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Research Paper

Genome wide exploration of the methylome in aggressive B-cell lymphoma in Golden Retrievers reveals a conserved hypermethylome

ORCID Icon, , &
Pages 2022-2038 | Received 11 May 2021, Accepted 14 Jul 2022, Published online: 31 Jul 2022

References

  • Seelig DM, Avery AC, Ehrhart EJ, et al. The comparative diagnostic features of canine and human lymphoma. Vet Sci. 2016;3(2). doi:10.3390/vetsci3020011
  • Elvers I, Turner-Maier J, Swofford R, et al. Exome sequencing of lymphomas from three dog breeds reveals somatic mutation patterns reflecting genetic background. Genome Res. 2015;25(11):1634–1645.
  • Bushell KR, Kim Y, Chan FC, et al. Genetic inactivation of TRAF3 in canine and human B-cell lymphoma. Blood. 2015;125(6):999–1005.
  • Seelig DM, Ito D, Forster CL, et al. Constitutive activation of alternative nuclear factor kappa B pathway in canine diffuse large B-cell lymphoma contributes to tumor cell survival and is a target of new adjuvant therapies. Leuk Lymphoma. 2017;58(7):1702–1710.
  • Mudaliar MA, Haggart RD, Miele G, et al. Comparative gene expression profiling identifies common molecular signatures of NF-kappaB activation in canine and human diffuse large B cell lymphoma (DLBCL). PLoS One. 2013;8(9):e72591.
  • Burton JH, Mazcko C, LeBlanc A, et al. NCI comparative oncology program testing of non-camptothecin indenoisoquinoline topoisomerase i inhibitors in naturally occurring canine lymphoma. Clin Cancer Res. 2018;24(23):5830–5840.
  • Marconato L, Frayssinet P, Rouquet N, et al. Randomized, placebo-controlled, double-blinded chemoimmunotherapy clinical trial in a pet dog model of diffuse large B-cell lymphoma. Clin Cancer Res. 2014;20(3):668–677.
  • Gardner HL, Rippy SB, Bear MD, et al. Phase I/II evaluation of RV1001, a novel PI3Kdelta inhibitor, in spontaneous canine lymphoma. PLoS One. 2018;13(4):e0195357.
  • Pasqualucci L, Dalla-Favera R. Genetics of diffuse large B-cell lymphoma. Blood. 2018;131(21):2307–2319.
  • Komaki S, Shiwa Y, Furukawa R, et al. iMETHYL: an integrative database of human DNA methylation, gene expression, and genomic variation. Hum Genome Var. 2018;5(1):18008.
  • Baylin SB, Jones PA. Epigenetic determinants of cancer. Cold Spring Harb Perspect Biol. 2016;8(9):a019505.
  • Shaknovich R, Geng H, Johnson NA, et al. DNA methylation signatures define molecular subtypes of diffuse large B-cell lymphoma. Blood. 2010;116(20):e81–9.
  • Chambwe N, Kormaksson M, Geng H, et al. Variability in DNA methylation defines novel epigenetic subgroups of DLBCL associated with different clinical outcomes. Blood. 2014;123(11):1699–1708.
  • Ferraresso S, Arico A, Sanavia T, et al. DNA methylation profiling reveals common signatures of tumorigenesis and defines epigenetic prognostic subtypes of canine diffuse large B-cell lymphoma. Sci Rep. 2017;7(1):11591.
  • Hsu CH, Tomiyasu H, Lee JJ, et al. Genome-wide DNA methylation analysis using MethylCap-seq in canine high-grade B-cell lymphoma. J Leukoc Biol. 2020;109(6):1089–1103.
  • Yamazaki J, Jelinek J, Hisamoto S, et al. Dynamic changes in DNA methylation patterns in canine lymphoma cell lines demonstrated by genome-wide quantitative DNA methylation analysis. Vet J. 2018;231:48–54.
  • Epiphanio TMF, Fernandes N, de Oliveira TF, et al. Global DNA methylation of peripheral blood leukocytes from dogs bearing multicentric non-Hodgkin lymphomas and healthy dogs: a comparative study. PLoS One. 2019;14(3):e0211898.
  • Martin-Subero JI, Kreuz M, Bibikova M, et al. New insights into the biology and origin of mature aggressive B-cell lymphomas by combined epigenomic, genomic, and transcriptional profiling. Blood. 2009;113(11):2488–2497.
  • Richards KL, Motsinger-Reif AA, Chen HW, et al. Gene profiling of canine B-cell lymphoma reveals germinal center and postgerminal center subtypes with different survival times, modeling human DLBCL. Cancer Res. 2013;73(16):5029–5039.
  • Avery AC. The genetic and molecular basis for canine models of human leukemia and lymphoma. Front Oncol. 2020;10:23.
