Genetic alterations in B cell lymphoma subtypes as potential biomarkers for noninvasive diagnosis, prognosis, therapy, and disease monitoring
Genetic alterations in B cell lymphoma subtypes as potential biomarkers for noninvasive diagnosis, prognosis, therapy, and disease monitoring
Neoplastic transformation of germinal center B (GCB) cells may give rise to a variety of different B cell lymphoma subtypes,most of which show substantial heterogeneity in terms of genetic alterations and clinical features. The mutations observed in cancerrelated genes in GCB cells are related to abnormalities in the immunogenetic mechanisms associated with germinal center reaction.Recent studies have rapidly identified genomic alterations in B cell lymphomas that may be useful for better subclassification, noninvasivediagnosis, and prediction of response to therapy. The WHO recognizes different lymphoma subsets classified within 2 major categoriesof B cell lymphoma: Hodgkin’s lymphoma (HL) and B cell non-Hodgkin’s lymphoma (NHL), each with distinct genetic aberrations,including chromosomal translocations, copy number abnormalities, or point mutations. Next-generation sequencing-based technologieshave allowed cancer researchers to identify somatic mutations and gene expression signatures at a rapid pace so that novel diagnostic orprognostic biomarkers, as well as therapeutic targets, can be discovered much faster than before. Indeed, deep sequencing studies haverecently revealed that lymphoma-specific somatic mutations may be detected in cell-free circulating DNA obtained from the peripheralblood of B cell lymphoma patients, suggesting the possibility of minimally invasive diagnosis, monitoring, and predicting response totherapy of B cell lymphoma patients. In this study, the current status of the recurrent genetic aberrations observed during diagnosis and/or relapse in HL and the major subtypes of B cell NHL (i.e. diffuse large B cell lymphoma, follicular lymphoma, mantle cell lymphoma,and Burkitt lymphoma) are discussed to shed light on their potential use as noninvasive diagnostic or prognostic biomarkers and toreveal their role in lymphomagenesis as a target in therapy for newly diagnosed and chemotherapy-resistant cases.
___
- Agarwal R, Chan YC, Tam CS, Hunter T, Vassiliadis D et al. (2019).
Dynamic molecular monitoring reveals that SWI–SNF
mutations mediate resistance to ibrutinib plus venetoclax
in mantle cell lymphoma. Nature Medicine 25: 119-129. doi:
10.1038/s41591-018-0243-z
- Alcaide M, Yu S, Bushell K, Fornika D, Nielsen JS et al. (2016).
Multiplex droplet digital PCR quantification of recurrent
somatic mutations in diffuse large b-cell and follicular
lymphoma. Clinical Chemistry 62 (9): 1238-1247. doi: 10.1373/
clinchem.2016.255315
- Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS et al. (2000).
Distinct types of diffuse large B-cell lymphoma identified by
gene expression profiling. Nature 403 (6769): 503-511. doi:
10.1038/35000501
- Al-Tourah AJ, Gill KK, Chhana Bhai M, Hoskins PJ, Klasa RJ et al.
(2008). Population-based analysis of incidence and outcome
of transformed non-Hodgkin’s lymphoma. Journal of Clinical
Oncology 26 (32): 5165-5169. doi: 10.1200/JCO.2008.16.0283
- Andor N, Simonds EF, Czerwinski DK, Chen J, Grimes SM et al.
(2019). Single-cell RNA-Seq of follicular lymphoma reveals
malignant B-cell types and coexpression of T-cell immune
checkpoints. Blood 133 (10): 1119-1129. doi: 10.1182/
blood-2018-08-862292
- Barth TFE, Martin-Subero JI, Joos S, Menz CK, Hasel C et al. (2003).
Gains of 2p involving the REL locus correlate with nuclear
c-Rel protein accumulation in neoplastic cells of classical
Hodgkin lymphoma. Blood 101 (9): 3681-3686. doi: 10.1182/
blood-2002-08-2577
- Beà S, Valdés-Mas R, Navarro A, Salaverria I, Martín-Garcia D et al.
