Knockdown of USF1 Inhibits the Vasculogenic Mimicry of Glioma Cells Via Stimulating SNHG16/miR-212-3p and Linc00667/miR-429 Axis

Overview

Journal Mol Ther Nucleic Acids

Publisher Cell Press

Date 2019 Feb 12

PMID 30743215

Citations 39

Authors

Di Wang

Jian Zheng

Xiaobai Liu

Yixue Xue

Libo Liu

Jun Ma

Qianru He

Zhen Li

Heng Cai

Yunhui Liu

Affiliations

Soon will be listed here.

Abstract

The anti-angiogenic treatment of malignant glioma cells is an effective method to treat high-grade gliomas. However, due to the presence of vasculogenic mimicry (VM), the anti-angiogenic treatment of gliomas is not significantly effective in improving overall patient median survival. Therefore, this study investigated the mechanism of mimic formation of angiogenesis in gliomas. The results of this experiment indicate that the expression of upstream transcription factor 1 (USF1) is upregulated in glioma tissues and cells. USF1 knockdown inhibits the proliferation, migration, invasion, VM, and expression of VM-associated proteins in glioma cells by stimulating SNHG16 and linc00667. These two long non-coding RNAs (lncRNAs) regulate ALHD1A1 through the competing endogenous RNA (ceRNA) mechanism influencing the VM of glioma. This study is the first to demonstrate that the USF1/SNHG16/miR-212-3p/ALDH1A1 (aldehyde dehydrogenase-1) and USF1/linc00667/miR-429/ALDH1A1 axis regulates the VM of glioma cells, and these findings might provide a novel strategy for glioma treatment.

Citing Articles

Glioblastoma-Specific Strategies of Vascularization: Implications in Anti-Angiogenic Therapy Resistance.

Buccarelli M, Castellani G, Ricci-Vitiani L J Pers Med. 2022; 12(10).

PMID: 36294763 PMC: 9604754. DOI: 10.3390/jpm12101625.

Repression of linc01555 up-regulates angiomotin-p130 via the microRNA-122-5p/clic1 axis to impact vasculogenic mimicry-mediated chemotherapy resistance in small cell lung cancer.

Li D, Shen Y, Ren H, Wang L, Yang J, Wang Y Cell Cycle. 2022; 22(2):255-268.

PMID: 36045598 DOI: 10.1080/15384101.2022.2112132.

Development and validation of a cancer-associated fibroblast-derived lncRNA signature for predicting clinical outcomes in colorectal cancer.

Pan H, Pan J, Wu J Front Immunol. 2022; 13:934221.

PMID: 35967425 PMC: 9374325. DOI: 10.3389/fimmu.2022.934221.

Evolving Insights Into the Biological Function and Clinical Significance of Long Noncoding RNA in Glioblastoma.

Liu K, Chen H, Wang Y, Jiang L, Li Y Front Cell Dev Biol. 2022; 10:846864.

PMID: 35531099 PMC: 9068894. DOI: 10.3389/fcell.2022.846864.

LINC00667 regulates MPP -induced neuronal injury in Parkinson's disease.

Huo X, Wang L, Shao J, Zhou C, Ying X, Zhao J Ann Clin Transl Neurol. 2022; 9(5):707-721.

PMID: 35426258 PMC: 9082386. DOI: 10.1002/acn3.51480.

References

Liu X, Wang X, Du W, Chen L, Wang G, Cui Y . Suppressor of fused (Sufu) represses Gli1 transcription and nuclear accumulation, inhibits glioma cell proliferation, invasion and vasculogenic mimicry, improving glioma chemo-sensitivity and prognosis. Oncotarget. 2014; 5(22):11681-94. PMC: 4294353. DOI: 10.18632/oncotarget.2585. View

Bruno M, West R, Schneeman T, Bresnick E, Kaetzel C . Upstream stimulatory factor but not c-Myc enhances transcription of the human polymeric immunoglobulin receptor gene. Mol Immunol. 2003; 40(10):695-708. DOI: 10.1016/j.molimm.2003.09.004. View

Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M . A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell. 2011; 147(2):358-69. PMC: 3234495. DOI: 10.1016/j.cell.2011.09.028. View

Kunnakkat S, Narayana A . Bevacizumab in the treatment of high-grade gliomas: an overview. Angiogenesis. 2011; 14(4):423-30. DOI: 10.1007/s10456-011-9232-2. View

