Involvement of MicroRNA in T-Cell Differentiation and Malignancy
-
Najmaldin Saki
,
Saeid Abroun
,
Masoud Soleimani
,
Saeideh Hajizamani
,
Mohammad Shahjahani
,
Richard E Kast
,
Yousef Mortazavi
Abstract
MicroRNAs are 19-22 nucleotide RNAs involved in such important processes as development, proliferation, differentiation and apoptosis. Different miRNAs are uniquely expressed in lymphoid T cells, and play a role indevelopment and differentiation of various subtypes by targeting their target genes. Recent studies have shown that aberrant miRNA expression may be involved in T cell leukemogenesis and lymphogenesis, and may function as tumor suppressor (such as miR-451, miR-31, miR-150, and miR-29a) or oncogene (e.g. miR-222, miR-223, miR-17-92, miR-155). MiRNAs can be used as new biomarkers for prognosis and diagnosis or as an index of disease severity in T-cell leukemia and lymphoma. This article presents a review of studies in recent years on the role of miRNAs in T-cell development and their aberrant expression in pathogenesis of T-cell leukemia and lymphoma. Characterizing miRNAs can help recognize their role as new important molecules with prognostic and therapeutic applications.
Zardo G, Ciolfi A, Vian L, et al. Transcriptional targeting by microRNA-Polycomb complexes: A novel route in cell fate determination. Cell Cycle. 2012; 11(19):3543-9.
Iorio MV, Croce CM. MicroRNAs in cancer: small molecules with a huge impact. Journal of Clinical Oncology. 2009; 27(34):5848-56.
Bianchi N, Zuccato C, Finotti A, Lampronti I, Borgatti M, Gambari R. Involvement of miRNA in erythroid differentiation. Epigenomics. 2012; 4(1):51-65.
Davidson-Moncada J, Papavasiliou FN, Tam W. MicroRNAs of the immune system: roles in inflammation and cancer. Annals of the New York Academy of Sciences. 2010 Jan; 1183:183-94.
Schickel R, Boyerinas B, Park SM, et al. MicroRNAs: key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene. [Review]. 2008 Oct 6; 27(45):5959-74.
Carissimi C, Fulci V, Macino G. MicroRNAs: novel regulators of immunity. Autoimmunity reviews. 2009 May; 8(6):520-4.
Staal FJ, Weerkamp F, Langerak AW, et al. Transcriptional control of T lymphocyte differentiation. Stem Cells. 2001; 19(3):165-79.
Crotty S, Johnston RJ, Schoenberger SP. Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nature immunology. 2010; 11(2):114-20.
Ghisi M, Corradin A, Basso K, et al. Modulation of microRNA expression in human T-cell development: targeting of NOTCH3 by miR-150. Blood. 2011; 117(26):7053-62.
Lawrie CH. MicroRNAs and lymphomagenesis: a functional review. British journal of haematology. 2012.
Baltimore D, Boldin MP, O'Connell RM, et al. MicroRNAs: new regulators of immune cell development and function. Nature immunology. 2008; 9(8):839-45.
Navarro F, Lieberman J. Small RNAs guide hematopoietic cell differentiation and function. The Journal of Immunology. 2010; 184(11):5939-47.
Yu D, Rao S, Tsai LM, et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity. 2009; 31(3):457-68.
Tsitsiou E, Lindsay MA. MicroRNAs and the immune response. Current opinion in pharmacology. 2009; 9(4):514-20.
Wu T, Wieland A, Araki K, et al. Temporal expression of microRNA cluster miR-17-92 regulates effector and memory CD8+ T-cell differentiation. Proceedings of the National Academy of Sciences. 2012; 109(25):9965-70.
Salaun B, Yamamoto T, Badran B, et al. Differentiation associated regulation of microRNA expression in vivo in human CD8+ T cell subsets. Journal of translational medicine. 2011;9:44.
Rossi RL, Rossetti G, Wenandy L, et al. Distinct microRNA signatures in human lymphocyte subsets and enforcement of the naive state in CD4+ T cells by the microRNA miR-125b. Nature immunology. 2011; 12(8):796-803.
