miR-181a Induces Macrophage Polarized to M2 Phenotype and Promotes M2 Macrophage-mediated Tumor Cell Metastasis by Targeting KLF6 and C/EBPα

Molecular Therapy Nucleic Acids

Volumn 5, Issue , 2016, Pages e368-

  Bi, Jia ^a   Zeng, Xianxin ^a   Zhao, Lin ^a   Wei, Qian ^a   Yu, Lifeng ^a   Wang, Xinnan ^a   Yu, Zhaojin ^a   Cao, Yaming ^a   Shan, Fengping ^a   Wei, Minjie ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

C EBP ; KLF6; macrophages; miR 181a; polarization

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; KRUPPEL LIKE FACTOR 6; MESSENGER RNA; MICRORNA; MICRORNA 181A; UNCLASSIFIED DRUG; ARG 1 PROTEIN; CD163 ANTIGEN; GAMMA INTERFERON; GELATINASE A; GELATINASE B; HLA DR ANTIGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 4; LIPOPOLYSACCHARIDE; MACROPHAGE DERIVED CHEMOKINE; PROTEIN; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; UPA PROTEIN; UVOMORULIN; VIMENTIN; YM 1 PROTEIN;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; BREAST CANCER CELL LINE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; HCT 116 CELL LINE; HUMAN; HUMAN CELL; MACROPHAGE; METASTASIS; MOUSE; NONHUMAN; OVARIAN CANCER CELL LINE; POLARIZATION; PRIORITY JOURNAL; TUMOR CELL; 3' UNTRANSLATED REGION; CANCER CELL; CARCINOMA CELL LINE; CELL PLASTICITY; CELL POLARITY; DOWN REGULATION; GENE CONTROL; GENE TARGETING; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE; LUCIFERASE ASSAY; MCF-7 CELL LINE; OVARY CARCINOMA; PHENOTYPE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

EID: 85015152775     PISSN: None     EISSN: 21622531     Source Type: Journal    
DOI: 10.1038/mtna.2016.71     Document Type: Article

References (47)

