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ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

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Review Article

Deciphering the Genetic Complexity of Classical Hodgkin Lymphoma: Insights and Effective Strategies

Author(s): Chaeyoung Lee* and Yeeun An

Volume 25, Issue 5, 2024

Published on: 24 May, 2024

Page: [334 - 342] Pages: 9

DOI: 10.2174/0113892029301904240513045755

Price: $65

Abstract

Understanding the genetics of susceptibility to classical Hodgkin lymphoma (cHL) is considerably limited compared to other cancers due to the rare Hodgkin and Reed-Sternberg (HRS) tumor cells, which coexist with the predominant non-malignant microenvironment. This article offers insights into genetic abnormalities in cHL, as well as nucleotide variants and their associated target genes, elucidated through recent technological advancements. Oncogenomes in HRS cells highlight the survival and proliferation of these cells through hyperactive signaling in specific pathways (e.g., NF-kB) and their interplay with microenvironmental cells (e.g., CD4+ T cells). In contrast, the susceptibility genes identified from genome-wide association studies and expression quantitative trait locus analyses only vaguely implicate their potential roles in susceptibility to more general cancers. To pave the way for the era of precision oncology, more intensive efforts are imperative, employing the following strategies: exploring genetic heterogeneity by gender and cHL subtype, investigating colocalization with various types of expression quantitative trait loci, and leveraging single-cell analysis. These approaches provide valuable perspectives for unraveling the genetic complexities of cHL.

