Research progress in the stemness regulation and targeted treatment of microRNA in gastric cancer stem cells_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

LIN Hao ¹ , WANG Chaoyang ¹ , ZHANG Haibao ¹ , JU Jiahua ¹ ,  YU Yongjiang ^1,2

1. The First Clinical Medical College of Lanzhou University, Lanzhou 730000, P. R. China;
2. Department of Gastrointestinal and Hernia and Abdominal Wall Surgery, The First Hospital of Lanzhou University, Lanzhou 730000, P. R. China;

Corresponding author：

YU Yongjiang, Email: ylongy@163.com

Keywords：

microRNA; stomach neoplasm; neoplastic stem cell; stemness characteristics

DOI：

10.7507/1007-9424.202209019

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the stemness regulation mechanism of microRNA on invasion, metastasis and chemoresistance of gastric cancer stem cells (GCSCs), and to explore the anti-tumor therapy based on miRNA targeting GCSCs. Method The literatures about the research progress of miRNA and GCSCs at home and abroad in recent years were collected and reviewed. Results MiRNA could regulate a series of important cellular processes such as proliferation, apoptosis, differentiation and epithelial-mesenchymal transition of GCSCs by participating in the expression of related target genes, which was associated with poor prognosis and high mortality of gastric cancer patients. Silencing or restoring the expression of candidate miRNA of GCSCs could provide a novel and promising approach for the treatment of gastric cancer. Conclusions GCSCs have an important relationship with the malignant biological behavior of gastric cancer, and studies have confirmed that miRNA play an important regulatory role in GCSCs. Therefore, miRNA can be used as a potential target for the treatment of gastric cancer. By regulating the expression of specific miRNA, it can inhibit tumor invasion and metastasis, and improve the sensitivity of chemotherapy drugs.

Citation： LIN Hao, WANG Chaoyang, ZHANG Haibao, JU Jiahua, YU Yongjiang. Research progress in the stemness regulation and targeted treatment of microRNA in gastric cancer stem cells. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2023, 30(3): 358-363. doi: 10.7507/1007-9424.202209019 Copy

