Abstract
Previous literature supports the variations in microRNAs expression levels among lymphoma patients due to EBV infection. These alterations can be observed in both EBV-encoded-microRNAs and EBV-induced cellular microRNAs. Moreover, changes in the microRNA profile could be significant in disease progression. This study aimed to assess published literature to obtain a microRNA profile for both EBV-encoded microRNAs and EBV-induced cellular microRNAs among lymphoma patients. We searched common available electronic databases by using relevant keywords. The result demonstrated that EBV infection could alter the microRNA expression levels among lymphoma patients. In Burkitt lymphoma, hsa-miR197 and miR510 were most frequently assessed human micro RNAs. Also, miR-BART6-3P and miR-BART17-5P were the most frequent viral micro RNAs in Burkitt lymphoma. Other human important micro RNAs were hsa-miR155 (in Diffuse large B cell lymphoma (DLBCL)), hsa-miR145 (in Nasal natural killer T cell lymphoma (NNKTCL)), miR-96, miR-128a, miR-128b, miR-129, and miR-205 (in Classic Hodgkin lymphoma (CHL)), miR-21, miR-142-3P, miR-126, miR-451 and miR-494-3P (in Nasal natural killer cell lymphoma (NNKCL)). Also, viral assessed micro RNAs were miR-BART1-5P (in DLBCL and NNKTCL), miR-BART-5 (in CHL), and EBV-miR-BART20-5P (in NNKCL). In conclusion, it could be suggested that EBV-encoded-microRNAs and EBV-induced cellular-microRNAs can be utilized as helpful factors for different types of lymphoma diagnoses or prognostic factors. Moreover, the mentioned microRNAs can also be promising therapeutic targets and can be used to modulate the oncogenes.
Similar content being viewed by others
References
Wahid F, Shehzad A, Khan T, Kim YY (2010) MicroRNAs: synthesis, mechanism, function, and recent clinical trials. Biochim Biophys Acta (BBA): Mol Cell Res 1803(11):1231–1243
Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233
Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH et al (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23(20):4051–4060
Hassani A, Khan G (2019) Epstein-Barr virus and miRNAs: partners in crime in the pathogenesis of multiple sclerosis? Front Immunol 10:695
Lu J, Murakami M, Verma SC, Cai Q, Haldar S, Kaul R et al (2011) Epstein–Barr virus nuclear antigen 1 (EBNA1) confers resistance to apoptosis in EBV-positive B-lymphoma cells through up-regulation of survivin. Virology 410(1):64–75
Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5):843–854
Wang M, Yu F, Wu W, Wang Y, Ding H, Qian L (2018) Epstein-Barr virus-encoded microRNAs as regulators in host immune responses. Int J Biol Sci 14(5):565
Zou P, Kawada J, Pesnicak L, Cohen JI (2007) Bortezomib induces apoptosis of Epstein-Barr virus (EBV)-transformed B cells and prolongs survival of mice inoculated with EBV-transformed B cells. J Virol 81(18):10029–10036
Pannone G, Zamparese R, Pace M, Pedicillo MC, Cagiano S, Somma P et al (2014) The role of EBV in the pathogenesis of Burkitt’s lymphoma: an Italian hospital based survey. Infect Agents Cancer 9(1):34
Roschewski M, Wilson WH (2012) EBV-associated lymphomas in adults. Best Pract Res Clin Haematol 25(1):75–89
Young LS, Murray PG (2003) Epstein–Barr virus and oncogenesis: from latent genes to tumours. Oncogene 22(33):5108–5121
Rickinson A, Kieff E (2007) Epstein-Barr virus. Fields Virol 2:2655–2700
Rickinson A (2006) Epstein-Barr virus and its replication. Virology 2:2603–2654
Carbone A, Gloghini A, Dotti G (2008) EBV-associated lymphoproliferative disorders: classification and treatment. Oncologist 13(5):577