1. 1 Lawrence, T, Natali, G, Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Imanol 11 (2011), 750–761.
2. 2 Novoselov, VV, Sazonova, MA, Ivanova, EA, Orekhov, AN, Study of the activated macrophage transcriptome. Exp Mol Pathol 99 (2015), 575–580.
3. 3 El Kasmi, KC, Stenmark, KR, Contribution of metabolic reprogramming to macrophage plasticity and function. Semin Immunol 27 (2015), 267–275.
4. 4 Juhas, U, Ryba-Stanisławowska, M, Szargiej, P, Myśliwska, J, Different pathways of macrophage activation and polarization. Postepy Hig Med Dosw (Online) 69 (2015), 496–502.
5. 5 Banerjee, S, Xie, N, Cui, H, Tan, Z, Yang, S, Icyuz, M, et al. MicroRNA let-7c regulates macrophage polarization. J Immunol 190 (2013), 6542–6549.
6. 6 Boscá, L, González-Ramos, S, Prieto, P, Fernández-Velasco, M, Mojena, M, Martín-Sanz, P, et al. Metabolic signatures linked to macrophage polarization: from glucose metabolism to oxidative phosphorylation. Biochem Soc Trans 43 (2015), 740–744.
7. 7 Ma, X, Wu, D, Zhou, S, Wan, F, Liu, H, Xu, X, et al. The pancreatic cancer secreted REG4 promotes macrophage polarization to M2 through EGFR/AKT/CREB pathway. Oncol Rep 35 (2016), 189–196.
8. 8 Laoui, D, Van Overmeire, E, De Baetselier, P, Van Ginderachter, JA, Raes, G, Functional relationship between tumor-associated macrophages and macrophage colony-stimulating factor as contributors to cancer progression. Front Immunol, 5, 2014, 489.
9. 9 Chanmee, T, Ontong, P, Konno, K, Itano, N, Tumor-associated macrophages as major players in the tumor microenvironment. Cancers (Basel) 6 (2014), 1670–1690.
10. 10 Cook, J, Hagemann, T, Tumour-associated macrophages and cancer. Curr Opin Pharmacol 13 (2013), 595–601.
11. 11 Cardoso, AP, Pinto, ML, Pinto, AT, Oliveira, MI, Pinto, MT, Gonçalves, R, et al. Macrophages stimulate gastric and colorectal cancer invasion through EGFR Y(1086), c-Src, Erk1/2 and Akt phosphorylation and smallGTPase activity. Oncogene 33 (2014), 2123–2133.
12. 12 Pickert, G, Lim, HY, Weigert, A, Häussler, A, Myrczek, T, Waldner, M, et al. Inhibition of GTP cyclohydrolase attenuates tumor growth by reducing angiogenesis and M2-like polarization of tumor associated macrophages. Int J Cancer 132 (2013), 591–604.
13. 13 Rolny, C, Mazzone, M, Tugues, S, Laoui, D, Johansson, I, Coulon, C, et al. HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 19 (2011), 31–44.
14. 14 Liu, G, Abraham, E, MicroRNAs in immune response and macrophage polarization. Arterioscler Thromb Vasc Biol 33 (2013), 170–177.
15. 15 Ma, S, Liu, M, Xu, Z, Li, Y, Guo, H, Ge, Y, et al. A double feedback loop mediated by microRNA-23a/27a/24-2 regulates M1 versus M2 macrophage polarization and thus regulates cancer progression. Oncotarget 7:12 (2015), 13502–13519.
16. 16 Lin, L, Lin, H, Wang, L, Wang, B, Hao, X, Shi, Y, miR-130a regulates macrophage polarization and is associated with non-small cell lung cancer. Oncol Rep 34 (2015), 3088–3096.
17. 17 Li, X, Tian, F, Wang, F, Rheumatoid arthritis-associated microRNA-155 targets SOCS1 and upregulates TNF-α and IL-1β in PBMCs. Int J Mol Sci 14 (2013), 23910–23921.
18. 18 Arranz, A, Doxaki, C, Vergadi, E, de la Torre, Y M, Vaporidi, K, Lagoudaki, ED, et al. Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization. Proc Natl Acad Sci USA 109 (2012), 9517–9522.
19. 19 He, M, Xu, Z, Ding, T, Kuang, DM, Zheng, L, MicroRNA-155 regulates inflammatory cytokine production in tumor-associated macrophages via targeting C/EBPbeta. Cell Mol Immunol 6 (2009), 343–352.
20. 20 Martinez-Nunez, RT, Louafi, F, Sanchez-Elsner, T, The interleukin 13 (IL-13) pathway in human macrophages is modulated by microRNA-155 via direct targeting of interleukin 13 receptor alpha1 (IL13Ralpha1). J Biol Chem 286 (2011), 1786–1794.
21. 21 Xie, W, Li, M, Xu, N, Lv, Q, Huang, N, He, J, et al. MiR-181a regulates inflammation responses in monocytes and macrophages. PLoS One, 8, 2013, e58639.
22. 22 Zhang, Y, Zhang, M, Zhong, M, Suo, Q, Lv, K, Expression profiles of miRNAs in polarized macrophages. Int J Mol Med 31 (2013), 797–802.
23. 23 Date, D, Das, R, Narla, G, Simon, DI, Jain, MK, Mahabeleshwar, GH, Kruppel-like transcription factor 6 regulates inflammatory macrophage polarization. J Biol Chem 289 (2014), 10318–10329.
24. 24 Guan, X, Gao, Y, Zhou, J, Wang, J, Zheng, F, Guo, F, et al. miR-223 Regulates adipogenic and osteogenic differentiation of mesenchymal stem cells through a C/EBPs/miR-223/FGFR2 regulatory feedback loop. Stem Cells 33 (2015), 1589–1600.
25. 25 Lee, B, Qiao, L, Lu, M, Yoo, HS, Cheung, W, Mak, R, et al. C/EBPα regulates macrophage activation and systemic metabolism. Am J Physiol Endocrinol Metab 306 (2014), E1144–E1154.
