Characterization of the essential role of bone morphogenetic protein 9 (BMP9) in osteogenic differentiation of mesenchymal stem cells (MSCs) through RNA interference

Prockop, 1997, Marrow stromal cells as stem cells for nonhematopoietic tissues, Science., 276, 71, 10.1126/science.276.5309.71 Caplan, 2001, Mesenchymal stem cells: building blocks for molecular medicine in the 21st century, Trends Mol Med, 7, 259, 10.1016/S1471-4914(01)02016-0 Deng, 2008, Regulation of osteogenic differentiation during skeletal development, Front Biosci, 13, 2001, 10.2741/2819 Rastegar, 2010, Mesenchymal stem cells: molecular characteristics and clinical applications, World J Stem Cell, 2, 67, 10.4252/wjsc.v2.i4.67 Shenaq, 2010, Mesenchymal progenitor cells and their orthopedic applications: forging a path towards clinical trials, Stem Cell Int, 2010, 519028 Teven, 2011, Epigenetic regulation of mesenchymal stem cells: a focus on osteogenic and adipogenic differentiation, Stem Cell Int, 2011, 201371 Liao, 2017, Notch signaling augments BMP9-induced bone formation by promoting the osteogenesis-angiogenesis coupling process in mesenchymal stem cells (MSCs), Cell Physiol Biochem, 41, 1905, 10.1159/000471945 Liao, 2017, lncRNA H19 mediates BMP9-induced osteogenic differentiation of mesenchymal stem cells (MSCs) through Notch signaling, Oncotarget, 8, 53581, 10.18632/oncotarget.18655 Noel, 2002, Regenerative medicine through mesenchymal stem cells for bone and cartilage repair, Curr Opin Investig Drugs, 3, 1000 Chan, 2006, Antigen-presenting property of mesenchymal stem cells occurs during a narrow window at low levels of interferon-gamma, Blood, 107, 4817, 10.1182/blood-2006-01-0057 Corcione, 2006, Human mesenchymal stem cells modulate B-cell functions, Blood, 107, 367, 10.1182/blood-2005-07-2657 Djouad, 2007, Mesenchymal stem cells inhibit the differentiation of dendritic cells through an interleukin-6-dependent mechanism, Stem Cells, 25, 2025, 10.1634/stemcells.2006-0548 Olsen, 2000, Bone development, Annu Rev Cell Dev Biol, 16, 191, 10.1146/annurev.cellbio.16.1.191 Raucci, 2008, Osteoblast proliferation or differentiation is regulated by relative strengths of opposing signaling pathways, J Cell Physiol, 215, 442, 10.1002/jcp.21323 Kim, 2013, Wnt signaling in bone formation and its therapeutic potential for bone diseases, Ther Adv Musculoskelet Dis, 5, 13, 10.1177/1759720X12466608 Yang, 2016, The evolving roles of canonical WNT signaling in stem cells and tumorigenesis: implications in targeted cancer therapies, Lab Invest, 96, 116, 10.1038/labinvest.2015.144 Denduluri, 2015, Insulin-like growth factor (IGF) signaling in tumorigenesis and the development of cancer drug resistance, Genes Dis, 2, 13, 10.1016/j.gendis.2014.10.004 Teven, 2014, Fibroblast growth factor (FGF) signaling in development and skeletal diseases, Genes Dis, 1, 199, 10.1016/j.gendis.2014.09.005 Jo, 2014, The versatile functions of Sox9 in development, stem cells, and human diseases, Genes Dis, 1, 149, 10.1016/j.gendis.2014.09.004 Louvi, 2012, Notch and disease: a growing field, Semin Cell Dev Biol, 23, 473, 10.1016/j.semcdb.2012.02.005 Zanotti, 2010, Notch and the skeleton, Mol Cell Biol, 30, 886, 10.1128/MCB.01285-09 Guruharsha, 2012, The Notch signalling