MiR-7b directly targets DC-STAMP causing suppression of NFATc1 and c-Fos signaling during osteoclast fusion and differentiation

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1839, Issue 11, 2014, Pages 1084-1096

  Dou, Ce ^a   Zhang, Chengcheng ^a   Kang, Fei ^a   Yang, Xiaochao ^a   Jiang, Hong ^a   Bai, Yan ^a   Xiang, Junyu ^a   Xu, Jianzhong ^a   Dong, Shiwu ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Cell fusion; DC STAMP; MicroRNA; Osteoclastogenesis

Indexed keywords

CD47 ANTIGEN; COLONY STIMULATING FACTOR 1; DENDRITIC CELL SPECIFIC TRANSMEMBRANE PROTEIN; IMMUNOGLOBULIN RECEPTOR; MEMBRANE PROTEIN; MICRORNA; MICRORNA 7B; OSTEOCLAST ASSOCIATED RECEPTOR; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOCLAST SPECIFIC TRANSMEMBRANE PROTEIN; PROTEIN C FOS; UNCLASSIFIED DRUG; DC-STAMP PROTEIN, MOUSE; MIRN7 MICRORNA, MOUSE; NERVE PROTEIN; NFATC1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR NFAT;

3' UNTRANSLATED REGION; AKT GENE; ANIMAL CELL; ARTICLE; CELL COUNT; CELL FUSION; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE EXPRESSION; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN GENE; LUCIFERASE ASSAY; MAPK1 GENE; MICROARRAY ANALYSIS; MOUSE; MULTINUCLEAR CELL; NFATC1 GENE; NONHUMAN; ONCOGENE C FOS; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; SIGNAL TRANSDUCTION; TRAP OSCAR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6 GENE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; ONCOGENE; PHYSIOLOGY; RNA INTERFERENCE;

ANIMALS; CELL DIFFERENTIATION; CELL FUSION; CELLS, CULTURED; DOWN-REGULATION; GENES, FOS; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICRORNAS; NERVE TISSUE PROTEINS; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84907482481     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2014.08.002     Document Type: Article

References (76)

1. Suda T., Udagawa N., Nakamura I., Miyaura C., Takahashi N. Modulation of osteoclast differentiation by local factors. Bone 1995, 17(2 Suppl.). 10.1016/8756-3282(95)00185-g.
2. Roodman G. Advances in bone biology: the osteoclast. Endocr. Rev. 1996, 17(4):308-332.
3. Roodman G. Cell biology of the osteoclast. Exp. Hematol. 1999, 27(8):1229-1241. 10.1016/s0301-472x(99)00061-2.
4. Anderson J. Multinucleated giant cells. Curr. Opin. Hematol. 2000, 7(1):40-47. 10.1097/00062752-200001000-00008.
5. Takahashi N., Akatsu T., Udagawa N., Sasaki T. Osteoblastic cells are involved in osteoclast formation. Endocrinology 1988, 123(5):2600-2602.
6. Lerner U. Osteoclast formation and resorption. Matrix Biol. 2000, 19(2):107-120.
7. Xiong J., Onal M., Jilka R., Weinstein R., Manolagas S., O'Brien C. Matrix-embedded cells control osteoclast formation. Nat. Med. 2011, 17(10):1235-1241. 10.1038/nm.2448.
8. Teitelbaum S. Bone resorption by osteoclasts. Science 2000, 289(5484):1504-1508. 10.1126/science.289.5484.1504.
9. Boyle W., Simonet W., Lacey D. Osteoclast differentiation and activation. Nature 2003, 423(6937):337-342. 10.1038/nature01658.
10. Miyamoto T., Suda T. Differentiation and function of osteoclasts. Keio J. Med. 2003, 52(1):1-7.
11. Arai F., Miyamoto T., Ohneda O., Inada T., Sudo T., Brasel K., Miyata T., Anderson D., Suda T. Commitment and differentiation of osteoclast precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor kappaB (RANK) receptors. J. Exp. Med. 1999, 190(12):1741-1754. 10.1084/jem.190.12.1741.
