Discovery of new microRNAs by small RNAome deep sequencing in childhood acute lymphoblastic leukemia
Abstract
MicroRNAs (miRNAs) relevant to acute lymphoblastic leukemia (ALL) in children are hypothesized to be largely unknown as most miRNAs have been identified in non-leukemic tissues. In order to discover these miRNAs, we applied high-throughput sequencing to pooled fractions of leukemic cells obtained from 89 pediatric cases covering seven well-defined genetic types of ALL and normal hematopoietic cells. This resulted into 78 million small RNA reads representing 554 known, 28 novel and 431 candidate novel miR genes. In all, 153 known, 16 novel and 170 candidate novel mature miRNAs and miRNA-star strands were only expressed in ALL, whereas 140 known, 2 novel and 82 candidate novel mature miRNAs and miRNA-star strands were unique to normal hematopoietic cells. Stem-loop reverse transcriptase (RT)-quantitative PCR analyses confirmed the differential expression of selected mature miRNAs in ALL types and normal cells. Expression of 14 new miRNAs inversely correlated with expression of predicted target genes (-0.49 ≤ Spearman's correlation coefficients (Rs)≤ -0.27, P ≤ 0.05); among others, low levels of novel sol-miR-23 associated with high levels of its predicted (antiapoptotic) target BCL2 (B-cell lymphoma 2) in precursor B-ALL (Rs -0.36, P = 0.007). The identification of >1000 miR genes expressed in different types of ALL forms a comprehensive repository for further functional studies that address the role of miRNAs in the biology of ALL.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
miR-23 is among differentially expressed miRNAs within 89 children cases with acute lymphoblastic leukemia by high throughput sequencing, and BCL2 was its anti-apoptotic target.
“miR-23 is among the differentially expressed miRNAs within 89 children cases with acute lymphoblastic leukemia (ALL) by high throughput sequencing, and B-cell lymphoma 2 (BCL2) was its anti-apoptotic target [93].”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [93]
Cites
Bartel (2004) · doi:10.1016/s0092-8674(04)00045-5 · Cited by 34,714 · see citing works
MicroRNAs: Target Recognition and Regulatory Functions
Bartel, D. P. (2009) · Cell · doi:10.1016/j.cell.2009.01.002 · Cited by 20,068 · see citing works
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository
Edgar, R. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.207 · Cited by 13,288 · see citing works
MicroRNA expression profiles classify human cancers
Lü, J., Getz, G. A., Miska, E. A., Alvarez-Saavedra, E., Lamb, J., Peck, D., Sweet-Cordero, A., Ebert, B. L., Mak, R. H., Ferrando, A. A., et al. (2005) · Nature · doi:10.1038/nature03702 · Cited by 9,497 · see citing works
Real-time quantification of microRNAs by stem-loop RT-PCR
Chen, C. (2005) · Nucleic Acids Research · doi:10.1093/nar/gni178 · Cited by 4,931 · see citing works
Self-citationA Mammalian microRNA Expression Atlas Based on Small RNA Library Sequencing
Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., Pfeffer, S., Rice, A., Kamphorst, A. O., Landthaler, M., et al. (2007) · Cell · doi:10.1016/j.cell.2007.04.040 · Cited by 3,626 · see citing works
The impact of microRNAs on protein output
Baek, D., Villén, J., Shin, C., Camargo, F. D., Gygi, S. P., & Bartel, D. P. (2008) · Nature · doi:10.1038/nature07242 · Cited by 3,592 · see citing works
Causes and consequences of microRNA dysregulation in cancer
Croce, C. M. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2634 · Cited by 3,003 · see citing works
Many roads to maturity: microRNA biogenesis pathways and their regulation
Winter, J. J., Jung, S., Keller, S., Gregory, R. I., & Diederichs, S. (2009) · Nature Cell Biology · doi:10.1038/ncb0309-228 · Cited by 2,646 · see citing works
Xie, X., Lu, J., Kulbokas, E. J., Golub, T. R., Mootha, V., Lindblad-Toh, K., Lander, E. S., & Kellis, M. (2005) · Nature · doi:10.1038/nature03441 · Cited by 1,872 · see citing works
Identification of hundreds of conserved and nonconserved human microRNAs
Bentwich, I., Avniel, A., Karov, Y., Aharonov, R., Gilad, S., Barad, O., Barzilai, A., Einat, P., Einav, U., Meiri, E., et al. (2005) · Nature Genetics · doi:10.1038/ng1590 · Cited by 1,465 · see citing works
A Genetic Screen Implicates miRNA-372 and miRNA-373 As Oncogenes in Testicular Germ Cell Tumors
