Significance of the microRNA‑17‑92 gene cluster expressed in B‑cell non‑Hodgkin's lymphoma

Yan,Shujie; Jia,Chuiming; Quan,Lina; Zhao,Lina; Tian,Yuyang; Liu,Aichun

doi:10.3892/mmr.2019.10448

Significance of the microRNA‑17‑92 gene cluster expressed in B‑cell non‑Hodgkin's lymphoma

Authors:
- Shujie Yan
- Chuiming Jia
- Lina Quan
- Lina Zhao
- Yuyang Tian
- Aichun Liu
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Affiliations: Department of Hematology, Harbin Medical University Cancer Hospital, Harbin, Heilongjiang 150080, P.R. China
Published online on: July 1, 2019 https://doi.org/10.3892/mmr.2019.10448
Pages: 2459-2467

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Abstract

To evaluate the prognostic value of the microRNA (miR)‑17‑92 gene cluster, the expression of miR‑17‑92 in B‑cell non‑Hodgkin's lymphoma (B‑NHL) was examined. Patients with B‑NHL, who received therapy in the Department of Hematology, Harbin Medical University Cancer Hospital between January 2012 and October 2014, were enrolled in the study. The expression of the miR‑17‑92 cluster in tumor tissue samples was detected by reverse transcription‑quantitative polymerase chain reaction analysis. The overall survival (OS) and event‑free survival (EFS) times were also investigated by the Kaplan‑Meier method and comparisons between groups were estimated using a log‑rank test. Three types of lymphoid cancer cells with wild‑type (WT), knockout of miR‑17‑92 (KO), and overexpression of miR‑17‑92 (TG), were utilized to establish a tumor xenograft model, and a reactive hyperplasia lymph cell was used as a control. The tumor incubation times and weights were examined. A total of 71 patients with B‑NHL were registered. No significant correlations were identified between the expression of miR‑17‑92 and clinical factors (P>0.05). Members of the miR‑17‑92 cluster exhibited various expression in the subtypes of B‑NHL, and the difference between follicular lymphoma (FL) and germinal center B‑cell like (GBC) was most marked. The overexpression of miR‑18, miR‑19a, and miR‑92a induced a marked reduction in the OS of patients with B‑NHL, and high‑levels of miR‑19a and miR‑92a led to a decline in EFS. The overexpression of miR‑17‑92 shortened the duration of incubation required for visualization of the xenograft tumor, whereas knockout led to inhibition of tumor formation. The expression of miR‑17‑92 in FL differed significantly from that in GBC, and miR‑19a may have a crucial effect on the OS and EFS of patients with B‑NHL.