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[1]
Küppers, R.; Rajewsky, K.; Zhao, M.; Simons, G.; Laumann, R.; Fischer, R.; Hansmann, M.L. Hodgkin disease: Hodgkin and Reed-Sternberg cells picked from histological sections show clonal immunoglobulin gene rearrangements and appear to be derived from B cells at various stages of development. Proc. Natl. Acad. Sci., 1994, 91(23), 10962-10966.
[http://dx.doi.org/10.1073/pnas.91.23.10962] [PMID: 7971992]
[2]
Marafioti, T.; Hummel, M.; Foss, H.D.; Laumen, H.; Korbjuhn, P.; Anagnostopoulos, I.; Lammert, H.; Demel, G.; Theil, J.; Wirth, T.; Stein, H. Hodgkin and Reed-Sternberg cells represent an expansion of a single clone originating from a germinal center B-cell with functional immunoglobulin gene rearrangements but defective immunoglobulin transcription. Blood, 2000, 95(4), 1443-1450.
[http://dx.doi.org/10.1182/blood.V95.4.1443.004k55_1443_1450] [PMID: 10666223]
[3]
Mack, T.M.; Cozen, W.; Shibata, D.K.; Weiss, L.M.; Nathwani, B.N.; Hernandez, A.M.; Taylor, C.R.; Hamilton, A.S.; Deapen, D.M.; Rappaport, E.B. Concordance for Hodgkin’s disease in identical twins suggesting genetic susceptibility to the young-adult form of the disease. N. Engl. J. Med., 1995, 332(7), 413-419.
[http://dx.doi.org/10.1056/NEJM199502163320701] [PMID: 7824015]
[4]
Kharazmi, E.; Fallah, M.; Pukkala, E.; Olsen, J.H.; Tryggvadottir, L.; Sundquist, K.; Tretli, S.; Hemminki, K. Risk of familial classical Hodgkin lymphoma by relationship, histology, age, and sex: A joint study from five Nordic countries. Blood, 2015, 126(17), 1990-1995.
[http://dx.doi.org/10.1182/blood-2015-04-639781] [PMID: 26311361]
[5]
Rudant, J.; Menegaux, F.; Leverger, G.; Baruchel, A.; Nelken, B.; Bertrand, Y.; Hartmann, O.; Pacquement, H.; Vérité, C.; Robert, A.; Michel, G.; Margueritte, G.; Gandemer, V.; Hémon, D.; Clavel, J. Family history of cancer in children with acute leukemia, Hodgkin’s lymphoma or non-Hodgkin’s lymphoma: The ESCALE study (SFCE). Int. J. Cancer, 2007, 121(1), 119-126.
[http://dx.doi.org/10.1002/ijc.22624] [PMID: 17330239]
[6]
Weniger, M.A.; Küppers, R. Molecular biology of Hodgkin lymphoma. Leukemia, 2021, 35(4), 968-981.
[http://dx.doi.org/10.1038/s41375-021-01204-6] [PMID: 33686198]
[7]
Tiacci, E.; Ladewig, E.; Schiavoni, G.; Penson, A.; Fortini, E.; Pettirossi, V.; Wang, Y.; Rosseto, A.; Venanzi, A.; Vlasevska, S.; Pacini, R.; Piattoni, S.; Tabarrini, A.; Pucciarini, A.; Bigerna, B.; Santi, A.; Gianni, A.M.; Viviani, S.; Cabras, A.; Ascani, S.; Crescenzi, B.; Mecucci, C.; Pasqualucci, L.; Rabadan, R.; Falini, B. Pervasive mutations of JAK-STAT pathway genes in classical Hodgkin lymphoma. Blood, 2018, 131(22), 2454-2465.
[http://dx.doi.org/10.1182/blood-2017-11-814913] [PMID: 29650799]
[8]
Reichel, J.; Chadburn, A.; Rubinstein, P.G.; Roth, G.L.; Tam, W.; Liu, Y.; Gaiolla, R.; Eng, K.; Brody, J.; Inghirami, G.; Stella, C.C.; Santoro, A.; Rahal, D.; Totonchy, J.; Elemento, O.; Cesarman, E.; Roshal, M. Flow sorting and exome sequencing reveal the oncogenome of primary Hodgkin and Reed-Sternberg cells. Blood, 2015, 125(7), 1061-1072.
[http://dx.doi.org/10.1182/blood-2014-11-610436] [PMID: 25488972]
[9]
Steidl, C.; Diepstra, A.; Lee, T.; Chan, F.C.; Farinha, P.; Tan, K.; Telenius, A.; Barclay, L.; Shah, S.P.; Connors, J.M.; van den Berg, A.; Gascoyne, R.D. Gene expression profiling of microdissected Hodgkin Reed-Sternberg cells correlates with treatment outcome in classical Hodgkin lymphoma. Blood, 2012, 120(17), 3530-3540.