26. 26 Zhang, J, Cao, J, Ma, S, Dong, R, Meng, W, Ying, M, et al. Tumor hypoxia enhances non-small cell lung cancer metastasis by selectively promoting macrophage M2 polarization through the activation of ERK signaling. Oncotarget 5 (2014), 9664–9677.
27. 27 Jia, X, Yu, F, Wang, J, Iwanowycz, S, Saaoud, F, Wang, Y, et al. Emodin suppresses pulmonary metastasis of breast cancer accompanied with decreased macrophage recruitment and M2 polarization in the lungs. Breast Cancer Res Treat 148 (2014), 291–302.
28. 28 Yang, J, Zhang, Z, Chen, C, Liu, Y, Si, Q, Chuang, TH, et al. MicroRNA-19a-3p inhibits breast cancer progression and metastasis by inducing macrophage polarization through downregulated expression of Fra-1 proto-oncogene. Oncogene 33 (2014), 3014–3023.
29. 29 Zhang, Y, Zhang, M, Zhong, M, Suo, Q, Lv, K, Expression profiles of miRNAs in polarized macrophages. Int J Mol Med 31 (2013), 797–802.
30. 30 Banerjee, S, Cui, H, Xie, N, Tan, Z, Yang, S, Icyuz, M, et al. miR-125a-5p regulates differential activation of macrophages and inflammation. J Biol Chem 288 (2013), 35428–35436.
31. 31 Vergadi, E, Vaporidi, K, Theodorakis, EE, Doxaki, C, Lagoudaki, E, Ieronymaki, E, et al. Akt2 deficiency protects from acute lung injury via alternative macrophage activation and miR-146a induction in mice. J Immunol 192 (2014), 394–406.
32. 32 Li, H, Chen, X, Guan, L, Qi, Q, Shu, G, Jiang, Q, et al. MiRNA-181a regulates adipogenesis by targeting tumor necrosis factor-α (TNF-α) in the porcine model. PLoS One, 8, 2013, e71568.
33. 33 Hulsmans, M, Sinnaeve, P, Van der Schueren, B, Mathieu, C, Janssens, S, Holvoet, P, Decreased miR-181a expression in monocytes of obese patients is associated with the occurrence of metabolic syndrome and coronary artery disease. J Clin Endocrinol Metab 97 (2012), E1213–E1218.
34. 34 Ozato, K, Tsujimura, H, Tamura, T, Toll-like receptor signaling and regulation of cytokine gene expression in the immune system. Biotechniques, Suppl, 2002, 66 68, 70, 72 passim.
35. 35 Friedman, AD, C/EBPalpha induces PU.1 and interacts with AP-1 and NF-kappaB to regulate myeloid development. Blood Cells Mol Dis 39 (2007), 340–343.
36. 36 Bouhlel, MA, Derudas, B, Rigamonti, E, Dièvart, R, Brozek, J, Haulon, S, et al. PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab 6 (2007), 137–143.
37. 37 Karuppagounder, V, Arumugam, S, Thandavarayan, RA, Pitchaimani, V, Sreedhar, R, Afrin, R, et al. Tannic acid modulates NFκB signaling pathway and skin inflammation in NC/Nga mice through PPARγ expression. Cytokine 76 (2015), 206–213.
38. 38 Birchmeier, W, Birchmeier, C, Epithelial-mesenchymal transitions in development and tumor progression. EXS 74 (1995), 1–15.
39. 39 Deryugina, EI, Quigley, JP, Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 25 (2006), 9–34.
40. 40 Liotta, LA, Tryggvason, K, Garbisa, S, Hart, I, Foltz, CM, Shafie, S, Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 284 (1980), 67–68.
41. 41 Zhang, J, Yan, Y, Yang, Y, Wang, L, Li, M, Wang, J, et al. High infiltration of tumor-associated macrophages influences poor prognosis in human gastric cancer patients, associates with the phenomenon of EMT. Medicine (Baltimore), 95, 2016, e2636.
42. 42 Li, W, Chen, C, Saud, SM, Geng, L, Zhang, G, Liu, R, et al. Fei-Liu-Ping ointment inhibits lung cancer growth and invasion by suppressing tumor inflammatory microenvironment. BMC Complement Altern Med, 14, 2014, 153.
43. 43 Wang, R, Zhang, J, Chen, S, Lu, M, Luo, X, Yao, S, et al. Tumor-associated macrophages provide a suitable microenvironment for non-small lung cancer invasion and progression. Lung Cancer 74 (2011), 188–196.
44. 44 Parikh, A, Lee, C, Joseph, P, Marchini, S, Baccarini, A, Kolev, V, et al. microRNA-181a has a critical role in ovarian cancer progression through the regulation of the epithelial-mesenchymal transition. Nat Commun, 5, 2014, 2977.
45. 45 Niu, J, Xue, A, Chi, Y, Xue, J, Wang, W, Zhao, Z, et al. Induction of miRNA-181a by genotoxic treatments promotes chemotherapeutic resistance and metastasis in breast cancer. Oncogene 35 (2016), 1302–1313.
46. 46 Ji, D, Chen, Z, Li, M, Zhan, T, Yao, Y, Zhang, Z, et al. MicroRNA-181a promotes tumor growth and liver metastasis in colorectal cancer by targeting the tumor suppressor WIF-1. Mol Cancer, 13, 2014, 86.
47. 47 Taylor, MA, Sossey-Alaoui, K, Thompson, CL, Danielpour, D, Schiemann, WP, TGF-β upregulates miR-181a expression to promote breast cancer metastasis. J Clin Invest 123 (2013), 150–163.