Research progress on the effect of non-coding RNA on the radiosensitivity of gastric cancer_West China Medical Journal

Authors：

DONG Na ¹ , DAI Ziying ¹ ,  LIU Xiaojun ^1,2

1. The First Clinical College of Lanzhou University, Lanzhou, Gansu 730000, P. R. China;
2. The Second Division of Radiotherapy, Gansu Provincial Hospital, Lanzhou, Gansu 730000, P. R. China;

Corresponding author：

LIU Xiaojun, Email: xjliu@lzu.edu.cn

Keywords：

Gastric cancer; non-coding RNA; radiotherapy

DOI：

10.7507/1002-0179.202210125

Video：

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Abstract Full text Figures/Tables Video References Cited by

Non-coding RNA (ncRNA) is a newly discovered functional RNA different from messenger RNA, which can participate in the regulation of tumor occurrence and development. Studies have shown that ncRNA can participate in the regulation of radiotherapy response to gastric cancer, and its mechanism may be related to its influence on DNA damage repair, gastric cancer cell stemness, apoptosis, and activation of epidermal growth factor receptor signal pathway. This article summarizes the mechanism of ncRNA regulating the response of gastric cancer to radiotherapy, and looks forward to the potential clinical application of ncRNA in the resistance of gastric cancer to radiotherapy.

Citation： DONG Na, DAI Ziying, LIU Xiaojun. Research progress on the effect of non-coding RNA on the radiosensitivity of gastric cancer. West China Medical Journal, 2023, 38(1): 130-133. doi: 10.7507/1002-0179.202210125 Copy

