Smad3 promotes cancer progression by inhibiting E4BP4-mediated NK cell development

Nature Communications

Volumn 8, Issue , 2017, Pages

  Tang, Patrick Ming Kuen ^a   Zhou, Shuang ^a,b,c   Meng, Xiao Ming ^a   Wang, Qing Ming ^a   Li, Chun Jie ^a   Lian, Guang Yu ^a   Huang, Xiao Ru ^a   Tang, Yong Jiang ^a   Guan, Xin Yuan ^d   Yan, Bryan Ping Yen ^a   To, Ka Fai ^a   Lan, Hui Yao ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b SHANGHAI PULMONARY HOSPITAL   (China)

^c TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 INTEGRIN; CD31 ANTIGEN; CD4 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; COLLAGENASE 3; GAMMA INTERFERON; GELATINASE A; GELATINASE B; GRANZYME B; GREEN FLUORESCENT PROTEIN; INTERLEUKIN 2; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NEUTRALIZING ANTIBODY; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FOXP3; VASCULOTROPIN; 6,7-DIMETHYL-2-(2E)-3-(1-METHYL-2-PHENYL-1H-PYRROLO(2,3-B)PYRIDIN-3-YL-PROP-2-ENOYL)-1,2,3,4-TETRAHYDROISOQUINOLINE HYDROCHLORIDE; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; ISOQUINOLINE DERIVATIVE; NFIL3 PROTEIN, MOUSE; PYRIDINE DERIVATIVE; PYRROLE DERIVATIVE;

CANCER; CELLS AND CELL COMPONENTS; DIFFERENTIATION; EXPERIMENTAL STUDY; GENETIC ANALYSIS; INHIBITION; INHIBITOR;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOLUMINESCENCE; BONE MARROW; BONE MARROW CELL; CANCER GROWTH; CANCER INHIBITION; CANCER MORTALITY; CELL DIFFERENTIATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG TARGETING; EX VIVO STUDY; EXON; GENE DELETION; GENE SILENCING; IMMUNOSURVEILLANCE; IN VIVO STUDY; LUCIFERASE ASSAY; LUNG; LUNG ADENOCARCINOMA; MELANOMA; METASTASIS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROMOTER REGION; REGULATORY T LYMPHOCYTE; SPLEEN; STROMA CELL; SYSTEMIC THERAPY; TUMOR INVASION; TUMOR MICROENVIRONMENT; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DISEASE EXACERBATION; EXPERIMENTAL NEOPLASM; FEMALE; GENETICS; IMMUNOLOGY; KAPLAN MEIER METHOD; KNOCKOUT MOUSE; MALE; METABOLISM; NONOBESE DIABETIC MOUSE; RNA INTERFERENCE; SCID MOUSE; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINE, TUMOR; DISEASE PROGRESSION; FEMALE; ISOQUINOLINES; KAPLAN-MEIER ESTIMATE; KILLER CELLS, NATURAL; MALE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; MICE, TRANSGENIC; NEOPLASMS, EXPERIMENTAL; PYRIDINES; PYRROLES; RNA INTERFERENCE; SMAD3 PROTEIN;

EID: 85014710614     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14677     Document Type: Article

References (54)

