Correlation between the overexpression of Yin Yang 1 and the expression levels of miRNAs in Burkitt's lymphoma: A computational study

Hafsi,Sameh; Candido,Saverio; Maestro,Roberta; Falzone,Luca; Soua,Zora; Bonavida,Benjamin; Spandidos,Demetrios  A.; Libra,Massimo

doi:10.3892/ol.2015.4031

Correlation between the overexpression of Yin Yang 1 and the expression levels of miRNAs in Burkitt's lymphoma: A computational study

Authors:
- Sameh Hafsi
- Saverio Candido
- Roberta Maestro
- Luca Falzone
- Zora Soua
- Benjamin Bonavida
- Demetrios A. Spandidos
- Massimo Libra
View Affiliations

Affiliations: Department of Biomedical and Biotechnological Sciences, Section of General and Clinical Pathology, and Oncology, University of Catania, I-95124 Catania, Italy, Experimental Oncology 1, CRO Aviano National Cancer Institute, IRCCS, I-33081 Aviano, Italy, U.R. Molecular Biology of Leukemia and Lymphoma, Faculty of Medicine, University of Sousse, Sousse 4002, Tunisia, Department of Microbiology, Immunology and Molecular Genetics, Jonsson Comprehensive Cancer Center, University of California, Los Angeles, CA 90095, USA, Laboratory of Clinical Virology, University of Crete Medical School, Heraklion 71409, Greece
Published online on: December 14, 2015 https://doi.org/10.3892/ol.2015.4031
Pages: 1021-1025
Copyright: © Hafsi et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

A growing number of studies have highlighted the role of microRNAs (miRNAs or miRs) in the development and progression of cancer. In particular, the aberrant expression of cancer-related proteins, such as oncogenes and tumor suppressors has been shown to correlate with the modulation of the expression of specific miRNAs. In the present study, we aimed to determine which downregulated miRNAs may be involved in modulating the expression of the oncogenic transcription factor, Yin Yang 1 (YY1). YY1 has been reported to be overexpressed in several malignancies and our previous studies have highlighted the significant correlation between the levels of YY1 and aggressive behavior in non-Hodgkin's lymphoma (NHL). A total of 57 miRNAs that are potentially capable of targeting YY1 was identified through in silico approaches. The search of publicly available NHL datasets, including paired mRNA and miRNA data (GSE23026) highlighted a significant correlation (Pearson's correlation, r>0.5) between the expression levels of YY1 and the expression levels of a limited set of miRNAs, including miR‑363, miR‑200a, miR‑23b, miR‑15a and miR‑15b. Intriguingly, both hsa‑miR‑363 and hsa‑miR‑200a belong to the top 20 miRNAs that were found to be downregulated in Burkitt's lymphoma (BL) tissue compared to normal tissue. Although further validation studies are warranted, the identification of these two miRNAs associated with the upregulation of YY1 in BL may provide further insight into the pathogenesis of this tumor and may contribute to more personalized and targeted treatment approaches for patients with this disease.

