bims-glucam Biomed News
on Glutamine cancer metabolism
Issue of 2021–09–19
fourteen papers selected by
Sreeparna Banerjee, Middle East Technical University



  1. Neuro Oncol. 2021 Sep 13. pii: noab219. [Epub ahead of print]
       BACKGROUND: We postulate that meningiomas undergo distinct metabolic reprogramming in tumorigenesis and unravelling their metabolic phenotypes provide new therapeutic insights. Glutamine catabolism is key to the growth and proliferation of tumors. Here, we investigated the metabolomics of freshly resected meningiomas and glutamine metabolism in patient-derived meningioma cells.
    METHODS: 1H NMR spectroscopy of tumor tissues from 33 meningioma patients was used to differentiate the metabolite profiles of grade-I and grade-II meningiomas. Glutamine metabolism was examined using 13C/ 15N glutamine tracer, in five patient-derived meningioma cells.
    RESULTS: Alanine, lactate, glutamate, glutamine, and glycine were predominantly elevated only in grade-II meningiomas by 74%, 76%, 35%, 75% and 33% respectively, with alanine, and glutamine being statistically significant (p ≤ 0.02). 13C/ 15N glutamine tracer experiments revealed that both grade-I and -II meningiomas actively metabolize glutamine to generate various key carbon intermediates including alanine and proline that are necessary for the tumor growth. Also, it is shown that glutaminase (GLS1) inhibitor, CB-839 is highly effective in downregulating glutamine metabolism and decreasing proliferation in meningioma cells.
    CONCLUSION: Alanine and glutamine/glutamate are mainly elevated in grade-II meningiomas. Grade-I meningiomas possess relatively higher glutamine metabolism providing carbon/nitrogen for the biosynthesis of key nonessential amino acids. GLS1 inhibitor (CB-839) would be very effective in downregulating glutamine metabolic pathways in grade-I meningiomas leading to decreased cellular proliferation.
    Keywords:  alanine; glutamine; meningioma; metabolic flux analysis; metabolomics
    DOI:  https://doi.org/10.1093/neuonc/noab219
  2. Mol Cancer Ther. 2021 Sep 13. pii: molcanther.0071.2021. [Epub ahead of print]
      Acute myeloid leukemia (AML) with a FLT3 internal tandem duplication (FLT3-ITD) mutation is an aggressive hematologic malignancy associated with frequent relapse and poor overall survival. The tyrosine kinase inhibitor gilteritinib is approved for the treatment of relapse/refractory AML with FLT3 mutations, yet its mechanism of action is not completely understood. Here, we sought to identify additional therapeutic targets that can be exploited to enhance gilteritinib's anti-leukemic effect. Based on unbiased transcriptomic analyses, we identified the glutamine transporter SNAT1 (SLC38A1) as a novel target of gilteritinib that leads to impaired glutamine uptake and utilization within leukemic cells. Using metabolomics and metabolic flux analyses, we found that gilteritinib decreased glutamine metabolism through the TCA cycle and cellular levels of the oncometabolite 2-hydroxyglutarate. Additionally, gilteritinib treatment was associated with decreased ATP production and glutathione synthesis and increased reactive oxygen species, resulting in cellular senescence. Lastly, we found that the glutaminase inhibitor CB-839 enhanced anti-leukemic effect of gilteritinib in ex vivo studies using human primary FLT3-ITD-positive AML cells harboring mutations in the enzyme isocitrate dehydrogenase, which catalyzes the oxidative decarboxylation of isocitrate, producing α-ketoglutarate. Collectively, this work has identified a previously unrecognized, gilteritinib-sensitive metabolic pathway downstream of SLC38A1 that causes decreased glutaminolysis and disruption of redox homeostasis. These findings provide a rationale for the development and therapeutic exploration of targeted combinatorial treatment strategies for this subset of relapse/refractory AML.
    DOI:  https://doi.org/10.1158/1535-7163.MCT-21-0071
  3. Gastroenterology. 2021 Sep 14. pii: S0016-5085(21)03496-X. [Epub ahead of print]
       BACKGROUND AND AIMS: A major clinical challenge for pancreatic cancer (PC) patients is metabolic adaptation. Neoplastic cells harboring molecular perturbations suffice for their increased anabolic demand and nucleotide biosynthesis to acquire chemoresistance. The mucin 5AC expressed de novo in malignant pancreas promotes cancer cell stemness and is significantly associated with poor patient survival. Identification of MUC5AC-associated drivers of chemoresistance through metabolic alterations may facilitate sculpting a new combinatorial regimen.
