MicroRNA-223 delivered by platelet-derived microvesicles promotes lung cancer cell invasion via targeting tumor suppressor EPB41L3
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- 作者：Hongwei Liang (1)
Xin Yan (2)
Yi Pan (1)
Yongsheng Wang (3)
Nan Wang (1)
Limin Li (1)
Yuan Liu (4)
Xi Chen (1)
Chen-Yu Zhang (1)
Hongwei Gu (1)
Ke Zen (1) (4)
1. From State Key Laboratory of Pharmaceutical Biotechnology ; Nanjing University School of Life Sciences ; Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology ; Nanjing ; Jiangsu ; 210093 ; China
2. The Comprehensive Cancer Center of Drum Tower Hospital affiliated to Medical School of Nanjing University & Clinical Cancer Institute of Nanjing University ; Nanjing ; Jiangsu ; 210008 ; China
3. Department of Respiratory Medicine ; Nanjing Drum Tower Hospital Affiliated to Medical School of Nanjing University ; 321 Zhongshan Road ; Nanjing ; 210008 ; Jiangsu Province ; China
4. Department of Biology ; Georgia State University ; Atlanta ; GA ; 30303 ; USA - 关键词：Platelet ; Microvesicles ; MicroR ; 223 ; Lung cancer
- 刊名：Molecular Cancer
- 出版年：2015
- 出版时间：December 2015
- 年：2015
- 卷：14
- 期：1
- 全文大小：2,940 KB
- 参考文献：1. Siegel, R, Naishadham, D, Jemal, A (2013) Cancer statistics, 2013. CA Cancer J Clin 63: pp. 11-30 CrossRef
2. Inamura, K, Ishikawa, Y (2010) Lung cancer progression and metastasis from the prognostic point of view. Clin Exp Metastasis 27: pp. 389-97 CrossRef
3. Kunita, A, Kashima, TG, Morishita, Y, Fukayama, M, Kato, Y, Tsuruo, T (2007) The platelet aggregation-inducing factor aggrus/podoplanin promotes pulmonary metastasis. Am J Pathol 170: pp. 1337-47 CrossRef
4. Gonzalez Barcala, FJ, Garcia Prim, JM, Moldes Rodriguez, M, Alvarez Fernandez, J, Rey Rey, MJ, Pose Reino, A (2010) Platelet count: association with prognosis in lung cancer. Med Oncol 27: pp. 357-62 CrossRef
5. Escola, JM, Kleijmeer, MJ, Stoorvogel, W, Griffith, JM, Yoshie, O, Geuze, HJ (1998) Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem 273: pp. 20121-7 CrossRef
6. Miyamoto, S, Kowalska, MA, Marcinkiewicz, C, Marcinkiewicz, MM, Mosser, D, Edmunds, LH (1998) Interaction of leukocytes with platelet microparticles derived from outdated platelet concentrates. Thromb Haemost 80: pp. 982-8
7. Thery, C, Zitvogel, L, Amigorena, S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2: pp. 569-79
8. Janiszewski, M, Do Carmo, AO, Pedro, MA, Silva, E, Knobel, E, Laurindo, FR (2004) Platelet-derived exosomes of septic individuals possess proapoptotic NAD(P)H oxidase activity: A novel vascular redox pathway. Crit Care Med 32: pp. 818-25 CrossRef
9. Janowska-Wieczorek, A, Wysoczynski, M, Kijowski, J, Marquez-Curtis, L, Machalinski, B, Ratajczak, J (2005) Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer 113: pp. 752-60 CrossRef
10. Hughes, M, Hayward, CP, Warkentin, TE, Horsewood, P, Chorneyko, KA, Kelton, JG (2000) Morphological analysis of microparticle generation in heparin-induced thrombocytopenia. Blood 96: pp. 188-94
11. Mallat, Z, Benamer, H, Hugel, B, Benessiano, J, Steg, PG, Freyssinet, JM (2000) Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation 101: pp. 841-3 CrossRef
12. Galli, M, Grassi, A, Barbui, T (1996) Platelet-derived microvesicles in thrombotic thrombocytopenic purpura and hemolytic uremic syndrome. Thromb Haemost 75: pp. 427-31
