MicroRNAs in lymphoma, from diagnosis to targeted therapy

Current Opinion in Oncology

Volumn 25, Issue 5, 2013, Pages 480-486

  Jardin, Fabrice ^a   Figeac, Martin ^b  

^a CENTRE HENRI BECQUEREL   (France)

^b UNIV LILLE   (France)

Author keywords

Diffuse large B cell lymphoma; MicroRNA; MiR 155, prognosis

Indexed keywords

ANTAGOMIR; CYCLOPHOSPHAMIDE; DOXORUBICIN; HISTONE DEACETYLASE INHIBITOR; MICRORNA; MICRORNA 155; MICRORNA 21; MICRORNA 29; MICRORNA 34A; RITUXIMAB; VINCRISTINE;

B CELL LYMPHOMA; BURKITT LYMPHOMA; CANCER CHEMOTHERAPY; CANCER DIAGNOSIS; EPSTEIN BARR VIRUS INFECTION; EXPERIMENTAL MODEL; FOLLICULAR LYMPHOMA; GENE TARGETING; GENETIC REGULATION; HUMAN; LARGE CELL LYMPHOMA; LYMPHOMA; MANTLE CELL LYMPHOMA; MARGINAL ZONE LYMPHOMA; MOLECULARLY TARGETED THERAPY; NONHUMAN; PRIMARY CENTRAL NERVOUS SYSTEM LYMPHOMA; PRIORITY JOURNAL; REVIEW; STABLE EXPRESSION; GENETICS; LYMPHOMA, B-CELL, MARGINAL ZONE; LYMPHOMA, LARGE B-CELL, DIFFUSE; PHYSIOLOGY; PROCEDURES; THEORETICAL MODEL;

GENE TARGETING; HUMANS; LYMPHOMA; LYMPHOMA, B-CELL, MARGINAL ZONE; LYMPHOMA, LARGE B-CELL, DIFFUSE; MICRORNAS; MODELS, THEORETICAL;

EID: 84883258954     PISSN: 10408746     EISSN: 1531703X     Source Type: Journal    
DOI: 10.1097/CCO.0b013e328363def2     Document Type: Review

References (45)