Voorhoeve, P. M., le Sage, C., Schrier, M., Gillis, A., Stoop, H., Nagel, R., Liu, Y. P., van Duijse, J., Drost, J., Griekspoor, A., et al. (2006) · Cell · doi:10.1016/j.cell.2006.02.037 · Cited by 1,263 · see citing works
Phylogenetic Shadowing and Computational Identification of Human microRNA Genes
Berezikov, E., Guryev, V., van de Belt, J., Wienholds, E., Plasterk, R. H. A., & Cuppen, E. (2005) · Cell · doi:10.1016/j.cell.2004.12.031 · Cited by 1,008 · see citing works
MicroRNAs accurately identify cancer tissue origin
Rosenfeld, N., Aharonov, R., Meiri, E., Rosenwald, S., Spector, Y., Zepeniuk, M., Benjamin, H., Shabes, N., Tabak, S., Levy, A., et al. (2008) · Nature Biotechnology · doi:10.1038/nbt1392 · Cited by 971 · see citing works
den Boer, M. L., van Slegtenhorst, M., de Menezes, R. X., Cheok, M. H.-C., Buijs-Gladdines, J. G. C. A. M., Peters, S. T. C. J. M., van Zutven, L. J. C. M., Beverloo, H. B., van der Spek, P. J., Escherich, G., et al. (2009) · The Lancet Oncology · doi:10.1016/s1470-2045(08)70339-5 · Cited by 927 · see citing works
Self-citationCummins, J. M., He, Y., Leary, R. J., Pagliarini, R. A., Diaz, L. A., Sjöblom, T., Barad, O., Bentwich, Z., Szafranska, A. E., Labourier, E., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511155103 · Cited by 927 · see citing works
MicroRNAs and Cancer: Short RNAs Go a Long Way
Ventura, A., & Jacks, T. (2009) · Cell · doi:10.1016/j.cell.2009.02.005 · Cited by 893 · see citing works
Felli, N., Fontana, L., Pelosi, E., Botta, R., Bonci, D., Facchiano, F., Liuzzi, F., Lulli, V., Morsilli, O., Santoro, S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506216102 · Cited by 760 · see citing works
Mammalian microRNAs: experimental evaluation of novel and previously annotated genes
Chiang, H. R., Schoenfeld, L. W., Ruby, J. G., Auyeung, V. C., Spies, N., Baek, D., Johnston, W. K., Russ, C., Luo, S., Babiarz, J. E., et al. (2010) · Genes & Development · doi:10.1101/gad.1884710 · Cited by 732 · see citing works
Keene, J. D., Komisarow, J. M., & Friedersdorf, M. B. (2006) · Nature Protocols · doi:10.1038/nprot.2006.47 · Cited by 612 · see citing works
Mi, S., Lü, J., Sun, M., Li, Z., Zhang, H., Neilly, M. B., Wang, Y., Qian, Z., Jin, J., Zhang, Y., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709313104 · Cited by 475 · see citing works
Approaches to microRNA discovery
Berezikov, E., Cuppen, E. P. J. G., & Plasterk, R. H. A. (2006) · Nature Genetics · doi:10.1038/ng1794 · Cited by 456 · see citing works
Diversity of microRNAs in human and chimpanzee brain
Berezikov, E., Thuemmler, F., van Laake, L. W., Kondova, I., Bontrop, R., Cuppen, E., & Plasterk, R. H. A. (2006) · Nature Genetics · doi:10.1038/ng1914 · Cited by 416 · see citing works
MicroRNA expression profiling in relation to the genetic heterogeneity of acute myeloid leukemia
Jongen‐Lavrencic, M., Sun, S. M., Dijkstra, M. K., Valk, P. J. M., & Löwenberg, B. (2008) · Blood · doi:10.1182/blood-2008-01-133355 · Cited by 401 · see citing works
Zhao, C., Sun, G., Li, S., Lang, M., Su, Y., Li, W., & Shi, Y. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908750107 · Cited by 388 · see citing works
BCL-2: Prevention of Apoptosis as a Mechanism of Drug Resistance
Reed, J. C. (1995) · Hematology/Oncology Clinics of North America · doi:10.1016/s0889-8588(18)30104-7 · Cited by 312 · see citing works
MicroRNAs as regulators of mammalian hematopoiesis
Chen, C., & Lodish, H. F. (2005) · Seminars in Immunology · doi:10.1016/j.smim.2005.01.001 · Cited by 209 · see citing works
Self-citationClinical relevance of BCL-2 overexpression in childhood acute lymphoblastic leukemia
Coustan‐Smith, E., Kitanaka, A., Pui, C., McNinch, L., We, E., Raimondi, S. C., Behm, F., Aricò, M., & Campana, D. (1996) · Blood · doi:10.1182/blood.v87.3.1140.bloodjournal8731140 · Cited by 207 · see citing works
Schotte, D., Chau, J., Sylvester, G., Liu, G. Y.-G., Chen, C., van der Velden, V. H. J., Broekhuis, M., Peters, T. C. J. M., Pieters, R., & den Boer, M. L. (2008) · Leukemia · doi:10.1038/leu.2008.286 · Cited by 198 · see citing works
Self-citationSchotte, D., Menezes, R. X. D., Moqadam, F. A., Khankahdani, L. M., Turenhout, E. A. M., Chen, C., Pieters, R., & den Boer, M. L. (2011) · Haematologica · doi:10.3324/haematol.2010.026138 · Cited by 197 · see citing works
Self-citationCharacterization of the Melanoma miRNAome by Deep Sequencing
