Advertisement

Pathology and Molecular Pathogenesis of Burkitt Lymphoma and Lymphoblastic Lymphoma

  • Hélène A. Poirel
  • Maria Raffaella Ambrosio
  • Pier Paolo Piccaluga
  • Lorenzo Leoncini
Chapter
Part of the Hematologic Malignancies book series (HEMATOLOGIC)

Abstract

Burkitt lymphoma and lymphoblastic lymphoma are highly aggressive lymphomas mostly occurring in children, adolescents, and young adults. They account for approximately 4–5% of all non-Hodgkin lymphomas in Western countries. These B-cell neoplasms were frequently grouped together in the past, due to their fast-growing clinical behavior, related to a short doubling time, and their frequent presentation as acute leukemia. Burkitt leukemia was formerly classified as a lymphoblastic leukemia with L3 morphology according to the FAB classification. However, the biological characterization, especially the immunophenotype of these lymphomas, showed that Burkitt leukemia/lymphoma and lymphoblastic leukemia/lymphoma correspond to radically different stages of lymphoid maturation, with a different cell of origin, justifying their classification as separate entities in the WHO classification: lymphoblastic lymphoma is a B- or T-cell precursor lymphoid neoplasm, while Burkitt lymphoma is a mature B-cell neoplasm. As with other subtypes of lymphomas, emerging data from gene expression profiling, next-generation sequencing, and related techniques help to define these entities more precisely and to better understand their pathogenesis in order to identify potential new rational therapeutic targets.

References

  1. 1.
    Bennett JM, Catovsky D, Daniel MT, et al. French-American-British (FAB Cooperative Group) Proposals for the classification of the acute leukaemias. Br J Haematol. 1976;33:451–8.PubMedGoogle Scholar
  2. 2.
    Swerdlow SH, Campo E, Harris NL, et al. WHO classification of tumours of haematopoietic and lymphoid tissues. Lyon, France: IARC Press; 2008.Google Scholar
  3. 3.
    Swerdlow SH, Campo E, Harris NL, et al. WHO classification of tumours of haematopoietic and lymphoid tissues. 4th ed. Lyon: IARC Press; 2017.Google Scholar
  4. 4.
    Basso K, Dalla-Favera R. Germinal centres and B cell lymphomagenesis. Nat Rev Immunol. 2015;15(3):172–84. Review.PubMedGoogle Scholar
  5. 5.
    Dominguez-Sola D, Victora GD, Ying CY, Phan RT, Saito M, Nussenzweig MC, Dalla-Favera R. The proto-oncogene MYC is required for selection in the germinal center and cyclic reentry. Nat Immunol. 2012;13(11):1083–91.PubMedPubMedCentralGoogle Scholar
  6. 6.
    Victora GD, Dominguez-Sola D, Holmes AB, Deroubaix S, Dalla-Favera R, Nussenzweig MC. Identification of human germinal center light and dark zone cells and their relationship to human B-cell lymphomas. Blood. 2012;120(11):2240–8.PubMedPubMedCentralGoogle Scholar
  7. 7.
    Ambrosio MR, Lo Bello G, Amato T, Lazzi S, Piccaluga PP, Leoncini L, Bellan C. The cell of origin of Burkitt lymphoma: germinal centre or not germinal centre? Histopathology. 2016;69(5):885–6.PubMedGoogle Scholar
  8. 8.
    Rowe M, Kelly GL, Bell AI, Rickinson AB. Burkitt’s lymphoma: the Rosetta Stone deciphering Epstein-Barr virus biology. Semin Cancer Biol. 2009;19(6):377–88.Google Scholar
  9. 9.
    Magrath I. Epidemiology: clues to the pathogenesis of Burkitt lymphoma. Br J Haematol. 2012;156(6):744–56.PubMedGoogle Scholar
  10. 10.
    Burkitt D. A sarcoma involving the jaws in African children. Br J Surg. 1958;46(197):218–23.PubMedGoogle Scholar
  11. 11.
    Magrath I. Denis Burkitt and the African lymphoma. Ecancermedicalscience. 2009;3:159.PubMedPubMedCentralGoogle Scholar
  12. 12.