View Figures

View References

1	Baek D, Villén J, Shin C, Camargo FD, Gygi SP and Bartel DP: The impact of microRNAs on protein output. Nature. 455:64–71. 2008. View Article : Google Scholar : PubMed/NCBI
2	Bartel DP: MicroRNAs: T arget recognition and regulatory functions. Cell. 136:215–233. 2009. View Article : Google Scholar : PubMed/NCBI
3	Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, Labourier E, Reinert KL, Brown D and Slack FJ: RAS is regulated by the let-7 microRNA family. Cell. 120:635–647. 2005. View Article : Google Scholar : PubMed/NCBI
4	Iorio MV and Croce CM: MicroRNA dysregulation in cancer: Diagnostics monitoring and therapeutics. Histopathology. EMBO Mol Med. 4:143–159. 2012. View Article : Google Scholar : PubMed/NCBI
5	Di Leva G, Garofalo M and Croce CM: MicroRNAs in cancer. Annu Rev Pathol. 9:287–314. 2014. View Article : Google Scholar : PubMed/NCBI
6	Jaffe ES: The 2008 WHO classification of lymphomas: Implications for clinical practice and translational research. Hematology Am Soc Hematol Educ Program. 2009:523–531. 2009. View Article : Google Scholar
7	Yunis JJ, Frizzera G, Oken MM, McKenna J, Theologides A and Arnesen M: Multiple recurrent genomic defects in follicular lymphoma. Histopathology. N Engl J Med. 316:79–84. 1987. View Article : Google Scholar : PubMed/NCBI
8	Ansell SM: Non-HodgkinL ymphoma: Diagnosis and Treatment. Mayo Clin Proc. 90:1152–1163. 2015. View Article : Google Scholar : PubMed/NCBI
9	Mehta-Shah N and Younes A: Novel targeted therapies in diffuse large B-cell lymphoma. Semin Hematol. 52:126–137. 2015. View Article : Google Scholar : PubMed/NCBI
10	Vega MI, Jazirehi AR, Huerta-Yepez S and Bonavida B: Rituximab-induced inhibition of YY1 and Bcl-xL expression in Ramos non-Hodgkin's lymphoma cell line via inhibition of NF-kappa B activity, role of YY1 and Bcl-xL in Fas resistance and chemoresistance, respectively. J Immunol. 175:2174–2183. 2005. View Article : Google Scholar : PubMed/NCBI
11	Gordon S, Akopyan G, Garban H and Bonavida B: Transcription factor YY1: Structure, function, and therapeutic implications in cancer biology. Oncogene. 25:1125–1142. 2006. View Article : Google Scholar : PubMed/NCBI
12	Castellano G, Torrisi E, Ligresti G, Malaponte G, Militello L, Russo AE, McCubrey JA, Canevari S and Libra M: The involvement of the transcription factor Yin Yang 1 in cancer development and progression. Cell Cycle. 8:1367–1372. 2009. View Article : Google Scholar : PubMed/NCBI
13	Bonavida B, Huerta-Yepez S, Baritaki S, Vega M, Liu H, Chen H and Berenson J: Overexpression of Yin Yang 1 in the pathogenesis of human hematopoietic malignancies. Crit Rev Oncog. 16:261–267. 2011. View Article : Google Scholar : PubMed/NCBI
14	Castellano G, Torrisi E, Ligresti G, Nicoletti F, Malaponte G, Traval S, McCubrey JA, Canevari S and Libra M: Yin Yang 1 overexpression in diffuse large B-cell lymphoma is associated with B-cell transformation and tumor progression. Cell Cycle. 9:557–563. 2010. View Article : Google Scholar : PubMed/NCBI
15	Maragkakis M, Alexiou P, Papadopoulos GL, Reczko M, Dalamagas T, Giannopoulos G, Goumas G, Koukis E, Kourtis K, Simossis VA, et al: Accurate microRNA target prediction correlates with protein repression levels. BMC Bioinformatics. 10:2952009. View Article : Google Scholar : PubMed/NCBI
16	John B, Enright AJ, Aravin A, Tuschl T, Sander C and Marks DS: Correction: Human MicroRNA targets. PLoS Biol. 3:e2642005. View Article : Google Scholar