system: recent insights into the complexity of a conserved pathway, Nat Rev Genet, 13, 654, 10.1038/nrg3272 Zhang, 2016, Wnt and BMP signaling crosstalk in regulating dental stem cells: implications in dental tissue engineering, Genes Dis, 3, 263, 10.1016/j.gendis.2016.09.004 Luu, 2007, Distinct roles of bone morphogenetic proteins in osteogenic differentiation of mesenchymal stem cells, J Orthop Res, 25, 665, 10.1002/jor.20359 Wang, 2014, Bone Morphogenetic Protein (BMP) signaling in development and human diseases, Genes Dis, 1, 87, 10.1016/j.gendis.2014.07.005 Reddi, 1998, Role of morphogenetic proteins in skeletal tissue engineering and regeneration, Nat Biotechnol, 16, 247, 10.1038/nbt0398-247 Zou, 1997, BMP signaling and vertebrate limb development, Cold Spring Harbor Symp Quant Biol, 62, 269, 10.1101/SQB.1997.062.01.033 Cheng, 2003, Osteogenic activity of the fourteen types of human bone morphogenetic proteins (BMPs), J Bone Joint Surg Am, 85-A, 1544, 10.2106/00004623-200308000-00017 Kang, 2004, Characterization of the distinct orthotopic bone-forming activity of 14 BMPs using recombinant adenovirus-mediated gene delivery, Gene Ther, 11, 1312, 10.1038/sj.gt.3302298 Luther, 2011, BMP-9 induced osteogenic differentiation of mesenchymal stem cells: molecular mechanism and therapeutic potential, Curr Gene Ther, 11, 229, 10.2174/156652311795684777 Lamplot, 2013, BMP9 signaling in stem cell differentiation and osteogenesis, Am J Stem Cells, 2, 1 Hammond, 2000, An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells, Nature, 404, 293, 10.1038/35005107 Castel, 2013, RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond, Nat Rev Genet, 14, 100, 10.1038/nrg3355 Dykxhoorn, 2003, Killing the messenger: short RNAs that silence gene expression, Nat Rev Mol Cell Biol, 4, 457, 10.1038/nrm1129 Ghildiyal, 2009, Small silencing RNAs: an expanding universe, Nat Rev Genet, 10, 94, 10.1038/nrg2504 Hammond, 2001, Post-transcriptional gene silencing by double-stranded RNA, Nat Rev Genet, 2, 110, 10.1038/35052556 Okamura, 2008, Endogenous small interfering RNAs in animals, Nat Rev Mol Cell Biol, 9, 673, 10.1038/nrm2479 Sarkies, 2014, Small RNAs break out: the molecular cell biology of mobile small RNAs, Nat Rev Mol Cell Biol, 15, 525, 10.1038/nrm3840 Deng, 2014, A simplified and versatile system for the simultaneous expression of multiple siRNAs in mammalian cells using Gibson DNA Assembly, PLoS One, 9, e113064, 10.1371/journal.pone.0113064 Bumcrot, 2006, RNAi therapeutics: a potential new class of pharmaceutical drugs, Nat Chem Biol, 2, 711, 10.1038/nchembio839 Czech, 2011, RNAi-based therapeutic strategies for metabolic disease, Nat Rev Endocrinol, 7, 473, 10.1038/nrendo.2011.57 de Fougerolles, 2007, Interfering with disease: a progress report on siRNA-based therapeutics, Nat Rev Drug Discov, 6, 443, 10.1038/nrd2310 Iorns, 2007, Utilizing RNA interference to enhance cancer drug discovery, Nat Rev Drug Discov, 6, 556, 10.1038/nrd2355 Kim, 2007, Strategies for silencing human disease using RNA interference, Nat Rev Genet, 8, 173, 10.1038/nrg2006 Pecot, 2011, RNA interference in the clinic: challenges and future directions, Nat Rev Cancer, 11, 59, 10.1038/nrc2966 Yoshinari, 2004, Effects on RNAi of the tight