    Epstein A. Burkitt lymphoma and the discovery of Epstein-Barr virus. Br J Haematol. 2012;156(6):777–9.PubMedGoogle Scholar
  13. 13.
    Van Krieken JHJM. Encyclopedia of pathology. Berlin Heidelberg: Springer-Verlag; 2014.Google Scholar
  14. 14.
    Ambrosio MR, Piccaluga PP, Ponzoni M, Rocca BJ, Malagnino V, Onorati M, De Falco G, Calbi V, Ogwang M, Naresh KN, Pileri SA, Doglioni C, Leoncini L, Lazzi S. The alteration of lipid metabolism in Burkitt lymphoma identifies a novel marker: adipophilin. PLoS One. 2012;7(8):e44315.PubMedPubMedCentralGoogle Scholar
  15. 15.
    Disanto MG, Ambrosio MR, Rocca BJ, Ibrahim HA, Leoncini L, Naresh KN. Optimal minimal panels of immunohistochemistry for diagnosis of B-cell lymphoma for application in countries with limited resources and for triaging cases before referral to specialist centers. Am J Clin Pathol. 2016;145(5):687–95.PubMedGoogle Scholar
  16. 16.
    Naresh KN, Ibrahim HA, Lazzi S, Rince P, Onorati M, Ambrosio MR, Bilhou-Nabera C, Amen F, Reid A, Mawanda M, Calbi V, Ogwang M, Rogena E, Byakika B, Sayed S, Moshi E, Mwakigonja A, Raphael M, Magrath I, Leoncini L. Diagnosis of Burkitt lymphoma using an algorithmic approach—applicable in both resource-poor and resource-rich countries. Br J Haematol. 2011;154(6):770–6.PubMedGoogle Scholar
  17. 17.
    Jaffe ES, Arber DA, Campo E, Lee Harris N, Quintanilla-Fend L. Hematopathology. 2nd ed. New York: Elsevier; 2016.Google Scholar
  18. 18.
    De Falco G, Ambrosio MR, Fuligni F, Onnis A, Bellan C, Rocca BJ, Navari M, Etebari M, Mundo L, Gazaneo S, Facchetti F, Pileri SA, Leoncini L, Piccaluga PP. Burkitt lymphoma beyond MYC translocation: N-MYC and DNA methyltransferases dysregulation. BMC Cancer. 2015;15:668.PubMedPubMedCentralGoogle Scholar
  19. 19.
    Nguyen L, Papenhausen P, Shao H. The role of c-MYC in B-cell lymphomas: diagnostic and molecular aspects. Genes (Basel). 2017;8(4):E116.Google Scholar
  20. 20.
    Vallespinós M, Fernández D, Rodríguez L, Alvaro-Blanco J, Baena E, Ortiz M, Dukovska D, Martínez D, Rojas A, Campanero MR, Moreno de Alborán I. B Lymphocyte commitment program is driven by the proto-oncogene c-Myc. J Immunol. 2011;186(12):6726–36.PubMedGoogle Scholar
  21. 21.
    Dave SS, Fu K, Wright GW, Lam LT, Kluin P, Boerma EJ, Greiner TC, Weisenburger DD, Rosenwald A, Ott G, Müller-Hermelink HK, Gascoyne RD, Delabie J, Rimsza LM, Braziel RM, Grogan TM, Campo E, Jaffe ES, Dave BJ, Sanger W, Bast M, Vose JM, Armitage JO, Connors JM, Smeland EB, Kvaloy S, Holte H, Fisher RI, Miller TP, Montserrat E, Wilson WH, Bahl M, Zhao H, Yang L, Powell J, Simon R, Chan WC, Staudt LM, Lymphoma/Leukemia Molecular Profiling Project. Molecular diagnosis of Burkitt’s lymphoma. N Engl J Med. 2006;354(23):2431–42.Google Scholar
  22. 22.
