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Functions of CircRNAs in osteogenic differentiation

Published on Feb. 20, 2021Total Views: 4004 timesTotal Downloads: 2101 timesDownloadMobile

Author: Hui-Xian DONG 1, 2 Jia-Lin ZHONG 1, 2 Qian-Zhou JIANG 1, 2

Affiliation: 1. Department of Endodontics, Affiliated Stomatology Hospital of Guangzhou Medical University, Guangzhou 510182, China 2. Guangzhou Key Laboratory of Basic and Applied Research of Oral Regenerative Medicine, Guangzhou 510182, China

Keywords: CircRNAs Osteogenesis Differentiation Regulation

DOI: 10.12173/j.issn.1004-5511.2021.01.04

Reference: Dong HX, Zhong JL, Jiang QZ. Functions of CircRNAs in osteogenic differentiation[J]. Yixue Xinzhi Zhazhi, 2021, 31(1): 23-32. DOI: 10.12173/j.issn.1004-5511.2021.01.04.[Article in Chinese]

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Abstract

CircRNAs are a special class of non-coding RNA (ncRNA) molecules. They have a closed circular structure and are formed by reverse splicing by non-classical splicing methods. They coexist in highly differentiated eukaryotes. More and more studies have shown that CircRNAs would change during osteogenic differentiation. This paper introduces the role of CircRNAs in tissue cell osteogenic differentiation, and reviews the current research status of the targets and signaling pathways of CircRNAs during osteogenic differentiation.

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References

1. Cocquerelle C, Mascrez B, Hétuin D, et al. Mis-splicing yields circular RNA molecules[J]. FASEB J, 1993, 7(1):155-160. DOI: 10.1096/fasebj.7.1.7678559. 

2. Sanger HL, Klotz G, Riesner D, et al. Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures[J]. Proc Natl Acad Sci USA, 1976, 73(11): 3852-3856. DOI: 10.1073/pnas.73.11.3852.

3. Jeck WR, Sorrentino JA, Wang K, et al. Circular RNAs are abundant, conserved, and associated with ALU repeats[J]. RNA, 2013, 19(2): 141-157. DOI: 10.1261/rna. 035667.112. 

4. Glažar P, Papavasileiou P, Rajewsky N. CircBase: a database for circular RNAs[J]. RNA, 2014, 20(11): 1666-1670. DOI: 10.1261/rna.043687.113.

5. Rybak-Wolf A, Stottmeister C, Glažar P, et al. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed[J]. Mol Cell, 2015, 58(5): 870-885. DOI: 10.1016/j.molcel.2015.03.027.

6. Yu CY, Li TC, Wu YY, et al. The circular RNA circBIRC6 participates in the molecular circuitry controlling human pluripotency[J]. Nat Commun, 2017, 8(1): 1149. DOI: 10.1038/s41467-017-01216-w.

7. You X, Vlatkovic I, Babic A, et al. Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity[J]. Nat Neurosci, 2015, 18(4): 603-610. DOI: 10.1038/nn.3975.

8. Han D, Li J, Wang H, et al. Circular RNA circMTO1 acts as the sponge of microRNA-9 to suppress hepatocellular carcinoma progression[J]. Hepatology, 2017, 66(4): 1151-1164. DOI: 10.1002/hep.29270.

9. Kristensen LS, Okholm TLH, Venø MT, et al. Circular RNAs are abundantly expressed and upregulated during human epidermal stem cell differentiation[J]. RNA Biol, 2018, 15(2): 280-291. DOI: 10.1080/15476286.2017.1409931.

10.  Du Y, Li J, Hou Y, et al. Alteration of circular RNA expression in rat dental follicle cells during osteogenic differentiation[J]. J Cell Biochem, 2019, 120(8): 13289-13301. DOI: 10.1002/jcb.28603.

11.  Peng W, Zhu S, Chen J, et al. Hsa_circRNA_33287 promotes the osteogenic differentiation of maxillary sinus membrane stem cells via miR-214-3p/Runx3[J]. Biomed Pharmacother, 2019, 109: 1709-1717. DOI: 10.1016/j.biopha.2018.10.159.

