Extracellular Vesicles Carry LncRNA SNHG16 to Promote Metastasis of Breast Cancer Cells the MiR-892b/PPAPDC1A Axis

Overview

Journal Front Cell Dev Biol

Specialty Cell Biology

Date 2021 Jul 12

PMID 34249903

Citations 13

Authors

Wenfei Xia

Yun Liu

Teng Cheng

Tao Xu

Menglu Dong

Xiaopeng Hu

Affiliations

Soon will be listed here.

Abstract

Breast cancer (BC) represents the most commonly diagnosed malignancy among women. Long non-coding RNAs (lncRNAs) can be transferred by extracellular vesicles (EVs) to participate in BC progression. This study demonstrated that SNHG16 expression was significantly increased in BC tissues and cells. Overexpression of SNHG16 promoted the migration, invasion, and epithelial-mesenchymal transition (EMT) of BC cells. SNHG16 was carried by EVs. Bioinformatics analysis predicted that SNHG16 regulated PPAPDC1A expression by sponging miR-892b, which was confirmed by RNA-fluorescence hybridization (FISH), RT-qPCR, dual-luciferase gene reporter assay, and RNA immunoprecipitation (RIP). MDA-MB-157 and HS578T cells were transfected with pcDNA3.1-SNHG16, miR-892b-mimic, or si-PPAPDC1A for functional rescue experiments , and the cells were treated with MDA-MB-231 cell-derived EVs. The results confirmed that enhanced miR-892b expression partially eliminated the increase of migration, invasion, and EMT of BC cells mediated by SNHG16 or EVs. The lung metastasis model in nude mice was established by injecting HS578T cells tail vein. The results showed that si-SNHG16 reduced the metastatic nodules and decreased the vimentin expression. In conclusion, EVs derived from BC cells transferred SNHG16 the miR-892b/PPAPDC1A axis, thus promoting EMT, migration, and invasion of BC.

Citing Articles

Quantitative estimates of the regulatory influence of long non-coding RNAs on global gene expression variation using TCGA breast cancer transcriptomic data.

Xie X, Sinha S PLoS Comput Biol. 2024; 20(6):e1012103.

PMID: 38838009 PMC: 11198904. DOI: 10.1371/journal.pcbi.1012103.

The role of extracellular vesicles in circulating tumor cell-mediated distant metastasis.

Guo S, Huang J, Li G, Chen W, Li Z, Lei J Mol Cancer. 2023; 22(1):193.

PMID: 38037077 PMC: 10688140. DOI: 10.1186/s12943-023-01909-5.

The role of non-coding RNAs in extracellular vesicles in breast cancer and their diagnostic implications.

Samuels M, Jones W, Towler B, Turner C, Robinson S, Giamas G Oncogene. 2023; 42(41):3017-3034.

PMID: 37670020 PMC: 10555829. DOI: 10.1038/s41388-023-02827-y.

Deciphering the Functional Status of Breast Cancers through the Analysis of Their Extracellular Vesicles.

Murillo Carrasco A, Otake A, Macedo-da-Silva J, Feijoli Santiago V, Palmisano G, Andrade L Int J Mol Sci. 2023; 24(16).

PMID: 37629204 PMC: 10455604. DOI: 10.3390/ijms241613022.

The value of urinary exosomal lncRNA SNHG16 as a diagnostic biomarker for bladder cancer.

Liu C, Xu P, Shao S, Wang F, Zheng Z, Li S Mol Biol Rep. 2023; 50(10):8297-8304.

PMID: 37592177 PMC: 10520200. DOI: 10.1007/s11033-023-08667-z.

References

Kong Q, Qiu M . Long noncoding RNA SNHG15 promotes human breast cancer proliferation, migration and invasion by sponging miR-211-3p. Biochem Biophys Res Commun. 2017; 495(2):1594-1600. DOI: 10.1016/j.bbrc.2017.12.013. View

Yang Y, Li C, Chan L, Wei Y, Hsu J, Xia W . Exosomal PD-L1 harbors active defense function to suppress T cell killing of breast cancer cells and promote tumor growth. Cell Res. 2018; 28(8):862-864. PMC: 6082826. DOI: 10.1038/s41422-018-0060-4. View

Maughan K, Lutterbie M, Ham P . Treatment of breast cancer. Am Fam Physician. 2010; 81(11):1339-46. View

Sun Y, Huo C, Qiao Z, Shang Z, Uzzaman A, Liu S . Comparative Proteomic Analysis of Exosomes and Microvesicles in Human Saliva for Lung Cancer. J Proteome Res. 2018; 17(3):1101-1107. DOI: 10.1021/acs.jproteome.7b00770. View

