Review article: Biomedical intelligence
Vol. 149 No. 0304 (2019)
Liquid biopsy in tissue-born lymphomas
- Valeria Spina
- Davide Rossi
Summary
In the era of personalised medicine, genetic information is critical to directing therapeutic options, aiding risk stratification and disease monitoring of lymphomas. Liquid biopsy is a novel noninvasive, real-time and tumour-specific technique, reliably reflecting the comprehensive tumour genetic profile, and thus holds great promise for the genetic assessment, response monitoring and relapse detection of lymphomas. Standard methods for disease response assessment in patients with lymphoma, including positron emission tomography, are imperfect. In other haematological malignancies, particularly leukaemias, the ability to detect minimal residual disease (MRD) is increasingly influencing treatment paradigms. However, in some subtypes of lymphoma, such as diffuse large B-cell lymphoma and classic Hodgkin’s lymphoma, the application of MRD assessment techniques such as flow cytometry or polymerase chain reaction-based methods has been challenged by the absence of circulating disease. The review summarises the applications of liquid biopsy in the assessment of tumour burden and response to therapy, noninvasive genomic profiling, and monitoring of clonal dynamics in patients with diffuse large B-cell lymphoma and classic Hodgkin’s lymphoma.
References
- Fleischhacker M, Schmidt B. Circulating nucleic acids (CNAs) and cancer--a survey. Biochim Biophys Acta. 2007;1775(1):181–232.
- Thierry AR, El Messaoudi S, Gahan PB, Anker P, Stroun M. Origins, structures, and functions of circulating DNA in oncology. Cancer Metastasis Rev. 2016;35(3):347–76. doi:.https://doi.org/10.1007/s10555-016-9629-x
- Thakur BK, Zhang H, Becker A, Matei I, Huang Y, Costa-Silva B, et al. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res. 2014;24(6):766–9. doi:.https://doi.org/10.1038/cr.2014.44
- Kahlert C, Melo SA, Protopopov A, Tang J, Seth S, Koch M, et al. Identification of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J Biol Chem. 2014;289(7):3869–75. doi:.https://doi.org/10.1074/jbc.C113.532267
- Jahr S, Hentze H, Englisch S, Hardt D, Fackelmayer FO, Hesch RD, et al. DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res. 2001;61(4):1659–65.
- Stroun M, Lyautey J, Lederrey C, Olson-Sand A, Anker P. About the possible origin and mechanism of circulating DNA: apoptosis and active DNA release. Clin Chim Acta. 2001;313(1-2):139–42. doi:.https://doi.org/10.1016/S0009-8981(01)00665-9
- Giacona MB, Ruben GC, Iczkowski KA, Roos TB, Porter DM, Sorenson GD. Cell-free DNA in human blood plasma: length measurements in patients with pancreatic cancer and healthy controls. Pancreas. 1998;17(1):89–97. doi:.https://doi.org/10.1097/00006676-199807000-00012
- Lo YM, Chan KC, Sun H, Chen EZ, Jiang P, Lun FM, et al. Maternal plasma DNA sequencing reveals the genome-wide genetic and mutational profile of the fetus. Sci Transl Med. 2010;2(61): 61–91. doi:.https://doi.org/10.1126/scitranslmed.3001720
- Thierry AR, Mouliere F, Gongora C, Ollier J, Robert B, Ychou M, et al. Origin and quantification of circulating DNA in mice with human colorectal cancer xenografts. Nucleic Acids Res. 2010;38(18):6159–75. doi:.https://doi.org/10.1093/nar/gkq421
- Mouliere F, El Messaoudi S, Pang D, Dritschilo A, Thierry AR. Multi-marker analysis of circulating cell-free DNA toward personalized medicine for colorectal cancer. Mol Oncol. 2014;8(5):927–41. doi:.https://doi.org/10.1016/j.molonc.2014.02.005
- Mouliere F, Robert B, Arnau Peyrotte E, Del Rio M, Ychou M, Molina F, et al. High fragmentation characterizes tumour-derived circulating DNA. PLoS One. 2011;6(9):e23418. doi:.https://doi.org/10.1371/journal.pone.0023418
- Roschewski M, Dunleavy K, Pittaluga S, Moorhead M, Pepin F, Kong K, et al. Circulating tumour DNA and CT monitoring in patients with untreated diffuse large B-cell lymphoma: a correlative biomarker study. Lancet Oncol. 2015;16(5):541–9. doi:.https://doi.org/10.1016/S1470-2045(15)70106-3
