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Current Medicinal Chemistry


ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

General Review Article

Role of microRNAs in Chronic Lymphocytic Leukemia Pathogenesis

Author(s): Ehsan Javandoost, Ehsan Firoozi-Majd, Hosein Rostamian, Mohammad Khakpoor- Koosheh and Hamid Reza Mirzaei*

Volume 27 , Issue 2 , 2020

Page: [282 - 297] Pages: 16

DOI: 10.2174/0929867326666190911114842

Price: $65


MicroRNAs (miRNAs) are a group of small endogenous non-coding RNAs involved in many cancers and various cellular processes such as cellular growth, DNA methylation, apoptosis, and differentiation. 13q14.3 chromosomal region contains miR-15 and miR-16 and deletion of this region is a commonly reported aberration in Chronic Lymphoblastic Leukemia (CLL), suggesting miRNAs involvement in CLL pathogenesis. MicroRNAs are known as oncogenes and tumor suppressors in CLL which may also serve as markers of onset and progression of the disease. The most prevalent form of leukemia diagnosed in adults in the western world, chronic lymphocytic leukemia, accounts for one-third of all leukemias. CLL is characterized by the presence of B Cell Malignant Clones in secondary lymphoid tissues, peripheral blood and bone marrow. The precise etiology of CLL is remained to be known, however, a number of Chromosomal Abnormalities such as deletions of 13q14.3, 11q and 17p and trisomy 12 have been detected. In this review, we offer our prospect on how miRNAs are involved in the CLL pathogenesis and disease progression. Further understanding of the underlying mechanisms and regulation of CLL pathogenesis has underscored the need for further research regarding their role in this disease.

Keywords: Chronic lymphoblastic leukemia, MicroRNAs, pathogenesis, Chronic Lymphoblastic Leukemia (CLL), B cell malignant clones, chromosomal abnormalities.

Pleyer, L.; Egle, A.; Hartmann, T.N.; Greil, R. Molecular and cellular mechanisms of CLL: novel therapeutic approaches. Nat. Rev. Clin. Oncol., 2009, 6(7), 405-418.
[] [PMID: 19488076]
Mirzaei, H.; Fathullahzadeh, S.; Khanmohammadi, R.; Darijani, M.; Momeni, F.; Masoudifar, A.; Goodarzi, M.; Mardanshah, O.; Stenvang, J.; Jaafari, M.R.; Mirzaei, H.R. State of the art in microRNA as diagnostic and therapeutic biomarkers in chronic lymphocytic leukemia. J. Cell. Physiol., 2018, 233(2), 888-900.
[] [PMID: 28084621]
Fathullahzadeh, S.; Mirzaei, H.; Honardoost, M.A.; Sahebkar, A.; Salehi, M. Circulating microRNA-192 as a diagnostic biomarker in human chronic lymphocytic leukemia. Cancer Gene Ther., 2016, 23(10), 327-332.
[] [PMID: 27659777]
Bartel, D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2), 281-297.
[] [PMID: 14744438]
Lee, R.C.; Feinbaum, R.L.; Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 1993, 75(5), 843-854.
[] [PMID: 8252621]
Mashreghi, M.; Azarpara, H.; Bazaz, M.R.; Jafari, A.; Masoudifar, A.; Mirzaei, H. Angiogenesis biomarkers and their targeting ligands as potential targets for tumor angiogenesis. J. Cell. Physiol., 2018, 233(4), 2949-2965.
[] [PMID: 28608549]
Masoudi, M.S.; Mehrabian, E.; Mirzaei, H. MiR-21: A key player in glioblastoma pathogenesis. J. Cell. Biochem., 2018, 119(2), 1285-1290.
[] [PMID: 28727188]
Rashidi, B.; Hoseini, Z.; Sahebkar, A.; Mirzaei, H. Anti-atherosclerotic effects of vitamins D and E in suppression of atherogenesis. J. Cell. Physiol., 2017, 232(11), 2968-2976.
[] [PMID: 27966778]
Rabieian, R.; Boshtam, M.; Zareei, M.; Kouhpayeh, S.; Masoudifar, A.; Mirzaei, H. Plasminogen activator inhibitor type-1 as a regulator of fibrosis. J. Cell. Biochem., 2018, 19(11), 17-27.
[] [PMID: 28520219]
Mirzaei, H.; Ferns, G.A.; Avan, A.; Mobarhan, M.G. Cytokines and MicroRNA in coronary artery disease. Adv. Clin. Chem., 2017, 82, 47-70.
[] [PMID: 28939213]
Jafari, S.H.; Saadatpour, Z.; Salmaninejad, A.; Momeni, F.; Mokhtari, M.; Nahand, J.S.; Rahmati, M.; Mirzaei, H. Breast cancer diagnosis: Imaging techniques and biochemical markers. J. Cell. Physiol., 2018, 233(7), 5200-5213.
[] [PMID: 29219189]
Khani, P.; Nasri, F.; Khani Chamani, F.; Saeidi, F.; Sadri Nahand, J.; Tabibkhooei, A.; Mirzaei, H. Genetic and epigenetic contribution to astrocytic gliomas pathogenesis. J. Neurochem., 2019, 148(2), 188-203.
[] [PMID: 30347482]
Banikazemi, Z.; Haji, H.A.; Mohammadi, M.; Taheripak, G.; Iranifar, E.; Poursadeghiyan, M.; Moridikia, A.; Rashidi, B.; Taghizadeh, M.; Mirzaei, H. Diet and cancer prevention: Dietary compounds, dietary MicroRNAs, and dietary exosomes. J. Cell. Biochem., 2018, 119(1), 185-196.
[] [PMID: 28657651]
Golabchi, K.; Soleimani-Jelodar, R.; Aghadoost, N.; Momeni, F.; Moridikia, A.; Nahand, J.S.; Masoudifar, A.; Razmjoo, H.; Mirzaei, H. MicroRNAs in retinoblastoma: Potential diagnostic and therapeutic biomarkers. J. Cell. Physiol., 2018, 233(4), 3016-3023.