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1	Siegel RL, Miller KD and Jemal A: Cancer statistics, 2018. CA Cancer J Clinicians. 68:7–30. 2018. View Article : Google Scholar
2	Song W, Liu MG, Zhang JB, Zhang JJ, Sun MM and Yu QK: Mechanism of action of EBV, Bcl-2, p53, c-Myc and Rb in non-Hodgkin's lymphoma. Eur Rev Med Pharmacol Sci. 20:1093–1097. 2016.PubMed/NCBI
3	Datta S, Chatterjee S, Policegoudra RS, Gogoi HK and Singh L: Hepatitis viruses and non-Hodgkin's lymphoma: A review. World J Virol. 1:162–173. 2012. View Article : Google Scholar : PubMed/NCBI
4	Sun CM and Luan CF: Overexpression of microRNA-21 in peripheral blood mononuclear cells of patients with B-cell non-Hodgkin's lymphoma is associated with disease stage and treatment outcome. Eur Rev Med Pharmacol Sci. 19:3397–3402. 2015.PubMed/NCBI
5	Zhu C, Ren C, Han J, Ding Y, Du J, Dai N, Dai J, Ma H, Hu Z, Shen H, et al: A five-microRNA panel in plasma was identified as potential biomarker for early detection of gastric cancer. Br J Cancer. 110:2291. 2014. View Article : Google Scholar : PubMed/NCBI
6	Xu L, Zhang Y, Wang H, Zhang G, Ding Y and Zhao L: Tumor suppressor miR-1 restrains epithelial-mesenchymal transition and metastasis of colorectal carcinoma via the MAPK and PI3K/AKT pathway. J Transl Med. 12:2442014. View Article : Google Scholar : PubMed/NCBI
7	Lu L, Katsaros D, Risch HA, Canuto EM, Biglia N and Yu H: MicroRNA let-7a modifies the effect of self-renewal gene HIWI on patient survival of epithelial ovarian cancer. Mol Carcinog. 55:357–365. 2016. View Article : Google Scholar : PubMed/NCBI
8	Bruni R, Marcantonio C, Pulsoni A, Tataseo P, De Angelis F, Spada E, Marcucci F, Panfilio S, Bianco P, Riminucci M, et al: microRNA levels in paraffin-embedded indolent B-cell non-Hodgkin lymphoma tissues from patients chronically infected with hepatitis B or C virus. BMC Infect Dis. 5:S62014. View Article : Google Scholar
9	Medina PP, Nolde M and Slack FJ: OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature. 467:86–90. 2010. View Article : Google Scholar : PubMed/NCBI
10	Lawrie CH, Soneji S, Marafioti T, Cooper CD, Palazzo S, Paterson JC, Cattan H, Enver T, Mager R, Boultwood J, et al: MicroRNA expression distinguishes between germinal center B cell-like and activated B cell-like subtypes of diffuse large B cell lymphoma. Int J Cancer. 121:1156–1161. 2007. View Article : Google Scholar : PubMed/NCBI
11	Eis PS, Tam W, Sun L, Chadburn A, Li Z, Gomez MF, Lund E and Dahlberg JE: Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc Nati Acad Sci USA. 102:3627–3632. 2005. View Article : Google Scholar
12	Akao Y, Nakagawa Y, Kitade Y, Kinoshita T and Naoe T: Downregulation of microRNAs-143 and −145 in B-cell malignancies. Cancer Sci. 98:1914–1920. 2007. View Article : Google Scholar : PubMed/NCBI
13	Ferrajoli A, Shanafelt TD, Ivan C, Shimizu M, Rabe KG, Nouraee N, Ikuo M, Ghosh AK, Lerner S, Rassenti LZ, et al: Prognostic value of miR-155 in individuals with monoclonal B-cell lymphocytosis and patients with B chronic lymphocytic leukemia. Blood. 122:1891–1899. 2013. View Article : Google Scholar : PubMed/NCBI
14	Döhner H, Stilgenbauer S, Benner A, Leupolt E, Kröber A, Bullinger L, Döhner K, Bentz M and Lichter P: Genomic aberrations and survival in chronic lymphocytic leukemia. N Engl J Med. 343:1910–1916. 2000. View Article : Google Scholar : PubMed/NCBI
15	Ota A, Tagawa H, Karnan S, Tsuzuki S, Karpas A, Kira S, Yoshida Y and Seto M: Identification and characterization of a Novel Gene, C13orf25, as a Target for 13q31-q32 amplification in malignant lymphoma. Cancer Res. 64:3087–3095. 2004. View Article : Google Scholar : PubMed/NCBI
16	Mendell JT: miRiad roles for the miR-17-92 cluster in development and disease. Cell. 133:217–222. 2008. View Article : Google Scholar : PubMed/NCBI
17	Tagawa H, Karube K, Tsuzuki S, Ohshima K and Seto M: Synergistic action of the microRNA-17 polycistron and Myc in aggressive cancer development. Cancer Sci. 98:1482–1490. 2007. View Article : Google Scholar : PubMed/NCBI
