Loss of exosomal miR-320a from cancer-associated fibroblasts contributes to HCC proliferation and metastasis

Cancer Letters

Volumn 397, Issue , 2017, Pages 33-42

  Zhang, Zhuochao ^a   Li, Xiao ^a   Sun, Wei ^a   Yue, Shuqiang ^a   Yang, Jingyue ^a   Li, Junjie ^a   Ma, Ben ^a   Wang, Jianlin ^a   Yang, Xisheng ^a   Pu, Meng ^a   Ruan, Bai ^a   Zhao, Ge ^a   Huang, Qike ^a   Wang, Lin ^a   Tao, Kaishan ^a   Dou, Kefeng ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

CAFs; Exosomes; miR 320a; PBX3; Tumourigenesis

Indexed keywords

CYCLIN DEPENDENT KINASE 2; GELATINASE A; MICRORNA; MICRORNA 320A; UNCLASSIFIED DRUG; CDK2 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; MIRN320 MICRORNA, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE; ONCOPROTEIN; PROTO-ONCOGENE PROTEIN PBX3;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER ASSOCIATED FIBROBLAST; CANCER CELL; CANCER GROWTH; CELL COUNT; CELL CYCLE G1 PHASE; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; EXOSOME; GENE; GENE EXPRESSION; GENE TARGETING; GENE THERAPY; GENE TRANSFER; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL CARCINOMA; LUNG METASTASIS; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; PBX GENE; PROTEIN EXPRESSION; STROMA CELL; UPREGULATION; ANIMAL; CELL MOTION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; LIVER TUMOR; METABOLISM; NUDE MOUSE; PARACRINE SIGNALING; PATHOLOGY; SECONDARY; SIGNAL TRANSDUCTION; TIME FACTOR; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; CANCER-ASSOCIATED FIBROBLASTS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE 2; DOWN-REGULATION; EXOSOMES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; LIVER NEOPLASMS; MICE, NUDE; MICRORNAS; NEOPLASM INVASIVENESS; PARACRINE COMMUNICATION; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 85016971754     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2017.03.004     Document Type: Article

References (40)