13. Ando, M, Iwata, A, Ozeki, Y, Tsuchiya, K, Akiba, T, Nihei, H (2002) Circulating platelet-derived microparticles with procoagulant activity may be a potential cause of thrombosis in uremic patients. Kidney Int 62: pp. 1757-63 CrossRef
14. Varon, D, Shai, E (2009) Role of platelet-derived microparticles in angiogenesis and tumor progression. Discov Med 8: pp. 237-41
15. Boilard, E, Nigrovic, PA, Larabee, K, Watts, GF, Coblyn, JS, Weinblatt, ME (2010) Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 327: pp. 580-3 CrossRef
16. Setzer, F, Oberle, V, Blass, M, Moller, E, Russwurm, S, Deigner, HP (2006) Platelet-derived microvesicles induce differential gene expression in monocytic cells: a DNA microarray study. Platelets 17: pp. 571-6 CrossRef
17. Majka, M, Kijowski, J, Lesko, E, Gozdizk, J, Zupanska, B, Ratajczak, MZ (2007) Evidence that platelet-derived microvesicles may transfer platelet-specific immunoreactive antigens to the surface of endothelial cells and CD34+ hematopoietic stem/progenitor cells鈥搃mplication for the pathogenesis of immune thrombocytopenias. Folia Histochem Cytobiol 45: pp. 27-32
18. Tan, KT, Lip, GY (2005) The potential role of platelet microparticles in atherosclerosis. Thromb Haemost 94: pp. 488-92
19. Bartel, DP (2007) MicroRNAs: Genomics, biogenesis, mechanism, and function (Reprinted from Cell, vol 116, pg 281鈥?97, 2004). Cell 131: pp. 11-29
20. Chen, X, Ba, Y, Ma, L, Cai, X, Yin, Y, Wang, K (2008) Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 18: pp. 997-1006 CrossRef
21. Zhang, Y, Liu, D, Chen, X, Li, J, Li, L, Bian, Z (2010) Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 39: pp. 133-44 CrossRef
22. Li, L, Zhu, D, Huang, L, Zhang, J, Bian, Z, Chen, X (2012) Argonaute 2 complexes selectively protect the circulating microRNAs in cell-secreted microvesicles. PLoS One 7: pp. e46957 CrossRef
23. Chen, X, Liang, H, Zhang, J, Zen, K, Zhang, CY (2012) Secreted microRNAs: a new form of intercellular communication. Trends Cell Biol 22: pp. 125-32 CrossRef
24. Landry, P, Plante, I, Ouellet, DL, Perron, MP, Rousseau, G, Provost, P (2009) Existence of a microRNA pathway in anucleate platelets. Nat Struct Mol Biol 16: pp. 961-6 CrossRef
25. Nagalla, S, Shaw, C, Kong, X, Kondkar, AA, Edelstein, LC, Ma, L (2011) Platelet microRNA-mRNA coexpression profiles correlate with platelet reactivity. Blood 117: pp. 5189-97 CrossRef
26. Kannan, M, Mohan, KV, Kulkarni, S, Atreya, C (2009) Membrane array-based differential profiling of platelets during storage for 52 miRNAs associated with apoptosis. Transfusion 49: pp. 1443-50 CrossRef
27. Kondkar, AA, Bray, MS, Leal, SM, Nagalla, S, Liu, DJ, Jin, Y (2010) VAMP8/endobrevin is overexpressed in hyperreactive human platelets: suggested role for platelet microRNA. J Thromb Haemost 8: pp. 369-78 CrossRef
28. Diehl, P, Fricke, A, Sander, L, Stamm, J, Bassler, N, Htun, N (2012) Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovasc Res 93: pp. 633-44 CrossRef
29. Laffont, B, Corduan, A, Ple, H, Duchez, AC, Cloutier, N, Boilard, E (2013) Activated platelets can deliver mRNA regulatory Ago2 microRNA complexes to endothelial cells via microparticles. Blood 122: pp. 253-61 CrossRef
30. Gidlof, O, Brug, M, Ohman, J, Gilje, P, Olde, B, Wahlestedt, C (2013) Platelets activated during myocardial infarction release functional miRNA, which can be taken up by endothelial cells and regulate ICAM1 expression. Blood 121: pp. 3908-17 CrossRef