12. Kim N., Kadono Y., Takami M., Lee J., Lee S.-H., Okada F., Kim J., Kobayashi T., Odgren P., Nakano H., Yeh W.-C., Lee S.-K., Lorenzo J., Choi Y. Osteoclast differentiation independent of the TRANCE-RANK-TRAF6 axis. J. Exp. Med. 2005, 202(5):589-595. 10.1084/jem.20050978.
13. Rodan G., Martin T. Therapeutic approaches to bone diseases. Science 2000, 289(5484):1508-1514. 10.1126/science.289.5484.1508.
14. Chiu Y., Shao T., Feng C., Mensah K., Thullen M., Schwarz E., Ritchlin C. CD16 (FcRgammaIII) as a potential marker of osteoclast precursors in psoriatic arthritis. Arthritis Res. Ther. 2010, 12(1). 10.1186/ar2915.
15. Ciolli S. Multiple myeloma. Clin Cases Miner. Bone Metab. 2012, 9(3):150-152.
16. Xu M., Song Z.-G., Xu C.-X., Rong G.-H., Fan K.-X., Cheng J.-Y., Zhang W., Jia J.-P., Han G., Wang W., Chai W., Liang W.-T., Bi W.-Z., Wang Y. IL-17A Stimulates the Progression of Giant Cell Tumors of Bone. Clin. Cancer Res. 2013, 10.1158/1078-0432.ccr-13-0251.
17. Cully M. Rheumatoid arthritis: Uncoupling bone and cartilage destruction. Nat. Rev. Rheumatol. 2013, 10.1038/nrrheum.2013.111.
18. Ell B., Mercatali L., Ibrahim T., Campbell N., Schwarzenbach H., Pantel K., Amadori D., Kang Y. Tumor-Induced Osteoclast miRNA Changes as Regulators and Biomarkers of Osteolytic Bone Metastasis. Cancer Cell 2013, 24(4):542-556. 10.1016/j.ccr.2013.09.008.
19. Mbalaviele G., Chen H., Boyce B., Mundy G., Yoneda T. The role of cadherin in the generation of multinucleated osteoclasts from mononuclear precursors in murine marrow. J. Clin. Invest. 1995, 95(6):2757-2765. 10.1172/JCI117979.
20. Saginario C., Sterling H., Beckers C., Kobayashi R., Solimena M., Ullu E., Vignery A. MFR, a putative receptor mediating the fusion of macrophages. Mol. Cell. Biol. 1998, 18(11):6213-6223.
21. de Vries T., Schoenmaker T., Beertsen W., van der Neut R., Everts V. Effect of CD44 deficiency on in vitro and in vivo osteoclast formation. J. Cell. Biochem. 2005, 94(5):954-966. 10.1002/jcb.20326.
22. Ishii M., Iwai K., Koike M., Ohshima S., Kudo-Tanaka E., Ishii T., Mima T., Katada Y., Miyatake K., Uchiyama Y., Saeki Y. RANKL-induced expression of tetraspanin CD9 in lipid raft membrane microdomain is essential for cell fusion during osteoclastogenesis. J. Bone Miner. Res. 2006, 21(6):965-976. 10.1359/jbmr.060308.
23. Han X., Sterling H., Chen Y., Saginario C., Brown E., Frazier W., Lindberg F., Vignery A. CD47, a ligand for the macrophage fusion receptor, participates in macrophage multinucleation. J. Biol. Chem. 2000, 275(48):37984-37992. 10.1074/jbc.M002334200.
24. Lee S.-H., Rho J., Jeong D., Sul J.-Y., Kim T., Kim N., Kang J.-S., Miyamoto T., Suda T., Lee S.-K., Pignolo R., Koczon-Jaremko B., Lorenzo J., Choi Y. v-ATPase V0 subunit d2-deficient mice exhibit impaired osteoclast fusion and increased bone formation. Nat. Med. 2006, 12(12):1403-1409. 10.1038/nm1514.
