bims-almceb Biomed News
on Acute Leukemia Metabolism and Cell Biology
Issue of 2022–05–22
eleven papers selected by
Camila Kehl Dias, Federal University of Rio Grande do Sul



  1. Front Oncol. 2022 ;12 899502
      Acute myeloid leukemia (AML) is a heterogeneous hematologic malignancy characterized by multiple cytogenetic and molecular abnormalities, with a very poor prognosis. Current treatments for AML often fail to eliminate leukemic stem cells (LSCs), which perpetuate the disease. LSCs exhibit a unique metabolic profile, especially dependent on oxidative phosphorylation (OXPHOS) for energy production. Whereas, normal hematopoietic stem cells (HSCs) and leukemic blasts rely on glycolysis for adenosine triphosphate (ATP) production. Thus, understanding the regulation of OXPHOS in LSCs may offer effective targets for developing clinical therapies in AML. This review summarizes these studies with a focus on the regulation of the electron transport chain (ETC) and tricarboxylic acid (TCA) cycle in OXPHOS and discusses potential therapies for eliminating LSCs.
    Keywords:  electron transport chain; leukemic stem cells (LSCs); mitochondria; oxidative phosphorylation (OXPHOS); tricarboxylic acid cycle (TCA cycle)
    DOI:  https://doi.org/10.3389/fonc.2022.899502
  2. Crit Rev Oncol Hematol. 2022 May 16. pii: S1040-8428(22)00134-2. [Epub ahead of print] 103710
      Relapse is common in acute myeloid leukemia (AML) and thought to be due to resistance of underlying leukemic stem cells (LSCs) to current standard therapies, although a lack of tools to measure the quantity and quality of these cells in patients precludes the clinical testing of this concept. This review discusses the current knowledge of LSC properties and appraises strategies aimed to bring the therapeutic targeting of LSCs to the bedside to improve patient outcomes. We highlight pathways and targets of interest and summarize available information on drugs that might eradicate LSCs. Future research is needed to close identified gaps in knowledge and provide evidence for the clinical efficacy of LSC-directed therapies to support the development of treatments that eliminate residual disease and prevent relapse, thereby increasing the cure rates of patients with AML.
    Keywords:  acute myeloid leukemia; leukemic stem cells; measurable residual disease
    DOI:  https://doi.org/10.1016/j.critrevonc.2022.103710
  3. Nat Commun. 2022 May 19. 13(1): 2801
      T-cell acute lymphoblastic leukemia (T-ALL) is commonly driven by activating mutations in NOTCH1 that facilitate glutamine oxidation. Here we identify oxidative phosphorylation (OxPhos) as a critical pathway for leukemia cell survival and demonstrate a direct relationship between NOTCH1, elevated OxPhos gene expression, and acquired chemoresistance in pre-leukemic and leukemic models. Disrupting OxPhos with IACS-010759, an inhibitor of mitochondrial complex I, causes potent growth inhibition through induction of metabolic shut-down and redox imbalance in NOTCH1-mutated and less so in NOTCH1-wt T-ALL cells. Mechanistically, inhibition of OxPhos induces a metabolic reprogramming into glutaminolysis. We show that pharmacological blockade of OxPhos combined with inducible knock-down of glutaminase, the key glutamine enzyme, confers synthetic lethality in mice harboring NOTCH1-mutated T-ALL. We leverage on this synthetic lethal interaction to demonstrate that IACS-010759 in combination with chemotherapy containing L-asparaginase, an enzyme that uncovers the glutamine dependency of leukemic cells, causes reduced glutaminolysis and profound tumor reduction in pre-clinical models of human T-ALL. In summary, this metabolic dependency of T-ALL on OxPhos provides a rational therapeutic target.
    DOI:  https://doi.org/10.1038/s41467-022-30396-3
  4. Redox Biol. 2022 May 13. pii: S2213-2317(22)00109-4. [Epub ahead of print]53 102337
      Recent studies demonstrate that redox imbalance of NAD+/NADH and NADP+/NADPH pairs due to impaired respiration may trigger two "hidden" metabolic pathways on the crossroad between mitochondrial dysfunction, senescence, and proliferation: "β-oxidation shuttle" and "hydride transfer complex (HTC) cycle". The "β-oxidation shuttle" induces NAD+/NADH redox imbalance in mitochondria, while HTC cycle maintains the redox balance of cytosolic NAD+/NADH, increasing the redox disbalance of NADP+/NADPH. Senescence appears to depend on high cytoplasmic NADH but low NADPH, while proliferation depends on high cytoplasmic NAD+ and NADPH that are under mitochondrial control. Thus, activating or deactivating the HTC cycle can be crucial to cell fate - senescence or proliferation. These pathways are a source of enormous cataplerosis. They support the production of large amounts of NADPH and intermediates for lipid synthesis and membrane biogenesis, as well as for DNA synthesis.