(2013). Landscape of somatic mutations and clonal evolution in
mantle cell lymphoma. Proceedings of the National Academy
of Sciences of the United States of America 110 (45): 18250-
18255. doi: 10.1073/pnas.1314608110
- Bevan MJ (2004). Helping the CD8(+) T-cell response. Nature
Reviews Immunology 4 (8): 595-602. doi: 10.1038/nri1413
- Bouska A, McKeithan TW, Deffenbacher KE, Lachel C, Wright
GW et al. (2014). Genome-wide copy-number analyses
reveal genomic abnormalities involved in transformation of
follicular lymphoma. Blood 123: 1681-1690. doi: 10.1182/
blood-2013-05-500595
- Bouska A, Zhang W, Gong Q, Iqbal J, Scuto A et al. (2017). Combined
copy number and mutation analysis identifies oncogenic
pathways associated with transformation of follicular
lymphoma. Leukemia 31: 83-91. doi: 10.1038/leu.2016.175
- Capaccioli S, Quattrone A, Schiavone N, Calastretti A, Copreni E et
al. (1996). A bcl-2/IgH antisense transcript deregulates bcl-2
gene expression in human follicular lymphoma t(14;18) cell
lines. Oncogene 13 (1): 105-115.
- Compagno M, Lim WK, Grunn A, Nandula SV, Brahmachary M
et al. (2009). Mutations of multiple genes cause deregulation
of NF-kappaB in diffuse large B-cell lymphoma. Nature 459
(7247): 717-721. doi: 10.1038/nature07968
- Correia C, Schneider PA, Dai H, Dogan A, Maurer MJ et al.
(2015). BCL2 mutations are associated with increased risk of
transformation and shortened survival in follicular lymphoma.
Blood 125 (4): 658-667. doi: 10.1182/blood-2014-04-571786
- Cortelazzo S, Ponzoni M, Ferreri AJM, Dreyling M (2012). Mantle
cell lymphoma. Critical Reviews in Oncology/Hematology 82
(1): 78-101. doi: 10.1016/j.critrevonc.2011.05.001
- Crowley E, Di Nicolantonio F, Loupakis F, Bardelli A (2013). Liquid
biopsy: monitoring cancer-genetics in the blood. Nature
Reviews Clinical Oncology 10 (8): 472-484. doi: 10.1038/
nrclinonc.2013.110
- Davids MS, Roberts AW, Seymour JF, Pagel JM, Kahl BS et al.
(2017). Phase I first-in-human study of venetoclax in patients
with relapsed or refractory non-Hodgkin lymphoma.
Journal of Clinical Oncology 35 (8): 826-833. doi: 10.1200/
JCO.2016.70.4320
- Davis RE, Brown KD, Siebenlist U, Staudt LM (2001). Constitutive
nuclear factor kappaB activity is required for survival of
activated B cell-like diffuse large B cell lymphoma cells. Journal
of Experimental Medicine 194 (12): 1861-1874. doi: 10.1084/
jem.194.12.1861
- Davis RE, Ngo VN, Lenz G, Tolar P, Young RM et al. (2010).
Chronic active B-cell-receptor signalling in diffuse large
B-cell lymphoma. Nature 463 (7277): 88-92. doi: 10.1038/
nature08638
- Deffenbacher KE, Iqbal J, Sanger W, Shen Y, Lachel C et al.
(2012). Molecular distinctions between pediatric and adult
mature B-cell non-Hodgkin lymphomas identified through
genomic profiling. Blood 119 (16): 3757-3766. doi: 10.1182/
blood-2011-05-349662
- Delfau-Larue MH, van der Gucht A, Dupuis J, Jais JP, Nel I et al.
