MicroRNA let-7, T cells, and patient survival in colorectal cancer

Cancer Immunology Research

Volumn 4, Issue 11, 2016, Pages 927-935

  Dou, Ruoxu ^a,b   Nishihara, Reiko ^a,c   Cao, Yin ^c,d   Hamada, Tsuyoshi ^a   Mima, Kosuke ^a   Masuda, Atsuhiro ^a   Masugi, Yohei ^a   Shi, Yan ^a   Gu, Mancang ^a   Li, Wanwan ^a   Da Silva, Annacarolina ^a   Nosho, Katsuhiko ^a,e   Zhang, Xuehong ^a   Meyerhardt, Jeffrey A ^a   Giovannucci, Edward L ^c   Chan, Andrew T ^a,d   Fuchs, Charles S ^a   Qian, Zhi Rong ^a   Ogino, Shuji ^a,c,f  

^a HARVARD MEDICAL SCHOOL   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; CD45RO ANTIGEN; K RAS PROTEIN; LET 7 PROTEIN; LET 7A PROTEIN; LET 7B PROTEIN; LONG INTERSPERSED NUCLEOTIDE ELEMENT 1; MICRORNA; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE CATALYTIC SUBUNIT ALPHA; TRANSCRIPTION FACTOR FOXP3; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; UNTRANSLATED RNA; BIOLOGICAL MARKER; MIRNLET7 MICRORNA, HUMAN; TUMOR MARKER;

AGED; ARTICLE; CANCER PATIENT; CANCER PROGNOSIS; CANCER TISSUE; CD3+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DENSITY; COLORECTAL CANCER; COMPUTER ASSISTED DIAGNOSIS; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HAZARD RATIO; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LOGISTIC REGRESSION ANALYSIS; LYMPHOCYTIC INFILTRATION; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; MOLECULAR EPIDEMIOLOGY; OUTCOME VARIABLE; PROPORTIONAL HAZARDS MODEL; PROTEIN METHYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL RATE; T LYMPHOCYTE; TISSUE MICROARRAY; TISSUE SECTION; TUMOR MICROENVIRONMENT; UNITED STATES; COLORECTAL TUMOR; FOLLOW UP; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; KAPLAN MEIER METHOD; LYMPHOCYTE COUNT; METABOLISM; MORTALITY; MUCOSA; MUTATION; ODDS RATIO; PATHOLOGY; PROGNOSIS; TUMOR ASSOCIATED LEUKOCYTE;

BIOMARKERS; BIOMARKERS, TUMOR; COLORECTAL NEOPLASMS; FOLLOW-UP STUDIES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOPHENOTYPING; KAPLAN-MEIER ESTIMATE; LYMPHOCYTE COUNT; LYMPHOCYTES, TUMOR-INFILTRATING; MICRORNAS; MUCOUS MEMBRANE; MUTATION; ODDS RATIO; PROGNOSIS; T-LYMPHOCYTES;

EID: 85016117736     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-16-0112     Document Type: Article

References (50)