17	Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, et al: Combinatorial microRNA target predictions. Nat Genet. 37:495–500. 2005. View Article : Google Scholar : PubMed/NCBI
18	Agarwal V, Bell GW, Nam JW and Bartel DP: Predicting effective microRNA target sites in mammalian mRNAs. Elife. 4:e050052015. View Article : Google Scholar
19	Bueno MJ Gómez, de Cedrón M, Gómez-López G, de Pérez Castro I, Di Lisio L, Montes-Moreno S, Martínez N, Guerrero M, Sánchez-Martínez R, Santos J, et al: Combinatorial effects of microRNAs to suppress the Myc oncogenic pathway. Blood. 117:6255–6266. 2011. View Article : Google Scholar : PubMed/NCBI
20	Di Lisio L, Sánchez-Beato M, Gómez-López G, Rodríguez ME, Montes-Moreno S, Mollejo M, Menárguez J, Martínez MA, Alves FJ, Pisano DG, et al: MicroRNA signatures in B-cell lymphomas. Blood Cancer J. 2:e572012. View Article : Google Scholar : PubMed/NCBI
21	Troppan K, Wenzl K, Deutsch A, Ling H, Neumeister P and Pichler M: MicroRNAs in diffuse large B-cell lymphoma, implications for pathogenesis, diagnosis, prognosis and therapy. Anticancer Res. 34:557–564. 2014.PubMed/NCBI
22	Musilova K and Mraz M: MicroRNAs in B-cell lymphomas: How a complex biology gets more complex. Leukemia. 29:1004–1017. 2015. View Article : Google Scholar : PubMed/NCBI
23	Garofalo M, Leva GD and Croce CM: MicroRNAs as anti-cancer therapy. Curr Pharm Des. 20:5328–5335. 2014. View Article : Google Scholar : PubMed/NCBI
24	Lim EL, Trinh DL, Scott DW, Chu A, Krzywinski M, Zhao Y, Robertson AG, Mungall AJ, Schein J, Boyle M, et al: Comprehensive miRNA sequence analysis reveals survival differences in diffuse large B-cell lymphoma patients. Genome Biol. 16:182015. View Article : Google Scholar : PubMed/NCBI
25	Shi Y, Seto E, Chang LS and Shenk T: Transcriptional repression by YY1, a human GLI-Krüppel-related protein, and relief of repression by adenovirus E1A protein. Cell. 67:377–388. 1991. View Article : Google Scholar : PubMed/NCBI
26	Lee HY, Chaudhary J, Walsh GL, Hong WK and Kurie JM: Suppression of c-Fos gene transcription with malignant transformation of human bronchial epithelial cells. Oncogene. 16:3039–3046. 1998. View Article : Google Scholar : PubMed/NCBI
27	Liao WR, Hsieh RH, Hsu KW, Wu MZ, Tseng MJ and Mai RT: WuL ee YH and Yeh TS: The CBF1-independent Notch1 signal pathway activates human c-myc expression partially via transcription factor YY1. Carcinogenesis. 28:1867–1876. 2007. View Article : Google Scholar : PubMed/NCBI
28	Allouche A, Nolens G, Tancredi A, Delacroix L, Mardaga J, Fridman V, Winkler R, Boniver J, Delvenne P and Begon DY: The combined immunodetection of AP-2alpha and YY1 transcription factors is associated with ERBB2 gene overexpression in primary breast tumors. Breast Cancer Res. 10:R92008. View Article : Google Scholar : PubMed/NCBI
29	Begon DY, Delacroix L, Vernimmen D, Jackers P and Winkler R: Yin Yang 1 cooperates with activator protein 2 to stimulate ERBB2 gene expression in mammary cancer cells. J Biol Chem. 280:24428–24434. 2005. View Article : Google Scholar : PubMed/NCBI
30	Wan M, Huang W, Kute TE, Miller LD, Zhang Q, Hatcher H, Wang J, Stovall DB, Russell GB, Cao PD, et al: Yin Yang 1 plays an essential role in breast cancer and negatively regulates p27. Am J Pathol. 180:2120–2133. 2012. View Article : Google Scholar : PubMed/NCBI