    DOI:  https://doi.org/10.1016/j.redox.2022.102337
  5. Ann Transl Med. 2022 Apr;10(8): 490
       Background: To evaluate whether homoharringtonine (HHT) combined with venetoclax could produce a synergistic anti-acute myeloid leukemia (AML) effect and determine the underlying mechanisms.
    Methods: The effect of HHT and venetoclax combination on cell viability, apoptosis, and mitochondrial membrane potential was investigated in vitro using AML cell lines and primary cells. High-throughput mRNA sequencing was used to analyze mRNA level changes after the application of HHT and venetoclax on OCI-AML3 cells. Western blotting was used to verify the changes in protein expression within the mitogen-activated protein kinases/extracellular signal-regulated kinase (MAPK/ERK), phosphatidylinositiol 3-kinase (PI3K)/AKT and p53 pathway. The efficacy of HHT and venetoclax in vivo and their effects on survival time were evaluated in a xenograft model established in severe immunodeficiency (NOD/SCID) mice.
    Results: Venetoclax and HHT synergistically inhibited the proliferation of AML cells, decreased the mitochondrial membrane potential, and promoted AML cell apoptosis in a time- and concentration-dependent manner. Venetoclax combined with HHT increased the expression of the caspase-3, Poly (ADP-ribose) polymerase (PARP), and γH2AX proteins. HHT enhanced the proapoptotic effect of venetoclax by reducing the expression of myeloid cell leukemia sequence 1 (Mcl-1). HHT arrested AML cells in G1 phase of the cell cycle. HHT enhanced the proapoptotic effect of venetoclax by inhibiting the activation of the MAPK/ERK and PI3K/AKT pathways and activating the p53 pathway. In vivo experiments confirmed that the combination of HHT and venetoclax could inhibit the growth of tumors in AML xenotransplanted mice and prolong the survival time of tumor-bearing mice.
    Conclusions: HHT combined with venetoclax synergistically promoted apoptosis in AML cell lines and primary cells by inhibiting the activation of the MAPK/ERK and PI3K/AKT pathways and activating the p53 pathway.
    Keywords:  Homoharringtonine (HHT); acute myeloid leukemia (AML); apoptosis; mechanism; venetoclax
    DOI:  https://doi.org/10.21037/atm-22-1459
  6. Immunol Cell Biol. 2022 May 16.
      Leukemia and lymphoma-the most common hematological malignant diseases-are often accompanied by complications such as drug resistance, refractory diseases, and relapse. Amino acids are important energy sources for malignant cells. Tumor-mediated amino acid metabolism is associated with the immunosuppressive properties of the tumor microenvironment, thereby assisting malignant cells to evade immune surveillance. Targeting abnormal amino acid metabolism in the tumor microenvironment may be an effective therapeutic approach to address the therapeutic challenges of leukemia and lymphoma. Here, we review the effects of glutamine, arginine, and tryptophan metabolism on tumorigenesis and immunomodulation, and define the differences between tumor cells and immune effector cells. We also comment on treatments targeting these amino acid metabolism pathways in lymphoma and leukemia and discuss how these treatments have profound adverse effects on tumor cells, but leave the immune cells unaffected or mildly affected.
    Keywords:  amino acid metabolism; immunomodulation; leukemia; lymphoma; tumor microenvironment
    DOI:  https://doi.org/10.1111/imcb.12557
  7. Cancer Drug Resist. 2022 ;5(1): 233-244
      Despite the outstanding advances in understanding the biology underlying the pathophysiology of acute myeloid leukemia (AML) and the promising preclinical data published lastly, AML treatment still relies on a classic chemotherapy regimen largely unchanged for the past five decades. Recently, new drugs have been approved for AML, but the real clinical benefit is still under evaluation. Nevertheless, primary refractory and relapse AML continue to represent the main clinical challenge, as the majority of AML patients will succumb to the disease despite achieving a complete remission during the induction phase. As such, treatments for chemoresistant AML represent an unmet need in this disease. Although great efforts have been made to decipher the biological basis for leukemogenesis, the mechanism by which AML cells become resistant to chemotherapy is largely unknown. The identification of the signaling pathways involved in resistance may lead to new combinatory therapies or new therapeutic approaches suitable for this subset of patients. Several mechanisms of chemoresistance have been identified, including drug transporters, key secondary messengers, and metabolic regulators. However, no therapeutic approach targeting chemoresistance has succeeded in clinical trials, especially due to broad secondary effects in healthy cells. Recent research has highlighted the importance of lysosomes in this phenomenon. Lysosomes' key role in resistance to chemotherapy includes the potential to sequester drugs, central metabolic signaling role, and gene expression regulation. These results provide further evidence to support the development of new therapeutic approaches that target lysosomes in AML.
