Metabolite and microbiome interplay in cancer immunotherapy

Cancer Research

Volumn 76, Issue 21, 2016, Pages 6146-6152

  Johnson, Caroline H ^a   Spilker, Mary E ^b   Goetz, Laura ^c   Peterson, Scott N ^d   Siuzdak, Gary ^e  

^a YALE UNIVERSITY   (United States)

^b PFIZER INC   (United States)

^c SCRIPPS CLINIC   (United States)

^d BURNHAM INSTITUTE   (United States)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; CORTICOSTEROID; CPG OLIGODEOXYNUCLEOTIDE; CYCLOPHOSPHAMIDE; IPILIMUMAB; NIVOLUMAB; PEMBROLIZUMAB; TOLL LIKE RECEPTOR;

BACTERIUM; BACTEROIDES; BIFIDOBACTERIUM; BIOFILM; CANCER GROWTH; CANCER IMMUNOTHERAPY; CELL CYCLE CHECKPOINT; COLITIS; COLON CANCER; COLON CARCINOMA; DATA BASE; DIARRHEA; HELPER CELL; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE SYSTEM; IMMUNITY; IMMUNOMODULATION; LYMPHOMA; MELANOMA; METABOLISM; METABOLITE; MICROBIOME; MUCOSA INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; RASH; REVIEW; SARCOMA; IMMUNOLOGY; IMMUNOTHERAPY; MICROFLORA; NEOPLASMS;

BACTERIA; BIOFILMS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOTHERAPY; MICROBIOTA; NEOPLASMS;

EID: 84995632354     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-0309     Document Type: Review

References (63)