- Armand P, Oki Y, Neuberg DS, Faham M, Cummings C, Klinger M, et al. Detection of circulating tumour DNA in patients with aggressive B-cell non-Hodgkin lymphoma. Br J Haematol. 2013;163(1):123–6. doi:.https://doi.org/10.1111/bjh.12439
- Hohaus S, Giachelia M, Massini G, Mansueto G, Vannata B, Bozzoli V, et al. Cell-free circulating DNA in Hodgkin’s and non-Hodgkin’s lymphomas. Ann Oncol. 2009;20(8):1408–13. doi:.https://doi.org/10.1093/annonc/mdp006
- Kurtz DM, Green MR, Bratman SV, Scherer F, Liu CL, Kunder CA, et al. Noninvasive monitoring of diffuse large B-cell lymphoma by immunoglobulin high-throughput sequencing. Blood. 2015;125(24):3679–87. doi:.https://doi.org/10.1182/blood-2015-03-635169
- Forshew T, Murtaza M, Parkinson C, Gale D, Tsui DW, Kaper F, et al. Noninvasive identification and monitoring of cancer mutations by targeted deep sequencing of plasma DNA. Sci Transl Med. 2012;4(136):136ra68. doi:.https://doi.org/10.1126/scitranslmed.3003726
- Ladetto M, Brüggemann M, Monitillo L, Ferrero S, Pepin F, Drandi D, et al. Next-generation sequencing and real-time quantitative PCR for minimal residual disease detection in B-cell disorders. Leukemia. 2014;28(6):1299–307. doi:.https://doi.org/10.1038/leu.2013.375
- Rossi D, Diop F, Spaccarotella E, Monti S, Zanni M, Rasi S, et al. Diffuse large B-cell lymphoma genotyping on the liquid biopsy. Blood. 2017;129(14):1947–57. doi:.https://doi.org/10.1182/blood-2016-05-719641
- Frickhofen N, Müller E, Sandherr M, Binder T, Bangerter M, Wiest C, et al. Rearranged Ig heavy chain DNA is detectable in cell-free blood samples of patients with B-cell neoplasia. Blood. 1997;90(12):4953–60.
- Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366(10):883–92. doi:.https://doi.org/10.1056/NEJMoa1113205
- Diaz LA, Jr, Bardelli A. Liquid biopsies: genotyping circulating tumor DNA. J Clin Oncol. 2014;32(6):579–86. doi:.https://doi.org/10.1200/JCO.2012.45.2011
- Kurtz DM, Scherer F, Newman AM, Craig AFM, Khodadoust MS, Lovejoy AF, et al. Prediction of therapeutic outcomes in DLBCL from circulating tumor DNA dynamics. In: 2016 ASCO Annual Meeting, Abstract, 175, 3679–3687.
- Newman AM, Bratman SV, To J, Wynne JF, Eclov NCW, Modlin LA, et al. An ultrasensitive method for quantitating circulating tumor DNA with broad patient coverage. Nat Med. 2014;20(5):548–54. doi:.https://doi.org/10.1038/nm.3519
- Scherer F, Kurtz DM, Newman AM, Shahrokh Esfahani M, Craig A, Stehr H, et al. Development and validation of biopsy-free genotyping for molecular subtyping of diffuse large B-cell lymphoma. Blood. 2016;128:1089.
- Scherer F, Kurtz DM, Newman AM, Stehr H, Liu CL, Zhou L, et al. Non invasive genotyping and assessment of treatment response in diffuse large B cell lymphoma. Blood. 2015;126(23):114.
- Scherer F, Kurtz DM, Newman AM, Stehr H, Craig AF, Esfahani MS, et al. Distinct biological subtypes and patterns of genome evolution in lymphoma revealed by circulating tumor DNA. Sci Transl Med. 2016;8(364):364ra155. doi:.https://doi.org/10.1126/scitranslmed.aai8545
- Bohers E, Viailly PJ, Dubois S, Bertrand P, Maingonnat C, Mareschal S, et al. Somatic mutations of cell-free circulating DNA detected by next-generation sequencing reflect the genetic changes in both germinal center B-cell-like and activated B-cell-like diffuse large B-cell lymphomas at the time of diagnosis. Haematologica. 2015;100(7):e280–4. doi:.https://doi.org/10.3324/haematol.2015.123612
- Spina V, Bruscaggin A, Cuccaro A, Martini M, Di Trani M, Forestieri G, et al. Circulating tumor DNA reveals genetics, clonal evolution, and residual disease in classical Hodgkin lymphoma. Blood. 2018;131(22):2413–25. doi:.https://doi.org/10.1182/blood-2017-11-812073