    Hummel M, Bentink S, Berger H, Klapper W, Wessendorf S, Barth TF, Bernd HW, Cogliatti SB, Dierlamm J, Feller AC, Hansmann ML, Haralambieva E, Harder L, Hasenclever D, Kühn M, Lenze D, Lichter P, Martin-Subero JI, Möller P, Müller-Hermelink HK, Ott G, Parwaresch RM, Pott C, Rosenwald A, Rosolowski M, Schwaenen C, Stürzenhofecker B, Szczepanowski M, Trautmann H, Wacker HH, Spang R, Loeffler M, Trümper L, Stein H, Siebert R, Molecular Mechanisms in Malignant Lymphomas Network Project of the Deutsche Krebshilfe. A biologic definition of Burkitt’s lymphoma from transcriptional and genomic profiling. N Engl J Med. 2006;354(23):2419–30.Google Scholar
  23. 23.
    Leucci E, Cocco M, Onnis A, De Falco G, van Cleef P, Bellan C, van Rijk A, Nyagol J, Byakika B, Lazzi S, Tosi P, van Krieken H, Leoncini L. MYC translocation-negative classical Burkitt lymphoma cases: an alternative pathogenetic mechanism involving miRNA deregulation. J Pathol. 2008;216(4):440–50.PubMedGoogle Scholar
  24. 24.
    Salaverria I, Martin-Guerrero I, Wagener R, Kreuz M, Kohler CW, Richter J, Pienkowska-Grela B, Adam P, Burkhardt B, Claviez A, Damm-Welk C, Drexler HG, Hummel M, Jaffe ES, Küppers R, Lefebvre C, Lisfeld J, Löffler M, Macleod RA, Nagel I, Oschlies I, Rosolowski M, Russell RB, Rymkiewicz G, Schindler D, Schlesner M, Scholtysik R, Schwaenen C, Spang R, Szczepanowski M, Trümper L, Vater I, Wessendorf S, Klapper W, Siebert R, Molecular Mechanisms in Malignant Lymphoma Network Project; Berlin-Frankfurt-Münster Non-Hodgkin Lymphoma Group. A recurrent 11q aberration pattern characterizes a subset of MYC-negative high-grade B-cell lymphomas resembling Burkitt lymphoma. Blood. 2014;123(8):1187–98.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Havelange V, Ameye G, Théate I, Callet-Bauchu E, Lippert E, Luquet I, Raphaël M, Vikkula M, Poirel HA. The peculiar 11q-gain/loss aberration reported in a subset of MYC-negative high-grade B-cell lymphomas can also occur in a MYC-rearranged lymphoma. Cancer Genet. 2016a;209(3):117–8.PubMedGoogle Scholar
  26. 26.
    Havelange V, Ameye G, Callet-Bauchu E, Dastugue N, Barin C, Penther D, Michaux L, Hagemeijer A, Mugneret F, Poirel HA. Patterns of genomic aberrations suggest that Burkitt lymphomas with complex karyotype remain different from the other aggressive B-cell lymphomas with MYC rearrangement. Genes Chromosomes Cancer. 2013;52(1):81–92.PubMedGoogle Scholar
  27. 27.
    Poirel HA, Cairo MS, Heerema NA, Swansbury J, Aupérin A, Launay E, Sanger WG, Talley P, Perkins SL, Raphael M, McCarthy K, Sposto R, Gerrard M, Bernheim A, Patte C, on behalf of the FAB LMB 96 International Study Committee. Specific cytogenetic abnormalities are associated with a significantly inferior outcome in children and adolescents with mature B-cell non-Hodgkin’s lymphoma: results of the FAB/LMB 96 international study. Leukemia. 2009;23(2):323–31.PubMedGoogle Scholar
  28. 28.
    Piccaluga PP, De Falco G, Kustagi M, Gazzola A, Agostinelli C, Tripodo C, Leucci E, Onnis A, Astolfi A, Sapienza MR, Bellan C, Lazzi S, Tumwine L, Mawanda M, Ogwang M, Calbi V, Formica S, Califano A, Pileri SA, Leoncini L. Gene expression analysis uncovers similarity and differences among Burkitt lymphoma subtypes. Blood. 2011;117(13):3596–608.PubMedGoogle Scholar
  29. 29.