18	Zheng RL, Jiang YJ and Wang X: Role of microRNAs on therapy resistance in non-Hodgkin's lymphoma. Int J Clin ExpMed. 7:3818–3832. 2014.
19	Zanette DL, Rivadavia F, Molfetta GA, Barbuzano FG, Proto-Siqueira R, Silva WA Jr, Falcão RP and Zago MA: miRNA expression profiles in chronic lymphocytic and acute lymphocytic leukemia. Braz J Med Biol Res. 40:1435–1440. 2007. View Article : Google Scholar : PubMed/NCBI
20	He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ and Hammond SM: A microRNA polycistron as a potential human oncogene. Nature. 435:828–833. 2005. View Article : Google Scholar : PubMed/NCBI
21	Ventura A Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, et al: Targeted deletion reveals essential and overlapping functions of the miR-17~92 Family of miRNA clusters. Cell. 132:875–886. 2008. View Article : Google Scholar : PubMed/NCBI
22	Jin HY, Oda H, Lai M, Skalsky RL, Bethel K, Shepherd J, Kang SG, Liu WH, Sabouri-Ghomi M, Cullen BR, et al: MicroRNA-17~92 plays a causative role in lymphomagenesis by coordinating multiple oncogenic pathways. Embo J. 32:2377–2391. 2013. View Article : Google Scholar : PubMed/NCBI
23	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔ C T method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
24	O'Donnell KA, Wentzel EA, Zeller KI, Dang CV and Mendell JT: c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 435:839–843. 2005. View Article : Google Scholar : PubMed/NCBI
25	Jin HY, Lai M and Xiao C: MicroRNA-17~92 is a powerful cancer driver and a therapeutic target. Cell Cycle. 13:495–496. 2014. View Article : Google Scholar : PubMed/NCBI
26	Robertus JL, Harms G, Blokzijl T, Booman M, de Jong D, van Imhoff G, Rosati S, Schuuring E, Kluin P and van den Berg A: Specific expression of miR-17-5p and miR-127 in testicular and central nervous system diffuse large B-cell lymphoma. Mod Pathol. 22:547–555. 2009. View Article : Google Scholar : PubMed/NCBI
27	Lenz G, Wright GW, Emre NC, Kohlhammer H, Dave SS, Davis RE, Carty S, Lam LT, Shaffer AL, Xiao W, et al: Molecular subtypes of diffuse large B-cell lymphoma arise by distinct genetic pathways. Proc Nati Acad Sci USA. 105:13520–13525. 2008. View Article : Google Scholar
28	Zhao JJ, Lin J, Lwin T, Yang H, Guo J, Kong W, Dessureault S, Moscinski LC, Rezania D, Dalton WS, et al: microRNA expression profile and identification of miR-29 as a prognostic marker and pathogenetic factor by targeting CDK6 in mantle cell lymphoma. Blood. 115:2630–2639. 2010. View Article : Google Scholar : PubMed/NCBI
29	Lawrie CH, Chi J, Taylor S, Tramonti D, Ballabio E, Palazzo S, Saunders NJ, Pezzella F, Boultwood J, Wainscoat JS and Hatton CS: Expression of microRNAs in diffuse large B cell lymphoma is associated with immunophenotype, survival and transformation from follicular lymphoma. J Cell Mol Med. 13:1248–1260. 2009. View Article : Google Scholar : PubMed/NCBI
30	Fassina A, Marino F, Siri M, Zambello R, Ventura L, Fassan M, Simonato F and Cappellesso R: The miR-17-92 microRNA cluster: A novel diagnostic tool in large B-cell malignancies. Lab Invest. 92:1574–1582. 2012. View Article : Google Scholar : PubMed/NCBI
31	Benetatos L and Vartholomatos G: Deregulated microRNAs in multiple myeloma. Cancer. 118:878–887. 2012. View Article : Google Scholar : PubMed/NCBI
32	Spaccarotella E, Pellegrino E, Ferracin M, Ferreri C, Cuccuru G, Liu C, Iqbal J, Cantarella D, Taulli R, Provero P, et al: STAT3-mediated activation of microRNA cluster 17~92 promotes proliferation and survival of ALK-positive anaplastic large cell lymphoma. Haematologica. 99:116–124. 2014. View Article : Google Scholar : PubMed/NCBI
33	Schotte D, Pieters R and Boer MLD: MicroRNAs in acute leukemia: From biological players to clinical contributors. Leukemia. 26:1–12. 2012. View Article : Google Scholar : PubMed/NCBI