[http://dx.doi.org/10.1182/blood-2012-06-439570] [PMID: 22955918]
[10]
Küppers, R. The biology of Hodgkin’s lymphoma. Nat. Rev. Cancer, 2009, 9(1), 15-27.
[http://dx.doi.org/10.1038/nrc2542] [PMID: 19078975]
[11]
Brune, MM; Juskevicius, D; Haslbauer, J; Dirnhofer, S; Tzankov, A Genomic Landscape of Hodgkin Lymphoma. Cancers., 2021, 13(4), 682.
[http://dx.doi.org/10.3390/cancers13040682]
[12]
Küppers, R.; Klein, U.; Schwering, I.; Distler, V.; Bräuninger, A.; Cattoretti, G.; Tu, Y.; Stolovitzky, G.A.; Califano, A.; Hansmann, M.L.; Favera, D.R. Identification of Hodgkin and Reed-Sternberg cell-specific genes by gene expression profiling. J. Clin. Invest., 2003, 111(4), 529-537.
[http://dx.doi.org/10.1172/JCI200316624] [PMID: 12588891]
[13]
Buchan, S.L.; Shamkhani, A.A. Distinct motifs in the intracellular domain of human CD30 differentially activate canonical and alternative transcription factor NF-κB signaling. PLoS One, 2012, 7(9), e45244.
[http://dx.doi.org/10.1371/journal.pone.0045244] [PMID: 23028875]
[14]
Carbone, A.; Gloghini, A.; Gattei, V.; Aldinucci, D.; Degan, M.; De Paoli, P.; Zagonel, V.; Pinto, A. Expression of functional CD40 antigen on Reed-Sternberg cells and Hodgkin’s disease cell lines. Blood, 1995, 85(3), 780-789.
[http://dx.doi.org/10.1182/blood.V85.3.780.bloodjournal853780] [PMID: 7530508]
[15]
Lee, S.P.; Constandinou, C.M.; Thomas, W.A.; Carter, C.D.; Blake, N.W.; Murray, P.G.; Crocker, J.; Rickinson, A.B. Antigen presenting phenotype of Hodgkin Reed-Sternberg cells: Analysis of the HLA class I processing pathway and the effects of interleukin-10 on epstein-barr virus-specific cytotoxic T-cell recognition. Blood, 1998, 92(3), 1020-1030.
[http://dx.doi.org/10.1182/blood.V92.3.1020] [PMID: 9680372]
[16]
Wienand, K.; Chapuy, B.; Stewart, C.; Dunford, A.J.; Wu, D.; Kim, J.; Kamburov, A.; Wood, T.R.; Cader, F.Z.; Ducar, M.D.; Thorner, A.R.; Nag, A.; Heubeck, A.T.; Buonopane, M.J.; Redd, R.A.; Bojarczuk, K.; Lawton, L.N.; Armand, P.; Rodig, S.J.; Fromm, J.R.; Getz, G.; Shipp, M.A. Genomic analyses of flow- sorted Hodgkin Reed-Sternberg cells reveal complementary mechanisms of immune evasion. Blood Adv., 2019, 3(23), 4065-4080.
[http://dx.doi.org/10.1182/bloodadvances.2019001012] [PMID: 31816062]
[17]
Wein, F.; Küppers, R. The role of T cells in the microenvironment of Hodgkin lymphoma. J. Leukoc. Biol., 2016, 99(1), 45-50.
[http://dx.doi.org/10.1189/jlb.3MR0315-136R] [PMID: 26320264]
[18]
Vari, F.; Arpon, D.; Keane, C.; Hertzberg, M.S.; Talaulikar, D.; Jain, S.; Cui, Q.; Han, E.; Tobin, J.; Bird, R.; Cross, D.; Hernandez, A.; Gould, C.; Birch, S.; Gandhi, M.K. Immune evasion via PD-1/PD-L1 on NK cells and monocyte/macrophages is more prominent in Hodgkin lymphoma than DLBCL. Blood, 2018, 131(16), 1809-1819.
[http://dx.doi.org/10.1182/blood-2017-07-796342] [PMID: 29449276]
[19]
Genetic Analysis of Psoriasis Consortium & the Wellcome Trust Case Control Consortium 2, Strange A, Capon F, et al. A genome-wide association study identifies new psoriasis susceptibility loci and an interaction between HLA-C and ERAP1. Nat Genet., 2010, 42(11), 985-990.
[http://dx.doi.org/10.1038/ng.694]
[20]
Frampton, M.; Filho, S.M.I.; Broderick, P.; Thomsen, H.; Försti, A.; Vijayakrishnan, J.; Cooke, R.; Mora, E.V.; Hoffmann, P.; Nöthen, M.M.; Lloyd, A.; Holroyd, A.; Eisele, L.; Jöckel, K.H.; Ponader, S.; von Strandmann, E.P.; Lightfoot, T.; Roman, E.; Lake, A.; Montgomery, D.; Jarrett, R.F.; Swerdlow, A.J.; Engert, A.; Hemminki, K.; Houlston, R.S. Variation at 3p24.1 and 6q23.3 influences the risk of Hodgkin’s lymphoma. Nat. Commun., 2013, 4(1), 2549.