12.  Qian DY, Yan GB, Bai B, et al. Differential circRNA expression profiles during the BMP2-induced osteogenic differentiation of MC3T3-E1 cells[J]. Biomed Pharmacother, 2017, 90: 492-499. DOI: 10.1016/j.biopha. 2017.03.051.

13.  Zheng Y, Li X, Huang Y, et al. The circular RNA landscape of periodontal ligament stem cells during osteogenesis[J]. J Periodontol, 2017, 88(9): 906-914. DOI: 10.1902/jop.2017.170078.

14.  Meng S, Zhou H, Feng Z, et al. CircRNA: functions and properties of a novel potential biomarker for cancer[J]. Mol Cancer, 2017, 16(1): 94. DOI: 10.1186/s12943-017-0663-2.

15.  Li X, Yang L, Chen LL. The biogenesis, functions, and challenges of circular RNAs[J]. Mol Cell, 2018, 71(3): 428-442. DOI: 10.1016/j.molcel.2018.06.034.

16.  Wesselhoeft RA, Kowalski PS, Anderson DG. Engineering circular RNA for potent and stable translation in eukaryotic cells[J]. Nat Commun, 2018, 9(1): 2629. DOI: 10.1038/s41 467-018-05096-6.

17.  Liang D, Wilusz JE. Short intronic repeat sequences facilitate circular RNA production[J]. Genes Dev, 2014, 28(20): 2233-2247. DOI: 10.1101/gad.251926.114.

18.  Dong R, Ma XK, Chen LL, et al. Increased complexity of circRNA expression during species evolution[J]. RNA Biol, 2017, 14(8): 1064-1074. DOI: 10.1080/15476286.2016.1269999.

19.  Werfel S, Nothjunge S, Schwarzmayr T, et al. Characterization of circular RNAs in human, mouse and rat hearts[J]. J Mol Cell Cardiol, 2016, 98: 103-107. DOI: 10.1016/j.yjmcc.2016.07.007.

20.  Chen W, Schuman E. Circular RNAs in brain and other tissues: a functional enigma[J]. Trends Neurosci, 2016, 39(9): 597-604. DOI: 10.1016/j.tins.2016.06.006.

21.  Bianco P, Cao X, Frenette PS, et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine[J]. Nat Med, 2013, 19(1): 35-42. DOI: 10.1038/nm.3028.

22.  Yousefi AM, James PF, Akbarzadeh R, et al. Prospect of stem cells in bone tissue engineering: a review[J]. Stem Cells Int, 2016, 2016: 6180487. DOI: 10.1155/2016/ 6180487.

23.  Zhang W, Dong R, Diao S, et al. Differential long noncoding RNA/mRNA expression profiling and functional network analysis during osteogenic differentiation of human bone marrow mesenchymal stem cells[J]. Stem Cell Res Ther, 2017, 8(1): 30. DOI: 10.1186/s13287-017-0485-6.

24.  Wu Y, Lian K, Sun C. LncRNA LEF1-AS1 promotes osteogenic differentiation of dental pulp stem cells via sponging miR-24-3p[J]. Mol Cell Biochem, 2020, 475(1-2): 161-169. DOI: 10.1007/s11010-020-03868-7.

25.  Li M, Cong R, Yang L, et al. A novel lncRNA LNC_000052 leads to the dysfunction of osteoporotic BMSCs via the miR-96-5p–PIK3R1 axis[J]. Cell Death Dis, 2020, 11(9): 795. DOI: 10.1038/s41419-020-03006-7.

26.  Wen J, Guan Z, Yu B, et al. Circular RNA hsa_circ_0076906 competes with OGN for miR-1305 biding site to alleviate the progression of osteoporosis[J]. Int J Biochem Cell Biol, 2020, 122: 105719. DOI: 10.1016/j.biocel.2020.105719.

27.  Yang L, Zeng Z, Kang N, et al. Circ-VANGL1 promotes the progression of osteoporosis by absorbing miRNA-217 to regulate RUNX2 expression[J]. Eur Rev Med Pharmacol Sci, 2019, 23(3): 949-957. DOI: 10.26355/eurrev_201902_16981.

