MicroRNA-155 influences B-cell receptor signaling and associates with aggressive disease in chronic lymphocytic leukemia

. 2014 Jul 24 ; 124 (4) : 546-54. [epub] 20140609

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid24914134

Grantová podpora
P01-CA81534 NCI NIH HHS - United States
R37-CA049870 NCI NIH HHS - United States
P01 CA081534 NCI NIH HHS - United States
R37 CA049870 NCI NIH HHS - United States
P30 CA023100 NCI NIH HHS - United States
P30 CA016058 NCI NIH HHS - United States

Odkazy

PubMed 24914134
PubMed Central PMC4110661
DOI 10.1182/blood-2014-03-559690
PII: S0006-4971(20)39936-5
Knihovny.cz E-zdroje

High-level leukemia cell expression of micro-RNA 155 (miR-155) is associated with more aggressive disease in patients with chronic lymphocytic leukemia (CLL), including those cases with a low-level expression of ζ-chain-associated protein of 70 kD. CLL with high-level miR-155 expressed lower levels of Src homology-2 domain-containing inositol 5-phosphatase 1 and were more responsive to B-cell receptor (BCR) ligation than CLL with low-level miR-155. Transfection with miR-155 enhanced responsiveness to BCR ligation, whereas transfection with a miR-155 inhibitor had the opposite effect. CLL in lymphoid tissue expressed higher levels of miR155HG than CLL in the blood of the same patient. Also, isolated CD5(bright)CXCR4(dim) cells, representing CLL that had been newly released from the microenvironment, expressed higher levels of miR-155 and were more responsive to BCR ligation than isolated CD5(dim)CXCR4(bright) cells of the same patient. Treatment of CLL or normal B cells with CD40-ligand or B-cell-activating factor upregulated miR-155 and enhanced sensitivity to BCR ligation, effects that could be blocked by inhibitors to miR-155. This study demonstrates that the sensitivity to BCR ligation can be enhanced by high-level expression of miR-155, which in turn can be induced by crosstalk within the tissue microenvironment, potentially contributing to its association with adverse clinical outcome in patients with CLL.

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Efremov DG, Gobessi S, Longo PG. Signaling pathways activated by antigen-receptor engagement in chronic lymphocytic leukemia B-cells. Autoimmun Rev. 2007;7(2):102–108. PubMed

Kil LP, Yuvaraj S, Langerak AW, Hendriks RW. The role of B cell receptor stimulation in CLL pathogenesis. Curr Pharm Des. 2012;18(23):3335–3355. PubMed

Chen L, Widhopf G, Huynh L, et al. Expression of ZAP-70 is associated with increased B-cell receptor signaling in chronic lymphocytic leukemia. Blood. 2002;100(13):4609–4614. PubMed

Chen L, Huynh L, Apgar J, et al. ZAP-70 enhances IgM signaling independent of its kinase activity in chronic lymphocytic leukemia. Blood. 2008;111(5):2685–2692. PubMed PMC

Woyach JA, Johnson AJ, Byrd JC. The B-cell receptor signaling pathway as a therapeutic target in CLL. Blood. 2012;120(6):1175–1184. PubMed PMC

Vigorito E, Perks KL, Abreu-Goodger C, et al. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity. 2007;27(6):847–859. PubMed PMC

Koralov SB, Muljo SA, Galler GR, et al. Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell. 2008;132(5):860–874. PubMed

Calin GA, Ferracin M, Cimmino A, et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005;353(17):1793–1801. PubMed

Mraz M, Pospisilova S, Malinova K, Slapak I, Mayer J. MicroRNAs in chronic lymphocytic leukemia pathogenesis and disease subtypes. Leuk Lymphoma. 2009;50(3):506–509. PubMed

Mraz M, Dolezalova D, Plevova K, et al. MicroRNA-650 expression is influenced by immunoglobulin gene rearrangement and affects the biology of chronic lymphocytic leukemia. Blood. 2012;119(9):2110–2113. PubMed

Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr Biol. 2002;12(9):735–739. PubMed

