Roles of circular RNAs in osteogenic differentiation of bone marrow mesenchymal stem cells (Review)
- Authors:
- Jicheng Wang
- Tengyun Wang
- Fujie Zhang
- Yangyang Zhang
- Yongzhi Guo
- Xin Jiang
- Bo Yang
-
Affiliations: Department of Joint Surgery, Weifang People's Hospital, Weifang, Shandong 261000, P.R. China - Published online on: May 20, 2022 https://doi.org/10.3892/mmr.2022.12743
- Article Number: 227
-
Copyright: © Wang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Friedenstein AJ, Chailakhyan RK and Gerasimov UV: Bone marrow osteogenic stem cells: In vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet. 20:263–272. 1987. | |
Kim N and Cho SG: Clinical applications of mesenchymal stem cells. Korean J Intern Med. 28:387–402. 2013. View Article : Google Scholar : PubMed/NCBI | |
Alves H, Mentink A, Le B, van Blitterswijk CA and de Boer J: Effect of antioxidant supplementation on the total yield, oxidative stress levels, and multipotency of bone marrow-derived human mesenchymal stromal cells. Tissue Eng Part A. 19:928–937. 2013. View Article : Google Scholar : PubMed/NCBI | |
Ren C, Gong W, Li F and Xie M: Pilose antler aqueous extract promotes the proliferation and osteogenic differentiation of bone marrow mesenchymal stem cells by stimulating the BMP-2/Smad1, 5/Runx2 signaling pathway. Chin J Nat Med. 17:756–767. 2019.PubMed/NCBI | |
Furuta T, Miyaki S, Ishitobi H, Ogura T, Kato Y, Kamei N, Miyado K, Higashi Y and Ochi M: Mesenchymal stem cell-derived exosomes promote fracture healing in a mouse model. Stem Cells Transl Med. 5:1620–1630. 2016. View Article : Google Scholar : PubMed/NCBI | |
Watanabe Y, Tsuchiya A, Seino S, Kawata Y, Kojima Y, Ikarashi S, Starkey Lewis PJ, Lu WY, Kikuta J, Kawai H, et al: Mesenchymal stem cells and induced bone marrow-derived macrophages synergistically improve liver fibrosis in mice. Stem Cells Transl Med. 8:271–284. 2019. View Article : Google Scholar : PubMed/NCBI | |
Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G and Mavilio F: Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 279:1528–1530. 1998. View Article : Google Scholar : PubMed/NCBI | |
Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, Boggs SS, Greenberger JS and Goff JP: Bone marrow as a potential source of hepatic oval cells. Science. 284:1168–1170. 1999. View Article : Google Scholar : PubMed/NCBI | |
Sanchez-Ramos J, Song S, Cardozo-Pelaez F, Hazzi C, Stedeford T, Willing A, Freeman TB, Saporta S, Janssen W, Patel N, et al: Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol. 164:247–256. 2000. View Article : Google Scholar | |
Owen M and Friedenstein AJ: Stromal stem cells: Marrow-derived osteogenic precursors. Ciba Found Symp. 136:42–60. 1988.PubMed/NCBI | |
Prockop DJ: Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 276:71–74. 1997. View Article : Google Scholar : PubMed/NCBI | |
Lasda E and Parker R: Circular RNAs: Diversity of form and function. RNA. 20:1829–1842. 2014. View Article : Google Scholar : PubMed/NCBI | |
Yu CX and Sun S: An emerging role for circular RNAs in osteoarthritis. Yonsei Med J. 59:349–355. 2018. View Article : Google Scholar : PubMed/NCBI | |
Sanger HL, Klotz G, Riesner D, Gross HJ and Kleinschmidt AK: Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc Natl Acad Sci USA. 73:3852–3856. 1976. View Article : Google Scholar : PubMed/NCBI | |
