Histological Transformation and Progression in Follicular Lymphoma: A Clonal Evolution Study

1. A clinical evaluation of the International Lymphoma Study Group classification of non-Hodgkin’s lymphoma. The Non-Hodgkin’s Lymphoma Classification Project. Blood. 1997;89(11):3909–18. 9166827

2. Anderson JR, Armitage JO, Weisenburger DD. Epidemiology of the non-Hodgkin’s lymphomas: distributions of the major subtypes differ by geographic locations. Non-Hodgkin’s Lymphoma Classification Project. Ann Oncol. 1998;9(7):717–20. 9739436

3. Bachy E, Houot R, Morschhauser F, Sonet A, Brice P, Belhadj K, et al. Long-term follow up of the FL2000 study comparing CHVP-interferon to CHVP-interferon plus rituximab in follicular lymphoma. Haematologica. 2013;98(7):1107–14. doi: 10.3324/haematol.2012.082412 23645690

4. Tan D, Horning SJ, Hoppe RT, Levy R, Rosenberg SA, Sigal BM, et al. Improvements in observed and relative survival in follicular grade 1–2 lymphoma during 4 decades: the Stanford University experience. Blood. 2013;122(6):981–7. doi: 10.1182/blood-2013-03-491514 23777769

5. Junlen HR, Peterson S, Kimby E, Lockmer S, Linden O, Nilsson-Ehle H, et al. Follicular lymphoma in Sweden: nationwide improved survival in the rituximab era, particularly in elderly women—a Swedish Lymphoma Registry study. Leukemia. 2014;29(3):668–76. doi: 10.1038/leu.2014.251 25151959

6. Montoto S, Davies AJ, Matthews J, Calaminici M, Norton AJ, Amess J, et al. Risk and clinical implications of transformation of follicular lymphoma to diffuse large B-cell lymphoma. J Clin Oncol. 2007;25(17):2426–33. doi: 10.1200/JCO.2006.09.3260 17485708

7. Al-Tourah AJ, Gill KK, Chhanabhai M, Hoskins PJ, Klasa RJ, Savage KJ, et al. Population-based analysis of incidence and outcome of transformed non-Hodgkin’s lymphoma. J Clin Oncol. 2008;26(32):5165–9. doi: 10.1200/JCO.2008.16.0283 18838711

8. Link BK, Maurer MJ, Nowakowski GS, Ansell SM, Macon WR, Syrbu SI, et al. Rates and outcomes of follicular lymphoma transformation in the immunochemotherapy era: a report from the University of Iowa/MayoClinic Specialized Program of Research Excellence Molecular Epidemiology Resource. J Clin Oncol. 2013;31(26):3272–8. doi: 10.1200/JCO.2012.48.3990 23897955

9. Mozessohn L, Cheung MC, Crump M, Buckstein R, Berinstein N, Imrie K, et al. Chemoimmunotherapy resistant follicular lymphoma: predictors of resistance, association with transformation and prognosis. Leuk Lymphoma. 2014;55(11):2502–7. doi: 10.3109/10428194.2014.885513 24450580

10. Casulo C, Byrtek M, Dawson KL, Zhou X, Farber CM, Flowers CR, et al. Early relapse of follicular lymphoma after rituximab plus cyclophosphamide, doxorubicin, vincristine, and prednisone defines patients at high risk for death: an analysis from the National LymphoCare Study. J Clin Oncol. 2015;33(23):2516–22. doi: 10.1200/JCO.2014.59.7534 26124482

11. Lerch K, Meyer AH, Stroux A, Hirt C, Keller U, Viardot A, et al. Impact of prior treatment on outcome of transformed follicular lymphoma and relapsed de novo diffuse large B cell lymphoma: a retrospective multicentre analysis. Ann Hematol. 2015;94(6):981–8. doi: 10.1007/s00277-015-2303-5 25645656

12. Wagner-Johnston ND, Link BK, Byrtek M, Dawson KL, Hainsworth J, Flowers CR, et al. Outcomes of transformed follicular lymphoma in the modern era: a report from the National LymphoCare Study (NLCS). Blood. 2015;126(7):851–8. doi: 10.1182/blood-2015-01-621375 26105149

13. Jurinovic V, Kridel R, Staiger AM, Szczepanowski M, Horn H, Dreyling MH, et al. Clinicogenetic risk models predict early progression of follicular lymphoma after first-line immunochemotherapy. Blood. 2016;128(8):1112–20. doi: 10.1182/blood-2016-05-717355 27418643

