Research progress on the mechanism of circular RNA involved in stem cell differentiation and its prospect of tissue engineering application_Journal of Biomedical Engineering

Authors：

ZHENG Xiao ,  CHEN Wenchuan

State Key Laboratory of Oral Diseases & National Clinical Research Center for Oral Diseases & Department of Prosthodontics 1, West China Hospital of Stomatology, Sichuan University, Chengdu 610041, P.R.China;

Corresponding author：

Keywords：

circular RNA; stem cells; differentiation; tissue engineering; biomedical engineering

DOI：

10.7507/1001-5515.201905034

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Circular RNA (circRNA) is a type of single-stranded RNA that binds in a closed loop structure by covalent bond. It is highly expressed and has diverse functions in the eukaryotic transcriptome, and it also has the potential to regulate the process of cell differentiation. Stem cells are important seed cells and common research tools in the field of tissue engineering, which have multi-directional differentiation potential and low immunogenicity. Its clinical application for the treatment of diseases has broad prospects, and the research on their differentiation mechanism has gradually penetrated to the molecular level. A number of studies have shown that circRNA participates in stem cell differentiation and plays a key role through a variety of pathways. This article focuses on the expression changes of circRNA during stem cell differentiation and its research advancement in regulating the differentiation mechanism of various stem cells. The review also prospects its possible role in tissue regeneration and repair, in order to further study the molecular mechanism of circRNA involved in stem cell differentiation and provide ideas for clinical practice of stem cells in biomedical engineering.

Citation： ZHENG Xiao, CHEN Wenchuan. Research progress on the mechanism of circular RNA involved in stem cell differentiation and its prospect of tissue engineering application. Journal of Biomedical Engineering, 2019, 36(6): 1038-1042. doi: 10.7507/1001-5515.201905034 Copy