1.	Goetze OT, Al-Batran SE, Chevallay M, et al. Multimodal treatment in locally advanced gastric cancer. Updates Surg, 2018, 70(2): 173-179.
2.	Lee J, Byun HK, Koom WS, et al. Efficacy of radiotherapy for gastric bleeding associated with advanced gastric cancer. Radiat Oncol, 2021, 16(1): 161.
3.	Lordick F, Nilsson M, Leong T. Adjuvant radiotherapy for gastric cancer-end of the road?. Ann Oncol, 2021, 32(3): 287-289.
4.	Chen X, Liu F, Yu X, et al. An auristatin-based peptide-drug conjugate targeting Kita-Kyushu lung cancer antigen 1 for precision chemoradiotherapy in gastric cancer. Eur J Med Chem, 2022, 241: 114617.
5.	Glinski K, Wasilewska-Tesluk E, Rucinska M, et al. Clinical outcome and toxicity of 3D-conformal radiotherapy combined with chemotherapy based on the Intergroup SWOG 9008/INT0116 study protocol for gastric cancer. J BUON, 2015, 20(2): 428-437.
6.	Zhu X, Wang Y, Tan L, et al. The pivotal role of DNA methylation in the radio-sensitivity of tumor radiotherapy. Cancer Med, 2018, 7(8): 3812-3819.
7.	Yang QS, Li B, Xu G, et al. Long noncoding RNA LINC00483/microRNA-144 regulates radiosensitivity and epithelial-mesenchymal transition in lung adenocarcinoma by interacting with HOXA10. J Cell Physiol, 2019, 234(7): 11805-11821.
8.	Liu F, Huang W, Hong J, et al. Long noncoding RNA LINC00630 promotes radio-resistance by regulating BEX1 gene methylation in colorectal cancer cells. IUBMB Life, 2020, 72(7): 1404-1414.
9.	He Y, Zheng L, Yuan M, et al. Exosomal circPRRX1 functions as a ceRNA for miR-596 to promote the proliferation, migration, invasion, and reduce radiation sensitivity of gastric cancer cells via the upregulation of NF-κB activating protein. Anticancer Drugs, 2022, 33(10): 1114-1125.
10.	Zhang X, Yang J. Role of non-coding RNAs on the radiotherapy sensitivity and resistance of head and neck cancer: from basic research to clinical application. Front Cell Dev Biol, 2021, 8: 637435.
11.	Carrassa L, Damia G. DNA damage response inhibitors: mechanisms and potential applications in cancer therapy. Cancer Treat Rev, 2017, 60: 139-151.
12.	Hu H, Zhao X, Jin Z, et al. Hsa-let-7g miRNA regulates the anti-tumor effects of gastric cancer cells under oxidative stress through the expression of DDR genes. J Toxicol Sci, 2015, 40(3): 329-338.
13.	Thapar R. Regulation of DNA double-strand break repair by non-coding RNAs. Molecules, 2018, 23(11): 2789.
14.	Shen YN, Bae IS, Park GH, et al. MicroRNA-196b enhances the radiosensitivity of SNU-638 gastric cancer cells by targeting RAD23B. Biomed Pharmacother, 2018, 105: 362-369.
15.	Jang YY, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood, 2007, 110(8): 3056-3063.
16.	赵瑞南. 长链非编码 RNA HNF1A-AS1 在胃癌细胞干性维持中的作用及相关机制研究. 济南: 山东大学, 2021: 1-55.
17.	Fan D, Ren B, Yang X, et al. Upregulation of miR-501-5p activates the wnt/β-catenin signaling pathway and enhances stem cell-like phenotype in gastric cancer. J Exp Clin Cancer Res, 2016, 35(1): 177.