14. Ding L, Ley TJ, Larson DE, Miller Ca, Koboldt DC, Welch JS, et al. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature. 2012;481(7382):506–10. doi: 10.1038/nature10738 22237025

15. Da Landau, Carter SL, Stojanov P, McKenna A, Stevenson K, Lawrence MS, et al. Evolution and impact of subclonal mutations in chronic lymphocytic leukemia. Cell. 2013;152(4):714–26. doi: 10.1016/j.cell.2013.01.019 23415222

16. Landau DA, Tausch E, Taylor-Weiner AN, Stewart C, Reiter JG, Bahlo J, et al. Mutations driving CLL and their evolution in progression and relapse. Nature. 2015;526(7574):525–30. doi: 10.1038/nature15395 26466571

17. Morrissy AS, Garzia L, Shih DJH, Zuyderduyn S, Huang X, Skowron P, et al. Divergent clonal selection dominates medulloblastoma at recurrence. Nature. 2016;529(7586):351–7. doi: 10.1038/nature16478 26760213

18. Walter MJ, Shen D, Ding L, Shao J, Koboldt DC, Chen K, et al. Clonal architecture of secondary acute myeloid leukemia. N Engl J Med. 2012;366(12):1090–8. doi: 10.1056/NEJMoa1106968 22417201

19. Fabbri G, Khiabanian H, Holmes AB, Wang J, Messina M, Mullighan CG, et al. Genetic lesions associated with chronic lymphocytic leukemia transformation to Richter syndrome. J Exp Med. 2013;210(11):2273–88. doi: 10.1084/jem.20131448 24127483

20. Okosun J, Bödör C, Wang J, Araf S, Yang CY, Pan C, et al. Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma. Nat Genet. 2014;46(2):176–81. doi: 10.1038/ng.2856 24362818

21. Pasqualucci L, Khiabanian H, Fangazio M, Vasishtha M, Messina M, Holmes A, et al. Genetics of follicular lymphoma transformation. Cell Rep. 2014;6(1):130–40. doi: 10.1016/j.celrep.2013.12.027 24388756

22. Yano T, Jaffe ES, Longo DL, Raffeld M. MYC rearrangements in histologically progressed follicular lymphomas. Blood. 1992;80(3):758–67. 1638027

23. Lossos IS, Alizadeh AA, Diehn M, Warnke R, Thorstenson Y, Oefner PJ, et al. Transformation of follicular lymphoma to diffuse large-cell lymphoma: alternative patterns with increased or decreased expression of c-myc and its regulated genes. Proc Natl Acad Sci U S A. 2002;99(13):8886–91. doi: 10.1073/pnas.132253599 12077300

24. Lo Coco F, Gaidano G, Louie DC, Offit K, Chaganti RS, Dalla-Favera R. p53 mutations are associated with histologic transformation of follicular lymphoma. Blood. 1993;82(8):2289–95. 8400281

25. Sander CA, Yano T, Clark HM, Harris C, Longo DL, Jaffe ES, et al. p53 mutation is associated with progression in follicular lymphomas. Blood. 1993;82(7):1994–2004. 8400252

26. Fitzgibbon J, Iqbal S, Davies A, O’Shea D, Carlotti E, Chaplin T, et al. Genome-wide detection of recurring sites of uniparental disomy in follicular and transformed follicular lymphoma. Leukemia. 2007;21(7):1514–20. doi: 10.1038/sj.leu.2404696 17495976

27. Davies AJ, Rosenwald A, Wright G, Lee A, Last KW, Weisenburger DD, et al. Transformation of follicular lymphoma to diffuse large B-cell lymphoma proceeds by distinct oncogenic mechanisms. Br J Haematol. 2007;136(2):286–93. doi: 10.1111/j.1365-2141.2006.06439.x 17278262

28. Carlotti E, Wrench D, Matthews J, Iqbal S, Davies A, Norton A, et al. Transformation of follicular lymphoma to diffuse large B-cell lymphoma may occur by divergent evolution from a common progenitor cell or by direct evolution from the follicular lymphoma clone. Blood. 2009;113(15):3553–7. doi: 10.1182/blood-2008-08-174839 19202129