Tam W, Ben-Yehuda D, Hayward WS. bic, a novel gene activated by proviral insertions in avian leukosis virus-induced lymphomas, is likely to function through its noncoding RNA. Mol Cell Biol. 1997;17(3):1490–1502. PubMed PMC

Leng RX, Pan HF, Qin WZ, Chen GM, Ye DQ. Role of microRNA-155 in autoimmunity. Cytokine Growth Factor Rev. 2011;22(3):141–147. PubMed

Eis PS, Tam W, Sun L, et al. Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc Natl Acad Sci USA. 2005;102(10):3627–3632. PubMed PMC

Kluiver J, Poppema S, de Jong D, et al. BIC and miR-155 are highly expressed in Hodgkin, primary mediastinal and diffuse large B cell lymphomas. J Pathol. 2005;207(2):243–249. PubMed

Zhang Y, Roccaro AM, Rombaoa C, et al. LNA-mediated anti-miR-155 silencing in low-grade B-cell lymphomas. Blood. 2012;120(8):1678–1686. PubMed

Calin GA, Liu CG, Sevignani C, et al. MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. Proc Natl Acad Sci USA. 2004;101(32):11755–11760. PubMed PMC

Marton S, Garcia MR, Robello C, et al. Small RNAs analysis in CLL reveals a deregulation of miRNA expression and novel miRNA candidates of putative relevance in CLL pathogenesis. Leukemia. 2008;22(2):330–338. PubMed

Wang M, Tan LP, Dijkstra MK, et al. miRNA analysis in B-cell chronic lymphocytic leukaemia: proliferation centres characterized by low miR-150 and high BIC/miR-155 expression. J Pathol. 2008;215(1):13–20. PubMed

Nana-Sinkam SP, Croce CM. MicroRNA in chronic lymphocytic leukemia: transitioning from laboratory-based investigation to clinical application. Cancer Genet Cytogenet. 2010;203(2):127–133. PubMed

Costinean S, Zanesi N, Pekarsky Y, et al. Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in E(mu)-miR155 transgenic mice. Proc Natl Acad Sci USA. 2006;103(18):7024–7029. PubMed PMC

Visone R, Rassenti LZ, Veronese A, et al. Karyotype-specific microRNA signature in chronic lymphocytic leukemia. Blood. 2009;114(18):3872–3879. PubMed PMC

Rossi S, Shimizu M, Barbarotto E, et al. microRNA fingerprinting of CLL patients with chromosome 17p deletion identify a miR-21 score that stratifies early survival. Blood. 2010;116(6):945–952. PubMed PMC

Vargova K, Curik N, Burda P, et al. MYB transcriptionally regulates the miR-155 host gene in chronic lymphocytic leukemia. Blood. 2011;117(14):3816–3825. PubMed

Zhu DX, Zhu W, Fang C, et al. miR-181a/b significantly enhances drug sensitivity in chronic lymphocytic leukemia cells via targeting multiple anti-apoptosis genes. Carcinogenesis. 2012;33(7):1294–1301. PubMed

O’Connell RM, Chaudhuri AA, Rao DS, Baltimore D. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci USA. 2009;106(17):7113–7118. PubMed PMC

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(5):288–295. PubMed PMC

Zolnierowicz S, Bollen M. Protein phosphorylation and protein phosphatases. De Panne, Belgium, September 19-24, 1999. EMBO J. 2000;19(4):483–488. PubMed PMC

Nakamura K, Brauweiler A, Cambier JC. Effects of Src homology domain 2 (SH2)-containing inositol phosphatase (SHIP), SH2-containing phosphotyrosine phosphatase (SHP)-1, and SHP-2 SH2 decoy proteins on Fc gamma RIIB1-effector interactions and inhibitory functions. J Immunol. 2000;164(2):631–638. PubMed

Herishanu Y, Pérez-Galán P, Liu D, et al. The lymph node microenvironment promotes B-cell receptor signaling, NF-kappaB activation, and tumor proliferation in chronic lymphocytic leukemia. Blood. 2011;117(2):563–574. PubMed PMC

