Dicer knockdown inhibits Endothelial cell tumor growth via microRNA 21a-3p targeting of nox-4

Journal of Biological Chemistry

Volumn 289, Issue 13, 2014, Pages 9027-9038

  Gordillo, Gayle M ^a   Biswas, Ayan ^a   Khanna, Savita ^a,b   Pan, Xueliang ^a   Sinha, Mithun ^a,b   Roy, Sashwati ^a,b   Sen, Chandan K ^a,b  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL PLANTS; ENDOTHELIAL CELLS; MAMMALS; PLANTS (BOTANY); RNA;

CHEMOATTRACTANTS; CONTROL GROUPS; HYDROGEN PEROXIDE PRODUCTION; LUCIFERASE ACTIVITIES; POST-TRANSCRIPTIONAL GENE SILENCING; SOFT TISSUE TUMOR; THERAPEUTIC TARGETS; TUMOR FORMATION;

TUMORS;

DICER; HYDROGEN PEROXIDE; MESSENGER RNA; MICRORNA; MICRORNA 21A 3P; MONOCYTE CHEMOTACTIC PROTEIN 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; MIRN21 MICRORNA, MOUSE; NOX4 PROTEIN, MOUSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RIBONUCLEASE III;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CANCER GROWTH; CANCER INHIBITION; CELL TRANSFER; CONTROLLED STUDY; DICER GENE; DRUG TARGETING; ENDOTHELIAL CELL TUMOR; ENZYME ACTIVITY; FEMALE; GENE SILENCING; GENE TARGETING; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MOUSE MODEL; NEOPLASM; NONHUMAN; NOX 4 GENE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA SYNTHESIS; ANIMAL; CELL PROLIFERATION; DEFICIENCY; ENDOTHELIUM CELL; GENETICS; HEMANGIOENDOTHELIOMA; HUMAN; PATHOLOGY;

ANIMALS; CELL PROLIFERATION; ENDOTHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; HEMANGIOENDOTHELIOMA; HUMANS; MICE; MICRORNAS; NADPH OXIDASE; RIBONUCLEASE III;

EID: 84897461815     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.519264     Document Type: Article

References (54)