Kieff E (1996) Epstein-Barr virus and its replication. In: Fields virology. Lippincott Williams & Wilkins, Philadelphia
Mani H, Jaffe ES (2009) Hodgkin lymphoma: an update on its biology with new insights into classification. Clin Lymphoma Myeloma 9(3):206–216
Lung RW-M, Tong JH-M, Sung Y-M, Leung P-S, Ng DC-H, Chau S-L et al (2009) Modulation of LMP2A expression by a newly identified Epstein-Barr virus-encoded microRNA miR-BART22. Neoplasia 11(11):1174–IN17
Cohen JI (2000) Epstein–Barr virus infection. N Engl J Med 343(7):481–492
Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P (2005) Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 309(5740):1577–1581
Triboulet R, Mari B, Lin Y-L, Chable-Bessia C, Bennasser Y, Lebrigand K et al (2007) Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science 315(5818):1579–1582
Ambrosio MR, Navari M, Di Lisio L, Leon EA, Onnis A, Gazaneo S et al (2014) The Epstein Barr-encoded BART-6-3p microRNA affects regulation of cell growth and immuno response in Burkitt lymphoma. Infect Agents Cancer 9(1):12
Piccaluga PP, Navari M, De Falco G, Ambrosio MR, Lazzi S, Fuligni F et al (2016) Virus-encoded microRNA contributes to the molecular profile of EBV-positive Burkitt lymphomas. Oncotarget 7(1):224
Zhou L, Bu Y, Liang Y, Zhang F, Zhang H, Li S (2016) Epstein-Barr Virus (EBV)-BamHI-A rightward transcript (BART)-6 and cellular microRNA-142 synergistically compromise immune defense of host cells in EBV-positive burkitt lymphoma. Med Sci Monitor: Int Med J Exp Clin Res 22:4114
Zhang YM, Yu Y, Zhao HP (2017) EBV-BART-6-3p and cellular microRNA-197 compromise the immune defense of host cells in EBV-positive Burkitt lymphoma. Mol Med Rep 15(4):1877–1883
Oduor CI, Movassagh M, Kaymaz Y, Chelimo K, Otieno J, Ong'echa JM et al (2017) Human and Epstein-barr virus miRNA profiling as predictive biomarkers for endemic Burkitt lymphoma. Front Microbiol 8:501
Navari M, Etebari M, De Falco G, Ambrosio MR, Gibellini D, Leoncini L et al (2015) The presence of Epstein-Barr virus significantly impacts the transcriptional profile in immunodeficiency-associated Burkitt lymphoma. Front Microbiol 6:556
Linnstaedt SD, Gottwein E, Skalsky RL, Luftig MA, Cullen BR (2010) Virally induced cellular microRNA miR-155 plays a key role in B-cell immortalization by Epstein-Barr virus. J Virol 84(22):11670–11678
Skalsky RL, Corcoran DL, Gottwein E, Frank CL, Kang D, Hafner M et al (2012) The viral and cellular microRNA targetome in lymphoblastoid cell lines. PLoS Pathog 8(1):e1002484
Harris-Arnold A, Arnold C, Schaffert S, Hatton O, Krams S, Esquivel C et al (2015) Epstein–Barr virus modulates host cell nicroRNA-194 to promote IL-10 production and B lymphoma cell survival. Am J Transplant 15(11):2814–2824
Kim JH, Kim WS, Park C (2012) Epstein–Barr virus latent membrane protein-1 protects B-cell lymphoma from rituximab-induced apoptosis through miR-155-mediated Akt activation and up-regulation of Mcl-1. Leukemia Lymphoma 53(8):1586–1591
Ayoubian H, Ludwig N, Fehlmann T, Menegatti J, Gröger L, Anastasiadou E et al (2019) Epstein-Barr virus infection of cell lines derived from diffuse large B-cell lymphomas alters microRNA loading of the Ago2 complex. J Virol 93(3):e01297–e01318
de Andrade TA, Evangelista AF, Campos AHF, Poles WA, Borges NM, Camillo CMC et al (2014) A microRNA signature profile in EBV+ diffuse large B-cell lymphoma of the elderly. Oncotarget 5(23):11813
Imig J, Motsch N, Zhu JY, Barth S, Okoniewski M, Reineke T et al (2010) microRNA profiling in Epstein–Barr virus-associated B-cell lymphoma. Nucleic Acids Res 39(5):1880–1893