Stark, M. S., Tyagi, S., Nancarrow, D. J., Boyle, G. M., Cook, A. L., Whiteman, D. C., Parsons, P. G., Schmidt, C., Sturm, R. A., & Hayward, N. K. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009685 · Cited by 196 · see citing works
Targeting FLT3 in primary MLL-gene-rearranged infant acute lymphoblastic leukemia
Stam, R. W. (2005) · Blood · doi:10.1182/blood-2004-09-3667 · Cited by 185 · see citing works
den Boer, M. L., Harms, D., Pieters, R., Kazemier, K. M., Göbel, U., Körholz, D., Graubner, U. B., Haas, R., Jorch, N., Spaar, H., et al. (2003) · Journal of Clinical Oncology · doi:10.1200/jco.2003.11.031 · Cited by 184 · see citing works
Self-citationLan, F., Wang, H., Chen, Y., Chan, C., Ng, S. S., Li, K., Xie, D., He, M., Lin, M. C.-M., & Kung, H. (2010) · International Journal of Cancer · doi:10.1002/ijc.25336 · Cited by 163 · see citing works
Analysis of microRNA transcriptome by deep sequencing of small RNA libraries of peripheral blood
Vaz, C., Ahmad, H. M., Sharma, P., Gupta, R., Kumar, L., Kulshreshtha, R., & Bhattacharya, A. (2010) · BMC Genomics · doi:10.1186/1471-2164-11-288 · Cited by 144 · see citing works
Identification of the Human Mature B Cell miRNome
Basso, K., Sumazin, P., Morozov, P. S., Schneider, C., Maute, R. L., Kitagawa, Y., Mandelbaum, J., Haddad, J., Chen, C., Califano, A., et al. (2009) · Immunity · doi:10.1016/j.immuni.2009.03.017 · Cited by 128 · see citing works
Self-citationA high throughput experimental approach to identify miRNA targets in human cells
Tan, L. P., Seinen, E., Duns, G., de Jong, D., Sibon, O. C. M., Poppema, S., Kroesen, B., Kok, K., & van den Berg, A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp715 · Cited by 114 · see citing works
Evolutionary flux of canonical microRNAs and mirtrons in Drosophila
Berezikov, E., Liu, N., Flynt, A. S., Hodges, E. C., Rooks, M. G., Hannon, G. J., & Lai, E. C. (2009) · Nature Genetics · doi:10.1038/ng0110-6 · Cited by 106 · see citing works
Swift: primary data analysis for the Illumina Solexa sequencing platform
Whiteford, N. E., Skelly, T., Curtis, C. N., Ritchie, M. E., Löhr, A., Zaranek, A. W., Abnizova, I., & Brown, C. G. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp383 · Cited by 105 · see citing works
Discovery of Novel MicroRNAs in Female Reproductive Tract Using Next Generation Sequencing
Creighton, C. J., Benham, A. L., Zhu, H., Khan, M. F., Reid, J. G., Nagaraja, A. K., Fountain, M. D., Dziadek, O. L., Han, D. Y., Ma, L., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009637 · Cited by 96 · see citing works
Role of miRNA in carcinogenesis and biomarker selection: a methodological view
Ahmed, F. (2007) · Expert Review of Molecular Diagnostics · doi:10.1586/14737159.7.5.569 · Cited by 94 · see citing works
Schotte, D., Turenhout, E. A. M., Stumpel, D. J. P. M., Stam, R. W., Buijs-Gladdines, J. G. C. A. M., Meijerink, J. P. P., Pieters, R., & den Boer, M. L. (2010) · Haematologica · doi:10.3324/haematol.2010.023481 · Cited by 93 · see citing works
Self-citationAge-related changes in the cellular composition of the thymus in children
Weerkamp, F., de Haas, E. F. E., Naber, B. A. E., Comans-Bitter, W. M., Bogers, A. J. J. C., van Dongen, J. J. M., & Staal, F. J. T. (2005) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2004.10.031 · Cited by 91 · see citing works
Complete characterization of the microRNAome in a patient with acute myeloid leukemia
Ramsingh, G., Koboldt, D. C., Trissal, M. C., Chiappinelli, K. B., Wylie, T., Koul, S., Chang, L., Nagarajan, R., Fehniger, T. A., Goodfellow, P. J., et al. (2010) · Blood · doi:10.1182/blood-2010-05-285395 · Cited by 68 · see citing works
Zhang, H., Yang, J., Zheng, Y., Zhang, P., Chen, X., Wu, J., Xu, L., Luo, X., Ke, Z., Zhou, H., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006849 · Cited by 49 · see citing works
Bcl-2 expression restores the leukemogenic potential of a BCR/ABL mutant defective in transformation
Cirinnà, M., Trotta, R., Salomoni, P., Kossev, P. M., Wasik, M. A., Perrotti, D., & Calabretta, B. (2000) · Blood · doi:10.1182/blood.v96.12.3915 · Cited by 33 · see citing works
Micro-RNAs and their potential target genes in leukemia pathogenesis
Dong, C., Ji, M., & Ji, C. (2009) · Cancer Biology & Therapy · doi:10.4161/cbt.8.3.7333 · Cited by 30 · see citing works
Flagged first, then by citations
1 of the 48 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