    METHODS: The contribution of MUC5AC on glutaminolysis and gemcitabine resistance were examined by TCGA data analysis, RNA sequencing, and immunohistochemistry analysis on pancreatic tissues of KrasG12D; Pdx1-Cre (KC) and KrasG12D; Pdx1-Cre; Muc5ac-/- (KCM) mice. These were followed by metabolite flux assays, biochemical and xenograft studies on MUC5AC-depleted human and murine PC cells. Murine and human pancreatic 3D-tumoroids were used to evaluate gemcitabine's efficacy in combination with β-catenin and glutaminolysis inhibitors.
    RESULTS: Transcriptional analysis demonstrated that high MUC5AC-expressing human and autochthonous murine PC tumors exhibit higher resistance to gemcitabine due to enhanced glutamine utilization and nucleotide biosynthesis. Gemcitabine treatment led to MUC5AC overexpression, resulting in disruption of E-Cadherin/β-catenin junctions and the nuclear translocation of β-catenin, which increased c-Myc expression with a concomitant rise in glutamine uptake and glutamate release. MUC5AC-depletion and glutamine deprivation sensitized human PC cells to gemcitabine, which was obviated by glutamine replenishment in MUC5AC-expressing cells. Co-administration of β-catenin and glutaminolysis inhibitors with gemcitabine abrogated the MUC5AC-mediated resistance in murine and human tumoroids.
    CONCLUSIONS: MUC5AC/β-catenin/c-Myc axis increases the uptake and utilization of glutamine in PC cells and co-targeting this axis along with gemcitabine may improve the therapeutic efficacy in PC.
    Keywords:  c-Myc; gemcitabine; glutamine; pancreatic cancer; β-catenin
    DOI:  https://doi.org/10.1053/j.gastro.2021.09.017
  4. Genes Dis. 2021 Nov;8(6): 731-745
      Cystine/glutamate antiporter solute carrier family 7 member 11 (SLC7A11; also known as xCT) plays a key role in antioxidant defense by mediating cystine uptake, promoting glutathione synthesis, and maintaining cell survival under oxidative stress conditions. Recent studies showed that, to prevent toxic buildup of highly insoluble cystine inside cells, cancer cells with high expression of SLC7A11 (SLC7A11high) are forced to quickly reduce cystine to more soluble cysteine, which requires substantial NADPH supply from the glucose-pentose phosphate pathway (PPP) route, thereby inducing glucose- and PPP-dependency in SLC7A11high cancer cells. Limiting glucose supply to SLC7A11high cancer cells results in significant NADPH "debt", redox "bankruptcy", and subsequent cell death. This review summarizes our current understanding of NADPH-generating and -consuming pathways, discusses the opposing role of SLC7A11 in protecting cells from oxidative stress-induced cell death such as ferroptosis but promoting glucose starvation-induced cell death, and proposes the concept that SLC7A11-mediated cystine uptake acts as a double-edged sword in cellular redox regulation. A detailed understanding of SLC7A11 in redox biology may identify metabolic vulnerabilities in SLC7A11high cancer for therapeutic targeting.
    Keywords:  Cysteine; Cystine; NADPH; Pentose phosphate pathway; SLC7A11; xCT
    DOI:  https://doi.org/10.1016/j.gendis.2020.11.010
  5. Cancer Cell Int. 2021 Sep 16. 21(1): 495
       BACKGROUND: Increasing studies focused on the regulatory roles of circular RNAs (circRNAs) in diverse cancers. This study was to evaluate the function and mechanism of circRNA Scm-like with four malignant brain tumor domains 2 (circ-SFMBT2) in esophageal cancer (EC).
    METHODS: The circ-SFMBT2, microRNA-107 (miR-107) and solute-linked carrier family A1 member 5 (SLC1A5) levels were analyzed by quantitative real-time polymerase chain reaction (qRT-PCR). Cell proliferation was evaluated by 3-(4, 5-dimethylthiazol-2-y1)-2, 5-diphenyl tetrazolium bromide (MTT) assay, colony formation assay and EdU assay. Cell apoptosis and invasion were detected by flow cytometry and transwell assay. Glutamine metabolism was assessed by the corresponding kits for glutamine consumption, α-ketoglutarate production and glutamate production. Western blot was used for protein quantification. The binding analysis was performed using dual-luciferase reporter assay, RNA immunoprecipitation (RIP) and pull-down assays. The functional research of circ-SFMBT2 in vivo was performed by xenograft tumor assay. Exosomes were identified by morphological observation and protein detection.
