MicroRNA-17-92a upregulation by estrogen leads to bim targeting and inhibition of osteoblast apoptosis

Journal of Cell Science

Volumn 126, Issue 4, 2013, Pages 978-988

  Guo, Lei ^a   Xu, Jiping ^a   Qi, Jin ^a   Zhang, Lianfang ^a   Wang, Jinsheng ^a   Liang, Jing ^a   Qian, Niandong ^a   Zhou, Hanbing ^a   Wei, Li ^a   Deng, Lianfu ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Apoptosis; Bim; Estrogen; MicroRNA 17 92a; Osteoporosis

Indexed keywords

BIM PROTEIN; DEXAMETHASONE; ESTROGEN; ETOPOSIDE; MICRORNA; MICRORNA 17; MICRORNA 20A; MICRORNA 92A; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; FLOW CYTOMETRY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOUSE; NEWBORN; NONHUMAN; OSTEOBLAST; PHENOTYPE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; UPREGULATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELLS, CULTURED; DEXAMETHASONE; ESTROGENS; ETOPOSIDE; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOBLASTS; PROTO-ONCOGENE PROTEINS; RNA INTERFERENCE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84876328882     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.117515     Document Type: Article

References (36)

1. Asada, S., Takahashi, T., Isodono, K., Adachi, A., Imoto, H., Ogata, T., Ueyama, T., Matsubara, H. and Oh, H. (2008). Downregulation of Dicer expression by serum withdrawal sensitizes human endothelial cells to apoptosis. Am. J. Physiol. Heart Circ. Physiol. 295, H2512-H2521.
2. Bhat-Nakshatri, P., Wang, G., Collins, N. R., Thomson, M. J., Geistlinger, T. R., Carroll, J. S., Brown, M., Hammond, S., Srour, E. F., Liu, Y. et al. (2009). Estradiol-regulated microRNAs control estradiol response in breast cancer cells. Nucleic Acids Res. 37, 4850-4861.
3. Castellano, L., Giamas, G., Jacob, J., Coombes, R. C., Lucchesi, W., Thiruchelvam, P., Barton, G., Jiao, L. R., Wait, R., Waxman, J. et al. (2009). The estrogen receptor-alpha-induced microRNA signature regulates itself and its transcriptional response. Proc. Natl. Acad. Sci. USA 106, 15732-15737.
4. Couzin, J. (2007). Genetics. Erasing microRNAs reveals their powerful punch. Science 316, 530.
5. Cuellar, T. L. and McManus, M. T. (2005). MicroRNAs and endocrine biology. J. Endocrinol. 187, 327-332.
6. Dai, R., Phillips, R. A., Zhang, Y., Khan, D., Crasta, O. and Ahmed, S. A. (2008). Suppression of LPS-induced Interferon-gamma and nitric oxide in splenic lymphocytes by select estrogen-regulated microRNAs: a novel mechanism of immune modulation. Blood 112, 4591-4597.
7. Di Leva, G., Gasparini, P., Piovan, C., Ngankeu, A., Garofalo, M., Taccioli, C., Iorio, M. V., Li, M., Volinia, S., Alder, H. et al. (2010). MicroRNA cluster 221-222 and estrogen receptor alpha interactions in breast cancer. J. Natl. Cancer Inst. 102, 706-721.
8. Dore, L. C., Amigo, J. D., Dos Santos, C. O., Zhang, Z., Gai, X., Tobias, J. W., Yu, D., Klein, A. M., Dorman, C., Wu, W. et al. (2008). A GATA-1-regulated microRNA locus essential for erythropoiesis. Proc. Natl. Acad. Sci. USA 105, 3333- 3338.
9. Ghodgaonkar, M. M., Shah, R. G., Kandan-Kulangara, F., Affar, E. B., Qi, H. H., Wiemer, E. and Shah, G. M. (2009). Abrogation of DNA vector-based RNAi during apoptosis in mammalian cells due to caspase-mediated cleavage and inactivation of Dicer-1. Cell Death Differ. 16, 858-868.
10. Glass, C. and Singla, D. K. (2011). MicroRNA-1 transfected embryonic stem cells enhance cardiac myocyte differentiation and inhibit apoptosis by modulating the PTEN/Akt pathway in the infarcted heart. Am. J. Physiol. Heart Circ. Physiol. 301, H2038-H2049.
11. Gocek, E., Wang, X., Liu, X., Liu, C. G. and Studzinski, G. P. (2011). MicroRNA-32 upregulation by 1,25-dihydroxyvitamin D3 in human myeloid leukemia cells leads to Bim targeting and inhibition of AraC-induced apoptosis. Cancer Res. 71, 6230-6239.
12. Gohel, A., McCarthy, M. B. and Gronowicz, G. (1999). Estrogen prevents glucocorticoid-induced apoptosis in osteoblasts in vivo and in vitro. Endocrinology 140, 5339-5347.
13. Hossain, A., Kuo, M. T. and Saunders, G. F. (2006). Mir-17-5p regulates breast cancer cell proliferation by inhibiting translation of AIB1 mRNA. Mol. Cell. Biol. 26, 8191- 8201.
