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Published in: Calcified Tissue International 1/2016

01-07-2016 | Review

Implications of the Interaction Between miRNAs and Autophagy in Osteoporosis

Authors: Gengyang Shen, Hui Ren, Ting Qiu, De Liang, Bo Xie, Zhida Zhang, Zhensong Yao, Zhidong Yang, Xiaobing Jiang

Published in: Calcified Tissue International | Issue 1/2016

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Abstract

Imbalances between bone formation and resorption are the primary cause of osteoporosis. However, currently, a detailed molecular mechanism of osteoporosis is not available. Autophagy is the conserved process characterized by degrading and recycling aggregated proteins, intracellular pathogens, and damaged organelles. MicroRNAs (miRNAs) are novel regulatory factors that play important roles in numerous cellular processes, including autophagy, through the posttranscriptional regulation of gene expression. Conversely, autophagy plays a role in the regulation of miRNA homeostasis. Recent advances have revealed that both autophagy and miRNAs are involved in the maintenance of bone homoeostasis, whereas the role of the interaction of miRNAs with autophagy in osteoporosis remains unclear. In this paper, we review previous reports on autophagy, miRNAs, and their interaction in osteoporosis.
Literature
1.
go back to reference Center JR, Nguyen TV, Schneider D, Sambrook PN, Eisman JA (1999) Mortality after all major types of osteoporotic fracture in men and women: an observational study. Lancet 353:878–882PubMedCrossRef Center JR, Nguyen TV, Schneider D, Sambrook PN, Eisman JA (1999) Mortality after all major types of osteoporotic fracture in men and women: an observational study. Lancet 353:878–882PubMedCrossRef
2.
go back to reference NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy (2001) Osteoporosis prevention, diagnosis, and therapy. JAMA 285:785–795CrossRef NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy (2001) Osteoporosis prevention, diagnosis, and therapy. JAMA 285:785–795CrossRef
3.
go back to reference Bliuc D, Nguyen ND, Milch VE, Nguyen TV, Eisman JA, Center JR (2009) Mortality risk associated with low-trauma osteoporotic fracture and subsequent fracture in men and women. JAMA 301:513–521PubMedCrossRef Bliuc D, Nguyen ND, Milch VE, Nguyen TV, Eisman JA, Center JR (2009) Mortality risk associated with low-trauma osteoporotic fracture and subsequent fracture in men and women. JAMA 301:513–521PubMedCrossRef
4.
go back to reference van Staa TP, Dennison EM, Leufkens HG, Cooper C (2001) Epidemiology of fractures in England and Wales. Bone 29:517–522PubMedCrossRef van Staa TP, Dennison EM, Leufkens HG, Cooper C (2001) Epidemiology of fractures in England and Wales. Bone 29:517–522PubMedCrossRef
5.
go back to reference Pasco JA, Lane SE, Brennan-Olsen SL, Holloway KL, Timney EN, Bucki-Smith G, Morse AG, Dobbins AG, Williams LJ, Hyde NK, Kotowicz MA (2015) The epidemiology of incident fracture from cradle to senescence. Calcif Tissue Int 97:568–576PubMedCrossRef Pasco JA, Lane SE, Brennan-Olsen SL, Holloway KL, Timney EN, Bucki-Smith G, Morse AG, Dobbins AG, Williams LJ, Hyde NK, Kotowicz MA (2015) The epidemiology of incident fracture from cradle to senescence. Calcif Tissue Int 97:568–576PubMedCrossRef
6.
go back to reference Wolski H, Bogacz A, Bartkowiak-Wieczorek J, Greber A, Pieńkowski W, Drews K, Klejewski A, Seremak-Mrozikiewicz A (2015) Polymorphism of bone morphogenetic protein (BMP2) and osteoporosis etiology. Ginekol Pol 86:203–209PubMedCrossRef Wolski H, Bogacz A, Bartkowiak-Wieczorek J, Greber A, Pieńkowski W, Drews K, Klejewski A, Seremak-Mrozikiewicz A (2015) Polymorphism of bone morphogenetic protein (BMP2) and osteoporosis etiology. Ginekol Pol 86:203–209PubMedCrossRef
7.
go back to reference Maiuri MC, Zalckvar E, Kimchi A, Kroemer G (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8:741–752PubMedCrossRef Maiuri MC, Zalckvar E, Kimchi A, Kroemer G (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8:741–752PubMedCrossRef
11.
go back to reference Kim KH, Lee MS (2014) Autophagy—a key player in cellular and body metabolism. Nat Rev Endocrinol 10:322–337PubMedCrossRef Kim KH, Lee MS (2014) Autophagy—a key player in cellular and body metabolism. Nat Rev Endocrinol 10:322–337PubMedCrossRef
12.
13.
14.
go back to reference Kim VN, Han J, Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10:126–139PubMedCrossRef Kim VN, Han J, Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10:126–139PubMedCrossRef
16.
go back to reference Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854PubMedCrossRef Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854PubMedCrossRef
18.
go back to reference Alvarez-Garcia I, Miska EA (2005) MicroRNA functions in animal development and human disease. Development 132:4653–4662PubMedCrossRef Alvarez-Garcia I, Miska EA (2005) MicroRNA functions in animal development and human disease. Development 132:4653–4662PubMedCrossRef
19.
go back to reference Kloosterman WP, Plasterk RH (2006) The diverse functions of microRNAs in animal development and disease. Dev Cell 11:441–450PubMedCrossRef Kloosterman WP, Plasterk RH (2006) The diverse functions of microRNAs in animal development and disease. Dev Cell 11:441–450PubMedCrossRef
20.
go back to reference Gibbings D, Mostowy S, Jay F, Schwab Y, Cossart P, Voinnet O (2012) Selective autophagy degrades DICER and AGO2 and regulates miRNA activity. Nat Cell Biol 14:1314–1321PubMedPubMedCentralCrossRef Gibbings D, Mostowy S, Jay F, Schwab Y, Cossart P, Voinnet O (2012) Selective autophagy degrades DICER and AGO2 and regulates miRNA activity. Nat Cell Biol 14:1314–1321PubMedPubMedCentralCrossRef
21.
go back to reference Lan SH, Wu SY, Zuchini R, Lin XZ, Su IJ, Tsai TF, Lin YJ, Wu CT, Liu HS (2014) Autophagy suppresses tumorigenesis of hepatitis B virus-associated hepatocellular carcinoma through degradation of microRNA-224. Hepatology 59:505–517PubMedPubMedCentralCrossRef Lan SH, Wu SY, Zuchini R, Lin XZ, Su IJ, Tsai TF, Lin YJ, Wu CT, Liu HS (2014) Autophagy suppresses tumorigenesis of hepatitis B virus-associated hepatocellular carcinoma through degradation of microRNA-224. Hepatology 59:505–517PubMedPubMedCentralCrossRef
22.
go back to reference Jing Z, Han W, Sui X, Xie J, Pan H (2015) Interaction of autophagy with microRNAs and their potential therapeutic implications in human cancers. Cancer Lett 356:332–338PubMedCrossRef Jing Z, Han W, Sui X, Xie J, Pan H (2015) Interaction of autophagy with microRNAs and their potential therapeutic implications in human cancers. Cancer Lett 356:332–338PubMedCrossRef
23.
24.