1.	Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
2.	Ho SWT, Tan P. Dissection of gastric cancer heterogeneity for precision oncology. Cancer Sci, 2019, 110(11): 3405-3414.
3.	Sai E, Miwa Y, Takeyama R, et al. Identification of candidates for driver oncogenes in scirrhous-type gastric cancer cell lines. Cancer Sci, 2019, 110(8): 2643-2651.
4.	Najafi M, Mortezaee K, Majidpoor J. Cancer stem cell (CSC) resistance drivers. Life Sci, 2019, 234: 116781. doi: 10.1016/j.lfs.2019.116781.
5.	Xiao S, Zhou L. Gastric stem cells: physiological and pathological perspectives. Front Cell Dev Biol, 2020, 8: 571536. doi: 10.3389/fcell.2020.571536.
6.	Su Z, Yang Z, Xu Y, et al. MicroRNAs in apoptosis, autophagy and necroptosis. Oncotarget, 2015, 6(11): 8474-8490.
7.	詹盼盼, 舒雄, 陈梦. 微小RNA-195抑制CD44⁺胃癌干细胞的干性特征和侵袭能力. 江苏医药, 2021, 47(5): 437-442, 446.
8.	Xing S, Tian Z, Zheng W, et al. Hypoxia downregulated miR-4521 suppresses gastric carcinoma progression through regulation of IGF2 and FOXM1. Mol Cancer, 2021, 20(1): 9. doi: 10.1186/s12943-020-01295-2.
9.	孙生安, 白明辉, 韩保卫, 等. Hsa-miR-29c在胃癌中的表达及其临床意义研究. 中国普外基础与临床杂志, 2021, 28(2): 200-207.
10.	Xiao Z, Zheng YB, Dao WX, et al. MicroRNA-328-3p facilitates the progression of gastric cancer via KEAP1/NRF2 axis. Free Radic Res, 2021, 55(6): 720-730.
11.	Huangfu L, He Q, Han J, et al. MicroRNA-135b/CAMK2D axis contribute to malignant progression of gastric cancer through EMT process remodeling. Int J Biol Sci, 2021, 17(8): 1940-1952.
12.	刘文能, 杨百仞, 李东, 等. 外周血中miRNA-196a在进展期胃癌中的表达及其临床及生物学意义. 中国普外基础与临床杂志, 2021, 28(8): 1025-1030.
13.	Ors-Kumoglu G, Gulce-Iz S, Biray-Avci C. Therapeutic microRNAs in human cancer. Cytotechnology, 2019, 71(1): 411-425.
14.	Mukohyama J, Isobe T, Hu Q, et al. miR-221 targets QKI to enhance the tumorigenic capacity of human colorectal cancer stem cells. Cancer Res, 2019, 79(20): 5151-5158.
15.	Ruggieri V, Russi S, Zoppoli P, et al. The role of microRNAs in the regulation of gastric cancer stem cells: a meta-analysis of the current status. J Clin Med, 2019, 8(5): 639. doi: 10.3390/jcm8050639.
16.	Ayob AZ, Ramasamy TS. Cancer stem cells as key drivers of tumour progression. J Biomed Sci, 2018, 25(1): 20. doi: 10.1186/s12929-018-0426-4.
17.	Atashzar MR, Baharlou R, Karami J, et al. Cancer stem cells: a review from origin to therapeutic implications. J Cell Physiol, 2020, 235(2): 790-803.
18.	Treisman D, Li Y, Zhu Y. Stem-like cell populations, p53-pathway activation and mechanisms of recurrence in sonic hedgehog medulloblastoma. Neuromolecular Med, 2022, 24(1): 13-17.
19.	Grassi ES, Ghiandai V, Persani L. Thyroid cancer stem-like cells: from microenvironmental niches to therapeutic strategies. J Clin Med, 2021, 10(7): 1455. doi: 10.3390/jcm10071455.
20.	Liu J, Ma L, Xu J, et al. Spheroid body-forming cells in the human gastric cancer cell line MKN-45 possess cancer stem cell properties. Int J Oncol, 2013, 42(2): 453-459.
21.	Takaishi S, Okumura T, Tu S, et al. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells, 2009, 27(5): 1006-1020.
22.	Zhang C, Li C, He F, et al. Identification of CD44⁺CD24⁺ gastric cancer stem cells. J Cancer Res Clin Oncol, 2011, 137(11): 1679-1686.