1. Ogino S, Galon J, Fuchs CS, Dranoff G. Cancer immunology-Analysis of host and tumor factors for personalized medicine. Nat Rev Clin Oncol 2011;8:711-9.
2. Mlecnik B, Bindea G, Angell HK, Maby P, Angelova M, Tougeron D, et al. Integrative analyses of colorectal cancer show immunoscore is a stronger predictor of patient survival than microsatellite instability. Immunity 2016;44:698-711.
3. Di CaroG, Marchesi F, Laghi L,Grizzi F. Immune cells: plastic players along colorectal cancer progression. J Cell Mol Med 2013;17:1088-95.
4. Ogino S, Nosho K, Irahara N, Meyerhardt JA, Baba Y, Shima K, 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: 6412-20.
5. Nosho K, Baba Y, Tanaka N, Shima K, Hayashi M, Meyerhardt JA, et al. Tumour-infiltrating T-cell subsets, molecular changes in colorectal cancer, and prognosis: cohort study and literature review. J Pathol 2010;222: 350-66.
6. Pages F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 2005;353:2654-66.
7. Mlecnik B, Tosolini M, Kirilovsky A, Berger A, Bindea G, Meatchi T, et al. Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol 2011;29: 610-8.
8. Smyth MJ, Ngiow SF, Ribas A, Teng MW. Combination cancer immunotherapies tailored to the tumour microenvironment.Nat Rev Clin Oncol 2016;13:143-58.
9. Le DT, Uram JN,WangH, Bartlett BR, KemberlingH, Eyring AD, et al. PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med 2015;372:2509-20.
10. Giannakis M, Mu XJ, Shukla SA, Qian ZR, Cohen O, Nishihara R, et al. Genomic correlates of immune-cell infiltrates in colorectal carcinoma. Cell Rep 2016;15:857-65.
11. Llosa NJ, Cruise M, Tam A,Wicks EC, Hechenbleikner EM, Taube JM, et al. The vigorous immune microenvironment of microsatellite instable colon cancer is balanced by multiple counter-inhibitory checkpoints. Cancer Discov 2015;5:43-51.
12. Jasinski-Bergner S, Mandelboim O, Seliger B. The role of microRNAs in the control of innate immune response in cancer. J Natl Cancer Inst 2014;106: dju257.
13. Li J, Tan S, Kooger R, Zhang C, Zhang Y. MicroRNAs as novel biological targets for detection and regulation. Chem Soc Rev 2014;43:506-17.
14. Cheng CJ, Bahal R, Babar IA, Pincus Z, Barrera F, Liu C, et al. MicroRNA silencing for cancer therapy targeted to the tumour microenvironment. Nature 2015;518:107-10.
15. Mima K, Nishihara R, Nowak JA, Kim SA, Song M, Inamura K, et al. MicroRNA MIR21 and T cells in colorectal cancer. Cancer Immunol Res 2016;4:33-40.
16. Chen XM, Splinter PL, O'Hara SP, LaRusso NF. A cellularmicro-RNA, let-7i, regulates Toll-like receptor 4 expression and contributes to cholangiocyte immune responses against Cryptosporidium parvum infection. J Biol Chem 2007;282:28929-38.
17. Androulidaki A, Iliopoulos D, Arranz A, Doxaki C, Schworer S, Zacharioudaki V, et al. The kinase Akt1 controls macrophage response to lipopolysaccharide by regulating microRNAs. Immunity 2009;31:220-31.
18. Almanza G, Fernandez A, Volinia S, Cortez-Gonzalez X, Croce CM, Zanetti M. Selected microRNAs define cell fate determination of murine central memory CD8 T cells. PLoS One 2010;5:e11243.
19. Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H, et al. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res 2004;64:3753-6.
20. Nam EJ, Yoon H, Kim SW, Kim H, Kim YT, Kim JH, et al. MicroRNA expression profiles in serous ovarian carcinoma. Clin Cancer Res 2008; 14:2690-5.
21. Lu L, Katsaros D, de la Longrais IA, Sochirca O, Yu H. Hypermethylation of let-7a-3 in epithelial ovarian cancer is associated with low insulin-like growth factor-II expression and favorable prognosis. Cancer Res 2007; 67:10117-22.
22. King CE, Wang L, Winograd R, Madison BB, Mongroo PS, Johnstone CN, et al. LIN28B fosters colon cancer migration, invasion and transformation through let-7-dependent and-independent mechanisms. Oncogene 2011;30:4185-93.
23. Liao X, Lochhead P, Nishihara R, Morikawa T, Kuchiba A, Yamauchi M, et al. Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival. N Engl J Med 2012;367:1596-606.
24. Nishihara R, Lochhead P, Kuchiba A, Jung S, Yamauchi M, Liao X, et al. Aspirin use and risk of colorectal cancer according to BRAF mutation status. JAMA 2013;309:2563-71.
25. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008;3:1101-8.
26. Ogino S, Kawasaki T, Kirkner GJ, Loda M, Fuchs CS. CpG island methylator phenotype-low (CIMP-low) in colorectal cancer: possible associations with male sex and KRAS mutations. J Mol Diagn 2006;8:582-8.
