Clonal evolution of the 3D chromatin landscape in patients with relapsed pediatric B-cell acute lymphoblastic leukemia

Nguyen, K. et al. Factors influencing survival after relapse from acute lymphoblastic leukemia: a Children’s Oncology Group study. Leukemia 22, 2142–2150 (2008).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Carroll, W. L. & Raetz, E. A. Clinical and laboratory biology of childhood acute lymphoblastic leukemia. J. Pediatr. 160, 10–18 (2012).Article 
PubMed 

Google Scholar 
Hunger, S. P. et al. Improved survival for children and adolescents with acute lymphoblastic leukemia between 1990 and 2005: a report from the children’s oncology group. J. Clin. Oncol. 30, 1663–1669 (2012).Article 
PubMed 
PubMed Central 

Google Scholar 
Park, J. H. et al. Long-term follow-up of CD19 CAR therapy in acute lymphoblastic leukemia. N. Engl. J. Med 378, 449–459 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Meyer, J. A. et al. Relapse-specific mutations in NT5C2 in childhood acute lymphoblastic leukemia. Nat. Genet 45, 290–294 (2013).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Evensen, N. A. et al. MSH6 haploinsufficiency at relapse contributes to the development of thiopurine resistance in pediatric B-lymphoblastic leukemia. Haematologica 103, 830–839 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Jones, C. L. et al. MAPK signaling cascades mediate distinct glucocorticoid resistance mechanisms in pediatric leukemia. Blood 126, 2202–2212 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Yang, J. J. et al. Genome-wide copy number profiling reveals molecular evolution from diagnosis to relapse in childhood acute lymphoblastic leukemia. Blood 112, 4178–4183 (2008).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Saint Fleur-Lominy, S. et al. Evolution of the epigenetic landscape in childhood B acute lymphoblastic leukemia and its role in drug resistance. Cancer Res. 80, 5189–5202 (2020).Article 
CAS 
PubMed Central 

Google Scholar 
Aronson, B. E. et al. A bipartite element with allele-specific functions safeguards DNA methylation imprints at the Dlk1-Dio3 locus. Dev. Cell 56, 3052–3065.e5 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Fortin, J. P. & Hansen, K. D. Reconstructing A/B compartments as revealed by Hi-C using long-range correlations in epigenetic data. Genome Biol. 16, 180 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Dixon, J. R. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376–380 (2012).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Nora, E. P. et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381–385 (2012).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Spielmann, M., Lupianez, D. G. & Mundlos, S. Structural variation in the 3D genome. Nat. Rev. Genet 19, 453–467 (2018).Article 
CAS 
PubMed 

Google Scholar 
Flavahan, W. A. et al. Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature 529, 110–114 (2016).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Lupianez, D. G. et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161, 1012–1025 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Kloetgen, A. et al. Three-dimensional chromatin landscapes in T cell acute lymphoblastic leukemia. Nat. Genet 52, 388–400 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Yusufova, N. et al. Histone H1 loss drives lymphoma by disrupting 3D chromatin architecture. Nature 589, 299–305 (2021).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Narang, S. et al. NSD2 E1099K drives relapse in pediatric acute lymphoblastic leukemia by disrupting 3D chromatin organization. Genome Biol. 24, 64 (2023).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Xu, J. et al. Subtype-specific 3D genome alteration in acute myeloid leukaemia. Nature 611, 387–398 (2022).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Pui, C. H. et al. Treating childhood acute lymphoblastic leukemia without cranial irradiation. N. Engl. J. Med. 360, 2730–2741 (2009).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Inaba, H. & Pui, C. H. Advances in the diagnosis and treatment of pediatric acute lymphoblastic leukemia. J. Clin. Med. 10, 1926 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Inaba, H. & Mullighan, C. G. Pediatric acute lymphoblastic leukemia. Haematologica 105, 2524–2539 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Lazaris, C., Kelly, S., Ntziachristos, P., Aifantis, I. & Tsirigos, A. HiC-bench: comprehensive and reproducible Hi-C data analysis designed for parameter exploration and benchmarking. BMC Genomics 18, 22 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Wang, X. et al. Genome-wide detection of enhancer-hijacking events from chromatin interaction data in rearranged genomes. Nat. Methods 18, 661–668 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Akers, N. K., Schadt, E. E. & Losic, B. STAR Chimeric Post for rapid detection of circular RNA and fusion transcripts. Bioinformatics 34, 2364–2370 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Dixon, J. R. et al. Integrative detection and analysis of structural variation in cancer genomes. Nat. Genet 50, 1388–1398 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Wang, S. et al. HiNT: a computational method for detecting copy number variations and translocations from Hi-C data. Genome Biol. 21, 73 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Robinson, J. T. et al. Juicebox.js provides a cloud-based visualization system for Hi-C data. Cell Syst. 6, 256–258.e1 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Zhang, Y. et al. PDGFRB mutation and tyrosine kinase inhibitor resistance in Ph-like acute lymphoblastic leukemia. Blood 131, 2256–2261 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Pui, C. H., Roberts, K. G., Yang, J. J. & Mullighan, C. G. Philadelphia chromosome-like acute lymphoblastic leukemia. Clin. Lymphoma Myeloma Leuk. 17, 464–470 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Devoucoux, M. et al. Oncogenic ZMYND11-MBTD1 fusion protein anchors the NuA4/TIP60 histone acetyltransferase complex to the coding region of active genes. Cell Rep. 39, 110947 (2022).Article 
CAS 
PubMed 

