Aim:
Characterising the genomic landscape of ZNF384-rearranged (ZNF384r) B-cell acute lymphoblastic leukaemia (B-ALL) will reveal subtype specific genomic alterations and define targetable pathways for assessment in precision therapeutic approaches.
Method:
Philadelphia chromosome-negative B-ALL samples (n=487) were transcriptionally sequenced to identify fusion genes and single nucleotide variants (SNV), and gene deletions were detected by multiplex ligation-dependent probe amplification. Signalling pathways were assessed on the EP300-ZNF384 driven human JIH-5 cell line by intracellular flow cytometry of STAT1/3/5 phosphorylation in the presence or absence of inhibitors.
Results:
Transcriptomic sequencing identified ZNF384r in 3.7% (18/487) of Ph-neg B-ALL at diagnosis (comprising children 1.4% (3/210), adolescent young adults 6.1% (10/165), adults 4.5% (5/112)). The 5’-partners identified were EP300(72%, 13/18), TCF3 (17%, 3/18), ARID1B (5.6%, 1/18) and CREBBP (5.6%, 1/18). IKZF1, RB1, CDKN2A, and PAX5 deletions (7% each, 1/14) occurred less frequently than deletions in ETV6 (35.6%, 5/14), BTG (21.4%, 3/14) and CDKN2B (21.4%, 3/14). SNVs were detected in RAS 27.8% (5/18), PTPN11 (5.6%, 1/18), JAK2 (5.6%, 1/18) and CREBBP (11.1%, 2/18). In relapse samples EP300 or TCF3 were the most common fusion partner, (37.5%, 3/8), in addition to 12.5% (1/8) TAF15 and 12.5% CREBBP. Upregulation of CLCF1, CXCL2, FLT3, STAT2, ICAM2, MMP11and SPKH1 gene expression was detected in ZNF384r B-ALL. An in vitro model of ZNF384r B-ALL demonstrated intrinsic phosphorylation of STAT3, (consistent with JAK/STAT signalling upregulation observed in ZNF384r B-ALL Gene-set enrichment analysis), but not STAT1 or STAT5. Dasatinib and ruxolitinib were unable to abrogate STAT3 phosphorylation, while dasatinib reduced JIH-5 total tyrosine-phosphorylation. Pathways involved in ZNF384-fusions are currently under investigation.
Conclusion:
We have characterised the transcriptome of one of the largest ZNF384r B-ALL cohorts and have revealed subtype specific targets warranting investigation for future precision approaches to therapy.