1.	Szabo L, Salzman J. Detecting circular RNAs: bioinformatic and experimental challenges. Nat Rev Genet, 2016, 17(11): 679-692.
2.	Liu Jing, Liu Tian, Wang Xiaman, et al. Circles reshaping the RNA world: from waste to treasure. Mol Cancer, 2017, 16(1): 58.
3.	Legnini I, Di Timoteo G, Rossi F, et al. Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell, 2017, 66(1): 22-37.
4.	Wang Yang, Wang Zefeng. Efficient backsplicing produces translatable circular mRNAs. RNA, 2015, 21(2): 172-179.
5.	Chen C Y, Sarnow P. Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science, 1995, 268(529): 415-417.
6.	Lasda E, Parker R. Circular RNAs: diversity of form and function. RNA, 2014, 20(12): 1829-1842.
7.	Li Xiang, Yang Li, Chen Lingling. The biogenesis, functions, and challenges of circular RNAs. Mol Cell, 2018, 71(3): 428-442.
8.	Soldner F, Jaenisch R. Stem cells, genome editing, and the path to translational medicine. Cell, 2018, 175(3): 615-632.
9.	Nolta J A. Research leads to approved therapies in the new era of living medicine. Stem Cells, 2018, 36(1): 1-3.
10.	Zhang Mengjun, Jia Lingfei, Zheng Yunfei. circRNA expression profiles in human bone marrow stem cells undergoing osteoblast differentiation. Stem Cell Reviews and Reports, 2019, 15(1): 126-138.
11.	Li Xiaoyun, Peng Bojia, Zhu Xiaofeng, et al. Changes in related circular RNAs following ER beta knockdown and the relationship to rBMSC osteogenesis. Biochem Biophys Res Commun, 2017, 493(1): 100-107.
12.	Maass P G, Glažar P, Memczak S, et al. A map of human circular RNAs in clinically relevant tissues. J Mol Med, 2017, 95(11): 1179-1189.
13.	Cherubini A, Barilani M, Rossi R L, et al. FOXP1 circular RNA sustains mesenchymal stem cell identity via microRNA inhibition. Nucleic Acids Res, 2019, 47(10): 5325-5340.
14.	Seo B M, Miura M, Gronthos S, et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet, 2004, 364(9429): 149-155.
15.	Ohta S, Yamada S, Matuzaka K, et al. The behavior of stem cells and progenitor cells in the periodontal ligament during wound healing as observed using immunohistochemical methods. J Periodontal Res, 2008, 43(6): 595-603.
16.	Zheng Yunfei, Li Xiaobei, Huang Yiping, et al. The circular RNA landscape of periodontal ligament stem cells during osteogenesis. J Periodontol, 2017, 88(9): 906-914.
17.	Gu Xiuge, Li Mengying, Jin Ye, et al. Identification and integrated analysis of differentially expressed lncRNAs and circRNAs reveal the potential ceRNA networks during PDLSC osteogenic differentiation. BMC Genet, 2017, 18(1): 100.
18.	Li Xiaobei, Zheng Yunfei, Zheng Yan, et al. Circular RNA CDR1as regulates osteoblastic differentiation of periodontal ligament stem cells via the miR-7/GDF5/SMAD and p38 MAPK signaling pathway. Stem Cell Res Ther, 2018, 9(1): 232.
19.	Memczak S, Jens M, Elefsinioti A, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature, 2013, 495(7441): 333-338.
20.	Kleaveland B, Shi C Y, Stefano J, et al. A network of noncoding regulatory RNAs acts in the mammalian brain. Cell, 2018, 174(2): 350-362.
21.	Piwecka M, Glazar P, Hernandez-Miranda L R, et al. Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function. Science, 2017, 357(6357): eaam8526.
22.	Peng Wei, Zhu Shuangxi, Wang Jin, et al. Lnc-NTF3-5 promotes osteogenic differentiation of maxillary sinus membrane stem cells via sponging miR-93-3p. Clin Implant Dent Relat Res, 2018, 20(2): 110-121.