Google Scholar 
Feng, Y., Li, L., Du, Y., Peng, X. & Chen, F. E2F4 functions as a tumour suppressor in acute myeloid leukaemia via inhibition of the MAPK signalling pathway by binding to EZH2. J. Cell Mol. Med 24, 2157–2168 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Ouyang, X., Handoko, S. D. & Kwoh, C. K. CScore: a simple yet effective scoring function for protein-ligand binding affinity prediction using modified CMAC learning architecture. J. Bioinform Comput Biol. 9, 1–14 (2011).Article 
PubMed 

Google Scholar 
Smith, C. A. & Fan, G. The saga of JAK2 mutations and translocations in hematologic disorders: pathogenesis, diagnostic and therapeutic prospects, and revised World Health Organization diagnostic criteria for myeloproliferative neoplasms. Hum. Pathol. 39, 795–810 (2008).Article 
CAS 
PubMed 

Google Scholar 
Mullighan, C. G. et al. JAK mutations in high-risk childhood acute lymphoblastic leukemia. Proc. Natl Acad. Sci. USA 106, 9414–9418 (2009).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Tirado, C. A. et al. Novel JAK2 rearrangement resulting from a t(9;22)(p24;q11.2) in B-acute lymphoblastic leukemia. Leuk. Res 34, 1674–1676 (2010).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Waanders, E. et al. Mutational landscape and patterns of clonal evolution in relapsed pediatric acute lymphoblastic leukemia. Blood Cancer Discov. 1, 96–111 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Lee, J. W. et al. DACH1 regulates cell cycle progression of myeloid cells through the control of cyclin D, Cdk 4/6 and p21Cip1. Biochem Biophys. Res Commun. 420, 91–95 (2012).Article 
CAS 
PubMed 

Google Scholar 
Chen, Y., Xiang, H., Zhang, Y., Wang, J. & Yu, G. Loss of PCDH9 is associated with the differentiation of tumor cells and metastasis and predicts poor survival in gastric cancer. Clin. Exp. Metastasis 32, 417–428 (2015).Article 
CAS 
PubMed 

Google Scholar 
Lv, J. et al. PCDH9 acts as a tumor suppressor inducing tumor cell arrest at G0/G1 phase and is frequently methylated in hepatocellular carcinoma. Mol. Med Rep. 16, 4475–4482 (2017).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Wang, C. et al. Dual inhibition of PCDH9 expression by miR-215-5p up-regulation in gliomas. Oncotarget 8, 10287–10297 (2017).Article 
PubMed 

Google Scholar 
Wang, C. et al. Downregulation of PCDH9 predicts prognosis for patients with glioma. J. Clin. Neurosci. 19, 541–545 (2012).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Xiao, X. et al. The Gene Encoding Protocadherin 9 (PCDH9), a Novel Risk Factor for Major Depressive Disorder. Neuropsychopharmacology 43, 1128–1137 (2018).Article 
CAS 
PubMed 