18.	Xia Y, Lv J, Jiang T, et al. CircFAM73A promotes the cancer stem cell-like properties of gastric cancer through the miR-490-3p/HMGA2 positive feedback loop and HNRNPK-mediated β-catenin stabilization. J Exp Clin Cancer Res, 2021, 40(1): 103.
19.	Xiao Y, Pan J, Geng Q, et al. LncRNA MALAT1 increases the stemness of gastric cancer cells via enhancing SOX2 mRNA stability. FEBS Open Bio, 2019, 9(7): 1212-1222.
20.	Ji Q, Hao X, Meng Y, et al. Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer, 2008, 8: 266.
21.	Liu Y, Xing R, Zhang X, et al. miR-375 targets the p53 gene to regulate cellular response to ionizing radiation and etoposide in gastric cancer cells. DNA Repair (Amst), 2013, 12(9): 741-750.
22.	Chun-Zhi Z, Lei H, An-Ling Z, et al. MicroRNA-221 and microRNA-222 regulate gastric carcinoma cell proliferation and radioresistance by targeting PTEN. BMC Cancer, 2010, 10: 367.
23.	王宝军, 周爱萍, 周红. 长链非编码 RNA GAS5 调控 miR-196a 抑制胃癌细胞增殖、诱导凋亡及放射增敏的机制. 中国老年学杂志, 2021, 41(4): 853-857.
24.	Zhen Y, Guanghui L, Xiefu Z. Knockdown of EGFR inhibits growth and invasion of gastric cancer cells. Cancer Gene Ther, 2014, 21(11): 491-497.
25.	Ji F, Sha H, Meng F, et al. Tumor-penetrating peptide fused EGFR single-domain antibody enhances radiation responses following EGFR inhibition in gastric cancer. Oncol Rep, 2018, 40(3): 1583-1591.
26.	Baumann M, Krause M. Targeting the epidermal growth factor receptor in radiotherapy: radiobiological mechanisms, preclinical and clinical results. Radiother Oncol, 2004, 72(3): 257-266.
27.	Ning T, Zhang H, Wang X, et al. miR-370 regulates cell proliferation and migration by targeting EGFR in gastric cancer. Oncol Rep, 2017, 38(1): 384-392.
28.	Kogo R, Mimori K, Tanaka F, et al. Clinical significance of miR-146a in gastric cancer cases. Clin Cancer Res, 2011, 17(13): 4277-4284.
29.	Wang Y, Zhang H, Ge S, et al. Effects of miR-138-5p and miR-204-5p on the migration and proliferation of gastric cancer cells by targeting EGFR. Oncol Rep, 2018, 39(6): 2624-2634.
30.	Zhou J, Wu L, Li W, et al. Long noncoding RNA LINC01485 promotes tumor growth and migration via inhibiting EGFR ubiquitination and activating EGFR/Akt signaling in gastric cancer. Onco Targets Ther, 2020, 13: 8413-8425.
31.	Li C, Zhang J, Zhou Y, et al. Long non-coding RNA CASC9 promotes the progression and development of gastric cancer via regulating miR-370/EGFR axis. Dig Liver Dis, 2021, 53(4): 509-516.
32.	Marie-Egyptienne DT, Lohse I, Hill RP. Cancer stem cells, the epithelial to mesenchymal transition (EMT) and radioresistance: potential role of hypoxia. Cancer Lett, 2013, 341(1): 63-72.
33.	Liu XH, Sun M, Nie FQ, et al. Lnc RNA HOTAIR functions as a competing endogenous RNA to regulate HER2 expression by sponging miR-331-3p in gastric cancer. Mol Cancer, 2014, 13: 92.