Cao P, Zhang M, Wang L, Sai B, Tang J, Luo Z et al (2018) miR-18a reactivates the Epstein-Barr virus through defective DNA damage response and promotes genomic instability in EBV-associated lymphomas. BMC Cancer 18(1):1293
Motsch N, Alles J, Imig J, Zhu J, Barth S, Reineke T et al (2012) MicroRNA profiling of Epstein-Barr virus-associated NK/T-cell lymphomas by deep sequencing. PLoS One 7(8):e42193
Chen H-H, Huang W-T, Yang L-W, Lin C-W (2015) The PTEN-AKT-mTOR/RICTOR pathway in nasal natural killer cell lymphoma is activated by miR-494-3p via PTEN but inhibited by miR-142-3p via RICTOR. Am J Pathol 185(5):1487–1499
Kluiver J, Haralambieva E, de Jong D, Blokzijl T, Jacobs S, Kroesen BJ et al (2006) Lack of BIC and microRNA miR-155 expression in primary cases of Burkitt lymphoma. Genes Chromosomes Cancer 45(2):147–153
Navarro A, Gaya A, Martinez A, Urbano-Ispizua A, Pons A, Balagué O et al (2008) MicroRNA expression profiling in classic Hodgkin lymphoma. Blood 111(5):2825–2832
Komabayashi Y, Kishibe K, Nagato T, Ueda S, Takahara M, Harabuchi Y (2017) Circulating Epstein-Barr virus–encoded micro-RNAs as potential biomarkers for nasal natural killer/T-cell lymphoma. Hematol Oncol 35(4):655–663
Ramakrishnan R, Donahue H, Garcia D, Tan J, Shimizu N, Rice AP et al (2011) Epstein-Barr virus BART9 miRNA modulates LMP1 levels and affects growth rate of nasal NK T cell lymphomas. PLoS One 6(11):e27271
Lin T-C, Liu T-Y, Hsu S-M, Lin C-W (2013) Epstein-Barr virus–encoded miR-BART20-5p Inhibits T-bet translation with secondary suppression of p53 in invasive Nasal NK/T-cell lymphoma. Am J Pathol 182(5):1865–1875
Martin-Perez D, Vargiu P, Montes-Moreno S, Leon E, Rodriguez-Pinilla S, Lisio L et al (2012) Epstein-Barr virus microRNAs repress BCL6 expression in diffuse large B-cell lymphoma. Leukemia 26(1):180
Xia T, O'Hara A, Araujo I, Barreto J, Carvalho E, Sapucaia JB et al (2008) EBV microRNAs in primary lymphomas and targeting of CXCL-11 by ebv-mir-BHRF1-3. Cancer Res 68(5):1436–1442
Qiu J, Cosmopoulos K, Pegtel M, Hopmans E, Murray P, Middeldorp J et al (2011) A novel persistence associated EBV miRNA expression profile is disrupted in neoplasia. PLoS Pathog 7(8):e1002193
Fink S, Gandhi M, Nourse J, Keane C, Jones K, Crooks P et al (2014) A comprehensive analysis of the cellular and EBV-specific microRNAome in primary CNS PTLD identifies different patterns among EBV-associated tumors. Am J Transplant 14(11):2577–2587
Huang W-T, Lin C-W (2014) EBV-Encoded miR-BART20-5p and miR-BART8 Inhibit the IFN-γ–STAT1 pathway associated with disease progression in Nasal NK-cell lymphoma. Am J Pathol 184(4):1185–1197
López-Facio KL, Eguía-Aguilar P, Valencia-Mayoral P, Pérezpeña-Díazconti M, Arenas-Huertero F (2013) Expression of BART-5, BART-16 and BART-22, and NF-κB factor in classic Hodgkin’s lymphoma in pediatric patients. Bol Med Hosp Infant Mex 70(2):98–106
Molyneux EM, Rochford R, Griffin B, Newton R, Jackson G, Menon G et al (2012) Burkitt's lymphoma. Lancet 379(9822):1234–1244
Epstein MA (1964) Virus particles in cultured lymphoblasts from Burkitt's lymphoma. Lancet 1:702–703
Geser A, De Thé G, Lenoir G, Day N, Williams E (1982) Final case reporting from the ugandan prospective study of the relationship between ebv and burktit's lymphoma. Int J Cancer 29(4):397–400
Epstein M, Achong B (1979) The relationship of the virus to Burkitt’s lymphoma. In: The Epstein-Barr Virus. Springer, Berlin, pp 321–337
Magrath I, Jain V, Bhatia K (1992) Epstein-Barr virus and Burkitt's lymphoma. Semin Cancer Biol 3(5):285–295