van de Bunt, M., Gaulton, K. J., Parts, L., Morán, I., Johnson, P. R. V., Lindgren, C. M., Ferrer, J. P., Gloyn, A. L., & McCarthy, M. I. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055272 · Cited by 197 · see citing works
MicroRNAs in acute leukemia: from biological players to clinical contributors
Schotte, D., Pieters, R., & den Boer, M. L. (2011) · Leukemia · doi:10.1038/leu.2011.151 · Cited by 134 · see citing works
Self-citationArısan, E. D., Dart, D. A., Grant, G. H., Arısan, S., Cuhadaroglu, S., Lange, S., & Onganer, P. U. (2020) · Viruses · doi:10.3390/v12060614 · Cited by 115 · see citing works
Different miRNA expression profiles between human breast cancer tumors and serum
Zhu, J., Zheng, Z., Wang, J., Sun, J., Wang, P., Cheng, X., Fu, L., Zhang, L., Wang, Z., & Li, Z. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00149 · Cited by 111 · see citing works
Ma, Y., Vilanova, D., Atalar, K., Delfour, O., Edgeworth, J., Ostermann, M., Hernández-Fuentes, M. P., Razafimahatratra, S., Michot, B., Persing, D. H., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075918 · Cited by 94 · see citing works
Moqadam, F. A., Turenhout, E. A. M., Ariës, I. M., Pieters, R., & den Boer, M. L. (2013) · Leukemia Research · doi:10.1016/j.leukres.2013.06.027 · Cited by 77 · see citing works
Self-citationSathipati, S. Y., & Ho, S. (2017) · Scientific Reports · doi:10.1038/s41598-017-07739-y · Cited by 74 · see citing works
Deregulation of microRNAs in myelodysplastic syndrome
Rhyasen, G. W., & Starczynowski, D. T. (2011) · Leukemia · doi:10.1038/leu.2011.221 · Cited by 70 · see citing works
Eisfeld, A., Marcucci, G., Maharry, K. S., Schwind, S., Radmacher, M. D., Nicolet, D., Becker, H., Mrózek, K., Whitman, S. P., Metzeler, K. H., et al. (2012) · Blood · doi:10.1182/blood-2012-02-408492 · Cited by 69 · see citing works
The hunting of targets: challenge in miRNA research
Moqadam, F. A., Pieters, R., & den Boer, M. L. (2012) · Leukemia · doi:10.1038/leu.2012.179 · Cited by 68 · see citing works
Self-citationAdvances in the molecular pathobiology of B-lymphoblastic leukemia
Zhou, Y., You, M. J., Young, K. H., Lin, P., Lu, G. G., Medeiros, L. J., & Bueso-Ramos, C. (2012) · Human Pathology · doi:10.1016/j.humpath.2012.02.004 · Cited by 62 · see citing works
Díaz‐Beyá, M., Brunet, S., Nomdedeu, J. F., Tejero, R., Díaz, T., Pratcorona, M., Tormo, M., Ribera, J., Escoda, L., Duarte, R. F., et al. (2013) · Leukemia · doi:10.1038/leu.2013.281 · Cited by 60 · see citing works
Noncoding RNA–related polymorphisms in pediatric acute lymphoblastic leukemia susceptibility
Gutiérrez-Camino, Á., López-López, E., Martín‐Guerrero, I., Piñán, M. A., García‐Miguel, P., Sánchez-Toledo, J., Bañeres, A. C., Úriz, J., Navajas, A., & García‐Orad, Á. (2014) · Pediatric Research · doi:10.1038/pr.2014.43 · Cited by 59 · see citing works
On the performance of pre-microRNA detection algorithms
Demirci, M. D. S., Baumbach, J., & Allmer, J. (2017) · Nature Communications · doi:10.1038/s41467-017-00403-z · Cited by 58 · see citing works
Ye, R.-S., Xi, Q., Qi, Q., Cheng, X. L., Chen, T., Li, H., Kallon, S., Shu, G., Wang, S., Jiang, Q., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057156 · Cited by 58 · see citing works
Nemes, K., Csóka, M., Nagy, N., Márk, Á., Váradi, Z., Dankó, T., Kovács, G., Kopper, L., & Sebestyén, A. R. (2014) · Pathology & Oncology Research · doi:10.1007/s12253-014-9861-z · Cited by 57 · see citing works
Talwar, S., Balasubramanian, S., Sundaramurthy, S., House, R. P., Wilusz, C. J., Kuppuswamy, D., D’Silva, N. J., Gillespie, M. B., Hill, E. G., & Palanisamy, V. (2013) · RNA Biology · doi:10.4161/rna.23315 · Cited by 56 · see citing works
microRNA analysis of gastric cancer patients from Saudi Arabian population
Bibi, F., Naseer, M. I., Alvi, S. A., Yasir, M., Jiman-Fatani, A. A., Sawan, A., Abuzenadah, A. M., Al-Qahtani, M. H., & Azhar, E. I. (2016) · BMC Genomics · doi:10.1186/s12864-016-3090-7 · Cited by 55 · see citing works
MicroRNA expression profiles discriminate childhood T‐ from B‐acute lymphoblastic leukemia
Almeida, R. S., Silva, M. C. E., Coutinho, L. L., Gomes, R. G., Pedrosa, F. D. P. R., Massaro, J. D., Donadi, E. A., & Lucena‐Silva, N. (2018) · Hematological Oncology · doi:10.1002/hon.2567 · Cited by 55 · see citing works
Classification of Widely and Rarely Expressed Genes with Recurrent Neural Network
Chen, L., Pan, X., Zhang, Y., Liu, M., Huang, T., & Cai, Y. (2018) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2018.12.002 · Cited by 51 · see citing works