Rassenti LZ, Huynh L, Toy TL, et al. ZAP-70 compared with immunoglobulin heavy-chain gene mutation status as a predictor of disease progression in chronic lymphocytic leukemia. N Engl J Med. 2004;351(9):893–901. PubMed

Haferlach T, Kohlmann A, Wieczorek L, et al. Clinical utility of microarray-based gene expression profiling in the diagnosis and subclassification of leukemia: report from the International Microarray Innovations in Leukemia Study Group. J Clin Oncol. 2010;28(15):2529–2537. PubMed PMC

Calissano C, Damle RN, Marsilio S, et al. Intraclonal complexity in chronic lymphocytic leukemia: fractions enriched in recently born/divided and older/quiescent cells. Mol Med. 2011;17(11-12):1374–1382. PubMed PMC

Ghia P, Strola G, Granziero L, et al. Chronic lymphocytic leukemia B cells are endowed with the capacity to attract CD4+, CD40L+ T cells by producing CCL22. Eur J Immunol. 2002;32(5):1403–1413. PubMed

Nishio M, Endo T, Tsukada N, et al. Nurselike cells express BAFF and APRIL, which can promote survival of chronic lymphocytic leukemia cells via a paracrine pathway distinct from that of SDF-1alpha. Blood. 2005;106(3):1012–1020. PubMed PMC

Papakonstantinou N, Ntoufa S, Chartomatsidou E, et al. Differential microRNA profiles and their functional implications in different immunogenetic subsets of chronic lymphocytic leukemia. Mol Med. 2013;19:115–123. PubMed PMC

Ferrajoli A, Shanafelt TD, Ivan C, et al. Prognostic value of miR-155 in individuals with monoclonal B-cell lymphocytosis and patients with B chronic lymphocytic leukemia. Blood. 2013;122(11):1891–1899. PubMed PMC

Tableman M, Kim JS. Survival Analysis Using S: Analysis of Time-to-Event Data. Boca Raton, FL: Chapman & Hall/CRC; 2004.

Lössner C, Meier J, Warnken U, et al. Quantitative proteomics identify novel miR-155 target proteins. PLoS ONE. 2011;6(7):e22146. PubMed PMC

Chang CC, Zhang QY, Liu Z, Clynes RA, Suciu-Foca N, Vlad G. Downregulation of inflammatory microRNAs by Ig-like transcript 3 is essential for the differentiation of human CD8(+) T suppressor cells. J Immunol. 2012;188(7):3042–3052. PubMed

di Iasio MG, Norcio A, Melloni E, Zauli G. SOCS1 is significantly up-regulated in Nutlin-3-treated p53(wild-type) B chronic lymphocytic leukemia (B-CLL) samples and shows an inverse correlation with miR-155. Invest New Drugs. 2012;30(6):2403–2406. PubMed

Neilsen PM, Noll JE, Mattiske S, et al. Mutant p53 drives invasion in breast tumors through up-regulation of miR-155. Oncogene. 2013;32(24):2992–3000. PubMed

Gaidano G, Foà R, Dalla-Favera R. Molecular pathogenesis of chronic lymphocytic leukemia. J Clin Invest. 2012;122(10):3432–3438. PubMed PMC

Endo T, Nishio M, Enzler T, et al. BAFF and APRIL support chronic lymphocytic leukemia B-cell survival through activation of the canonical NF-kappaB pathway. Blood. 2007;109(2):703–710. PubMed PMC

Zarnegar B, He JQ, Oganesyan G, Hoffmann A, Baltimore D, Cheng G. Unique CD40-mediated biological program in B cell activation requires both type 1 and type 2 NF-kappaB activation pathways. Proc Natl Acad Sci USA. 2004;101(21):8108–8113. PubMed PMC

Kluiver J, van den Berg A, de Jong D, et al. Regulation of pri-microRNA BIC transcription and processing in Burkitt lymphoma. Oncogene. 2007;26(26):3769–3776. PubMed

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