Long Non-coding RNAs in the Development and Maintenance of Lymphoid Malignancies

  • Melanie Winkle
  • Agnieszka Dzikiewicz-Krawczyk
  • Joost KluiverEmail author
  • Anke van den Berg


The development of lymphoid cells (i.e. B and T cells) is a complicated process involving various differentiation substages in bone marrow, thymus, lymph nodes and the circulation. Long noncoding (lnc)RNAs are in many ways involved in both normal lymphoid development and malignant transformation of lymphoid cells. In this chapter, we give an overview of the current state of knowledge on the diverse roles of lncRNAs in lymphoid malignancies. One remarkable finding is the direct involvement of lncRNA transcription in genome integrity and malignant transformation. B and T cell receptor rearrangements involve the introduction of double strand DNA breaks followed by their directed repair. LncRNA transcription was associated with off-targeting of endonucleases introducing these double strand breaks, which can lead to chromosomal translocation of oncogene loci, and as a consequence aberrant expression and development of a malignancy. Oncogenic fusion genes present in a subset of T-cell malignancies were furthermore shown to influence expression of a subset of lncRNAs. These expression changes in turn, were directly linked to oncogenic pathways, treatment response and patient outcome. Overexpression of oncogenes also induced changes in lncRNA expression patterns. These oncogene-regulated lncRNAs in turn play essential roles in the mediation of the downstream effects of the respective oncogene. In addition, some lncRNAs are involved in the upstream regulation of common oncogenes. We furthermore discuss a few specific lncRNAs that have been functionally characterized in detail in one or multiple lymphoid cancers. Lastly, we address noncoding genome variants and their association with the susceptibility to lymphoid malignancies. We conclude that lncRNAs are major players in all aspects of lymphoid development and malignant transformation. This strongly suggests that lncRNAs can be exploited for prognostic and therapeutic purposes in lymphoid malignancies in the future.


  1. Aguilo, F., Zhou, M. M., & Walsh, M. J. (2011). Long noncoding RNA, polycomb, and the ghosts haunting INK4b-ARF-INK4a expression. Cancer Research, 71, 5365–5369.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Alvarez-Dominguez, J. R., & Lodish, H. F. (2017). Emerging mechanisms of long noncoding RNA function during normal and malignant hematopoiesis. Blood, 130(18), 1965–1975.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Amodio, N., Stamato, M. A., Juli, G., Morelli, E., Fulciniti, M., Manzoni, M., et al. (2018). Drugging the lncRNA MALAT1 via LNA gapmeR ASO inhibits gene expression of proteasome subunits and triggers anti-multiple myeloma activity. Leukemia, 32(9), 1948–1957.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Basu, U., Meng, F. L., Keim, C., Grinstein, V., Pefanis, E., Eccleston, J., et al. (2011). The RNA exosome targets the AID cytidine deaminase to both strands of transcribed duplex DNA substrates. Cell, 144, 353–363.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Beck-Engeser, G. B., Lum, A. M., Huppi, K., Caplen, N. J., Wang, B. B., & Wabl, M. (2008). Pvt1-encoded microRNAs in oncogenesis. Retrovirology, 5, 4.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Beekman, R., Amador, V., & Campo, E. (2018). SOX11, a key oncogenic factor in mantle cell lymphoma. Current Opinion in Hematology, 25, 299–306.PubMedCrossRefPubMedCentralGoogle Scholar