Identification and Pathway Analysis of microRNAs with No Previous Involvement in Breast Cancer
Romero-Cordoba, S. L., Rodriguez-Cuevas, S. A., Rebollar‐Vega, R., Quintanar‐Jurado, V., Maffuz‐Aziz, A., Jiménez‐Sánchez, G., Bautista‐Piña, V., Arellano-Llamas, R., & Hidalgo‐Miranda, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031904 · Cited by 49 · see citing works
Extent, Causes, and Consequences of Small RNA Expression Variation in Human Adipose Tissue
Parts, L., Hedman, Å. K., Keildson, S., Knights, A. J., Abreu‐Goodger, C., van de Bunt, M., Guerra‐Assunção, J. A., Bartoniček, N., van Dongen, S., Mägi, R., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002704 · Cited by 50 · see citing works
Ciechomska, M., Bonek, K., Merdas, M., Zarecki, P., Świerkot, J., Głuszko, P., Bogunia‐Kubik, K., & Maśliński, W. (2018) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-018-0513-y · Cited by 48 · see citing works
MicroRNA expression and activity in pediatric acute lymphoblastic leukemia (ALL)
de Oliveira, J. C., Brassesco, M. S., Scrideli, C. A., Tone, L. G., & Narendran, A. (2012) · Pediatric Blood & Cancer · doi:10.1002/pbc.24167 · Cited by 45 · see citing works
Jiang, Z., Zhang, Y., Cao, R., Li, L., Zhong, K., Chen, Q., & Xiao, J. A. (2017) · Oncology Research Featuring Preclinical and Clinical Cancer Therapeutics · doi:10.3727/096504016x14831120463349 · Cited by 45 · see citing works
The importance of miRNAs and epigenetics in acute lymphoblastic leukemia prognosis
Ranjbar, R., Karimian, A., Fard, A. A., Tourani, M., Majidinia, M., Jadidi‐Niaragh, F., & Yousefi, B. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.26510 · Cited by 41 · see citing works
Tabibkhooei, A., Izadpanahi, M., Arab, A., Zare‐Mirzaie, A., Minaeian, S., Rostami, A., & Mohsenian, A. (2019) · Clinical Neurology and Neurosurgery · doi:10.1016/j.clineuro.2019.105652 · Cited by 41 · see citing works
Identification of Endogenous Control miRNAs for RT-qPCR in T-Cell Acute Lymphoblastic Leukemia
Drobna‐Śledzińska, M., Szarzyńska‐Zawadzka, B., Daca‐Roszak, P., Kosmalska, M., Jaksik, R., Witt, M., & Dawidowska, M. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19102858 · Cited by 38 · see citing works
Retracted: Overexpression of miR-708 and its targets in the childhood common precursor B-cell ALL
Li, X., Li, D., Zhuang, Y., Shi, Q., Wei, W., & Ju, X. (2013) · Pediatric Blood & Cancer · doi:10.1002/pbc.24583 · Cited by 34 · see citing works
RetractedDrobna‐Śledzińska, M., Szarzyńska‐Zawadzka, B., & Dawidowska, M. (2018) · Blood Reviews · doi:10.1016/j.blre.2018.04.003 · Cited by 33 · see citing works
Transcription Factors Are Targeted by Differentially Expressed miRNAs in Primates
Dannemann, M., Prüfer, K., Lizano, E., Nickel, B., Burbano, H. A., & Kelso, J. F. (2012) · Genome Biology and Evolution · doi:10.1093/gbe/evs033 · Cited by 30 · see citing works
Dawidowska, M., Jaksik, R., Drobna‐Śledzińska, M., Szarzyńska‐Zawadzka, B., Kosmalska, M., Sędek, Ł., Machowska, L., Lalik, A., Lejman, M., Ussowicz, M., et al. (2019) · Neoplasia · doi:10.1016/j.neo.2019.01.004 · Cited by 31 · see citing works
Szczepanek, J. (2020) · World Journal of Clinical Oncology · doi:10.5306/wjco.v11.i6.348 · Cited by 31 · see citing works
miR-361-3p regulates FSH by targeting FSHB in a porcine anterior pituitary cell model
Ye, R.-S., Li, M., Li, C.-Y., Qi, Q., Chen, T., Cheng, X. L., Wang, S., Shu, G., Wang, L., Zhu, X., et al. (2016) · Reproduction · doi:10.1530/rep-16-0373 · Cited by 31 · see citing works
MicroRNA-33a-5p suppresses growth of osteosarcoma cells and is downregulated in human osteosarcoma
Zhang, J., Wang, D., Xiong, J., Chen, L., & Huang, J. (2015) · Oncology Letters · doi:10.3892/ol.2015.3503 · Cited by 28 · see citing works
T-ALL and thymocytes: a message of noncoding RNAs
Wallaert, A., Durinck, K., Taghon, T., Vlierberghe, P. V., & Speleman, F. (2017) · Journal of Hematology & Oncology · doi:10.1186/s13045-017-0432-0 · Cited by 28 · see citing works
Kyriakidis, I., Kyriakidis, K., & Tsezou, A. (2022) · Cancers · doi:10.3390/cancers14163976 · Cited by 27 · see citing works
Dissecting the Roles of Divergent and Convergent Transcription in Chromosome Instability
Pannunzio, N. R., & Lieber, M. R. (2016) · Cell Reports · doi:10.1016/j.celrep.2015.12.098 · Cited by 27 · see citing works
Fine mapping of variants associated with endometriosis in the WNT4 region on chromosome 1p36.