    Lenze D, Leoncini L, Hummel M, Volinia S, Liu CG, Amato T, De Falco G, Githanga J, Horn H, Nyagol J, Ott G, Palatini J, Pfreundschuh M, Rogena E, Rosenwald A, Siebert R, Croce CM, Stein H. The different epidemiologic subtypes of Burkitt lymphoma share a homogenous micro RNA profile distinct from diffuse large B-cell lymphoma. Leukemia. 2011;25(12):1869–76.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Havelange V, Pepermans X, Ameye G, Théate I, Callet-Bauchu E, Barin C, Penther D, Lippert E, Michaux L, Mugneret F, Dastugue N, Raphaël M, Vikkula M, Poirel HA. Genetic differences between pediatric and adult Burkitt lymphomas. Br J Haematol. 2016b;173(1):137–44.PubMedGoogle Scholar
  31. 31.
    Love C, Sun Z, Jima D, Li G, Zhang J, Miles R, Richards KL, Dunphy CH, Choi WW, Srivastava G, Lugar PL, Rizzieri DA, Lagoo AS, Bernal-Mizrachi L, Mann KP, Flowers CR, Naresh KN, Evens AM, Chadburn A, Gordon LI, Czader MB, Gill JI, Hsi ED, Greenough A, Moffitt AB, McKinney M, Banerjee A, Grubor V, Levy S, Dunson DB, Dave SS. The genetic landscape of mutations in Burkitt lymphoma. Nat Genet. 2012;44(12):1321–5.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Schmitz R, Young RM, Ceribelli M, Jhavar S, Xiao W, Zhang M, Wright G, Shaffer AL, Hodson DJ, Buras E, Liu X, Powell J, Yang Y, Xu W, Zhao H, Kohlhammer H, Rosenwald A, Kluin P, Müller-Hermelink HK, Ott G, Gascoyne RD, Connors JM, Rimsza LM, Campo E, Jaffe ES, Delabie J, Smeland EB, Ogwang MD, Reynolds SJ, Fisher RI, Braziel RM, Tubbs RR, Cook JR, Weisenburger DD, Chan WC, Pittaluga S, Wilson W, Waldmann TA, Rowe M, Mbulaiteye SM, Rickinson AB, Staudt LM. Burkitt lymphoma pathogenesis and therapeutic targets from structural and functional genomics. Nature. 2012;490(7418):116–20.PubMedPubMedCentralGoogle Scholar
  33. 33.
    Schmitz R, Ceribelli M, Pittaluga S, Wright G, Staudt LM. Oncogenic mechanisms in Burkitt lymphoma. Cold Spring Harb Perspect Med. 2014;4(2):a014282.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Richter J, Schlesner M, Hoffmann S, Kreuz M, Leich E, Burkhardt B, Rosolowski M, Ammerpohl O, Wagener R, Bernhart SH, Lenze D, Szczepanowski M, Paulsen M, Lipinski S, Russell RB, Adam-Klages S, Apic G, Claviez A, Hasenclever D, Hovestadt V, Hornig N, Korbel JO, Kube D, Langenberger D, Lawerenz C, Lisfeld J, Meyer K, Picelli S, Pischimarov J, Radlwimmer B, Rausch T, Rohde M, Schilhabel M, Scholtysik R, Spang R, Trautmann H, Zenz T, Borkhardt A, Drexler HG, Möller P, MacLeod RA, Pott C, Schreiber S, Trümper L, Loeffler M, Stadler PF, Lichter P, Eils R, Küppers R, Hummel M, Klapper W, Rosenstiel P, Rosenwald A, Brors B, Siebert R, MMML-Seq Project ICGC. Recurrent mutation of the ID3 gene in Burkitt lymphoma identified by integrated genome, exome and transcriptome sequencing. Nat Genet. 2012;44:1316–20.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Greenough A, Dave SS. New clues to the molecular pathogenesis of Burkitt lymphoma revealed through next-generation sequencing. Curr Opin Hematol. 2014;21(4):326–32.PubMedGoogle Scholar
  36. 36.