structure, sequence and position of the targeted region, Nucleic Acids Res, 32, 691, 10.1093/nar/gkh221 Dudek, 2004, T7 RNAi oligo designer, Nucleic Acids Res, 32, W121, 10.1093/nar/gkh360 Collins, 2005, Structural domains in RNAi, FEBS Lett, 579, 5841, 10.1016/j.febslet.2005.07.072 Luo, 2007, Selection and validation of optimal siRNA target sites for RNAi-mediated gene silencing, Gene, 395, 160, 10.1016/j.gene.2007.02.030 Wu, 2014, Overexpression of Ad5 precursor terminal protein accelerates recombinant adenovirus packaging and amplification in HEK-293 packaging cells, Gene Ther, 21, 629, 10.1038/gt.2014.40 Wei, 2017, Engineering the rapid adenovirus production and amplification (RAPA) cell line to expedite the generation of recombinant adenoviruses, Cell Physiol Biochem, 41, 2383, 10.1159/000475909 Lu, 2016, Bone morphogenetic protein 9 (BMP9) induces effective bone formation from reversibly immortalized multipotent adipose-derived (iMAD) mesenchymal stem cells, Am J Transl Res, 8, 3710 Zhao, 2017, Sox9 augments BMP2-induced chondrogenic differentiation by downregulating Smad7 in mesenchymal stem cells (MSCs), Genes Dis, 4, 229, 10.1016/j.gendis.2017.10.004 Hu, 2017, CRISPR/Cas9-mediated reversibly immortalized mouse bone marrow stromal stem cells (BMSCs) retain multipotent features of mesenchymal stem cells (MSCs), Oncotarget, 8, 111847, 10.18632/oncotarget.22915 Liao, 2017, Characterization of retroviral infectivity and superinfection resistance during retrovirus-mediated transduction of mammalian cells, Gene Ther, 24, 333, 10.1038/gt.2017.24 Huang, 2009, Retinoic acid signalling induces the differentiation of mouse fetal liver-derived hepatic progenitor cells, Liver Int, 29, 1569, 10.1111/j.1478-3231.2009.02111.x He, 1998, A simplified system for generating recombinant adenoviruses, Proc Natl Acad Sci U S A, 95, 2509, 10.1073/pnas.95.5.2509 Luo, 2007, A protocol for rapid generation of recombinant adenoviruses using the AdEasy system, Nat Protoc, 2, 1236, 10.1038/nprot.2007.135 Lee, 2017, Adenovirus-mediated gene delivery: potential applications for gene and cell-based therapies in the new era of personalized medicine, Genes Dis, 4, 43, 10.1016/j.gendis.2017.04.001 Fan, 2017, Noncanonical Wnt signaling plays an important role in modulating canonical Wnt-regulated stemness, proliferation and terminal differentiation of hepatic progenitors, Oncotarget, 8, 27105, 10.18632/oncotarget.15637 Song, 2017, BMP9 induces osteogenesis and adipogenesis in the immortalized human cranial suture progenitors from the patent sutures of craniosynostosis patients, J Cell Mol Med, 21, 2782, 10.1111/jcmm.13193 Wang, 2014, Adenovirus-mediated efficient gene transfer into cultured three-dimensional organoids, PLoS One, 9, e93608, 10.1371/journal.pone.0093608 Wang, 2014, The piggyBac transposon-mediated expression of SV40 T antigen efficiently immortalizes mouse embryonic fibroblasts (MEFs), PLoS One, 9, e97316, 10.1371/journal.pone.0097316 Zhao, 2014, Adenovirus-mediated gene transfer in mesenchymal stem cells can be significantly enhanced by the cationic polymer polybrene, PLoS One, 9, e92908, 10.1371/journal.pone.0092908 Zhang, 2015, TqPCR: a touchdown qPCR assay with significantly improved detection sensitivity and amplification