Generic placeholder image

Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Review Article

Regulation of Histone Deacetylases by MicroRNAs in Bone

Author(s): S. Shreya, D. Malavika, V. Raj Priya and N. Selvamurugan*

Volume 20, Issue 4, 2019

Page: [356 - 367] Pages: 12

DOI: 10.2174/1389203720666181031143129

Price: $65

Abstract

Formation of new bone by osteoblasts is mediated via the activation of signaling pathways, such as TGF-β, BMP, and Wnt. A number of transcription factors participate in the signaling cascades that are tightly regulated by other regulatory factors. Histone deacetylases (HDACs) are one such class of regulatory factors that play an essential role in influencing chromatin architecture and regulate the expression of the genes that play a role in osteoblast differentiation by the mechanism of deacetylation. Four classes of HDACs have been identified namely, class I, class II A, class II B, class III and class IV. MicroRNAs (miRNAs) are small fragments of non-coding RNAs typically 19-25 nucleotides long that target mRNAs to upregulate or downregulate gene expression at a post-transcriptional level. A number of miRNAs that target HDACs in bone have been recently reported. Hence, in this review, we elaborate on the various miRNAs that target the different classes of HDACs and impact of the same on osteogenesis.

Keywords: Bone, HDACs, MicroRNA, osteogenesis, runx2, deacetylation.

Graphical Abstract
[1]
Dhivya, S.; Ajita, J.; Selvamurugan, N. Metallic nanomaterials for bone tissue engineering. J. Biomed. Nanotechnol., 2015, 11(10), 1675-1700.
[2]
Clarke, B. Normal bone anatomy and physiology. Clin. J. Am. Soc. Nephrol., 2008, 3(Suppl. 3), S131-S139.
[3]
Poundarik, A.A.; Wu, P.C.; Evis, Z.; Sroga, G.E.; Ural, A.; Rubin, M.; Vashishth, D. A direct role of collagen glycation in bone fracture. J. Mech. Behav. Biomed, 2015, 52, 120-130.
[4]
Porter, J.R.; Porter, J.R.; Ruckh, T.T.; Popat, K.C. Bone tissue engineering: A review in bone biomimetics and drug delivery strategies. Biotechnol. Prog., 2009, 25(6), 1539-1560.
[5]
Taichman, R.S. Blood and bone: Two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood, 2005, 105(7), 2631-2639.
[6]
Wozney, J.M. Novel regulators of bone formation: Molecular clones and activities. Science, 1988, 242(4885), 1528-1534.
[7]
Sims, N.A.; Martin, T.J. Coupling the activities of bone formation and resorption: A multitude of signals within the basic multicellular unit. Bonekey Rep., 2014, 3, 481.
[8]
Bruder, S.P.; Fink, D.J.; Caplan, A.I. Mesenchymal stem cells in bone development, bone repair, and skeletal regenaration therapy. J. Cell. Biochem., 1994, 56(3), 283-294.
[9]
Ducy, P.; Schinke, T.; Karsenty, G. The osteoblast: A sophisticated fibroblast under central surveillance. Science, 2000, 289(5484), 1501-1504.
[10]
Caetano-Lopes, J.; Canhão, H.; Fonseca, J.E. Osteoblasts and bone formation. Acta Reumatol. Port., 2007, 32(2), 103-110.
[11]
Olsen, B.R.; Reginato, A.M.; Wang, W. Bone development. Annu. Rev. Cell Dev. Biol., 2000, 16(1), 191-220.
[12]
Manolagas, S.C.; Jilka, R.L. Bone marrow, cytokines, and bone remodeling-emerging insights into the pathophysiology of osteoporosis. N. Engl. J. Med., 1995, 332(5), 305-311.
[13]
Manolagas, S.C. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr. Rev., 2000, 21(2), 115-137.
[14]
Jang, W.G.; Kim, E.J.; Kim, D.K.; Ryoo, H.M.; Lee, K.B.; Kim, S.H.; Choi, H.S.; Koh, J.T. BMP2 regulates osteocalcin expression via Runx2 mediated ATF6 gene transcription. J. Biol. Chem., 2012, 287(2), 905-915.
[15]
Komori, T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell, 1997, 89(5), 755-764.
[16]
Nakashima, K. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell, 2002, 108(1), 17-29.
[17]
Chen, G.; Deng, C.; Li, Y.P. TGF-β and BMP signaling in osteoblast differentiation and bone formation. Int. J. Biol. Sci., 2012, 8(2), 272.
[18]
Shorey, S.; Heersche, J.N.M.; Manolson, M.F. The relative contribution of cysteine proteinases and matrix metalloproteinases to the resorption process in osteoclasts derived from long bone and scapula. Bone, 2004, 35(4), 909-917.