Hsu MT and Coca-Prados M: Electron microscopic evidence for the circular form of RNA in the cytoplasm of eukaryotic cells. Nature. 280:339–340. 1979. View Article : Google Scholar : PubMed/NCBI | |
Kos A, Dijkema R, Arnberg AC, van der Meide PH and Schellekens H: The hepatitis delta (delta) virus possesses a circular RNA. Nature. 323:558–560. 1986. View Article : Google Scholar : PubMed/NCBI | |
Salzman J, Gawad C, Wang PL, Lacayo N and Brown PO: Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS One. 7:e307332012. View Article : Google Scholar : PubMed/NCBI | |
Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, Marzluff WF and Sharpless NE: Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA. 19:141–157. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hou LD and Zhang J: Circular RNAs: An emerging type of RNA in cancer. Int J Immunopathol Pharmacol. 30:1–6. 2017. View Article : Google Scholar | |
Chen LL and Yang L: Regulation of circRNA biogenesis. RNA Biol. 12:381–388. 2015. View Article : Google Scholar | |
Vicens Q and Westhof E: Biogenesis of circular RNAs. Cell. 159:13–14. 2014. View Article : Google Scholar | |
Wang Y and Wang Z: Efficient backsplicing produces translatable circular mRNAs. RNA. 21:172–179. 2015. View Article : Google Scholar : PubMed/NCBI | |
Chen I, Chen CY and Chuang TJ: Biogenesis, identification, and function of exonic circular RNAs. Wiley Interdiscip Rev RNA. 6:563–579. 2015. View Article : Google Scholar : PubMed/NCBI | |
Li Z, Huang C, Bao C, Chen L, Lin M, Wang X, Zhong G, Yu B, Hu W, Dai L, et al: Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol. 22:256–264. 2015. View Article : Google Scholar | |
Zhang Y, Zhang XO, Chen T, Xiang JF, Yin QF, Xing YH, Zhu S, Yang L and Chen LL: Circular intronic long noncoding RNAs. Mol Cell. 51:792–806. 2013. View Article : Google Scholar | |
Conn SJ, Pillman KA, Toubia J, Conn VM, Salmanidis M, Phillips CA, Roslan S, Schreiber AW, Gregory PA and Goodall GJ: The RNA binding protein quaking regulates formation of circRNAs. Cell. 160:1125–1134. 2015. View Article : Google Scholar | |
Ashwal-Fluss R, Meyer M, Pamudurti NR, Ivanov A, Bartok O, Hanan M, Evantal N, Memczak S, Rajewsky N and Kadener S: circRNA biogenesis competes with pre-mRNA splicing. Mol Cell. 56:55–66. 2014. View Article : Google Scholar | |
Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, et al: Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 495:333–338. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK and Kjems J: Natural RNA circles function as efficient microRNA sponges. Nature. 495:384–388. 2013. View Article : Google Scholar : PubMed/NCBI | |
You X, Vlatkovic I, Babic A, Will T, Epstein I, Tushev G, Akbalik G, Wang M, Glock C, Quedenau C, et al: Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nat Neurosci. 18:603–610. 2015. View Article : Google Scholar | |
Huang S, Yang B, Chen BJ, Bliim N, Ueberham U, Arendt T and Janitz M: The emerging role of circular RNAs in transcriptome regulation. Genomics. 109:401–407. 2017. View Article : Google Scholar : PubMed/NCBI | |
Chen X, Han P, Zhou T, Guo X, Song X and Li Y: circRNADb: A comprehensive database for human circular RNAs with protein-coding annotations. Sci Rep. 6:349852016. View Article : Google Scholar : PubMed/NCBI | |