25.
go back to reference Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O’Kane CJ, Rubinsztein DC (2004) Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 36:585–595PubMedCrossRef Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O’Kane CJ, Rubinsztein DC (2004) Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 36:585–595PubMedCrossRef
26.
go back to reference Daroszewska A, van’t Hof RJ, Rojas JA, Layfield R, Landao-Basonga E, Rose L, Rose K, Ralston SH (2011) A point mutation in the ubiquitin-associated domain of SQSMT1 is sufficient to cause a Paget’s disease-like disorder in mice. Hum Mol Genet 20:2734–2744PubMedCrossRef Daroszewska A, van’t Hof RJ, Rojas JA, Layfield R, Landao-Basonga E, Rose L, Rose K, Ralston SH (2011) A point mutation in the ubiquitin-associated domain of SQSMT1 is sufficient to cause a Paget’s disease-like disorder in mice. Hum Mol Genet 20:2734–2744PubMedCrossRef
27.
go back to reference Shapiro IM, Layfield R, Lotz M, Settembre C, Whitehouse C (2014) Boning up on autophagy: the role of autophagy in skeletal biology. Autophagy 10:7–19PubMedPubMedCentralCrossRef Shapiro IM, Layfield R, Lotz M, Settembre C, Whitehouse C (2014) Boning up on autophagy: the role of autophagy in skeletal biology. Autophagy 10:7–19PubMedPubMedCentralCrossRef
28.
go back to reference Romero DF, Buchinsky FJ, Rucinski B, Cvetkovic M, Bryer HP, Liang XG, Ma YF, Jee WS, Epstein S (1995) Rapamycin: a bone sparing immunosuppressant? J Bone Miner Res 10:760–768PubMedCrossRef Romero DF, Buchinsky FJ, Rucinski B, Cvetkovic M, Bryer HP, Liang XG, Ma YF, Jee WS, Epstein S (1995) Rapamycin: a bone sparing immunosuppressant? J Bone Miner Res 10:760–768PubMedCrossRef
29.
go back to reference Alvarez-Garcia O, Carbajo-Pérez E, Garcia E, Gil H, Molinos I, Rodriguez J, Ordoñez FA, Santos F (2007) Rapamycin retards growth and causes marked alterations in the growth plate of young rats. Pediatr Nephrol 22:954–961PubMedCrossRef Alvarez-Garcia O, Carbajo-Pérez E, Garcia E, Gil H, Molinos I, Rodriguez J, Ordoñez FA, Santos F (2007) Rapamycin retards growth and causes marked alterations in the growth plate of young rats. Pediatr Nephrol 22:954–961PubMedCrossRef
31.
go back to reference Hussein O, Tiedemann K, Murshed M, Komarova SV (2012) Rapamycin inhibits osteolysis and improves survival in a model of experimental bone metastases. Cancer Lett 314:176–184PubMedCrossRef Hussein O, Tiedemann K, Murshed M, Komarova SV (2012) Rapamycin inhibits osteolysis and improves survival in a model of experimental bone metastases. Cancer Lett 314:176–184PubMedCrossRef
32.
go back to reference Alvarez-García O, García-López E, Loredo V, Gil-Peña H, Rodríguez-Suárez J, Ordóñez FA, Carbajo-Pérez E, Santos F (2010) Rapamycin induces growth retardation by disrupting angiogenesis in the growth plate. Kidney Int 78:561–568PubMedCrossRef Alvarez-García O, García-López E, Loredo V, Gil-Peña H, Rodríguez-Suárez J, Ordóñez FA, Carbajo-Pérez E, Santos F (2010) Rapamycin induces growth retardation by disrupting angiogenesis in the growth plate. Kidney Int 78:561–568PubMedCrossRef
33.
go back to reference Holstein JH, Klein M, Garcia P, Histing T, Culemann U, Pizanis A, Laschke MW, Scheuer C, Meier C, Schorr H, Pohlemann T, Menger MD (2008) Rapamycin affects early fracture healing in mice. Br J Pharmacol 154:1055–1062PubMedPubMedCentralCrossRef Holstein JH, Klein M, Garcia P, Histing T, Culemann U, Pizanis A, Laschke MW, Scheuer C, Meier C, Schorr H, Pohlemann T, Menger MD (2008) Rapamycin affects early fracture healing in mice. Br J Pharmacol 154:1055–1062PubMedPubMedCentralCrossRef
34.
go back to reference Huang B, Wang Y, Wang W, Chen J, Lai P, Liu Z, Yan B, Xu S, Zhang Z, Zeng C, Rong L, Liu B, Cai D, Jin D, Bai X (2015) MTORC1 prevents preosteoblast differentiation through the Notch signaling pathway. PLoS Genet 11:e1005426PubMedPubMedCentralCrossRef Huang B, Wang Y, Wang W, Chen J, Lai P, Liu Z, Yan B, Xu S, Zhang Z, Zeng C, Rong L, Liu B, Cai D, Jin D, Bai X (2015) MTORC1 prevents preosteoblast differentiation through the Notch signaling pathway. PLoS Genet 11:e1005426PubMedPubMedCentralCrossRef
35.
go back to reference Darcy A, Meltzer M, Miller J, Lee S, Chappell S, Ver Donck K, Montano M (2012) A novel library screen identifies immunosuppressors that promote osteoblast differentiation. Bone 50:1294–1303PubMedPubMedCentralCrossRef Darcy A, Meltzer M, Miller J, Lee S, Chappell S, Ver Donck K, Montano M (2012) A novel library screen identifies immunosuppressors that promote osteoblast differentiation. Bone 50:1294–1303PubMedPubMedCentralCrossRef
36.
go back to reference Ogawa T, Tokuda M, Tomizawa K, Matsui H, Itano T, Konishi R, Nagahata S, Hatase O (1998) Osteoblastic differentiation is enhanced by rapamycin in rat osteoblast-like osteosarcoma (ROS 17/2.8) cells. Biochem Biophys Res Commun 249:226–230PubMedCrossRef Ogawa T, Tokuda M, Tomizawa K, Matsui H, Itano T, Konishi R, Nagahata S, Hatase O (1998) Osteoblastic differentiation is enhanced by rapamycin in rat osteoblast-like osteosarcoma (ROS 17/2.8) cells. Biochem Biophys Res Commun 249:226–230PubMedCrossRef
37.