[19]
Ogura, K.; Iimura, T.; Makino, Y.; Sugie-Oya, A.; Takakura, A.; Takao-Kawabata, R.; Ishizuya, T.; Moriyama, K.; Yamaguchi, A. Short-term intermittent administration of parathyroid hormone facilitates osteogenesis by different mechanisms in cancellous and cortical bone. Bone Rep., 2016, 5, 7-14.
[20]
Lee, H.W.; Suh, J.H.; Kim, A.Y.; Lee, Y.S.; Park, S.Y.; Kim, J.B. Histone deacetylase 1-mediated histone modification regulates osteoblast differentiation. Mol. Endocrinol., 2006, 20(10), 2432-2443.
[21]
Kang, H.; Hata, A. The role of microRNAs in cell fate determination of mesenchymal stem cells: Balancing adipogenesis and osteogenesis. BMB Rep., 2015, 48(6), 319.
[22]
Vishal, M.; Ajeetha, R.; Keerthana, R.; Selvamurugan, N. Regulation of Runx2 by histone deacetylases in bone. Curr. Protein Pept. Sci., 2016, 17(4), 343-351.
[23]
Gallinari, P.; Di Marco, S.; Jones, P.; Pallaoro, M.; Steinkühler, C. HDACs, histone deacetylation and gene transcription: From molecular biology to cancer therapeutics. Cell Res., 2007, 17(3), 195.
[24]
Sengupta, N.; Seto, E. Regulation of histone deacetylase activities. J. Cell. Biochem., 2004, 93(1), 57-67.
[25]
Marks, P.A.; Miller, T.; Richon, V.M. Histone deacetylases. Curr. Opin. Pharmacol., 2003, 3(4), 344-351.
[26]
Lombardi, P.M.; Cole, K.E.; Dowling, D.P.; Christianson, D.W. Structure, mechanism, and inhibition of histone deacetylases and related metalloenzymes. Curr. Opin. Struct. Biol., 2011, 21(6), 735-743.
[27]
Christianson, D.W. Arginase: Structure, mechanism, and physiological role in male and female sexual arousal. Acc. Chem. Res., 2005, 38(3), 191-201.
[28]
Dowling, D.P.; Di Costanzo, L.; Gennadios, H.A.; Christianson, D.W. Evolution of the arginase fold and functional diversity. Cell. Mol. Life Sci., 2008, 65(13), 2039-2055.
[29]
Bottomley, M.J.; Lo Surdo, P.; Di Giovine, P.; Cirillo, A.; Scarpelli, R.; Ferrigno, F.; Jones, P.; Neddermann, P.; De Francesco, R.; Steinkühler, C.; Gallinari, P.; Carfí, A. Structural and functional analysis of the human HDAC4 catalytic domain reveals a regulatory structural zinc-binding domain. J. Biol. Chem., 2008, 283(39), 26694-26704.
[30]
Somoza, J.R.; Skene, R.J.; Katz, B.A.; Mol, C.; Ho, J.D.; Jennings, A.J.; Luong, C.; Arvai, A.; Buggy, J.J.; Chi, E.; Tang, J.; Sang, B.C.; Verner, E.; Wynands, R.; Leahy, E.M.; Dougan, D.R.; Snell, G.; Navre, M.; Knuth, M.W.; Swanson, R.V.; McRee, D.E.; Tari, L.W. Structural snapshots of human HDAC8 provide insights into the class I histone deacetylases. Structure, 2004, 12(7), 1325-1334.
[31]
Polo, S.E.; Geneviève, A. Histone metabolic pathways and chromatin assembly factors as proliferation markers. Cancer Lett., 2005, 220(1), 1-9.
[32]
de Ruijter, A.J.; van Gennip, A.H.; Caron, H.N.; Kemp, S.; van Kuilenburg, A.B. Histone deacetylases (HDACs): Characterization of the classical HDAC family. Biochem. J., 2003, 370(3), 737-749.
[33]
Yang, X.J.; Seto, E. Collaborative spirit of histone deacetylases in regulating chromatin structure and gene expression. Curr. Opin. Genet. Dev., 2003, 13(2), 143-153.
[34]
Marks, P.; Rifkind, R.A.; Richon, V.M.; Breslow, R.; Miller, T.; Kelly, W.K. Histone deacetylases and cancer: Causes and therapies. Nat. Rev. Cancer, 2001, 1(3), 194.
[35]
Carmen, A.A.; Griffin, P.R.; Calaycay, J.R.; Rundlett, S.E.; Suka, Y.; Grunstein, M. Yeast HOS3 forms a novel trichostatin A-insensitive homodimer with intrinsic histone deacetylase activity. Proc. Natl. Acad. Sci. USA, 1999, 96(22), 12356-12361.