[] [PMID: 28657205]
Simonian, M.; Mosallayi, M.; Mirzaei, H. Circulating miR-21 as novel biomarker in gastric cancer: Diagnostic and prognostic biomarker. J. Cancer Res. Ther., 2018, 14(2), 475.
[] [PMID: 29516946]
Keshavarzi, M.; Sorayayi, S.; Jafar Rezaei, M.; Mohammadi, M.; Ghaderi, A.; Rostamzadeh, A.; Masoudifar, A.; Mirzaei, H. MicroRNAs-based imaging techniques in cancer diagnosis and therapy. J. Cell. Biochem., 2017, 118(12), 4121-4128.
[] [PMID: 28370207]
Gholamin, S.; Mirzaei, H. GD2-targeted immunotherapy and potential value of circulating microRNAs in neuroblastoma. J. Cell. Physiol., 2018, 233(2), 866-879.
[] [PMID: 28145567]
Jamali, L.; Tofigh, R.; Tutunchi, S.; Panahi, G.; Borhani, F.; Akhavan, S.; Nourmohammadi, P.; Ghaderian, S.M.H.; Rasouli, M.; Mirzaei, H. Circulating microRNAs as diagnostic and therapeutic biomarkers in gastric and esophageal cancers. J. Cell. Physiol., 2018, 233(11), 8538-8538.
[] [PMID: 29923196]
Keshavarzi, M.; Darijani, M. Molecular imaging and oral cancer diagnosis and therapy. J. Cell. Biochem., 2017, 118(10), 3055-3060.
[] [PMID: 28390191]
Nahand, J.S.; Taghizadeh-Boroujeni, S.; Karimzadeh, M.; Borran, S.; Pourhanifeh, M.H.; Moghoofei, M.; Bokharaei-Salim, F.; Karampoor, S.; Jafari, A.; Asemi, Z.; Tbibzadeh, A.; Namdar, A.; Mirzaei, H. microRNAs: New prognostic, diagnostic, and therapeutic bi-omarkers in cervical cancer. J. Cell. Physiol., 2019, 234(10), 17064-17099.
[] [PMID: 30891784]
Aghdam, A.M.; Amiri, A.; Salarinia, R.; Masoudifar, A.; Ghasemi, F.; Mirzaei, H. MicroRNAs as diagnostic, prognostic, and therapeutic biomarkers in prostate cancer. Crit. Rev. Eukaryot. Gene Expr., 2019, 29(2), 127-139.
[] [PMID: 31679268]
Shabaninejad, Z.; Yousefi, F.; Movahedpour, A.; Ghasemi, Y.; Dokanehiifard, S.; Rezaei, S.; Aryan, R.; Savardashtaki, A.; Mirzaei, H. Electrochemical-based biosensors for microRNA detection: Nanotechnology comes into view. Anal. Biochem., 2019, 581, 113349
[] [PMID: 31254490]
Mirzaei, H. Stroke in women: risk factors and clinical biomarkers. J. Cell. Biochem., 2017, 118(12), 4191-4202.
[] [PMID: 28498508]
Bartel, D.P. MicroRNAs: target recognition and regulatory functions. Cell, 2009, 136(2), 215-233.
[] [PMID: 19167326]
Wightman, B.; Ha, I.; Ruvkun, G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell, 1993, 75(5), 855-862.
[] [PMID: 8252622]
Moussay, E.; Wang, K.; Cho, J-H.; van Moer, K.; Pierson, S.; Paggetti, J.; Nazarov, P.V.; Palissot, V.; Hood, L.E.; Berchem, G.; Galas, D.J. MicroRNA as biomarkers and regulators in B-cell chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. USA, 2011, 108(16), 6573-6578.
[] [PMID: 21460253]
Saeedi Borujeni, M.J.; Esfandiary, E.; Taheripak, G.; Codoner-Franch, P.; Alonso-Iglesias, E.; Mirzaei, H. Molecular aspects of diabetes mellitus: Resistin, microRNA, and exosome. J. Cell. Biochem., 2018, 119(2), 1257-1272.
[] [PMID: 28688216]
Tavakolizadeh, J.; Roshanaei, K.; Salmaninejad, A.; Yari, R.; Nahand, J.S.; Sarkarizi, H.K.; Mousavi, S.M.; Salarinia, R.; Rahmati, M.; Mousavi, S.F.; Mokhtari, R.; Mirzaei, H. MicroRNAs and exosomes in depression: Potential diagnostic biomarkers. J. Cell. Biochem., 2018, 119(5), 3783-3797.
[] [PMID: 29236313]
Ferracin, M.; Zagatti, B.; Rizzotto, L.; Cavazzini, F.; Veronese, A.; Ciccone, M.; Saccenti, E.; Lupini, L.; Grilli, A.; De Angeli, C.; Negrini, M.; Cuneo, A. MicroRNAs involvement in fludarabine refractory chronic lymphocytic leukemia. Mol. Cancer, 2010, 9(1), 123.
[] [PMID: 20504344]
Cui, B.; Chen, L.; Zhang, S.; Mraz, M.; Fecteau, J-F.; Yu, J.; Ghia, E.M.; Zhang, L.; Bao, L.; Rassenti, L.Z.; Messer, K.; Calin, G.A.; Croce, C.M.; Kipps, T.J. MicroRNA-155 influences B-cell receptor signaling and associates with aggressive disease in chronic lymphocytic leukemia. Blood, 2014, 124(4), 546-554.
[] [PMID: 24914134]
Calin, G.A.; Ferracin, M.; Cimmino, A.; Di Leva, G.; Shimizu, M.; Wojcik, S.E.; Iorio, M.V.; Visone, R.; Sever, N.I.; Fabbri, M.; Iuliano, R.; Palumbo, T.; Pichiorri, F.; Roldo, C.; Garzon, R.; Sevignani, C.; Rassenti, L.; Alder, H.; Volinia, S.; Liu, C.G.; Kipps, T.J.; Negrini, M.; Croce, C.M. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N. Engl. J. Med., 2005, 353(17), 1793-1801.