Luong, H. T., Painter, J. N., Shakhbazov, K., Chapman, B. M., Henders, A. K., Powell, J. E., Nyholt, D. R., & Montgomery, G. W. (2013) · Europe PMC (PubMed Central) · Cited by 24 · see citing works
Polymorphisms in MicroRNAs Are Associated with Survival in Non–Small Cell Lung Cancer
Zhao, Y., Wei, Q., Hu, L., Chen, F., Hu, Z., Heist, R. S., Su, L., Amos, C. I., Shen, H., & Christiani, D. C. (2014) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-14-0389 · Cited by 22 · see citing works
Fang, C., Li, X., Gong, W., Wu, N., Tang, J., Yin, J., Li, X., Zhang, W., Zhou, H., & Liu, Z. (2016) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.12704 · Cited by 22 · see citing works
Role of miRNAs in Treatment Response and Toxicity of Childhood Acute Lymphoblastic Leukemia
Umerez, M., García‐Obregón, S., Martín‐Guerrero, I., Astigarraga, I., Gutiérrez-Camino, Á., & García‐Orad, Á. (2018) · Pharmacogenomics · doi:10.2217/pgs-2017-0164 · Cited by 22 · see citing works
Involvement of SNPs in miR-3117 and miR-3689d2 in childhood acute lymphoblastic leukemia risk
Gutiérrez-Camino, Á., Martín‐Guerrero, I., Dolžan, V., Jazbec, J., Bañeres, A. C., de Andoín, N. G., Sastre, A., Astigarraga, I., Navajas, A., & García‐Orad, Á. (2018) · Oncotarget · doi:10.18632/oncotarget.25144 · Cited by 22 · see citing works
miR-192 Is Overexpressed and Promotes Cell Proliferation in Prostate Cancer
Chen, Z.-J., Yan, Y., Shen, H., Zhou, J., Yang, G., Liao, Y., Zeng, J., & Yang, T. (2018) · Medical Principles and Practice · doi:10.1159/000496206 · Cited by 22 · see citing works
A genetic variant in miR‐100 is a protective factor of childhood acute lymphoblastic leukemia
Xue, Y., Yang, X., Hu, S., Kang, M., Chen, J., & Fang, Y. (2019) · Cancer Medicine · doi:10.1002/cam4.2082 · Cited by 22 · see citing works
A miRNA Host Response Signature Accurately Discriminates Acute Respiratory Infection Etiologies
Poore, G. D., Ko, E. R., Valente, A. M., Henao, R., Sumner, K. M., Hong, C., Burke, T. W., Nichols, M., McClain, M. T., Huang, E. S., et al. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02957 · Cited by 21 · see citing works
Intronic miR-3151 Within BAALC Drives Leukemogenesis by Deregulating the TP53 Pathway
Eisfeld, A., Schwind, S., Patel, R. K., Huang, X., Santhanam, R., Walker, C. J., Markowitz, J., Hoag, K. W., Järvinen, T. M., Leffel, B., et al. (2014) · Science Signaling · doi:10.1126/scisignal.2004762 · Cited by 20 · see citing works
Díaz‐Beyá, M., Brunet, S., Nomdedeu, J. F., Cordeiro, A., Tormo, M., Escoda, L., Ribera, J., Arnán, M., Heras, I. D. L., Gallardo, D., et al. (2015) · Blood Cancer Journal · doi:10.1038/bcj.2015.76 · Cited by 20 · see citing works
Ali, H. S., Kamel, M. M., Agwa, S. H. A., Abdel-Hakeem, M. S., El‐Meteini, M., & Matboli, M. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1131171 · Cited by 19 · see citing works
Clinical application of microRNA in gastric cancer in Eastern Asian area
Gao, M. (2013) · World Journal of Gastroenterology · doi:10.3748/wjg.v19.i13.2019 · Cited by 19 · see citing works
miRNA Deregulation in Childhood Acute Lymphoblastic Leukemia: A Systematic Review
Gutiérrez-Camino, Á., García‐Obregón, S., López-López, E., Astigarraga, I., & García‐Orad, Á. (2019) · Epigenomics · doi:10.2217/epi-2019-0154 · Cited by 18 · see citing works
Zhang, J., Liu, Y., Zhang, X., Pan, J., Nie, Z., Zhang, W., Yu, W., Chen, J., Liu, L., Li, J., et al. (2013) · Gene · doi:10.1016/j.gene.2013.06.012 · Cited by 18 · see citing works
Qin, L., Deng, H.-Y., Chen, S., Wei, W., & Zhang, Y. (2017) · Europe PMC (PubMed Central) · Cited by 17 · see citing works
Moez, M. J., Bjeije, H., & Soltani, B. M. (2019) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2019.01.001 · Cited by 17 · see citing works
Mahmood, S., Bhatti, A., Syed, N. A., & John, P. C. L. (2015) · Journal of Receptors and Signal Transduction · doi:10.3109/10799893.2015.1080273 · Cited by 15 · see citing works
RNA Polymerase Collision versus DNA Structural Distortion: Twists and Turns Can Cause Break Failure