Granados-Riveron JT and Aquino-Jarquin G: The complexity of the translation ability of circRNAs. Biochim Biophys Acta. 1859:1245–1251. 2016. View Article : Google Scholar | |
Ebert MS and Sharp PA: MicroRNA sponges: Progress and possibilities. RNA. 16:2043–2050. 2010. View Article : Google Scholar : PubMed/NCBI | |
Abdelmohsen K, Kuwano Y, Kim HH and Gorospe M: Posttranscriptional gene regulation by RNA-binding proteins during oxidative stress: Implications for cellular senescence. Biol Chem. 389:243–255. 2008. View Article : Google Scholar : PubMed/NCBI | |
Yin QF, Yang L, Zhang Y, Xiang JF, Wu YW, Carmichael GG and Chen LL: Long noncoding RNAs with snoRNA ends. Mol Cell. 48:219–230. 2012. View Article : Google Scholar | |
Qu S, Yang X, Li X, Wang J, Gao Y, Shang R, Sun W, Dou K and Li H: Circular RNA: A new star of noncoding RNAs. Cancer Lett. 365:141–148. 2015. View Article : Google Scholar | |
Chen CY and Sarnow P: Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science. 268:415–417. 1995. View Article : Google Scholar : PubMed/NCBI | |
Yang Y, Fan X, Mao M, Song X, Wu P, Zhang Y, Jin Y, Yang Y, Chen LL, Wang Y, et al: Extensive translation of circular RNAs driven by N6-methyladenosine. Cell Res. 27:626–641. 2017. View Article : Google Scholar : PubMed/NCBI | |
Pamudurti NR, Bartok O, Jens M, Ashwal-Fluss R, Stottmeister C, Ruhe L, Hanan M, Wyler E, Perez-Hernandez D, Ramberger E, et al: Translation of CircRNAs. Mol Cell. 66:9–21.e7. 2017. View Article : Google Scholar | |
Lin Z, Tang X, Wan J, Zhang X, Liu C and Liu T: Functions and mechanisms of circular RNAs in regulating stem cell differentiation. RNA Biol. 18:2136–2149. 2021. View Article : Google Scholar | |
Fu M, Fang L, Xiang X, Fan X, Wu J and Wang J: Microarray analysis of circRNAs sequencing profile in exosomes derived from bone marrow mesenchymal stem cells in postmenopausal osteoporosis patients. J Clin Lab Anal. 36:e239162022. View Article : Google Scholar | |
Zhang Y, Jia S, Wei Q, Zhuang Z, Li J, Fan Y, Zhang L, Hong Z, Ma X, Sun R, et al: CircRNA_25487 inhibits bone repair in trauma-induced osteonecrosis of femoral head by sponging miR-134-3p through p21. Regen Ther. 16:23–31. 2020. View Article : Google Scholar : PubMed/NCBI | |
Chen W, Zhang B and Chang X: Emerging roles of circular RNAs in osteoporosis. J Cell Mol Med. 25:9089–9101. 2021. View Article : Google Scholar : PubMed/NCBI | |
Zhang M, Jia L and Zheng Y: circRNA expression profiles in human bone marrow stem cells undergoing osteoblast differentiation. Stem Cell Rev Rep. 15:126–138. 2019. View Article : Google Scholar : PubMed/NCBI | |
Chen G, Wang Q, Li Z, Yang Q, Liu Y, Du Z, Zhang G and Song Y: Circular RNA CDR1as promotes adipogenic and suppresses osteogenic differentiation of BMSCs in steroid-induced osteonecrosis of the femoral head. Bone. 133:1152582020. View Article : Google Scholar : PubMed/NCBI | |
Rademacher S and Eickholt BJ: PTEN in Autism and neurodevelopmental disorders. Cold Spring Harb Perspect Med. 9:a0367802019. View Article : Google Scholar : PubMed/NCBI | |
Kuang MJ, Xing F, Wang D, Sun L, Ma JX and Ma XL: CircUSP45 inhibited osteogenesis in glucocorticoid-induced osteonecrosis of femoral head by sponging miR-127-5p through PTEN/AKT signal pathway: Experimental studies. Biochem Biophys Res Commun. 509:255–261. 2019. View Article : Google Scholar : PubMed/NCBI | |