[] [PMID: 16251535]
Vigorito, E.; Perks, K.L.; Abreu-Goodger, C.; Bunting, S.; Xiang, Z.; Kohlhaas, S.; Das, P.P.; Miska, E.A.; Rodriguez, A.; Bradley, A.; Smith, K.G.; Rada, C.; Enright, A.J.; Toellner, K.M.; Maclennan, I.C.; Turner, M. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity, 2007, 27(6), 847-859.
[] [PMID: 18055230]
Orchard, J.A.; Ibbotson, R.E.; Davis, Z.; Wiestner, A.; Rosenwald, A.; Thomas, P.W.; Hamblin, T.J.; Staudt, L.M.; Oscier, D.G. ZAP-70 expression and prognosis in chronic lymphocytic leukaemia. Lancet, 2004, 363(9403), 105-111.
[] [PMID: 14726163]
Hallek, M.; Cheson, B.D.; Catovsky, D.; Caligaris-Cappio, F.; Dighiero, G.; Döhner, H.; Hillmen, P.; Keating, M.J.; Montserrat, E.; Rai, K.R.; Kipps, T.J. International Workshop on Chronic Lymphocytic Leukemia. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute-Working Group 1996 guidelines. Blood, 2008, 111(12), 5446-5456.
[] [PMID: 18216293]
Allegra, D.; Bilan, V.; Garding, A.; Döhner, H.; Stilgenbauer, S.; Kuchenbauer, F.; Mertens, D.; Zucknick, M. Defective DROSHA processing contributes to downregulation of MiR-15/-16 in chronic lymphocytic leukemia. Leukemia, 2014, 28(1), 98-107.
[] [PMID: 23974981]
Asslaber, D.; Piñón, J.D.; Seyfried, I.; Desch, P.; Stöcher, M.; Tinhofer, I.; Egle, A.; Merkel, O.; Greil, R. microRNA-34a expression correlates with MDM2 SNP309 polymorphism and treatment-free survival in chronic lymphocytic leukemia. Blood, 2010, 115(21), 4191-4197.
[] [PMID: 20089965]
Mertens, D.; Wolf, S.; Tschuch, C.; Mund, C.; Kienle, D.; Ohl, S.; Schroeter, P.; Lyko, F.; Döhner, H.; Stilgenbauer, S.; Lichter, P. Allelic silencing at the tumor-suppressor locus 13q14.3 suggests an epigenetic tumor-suppressor mechanism. Proc. Natl. Acad. Sci. USA, 2006, 103(20), 7741-7746.
[] [PMID: 16684883]
Rossi, S.; Shimizu, M.; Barbarotto, E.; Nicoloso, M.S.; Dimitri, F.; Sampath, D.; Fabbri, M.; Lerner, S.; Barron, L.L.; Rassenti, L.Z.; Jiang, L.; Xiao, L.; Hu, J.; Secchiero, P.; Zauli, G.; Volinia, S.; Negrini, M.; Wierda, W.; Kipps, T.J.; Plunkett, W.; Coombes, K.R.; Abruzzo, L.V.; Keating, M.J.; Calin, G.A. microRNA fingerprinting of CLL patients with chromosome 17p deletion identify a miR-21 score that stratifies early survival. Blood, 2010, 116(6), 945-952.
[] [PMID: 20393129]
Veronese, A.; Pepe, F.; Chiacchia, J.; Pagotto, S.; Lanuti, P.; Veschi, S.; Di Marco, M.; D’Argenio, A.; Innocenti, I.; Vannata, B.; Autore, F.; Marchisio, M.; Wernicke, D.; Verginelli, F.; Leone, G.; Rassenti, L.Z.; Kipps, T.J.; Mariani-Costantini, R.; Laurenti, L.; Croce, C.M.; Visone, R. Allele-specific loss and transcription of the miR-15a/16-1 cluster in chronic lymphocytic leukemia. Leukemia, 2015, 29(1), 86-95.
[] [PMID: 24732594]
Calin, G.A.; Dumitru, C.D.; Shimizu, M.; Bichi, R.; Zupo, S.; Noch, E.; Aldler, H.; Rattan, S.; Keating, M.; Rai, K.; Rassenti, L.; Kipps, T.; Negrini, M.; Bullrich, F.; Croce, C.M. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. USA, 2002, 99(24), 15524-15529.
[] [PMID: 12434020]
Esquela-Kerscher, A.; Slack, F.J. Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer, 2006, 6(4), 259-269.
[] [PMID: 16557279]
Migliazza, A.; Bosch, F.; Komatsu, H.; Cayanis, E.; Martinotti, S.; Toniato, E.; Guccione, E.; Qu, X.; Chien, M.; Murty, V.V.; Gaidano, G.; Inghirami, G.; Zhang, P.; Fischer, S.; Kalachikov, S.M.; Russo, J.; Edelman, I.; Efstratiadis, A.; Dalla-Favera, R. Nucleotide sequence, transcription map, and mutation analysis of the 13q14 chromosomal region deleted in B-cell chronic lymphocytic leukemia. Blood, 2001, 97(7), 2098-2104.
[] [PMID: 11264177]
Bullrich, F.; Fujii, H.; Calin, G.; Mabuchi, H.; Negrini, M.; Pekarsky, Y.; Rassenti, L.; Alder, H.; Reed, J.C.; Keating, M.J.; Kipps, T.J.; Croce, C.M. Characterization of the 13q14 tumor suppressor locus in CLL: identification of ALT1, an alternative splice variant of the LEU2 gene. Cancer Res., 2001, 61(18), 6640-6648.
[PMID: 11559527]
Kwok, M.; Rawstron, A.; Agathanggelou, A.; Goel, A.; Oldreive, C.; Jones, R.E.; Drennan, S.; Sharma-Oates, A.; Evans, P.; Smith, E. EBCR unresponsiveness and 13q14 duplication underpin spontaneous disease regression in chronic lymphocytic leukemia. Am. Soc. Hematology, 2017.