Ni C, Fang Q, Chen W, Jiang J, Jiang Z, Ye J . Breast cancer-derived exosomes transmit lncRNA SNHG16 to induce CD73+γδ1 Treg cells. Signal Transduct Target Ther. 2020; 5(1):41. PMC: 7188864. DOI: 10.1038/s41392-020-0129-7. View

Wang J, Yang K, Yuan W, Gao Z . Determination of Serum Exosomal H19 as a Noninvasive Biomarker for Bladder Cancer Diagnosis and Prognosis. Med Sci Monit. 2018; 24:9307-9316. PMC: 6320644. DOI: 10.12659/MSM.912018. View

Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi P . A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language?. Cell. 2011; 146(3):353-8. PMC: 3235919. DOI: 10.1016/j.cell.2011.07.014. View

Yang J, Li C, Zhang L, Wang X . Extracellular Vesicles as Carriers of Non-coding RNAs in Liver Diseases. Front Pharmacol. 2018; 9:415. PMC: 5928552. DOI: 10.3389/fphar.2018.00415. View

Zhang X, Zhang L, Lin B, Chai X, Li R, Liao Y . Phospholipid Phosphatase 4 promotes proliferation and tumorigenesis, and activates Ca-permeable Cationic Channel in lung carcinoma cells. Mol Cancer. 2017; 16(1):147. PMC: 5576330. DOI: 10.1186/s12943-017-0717-5. View

10.

Akram M, Iqbal M, Daniyal M, Khan A . Awareness and current knowledge of breast cancer. Biol Res. 2017; 50(1):33. PMC: 5625777. DOI: 10.1186/s40659-017-0140-9. View

11.

Du S . The SNHG16/miR-30a axis promotes breast cancer cell proliferation and invasion by regulating RRM2. Neoplasma. 2020; 67(3):567-575. DOI: 10.4149/neo_2020_190625N550. View

12.

Wang H, Gires O . Tumor-derived extracellular vesicles in breast cancer: From bench to bedside. Cancer Lett. 2019; 460:54-64. DOI: 10.1016/j.canlet.2019.06.012. View

13.

Stavast C, Erkeland S . The Non-Canonical Aspects of MicroRNAs: Many Roads to Gene Regulation. Cells. 2019; 8(11). PMC: 6912820. DOI: 10.3390/cells8111465. View

14.

Liao S, Xing S, Ma Y . LncRNA SNHG16 sponges miR-98-5p to regulate cellular processes in osteosarcoma. Cancer Chemother Pharmacol. 2019; 83(6):1065-1074. DOI: 10.1007/s00280-019-03822-5. View

15.

Zhang R, Xia Y, Wang Z, Zheng J, Chen Y, Li X . Serum long non coding RNA MALAT-1 protected by exosomes is up-regulated and promotes cell proliferation and migration in non-small cell lung cancer. Biochem Biophys Res Commun. 2017; 490(2):406-414. DOI: 10.1016/j.bbrc.2017.06.055. View

16.

Xiao Y, Xiao T, Ou W, Wu Z, Wu J, Tang J . LncRNA SNHG16 as a potential biomarker and therapeutic target in human cancers. Biomark Res. 2020; 8:41. PMC: 7487997. DOI: 10.1186/s40364-020-00221-4. View

17.

Zhou C, Zhao J, Liu J, Wei S, Xia Y, Xia W . LncRNA SNHG16 promotes epithelial- mesenchymal transition via down-regulation of DKK3 in gastric cancer. Cancer Biomark. 2019; 26(4):393-401. DOI: 10.3233/CBM-190497. View

18.

Milane L, Singh A, Mattheolabakis G, Suresh M, Amiji M . Exosome mediated communication within the tumor microenvironment. J Control Release. 2015; 219:278-294. DOI: 10.1016/j.jconrel.2015.06.029. View

19.

Manzano R, Martinez-Navarro E, Forteza J, Brugarolas A . Microarray phosphatome profiling of breast cancer patients unveils a complex phosphatase regulatory role of the MAPK and PI3K pathways in estrogen receptor-negative breast cancers. Int J Oncol. 2014; 45(6):2250-66. PMC: 4215587. DOI: 10.3892/ijo.2014.2648. View

20.

Yu D, Wu Y, Shen H, Lv M, Chen W, Zhang X . Exosomes in development, metastasis and drug resistance of breast cancer. Cancer Sci. 2015; 106(8):959-64. PMC: 4556383. DOI: 10.1111/cas.12715. View