27. Ogino S, Kawasaki T, Brahmandam M, Yan L, Cantor M, Namgyal C, et al. Sensitive sequencing method for KRAS mutation detection by Pyrosequencing. J Mol Diagn 2005;7:413-21.
28. Imamura Y, Lochhead P, Yamauchi M, Kuchiba A, Qian ZR, Liao X, 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.
29. Liao X, Morikawa T, Lochhead P, Imamura Y, Kuchiba A, Yamauchi M, et al. Prognostic role of PIK3CA mutation in colorectal cancer: cohort study and literature review. Clin Cancer Res 2012;18:2257-68.
30. Ogino S, Nosho K, Kirkner GJ, Kawasaki T, Meyerhardt JA, Loda M, et al. CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut 2009;58:90-6.
31. Ogino S, Nosho K, Kirkner GJ, Kawasaki T, Chan AT, Schernhammer ES, et al. A cohort study of tumoral LINE-1 hypomethylation and prognosis in colon cancer. J Natl Cancer Inst 2008;100:1734-8.
32. Irahara N, Nosho K, Baba Y, Shima K, Lindeman NI, Hazra A, et al. Precision of pyrosequencing assay tomeasure LINE-1methylation in colon cancer, normal colonic mucosa, and peripheral blood cells. J Mol Diagn 2010;12:177-83.
33. Hu G, Zhou R, Liu J, Gong AY, Eischeid AN, Dittman JW, et al. MicroRNA-98 and let-7 confer cholangiocyte expression of cytokine-inducible Src homology 2-containing protein in response to microbial challenge. J Immunol 2009;183:1617-24.
34. Kumar M, Sahu SK, Kumar R, Subuddhi A, Maji RK, Jana K, et al. MicroRNA let-7 modulates the immune response to mycobacterium tuberculosis infection via control of A20, an inhibitor of the NF-kappaB pathway. Cell Host Microbe 2015;17:345-56.
35. Schulte LN, Eulalio A, Mollenkopf HJ, Reinhardt R, Vogel J. Analysis of the host microRNA response to Salmonella uncovers the control of major cytokines by the let-7 family. EMBO J 2011;30:1977-89.
36. Marcais A, Blevins R, Graumann J, Feytout A, Dharmalingam G, Carroll T, et al. microRNA-mediated regulation of mTOR complex components facilitates discrimination between activation and anergy in CD4 T cells. J Exp Med 2014;211:2281-95.
37. Zhang Y, Wang X, Zhong M, Zhang M, Suo Q, Lv K. MicroRNA let-7a ameliorates con A-induced hepatitis by inhibiting IL-6-dependent Th17 cell differentiation. J Clin Immunol 2013;33:630-9.
38. Colussi D, Brandi G, Bazzoli F, Ricciardiello L. Molecular pathways involved in colorectal cancer: implications for disease behavior and prevention. Int J Mol Sci 2013;14:16365-85.
39. Kuipers EJ, Grady WM, Lieberman D, Seufferlein T, Sung JJ, Boelens PG, et al. Colorectal cancer. Nat Rev Dis Primers 2015;1:15065.
40. Rooney MS, Shukla SA,Wu CJ, Getz G, Hacohen N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell 2015;160:48-61.
41. Fridman WH, Pages F, Sautes-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012;12:298-306.
42. Galon J, Mlecnik B, Bindea G, Angell HK, Berger A, Lagorce C, et al. Towards the introduction of the 'Immunoscore' in the classification of malignant tumours. J Pathol 2014;232:199-209.
43. Rozek LS, Schmit SL, Greenson JK, Tomsho LP, Rennert HS, Rennert G, et al. Tumor-infiltrating lymphocytes, Crohn's-like lymphoid reaction, and survival from colorectal cancer. J Natl Cancer Inst 2016;108:djw027.
44. Masugi Y, Nishihara R, Yang J, Mima K, da Silva A, Shi Y, et al. Tumour CD274 (PD-L1) expression and T cells in colorectal cancer. Gut 2016; DOI 10.1136/gutjnl-2016-311421.
45. Rosenbaum MW, Bledsoe JR, Morales-Oyarvide V, Huynh TG, Mino-Kenudson M. PD-L1 expression in colorectal cancer is associated with microsatellite instability, BRAF mutation, medullary morphology and cytotoxic tumor-infiltrating lymphocytes. Mod Pathol 2016;29: 1104-12.
46. Akbay EA, Koyama S, Carretero J, Altabef A, Tchaicha JH, Christensen CL, et al. Activation of the PD-1 pathway contributes to immune escape in EGFR-driven lung tumors. Cancer Discov 2013;3:1355-63.
47. Schetter AJ, Leung SY, Sohn JJ, Zanetti KA, Bowman ED, Yanaihara N, et al. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA 2008;299:425-36.
48. Slattery ML, Herrick JS, Mullany LE, Valeri N, Stevens J, Caan BJ, et al. An evaluation and replication of miRNAs with disease stage and colorectal cancer-specific mortality. Int J Cancer 2015;137:428-38.
49. Ogino S, Chan AT, Fuchs CS, Giovannucci E. Molecular pathological epidemiology of colorectal neoplasia: an emerging transdisciplinary and interdisciplinary field. Gut 2011;60:397-411.
50. Ogino S, Nishihara R, VanderWeele TJ,WangM,Nishi A, Lochhead P, et al. Review article: the role of molecular pathological epidemiology in the study of neoplastic and non-neoplastic diseases in the era of precision medicine. Epidemiology 2016;27:602-11.