Combination Therapy of TGF-β Blockade and Commensal-derived Probiotics Provides Enhanced Antitumor Immune Response and Tumor Suppression

Theranostics

Volumn 9, Issue 14, 2019, Pages 4115-4129

  Shi, Linlin ^a   Sheng, Jianyong ^a   Wang, Mengli ^a   Luo, Han ^a   Zhu, Jun ^a,b   Zhang, Bixiang ^c   Liu, Zhi ^a   Yang, Xiangliang ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Cancer treatment; Gut microbiota; Immunotherapy; TGF blockade; Tumor immune microenvironment

Indexed keywords

GALUNISERTIB; PROBIOTIC AGENT; RNA 16S; TRANSFORMING GROWTH FACTOR BETA;

4T1 CELL LINE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BACTERIAL STRAIN; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CELL ACTIVATION; CLINICAL EFFECTIVENESS; COLONY FORMING UNIT; CONTROLLED STUDY; DENDRITIC CELL; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; EFFECTOR CELL; EMBRYO; ESCHERICHIA COLI; FECES ANALYSIS; FLOW CYTOMETRY; GENE SEQUENCE; H22 CELL LINE; HISTOLOGY; IMMUNE RESPONSE; INTESTINE FLORA; LIVER CELL CARCINOMA; METASTASIS; MOUSE; NONHUMAN; SPECIES DIVERSITY; TREATMENT OUTCOME; TUMOR GROWTH; TUMOR INVASION; TUMOR MICROENVIRONMENT; TUMOR VOLUME; TUMOR XENOGRAFT; ZEBRA FISH; ANIMAL; BREAST TUMOR; FEMALE; GENETICS; HUMAN; IMMUNOTHERAPY; INTESTINE MUCOSA; LIVER TUMOR; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PROCEDURES; TRANSGENIC ANIMAL; TUMOR CELL LINE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; FLOW CYTOMETRY; GASTROINTESTINAL MICROBIOME; HUMANS; IMMUNOTHERAPY; INTESTINAL MUCOSA; LIVER NEOPLASMS; MICE; PROBIOTICS; RNA, RIBOSOMAL, 16S; TRANSFORMING GROWTH FACTOR BETA; TUMOR MICROENVIRONMENT;

EID: 85067098815     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.35131     Document Type: Article

References (45)