Maniotis A, Folberg R, Hess A, Seftor E, Gardner L, Peer J . Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol. 1999; 155(3):739-52. PMC: 1866899. DOI: 10.1016/S0002-9440(10)65173-5. View

Ke J, Yao Y, Zheng J, Wang P, Liu Y, Ma J . Knockdown of long non-coding RNA HOTAIR inhibits malignant biological behaviors of human glioma cells via modulation of miR-326. Oncotarget. 2015; 6(26):21934-49. PMC: 4673137. DOI: 10.18632/oncotarget.4290. View

Chen H, Lu S, Zhou J, Bai Z, Fu H, Xu X . An integrated approach for the identification of USF1-centered transcriptional regulatory networks during liver regeneration. Biochim Biophys Acta. 2014; 1839(5):415-23. DOI: 10.1016/j.bbagrm.2014.03.010. 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

Chen W, Zhang B, Guo W, Gao L, Shi L, Li H . miR-429 inhibits glioma invasion through BMK1 suppression. J Neurooncol. 2015; 125(1):43-54. DOI: 10.1007/s11060-015-1887-x. View

10.

Liu D, Ren C, Yuan X, Zhang L, Liu J, Liu Q . ALDH1 expression is correlated with pathologic grade and poor clinical outcome in patients with astrocytoma. J Clin Neurosci. 2012; 19(12):1700-5. DOI: 10.1016/j.jocn.2012.01.036. View

11.

Liu X, Zhang Q, Mu Y, Zhang X, Sai K, Pang J . Clinical significance of vasculogenic mimicry in human gliomas. J Neurooncol. 2011; 105(2):173-9. PMC: 3198193. DOI: 10.1007/s11060-011-0578-5. View

12.

Yoshida A, Rzhetsky A, Hsu L, Chang C . Human aldehyde dehydrogenase gene family. Eur J Biochem. 1998; 251(3):549-57. DOI: 10.1046/j.1432-1327.1998.2510549.x. View

13.

Bouafia A, Corre S, Gilot D, Mouchet N, Prince S, Galibert M . p53 requires the stress sensor USF1 to direct appropriate cell fate decision. PLoS Genet. 2014; 10(5):e1004309. PMC: 4022457. DOI: 10.1371/journal.pgen.1004309. View

14.

Wen P, Reardon D . Neuro-oncology in 2015: Progress in glioma diagnosis, classification and treatment. Nat Rev Neurol. 2016; 12(2):69-70. DOI: 10.1038/nrneurol.2015.242. View

15.

Ren K, Yao N, Wang G, Tian L, Ma J, Shi X . Vasculogenic mimicry: a new prognostic sign of human osteosarcoma. Hum Pathol. 2014; 45(10):2120-9. DOI: 10.1016/j.humpath.2014.06.013. View

16.

Chen Y, Chen Z . Vasculogenic mimicry: a novel target for glioma therapy. Chin J Cancer. 2013; 33(2):74-9. PMC: 3935008. DOI: 10.5732/cjc.012.10292. View

17.

Christensen L, True K, Hamilton M, Nielsen M, Damas N, Damgaard C . SNHG16 is regulated by the Wnt pathway in colorectal cancer and affects genes involved in lipid metabolism. Mol Oncol. 2016; 10(8):1266-82. PMC: 5423192. DOI: 10.1016/j.molonc.2016.06.003. View

18.

Xu F, Zhang J . Long non-coding RNA HOTAIR functions as miRNA sponge to promote the epithelial to mesenchymal transition in esophageal cancer. Biomed Pharmacother. 2017; 90:888-896. DOI: 10.1016/j.biopha.2017.03.103. View

19.

Currie M, Beardsley B, Harris G, Gunningham S, Dachs G, Dijkstra B . Immunohistochemical analysis of cancer stem cell markers in invasive breast carcinoma and associated ductal carcinoma in situ: relationships with markers of tumor hypoxia and microvascularity. Hum Pathol. 2012; 44(3):402-11. DOI: 10.1016/j.humpath.2012.06.004. View

20.

Su R, Cao S, Ma J, Liu Y, Liu X, Zheng J . Knockdown of SOX2OT inhibits the malignant biological behaviors of glioblastoma stem cells via up-regulating the expression of miR-194-5p and miR-122. Mol Cancer. 2017; 16(1):171. PMC: 5683208. DOI: 10.1186/s12943-017-0737-1. View