[36]
Hu, E.; Chen, Z.; Fredrickson, T.; Zhu, Y.; Kirkpatrick, R.; Zhang, G.F.; Johanson, K.; Sung, C.M.; Liu, R.; Winkler, J. Cloning and characterization of a novel human class I histone deacetylase that functions as a transcription repressor. J. Biol. Chem., 2000, 275(20), 15254-15264.
[37]
Lee, H.; Rezai-Zadeh, N.; Seto, E. Negative regulation of histone deacetylase 8 activity by cyclic AMP-dependent protein kinase. Mol. Cell. Biol., 2004, 24(2), 765-773.
[38]
Kirsh, O.; Seeler, J.S.; Pichler, A.; Gast, A.; Müller, S.; Miska, E.; Mathieu, M.; Harel-Bellan, A.; Kouzarides, T.; Melchior, F.; Dejean, A. The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. EMBO J., 2002, 21(11), 2682-2691.
[39]
Kosik, K.S. MicroRNAs and cellular phenotypy. Cell, 2010, 143(1), 21-26.
[40]
Hammond, S.M. An overview of microRNAs. Adv. Drug Deliv. Rev., 2015, 87, 3-14.
[41]
Selbach, M.; Schwanhäusser, B.; Thierfelder, N.; Fang, Z.; Khanin, R.; Rajewsky, N. Widespread changes in protein synthesis induced by microRNAs. Nature, 2008, 455(7209), 58.
[42]
Rodriguez, A.; Griffiths-Jones, S.; Ashurst, J.L.; Bradley, A. Identification of mammalian microRNA host genes and transcription units. Genome Res., 2004, 14(10a), 1902-1910.
[43]
Blahna, M.T.; Hata, A. Smad-mediated regulation of microRNA biosynthesis. FEBS Lett., 2012, 586(14), 1906-1912.
[44]
Lee, I.; Ajay, S.S.; Yook, J.I.; Kim, H.S.; Hong, S.H.; Kim, N.H.; Dhanasekaran, S.M.; Chinnaiyan, A.M.; Athey, B.D. New class of microRNA targets containing simultaneous 5′-UTR and 3′-UTR interaction sites. Genome Res., 2009, 19, 1175-1183.
[45]
Shin, C.; Nam, J.W.; Farh, K.K.; Chiang, H.R.; Shkumatava, A.; Bartel, D.P. Expanding the microRNA targeting code: Functional sites with centered pairing. Mol. Cell, 2010, 38(6), 789-802.
[46]
Pasquinelli, A.E. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat. Rev. Genet., 2012, 13(4), 271.
[47]
Vimalraj, S.; Selvamurugan, N. MicroRNAs: Synthesis, gene regulation and osteoblast differentiation. Curr. Issues Mol. Biol., 2012, 15(1), 7-18.
[48]
Vasudevan, S. Posttranscriptional upregulation by microRNAs. WIRES RNA, 2012, 3(3), 311-330.
[49]
Abdallah, B.M.; Moustapha, K. Human mesenchymal stem cells: From basic biology to clinical applications. Gene Ther., 2008, 15(2), 109.
[50]
Inose, H.; Ochi, H.; Kimura, A.; Fujita, K.; Xu, R.; Sato, S.; Iwasaki, M.; Sunamura, S.; Takeuchi, Y.; Fukumoto, S.; Saito, K.; Nakamura, T.; Siomi, H.; Ito, H.; Arai, Y.; Shinomiya, K.; Takeda, S. A microRNA regulatory mechanism of osteoblast differentiation. Proc. Natl. Acad. Sci. USA, 2009, 106(49), 20794-20799.
[51]
Arfat, Y.; Basra, M.A.R.; Shahzad, M.; Majeed, K.; Mahmood, N.; Munir, H. miR-208a-3p suppresses osteoblast differentiation and inhibits bone formation by targeting ACVR1. Mol. Ther. Nucleic Acids, 2018, 11, 323-336.
[52]
Lian, J.B.; Stein, G.S.; van Wijnen, A.J.; Stein, J.L.; Hassan, M.Q.; Gaur, T.; Zhang, Y. MicroRNA control of bone formation and homeostasis. Nat. Rev. Endocrinol., 2012, 8, 212-227.
[53]
Vimalraj, S.; Partridge, N.C.; Selvamurugan, N. A positive role of microRNA-15b on regulation of osteoblast differentiation. J. Cell. Physiol., 2014, 229, 1236-1244.
[54]
Miyaki, S.; Sato, T.; Inoue, A.; Otsuki, S.; Ito, Y.; Yokoyama, S. MicroRNA-140 plays dual roles in both cartilage development and homeostasis. Genes Dev., 2010, 24(11), 1173-1185.
[55]
Vishal, M.; Vimalraj, S.; Ajeetha, R.; Gokulnath, M.; Keerthana, R.; He, Z.; Partridge, N.C.; Selvamurugan, N. MicroRNA-590-5p stabilizes Runx2 by targeting Smad7 during osteoblast differentiation. J. Cell. Physiol., 2017, 232, 371-380.