1. Gao S, Yang D, Fang Y, Lin X, Jin X, Wang Q, et al. Engineering Nanoparticles for Targeted Remodeling of the Tumor Microenvironment to Improve Cancer Immunotherapy. Theranostics. 2019; 9: 126-51.
2. Littman DR. Releasing the Brakes on Cancer Immunotherapy. Cell. 2015; 162: 1186-90.
3. Lizee G, Overwijk WW, Radvanyi L, Gao J, Sharma P, Hwu P. Harnessing the power of the immune system to target cancer. Annu Rev Med. 2013; 64: 71-90.
4. Yang Y. Cancer immunotherapy: harnessing the immune system to battle cancer. J Clin Invest. 2015; 125: 3335-7.
5. Topalian SL. Targeting Immune Checkpoints in Cancer Therapy. JAMA. 2017; 318: 1647-8.
6. Weigmann K. Releasing the brakes to fight cancer: The recent discovery of checkpoints has boosted the field of cancer immunotherapy. EMBO Rep. 2016; 17: 1257-60.
7. Neuzillet C, Tijeras-Raballand A, Cohen R, Cros J, Faivre S, Raymond E, et al. Targeting the TGFbeta pathway for cancer therapy. Pharmacol Ther. 2015; 147: 22-31.
8. Bueno L, de Alwis DP, Pitou C, Yingling J, Lahn M, Glatt S, et al. Semi-mechanistic modelling of the tumour growth inhibitory effects of LY2157299, a new type I receptor TGF-beta kinase antagonist, in mice. Eur J Cancer. 2008; 44: 142-50.
9. Rothenberg ML, Carbone DP, Johnson DH. Improving the evaluation of new cancer treatments: challenges and opportunities. Nat Rev Cancer. 2003; 3: 303-9.
10. Yarchoan M, Hopkins A, Jaffee EM. Tumor Mutational Burden and Response Rate to PD-1 Inhibition. N Engl J Med. 2017; 377: 2500-1.
11. Pitt JM, Vetizou M, Daillere R, Roberti MP, Yamazaki T, Routy B, et al. Resistance Mechanisms to Immune-Checkpoint Blockade in Cancer: Tumor-Intrinsic and -Extrinsic Factors. Immunity. 2016; 44: 1255-69.
12. Akhurst RJ, Hata A. Targeting the TGFbeta signalling pathway in disease. Nat Rev Drug Discov. 2012; 11: 790-811.
13. [Internet] A study of galunisertib (LY2157299) in combination with nivolumab in advanced refractory solid tumors and in recurrent or refractory NSCLC, or hepatocellular carcinoma. 2015. https://clinicaltrials.gov/ct2/show/NCT02423343
14. Nelson MH, Diven MA, Huff LW, Paulos CM. Harnessing the Microbiome to Enhance Cancer Immunotherapy. J Immunol Res. 2015; 2015: 368736.
15. Routy B, Gopalakrishnan V, Daillere R, Zitvogel L, Wargo JA, Kroemer G. The gut microbiota influences anticancer immunosurveillance and general health. Nat Rev Clin Oncol. 2018; 15: 382-96.
16. Pope JL, Tomkovich S, Yang Y, Jobin C. Microbiota as a mediator of cancer progression and therapy. Transl Res. 2017; 179: 139-54.
17. Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer. 2013; 13: 800-12.
18. Routy B, Le Chatelier E. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science. 2018; 359: 91-7.
19. Vetizou M, Pitt JM, Daillere R, Lepage P, Waldschmitt N, Flament C, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015; 350: 1079-84.
20. Sonnenborn U. Escherichia coli strain Nissle 1917-from bench to bedside and back: history of a special Escherichia coli strain with probiotic properties. FEMS Microbiol Lett. 2016; 363.
21. Secher T, Kassem S, Benamar M, Bernard I, Boury M, Barreau F, et al. Oral administration of the probiotic strain Escherichia coli nissle 1917 reduces susceptibility to neuroinflammation and repairs experimental autoimmune encephalomyelitis-induced intestinal barrier dysfunction. Front Immunol. 2017; 8: 1096.
22. Scaldaferri F, Gerardi V, Mangiola F, Lopetuso LR, Pizzoferrato M, Petito V, et al. Role and mechanisms of action of Escherichia coli Nissle 1917 in the maintenance of remission in ulcerative colitis patients: An update. World J Gastroenterol. 2016; 22: 5505-11.
23. Lasaro MA, Salinger N, Zhang J, Wang Y, Zhong Z, Goulian M, et al. F1C fimbriae play an important role in biofilm formation and intestinal colonization by the Escherichia coli commensal strain Nissle 1917. Appl Environ Microbiol. 2009; 75: 246-51.
24. Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, Dugar B, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 2011; 472: 57-63.
25. Dong W, Zhang H, Yin X, Liu Y, Chen D, Liang X, et al. Oral delivery of tumor microparticle vaccines activates NOD2 signaling pathway in ileac epithelium rendering potent antitumor T cell immunity. Oncoimmunology. 2017; 6: e1282589.
26. Maier A, Peille AL, Vuaroqueaux V, Lahn M. Anti-tumor activity of the TGF-beta receptor kinase inhibitor galunisertib (LY2157299 monohydrate) in patient-derived tumor xenografts. Cell Oncol (Dordr). 2015; 38: 131-44.
27. Derynck R, Akhurst RJ, Balmain A. TGF-beta signaling in tumor suppression and cancer progression. Nat Genet. 2001; 29: 117-29.
28. Herbertz S, Sawyer JS, Stauber AJ, Gueorguieva I, Driscoll KE, Estrem ST, et al. Clinical development of galunisertib (LY2157299 monohydrate), a small molecule inhibitor of transforming growth factor-beta signaling pathway. Drug Des Devel Ther. 2015; 9: 4479-99.
29. Park J, Wrzesinski SH, Stern E, Look M, Criscione J, Ragheb R, et al. Combination delivery of TGF-beta inhibitor and IL-2 by nanoscale liposomal polymeric gels enhances tumour immunotherapy. Nat Mater. 2012; 11: 895-905.
30. Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med. 2013; 19: 1423-37.
31. McAllister SS, Weinberg RA. The tumour-induced systemic environment as a critical regulator of cancer progression and metastasis. Nat Cell Biol. 2014; 16: 717-27.
32. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer. 2006; 6: 24-37.
33. Whiteside TL. The tumor microenvironment and its role in promoting tumor growth. Oncogene. 2008; 27: 5904-12.
34. Vivarelli S, Salemi R, Candido S, Falzone L, Santagati M. Gut Microbiota and Cancer: From Pathogenesis to Therapy. Cancers (Basel). 2019; 11(1).
35. Tsilimigras MC, Fodor A, Jobin C. Carcinogenesis and therapeutics: the microbiota perspective. Nat Microbiol. 2017; 2: 17008.
36. Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillere R, Hannani D, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science. 2013; 342: 971-6.
37. Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science. 2015; 350: 1084-9.
38. Elkrief A, Derosa L, Zitvogel L, Kroemer G. The intimate relationship between gut microbiota and cancer immunotherapy. Gut Microbes. 2018: 1-5.
39. Hancock V, Dahl M, Klemm P. Probiotic Escherichia coli strain Nissle 1917 outcompetes intestinal pathogens during biofilm formation. J Med Microbiol. 2010; 59: 392-9.
40. Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 2013; 342: 967-70.
41. de Vos WM. Microbe Profile: Akkermansia muciniphila: a conserved intestinal symbiont that acts as the gatekeeper of our mucosa. Microbiology. 2017; 163: 646-8.
42. Chaput N, Lepage P, Coutzac C, Soularue E, Le Roux K, Monot C, et al. Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol. 2017; 28: 1368-79
43. Lazar V, Ditu LM, Pircalabioru GG, Gheorghe I, Curutiu C, Holban AM, et al. Aspects of Gut Microbiota and Immune System Interactions in Infectious Diseases, Immunopathology, and Cancer. Front Immunol. 2018; 9: 1830.
44. Banna GL, Torino F, Marletta F, Santagati M, Salemi R, Cannarozzo E, et al. Lactobacillus rhamnosus GG: An Overview to Explore the Rationale of Its Use in Cancer. Front Pharmacol. 2017; 8: 603.
45. Cai S, Kandasamy M. Lactobacillus rhamnosus GG Activation of Dendritic Cells and Neutrophils Depends on the Dose and Time of Exposure. J Immunol Res. 2016; 2016: 7402760.