38.
go back to reference Isomoto S, Hattori K, Ohgushi H, Nakajima H, Tanaka Y, Takakura Y (2007) Rapamycin as an inhibitor of osteogenic differentiation in bone marrow-derived mesenchymal stem cells. J Orthop Sci 12:83–88PubMedCrossRef Isomoto S, Hattori K, Ohgushi H, Nakajima H, Tanaka Y, Takakura Y (2007) Rapamycin as an inhibitor of osteogenic differentiation in bone marrow-derived mesenchymal stem cells. J Orthop Sci 12:83–88PubMedCrossRef
39.
go back to reference Hirose K, Shiomi T, Hozumi S, Kikuchi Y (2014) Mechanistic target of rapamycin complex 1 signaling regulates cell proliferation, cell survival, and differentiation in regenerating zebrafish fins. BMC Dev Biol 14:42PubMedPubMedCentralCrossRef Hirose K, Shiomi T, Hozumi S, Kikuchi Y (2014) Mechanistic target of rapamycin complex 1 signaling regulates cell proliferation, cell survival, and differentiation in regenerating zebrafish fins. BMC Dev Biol 14:42PubMedPubMedCentralCrossRef
40.
go back to reference Singha UK, Jiang Y, Yu S, Luo M, Lu Y, Zhang J, Xiao G (2008) Rapamycin inhibits osteoblast proliferation and differentiation in MC3T3-E1 cells and primary mouse bone marrow stromal cells. J Cell Biochem 103:434–446PubMedCrossRef Singha UK, Jiang Y, Yu S, Luo M, Lu Y, Zhang J, Xiao G (2008) Rapamycin inhibits osteoblast proliferation and differentiation in MC3T3-E1 cells and primary mouse bone marrow stromal cells. J Cell Biochem 103:434–446PubMedCrossRef
41.
go back to reference Yeh LC, Ma X, Ford JJ, Adamo ML, Lee JC (2013) Rapamycin inhibits BMP-7-induced osteogenic and lipogenic marker expressions in fetal rat calvarial cells. J Cell Biochem 114:1760–1771PubMedCrossRef Yeh LC, Ma X, Ford JJ, Adamo ML, Lee JC (2013) Rapamycin inhibits BMP-7-induced osteogenic and lipogenic marker expressions in fetal rat calvarial cells. J Cell Biochem 114:1760–1771PubMedCrossRef
42.
go back to reference Kim J, Jung Y, Sun H, Joseph J, Mishra A, Shiozawa Y, Wang J, Krebsbach PH, Taichman RS (2012) Erythropoietin mediated bone formation is regulated by mTOR signaling. J Cell Biochem 113:220–228PubMedPubMedCentralCrossRef Kim J, Jung Y, Sun H, Joseph J, Mishra A, Shiozawa Y, Wang J, Krebsbach PH, Taichman RS (2012) Erythropoietin mediated bone formation is regulated by mTOR signaling. J Cell Biochem 113:220–228PubMedPubMedCentralCrossRef
43.
go back to reference Li SF, Tang JJ, Chen J, Zhang P, Wang T, Chen TY, Yan B, Huang B, Wang L, Huang MJ, Zhang ZM, Jin DD (2015) Regulation of bone formation by baicalein via the mTORC1 pathway. Drug Des Dev Ther 9:5169–5183 Li SF, Tang JJ, Chen J, Zhang P, Wang T, Chen TY, Yan B, Huang B, Wang L, Huang MJ, Zhang ZM, Jin DD (2015) Regulation of bone formation by baicalein via the mTORC1 pathway. Drug Des Dev Ther 9:5169–5183
44.
go back to reference Sun H, Kim JK, Mortensen R, Mutyaba LP, Hankenson KD, Krebsbach PH (2013) Osteoblast-targeted suppression of PPARgamma increases osteogenesis through activation of mTOR signaling. Stem Cells 31:2183–2192PubMedCrossRef Sun H, Kim JK, Mortensen R, Mutyaba LP, Hankenson KD, Krebsbach PH (2013) Osteoblast-targeted suppression of PPARgamma increases osteogenesis through activation of mTOR signaling. Stem Cells 31:2183–2192PubMedCrossRef
45.
go back to reference Fan JB, Liu W, Zhu XH, Yuan K, Xu DW, Chen JJ, Cui ZM (2015) EGFR-AKT-mTOR activation mediates epiregulin-induced pleiotropic functions in cultured osteoblasts. Mol Cell Biochem 398:105–113PubMedCrossRef Fan JB, Liu W, Zhu XH, Yuan K, Xu DW, Chen JJ, Cui ZM (2015) EGFR-AKT-mTOR activation mediates epiregulin-induced pleiotropic functions in cultured osteoblasts. Mol Cell Biochem 398:105–113PubMedCrossRef
46.
go back to reference Lisse TS, Liu T, Irmler M, Beckers J, Chen H, Adams JS, Hewison M (2011) Gene targeting by the vitamin D response element binding protein reveals a role for vitamin D in osteoblast mTOR signaling. FASEB J 25:937–947PubMedPubMedCentralCrossRef Lisse TS, Liu T, Irmler M, Beckers J, Chen H, Adams JS, Hewison M (2011) Gene targeting by the vitamin D response element binding protein reveals a role for vitamin D in osteoblast mTOR signaling. FASEB J 25:937–947PubMedPubMedCentralCrossRef
47.
go back to reference Tchetina EV, Maslova KA, Krylov MY, Myakotkin VA (2015) Association of bone loss with the upregulation of survival-related genes and concomitant downregulation of Mammalian target of rapamycin and osteoblast differentiation-related genes in the peripheral blood of late postmenopausal osteoporotic women. J Osteoporos 2015:802694PubMedPubMedCentralCrossRef Tchetina EV, Maslova KA, Krylov MY, Myakotkin VA (2015) Association of bone loss with the upregulation of survival-related genes and concomitant downregulation of Mammalian target of rapamycin and osteoblast differentiation-related genes in the peripheral blood of late postmenopausal osteoporotic women. J Osteoporos 2015:802694PubMedPubMedCentralCrossRef
48.
go back to reference Fang F, Sun S, Wang L, Guan JL, Giovannini M, Zhu Y, Liu F (2015) Neural crest-specific TSC1 deletion in mice leads to sclerotic craniofacial bone lesion. J Bone Miner Res 30:1195–1205PubMedPubMedCentralCrossRef Fang F, Sun S, Wang L, Guan JL, Giovannini M, Zhu Y, Liu F (2015) Neural crest-specific TSC1 deletion in mice leads to sclerotic craniofacial bone lesion. J Bone Miner Res 30:1195–1205PubMedPubMedCentralCrossRef
49.
go back to reference Zeng Z, Jing D, Zhang X, Duan Y, Xue F (2015) Cyclic mechanical stretch promotes energy metabolism in osteoblast-like cells through an mTOR signaling-associated mechanism. Int J Mol Med 36:947–956PubMedPubMedCentral Zeng Z, Jing D, Zhang X, Duan Y, Xue F (2015) Cyclic mechanical stretch promotes energy metabolism in osteoblast-like cells through an mTOR signaling-associated mechanism. Int J Mol Med 36:947–956PubMedPubMedCentral
50.
go back to reference Riddle RC, Leslie JM, Gross TS, Clemens TL (2011) Hypoxia-inducible factor-1alpha protein negatively regulates load-induced bone formation. J Biol Chem 286:44449–44456PubMedPubMedCentralCrossRef Riddle RC, Leslie JM, Gross TS, Clemens TL (2011) Hypoxia-inducible factor-1alpha protein negatively regulates load-induced bone formation. J Biol Chem 286:44449–44456PubMedPubMedCentralCrossRef
51.