25. Kim M., Day C., Morrison N. MCP-1 is induced by receptor activator of nuclear factor-{kappa}B ligand, promotes human osteoclast fusion, and rescues granulocyte macrophage colony-stimulating factor suppression of osteoclast formation. J. Biol. Chem. 2005, 280(16):16163-16169. 10.1074/jbc.M412713200.
26. Paloneva J., Mandelin J., Kiialainen A., Bohling T., Prudlo J., Hakola P., Haltia M., Konttinen Y., Peltonen L. DAP12/TREM2 deficiency results in impaired osteoclast differentiation and osteoporotic features. J. Exp. Med. 2003, 198(4):669-675. 10.1084/jem.20030027.
27. Hartgers F., Looman M., van der Woning B., Merkx G., Figdor C., Adema G. Genomic organization, chromosomal localization, and 5' upstream region of the human DC-STAMP gene. Immunogenetics 2001, 53(2):145-149.
28. Hartgers F., Vissers J., Looman M., van Zoelen C., Huffine C., Figdor C., Adema G. DC-STAMP, a novel multimembrane-spanning molecule preferentially expressed by dendritic cells. Eur. J. Immunol. 2000, 30(12):3585-3590. 10.1002/1521-4141(200012)30:12<3585::AID-IMMU3585>3.0.CO;2-Y.
29. Kukita T., Wada N., Kukita A., Kakimoto T., Sandra F., Toh K., Nagata K., Iijima T., Horiuchi M., Matsusaki H., Hieshima K., Yoshie O., Nomiyama H. RANKL-induced DC-STAMP is essential for osteoclastogenesis. J. Exp. Med. 2004, 200(7):941-946. 10.1084/jem.20040518.
30. Yagi M., Miyamoto T., Sawatani Y., Iwamoto K., Hosogane N., Fujita N., Morita K., Ninomiya K., Suzuki T., Miyamoto K., Oike Y., Takeya M., Toyama Y., Suda T. DC-STAMP is essential for cell-cell fusion in osteoclasts and foreign body giant cells. J. Exp. Med. 2005, 202(3):345-351. 10.1084/jem.20050645.
31. Chiu Y.-H., Mensah K., Schwarz E., Ju Y., Takahata M., Feng C., McMahon L., Hicks D., Panepento B., Keng P., Ritchlin C. Regulation of human osteoclast development by dendritic cell-specific transmembrane protein (DC-STAMP). J. Bone Miner. Res. 2012, 27(1):79-92. 10.1002/jbmr.531.
32. Courtial N., Smink J., Kuvardina O., Leutz A., Göthert J., Lausen J. Tal1 regulates osteoclast differentiation through suppression of the master regulator of cell fusion DC-STAMP. FASEB J. 2012, 26(2):523-532. 10.1096/fj.11-190850.
33. Eleveld-Trancikova D., Janssen R., Hendriks I., Looman M., Moulin V., Jansen B., Jansen J., Figdor C., Adema G. The DC-derived protein DC-STAMP influences differentiation of myeloid cells. Leukemia 2008, 22(2):455-459. 10.1038/sj.leu.2404910.
34. Eleveld-Trancikova D., Sanecka A., van Hout-Kuijer M., Looman M., Hendriks I., Jansen B., Adema G. DC-STAMP interacts with ER-resident transcription factor LUMAN which becomes activated during DC maturation. Mol. Immunol. 2010, 47(11-12):1963-1973. 10.1016/j.molimm.2010.04.019.
35. Eleveld-Trancikova D., Triantis V., Moulin V., Looman M., Wijers M., Fransen J., Lemckert A., Havenga M., Figdor C., Janssen R., Adema G. The dendritic cell-derived protein DC-STAMP is highly conserved and localizes to the endoplasmic reticulum. J. Leukoc. Biol. 2005, 77(3):337-343. 10.1189/jlb.0804441.
36. Jansen B., Eleveld-Trancikova D., Sanecka A., van Hout-Kuijer M., Hendriks I., Looman M., Leusen J., Adema G. OS9 interacts with DC-STAMP and modulates its intracellular localization in response to TLR ligation. Mol. Immunol. 2009, 46(4):505-515. 10.1016/j.molimm.2008.06.032.