1. Boroughs LK, De Berardinis RJ. Metabolic pathways promoting cancer cell survival and growth. Nat Cell Biol 2015; 17:351-9.
2. Kobayashi T, Glatz M, Horiuchi K, Kawasaki H, Akiyama H, Kaplan DH, et al. Dysbiosis and staphylococcus aureus colonization drives inflammation in atopic dermatitis. Immunity 2015;42:756-66.
3. Groeger D, O'Mahony L, Murphy EF, Bourke JF, Dinan TG, Kiely B, et al. Bifidobacterium infantis 35624 modulates host inflammatory processes beyond the gut. Gut Microbes 2013;4:325-39.
4. Marsland BJ, Gollwitzer ES. Host-microorganism interactions in lung diseases. Nat Rev Immunol 2014;14:827-35.
5. Brassard P, Vutcovici M, Ernst P, Patenaude V, Sewitch M, Suissa S, et al. Increased incidence of inflammatory bowel disease in Quebec residents with airway diseases. Eur Respir J 2015;45:962-8.
6. Farrell JJ, Zhang L, Zhou H, Chia D, Elashoff D, Akin D, et al. Variations of oral microbiota are associated with pancreatic diseases including pancreatic cancer. Gut 2012;61:582-8.
7. Aviles-Jimenez F, Vazquez-Jimenez F, Medrano-Guzman R, Mantilla A, Torres J. Stomach microbiota composition varies between patients with non-atrophic gastritis and patients with intestinal type of gastric cancer. Sci Rep 2014;4:4202.
8. Xie G, Wang X, Liu P, Wei R, Chen W, Rajani C, et al. Distinctly altered gut microbiota in the progression of liver disease. Oncotarget 2016;7: 19355-66.
9. Mima K, Nishihara R, Qian ZR, Cao Y, Sukawa Y, Nowak JA, et al. Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut. 2015 Aug 26. [Epub ahead of print].
10. Zambirinis CP, Levie E, Nguy S, Avanzi A, Barilla R, Xu Y, et al. TLR9 ligation in pancreatic stellate cells promotes tumorigenesis. J Exp Med 2015;212:2077-94.
11. Mu C, Yang Y, Luo Z, Guan L, Zhu W. The colonic microbiome and epithelial transcriptome are altered in rats fed a high-protein diet compared with a normal-protein diet. J Nutr 2016;146:474-83.
12. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013;504:446-50.
13. Zhang C, Zhang M, Wang S, Han R, Cao Y, Hua W, et al. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J 2010;4:232-41.
14. Moya A, Ferrer M. Functional redundancy-induced stability of gut microbiota subjected to disturbance. Trends Microbiol 2016;24:402-13.
15. von Rosenvinge EC, O'May GA, Macfarlane S, Macfarlane GT, Shirtliff ME. Microbial biofilms and gastrointestinal diseases. Pathog Dis 2013;67: 25-38.
16. Probert HM, Gibson GR. Bacterial biofilms in the human gastrointestinal tract. Curr Issues Intest Microbiol 2002;3:23-7.
17. Dejea CM, Wick EC, Hechenbleikner EM, White JR, Mark Welch JL, Rossetti BJ, et al. Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci U S A 2014;111:18321-6.
18. Dejea CM, Sears CL. Do biofilms confer a pro-carcinogenic state? Gut Microbes 2016;7:54-7.
19. Benedix F, Kube R, Meyer F, Schmidt U, Gastinger I, Lippert H, et al. Comparison of 17,641 patients with right- and left-sided colon cancer: differences in epidemiology, perioperative course, histology, and survival. Dis Colon Rectum 2010;53:57-64.
20. Benedix F, Meyer F, Kube R, Kropf S, Kuester D, Lippert H, et al. Influence of anatomical subsite on the incidence of microsatellite instability, and KRAS and BRAF mutation rates in patients with colon carcinoma. Pathol Res Pract 2012;208:592-7.
21. Meguid RA, Slidell MB, Wolfgang CL, Chang DC, Ahuja N. Is there a difference in survival between right- versus left-sided colon cancers? Ann Surg Oncol 2008;15:2388-94.
22. Cammarota G, Branca G, Ardito F, Sanguinetti M, Ianiro G, Cianci R, et al. Biofilm demolition and antibiotic treatment to eradicate resistant Helicobacter pylori: a clinical trial. Clin Gastroenterol Hepatol 2010; 8:817-20.
23. Johnson CH, Dejea CM, Edler D, Hoang LT, Santidrian AF, Felding BH, et al. Metabolism links bacterial biofilms and colon carcinogenesis. Cell Metab 2015;21:891-7.
24. Gerner EW, Meyskens FL Jr. Polyamines and cancer: old molecules, new understanding. Nat Rev Cancer 2004;4:781-92.
25. Babbar N, Gerner EW. Targeting polyamines and inflammation for cancer prevention. Recent Results Cancer Res 2011;188:49-64.
26. Plate L, Marletta MA. Nitric oxide modulates bacterial biofilm formation through a multicomponent cyclic-di-GMP signaling network. Mol Cell 2012;46:449-60.
27. Franks I. Gut microbiota: FUT2 genotype influences the gut microbiota in patients with Crohn's disease and healthy individuals. Nat Rev Gastroenterol Hepatol 2012;9:2.
28. Kim YS. Mucin glycoproteins in colonic neoplasia. Keio J Med 1998;47: 10-8.
29. Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, Peters EC, et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A 2009;106:3698-703.