    Keywords:  AML; Lysosome; chemoresistance; lysosomal sequestration; lysosomotropic drug; refractory AML
    DOI:  https://doi.org/10.20517/cdr.2021.122
  8. Cancer Drug Resist. 2020 ;3(3): 252-275
      Immune checkpoint inhibitors (ICIs) have revolutionized the treatment of cancer over the last decade, bringing about a paradigm shift in systemic cancer therapy away from traditional cytotoxic and targeted therapies. While some patients have dramatic treatment responses, it is sobering to note that most tumors are either resistant at the outset, or develop resistance after initial response. A major area of translational and clinical research is in identifying therapeutic strategies to overcome resistance to ICIs. We have performed an in-depth review of the different mechanisms of resistance and potential avenues to overcome resistance through rationally designed combination treatment with ICIs.
    Keywords:  CTLA-4; Immunotherapy resistance; PD-1; PD-L1; tumor microenvironment
    DOI:  https://doi.org/10.20517/cdr.2020.11
  9. Cancer Drug Resist. 2021 ;4(2): 503-511
      Cancer cells are highly proliferative, invasive, metastatic and initiate angiogenesis. These activities demand plentiful energy and bountiful stores of anabolic precursors, a situation that puts significant strain on metabolic pathways and necessitates juggling of finite resources. However, the location and erratic structural organisation of tumours means they reside in a nutrient-poor environment. The glycolytic phenotype has evolved in cancer cells to provide a suitable balance between bioenergetic and biosynthetic pathways. Does this adopted strategy also support the overexpression of an ATP-dependent transporter (P-glycoprotein) to maintain resistance against chemotherapy? This article highlights the metabolic adaptations used by cancer cells to maintain both a glycolytic phenotype and sustain the activity of P-glycoprotein. We argue that these cells negotiate an energy precipice to achieve these adaptations. Finally, we advocate the use of compounds that place resistant cells expressing P-glycoprotein under further metabolic strain and how uncoupling protein-2 may provide an ideal target for them.
    Keywords:  P-glycoprotein; chemotherapy; collateral sensitivity; glycolytic phenotype; mitochondria; multidrug resistance; uncoupling protein
    DOI:  https://doi.org/10.20517/cdr.2020.105
  10. Nature. 2022 May 18.
      
    Keywords:  Cancer; Medical research; Metabolism
    DOI:  https://doi.org/10.1038/d41586-022-01301-1
  11. Nature. 2022 May 18.
      Cancer metastasis requires the transient activation of cellular programs enabling dissemination and seeding in distant organs1. Genetic, transcriptional and translational heterogeneity contributes to this dynamic process2,3. Metabolic heterogeneity has also been observed4, yet its role in cancer progression is less explored. Here we find that the loss of phosphoglycerate dehydrogenase (PHGDH) potentiates metastatic dissemination. Specifically, we find that heterogeneous or low PHGDH expression in primary tumours of patients with breast cancer is associated with decreased metastasis-free survival time. In mice, circulating tumour cells and early metastatic lesions are enriched with Phgdhlow cancer cells, and silencing Phgdh in primary tumours increases metastasis formation. Mechanistically, Phgdh interacts with the glycolytic enzyme phosphofructokinase, and the loss of this interaction activates the hexosamine-sialic acid pathway, which provides precursors for protein glycosylation. As a consequence, aberrant protein glycosylation occurs, including increased sialylation of integrin αvβ3, which potentiates cell migration and invasion. Inhibition of sialylation counteracts the metastatic ability of Phgdhlow cancer cells. In conclusion, although the catalytic activity of PHGDH supports cancer cell proliferation, low PHGDH protein expression non-catalytically potentiates cancer dissemination and metastasis formation. Thus, the presence of PHDGH heterogeneity in primary tumours could be considered a sign of tumour aggressiveness.
    DOI:  https://doi.org/10.1038/s41586-022-04758-2