Cimmino, A.; Calin, G.A.; Fabbri, M.; Iorio, M.V.; Ferracin, M.; Shimizu, M.; Wojcik, S.E.; Aqeilan, R.I.; Zupo, S.; Dono, M.; Rassenti, L.; Alder, H.; Volinia, S.; Liu, C.G.; Kipps, T.J.; Negrini, M.; Croce, C.M. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc. Natl. Acad. Sci. USA, 2005, 102(39), 13944-13949.
[] [PMID: 16166262]
Cory, S.; Adams, J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer, 2002, 2(9), 647-656.
[] [PMID: 12209154]
Liu, Q.; Fu, H.; Sun, F.; Zhang, H.; Tie, Y.; Zhu, J.; Xing, R.; Sun, Z.; Zheng, X. miR-16 family induces cell cycle arrest by regulating multiple cell cycle genes. Nucleic Acids Res., 2008, 36(16), 5391-5404.
[] [PMID: 18701644]
Calin, G.A.; Cimmino, A.; Fabbri, M.; Ferracin, M.; Wojcik, S.E.; Shimizu, M.; Taccioli, C.; Zanesi, N.; Garzon, R.; Aqeilan, R.I.; Alder, H.; Volinia, S.; Rassenti, L.; Liu, X.; Liu, C.G.; Kipps, T.J.; Negrini, M.; Croce, C.M. MiR-15a and miR-16-1 cluster functions in human leukemia. Proc. Natl. Acad. Sci. USA, 2008, 105(13), 5166-5171.
[] [PMID: 18362358]
Cutrona, G.; Matis, S.; Colombo, M.; Massucco, C.; Baio, G.; Valdora, F.; Emionite, L.; Fabris, S.; Recchia, A.G.; Gentile, M.; Neumaier, C.E.; Reverberi, D.; Massara, R.; Boccardo, S.; Basso, L.; Salvi, S.; Rosa, F.; Cilli, M.; Zupo, S.; Truini, M.; Tassone, P.; Calabrese, M.; Negrini, M.; Neri, A.; Morabito, F.; Fais, F.; Ferrarini, M. Effects of miRNA-15 and miRNA-16 expression replacement in chronic lymphocytic leukemia: implication for therapy. Leukemia, 2017, 31(9), 1894-1904.
[] [PMID: 28053325]
Palamarchuk, A.; Efanov, A.; Nazaryan, N.; Santanam, U.; Alder, H.; Rassenti, L.; Kipps, T.; Croce, C.M.; Pekarsky, Y. 13q14 deletions in CLL involve cooperating tumor suppressors. Blood, 2010, 115(19), 3916-3922.
[] [PMID: 20071661]
Fabbri, M.; Bottoni, A.; Shimizu, M.; Spizzo, R.; Nicoloso, M.S.; Rossi, S.; Barbarotto, E.; Cimmino, A.; Adair, B.; Wojcik, S.E.; Valeri, N.; Calore, F.; Sampath, D.; Fanini, F.; Vannini, I.; Musuraca, G.; Dell’Aquila, M.; Alder, H.; Davuluri, R.V.; Rassenti, L.Z.; Negrini, M.; Nakamura, T.; Amadori, D.; Kay, N.E.; Rai, K.R.; Keating, M.J.; Kipps, T.J.; Calin, G.A.; Croce, C.M. Association of a microRNA/TP53 feedback circuitry with pathogenesis and outcome of B-cell chronic lymphocytic leukemia. JAMA, 2011, 305(1), 59-67.
[] [PMID: 21205967]
Zenz, T.; Häbe, S.; Denzel, T.; Mohr, J.; Winkler, D.; Bühler, A.; Sarno, A.; Groner, S.; Mertens, D.; Busch, R.; Hallek, M.; Döhner, H.; Stilgenbauer, S. Detailed analysis of p53 pathway defects in fludarabine-refractory chronic lymphocytic leukemia (CLL): dissecting the contribution of 17p deletion, TP53 mutation, p53-p21 dysfunction, and miR34a in a prospective clinical trial. Blood, 2009, 114(13), 2589-2597.
[] [PMID: 19643983]
Dijkstra, M.K.; van Lom, K.; Tielemans, D.; Elstrodt, F.; Langerak, A.W.; van ’t Veer, M.B.; Jongen-Lavrencic, M. 17p13/TP53 deletion in B-CLL patients is associated with microRNA-34a downregulation. Leukemia, 2009, 23(3), 625-627.
[] [PMID: 18818704]
Balatti, V.; Tomasello, L.; Rassenti, L.Z.; Veneziano, D.; Nigita, G.; Wang, H-Y.; Thorson, J.A.; Kipps, T.J.; Pekarsky, Y.; Croce, C.M. miR-125a and miR-34a expression predicts Richter syndrome in chronic lymphocytic leukemia patients. Blood, 2018, 132(20), 2179-2182.
[] [PMID: 30242085]
Santanam, U.; Zanesi, N.; Efanov, A.; Costinean, S.; Palamarchuk, A.; Hagan, J.P.; Volinia, S.; Alder, H.; Rassenti, L.; Kipps, T.; Croce, C.M.; Pekarsky, Y. Chronic lymphocytic leukemia modeled in mouse by targeted miR-29 expression. Proc. Natl. Acad. Sci. USA, 2010, 107(27), 12210-12215.
[] [PMID: 20566844]
Zhu, W.; Shan, X.; Wang, T.; Shu, Y.; Liu, P. miR-181b modulates multidrug resistance by targeting BCL2 in human cancer cell lines. Int. J. Cancer, 2010, 127(11), 2520-2529.
[] [PMID: 20162574]
Pekarsky, Y.; Santanam, U.; Cimmino, A.; Palamarchuk, A.; Efanov, A.; Maximov, V.; Volinia, S.; Alder, H.; Liu, C-G.; Rassenti, L.; Calin, G.A.; Hagan, J.P.; Kipps, T.; Croce, C.M. Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res., 2006, 66(24), 11590-11593.