(2018). Total metabolic tumor volume, circulating tumor
cells, cell-free DNA: distinct prognostic value in follicular
lymphoma. Blood Advances 2: 871-876. doi: 10.1182/
bloodadvances.2017015164
- Dubois S, Jardin F (2018). Novel molecular classifications of DLBCL.
Nature Reviews Clinical Oncology 15 (8): 474-476. doi:
10.1038/s41571-018-0041-z
- Einerson RR, Kurtin PJ, Dayharsh GA, Kimlinger TK, Remstein ED
(2005). FISH is superior to PCR in detecting t(14;18)(q32;q21)-
IgH/bcl-2 in follicular lymphoma using paraffin-embedded
tissue samples. American Journal of Clinical Pathology 24 (3):
421-429. doi: 10.1309/BLH8-MMK8-5UBQ-4K6R
- Eskelund CW, Dahl C, Hansen JW, Westman M, Kolstad A et
al. (2017). TP53 mutations identify younger mantle cell
lymphoma patients who do not benefit from intensive
chemoimmunotherapy. Blood 130 (17): 1903-1910. doi:
10.1182/blood-2017-04-779736
- Falini B, Flenghi L, Aversa F, Barbabietola G, Martelli MF et al. (1992).
Response of refractory Hodgkin’s disease to monoclonal antiCD30 immunotoxin. Lancet 339 (8803): 1195-1196. doi:
10.1016/0140-6736(92)91135-U
- Farrell K, Jarrett RF (2011). The molecular pathogenesis of Hodgkin
lymphoma. Histopathology 58 (1): 15-25. doi: 10.1111/j.1365-
2559.2010.03705.x
- Fernàndez V, Salamero O, Espinet B, Solé F, Royo C et al. (2010).
Genomic and gene expression profiling defines indolent forms
of mantle cell lymphoma. Cancer Research 70 (4): 1408-1418.
doi: 10.1158/0008-5472.CAN-09-3419
- Gaidano G, Ballerini P, Gong JZ, Inghirami G, Neri A et al. (1991).
p53 mutations in human lymphoid malignancies: association
with Burkitt lymphoma and chronic lymphocytic leukemia.
Proceedings of the National Academy of Sciences of the
United States of America 88 (12): 5413-5417. doi: 10.1073/
pnas.88.12.5413
- Grande BM, Gerhard DS, Jiang A, Griner NB, Abramson JS et
al. (2019). Genome-wide discovery of somatic coding and
noncoding mutations in pediatric endemic and sporadic
Burkitt lymphoma. Blood 133 (12): 1313-1324. doi: 10.1182/
blood-2018-09-871418
- Greiner TC, Moynihan MJ, Chan WC, Lytle DM, Pedersen A et al.
(1996). p53 mutations in mantle cell lymphoma are associated
with variant cytology and predict a poor prognosis. Blood 87
(10): 4302-4310.
- Halldórsdóttir AM, Lundin A, Murray F, Mansouri L, Knuutila S et
al. (2011). Impact of TP53 mutation and 17p deletion in mantle
cell lymphoma. Leukemia 25 (12): 1904-1908. doi: 10.1038/
leu.2011.162
- Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J
et al. (2004). Confirmation of the molecular classification of
diffuse large B-cell lymphoma by immunohistochemistry
using a tissue microarray. Blood 103 (1): 275-282. doi: 10.1182/
blood-2003-05-1545
- Hoster E, Dreyling M, Klapper W, Gisselbrecht C, van Hoof A et
al. (2008). A new prognostic index (MIPI) for patients with
advanced-stage mantle cell lymphoma. Blood 111 (2): 558-565.
doi: 10.1182/blood-2007-06-095331
- Hu S, Xu-Monette ZY, Tzankov A, Green T, Wu L et al. (2013).
