Fusobacterium nucleatum and T cells in colorectal carcinoma

JAMA Oncology

Volumn 1, Issue 5, 2015, Pages 653-661

  Mima, Kosuke ^a   Sukawa, Yasutaka ^a   Nishihara, Reiko ^b   Qian, Zhi Rong ^a   Yamauchi, Mai ^a   Inamura, Kentaro ^a,c   Kim, Sun A ^a   Masuda, Atsuhiro ^a   Nowak, Jonathan A ^d   Nosho, Katsuhiko ^e   Kostic, Aleksandar D ^b,f   Giannakis, Marios ^a,f   Watanabe, Hideo ^a,f   Bullman, Susan ^a,f   Milner, Danny A ^b,d   Harris, Curtis C ^c   Giovannucci, Edward ^b   Garraway, Levi A ^a,f   Freeman, Gordon J ^a,d   Dranoff, Glenn ^a,d   Chan, Andrew T ^a,g   Garrett, Wendy S ^a,f   Huttenhower, Curtis ^b,f   Fuchs, Charles S ^a   Ogino, Shuji ^a,b,d   more..

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^g MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; TUMOR MARKER;

ADAPTIVE IMMUNITY; AGED; CARCINOMA; CLINICAL TRIAL; COLORECTAL TUMOR; CROSS-SECTIONAL STUDY; DNA METHYLATION; FEMALE; FUSOBACTERIUM NUCLEATUM; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; LYMPHOCYTE COUNT; MALE; MICROBIOLOGY; MICROSATELLITE INSTABILITY; MIDDLE AGED; MULTICENTER STUDY; MULTIVARIATE ANALYSIS; MUTATION; ODDS RATIO; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; RIBOTYPING; RISK FACTOR; STATISTICAL MODEL; T LYMPHOCYTE; TISSUE MICROARRAY; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; UNITED STATES;

ADAPTIVE IMMUNITY; AGED; BIOMARKERS, TUMOR; CARCINOMA; COLORECTAL NEOPLASMS; CROSS-SECTIONAL STUDIES; DNA METHYLATION; DNA, BACTERIAL; FEMALE; FUSOBACTERIUM NUCLEATUM; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOHISTOCHEMISTRY; LOGISTIC MODELS; LYMPHOCYTE COUNT; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; MULTIVARIATE ANALYSIS; MUTATION; ODDS RATIO; REAL-TIME POLYMERASE CHAIN REACTION; RIBOTYPING; RISK FACTORS; T-LYMPHOCYTES; TISSUE ARRAY ANALYSIS; TUMOR MICROENVIRONMENT; UNITED STATES;

EID: 85010756263     PISSN: 23742437     EISSN: 23742445     Source Type: Journal    
DOI: 10.1001/jamaoncol.2015.1377     Document Type: Article

References (49)