52.
go back to reference van der Merwe SW, Conradie MM, Bond R, Olivier BJ, Fritz E, Nieuwoudt M, Delport R, Slavik T, Engelbrecht G, Kahn D, Shephard EG, Kotze MJ, de Villiers NP, Hough S (2006) Effect of rapamycin on hepatic osteodystrophy in rats with portasystemic shunting. World J Gastroenterol 12:4504–4510PubMedPubMedCentralCrossRef van der Merwe SW, Conradie MM, Bond R, Olivier BJ, Fritz E, Nieuwoudt M, Delport R, Slavik T, Engelbrecht G, Kahn D, Shephard EG, Kotze MJ, de Villiers NP, Hough S (2006) Effect of rapamycin on hepatic osteodystrophy in rats with portasystemic shunting. World J Gastroenterol 12:4504–4510PubMedPubMedCentralCrossRef
53.
go back to reference Liu N, Xu N, Wei LH, Chai GL (2013) Mammalian target of rapamycin inhibitor abrogates abnormal osteoclastogenesis in neurofibromatosis type 1. Chin Med J (Engl) 126:101–107CrossRef Liu N, Xu N, Wei LH, Chai GL (2013) Mammalian target of rapamycin inhibitor abrogates abnormal osteoclastogenesis in neurofibromatosis type 1. Chin Med J (Engl) 126:101–107CrossRef
54.
go back to reference Kloos B, Chakraborty S, Lindner SG, Noack K, Harre U, Schett G, Krämer OH, Kubatzky KF (2015) Pasteurella multocida toxin-induced osteoclastogenesis requires mTOR activation. Cell Commun Signal 13:40PubMedPubMedCentralCrossRef Kloos B, Chakraborty S, Lindner SG, Noack K, Harre U, Schett G, Krämer OH, Kubatzky KF (2015) Pasteurella multocida toxin-induced osteoclastogenesis requires mTOR activation. Cell Commun Signal 13:40PubMedPubMedCentralCrossRef
55.
go back to reference Francis LK, Alsayed Y, Leleu X, Jia X, Singha UK, Anderson J, Timm M, Ngo H, Lu G, Huston A, Ehrlich LA, Dimmock E, Lentzsch S, Hideshima T, Roodman GD, Anderson KC, Ghobrial IM (2006) Combination mammalian target of rapamycin inhibitor rapamycin and HSP90 inhibitor 17-allylamino-17-demethoxygeldanamycin has synergistic activity in multiple myeloma. Clin Cancer Res 12:6826–6835PubMedCrossRef Francis LK, Alsayed Y, Leleu X, Jia X, Singha UK, Anderson J, Timm M, Ngo H, Lu G, Huston A, Ehrlich LA, Dimmock E, Lentzsch S, Hideshima T, Roodman GD, Anderson KC, Ghobrial IM (2006) Combination mammalian target of rapamycin inhibitor rapamycin and HSP90 inhibitor 17-allylamino-17-demethoxygeldanamycin has synergistic activity in multiple myeloma. Clin Cancer Res 12:6826–6835PubMedCrossRef
56.
go back to reference Indo Y, Takeshita S, Ishii KA, Hoshii T, Aburatani H, Hirao A, Ikeda K (2013) Metabolic regulation of osteoclast differentiation and function. J Bone Miner Res 28:2392–2399PubMedCrossRef Indo Y, Takeshita S, Ishii KA, Hoshii T, Aburatani H, Hirao A, Ikeda K (2013) Metabolic regulation of osteoclast differentiation and function. J Bone Miner Res 28:2392–2399PubMedCrossRef
57.
go back to reference Owen HC, Vanhees I, Gunst J, Van Cromphaut S, Van den Berghe G (2015) Critical illness-induced bone loss is related to deficient autophagy and histone hypomethylation. Intensive Care Med Exp 3:52PubMedCrossRef Owen HC, Vanhees I, Gunst J, Van Cromphaut S, Van den Berghe G (2015) Critical illness-induced bone loss is related to deficient autophagy and histone hypomethylation. Intensive Care Med Exp 3:52PubMedCrossRef
58.
go back to reference Smink JJ, Tunn PU, Leutz A (2012) Rapamycin inhibits osteoclast formation in giant cell tumor of bone through the C/EBPbeta-MafB axis. J Mol Med (Berl) 90:25–30CrossRef Smink JJ, Tunn PU, Leutz A (2012) Rapamycin inhibits osteoclast formation in giant cell tumor of bone through the C/EBPbeta-MafB axis. J Mol Med (Berl) 90:25–30CrossRef
59.
go back to reference Blaslov K, Katalinic L, Kes P, Spasovski G, Smalcelj R, Basic-Jukic N (2014) What is the impact of immunosuppressive treatment on the post-transplant renal osteopathy? Int Urol Nephrol 46:1019–1024PubMedCrossRef Blaslov K, Katalinic L, Kes P, Spasovski G, Smalcelj R, Basic-Jukic N (2014) What is the impact of immunosuppressive treatment on the post-transplant renal osteopathy? Int Urol Nephrol 46:1019–1024PubMedCrossRef
60.
go back to reference Cejka D, Hayer S, Niederreiter B, Sieghart W, Fuereder T, Zwerina J, Schett G (2010) Mammalian target of rapamycin signaling is crucial for joint destruction in experimental arthritis and is activated in osteoclasts from patients with rheumatoid arthritis. Arthritis Rheum 62:2294–2302PubMedCrossRef Cejka D, Hayer S, Niederreiter B, Sieghart W, Fuereder T, Zwerina J, Schett G (2010) Mammalian target of rapamycin signaling is crucial for joint destruction in experimental arthritis and is activated in osteoclasts from patients with rheumatoid arthritis. Arthritis Rheum 62:2294–2302PubMedCrossRef
61.
go back to reference Sugatani T, Hruska KA (2005) Akt1/Akt2 and mammalian target of rapamycin/Bim play critical roles in osteoclast differentiation and survival, respectively, whereas Akt is dispensable for cell survival in isolated osteoclast precursors. J Biol Chem 280:3583–3589PubMedCrossRef Sugatani T, Hruska KA (2005) Akt1/Akt2 and mammalian target of rapamycin/Bim play critical roles in osteoclast differentiation and survival, respectively, whereas Akt is dispensable for cell survival in isolated osteoclast precursors. J Biol Chem 280:3583–3589PubMedCrossRef
62.
go back to reference Glantschnig H, Fisher JE, Wesolowski G, Rodan GA, Reszka AA (2003) M-CSF, TNFalpha and RANK ligand promote osteoclast survival by signaling through mTOR/S6 kinase. Cell Death Differ 10:1165–1177PubMedCrossRef Glantschnig H, Fisher JE, Wesolowski G, Rodan GA, Reszka AA (2003) M-CSF, TNFalpha and RANK ligand promote osteoclast survival by signaling through mTOR/S6 kinase. Cell Death Differ 10:1165–1177PubMedCrossRef
63.
go back to reference Hadji P, Coleman R, Gnant M (2013) Bone effects of mammalian target of rapamycin (mTOR) inhibition with everolimus. Crit Rev Oncol Hematol 87:101–111PubMedCrossRef Hadji P, Coleman R, Gnant M (2013) Bone effects of mammalian target of rapamycin (mTOR) inhibition with everolimus. Crit Rev Oncol Hematol 87:101–111PubMedCrossRef
64.
go back to reference Durán A, Serrano M, Leitges M, Flores JM, Picard S, Brown JP, Moscat J, Diaz-Meco MT (2004) The atypical PKC-interacting protein p62 is an important mediator of RANK-activated osteoclastogenesis. Dev Cell 6:303–309PubMedCrossRef Durán A, Serrano M, Leitges M, Flores JM, Picard S, Brown JP, Moscat J, Diaz-Meco MT (2004) The atypical PKC-interacting protein p62 is an important mediator of RANK-activated osteoclastogenesis. Dev Cell 6:303–309PubMedCrossRef
65.