  • Wu Y, Chang YM, Polton G, et al. Gene expression profiling of B cell lymphoma in dogs reveals dichotomous metabolic signatures distinguished by oxidative phosphorylation. Front Oncol. 2020;10:307.
  • Curran KM, Schaffer PA, Frank CB, et al. BCL2 and MYC are expressed at high levels in canine diffuse large B-cell lymphoma but are not predictive for outcome in dogs treated with CHOP chemotherapy. Vet Comp Oncol. 2017;15(4):1269–1279.
  • Schmitz R, Wright GW, Huang DW, et al. Genetics and pathogenesis of diffuse large B-cell lymphoma. N Engl J Med. 2018;378(15):1396–1407.
  • Sparks A, Woods JP, Bienzle D, et al. Whole genome sequencing analysis of high confidence variants of B-cell lymphoma in Canis familiaris. PLoS One. 2020;15(8):e0238183.
  • Aberg KA, McClay JL, Nerella S, et al. MBD-seq as a cost-effective approach for methylome-wide association studies: demonstration in 1500 case–control samples. Epigenomics. 2012;4(6):605–621.
  • Almamun M, Levinson BT, Gater ST, et al. Genome-wide DNA methylation analysis in precursor B-cells. Epigenetics. 2014;9(12):1588–1595.
  • Almamun M, Levinson BT, van Swaay AC, et al. Integrated methylome and transcriptome analysis reveals novel regulatory elements in pediatric acute lymphoblastic leukemia. Epigenetics. 2015;10(9):882–890.
  • Harris RA, Wang T, Coarfa C, et al. Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat Biotechnol. 2010;28(10):1097–1105.
  • Aberg KA, Chan RF, van den Oord EJCG. MBD-seq - realities of a misunderstood method for high-quality methylome-wide association studies. Epigenetics. 2020;15(4):431–438.
  • Glickman LG, Nita T, and Roland. The Golden Retriever Club of America National Health Survey 1998-199899. Texas: Golden Retriever Club of America; 1999.
  • Villamil JA, Henry CJ, Hahn AW, et al. Hormonal and sex impact on the epidemiology of canine lymphoma. J Cancer Epidemiol. 2009;2009:591753.
  • Irizarry RA, Ladd-Acosta C, Wen B, et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet. 2009;41(2):178–186.
  • Zhang Y, Parmigiani G, Johnson WE. batch effect adjustment for RNA-seq count data. NAR Genom Bioinform. 2020;2(3):lqaa078
  • Price EM, Robinson WP. Adjusting for batch effects in DNA methylation microarray data, a lesson learned. Front Genet. 2018;9:83.
  • Nehme E, Rahal Z, Sinjab A, et al. Epigenetic suppression of the T-box Subfamily 2 (TBX2) in human non-small cell lung cancer. Int J Mol Sci. 2019;20(5):1159.
  • Wansleben S, Peres J, Hare S, et al. T-box transcription factors in cancer biology. Biochim Biophys Acta. 2014;1846(2):380–391.
  • Aresu L, Ferraresso S, Marconato L, et al. New molecular and therapeutic insights into canine diffuse large B cell lymphoma elucidates the role of the dog as a model for human disease. Haematologica. 2018;104(6):e256–e259.
  • Costa VL, Henrique R, Danielsen SA, et al. TCF21 and PCDH17 methylation: an innovative panel of biomarkers for a simultaneous detection of urological cancers. Epigenetics. 2011;6(9):1120–1130.
  • Lin YL, Xie PG, Wang L, et al. Aberrant methylation of protocadherin 17 and its clinical significance in patients with prostate cancer after radical prostatectomy. Med Sci Monit. 2014;20:1376–1382.
  • Haruki S, Imoto I, Kozaki K, et al. Frequent silencing of protocadherin 17, a candidate tumour suppressor for esophageal squamous cell carcinoma. Carcinogenesis. 2010;31(6):1027–1036.
  • Model F, Osborn N, Ahlquist D, et al. Identification and validation of colorectal neoplasia-specific methylation markers for accurate classification of disease. Mol Cancer Res. 2007;5(2):153–163.
  • Uyen TN, Sakashita K, Al-Kzayer LF, et al. Aberrant methylation of protocadherin 17 and its prognostic value in pediatric acute lymphoblastic leukemia. Pediatr Blood Cancer. 2017;64(3):e26259.
  • Huang W, Xue X, Shan L, et al. Clinical significance of PCDH10 promoter methylation in diffuse large B-cell lymphoma. BMC Cancer. 2017;17(1):815.
  • Ying J, Li H, Seng TJ, et al. Functional epigenetics identifies a protocadherin PCDH10 as a candidate tumor suppressor for nasopharyngeal, esophageal and multiple other carcinomas with frequent methylation. Oncogene. 2006;25(7):1070–1080.