34.	Yao Z, Zhang Y, Xu D, et al. Research progress on long non-coding RNA and radiotherapy. Med Sci Monit, 2019, 25: 5757-5770.
35.	Chen Z, Wu J, Huang W, et al. Long non-coding RNA RP11-789C1. 1 suppresses epithelial to mesenchymal transition in gastric cancer through the RP11-789C1. 1/MiR-5003/E-Cadherin axis. Cell Physiol Biochem, 2018, 47(6): 2432-2444.
36.	Zhou X, Ye F, Yin C, et al. The interaction between miR-141 and lncRNA-H19 in regulating cell proliferation and migration in gastric cancer. Cell Physiol Biochem, 2015, 36(4): 1440-1452.
37.	郭佳星, 郁志龙, 宝莹娜. 恶性肿瘤糖代谢与放射治疗关系的研究进展. 肿瘤代谢与营养电子杂志, 2017, 4(4): 390-396.
38.	Broadley K, Larsen L, Herst PM, et al. The novel phloroglucinol PMT7 kills glycolytic cancer cells by blocking autophagy and sensitizing to nutrient stress. J Cell Biochem, 2011, 112(7): 1869-1879.
39.	Li L, Liu H, Du L, et al. miR-449a suppresses LDHA-mediated glycolysis to enhance the sensitivity of non-small cell lung cancer cells to ionizing radiation. Oncol Res, 2018, 26(4): 547-556.
40.	Fan L, Huang C, Li J, et al. Long non-coding RNA urothelial cancer associated 1 regulates radioresistance via the hexokinase 2/glycolytic pathway in cervical cancer. Int J Mol Med, 2018, 42(4): 2247-2259.
41.	Guan Y, Cao Z, Du J, et al. Circular RNA circPITX1 knockdown inhibits glycolysis to enhance radiosensitivity of glioma cells by miR-329-3p/NEK2 axis. Cancer Cell Int, 2020, 20: 80.
42.	Qian Y, Wu X, Wang H, et al. MicroRNA-4290 suppresses PDK1-mediated glycolysis to enhance the sensitivity of gastric cancer cell to cisplatin. Braz J Med Biol Res, 2020, 53(5): e9330.
43.	Jin HF, Wang JF, Shao M, et al. Down-regulation of miR-7 in gastric cancer is associated with elevated LDH-A expression and chemoresistance to cisplatin. Front Cell Dev Biol, 2020, 8: 555937.
44.	Cohen NA, Lai SY, Ziober AF, et al. Dysregulation of hypoxia inducible factor-1alpha in head and neck squamous cell carcinoma cell lines correlates with invasive potential. Laryngoscope, 2004, 114(3): 418-423.
45.	Meijer TW, Kaanders JH, Span PN, et al. Targeting hypoxia, HIF-1, and tumor glucose metabolism to improve radiotherapy efficacy. Clin Cancer Res, 2012, 18(20): 5585-5594.
46.	Cao L, Wang M, Dong Y, et al. Circular RNA circRNF20 promotes breast cancer tumorigenesis and Warburg effect through miR-487a/HIF-1α/HK2. Cell Death Dis, 2020, 11(2): 145.
47.	Zhou L, Wang Y, Zhou M, et al. HOXA9 inhibits HIF-1α-mediated glycolysis through interacting with CRIP2 to repress cutaneous squamous cell carcinoma development. Nat Commun, 2018, 9(1): 1480.
48.	Zhu T, Wang Z, Wang G, et al. Long non-coding RNA ZFAS1 promotes the expression of EPAS1 in gastric cardia adenocarcinoma. J Adv Res, 2020, 28: 7-15.
49.	Wang J, Yu Z, Wang J, et al. LncRNA NUTM2A-AS1 positively modulates TET1 and HIF-1A to enhance gastric cancer tumorigenesis and drug resistance by sponging miR-376a. Cancer Med, 2020, 9(24): 9499-9510.