23.	Ni T, Wang H, Zhan D, et al. CD133⁺/CD166⁺ human gastric adenocarcinoma cells present the properties of neoplastic stem cells and emerge more malignant features. Life Sci, 2021, 269: 119021. doi: 10.1016/j.lfs.2021.119021.
24.	张东阳, 陈小龙, 宋小海, 等. 胃癌患者外周血中CD45^–CD44⁺CD54⁺细胞亚群含量及其临床意义. 中国普外基础与临床杂志, 2020, 27(4): 434-441.
25.	Chen S, Chen C, Hu Y, et al. Three-dimensional ex vivo culture for drug responses of patient-derived gastric cancer tissue. Front Oncol, 2021, 10: 614096. doi: 10.3389/fonc.2020.614096.
26.	Kim DH, Lee S, Kang HG, et al. Synergistic antitumor activity of a DLL4/VEGF bispecific therapeutic antibody in combination with irinotecan in gastric cancer. BMB Rep, 2020, 53(10): 533-538.
27.	Hui Y, Yang Y, Li D, et al. LncRNA FEZF1-AS1 modulates cancer stem cell properties of human gastric cancer through miR-363-3p/HMGA2. Cell Transplant, 2020, 29: 963689720925059. doi: 10.1177/0963689720925059.
28.	Ni H, Qin H, Sun C, et al. MiR-375 reduces the stemness of gastric cancer cells through triggering ferroptosis. Stem Cell Res Ther, 2021, 12(1): 325. doi: 10.1186/s13287-021-02394-7.
29.	Wu K, Ma L, Zhu J. miR-483-5p promotes growth, invasion and self-renewal of gastric cancer stem cells by Wnt/β-catenin signaling. Mol Med Rep, 2016, 14(4): 3421-3428.
30.	Sun B, Han Y, Cai H, et al. Long non-coding RNA SNHG3, induced by IL-6/STAT3 transactivation, promotes stem cell-like properties of gastric cancer cells by regulating the miR-3619-5p/ARL2 axis. Cell Oncol (Dordr), 2021, 44(1): 179-192.
31.	Dastmalchi N, Safaralizadeh R, Teimourian S. An updated review of the contribution of noncoding RNAs to the progression of gastric cancer stem cells: molecular mechanisms of viability, invasion, and chemoresistance of gastric cancer stem cells. Curr Stem Cell Res Ther, 2022, 17(5): 440-445.
32.	Xin L, Liu L, Liu C, et al. DNA-methylation-mediated silencing of miR-7-5p promotes gastric cancer stem cell invasion via increasing Smo and Hes1. J Cell Physiol, 2020, 235(3): 2643-2654.
33.	Mirzaei S, Baghaei K, Parivar K, et al. The expression level changes of microRNAs 200a/205 in the development of invasive properties in gastric cancer cells through epithelial-mesenchymal transition. Eur J Pharmacol, 2019, 857: 172426. doi: 10.1016/j.ejphar.2019.172426.
34.	Song H, Shi L, Xu Y, et al. BRD4 promotes the stemness of gastric cancer cells via attenuating miR-216a-3p-mediated inhibition of Wnt/β-catenin signaling. Eur J Pharmacol, 2019, 852: 189-197.
35.	Peng X, Kang Q, Wan R, et al. miR-26a/HOXC9 dysregulation promotes metastasis and stem cell-like phenotype of gastric cancer. Cell Physiol Biochem, 2018, 49(4): 1659-1676.
36.	Li L, Zhao J, Huang S, et al. MiR-93-5p promotes gastric cancer-cell progression via inactivation of the Hippo signaling pathway. Gene, 2018, 641: 240-247.
37.	Du M, Zhuang Y, Tan P, et al. microRNA-95 knockdown inhibits epithelial-mesenchymal transition and cancer stem cell phenotype in gastric cancer cells through MAPK pathway by upregulating DUSP5. J Cell Physiol, 2020, 235(2): 944-956.
38.	Lampis A, Hahne JC, Hedayat S, et al. MicroRNAs as mediators of drug resistance mechanisms. Curr Opin Pharmacol, 2020, 54: 44-50.
39.	Divisato G, Piscitelli S, Elia M, et al. MicroRNAs and stem-like properties: the complex regulation underlying stemness maintenance and cancer development. Biomolecules, 2021, 11(8): 1074. doi: 10.3390/biom11081074.