23.	Peng Wei, Zhu Shuangxi, Chen Junlan, et al. Hsa_circRNA_33287 promotes the osteogenic differentiation of maxillary sinus membrane stem cells via miR-214-3p/Runx3. Biomed Pharmacother, 2019, 109: 1709-1717.
24.	Li Zehan, Li Na, Ge Xingyun, et al. Differential circular RNA expression profiling during osteogenic differentiation of stem cells from apical papilla. Epigenomics, 2019, 11(9): 1056-1073.
25.	Goode D K, Obier N, Vijayabaskar M, et al. Dynamic gene regulatory networks drive hematopoietic specification and differentiation. Dev Cell, 2016, 36(5): 572-587.
26.	Xia Pengyan, Wang Shuo, Ye Buqing, et al. A circular RNA protects dormant hematopoietic stem cells from DNA sensor cGAS-Mediated exhaustion. Immunity, 2018, 48(4): 688-701.
27.	Nicolet B P, Engels S, Aglialoro F, et al. Circular RNA expression in human hematopoietic cells is widespread and cell-type specific. Nucleic Acids Res, 2018, 46(16): 8168-8180.
28.	Xie Fang, Zhao Yun, Wang Shida, et al. Identification, characterization, and functional investigation of circular RNAs in subventricular zone of adult rat brain. J Cell Biochem, 2019, 120(3): 3428-3437.
29.	Yang Qichang, Wu Jing, Zhao Jian, et al. Circular RNA expression profiles during the differentiation of mouse neural stem cells. BMC Syst Biol, 2018, 12(Suppl 8): 128.
30.	Arnaiz E, Sole C, Manterola L, et al. CircRNAs and cancer: biomarkers and master regulators. Semin Cancer Biol, 2019, 58: 90-99.
31.	Wang Miao, Yang Yuxi, Xu Jian, et al. CircRNAs as biomarkers of cancer: a meta-analysis. BMC Cancer, 2018, 18(1): 303.
32.	Yan Ningning, Xu Haiyan, Zhang Jinnan, et al. Circular RNA profile indicates circular RNA VRK1 is negatively related with breast cancer stem cells. Oncotarget, 2017, 8(56): 95704-95718.
33.	Wu Yongyan, Zhang Yuliang, Niu Min, et al. Whole-transcriptome analysis of CD133+ CD144+ cancer stem cells derived from human laryngeal squamous cell carcinoma cells. Cell Physiol Biochem, 2018, 47(4): 1696-1710.
34.	Li Xiaoyong, Ao Junping, Wu Ji. Systematic identification and comparison of expressed profiles of lncRNAs and circRNAs with associated co-expression and ceRNA networks in mouse germline stem cells. Oncotarget, 2017, 8(16): 26573-26590.
35.	Kristensen L S, Okholm T L H, Veno M T, et al. Circular RNAs are abundantly expressed and upregulated during human epidermal stem cell differentiation. RNA Biol, 2018, 15(2): 280-291.
36.	Ruan Zhongbao, Chen Gecai, Zhang Rui, et al. Circular RNA expression profiles during the differentiation of human umbilical cord-derived mesenchymal stem cells into cardiomyocyte-like cells. J Cell Physiol, 2019, 234(9): 16412-16423.
37.	Errichelli L, Modigliani S D, Laneve P, et al. FUS affects circular RNA expression in murine embryonic stem cell-derived motor neurons. Nat Commun, 2017, 8: 14741.
38.	Siede D, Rapti K, Gorska A A, et al. Identification of circular RNAs with host gene-independent expression in human model systems for cardiac differentiation and disease. J Mol Cell Cardiol, 2017, 109: 48-56.
39.	Lei Wei, Feng Tingting, Fang Xing, et al. Signature of circular RNAs in human induced pluripotent stem cells and derived cardiomyocytes. Stem Cell Res Ther, 2018, 9(1): 56.
40.	Yu Chunying, Li T C, Wu Yiying, et al. The circular RNA circBIRC6 participates in the molecular circuitry controlling human pluripotency. Nat Commun, 2017, 8(1): 1149.