1. Di Lisio L, Martinez N, Montes-Moreno S, et al. The role of miRNAs in the pathogenesis and diagnosis of B-cell lymphomas. Blood 2012; 120: 1782-1790.
2. Culpin RE, Sieniawski M, Proctor SJ, et al. MicroRNAs are suitable for assessment as biomarkers from formalin-fixed paraffin-embedded tissue, and miR-24 represents an appropriate reference microRNA for diffuse large B-cell lymphoma studies. J Clin Pathol 2013; 66: 249-252.
3. Lawrie CH. MicroRNAs and lymphomagenesis: a functional review. Br J Haematol 2013; 160: 571-581. In this notable review, Lawrie focuses on the miRNAs that display an experimentally confirmed function in lymphoma pathogenesis, including miR-155, miR-21, miR-17-92, miR-15a/miR-16-1 cluster, miR-34a, and miR-125B.
4. Kluiver J, Slezak-Prochazka I, van den Berg A. Studying microRNAs in lymphoma. Methods Mol Biol 2013; 971: 265-276.
5. Montes-Moreno S, Martinez N, Sanchez-Espiridion B, et al. miRNA expression in diffuse large B-cell lymphoma treated with chemoimmunotherapy. Blood 2011; 118: 1034-1040.
6. Zhong H, Xu L, Zhong JH, et al. Clinical and prognostic significance of miR- 155 and miR-146a expression levels in formalin-fixed/paraffin-embedded tissue of patients with diffuse large B-cell lymphoma. Exp Ther Med 2012; 3: 763-770.
7. Fang C, Zhu DX, Dong HJ, et al. Serum microRNAs are promising novel biomarkers for diffuse large B cell lymphoma. Ann Hematol 2012; 91: 553-559.
8. Lawrie CH, Gal S, Dunlop HM, et al. Detection of elevated levels of tumourassociated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol 2008; 141: 672-675.
9. Dagan LN, Jiang X, Bhatt S, et al. miR-155 regulates HGAL expression and increases lymphoma cell motility. Blood 2012; 119: 513-520. In this work, the impact of miR-155 on lymphoma cell motility mediated via HGAL and RhoA was clearly demonstrated, pointing to a novel role of this miRNA in both normal and pathological B-cell biology.
10. Thompson RC, Herscovitch M, Zhao I, et al. NF-kappaB down-regulates expression of the B-lymphoma marker CD10 through a miR-155/PU.1 pathway. J Biol Chem 2011; 286: 1675-1682.
11. Babar IA, Cheng CJ, Booth CJ, et al. Nanoparticle-based therapy in an in vivo microRNA-155 (miR-155)-dependent mouse model of lymphoma. Proc Natl Acad Sci USA 2012; 109:E1695-E1704. Similarly to their previous research on miR-21, these authors generated a mouse model that exhibited B-cell proliferation with an addiction for miR-155. Using a model involving nanoparticles coated with peptides, termed penetratin, which contained antagomir molecules, they blocked the growth of the pre-B-cell tumors.
12. Rai D, Kim SW, McKeller MR, et al. Targeting of SMAD5 links microRNA-155 to the TGF-beta pathway and lymphomagenesis. Proc Natl Acad Sci USA 2010; 107: 3111-3116.
13. Sandhu SK, Volinia S, Costinean S, et al. miR-155 targets histone deacetylase 4 (HDAC4) and impairs transcriptional activity of B-cell lymphoma 6 (BCL6) in the Emu-miR-155 transgenic mouse model. Proc Natl Acad Sci USA 2012; 109: 20047-20052. In this remarkable work, it was demonstrated that Bcl6 is indirectly regulated by miR-155 through Mxd1/Mad1 upregulation, subsequently leading to de-repression of some known Bcl6- targets, such as inhibitor of differentiation (Id2), interleukin-6 (IL6), cMyc, Cyclin D1, and Mip1k. miR-155 directly targets HDAC4, a corepressor partner of BCL6. miR-155 is inversely correlated with Bcl6 and Hdac4, all of which promote cell survival and proliferation.
14. Huang X, Shen Y, Liu M, et al. Quantitative proteomics reveals that miR-155 regulates the PI3K-AKT pathway in diffuse large B-cell lymphoma. Am J Pathol 2012; 181: 26-33.
15. Peveling-Oberhag J, Crisman G, Schmidt A, et al. Dysregulation of global microRNA expression in splenic marginal zone lymphoma and influence of chronic hepatitis C virus infection. Leukemia 2012; 26: 1654-1662.