Google Scholar 
Chen, E. Y. et al. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinforma. 14, 128 (2013).Article 

Google Scholar 
Kuleshov, M. V. et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res 44, W90–W97 (2016).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Xie, Z. et al. Gene Set Knowledge Discovery with Enrichr. Curr. Protoc. 1, e90 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Hogan, L. E. et al. Integrated genomic analysis of relapsed childhood acute lymphoblastic leukemia reveals therapeutic strategies. Blood 118, 5218–5226 (2011).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Kaul, A., Bhattacharyya, S. & Ay, F. Identifying statistically significant chromatin contacts from Hi-C data with FitHiC2. Nat. Protoc. 15, 991–1012 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Ay, F., Bailey, T. L. & Noble, W. S. Statistical confidence estimation for Hi-C data reveals regulatory chromatin contacts. Genome Res 24, 999–1011 (2014).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Sheffield, N. C. & Bock, C. LOLA: enrichment analysis for genomic region sets and regulatory elements in R and Bioconductor. Bioinformatics 32, 587–589 (2016).Article 
CAS 
PubMed 

Google Scholar 
Fragoso, R. et al. VEGFR-1 (FLT-1) activation modulates acute lymphoblastic leukemia localization and survival within the bone marrow, determining the onset of extramedullary disease. Blood 107, 1608–1616 (2006).Article 
CAS 
PubMed 

Google Scholar 
Chow, Y. P., Alias, H. & Jamal, R. Meta-analysis of gene expression in relapsed childhood B-acute lymphoblastic leukemia. BMC Cancer 17, 120 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Oshima, K. et al. Mutational and functional genetics mapping of chemotherapy resistance mechanisms in relapsed acute lymphoblastic leukemia. Nat. Cancer 1, 1113–1127 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
MN1 Linked to syndrome characterized by craniofacial abnormalities and severe developmental delay. Am J Med Genet A 182, 615–616 (2020).Carella, C. et al. MN1 overexpression is an important step in the development of inv(16) AML. Leukemia 21, 1679–1690 (2007).Article 
CAS 
PubMed 

Google Scholar 
Kang, S. & Hong, S. Molecular pathogenesis of spinocerebellar ataxia type 1 disease. Mol. Cells 27, 621–627 (2009).Article 
CAS 
PubMed 

Google Scholar 
Alluri, R. V. et al. Molecular analysis of CAG repeats at five different spinocerebellar ataxia loci: correlation and alternative explanations for disease pathogenesis. Mol. Cells 24, 338–342 (2007).Article 
CAS 
PubMed 

Google Scholar 
Li, J. et al. ZMYND11-MBTD1 induces leukemogenesis through hijacking NuA4/TIP60 acetyltransferase complex and a PWWP-mediated chromatin association mechanism. Nat. Commun. 12, 1045 (2021).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Yuan, F. et al. A Novel Immune Classification for Predicting Immunotherapy Responsiveness in Patients With Adamantinomatous Craniopharyngioma. Front Neurol. 12, 704130 (2021).Article 
PubMed 
PubMed Central 

Google Scholar 
Jiang, Y. et al. [Study on expression and mechanism of serum differential proteins after rush immunotherapy of allergic rhinitis]. Lin. Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 34, 683–689 (2020).
Google Scholar 
Reardon, D. A., Hanson, C. A., Roth, M. S. & Castle, V. P. Lineage switch in Philadelphia chromosome-positive acute lymphoblastic leukemia. Cancer 73, 1526–1532 (1994).Article 
CAS 
PubMed 

Google Scholar 
Grosveld, G. C. MN1, a novel player in human AML. Blood Cells Mol. Dis. 39, 336–339 (2007).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Relling, M. V. et al. Pharmacogenetic risk factors for osteonecrosis of the hip among children with leukemia. J. Clin. Oncol. 22, 3930–3936 (2004).Article 
PubMed 

Google Scholar 
Sherief, L. M. et al. Genetic polymorphism of vitamin D receptors and plasminogen activator inhibitor-1 and osteonecrosis risk in childhood acute lymphoblastic leukemia. Mol. Genet Genom. Med. 9, e1700 (2021).Article 
CAS 