    RESULTS: Circ-SFMBT2 was overexpressed in EC samples and cells. Circ-SFMBT2 downregulation inhibited EC cell proliferation, invasion and glutamine metabolism. Circ-SFMBT2 targeted miR-107 and the regulation of circ-SFMBT2 was achieved by sponging miR-107. SLC1A5 was a target of miR-107, and it worked as an oncogene in EC cells. MiR-107 retarded the EC progression by downregulating SLC1A5. Circ-SFMBT2 could affect the SLC1A5 expression by targeting miR-107. Circ-SFMBT2 regulated EC progression in vivo by miR-107/SLC1A5 axis. Circ-SFMBT2 was transferred by exosomes in EC cells.
    CONCLUSION: These results suggested that circ-SFMBT2 upregulated the SLC1A5 expression to promote the malignant development of EC by serving as a miR-107 sponge.
    Keywords:  Circ-SFMBT2; Esophageal cancer; SLC1A5; miR-107
    DOI:  https://doi.org/10.1186/s12935-021-02156-8
  6. Mol Carcinog. 2021 Sep 17.
      Cancer cells undergo metabolic reprogramming to support increased demands in bioenergetics and biosynthesis and to maintain reactive oxygen species at optimum levels. As metabolic alterations are broadly observed across many cancer types, metabolic reprogramming is considered a hallmark of cancer. A metabolic alteration commonly seen in cancer cells is an increased demand for certain amino acids. Amino acids are involved in a wide range of cellular functions, including proliferation, redox balance, bioenergetic and biosynthesis support, and homeostatic functions. Thus, targeting amino acid dependency in cancer is an attractive strategy for a number of cancers. In particular, pharmacologically mediated amino acid depletion has been evaluated as a cancer treatment option for several cancers. Amino acids that have been investigated for the feasibility of drug-induced depletion in preclinical and clinical studies for cancer treatment include arginine, asparagine, cysteine, glutamine, lysine, and methionine. In this review, we will summarize the status of current research on pharmacologically mediated amino acid depletion as a strategy for cancer treatment and potential chemotherapeutic combinations that synergize with amino acid depletion to further inhibit tumor growth and progression.
    Keywords:  amino acid depletion; amino acid metabolism; cancer; cancer therapy; metabolic reprogramming
    DOI:  https://doi.org/10.1002/mc.23349
  7. Theranostics. 2021 ;11(18): 9089-9106
      Rationale: Cancer cells rely on glucose metabolism for fulfilling their high energy demands. We previously reported that monoethanolamine (Etn), an orally deliverable lipid formulation, reduced intracellular glucose and glutamine levels in prostate cancer (PCa). Glucose deprivation upon Etn treatment exacerbated metabolic stress in PCa, thereby enhancing cell death. Moreover, Etn was potent in inhibiting tumor growth in a PCa xenograft model. However, the precise mechanisms underlying Etn-induced metabolic stress in PCa remain elusive. The purpose of the present study was to elucidate the mechanisms contributing to Etn-mediated metabolic rewiring in PCa. Methods: Glucose transporters (GLUTs) facilitate glucose transport across the plasma membrane. Thus, we assessed the expression of GLUTs and the internalization of GLUT1 in PCa. We also evaluated the effects of Etn on membrane dynamics, mitochondrial structure and function, lipid droplet density, autophagy, and apoptosis in PCa cells. Results: Compared to other GLUTs, GLUT1 was highly upregulated in PCa. We observed enhanced GLUT1 internalization, altered membrane dynamics, and perturbed mitochondrial structure and function upon Etn treatment. Etn-induced bioenergetic stress enhanced lipolysis, decreased lipid droplet density, promoted accumulation of autophagosomes, and increased apoptosis. Conclusion: We provide the first evidence that Etn alters GLUT1 trafficking leading to metabolic stress in PCa. By upregulating phosphatidylethanolamine (PE), Etn modulates membrane fluidity and affects mitochondrial structure and function. Etn also induces autophagy in PCa cells, thereby promoting apoptosis. These data strongly suggest that Etn rewires cellular bioenergetics and could serve as a promising anticancer agent for PCa.