efficiency of SYBR Green qPCR, PLoS One, 10, e0132666, 10.1371/journal.pone.0132666 Ye, 2016, A thermoresponsive polydiolcitrate-gelatin scaffold and delivery system mediates effective bone formation from BMP9-transduced mesenchymal stem cells, Biomed Mater, 11, 025021, 10.1088/1748-6041/11/2/025021 Li, 2015, The calcium-binding protein S100A6 accelerates human osteosarcoma growth by promoting cell proliferation and inhibiting osteogenic differentiation, Cell Physiol Biochem, 37, 2375, 10.1159/000438591 Li, 2016, The prodomain-containing BMP9 produced from a stable line effectively regulates the differentiation of mesenchymal stem cells, Int J Med Sci, 13, 8, 10.7150/ijms.13333 Huang, 2012, Conditionally immortalized mouse embryonic fibroblasts retain proliferative activity without compromising multipotent differentiation potential, PLoS One, 7, e32428, 10.1371/journal.pone.0032428 Huang, 2012, Growth hormone synergizes with BMP9 in osteogenic differentiation by activating the JAK/STAT/IGF1 pathway in murine multilineage cells, J Bone Miner Res, 27, 1566, 10.1002/jbmr.1622 Tang, 2009, BMP9-induced osteogenic differentiation of mesenchymal progenitors requires functional canonical Wnt/beta-catenin signaling, J Cell Mol Med, 13, 2448, 10.1111/j.1582-4934.2008.00569.x Zhang, 2015, Canonical Wnt signaling acts synergistically on BMP9-induced osteo/odontoblastic differentiation of stem cells of dental apical papilla (SCAPs), Biomaterials, 39, 145, 10.1016/j.biomaterials.2014.11.007 Liu, 2013, Cross-talk between EGF and BMP9 signalling pathways regulates the osteogenic differentiation of mesenchymal stem cells, J Cell Mol Med, 17, 1160, 10.1111/jcmm.12097 Wang, 2017, Nel-like Molecule-1 (Nell1) is regulated by bone morphogenetic protein 9 (BMP9) and potentiates BMP9-induced osteogenic differentiation at the expense of adipogenesis in mesenchymal stem cells, Cell Physiol Biochem, 41, 484, 10.1159/000456885 Wang, 2014, Bone morphogenetic Protein-9 (BMP9) effectively induces osteo/odontoblastic differentiation of the reversibly immortalized stem cells of dental apical papilla, Stem Cell Dev, 23, 1405, 10.1089/scd.2013.0580 Kang, 2009, A comprehensive analysis of the dual roles of BMPs in regulating adipogenic and osteogenic differentiation of mesenchymal progenitor cells, Stem Cell Dev, 18, 545, 10.1089/scd.2008.0130 Li, 2014, Targeting BMP9-promoted human osteosarcoma growth by inactivation of notch signaling, Curr Cancer Drug Targets, 14, 274, 10.2174/1568009614666140305105805 Luo, 2010, TGFbeta/BMP type I receptors ALK1 and ALK2 are essential for BMP9-induced osteogenic signaling in mesenchymal stem cells, J Biol Chem, 285, 29588, 10.1074/jbc.M110.130518 Hu, 2013, BMP9-regulated angiogenic signaling plays an important role in the osteogenic differentiation of mesenchymal progenitor cells, J Cell Sci, 126, 532, 10.1242/jcs.114231 Chen, 2010, Insulin-like growth factor 2 (IGF-2) potentiates BMP-9-induced osteogenic differentiation and bone formation, J Bone Miner Res, 25, 2447, 10.1002/jbmr.133 Zhang, 2017, Anthelmintic mebendazole enhances cisplatin's effect on suppressing cell proliferation and promotes differentiation of head and neck squamous cell carcinoma (HNSCC), Oncotarget, 8, 12968, 10.18632/oncotarget.14673 