[56]
Fang, S.; Deng, Y.; Gu, P.; Fan, X. MicroRNAs regulate bone development and regeneration. Int. J. Mol. Sci., 2015, 16(4), 8227-8253.
[57]
Mohanakrishnan, V.; Balasubramanian, A.; Mahalingam, G.; Partridge, N.C.; Ramachandran, I.; Selvamurugan, N. Parathyroid hormone-induced down-regulation of miR-532-5p for matrix metalloproteinase-13 expression in rat osteoblasts. J. Cell. Biochem., 2018, 119, 6181-6193.
[58]
Shivdasani, R.A. MicroRNAs: Regulators of gene expression and cell differentiation. Blood, 2006, 108(12), 3646-3653.
[59]
Watson, P.J.; Fairall, L.; Santos, G.M.; Schwabe, J.W. Structure of HDAC3 bound to co-repressor and inositol tetraphosphate. Nature, 2012, 481(7381), 335.
[60]
Millard, C.J.; Watson, P.J.; Celardo, I.; Gordiyenko, Y.; Cowley, S.M.; Robinson, C.V.; Schwabe, J.W.; Class, I. HDACs share a common mechanism of regulation by inositol phosphates. Mol. Cell, 2013, 51(1), 57-67.
[61]
Itoh, T.; Fairall, L.; Muskett, F.W.; Milano, C.P.; Watson, P.J.; Arnaudo, N.; Schwabe, J.W. Structural and functional characterization of a cell cycle associated HDAC1/2 complex reveals the structural basis for complex assembly and nucleosome targeting. Nucleic Acids Res., 2015, 43(4), 2033-2044.
[62]
Watson, P.J.; Fairall, L.; Schwabe, J.W. Nuclear hormone receptor co-repressors: structure and function. Mol. Cell. Endocrinol., 2012, 348(2), 440-449.
[63]
Bantscheff, M.; Hopf, C.; Savitski, M.M.; Dittmann, A.; Grandi, P.; Michon, A.M.; Boesche, M. Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes. Nat. Biotechnol., 2011, 29(3), 255.
[64]
Watson, P.J.; Millard, C.J.; Riley, A.M.; Robertson, N.S.; Wright, L.C.; Godage, H.Y.; Schwabe, J.W. Insights into the activation mechanism of class I HDAC complexes by inositol phosphates. Nat. Commun., 2016, 7, 11262.
[65]
Bradley, E.W.; McGee-Lawrence, M.E.; Westendorf, J.J. Hdac-mediated control of endochondral and intramembranous ossification. Crit. Rev. Eukar. Gene, 2011, 21(2), 101-113.
[66]
Cantley, M.D.; Fairlie, D.P.; Bartold, P.M.; Marino, V.; Gupta, P.K.; Haynes, D.R. Inhibiting histone deacetylase 1 suppresses both inflammation and bone loss in arthritis. Rheumatology, 2015, 54(9), 1713-1723.
[67]
Jensen, E.D.; Nair, A.K.; Westendorf, J.J. Histone deacetylase co-repressor complex control of Runx2 and bone formation. Crit. Rev. Eukar. Gene, 2007, 17(3), 187-196.
[68]
Jin, J.; Iakova, P.; Jiang, Y.; Lewis, K.; Sullivan, E.; Jawanmardi, N.; Timchenko, N. Transcriptional and translational regulation of C/EBPbeta-HDAC1 complexes controls different levels of p53, SIRT1 and PGC1alpha proteins at early and late stages of liver cancer. J. Biol. Chem., 2013, 288(20), 14451-14462.
[69]
Wilting, R.H.; Yanover, E.; Heideman, M.R.; Jacobs, H.; Horner, J.; Van Der Torre, J.; Dannenberg, J.H. Overlapping functions of Hdac1 and Hdac2 in cell cycle regulation and haematopoiesis. EMBO J., 2010, 29(15), 2586-2597.
[70]
Zhang, Y.; Ma, C.; Liu, X.; Wu, Z.; Yan, P.; Ma, N.; Zhao, Q. Epigenetic landscape in PPARγ2 in the enhancement of adipogenesis of mouse osteoporotic bone marrow stromal cell. Biochim. Biophys. Acta, 2015, 1852(11), 2504-2516.
[71]
Wang, J.; Wang, C.D.; Zhang, N.; Tong, W.X.; Zhang, Y.F.; Shan, S.Z.; Li, Q.F. Mechanical stimulation orchestrates the osteogenic differentiation of human bone marrow stromal cells by regulating HDAC1. Cell Death Dis., 2017, 7(5), e2221.