37. Mensah K., Ritchlin C., Schwarz E. RANKL induces heterogeneous DC-STAMP(lo) and DC-STAMP(hi) osteoclast precursors of which the DC-STAMP(lo) precursors are the master fusogens. J. Cell. Physiol. 2010, 223(1):76-83. 10.1002/jcp.22012.
38. Lian J., Stein G., van Wijnen A., Stein J., Hassan M., Gaur T., Zhang Y. MicroRNA control of bone formation and homeostasis. Nat. Rev. Endocrinol. 2012, 8(4):212-227. 10.1038/nrendo.2011.234.
39. Chen C., Cheng P., Xie H., Zhou H.-D., Wu X.-P., Liao E.-Y., Luo X.-H. MiR-503 regulates osteoclastogenesis via targeting RANK. J. Bone Miner. Res. 2013, 10.1002/jbmr.2032.
40. Cheng P., Chen C., He H.-B., Hu R., Zhou H.-D., Xie H., Zhu W., Dai R.-C., Wu X.-P., Liao E.-Y., Luo X.-H. miR-148a regulates osteoclastogenesis by targeting V-maf musculoaponeurotic fibrosarcoma oncogene homolog B. J. Bone Miner. Res. 2013, 28(5):1180-1190. 10.1002/jbmr.1845.
41. Franceschetti T., Kessler C., Lee S.-K., Delany A. miR-29 Promotes Murine Osteoclastogenesis by Regulating Osteoclast Commitment and Migration. J. Biol. Chem. 2013, 10.1074/jbc.M113.484568.
42. Lee Y., Kim H., Park C., Kim Y.-G., Lee H.-J., Kim J.-Y., Kim H.-H. MicroRNA-124 regulates osteoclast differentiation. Bone 2013, 56(2):383-389. 10.1016/j.bone.2013.07.007.
43. Mann M., Barad O., Agami R., Geiger B., Hornstein E. miRNA-based mechanism for the commitment of multipotent progenitors to a single cellular fate. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(36):15804-15809. 10.1073/pnas.0915022107.
44. Mizoguchi F., Izu Y., Hayata T., Hemmi H., Nakashima K., Nakamura T., Kato S., Miyasaka N., Ezura Y., Noda M. Osteoclast-specific Dicer gene deficiency suppresses osteoclastic bone resorption. J. Cell. Biochem. 2010, 109(5):866-875. 10.1002/jcb.22228.
45. Mizoguchi F., Murakami Y., Saito T., Miyasaka N., Kohsaka H. miR-31 controls osteoclast formation and bone resorption by targeting RhoA. Arthritis Res. Ther. 2013, 15(5). 10.1186/ar4282.
46. Paik J., Jang J.-Y., Jeon Y., Kim W., Kim T., Heo D., Kim C.-W. MicroRNA-146a downregulates NFκB activity via targeting TRAF6 and functions as a tumor suppressor having strong prognostic implications in NK/T cell lymphoma. Clin. Cancer Res. 2011, 17(14):4761-4771. 10.1158/1078-0432.ccr-11-0494.
47. Rossi M., Pitari M., Amodio N., Di Martino M., Conforti F., Leone E., Botta C., Paolino F., Del Giudice T., Iuliano E., Caraglia M., Ferrarini M., Giordano A., Tagliaferri P., Tassone P. miR-29b negatively regulates human osteoclastic cell differentiation and function: Implications for the treatment of multiple myeloma-related bone disease. J. Cell. Physiol. 2012, 10.1002/jcp.24306.
48. Sugatani T., Hruska K. MicroRNA-223 is a key factor in osteoclast differentiation. J. Cell. Biochem. 2007, 101(4):996-999. 10.1002/jcb.21335.
49. Sugatani T., Hruska K. Down-regulation of miR-21 biogenesis by estrogen action contributes to osteoclastic apoptosis. J. Cell. Biochem. 2013, 114(6):1217-1222. 10.1002/jcb.24471.