[http://dx.doi.org/10.1038/ncomms3549] [PMID: 24149102]
[21]
Pon, J.R.; Marra, M.A. Driver and passenger mutations in cancer. Annu. Rev. Pathol., 2015, 10(1), 25-50.
[http://dx.doi.org/10.1146/annurev-pathol-012414-040312] [PMID: 25340638]
[22]
Salipante, S.J.; Mealiffe, M.E.; Wechsler, J.; Krem, M.M.; Liu, Y.; Namkoong, S.; Bhagat, G.; Kirchhoff, T.; Offit, K.; Lynch, H.; Wiernik, P.H.; Roshal, M.; McMaster, M.L.; Tucker, M.; Fromm, J.R.; Goldin, L.R.; Horwitz, M.S. Mutations in a gene encoding a midbody kelch protein in familial and sporadic classical Hodgkin lymphoma lead to binucleated cells. Proc. Natl. Acad. Sci., 2009, 106(35), 14920-14925.
[http://dx.doi.org/10.1073/pnas.0904231106] [PMID: 19706467]
[23]
Rotunno, M.; McMaster, M.L.; Boland, J.; Bass, S.; Zhang, X.; Burdett, L.; Hicks, B.; Ravichandran, S.; Luke, B.T.; Yeager, M.; Fontaine, L.; Hyland, P.L.; Goldstein, A.M.; Chanock, S.J.; Caporaso, N.E.; Tucker, M.A.; Goldin, L.R. Whole exome sequencing in families at high risk for Hodgkin lymphoma: Identification of a predisposing mutation in the KDR gene. Haematologica, 2016, 101(7), 853-860.
[http://dx.doi.org/10.3324/haematol.2015.135475] [PMID: 27365461]
[24]
McTigue, M.A.; Wickersham, J.A.; Pinko, C.; Showalter, R.E.; Parast, C.V.; Russell, T.A.; Gehring, M.R.; Mroczkowski, B.; Kan, C.C.; Villafranca, J.E.; Appelt, K. Crystal structure of the kinase domain of human vascular endothelial growth factor receptor 2: A key enzyme in angiogenesis. Structure, 1999, 7(3), 319-330.
[http://dx.doi.org/10.1016/S0969-2126(99)80042-2] [PMID: 10368301]
[25]
Cooper, P.S.; Lipshultz, D.; Matten, W.T.; McGinnis, S.D.; Pechous, S.; Romiti, M.L.; Tao, T.; Gratian, V.M.; Sayers, E.W. Education resources of the National Center for Biotechnology Information. Brief. Bioinform., 2010, 11(6), 563-569.
[http://dx.doi.org/10.1093/bib/bbq022] [PMID: 20570844]
[26]
An, Y; Lee, C. Identification and Interpretation of eQTL and eGenes for Hodgkin Lymphoma Susceptibility. Genes., 2023, 14(6), 1142.
[http://dx.doi.org/10.3390/genes14061142]
[27]
Cai, H.H.; Sun, Y.M.; Miao, Y.; Gao, W.T.; Peng, Q.; Yao, J.; Zhao, H.L. Aberrant methylation frequency of TNFRSF10C Promoter in pancreatic cancer cell lines. Hepatobiliary Pancreat. Dis. Int., 2011, 10(1), 95-100.
[http://dx.doi.org/10.1016/S1499-3872(11)60014-3] [PMID: 21269942]
[28]
Cheng, Y.; Kim, J.W.; Liu, W.; Dunn, T.A.; Luo, J.; Loza, M.J.; Kim, S.T.; Zheng, S.L.; Xu, J.; Isaacs, W.B.; Chang, B.L. Genetic and epigenetic inactivation of TNFRSF10C in human prostate cancer. Prostate, 2009, 69(3), 327-335.
[http://dx.doi.org/10.1002/pros.20882] [PMID: 19035483]
[29]
Chughtai, S.A.; Crundwell, M.C.; Cruickshank, N.R.J.; Affie, E.; Armstrong, S.; Knowles, M.A.; Takle, L.A.; Kuo, M.; Khan, N.; Phillips, S.M.A.; Neoptolemos, J.P.; Morton, D.G. Two novel regions of interstitial deletion on chromosome 8p in colorectal cancer. Oncogene, 1999, 18(3), 657-665.
[http://dx.doi.org/10.1038/sj.onc.1202340] [PMID: 9989816]
[30]
Wistuba, I.I.; Behrens, C.; Virmani, A.K.; Milchgrub, S.; Syed, S.; Lam, S.; Mackay, B.; Minna, J.D.; Gazdar, A.F. Allelic losses at chromosome 8p21-23 are early and frequent events in the pathogenesis of lung cancer. Cancer Res., 1999, 59(8), 1973-1979.
[PMID: 10213509]
[31]
Jauffret, C.E.; Moulin, J.F.; Ginestier, C.; Bechlian, D.; Conte, N.; Geneix, J.; Adélaïde, J.; Noguchi, T.; Hassoun, J.; Jacquemier, J.; Birnbaum, D. Loss of heterozygosity at microsatellite markers from region p11-21 of chromosome 8 in microdissected breast tumor but not in peritumoral cells. Int. J. Oncol., 2002, 21(5), 989-996.