[] [PMID: 17178851]
Visone, R.; Veronese, A.; Rassenti, L.Z.; Balatti, V.; Pearl, D.K.; Acunzo, M.; Volinia, S.; Taccioli, C.; Kipps, T.J.; Croce, C.M. miR-181b is a biomarker of disease progression in chronic lymphocytic leukemia. Blood, 2011, 118(11), 3072-3079.
[] [PMID: 21636858]
Palamarchuk, A.; Yan, P.S.; Zanesi, N.; Wang, L.; Rodrigues, B.; Murphy, M.; Balatti, V.; Bottoni, A.; Nazaryan, N.; Alder, H.; Rassenti, L.; Kipps, T.J.; Freitas, M.; Croce, C.M.; Pekarsky, Y. Tcl1 protein functions as an inhibitor of de novo DNA methylation in B-cell chronic lymphocytic leukemia (CLL). Proc. Natl. Acad. Sci. USA, 2012, 109(7), 2555-2560.
[] [PMID: 22308499]
Mott, J.L.; Kobayashi, S.; Bronk, S.F.; Gores, G.J. mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene, 2007, 26(42), 6133-6140.
[] [PMID: 17404574]
Zhao, J-J.; Lin, J.; Lwin, T.; Yang, H.; Guo, J.; Kong, W.; Dessureault, S.; Moscinski, L.C.; Rezania, D.; Dalton, W.S.; Sotomayor, E.; Tao, J.; Cheng, J.Q. microRNA expression profile and identification of miR-29 as a prognostic marker and pathogenetic factor by targeting CDK6 in mantle cell lymphoma. Blood, 2010, 115(13), 2630-2639.
[] [PMID: 20086245]
Herling, M.; Patel, K.A.; Khalili, J.; Schlette, E.; Kobayashi, R.; Medeiros, L.J.; Jones, D. TCL1 shows a regulated expression pattern in chronic lymphocytic leukemia that correlates with molecular subtypes and proliferative state. Leukemia, 2006, 20(2), 280-285.
[] [PMID: 16341048]
Faraoni, I.; Antonetti, F.R.; Cardone, J.; Bonmassar, E. miR-155 gene: a typical multifunctional microRNA. Biochim. Biophys. Acta, 2009, 1792(6), 497-505.
[] [PMID: 19268705]
Ferrajoli, A.; Shanafelt, T.D.; Ivan, C.; Shimizu, M.; Rabe, K.G.; Nouraee, N.; Ikuo, M.; Ghosh, A.K.; Lerner, S.; Rassenti, L.Z.; Xiao, L.; Hu, J.; Reuben, J.M.; Calin, S.; You, M.J.; Manning, J.T.; Wierda, W.G.; Estrov, Z.; O’Brien, S.; Kipps, T.J.; Keating, M.J.; Kay, N.E.; Calin, G.A. 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.
[] [PMID: 23821659]
Thai, T.H.; Calado, D.P.; Casola, S.; Ansel, K.M.; Xiao, C.; Xue, Y.; Murphy, A.; Frendewey, D.; Valenzuela, D.; Kutok, J.L.; Schmidt-Supprian, M.; Rajewsky, N.; Yancopoulos, G.; Rao, A.; Rajewsky, K. Regulation of the germinal center response by microRNA-155. Science, 2007, 316(5824), 604-608.
[] [PMID: 17463289]
Guinn, D.; Ruppert, A.S.; Maddocks, K.; Jaglowski, S.; Gordon, A.; Lin, T.S.; Larson, R.; Marcucci, G.; Hertlein, E.; Woyach, J.; Johnson, A.J.; Byrd, J.C. miR-155 expression is associated with chemoimmunotherapy outcome and is modulated by Bruton’s tyrosine kinase inhibition with Ibrutinib. Leukemia, 2015, 29(5), 1210-1213.
[] [PMID: 25486872]
Lu, J.; Guo, S.; Ebert, B.L.; Zhang, H.; Peng, X.; Bosco, J.; Pretz, J.; Schlanger, R.; Wang, J.Y.; Mak, R.H.; Dombkowski, D.M.; Preffer, F.I.; Scadden, D.T.; Golub, T.R. MicroRNA-mediated control of cell fate in megakaryocyte-erythrocyte progenitors. Dev. Cell, 2008, 14(6), 843-853.
[] [PMID: 18539114]
Xiao, C.; Calado, D.P.; Galler, G.; Thai, T.H.; Patterson, H.C.; Wang, J.; Rajewsky, N.; Bender, T.P.; Rajewsky, K. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell, 2007, 131(1), 146-159.
[] [PMID: 17923094]
Mraz, M.; Chen, L.; Rassenti, L.Z.; Ghia, E.M.; Li, H.; Jepsen, K.; Smith, E.N.; Messer, K.; Frazer, K.A.; Kipps, T.J. miR-150 influences B-cell receptor signaling in chronic lymphocytic leukemia by regulating expression of GAB1 and FOXP1. Blood, 2014, 124(1), 84-95.
[] [PMID: 24787006]
Stamatopoulos, B.; Van Damme, M.; Crompot, E.; Dessars, B.; Housni, H.E.; Mineur, P.; Meuleman, N.; Bron, D.; Lagneaux, L. Opposite prognostic significance of cellular and serum circulating microRNA-150 in patients with chronic lymphocytic leukemia. Mol. Med., 2015, 21(1), 123-133.
[] [PMID: 25584781]
Li, S.; Moffett, H.F.; Lu, J.; Werner, L.; Zhang, H.; Ritz, J.; Neuberg, D.; Wucherpfennig, K.W.; Brown, J.R.; Novina, C.D. MicroRNA expression profiling identifies activated B cell status in chronic lymphocytic leukemia cells. PLoS One, 2011, 6(3), e16956
[] [PMID: 21408091]
Mraz, M.; Kipps, T.J. MicroRNAs and B cell receptor signaling in chronic lymphocytic leukemia. Leuk. Lymphoma, 2013, 54(8), 1836-1839.