Geng Y, Chen J, Chang C, Zhang Y, Duan L, Zhu W, Mou L, Xiong J and Wang D: Systematic analysis of mRNAs and ncRNAs in BMSCs of senile osteoporosis patients. Front Genet. 12:7769842021. View Article : Google Scholar | |
Seppala M, Thivichon-Prince B, Xavier GM, Shaffie N, Sangani I, Birjandi AA, Rooney J, Lau JNS, Dhaliwal R, Rossi O, et al: Gas1 regulates patterning of the murine and human dentitions through sonic hedgehog. J Dent Res. 101:473–482. 2022. View Article : Google Scholar : PubMed/NCBI | |
Wang X, Chen T, Deng Z, Gao W, Liang T, Qiu X, Gao B, Wu Z, Qiu J, Zhu Y, et al: Melatonin promotes bone marrow mesenchymal stem cell osteogenic differentiation and prevents osteoporosis development through modulating circ_0003865 that sponges miR-3653-3p. Stem Cell Res Ther. 12:1502021. View Article : Google Scholar : PubMed/NCBI | |
Xiang S, Li Z and Weng X: Changed cellular functions and aberrantly expressed miRNAs and circRNAs in bone marrow stem cells in osteonecrosis of the femoral head. Int J Mol Med. 45:805–815. 2020.PubMed/NCBI | |
Komori T: Roles of Runx2 in skeletal development. Adv Exp Med Biol. 962:83–93. 2017. View Article : Google Scholar | |
Komori T: Regulation of proliferation, differentiation and functions of osteoblasts by Runx2. Int J Mol Sci. 20:16942019. View Article : Google Scholar | |
Ji H, Cui X, Yang Y and Zhou X: CircRNA hsa_circ_0006215 promotes osteogenic differentiation of BMSCs and enhances osteogenesis-angiogenesis coupling by competitively binding to miR-942-5p and regulating RUNX2 and VEGF. Aging (Albany NY). 13:10275–10288. 2021. View Article : Google Scholar : PubMed/NCBI | |
Cao G, Meng X, Han X and Li J: Exosomes derived from circRNA Rtn4-modified BMSCs attenuate TNF-α-induced cytotoxicity and apoptosis in murine MC3T3-E1 cells by sponging miR-146a. Biosci Rep. 40:BSR201934362020. View Article : Google Scholar : PubMed/NCBI | |
Mikami R, Mizutani K, Aoki A, Tamura Y, Aoki K and Izumi Y: Low-level ultrahigh-frequency and ultrashort-pulse blue laser irradiation enhances osteoblast extracellular calcification by upregulating proliferation and differentiation via transient receptor potential vanilloid 1. Lasers Surg Med. 50:340–352. 2018. View Article : Google Scholar : PubMed/NCBI | |
Rosa AP, de Sousa LG, Regalo SC, Issa JP, Barbosa AP, Pitol DL, de Oliveira RH, de Vasconcelos PB, Dias FJ, Chimello DT and Siéssere S: Effects of the combination of low-level laser irradiation and recombinant human bone morphogenetic protein-2 in bone repair. Lasers Med Sci. 27:971–977. 2012. View Article : Google Scholar | |
Hou JF, Zhang H, Yuan X, Li J, Wei YJ and Hu SS: In vitro effects of low-level laser irradiation for bone marrow mesenchymal stem cells: Proliferation, growth factors secretion and myogenic differentiation. Lasers Surg Med. 40:726–733. 2008. View Article : Google Scholar : PubMed/NCBI | |
Abramovitch-Gottlib L, Gross T, Naveh D, Geresh S, Rosenwaks S, Bar I and Vago R: Low level laser irradiation stimulates osteogenic phenotype of mesenchymal stem cells seeded on a three-dimensional biomatrix. Lasers Med Sci. 20:138–146. 2005. View Article : Google Scholar | |