16. Saito Y, Suzuki H, Tsugawa H, et al. Overexpression of miR-142-5p and miR- 155 in gastric mucosa-associated lymphoid tissue (MALT) lymphoma resistant to Helicobacter pylori eradication. PLoS One 2012; 7:e47396.
17. Zhang Y, Roccaro AM, Rombaoa C, et al. LNA-mediated antimiR-155 silencing in low-grade B-cell lymphomas. Blood 2012; 120: 1678-1686. On the basis of the use of an 8-mer locked nucleic acid (LNA) antimiR-155 oligonucleotide targeting the seed region of miR-155, delivered systemically, this study showed that it is possible to inhibit cell proliferation in Waldenstrom macroglobulinemia and chronic lymphocytic leukemia.
18. Bouteloup M, Verney A, Rachinel N, et al. MicroRNA expression profile in splenic marginal zone lymphoma. Br J Haematol 2012; 156: 279-281.
19. Di Lisio L, Sanchez-Beato M, Gomez-Lopez G, et al. MicroRNA signatures in B-cell lymphomas. Blood Cancer J 2012; 2:e57.
20. Pedersen IM, Otero D, Kao E, et al. Onco-miR-155 targets SHIP1 to promote TNFalpha-dependent growth of B cell lymphomas. EMBO Mol Med 2009; 1: 288-295.
21. Martin-Perez D, Vargiu P, Montes-Moreno S, et al. Epstein-Barr virus micro-RNAs repress BCL6 expression in diffuse large B-cell lymphoma. Leukemia 2012; 26: 180-183.
22. Kim SW, Ramasamy K, Bouamar H, et al. MicroRNAs miR-125a and miR-125b constitutively activate the NF-kappaB pathway by targeting the tumor necrosis factor alpha-induced protein 3 (TNFAIP3, A20). Proc Natl Acad Sci USA 2012; 109: 7865-7870. In this study, it was shown that the effects of miR-125a/miR-125b on NF-kB activity are mediated via the repression of TNFAIP3 (A20) expression. miR-125a/miR-125b expression and genetic loss of TNFAIP3 are exclusive events. By contrast, high miR-125a/miR-125b levels appear to cosegregate with gain-offunction mutations targeting, for instance, MYD88 or CD79b.
23. Ji M, Rao E, Ramachandrareddy H, et al. The miR-17-92 microRNA cluster is regulated by multiple mechanisms in B-cell malignancies. Am J Pathol 2011; 179: 1645-1656.
24. Fassina A, Marino F, Siri M, et al. The miR-17-92 microRNA cluster: a novel diagnostic tool in large B-cell malignancies. Lab Invest 2012; 92: 1574-1582.
25. Mian M, Scandurra M, Chigrinova E, et al. Clinical and molecular characterization of diffuse large B-cell lymphomas with 13q14.3 deletion. Ann Oncol 2012; 23: 729-735.
26. Baraniskin A, Kuhnhenn J, Schlegel U, et al. MicroRNAs in cerebrospinal fluid as biomarker for disease course monitoring in primary central nervous system lymphoma. J Neurooncol 2012; 109: 239-244. These researchers showed that miRNAs can be detected in the CSF of PCNSL patients and may represent novel noninvasive biomarkers for this disease. This observation contrasts with the lack of elevated miRNA levels observed in the serum of PCNSL patients compared to controls.
27. Medina PP, Nolde M, Slack FJ. OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature 2010; 467: 86-90.
28. Thapa DR, Bhatia K, Bream JH, et al. B-cell activation induced microRNA-21 is elevated in circulating B cells preceding the diagnosis of AIDS-related non-Hodgkin lymphomas. AIDS 2012; 26: 1177-1180.
29. Watkins AJ, Hamoudi RA, Zeng N, et al. An integrated genomic and expression analysis of 7q deletion in splenic marginal zone lymphoma. PLoS One 2012; 7:e44997.
30. Arribas AJ, Campos-Martin Y, Gomez-Abad C, et al. Nodal marginal zone lymphoma: gene expression and miRNA profiling identify diagnostic markers and potential therapeutic targets. Blood 2012; 119:e9-e21.
