miR-584-5p inhibited the biological behavior of breast cancer cells by down-regulating MMP-14_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

LIU Chenmeiqi ¹ ,  LI Hailin ²

1. Clinical Medical College of Jiamusi University, Jiamusi, Heilongjiang 154007, P. R. China;
2. Department of Second General Surgery, Hongqi Hospital Affiliated to Mudanjiang Medical College, Mudanjiang, Heilongjiang 157011, P. R. China;

Corresponding?author：

LI Hailin, Email: 874713051@qq.com

Keywords：

microRNA-584-5p; matrix metalloproteinase-14; breast cancer; biological behavior

DOI：

10.7507/1007-9424.202210002

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Objective To investigate the effect of microRNA-584-5p (miR-584-5p) on the biological behavior (proliferation, migration and invasion) of breast cancer cells and its mechanism. Methods Human normal breast epithelial cells MCF10A and breast cancer cells MDA-MB-231, SK-BR-3 and MCF-7 were selected; take MCF-7 cells in logarithmic growth phase, transfect them with Lipofectamine^TM 2000 transfection kit, and divide them into seven groups: blank group (untransfected MCF-7 cells), mimic-negative control (mimic-NC) group (transfected mimic-NC), miR-584-5p mimic group (transfected miR-584-5p mimic), pcDNA group [transfected with overexpression of matrix metalloproteinase-14 (MMP-14) pcDNA3.1 plasmid negative control (pcDNA3.1)], MMP-14 group [transfected with overexpression of MMP-14 pcDNA3.1 plasmid (pcDNA3.1-MMP-14)], mimic-NC+MMP-14 group (co-transfected with mimic NC and pcDNA3.1-MMP-14), and miR-584-5p mimic+MMP-14 group (co-transfected with miR-584-5p mimic and pcDNA3.1-MMP-14). The mRNA expression levels of miR-584-5p in MCF10A, MDA-MB-231, SK-BR-3 and MCF-7 cells and the expression levels of miR-584-5p and MMP-14 mRNA of MCF-7 cell in each group were detected by fluorescence quantitative PCR. The protein expressions of MMP-14 of MCF-7 cell in each group were detected by Western blotting. The proliferation, migration and invasion of MCF-7 cell in each group were detected by cell counting kit - 8 (CCK-8), scratch test and Transwell test. The targeting relationship between miR-584-5p and MMP-14 was detected by double luciferase reporter gene assay. Results Compared with the human normal mammary epithelial cells MCF10A, the expression levels of miR-584-5p in breast cancer cells MDA-MB-231, SK-BR-3 and MCF-7 were decreased (P<0.05), and the expression level of miR-584-5p in MCF-7 cells was the lowest. Compared with the blank group and the mimic-NC group, the expression level of miR-584-5p of MCF-7 cells in the miR-584-5p mimic group was increased, and the expression levels of MMP-14 mRNA and protein, proliferation activity, scratch healing rate and invasive cell number were decreased or reduced (P<0.05). Compared with the blank group and the pcDNA group, the expression levels of MMP-14 mRNA and protein, proliferation activity, scratch healing rate and invasive cell number of MCF-7 cells in the MMP-14 group were increased (P<0.05). Compared with the MMP-14 group and the mimic-NC+MMP-14 group, the expression level of miR-584-5p of MCF-7 cells in the miR-584-5p mimic+MMP-14 group was increased, the expression levels of MMP-14 mRNA and protein, proliferation activity, scratch healing rate and invasive cell number were decreased or reduced (P<0.05). The expression levels of MMP-14 mRNA and protein, proliferation activity, scratch healing rate and invasive cell number of MCF-7 cells in the miR-584-5p mimic+MMP-14 group were higher or morer than those in the miR-584-5p mimic group (P<0.05). The results of double luciferase reporter gene test showed that miR-584-5p could targeted action on the MMP-14 promoter region. Conclusions MiR-584-5p can targetable regulate the expression of MMP-14. Overexpression of miR-584-5p inhibits the proliferation, migration and invasion of breast cancer cells by down-regulating MMP-14.