[] [PMID: 23597135]
Fulci, V.; Chiaretti, S.; Goldoni, M.; Azzalin, G.; Carucci, N.; Tavolaro, S.; Castellano, L.; Magrelli, A.; Citarella, F.; Messina, M.; Maggio, R.; Peragine, N.; Santangelo, S.; Mauro, F.R.; Landgraf, P.; Tuschl, T.; Weir, D.B.; Chien, M.; Russo, J.J.; Ju, J.; Sheridan, R.; Sander, C.; Zavolan, M.; Guarini, A.; Foà, R.; Macino, G. Quantitative technologies establish a novel microRNA profile of chronic lymphocytic leukemia. Blood, 2007, 109(11), 4944-4951.
[] [PMID: 17327404]
Xiao, C.; Srinivasan, L.; Calado, D.P.; Patterson, H.C.; Zhang, B.; Wang, J.; Henderson, J.M.; Kutok, J.L.; Rajewsky, K. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat. Immunol., 2008, 9(4), 405-414.
[] [PMID: 18327259]
Fedeli, M.; Riba, M.; Garcia Manteiga, J.M.; Tian, L.; Viganò, V.; Rossetti, G.; Pagani, M.; Xiao, C.; Liston, A.; Stupka, E.; Cittaro, D.; Abrignani, S.; Provero, P.; Dellabona, P.; Casorati, G. miR-17∼92 family clusters control iNKT cell ontogenesis via modulation of TGF-β signaling. Proc. Natl. Acad. Sci. USA, 2016, 113(51), E8286-E8295.
[] [PMID: 27930306]
Ivanovska, I.; Ball, A.S.; Diaz, R.L.; Magnus, J.F.; Kibukawa, M.; Schelter, J.M.; Kobayashi, S.V.; Lim, L.; Burchard, J.; Jackson, A.L.; Linsley, P.S.; Cleary, M.A. MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol. Cell. Biol., 2008, 28(7), 2167-2174.
[] [PMID: 18212054]
O’Donnell, K.A.; Wentzel, E.A.; Zeller, K.I.; Dang, C.V.; Mendell, J.T. c-Myc-regulated microRNAs modulate E2F1 expression. Nature, 2005, 435(7043), 839-843.
[] [PMID: 15944709]
Ventura, A.; Young, A.G.; Winslow, M.M.; Lintault, L.; Meissner, A.; Erkeland, S.J.; Newman, J.; Bronson, R.T.; Crowley, D.; Stone, J.R.; Jaenisch, R.; Sharp, P.A.; Jacks, T. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell, 2008, 132(5), 875-886.
[] [PMID: 18329372]
Koralov, S.B.; Muljo, S.A.; Galler, G.R.; Krek, A.; Chakraborty, T.; Kanellopoulou, C.; Jensen, K.; Cobb, B.S.; Merkenschlager, M.; Rajewsky, N.; Rajewsky, K. Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell, 2008, 132(5), 860-874.
[] [PMID: 18329371]
Wong, P.; Iwasaki, M.; Somervaille, T.C.; Ficara, F.; Carico, C.; Arnold, C.; Chen, C-Z.; Cleary, M.L. The miR-17-92 microRNA polycistron regulates MLL leukemia stem cell potential by modulating p21 expression. Cancer Res., 2010, 70(9), 3833-3842.
[] [PMID: 20406979]
Bloomston, M.; Frankel, W.L.; Petrocca, F.; Volinia, S.; Alder, H.; Hagan, J.P.; Liu, C-G.; Bhatt, D.; Taccioli, C.; Croce, C.M. MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA, 2007, 297(17), 1901-1908.
[] [PMID: 17473300]
Garzon, R.; Volinia, S.; Liu, C-G.; Fernandez-Cymering, C.; Palumbo, T.; Pichiorri, F.; Fabbri, M.; Coombes, K.; Alder, H.; Nakamura, T.; Flomenberg, N.; Marcucci, G.; Calin, G.A.; Kornblau, S.M.; Kantarjian, H.; Bloomfield, C.D.; Andreeff, M.; Croce, C.M. MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia. Blood, 2008, 111(6), 3183-3189.
[] [PMID: 18187662]
Schetter, A.J.; Leung, S.Y.; Sohn, J.J.; Zanetti, K.A.; Bowman, E.D.; Yanaihara, N.; Yuen, S.T.; Chan, T.L.; Kwong, D.L.; Au, G.K.; Liu, C.G.; Calin, G.A.; Croce, C.M.; Harris, C.C. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA, 2008, 299(4), 425-436.
[] [PMID: 18230780]
Felli, N.; Fontana, L.; Pelosi, E.; Botta, R.; Bonci, D.; Facchiano, F.; Liuzzi, F.; Lulli, V.; Morsilli, O.; Santoro, S.; Valtieri, M.; Calin, G.A.; Liu, C.G.; Sorrentino, A.; Croce, C.M.; Peschle, C. MicroRNAs 221 and 222 inhibit normal erythropoiesis and erythroleukemic cell growth via kit receptor down-modulation. Proc. Natl. Acad. Sci. USA, 2005, 102(50), 18081-18086.
[] [PMID: 16330772]
Calin, G.A.; Liu, C-G.; Sevignani, C.; Ferracin, M.; Felli, N.; Dumitru, C.D.; Shimizu, M.; Cimmino, A.; Zupo, S.; Dono, M.; Dell’Aquila, M.L.; Alder, H.; Rassenti, L.; Kipps, T.J.; Bullrich, F.; Negrini, M.; Croce, C.M. MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. Proc. Natl. Acad. Sci. USA, 2004, 101(32), 11755-11760.
[] [PMID: 15284443]
Iorio, M.V.; Ferracin, M.; Liu, C-G.; Veronese, A.; Spizzo, R.; Sabbioni, S.; Magri, E.; Pedriali, M.; Fabbri, M.; Campiglio, M.; Ménard, S.; Palazzo, J.P.; Rosenberg, A.; Musiani, P.; Volinia, S.; Nenci, I.; Calin, G.A.; Querzoli, P.; Negrini, M.; Croce, C.M. MicroRNA gene expression deregulation in human breast cancer. Cancer Res., 2005, 65(16), 7065-7070.