31. Pan, Y, Liang, H, Liu, H, Li, D, Chen, X, Li, L (2014) Platelet-secreted microRNA-223 promotes endothelial cell apoptosis induced by advanced glycation end products via targeting the insulin-like growth factor 1 receptor. J Immunol 192: pp. 437-46 CrossRef
32. Laffont, B, Corduan, A, Ple, H, Duchez, AC, Cloutier, N, Boilard, E (2013) Activated platelets can deliver mRNA regulatory Ago2.microRNA complexes to endothelial cells via microparticles. Blood 122: pp. 253-61 CrossRef
33. Yang, M, Chen, J, Su, F, Yu, B, Lin, L, Liu, Y (2011) Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer 10: pp. 117 CrossRef
34. Li, X, Zhang, Y, Zhang, H, Liu, X, Gong, T, Li, M (2011) miRNA-223 promotes gastric cancer invasion and metastasis by targeting tumor suppressor EPB41L3. Mol Cancer Res 9: pp. 824-33 CrossRef
35. Tran, YK, Bogler, O, Gorse, KM, Wieland, I, Green, MR, Newsham, IF (1999) A novel member of the NF2/ERM/4.1 superfamily with growth suppressing properties in lung cancer. Cancer Res 59: pp. 35-43
36. Laios, A, O鈥橳oole, S, Flavin, R, Martin, C, Kelly, L, Ring, M (2008) Potential role of miR-9 and miR-223 in recurrent ovarian cancer. Mol Cancer 7: pp. 35 CrossRef
37. Hitzler, W, Vamvakas, EC (2011) Platelet microRNA profiles and the effect of pathogen reduction on platelet function. Clin Lab 57: pp. 451-4
38. Alexandru, N, Popov, D, Georgescu, A (2012) Platelet dysfunction in vascular pathologies and how can it be treated. Thromb Res 129: pp. 116-26 CrossRef
39. Combes, V, Simon, AC, Grau, GE, Arnoux, D, Camoin, L, Sabatier, F (1999) In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J Clin Invest 104: pp. 93-102 CrossRef
40. Ismail, A, AlDorry, A, Shaker, M, Elwekeel, R, Mokbel, K, Zakaria, D (2011) Simultaneous injection of autologous mononuclear cells with TACE in HCC patients; preliminary study. J Gastrointest Cancer 42: pp. 11-9 CrossRef
41. Tantawy, AA, Adly, AA, Ismail, EA, Habeeb, NM (2013) Flow cytometric assessment of circulating platelet and erythrocytes microparticles in young thalassemia major patients: relation to pulmonary hypertension and aortic wall stiffness. Eur J Haematol 90: pp. 508-18 CrossRef
42. Janowska-Wieczorek, A, Marquez-Curtis, LA, Wysoczynski, M, Ratajczak, MZ (2006) Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion 46: pp. 1199-209 CrossRef
43. Bastida, E, Ordinas, A (1988) Platelet contribution to the formation of metastatic foci: the role of cancer cell-induced platelet activation. Haemostasis 18: pp. 29-36
44. Gimm, JA, An, X, Nunomura, W, Mohandas, N (2002) Functional characterization of spectrin-actin-binding domains in 4.1 family of proteins. Biochemistry 41: pp. 7275-82 CrossRef
45. Gutmann, DH, Hirbe, AC, Huang, ZY, Haipek, CA (2001) The protein 4.1 tumor suppressor, DAL-1, impairs cell motility, but regulates proliferation in a cell-type-specific fashion. Neurobiol Dis 8: pp. 266-78 CrossRef
46. Charboneau, AL, Singh, V, Yu, T, Newsham, IF (2002) Suppression of growth and increased cellular attachment after expression of DAL-1 in MCF-7 breast cancer cells. Int J Cancer 100: pp. 181-8 CrossRef
47. Cavanna, T, Pokorna, E, Vesely, P, Gray, C, Zicha, D (2007) Evidence for protein 4.1B acting as a metastasis suppressor. J Cell Sci 120: pp. 606-16 CrossRef
48. Surace, EI, Lusis, E, Murakami, Y, Scheithauer, BW, Perry, A, Gutmann, DH (2004) Loss of tumor suppressor in lung cancer-1 (TSLC1) expression in meningioma correlates with increased malignancy grade and reduced patient survival. J Neuropathol Exp Neurol 63: pp. 1015-27