  7. Blume, C. J., Hotz-Wagenblatt, A., Hullein, J., Sellner, L., Jethwa, A., Stolz, T., et al. (2015). p53-dependent non-coding RNA networks in chronic lymphocytic leukemia. Leukemia, 29, 2015–2023.PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bonnal, R. J., Ranzani, V., Arrigoni, A., Curti, S., Panzeri, I., Gruarin, P., et al. (2015). De novo transcriptome profiling of highly purified human lymphocytes primary cells. Scientific Data, 2, 150051.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Casero, D., Sandoval, S., Seet, C. S., Scholes, J., Zhu, Y., Ha, V. L., et al. (2015). Long non-coding RNA profiling of human lymphoid progenitor cells reveals transcriptional divergence of B cell and T cell lineages. Nature Immunology, 16, 1282–1291.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Cerhan, J. R., Berndt, S. I., Vijai, J., Ghesquieres, H., McKay, J., Wang, S. S., et al. (2014). Genome-wide association study identifies multiple susceptibility loci for diffuse large B cell lymphoma. Nature Genetics, 46, 1233–1238.PubMedPubMedCentralCrossRefGoogle Scholar
  11. Chiarle, R., Zhang, Y., Frock, R. L., Lewis, S. M., Molinie, B., Ho, Y. J., et al. (2011). Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell, 147, 107–119.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Cho, S. F., Chang, Y. C., Chang, C. S., Lin, S. F., Liu, Y. C., Hsiao, H. H., et al. (2014). MALAT1 long non-coding RNA is overexpressed in multiple myeloma and may serve as a marker to predict disease progression. BMC Cancer, 14, 809.PubMedPubMedCentralCrossRefGoogle Scholar
  13. Conde, L., Riby, J., Zhang, J., Bracci, P. M., & Skibola, C. F. (2014). Copy number variation analysis on a non-Hodgkin lymphoma case-control study identifies an 11q25 duplication associated with diffuse large B-cell lymphoma. PLoS One, 9, e105382.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Derrien, T., Johnson, R., Bussotti, G., Tanzer, A., Djebali, S., Tilgner, H., et al. (2012). The GENCODE v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression. Genome Research, 22, 1775–1789.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Doose, G., Haake, A., Bernhart, S. H., Lopez, C., Duggimpudi, S., Wojciech, F., et al. (2015). MINCR is a MYC-induced lncRNA able to modulate MYC’s transcriptional network in Burkitt lymphoma cells. Proceedings of the National Academy of Sciences of the United States of America, 112, E5261–E5270.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Durinck, K., Wallaert, A., Van de Walle, I., Van Loocke, W., Volders, P. J., Vanhauwaert, S., et al. (2014). The Notch driven long non-coding RNA repertoire in T-cell acute lymphoblastic leukemia. Haematologica, 99, 1808–1816.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Dzikiewicz-Krawczyk, A., Kok, K., Slezak-Prochazka, I., Robertus, J. L., Bruining, J., Tayari, M. M., et al. (2017). ZDHHC11 and ZDHHC11B are critical novel components of the oncogenic MYC-miR-150-MYB network in Burkitt lymphoma. Leukemia, 31, 1470–1473.PubMedCrossRefPubMedCentralGoogle Scholar