40.	Xiao WS, Li DF, Tang YP, et al. Inhibition of epithelial-mesenchymal transition in gastric cancer cells by miR-711-mediated downregulation of CD44 expression. Oncol Rep, 2018, 40(5): 2844-2853.
41.	Pan Y, Shu X, Sun L, et al. miR-196a-5p modulates gastric cancer stem cell characteristics by targeting Smad4. Int J Oncol, 2017, 50(6): 1965-1976.
42.	Zhang J, Wang C, Yan S, et al. miR-345 inhibits migration and stem-like cell phenotype in gastric cancer via inactivation of Rac1 by targeting EPS8. Acta Biochim Biophys Sin (Shanghai), 2020, 52(3): 259-267.
43.	Wu S, Xie J, Shi H, et al. miR-492 promotes chemoresistance to CDDP and metastasis by targeting inhibiting DNMT3B and induces stemness in gastric cancer. Biosci Rep, 2020, 40(3): BSR20194342. doi: 10.1042/BSR20194342.
44.	Shen C, Wang J, Xu Z, et al. ONECUT2 which is targeted by hsa-miR-15a-5p enhances stemness maintenance of gastric cancer stem cells. Exp Biol Med (Maywood), 2021, 246(24): 2645-2659.
45.	Zhan P, Shu X, Chen M, et al. miR-98-5p inhibits gastric cancer cell stemness and chemoresistance by targeting branched-chain aminotransferases 1. Life Sci, 2021, 276: 119405. doi: 10.1016/j.lfs.2021.119405.
46.	Hwang GR, Yuen JG, Ju J. Roles of microRNAs in gastrointestinal cancer stem cell resistance and therapeutic development. Int J Mol Sci, 2021, 22(4): 1624. doi: 10.3390/ijms22041624.
47.	Lee SD, Yu D, Lee DY, et al. Upregulated microRNA-193a-3p is responsible for cisplatin resistance in CD44(+) gastric cancer cells. Cancer Sci, 2019, 110(2): 662-673.
48.	Baldessari C, Gelsomino F, Spallanzani A, et al. Beyond the beyond: a case of an extraordinary response to multiple lines of therapy in a de novo metastatic HER2-negative gastric cancer patient. Gastrointest Tumors, 2018, 5(1-2): 14-20.
49.	Wei C, Chen M, Deng W, et al. Characterization of gastric cancer stem-like molecular features, immune and pharmacogenomic landscapes. Brief Bioinform, 2022, 23(1): bbab386. doi: 10.1093/bib/bbab386.
50.	Peng C, Huang K, Liu G, et al. MiR-876-3p regulates cisplatin resistance and stem cell-like properties of gastric cancer cells by targeting TMED3. J Gastroenterol Hepatol, 2019, 34(10): 1711-1719.
51.	刘云霞, 徐叶峰, 王翌庆, 等. miRNA-139-5p靶向Notch1/Jagged1调控胃癌干细胞增殖转移及益气补肾方的干预作用. 中华中医药杂志, 2021, 36(1): 441-445.
52.	Ratti M, Lampis A, Ghidini M, et al. MicroRNAs (miRNAs) and long non-coding RNAs (lncRNAs) as new tools for cancer therapy: first steps from bench to bedside. Target Oncol, 2020, 15(3): 261-278.
53.	Hanna J, Hossain GS, Kocerha J. The potential for microRNA therapeutics and clinical research. Front Genet, 2019, 10: 478. doi: 10.3389/fgene.2019.00478.
54.	Ganju A, Khan S, Hafeez BB, et al. miRNA nanotherapeutics for cancer. Drug Discov Today, 2017, 22(2): 424-432.
55.	Liu Q, Li RT, Qian HQ, et al. Targeted delivery of miR-200c/DOC to inhibit cancer stem cells and cancer cells by the gelatinases-stimuli nanoparticles. Biomaterials, 2013, 34(29): 7191-7203.
56.	Qian L, Liu F, Chu Y, et al. MicroRNA-200c nanoparticles sensitized gastric cancer cells to radiotherapy by regulating PD-L1 expression and EMT. Cancer Manag Res, 2020, 12: 12215-12223.

1. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
2. Ho SWT, Tan P. Dissection of gastric cancer heterogeneity for precision oncology. Cancer Sci, 2019, 110(11): 3405-3414.
3. Sai E, Miwa Y, Takeyama R, et al. Identification of candidates for driver oncogenes in scirrhous-type gastric cancer cell lines. Cancer Sci, 2019, 110(8): 2643-2651.
4. Najafi M, Mortezaee K, Majidpoor J. Cancer stem cell (CSC) resistance drivers. Life Sci, 2019, 234: 116781. doi: 10.1016/j.lfs.2019.116781.
5. Xiao S, Zhou L. Gastric stem cells: physiological and pathological perspectives. Front Cell Dev Biol, 2020, 8: 571536. doi: 10.3389/fcell.2020.571536.
6. Su Z, Yang Z, Xu Y, et al. MicroRNAs in apoptosis, autophagy and necroptosis. Oncotarget, 2015, 6(11): 8474-8490.
7. 詹盼盼, 舒雄, 陈梦. 微小RNA-195抑制CD44⁺胃癌干细胞的干性特征和侵袭能力. 江苏医药, 2021, 47(5): 437-442, 446.
8. Xing S, Tian Z, Zheng W, et al. Hypoxia downregulated miR-4521 suppresses gastric carcinoma progression through regulation of IGF2 and FOXM1. Mol Cancer, 2021, 20(1): 9. doi: 10.1186/s12943-020-01295-2.
9. 孙生安, 白明辉, 韩保卫, 等. Hsa-miR-29c在胃癌中的表达及其临床意义研究. 中国普外基础与临床杂志, 2021, 28(2): 200-207.
10. Xiao Z, Zheng YB, Dao WX, et al. MicroRNA-328-3p facilitates the progression of gastric cancer via KEAP1/NRF2 axis. Free Radic Res, 2021, 55(6): 720-730.
11. Huangfu L, He Q, Han J, et al. MicroRNA-135b/CAMK2D axis contribute to malignant progression of gastric cancer through EMT process remodeling. Int J Biol Sci, 2021, 17(8): 1940-1952.
12. 刘文能, 杨百仞, 李东, 等. 外周血中miRNA-196a在进展期胃癌中的表达及其临床及生物学意义. 中国普外基础与临床杂志, 2021, 28(8): 1025-1030.
13. Ors-Kumoglu G, Gulce-Iz S, Biray-Avci C. Therapeutic microRNAs in human cancer. Cytotechnology, 2019, 71(1): 411-425.
14. Mukohyama J, Isobe T, Hu Q, et al. miR-221 targets QKI to enhance the tumorigenic capacity of human colorectal cancer stem cells. Cancer Res, 2019, 79(20): 5151-5158.
15. Ruggieri V, Russi S, Zoppoli P, et al. The role of microRNAs in the regulation of gastric cancer stem cells: a meta-analysis of the current status. J Clin Med, 2019, 8(5): 639. doi: 10.3390/jcm8050639.
16. Ayob AZ, Ramasamy TS. Cancer stem cells as key drivers of tumour progression. J Biomed Sci, 2018, 25(1): 20. doi: 10.1186/s12929-018-0426-4.
17. Atashzar MR, Baharlou R, Karami J, et al. Cancer stem cells: a review from origin to therapeutic implications. J Cell Physiol, 2020, 235(2): 790-803.
18. Treisman D, Li Y, Zhu Y. Stem-like cell populations, p53-pathway activation and mechanisms of recurrence in sonic hedgehog medulloblastoma. Neuromolecular Med, 2022, 24(1): 13-17.
19. Grassi ES, Ghiandai V, Persani L. Thyroid cancer stem-like cells: from microenvironmental niches to therapeutic strategies. J Clin Med, 2021, 10(7): 1455. doi: 10.3390/jcm10071455.
20. Liu J, Ma L, Xu J, et al. Spheroid body-forming cells in the human gastric cancer cell line MKN-45 possess cancer stem cell properties. Int J Oncol, 2013, 42(2): 453-459.
21. Takaishi S, Okumura T, Tu S, et al. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells, 2009, 27(5): 1006-1020.
22. Zhang C, Li C, He F, et al. Identification of CD44⁺CD24⁺ gastric cancer stem cells. J Cancer Res Clin Oncol, 2011, 137(11): 1679-1686.
23. Ni T, Wang H, Zhan D, et al. CD133⁺/CD166⁺ human gastric adenocarcinoma cells present the properties of neoplastic stem cells and emerge more malignant features. Life Sci, 2021, 269: 119021. doi: 10.1016/j.lfs.2021.119021.