28.  Xu X, Chen Y, Tan B, et al. Circular RNA circ_0011269 sponges miR-122 to regulate RUNX2 expression and promotes osteoporosis progression[J]. J Cell Biochem, 2020, 121(12): 4819-4826. DOI: 10.1002/jcb.29709.

29.  Yu L, Liu Y. CircRNA_0016624 could sponge miR-98 to regulate BMP2 expression in postmenopausal osteoporosis[J]. Biochem Biophys Res Commun, 2019, 516(2): 546-550. DOI: 10.1016/j.bbrc.2019.06.087.

30.  Yin Q, Wang J, Fu Q, et al. CircRUNX2 through has‐miR‐203 regulates RUNX2 to prevent osteoporosis[J]. J Cell Mol Med, 2018, 22(12): 6112-6121. DOI: 10.1111/jcmm.13888.

31.  Han S, Kuang M, Sun C, et al. Circular RNA hsa_circ_0076690 acts as a prognostic biomarker in osteoporosis and regulates osteogenic differentiation of hBMSCs via sponging miR-152[J]. Aging (Albany NY),  2020, 12(14): 15011-15020. DOI: 10.18632/aging.103560. 

32.  Huang Y, Xiao D, Huang S, et al. Circular RNA YAP1 attenuates osteoporosis through up-regulation of YAP1 and activation of Wnt/beta-catenin pathway[J]. Biomed Pharmacother, 2020, 129: 110365. DOI: 10.1016/j.biopha.2020.110365.

33.  Wang XB, Li PB, Guo SF, et al. CircRNA_0006393 promotes osteogenesis in glucocorticoidinduced osteoporosis by sponging miR1455p and upregulating FOXO1[J]. Mol Med Rep, 2019, 20(3): 2851-2858. DOI: 10.3892/mmr.2019.10497.

34.  Zhong W , Li X , Pathak JL, 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[J]. Biomater Sci, 2020, 8(13): 3664-3677. DOI: 10.1039/d0bm00459f.

35.  Ouyang Z, Tan T, Zhang X, et al. CircRNA hsa_circ_0074834 promotes the osteogenesis-angiogenesis coupling process in bone mesenchymal stem cells (BMSCs) by acting as a ceRNA for miR-942-5p[J]. Cell Death Dis,  2019, 10(12): 932. DOI: 10.1038/s41419-019-2161-5.

36.  Lin C, Zhong W, Yan W, et al. Circ-SLC8A1 regulates osteoporosis through blocking the inhibitory effect of miR-516b-5p on AKAP2 expression[J]. J Gene Med, 2020, 22(11): e3263. DOI: 10.1002/jgm.3263.

37.  Zhang M, Jia L, Zheng Y. CircRNA expression profiles in human bone marrow stem cells undergoing osteoblast differentiation[J]. Stem Cell Rev Rep, 2019, 15(1): 126-138. DOI: 10.1007/s12015-018-9841-x.

38.  Kuang MJ, Xing F, Wang D, et al. CircUSP45 inhibited osteogenesis in glucocorticoid-induced osteonecrosis of femoral head by sponging miR-127-5p through PTEN/AKT signal pathway: experimental studies[J]. Biochem Biophys Res Commun, 2019. 509(1): 255-261. DOI: 10.1016/j.bbrc.2018.12.116.

39.  Zhu S, Zhu Y, Wang Z, et al. Bioinformatics analysis and identification of circular RNAs promoting the osteogenic differentiation of human bone marrow mesenchymal stem cells on titanium treated by surface mechanical attrition[J]. PeerJ, 2020, 8: e9292. DOI: 10.7717/peerj.9292.

40.  Ge X, Li Z, Jing S, et al. Parathyroid hormone enhances the osteo/odontogenic differentiation of dental pulp stem cells via ERK and P38 MAPK pathways[J]. J Cell Physiol, 2020, 235(2): 1209-1221. DOI: 10.1002/jcp.29034.

41.  Li C, Jiang H. Altered expression of circular RNA in human dental pulp cells during odontogenic differentiation[J]. Mol Med Rep, 2019, 20(2): 871-878. DOI: 10.3892/mmr.2019.10359.