Bellon M, Lepelletier Y, Hermine O, et al. Deregulation of microRNA involved in hematopoiesis and the immune response in HTLV-I adult T-cell leukemia. Blood. 2009 May 14; 113(20):4914-7.
Shaham L, Binder V, Gefen N, Borkhardt A, Izraeli S. MiR-125 in normal and malignant hematopoiesis. Leukemia. 2012; 26(9):2011-8.
Ooi AL, Sahoo D, Adorno M, et al. MicroRNA-125b expands hematopoietic stem cells and enriches for the lymphoid-balanced and lymphoid-biased subsets. Proceedings of the National Academy of Sciences. 2010; 107(50):21505-10.
Schotte D, Pieters R, Den Boer M. MicroRNAs in acute leukemia: from biological players to clinical contributors. Leukemia. 2011; 26(1):1-12.
Starczynowski DT, Kuchenbauer F, Wegrzyn J, et al. MicroRNA-146a disrupts hematopoietic differentiation and survival. Experimental hematology. 2011; 39(2):167-78. e4.
Lu L-F, Boldin MP, Chaudhry A, Lin L-L, Taganov KD, Hanada T. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell. 2010; 142(6):914-29.
Belver L, Papavasiliou FN, Ramiro AR. MicroRNA control of lymphocyte differentiation and function. Current opinion in immunology. 2011 Jun; 23(3):368-73.
Chung Y, Chang SH, Martinez GJ, et al. Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity. 2009;30(4):576-87.
Maitra U, Davis S, Reilly CM, et al. Differential regulation of Foxp3 and IL-17 expression in CD4 T helper cells by IRAK-1. The Journal of Immunology. 2009; 182(9):5763-9.
Rusca N, Deho L, Montagner S, et al. MiR-146a and NF-kappaB1 regulate mast cell survival and T lymphocyte differentiation. Mol Cell Biol. 2012 Nov;32(21):4432-44.
Quinn EM, Wang JH, O'Callaghan G, et al. MicroRNA-146a is upregulated by and negatively regulates TLR2 signaling. PLoS One. 2013; 8(4):e62232.
Niimoto T, Nakasa T, Ishikawa M, et al. MicroRNA-146a expresses in interleukin-17 producing T cells in rheumatoid arthritis patients. BMC musculoskeletal disorders. 2010; 11(1):209.
Curtale G, Citarella F, Carissimi C, et al. An emerging player in the adaptive immune response: microRNA-146a is a modulator of IL-2 expression and activation-induced cell death in T lymphocytes. Blood. 2010; 115(2):265-73.
Monticelli S, Ansel KM, Xiao C, et al. MicroRNA profiling of the murine hematopoietic system. Genome Biol. 2005; 6(8):R71.
Saki N, Abroun S, Soleimani M, et al. The roles of miR-146a in the differentiation of Jurkat T-lymphoblasts. Hematology. 2013 Jun 22.
Fallah P, Arefian E, Naderi M, et al. miR-146a and miR-150 promote the differentiation of CD133 (+) cells into T-lymphoid lineage. Mol Biol Rep. 2013 Aug; 40(8):4713-9.
Merkerova M, Belickova M, Bruchova H. Differential expression of microRNAs in hematopoietic cell lineages. Eur J Haematol. 2008 Oct; 81(4):304-10.
Zhou B, Wang S, Mayr C, et al. miR-150, a microRNA expressed in mature B and T cells, blocks early B cell development when expressed prematurely. Proc Natl Acad Sci U S A. 2007 Apr 24; 104(17):7080-5.
Tano N, Kim HW, Ashraf M. microRNA-150 regulates mobilization and migration of bone marrow-derived mononuclear cells by targeting Cxcr4. PLoS One. 2011; 6(10):e23114.
Dunand-Sauthier I, Santiago-Raber ML, Capponi L, et al. Silencing of c-Fos expression by microRNA-155 is critical for dendritic cell maturation and function. Blood. 2011 Apr 28; 117(17):4490-500.
O'Connell RM, Rao DS, Chaudhuri AA, et al. Physiological and pathological roles for microRNAs in the immune system. Nature Reviews Immunology. 2010; 10(2):111-22.
