Association between miR‑212‑3p and SOX11, and the effects of miR‑212‑3p on cell proliferation and migration in mantle cell lymphoma

Tian,Yuyang; Wang,Li; Zhang,Yanming; Li,Lianqiao; Fei,Yingying; Zhang,Xingxia; Lin,Guoqiang

doi:10.3892/ol.2021.12970

Association between miR‑212‑3p and SOX11, and the effects of miR‑212‑3p on cell proliferation and migration in mantle cell lymphoma

Authors:
- Yuyang Tian
- Li Wang
- Yanming Zhang
- Lianqiao Li
- Yingying Fei
- Xingxia Zhang
- Guoqiang Lin
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Affiliations: Department of Hematology, Hainan Cancer Hospital, Haikou, Hainan 571000, P.R. China, Department of Hematology, Huai'an Hospital Affiliated to Xuzhou Medical College and Huai'an Second People's Hospital, Huai'an, Jiangsu 223002, P.R. China, Department of Radiotherapy, Huai'an Hospital Affiliated to Xuzhou Medical College and Huai'an Second People's Hospital, Huai'an, Jiangsu 223002, P.R. China
Published online on: August 5, 2021 https://doi.org/10.3892/ol.2021.12970
Article Number: 709
Copyright: © Tian et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

To the best of our knowledge, the effect of miR‑212‑3p on sex‑determining region Y‑box 11 (SOX11) expression has not been previously investigated and how this effect affects cell proliferation and migration in lymphoma remains unclear. The present study aimed to assess the association between microRNA‑212‑3p (miR‑212‑3p) and SOX11, and the effects of miR‑212‑3p on cell proliferation and migration in mantle cell lymphoma. Cancer tissue and corresponding paracancerous tissue samples were collected from 65 patients with mantle cell lymphoma. The mRNA expression levels of miR‑212‑3p and SOX11 were analyzed using quantitative PCR, and SOX11 protein expression was determined using western blotting. Following transfection, the miR‑212‑3p mimic group exhibited a significantly lower SOX11 mRNA and protein expression than the miR‑NC group. After 48‑72 h of transfection, cell proliferation in the miR‑212‑3p mimic group was significantly lower than that in the miR‑NC group. Furthermore, the miR‑212‑3p mimic group exhibited significantly lower cell invasion and significantly higher apoptosis than the miR‑NC group. The current results suggested that miR‑212‑3p inhibited lymphoma cell proliferation and migration, and promoted their apoptosis by specifically regulating SOX11. Therefore, miR‑212‑3p may serve as a novel therapeutic target and marker for lymphoma.