[72]
Chen, J.; Zhou, J.; Chen, X.; Yang, B.; Wang, D.; Yang, P.; Li, H. miRNA-449a is downregulated in osteosarcoma and promotes cell apoptosis by targeting BCL2. Tumour Biol., 2015, 36(10), 8221-8822.
[73]
Poddar, S.; Kesharwani, D.; Datta, M. Histone deacetylase inhibition regulates miR-449a levels in skeletal muscle cells. Epigenetics, 2016, 11(8), 579-587.
[74]
Kushwaha, P.; Khedgikar, V.; Sharma, D.; Yuen, T.; Gautam, J.; Ahmad, N.; Bhadada, S.K.; Zaidi, M.; Trivedi, R. MicroRNA-874-3p exerts skeletal anabolic effects epigenetically during weaning by suppressing Hdac1. J. Biol. Chem., 2016, 291(8), 3959-3966.
[75]
McGee-Lawrence, M.; Bradley, E.; Dudakovic, A.; Carlson, S.; Ryan, Z.; Kumar, R.; Dadsetan, M.; Yaszemski, M.; Chen, Q.; An, K.; Westendorf, J. Histone deacetylase 3 is required for maintenance of bone mass during aging. Bone, 2013, 52, 296-307.
[76]
Bhaskara, S.; Chyla, B.J.; Amann, J.M.; Knutson, S.K.; Cortez, D.; Sun, Z.W.; Hiebert, S.W. Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol. Cell, 2008, 30(1), 61-72.
[77]
Hesse, E.; Saito, H.; Kiviranta, R.; Correa, D.; Yamana, K.; Neff, L.; Toben, D.; Duda, G.; Atfi, A.; Geoffroy, V.; Horne, W.; Baron, R. Zfp521 controls bone mass by hdac3-dependent attenuation of Runx2 activity. J. Cell Biol., 2010, 191, 1271-1283.
[78]
Wu, M.; Hesse, E.; Morvan, F.; Zhang, J.P.; Correa, D.; Rowe, G.C.; Baron, R. Zfp521 antagonizes Runx2, delays osteoblast differentiation in vitro, and promotes bone formation in vivo. Bone, 2009, 44(4), 528-536.
[79]
Kim, J.; Ko, J. A novel PPARγ2 modulator slzip controls the balance between adipogenesis and osteogenesis during mesenchymal stem cell differentiation. Cell Death Differ., 2014, 21, 1642-1655.
[80]
Bradley, E.W.; Carpio, L.R.; Van Wijnen, A.J.; McGee-Lawrence, M.E.; Westendorf, J.J. Histone deacetylases in bone development and skeletal disorders. Physiol. Rev., 2015, 95(4), 1359-1381.
[81]
Kim, H.N.; Lee, J.H.; Bae, S.C.; Ryoo, H.M.; Kim, H.H.; Ha, H.; Lee, Z.H. Histone deacetylase inhibitor MS‐275 stimulates bone formation in part by enhancing Dhx36‐mediated TNAP transcription. J. Bone Miner. Res., 2011, 26(9), 2161-2173.
[82]
McGee-Lawrence, M.E.; Westendorf, J.J. Histone deacetylases in skeletal development and bone mass maintenance. Gene, 2011, 474(1), 1-11.
[83]
Meng, F.; Li, Z.; Zhang, Z.; Yang, Z.; Kang, Y.; Zhao, X.; Wu, P. MicroRNA-193b-3p regulates chondrogenesis and chondrocyte metabolism by targeting HDAC3. Theranostics, 2018, 8(10), 2862.
[84]
Gantt, S.L.; Joseph, C.G.; Fierke, C.A. Activation and inhibition of histone deacetylase 8 by monovalent cations. J. Biol. Chem., 2010, 285(9), 6036-6043.
[85]
Haberland, M.; Mokalled, M.H.; Montgomery, R.L.; Olson, E.N. Epigenetic control of skull morphogenesis by histone deacetylase 8. Genes Dev., 2009, 23(14), 1625-1630.
[86]
Haberland, M.; Montgomery, R.L.; Olson, E.N. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet., 2009, 10(1), 32.
[87]
Fu, Y.; Zhang, P.; Ge, J.; Cheng, J.; Dong, W.; Yuan, H.; Du, Y.; Yang, M.; Sun, R.; Jiang, H. Histone deacetylase 8 suppresses osteogenic differentiation of bone marrow stromal cells by inhibit-ing histone H3K9 acetylation and RUNX2 activity. Int. J. Biochem. Cell Biol., 2014, 54, 68-77.
[88]
McGee-Lawrence, M.E.; McCleary-Wheeler, A.L.; Secreto, F.J.; Razidlo, D.F.; Zhang, M.; Stensgard, B.A.; Westendorf, J.J. Suberoylanilide hydroxamic acid (SAHA; vorinostat) causes bone loss by inhibiting immature osteoblasts. Bone, 2011, 48(5), 1117-1126.