[http://dx.doi.org/10.3892/ijo.21.5.989] [PMID: 12370745]
[32]
Adams, J.; Williams, S.V.; Aveyard, J.S.; Knowles, M.A. Loss of heterozygosity analysis and DNA copy number measurement on 8p in bladder cancer reveals two mechanisms of allelic loss. Cancer Res., 2005, 65(1), 66-75.
[http://dx.doi.org/10.1158/0008-5472.66.65.1] [PMID: 15665280]
[33]
Xue, A.; Chang, J.W.; Chung, L.; Samra, J.; Hugh, T.; Gill, A.; Butturini, G.; Baxter, R.C.; Smith, R.C. Serum apolipoprotein C-II is prognostic for survival after pancreatic resection for adenocarcinoma. Br. J. Cancer, 2012, 107(11), 1883-1891.
[http://dx.doi.org/10.1038/bjc.2012.458] [PMID: 23169340]
[34]
Harima, Y; Ariga, T; Kaneyasu, Y Clinical value of serum biomarkers, squamous cell carcinoma antigen and apolipoprotein C-II in follow-up of patients with locally advanced cervical squamous cell carcinoma treated with radiation: A multicenter prospective cohort study. PLoS One, 2021, 16(11), e0259235.
[http://dx.doi.org/10.1371/journal.pone.0259235]
[35]
Kaseb, H.; Babiker, H.M. Hodgkin lymphoma. 2021. Available from: https://www.ncbi.nlm.nih.gov/books/NBK499969 (Accessed on: 21 Feb 2022).
[36]
Lee, C. Genome-wide expression quantitative trait loci analysis using mixed models. Front Genet., 2018, 9, 341.
[http://dx.doi.org/10.3389/fgene.2018.00341]
[37]
Lee, C. Towards the genetic architecture of complex gene expression traits: Challenges and prospects for eQTL mapping in humans. Genes, 2022, 13(2), 235.
[http://dx.doi.org/10.3390/genes13020235] [PMID: 35205280]
[38]
Yazar, S.; Hernandez, S.J.; Wing, K.; Senabouth, A.; Gordon, M.G.; Andersen, S.; Lu, Q.; Rowson, A.; Taylor, T.R.P.; Clarke, L.; Maccora, K.; Chen, C.; Cook, A.L.; Ye, C.J.; Fairfax, K.A.; Hewitt, A.W.; Powell, J.E. Single-cell eQTL mapping identifies cell type–specific genetic control of autoimmune disease. Science, 2022, 376(6589), eabf3041.
[http://dx.doi.org/10.1126/science.abf3041] [PMID: 35389779]
[39]
McAulay, K.A.; Jarrett, R.F. Human leukocyte antigens and genetic susceptibility to lymphoma. Tissue Antigens, 2015, 86(2), 98-113.
[http://dx.doi.org/10.1111/tan.12604] [PMID: 26189878]
[40]
Hjalgrim, H.; Rostgaard, K.; Johnson, P.C.D.; Lake, A.; Shield, L.; Little, A.M.; Smedby, E.K.; Adami, H.O.; Glimelius, B.; Dutoit, H.S.; Kane, E.; Taylor, G.M.; McConnachie, A.; Ryder, L.P.; Sundstrom, C.; Andersen, P.S.; Chang, E.T.; Alexander, F.E.; Melbye, M.; Jarrett, R.F. HLA-A alleles and infectious mononucleosis suggest a critical role for cytotoxic T-cell response in EBV-related Hodgkin lymphoma. Proc. Natl. Acad. Sci., 2010, 107(14), 6400-6405.
[http://dx.doi.org/10.1073/pnas.0915054107] [PMID: 20308568]
[41]
Cozen, W.; Timofeeva, M.N.; Li, D.; Diepstra, A.; Hazelett, D.; Sourdeix, D.M.; Edlund, C.K.; Franke, L.; Rostgaard, K.; Van Den Berg, D.J.; Cortessis, V.K.; Smedby, K.E.; Glaser, S.L.; Westra, H.J.; Robison, L.L.; Mack, T.M.; Ghesquieres, H.; Hwang, A.E.; Nieters, A.; de Sanjose, S.; Lightfoot, T.; Becker, N.; Maynadie, M.; Foretova, L.; Roman, E.; Benavente, Y.; Rand, K.A.; Nathwani, B.N.; Glimelius, B.; Staines, A.; Boffetta, P.; Link, B.K.; Kiemeney, L.; Ansell, S.M.; Bhatia, S.; Strong, L.C.; Galan, P.; Vatten, L.; Habermann, T.M.; Duell, E.J.; Lake, A.; Veenstra, R.N.; Visser, L.; Liu, Y.; Urayama, K.Y.; Montgomery, D.; Gaborieau, V.; Weiss, L.M.; Byrnes, G.; Lathrop, M.; Cocco, P.; Best, T.; Skol, A.D.; Adami, H.O.; Melbye, M.; Cerhan, J.R.; Gallagher, A.; Taylor, G.M.; Slager, S.L.; Brennan, P.; Coetzee, G.A.; Conti, D.V.; Onel, K.; Jarrett, R.F.; Hjalgrim, H.; van den Berg, A.; McKay, J.D. A meta-analysis of Hodgkin lymphoma reveals 19p13.3 TCF3 as a novel susceptibility locus. Nat. Commun., 2014, 5(1), 3856.