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1	Cheah CY, Seymour JF and Wang ML: Mantle cell lymphoma. J Clin Oncol. 34:1256–1269. 2016. View Article : Google Scholar : PubMed/NCBI
2	Robak T, Huang H, Jin J, Zhu J, Liu T, Samoilova O, Pylypenko H, Verhoef G, Siritanaratkul N, Osmanov E, et al: Bortezomib-based therapy for newly diagnosed mantle-cell lymphoma. N Engl J Med. 372:944–953. 2015. View Article : Google Scholar : PubMed/NCBI
3	Vose JM: Mantle cell lymphoma: 2013 Update on diagnosis, risk-stratification, and clinical management. Am J Hematol. 88:1082–1088. 2013. View Article : Google Scholar : PubMed/NCBI
4	Pérez-Galán P, Dreyling M and Wiestner A: Mantle cell lymphoma: Biology, pathogenesis, and the molecular basis of treatment in the genomic era. Blood. 117:26–38. 2011. View Article : Google Scholar : PubMed/NCBI
5	Mohanty A, Sandoval N, Das M, Pillai R, Chen L, Chen RW, Amin HM, Wang M, Marcucci G, Weisenburger DD, et al: CCND1 mutations increase protein stability and promote ibrutinib resistance in mantle cell lymphoma. Oncotarget. 7:73558–73572. 2016. View Article : Google Scholar : PubMed/NCBI
6	Dreyling M and Ferrero S; European Mantle Cell Lymphoma Network, : The role of targeted treatment in mantle cell lymphoma: Is transplant dead or alive? Haematologica. 101:104–114. 2016. View Article : Google Scholar : PubMed/NCBI
7	Beà S and Amador V: Role of SOX11 and genetic events cooperating with cyclin D1 in mantle cell lymphoma. Curr Oncol Rep. 19:432017. View Article : Google Scholar : PubMed/NCBI
8	Lord M, Wasik AM, Christensson B and Sander B: The utility of mRNA analysis in defining SOX11 expression levels in mantle cell lymphoma and reactive lymph nodes. Haematologica. 100:e369–e372. 2015. View Article : Google Scholar : PubMed/NCBI
9	Palomero J, Vegliante MC, Eguileor A, Rodriguez ML, Balsas P, Martinez D, Campo E and Amador V: SOX11 defines two different subtypes of mantle cell lymphoma through transcriptional regulation of BCL6. Leukemia. 30:1596–1599. 2016. View Article : Google Scholar : PubMed/NCBI
10	Fang G, Liu J, Wang Q, Huang X, Yang R, Pang Y and Yang M: MicroRNA-223-3p regulates ovarian cancer cell proliferation and invasion by targeting SOX11 expression. Int J Mol Sci. 18:12082017. View Article : Google Scholar : PubMed/NCBI
11	Shepherd JH, Uray IP, Mazumdar A, Tsimelzon A, Savage M, Hilsenbeck SG and Brown PH: The SOX11 transcription factor is a critical regulator of basal-like breast cancer growth, invasion, and basal-like gene expression. Oncotarget. 7:13106–13121. 2016. View Article : Google Scholar : PubMed/NCBI
12	Palomero J, Vegliante MC, Rodríguez ML, Eguileor Á, Castellano G, Planas-Rigol E, Jares P, Ribera-Cortada I, Cid MC, Campo E and Amador V: SOX11 promotes tumor angiogenesis through transcriptional regulation of PDGFA in mantle cell lymphoma. Blood. 124:2235–2247. 2014. View Article : Google Scholar : PubMed/NCBI
13	Balsas P, Palomero J, Eguileor Á, Rodríguez ML, Vegliante MC, Planas-Rigol E, Sureda-Gómez M, Cid MC, Campo E and Amador V: SOX11 promotes tumor protective microenvironment interactions through CXCR4 and FAK regulation in mantle cell lymphoma. Blood. 130:501–513. 2017. View Article : Google Scholar : PubMed/NCBI
14	Zhang X, Gee H, Rose B, Lee CS, Clark J, Elliott M, Gamble JR, Cairns MJ, Harris A, Khoury S and Tran N: Regulation of the tumour suppressor PDCD4 by miR-499 and miR-21 in oropharyngeal cancers. BMC Cancer. 16:862016. View Article : Google Scholar : PubMed/NCBI
15	Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, et al: A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 103:2257–2261. 2006. View Article : Google Scholar : PubMed/NCBI
16	Wang H, Guo Q, Yang P and Long G: Restoration of microRNA-212 causes a G0/G1 cell cycle arrest and apoptosis in adult T-cell leukemia/lymphoma cells by repressing CCND3 expression. J Investig Med. 65:82–87. 2017. View Article : Google Scholar : PubMed/NCBI