Rodriguez A, Vigorito E, Clare S, et al. Requirement of bic/microRNA-155 for normal immune function. Science. 2007 Apr 27; 316(5824):608-11.
Kohlhaas S, Garden OA, Scudamore C, et al. Cutting edge: the Foxp3 target miR-155 contributes to the development of regulatory T cells. J Immunol. 2009 Mar 1; 182(5):2578-82.
Banerjee A, Schambach F, DeJong CS, et al. Micro-RNA-155 inhibits IFN-gamma signaling in CD4+ T cells. Eur J Immunol. 2010 Jan; 40(1):225-31.
Gracias DT, Stelekati E, Hope JL, et al. The microRNA miR-155 controls CD8 (+) T cell responses by regulating interferon signaling. Nature immunology. 2013 Jun; 14(6):593-602.
McCoy CE, Sheedy FJ, Qualls JE, et al. IL-10 inhibits miR-155 induction by toll-like receptors. J Biol Chem. 2010 Jul 2; 285(27):20492-8.
Stefani G, Slack FJ. Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol. 2008 Mar; 9(3):219-30.
Chen CZ, Li L, Lodish HF, et al. MicroRNAs modulate hematopoietic lineage differentiation. Science. 2004 Jan 2; 303(5654):83-6.
Xue Q, Guo ZY, Li W, et al. Human activated CD4(+) T lymphocytes increase IL-2 expression by downregulating microRNA-181c. Molecular Immunology. 2011 Jan; 48(4):592-9.
Labrecque N, Baldwin T, Lesage S. Molecular and genetic parameters defining T-cell clonal selection. Immunol Cell Biol. 2011 Jan;89(1):16-26.
Liu G, Min H, Yue S, et al. Pre-miRNA loop nucleotides control the distinct activities of mir-181a-1 and mir-181c in early T cell development. PLoS One. 2008; 3(10):e3592.
Laufer TM. T-cell sensitivity: a microRNA regulates the sensitivity of the T-cell receptor. Immunol Cell Biol. 2007 Jul; 85(5):346-7.
Li QJ, Chau J, Ebert PJ, et al. miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell. 2007 Apr 6; 129(1):147-61.
Marengère LE, Waterhouse P, Duncan GS, et al. Regulation of T cell receptor signaling by tyrosine phosphatase SYP association with CTLA-4. Science. 1996; 272(5265):1170-3.
Fragoso R, Mao T, Wang S, et al. Modulating the strength and threshold of NOTCH oncogenic signals by mir-181a-1/b-1. PLoS Genet. 2012; 8(8):e1002855.
Haftmann C, Stittrich AB, Sgouroudis E, et al. Lymphocyte signaling: regulation of FoxO transcription factors by microRNAs. Annals of the New York Academy of Sciences. 2012 Jan; 1247:46-55.
Stittrich AB, Haftmann C, Sgouroudis E, et al. The microRNA miR-182 is induced by IL-2 and promotes clonal expansion of activated helper T lymphocytes. Nature immunology. 2010 Nov; 11(11):1057-62.
Alexander T, Haftmann C, Templin L, et al. A3. 22 Upregulated microRNA-182 Expression is Associated with Enhanced Conventional CD4+ T Cell Proliferation in SLE. Annals of the Rheumatic Diseases. 2013; 72(Suppl 1):A21-A.
Huang B, Zhao J, Lei Z, et al. miR-142-3p restricts cAMP production in CD4+CD25- T cells and CD4+CD25+ TREG cells by targeting AC9 mRNA. EMBO Rep. 2009 Feb; 10(2):180-5.
Zhou Q, Haupt S, Prots I, Thummler K, Kremmer E, Lipsky PE, et al. miR-142-3p is involved in CD25+ CD4 T cell proliferation by targeting the expression of glycoprotein A repetitions predominant. J Immunol. 2013 Jun 15; 190(12):6579-88.
Wu H, Neilson JR, Kumar P, et al. miRNA profiling of naive, effector and memory CD8 T cells. PLoS One. 2007; 2(10):e1020.