1. Sharma P, Allison JP. The future of immune checkpoint therapy. Science. 2015;348(6230):56-61.
2. Vanneman M, Dranoff G. Combining immunotherapy and targeted therapies in cancer treatment. Nat Rev Cancer. 2012;12(4):237-251.
3. Mlecnik B, Bindea G, Angell HK, et al. Functional network pipeline reveals genetic determinants associated with in situ lymphocyte proliferation and survival of cancer patients. Sci Transl Med. 2014;6 (228):228ra37.
4. Di Caro G, Bergomas F, Grizzi F, et al. Occurrence of tertiary lymphoid tissue is associated with T cell infiltration and predicts better prognosis in early-stage colorectal cancers. Clin Cancer Res. 2014;20(8):2147-2158.
5. Nosho K, Baba Y, Tanaka N, et al. Tumour-infiltrating T cell subsets, molecular changes in colorectal cancer, and prognosis: cohort study and literature review. J Pathol. 2010;222(4):350-366.
6. Salama P, Phillips M, Grieu F, et al. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Oncol. 2009;27(2):186-192.
7. Llosa NJ, Cruise M, Tam A, et al. The vigorous immune microenvironment of microsatellite instable colon cancer is balanced by multiple counter-inhibitory checkpoints. Cancer Discov. 2015;5(1):43-51.
8. Xiao Y, Freeman GJ. The microsatellite instable subset of colorectal cancer is a particularly good candidate for checkpoint blockade immunotherapy. Cancer Discov. 2015;5(1):16-18.
9. Alexander J, Watanabe T, Wu TT, Rashid A, Li S, Hamilton SR. Histopathological identification of colon cancer with microsatellite instability. Am J Pathol. 2001;158(2):527-535.
10. Tougeron D, Fauquembergue E, Rouquette A, et al. Tumor-infiltrating lymphocytes in colorectal cancers with microsatellite instability are correlated with the number and spectrum of frameshift mutations. Mod Pathol. 2009;22(9):1186-1195.
11. Ogino S, Nosho K, Irahara N, et al. Lymphocytic reaction to colorectal cancer is associated with longer survival, independent of lymph node count, microsatellite instability, and CpG island methylator phenotype. Clin Cancer Res. 2009;15(20):6412-6420.
12. Louis P, Hold GL, Flint HJ. The gut microbiota, bacterialmetabolites and colorectal cancer. Nat Rev Microbiol. 2014;12(10):661-672.
13. Arthur JC, Perez-Chanona E, Mühlbauer M, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science. 2012;338(6103): 120-123.
14. Grivennikov SI, Wang K, Mucida D, et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature. 2012;491(7423):254-258.
15. Belcheva A, Irrazabal T, Robertson SJ, et al. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell. 2014;158 (2):288-299.
16. Ahn J, Sinha R, Pei Z, et al. Human gut microbiome and risk for colorectal cancer. J Natl Cancer Inst. 2013;105(24):1907-1911.
17. Bonnet M, Buc E, Sauvanet P, et al. Colonization of the human gut by E. coli and colorectal cancer risk. Clin Cancer Res. 2014;20(4):859-867.
18. Dejea CM, Wick EC, Hechenbleikner EM, et al. Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci U S A. 2014;111(51):18321-18326.
19. Gagliani N, Hu B, Huber S, Elinav E, Flavell RA. The fire within:microbes inflame tumors. Cell. 2014;157(4):776-783.
20. Irrazábal T, Belcheva A, Girardin SE, Martin A, Philpott DJ. The multifaceted role of the intestinal microbiota in colon cancer. Mol Cell. 2014;54(2): 309-320.
21. Brenner H, Kloor M, Pox CP. Colorectal cancer. Lancet. 2014;383(9927):1490-1502.
22. Ogino S, Galon J, Fuchs CS, Dranoff G. Cancer immunology-analysis of host and tumor factors for personalized medicine. Nat Rev Clin Oncol. 2011;8 (12):711-719.
23. Kostic AD, Gevers D, Pedamallu CS, et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 2012;22(2):292-298.
24. Castellarin M, Warren RL, Freeman JD, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012;22 (2):299-306.
25. Tahara T, Yamamoto E, Suzuki H, et al. Fusobacterium in colonic flora and molecular features of colorectal carcinoma. Cancer Res. 2014; 74(5):1311-1318.
26. Kaplan CW, Ma X, Paranjpe A, et al. Fusobacterium nucleatum outer membrane proteins Fap2 and RadD induce cell death in human lymphocytes. Infect Immun. 2010;78(11):4773-4778.
27. Gur C, Ibrahim Y, Isaacson B, et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity. 2015;42(2):344-355.
28. Kostic AD, Chun E, Robertson L, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 2013;14(2): 207-215.
29. Liao X, Lochhead P, Nishihara R, et al. Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival. N Engl J Med. 2012;367(17):1596-1606.
30. Nishihara R, Wu K, Lochhead P, et al. Long-term colorectal-cancer incidence and mortality after lower endoscopy. N Engl J Med. 2013;369(12):1095-1105.
31. Yamauchi M, Lochhead P, Morikawa T, et al. Colorectal cancer: a tale of two sides or a continuum? Gut. 2012;61(6):794-797.
32. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T)method. Nat Protoc. 2008;3(6):1101-1108.
33. Ogino S, Nosho K, Kirkner GJ, et al. CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut. 2009;58(1):90-96.
34. Ogino S, Kawasaki T, Nosho K, et al. LINE-1 hypomethylation is inversely associated with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Int J Cancer. 2008;122(12):2767-2773.
35. Ogino S, Kawasaki T, Brahmandam M, et al. Precision and performance characteristics of bisulfite conversion and real-time PCR (MethyLight) for quantitative DNA methylation analysis. J Mol Diagn. 2006;8(2):209-217.
36. Irahara N, Nosho K, Baba Y, et al. Precision of pyrosequencing assay to measure LINE-1 methylation in colon cancer, normal colonic mucosa, and peripheral blood cells. J Mol Diagn. 2010;12(2):177-183.
37. Nosho K, Irahara N, Shima K, et al. Comprehensive biostatistical analysis of CpG island methylator phenotype in colorectal cancer using a large population-based sample. PLoS One. 2008;3 (11):e3698.
38. Ogino S, Kawasaki T, Brahmandam M, et al. Sensitive sequencing method for KRAS mutation detection by pyrosequencing. J Mol Diagn. 2005;7 (3):413-421.
39. Imamura Y, Lochhead P, Yamauchi M, et al. Analyses of clinicopathological, molecular, and prognostic associations of KRAS codon 61 and codon 146 mutations in colorectal cancer: cohort study and literature review. Mol Cancer. 2014;13:135.
40. Liao X, Morikawa T, Lochhead P, et al. Prognostic role of PIK3CA mutation in colorectal cancer: cohort study and literature review. Clin Cancer Res. 2012;18(8):2257-2268.
41. Galon J, Mlecnik B, Bindea G, et al. Towards the introduction of the 'Immunoscore' in the classification of malignant tumours. J Pathol. 2014; 232(2):199-209.
42. Gebert B, Fischer W, Weiss E, Hoffmann R, Haas R. Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science. 2003;301 (5636):1099-1102.
43. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation ofmyeloid cells by tumours. Nat Rev Immunol. 2012;12(4):253-268.
44. Mowat AM, Agace WW. Regional specialization within the intestinal immune system. Nat Rev Immunol. 2014;14(10):667-685.
45. Li X, LeBlanc J, Truong A, et al. Ametaproteomic approach to study human-microbial ecosystems at the mucosal luminal interface. PLoS One. 2011;6(11):e26542.
46. Yamauchi M, Morikawa T, Kuchiba A, et al. Assessment of colorectal cancer molecular features along bowel subsites challenges the conception of distinct dichotomy of proximal versus distal colorectum. Gut. 2012;61(6):847-854.
47. Phipps AI, Limburg PJ, Baron JA, et al. Association between molecular subtypes of colorectal cancer and patient survival. Gastroenterology. 2015;148(1):77-87.e2.
48. Samadder NJ, Curtin K, Tuohy TM, et al. Characteristics ofmissed or interval colorectal cancer and patient survival: a population-based study. Gastroenterology. 2014;146(4):950-960.
49. Zitvogel L, Galluzzi L, Viaud S, et al. Cancer and the gut microbiota: an unexpected link. Sci Transl Med. 2015;7(271):271ps1.