MYC/BCL2 protein coexpression contributes to the inferior
survival of activated B-cell subtype of diffuse large B-cell
lymphoma and demonstrates high-risk gene expression
signatures: a report from the International DLBCL RituximabCHOP Consortium Program. Blood 121 (20): 4021-4031. doi:
10.1182/blood-2012-10-460063
- Hu X, Baytak E, Li J, Akman B, Okay K et al. (2017). The relationship
of REL proto-oncogene to pathobiology and chemoresistance
in follicular and transformed follicular lymphoma. Leukemia
Research 54: 30-38. doi: 10.1016/j.leukres.2017.01.001
- Hüllein J, Słabicki M, Rosolowski M, Jethwa A, Habringer S et al.
(2019). MDM4Is targeted by 1q gain and drives disease in
Burkitt lymphoma. Cancer Research 79 (12): 3125-3138. doi:
10.1158/0008-5472.CAN-18-3438
- Ichikawa A, Kinoshita T, Watanabe T, Kato H, Nagai H et al. (1997).
Mutations of the p53 gene as a prognostic factor in aggressive
B-cell lymphoma. New England Journal of Medicine 337 (8):
529-534. doi: 10.1056/NEJM199708213370804
- Italiano A, Soria JC, Toulmonde M, Michot JM, Lucchesi C et al. (2018).
Tazemetostat, an EZH2 inhibitor, in relapsed or refractory B-cell
non-Hodgkin lymphoma and advanced solid tumours: a firstin-human, open-label, phase 1 study. Lancet Oncology 19 (5):
649-659. doi: 10.1016/S1470-2045(18)30145-1
- Jain N, Hartert K, Tadros S, Fiskus W, Havranek O et al. (2019).
Targetable genetic alterations of TCF4 ( E2-2 ) drive
immunoglobulin expression in diffuse large B cell lymphoma.
Science Translational Medicine 11 (497): eaav5599. doi: 10.1126/
scitranslmed.aav5599
- Joos S, Falk MH, Lichter P, Haluska FG, Henglein B et al. (1992).
Variable breakpoints in Burkitt lymphoma cells with
chromosomal t(8;14) translocation separate c-myc and the IgH
locus up to several hundred kb. Human Molecular Genetics 1
(8): 625-632. doi: 10.1093/hmg/1.8.625
- Juskevicius D, Jucker D, Klingbiel D, Mamot C, Dirnhofer S et al.
(2017). Mutations of CREBBP and SOCS1 are independent
prognostic factors in diffuse large B cell lymphoma: mutational
analysis of the SAKK 38/07 prospective clinical trial cohort.
Journal of Hematology & Oncology 10 (1): 70. doi: 10.1186/
s13045-017-0438-7
- Kanzler H, Küppers R, Hansmann ML, Rajewsky K (1996). Hodgkin
and Reed-Sternberg cells in Hodgkin’s disease represent the
outgrowth of a dominant tumor clone derived from (crippled)
germinal center B cells. Journal of Experimental Medicine 184
(4): 1495-1505. doi: 10.1084/jem.184.4.1495
- Kridel R, Meissner B, Rogic S, Boyle M, Telenius A et al. (2012).
Whole transcriptome sequencing reveals recurrent NOTCH1
mutations in mantle cell lymphoma. Blood 119 (9): 1963-1971.
doi: 10.1182/blood-2011-11-391474
- Kridel R, Sehn LH, Gascoyne RD (2012). Pathogenesis of follicular
lymphoma. Journal of Clinical Investigation 122 (10): 3424-
3431. doi: 10.1172/JCI63186
- Küppers R (2005). Mechanisms of B-cell lymphoma pathogenesis.
Nature Reviews Cancer 5 (4): 251-262. doi: 10.1038/nrc1589
- Küppers R (2009). The biology of Hodgkin’s lymphoma. Nature
Reviews Cancer 9 (1): 15-27. doi: 10.1038/nrc2542
- Kurşun D, Küçük C (2019). Systematic analysis of the frequently
amplified 2p15-p16.1 locus reveals PAPOLG as a potential protooncogene in follicular and transformed follicular lymphoma.