Citation： LIU Chenmeiqi, LI Hailin. miR-584-5p inhibited the biological behavior of breast cancer cells by down-regulating MMP-14. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2023, 30(3): 302-308. doi: 10.7507/1007-9424.202210002 Copy

1.	Yau C, Osdoit M, van der Noordaa M, et al. Residual cancer burden after neoadjuvant chemotherapy and long-term survival outcomes in breast cancer: a multicentre pooled analysis of 5 161 patients. Lancet Oncol, 2022, 23(1): 149-160.
2.	Katsura C, Ogunmwonyi I, Kankam HK, et al. Breast cancer: presentation, investigation and management. Br J Hosp Med (Lond), 2022, 83(2): 1-7.
3.	Chlebowski RT, Aragaki AK, Pan K. Breast cancer prevention and breast cancer mortality. JCO Oncol Pract, 2022, 18(7): 522-523.
4.	Baranova A, Krasnoselskyi M, Starikov V, et al. Triple-negative breast cancer: current treatment strategies and factors of negative prognosis. J Med Life, 2022, 15(2): 153-161.
5.	Huang Y, Wang X, Zheng Y, et al. Construction of an mRNA-miRNA-lncRNA network prognostic for triple-negative breast cancer. Aging (Albany NY), 2021, 13(1): 1153-1175.
6.	Li Q, Li Z, Wei S, et al. Overexpression of miR-584-5p inhibits proliferation and induces apoptosis by targeting WW domain-containing E3 ubiquitin protein ligase 1 in gastric cancer. J Exp Clin Cancer Res, 2017, 36(1): 59-75.
7.	Chen N, Zhang G, Fu J, et al. Matrix metalloproteinase-14 (MMP-14) downregulation inhibits esophageal squamous cell carcinoma cell migration, invasion, and proliferation. Thorac Cancer, 2020, 11(11): 3168-3174.
8.	王婧, 毛杰, 周蓓, 等. MMP-14和c-myc基因在乳腺癌組織中表達及臨床意義. 生物醫學工程與臨床, 2020, 24(1): 81-86.
9.	Diener C, Keller A, Meese E. Emerging concepts of miRNA therapeutics: from cells to clinic. Trends Genet, 2022, 38(6): 613-626.
10.	張蘭, 徐源, 趙冰, 等. miR-92a在乳腺癌組織中表達及通過靶向調控KLF4影響乳腺癌細胞的遷移及侵襲行為. 中國普外基礎與臨床雜志, 2022, 29(2): 173-178.
11.	Zhang X, Xiong H, Zhao Y, et al. Circular RNA LONP2 regulates proliferation, invasion, and apoptosis of bladder cancer cells by sponging microRNA-584-5p. Bioengineered, 2022, 13(4): 8823-8835.
12.	Chen X, Li G, Zhong G, et al. Long non-coding RNA DUXAP8 acts as an oncogene in sinonasal squamous cell carcinoma through miR-584-5p/FNDC3B pathway. Am J Rhinol Allergy, 2022, 36(6): 708-718.
13.	王時梅, 黃永塔, 葉秋容, 等. miR-584-5p對鼻咽癌遠處轉移及臨床預后的預測作用. 廣東醫學, 2018, 39(18): 2746-2749.