Pannunzio, N. R., & Lieber, M. R. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.03.034 · Cited by 12 · see citing works
Lu, C., Zhang, J., Nie, Z., Chen, J., Zhang, W., Ren, X., Yu, W., Liu, L., Jiang, C., Zhang, Y., et al. (2013) · BioMed Research International · doi:10.1155/2013/795676 · Cited by 12 · see citing works
Sun, X., Guan, G., Dai, Y., Zhao, P., Liu, L., Wang, Q., & Li, X. (2021) · Laboratory Investigation · doi:10.1038/s41374-021-00638-x · Cited by 10 · see citing works
Yu, S., Li, L., Fan, K., Li, Y., & Gao, Y. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.696713 · Cited by 9 · see citing works
The identification of microRNAs in Ganoderma lingzhi sporocarp
Li, B., Cheng, X., Zhang, T., Liu, L., Nie, Z., & Sheng, Q. (2016) · Mycoscience · doi:10.1016/j.myc.2016.03.004 · Cited by 8 · see citing works
Human Lymphoid Translocation Fragile Zones Are Hypomethylated and Have Accessible Chromatin
Lu, Z., Lieber, M. R., Tsai, A. G., Pardo, C. E., Müschen, M., Kladde, M. P., & Hsieh, C. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.01085-14 · Cited by 8 · see citing works
Novel MicroRNAs regulating proliferation and apoptosis in uterine papillary serous carcinomas
Mach, C. M., Kim, J. K., Soibam, B., Creighton, C. J., Hawkins, S. M., Zighelboim, I., Goodfellow, P. J., Gunaratne, P. H., Odunsi, K. O., Salem, P. A., et al. (2013) · Cancer Letters · doi:10.1016/j.canlet.2013.02.043 · Cited by 7 · see citing works
Xu, L.-Y., & Cao, L. (2013) · Tumor Biology · doi:10.1007/s13277-013-1197-x · Cited by 6 · see citing works
Li, M., Ren, C., Wu, C., Li, X., Li, X., & Mao, W. (2020) · Cardiology Research and Practice · doi:10.1155/2020/3162581 · Cited by 6 · see citing works
Recent advances of miR-23 in human diseases and growth development
Qian, X., Jiang, Y., Yang, Y., Zhang, Y., Xu, N., Xu, B., Pei, K., Yu, Z., & Wu, W. (2025) · Non-coding RNA Research · doi:10.1016/j.ncrna.2024.12.010 · Cited by 5 · see citing works
Zheng, L., Deng, K.-W., Deng, A.-C., Wu, J., Yang, J., Lun, Z., & Qu, L. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00126 · Cited by 6 · see citing works
Role of rs10406069 in miR-5196 in Hyperdiploid Childhood Acute Lymphoblastic Leukemia
Gutiérrez-Camino, Á., Richer, C., St-Onge, P., López-López, E., Bañeres, A. C., de Andoín, N. G., Sastre, A., Astigarraga, I., Martín‐Guerrero, I., Sinnett, D., et al. (2020) · Epigenomics · doi:10.2217/epi-2020-0152 · Cited by 5 · see citing works
Fakhrezare, F., Ebrahimi, S. O., & Reiisi, S. (2022) · Molecular Biology Reports · doi:10.1007/s11033-022-08027-3 · Cited by 5 · see citing works
Next generation sequencing identifies novel diagnostic biomarkers for head and neck cancers
Fadhil, R., NAIR, R. G., Nikolarakos, D., & Wei, M. Q. (2019) · Oral Cancer · doi:10.1007/s41548-019-00019-5 · Cited by 5 · see citing works
Small gene, big number, many effects
Călin, G. A., & Konopleva, M. Y. (2012) · Blood · doi:10.1182/blood-2012-05-427393 · Cited by 5 · see citing works
Almeida, R. S., Gomes, T. T., Araújo, F. S., de Oliveira, S. A. V., dos Santos, J. F., Donadi, E. A., & Lucena‐Silva, N. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.871972 · Cited by 4 · see citing works
Taniguchi‐Ponciano, K., Huerta-Padilla, V., Baeza-Xochihua, V., Ponce-Navarrete, G., Salcedo, E., Apo, E. G., Chávez-Macías, L., Avilés-Durán, J. C., Ruiz-Sanchez, H., Valdivia, A., et al. (2019) · Archives of Medical Research · doi:10.1016/j.arcmed.2019.11.005 · Cited by 4 · see citing works
Unveiling novel regulatory mechanisms of miR-5195-3p in pelvic organ prolapse pathogenesis
Zhang, H., Wang, X., Dong, M., Wang, J., & Ren, W. (2024) · Biology of Reproduction · doi:10.1093/biolre/ioae162 · Cited by 3 · see citing works
Örsten, S., Baysal, İ., Akdoğan, N., İnal, N., Bostan, E., Ciftci, S. Y., & Akyön, Y. (2022) · Experimental Parasitology · doi:10.1016/j.exppara.2022.108453 · Cited by 3 · see citing works
Micro RNA s implicated in canine diffuse large B‐cell lymphoma prognosis