Google Scholar 
Toth, K. et al. Retinoids enhance glucocorticoid-induced apoptosis of T cells by facilitating glucocorticoid receptor-mediated transcription. Cell Death Differ. 18, 783–792 (2011).Article 
CAS 
PubMed 

Google Scholar 
Lee, Y. et al. ATXN1 protein family and CIC regulate extracellular matrix remodeling and lung alveolarization. Dev. Cell 21, 746–757 (2011).Article 
CAS 
PubMed Central 

Google Scholar 
Safaei, S. et al. Double sword role of EZH2 in leukemia. Biomed. Pharmacother. 98, 626–635 (2018).Article 
CAS 
PubMed 

Google Scholar 
Pierro, J. et al. The NSD2 p.E1099K Mutation Is Enriched at Relapse and Confers Drug Resistance in a Cell Context-Dependent Manner in Pediatric Acute Lymphoblastic Leukemia. Mol. Cancer Res 18, 1153–1165 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Li, J. et al. PRC2 Inhibitors Overcome Glucocorticoid Resistance Driven by NSD2 Mutation in Pediatric Acute Lymphoblastic Leukemia. Cancer Discov. 12, 186–203 (2022).Martens, J. H. et al. PML-RARalpha/RXR Alters the Epigenetic Landscape in Acute Promyelocytic Leukemia. Cancer Cell 17, 173–185 (2010).Article 
CAS 
PubMed 

Google Scholar 
Churchman, M. L. et al. Efficacy of Retinoids in IKZF1-Mutated BCR-ABL1 Acute Lymphoblastic Leukemia. Cancer Cell 28, 343–356 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Kaufmann, K. B. et al. A novel murine model of myeloproliferative disorders generated by overexpression of the transcription factor NF-E2. J. Exp. Med. 209, 35–50 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Mullighan, C. G. et al. CREBBP mutations in relapsed acute lymphoblastic leukaemia. Nature 471, 235–239 (2011).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Fu, Y. et al. The histone demethylase PHF8 promotes adult acute lymphoblastic leukemia through interaction with the MEK/ERK signaling pathway. Biochem Biophys. Res. Commun. 496, 981–987 (2018).Article 
CAS 
PubMed 

Google Scholar 
Buenrostro, J. D., Wu, B., Chang, H. Y. & Greenleaf, W. J. ATAC-seq: A Method for Assaying Chromatin Accessibility Genome-Wide. Curr. Protoc. Mol. Biol. 109, 21 29 1–21 29 9 (2015).PubMed 

Google Scholar 
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).Article 
CAS 
PubMed 

Google Scholar 
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).Article 
CAS 
PubMed 

Google Scholar 
Ramirez, F., Dundar, F., Diehl, S., Gruning, B. A. & Manke, T. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res 42, W187–W191 (2014).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Tarasov, A., Vilella, A. J., Cuppen, E., Nijman, I. J. & Prins, P. Sambamba: fast processing of NGS alignment formats. Bioinformatics 31, 2032–2034 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).Article 
PubMed 
PubMed Central 

Google Scholar 
Ross-Innes, C. S. et al. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature 481, 389–393 (2012).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Yu, G., Wang, L. G. & He, Q. Y. ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics 31, 2382–2383 (2015).Article 
CAS 
PubMed 

Google Scholar 
Imakaev, M. et al. Iterative correction of Hi-C data reveals hallmarks of chromosome organization. Nat. Methods 9, 999–1003 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Wang, X., Luan, Y. & Yue, F. EagleC: A deep-learning framework for detecting a full range of structural variations from bulk and single-cell contact maps. Sci. Adv. 8, eabn9215 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Haas, B. J. et al. Accuracy assessment of fusion transcript detection via read-mapping and de novo fusion transcript assembly-based methods. Genome Biol. 20, 213 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Quinlan, A. R. BEDTools: The Swiss-Army Tool for Genome Feature Analysis. Curr. Protoc. Bioinforma. 47, 11 12 1–11 12 34 (2014).Article 

Google Scholar