  18. Enciso-Mora, V., Broderick, P., Ma, Y., Jarrett, R. F., Hjalgrim, H., Hemminki, K., et al. (2010). A genome-wide association study of Hodgkin’s lymphoma identifies new susceptibility loci at 2p16.1 (REL), 8q24.21 and 10p14 (GATA3). Nature Genetics, 42, 1126–1130.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Enninga, J., Levay, A., & Fontoura, B. M. (2003). Sec13 shuttles between the nucleus and the cytoplasm and stably interacts with Nup96 at the nuclear pore complex. Molecular and Cellular Biology, 23, 7271–7284.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Fang, K., Han, B. W., Chen, Z. H., Lin, K. Y., Zeng, C. W., Li, X. J., et al. (2014). A distinct set of long non-coding RNAs in childhood MLL-rearranged acute lymphoblastic leukemia: Biology and epigenetic target. Human Molecular Genetics, 23, 3278–3288.PubMedCrossRefGoogle Scholar
  21. Fernando, T. R., Rodriguez-Malave, N. I., Waters, E. V., Yan, W., Casero, D., Basso, G., et al. (2015). LncRNA expression discriminates karyotype and predicts survival in B-lymphoblastic leukemia. Molecular Cancer Research, 13, 839–851.PubMedCrossRefGoogle Scholar
  22. Fernando, T. R., Contreras, J. R., Zampini, M., Rodriguez-Malave, N. I., Alberti, M. O., Anguiano, J., et al. (2017). The lncRNA CASC15 regulates SOX4 expression in RUNX1-rearranged acute leukemia. Molecular Cancer, 16, 126.PubMedPubMedCentralCrossRefGoogle Scholar
  23. Gao, D., Lv, A. E., Li, H. P., Han, D. H., & Zhang, Y. P. (2017). LncRNA MALAT-1 elevates HMGB1 to promote autophagy resulting in inhibition of tumor cell apoptosis in multiple myeloma. Journal of Cellular Biochemistry, 118, 3341–3348.PubMedCrossRefGoogle Scholar
  24. Ghazavi, F., De Moerloose, B., Van Loocke, W., Wallaert, A., Helsmoortel, H. H., Ferster, A., et al. (2016). Unique long non-coding RNA expression signature in ETV6/RUNX1-driven B-cell precursor acute lymphoblastic leukemia. Oncotarget, 7, 73769–73780.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Ghesquieres, H., Larrabee, B. R., Casasnovas, O., Maurer, M. J., McKay, J. D., Ansell, S. M., et al. (2018). A susceptibility locus for classical Hodgkin lymphoma at 8q24 near MYC/PVT1 predicts patient outcome in two independent cohorts. British Journal of Haematology, 180, 286–290.PubMedCrossRefPubMedCentralGoogle Scholar
  26. Gioia, R., Drouin, S., Ouimet, M., Caron, M., St-Onge, P., Richer, C., et al. (2017). LncRNAs downregulated in childhood acute lymphoblastic leukemia modulate apoptosis, cell migration, and DNA damage response. Oncotarget, 8, 80645–80650.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Gu, Y., Xiao, X., & Yang, S. (2017). LncRNA MALAT1 acts as an oncogene in multiple myeloma through sponging miR-509-5p to modulate FOXP1 expression. Oncotarget, 8, 101984–101993.PubMedPubMedCentralGoogle Scholar
  28. Gutierrez-Camino, A., Martin-Guerrero, I., Garcia de Andoin, N., Sastre, A., Carbone Baneres, A., Astigarraga, I., et al. (2017). Confirmation of involvement of new variants at CDKN2A/B in pediatric acute lymphoblastic leukemia susceptibility in the Spanish population. PLoS One, 12, e0177421.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Handa, H., Kuroda, Y., Kimura, K., Masuda, Y., Hattori, H., Alkebsi, L., et al. (2017). Long non-coding RNA MALAT1 is an inducible stress response gene associated with extramedullary spread and poor prognosis of multiple myeloma. British Journal of Haematology, 179, 449–460.PubMedCrossRefPubMedCentralGoogle Scholar
  30. Hart, J. R., Roberts, T. C., Weinberg, M. S., Morris, K. V., & Vogt, P. K. (2014). MYC regulates the non-coding transcriptome. Oncotarget, 5, 12543–12554.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Heinaniemi, M., Vuorenmaa, T., Teppo, S., Kaikkonen, M. U., Bouvy-Liivrand, M., Mehtonen, J., et al. (2016). Transcription-coupled genetic instability marks acute lymphoblastic leukemia structural variation hotspots. eLife, 5, e13087. Scholar