1. Schreiber, R. D., Old, L. J., Smyth, M. J. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 331, 1565-1570 (2011).
2. Junttila, M. R., de Sauvage, F. J. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature 501, 346-354 (2013).
3. Derynck, R., Akhurst, R. J., Balmain, A. TGF-b signaling in tumor suppression and cancer progression. Nat. Genet. 29, 117-129 (2001).
4. Massagué, J. TGFbeta in cancer. Cell 134, 215-230 (2008).
5. Ikushima, H., Miyazono, K. TGFbeta signalling: a complex web in cancer progression. Nat. Rev. Cancer 10, 415-424 (2010).
6. Pickup, M., Novitskiy, S., Moses, H. L. The roles of TGFb in the tumour microenvironment. Nat. Rev. Cancer 13, 788-799 (2013).
7. Yang, L., Pang, Y., Moses, H. L. TGF-beta and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol. 31, 220-227 (2010).
8. Flavell, R. A., Sanjabi, S., Wrzesinski, S. H., Licona-Limón, P. The polarization of immune cells in the tumour environment by TGFbeta. Nat. Rev. Immunol. 10, 554-567 (2010).
9. Datto, M. B., et al. Targeted disruption of Smad3 reveals an essential role in transforming growth factor beta-mediated signal transduction. Mol. Cell Biol. 19, 2495-2504 (1999).
10. Yang, X., et al. Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-beta. EMBO J. 18, 1280-1291 (1999).
11. Giroux, M., et al. SMAD3 prevents graft-versus-host disease by restraining Th1 differentiation and granulocyte-mediated tissue damage. Blood 117, 1734-1744 (2011).
12. Schlenner, S. M., Weigmann, B., Ruan, Q., Chen, Y., von Boehmer, H. Smad3 binding to the foxp3 enhancer is dispensable for the development of regulatory T cells with the exception of the gut. J. Exp. Med. 209, 1529-1535 (2012).
13. Martinez, G. J., et al. Smad3 differentially regulates the induction of regulatory and inflammatory T cell differentiation. J. Biol. Chem. 284, 35283-35286 (2009).
14. Gu, A. D., Wang, Y., Lin, L., Zhang, S. S., Wan, Y. Y. Requirements of transcription factor Smad-dependent and-independent TGF-b signaling to control discrete T-cell functions. Proc. Natl Acad. Sci. USA 109, 905-910 (2012).
15. Rook, A. H., et al. Effects of transforming growth factor beta on the functions of natural killer cells: depressed cytolytic activity and blunting of interferon responsiveness. J. Immunol. 136, 3916-3920 (1986).
16. Bellone, G., Aste-Amezaga, M., Trinchieri, G., Rodeck, U. Regulation of NK cell functions by TGF-beta 1. J. Immunol. 155, 1066-1073 (1995).
17. Trotta, R., et al. TGF-beta utilizes SMAD3 to inhibit CD16-mediated IFNgamma production and antibody-dependent cellular cytotoxicity in human NK cells. J. Immunol. 181, 3784-3792 (2008).
18. Zhu, Y., Richardson, J. A., Parada, L. F., Graff, J. M. Smad3 mutant mice develop metastatic colorectal cancer. Cell 94, 703-714 (1998).
19. Maggio-Price, L., et al. Helicobacter infection is required for inflammation and colon cancer in SMAD3-deficient mice. Cancer Res. 66, 828-838 (2006).
20. Maggio-Price, L., et al. Bacterial infection of Smad3/Rag2 double-null mice with transforming growth factor-beta dysregulation as a model for studying inflammation-associated colon cancer. Am. J. Pathol. 174, 317-329 (2009).
21. Li, A. G., Lu, S. L., Zhang, M. X., Deng, C., Wang, X. J. Smad3 knockout mice exhibit a resistance to skin chemical carcinogenesis. Cancer Res. 64, 7836-7845 (2004).
22. Male, V., et al. The transcription factor E4bp4/Nfil3 controls commitment to the NK lineage and directly regulates Eomes and Id2 expression. J. Exp. Med. 211, 635-642 (2014).
23. Kamizono, S., et al. Nfil3/E4bp4 is required for the development and maturation of NK cells in vivo. J. Exp. Med. 206, 2977-2986 (2009).
24. Gascoyne, D. M., et al. The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat. Immunol. 10, 1118-1124 (2009).
25. Lo, R. S., Witte, O. N. Transforming growth factor-beta activation promotes genetic context-dependent invasion of immortalized melanocytes. Cancer Res. 68, 4248-4257 (2008).
26. Du, G., et al. Naringenin: a potential immunomodulator for inhibiting lung fibrosis and metastasis. Cancer Res. 69, 3205-3212 (2009).
27. Ovcharenko, I., Nobrega, M. A., Loots, G. G., Stubbs, L. ECR Browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Nucleic Acids Res. 32, W280-W286 (2004).
28. Shultz, L. D., et al. Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J. Immunol. 154, 180-191 (1995).