    Abate F, Ambrosio MR, Mundo L, Laginestra MA, Fuligni F, Rossi M, Zairis S, Gazaneo S, De Falco G, Lazzi S, Bellan C, Rocca BJ, Amato T, Marasco E, Etebari M, Ogwang M, Calbi V, Ndede I, Patel K, Chumba D, Piccaluga PP, Pileri S, Leoncini L, Rabadan R. Distinct viral and mutational spectrum of endemic burkitt lymphoma. PLoS Pathog. 2015;11(10):e1005158.PubMedPubMedCentralGoogle Scholar
  37. 37.
    Küppers R. Mechanisms of B-cell lymphoma 7pathogenesis. Nat Rev Cancer. 2005;5(4):251–62. Review.PubMedGoogle Scholar
  38. 38.
    Sander S, Calado DP, Srinivasan L, Köchert K, Zhang B, Rosolowski M, Rodig SJ, Holzmann K, Stilgenbauer S, Siebert R, Bullinger L, Rajewsky K. Synergy between PI3K signaling and MYC in Burkitt lymphomagenesis. Cancer Cell. 2012;22(2):167–79.PubMedPubMedCentralGoogle Scholar
  39. 39.
    Amato T, Abate F, Piccaluga P, Iacono M, Fallerini C, Renieri A, De Falco G, Ambrosio MR, Mourmouras V, Ogwang M, Calbi V, Rabadan R, Hummel M, Pileri S, Leoncini L, Bellan C. Clonality analysis of immunoglobulin gene rearrangement by next-generation sequencing in endemic Burkitt lymphoma suggests antigen drive activation of BCR as opposed to sporadic Burkitt lymphoma. Am J Clin Pathol. 2016;145(1):116–27.PubMedGoogle Scholar
  40. 40.
    Cai Q, Medeiros LJ, Xu X, Young KH. MYC-driven aggressive B-cell lymphomas: biology, entity, differential diagnosis and clinical management. Oncotarget. 2015;6(36):38591–616.PubMedPubMedCentralGoogle Scholar
  41. 41.
    Moormann AM, Snider CJ, Chelimo K. The company malaria keeps: how co-infection with Epstein-Barr virus leads to endemic Burkitt lymphoma. Curr Opin Infect Dis. 2011;24:435–41.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Rochford R, Cannon MJ, Moormann AM. Endemic Burkitt’s lymphoma: a polymicrobial disease? Nat Rev Microbiol. 2005;3(2):182–7.Google Scholar
  43. 43.
    Thorley-Lawson DA, Hawkins JB, Tracy SI, Shapiro M. The pathogenesis of Epstein-Barr virus persistent infection. Curr Opin Virol. 2013;3:227–32.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Ambrosio MR, Navari M, Di Lisio L, Leon EA, Onnis A, Gazaneo S, Mundo L, Ulivieri C, Gomez G, Lazzi S, Piris MA, Leoncini L, De Falco G. The Epstein Barr-encoded BART-6-3p microRNA affects regulation of cell growth and immuno response in Burkitt lymphoma. Infect Agent Cancer. 2014a;14(9):12.Google Scholar
  45. 45.
    Ambrosio MR, De Falco G, Gozzetti A, Rocca BJ, Amato T, Mourmouras V, Gazaneo S, Mundo L, Candi V, Piccaluga PP, Cusi MG, Leoncini L, Lazzi S. Plasmablastic transformation of a pre-existing plasmacytoma: a possible role for reactivation of Epstein Barr virus infection. Haematologica. 2014b;99(11):e235–7.PubMedPubMedCentralGoogle Scholar
  46. 46.
    Arvey A, Ojesina AI, Pedamallu CS, Ballon G, Jung J, et al. The tumor virus landscape of AIDS-related lymphomas. Blood. 2015;125:e14–22.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Piccaluga PP, Navari M, De Falco G, Ambrosio MR, Lazzi S, Fuligni F, Bellan C, Rossi M, Sapienza MR, Laginestra MA, Etebari M, Rogena EA, Tumwine L, Tripodo C, Gibellini D, Consiglio J, Croce CM, Pileri SA, Leoncini L. Virus-encoded microRNA contributes to the molecular profile of EBV-positive Burkitt lymphomas. Oncotarget. 2016;7(1):224–40.PubMedGoogle Scholar
  48. 48.