42.  Ferrarotti F, Romano F, Gamba MN, et al. Human intrabony defect regeneration with micrografts containing dental pulp stem cells: a randomized controlled clinical trial[J].  J Clin Periodontol, 2018, 45(7): 841-850. DOI: 10.1111/jcpe.12931.

43.  Ji F, Zhu L, Pan J, et al. Hsa_circ_0026827 promotes osteoblast differentiation of human dental pulp stem cells through the beclin1 and RUNX1 signaling pathways by sponging miR-188-3p[J]. Front Cell Dev Biol, 2020, 8: 470. DOI: 10.3389/fcell.2020.00470.

44.  Laloze J, Fiévet L, Desmoulière A. Adipose-derived stromal cell in regenerative medicine: a review[J]. Adv Wound Care (New Rochelle), 2021, 10(1): 24-28. DOI: 10.1089/wound.2020.1175.

45.  Betz VM, Kochanek S, Rammelt S, et al. Recent advances in gene‐enhanced bone tissue engineering[J]. The Journal of Gene Medicine, 2018, 20(6): e3018. DOI: 10.1002/jgm.3018.

46.  Zhang D, Ni N, Wang Y, et al. CircRNA-vgll3 promotes osteogenic differentiation of adipose-derived mesenchymal stem cells via modulating miRNA-dependent integrin α5 expression[J]. Cell Death Differ, 2021, 28(1): 283-302.DOI: 10.1038/s41418-020-0600-6.

47.  Huang X, Cen X, Zhang B, et al. The roles of circRFWD2 and circINO80 during NELL‐1‐induced osteogenesis[J]. J Cell Mol Med, 2019, 23(12): 8432-8441. DOI: 10.1111/jcmm.14726.

48.  Gu X, Li M, Jin Y, et al. Identification and integrated analysis of differentially expressed lncRNAs and circRNAs reveal the potential ceRNA networks during PDLSC osteogenic differentiation[J]. BMC Genet, 2017, 18(1): 100. DOI: 10.1186/s12863-017-0569-4.

49.  Li X, Zheng Y, Zheng Y, et al. Circular RNA CDR1as regulates osteoblastic differentiation of periodontal ligament stem cells via the miR-7/GDF5/SMAD and p38 MAPK signaling pathway[J]. Stem Cell Res Ther, 2018, 9(1): 232. DOI: 10.1186/s13287-018-0976-0.

50.  Wang H, Feng C, Jin Y, et al. Identification and characterization of circular RNAs involved in mechanical force‐induced periodontal ligament stem cells[J]. J Cell Physiol, 2019, 234(7): 10166-10177. DOI: 10.1002/jcp. 27686.

51.  Quarles LD, Yohay DA, Lever LW, et al. Distinct proliferative and differentiated stages of murine MC3T3‐E1 cells in culture: an in vitro model of osteoblast development[J]. J Bone Miner Res, 1992, 7(6): 683-692.DOI: 10.1002/jbmr.5650070613.

52.  Wu C, Zheng Z, Ren W, et al. Mm9_circ_009056 enhances osteogenesis by targeting BMP7 via CGRP-mediated miR-22–3p[J]. Biochem Biophys Res Commun, 2018, 501(1): 199-205. DOI: 10.1016/j.bbrc.2018.04.215.

53.  Zhu X, Zhao Z, Zeng C, et al. HNGF6A inhibits oxidative stress-induced MC3T3-E1 cell apoptosis and osteoblast phenotype inhibition by targeting circ_0001843/mir-214 pathway[J]. Calcif Tissue Int, 2020, 106(5): 518-532. DOI: 10.1007/s00223-020-00660-z.

54.  Cao Z, Zhang Y, Wei S, et al. Comprehensive circRNA expression profile and function network in osteoblast-like cells under simulated microgravity[J]. Gene, 2021, 764: 145106. DOI: 10.1016/j.gene.2020.145106.

55.  Mi B, Xiong Y, Chen L, et al. CircRNA AFF4 promotes osteoblast cells proliferation and inhibits apoptosis via the Mir-7223-5p/PIK3R1 axis[J]. Aging (Albany NY), 2019 , 11(24): 11988-12001. DOI: 10.18632/aging.102524.