go back to reference Li H, Xie H, Liu W, Hu R, Huang B, Tan YF, Xu K, Sheng ZF, Zhou HD, Wu XP, Luo XH (2009) A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contributes to primary osteoporosis in humans. J Clin Invest 119:3666–3677PubMedPubMedCentralCrossRef Li H, Xie H, Liu W, Hu R, Huang B, Tan YF, Xu K, Sheng ZF, Zhou HD, Wu XP, Luo XH (2009) A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contributes to primary osteoporosis in humans. J Clin Invest 119:3666–3677PubMedPubMedCentralCrossRef
66.
go back to reference Wang Y, Li L, Moore BT, Peng XH, Fang X, Lappe JM, Recker RR, Xiao P (2012) MiR-133a in human circulating monocytes: a potential biomarker associated with postmenopausal osteoporosis. PLoS One 7:e34641PubMedPubMedCentralCrossRef Wang Y, Li L, Moore BT, Peng XH, Fang X, Lappe JM, Recker RR, Xiao P (2012) MiR-133a in human circulating monocytes: a potential biomarker associated with postmenopausal osteoporosis. PLoS One 7:e34641PubMedPubMedCentralCrossRef
67.
go back to reference Wang X, Guo B, Li Q et al (2013) MiR-214 targets ATF4 to inhibit bone formation. Nat Med 19:93–100PubMedCrossRef Wang X, Guo B, Li Q et al (2013) MiR-214 targets ATF4 to inhibit bone formation. Nat Med 19:93–100PubMedCrossRef
69.
go back to reference Seeliger C, Karpinski K, Haug AT, Vester H, Schmitt A, Bauer JS, van Griensven M (2014) Five freely circulating miRNAs and bone tissue miRNAs are associated with osteoporotic fractures. J Bone Miner Res 29:1718–1728PubMedCrossRef Seeliger C, Karpinski K, Haug AT, Vester H, Schmitt A, Bauer JS, van Griensven M (2014) Five freely circulating miRNAs and bone tissue miRNAs are associated with osteoporotic fractures. J Bone Miner Res 29:1718–1728PubMedCrossRef
70.
go back to reference Bae Y, Yang T, Zeng HC, Campeau PM, Chen Y, Bertin T, Dawson BC, Munivez E, Tao J, Lee BH (2012) miRNA-34c regulates Notch signaling during bone development. Hum Mol Genet 21:2991–3000PubMedPubMedCentralCrossRef Bae Y, Yang T, Zeng HC, Campeau PM, Chen Y, Bertin T, Dawson BC, Munivez E, Tao J, Lee BH (2012) miRNA-34c regulates Notch signaling during bone development. Hum Mol Genet 21:2991–3000PubMedPubMedCentralCrossRef
71.
go back to reference Yang N, Wang G, Hu C, Shi Y, Liao L, Shi S, Cai Y, Cheng S, Wang X, Liu Y, Tang L, Ding Y, Jin Y (2013) Tumor necrosis factor alpha suppresses the mesenchymal stem cell osteogenesis promoter miR-21 in estrogen deficiency-induced osteoporosis. J Bone Miner Res 28:559–573PubMedCrossRef Yang N, Wang G, Hu C, Shi Y, Liao L, Shi S, Cai Y, Cheng S, Wang X, Liu Y, Tang L, Ding Y, Jin Y (2013) Tumor necrosis factor alpha suppresses the mesenchymal stem cell osteogenesis promoter miR-21 in estrogen deficiency-induced osteoporosis. J Bone Miner Res 28:559–573PubMedCrossRef
72.
go back to reference Ell B, Mercatali L, Ibrahim T, Campbell N, Schwarzenbach H, Pantel K, Amadori D, Kang Y (2013) Tumor-induced osteoclast miRNA changes as regulators and biomarkers of osteolytic bone metastasis. Cancer Cell 24:542–556PubMedCrossRef Ell B, Mercatali L, Ibrahim T, Campbell N, Schwarzenbach H, Pantel K, Amadori D, Kang Y (2013) Tumor-induced osteoclast miRNA changes as regulators and biomarkers of osteolytic bone metastasis. Cancer Cell 24:542–556PubMedCrossRef
74.
go back to reference Baron R, Kneissel M (2013) WNT signaling in bone homeostasis and disease: from human mutations to treatments. Nat Med 19:179–192PubMedCrossRef Baron R, Kneissel M (2013) WNT signaling in bone homeostasis and disease: from human mutations to treatments. Nat Med 19:179–192PubMedCrossRef
75.
go back to reference Qiu W, Kassem M (2014) MiR-141-3p inhibits human stromal (mesenchymal) stem cell proliferation and differentiation. Biochim Biophys Acta 1843:2114–2121PubMedCrossRef Qiu W, Kassem M (2014) MiR-141-3p inhibits human stromal (mesenchymal) stem cell proliferation and differentiation. Biochim Biophys Acta 1843:2114–2121PubMedCrossRef
76.
go back to reference Chen Q, Liu W, Sinha KM, Yasuda H, de Crombrugghe B (2013) Identification and characterization of microRNAs controlled by the osteoblast-specific transcription factor Osterix. PLoS One 8:e58104PubMedPubMedCentralCrossRef Chen Q, Liu W, Sinha KM, Yasuda H, de Crombrugghe B (2013) Identification and characterization of microRNAs controlled by the osteoblast-specific transcription factor Osterix. PLoS One 8:e58104PubMedPubMedCentralCrossRef
77.
go back to reference Kapinas K, Kessler CB, Delany AM (2009) MiR-29 suppression of osteonectin in osteoblasts: regulation during differentiation and by canonical Wnt signaling. J Cell Biochem 108:216–224PubMedPubMedCentralCrossRef Kapinas K, Kessler CB, Delany AM (2009) MiR-29 suppression of osteonectin in osteoblasts: regulation during differentiation and by canonical Wnt signaling. J Cell Biochem 108:216–224PubMedPubMedCentralCrossRef
78.
go back to reference Li Z, Hassan MQ, Jafferji M, Aqeilan RI, Garzon R, Croce CM, van Wijnen AJ, Stein JL, Stein GS, Lian JB (2009) Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem 284:15676–15684PubMedPubMedCentralCrossRef Li Z, Hassan MQ, Jafferji M, Aqeilan RI, Garzon R, Croce CM, van Wijnen AJ, Stein JL, Stein GS, Lian JB (2009) Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem 284:15676–15684PubMedPubMedCentralCrossRef
79.
go back to reference Kapinas K, Kessler C, Ricks T, Gronowicz G, Delany AM (2010) MiR-29 modulates Wnt signaling in human osteoblasts through a positive feedback loop. J Biol Chem 285:25221–25231PubMedPubMedCentralCrossRef Kapinas K, Kessler C, Ricks T, Gronowicz G, Delany AM (2010) MiR-29 modulates Wnt signaling in human osteoblasts through a positive feedback loop. J Biol Chem 285:25221–25231PubMedPubMedCentralCrossRef
80.
go back to reference Wang T, Xu Z (2010) MiR-27 promotes osteoblast differentiation by modulating Wnt signaling. Biochem Biophys Res Commun 402:186–189PubMedCrossRef Wang T, Xu Z (2010) MiR-27 promotes osteoblast differentiation by modulating Wnt signaling. Biochem Biophys Res Commun 402:186–189PubMedCrossRef
81.