    Navari M, Etebari M, De Falco G, Ambrosio MR, Gibellini D, Leoncini L, Piccaluga PP. The presence of Epstein-Barr virus significantly impacts the transcriptional profile in immunodeficiency-associated Burkitt lymphoma. Front Microbiol. 2015;6:556.PubMedPubMedCentralGoogle Scholar
  49. 49.
    Navari M, Fuligni F, Laginestra MA, Etebari M, Ambrosio MR, Sapienza MR, Rossi M, De Falco G, Gibellini D, Tripodo C, Pileri SA, Leoncini L, Piccaluga PP. Molecular signature of Epstein Barr virus-positive Burkitt lymphoma and post-transplant lymphoproliferative disorder suggest different roles for Epstein Barr virus. Front Microbiol. 2014;5:728.PubMedPubMedCentralGoogle Scholar
  50. 50.
    Mundo L, Ambrosio MR, Picciolini M, Lo Bello G, Gazaneo S, Del Porro L, Lazzi S, Navari M, Onyango N, Granai M, Bellan C, De Falco G, Gibellini D, Piccaluga PP, Leoncini L. Unveiling another missing piece in EBV-driven lymphomagenesis: EBV-encoded MicroRNAs expression in EBER-negative Burkitt lymphoma cases. Front Microbiol. 2017;8:229.PubMedPubMedCentralGoogle Scholar
  51. 51.
    Vereide D, Sugden B. Proof for EBV’s sustaining role in Burkitt’s lymphomas. Semin Cancer Biol. 2009;19:389–93.PubMedPubMedCentralGoogle Scholar
  52. 52.
    Ambrosio MR, Rocca BJ, Ginori A, Mourmouras V, Amato T, Vindigni C, Lazzi S, Leoncini L. A look into the evolution of Epstein-Barr virus-induced lymphoproliferative disorders: a case study. Am J Clin Pathol. 2015;144(5):817–22.PubMedGoogle Scholar
  53. 53.
    Mannucci S, Luzzi A, Carugi A, Gozzetti A, Lazzi S, Malagnino V, Simmonds M, Cusi MG, Leoncini L, van den Bosch CA, De Falco G. Endemic Burkitt lymphoma. Adv Hematol. 2012;2012:149780.PubMedPubMedCentralGoogle Scholar
  54. 54.
    Bassan R, Maino E, Cortelazzo S. Lymphoblastic lymphoma: an updated review on biology, diagnosis, and treatment. Eur J Haematol. 2016;96(5):447–60. Review.PubMedGoogle Scholar
  55. 55.
    Paolini S, Gazzola A, Sabattini E, Bacci F, Pileri S, Piccaluga PP. Pathobiology of acute lymphoblastic leukemia. Semin Diagn Pathol. 2011;28(2):124–34.PubMedGoogle Scholar
  56. 56.
    Kratz CP, Stanulla M, Cavé H. Genetic predisposition to acute lymphoblastic leukemia: overview on behalf of the I-BFM ALL Host Genetic Variation Working Group. Eur J Med Genet. 2016;59(3):111–5. Review.PubMedGoogle Scholar
  57. 57.
    Cortelazzo S, Ferreri A, Hoelzer D, Ponzoni M. Lymphoblastic lymphoma. Crit Rev Oncol Hematol. 2017;113:304–17.PubMedGoogle Scholar
  58. 58.
    Geyer JT, Subramaniyam S, Jiang Y, Elemento O, Ferry JA, de Leval L, Nakashima MO, Liu YC, Martin P, Mathew S, Orazi A, Tam W. Lymphoblastic transformation of follicular lymphoma: a clinicopathologic and molecular analysis of 7 patients. Hum Pathol. 2015;46(2):260–71.PubMedGoogle Scholar
  59. 59.