  32. Hu, G., Lou, Z., & Gupta, M. (2014). The long non-coding RNA GAS5 cooperates with the eukaryotic translation initiation factor 4E to regulate c-Myc translation. PLoS One, 9, e107016.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Hu, A. X., Huang, Z. Y., Zhang, L., & Shen, J. (2017a). Potential prognostic long non-coding RNA identification and their validation in predicting survival of patients with multiple myeloma. Tumour Biology, 39, 1010428317694563.PubMedPubMedCentralGoogle Scholar
  34. Hu, G., Gupta, S. K., Troska, T. P., Nair, A., & Gupta, M. (2017b). Long non-coding RNA profile in mantle cell lymphoma identifies a functional lncRNA ROR1-AS1 associated with EZH2/PRC2 complex. Oncotarget, 8, 80223–80234.PubMedPubMedCentralGoogle Scholar
  35. Hu, Y., Lin, J., Fang, H., Fang, J., Li, C., Chen, W., et al. (2018). Targeting the MALAT1/PARP1/LIG3 complex induces DNA damage and apoptosis in multiple myeloma. Leukemia, 32(10), 2250–2262.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Hung, T., Wang, Y., Lin, M. F., Koegel, A. K., Kotake, Y., Grant, G. D., et al. (2011). Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nature Genetics, 43, 621–629.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Hungate, E. A., Vora, S. R., Gamazon, E. R., Moriyama, T., Best, T., Hulur, I., et al. (2016). A variant at 9p21.3 functionally implicates CDKN2B in paediatric B-cell precursor acute lymphoblastic leukaemia aetiology. Nature Communications, 7, 10635.PubMedPubMedCentralCrossRefGoogle Scholar
  38. Huppi, K., & Siwarski, D. (1994). Chimeric transcripts with an open reading frame are generated as a result of translocation to the Pvt-1 region in mouse B-cell tumors. International Journal of Cancer, 59, 848–851.PubMedCrossRefPubMedCentralGoogle Scholar
  39. Iyer, M. K., Niknafs, Y. S., Malik, R., Singhal, U., Sahu, A., Hosono, Y., et al. (2015). The landscape of long noncoding RNAs in the human transcriptome. Nature Genetics, 47, 199–208.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Karube, K., & Campo, E. (2015). MYC alterations in diffuse large B-cell lymphomas. Seminars in Hematology, 52, 97–106.PubMedCrossRefPubMedCentralGoogle Scholar
  41. Kim, S. H., Kim, S. H., Yang, W. I., Kim, S. J., & Yoon, S. O. (2017). Association of the long non-coding RNA MALAT1 with the polycomb repressive complex pathway in T and NK cell lymphoma. Oncotarget, 8, 31305–31317.PubMedPubMedCentralGoogle Scholar
  42. Kim, M., Morales, L. D., Jang, I. S., Cho, Y. Y., & Kim, D. J. (2018). Protein tyrosine phosphatases as potential regulators of STAT3 signaling. International Journal of Molecular Sciences, 19, E2708. Scholar
  43. Klein, I. A., Resch, W., Jankovic, M., Oliveira, T., Yamane, A., Nakahashi, H., et al. (2011). Translocation-capture sequencing reveals the extent and nature of chromosomal rearrangements in B lymphocytes. Cell, 147, 95–106.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Korac, P., Dotlic, S., Matulic, M., Zajc Petranovic, M., & Dominis, M. (2017). Role of MYC in B cell lymphomagenesis. Genes (Basel), 8, E115. Scholar
  45. Kotake, Y., Kitagawa, K., Ohhata, T., Sakai, S., Uchida, C., Niida, H., et al. (2016). Long non-coding RNA, PANDA, contributes to the stabilization of p53 tumor suppressor protein. Anticancer Research, 36, 1605–1611.PubMedPubMedCentralGoogle Scholar