Turkish Journal of Biology 43: 124-132. doi: 10.3906/biy-1810-2
- Kurtz DM, Scherer F, Jin MC, Soo J, Craig AFM et al. (2018).
Circulating tumor DNA measurements as early outcome
predictors in diffuse large B-cell lymphoma. Journal of Clinical
Oncology 36: 2845-2853. doi: 10.1200/JCO.2018.78.5246
- Laursen MB, Reinholdtz L, Schönherz AA, Due H, Jespersen DS et
al. (2019). High CXCR4 expression impairs rituximab response
and the prognosis of R-CHOP-treated diffuse large B-cell
lymphoma patients. Oncotarget 10 (7): 717-731. doi: 10.18632/
oncotarget.26588
- Lenz G, Davis RE, Ngo VN, Lam L, George TC et al. (2008). Oncogenic
CARD11 mutations in human diffuse large B cell lymphoma.
Science 319 (5870): 1676-1679. doi: 10.1126/science.1153629
- Lenz G, Nagel I, Siebert R, Roschke AV, Sanger W et al. (2007).
Aberrant immunoglobulin class switch recombination and
switch translocations in activated B cell-like diffuse large B cell
lymphoma. Journal of Experimental Medicine 204 (3): 633-
643. doi: 10.1084/jem.20062041
- Lenz G, Wright GW, Emre NCT, Kohlhammer H, Dave SS et al.
(2008). Molecular subtypes of diffuse large B-cell lymphoma
arise by distinct genetic pathways. Proceedings of the National
Academy of Sciences of the United States of America 105 (36):
13520-13525. doi: 10.1073/pnas.0804295105
- Liu YY, Leboeuf C, Shi JY, Li JM, Wang L et al. (2007). Rituximab plus
CHOP (R-CHOP) overcomes PRDM1-associated resistance to
chemotherapy in patients with diffuse large B-cell lymphoma.
Blood 110 (1): 339-344. doi: 10.1182/blood-2006-09-049189
- Lo Coco F, Gaidano G, Louie DC, Offit K, Chaganti RS et al. (1993).
p53 mutations are associated with histologic transformation of
follicular lymphoma. Blood 82 (8): 2289-2295.
- Lossos IS, Gascoyne RD (2011). Transformation of follicular
lymphoma. Best Practice & Research: Clinical Haematology
24: 147-163. doi: 10.1016/j.beha.2011.02.006
- Love C, Sun Z, Jima D, Li G, Zhang J et al. (2012). The genetic
landscape of mutations in Burkitt lymphoma. Nature Genetics
44 (12): 1321-1325. doi: 10.1038/ng.2468
- Matolcsy A, Casali P, Warnke RA, Knowles DM (1996). Morphologic
transformation of follicular lymphoma is associated with
somatic mutation of the translocated Bcl-2 gene. Blood 88 (10):
3937-3944.
- Minard-Colin V, Brugières L, Reiter A, Cairo MS, Gross TG et al.
(2015). Non-Hodgkin lymphoma in children and adolescents:
progress through effective collaboration, current knowledge,
and challenges ahead. Journal of Clinical Oncology 33 (27):
2963-2974. doi: 10.1200/JCO.2014.59.5827
- Mohanty A, Sandoval N, Das M, Pillai R, Chen L et al. (2016).
CCND1 mutations increase protein stability and promote
ibrutinib resistance in mantle cell lymphoma. Oncotarget 7
(45): 73558-73572. doi: 10.18632/oncotarget.12434
- Monteil M, Callanan M, Dascalescu C, Sotto JJ, Leroux D (1996).
Molecular diagnosis of t(11;14) in mantle cell lymphoma
using two-colour interphase fluorescence in situ hybridization.