    Oschlies I, Burkhardt B, Chassagne-Clement C, d’Amore ES, Hansson U, Hebeda K, Mc Carthy K, Kodet R, Maldyk J, Müllauer L, Porwit A, Schmatz AI, Tinguely M, Abramov D, Wotherspoon A, Zimmermann M, Reiter A, Klapper W. Diagnosis and immunophenotype of 188 pediatric lymphoblastic lymphomas treated within a randomized prospective trial: experiences and preliminary recommendations from the European childhood lymphoma pathology panel. Am J Surg Pathol. 2011;35(6):836–44.  https://doi.org/10.1097/PAS.0b013e318213e90e.
  60. 60.
    Burkhardt B, Bruch J, Zimmermann M, Strauch K, Parwaresch R, Ludwig WD, Harder L, Schlegelberger B, Mueller F, Harbott J, Reiter A. Loss of heterozygosity on chromosome 6q14-q24 is associated with poor outcome in children and adolescents with T-cell lymphoblastic lymphoma. Leukemia. 2006;20:1422–9.PubMedGoogle Scholar
  61. 61.
    Burkhardt B. Paediatric lymphoblastic T-cell leukaemia and lymphoma: one or two diseases? Br J Haematol. 2010;149:653–68.PubMedGoogle Scholar
  62. 62.
    Lones MA, Heerema NA, Le Beau MM, Sposto R, Perkins SL, Kadin ME, Kjeldsberg CR, Meadows A, Siegel S, Buckley J, Abromowitch M, Kersey J, Bergeron S, Cairo MS, Sanger WG. Chromosome abnormalities in advanced stage lymphoblastic lymphoma of children and adolescents: a report from CCG-E08. Cancer Genet Cytogenet. 2007;172:1–11.PubMedGoogle Scholar
  63. 63.
    Sekimizu M, Sunami S, Nakazawa A, Hayashi Y, Okimoto Y, Saito AM, Horibe K, Tsurusawa M, Mori T. Chromosome abnormalities in advanced stage T-cell lymphoblastic lymphoma of children and adolescents: a report from Japanese Paediatric Leukaemia/Lymphoma Study Group (JPLSG) and review of the literature. Br J Haematol. 2011;154(5):612–7.PubMedGoogle Scholar
  64. 64.
    Uyttebroeck A, Vanhentenrijk V, Hagemeijer A, Boeckx N, Renard M, Wlodarska I, Vandenberghe P, Depaepe P, De Wolf-Peeters C. Is there a difference in childhood T-cell acute lymphoblastic leukaemia and T-cell lymphoblastic lymphoma? Leuk Lymphoma. 2007;48:1745–54.PubMedGoogle Scholar
  65. 65.
    You MJ, Medeiros LJ, Hsi ED. T-lymphoblastic leukemia/lymphoma. Am J Clin Pathol. 2015;144(3):411–22.PubMedGoogle Scholar
  66. 66.
    Baleydier F, Decouvelaere AV, Bergeron J, Gaulard P, Canioni D, Bertrand Y, Lepretre S, Petit B, Dombret H, Beldjord K, Molina T, Asnafi V, Macintyre E. T cell receptor genotyping and HOXA/TLX1 expression define three T lymphoblastic lymphoma subsets which might affect clinical outcome. Clin Cancer Res. 2008;14(3):692–700.PubMedGoogle Scholar
  67. 67.
    Kaneko Y, Frizzera G, Maseki N, Sakurai M, Komada Y, Hiyoshi Y, Nakadate H, Takeda T. A novel translocation, t(9;17)(q34;q23), in aggressive childhood lymphoblastic lymphoma. Leukemia. 1998;2:745–8.Google Scholar
  68. 68.
    Schraders M, Van Reijmersdal SV, Kamping EJ, Van Krieken JH, Van Kessel AG, Groenen PJ, Hoogerbrugge PM, Kuiper RP. High-resolution genomic profiling of pediatric lymphoblastic lymphomas reveals subtle differences with pediatric acute lymphoblastic leukemias in the B-lineage. Cancer Genet Cytogenet. 2009;191:27–33.PubMedGoogle Scholar
  69. 69.
    Bonn BR, Rohde M, Zimmermann M, Krieger D, Oschlies I, Niggli F, et al. Incidence and prognostic relevance of genetic variations in T-cell lymphoblastic lymphoma in childhood and adolescence. Blood. 2013;121:3153–60.PubMedGoogle Scholar
  70. 70.