24. 张东阳, 陈小龙, 宋小海, 等. 胃癌患者外周血中CD45^–CD44⁺CD54⁺细胞亚群含量及其临床意义. 中国普外基础与临床杂志, 2020, 27(4): 434-441.
25. Chen S, Chen C, Hu Y, et al. Three-dimensional ex vivo culture for drug responses of patient-derived gastric cancer tissue. Front Oncol, 2021, 10: 614096. doi: 10.3389/fonc.2020.614096.
26. Kim DH, Lee S, Kang HG, et al. Synergistic antitumor activity of a DLL4/VEGF bispecific therapeutic antibody in combination with irinotecan in gastric cancer. BMB Rep, 2020, 53(10): 533-538.
27. Hui Y, Yang Y, Li D, et al. LncRNA FEZF1-AS1 modulates cancer stem cell properties of human gastric cancer through miR-363-3p/HMGA2. Cell Transplant, 2020, 29: 963689720925059. doi: 10.1177/0963689720925059.
28. Ni H, Qin H, Sun C, et al. MiR-375 reduces the stemness of gastric cancer cells through triggering ferroptosis. Stem Cell Res Ther, 2021, 12(1): 325. doi: 10.1186/s13287-021-02394-7.
29. Wu K, Ma L, Zhu J. miR-483-5p promotes growth, invasion and self-renewal of gastric cancer stem cells by Wnt/β-catenin signaling. Mol Med Rep, 2016, 14(4): 3421-3428.
30. Sun B, Han Y, Cai H, et al. Long non-coding RNA SNHG3, induced by IL-6/STAT3 transactivation, promotes stem cell-like properties of gastric cancer cells by regulating the miR-3619-5p/ARL2 axis. Cell Oncol (Dordr), 2021, 44(1): 179-192.
31. Dastmalchi N, Safaralizadeh R, Teimourian S. An updated review of the contribution of noncoding RNAs to the progression of gastric cancer stem cells: molecular mechanisms of viability, invasion, and chemoresistance of gastric cancer stem cells. Curr Stem Cell Res Ther, 2022, 17(5): 440-445.
32. Xin L, Liu L, Liu C, et al. DNA-methylation-mediated silencing of miR-7-5p promotes gastric cancer stem cell invasion via increasing Smo and Hes1. J Cell Physiol, 2020, 235(3): 2643-2654.
33. Mirzaei S, Baghaei K, Parivar K, et al. The expression level changes of microRNAs 200a/205 in the development of invasive properties in gastric cancer cells through epithelial-mesenchymal transition. Eur J Pharmacol, 2019, 857: 172426. doi: 10.1016/j.ejphar.2019.172426.
34. Song H, Shi L, Xu Y, et al. BRD4 promotes the stemness of gastric cancer cells via attenuating miR-216a-3p-mediated inhibition of Wnt/β-catenin signaling. Eur J Pharmacol, 2019, 852: 189-197.
35. Peng X, Kang Q, Wan R, et al. miR-26a/HOXC9 dysregulation promotes metastasis and stem cell-like phenotype of gastric cancer. Cell Physiol Biochem, 2018, 49(4): 1659-1676.
36. Li L, Zhao J, Huang S, et al. MiR-93-5p promotes gastric cancer-cell progression via inactivation of the Hippo signaling pathway. Gene, 2018, 641: 240-247.
37. Du M, Zhuang Y, Tan P, et al. microRNA-95 knockdown inhibits epithelial-mesenchymal transition and cancer stem cell phenotype in gastric cancer cells through MAPK pathway by upregulating DUSP5. J Cell Physiol, 2020, 235(2): 944-956.
38. Lampis A, Hahne JC, Hedayat S, et al. MicroRNAs as mediators of drug resistance mechanisms. Curr Opin Pharmacol, 2020, 54: 44-50.
39. Divisato G, Piscitelli S, Elia M, et al. MicroRNAs and stem-like properties: the complex regulation underlying stemness maintenance and cancer development. Biomolecules, 2021, 11(8): 1074. doi: 10.3390/biom11081074.