14.	Ma D, Qin Y, Huang C, et al. Circular RNA ABCB10 promotes non-small cell lung cancer progression by increasing E2F5 expression through sponging miR-584-5p. Cell Cycle, 2020, 19(13): 1611-1620.
15.	Liu Q, Wang C, Jiang Z, et al. circRNA 001306 enhances hepatocellular carcinoma growth by up-regulating CDK16 expression via sponging miR-584-5p. J Cell Mol Med, 2020, 24(24): 14306-14315.
16.	Lee SB, Park YS, Sung JS, et al. Tumor suppressor miR-584-5p inhibits migration and invasion in smoking related non-small cell lung cancer cells by targeting YKT6. Cancers (Basel), 2021, 13(5): 1159-1178.
17.	Vos MC, Hollemans E, van der Steen SCHA, et al. Primary ovarian tumors with lymphogenic and hematogenic metastasis express high MMP-14, which colocalizes with highly sulfated chondroitin sulfate in the stroma. Int J Gynecol Pathol, 2020, 39(2): 184-192.
18.	Butler SS, Date K, Okumura T, et al. Membrane-bound MMP-14 protease-activatable adeno-associated viral vectors for gene delivery to pancreatic tumors. Gene Ther, 2022, 29(3-4): 138-146.
19.	吐爾遜江·艾力, 曹國磊, 陳慧芳, 等. miR-9和MMP-14在非小細胞肺癌中的表達及臨床意義. 臨床腫瘤學雜志, 2021, 26(6): 554-558.
20.	李剛, 劉江豪, 羅璟璐, 等. MMP14通過調節Wnt/β-catenin信號通路影響胃癌的發生、發展機制研究. 醫學研究雜志, 2020, 49(2): 92-98.
21.	王小清, 王金蓮, 林帥, 等. miR-369-3p靶向MMP14調節乳頭狀甲狀腺癌細胞侵襲、遷移和上皮間質轉化的作用. 中國免疫學雜志, 2019, 35(21): 2576-2581.
22.	Di D, Chen L, Guo Y, et al. Association of BCSC-1 and MMP-14 with human breast cancer. Oncol Lett, 2018, 15(4): 5020-5026.
23.	Xiang X, Mei H, Qu H, et al. miRNA-584-5p exerts tumor suppressive functions in human neuroblastoma through repressing transcription of matrix metalloproteinase 14. Biochim Biophys Acta, 2015, 1852(9): 1743-1754.
24.	Guo T, Zheng C, Wang Z, et al. miR-584-5p regulates migration and invasion in non-small cell lung cancer cell lines through regulation of MMP-14. Mol Med Rep, 2019, 19(3): 1747-1752.
25.	Liu Z, Lu J, Fang H, et al. m6A modification-mediated DUXAP8 regulation of malignant phenotype and chemotherapy resistance of hepatocellular carcinoma through miR-584-5p/MAPK1/ERK pathway axis. Front Cell Dev Biol, 2021, 9: 783385. doi: 10.3389/fcell.2021.783385.
26.	尚希, 葉玉平, 方紅燕, 等. Fbxw7上調對乳腺癌MDA-MB-231細胞侵襲、遷移及MAPK/ERK通路的影響. 重慶醫學, 2020, 49(7): 1058-1062.
27.	Safi A, Heidarian E, Ahmadi R. Quercetin synergistically enhances the anticancer efficacy of docetaxel through induction of apoptosis and modulation of PI3K/AKT, MAPK/ERK, and JAK/STAT3 signaling pathways in MDA-MB-231 breast cancer cell line. Int J Mol Cell Med, 2021, 10(1): 11-22.