50. Sugatani T., Vacher J., Hruska K. A microRNA expression signature of osteoclastogenesis. Blood 2011, 117(13):3648-3657. 10.1182/blood-2010-10-311415.
51. Wang F.-S., Chung P.-C., Lin C.-L., Chen M.-W., Ke H.-J., Chang Y.-H., Chen Y.-S., Wu S.-L., Ko J.-Y. MicroRNA-29a Protects Against Glucocorticoid-Induced Bone Loss and Fragility in Rats by Orchestrating Bone Acquisition and Resorption. Arthritis Rheum. 2013, 65(6):1530-1540. 10.1002/art.37948.
52. Wang Y., Li L., Moore B., Peng X.-H., Fang X., Lappe J., Recker R., Xiao P. MiR-133a in human circulating monocytes: a potential biomarker associated with postmenopausal osteoporosis. PLoS ONE 2012, 7(4). 10.1371/journal.pone.0034641.
53. Wu Z., Yin H., Liu T., Yan W., Li Z., Chen J., Chen H., Wang T., Jiang Z., Zhou W., Xiao J. MiR-126-5p regulates osteoclast differentiation and bone resorption in giant cell tumor through inhibition of MMP-13. Biochem. Biophys. Res. Commun. 2013, 10.1016/j.bbrc.2013.12.075.
54. Kagiya T., Nakamura S. Expression profiling of microRNAs in RAW264.7 cells treated with a combination of tumor necrosis factor alpha and RANKL during osteoclast differentiation. J. Periodontal Res. 2013, 48(3):373-385. 10.1111/jre.12017.
55. Lee Y.-S., Kim Y.-S., Lee S.-Y., Kim G.-H., Kim B.-J., Lee S.-H., Lee K.-U., Kim G.-S., Kim S.-W., Koh J.-M. AMP kinase acts as a negative regulator of RANKL in the differentiation of osteoclasts. Bone 2010, 47(5):926-937. 10.1016/j.bone.2010.08.001.
56. Yamaguchi N., Kukita T., Li Y.-J., Kamio N., Fukumoto S., Nonaka K., Ninomiya Y., Hanazawa S., Yamashita Y. Adiponectin inhibits induction of TNF-alpha/RANKL-stimulated NFATc1 via the AMPK signaling. FEBS Lett. 2008, 582(3):451-456. 10.1016/j.febslet.2007.12.037.
57. Hirose J., Masuda H., Tokuyama N., Omata Y., Matsumoto T., Yasui T., Kadono Y., Hennighausen L., Tanaka S. Bone resorption is regulated by cell-autonomous negative feedback loop of Stat5-Dusp axis in the osteoclast. J. Exp. Med. 2014, 211(1):153-163. 10.1084/jem.20130538.
58. Maruyama K., Uematsu S., Kondo T., Takeuchi O., Martino M., Kawasaki T., Akira S. Strawberry notch homologue 2 regulates osteoclast fusion by enhancing the expression of DC-STAMP. J. Exp. Med. 2013, 10.1084/jem.20130512.
59. Zhang C., Dou C., Xu J., Dong S. DC-STAMP, the Key Fusion-Mediating Molecule in Osteoclastogenesis. J. Cell. Physiol. 2014, 10.1002/jcp.24553.
60. Vignery A. Macrophage fusion: the making of osteoclasts and giant cells. J. Exp. Med. 2005, 202(3):337-340. 10.1084/jem.20051123.
61. Rho J., Altmann C., Socci N., Merkov L., Kim N., So H., Lee O., Takami M., Brivanlou A., Choi Y. Gene expression profiling of osteoclast differentiation by combined suppression subtractive hybridization (SSH) and cDNA microarray analysis. DNA Cell Biol. 2002, 21(8):541-549. 10.1089/104454902320308915.
62. Iwasaki R., Ninomiya K., Miyamoto K., Suzuki T., Sato Y., Kawana H., Nakagawa T., Suda T., Miyamoto T. Cell fusion in osteoclasts plays a critical role in controlling bone mass and osteoblastic activity. Biochem. Biophys. Res. Commun. 2008, 377(3):899-904. 10.1016/j.bbrc.2008.10.076.