[89]
Chen, W.; Chen, L.; Zhang, Z.; Meng, F.; Huang, G.; Sheng, P.; Liao, W. MicroRNA-455-3p modulates cartilage development and degeneration through modification of histone H3 acetylation. Biochim. Biophys. Acta, 2016, 1863(12), 2881-2891.
[90]
Verdin, E.; Dequiedt, F.; Kasler, H.G. Class II histone deacetylases: versatile regulators. Trends Genet., 2003, 19(5), 286-293.
[91]
Falkenberg, K.J.; Johnstone, R.W. Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders. Nat. Rev. Drug Discov., 2014, 13(9), 673.
[92]
Grozinger, C.M.; Schreiber, S.L. Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc. Natl. Acad. Sci. USA, 2000, 97(14), 7835-7840.
[93]
Yang, X.J.; Grégoire, S. Class II histone deacetylases: from sequence to function, regulation, and clinical implication. Mol. Cell. Biol., 2005, 25(8), 2873-2884.
[94]
McKinsey, T.A.; Zhang, C.L.; Olson, E.N. Control of muscle development by dueling HATs and HDACs. Curr. Opin. Genet. Dev., 2001, 11(5), 497-504.
[95]
Miska, E.A.; Karlsson, C.; Langley, E.; Nielsen, S.J.; Pines, J.; Kouzarides, T. HDAC4 deacetylase associates with and represses the MEF2 transcription factor. EMBO J., 1999, 18(18), 5099-5107.
[96]
Martin, M.; Kettmann, R.; Dequiedt, F. Class IIa histone deacetylases: regulating the regulators. Oncogene, 2007, 26(37), 5450.
[97]
Wang, A.H.; Bertos, N.R.; Vezmar, M.; Pelletier, N.; Crosato, M.; Heng, H.H.; Yang, X.J. HDAC4, a human histone deacetylase related to yeast HDA1, is a transcriptional corepressor. Mol. Cell. Biol., 1999, 19(11), 7816-7827.
[98]
Martin, M.; Kettmann, R.; Dequiedt, F. Class IIa histone deacetylases: Conducting development and differentiation. Int. J. Dev. Biol., 2009, 53(2-3), 291-301.
[99]
Clocchiatti, A.; Florean, C.; Brancolini, C. Class IIa HDACs: From important roles in differentiation to possible implications in tumourigenesis. J. Cell. Mol. Med., 2011, 15(9), 1833-1846.
[100]
Shimizu, E.; Nakatani, T.; He, Z.; Partridge, N.C. Parathyroid hormone regulates histone deacetylase (HDAC) 4 through protein kinase A-mediated phosphorylation and dephosphorylation in osteoblastic cells. J. Biol. Chem., 2014, 289(31), 21340-21350.
[101]
Ko, J.Y.; Chuang, P.C.; Ke, H.J.; Chen, Y.S.; Sun, Y.C.; Wang, F.S. MicroRNA-29a mitigates glucocorticoid induction of bone loss and fatty marrow by rescuing Runx2 acetylation. Bone, 2015, 81, 80-88.
[102]
Zhao, W.; Zhang, S.; Wang, B.; Huang, J.; Lu, W.W.; Chen, D. Runx2 and microRNA regulation in bone and cartilage diseases. Ann. N. Y. Acad. Sci., 2016, 1383(1), 80-87.
[103]
Li, Z.; Hassan, M.Q.; Jafferji, M.; Aqeilan, R.I.; Garzon, R.; Croce, C.M.; Lian, J.B. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J. Biol. Chem., 2009, 284(23), 15676-15684.
[104]
Tuddenham, L.; Wheeler, G.; Ntounia-Fousara, S.; Waters, J.; Hajihosseini, M.K.; Clark, I.; Dalmay, T. The cartilage specific microRNA‐140 targets histone deacetylase 4 in mouse cells. FEBS Lett., 2006, 580(17), 4214-4217.
[105]
Kang, J.S.; Alliston, T.; Delston, R.; Derynck, R. Repression of Runx2 function by TGF‐β through recruitment of class II histone deacetylases by Smad3. EMBO J., 2005, 24(14), 2543-2555.
[106]
Vega, R.B.; Matsuda, K.; Oh, J.; Barbosa, A.C.; Yang, X.; Meadows, E.; Karsenty, G. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell, 2004, 119(4), 555-566.
[107]
Jeon, E.J.; Lee, K.Y.; Choi, N.S.; Lee, M.H.; Kim, H.N.; Jin, Y.H.; Oh, B.C. Bone morphogenetic protein-2 stimulates Runx2 acetylation. J. Biol. Chem., 2006, 281(24), 16502-16511.
