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Article

MEG3-Mediated Oral Squamous-Cell-Carcinoma-Derived Exosomal miR-421 Activates Angiogenesis by Targeting HS2ST1 in Vascular Endothelial Cells

by
Chia-Yun Huang
1,2,†,
Sung-Tau Chou
1,†,
Yuan-Ming Hsu
1,
Wan-Ju Chao
1,
Guan-Hsun Wu
1,
Jenn-Ren Hsiao
3,
Horng-Dar Wang
2 and
Shine-Gwo Shiah
1,4,5,*
1
National Institute of Cancer Research, National Health Research Institutes, Miaoli 350401, Taiwan
2
Institute of Biotechnology, National Tsing Hua University, Hsinchu 300044, Taiwan
3
Head and Neck Collaborative Oncology Group, Department of Otolaryngology, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan 704302, Taiwan
4
Program in Environmental and Occupational Medicine, Kaohsiung Medical University, Kaohsiung 80708, Taiwan
5
Cancer Center, Wan Fang Hospital, Taipei Medical University, Taipei 116079, Taiwan
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2024, 25(14), 7576; https://doi.org/10.3390/ijms25147576
Submission received: 2 April 2024 / Revised: 21 June 2024 / Accepted: 8 July 2024 / Published: 10 July 2024
(This article belongs to the Special Issue The Roles of RNA (Coding and Non-coding) in Human Disease)
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Abstract

Exosomal microRNAs (miRNAs) from cancer cells play a key role in mediating the oral squamous cell carcinoma (OSCC) microenvironment. The objective of this study was to investigate how the long non-coding RNA (lncRNA) MEG3 affects OSCC angiogenesis through exosomal miR-421. Global miRNA microarray analysis and quantitative real-time PCR (qRT-PCR) were performed to determine the level of miRNAs in OSCC cell-derived exosomes. Cell migration, invasion, tube formation, immunohistochemistry, and hemoglobin concentrations were used to study the effects of exosomal miR-421 in angiogenesis. Western blotting was used to determine the expression level of HS2ST1 and VEGFR2-related downstream proteins. MiRNA array and qRT-PCR identified the upregulation of miR-421 in OSCC cell-derived exosomes. Furthermore, exosomal miR-421 can be taken up by human umbilical vein endothelial cells (HUVECs) and then target HS2ST1 through VEGF-mediated ERK and AKT phosphorylation, thereby promoting HUVEC migration, invasion, and tube formation. Additionally, forced expression of the lncRNA MEG3 in OSCC cells reduced exosomal miR-421 levels and then increased HS2ST1 expression, thereby reducing the VEGF/VEGFR2 pathway in HUVECs. Our results demonstrate a novel mechanism by which lncRNA MEG3 can act as a tumor suppressor and regulate endothelial angiogenesis through the exosomal miR-421/HS2ST1 axis, which provides a potential therapeutic strategy for OSCC angiogenesis.
Keywords: microRNA; long non-coding RNA (lncRNA); oral squamous cell carcinoma (OSCC); exosome; angiogenesis; miR-421; HS2ST1 microRNA; long non-coding RNA (lncRNA); oral squamous cell carcinoma (OSCC); exosome; angiogenesis; miR-421; HS2ST1

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MDPI and ACS Style

Huang, C.-Y.; Chou, S.-T.; Hsu, Y.-M.; Chao, W.-J.; Wu, G.-H.; Hsiao, J.-R.; Wang, H.-D.; Shiah, S.-G. MEG3-Mediated Oral Squamous-Cell-Carcinoma-Derived Exosomal miR-421 Activates Angiogenesis by Targeting HS2ST1 in Vascular Endothelial Cells. Int. J. Mol. Sci. 2024, 25, 7576. https://doi.org/10.3390/ijms25147576

AMA Style

Huang C-Y, Chou S-T, Hsu Y-M, Chao W-J, Wu G-H, Hsiao J-R, Wang H-D, Shiah S-G. MEG3-Mediated Oral Squamous-Cell-Carcinoma-Derived Exosomal miR-421 Activates Angiogenesis by Targeting HS2ST1 in Vascular Endothelial Cells. International Journal of Molecular Sciences. 2024; 25(14):7576. https://doi.org/10.3390/ijms25147576

Chicago/Turabian Style

Huang, Chia-Yun, Sung-Tau Chou, Yuan-Ming Hsu, Wan-Ju Chao, Guan-Hsun Wu, Jenn-Ren Hsiao, Horng-Dar Wang, and Shine-Gwo Shiah. 2024. "MEG3-Mediated Oral Squamous-Cell-Carcinoma-Derived Exosomal miR-421 Activates Angiogenesis by Targeting HS2ST1 in Vascular Endothelial Cells" International Journal of Molecular Sciences 25, no. 14: 7576. https://doi.org/10.3390/ijms25147576

APA Style

Huang, C.-Y., Chou, S.-T., Hsu, Y.-M., Chao, W.-J., Wu, G.-H., Hsiao, J.-R., Wang, H.-D., & Shiah, S.-G. (2024). MEG3-Mediated Oral Squamous-Cell-Carcinoma-Derived Exosomal miR-421 Activates Angiogenesis by Targeting HS2ST1 in Vascular Endothelial Cells. International Journal of Molecular Sciences, 25(14), 7576. https://doi.org/10.3390/ijms25147576

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