1. [1] Forner, A., Llovet, J.M., Bruix, J., Hepatocellular carcinoma. Lancet 379 (2012), 1245–1255.
2. [2] Tlsty, T.D., Coussens, L.M., Tumor stroma and regulation of cancer development. Annu. Rev. Pathol. 1 (2006), 119–150.
3. [3] Dakhova, O., Ozen, M., Creighton, C.J., Li, R., Ayala, G., Rowley, D., et al. Global gene expression analysis of reactive stroma in prostate cancer. Clin. Cancer Res. 15 (2009), 3979–3989.
4. [4] Kuperwasser, C., Chavarria, T., Wu, M., Magrane, G., Gray, J.W., Carey, L., et al. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 4966–4971.
5. [5] Schor, S.L., Haggie, J.A., Durning, P., Howell, A., Smith, L., Sellwood, R.A., et al. Occurrence of a fetal fibroblast phenotype in familial breast cancer. Int. J. Cancer 37 (1986), 831–836.
6. [6] Orimo, A., Gupta, P.B., Sgroi, D.C., Arenzana-Seisdedos, F., Delaunay, T., Naeem, R., et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121 (2005), 335–348.
7. [7] Cocucci, E., Racchetti, G., Meldolesi, J., Shedding microvesicles: artefacts no more. Trends Cell Biol. 19 (2009), 43–51.
8. [8] Haga, H., Yan, I.K., Takahashi, K., Wood, J., Zubair, A., Patel, T., Tumour cell-derived extracellular vesicles interact with mesenchymal stem cells to modulate the microenvironment and enhance cholangiocarcinoma growth. J. Extracell. Vesicles, 4, 2015, 24900.
9. [9] Li, L., Li, C., Wang, S., Wang, Z., Jiang, J., Wang, W., et al. Exosomes derived from hypoxic oral squamous cell carcinoma cells deliver miR-21 to normoxic cells to elicit a prometastatic phenotype. Cancer Res. 76 (2016), 1770–1780.
10. [10] Piper, R.C., Katzmann, D.J., Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23 (2007), 519–547.
11. [11] Au Yeung, C.L., Co, N.N., Tsuruga, T., Yeung, T.L., Kwan, S.Y., Leung, C.S., et al. Exosomal transfer of stroma-derived miR21 confers paclitaxel resistance in ovarian cancer cells through targeting APAF1. Nat. Commun., 7, 2016, 11150.
12. [12] Aucher, A., Rudnicka, D., Davis, D.M., MicroRNAs transfer from human macrophages to hepato-carcinoma cells and inhibit proliferation. J. Immunol. 191 (2013), 6250–6260.
13. [13] Challagundla, K.B., Wise, P.M., Neviani, P., Chava, H., Murtadha, M., Xu, T., et al. Exosome-mediated transfer of microRNAs within the tumor microenvironment and neuroblastoma resistance to chemotherapy. J. Natl. Cancer Inst., 107, 2015.
14. [14] Yang, M., Chen, J., Su, F., Yu, B., Su, F., Lin, L., et al. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol. Cancer, 10, 2011, 117.
15. [15] Bovy, N., Blomme, B., Freres, P., Dederen, S., Nivelles, O., Lion, M., et al. Endothelial exosomes contribute to the antitumor response during breast cancer neoadjuvant chemotherapy via microRNA transfer. Oncotarget 6 (2015), 10253–10266.
16. [16] Desrochers, L.M., Antonyak, M.A., Cerione, R.A., Extracellular vesicles: satellites of information transfer in cancer and stem cell biology. Dev. Cell 37 (2016), 301–309.
17. [17] Chou, J., Werb, Z., MicroRNAs play a big role in regulating ovarian cancer-associated fibroblasts and the tumor microenvironment. Cancer Discov. 2 (2012), 1078–1080.
18. [18] Zhao, L., Sun, Y., Hou, Y., Peng, Q., Wang, L., Luo, H., et al. MiRNA expression analysis of cancer-associated fibroblasts and normal fibroblasts in breast cancer. Int. J. Biochem. Cell Biol. 44 (2012), 2051–2059.
19. [19] Junttila, M.R., de Sauvage, F.J., Influence of tumour micro-environment heterogeneity on therapeutic response. Nature 501 (2013), 346–354.
20. [20] Luo, Z., Wang, Q., Lau, W.B., Lau, B., Xu, L., Zhao, L., et al. Tumor microenvironment: the culprit for ovarian cancer metastasis?,. Cancer Lett. 377 (2016), 174–182.
21. [21] Mueller, M.M., Fusenig, N.E., Friends or foes – bipolar effects of the tumour stroma in cancer. Nat. Rev. Cancer 4 (2004), 839–849.
22. [22] Hanahan, D., Coussens, L.M., Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 21 (2012), 309–322.
23. [23] Avgustinova, A., Iravani, M., Robertson, D., Fearns, A., Gao, Q., Klingbeil, P., et al. Tumour cell-derived Wnt7a recruits and activates fibroblasts to promote tumour aggressiveness. Nat. Commun., 7, 2016, 10305.
24. [24] Albrengues, J., Bourget, I., Pons, C., Butet, V., Hofman, P., Tartare-Deckert, S., et al. LIF mediates proinvasive activation of stromal fibroblasts in cancer. Cell Rep. 7 (2014), 1664–1678.
25. [25] Sternlicht, M.D., Lochter, A., Sympson, C.J., Huey, B., Rougier, J.P., Gray, J.W., et al. The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis,. Cell 98 (1999), 137–146.
26. [26] Boire, A., Covic, L., Agarwal, A., Jacques, S., Sherifi, S., Kuliopulos, A., PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell 120 (2005), 303–313.
27. [27] Silzle, T., Randolph, G.J., Kreutz, M., Kunz-Schughart, L.A., The fibroblast: sentinel cell and local immune modulator in tumor tissue,. Int. J. Cancer 108 (2004), 173–180.
28. [28] Tkach, M., Thery, C., Communication by extracellular vesicles: where we are and where we need to go. Cell 164 (2016), 1226–1232.
29. [29] Vader, P., Breakefield, X.O., Wood, M.J., Extracellular vesicles: emerging targets for cancer therapy. Trends Mol. Med. 20 (2014), 385–393.
30. [30] Ohno, S., Ishikawa, A., Kuroda, M., Roles of exosomes and microvesicles in disease pathogenesis. Adv. Drug Deliv. Rev. 65 (2013), 398–401.
31. [31] Tang, M.K., Wong, A.S., Exosomes: emerging biomarkers and targets for ovarian cancer. Cancer Lett. 367 (2015), 26–33.
32. [32] Lemoinne, S., Thabut, D., Housset, C., Moreau, R., Valla, D., Boulanger, C.M., et al. The emerging roles of microvesicles in liver diseases,. Nat. Rev. Gastroenterol. Hepatol. 11 (2014), 350–361.
33. [33] Zhao, H., Dong, T., Zhou, H., Wang, L., Huang, A., Feng, B., et al. miR-320a suppresses colorectal cancer progression by targeting Rac1. Carcinogenesis 35 (2014), 886–895.
34. [34] Wang, Y., Zeng, J., Pan, J., Geng, X., Li, L., Wu, J., et al. MiR-320a inhibits gastric carcinoma by targeting activity in the FoxM1-P27KIP1 axis. Oncotarget 7 (2016), 29275–29286.
35. [35] Zhang, G., Jiang, G., Wang, C., Zhong, K., Zhang, J., Xue, Q., et al. Decreased expression of microRNA-320a promotes proliferation and invasion of non-small cell lung cancer cells by increasing VDAC1 expression. Oncotarget 7 (2016), 49470–49480.
36. [36] Agaram, N.P., Chen, H.W., Zhang, L., Sung, Y.S., Panicek, D., Healey, J.H., et al. EWSR1-PBX3: a novel gene fusion in myoepithelial tumors. Genes Chromosom. Cancer 54 (2015), 63–71.
37. [37] Ramberg, H., Grytli, H.H., Nygard, S., Wang, W., Ogren, O., Zhao, S., et al. PBX3 is a putative biomarker of aggressive prostate cancer. Int. J. Cancer 139 (2016), 1810–1820.
38. [38] Han, S.Y., Han, H.B., Tian, X.Y., Sun, H., Xue, D., Zhao, C., et al. MicroRNA-33a-3p suppresses cell migration and invasion by directly targeting PBX3 in human hepatocellular carcinoma. Oncotarget 7 (2016), 42461–42473.
39. [39] Yuan, S.X., Wang, J., Yang, F., Tao, Q.F., Zhang, J., Wang, L.L., et al. Long noncoding RNA DANCR increases stemness features of hepatocellular carcinoma by derepression of CTNNB1. Hepatology 63 (2016), 499–511.
40. [40] Sun, L., Liu, B., Lin, Z., Yao, Y., Chen, Y., Li, Y., et al. MiR-320a acts as a prognostic factor and Inhibits metastasis of salivary adenoid cystic carcinoma by targeting ITGB3. Mol. Cancer, 14, 2015, 96.