go back to reference Hu W, Ye Y, Zhang W, Wang J, Chen A, Guo F (2013) MiR1423p promotes osteoblast differentiation by modulating Wnt signaling. Mol Med Rep 7:689–693PubMed Hu W, Ye Y, Zhang W, Wang J, Chen A, Guo F (2013) MiR1423p promotes osteoblast differentiation by modulating Wnt signaling. Mol Med Rep 7:689–693PubMed
82.
go back to reference Zhang J, Tu Q, Bonewald LF, He X, Stein G, Lian J, Chen J (2011) Effects of miR-335-5p in modulating osteogenic differentiation by specifically downregulating Wnt antagonist DKK1. J Bone Miner Res 26:1953–1963PubMedCrossRef Zhang J, Tu Q, Bonewald LF, He X, Stein G, Lian J, Chen J (2011) Effects of miR-335-5p in modulating osteogenic differentiation by specifically downregulating Wnt antagonist DKK1. J Bone Miner Res 26:1953–1963PubMedCrossRef
83.
go back to reference Zhang WB, Zhong WJ, Wang L (2014) A signal-amplification circuit between miR-218 and Wnt/beta-catenin signal promotes human adipose tissue-derived stem cells osteogenic differentiation. Bone 58:59–66PubMedCrossRef Zhang WB, Zhong WJ, Wang L (2014) A signal-amplification circuit between miR-218 and Wnt/beta-catenin signal promotes human adipose tissue-derived stem cells osteogenic differentiation. Bone 58:59–66PubMedCrossRef
84.
go back to reference Wang FS, Chuang PC, Lin CL, Chen MW, Ke HJ, Chang YH, Chen YS, Wu SL, Ko JY (2013) MicroRNA-29a protects against glucocorticoid-induced bone loss and fragility in rats by orchestrating bone acquisition and resorption. Arthritis Rheum 65:1530–1540PubMedCrossRef Wang FS, Chuang PC, Lin CL, Chen MW, Ke HJ, Chang YH, Chen YS, Wu SL, Ko JY (2013) MicroRNA-29a protects against glucocorticoid-induced bone loss and fragility in rats by orchestrating bone acquisition and resorption. Arthritis Rheum 65:1530–1540PubMedCrossRef
85.
go back to reference Shi C, Huang P, Kang H, Hu B, Qi J, Jiang M, Zhou H, Guo L, Deng L (2015) Glucocorticoid inhibits osteoblasts proliferation by microRNA-199a targeting WNT signaling. J Mol Endocrinol 54:325–337PubMedCrossRef Shi C, Huang P, Kang H, Hu B, Qi J, Jiang M, Zhou H, Guo L, Deng L (2015) Glucocorticoid inhibits osteoblasts proliferation by microRNA-199a targeting WNT signaling. J Mol Endocrinol 54:325–337PubMedCrossRef
86.
go back to reference Xu JF, Yang GH, Pan XH, Zhang SJ, Zhao C, Qiu BS, Gu HF, Hong JF, Cao L, Chen Y, Xia B, Bi Q, Wang YP (2014) Altered microRNA expression profile in exosomes during osteogenic differentiation of human bone marrow-derived mesenchymal stem cells. PLoS One 9:e114627PubMedPubMedCentralCrossRef Xu JF, Yang GH, Pan XH, Zhang SJ, Zhao C, Qiu BS, Gu HF, Hong JF, Cao L, Chen Y, Xia B, Bi Q, Wang YP (2014) Altered microRNA expression profile in exosomes during osteogenic differentiation of human bone marrow-derived mesenchymal stem cells. PLoS One 9:e114627PubMedPubMedCentralCrossRef
87.
go back to reference Kim YJ, Bae SW, Yu SS, Bae YC, Jung JS (2009) MiR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. J Bone Miner Res 24:816–825PubMedCrossRef Kim YJ, Bae SW, Yu SS, Bae YC, Jung JS (2009) MiR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. J Bone Miner Res 24:816–825PubMedCrossRef
88.
go back to reference Mizuno Y, Tokuzawa Y, Ninomiya Y, Yagi K, Yatsuka-Kanesaki Y, Suda T, Fukuda T, Katagiri T, Kondoh Y, Amemiya T, Tashiro H, Okazaki Y (2009) MiR-210 promotes osteoblastic differentiation through inhibition of AcvR1b. FEBS Lett 583:2263–2268PubMedCrossRef Mizuno Y, Tokuzawa Y, Ninomiya Y, Yagi K, Yatsuka-Kanesaki Y, Suda T, Fukuda T, Katagiri T, Kondoh Y, Amemiya T, Tashiro H, Okazaki Y (2009) MiR-210 promotes osteoblastic differentiation through inhibition of AcvR1b. FEBS Lett 583:2263–2268PubMedCrossRef
89.
go back to reference Cheng P, Chen C, He HB, Hu R, Zhou HD, Xie H, Zhu W, Dai RC, Wu XP, Liao EY, Luo XH (2013) MiR-148a regulates osteoclastogenesis by targeting V-maf musculoaponeurotic fibrosarcoma oncogene homolog B. J Bone Miner Res 28:1180–1190PubMedCrossRef Cheng P, Chen C, He HB, Hu R, Zhou HD, Xie H, Zhu W, Dai RC, Wu XP, Liao EY, Luo XH (2013) MiR-148a regulates osteoclastogenesis by targeting V-maf musculoaponeurotic fibrosarcoma oncogene homolog B. J Bone Miner Res 28:1180–1190PubMedCrossRef
90.
go back to reference Kim K, Kim JH, Lee J, Jin HM, Kook H, Kim KK, Lee SY, Kim N (2007) MafB negatively regulates RANKL-mediated osteoclast differentiation. Blood 109:3253–3259PubMedCrossRef Kim K, Kim JH, Lee J, Jin HM, Kook H, Kim KK, Lee SY, Kim N (2007) MafB negatively regulates RANKL-mediated osteoclast differentiation. Blood 109:3253–3259PubMedCrossRef
92.
go back to reference Cao Z, Moore BT, Wang Y, Peng XH, Lappe JM, Recker RR, Xiao P (2014) MiR-422a as a potential cellular microRNA biomarker for postmenopausal osteoporosis. PLoS One 9:e97098PubMedPubMedCentralCrossRef Cao Z, Moore BT, Wang Y, Peng XH, Lappe JM, Recker RR, Xiao P (2014) MiR-422a as a potential cellular microRNA biomarker for postmenopausal osteoporosis. PLoS One 9:e97098PubMedPubMedCentralCrossRef
93.
go back to reference Guo LJ, Liao L, Yang L, Li Y, Jiang TJ (2014) MiR-125a TNF receptor-associated factor 6 to inhibit osteoclastogenesis. Exp Cell Res 321:142–152PubMedCrossRef Guo LJ, Liao L, Yang L, Li Y, Jiang TJ (2014) MiR-125a TNF receptor-associated factor 6 to inhibit osteoclastogenesis. Exp Cell Res 321:142–152PubMedCrossRef
94.