  • Su J, Huang YH, Cui X, et al. Homeobox oncogene activation by pan-cancer DNA hypermethylation. Genome Biol. 2018;19(1):108.
  • Comazzi S, Marelli S, Cozzi M, et al. Breed-associated risks for developing canine lymphoma differ among countries: an European canine lymphoma network study. BMC Vet Res. 2018;14(1):232.
  • Arendt ML, Melin M, Tonomura N, et al. Genome-wide association study of Golden Retrievers identifies germ-line risk factors predisposing to mast cell tumours. PLoS Genet. 2015;11(11):e1005647.
  • Quignon P, Herbin L, Cadieu E, et al. Canine population structure: assessment and impact of intra-breed stratification on SNP-based association studies. PLoS One. 2007;2(12):e1324.
  • Johnstone SE, Reyes A, Qi Y, et al. Large-scale topological changes restrain malignant progression in colorectal cancer. Cell. 2020;182(6):1474–89.e23.
  • Eden A, Gaudet F, Waghmare A, et al. Chromosomal instability and tumors promoted by DNA hypomethylation. Science. 2003;300(5618):455.
  • Yegnasubramanian S, Haffner MC, Zhang Y, et al. DNA hypomethylation arises later in prostate cancer progression than CpG island hypermethylation and contributes to metastatic tumor heterogeneity. Cancer Res. 2008;68(21):8954–8967.
  • Bock C, Tomazou EM, Brinkman AB, et al. Quantitative comparison of genome-wide DNA methylation mapping technologies. Nat Biotechnol. 2010;28(10):1106–1114.
  • Olkhov-Mitsel E, Bapat B. Strategies for discovery and validation of methylated and hydroxymethylated DNA biomarkers. Cancer Med. 2012;1(2):237–260.
  • Chen YC, Elnitski L. Aberrant DNA methylation defines isoform usage in cancer, with functional implications. PLoS Comput Biol. 2019;15(7):e1007095.
  • Shukla S, Kavak E, Gregory M, et al. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature. 2011;479(7371):74–79.
  • Ringrose L, Paro R. Epigenetic regulation of cellular memory by the polycomb and trithorax group proteins. Annu Rev Genet. 2004;38(1):413–443.
  • Widschwendter M, Fiegl H, Egle D, et al. Epigenetic stem cell signature in cancer. Nat Genet. 2007;39(2):157–158.
  • Boyer LA, Plath K, Zeitlinger J, et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature. 2006;441(7091):349–353.
  • Yassi M, Shams Davodly E, Mojtabanezhad Shariatpanahi A, et al. DMRFusion: a differentially methylated region detection tool based on the ranked fusion method. Genomics. 2018;110(6):366–374.
  • Mishra NK, Guda C. Genome-wide DNA methylation analysis reveals molecular subtypes of pancreatic cancer. Oncotarget. 2017;8(17):28990–29012.
  • Kuasne H, Colus IM, Busso AF, et al. Genome-wide methylation and transcriptome analysis in penile carcinoma: uncovering new molecular markers. Clin Epigenetics. 2015;7(1):46.
  • Lai HC, Lin YW, Huang TH, et al. Identification of novel DNA methylation markers in cervical cancer. Int J Cancer. 2008;123(1):161–167.
  • Song MA, Tiirikainen M, Kwee S, et al. Elucidating the landscape of aberrant DNA methylation in hepatocellular carcinoma. PLoS One. 2013;8(2):e55761.
  • Kim JH, Karnovsky A, Mahavisno V, et al. LRpath analysis reveals common pathways dysregulated via DNA methylation across cancer types. BMC Genomics. 2012;13(1):526.
  • Morin RD, Mungall K, Pleasance E, et al. Mutational and structural analysis of diffuse large B-cell lymphoma using whole-genome sequencing. Blood. 2013;122(7):1256–1265.
  • Shah N, Sukumar S. The Hox genes and their roles in oncogenesis. Nat Rev Cancer. 2010;10(5):361–371.
  • Shiraishi M, Sekiguchi A, Oates AJ, et al. HOX gene clusters are hotspots of de novo methylation in CpG islands of human lung adenocarcinomas. Oncogene. 2002;21(22):3659–3662.
  • Strathdee G, Holyoake TL, Sim A, et al. Inactivation of HOXA genes by hypermethylation in myeloid and lymphoid malignancy is frequent and associated with poor prognosis. Clin Cancer Res. 2007;13(17):5048–5055.
  • Choi JH, Li Y, Guo J, et al. Genome-wide DNA methylation maps in follicular lymphoma cells determined by methylation-enriched bisulfite sequencing. PLoS One. 2010;5(9):e13020.