49. Shabalina, SA, Spiridonov, NA (2004) The mammalian transcriptome and the function of non-coding DNA sequences. Genome Biol 5: pp. 105 CrossRef
50. Hunter, MP, Ismail, N, Zhang, X, Aguda, BD, Lee, EJ, Yu, L (2008) Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 3: pp. e3694 CrossRef
51. Skog, J, Wurdinger, T, Rijn, S, Meijer, DH, Gainche, L, Sena-Esteves, M (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10: pp. 1470-6 CrossRef
52. Valadi, H, Ekstrom, K, Bossios, A, Sjostrand, M, Lee, JJ, Lotvall, JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: pp. 654-9 CrossRef
53. Johnnidis, JB, Harris, MH, Wheeler, RT, Stehling-Sun, S, Lam, MH, Kirak, O (2008) Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 451: pp. 1125-9 CrossRef
54. Sun, W, Shen, W, Yang, S, Hu, F, Li, H, Zhu, TH (2010) miR-223 and miR-142 attenuate hematopoietic cell proliferation, and miR-223 positively regulates miR-142 through LMO2 isoforms and CEBP-beta. Cell Res 20: pp. 1158-69 CrossRef
55. Chen, X, Gao, C, Li, H, Huang, L, Sun, Q, Dong, Y (2010) Identification and characterization of microRNAs in raw milk during different periods of lactation, commercial fluid, and powdered milk products. Cell Res 20: pp. 1128-37 CrossRef
56. Harraz, MM, Eacker, SM, Wang, X, Dawson, TM, Dawson, VL (2012) MicroRNA-223 is neuroprotective by targeting glutamate receptors. Proc Natl Acad Sci U S A 109: pp. 18962-7 CrossRef
57. Jia, CY, Li, HH, Zhu, XC, Dong, YW, Fu, D, Zhao, QL (2011) MiR-223 suppresses cell proliferation by targeting IGF-1R. PLoS One 6: pp. e27008 CrossRef
58. Palumbo, JS, Kombrinck, KW, Drew, AF, Grimes, TS, Kiser, JH, Degen, JL (2000) Fibrinogen is an important determinant of the metastatic potential of circulating tumor cells. Blood 96: pp. 3302-9
59. Fabbri, M, Paone, A, Calore, F, Galli, R, Gaudio, E, Santhanam, R (2012) MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci U S A 109: pp. E2110-6 CrossRef - 刊物主题：Cancer Research; Oncology;
- 出版者：BioMed Central
- ISSN：1476-4598
文摘
Background Patients with hematogenous metastatic lung cancer displayed significantly increased platelet count and aggregation compared to lung cancer patients without hematogenous metastasis. The mechanism underlying the correlation between the lung cancer hematogenous metastasis and platelet activation remains unknown. Results In the present study, we explored the role of microRNA-223 (miR-223) derived from platelets in modulating lung cancer cell invasion. Our results demonstrated that platelets from NSCLC patients contain higher level of miR-223 than that from healthy subjects. The concentration of miR-223 in the platelet-secreted microvesicles (P-MVs) from NSCLC patients was also increased compared to that from healthy subjects. Incubation of human lung cancer A549 cells with P-MVs resulted in rapid delivery of miR-223 into A549 cells, in which platelet miR-223 targeted EPB41L3 and thus promoted A549 cell invasion. The effect of P-MVs on reducing EPB41L3 in A549 cells but promoting tumor cell invasion could be largely abolished by depletion of miR-223 via transfection with miR-223 antagomir. The role of EPB41L3 in inhibiting A549 cell invasion was further validated by directly downregulating EPB41L3 via transfecting cells with EPB41L3 siRNA or miR-223 mimic. Conclusions Our study demonstrates for the first time that platelet-secreted miR-223 via P-MVs can promote lung cancer cell invasion via targeting tumor suppressor EPB41L3.