Kipshidze N, Nikolaychik V, Keelan MH, Shankar LR, Khanna A, Kornowski R, Leon M and Moses J: Low-power helium: Neon laser irradiation enhances production of vascular endothelial growth factor and promotes growth of endothelial cells in vitro. Lasers Surg Med. 28:355–364. 2001. View Article : Google Scholar : PubMed/NCBI | |
Liu N, Lu W, Qu X and Zhu C: LLLI promotes BMSC proliferation through circRNA_0001052/miR-124-3p. Lasers Med Sci. 37:849–856. 2022. View Article : Google Scholar | |
Zheng J, Lin Y, Tang F, Guo H, Yan L, Hu S and Wu H: Promotive role of CircATRNL1 on chondrogenic differentiation of BMSCs mediated by miR-338-3p. Arch Med Res. 52:514–522. 2021. View Article : Google Scholar : PubMed/NCBI | |
Wen X, Zhang J, Yang W, Nie X, Gui R, Shan D, Huang R and Deng H: CircRNA-016901 silencing attenuates irradiation-induced injury in bone mesenchymal stem cells via regulating the miR-1249-5p/HIPK2 axis. Exp Ther Med. 21:3552021. View Article : Google Scholar : PubMed/NCBI | |
Li X, Chen R, Lei X, Wang P, Zhu X, Zhang R and Yang L: Quercetin regulates ERα mediated differentiation of BMSCs through circular RNA. Gene. 769:1451722021. View Article : Google Scholar : PubMed/NCBI | |
Zhao YS, Lin P, Tu YC, An T, Wu YP and Li XF: Lentivirus mediated siRNA hsa-circ-0000885 transfection of BMSCs and osteoclast co-culture system on cell differentiation, proliferation and apoptosis. Zhongguo Gu Shang. 34:978–984. 2021.(In Chinese). PubMed/NCBI | |
Wang H, Zhou K, Xiao F, Huang Z, Xu J, Chen G, Liu Y and Gu H: Identification of circRNA-associated ceRNA network in BMSCs of OVX models for postmenopausal osteoporosis. Sci Rep. 10:108962020. View Article : Google Scholar : PubMed/NCBI | |
Lin C, Chen Z, Guo D, Zhou L, Lin S, Li C..Li S, Wang X, Lin B and Ding Y: Increased expression of osteopontin in subchondral bone promotes bone turnover and remodeling, and accelerates the progression of OA in a mouse model. Aging (Albany NY). 14:253–271. 2022. View Article : Google Scholar : PubMed/NCBI | |
Liu Z, Liu Q, Chen S, Su H and Jing T: Circular RNA Circ_0005564 promotes osteogenic differentiation of bone marrow mesenchymal cells in osteoporosis. Bioengineered. 12:4911–4923. 2021. View Article : Google Scholar : PubMed/NCBI | |
Chia W, Liu J, Huang YG and Zhang C: A circular RNA derived from DAB1 promotes cell proliferation and osteogenic differentiation of BMSCs via RBPJ/DAB1 axis. Cell Death Dis. 11:3722020. View Article : Google Scholar : PubMed/NCBI | |
Zhong W, Li X, Pathak JL, Chen L, Cao W, Zhu M, Luo Q, Wu A, Chen Y, Yi L, et al: Dicalcium silicate microparticles modulate the differential expression of circRNAs and mRNAs in BMSCs and promote osteogenesis via circ_1983-miR-6931-Gas7 interaction. Biomater Sci. 8:3664–3677. 2020. View Article : Google Scholar | |
Hao Y, Lu C, Zhang B, Xu Z, Guo H and Zhang G: CircPVT1 up-regulation attenuates steroid-induced osteonecrosis of the femoral head through regulating miR-21-5p-mediated Smad7/TGFβ signalling pathway. J Cell Mol Med. 25:4608–4622. 2021. View Article : Google Scholar : PubMed/NCBI | |
Zhou R, Miao S, Xu J, Sun L and Chen Y: Circular RNA circ_0000020 promotes osteogenic differentiation to reduce osteoporosis via sponging microRNA miR-142-5p to up-regulate bone morphogenetic protein BMP2. Bioengineered. 12:3824–3836. 2021. View Article : Google Scholar : PubMed/NCBI |