- Camus V, Sarafan-Vasseur N, Bohers E, Dubois S, Mareschal S, Bertrand P, et al. Digital PCR for quantification of recurrent and potentially actionable somatic mutations in circulating free DNA from patients with diffuse large B-cell lymphoma. Leuk Lymphoma. 2016;57(9):2171–9. doi:.https://doi.org/10.3109/10428194.2016.1139703
- Camus V, Stamatoullas A, Mareschal S, Viailly PJ, Sarafan-Vasseur N, Bohers E, et al. Detection and prognostic value of recurrent exportin 1 mutations in tumor and cell-free circulating DNA of patients with classical Hodgkin lymphoma. Haematologica. 2016;101(9):1094–101. doi:.https://doi.org/10.3324/haematol.2016.145102
- Hattori K, Sakata-Yanagimoto M, Suehara Y, Yokoyama Y, Kato T, Kurita N, et al. Clinical significance of disease-specific MYD88 mutations in circulating DNA in primary central nervous system lymphoma. Cancer Sci. 2018;109(1):225–30. doi:.https://doi.org/10.1111/cas.13450
- Suehara Y, Sakata-Yanagimoto M, Hattori K, Nanmoku T, Itoh T, Kaji D, et al. Liquid biopsy for the identification of intravascular large B-cell lymphoma. Haematologica. 2018;103(6):e241–4. doi:.https://doi.org/10.3324/haematol.2017.178830
- Herrera AF, Kim HT, Kong KA, Faham M, Sun H, Sohani AR, et al. Next-generation sequencing-based detection of circulating tumour DNA After allogeneic stem cell transplantation for lymphoma. Br J Haematol. 2016;175(5):841–50. doi:.https://doi.org/10.1111/bjh.14311
- Schmitt MW, Kennedy SR, Salk JJ, Fox EJ, Hiatt JB, Loeb LA. Detection of ultra-rare mutations by next-generation sequencing. Proc Natl Acad Sci USA. 2012;109(36):14508–13. doi:.https://doi.org/10.1073/pnas.1208715109
- Morschhauser F, Salles G, McKay P, Tilly H, Schmitt A, Gerecitano J, et al. Interim report from a phase 2 multicenter study of tazemetostat, an EZH2 inhibitor, in patients with relapsed or refractory B‐cell non‐Hodgkin Lymphomas. Hematol Oncol. 2017;35(S2):24–5. [Abstract 4]. doi: https://doi.org/10.1002/hon.2437_3
- Kurtz DM, Scherer F, Jin MC, Soo J, Craig AFM, Esfahani MS, et al. Circulating Tumor DNA Measurements As Early Outcome Predictors in Diffuse Large B-Cell Lymphoma. J Clin Oncol. 2018;36(28):2845–53. doi:.https://doi.org/10.1200/JCO.2018.78.5246
- Roschewski M, Staudt LM, Wilson WH. Dynamic monitoring of circulating tumor DNA in non-Hodgkin lymphoma. Blood. 2016;127(25):3127–32. doi:.https://doi.org/10.1182/blood-2016-03-635219
- Mattocks CJ, Morris MA, Matthijs G, Swinnen E, Corveleyn A, Dequeker E, et al.; EuroGentest Validation Group. A standardized framework for the validation and verification of clinical molecular genetic tests. Eur J Hum Genet. 2010;18(12):1276–88. doi:.https://doi.org/10.1038/ejhg.2010.101
- Kennedy SR, Schmitt MW, Fox EJ, Kohrn BF, Salk JJ, Ahn EH, et al. Detecting ultralow-frequency mutations by Duplex Sequencing. Nat Protoc. 2014;9(11):2586–606. doi:.. Correction in: Nat Protoc. 2014;9:2903. doi:https://doi.org/10.1038/nprot1214-2903d.https://doi.org/10.1038/nprot.2014.170
- Hiatt JB, Pritchard CC, Salipante SJ, O’Roak BJ, Shendure J. Single molecule molecular inversion probes for targeted, high-accuracy detection of low-frequency variation. Genome Res. 2013;23(5):843–54. doi:.https://doi.org/10.1101/gr.147686.112
- Kinde I, Wu J, Papadopoulos N, Kinzler KW, Vogelstein B. Detection and quantification of rare mutations with massively parallel sequencing. Proc Natl Acad Sci USA. 2011;108(23):9530–5. doi:.https://doi.org/10.1073/pnas.1105422108
- Peng Q, Vijaya Satya R, Lewis M, Randad P, Wang Y. Reducing amplification artifacts in high multiplex amplicon sequencing by using molecular barcodes. BMC Genomics. 2015;16(1):589. doi:.https://doi.org/10.1186/s12864-015-1806-8
- Simpson RJ, Lim JW, Moritz RL, Mathivanan S. Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics. 2009;6(3):267–83. doi:.https://doi.org/10.1586/epr.09.17
- Heitzer E, Auer M, Ulz P, Geigl JB, Speicher MR. Circulating tumor cells and DNA as liquid biopsies. Genome Med. 2013;5(8):73. doi:.https://doi.org/10.1186/gm477