[] [PMID: 16103053]
Frenquelli, M.; Muzio, M.; Scielzo, C.; Fazi, C.; Scarfò, L.; Rossi, C.; Ferrari, G.; Ghia, P.; Caligaris-Cappio, F. MicroRNA and proliferation control in chronic lymphocytic leukemia: functional relationship between miR-221/222 cluster and p27. Blood, 2010, 115(19), 3949-3959.
[] [PMID: 20203269]
Monteleone, N.J.; Lutz, C.S. miR-708-5p: a microRNA with emerging roles in cancer. Oncotarget, 2017, 8(41), 71292-71316.
[] [PMID: 29050362]
Dürig, J.; Naschar, M.; Schmücker, U.; Renzing-Köhler, K.; Hölter, T.; Hüttmann, A.; Dührsen, U. CD38 expression is an important prognostic marker in chronic lymphocytic leukaemia. Leukemia, 2002, 16(1), 30-35.
[] [PMID: 11840260]
Baer, C.; Oakes, C.C.; Ruppert, A.S.; Claus, R.; Kim-Wanner, S.Z.; Mertens, D.; Zenz, T.; Stilgenbauer, S.; Byrd, J.C.; Plass, C. Epigenetic silencing of miR-708 enhances NF-κB signaling in chronic lymphocytic leukemia. Int. J. Cancer, 2015, 137(6), 1352-1361.
[] [PMID: 25704289]
Baer, C.; Claus, R.; Frenzel, L.P.; Zucknick, M.; Park, Y.J.; Gu, L.; Weichenhan, D.; Fischer, M.; Pallasch, C.P.; Herpel, E.; Rehli, M.; Byrd, J.C.; Wendtner, C.M.; Plass, C. Extensive promoter DNA hypermethylation and hypomethylation is associated with aberrant microRNA expression in chronic lymphocytic leukemia. Cancer Res., 2012, 72(15), 3775-3785.
[] [PMID: 22710432]
Rossi, D.; Rasi, S.; Fabbri, G.; Spina, V.; Fangazio, M.; Forconi, F.; Marasca, R.; Laurenti, L.; Bruscaggin, A.; Cerri, M.; Monti, S.; Cresta, S.; Famà, R.; De Paoli, L.; Bulian, P.; Gattei, V.; Guarini, A.; Deaglio, S.; Capello, D.; Rabadan, R.; Pasqualucci, L.; Dalla-Favera, R.; Foà, R.; Gaidano, G. Mutations of NOTCH1 are an independent predictor of survival in chronic lymphocytic leukemia. Blood, 2012, 119(2), 521-529.
[] [PMID: 22077063]
Peter, M.E.; Hadji, A.; Murmann, A.E.; Brockway, S.; Putzbach, W.; Pattanayak, A.; Ceppi, P. The role of CD95 and CD95 ligand in cancer. Cell Death Differ., 2015, 22(4), 549-559.
[] [PMID: 25656654]
Berg, V.; Rusch, M.; Vartak, N.; Jüngst, C.; Schauss, A.; Waldmann, H.; Hedberg, C.; Pallasch, C.P.; Bastiaens, P.I.; Hallek, M.; Wendtner, C.M.; Frenzel, L.P. miRs-138 and -424 control palmitoylation-dependent CD95-mediated cell death by targeting acyl protein thioesterases 1 and 2 in CLL. Blood, 2015, 125(19), 2948-2957.
[] [PMID: 25670628]
Mraz, M.; Dolezalova, D.; Plevova, K.; Stano Kozubik, K.; Mayerova, V.; Cerna, K.; Musilova, K.; Tichy, B.; Pavlova, S.; Borsky, M.; Verner, J.; Doubek, M.; Brychtova, Y.; Trbusek, M.; Hampl, A.; Mayer, J.; Pospisilova, S. MicroRNA-650 expression is influenced by immunoglobulin gene rearrangement and affects the biology of chronic lymphocytic leukemia. Blood, 2012, 119(9), 2110-2113.
[] [PMID: 22234685]
Yang, Y-Q.; Tian, T.; Zhu, H-Y.; Liang, J-H.; Wu, W.; Wu, J-Z.; Xia, Y.; Wang, L.; Fan, L.; Li, J-Y.; Xu, W. NDRG2 mRNA levels and miR-28-5p and miR-650 activity in chronic lymphocytic leukemia. BMC Cancer, 2018, 18(1), 1009.
[] [PMID: 30348117]
Akao, Y.; Nakagawa, Y.; Kitade, Y.; Kinoshita, T.; Naoe, T. Downregulation of microRNAs-143 and -145 in B-cell malignancies. Cancer Sci., 2007, 98(12), 1914-1920.
[] [PMID: 17892514]
Wang, J.; Yin, D.; Xie, C.; Zheng, T.; Liang, Y.; Hong, X.; Lu, Z.; Song, X.; Song, R.; Yang, H.; Sun, B.; Bhatta, N.; Meng, X.; Pan, S.; Jiang, H.; Liu, L. The iron chelator Dp44mT inhibits hepatocellular carcinoma metastasis via N-Myc downstream-regulated gene 2 (NDRG2)/gp130/STAT3 pathway. Oncotarget, 2014, 5(18), 8478-8491.
[] [PMID: 25261367]
Ichikawa, T.; Nakahata, S.; Fujii, M.; Iha, H.; Morishita, K. Loss of NDRG2 enhanced activation of the NF-κB pathway by PTEN and NIK phosphorylation for ATL and other cancer development. Sci. Rep., 2015, 5, 12841.
[] [PMID: 26269411]
Calin, G.A.; Croce, C.M. Chronic lymphocytic leukemia: interplay between noncoding RNAs and protein-coding genes. Blood, 2009, 114(23), 4761-4770.
[] [PMID: 19745066]
Sachdeva, M.; Zhu, S.; Wu, F.; Wu, H.; Walia, V.; Kumar, S.; Elble, R.; Watabe, K.; Mo, Y.Y. p53 represses c-Myc through induction of the tumor suppressor miR-145. Proc. Natl. Acad. Sci. USA, 2009, 106(9), 3207-3212.