[http://dx.doi.org/10.1038/ncomms4856] [PMID: 24920014]
[42]
Connors, J.M.; Cozen, W.; Steidl, C.; Carbone, A.; Hoppe, R.T.; Flechtner, H.H.; Bartlett, N.L. Hodgkin lymphoma. Nat. Rev. Dis. Primers, 2020, 6(1), 61.
[http://dx.doi.org/10.1038/s41572-020-0189-6] [PMID: 32703953]
[43]
Shin, J.; Lee, C. A mixed model reduces spurious genetic associations produced by population stratification in genome-wide association studies. Genomics, 2015, 105(4), 191-196.
[http://dx.doi.org/10.1016/j.ygeno.2015.01.006] [PMID: 25640449]
[44]
Edwards, T.L.; Gao, X. Methods for detecting and correcting for population stratification; Curr Protoc Hum Genet, 2012, pp. 1-14.
[http://dx.doi.org/10.1002/0471142905.hg0122s73]
[45]
Lee, C. Analytical models for genetics of human traits influenced by sex. Curr. Genomics, 2016, 17(5), 439-443.
[http://dx.doi.org/10.2174/1389202917666160420142601] [PMID: 28217000]
[46]
Lee, C. Heterogeneous genetic architecture by gender for precision medicine of cardiovascular disease. J. Geriatr. Cardiol., 2018, 15(5), 325-327.
[http://dx.doi.org/10.11909/j.issn.1671-5411.2018.05.001] [PMID: 30083184]
[47]
Lee, C. Bayesian inference for mixed model-based genome-wide analysis of expression quantitative trait loci by Gibbs sampling. Front Genet., 2019, 10, 199.
[http://dx.doi.org/10.3389/fgene.2019.00199]
[48]
Lee, C. Best linear unbiased prediction of individual polygenic susceptibility to sporadic vascular dementia. J. Alzheimers Dis., 2016, 53(3), 1115-1119.
[http://dx.doi.org/10.3233/JAD-160391] [PMID: 27258425]
[49]
Zou, J.; Huss, M.; Abid, A.; Mohammadi, P.; Torkamani, A.; Telenti, A. A primer on deep learning in genomics. Nat. Genet., 2019, 51(1), 12-18.
[http://dx.doi.org/10.1038/s41588-018-0295-5] [PMID: 30478442]
[50]
Zuber, V.; Grinberg, N.F.; Gill, D.; Manipur, I.; Slob, E.A.W.; Patel, A.; Wallace, C.; Burgess, S. Combining evidence from Mendelian randomization and colocalization: Review and comparison of approaches. Am. J. Hum. Genet., 2022, 109(5), 767-782.
[http://dx.doi.org/10.1016/j.ajhg.2022.04.001] [PMID: 35452592]
[51]
Han, J.; Lee, C. Antagonistic regulatory effects of a single cis-acting expression quantitative trait locus between transcription and translation of the MRPL43 gene. BMC Genomic Data, 2022, 23(1), 42.
[http://dx.doi.org/10.1186/s12863-022-01057-7] [PMID: 35659240]
[52]
Alig, S.K.; Esfahani, S.M.; Garofalo, A.; Li, M.Y.; Rossi, C.; Flerlage, T.; Flerlage, J.E.; Adams, R.; Binkley, M.S.; Shukla, N.; Jin, M.C.; Olsen, M.; Telenius, A.; Mutter, J.A.; Martin, S.J.G.; Sworder, B.J.; Rai, S.; King, D.A.; Schultz, A.; Bögeholz, J.; Su, S.; Kathuria, K.R.; Liu, C.L.; Kang, X.; Strohband, M.J.; Langfitt, D.; Piza, P.K.F.; Surman, S.; Tian, F.; Spina, V.; Tousseyn, T.; Buedts, L.; Hoppe, R.; Natkunam, Y.; Fornecker, L.M.; Castellino, S.M.; Advani, R.; Rossi, D.; Lynch, R.; Ghesquières, H.; Casasnovas, O.; Kurtz, D.M.; Marks, L.J.; Link, M.P.; André, M.; Vandenberghe, P.; Steidl, C.; Diehn, M.; Alizadeh, A.A. Distinct Hodgkin lymphoma subtypes defined by noninvasive genomic profiling. Nature, 2024, 625(7996), 778-787.
[http://dx.doi.org/10.1038/s41586-023-06903-x] [PMID: 38081297]

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