  46. Lajoie, M., Drouin, S., Caron, M., St-Onge, P., Ouimet, M., Gioia, R., et al. (2017). Specific expression of novel long non-coding RNAs in high-hyperdiploid childhood acute lymphoblastic leukemia. PLoS One, 12, e0174124.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Li, B., Chen, P., Qu, J., Shi, L., Zhuang, W., Fu, J., et al. (2014). Activation of LTBP3 gene by a long noncoding RNA (lncRNA) MALAT1 transcript in mesenchymal stem cells from multiple myeloma. The Journal of Biological Chemistry, 289, 29365–29375.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Limon, J. J., & Fruman, D. A. (2012). Akt and mTOR in B cell activation and differentiation. Frontiers in Immunology, 3, 228.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Lollies, A., Hartmann, S., Schneider, M., Bracht, T., Weiss, A. L., Arnolds, J., et al. (2018). An oncogenic axis of STAT-mediated BATF3 upregulation causing MYC activity in classical Hodgkin lymphoma and anaplastic large cell lymphoma. Leukemia, 32, 92–101.PubMedCrossRefPubMedCentralGoogle Scholar
  50. Lu, Z., Pannunzio, N. R., Greisman, H. A., Casero, D., Parekh, C., & Lieber, M. R. (2015). Convergent BCL6 and lncRNA promoters demarcate the major breakpoint region for BCL6 translocations. Blood, 126, 1730–1731.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Macchia, G., Lonoce, A., Venuto, S., Macri, E., Palumbo, O., Carella, M., et al. (2016). A rare but recurrent t(8;13)(q24;q14) translocation in B-cell chronic lymphocytic leukaemia causing MYC up-regulation and concomitant loss of PVT1, miR-15/16 and DLEU7. British Journal of Haematology, 172, 296–299.PubMedCrossRefPubMedCentralGoogle Scholar
  52. Malouf, C., & Ottersbach, K. (2018). Molecular processes involved in B cell acute lymphoblastic leukaemia. Cellular and Molecular Life Sciences, 75, 417–446.PubMedCrossRefPubMedCentralGoogle Scholar
  53. Matthews, A. J., Zheng, S., DiMenna, L. J., & Chaudhuri, J. (2014). Regulation of immunoglobulin class-switch recombination: Choreography of noncoding transcription, targeted DNA deamination, and long-range DNA repair. Advances in Immunology, 122, 1–57.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Medyouf, H., Gusscott, S., Wang, H., Tseng, J. C., Wai, C., Nemirovsky, O., et al. (2011). High-level IGF1R expression is required for leukemia-initiating cell activity in T-ALL and is supported by Notch signaling. The Journal of Experimental Medicine, 208, 1809–1822.PubMedPubMedCentralCrossRefGoogle Scholar
  55. Melo, C. P., Campos, C. B., Rodrigues Jde, O., Aguirre-Neto, J. C., Atalla, A., Pianovski, M. A., et al. (2016). Long non-coding RNAs: Biomarkers for acute leukaemia subtypes. British Journal of Haematology, 173, 318–320.PubMedCrossRefPubMedCentralGoogle Scholar
  56. Meng, F. L., Du, Z., Federation, A., Hu, J., Wang, Q., Kieffer-Kwon, K. R., et al. (2014). Convergent transcription at intragenic super-enhancers targets AID-initiated genomic instability. Cell, 159, 1538–1548.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Meng, H., Han, L., Hong, C., Ding, J., & Huang, Q. (2018). Aberrant lncRNA expression in multiple myeloma. Oncology Research, 26, 809–816.PubMedCrossRefPubMedCentralGoogle Scholar
  58. Mladenov, E., Magin, S., Soni, A., & Iliakis, G. (2013). DNA double-strand break repair as determinant of cellular radiosensitivity to killing and target in radiation therapy. Frontiers in Oncology, 3, 113.PubMedPubMedCentralCrossRefGoogle Scholar
  59. Mourtada-Maarabouni, M., & Williams, G. T. (2014). Role of GAS5 noncoding RNA in mediating the effects of rapamycin and its analogues on mantle cell lymphoma cells. Clinical Lymphoma, Myeloma and Leukemia, 14, 468–473.PubMedCrossRefPubMedCentralGoogle Scholar