1. Yau C, Osdoit M, van der Noordaa M, et al. Residual cancer burden after neoadjuvant chemotherapy and long-term survival outcomes in breast cancer: a multicentre pooled analysis of 5 161 patients. Lancet Oncol, 2022, 23(1): 149-160.
2. Katsura C, Ogunmwonyi I, Kankam HK, et al. Breast cancer: presentation, investigation and management. Br J Hosp Med (Lond), 2022, 83(2): 1-7.
3. Chlebowski RT, Aragaki AK, Pan K. Breast cancer prevention and breast cancer mortality. JCO Oncol Pract, 2022, 18(7): 522-523.
4. Baranova A, Krasnoselskyi M, Starikov V, et al. Triple-negative breast cancer: current treatment strategies and factors of negative prognosis. J Med Life, 2022, 15(2): 153-161.
5. Huang Y, Wang X, Zheng Y, et al. Construction of an mRNA-miRNA-lncRNA network prognostic for triple-negative breast cancer. Aging (Albany NY), 2021, 13(1): 1153-1175.
6. Li Q, Li Z, Wei S, et al. Overexpression of miR-584-5p inhibits proliferation and induces apoptosis by targeting WW domain-containing E3 ubiquitin protein ligase 1 in gastric cancer. J Exp Clin Cancer Res, 2017, 36(1): 59-75.
7. Chen N, Zhang G, Fu J, et al. Matrix metalloproteinase-14 (MMP-14) downregulation inhibits esophageal squamous cell carcinoma cell migration, invasion, and proliferation. Thorac Cancer, 2020, 11(11): 3168-3174.
8. 王婧, 毛杰, 周蓓, 等. MMP-14和c-myc基因在乳腺癌組織中表達及臨床意義. 生物醫學工程與臨床, 2020, 24(1): 81-86.
9. Diener C, Keller A, Meese E. Emerging concepts of miRNA therapeutics: from cells to clinic. Trends Genet, 2022, 38(6): 613-626.
10. 張蘭, 徐源, 趙冰, 等. miR-92a在乳腺癌組織中表達及通過靶向調控KLF4影響乳腺癌細胞的遷移及侵襲行為. 中國普外基礎與臨床雜志, 2022, 29(2): 173-178.
11. Zhang X, Xiong H, Zhao Y, et al. Circular RNA LONP2 regulates proliferation, invasion, and apoptosis of bladder cancer cells by sponging microRNA-584-5p. Bioengineered, 2022, 13(4): 8823-8835.
12. Chen X, Li G, Zhong G, et al. Long non-coding RNA DUXAP8 acts as an oncogene in sinonasal squamous cell carcinoma through miR-584-5p/FNDC3B pathway. Am J Rhinol Allergy, 2022, 36(6): 708-718.
13. 王時梅, 黃永塔, 葉秋容, 等. miR-584-5p對鼻咽癌遠處轉移及臨床預后的預測作用. 廣東醫學, 2018, 39(18): 2746-2749.
14. Ma D, Qin Y, Huang C, et al. Circular RNA ABCB10 promotes non-small cell lung cancer progression by increasing E2F5 expression through sponging miR-584-5p. Cell Cycle, 2020, 19(13): 1611-1620.
15. Liu Q, Wang C, Jiang Z, et al. circRNA 001306 enhances hepatocellular carcinoma growth by up-regulating CDK16 expression via sponging miR-584-5p. J Cell Mol Med, 2020, 24(24): 14306-14315.
16. Lee SB, Park YS, Sung JS, et al. Tumor suppressor miR-584-5p inhibits migration and invasion in smoking related non-small cell lung cancer cells by targeting YKT6. Cancers (Basel), 2021, 13(5): 1159-1178.
17. Vos MC, Hollemans E, van der Steen SCHA, et al. Primary ovarian tumors with lymphogenic and hematogenic metastasis express high MMP-14, which colocalizes with highly sulfated chondroitin sulfate in the stroma. Int J Gynecol Pathol, 2020, 39(2): 184-192.
18. Butler SS, Date K, Okumura T, et al. Membrane-bound MMP-14 protease-activatable adeno-associated viral vectors for gene delivery to pancreatic tumors. Gene Ther, 2022, 29(3-4): 138-146.
19. 吐爾遜江·艾力, 曹國磊, 陳慧芳, 等. miR-9和MMP-14在非小細胞肺癌中的表達及臨床意義. 臨床腫瘤學雜志, 2021, 26(6): 554-558.
20. 李剛, 劉江豪, 羅璟璐, 等. MMP14通過調節Wnt/β-catenin信號通路影響胃癌的發生、發展機制研究. 醫學研究雜志, 2020, 49(2): 92-98.
21. 王小清, 王金蓮, 林帥, 等. miR-369-3p靶向MMP14調節乳頭狀甲狀腺癌細胞侵襲、遷移和上皮間質轉化的作用. 中國免疫學雜志, 2019, 35(21): 2576-2581.
22. Di D, Chen L, Guo Y, et al. Association of BCSC-1 and MMP-14 with human breast cancer. Oncol Lett, 2018, 15(4): 5020-5026.
23. Xiang X, Mei H, Qu H, et al. miRNA-584-5p exerts tumor suppressive functions in human neuroblastoma through repressing transcription of matrix metalloproteinase 14. Biochim Biophys Acta, 2015, 1852(9): 1743-1754.
24. Guo T, Zheng C, Wang Z, et al. miR-584-5p regulates migration and invasion in non-small cell lung cancer cell lines through regulation of MMP-14. Mol Med Rep, 2019, 19(3): 1747-1752.
25. Liu Z, Lu J, Fang H, et al. m6A modification-mediated DUXAP8 regulation of malignant phenotype and chemotherapy resistance of hepatocellular carcinoma through miR-584-5p/MAPK1/ERK pathway axis. Front Cell Dev Biol, 2021, 9: 783385. doi: 10.3389/fcell.2021.783385.
26. 尚希, 葉玉平, 方紅燕, 等. Fbxw7上調對乳腺癌MDA-MB-231細胞侵襲、遷移及MAPK/ERK通路的影響. 重慶醫學, 2020, 49(7): 1058-1062.
27. Safi A, Heidarian E, Ahmadi R. Quercetin synergistically enhances the anticancer efficacy of docetaxel through induction of apoptosis and modulation of PI3K/AKT, MAPK/ERK, and JAK/STAT3 signaling pathways in MDA-MB-231 breast cancer cell line. Int J Mol Cell Med, 2021, 10(1): 11-22.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

miR-584-5p inhibited the biological behavior of breast cancer cells by down-regulating MMP-14

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