncol. 2020;15(7):1147–1159. doi:10.1016/j.jtho.2020.03.002.
  • Daillere R, Vetizou M, Waldschmitt N, Yamazaki T, Isnard C, Poirier-Colame V, Duong CM, Flament C, Lepage P, Roberti M. et al. Enterococcus hirae and Barnesiella intestinihominis facilitate cyclophosphamide-induced therapeutic immunomodulatory effects. Immunity. 2016;45(4):931–43. doi:10.1016/j.immuni.2016.09.009.
  • Tomita Y, Ikeda T, Sakata S, Saruwatari K, Sato R, Iyama S, Jodai T, Akaike K, Ishizuka S, Saeki S. et al. Association of Probiotic Clostridium butyricum Therapy with survival and response to Immune Checkpoint Blockade in patients with lung cancer. Cancer Immunol Res. 2020;8(10):1236–1242. doi:10.1158/2326-6066.CIR-20-0051.
  • Tomita Y, Goto Y, Sakata S, Imamura K, Minemura A, Oka K, Hayashi A, Jodai T, Akaike K, Anai M. et al. Clostridium butyricum therapy restores the decreased efficacy of immune checkpoint blockade in lung cancer patients receiving proton pump inhibitors. Oncoimmunology. 2022;11(1):2081010. doi:10.1080/2162402X.2022.2081010.
  • Dizman N, Meza L, Bergerot P, Alcantara M, Dorff T, Lyou Y, Frankel P, Cui Y, Mira V, Llamas M. et al. Nivolumab plus ipilimumab with or without live bacterial supplementation in metastatic renal cell carcinoma: a randomized phase 1 trial. Nat Med. 2022;28(4):704–12. doi:10.1038/s41591-022-01694-6.
  • Seki H, Shiohara M, Matsumura T, Miyagawa N, Tanaka M, Komiyama A, KURATA S. Prevention of antibiotic-associated diarrhea in children by Clostridium butyricum MIYAIRI. Pediatr Int. 2003;45(1):86–90. doi:10.1046/j.1442-200X.2003.01671.x.
  • Hayashi A, Sato T, Kamada N, Mikami Y, Matsuoka K, Hisamatsu T, Hibi T, Roers A, Yagita H, Ohteki T. et al. A single strain of Clostridium butyricum induces intestinal IL-10-producing macrophages to suppress acute experimental colitis in mice. Cell Host Microbe. 2013;13(6):711–22. doi:10.1016/j.chom.2013.05.013.
  • Kashiwagi I, Morita R, Schichita T, Komai K, Saeki K, Matsumoto M, Takeda K, Nomura M, Hayashi A, Kanai T. et al. Smad2 and Smad3 Inversely Regulate TGF-β Autoinduction in Clostridium butyricum-Activated Dendritic Cells. Immunity. 2015;43(1):65–79. doi:10.1016/j.immuni.2015.06.010.
  • Li HY, McSharry M, Bullock B, Nguyen TT, Kwak J, Poczobutt JM, Sippel TR, Heasley LE, Weiser-Evans MC, Clambey ET. et al. The tumor microenvironment regulates sensitivity of murine lung tumors to PD-1/PD-L1 antibody blockade. Cancer Immunol Res. 2017;5(9):767–777. doi:10.1158/2326-6066.CIR-16-0365.
  • Blatner NR, Mulcahy MF, Dennis KL, Scholtens D, Bentrem DJ, Phillips JD, Ham S, Sandall BP, Khan MW, Mahvi DM. et al. Expression of RORγt marks a pathogenic regulatory T cell subset in human colon cancer. Sci Transl Med. 2012;4(164):164ra59. doi:10.1126/scitranslmed.3004566.
  • Kedmi R, Najar TA, Mesa KR, Grayson A, Kroehling L, Hao Y, Hao S, Pokrovskii M, Xu M, Talbot J. et al. A RORγt+ cell instructs gut microbiota-specific Treg cell differentiation. Nature. 2022;610(7933):737–743. doi:10.1038/s41586-022-05089-y.
  • Sefik E, Geva-Zatorsky N, Oh S, Konnikova L, Zemmour D, McGuire AM, Burzyn D, Ortiz-Lopez A, Lobera M, Yang J. et al. Individual intestinal symbionts induce a distinct population of RORγ + regulatory T cells. Science. 2015;349(6251):993–997. doi:10.1126/science.aaa9420.
  • Fidelle M, Rauber C, Alves Costa Silva C, Tian AL, Lahmar I, de La Varende AM, Zhao L, Thelemaque C, Lebhar I, Messaoudene M. et al. A microbiota-modulated checkpoint directs immunosuppressive intestinal T cells into cancers. Science. 2023;380(6649):eabo2296. doi:10.1126/science.abo2296.
  • Derosa L, Routy B, Thomas AM, Iebba V, Zalcman G, Friard S, Mazieres J, Audigier-Valette C, Moro-Sibilot D, Goldwasser F. et al. Intestinal Akkermansia muciniphila predicts clinical response to PD-1 blockade in patients with advanced non-small-cell lung cancer. Nat Med. 2022;28(2):315–24. doi:10.1038/s41591-021-01655-5.
  • Sato R, Tanaka M. Intestinal distribution and intraluminal localization of orally administered Clostridium butyricum in rats. Microbiol Immunol. 1997;41(9):665–71. doi:10.1111/j.1348-0421.1997.tb01909.x.
  • Liu W, Ma F, Sun B, Liu Y, Tang H, Luo J, Chen H, Luo Z. Intestinal microbiome associated with immune-related adverse events for patients treated with anti-PD-1 inhibitors, a real-world study. Front Immunol. 2021;12:756872. doi:10.3389/fimmu.2021.756872.