British Journal of Haematology 93 (3): 656-660. doi: 10.1046/
j.1365-2141.1996.d01-1675.x
- Morin RD, Johnson NA, Severson TM, Mungall AJ, An J et al. (2010).
Somatic mutations altering EZH2 (Tyr641) in follicular and
diffuse large B-cell lymphomas of germinal-center origin.
Nature Genetics 42 (2): 181-185. doi: 10.1038/ng.518
- Mounier N, Briere J, Gisselbrecht C, Emile JF, Lederlin P et al. (2003).
Rituximab plus CHOP (R-CHOP) overcomes bcl-2-associated
resistance to chemotherapy in elderly patients with diffuse
large B-cell lymphoma (DLBCL). Blood 101 (11): 4279-4284.
doi: 10.1182/blood-2002-11-3442
- Ngo VN, Young RM, Schmitz R, Jhavar S, Xiao W et al. (2011).
Oncogenically active MYD88 mutations in human lymphoma.
Nature 470 (7332): 115-119. doi: 10.1038/nature09671
- O’Hayre M, Inoue A, Kufareva I, Wang Z, Mikelis CM et al. (2016).
Inactivating mutations in GNA13 and RHOA in Burkitt’s
lymphoma and diffuse large B-cell lymphoma: a tumor
suppressor function for the Gα13/RhoA axis in B cells.
Oncogene 35 (29): 3771-3780. doi: 10.1038/onc.2015.442
- Okosun J, Bödör C, Wang J, Araf S, Yang CY et al. (2014). Integrated
genomic analysis identifies recurrent mutations and evolution
patterns driving the initiation and progression of follicular
lymphoma. Nature Genetics 46 (2): 176-181. doi: 10.1038/
ng.2856
- Pasqualucci L, Migliazza A, Basso K, Houldsworth J, Chaganti RSK
et al. (2003). Mutations of the BCL6 proto-oncogene disrupt
its negative autoregulation in diffuse large B-cell lymphoma.
Blood 101 (8): 2914-2923. doi: 10.1182/blood-2002-11-3387
- Pastore A, Jurinovic V, Kridel R, Hoster E, Staiger AM et al.
(2015). 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 Oncology 16 (9): 1111-1122. doi: 10.1016/S1470-
2045(15)00169-2
- Piccaluga PP, De Falco G, Kustagi M, Gazzola A, Agostinelli C et
al. (2011). Gene expression analysis uncovers similarity and
differences among Burkitt lymphoma subtypes. Blood 117
(13): 3596-3608. doi: 10.1182/blood-2010-08-301556
- Portis T, Dyck P, Longnecker R (2003). Epstein-Barr virus (EBV)
LMP2A induces alterations in gene transcription similar to
those observed in Reed-Sternberg cells of Hodgkin lymphoma.
Blood 102 (12): 4166-4178. doi: 10.1182/blood-2003-04-1018
- Quesada AE, Medeiros LJ, Desai PA, Lin P, Westin JR et al. (2017).
Increased MYC copy number is an independent prognostic
factor in patients with diffuse large B-cell lymphoma. Modern
Pathology 30 (12): 1688-1697. doi: 10.1038/modpathol.2017.93
- Rossi D, Diop F, Spaccarotella E, Monti S, Zanni M et al. (2017). Diffuse
large B-cell lymphoma genotyping on the liquid biopsy. Blood
129 (14): 1947-1957. doi: 10.1182/blood-2016-05-719641
- Schaffner C, Idler I, Stilgenbauer S, Döhner H, Lichter P (2000).
Mantle cell lymphoma is characterized by inactivation of the
ATM gene. Proceedings of the National Academy of Sciences
of the United States of America 97 (6): 2773-2778. doi: 10.1073/
pnas.050400997
- Schmitz R, Wright GW, Huang DW, Johnson CA, Phelan JD et al.