31	Rayess H, Wang MB and Srivatsan ES: Cellular senescence and tumor suppressor gene p16. Int J Cancer. 130:1715–1725. 2012. View Article : Google Scholar : PubMed/NCBI
32	Wu S, Murai S, Kataoka K and Miyagishi M: Cooperative regulation og p73 promoter by Yin Yang 1 and E2F1. Nucleic Acids Symp Ser (Oxf). 51:347–348. 2007. View Article : Google Scholar : PubMed/NCBI
33	Grönroos E, Terentiev AA, Punga T and Ericsson J: YY1 inhibits the activation of the p53 tumor suppressor in response to genotoxic stress. Proc Natl Acad Sci USA. 101:12165–12170. 2004. View Article : Google Scholar : PubMed/NCBI
34	Migliazza A, Martinotti S, Chen W, Fusco C, Ye BH, Knowles DM, Offit K, Chaganti RS and Dalla-Favera R: Frequent somatic hypermutation of the 5′ noncoding region of the BCL6 gene in B-cell lymphoma. Proc Natl Acad Sci USA. 92:12520–12524. 1995. View Article : Google Scholar : PubMed/NCBI
35	Libra M, Torrisi E, Castellano G, Nicoletti F, Malaponte G, Mazzarino MC, Marconi A, Proietti L, Militello L, Bonavida B, et al: Computational Evaluation of Yin Yang 1 Transcript Levels in the Spectrum of B-cell Neoplasia. Immunopathol Dis Therap. 1:115–125. 2010.
36	Sui G, Affar B, Shi Y, Brignone C, Wall NR, Yin P, Donohoe M, Luke MP, Calvo D, Grossman SR, et al: Yin Yang 1 is a negative regulator of p53. Cell. 117:859–872. 2004. View Article : Google Scholar : PubMed/NCBI
37	Affar B, Gay F and Shi Y, Liu H, Huarte M, Wu S, Collins T, Li E and Shi Y: Essential dosage-dependent functions of the transcription factor yin yang 1 in late embryonic development and cell cycle progression. Mol Cell Biol. 26:3565–3581. 2006. View Article : Google Scholar : PubMed/NCBI
38	Maestro R, Gloghini A, Doglioni C, Piccinin S, Vukosavljevic T, Gasparotto D, Carbone A and Boiocchi M: Human non-Hodgkin's lymphomas overexpress a wild-type form of p53 which is a functional transcriptional activator of the cyclin-dependent kinase inhibitor p21. Blood. 89:2523–2528. 1997.PubMed/NCBI
39	Chim CS, Wong KY, Qi Y, Loong F, Lam WL, Wong LG, Jin DY, Costello JF and Liang R: Epigenetic inactivation of the miR-34a in hematological malignancies. Carcinogenesis. 31:745–750. 2010. View Article : Google Scholar : PubMed/NCBI
40	McCubrey JA, Abrams SL, Ligresti G, Misaghian N, Wong EW, Steelman LS, Bäsecke J, Troppmair J, Libra M, Nicoletti F, et al: Involvement of p53 and Raf/MEK/ERK pathways in hematopoietic drug resistance. Leukemia. 22:2080–2090. 2008. View Article : Google Scholar : PubMed/NCBI
41	van Kempen LC, van den Hurk K, Lazar V, Michiels S, Winnepenninckx V, Stas M, Spatz A and van den Oord JJ: Loss of microRNA-200a and c, and microRNA-203 expression at the invasive front of primary cutaneous melanoma is associated with increased thickness and disease progression. Virchows Arch. 461:441–448. 2012. View Article : Google Scholar : PubMed/NCBI
42	Cai J, Liu X, Cheng J, Li Y, Huang X, Li Y, Ma X, Yu H, Liu H and Wei R: MicroRNA-200 is commonly repressed in conjunctival MALT lymphoma, and targets cyclin E2. Graefes Arch Clin Exp Ophthalmol. 250:523–531. 2012. View Article : Google Scholar : PubMed/NCBI
43	Sandhu SK, Croce CM and Garzon R: Micro-RNA expression and function in lymphomas. Adv Hematol. 2011:3471372011. View Article : Google Scholar : PubMed/NCBI
44	Zou J, Yin F, Wang Q, Zhang W and Li L: Analysis of microarray-identified genes and microRNAs associated with drug resistance in ovarian cancer. Int J Clin Exp Pathol. 8:6847–6858. 2015.PubMed/NCBI