  60. Mourtada-Maarabouni, M., Hedge, V. L., Kirkham, L., Farzaneh, F., & Williams, G. T. (2008). Growth arrest in human T-cells is controlled by the non-coding RNA growth-arrest-specific transcript 5 (GAS5). Journal of Cell Science, 121, 939–946.PubMedCrossRefGoogle Scholar
  61. Nagoshi, H., Taki, T., Hanamura, I., Nitta, M., Otsuki, T., Nishida, K., et al. (2012). Frequent PVT1 rearrangement and novel chimeric genes PVT1-NBEA and PVT1-WWOX occur in multiple myeloma with 8q24 abnormality. Cancer Research, 72, 4954–4962.PubMedCrossRefGoogle Scholar
  62. Nakamura, Y., Takahashi, N., Kakegawa, E., Yoshida, K., Ito, Y., Kayano, H., et al. (2008). The GAS5 (growth arrest-specific transcript 5) gene fuses to BCL6 as a result of t(1;3)(q25;q27) in a patient with B-cell lymphoma. Cancer Genetics and Cytogenetics, 182, 144–149.PubMedCrossRefGoogle Scholar
  63. Ngoc, P. C. T., Tan, S. H., Tan, T. K., Chan, M. M., Li, Z., Yeoh, A. E. J., et al. (2018). Identification of novel lncRNAs regulated by the TAL1 complex in T-cell acute lymphoblastic leukemia. Leukemia, 32(10), 2138–2151.PubMedCrossRefGoogle Scholar
  64. Ouimet, M., Drouin, S., Lajoie, M., Caron, M., St-Onge, P., Gioia, R., et al. (2017). A childhood acute lymphoblastic leukemia-specific lncRNA implicated in prednisolone resistance, cell proliferation, and migration. Oncotarget, 8, 7477–7488.PubMedCrossRefGoogle Scholar
  65. Pefanis, E., Wang, J., Rothschild, G., Lim, J., Chao, J., Rabadan, R., et al. (2014). Noncoding RNA transcription targets AID to divergently transcribed loci in B cells. Nature, 514, 389–393.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Petri, A., Dybkaer, K., Bogsted, M., Thrue, C. A., Hagedorn, P. H., Schmitz, A., et al. (2015). Long noncoding RNA expression during human B-cell development. PLoS One, 10, e0138236.PubMedPubMedCentralCrossRefGoogle Scholar
  67. Petrich, A. M., Nabhan, C., & Smith, S. M. (2014). MYC-associated and double-hit lymphomas: A review of pathobiology, prognosis, and therapeutic approaches. Cancer, 120, 3884–3895.PubMedCrossRefGoogle Scholar
  68. Pike, K. A., & Tremblay, M. L. (2016). TC-PTP and PTP1B: Regulating JAK-STAT signaling, controlling lymphoid malignancies. Cytokine, 82, 52–57.PubMedCrossRefGoogle Scholar
  69. Poi, M. J., Li, J., Sborov, D. W., VanGundy, Z., Cho, Y. K., Lamprecht, M., et al. (2017). Polymorphism in ANRIL is associated with relapse in patients with multiple myeloma after autologous stem cell transplant. Molecular Carcinogenesis, 56, 1722–1732.PubMedCrossRefGoogle Scholar
  70. Puvvula, P. K., Desetty, R. D., Pineau, P., Marchio, A., Moon, A., Dejean, A., et al. (2014). Long noncoding RNA PANDA and scaffold-attachment-factor SAFA control senescence entry and exit. Nature Communications, 5, 5323.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Qian, J., Wang, Q., Dose, M., Pruett, N., Kieffer-Kwon, K. R., Resch, W., et al. (2014). B cell super-enhancers and regulatory clusters recruit AID tumorigenic activity. Cell, 159, 1524–1537.PubMedPubMedCentralCrossRefGoogle Scholar
  72. Radhakrishnan, S. K., Lee, C. S., Young, P., Beskow, A., Chan, J. Y., & Deshaies, R. J. (2010). Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Molecular Cell, 38, 17–28.PubMedPubMedCentralCrossRefGoogle Scholar