(2018). Genetics and pathogenesis of diffuse large B-cell
lymphoma. New England Journal of Medicine 378 (15): 1396-
1407. doi: 10.1056/NEJMoa1801445
- Schmitz R, Young RM, Ceribelli M, Jhavar S, Xiao W et al. (2012).
Burkitt lymphoma pathogenesis and therapeutic targets from
structural and functional genomics. Nature 490 (7418): 116-
120. doi: 10.1038/nature11378
- Schnell R, Staak O, Borchmann P, Schwartz C, Matthey B et al. (2002).
A phase I study with an anti-CD30 ricin a-chain immunotoxin
(ki-4.dgA) in patients with refractory CD30+ Hodgkin’s and
non-Hodgkin’s lymphoma. Clinical Cancer Research 8 (6):
1779-1786.
- Schuetz JM, Johnson NA, Morin RD, Scott DW, Tan K et al. (2012).
BCL2 mutations in diffuse large B-cell lymphoma. Leukemia
26 (6): 1383-1390. doi: 10.1038/leu.2011.378
- Shanbhag S, Ambinder RF (2018). Hodgkin lymphoma: A review
and update on recent progress. CA: A Cancer Journal for
Clinicians 68 (2): 116-132. doi: 10.3322/caac.21438
- Shankland KR, Armitage JO, Hancock BW (2012). Non-Hodgkin
lymphoma. Lancet 380 (9844): 848-857. doi: 10.1016/S0140-
6736(12)60605-9
- Shannon-Lowe C, Rickinson AB, Bell AI (2017). Epstein–Barr virusassociated lymphomas. Philosophical Transactions of the
Royal Society B Biological Sciences 372 (1732): 20160271. doi:
10.1098/rstb.2016.0271.
- Siebert R, Matthiesen P, Harder S, Zhang Y, Borowski A et al. (1998).
Application of interphase fluorescence in situ Hybridization
for the detection of the Burkitt translocation t(8;14)(q24;q32)
in B-cell lymphomas. Blood 91 (3): 984-990.
- Slifka MK, Antia R, Whitmire JK, Ahmed R (1998). Humoral
immunity due to long-lived plasma cells. Immunity 8 (3): 363-
372.
- Spina V, Bruscaggin A, Cuccaro A, Martini M, Trani M Di et al. (2018).
Circulating tumor DNA reveals genetics, clonal evolution, and
residual disease in classical Hodgkin lymphoma. Blood 131
(22): 2413-2425. doi: 10.1182/blood-2017-11-812073
- Swerdlow SH, Campo E, Pileri SA, Harris NL, Stein H et al.
(2016). The 2016 revision of the World Health Organization
classification of lymphoid neoplasms. Blood 127 (20): 2375-
2390. doi: 10.1182/blood-2016-01-643569
- Tiacci E, Ladewig E, Schiavoni G, Penson A, Fortini E et al. (2018).
Pervasive mutations of JAK-STAT pathway genes in classical
Hodgkin lymphoma. Blood 131 (22): 2454-2465. doi: 10.1182/
blood-2017-11-814913
- Tsujimoto Y, Finger LR, Yunis J, Nowell PC, Croce CM (1984).
Cloning of the chromosome breakpoint of neoplastic B cells
with the t(14;18) chromosome translocation. Science 226
(4678): 1097-1099. doi: 10.1126/science.6093263
- Vaandrager JW, Schuuring E, Raap T, Philippo K, Kleiverda K et al.
(2000). Interphase FISH detection of BCL2 rearrangement in
follicular lymphoma using breakpoint-flanking probes. Genes
Chromosomes Cancer 27 (1): 85-94.
- Van den Neste E, André M, Gastinne T, Stamatoullas A, Haioun
C et al. (2018). A phase II study of the oral JAK1/JAK2
inhibitor ruxolitinib in advanced relapsed/refractory Hodgkin
lymphoma. Haematologica 103 (5): 840-848. doi: 10.3324/
haematol.2017.180554
- Van Gijn J, Gijselhart JP (2012). Thomas Hodgkin and his disease.