Chen Y, Gelfond JA, McManus LM, Shireman PK (2009) Reproducibility of quantitative RT-PCR array in miRNA expression profiling and comparison with microarray analysis. BMC Genomics 10(1):407
Cho WC (2012) MicroRNAs as therapeutic targets and their potential applications in cancer therapy. Expert Opin Ther Targets 16(8):747–759
Nana-Sinkam SP, Croce CM (2011) MicroRNAs as therapeutic targets in cancer. Transl Res 157(4):216–225
Gandellini P, Profumo V, Folini M, Zaffaroni N (2011) MicroRNAs as new therapeutic targets and tools in cancer. Expert Opin Ther Targets 15(3):265–279
Ok CY, Li L, Xu-Monette ZY, Visco C, Tzankov A, Manyam GC et al (2014) Prevalence and clinical implications of Epstein–Barr virus infection in de novo diffuse large B-cell lymphoma in Western countries. Clin Cancer Res 20(9):2338–2349
Park S, Lee J, Ko YH, Han A, Jun HJ, Lee SC et al (2007) The impact of Epstein-Barr virus status on clinical outcome in diffuse large B-cell lymphoma. Blood. J Am Soc Hematol 110(3):972–978
Green M, Michaels M (2013) Epstein–Barr virus infection and posttransplant lymphoproliferative disorder. Am J Transplant 13(s3):41–54
Beatty PR, Krams SM, Martinez OM (1997) Involvement of IL-10 in the autonomous growth of EBV-transformed B cell lines. J Immunol 158(9):4045–4051
Testa JR, Tsichlis PN (2005) AKT signaling in normal and malignant cells. Oncogene 24(50):7391–7393
Ogawara Y, Kishishita S, Obata T, Isazawa Y, Suzuki T, Tanaka K et al (2002) Akt enhances Mdm2-mediated ubiquitination and degradation of p53. J Biol Chem 277(24):21843–21850
Abe W, Nasu K, Tsuno A, Kawano Y, Narahara H (2016) Gynecol Minimally Invas Ther 5:106–108
Young H, Bream J. (2007) IFN-γ: recent advances in understanding regulation of expression, biological functions, and clinical applications. Interferon: The 50th Anniversary: Springer, pp. 97–117
Lanier LL (2008) Evolutionary struggles between NK cells and viruses. Nat Rev Immunol 8(4):259–268
Jaffe ES (2001) World Health Organization classification of tumours. In: Pathology and genetics of tumours of haematopoietic and lymphoid tissues. IARC Press, Lyon
Acknowledgements
We gratefully acknowledge the Vice-Chancellor for Research and Technology, Hormozgan University of Medical Sciences, Bandar Abbas, and Tehran University of Medical Sciences, Tehran, Iran. Also, we are sincerely thankful to our counsellors in Clinical Research Development Center of Shahid Mohammadi Hospital, Hormozgan University of Medical Sciences, Bandar Abbas, Iran.
Funding
Not applicable.
Author information
Authors and Affiliations
Contributions
SS and AF designed the study, carried out the search, study selection, data abstraction, analysis and drafted the manuscript. AT, AZ, AMZ and MZ carried out the search, study selection, data abstraction, analysis and drafted the manuscript. AT, SASI, and SASE participated in study selection, checked data abstraction and analysis. All authors reviewed and edited the manuscript and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflicts of interest/Competing interests
The authors report no declarations of interest.
Availability of data and material
All data generated or analyzed during this study are included in this published article.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Soltani, S., Zakeri, A., Tabibzadeh, A. et al. A review on EBV encoded and EBV-induced host microRNAs expression profile in different lymphoma types. Mol Biol Rep 48, 1801–1817 (2021). https://doi.org/10.1007/s11033-021-06152-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-021-06152-z