29. Jinnin, M., Ihn, H., Tamaki, K. Characterization of SIS3, a novel specific inhibitor of Smad3, and its effect on transforming growth factorbeta1-induced extracellular matrix expression. Mol. Pharmacol. 69, 597-607 (2006).
30. Laouar, Y., Sutterwala, F. S., Gorelik, L., Flavell, R. A. Transforming growth factor-b controls T helper type 1 cell development through regulation of natural killer cell interferon-g. Nat. Immunol. 6, 600-607 (2005).
31. Lee, J. C., Lee, K. M., Kim, D. W., Heo, D. S. Elevated TGF-beta1 secretion and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. J. Immunol. 172, 7335-7340 (2004).
32. Mamessier, E., et al. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J. Clin. Invest. 121, 3609-3622 (2011).
33. Wu, Y., et al. Monocyte/macrophage-elicited natural killer cell dysfunction in hepatocellular carcinoma is mediated by CD48/2B4 interactions. Hepatology 57, 1107-1116 (2013).
34. Wilson, E. B., et al. Human tumour immune evasion via TGF-b blocks NK cell activation but not survival allowing therapeutic restoration of anti-tumour activity. PLoS ONE 6, e22842 (2011).
35. Imai, K., et al. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 356, 1795-1799 (2000).
36. Pasero, C., et al. Highly effective NK cells are associated with good prognosis in patients with metastatic prostate cancer. Oncotarget 6, 14360-14373 (2015).
37. Harms Pritchard, G., et al. Diverse roles for T-bet in the effector responses required for resistance to infection. J. Immunol. 194, 1131-1140 (2015).
38. Yu, J., Freud, A. G., Caligiuri, M. A. Location and cellular stages of natural killer cell development. Trends Immunol. 34, 573-582 (2013).
39. Nakagawa, T., et al. TGF-beta induces proangiogenic and antiangiogenic factors via parallel but distinct Smad pathways. Kidney Int. 66, 605-613 (2004).
40. Leivonen, S. K., et al. Activation of Smad signaling enhances collagenase-3 (MMP-13) expression and invasion of head and neck squamous carcinoma cells. Oncogene 25, 2588-2600 (2006).
41. Weis, S. M., Cheresh, D. A. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat. Med. 17, 1359-1370 (2011).
42. Kessenbrock, K., Plaks, V., Werb, Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141, 52-67 (2010).
43. Bertran, E., et al. Overactivation of the TGF-b pathway confers a mesenchymallike phenotype and CXCR4-dependent migratory properties to liver tumor cells. Hepatology 58, 2032-2044 (2013).
44. Ghiringhelli, F., et al. CD4\+CD25\+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-beta-dependent manner. J. Exp. Med. 202, 1075-1085 (2005).
45. Jie, H. B., et al. CTLA-4\+ Regulatory T cells increased in cetuximab-treated head and neck cancer patients suppress NK cell cytotoxicity and correlate with poor prognosis. Cancer Res. 75, 2200-2210 (2015).
46. Zaharoff, D. A., Hance, K. W., Rogers, C. J., Schlom, J., Greiner, J. W. Intratumoral immunotherapy of established solid tumors with chitosan/IL-12. J. Immunother. 33, 697-7052010 (2010).
47. Zhou, S., et al. Combination therapy of VEGF-trap and gemcitabine results in improved anti-tumor efficacy in a mouse lung cancer model. PLoS ONE 8, e68589 (2013).
48. Zhou, S., et al. CCR7 expression and intratumoral FOXP3\+ regulatory T cells are correlated with overall survival and lymph node metastasis in gastric cancer. PLoS ONE 8, e74430 (2013).
49. Kataoka, S., et al. Immunologic aspects of the nonobese diabetic (NOD) mouse. Abnormalities of cellular immunity. Diabetes 32, 247-253 (1983).
50. Imamura, M., et al. Autonomous growth and increased cytotoxicity of natural killer cells expressing membrane-bound interleukin-15. Blood 124, 1081-1088 (2014).
51. Weidner, N., Semple, J. P., Welch, W. R., Folkman, J. Tumor angiogenesis and metastasis: correlation in invasive breast carcinoma. N. Engl. J. Med. 324, 1-8 (1991).
52. Meng, X. M., et al. Smad2 protects against TGF-beta/Smad3-mediated renal fibrosis. J. Am. Soc. Nephrol. 21, 1477-1487 (2010).
53. Zhou, Q., Huang, X. R., Yu, J., Yu, X., Lan, H. Y. Long noncoding RNA Arid2-IR is a novel therapeutic target for renal inflammation. Mol. Ther. 23, 1034-1043 (2015).
54. Fathman, J. W., et al. Identification of the earliest natural killer cell-committed progenitor in murine bone marrow. Blood 118, 5439-5447 (2011).