1. Goetze OT, Al-Batran SE, Chevallay M, et al. Multimodal treatment in locally advanced gastric cancer. Updates Surg, 2018, 70(2): 173-179.
2. Lee J, Byun HK, Koom WS, et al. Efficacy of radiotherapy for gastric bleeding associated with advanced gastric cancer. Radiat Oncol, 2021, 16(1): 161.
3. Lordick F, Nilsson M, Leong T. Adjuvant radiotherapy for gastric cancer-end of the road?. Ann Oncol, 2021, 32(3): 287-289.
4. Chen X, Liu F, Yu X, et al. An auristatin-based peptide-drug conjugate targeting Kita-Kyushu lung cancer antigen 1 for precision chemoradiotherapy in gastric cancer. Eur J Med Chem, 2022, 241: 114617.
5. Glinski K, Wasilewska-Tesluk E, Rucinska M, et al. Clinical outcome and toxicity of 3D-conformal radiotherapy combined with chemotherapy based on the Intergroup SWOG 9008/INT0116 study protocol for gastric cancer. J BUON, 2015, 20(2): 428-437.
6. Zhu X, Wang Y, Tan L, et al. The pivotal role of DNA methylation in the radio-sensitivity of tumor radiotherapy. Cancer Med, 2018, 7(8): 3812-3819.
7. Yang QS, Li B, Xu G, et al. Long noncoding RNA LINC00483/microRNA-144 regulates radiosensitivity and epithelial-mesenchymal transition in lung adenocarcinoma by interacting with HOXA10. J Cell Physiol, 2019, 234(7): 11805-11821.
8. Liu F, Huang W, Hong J, et al. Long noncoding RNA LINC00630 promotes radio-resistance by regulating BEX1 gene methylation in colorectal cancer cells. IUBMB Life, 2020, 72(7): 1404-1414.
9. He Y, Zheng L, Yuan M, et al. Exosomal circPRRX1 functions as a ceRNA for miR-596 to promote the proliferation, migration, invasion, and reduce radiation sensitivity of gastric cancer cells via the upregulation of NF-κB activating protein. Anticancer Drugs, 2022, 33(10): 1114-1125.
10. Zhang X, Yang J. Role of non-coding RNAs on the radiotherapy sensitivity and resistance of head and neck cancer: from basic research to clinical application. Front Cell Dev Biol, 2021, 8: 637435.
11. Carrassa L, Damia G. DNA damage response inhibitors: mechanisms and potential applications in cancer therapy. Cancer Treat Rev, 2017, 60: 139-151.
12. Hu H, Zhao X, Jin Z, et al. Hsa-let-7g miRNA regulates the anti-tumor effects of gastric cancer cells under oxidative stress through the expression of DDR genes. J Toxicol Sci, 2015, 40(3): 329-338.
13. Thapar R. Regulation of DNA double-strand break repair by non-coding RNAs. Molecules, 2018, 23(11): 2789.
14. Shen YN, Bae IS, Park GH, et al. MicroRNA-196b enhances the radiosensitivity of SNU-638 gastric cancer cells by targeting RAD23B. Biomed Pharmacother, 2018, 105: 362-369.
15. Jang YY, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood, 2007, 110(8): 3056-3063.
16. 赵瑞南. 长链非编码 RNA HNF1A-AS1 在胃癌细胞干性维持中的作用及相关机制研究. 济南: 山东大学, 2021: 1-55.
17. Fan D, Ren B, Yang X, et al. Upregulation of miR-501-5p activates the wnt/β-catenin signaling pathway and enhances stem cell-like phenotype in gastric cancer. J Exp Clin Cancer Res, 2016, 35(1): 177.
18. Xia Y, Lv J, Jiang T, et al. CircFAM73A promotes the cancer stem cell-like properties of gastric cancer through the miR-490-3p/HMGA2 positive feedback loop and HNRNPK-mediated β-catenin stabilization. J Exp Clin Cancer Res, 2021, 40(1): 103.
19. Xiao Y, Pan J, Geng Q, et al. LncRNA MALAT1 increases the stemness of gastric cancer cells via enhancing SOX2 mRNA stability. FEBS Open Bio, 2019, 9(7): 1212-1222.
20. Ji Q, Hao X, Meng Y, et al. Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer, 2008, 8: 266.
21. Liu Y, Xing R, Zhang X, et al. miR-375 targets the p53 gene to regulate cellular response to ionizing radiation and etoposide in gastric cancer cells. DNA Repair (Amst), 2013, 12(9): 741-750.
22. Chun-Zhi Z, Lei H, An-Ling Z, et al. MicroRNA-221 and microRNA-222 regulate gastric carcinoma cell proliferation and radioresistance by targeting PTEN. BMC Cancer, 2010, 10: 367.
23. 王宝军, 周爱萍, 周红. 长链非编码 RNA GAS5 调控 miR-196a 抑制胃癌细胞增殖、诱导凋亡及放射增敏的机制. 中国老年学杂志, 2021, 41(4): 853-857.
24. Zhen Y, Guanghui L, Xiefu Z. Knockdown of EGFR inhibits growth and invasion of gastric cancer cells. Cancer Gene Ther, 2014, 21(11): 491-497.
25. Ji F, Sha H, Meng F, et al. Tumor-penetrating peptide fused EGFR single-domain antibody enhances radiation responses following EGFR inhibition in gastric cancer. Oncol Rep, 2018, 40(3): 1583-1591.