Nederlands Tijdschrift voor Geneeskunde 156 (15): A4332.
- Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S (2008).
Functions of natural killer cells. Nature Immunology 9 (5):
503-510. doi: 10.1038/ni1582.
- Weniger MA, Küppers R (2016). NF-κB deregulation in Hodgkin
lymphoma. Seminars in Cancer Biology 39: 32-39. doi:
10.1016/j.semcancer.2016.05.001.
- Weniger MA, Melzner I, Menz CK, Wegener S, Bucur AJ et al. (2006).
Mutations of the tumor suppressor gene SOCS-1 in classical
Hodgkin lymphoma are frequent and associated with nuclear
phospho-STAT5 accumulation. Oncogene 25 (18): 2679-2684.
doi: 10.1038/sj.onc.1209151.
- Weniger MA, Tiacci E, Schneider S, Arnolds J, Rüschenbaum S et al.
(2018). Human CD30+ B cells represent a unique subset related
to Hodgkin lymphoma cells. Journal of Clinical Investigation
128 (7): 2996-3007. doi: 10.1172/JCI95993
- Wiestner A, Tehrani M, Chiorazzi M, Wright G, Gibellini F et al.
(2007). Point mutations and genomic deletions in CCND1
create stable truncated cyclin D1 mRNAs that are associated
with increased proliferation rate and shorter survival. Blood
109 (11): 4599-4606. doi: 10.1182/blood-2006-08-039859
- Willis TG, Dyer MJ (2000). The role of immunoglobulin
translocations in the pathogenesis of B-cell malignancies.
Blood 96 (3): 808-822.
- Wilson WH, Young RM, Schmitz R, Yang Y, Pittaluga S et al. (2015).
Targeting B cell receptor signaling with ibrutinib in diffuse
large B cell lymphoma. Nature Medicine 21: 922-926. doi:
10.1038/nm.3884
- Wlodarska I, Nooyen P, Maes B, Martin-Subero JI, Siebert R et al.
(2003). Frequent occurrence of BCL6 rearrangements in
nodular lymphocyte predominance Hodgkin lymphoma but
not in classical Hodgkin lymphoma. Blood 101 (2): 706-710.
doi: 10.1182/blood-2002-05-1592
- Wu C, de Miranda NF, Chen L, Wasik AM, Mansouri L et al.
(2016). Genetic heterogeneity in primary and relapsed mantle
cell lymphomas: impact of recurrent CARD11 mutations.
Oncotarget 7: 38180-38190. doi: 10.18632/oncotarget.9500
- Xu P, Liu X, Ouyang J, Chen B (2017). TP53 mutation predicts the
poor prognosis of non-Hodgkin lymphomas: evidence from
a meta-analysis. PLoS One 12 (4): e0174809. doi: 10.1371/
journal.pone.0174809
- Yap DB, Chu J, Berg T, Schapira M, Cheng SWG et al. (2011).
Somatic mutations at EZH2 Y641 act dominantly through a
mechanism of selectively altered PRC2 catalytic activity, to
increase H3K27 trimethylation. Blood 117 (8): 2451-2459. doi:
10.1182/blood-2010-11-321208
- Yuan WX, Gui YX, Na WN, Chao J, Yang X (2016). Circulating
microRNA-125b and microRNA-130a expression profiles
predict chemoresistance to R-CHOP in diffuse large B-cell
lymphoma patients. Oncology Letters 11: 423-432. doi:
10.3892/ol.2015.3866
- Zainuddin N, Berglund M, Wanders A, Ren ZP, Amini RM et
al. (2009). TP53 mutations predict for poor survival in de
novo diffuse large B-cell lymphoma of germinal center
subtype. Leukemia Research 33 (1): 60-66. doi: 10.1016/j.
leukres.2008.06.022