  • Kanduri M, Sander B, Ntoufa S, et al. A key role for EZH2 in epigenetic silencing of HOX genes in mantle cell lymphoma. Epigenetics. 2013;8(12):1280–1288.
  • Ishizaki T, Yamazaki J, Jelinek J, et al. Genome-wide DNA methylation analysis identifies promoter hypermethylation in canine malignant melanoma. Res Vet Sci. 2020;132:521–526.
  • Remacha L, Curras-Freixes M, Torres-Ruiz R, et al. Gain-of-function mutations in DNMT3A in patients with paraganglioma. Genet Med. 2018;20(12):1644–1651.
  • Velichutina I, Shaknovich R, Geng H, et al. EZH2-mediated epigenetic silencing in germinal center B cells contributes to proliferation and lymphomagenesis. Blood. 2010;116(24):5247–5255.
  • Ropa J, Saha N, and Hu H, et al. SETDB1 mediated histone H3 lysine 9 methylation suppresses MLL-fusion target expression and leukemic transformation. Haematolo-gica. 2020 105 9 2273–2285 .
  • Choi HJ, Lee HB, Park HK, et al. EZH2 expression in naturally occurring canine tumors. Comp Med. 2018;68(2):148–155.
  • Heery R, Schaefer MH. DNA methylation variation along the cancer epigenome and the identification of novel epigenetic driver events. Nucleic Acids Res. 2021;49(22):12692–12705.
  • Patani H, Rushton MD, Higham J, et al. Transition to naïve human pluripotency mirrors pan-cancer DNA hypermethylation. Nat Commun. 2020;11(1):3671.
  • Rout ED, Avery PR. Lymphoid neoplasia: correlations between morphology and flow cytometry. Vet Clin North Am Small Anim Pract. 2017;47(1):53–70.
  • Wolf-Ringwall A, Lopez L, Elmslie R, et al. Prospective evaluation of flow cytometric characteristics, histopathologic diagnosis and clinical outcome in dogs with naive B-cell lymphoma treated with a 19-week CHOP protocol. Vet Comp Oncol. 2019;18(3):342–352.
  • Ponce F, Marchal T, Magnol JP, et al. A morphological study of 608 cases of canine malignant lymphoma in France with a focus on comparative similarities between canine and human lymphoma morphology. Vet Pathol. 2010;47(3):414–433.
  • Vezzali E, Parodi AL, Marcato PS, et al. Histopathologic classification of 171 cases of canine and feline non-Hodgkin lymphoma according to the WHO. Vet Comp Oncol. 2010;8(1):38–49.
  • Valli VE, San Myint M, Barthel A, et al. Classification of canine malignant lymphomas according to the World Health Organization criteria. Vet Pathol. 2011;48(1):198–211.
  • Lautscham EM, Kessler M, Ernst T, et al. Comparison of a CHOP-LAsp-based protocol with and without maintenance for canine multicentric lymphoma. Vet Rec. 2017;180(12):303.
  • Curran K, Thamm DH. Retrospective analysis for treatment of naive canine multicentric lymphoma with a 15-week, maintenance-free CHOP protocol. Vet Comp Oncol. 2016;14(Suppl 1):147–155.
  • Burton JH, Garrett-Mayer E, Thamm DH. Evaluation of a 15-week CHOP protocol for the treatment of canine multicentric lymphoma. Vet Comp Oncol. 2013;11(4):306–315.
  • Childress MO, Ramos-Vara JA, Ruple A. Retrospective analysis of factors affecting clinical outcome following CHOP-based chemotherapy in dogs with primary nodal diffuse large B-cell lymphoma. Vet Comp Oncol. 2018;16(1):E159–E68.
  • Sorenmo K, Overley B, Krick E, et al. Outcome and toxicity associated with a dose-intensified, maintenance-free CHOP-based chemotherapy protocol in canine lymphoma: 130 cases. Vet Comp Oncol. 2010;8(3):196–208.
  • Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal. 2011;17(1):10–12.
  • Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–2120.
  • Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754–1760.
  • Lienhard M, Grimm C, Morkel M, et al. MEDIPS: genome-wide differential coverage analysis of sequencing data derived from DNA enrichment experiments. Bioinformatics. 2014;30(2):284–286.
  • Lizio M, Harshbarger J, Shimoji H, et al. Gateways to the FANTOM5 promoter level mammalian expression atlas. Genome Biol. 2015;16(1):22.
  • Lizio M, Mukarram AK, Ohno M, et al. Monitoring transcription initiation activities in rat and dog. Sci Data. 2017;4(1):170173.
  • Dreos R, Ambrosini G, Perier RC, et al. The Eukaryotic promoter database: expansion of EPDnew and new promoter analysis tools. Nucleic Acids Res. 2015;43( Database issue):D92–6.
  • Breiman L. Random Forests. Mach Learn. 2001;45(1):5–32.

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