Kuchen S, Resch W, Yamane A, et al. Regulation of microRNA expression and abundance during lymphopoiesis. Immunity. 2010; 32(6):828-39.
Rouas R, Fayyad-Kazan H, El Zein N, et al. Human natural Treg microRNA signature: role of microRNA-31 and microRNA-21 in FOXP3 expression. Eur J Immunol. 2009 Jun;39(6):1608-18.
Du C, Liu C, Kang J, , et al. MicroRNA miR-326 regulates TH-17 differentiation and is associated with the pathogenesis of multiple sclerosis. Nature immunology. 2009 Dec; 10(12):1252-9.
Bellon M, Lepelletier Y, Hermine O, et al. Deregulation of microRNA involved in hematopoiesis and the immune response in HTLV-I adult T-cell leukemia. Blood. 2009; 113(20):4914-7.
Bhatia S, Kaul D, Varma N. Functional genomics of tumor suppressor miR-196b in T-cell acute lymphoblastic leukemia. Mol Cell Biochem. 2011 Jan; 346(1-2):103-16.
Iacobucci I, Papayannidis C, Lonetti A, et al. Cytogenetic and molecular predictors of outcome in acute lymphocytic leukemia: recent developments. Curr Hematol Malig Rep. 2012;7(2):133-43.
Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer. 2006 Nov; 6(11):857-66.
de Oliveira JC, Brassesco MS, Scrideli CA, et al. MicroRNA expression and activity in pediatric acute lymphoblastic leukemia (ALL). Pediatr Blood Cancer. 2012 Oct; 59(4):599-604.
Fulci V, Colombo T, Chiaretti S, et al. Characterization of B- and T-lineage acute lymphoblastic leukemia by integrated analysis of MicroRNA and mRNA expression profiles. Genes Chromosomes Cancer. 2009 Dec; 48(12):1069-82.
Schotte D, Lange-Turenhout EA, Stumpel DJ, et al. Expression of miR-196b is not exclusively MLL-driven but is especially linked to activation of HOXA genes in pediatric acute lymphoblastic leukemia. Haematologica. 2010 Oct; 95(10):1675-82.
Mansour MR, Sanda T, Lawton LN, et al. The TAL1 complex targets the FBXW7 tumor suppressor by activating miR-223 in human T cell acute lymphoblastic leukemia. J Exp Med. 2013 Jul 29; 210(8):1545-57.
Mavrakis KJ, Van Der Meulen J, Wolfe AL, et al. A cooperative microRNA-tumor suppressor gene network in acute T-cell lymphoblastic leukemia (T-ALL). Nat Genet. 2011 Jul;43(7):673-8.
Chiaretti S, Messina M, Tavolaro S, et al. Gene expression profiling identifies a subset of adult T-cell acute lymphoblastic leukemia with myeloid-like gene features and over-expression of miR-223. Haematologica. 2010 Jul; 95(7):1114-21.
Gusscott S, Kuchenbauer F, Humphries RK, et al. Notch-mediated repression of miR-223 contributes to IGF1R regulation in T-ALL. Leuk Res. 2012 Jul; 36(7):905-11.
Lawrie CH. MicroRNAs and haematology: small molecules, big function. British journal of haematology. 2007 Jun; 137(6):503-12.
Coskun E, Neumann M, Schlee C, et al. MicroRNA profiling reveals aberrant microRNA expression in adult ETP-ALL and functional studies implicate a role for miR-222 in acute leukemia. Leuk Res. 2013 Jun; 37(6):647-56.
van Oirschot BA, Stahl M, Lens SM, et al. Protein kinase A regulates expression of p27 (kip1) and cyclin D3 to suppress proliferation of leukemic T cell lines. J Biol Chem. 2001 Sep 7; 276(36):33854-60.
Lv M, Zhang X, Jia H, et al. An oncogenic role of miR-142-3p in human T-cell acute lymphoblastic leukemia (T-ALL) by targeting glucocorticoid receptor-alpha and cAMP/PKA pathways. Leukemia. 2012 Apr; 26(4):769-77.