17	Ambrosio MR, Mundo L, Gazaneo S, Picciolini M, Vara PS, Sayed S, Ginori A, Lo Bello G, Del Porro L, Navari M, et al: MicroRNAs sequencing unveils distinct molecular subgroups of plasmablastic lymphoma. Oncotarget. 8:107356–107373. 2017. View Article : Google Scholar : PubMed/NCBI
18	Ju C, Zhou R, Sun J, Zhang F, Tang X, Chen KK, Zhao J, Lan X, Lin S, Zhang Z and Lv XB: LncRNA SNHG5 promotes the progression of osteosarcoma by sponging the miR-212-3p/SGK3 axis. Cancer Cell Int. 18:1412018. View Article : Google Scholar : PubMed/NCBI
19	Liu H, Li C, Shen C, Yin F, Wang K, Liu Y, Zheng B, Zhang W, Hou X, Chen X, et al: miR-212-3p inhibits glioblastoma cell proliferation by targeting SGK3. J Neurooncol. 122:431–439. 2015. View Article : Google Scholar : PubMed/NCBI
20	Hou P, Kang Y and Luo J: Hypoxia-mediated miR-212-3p downregulation enhances progression of intrahepatic cholangiocarcinoma through upregulation of Rab1a. Cancer Biol Ther. 19:984–993. 2018. View Article : Google Scholar : PubMed/NCBI
21	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
22	Yuan S, Dong Y, Peng L, Yang M, Niu L, Liu Z and Xie J: Tumor-associated macrophages affect the biological behavior of lung adenocarcinoma A549 cells through the PI3K/AKT signaling pathway. Oncol Lett. 18:1840–1846. 2019.PubMed/NCBI
23	Danilov AV and Persky DO: Incorporating acalabrutinib, a selective next-generation Bruton tyrosine kinase inhibitor, into clinical practice for the treatment of haematological malignancies. Br J Haematol. 193:15–25. 2021. View Article : Google Scholar : PubMed/NCBI
24	Kuo PY, Leshchenko VV, Fazzari MJ, Perumal D, Gellen T, He T, Iqbal J, Baumgartner-Wennerholm S, Nygren L, Zhang F, et al: High-resolution chromatin immunoprecipitation (ChIP) sequencing reveals novel binding targets and prognostic role for SOX11 in mantle cell lymphoma. Oncogene. 34:1231–1240. 2015. View Article : Google Scholar : PubMed/NCBI
25	Beekman R, Amador V and Campo E: SOX11, a key oncogenic factor in mantle cell lymphoma. Curr Opin Hematol. 25:299–306. 2018. View Article : Google Scholar : PubMed/NCBI
26	Xia L, Li D, Lin C, Ou S, Li X and Pan S: Comparative study of joint bioinformatics analysis of underlying potential of ‘neurimmiR’, miR-212-3P/miR-132-3P, being involved in epilepsy and its emerging role in human cancer. Oncotarget. 8:40668–40682. 2017. View Article : Google Scholar : PubMed/NCBI
27	Haenisch S, Zhao Y, Chhibber A, Kaiboriboon K, Do LV, Vogelgesang S, Barbaro NM, Alldredge BK, Lowenstein DH, Cascorbi I and Kroetz DL: SOX11 identified by target gene evaluation of miRNAs differentially expressed in focal and non-focal brain tissue of therapy-resistant epilepsy patients. Neurobiol Dis. 77:127–140. 2015. View Article : Google Scholar : PubMed/NCBI
28	Yang Z, Jiang S, Lu C, Ji T, Yang W, Li T, Lv J, Hu W, Yang Y and Jin Z: SOX11: Friend or foe in tumor prevention and carcinogenesis? Ther Adv Med Oncol. 11:17588359198534492019. View Article : Google Scholar : PubMed/NCBI
29	Yao Z, Sun B, Hong Q, Yan J, Mu D, Li J, Sheng H and Guo H: The role of tumor suppressor gene SOX11 in prostate cancer. Tumour Biol. 36:6133–6138. 2015. View Article : Google Scholar : PubMed/NCBI
30	Tsang SM, Oliemuller E and Howard BA: Regulatory roles for SOX11 in development, stem cells and cancer. Semin Cancer Biol. 67:3–11. 2020. View Article : Google Scholar : PubMed/NCBI
31	Huang J, Ji EH, Zhao X, Cui L, Misuno K, Guo M, Huang Z, Chen X and Hu S: Sox11 promotes head and neck cancer progression via the regulation of SDCCAG8. J Exp Clin Cancer Res. 38:1382019. View Article : Google Scholar : PubMed/NCBI
32	Wang L, Shen YF, Shi ZM, Shang XJ, Jin DL and Xi F: Overexpression miR-211-5p hinders the proliferation, migration, and invasion of thyroid tumor cells by downregulating SOX. J Clin Lab Anal. 32:e222932018. View Article : Google Scholar : PubMed/NCBI