[108]
Maeda, S.; Hayashi, M.; Komiya, S.; Imamura, T.; Miyazono, K. Endogenous TGF‐β signaling suppresses maturation of osteoblastic mesenchymal cells. EMBO J., 2004, 23(3), 552-563.
[109]
Bodine, P.V.; Komm, B.S. Wnt signaling and osteoblastogenesis. Rev. Endocr. Metab. Disord., 2006, 7(1-2), 33-39.
[110]
Ikenoue, T.; Jingushi, S.; Urabe, K.; Okazaki, K.; Iwamoto, Y. Inhibitory effects of activin‐A on osteoblast differentiation during cultures of fetal rat calvarial cells. J. Cell. Biochem., 1999, 75(2), 206-214.
[111]
Eijken, M.; Swagemakers, S.; Koedam, M.; Steenbergen, C.; Derkx, P.; Uitterlinden, A.G.; van Leeuwen, J.P. The activin A-follistatin system: Potent regulator of human extracellular matrix mineralization. FASEB J., 2007, 21(11), 2949-2960.
[112]
Caunt, C.J.; Rivers, C.A.; Conway-Campbell, B.L.; Norman, M.R.; McArdle, C.A. EGF receptor and protein kinase C signaling to ERK2: Spatiotemporal regulation of ERK2 by dual-specificity phosphatases. J. Biol. Chem., 2008, 283(10), 6241-6252.
[113]
Daniels, D.L.; Weis, W.I. ICAT inhibits β-catenin binding to Tcf/Lef-family transcription factors and the general coactivator p300 using independent structural modules. Mol. Cell, 2002, 10(3), 573-584.
[114]
Trompeter, H.I.; Dreesen, J.; Hermann, E.; Iwaniuk, K.M.; Hafner, M.; Renwick, N.; Wernet, P. MicroRNAs miR-26a, miR-26b, and miR-29b accelerate osteogenic differentiation of unrestricted somatic stem cells from human cord blood. BMC Genomics, 2013, 14(1), 111.
[115]
Yuan, Y.; Zhang, L.; Tong, X.; Zhang, M.; Zhao, Y.; Guo, J.; Zou, J. Mechanical stress regulates bone metabolism through micrornas. J. Cell. Physiol., 2017, 232(6), 1239-1245.
[116]
Xiao, Q.; Huang, L.; Zhang, Z.; Chen, X.; Luo, J.; Zhang, Z.; Cao, K. Overexpression of miR-140 inhibits proliferation of osteosarcoma cells via suppression of histone deacetylase 4. Oncol. Res., 2017, 25(2), 267-275.
[117]
Moorthi, A.; Vimalraj, S.; Avani, C.; He, Z.; Partridge, N.C.; Selvamurugan, N. Expression of microRNA-30c and its target genes in human osteoblastic cells by nano-bioglass ceramic-treatment. Int. J. Biol. Macromol., 2013, 56, 181-185.
[118]
Song, J.; Jin, E.H.; Kim, D.; Kim, K.Y.; Chun, C.H.; Jin, E.J. MicroRNA-222 regulates MMP-13 via targeting HDAC4 during osteoarthritis pathogenesis. BBA Clin., 2015, 3, 79-89.
[119]
Chen, W.; Sheng, P.; Huang, Z.; Meng, F.; Kang, Y.; Huang, G.; Zhang, Z. MicroRNA-381 regulates chondrocyte hypertrophy by inhibiting histone deacetylase 4 expression. Int. J. Mol. Sci., 2016, 17(9), 1377.
[120]
Li, P.; Wei, X.; Guan, Y.; Chen, Q.; Zhao, T.; Sun, C.; Wei, L. MicroRNA-1 regulates chondrocyte phenotype by repressing histone deacetylase 4 during growth plate development. FASEB J., 2014, 28(9), 3930-3941.
[121]
121. Blixt, N.C.; Faulkner, B.K.; Astleford, K.; Lelich, R.; Schering, J.; Spencer, E.; Gopalakrishnan, R.; Jensen, E.D.; Mansky, K.C. Class II and IV HDACs function as inhibitors of osteoclast differentiation. PLoS One, 2017, 12(9), e0185441.
[122]
Li, H.; Xie, H.; Liu, W.; Hu, R.; Huang, B.; Tan, Y.F.; Xu, K.; Sheng, Z.F.; Zhou, H.D.; Wu, X.P.; Luo, X.H. A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contributes to primary osteoporosis in humans. J. Clin. Invest., 2009, 119(12), 3666-3677.
[123]
Alliston, T.; Choy, L.; Ducy, P.; Karsenty, G.; Derynck, R. TGF‐β‐induced repression of CBFA1 by Smad3 decreases cbfa1 and osteocalcin expression and inhibits osteoblast differentiation. EMBO J., 2001, 20(9), 2254-2272.