Zhang, 2013, Endoplasmic reticulum (ER) stress inducible factor cysteine-rich with EGF-like domains 2 (Creld2) is an important mediator of BMP9-regulated osteogenic differentiation of mesenchymal stem cells, PLoS One, 8, e73086, 10.1371/journal.pone.0073086 Gao, 2013, Crosstalk between Wnt/beta-catenin and estrogen receptor signaling synergistically promotes osteogenic differentiation of mesenchymal progenitor cells, PLoS One, 8, e82436, 10.1371/journal.pone.0082436 Song, 1995, Bone morphogenetic protein-9 binds to liver cells and stimulates proliferation, Endocrinology, 136, 4293, 10.1210/endo.136.10.7664647 Wang, 2013, Noggin resistance contributes to the potent osteogenic capability of BMP9 in mesenchymal stem cells, J Orthop Res, 31, 1796, 10.1002/jor.22427 Peng, 2003, Transcriptional characterization of bone morphogenetic proteins (BMPs)-mediated osteogenic signaling, J Cell Biochem, 90, 1149, 10.1002/jcb.10744 Peng, 2004, Inhibitor of DNA binding/differentiation helix-loop-helix proteins mediate bone morphogenetic protein-induced osteoblast differentiation of mesenchymal stem cells, J Biol Chem, 279, 32941, 10.1074/jbc.M403344200 Luo, 2004, Connective tissue growth factor (CTGF) is regulated by Wnt and bone morphogenetic proteins signaling in osteoblast differentiation of mesenchymal stem cells, J Biol Chem, 279, 55958, 10.1074/jbc.M407810200 Sharff, 2009, Hey1 basic helix-loop-helix protein plays an important role in mediating BMP9-induced osteogenic differentiation of mesenchymal progenitor cells, J Biol Chem, 284, 649, 10.1074/jbc.M806389200 Zhang, 2010, Retinoic acids potentiate BMP9-induced osteogenic differentiation of mesenchymal progenitor cells, PLoS One, 5, e11917, 10.1371/journal.pone.0011917 Zhang, 2015, Activation of PKA/CREB signaling is involved in BMP9-induced osteogenic differentiation of mesenchymal stem cells, Cell Physiol Biochem, 37, 548, 10.1159/000430376 Fellmann, 2014, Stable RNA interference rules for silencing, Nat Cell Biol, 16, 10, 10.1038/ncb2895 Breyer, 2001, Adenoviral vector-mediated gene transfer for human gene therapy, Curr Gene Ther, 1, 149, 10.2174/1566523013348689 Hsu, 2014, Development and applications of CRISPR-Cas9 for genome engineering, Cell, 157, 1262, 10.1016/j.cell.2014.05.010 Doudna, 2014, Genome editing. The new frontier of genome engineering with CRISPR-Cas9, Science., 346, 1258096, 10.1126/science.1258096 Dominguez, 2016, Beyond editing: repurposing CRISPR-Cas9 for precision genome regulation and interrogation, Nat Rev Mol Cell Biol, 17, 5, 10.1038/nrm.2015.2 Kim, 2014, A guide to genome engineering with programmable nucleases, Nat Rev Genet, 15, 321, 10.1038/nrg3686 Zhang, 2014, CRISPR clear? Dimeric Cas9-Fok1 nucleases improve genome-editing specificity, Genes Dis, 1, 6, 10.1016/j.gendis.2014.08.004 Mali, 2013, Cas9 as a versatile tool for engineering biology, Nat Methods, 10, 957, 10.1038/nmeth.2649 Ran, 2013, Genome engineering using the CRISPR-Cas9 system, Nat Protoc, 8, 2281, 10.1038/nprot.2013.143 Sander, 2015, CRISPR-Cas systems for editing, regulating and targeting genomes, Nat Biotechnol, 32, 347, 10.1038/nbt.2842 Wang, 2016, CRISPR/Cas9 in genome editing and beyond, Annu Rev Biochem, 85, 227, 10.1146/annurev-biochem-060815-014607