56.  Huang P, Yan R, Zhang X, et al. Activating Wnt/β-catenin signaling pathway for disease therapy: challenges and opportunities[J]. Pharmacol Ther, 2019, 196: 79-90. DOI: 10.1016/j.pharmthera.2018.11.008.

57.  Baron R, Kneissel M. WNT signaling in bone homeostasis and disease: from human mutations to treatments[J]. Nat Med, 2013, 19(2): 179-192. DOI: 10.1038/nm.3074.

58.  Zhao R, Li Y, Lin Z, et al. miR-199b-5p modulates BMSC osteogenesis via suppressing GSK-3β/β-catenin signaling pathway[J]. Biochem Biophys Res Commun, 2016, 477(4): 749-754. DOI: 10.1016/j.bbrc.2016.06.130.

59.  Jiang N, Chen WJ, Zhang JW, et al. Downregulation of miR-432 activates Wnt/β-catenin signaling and promotes human hepatocellular carcinoma proliferation[J]. Oncotarget, 2015, 6(10): 7866-7879. DOI: 10.18632/oncotarget.3492.

60.  Kim HY, Park SY, Choung SY. Enhancing effects of myricetin on the osteogenic differentiation of human periodontal ligament stem cells via BMP-2/Smad and ERK/JNK/p38 mitogen-activated protein kinase signaling pathway[J]. Eur J Pharmacol, 2018, 834: 84-91. DOI: 10.1016/j.ejphar.2018.07.012.

61.  Zhang M, Yuan SZ, Sun H, et al. miR-199b-5p promoted chondrogenic differentiation of C3H10T1/2 cells by regulating JAG1[J]. J Tissue Eng Regen Med, 2020, 14(11): 1618-1629. DOI: 10.1002/term.3122.

62.  Chia W, Liu J, Huang YG, et al. A circular RNA derived from DAB1 promotes cell proliferation and osteogenic differentiation of BMSCs via RBPJ/DAB1 axis[J]. Cell Death Dis, 2020, 11(5): 372. DOI: 10.1038/s41419-020-2572-3.

63.  Mevel R, Draper JE, Lie-A-Ling M, et al. RUNX transcription factors: orchestrators of development[J]. Development, 2019, 146(17): dev148296. DOI: 10.1242/dev.148296.

64.  Chen G, Xu H, Yao Y, et al. BMP signaling in the development and regeneration of cranium bones and maintenance of calvarial stem cells[J]. Front Cell Dev Biol, 2020, 8: 135. DOI: 10.3389/fcell.2020.00135.

65.  Ge X, Li Z, Zhou Z, et al. Circular RNA SIPA1L1 promotes osteogenesis via regulating the miR-617/Smad3 axis in dental pulp stem cells[J]. Stem Cell Res Ther, 2020, 11(1): 364. DOI: 10.1186/s13287-020-01877-3.

66.  Chen X, Ouyang H, Wang Z, et al. A novel circular RNA generated by FGFR2 gene promotes myoblast proliferation and differentiation by sponging miR-133a-5p and miR-29b-1-5p[J]. Cells, 2018, 7(11): 199. DOI: 10.3390/cells7110199.

67.  Lee NJ, Ali N, Zhang L, et al. Osteoglycin, a novel coordinator of bone and glucose homeostasis[J]. Mol Metab, 2018, 13: 30-44. DOI: 10.1016/j.molmet.2018.05.004.

68.  Li W, Li Y, Zhang L, et al. AKAP2 identified as a novel gene mutated in a Chinese family with adolescent idiopathic scoliosis[J]. J Med Genet, 2016, 53(7): 488-493. DOI: 10.1136/jmedgenet-2015-103684.

69.  Liao L, Su X, Yang X, et al. TNF-α inhibits FoxO1 by upregulating miR-705 to aggravate oxidative damage in bone marrow-derived mesenchymal stem cells during osteoporosis[J]. Stem Cells, 2016, 34(4): 1054-1067. DOI: 10.1002/stem.2274.