29. O’Shea D, O’Riain C, Gupta M, Waters R, Yang Y, Wrench D, et al. Regions of acquired uniparental disomy at diagnosis of follicular lymphoma are associated with both overall survival and risk of transformation. Blood. 2009;113(10):2298–301. doi: 10.1182/blood-2008-08-174953 19141865

30. Yunis JJ, Frizzera G, Oken MM, McKenna J, Theologides A, Arnesen M. Multiple recurrent genomic defects in follicular lymphoma. A possible model for cancer. N Engl J Med. 1987;316(2):79–84. doi: 10.1056/NEJM198701083160204 3537802

31. Tilly H, Rossi A, Stamatoullas A, Lenormand B, Bigorgne C, Kunlin a, et al. Prognostic value of chromosomal abnormalities in follicular lymphoma. Blood. 1994;84(4):1043–9. 8049424

32. Höglund M, Sehn L, Connors JM, Gascoyne RD, Siebert R, Säll T, et al. Identification of cytogenetic subgroups and karyotypic pathways of clonal evolution in follicular lymphomas. Genes Chromosomes Cancer. 2004;39(3):195–204. doi: 10.1002/gcc.10314 14732921

33. O’Shea D, O’Riain C, Taylor C, Waters R, Carlotti E, Macdougall F, et al. The presence of TP53 mutation at diagnosis of follicular lymphoma identifies a high-risk group of patients with shortened time to disease progression and poorer overall survival. Blood. 2008;112(8):3126–9. doi: 10.1182/blood-2008-05-154013 18628487

34. D’Amore F, Chan E, Iqbal J, Geng H, Young K, Xiao L, et al. Clonal evolution in t(14;18)-positive follicular lymphoma, evidence for multiple common pathways, and frequent parallel clonal evolution. Clin Cancer Res. 2008;14(22):7180–7. doi: 10.1158/1078-0432.CCR-08-0752 19010834

35. Cheung KJJ, Shah SP, Steidl C, Johnson N, Relander T, Telenius A, et al. Genome-wide profiling of follicular lymphoma by array comparative genomic hybridization reveals prognostically significant DNA copy number imbalances. Blood. 2009;113(1):137–48. doi: 10.1182/blood-2008-02-140616 18703704

36. Alhejaily A, Day AG, Feilotter HE, Baetz TD, Lebrun DP. Inactivation of the CDKN2A tumor suppressor gene by deletion or methylation is common at diagnosis in follicular lymphoma and associated with poor clinical outcome. Clin Cancer Res. 2014;20(6):1676–86. doi: 10.1158/1078-0432.CCR-13-2175 24449825

37. Pastore A, Jurinovic V, Kridel R, Hoster E, Staiger AM, Szczepanowski M, et al. Integration of gene mutations in risk prognostication for patients receiving first-line immunochemotherapy for follicular lymphoma: a retrospective analysis of a prospective clinical trial and validation in a population-based registry. Lancet Oncol. 2015;2045(15):1–12.

38. Roth A, Khattra J, Yap D, Wan A, Laks E, Biele J, et al. PyClone: statistical inference of clonal population structure in cancer. Nat Methods. 2014;11(4):396–8. doi: 10.1038/nmeth.2883 24633410

39. Malikic S, McPherson AW, Donmez N, Sahinalp CS. Clonality inference in multiple tumor samples using phylogeny. Bioinformatics. 2015;31(9):1349–56. doi: 10.1093/bioinformatics/btv003 25568283

40. Muppidi JR, Schmitz R, Green JA, Xiao W, Larsen AB, Braun SE, et al. Loss of signalling via Gα13 in germinal centre B-cell-derived lymphoma. Nature. 2014;516(7530):254–8. doi: 10.1038/nature13765 25274307

41. Schiffels S, Szöllosi GJ, Mustonen V, Lässig M. Emergent neutrality in adaptive asexual evolution. Genetics. 2011;189(4):1361–75. doi: 10.1534/genetics.111.132027 21926305

42. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature. 2012;486(7403):346–52. doi: 10.1038/nature10983 22522925

43. Green MR, Monti S, Rodig SJ, Juszczynski P, Currie T, O’Donnell E, et al. Integrative analysis reveals selective 9p24.1 amplification, increased PD-1 ligand expression, and further induction via JAK2 in nodular sclerosing Hodgkin lymphoma and primary mediastinal large B-cell lymphoma. Blood. 2010;116(17):3268–77. doi: 10.1182/blood-2010-05-282780 20628145