31. Wang W, Corrigan-Cummins M, Hudson J, et al. MicroRNA profiling of follicular lymphoma identifies microRNAs related to cell proliferation and tumor response. Haematologica 2012; 97: 586-594. In this work, gene-expression profiles were obtained from follicular lymphoma samples following B-cell and T-cell separation. Compared with normal B-cells, 10 microRNAs were found to be increased (miR-193a-5p, miR-193b-, miR-345, miR- 513b, miR-574-3p, miR-584, miR-663, miR-1287, miR-1295, and miR-1471), 11 microRNAs were found to be decreased (miR-17-, miR-30a, miR-33a, miR-106a-, miR-141, miR-202, miR-205, miR-222, miR-301b, miR-431-, and miR-570), and 23 microRNAs were found to form a group with variable expression and clinical impacts in the follicular lymphoma samples.
32. Husby S, Geisler C, Gronbaek K. microRNAs in mantle cell lymphoma. Leuk Lymphoma 2013. [Epub ahead of print]
33. Iqbal J, Shen Y, Liu Y, et al. Genome-wide miRNA profiling of mantle cell lymphoma reveals a distinct subgroup with poor prognosis. Blood 2012; 119: 4939-4948.
34. Rao E, Jiang C, Ji M, et al. The miRNA-17 approximately 92 cluster mediates chemoresistance and enhances tumor growth in mantle cell lymphoma via PI3K/AKT pathway activation. Leukemia 2012; 26: 1064-1072. In addition to PTEN and BIM, these researchers showed that in MCL, miR-17-92 targets the protein phosphatase PHLPP2, which is an important negative regulator of the PI3K/AKT pathway.
35. Onnis A, Navari M, Antonicelli G, et al. Epstein-Barr nuclear antigen 1 induces expression of the cellular microRNA hsa-miR-127 and impairing B-cell differentiation in EBV-infected memory B cells. New insights into the pathogenesis of Burkitt lymphoma. Blood Cancer J 2012; 2:e84.
36. Kim JH, Kim WS, Park C. 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. Leuk Lymphoma 2012; 53: 1586-1591.
37. Lenze D, Leoncini L, Hummel M, et al. The different epidemiologic subtypes of Burkitt lymphoma share a homogenous micro RNA profile distinct from diffuse large B-cell lymphoma. Leukemia 2011; 25: 1869-1876.
38. Schneider B, Nagel S, Ehrentraut S, et al. Neoplastic miR-17-92 deregulation at a DNA fragility motif (SIDD). Genes Chromosomes Cancer 2012; 51: 219-228.
39. Kwanhian W, Lenze D, Alles J, et al. MicroRNA-142 is mutated in about 20% of diffuse large B-cell lymphoma. Cancer Med 2012; 1: 141-155.
40. Lin J, Lwin T, Zhao JJ, et al. Follicular dendritic cell-induced microRNAmediated upregulation of PRDM1 and downregulation of BCL-6 in non-Hodgkin's B-cell lymphomas. Leukemia 2011; 25: 145-152.
41. Zhang X, Chen X, Lin J, et al. Myc represses miR-15a/miR-16-1 expression through recruitment of HDAC3 in mantle cell and other non-Hodgkin B-cell lymphomas. Oncogene 2012; 31: 3002-3008.
42. Zhang X, Zhao X, Fiskus W, et al. Coordinated silencing of MYC-mediated miR-29 by HDAC3 and EZH2 as a therapeutic target of histone modification in aggressive B-Cell lymphomas. Cancer Cell 2012; 22: 506-523. In this study, the expression of the tumor suppressor miR-29 was restored by the disruption of the corepressor complex including MYC, HDAC3, and EZH2.
43. Maute RL, Schneider C, Sumazin P, et al. tRNA-derived microRNA modulates proliferation and the DNA damage response and is down-regulated in B cell lymphoma. Proc Natl Acad Sci USA 2013; 110: 1404-1409. In this work, it was demonstrated that a functional miRNA can be generated from tRNA. The miRNA CU1276 was the first such example in lymphoma. This miRNA is abundant in the normal germinal center B cells and targets RPA1, an essential gene involved in many aspects of DNA dynamics.
44. Craig VJ, Tzankov A, Flori M, et al. Systemic microRNA-34a delivery induces apoptosis and abrogates growth of diffuse large B-cell lymphoma in vivo. Leukemia 2012; 26: 2421-2424. In this model, the tumor-suppressive effect of miR-34a was restored and could be explained by the proapoptotic properties of this miRNA and by the specific knockdown of FOXP1.
45. Craig VJ, Cogliatti SB, Imig J, et al. Myc-mediated repression of microRNA- 34a promotes high-grade transformation of B-cell lymphoma by dysregulation of FoxP1. Blood 2011; 117: 6227-6236.