  73. Ranzani, V., Rossetti, G., Panzeri, I., Arrigoni, A., Bonnal, R. J., Curti, S., et al. (2015). The long intergenic noncoding RNA landscape of human lymphocytes highlights the regulation of T cell differentiation by linc-MAF-4. Nature Immunology, 16, 318–325.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Rodriguez-Malave, N. I., Fernando, T. R., Patel, P. C., Contreras, J. R., Palanichamy, J. K., Tran, T. M., et al. (2015). BALR-6 regulates cell growth and cell survival in B-lymphoblastic leukemia. Molecular Cancer, 14, 214.PubMedPubMedCentralCrossRefGoogle Scholar
  75. Ronchetti, D., Agnelli, L., Taiana, E., Galletti, S., Manzoni, M., Todoerti, K., et al. (2016a). Distinct lncRNA transcriptional fingerprints characterize progressive stages of multiple myeloma. Oncotarget, 7, 14814–14830.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Ronchetti, D., Manzoni, M., Agnelli, L., Vinci, C., Fabris, S., Cutrona, G., et al. (2016b). lncRNA profiling in early-stage chronic lymphocytic leukemia identifies transcriptional fingerprints with relevance in clinical outcome. Blood Cancer Journal, 6, e468.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Sanchez-Martin, M., & Ferrando, A. (2017). The NOTCH1-MYC highway toward T-cell acute lymphoblastic leukemia. Blood, 129, 1124–1133.PubMedCrossRefPubMedCentralGoogle Scholar
  78. Savage, K. J., Johnson, N. A., Ben-Neriah, S., Connors, J. M., Sehn, L. H., Farinha, P., et al. (2009). MYC gene rearrangements are associated with a poor prognosis in diffuse large B-cell lymphoma patients treated with R-CHOP chemotherapy. Blood, 114, 3533–3537.PubMedCrossRefPubMedCentralGoogle Scholar
  79. Schrader, A., Bentink, S., Spang, R., Lenze, D., Hummel, M., Kuo, M., et al. (2012). High Myc activity is an independent negative prognostic factor for diffuse large B cell lymphomas. International Journal of Cancer, 131, E348–E361.PubMedCrossRefPubMedCentralGoogle Scholar
  80. Sehgal, L., Mathur, R., Braun, F. K., Wise, J. F., Berkova, Z., Neelapu, S., et al. (2014). FAS-antisense 1 lncRNA and production of soluble versus membrane FAS in B-cell lymphoma. Leukemia, 28, 2376–2387.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Smith, C. M., & Steitz, J. A. (1998). Classification of gas5 as a multi-small-nucleolar-RNA (snoRNA) host gene and a member of the 5′-terminal oligopyrimidine gene family reveals common features of snoRNA host genes. Molecular and Cellular Biology, 18, 6897–6909.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Sun, J., Cheng, L., Shi, H., Zhang, Z., Zhao, H., Wang, Z., et al. (2016). A potential panel of six-long non-coding RNA signature to improve survival prediction of diffuse large-B-cell lymphoma. Scientific Reports, 6, 27842.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Swier, L. J. Y. M., Dzikiewicz-Krawczyk, A., Winkle, M., van den Berg, A., & Kluiver, J. (2019). Intricate crosstalk between MYC and non-coding RNAs regulates hallmarks of cancer. Molecular Oncology, 13(1), 26–45. Scholar
  84. Tayari, M. M., Winkle, M., Kortman, G., Sietzema, J., de Jong, D., Terpstra, M., et al. (2016). Long noncoding RNA expression profiling in normal B-cell subsets and Hodgkin lymphoma reveals Hodgkin and reed-Sternberg cell-specific long noncoding RNAs. The American Journal of Pathology, 186, 2462–2472.PubMedCrossRefPubMedCentralGoogle Scholar
  85. Trimarchi, T., Bilal, E., Ntziachristos, P., Fabbri, G., Dalla-Favera, R., Tsirigos, A., et al. (2014). Genome-wide mapping and characterization of Notch-regulated long noncoding RNAs in acute leukemia. Cell, 158, 593–606.PubMedPubMedCentralCrossRefGoogle Scholar