go back to reference Zhao C, Sun W, Zhang P, Ling S, Li Y, Zhao D, Peng J, Wang A, Li Q, Song J, Wang C, Xu X, Xu Z, Zhong G, Han B, Chang YZ, Li Y (2015) MiR-214 promotes osteoclastogenesis by targeting Pten/PI3k/Akt pathway. RNA Biol 12:343–353PubMedPubMedCentralCrossRef Zhao C, Sun W, Zhang P, Ling S, Li Y, Zhao D, Peng J, Wang A, Li Q, Song J, Wang C, Xu X, Xu Z, Zhong G, Han B, Chang YZ, Li Y (2015) MiR-214 promotes osteoclastogenesis by targeting Pten/PI3k/Akt pathway. RNA Biol 12:343–353PubMedPubMedCentralCrossRef
95.
go back to reference Krzeszinski JY, Wei W, Huynh H, Jin Z, Wang X, Chang TC, Xie XJ, He L, Mangala LS, Lopez-Berestein G, Sood AK, Mendell JT, Wan Y (2014) MiR-34a blocks osteoporosis and bone metastasis by inhibiting osteoclastogenesis and Tgif2. Nature 512:431–435PubMedCrossRef Krzeszinski JY, Wei W, Huynh H, Jin Z, Wang X, Chang TC, Xie XJ, He L, Mangala LS, Lopez-Berestein G, Sood AK, Mendell JT, Wan Y (2014) MiR-34a blocks osteoporosis and bone metastasis by inhibiting osteoclastogenesis and Tgif2. Nature 512:431–435PubMedCrossRef
96.
go back to reference Chen C, Cheng P, Xie H, Zhou HD, Wu XP, Liao EY, Luo XH (2014) MiR-503 regulates osteoclastogenesis via targeting RANK. J Bone Miner Res 29:338–347PubMedCrossRef Chen C, Cheng P, Xie H, Zhou HD, Wu XP, Liao EY, Luo XH (2014) MiR-503 regulates osteoclastogenesis via targeting RANK. J Bone Miner Res 29:338–347PubMedCrossRef
97.
go back to reference Kagiya T, Nakamura S (2013) 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 48:373–385PubMedCrossRef Kagiya T, Nakamura S (2013) 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 48:373–385PubMedCrossRef
98.
go back to reference Rossi M, Pitari MR, Amodio N, Di Martino MT, Conforti F, Leone E, Botta C, Paolino FM, Del Giudice T, Iuliano E, Caraglia M, Ferrarini M, Giordano A, Tagliaferri P, Tassone P (2013) MiR-29b negatively regulates human osteoclastic cell differentiation and function: implications for the treatment of multiple myeloma-related bone disease. J Cell Physiol 228:1506–1515PubMedCrossRef Rossi M, Pitari MR, Amodio N, Di Martino MT, Conforti F, Leone E, Botta C, Paolino FM, Del Giudice T, Iuliano E, Caraglia M, Ferrarini M, Giordano A, Tagliaferri P, Tassone P (2013) MiR-29b negatively regulates human osteoclastic cell differentiation and function: implications for the treatment of multiple myeloma-related bone disease. J Cell Physiol 228:1506–1515PubMedCrossRef
99.
go back to reference Lee Y, Kim HJ, Park CK, Kim YG, Lee HJ, Kim JY, Kim HH (2013) MicroRNA-124 regulates osteoclast differentiation. Bone 56:383–389PubMedCrossRef Lee Y, Kim HJ, Park CK, Kim YG, Lee HJ, Kim JY, Kim HH (2013) MicroRNA-124 regulates osteoclast differentiation. Bone 56:383–389PubMedCrossRef
102.
go back to reference Kim KM, Lim SK (2014) Role of miRNAs in bone and their potential as therapeutic targets. Curr Opin Pharmacol 16:133–141PubMedCrossRef Kim KM, Lim SK (2014) Role of miRNAs in bone and their potential as therapeutic targets. Curr Opin Pharmacol 16:133–141PubMedCrossRef
103.
go back to reference Hocking LJ, Whitehouse C, Helfrich MH (2012) Autophagy: a new player in skeletal maintenance? J Bone Miner Res 27:1439–1447PubMedCrossRef Hocking LJ, Whitehouse C, Helfrich MH (2012) Autophagy: a new player in skeletal maintenance? J Bone Miner Res 27:1439–1447PubMedCrossRef
104.
go back to reference Zhang GY, Wang J, Jia YJ, Han R, Li P, Zhu DN (2015) MicroRNA-9 promotes the neuronal differentiation of rat bone marrow mesenchymal stem cells by activating autophagy. Neural Regen Res 10:314–320PubMedPubMedCentralCrossRef Zhang GY, Wang J, Jia YJ, Han R, Li P, Zhu DN (2015) MicroRNA-9 promotes the neuronal differentiation of rat bone marrow mesenchymal stem cells by activating autophagy. Neural Regen Res 10:314–320PubMedPubMedCentralCrossRef
105.
go back to reference You L, Gu W, Chen L, Pan L, Chen J, Peng Y (2014) MiR-378 overexpression attenuates high glucose-suppressed osteogenic differentiation through targeting CASP3 and activating PI3K/Akt signaling pathway. Int J Clin Exp Pathol 7:7249–7261PubMedPubMedCentral You L, Gu W, Chen L, Pan L, Chen J, Peng Y (2014) MiR-378 overexpression attenuates high glucose-suppressed osteogenic differentiation through targeting CASP3 and activating PI3K/Akt signaling pathway. Int J Clin Exp Pathol 7:7249–7261PubMedPubMedCentral
106.
go back to reference Li H, Li T, Fan J, Li T, Fan L, Wang S, Weng X, Han Q, Zhao RC (2015) MiR-216a rescues dexamethasone suppression of osteogenesis, promotes osteoblast differentiation and enhances bone formation, by regulating c-Cbl-mediated PI3K/AKT pathway. Cell Death Differ 22:1935–1945PubMedCrossRef Li H, Li T, Fan J, Li T, Fan L, Wang S, Weng X, Han Q, Zhao RC (2015) MiR-216a rescues dexamethasone suppression of osteogenesis, promotes osteoblast differentiation and enhances bone formation, by regulating c-Cbl-mediated PI3K/AKT pathway. Cell Death Differ 22:1935–1945PubMedCrossRef
107.
go back to reference Weinbaum S, Cowin SC, Zeng Y (1994) A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 27:339–360PubMedCrossRef Weinbaum S, Cowin SC, Zeng Y (1994) A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 27:339–360PubMedCrossRef
108.
go back to reference Kreke MR, Huckle WR, Goldstein AS (2005) Fluid flow stimulates expression of osteopontin and bone sialoprotein by bone marrow stromal cells in a temporally dependent manner. Bone 36:1047–1055PubMedCrossRef Kreke MR, Huckle WR, Goldstein AS (2005) Fluid flow stimulates expression of osteopontin and bone sialoprotein by bone marrow stromal cells in a temporally dependent manner. Bone 36:1047–1055PubMedCrossRef
109.
go back to reference Mukai M, Yoshimine Y, Akamine A, Maeda K (1993) Bone-like nodules formed in vitro by rat periodontal ligament cells. Cell Tissue Res 271:453–460PubMedCrossRef Mukai M, Yoshimine Y, Akamine A, Maeda K (1993) Bone-like nodules formed in vitro by rat periodontal ligament cells. Cell Tissue Res 271:453–460PubMedCrossRef
110.