Greenstein S, Ghias K, Krett NL, et al. Mechanisms of glucocorticoid-mediated apoptosis in hematological malignancies. Clin Cancer Res. 2002 Jun;8(6):1681-94.
Gimenes-Teixeira HL, Lucena-Araujo AR, Dos Santos GA, et al. Increased expression of miR-221 is associated with shorter overall survival in T-cell acute lymphoid leukemia. Exp Hematol Oncol. 2013; 2(1):10.
Schotte D, De Menezes RX, Akbari Moqadam F, et al. MicroRNA characterize genetic diversity and drug resistance in pediatric acute lymphoblastic leukemia. Haematologica. 2011 May; 96(5):703-11.
Coskun E, von der Heide EK, Schlee C, et al. The role of microRNA-196a and microRNA-196b as ERG regulators in acute myeloid leukemia and acute T-lymphoblastic leukemia. Leuk Res. 2011 Feb; 35(2):208-13.
Baldus CD, Burmeister T, Martus P, et al. High expression of the ETS transcription factor ERG predicts adverse outcome in acute T-lymphoblastic leukemia in adults. J Clin Oncol. 2006 Oct 10; 24(29):4714-20.
Ye H, Liu X, Lv M, Wu Y, et al. MicroRNA and transcription factor co-regulatory network analysis reveals miR-19 inhibits CYLD in T-cell acute lymphoblastic leukemia. Nucleic Acids Res. 2012 Jul; 40(12):5201-14.
Li X, Sanda T, Look AT,et al. Repression of tumor suppressor miR-451 is essential for NOTCH1-induced oncogenesis in T-ALL. J Exp Med. 2011 Apr 11; 208(4):663-75.
Nagel S, Venturini L, Przybylski GK, et al. Activation of miR-17-92 by NK-like homeodomain proteins suppresses apoptosis via reduction of E2F1 in T-cell acute lymphoblastic leukemia. Leuk Lymphoma. 2009 Jan; 50(1):101-8.
Matsuoka M, Jeang K-T. Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nature Reviews Cancer. 2007; 7(4):270-80.
Ishihara K, Sasaki D, Tsuruda K, et al. Impact of miR-155 and miR-126 as novel biomarkers on the assessment of disease progression and prognosis in adult T-cell leukemia. Cancer Epidemiol. 2012 Dec; 36(6):560-5.
Tomita M. Important Roles of Cellular MicroRNA miR-155 in Leukemogenesis by Human T-Cell Leukemia Virus Type 1 Infection. ISRN Microbiol. 2012; 2012:978607.
Tomita M, Tanaka Y, Mori N. MicroRNA miR-146a is induced by HTLV-1 tax and increases the growth of HTLV-1-infected T-cells. Int J Cancer. 2012 May 15; 130(10):2300-9.
Yamagishi M, Watanabe T. Molecular hallmarks of adult T cell leukemia. Front Microbiol. 2012; 3:334.
Yamagishi M, Nakano K, Miyake A, et al. Polycomb-mediated loss of miR-31 activates NIK-dependent NF-kappaB pathway in adult T cell leukemia and other cancers. Cancer Cell. 2012 Jan 17;21(1):121-35.
Chan TS, Kwong YL, Tse E. Novel therapeutic agents for T-cell lymphomas. Discov Med. 2013 Aug; 16(86):27-35.
Jaffe ES, Nicolae A, Pittaluga S. Peripheral T-cell and NK-cell lymphomas in the WHO classification: pearls and pitfalls. Mod Pathol. 2013 Jan; 26 Suppl 1:S71-87.
Ralfkiaer U, Hagedorn PH, Bangsgaard N, et al. Diagnostic microRNA profiling in cutaneous T-cell lymphoma (CTCL). Blood. 2011 Nov 24; 118(22):5891-900.
Manfe V, Biskup E, Rosbjerg A, et al. miR-122 regulates p53/Akt signalling and the chemotherapy-induced apoptosis in cutaneous T-cell lymphoma. PLoS One. 2012; 7(1):e29541.