26. Baumann M, Krause M. Targeting the epidermal growth factor receptor in radiotherapy: radiobiological mechanisms, preclinical and clinical results. Radiother Oncol, 2004, 72(3): 257-266.
27. Ning T, Zhang H, Wang X, et al. miR-370 regulates cell proliferation and migration by targeting EGFR in gastric cancer. Oncol Rep, 2017, 38(1): 384-392.
28. Kogo R, Mimori K, Tanaka F, et al. Clinical significance of miR-146a in gastric cancer cases. Clin Cancer Res, 2011, 17(13): 4277-4284.
29. Wang Y, Zhang H, Ge S, et al. Effects of miR-138-5p and miR-204-5p on the migration and proliferation of gastric cancer cells by targeting EGFR. Oncol Rep, 2018, 39(6): 2624-2634.
30. Zhou J, Wu L, Li W, et al. Long noncoding RNA LINC01485 promotes tumor growth and migration via inhibiting EGFR ubiquitination and activating EGFR/Akt signaling in gastric cancer. Onco Targets Ther, 2020, 13: 8413-8425.
31. Li C, Zhang J, Zhou Y, et al. Long non-coding RNA CASC9 promotes the progression and development of gastric cancer via regulating miR-370/EGFR axis. Dig Liver Dis, 2021, 53(4): 509-516.
32. Marie-Egyptienne DT, Lohse I, Hill RP. Cancer stem cells, the epithelial to mesenchymal transition (EMT) and radioresistance: potential role of hypoxia. Cancer Lett, 2013, 341(1): 63-72.
33. Liu XH, Sun M, Nie FQ, et al. Lnc RNA HOTAIR functions as a competing endogenous RNA to regulate HER2 expression by sponging miR-331-3p in gastric cancer. Mol Cancer, 2014, 13: 92.
34. Yao Z, Zhang Y, Xu D, et al. Research progress on long non-coding RNA and radiotherapy. Med Sci Monit, 2019, 25: 5757-5770.
35. Chen Z, Wu J, Huang W, et al. Long non-coding RNA RP11-789C1. 1 suppresses epithelial to mesenchymal transition in gastric cancer through the RP11-789C1. 1/MiR-5003/E-Cadherin axis. Cell Physiol Biochem, 2018, 47(6): 2432-2444.
36. Zhou X, Ye F, Yin C, et al. The interaction between miR-141 and lncRNA-H19 in regulating cell proliferation and migration in gastric cancer. Cell Physiol Biochem, 2015, 36(4): 1440-1452.
37. 郭佳星, 郁志龙, 宝莹娜. 恶性肿瘤糖代谢与放射治疗关系的研究进展. 肿瘤代谢与营养电子杂志, 2017, 4(4): 390-396.
38. Broadley K, Larsen L, Herst PM, et al. The novel phloroglucinol PMT7 kills glycolytic cancer cells by blocking autophagy and sensitizing to nutrient stress. J Cell Biochem, 2011, 112(7): 1869-1879.
39. Li L, Liu H, Du L, et al. miR-449a suppresses LDHA-mediated glycolysis to enhance the sensitivity of non-small cell lung cancer cells to ionizing radiation. Oncol Res, 2018, 26(4): 547-556.
40. Fan L, Huang C, Li J, et al. Long non-coding RNA urothelial cancer associated 1 regulates radioresistance via the hexokinase 2/glycolytic pathway in cervical cancer. Int J Mol Med, 2018, 42(4): 2247-2259.
41. Guan Y, Cao Z, Du J, et al. Circular RNA circPITX1 knockdown inhibits glycolysis to enhance radiosensitivity of glioma cells by miR-329-3p/NEK2 axis. Cancer Cell Int, 2020, 20: 80.
42. Qian Y, Wu X, Wang H, et al. MicroRNA-4290 suppresses PDK1-mediated glycolysis to enhance the sensitivity of gastric cancer cell to cisplatin. Braz J Med Biol Res, 2020, 53(5): e9330.
43. Jin HF, Wang JF, Shao M, et al. Down-regulation of miR-7 in gastric cancer is associated with elevated LDH-A expression and chemoresistance to cisplatin. Front Cell Dev Biol, 2020, 8: 555937.
44. Cohen NA, Lai SY, Ziober AF, et al. Dysregulation of hypoxia inducible factor-1alpha in head and neck squamous cell carcinoma cell lines correlates with invasive potential. Laryngoscope, 2004, 114(3): 418-423.
45. Meijer TW, Kaanders JH, Span PN, et al. Targeting hypoxia, HIF-1, and tumor glucose metabolism to improve radiotherapy efficacy. Clin Cancer Res, 2012, 18(20): 5585-5594.
46. Cao L, Wang M, Dong Y, et al. Circular RNA circRNF20 promotes breast cancer tumorigenesis and Warburg effect through miR-487a/HIF-1α/HK2. Cell Death Dis, 2020, 11(2): 145.
47. Zhou L, Wang Y, Zhou M, et al. HOXA9 inhibits HIF-1α-mediated glycolysis through interacting with CRIP2 to repress cutaneous squamous cell carcinoma development. Nat Commun, 2018, 9(1): 1480.
48. Zhu T, Wang Z, Wang G, et al. Long non-coding RNA ZFAS1 promotes the expression of EPAS1 in gastric cardia adenocarcinoma. J Adv Res, 2020, 28: 7-15.
49. Wang J, Yu Z, Wang J, et al. LncRNA NUTM2A-AS1 positively modulates TET1 and HIF-1A to enhance gastric cancer tumorigenesis and drug resistance by sponging miR-376a. Cancer Med, 2020, 9(24): 9499-9510.

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