  • Yang BY, Zhao FZ, Li XH, Zhao MS, Lv JC, Shi MJ, Li J, Zhou Z-Y, Wang J-J, Song J. et al. Alteration of pro-carcinogenic gut microbiota is associated with clear cell renal cell carcinoma tumorigenesis. Front Microbiol. 2023;14:1133782. doi:10.3389/fmicb.2023.1133782.
  • Ohnmacht C, Park JH, Cording S, Wing JB, Atarashi K, Obata Y, Gaboriau-Routhiau V, Marques R, Dulauroy S, Fedoseeva M. et al. The microbiota regulates type 2 immunity through RORγt + T cells. Science. 2015;349(6251):989–993. doi:10.1126/science.aac4263.
  • Baban B, Chandler PR, Sharma MD, Pihkala J, Koni PA, Munn DH, Mellor AL. IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J Immunol. 2009;183(4):2475–2483. doi:10.4049/jimmunol.0900986.
  • Sharma MD, Baban B, Chandler P, Hou DY, Singh N, Yagita H, Azuma M, Blazar BR, Mellor AL, Munn DH. et al. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature tregs via indoleamine 2,3-dioxygenase. J Clin Invest. 2007;117(9):2570–82. doi:10.1172/JCI31911.
  • Rankin LC, Kaiser KA, de Los Santos-Alexis K, Park H, Uhlemann AC, Gray DHD, Arpaia N. Dietary tryptophan deficiency promotes gut RORγt+ Treg cells at the expense of Gata3+ Treg cells and alters commensal microbiota metabolism. Cell Rep. 2023;42(3):112135. doi:10.1016/j.celrep.2023.112135.
  • Qiao M, Zhou F, Liu X, Jiang T, Wang H, Jia Y, Li X, Zhao C, Cheng L, Chen X. et al. Interleukin-10 induces expression of CD39 on CD8+T cells to potentiate anti-PD1 efficacy in EGFR-mutated non-small cell lung cancer. J Immunother Cancer. 2022;10(12):10. doi:10.1136/jitc-2022-005436.
  • Qiao J, Liu Z, Dong C, Luan Y, Zhang A, Moore C, Fu K, Peng J, Wang Y, Ren Z. et al. Targeting tumors with IL-10 Prevents Dendritic Cell-Mediated CD8(+) T Cell apoptosis. Cancer Cell. 2019;35(6):901–915.e4. doi:10.1016/j.ccell.2019.05.005.
  • Lee GK, Park HJ, Macleod M, Chandler P, Munn DH, Mellor AL. Tryptophan deprivation sensitizes activated T cells to apoptosis prior to cell division. Immunology. 2002;107(4):452–60. doi:10.1046/j.1365-2567.2002.01526.x.
  • Habtezion A, Nguyen LP, Hadeiba H, Butcher EC. Leukocyte trafficking to the small intestine and colon. Gastroenterology. 2016;150(2):340–54. doi:10.1053/j.gastro.2015.10.046.
  • Bliss SK, Bliss SP, Beiting DP, Alcaraz A, Appleton JA. IL-10 regulates movement of intestinally derived CD4+ T cells to the liver. J Immunol. 2007;178(12):7974–83. doi:10.4049/jimmunol.178.12.7974.
  • Yurchenko E, Shio MT, Huang TC, Da Silva Martins M, Szyf M, Levings MK, Olivier M, Piccirillo CA. Inflammation-driven reprogramming of CD4+ Foxp3+ regulatory T cells into pathogenic Th1/Th17 T effectors is abrogated by mTOR inhibition in vivo. PloS One. 2012;7(4):e35572. doi:10.1371/journal.pone.0035572.
  • Hagihara M, Yamashita R, Matsumoto A, Mori T, Kuroki Y, Kudo H, Oka K, Takahashi M, Nonogaki T, Yamagishi Y. et al. The impact of Clostridium butyricum MIYAIRI 588 on the murine gut microbiome and colonic tissue. Anaerobe. 2018;54:8–18. doi:10.1016/j.anaerobe.2018.07.012.
  • Ariyoshi T, Hagihara M, Eguchi S, Fukuda A, Iwasaki K, Oka K, Takahashi M, Yamagishi Y, Mikamo H. Clostridium butyricum MIYAIRI 588-induced protectin D1 has an anti-inflammatory effect on antibiotic-induced intestinal disorder. Front Microbiol. 2020;11:587725. doi:10.3389/fmicb.2020.587725.
  • Kanai T, Mikami Y, Hayashi A. A breakthrough in probiotics: Clostridium butyricum regulates gut homeostasis and anti-inflammatory response in inflammatory bowel disease. J Gastroenterol. 2015;50(9):928–39. doi:10.1007/s00535-015-1084-x.
  • Hagihara M, Kuroki Y, Ariyoshi T, Higashi S, Fukuda K, Yamashita R, Matsumoto A, Mori T, Mimura K, Yamaguchi N. et al. Clostridium butyricum modulates the microbiome to protect intestinal barrier function in mice with Antibiotic-Induced Dysbiosis. iScience. 2020;23(1):100772. doi:10.1016/j.isci.2019.100772.
  • Bain CC, Bravo-Blas A, Scott CL, Perdiguero EG, Geissmann F, Henri S, Malissen B, Osborne LC, Artis D, Mowat AM. et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat Immunol. 2014;15(10):929–37. doi:10.1038/ni.2967.
  • Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–7. doi:10.1038/s41587-019-0209-9.
  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–3. doi:10.1038/nmeth.3869.
  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(D1):D590–6. doi:10.1093/nar/gks1219.