go back to reference Cho MI, Matsuda N, Lin WL, Moshier A, Ramakrishnan PR (1992) In vitro formation of mineralized nodules by periodontal ligament cells from the rat. Calcif Tissue Int 50:459–467PubMedCrossRef Cho MI, Matsuda N, Lin WL, Moshier A, Ramakrishnan PR (1992) In vitro formation of mineralized nodules by periodontal ligament cells from the rat. Calcif Tissue Int 50:459–467PubMedCrossRef
111.
go back to reference Qi L, Zhang Y (2014) The microRNA 132 regulates fluid shear stress-induced differentiation in periodontal ligament cells through mTOR signaling pathway. Cell Physiol Biochem 33:433–445PubMedCrossRef Qi L, Zhang Y (2014) The microRNA 132 regulates fluid shear stress-induced differentiation in periodontal ligament cells through mTOR signaling pathway. Cell Physiol Biochem 33:433–445PubMedCrossRef
112.
go back to reference Yang M, Pan Y, Zhou Y (2014) MiR-96 promotes osteogenic differentiation by suppressing HBEGF-EGFR signaling in osteoblastic cells. FEBS Lett 588:4761–4768PubMedCrossRef Yang M, Pan Y, Zhou Y (2014) MiR-96 promotes osteogenic differentiation by suppressing HBEGF-EGFR signaling in osteoblastic cells. FEBS Lett 588:4761–4768PubMedCrossRef
113.
go back to reference Yu S, Geng Q, Ma J, Sun F, Yu Y, Pan Q, Hong A (2013) Heparin-binding EGF-like growth factor and miR-1192 exert opposite effect on Runx2-induced osteogenic differentiation. Cell Death Dis 4:e868PubMedPubMedCentralCrossRef Yu S, Geng Q, Ma J, Sun F, Yu Y, Pan Q, Hong A (2013) Heparin-binding EGF-like growth factor and miR-1192 exert opposite effect on Runx2-induced osteogenic differentiation. Cell Death Dis 4:e868PubMedPubMedCentralCrossRef
114.
go back to reference Sun KT, Chen MY, Tu MG, Wang IK, Chang SS, Li CY (2015) MicroRNA-20a regulates autophagy related protein-ATG16L1 in hypoxia-induced osteoclast differentiation. Bone 73:145–153PubMedCrossRef Sun KT, Chen MY, Tu MG, Wang IK, Chang SS, Li CY (2015) MicroRNA-20a regulates autophagy related protein-ATG16L1 in hypoxia-induced osteoclast differentiation. Bone 73:145–153PubMedCrossRef
115.
go back to reference Jin Y, Tymen SD, Chen D, Fang ZJ, Zhao Y, Dragas D, Dai Y, Marucha PT, Zhou X (2013) MicroRNA-99 family targets AKT/mTOR signaling pathway in dermal wound healing. PLoS One 8:e64434PubMedPubMedCentralCrossRef Jin Y, Tymen SD, Chen D, Fang ZJ, Zhao Y, Dragas D, Dai Y, Marucha PT, Zhou X (2013) MicroRNA-99 family targets AKT/mTOR signaling pathway in dermal wound healing. PLoS One 8:e64434PubMedPubMedCentralCrossRef
116.
go back to reference Wei F, Liu Y, Guo Y, Xiang A, Wang G, Xue X, Lu Z (2013) miR-99b-targeted mTOR induction contributes to irradiation resistance in pancreatic cancer. Mol Cancer 12:81PubMedPubMedCentralCrossRef Wei F, Liu Y, Guo Y, Xiang A, Wang G, Xue X, Lu Z (2013) miR-99b-targeted mTOR induction contributes to irradiation resistance in pancreatic cancer. Mol Cancer 12:81PubMedPubMedCentralCrossRef
117.
go back to reference Franceschetti T, Dole NS, Kessler CB, Lee SK, Delany AM (2014) Pathway analysis of microRNA expression profile during murine osteoclastogenesis. PLoS One 9:e107262PubMedPubMedCentralCrossRef Franceschetti T, Dole NS, Kessler CB, Lee SK, Delany AM (2014) Pathway analysis of microRNA expression profile during murine osteoclastogenesis. PLoS One 9:e107262PubMedPubMedCentralCrossRef
118.
go back to reference M’Baya-Moutoula E, Louvet L, Metzinger-Le Meuth V, Massy ZA, Metzinger L (2015) High inorganic phosphate concentration inhibits osteoclastogenesis by modulating miR-223. Biochim Biophys Acta 1852:2202–2212PubMedCrossRef M’Baya-Moutoula E, Louvet L, Metzinger-Le Meuth V, Massy ZA, Metzinger L (2015) High inorganic phosphate concentration inhibits osteoclastogenesis by modulating miR-223. Biochim Biophys Acta 1852:2202–2212PubMedCrossRef
119.
go back to reference Yao Y, Jia T, Pan Y, Gou H, Li Y, Sun Y, Zhang R, Zhang K, Lin G, Xie J, Li J, Wang L (2015) Using a novel microRNA delivery system to inhibit osteoclastogenesis. Int J Mol Sci 16:8337–8350PubMedPubMedCentralCrossRef Yao Y, Jia T, Pan Y, Gou H, Li Y, Sun Y, Zhang R, Zhang K, Lin G, Xie J, Li J, Wang L (2015) Using a novel microRNA delivery system to inhibit osteoclastogenesis. Int J Mol Sci 16:8337–8350PubMedPubMedCentralCrossRef
120.
go back to reference Youngson NA, Lin PC, Lin SS (2014) The convergence of autophagy, small RNA and the stress response-implications for transgenerational epigenetic inheritance in plants. Biomol Concepts 5:1–8PubMedCrossRef Youngson NA, Lin PC, Lin SS (2014) The convergence of autophagy, small RNA and the stress response-implications for transgenerational epigenetic inheritance in plants. Biomol Concepts 5:1–8PubMedCrossRef
122.
123.
go back to reference Deng H, Gao K, Jankovic J (2014) The role of FUS gene variants in neurodegenerative diseases. Nat Rev Neurol 10:337–348PubMedCrossRef Deng H, Gao K, Jankovic J (2014) The role of FUS gene variants in neurodegenerative diseases. Nat Rev Neurol 10:337–348PubMedCrossRef
124.
go back to reference Ryu HH, Jun MH, Min KJ, Jang DJ, Lee YS, Kim HK, Lee JA (2014) Autophagy regulates amyotrophic lateral sclerosis-linked fused in sarcoma-positive stress granules in neurons. Neurobiol Aging 35:2822–2831PubMedCrossRef Ryu HH, Jun MH, Min KJ, Jang DJ, Lee YS, Kim HK, Lee JA (2014) Autophagy regulates amyotrophic lateral sclerosis-linked fused in sarcoma-positive stress granules in neurons. Neurobiol Aging 35:2822–2831PubMedCrossRef
Metadata
Title
Implications of the Interaction Between miRNAs and Autophagy in Osteoporosis
Authors
Gengyang Shen
Hui Ren
Ting Qiu
De Liang
Bo Xie
Zhida Zhang
Zhensong Yao
Zhidong Yang
Xiaobing Jiang
Publication date
01-07-2016
Publisher
Springer US
Published in
Calcified Tissue International / Issue 1/2016
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-016-0122-x

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