    Weng AP, Ferrando AA, Lee W, et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science. 2004;306(5694):269–71.PubMedGoogle Scholar
  71. 71.
    Bonn BR, Huge A, Rohde M, Oschlies I, Klapper W, Voss R, Makarova O, Rossig C, Jürgens H, Seggewiss J, Burkhardt B. Whole exome sequencing hints at a unique mutational profile of paediatric T-cell lymphoblastic lymphoma. Br J Haematol. 2015;168(2):308–13.PubMedGoogle Scholar
  72. 72.
    Raetz EA, Perkins SL, Bhojwani D, Smock K, Philip M, Carroll WL, et al. Gene expression profiling reveals intrinsic differences between T-cell acute lymphoblastic leukemia and T-cell lymphoblastic lymphoma. Pediatr Blood Cancer. 2006;47:130–40.PubMedGoogle Scholar
  73. 73.
    Basso K, Mussolin L, Lettieri A, Brahmachary M, Lim WK, Califano A, et al. T-cell lymphoblastic lymphoma shows differences and similarities with T-cell acute lymphoblastic leukemia by genomic and gene expression analyses. Genes Chromosomes Cancer. 2011;50:1063–75.PubMedGoogle Scholar
  74. 74.
    Crazzolara R, Kreczy A, Mann G, et al. High expression of the chemokine receptor CXCR4 predicts extramedullary organ infiltration in childhood acute lymphoblastic leukaemia. Br J Haematol. 2001;115(3):545–53.PubMedGoogle Scholar
  75. 75.
    Herold T, Gökbuget N. Philadelphia-like acute lymphoblastic leukemia in adults. Curr Oncol Rep. 2017;19(5):31.  https://doi.org/10.1007/s11912-017-0589-2. Review.PubMedGoogle Scholar
  76. 76.
    Agirre X, Martínez-Climent JA, Odero MD, Prósper F. Epigenetic regulation of miRNA genes in acute leukemia. Leukemia. 2012;26(3):395–403.PubMedGoogle Scholar
  77. 77.
    Yeh CH, Moles R, Nicot C. Clinical significance of microRNAs in chronic and acute human leukemia. Mol Cancer. 2016;15(1):37.PubMedPubMedCentralGoogle Scholar
  78. 78.
    Fulci V, et al. Characterization of B- and T-lineage acute lymphoblastic leukemia by integrated analysis of MicroRNA and mRNA expression profiles. Genes Chromosomes Cancer. 2009;48(12):1069–82.PubMedGoogle Scholar
  79. 79.
    Luan C, Yang Z, Chen B. The functional role of microRNA in acute lymphoblastic leukemia: relevance for diagnosis, differential diagnosis, prognosis, and therapy. Onco Targets Ther. 2015;8:2903–14.PubMedPubMedCentralGoogle Scholar
  80. 80.
    Schotte D, et al. MicroRNA characterize genetic diversity and drug resistance in pediatric acute lymphoblastic leukemia. Haematologica. 2011;96(5):703–11.PubMedPubMedCentralGoogle Scholar
  81. 81.
    Nemes K, et al. Expression of certain leukemia/lymphoma related microRNAs and its correlation with prognosis in childhood acute lymphoblastic leukemia. Pathol Oncol Res. 2015;21(3):597–604.PubMedGoogle Scholar
  82. 82.
    Rainer J, et al. Glucocorticoid-regulated microRNAs and mirtrons in acute lymphoblastic leukemia. Leukemia. 2009;23(4):746–52.PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Hélène A. Poirel
    • 1
  • Maria Raffaella Ambrosio
    • 2
  • Pier Paolo Piccaluga
    • 3
  • Lorenzo Leoncini
    • 2
  1. 1.Belgian Cancer Registry and GenHAPBrusselsBelgium
  2. 2.Section of Pathology, Department of Medical BiotechnologyUniversity of SienaSienaItaly
  3. 3.Department of Experimental, Diagnostic, and Specialty MedicineUniversity of BolognaBolognaItaly

Personalised recommendations