1. Haggstrom, A. N., Drolet, B. A., Baselga, E., Chamlin, S. L., Garzon, M. C., Horii, K. A., Lucky, A. W., Mancini, A. J., Metry, D. W., Newell, B., Nopper, A. J., and Frieden, I. J. (2006) Prospective study of infantile hemangiomas. Clinical characteristics predicting complications and treatment. Pediatrics 118, 882-887 (Pubitemid 46091612)
2. Jacobs, A. H., and Walton, R. G. (1976) The incidence of birthmarks in the neonate. Pediatrics 58, 218-222
3. Mulliken, J. B. (1988) Diagnosis and natural history of hemangiomas. In Vascular Birthmarks: Hemangiomas and Malformations (Mulliken, J. B., and Young, A. E., eds) pp. 41-62, WB Saunders, Philadelphia, PA
4. Paller, A. S. (2000) Responses to anti-angiogenic therapies. J. Investig. Dermatol. Symp. Proc. 5, 83-86
5. Hoak, J. C., Warner, E. D., Cheng, H. F., Fry, G. L., and Hankenson, R. R. (1971) Hemangioma with thrombocytopenia and microangiopathic anemia (Kasabach-Merritt syndrome). An animal model. J. Lab. Clin. Med. 77, 941-950
6. Warner, E. D., Hoak, J. C., and Fry, G. L. (1971) Hemangioma, thrombocytopenia, and anemia. The Kasabach-Merritt syndrome in an animal model. Arch. Pathol. 91, 523-528
7. Gordillo, G. M., Onat, D., Stockinger, M., Roy, S., Atalay, M., Beck, F. M., and Sen, C. K. (2004) A key angiogenic role of monocyte chemoattractant protein-1 in hemangioendothelioma proliferation. Am. J. Physiol. Cell Physiol. 287, C866-C873 (Pubitemid 39238309)
8. 2 drives DNA oxidation resulting in 8-OHdG as urinary biomarker and hemangioendothelioma formation. Antioxid. Redox. Signal. 12, 933-943
9. Gordillo, G., Fang, H., Khanna, S., Harper, J., Phillips, G., and Sen, C. (2009) Oral administration of blueberry inhibits angiogenic tumor growth and enhances survival of mice with endothelail cell neoplasm. Antioxid. Redox Signal. 11, 47-58
10. Jakymiw, A., Patel, R. S., Deming, N., Bhattacharyya, I., Shah, P., Lamont, R. J., Stewart, C. M., Cohen, D. M., and Chan, E. K. (2010) Overexpression of dicer as a result of reduced let-7 MicroRNA levels contributes to increased cell proliferation of oral cancer cells. Genes Chromosomes Cancer 49, 549-559
11. Dudek, H., Wong, D. H., Arvan, R., Shah, A., Wortham, K., Ying, B., Diwanji, R., Zhou, W., Holmes, B., Yang, H., Cyr, W. A., Zhou, Y., Shah, A., Farkiwala, R., Lee, M., Li, Y., Rettig, G. R., Collingwood, M. A., Basu, S. K., Behlke, M. A., and Brown, B. D. (2014) Knockdown of β-catenin with dicer-substrate siRNAs reduces liver tumor burden in Vivo. Mol. Ther. 22, 92-101
12. Ma, X., Fan, Y., Gao, Y., Zhang, Y., Huang, Q., Ai, Q., Ni, D., Chen, W., Zhang, P., Song, E., Wang, B., Shi, T., Zheng, T., and Zhang, X. (2014) Dicer is down-regulated in clear cell renal cell carcinoma and in vitro Dicer knockdown enhances malignant phenotype transformation. Urol. Oncol. 32, 46
13. Gordillo, G. M., Atalay, M., Roy, S., and Sen, C. K. (2002) Hemangioma model for in vivo angiogenesis. Inducible oxidative stress and MCP-1 expression in EOMA cells. Methods Enzymol. 352, 422-432 (Pubitemid 41103202)
14. Chan, Y. C., Roy, S., Huang, Y., Khanna, S., and Sen, C. K. (2012) The microRNA miR-199a-5p down-regulation switches on wound angiogenesis by derepressing the v-ets erythroblastosis virus E26 oncogene homolog 1-matrix metalloproteinase-1 pathway. J. Biol. Chem. 287, 41032-41043
15. Chan, Y. C., Roy, S., Khanna, S., and Sen, C. K. (2012) Downregulation of endothelial microRNA-200b supports cutaneous wound angiogenesis by desilencing GATA binding protein 2 and vascular endothelial growth factor receptor 2. Arterioscler. Thromb. Vasc. Biol. 32, 1372-1382
16. Park, H. A., Kubicki, N., Gnyawali, S., Chan, Y. C., Roy, S., Khanna, S., and Sen, C. K. (2011) Natural vitamin E α-tocotrienol protects against ischemic stroke by induction of multidrug resistance-associated protein 1. Stroke 42, 2308-2314
17. Shilo, S., Roy, S., Khanna, S., and Sen, C. K. (2008) Evidence for the involvement of miRNA in redox regulated angiogenic response of human microvascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 28, 471-477
18. Schmittgen, T. D. (2008) Regulation of microRNA processing in development, differentiation and cancer. J. Cell Mol. Med. 12, 1811-1819
19. Chen, J. Q., Heldman, M. R., Herrmann, M. A., Kedei, N., Woo, W., Blumberg, P. M., and Goldsmith, P. K. (2013) Absolute quantitation of endogenous proteins with precision and accuracy using a capillary Western system. Anal. Biochem. 442, 97-103
20. Rustandi, R. R., Loughney, J. W., Hamm, M., Hamm, C., Lancaster, C., Mach, A., and Ha, S. (2012) Qualitative and quantitative evaluation of Simon, a new CE-based automated Western blot system as applied to vaccine development. Electrophoresis 33, 2790-2797
21. Tan, L. P., Seinen, E., Duns, G., de Jong, D., Sibon, O. C., Poppema, S., Kroesen, B. J., Kok, K., and van den Berg, A. (2009) A high throughput experimental approach to identify miRNA targets in human cells. Nucleic Acids Res. 37, e137
22. Yu, H., He, Y., Zhang, X., Peng, Z., Yang, Y., Zhu, R., Bai, J., Tian, Y., Li, X., Chen, W., Fang, D., and Wang, R. (2011) The rat IgGFcγBP and Muc2 C-terminal domains and TFF3 in two intestinal mucus layers bind together by covalent interaction. PLoS One 6, e20334
23. Fish, J. E., and Srivastava, D. (2009) MicroRNAs. Opening a new vein in angiogenesis research. Sci. Signal. 2, pe1
24. Urbich, C., Kuehbacher, A., and Dimmeler, S. (2008) Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc. Res. 79, 581-588
25. Wang, S., and Olson, E. N. (2009) AngiomiRs. Key regulators of angiogenesis. Curr. Opin. Genet. Dev. 19, 205-211
26. Hinkal, G. W., Grelier, G., Puisieux, A., and Moyret-Lalle, C. (2011) Complexity in the regulation of Dicer expression. Dicer variant proteins are differentially expressed in epithelial and mesenchymal breast cancer cells and decreased during EMT. Br J. Cancer 104, 387-388
27. Kitagawa, N., Ojima, H., Shirakihara, T., Shimizu, H., Kokubu, A., Urushidate, T., Totoki, Y., Kosuge, T., Miyagawa, S., and Shibata, T. (2013) Downregulation of the microRNA biogenesis components and its association with poor prognosis in hepatocellular carcinoma. Cancer Sci. 104, 543-551
28. Krichevsky, A. M., and Gabriely, G. (2009) miR-21. A small multi-faceted RNA. J. Cell Mol. Med. 13, 39-53
29. Kumarswamy, R., Volkmann, I., and Thum, T. (2011) Regulation and function of miRNA-21 in health and disease. RNA Biol. 8, 706-713
30. Pesta, M., Klecka, J., Kulda, V., Topolcan, O., Hora, M., Eret, V., Ludvikova, M., Babjuk, M., Novak, K., Stolz, J., and Holubec, L. (2010) Importance of miR-20a expression in prostate cancer tissue. Anticancer Res. 30, 3579-3583
31. Slack, F. J., and Weidhaas, J. B. (2008) MicroRNA in cancer prognosis. N. Engl. J. Med. 359, 2720-2722
32. Su, X., Chakravarti, D., Cho, M. S., Liu, L., Gi, Y. J., Lin, Y. L., Leung, M. L., El-Naggar, A., Creighton, C. J., Suraokar, M. B., Wistuba, I., and Flores, E. R. (2010) TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature 467, 986-990
33. Taulli, R., Bersani, F., Foglizzo, V., Linari, A., Vigna, E., Ladanyi, M., Tuschl, T., and Ponzetto, C. (2009) The muscle-specific microRNA miR-206 blocks human rhabdomyosarcoma growth in xenotransplanted mice by promoting myogenic differentiation. J. Clin. Invest. 119, 2366-2378
34. Grelier, G., Voirin, N., Ay, A. S., Cox, D. G., Chabaud, S., Treilleux, I., Léon-Goddard, S., Rimokh, R., Mikaelian, I., Venoux, C., Puisieux, A., Lasset, C., and Moyret-Lalle, C. (2009) Prognostic value of Dicer expression in human breast cancers and association with the mesenchymal phenotype. Br J. Cancer 101, 673-683
35. Merritt, W. M., Lin, Y. G., Han, L. Y., Kamat, A. A., Spannuth, W. A., Schmandt, R., Urbauer, D., Pennacchio, L. A., Cheng, J. F., Nick, A. M., Deavers, M. T., Mourad-Zeidan, A., Wang, H., Mueller, P., Lenburg, M. E., Gray, J. W., Mok, S., Birrer, M. J., Lopez-Berestein, G., Coleman, R. L., Bar-Eli, M., and Sood, A. K. (2008) Dicer, Drosha, and outcomes in patients with ovarian cancer. N. Engl. J. Med. 359, 2641-2650
36. Sand, M., Gambichler, T., Skrygan, M., Sand, D., Scola, N., Altmeyer, P., and Bechara, F. G. (2010) Expression levels of the microRNA processing enzymes Drosha and dicer in epithelial skin cancer. Cancer Invest. 28, 649-653
37. Gantier, M. P., McCoy, C. E., Rusinova, I., Saulep, D., Wang, D., Xu, D., Irving, A. T., Behlke, M. A., Hertzog, P. J., Mackay, F., and Williams, B. R. (2011) Analysis of microRNA turnover in mammalian cells following Dicer1 ablation. Nucleic Acids Res. 39, 5692-5703
38. Koscianska, E., Starega-Roslan, J., and Krzyzosiak, W. J. (2011) The role of Dicer protein partners in the processing of microRNA precursors. PLoS One 6, e28548
39. Hanahan, D., and Weinberg, R. A. (2000) The hallmarks of cancer. Cell 100, 57-70 (Pubitemid 30046295)
40. Lord, C. J., and Ashworth, A. (2012) The DNA damage response and cancer therapy. Nature 481, 287-294
41. Fu, Y., Zhang, Y., Wang, Z., Wang, L., Wei, X., Zhang, B., Wen, Z., Fang, H., Pang, Q., and Yi, F. (2010) Regulation of NADPH oxidase activity is associated with miRNA-25-mediated NOX4 expression in experimental diabetic nephropathy. Am. J. Nephrol. 32, 581-589
42. Calin, G. A., and Croce, C. M. (2006) MicroRNA signatures in human cancers. Nat. Rev. Cancer 6, 857-866 (Pubitemid 44629897)
43. Volinia, S., Calin, G. A., Liu, C. G., Ambs, S., Cimmino, A., Petrocca, F., Visone, R., Iorio, M., Roldo, C., Ferracin, M., Prueitt, R. L., Yanaihara, N., Lanza, G., Scarpa, A., Vecchione, A., Negrini, M., Harris, C. C., and Croce, C. M. (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. U.S.A. 103, 2257-2261 (Pubitemid 43271657)
44. Das, A., Ganesh, K., Khanna, S., Sen, C. K., and Roy, S. (2014) Engulfment of apoptotic cells by macrophages. A role of microRNA-21 in the resolution of wound inflammation. J. Immunol. 192, 1120-1129
45. Roy, S., Khanna, S., Hussain, S. R., Biswas, S., Azad, A., Rink, C., Gnyawali, S., Shilo, S., Nuovo, G. J., and Sen, C. K. (2009) MicroRNA expression in response to murine myocardial infarction. miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovasc. Res. 82, 21-29
46. Anglesio, M. S., Wang, Y., Yang, W., Senz, J., Wan, A., Heravi-Moussavi, A., Salamanca, C., Maines-Bandiera, S., Huntsman, D. G., and Morin, G. B. (2013) Cancer-associated somatic DICER1 hotspot mutations cause defective miRNA processing and reverse-strand expression bias to predominantly mature 3p strands through loss of 5p strand cleavage. J. Pathol. 229, 400-409
47. Berger, S. M., Pesold, B., Reber, S., Schönig, K., Berger, A. J., Weidenfeld, I., Miao, J., Berger, M. R., Gruss, O. J., and Bartsch, D. (2010) Quantitative analysis of conditional gene inactivation using rationally designed, tetracycline-controlled miRNAs. Nucleic Acids Res. 38, e168
48. Ziech, D., Franco, R., Pappa, A., and Panayiotidis, M. I. (2011) Reactive oxygen species (ROS)-induced genetic and epigenetic alterations in human carcinogenesis. Mutat Res. 711, 167-173
49. Kuo, H. W., Chou, S. Y., Hu, T. W., Wu, F. Y., and Chen, D. J. (2007) Urinary 8-hydroxy-2′-deoxyguanosine (8-OHdG) and genetic polymorphisms in breast cancer patients. Mutat Res. 631, 62-68
50. Yano, T., Shoji, F., Baba, H., Koga, T., Shiraishi, T., Orita, H., and Kohno, H. (2009) Significance of the urinary 8-OHdG level as an oxidative stress marker in lung cancer patients. Lung Cancer 63, 111-114
51. Soini, Y., Haapasaari, K. M., Vaarala, M. H., Turpeenniemi-Hujanen, T., Kärjä, V., and Karihtala, P. (2011) 8-hydroxydeguanosine and nitrotyrosine are prognostic factors in urinary bladder carcinoma. Int. J. Clin. Exp. Pathol. 4, 267-275
52. Pache, J. C., Carnesecchi, S., Deffert, C., Donati, Y., Herrmann, F. R., Barazzone-Argiroffo, C., and Krause, K. H. (2011) NOX-4 is expressed in thickened pulmonary arteries in idiopathic pulmonary fibrosis. Nat. Med. 17, 31-33
53. Chamberlain, J., Francis, S., Brookes, Z., Shaw, G., Graham, D., Alp, N. J., Dower, S., and Crossman, D. C. (2009) Interleukin-1 regulates multiple atherogenic mechanisms in response to fat feeding. PLoS One 4, e5073
54. Lu, J., Getz, G., Miska, E. A., Alvarez-Saavedra, E., Lamb, J., Peck, D., Sweet-Cordero, A., Ebert, B. L., Mak, R. H., Ferrando, A. A., Downing, J. R., Jacks, T., Horvitz, H. R., and Golub, T. R. (2005) MicroRNA expression profiles classify human cancers. Nature 435, 834-838 (Pubitemid 40839735)