14. Hughes, D. E., Dai, A., Tiffee, J. C., Li, H. H., Mundy, G. R. and Boyce, B. F. (1996). Estrogen promotes apoptosis of murine osteoclasts mediated by TGF-beta. Nat. Med. 2, 1132-1136.
15. Klinge, C. M. (2009). Estrogen Regulation of MicroRNA Expression. Curr. Genomics 10, 169-183.
16. Kole, A. J., Swahari, V., Hammond, S. M. and Deshmukh, M. (2011). miR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosis. Genes Dev. 25, 125-130.
17. Kovalchuk, O., Tryndyak, V. P., Montgomery, B., Boyko, A., Kutanzi, K., Zemp, F., Warbritton, A. R., Latendresse, J. R., Kovalchuk, I., Beland, F. A. et al. (2007). Estrogen-induced rat breast carcinogenesis is characterized by alterations in DNA methylation, histone modifications and aberrant microRNA expression. Cell Cycle 6, 2010-2018.
18. Lwin, T., Lin, J., Choi, Y. S., Zhang, X., Moscinski, L. C., Wright, K. L., Sotomayor, E. M., Dalton, W. S. and Tao, J. (2010). Follicular dendritic cell-dependent drug resistance of non-Hodgkin lymphoma involves cell adhesion-mediated Bim downregulation through induction of microRNA-181a. Blood 116, 5228-5236.
19. Manolagas, S. C. (2000). Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr. Rev. 21, 115-137.
20. Manolagas, S. C., Kousteni, S. and Jilka, R. L. (2002). Sex steroids and bone. Recent Prog. Horm. Res. 57, 385-409.
21. Mi, S., Li, Z., Chen, P., He, C., Cao, D., Elkahloun, A., Lu, J., Pelloso, L. A., Wunderlich, M., Huang, H. et al. (2010). Aberrant overexpression and function of the miR-17-92 cluster in MLL-rearranged acute leukemia. Proc. Natl. Acad. Sci. USA 107, 3710-3715.
22. Miyazaki, T., Katagiri, H., Kanegae, Y., Takayanagi, H., Sawada, Y., Yamamoto, A., Pando, M. P., Asano, T., Verma, I. M., Oda, H. et al. (2000). Reciprocal role of ERK and NF-kappaB pathways in survival and activation of osteoclasts. J. Cell Biol. 148, 333-342.
23. Pan, Q., Luo, X. and Chegini, N. (2008). Differential expression of microRNAs in myometrium and leiomyomas and regulation by ovarian steroids. J. Cell. Mol. Med. 12, 227-240.
24. Pullamsetti, S. S., Doebele, C., Fischer, A., Savai, R., Kojonazarov, B., Dahal, B. K., Ghofrani, H. A., Weissmann, N., Grimminger, F., Bonauer, A. et al. (2012). Inhibition of microRNA-17 improves lung and heart function in experimental pulmonary hypertension. Am. J. Respir. Crit. Care Med. 185, 409-419.
25. Qian, L., Van Laake, L. W., Huang, Y., Liu, S., Wendland, M. F. and Srivastava, D. (2011). miR-24 inhibits apoptosis and represses Bim in mouse cardiomyocytes. J. Exp. Med. 208, 549-560.
26. Seeman, E. (2001). Clinical review 137: Sexual dimorphism in skeletal size, density, and strength. J. Clin. Endocrinol. Metab. 86, 4576-4584.
27. Seeman, E. (2003). The structural and biomechanical basis of the gain and loss of bone strength in women and men. Endocrinol. Metab. Clin. North Am. 32, 25-38.
28. Song, G., Zhang, Y. and Wang, L. (2009). MicroRNA-206 targets notch3, activates apoptosis, and inhibits tumor cell migration and focus formation. J. Biol. Chem. 284, 31921-31927.
29. Vasudevan, S., Tong, Y. and Steitz, J. A. (2007). Switching from repression to activation: microRNAs can up-regulate translation. Science 318, 1931-1934.
30. Wiesen, J. L. and Tomasi, T. B. (2009). Dicer is regulated by cellular stresses and interferons. Mol. Immunol. 46, 1222-1228.
31. Willis, S. N. and Adams, J. M. (2005). Life in the balance: how BH3-only proteins induce apoptosis. Curr. Opin. Cell Biol. 17, 617-625.
32. Wu, X., McKenna, M. A., Feng, X., Nagy, T. R. and McDonald, J. M. (2003). Osteoclast apoptosis: the role of Fas in vivo and in vitro. Endocrinology 144, 5545- 5555.
33. Yamagata, K., Fujiyama, S., Ito, S., Ueda, T., Murata, T., Naitou, M., Takeyama, K., Minami, Y., O'Malley, B. W. and Kato, S. (2009). Maturation of microRNA is hormonally regulated by a nuclear receptor. Mol. Cell 36, 340-347.
34. Yang, B., Lin, H., Xiao, J., Lu, Y., Luo, X., Li, B., Zhang, Y., Xu, C., Bai, Y., Wang, H. et al. (2007). The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nat. Med. 13, 486-491.
35. Zamore, P. D. and Haley, B. (2005). Ribo-gnome: the big world of small RNAs. Science 309, 1519-1524.
36. Zeng, Y. (2006). Principles of micro-RNA production and maturation. Oncogene 25, 6156-6162