63. Yagi M., Ninomiya K., Fujita N., Suzuki T., Iwasaki R., Morita K., Hosogane N., Matsuo K., Toyama Y., Suda T., Miyamoto T. Induction of DC-STAMP by alternative activation and downstream signaling mechanisms. J. Bone Miner. Res. 2007, 22(7):992-1001. 10.1359/jbmr.070401.
64. Zhu M., Van Dyke T., Gyurko R. Resolvin E1 regulates osteoclast fusion via DC-STAMP and NFATc1. FASEB J. 2013, 27(8):3344-3353. 10.1096/fj.12-220228.
65. Kim H.-J., Hong J., Jung J.-W., Kim T.-H., Kim J., Kim Y., Kim S.-Y. Gymnasterkoreayne F inhibits osteoclast formation by suppressing NFATc1 and DC-STAMP expression. Int. Immunopharmacol. 2010, 10(11):1440-1447. 10.1016/j.intimp.2010.08.017.
66. Choi J., Choi S., Lee S., Lee J., Kim H., Lee S., Lee N. Caffeine enhances osteoclast differentiation and maturation through p38 MAP kinase/Mitf and DC-STAMP/CtsK and TRAP pathway. Cell. Signal. 2013, 25(5):1222-1227. 10.1016/j.cellsig.2013.02.015.
67. Fujita K., Iwasaki M., Ochi H., Fukuda T., Ma C., Miyamoto T., Takitani K., Negishi-Koga T., Sunamura S., Kodama T., Takayanagi H., Tamai H., Kato S., Arai H., Shinomiya K., Itoh H., Okawa A., Takeda S. Vitamin E decreases bone mass by stimulating osteoclast fusion. Nat. Med. 2012, 18(4):589-594. 10.1038/nm.2659.
68. Yang M., Birnbaum M., MacKay C., Mason-Savas A., Thompson B., Odgren P. Osteoclast stimulatory transmembrane protein (OC-STAMP), a novel protein induced by RANKL that promotes osteoclast differentiation. J. Cell. Physiol. 2008, 215(2):497-505. 10.1002/jcp.21331.
69. Yang B., Guo H., Zhang Y., Chen L., Ying D., Dong S. MicroRNA-145 regulates chondrogenic differentiation of mesenchymal stem cells by targeting Sox9. PLoS ONE 2011, 6(7). 10.1371/journal.pone.0021679.
70. Sissons J., Peschon J., Schmitz F., Suen R., Gilchrist M., Aderem A. Cutting edge: microRNA regulation of macrophage fusion into multinucleated giant cells. J. Immunol. 2012, 189(1):23-27. 10.4049/jimmunol.1102477.
71. Negishi-Koga T., Takayanagi H. Ca2+-NFATc1 signaling is an essential axis of osteoclast differentiation. Immunol. Rev. 2009, 231(1):241-256. 10.1111/j.1600-065X.2009.00821.x.
72. Humphrey M., Lanier L., Nakamura M. Role of ITAM-containing adapter proteins and their receptors in the immune system and bone. Immunol. Rev. 2005, 208:50-65. 10.1111/j.0105-2896.2005.00325.x.
73. Ivashkiv L. Cross-regulation of signaling by ITAM-associated receptors. Nat. Immunol. 2009, 10(4):340-347. 10.1038/ni.1706.
74. Pinheiro da Silva F., Aloulou M., Benhamou M., Monteiro R. Inhibitory ITAMs: a matter of life and death. Trends Immunol. 2008, 29(8):366-373. 10.1016/j.it.2008.05.001.
75. Wheal B., Beach R., Tanabe N., Dixon S., Sims S. Subcellular elevation of cytosolic free Ca(2+) is required for osteoclast migration. J. Bone Miner. Res. 2013, 10.1002/jbmr.2068.
76. Lee H.J., Palkovits M., Young W.S. miR-7b, a microRNA up-regulated in the hypothalamus after chronic hyperosmolar stimulation, inhibits Fos translation. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(42):15669-15674.