[124]
Huang; Yiping. Long noncoding RNA H19 promotes osteoblast differentiation via TGF‐β1/Smad3/HDAC signaling pathway by deriving miR‐675. Stem Cells, 2015, 33(12), 3481-3492.
[125]
Petrie, K.; Guidez, F.; Howell, L.; Healy, L.; Waxman, S.; Greaves, M.; Zelent, A. The histone deacetylase 9 gene encodes multiple protein isoforms. J. Biol. Chem., 2003, 278(18), 16059-16072.
[126]
Clocchiatti, A.; Florean, C.; Brancolini, C. Class IIa HDACs: From important roles in differentiation to possible implications in tumourigenesis. J. Cell. Mol. Med., 2011, 15(9), 1833-1846.
[127]
Jin, Z.; Wei, W.; Huynh, H.; Wan, Y. HDAC9 inhibits osteoclastogenesis via mutual suppression of PPARγ/RANKL signaling. Mol. Endocrinol., 2015, 29(5), 730-738.
[128]
Li, L.; Liu, W.; Wang, H.; Yang, Q.; Zhang, L.; Jin, F.; Jin, Y. Mutual inhibition between HDAC9 and miR-17 regulates osteogenesis of human periodontal ligament stem cells in inflammatory conditions. Cell Death Dis., 2018, 9(5), 480.
[129]
Scognamiglio, A.; Nebbioso, A.; Manzo, F.; Valente, S.; Mai, A.; Altucci, L. HDAC-class II specific inhibition involves HDAC proteasome-dependent degradation mediated by RANBP2. Biochim. Biophys. Acta, 2008, 1783(10), 2030-2038.
[130]
Rao, R.; Nalluri, S.; Kolhe, R.; Yang, Y.; Fiskus, W.; Chen, J.; Ha, K.; Buckley, K.M.; Balusu, R.; Coothankandaswamy, V.; Joshi, A.; Atadja, P.; Bhalla, K.N. Treatment with panobinostat induces glucose-regulated protein 78 acetylation and endoplasmic reticulum stress in breast cancer cells. Mol. Cancer Ther., 2010, 9(4), 942-952.
[131]
Powers, J.; Lienlaf, M.; Perez-Villarroel, P.; Deng, S.; Knox, T.; Villagra, A.; Sahakian, E. Expression and function of histone deacetylase 10 (HDA10) in B cell malignancies. Methods Mol. Biol., 2016, 1436, 129-145.
[132]
Huang, S.; Wang, S.; Bian, C.; Yang, Z.; Zhou, H.; Zeng, Y.; Li, H.; Han, Q.; Zhao, R.C. Upregulation of miR-22 promotes osteogenic differentiation and inhibits adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells by repressing HDAC6 protein expression. Stem Cells Dev., 2012, 21(13), 2531-2540.
[133]
Westendorf, J.J.; Zaidi, S.K.; Cascino, J.E.; Kahler, R.; van Wijnen, A.J.; Lian, J.B.; Yoshida, M.; Stein, G.S.; Li, X. Runx2 (Cbfa1, AML-3) interacts with histone deacetylase 6 and represses the p21CIP1/WAF1 promoter. Mol. Cell. Biol., 2002, 22(22), 7982-7992.
[134]
Berger, S.L. Histone modifications in transcriptional regulation. Curr. Opin. Genet. Dev., 2002, 12(2), 142-148.
[135]
Huang, J.; Zhao, L.; Xing, L.; Chen, D. MicroRNA‐204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem Cells, 2010, 28(2), 357-364.
[136]
Enomoto, H.; Furuichi, T.; Zanma, A.; Yamana, K.; Yoshida, C.; Sumitani, S.; Yamamoto, H.; Enomoto-Iwamoto, M.; Iwamoto, M.; Komori, T. Runx2 deficiency in chondrocytes causes adipogenic changes in vitro. J. Cell Sci., 2004, 117(3), 417-425.
[137]
Takigawa, S.; Chen, A.; Wan, Q.; Na, S.; Sudo, A.; Yokota, H.; Hamamura, K. Role of miR-222-3p in c-Src-mediated regulation of osteoclastogenesis. Int. J. Mol. Sci., 2016, 17(2), 240.
[138]
Sun, T.; Leung, F.; Lu, W.W. MiR-9-5p, miR-675-5p and miR-138-5p damages the strontium and LRP5-mediated skeletal cell proliferation, differentiation, and adhesion. Int. J. Mol. Sci., 2016, 17(2), 236.
[139]
Shi, C.; Qi, J.; Huang, P.; Jiang, M.; Zhou, Q.; Zhou, H.; Deng, L. MicroRNA-17/20a inhibits glucocorticoid-induced osteoclast differentiation and function through targeting RANKL expression in osteoblast cells. Bone, 2014, 68, 67-75.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy