MicroRNA-19a-3p inhibits breast cancer progression and metastasis by inducing macrophage polarization through downregulated expression of Fra-1 proto-oncogene

Oncogene

Volumn 33, Issue 23, 2014, Pages 3014-3023

  Yang, J ^a,b   Zhang, Z ^b   Chen, C ^a   Liu, Y ^a   Si, Q ^a   Chuang, T H ^c   Li, N ^b   Gomez Cabrero, A ^d   Reisfeld, R A ^d   Xiang, R ^b   Luo, Y ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b NANKAI UNIVERSITY   (China)

^c NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Fra 1; miR 19a 3p; tumor microenvironment; tumor Associated macrophages

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 6; MICRORNA; MICRORNA 19A 3P; MONOCYTE CHEMOTACTIC PROTEIN 1; STAT3 PROTEIN; TRANSCRIPTION FACTOR FRA 1; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN A;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER INHIBITION; CELL CULTURE; CELL MIGRATION; COCULTURE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FLOW CYTOMETRY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTO ONCOGENE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAT3 GENE; TRANSCRIPTION FACTOR FRA 1 GENE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL; TUMOR INVASION; UPREGULATION; VASCULOTROPIN GENE;

VERTEBRATA;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MACROPHAGES; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-FOS; SIGNAL TRANSDUCTION; TRANSFECTION; TUMOR MICROENVIRONMENT; U937 CELLS;

EID: 84902129290     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.258     Document Type: Article

References (39)

1. Eulalio A, Schulte L, Vogel J. The mammalian microRNA response to bacterial infections. RNA Biol 2012; 9: 742-750.
2. Kincaid RP, Burke JM, Sullivan CS. RNA virus microRNA that mimics a B-cell oncomiR. Proc Natl Acad Sci USA 2012; 109: 3077-3082.
3. Thomas RM, Fleming JB. MicroRNA dissects out dangerous pancreatic cysts from all the rest. Clin Cancer Res 2012; 18: 4482-4484.
4. De Vito C, Riggi N, Cornaz S, Suva ML, Baumer K, Provero P et al. A TARBP2-dependent miRNA expression profile underlies cancer stem cell properties and provides candidate therapeutic reagents in Ewing sarcoma. Cancer Cell 2012; 21: 807-821.
5. Garzon R, Marcucci G. Potential of microRNAs for cancer diagnostics, prognostication and therapy. Curr Opin Oncol 2012; 24: 655-659.
6. Hermeking H. MicroRNAs in the p53 network: micromanagement of tumour suppression. Nat Rev Cancer 2012; 12: 613-626.
7. Giordano S, Columbano A. MicroRNAs: new tools for diagnosis, prognosis and therapy in HCC? Hepatology 2013; 57: 840-847.
8. Song JH, Meltzer SJ. MicroRNAs in pathogenesis, diagnosis, and treatment of gastroesophageal cancers. Gastroenterology 2012; 143: 35-47e2.
9. Valleron W, Ysebaert L, Berquet L, Fataccioli V, Quelen C, Martin A et al. Small nucleolar RNA expression profiling identifies potential prognostic markers in peripheral T-cell lymphoma. Blood 2012; 120: 3997-4005.
10. Volinia S, Galasso M, Sana ME, Wise TF, Palatini J, Huebner K et al. Breast cancer signatures for invasiveness and prognosis defined by deep sequencing of microRNA. Proc Natl Acad Sci USA 2012; 109: 3024-3029.
11. 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 2011; 19: 31-44.
12. Murdoch C, Lewis CE. Macrophage migration and gene expression in response to tumor hypoxia. Int J Cancer 2005; 117: 701-708. (Pubitemid 41598819)
13. Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res 2006; 66: 605-612. (Pubitemid 43165918)
14. Sica A, Larghi P, Mancino A, Rubino L, Porta C, Totaro MG et al. Macrophage polarization in tumour progression. Semin Cancer Biol 2008; 18: 349-355.
15. Tai SK, Chang HC, Lan KL, Lee CT, Yang CY, Chen NJ et al. Decoy receptor 3 enhances tumor progression via induction of tumor-Associated macrophages. J Immunol 2012; 188: 2464-2471.
16. Kustikova O, Kramerov D, Grigorian M, Berezin V, Bock E, Lukanidin E et al. Fra-1 induces morphological transformation and increases in vitro invasiveness and motility of epithelioid adenocarcinoma cells. Mol Cell Biol 1998; 18: 7095-7105. (Pubitemid 28533029)
17. Kesari S, Bota DA. Fos-related antigen-1 (Fra-1) is a regulator of glioma cell malignant phenotype. Cancer Biol Ther 2011; 11: 307-310.
18. Usui A, Hoshino I, Akutsu Y, Sakata H, Nishimori T, Murakami K et al. The molecular role of Fra-1 and its prognostic significance in human esophageal squamous cell carcinoma. Cancer 2012; 118: 3387-3396.
19. Luo YP, Zhou H, Krueger J, Kaplan C, Liao D, Markowitz D et al. The role of protooncogene Fra-1 in remodeling the tumor microenvironment in support of breast tumor cell invasion and progression. Oncogene 2010; 29: 662-673.
20. Wang Q, Ni H, Lan L, Wei X, Xiang R, Wang Y. Fra-1 protooncogene regulates IL-6 expression in macrophages and promotes the generation of M2d macrophages. Cell Res 2010; 20: 701-712.
21. Wu J, Wu G, Lv L, Ren YF, Zhang XJ, Xue YF et al. MicroRNA-34a inhibits migration and invasion of colon cancer cells via targeting to Fra-1. Carcinogenesis 2012; 33: 519-528.
22. Yang S, Li Y, Gao J, Zhang T, Li S, Luo A et al. MicroRNA-34 suppresses breast cancer invasion and metastasis by directly targeting Fra-1. Oncogene 2013; 32: 4294-4303.
23. Bluml S, Bonelli M, Niederreiter B, Puchner A, Mayr G, Hayer S et al. Essential role of microRNA-155 in the pathogenesis of autoimmune arthritis in mice. Arthritis Rheum 2011; 63: 1281-1288.
24. Mizoguchi F, Izu Y, Hayata T, Hemmi H, Nakashima K, Nakamura T et al. Osteoclast- specific Dicer gene deficiency suppresses osteoclastic bone resorption. J Cell Biochem 2010; 109: 866-875.
25. Sugatani T, Vacher J, Hruska KA. A microRNA expression signature of osteoclastogenesis. Blood 2011; 117: 3648-3657.
26. Setoyama T, Ling H, Natsugoe S, Calin GA. Non-coding RNAs for medical practice in oncology. Keio J Med 2011; 60: 106-113.
27. Mikhaylova O, Stratton Y, Hall D, Kellner E, Ehmer B, Drew AF et al. VHL-regulated MiR-204 suppresses tumor growth through inhibition of LC3B-mediated autophagy in renal clear cell carcinoma. Cancer Cell 2012; 21: 532-546.
28. Singh PK, Brand RE, Mehla K. MicroRNAs in pancreatic cancer metabolism. Nat Rev Gastroenterol Hepatol 2012; 9: 334-344.
29. Yang P, Li QJ, Feng Y, Zhang Y, Markowitz GJ, Ning S et al. TGF-beta-miR-34a- CCL22 signaling-induced treg cell recruitment promotes venous metastases of HBV-positive hepatocellular carcinoma. Cancer Cell 2012; 22: 291-303.
30. Liu D, Song L, Wei J, Courtney AN, Gao X, Marinova E et al. IL-15 protects NKT cells from inhibition by tumor-Associated macrophages and enhances antimetastatic activity. J Clin Invest 2012; 122: 2221-2233.
31. Ruffell B, Affara NI, Coussens LM. Differential macrophage programming in the tumor microenvironment. Trends Immunol 2012; 33: 119-126.
32. Yang W, Lu Y, Xu Y, Xu L, Zheng W, Wu Y et al. Estrogen represses hepatocellular carcinoma (HCC) growth via inhibiting alternative activation of tumor-Associated macrophages (TAMs). J Biol Chem 2012; 7: 40140-40149.
33. Yang M, Zheng J, Miao Y, Wang Y, Cui W, Guo J et al. Serum-glucocorticoid regulated kinase 1 regulates alternatively activated macrophage polarization contributing to angiotensin II-induced inflammation and cardiac fibrosis. Arterioscler Thromb Vasc Biol 2012; 32: 1675-1686.
34. Diehl S, Rincon M. The two faces of IL-6 on Th1/Th2 differentiation. Mol Immunol 2002; 39: 531-536. (Pubitemid 35341492)
35. Babykutty S, Suboj P, Srinivas P, Nair AS, Chandramohan K, Gopala S. Insidious role of nitric oxide in migration/invasion of colon cancer cells by upregulating MMP-2/9 via activation of cGMP-PKG-ERK signaling pathways. Clin Exp Metastasis 2012; 29: 471-492.
36. Chandrasekar B, Mummidi S, Mahimainathan L, Patel DN, Bailey SR, Imam SZ et al. Interleukin-18-induced human coronary artery smooth muscle cell migration is dependent on NF-kappaB- and AP-1-mediated matrix metalloproteinase-9 expression and is inhibited by atorvastatin. J Biol Chem 2006; 281: 15099-15109. (Pubitemid 43855099)
37. Milde-Langosch K, Roder H, Andritzky B, Aslan B, Hemminger G, Brinkmann A et al. The role of the AP-1 transcription factors c-Fos, FosB, Fra-1 and Fra-2 in the invasion process of mammary carcinomas. Breast Cancer Res Treat 2004; 86: 139-152. (Pubitemid 38988017)
38. Iorio MV, Croce CM. MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med 2012; 4: 143-159.
39. Cubillos-Ruiz JR, Sempere LF, Conejo-Garcia JR. Good things come in small packages: Therapeutic anti-Tumor immunity induced by microRNA nanoparticles. Oncoimmunology 2012; 1: 968-970.