Elshafie, N. O., Gribskov, M., Lichti, N. I., Sayedahmed, E. E., Childress, M. O., & dos Santos, A. P. (2024) · FEBS Open Bio · doi:10.1002/2211-5463.13887 · Cited by 2 · see citing works
AutoML identification of microRNA biomarkers in high-risk pediatric acute lymphoblastic leukemia
Kyriakidis, I., Papadovasilakis, Z., Παπουτσόγλου, Γ., Pelagiadis, I., Papadaki, H. Α., Pontikoglou, C. G., & Stiakaki, E. (2025) · Non-coding RNA Research · doi:10.1016/j.ncrna.2025.08.003 · Cited by 2 · see citing works
Ma, D.-Q. (2019) · Technology in Cancer Research & Treatment · doi:10.1177/1533033819867361 · Cited by 2 · see citing works
Sampath, D. (2012) · Springer eBooks · doi:10.1007/978-94-007-4655-8_7 · Cited by 2 · see citing works
Formation of a G-quadruplex structure from human mature miR-5196-5p
Tan, W., Zhang, L., Zhou, J., Chen, H., & Yuan, G. (2017) · Spectroscopy Letters · doi:10.1080/00387010.2017.1367309 · Cited by 2 · see citing works
Genetic Studies in Acute Lymphoblastic Leukemia, from Diagnosis to Optimal Patient’s Treatment
Krawczyk-Kuli, M. (2012) · InTech eBooks · doi:10.5772/35593 · Cited by 1 · see citing works
Modulation of Cancer Progression by Tumor Microenvironmental Leukocyte-Expressed microRNAs
Sempere, L. F., & Conejo-Garci, J. (2012) · InTech eBooks · doi:10.5772/32026
Next-Generation Sequencing in Cancer Epigenomics and Potential Clinical Applications
Ng, H. K., Roukos, D. H., Iacopetta, B. J., & Ku, C. (2013) · Springer eBooks · doi:10.1007/978-1-4614-7645-0_2 · Cited by 1 · see citing works
MicroRNA as Biomarkers in Cancer Diagnostics and Therapy
Sempere, L. F. (2019) · MDPI eBooks · doi:10.3390/books978-3-03921-250-7 · Cited by 1 · see citing works
MicroRNAs in Pediatric Acute Lymphoblastic Leukemia: Small players with huge potential
Schotte, D. (2011) · RePub (Erasmus University Rotterdam)
Self-citationAdvances in Next Generation Sequencing Technologies and Cancer Epigenomics
Ng, H. K., Ku, C., Wu, M., Iacopetta, B. J., & Soong, R. C. T. (2012) · Encyclopedia of Life Sciences · doi:10.1002/9780470015902.a0023507
microRNA expression and function in virus-associated human cancers
Xie, H. Y. (2013) · Figshare
Hücre Serilerinde Kilitli Nükleik Asitler İle MIR223 Gen Sessizleştirmesi
Taşar, O., Sayitoğlu, M., & Ng, Ö. H. (2020) · Sağlık Bilimlerinde İleri Araştırmalar Dergisi / Journal of Advanced Research in Health Sciences · doi:10.26650/jarhs2020-739221
Kheyrandish, S., Pilehvari, N., Rastgar, A., bakhshian-Farsani, M., Chahardouli, B., Nazari, Z., Rostami, S., Mohammadi, S., & Gharehbaghian, A. (2025) · Molecular Biology Reports · doi:10.1007/s11033-025-11244-1
Gim, J., Kwak, K., Park, Y., Kim, B. S., & Kang, K. (2026) · PLoS ONE · doi:10.1371/journal.pone.0352501
- Authors
- Schotte, D., Moqadam, F. A., Lange-Turenhout, E. A. M., Chen, C., van IJcken, W. F. J., Pieters, R., & den Boer, M. L.
- Affiliations
- Erasmus MC (NL)
- ORCID
- Venue
- Leukemia
- Published
- 2011-05-24
- Volume
- 25
- Issue
- 9
- Pages
- 1389-1399
- ISSN
- 0887-6924 (ISSN-L)
- 1476-5551
- OpenAlex
- W2057346914
- Cited by
- 89
- References
- 48
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 3 · 2023: 1 · 2022: 4 · 2021: 2 · 2020: 5 · 2019: 9 · 2018: 10 · 2017: 7 · 2016: 6 · 2015: 4 · 2014: 5 · 2013: 15 · 2012: 12
- FWCI
- 0.81
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Leukemia (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Acute Lymphoblastic Leukemia research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Keywords
- microRNA, childhood acute lymphoblastic leukemia, novel miRNA discovery, miRNA target genes, Bcl-2, B-cell precursor acute lymphoblastic leukemia, miRNA expression profiling, normal hematopoietic cells
- MeSH terms
- Child, Humans, RNA, Gene Library, Sequence Analysis, DNA, Computational Biology, Gene Expression Profiling, MicroRNAs, Precursor Cell Lymphoblastic Leukemia-Lymphoma, High-Throughput Nucleotide Sequencing
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