  86. Tseng, Y. Y., Moriarity, B. S., Gong, W., Akiyama, R., Tiwari, A., Kawakami, H., et al. (2014). PVT1 dependence in cancer with MYC copy-number increase. Nature, 512, 82–86.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Tsutsumi, Y., Chinen, Y., Sakamoto, N., Nagoshi, H., Nishida, K., Kobayashi, S., et al. (2013). Deletion or methylation of CDKN2A/2B and PVT1 rearrangement occur frequently in highly aggressive B-cell lymphomas harboring 8q24 abnormality. Leukemia and Lymphoma, 54, 2760–2764.PubMedCrossRefPubMedCentralGoogle Scholar
  88. Verboom, K., Van Loocke, W., Volders, P. J., Decaesteker, B., Avila Cobos, F., Bornschein, S., et al. (2018). A comprehensive inventory of TLX1 controlled long non-coding RNAs in T-cell acute lymphoblastic leukemia through polyA+ and total RNA sequencing. Haematologica, 103(12), e585–e589.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Wallaert, A., Durinck, K., Van Loocke, W., Van de Walle, I., Matthijssens, F., Volders, P. J., et al. (2016). Long noncoding RNA signatures define oncogenic subtypes in T-cell acute lymphoblastic leukemia. Leukemia, 30, 1927–1930.PubMedCrossRefPubMedCentralGoogle Scholar
  90. Wang, Y., Wu, P., Lin, R., Rong, L., Xue, Y., & Fang, Y. (2015). LncRNA NALT interaction with NOTCH1 promoted cell proliferation in pediatric T cell acute lymphoblastic leukemia. Scientific Reports, 5, 13749.PubMedPubMedCentralCrossRefGoogle Scholar
  91. Wang, X., Sehgal, L., Jain, N., Khashab, T., Mathur, R., & Samaniego, F. (2016). LncRNA MALAT1 promotes development of mantle cell lymphoma by associating with EZH2. Journal of Translational Medicine, 14, 346.PubMedPubMedCentralCrossRefGoogle Scholar
  92. Wang, Y., Zhang, M., Xu, H., Wang, Y., Li, Z., Chang, Y., et al. (2017). Discovery and validation of the tumor-suppressive function of long noncoding RNA PANDA in human diffuse large B-cell lymphoma through the inactivation of MAPK/ERK signaling pathway. Oncotarget, 8, 72182–72196.PubMedPubMedCentralGoogle Scholar
  93. Weng, A. P., Ferrando, A. A., Lee, W., Morris, J. P., Silverman, L. B., Sanchez-Irizarry, C., et al. (2004). Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science, 306, 269–271.PubMedCrossRefPubMedCentralGoogle Scholar
  94. Winkle, M., van den Berg, A., Tayari, M., Sietzema, J., Terpstra, M., Kortman, G., et al. (2015). Long noncoding RNAs as a novel component of the Myc transcriptional network. The FASEB Journal, 29, 2338–2346.PubMedCrossRefPubMedCentralGoogle Scholar
  95. Zeidler, R., Joos, S., Delecluse, H. J., Klobeck, G., Vuillaume, M., Lenoir, G. M., et al. (1994). Breakpoints of Burkitt’s lymphoma t(8;22) translocations map within a distance of 300 kb downstream of MYC. Genes, Chromosomes and Cancer, 9, 282–287.PubMedCrossRefPubMedCentralGoogle Scholar
  96. Zhou, M., Zhao, H., Xu, W., Bao, S., Cheng, L., & Sun, J. (2017). Discovery and validation of immune-associated long non-coding RNA biomarkers associated with clinically molecular subtype and prognosis in diffuse large B cell lymphoma. Molecular Cancer, 16, 16.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Melanie Winkle
    • 1
  • Agnieszka Dzikiewicz-Krawczyk
    • 2
  • Joost Kluiver
    • 1
    Email author
  • Anke van den Berg
    • 1
  1. 1.Department of Pathology and Medical BiologyUniversity of Groningen, University Medical Center Groningen (UMCG)GroningenThe Netherlands
  2. 2.Institute of Human Genetics, Polish Academy of SciencesPoznanPoland

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