Fabbri M, Garzon R, Andreeff M, et al. MicroRNAs and noncoding RNAs in hematological malignancies: molecular, clinical and therapeutic implications. Leukemia. 2008 Jun; 22(6):1095-105.
Ballabio E, Mitchell T, van Kester MS, et al. MicroRNA expression in Sezary syndrome: identification, function, and diagnostic potential. Blood. 2010 Aug 19; 116(7):1105-13.
Qin Y, Buermans HP, van Kester MS, et al. Deep-sequencing analysis reveals that the miR-199a2/214 cluster within DNM3os represents the vast majority of aberrantly expressed microRNAs in Sezary syndrome. J Invest Dermatol. 2012 May; 132(5):1520-2.
Narducci MG, Arcelli D, Picchio MC, et al. MicroRNA profiling reveals that miR-21, miR486 and miR-214 are upregulated and involved in cell survival in Sezary syndrome. Cell Death Dis. 2011; 2:e151.
Kopp KL, Ralfkiaer U, Gjerdrum LM, et al. STAT5-mediated expression of oncogenic miR-155 in cutaneous T-cell lymphoma. Cell Cycle. 2013 Jun 15; 12(12):1939-47.
Van Kester MS, Ballabio E, Benner MF, et al. miRNA expression profiling of mycosis fungoides. Mol Oncol. 2011 Jun; 5(3):273-80.
Maj J, Jankowska-Konsur A, Sadakierska-Chudy A, et al. Altered microRNA expression in mycosis fungoides. Br J Dermatol. 2012 Feb; 166(2):331-6.
Ng SB, Yan J, Huang G, et al. Dysregulated microRNAs affect pathways and targets of biologic relevance in nasal-type natural killer/T-cell lymphoma. Blood. 2011 Nov 3;118(18):4919-29.
Yamanaka Y, Tagawa H, Takahashi N, , et al. Aberrant overexpression of microRNAs activate AKT signaling via down-regulation of tumor suppressors in natural killer-cell lymphoma/leukemia. Blood. 2009 Oct 8; 114(15):3265-75.
Watanabe A, Tagawa H, Yamashita J, et al. The role of microRNA-150 as a tumor suppressor in malignant lymphoma. Leukemia. 2011 Aug;25(8):1324-34.
Guo HQ, Huang GL, Guo CC, et al. Diagnostic and prognostic value of circulating miR-221 for extranodal natural killer/T-cell lymphoma. Dis Markers. 2010; 29(5):251-8.
Huang HB, Zhan R, Wu SQ, et al. [Expression of MCL-1 and microRNA-29a in extranodal NK/T-cell lymphoma tissue]. Zhongguo Shi Yan Xue Ye Xue Za Zhi. 2013 Feb; 21(1):95-8.
Ti HJ, Nong L, Wang W, et al. [Expression of microRNA in extranodal NK/T cell lymphoma, nasal type]. Zhonghua Bing Li Xue Za Zhi. 2011 Sep; 40(9):610-5.
Xi Y, Li J, Zan L, et al. Micro-RNA-16 expression in paraffin-embedded specimen correlates with overall survival of T-lymphoblastic lymphoma/leukemia. Hum Pathol. 2013 Jun; 44(6):1011-6.
Gonzalez-Gugel E, Villa-Morales M, Santos J, et al. Down-regulation of specific miRNAs enhances the expression of the gene Smoothened and contributes to T-cell lymphoblastic lymphoma development. Carcinogenesis. 2013 Apr; 34(4):902-8.
Cimmino A, Calin GA, Fabbri M, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci U S A. 2005 Sep 27; 102(39):13944-9.
Vasilatou D, Papageorgiou S, Pappa V, et al. The role of microRNAs in normal and malignant hematopoiesis. Eur J Haematol. 2010 Jan 1; 84(1):1-16.
Muljo SA, Ansel KM, Kanellopoulou C, et al. Aberrant T cell differentiation in the absence of Dicer. J Exp Med. 2005 Jul 18; 202(2):261-9.
Zhang N, Bevan MJ. Dicer controls CD8+ T-cell activation, migration, and survival. Proc Natl Acad Sci U S A. 2010 Dec 14; 107(50):21629-34.
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