[] [PMID: 19202062]
Wang, L.Q.; Kwong, Y.L.; Kho, C.S.B.; Wong, K.F.; Wong, K.Y.; Ferracin, M.; Calin, G.A.; Chim, C.S. Epigenetic inactivation of miR-9 family microRNAs in chronic lymphocytic leukemia--implications on constitutive activation of NFκB pathway. Mol. Cancer, 2013, 12(1), 173.
[] [PMID: 24373626]
Filip, A.A.; Grenda, A.; Popek, S.; Koczkodaj, D.; Michalak-Wojnowska, M.; Budzyński, M.; Wąsik-Szczepanek, E.; Zmorzyński, S.; Karczmarczyk, A.; Giannopoulos, K. Expression of circulating miRNAs associated with lymphocyte differentiation and activation in CLL-another piece in the puzzle. Ann. Hematol., 2017, 96(1), 33-50.
[] [PMID: 27730344]
Kawaguchi, T.; Komatsu, S.; Ichikawa, D.; Tsujiura, M.; Takeshita, H.; Hirajima, S.; Miyamae, M.; Okajima, W.; Ohashi, T.; Imamura, T.; Kiuchi, J.; Konishi, H.; Shiozaki, A.; Okamoto, K.; Otsuji, E. Circulating microRNAs: a next-generation clinical biomarker for digestive system cancers. Int. J. Mol. Sci., 2016, 17(9), 1459.
[] [PMID: 27598137]
Balatti, V.; Pekarky, Y.; Croce, C.M. Role of microRNA in chronic lymphocytic leukemia onset and progression. J. Hematol. Oncol., 2015, 8, 12.
[] [PMID: 25886051]
Patki, M.; Chari, V.; Sivakumaran, S.; Gonit, M.; Trumbly, R.; Ratnam, M. The ETS domain transcription factor ELK1 directs a critical component of growth signaling by the androgen receptor in prostate cancer cells. J. Biol. Chem., 2013, 288(16), 11047-11065.
[] [PMID: 23426362]
Yang, S-H.; Jaffray, E.; Hay, R.T.; Sharrocks, A.D. Dynamic interplay of the SUMO and ERK pathways in regulating Elk-1 transcriptional activity. Mol. Cell, 2003, 12(1), 63-74.
[] [PMID: 12887893]
Kefas, B.; Comeau, L.; Floyd, D.H.; Seleverstov, O.; Godlewski, J.; Schmittgen, T.; Jiang, J.; diPierro, C.G.; Li, Y.; Chiocca, E.A.; Lee, J.; Fine, H.; Abounader, R.; Lawler, S.; Purow, B. The neuronal microRNA miR-326 acts in a feedback loop with notch and has therapeutic potential against brain tumors. J. Neurosci., 2009, 29(48), 15161-15168.
[] [PMID: 19955368]
Rowntree, C.; Duke, V.; Panayiotidis, P.; Kotsi, P.; Palmisano, G.L.; Hoffbrand, A.V.; Foroni, L. Deletion analysis of chromosome 13q14.3 and characterisation of an alternative splice form of LEU1 in B cell chronic lymphocytic leukemia. Leukemia, 2002, 16(7), 1267-1275.
[] [PMID: 12094250]
Burr, M.L.; Sparbier, C.E.; Chan, Y-C.; Williamson, J.C.; Woods, K.; Beavis, P.A.; Lam, E.Y.N.; Henderson, M.A.; Bell, C.C.; Stolzenburg, S.; Gilan, O.; Bloor, S.; Noori, T.; Morgens, D.W.; Bassik, M.C.; Neeson, P.J.; Behren, A.; Darcy, P.K.; Dawson, S.J.; Voskoboinik, I.; Trapani, J.A.; Cebon, J.; Lehner, P.J.; Dawson, M.A. CMTM6 maintains the expression of PD-L1 and regulates anti-tumour immunity. Nature, 2017, 549(7670), 101-105.
[] [PMID: 28813417]
Li, J.; Qin, Y.; Zhang, H. Identification of key miRNA-gene pairs in chronic lymphocytic leukemia through integrated analysis of mRNA and miRNA microarray. Oncol. Lett., 2018, 15(1), 361-367.
[PMID: 29285196]
Bresin, A.; Callegari, E.; D’Abundo, L.; Cattani, C.; Bassi, C.; Zagatti, B.; Narducci, M.G.; Caprini, E.; Pekarsky, Y.; Croce, C.M.; Sabbioni, S.; Russo, G.; Negrini, M. miR-181b as a therapeutic agent for chronic lymphocytic leukemia in the Eµ-TCL1 mouse model. Oncotarget, 2015, 6(23), 19807-19818.
[] [PMID: 26090867]
Dereani, S.; Macor, P.; D’Agaro, T.; Mezzaroba, N.; Dal-Bo, M.; Capolla, S.; Zucchetto, A.; Tissino, E.; Del Poeta, G.; Zorzet, S.; Gattei, V.; Bomben, R. Potential therapeutic role of antagomiR17 for the treatment of chronic lymphocytic leukemia. J. Hematol. Oncol., 2014, 7(1), 79.
[] [PMID: 25339346]
Zenz, T.; Mohr, J.; Eldering, E.; Kater, A.P.; Bühler, A.; Kienle, D.; Winkler, D.; Dürig, J.; van Oers, M.H.; Mertens, D.; Döhner, H.; Stilgenbauer, S. miR-34a as part of the resistance network in chronic lymphocytic leukemia. Blood, 2009, 113(16), 3801-3808.
[] [PMID: 18941118]
Sandhu, S.K.; Fassan, M.; Volinia, S.; Lovat, F.; Balatti, V.; Pekarsky, Y.; Croce, C.M. B-cell malignancies in microRNA Eμ-miR-17~92 transgenic mice. Proc. Natl. Acad. Sci. USA, 2013, 110(45), 18208-18213.
[] [PMID: 24145403]

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