30. Zheng X, Xie G, Zhao A, Zhao L, Yao C, Chiu NH, et al. The footprints of gut microbial-mammalian co-metabolism. J Proteome Res 2011;10:5512-22.
31. Faith JJ, Colombel JF, Gordon JI. Identifying strains that contribute to complex diseases through the study of microbial inheritance. Proc Natl Acad Sci U S A 2015;112:633-40.
32. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 2013;341:1241214.
33. O'Keefe SJ, Li JV, Lahti L, Ou J, Carbonero F, Mohammed K, et al. Fat, fibre and cancer risk in African Americans and rural Africans. Nat Commun 2015;6:6342.
34. Bouslimani A, Porto C, Rath CM, Wang M, Guo Y, Gonzalez A, et al. Molecular cartography of the human skin surface in 3D. Proc Natl Acad Sci U S A 2015;112:E2120-9.
35. Shoaie S, Ghaffari P, Kovatcheva-Datchary P, Mardinoglu A, Sen P, Pujos-Guillot E, et al. Quantifying diet-induced metabolic changes of the human gut microbiome. Cell Metab 2015;22:320-31.
36. Posma JM, Robinette SL, Holmes E, Nicholson JK. Metabo Networks, an interactive Matlab-based toolbox for creating, customizing and exploring sub-networks from KEGG. Bioinformatics 2014;30:893-5.
37. Human Microbiome Project Consortium. A framework for human microbiome research. Nature 2012;486:215-21.
38. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335-6.
39. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, et al. The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 2008;9:386.
40. Smith CA, O'Maille G, Want EJ, Qin C, Trauger SA, Brandon TR, et al. METLIN - A metabolite mass spectral database. Ther Drug Monit 2005;27: 747-51.
41. Wishart DS, Tzur D, Knox C, Eisner R, Guo AC, Young N, et al. HMDB: the Human Metabolome Database. Nucleic Acids Res 2007;35:D521-6.
42. Sung JH, Hale V, Merkel AC, Kim P, Chia N. Metabolic modeling with Big Data and the gut microbiome. Appl Transl Genomics 2016;10:10-5.
43. Palsson B, Zengler K. The challenges of integrating multi-omic data sets. Nat Chem Biol 2010;6:787-9.
44. Weir TL, Manter DK, Sheflin AM, Barnett BA, Heuberger AL, Ryan EP. Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults. PLoS One 2013;8:e70803.
45. Markert EK, Vazquez A. Mathematical models of cancer metabolism. Cancer Metab 2015;3:14.
46. Heinken A, Thiele I. Systems biology of host-microbe metabolomics. Wiley Interdiscip Rev Syst Biol Med 2015;7:195-219.
47. Orth JD, Thiele I, Palsson BO. What is flux balance analysis? Nat Biotechnol 2010;28:245-8.
48. McHardy IH, Goudarzi M, Tong M, Ruegger PM, Schwager E, Weger JR, et al. Integrative analysis of the microbiome and metabolome of the human intestinal mucosal surface reveals exquisite inter-relationships. Microbiome 2013;1:17.
49. Tong M, McHardy I, Ruegger P, Goudarzi M, Kashyap PC, Haritunians T, et al. Reprograming of gut microbiome energy metabolism by the FUT2 Crohn's disease risk polymorphism. ISME J 2014;8:2193-206.
50. Heberling C, Dhurjati P. Novel systems modeling methodology in comparative microbial metabolomics: identifying key enzymes and metabolites implicated in autism spectrum disorders. Int J Mol Sci 2015;16:8949-67.
51. De Vita VT, Hellman S, Rosenberg SA. Biologic therapy of cancer. Philadelphia, PA: Lippincott; 1991.
52. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, de Roos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013;504:451-5.
53. Park J, Kim M, Kang SG, Jannasch AH, Cooper B, Patterson J, et al. Shortchain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR-S6K pathway. Mucosal Immunol 2015;8:80-93.
54. O'Sullivan D, Pearce EL. Targeting T cell metabolism for therapy. Trends Immunol 2015;36:71-80.
55. 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.
56. Vetizou M, Pitt JM, Daillére 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.
57. Mockler MB, Conroy MJ, Lysaght J. Targeting T cellimmunometabolism for cancer immunotherapy; understanding the impact of the tumor microenvironment. Front Oncol 2014;4:107.
58. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A 2010;107:12204-9.
59. Faith JJ, Ahern PP, Ridaura VK, Cheng J, Gordon JI. Identifying gut microbehost phenotype relationships using combinatorial communities in gnotobiotic mice. Science Transl Med 2014;6:220ra11.
60. Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillére R, Hannani D, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 2013;342:971-6.
61. 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.
62. Sharma P, Allison JP. The future of immune checkpoint therapy. Science 2015;348:56-61.
63. Dubin K, Callahan MK, Ren B, Khanin R, Viale A, Ling L, et al. Intestinal microbiome analyses identify melanoma patients at risk for checkpoint-blockade-induced colitis. Nat Commun 2016;7:10391.