40. Xiao WS, Li DF, Tang YP, et al. Inhibition of epithelial-mesenchymal transition in gastric cancer cells by miR-711-mediated downregulation of CD44 expression. Oncol Rep, 2018, 40(5): 2844-2853.
41. Pan Y, Shu X, Sun L, et al. miR-196a-5p modulates gastric cancer stem cell characteristics by targeting Smad4. Int J Oncol, 2017, 50(6): 1965-1976.
42. Zhang J, Wang C, Yan S, et al. miR-345 inhibits migration and stem-like cell phenotype in gastric cancer via inactivation of Rac1 by targeting EPS8. Acta Biochim Biophys Sin (Shanghai), 2020, 52(3): 259-267.
43. Wu S, Xie J, Shi H, et al. miR-492 promotes chemoresistance to CDDP and metastasis by targeting inhibiting DNMT3B and induces stemness in gastric cancer. Biosci Rep, 2020, 40(3): BSR20194342. doi: 10.1042/BSR20194342.
44. Shen C, Wang J, Xu Z, et al. ONECUT2 which is targeted by hsa-miR-15a-5p enhances stemness maintenance of gastric cancer stem cells. Exp Biol Med (Maywood), 2021, 246(24): 2645-2659.
45. Zhan P, Shu X, Chen M, et al. miR-98-5p inhibits gastric cancer cell stemness and chemoresistance by targeting branched-chain aminotransferases 1. Life Sci, 2021, 276: 119405. doi: 10.1016/j.lfs.2021.119405.
46. Hwang GR, Yuen JG, Ju J. Roles of microRNAs in gastrointestinal cancer stem cell resistance and therapeutic development. Int J Mol Sci, 2021, 22(4): 1624. doi: 10.3390/ijms22041624.
47. Lee SD, Yu D, Lee DY, et al. Upregulated microRNA-193a-3p is responsible for cisplatin resistance in CD44(+) gastric cancer cells. Cancer Sci, 2019, 110(2): 662-673.
48. Baldessari C, Gelsomino F, Spallanzani A, et al. Beyond the beyond: a case of an extraordinary response to multiple lines of therapy in a de novo metastatic HER2-negative gastric cancer patient. Gastrointest Tumors, 2018, 5(1-2): 14-20.
49. Wei C, Chen M, Deng W, et al. Characterization of gastric cancer stem-like molecular features, immune and pharmacogenomic landscapes. Brief Bioinform, 2022, 23(1): bbab386. doi: 10.1093/bib/bbab386.
50. Peng C, Huang K, Liu G, et al. MiR-876-3p regulates cisplatin resistance and stem cell-like properties of gastric cancer cells by targeting TMED3. J Gastroenterol Hepatol, 2019, 34(10): 1711-1719.
51. 刘云霞, 徐叶峰, 王翌庆, 等. miRNA-139-5p靶向Notch1/Jagged1调控胃癌干细胞增殖转移及益气补肾方的干预作用. 中华中医药杂志, 2021, 36(1): 441-445.
52. Ratti M, Lampis A, Ghidini M, et al. MicroRNAs (miRNAs) and long non-coding RNAs (lncRNAs) as new tools for cancer therapy: first steps from bench to bedside. Target Oncol, 2020, 15(3): 261-278.
53. Hanna J, Hossain GS, Kocerha J. The potential for microRNA therapeutics and clinical research. Front Genet, 2019, 10: 478. doi: 10.3389/fgene.2019.00478.
54. Ganju A, Khan S, Hafeez BB, et al. miRNA nanotherapeutics for cancer. Drug Discov Today, 2017, 22(2): 424-432.
55. Liu Q, Li RT, Qian HQ, et al. Targeted delivery of miR-200c/DOC to inhibit cancer stem cells and cancer cells by the gelatinases-stimuli nanoparticles. Biomaterials, 2013, 34(29): 7191-7203.
56. Qian L, Liu F, Chu Y, et al. MicroRNA-200c nanoparticles sensitized gastric cancer cells to radiotherapy by regulating PD-L1 expression and EMT. Cancer Manag Res, 2020, 12: 12215-12223.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Research progress in the stemness regulation and targeted treatment of microRNA in gastric cancer stem cells

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