1. Szabo L, Salzman J. Detecting circular RNAs: bioinformatic and experimental challenges. Nat Rev Genet, 2016, 17(11): 679-692.
2. Liu Jing, Liu Tian, Wang Xiaman, et al. Circles reshaping the RNA world: from waste to treasure. Mol Cancer, 2017, 16(1): 58.
3. Legnini I, Di Timoteo G, Rossi F, et al. Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell, 2017, 66(1): 22-37.
4. Wang Yang, Wang Zefeng. Efficient backsplicing produces translatable circular mRNAs. RNA, 2015, 21(2): 172-179.
5. Chen C Y, Sarnow P. Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science, 1995, 268(529): 415-417.
6. Lasda E, Parker R. Circular RNAs: diversity of form and function. RNA, 2014, 20(12): 1829-1842.
7. Li Xiang, Yang Li, Chen Lingling. The biogenesis, functions, and challenges of circular RNAs. Mol Cell, 2018, 71(3): 428-442.
8. Soldner F, Jaenisch R. Stem cells, genome editing, and the path to translational medicine. Cell, 2018, 175(3): 615-632.
9. Nolta J A. Research leads to approved therapies in the new era of living medicine. Stem Cells, 2018, 36(1): 1-3.
10. Zhang Mengjun, Jia Lingfei, Zheng Yunfei. circRNA expression profiles in human bone marrow stem cells undergoing osteoblast differentiation. Stem Cell Reviews and Reports, 2019, 15(1): 126-138.
11. Li Xiaoyun, Peng Bojia, Zhu Xiaofeng, et al. Changes in related circular RNAs following ER beta knockdown and the relationship to rBMSC osteogenesis. Biochem Biophys Res Commun, 2017, 493(1): 100-107.
12. Maass P G, Glažar P, Memczak S, et al. A map of human circular RNAs in clinically relevant tissues. J Mol Med, 2017, 95(11): 1179-1189.
13. Cherubini A, Barilani M, Rossi R L, et al. FOXP1 circular RNA sustains mesenchymal stem cell identity via microRNA inhibition. Nucleic Acids Res, 2019, 47(10): 5325-5340.
14. Seo B M, Miura M, Gronthos S, et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet, 2004, 364(9429): 149-155.
15. Ohta S, Yamada S, Matuzaka K, et al. The behavior of stem cells and progenitor cells in the periodontal ligament during wound healing as observed using immunohistochemical methods. J Periodontal Res, 2008, 43(6): 595-603.
16. Zheng Yunfei, Li Xiaobei, Huang Yiping, et al. The circular RNA landscape of periodontal ligament stem cells during osteogenesis. J Periodontol, 2017, 88(9): 906-914.
17. Gu Xiuge, Li Mengying, Jin Ye, et al. Identification and integrated analysis of differentially expressed lncRNAs and circRNAs reveal the potential ceRNA networks during PDLSC osteogenic differentiation. BMC Genet, 2017, 18(1): 100.
18. Li Xiaobei, Zheng Yunfei, Zheng Yan, et al. Circular RNA CDR1as regulates osteoblastic differentiation of periodontal ligament stem cells via the miR-7/GDF5/SMAD and p38 MAPK signaling pathway. Stem Cell Res Ther, 2018, 9(1): 232.
19. Memczak S, Jens M, Elefsinioti A, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature, 2013, 495(7441): 333-338.
20. Kleaveland B, Shi C Y, Stefano J, et al. A network of noncoding regulatory RNAs acts in the mammalian brain. Cell, 2018, 174(2): 350-362.
21. Piwecka M, Glazar P, Hernandez-Miranda L R, et al. Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function. Science, 2017, 357(6357): eaam8526.
22. Peng Wei, Zhu Shuangxi, Wang Jin, et al. Lnc-NTF3-5 promotes osteogenic differentiation of maxillary sinus membrane stem cells via sponging miR-93-3p. Clin Implant Dent Relat Res, 2018, 20(2): 110-121.
23. Peng Wei, Zhu Shuangxi, Chen Junlan, et al. Hsa_circRNA_33287 promotes the osteogenic differentiation of maxillary sinus membrane stem cells via miR-214-3p/Runx3. Biomed Pharmacother, 2019, 109: 1709-1717.
24. Li Zehan, Li Na, Ge Xingyun, et al. Differential circular RNA expression profiling during osteogenic differentiation of stem cells from apical papilla. Epigenomics, 2019, 11(9): 1056-1073.
25. Goode D K, Obier N, Vijayabaskar M, et al. Dynamic gene regulatory networks drive hematopoietic specification and differentiation. Dev Cell, 2016, 36(5): 572-587.
26. Xia Pengyan, Wang Shuo, Ye Buqing, et al. A circular RNA protects dormant hematopoietic stem cells from DNA sensor cGAS-Mediated exhaustion. Immunity, 2018, 48(4): 688-701.
27. Nicolet B P, Engels S, Aglialoro F, et al. Circular RNA expression in human hematopoietic cells is widespread and cell-type specific. Nucleic Acids Res, 2018, 46(16): 8168-8180.
28. Xie Fang, Zhao Yun, Wang Shida, et al. Identification, characterization, and functional investigation of circular RNAs in subventricular zone of adult rat brain. J Cell Biochem, 2019, 120(3): 3428-3437.
29. Yang Qichang, Wu Jing, Zhao Jian, et al. Circular RNA expression profiles during the differentiation of mouse neural stem cells. BMC Syst Biol, 2018, 12(Suppl 8): 128.
30. Arnaiz E, Sole C, Manterola L, et al. CircRNAs and cancer: biomarkers and master regulators. Semin Cancer Biol, 2019, 58: 90-99.
31. Wang Miao, Yang Yuxi, Xu Jian, et al. CircRNAs as biomarkers of cancer: a meta-analysis. BMC Cancer, 2018, 18(1): 303.
32. Yan Ningning, Xu Haiyan, Zhang Jinnan, et al. Circular RNA profile indicates circular RNA VRK1 is negatively related with breast cancer stem cells. Oncotarget, 2017, 8(56): 95704-95718.
33. Wu Yongyan, Zhang Yuliang, Niu Min, et al. Whole-transcriptome analysis of CD133+ CD144+ cancer stem cells derived from human laryngeal squamous cell carcinoma cells. Cell Physiol Biochem, 2018, 47(4): 1696-1710.
34. Li Xiaoyong, Ao Junping, Wu Ji. Systematic identification and comparison of expressed profiles of lncRNAs and circRNAs with associated co-expression and ceRNA networks in mouse germline stem cells. Oncotarget, 2017, 8(16): 26573-26590.
35. Kristensen L S, Okholm T L H, Veno M T, et al. Circular RNAs are abundantly expressed and upregulated during human epidermal stem cell differentiation. RNA Biol, 2018, 15(2): 280-291.
36. Ruan Zhongbao, Chen Gecai, Zhang Rui, et al. Circular RNA expression profiles during the differentiation of human umbilical cord-derived mesenchymal stem cells into cardiomyocyte-like cells. J Cell Physiol, 2019, 234(9): 16412-16423.
37. Errichelli L, Modigliani S D, Laneve P, et al. FUS affects circular RNA expression in murine embryonic stem cell-derived motor neurons. Nat Commun, 2017, 8: 14741.
38. Siede D, Rapti K, Gorska A A, et al. Identification of circular RNAs with host gene-independent expression in human model systems for cardiac differentiation and disease. J Mol Cell Cardiol, 2017, 109: 48-56.
39. Lei Wei, Feng Tingting, Fang Xing, et al. Signature of circular RNAs in human induced pluripotent stem cells and derived cardiomyocytes. Stem Cell Res Ther, 2018, 9(1): 56.
40. Yu Chunying, Li T C, Wu Yiying, et al. The circular RNA circBIRC6 participates in the molecular circuitry controlling human pluripotency. Nat Commun, 2017, 8(1): 1149.

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