Background
Despite advances with tyrosine kinase inhibitors (TKIs), chronic myeloid leukemia (CML) remains largely incurable due to therapy resistance and disease persistence. Leukemic stem/progenitor cells (LSPCs) survive through enhanced oxidative phosphorylation (OXPHOS). Mitochondrial DNA (mtDNA) encodes key OXPHOS components, and somatic mtDNA mutations may contribute to metabolic heterogeneity and affect therapeutic response, yet their role in CML resistance is not well understood.
Aims
We investigated the impact of mtDNA mutations on LSPC metabolism and their influence on TKI response.
Methods and Results
Total white cells from 124 CML patients at diagnosis treated with imatinib (n=80; ALLG TIDEL I/II) or nilotinib (n=44; PINNACLE/ENESTxtnd) were analysed, using remission samples or mesenchymal stem cells/hair follicles as germline controls. We identified 244 somatic mtDNA point mutations in 75% of patients (median 2/patient). Most were heteroplasmic (median VAF 9.6%), while 29 were homoplasmic (VAF ≥98%), predominantly in the D-loop control region (29 mutations in 9 patients).
Imatinib-treated patients were classified as sensitive (IM-S, n=41) or resistant (IM-Res, n=39). IM-S showed a trend toward higher mutational burden (139 vs 49 mutations, p=0.062) and had non-synonymous mutations at higher VAF (median 17% vs 6%, p=0.014); all homoplasmic mutations occurred in IM-S. D-loop mutations were more frequent in IM-S (25 vs 1, p<0.0001). Patients with ≥3 mutations had higher cumulative incidence of MMR (90% vs 68%, p=0.004) and MR4.5 (63% vs 37%, p=0.011) at 24 months. Mutations in D-loop and MT-CO1 were similarly associated with superior molecular responses.
Single-cell RNA sequencing of bone marrow LSPCs confirmed enrichment of non-synonymous mtDNA variants in IM-S (n=6) versus blast crisis patients (n=3; p=0.047) and trending versus MMR failures (n=5; p=0.056). TKI-resistant LSPCs upregulated mitochondrial biogenesis, mitochondrial gene expression, lipid metabolism, and anaplerotic pathways, consistent with enhanced OXPHOS capacity and metabolic flexibility. Seahorse analysis confirmed enhanced OXPHOS in TKI-Res cells, with higher spare respiratory capacity (126 vs 53 pmol/min/10⁵, p=0.001), while MitoTracker_green showed a modest 1.4-fold higher mitochondrial content (p=0.045).
Conclusions
These data support a model in which mtDNA mutations in IM-S patients impair mitochondrial fitness, whereas resistant LSPCs maintain metabolic flexibility, linking mitochondrial alterations to transcriptional reprogramming and TKI response.