    Keywords:  apoptosis; autophagy; metabolism; monoethanolamine; prostate cancer
    DOI:  https://doi.org/10.7150/thno.62724
  8. Free Radic Biol Med. 2021 Sep 11. pii: S0891-5849(21)00720-6. [Epub ahead of print]
      Cancer cells frequently lack nutrients like glucose, due to insufficient vascular networks. Mitochondrial phosphoenolpyruvate carboxykinase, PCK2, has recently been found to mediate partial gluconeogenesis and hence anabolic metabolism in glucose starved cancer cells. Here we show that PCK2 acts as a regulator of mitochondrial respiration and maintains the redox balance in nutrient-deprived human lung cancer cells. PCK2 silencing increased the abundance and interconversion of tricarboxylic acid (TCA) cycle intermediates, augmented mitochondrial respiration and enhanced glutathione oxidation under glucose and serum starvation, in a PCK2 re-expression reversible manner. Moreover, enhancing the TCA cycle by PCK2 inhibition severely reduced colony formation of lung cancer cells under starvation. As a conclusion, PCK2 contributes to maintaining a reduced glutathione pool in starved cancer cells besides mediating the biosynthesis of gluconeogenic/glycolytic intermediates. The study sheds light on adaptive responses in cancer cells to nutrient deprivation and shows that PCK2 confers protection against respiration-induced oxidative stress.
    Keywords:  Adaptation; Cancer metabolism; Gluconeogenesis; Metabolic flexibility; Mitochondria; Redox balance; Respiration
    DOI:  https://doi.org/10.1016/j.freeradbiomed.2021.09.007
  9. Commun Biol. 2021 Sep 17. 4(1): 1093
      TOR complex 1 (TORC1) is an evolutionarily-conserved protein kinase that controls cell growth and metabolism in response to nutrients, particularly amino acids. In mammals, several amino acid sensors have been identified that converge on the multi-layered machinery regulating Rag GTPases to trigger TORC1 activation; however, these sensors are not conserved in many other organisms including yeast. Previously, we reported that glutamine activates yeast TORC1 via a Gtr (Rag ortholog)-independent mechanism involving the vacuolar protein Pib2, although the identity of the supposed glutamine sensor and the exact TORC1 activation mechanism remain unclear. In this study, we successfully reconstituted glutamine-responsive TORC1 activation in vitro using only purified Pib2 and TORC1. In addition, we found that glutamine specifically induced a change in the folding state of Pib2. These findings indicate that Pib2 is a glutamine sensor that directly activates TORC1, providing a new model for the metabolic control of cells.
    DOI:  https://doi.org/10.1038/s42003-021-02625-w
  10. Blood. 2021 Sep 15. pii: blood.2021013201. [Epub ahead of print]
      AML is characterized by the presence of leukemia stem cells (LSCs), and failure to fully eradicate this population contributes to disease persistence/relapse. Prior studies have characterized metabolic vulnerabilities of LSCs, which demonstrate preferential reliance on oxidative phosphorylation (OXPHOS) for energy metabolism and survival. In the present study, using both genetic and pharmacologic strategies in primary human AML specimens, we show that signal transducer and activator of transcription 3 (STAT3) mediates OXPHOS in LSCs. STAT3 regulates AML-specific expression of MYC, which in turn controls transcription of the neutral amino acid transporter SLC1A5. We show that genetic inhibition of MYC or SLC1A5 acts to phenocopy the impairment of OXPHOS observed with STAT3 inhibition, thereby establishing this axis as a regulatory mechanism linking STAT3 to energy metabolism. Inhibition of SLC1A5 reduces intracellular levels of glutamine, glutathione and multiple TCA metabolites, leading to reduced TCA cycle activity and inhibition of OXPHOS. Based on these findings, we used a novel small molecule STAT3 inhibitor, that binds STAT3 and disrupts STAT3-DNA, to evaluate the biological role of STAT3. We show that STAT3 inhibition selectively leads to cell death in AML stem and progenitor cells derived from newly diagnosed and relapsed patients, while sparing normal hematopoietic cells. Together, these findings establish a STAT3-mediated mechanism that controls energy metabolism and survival in primitive AML cells.
    DOI:  https://doi.org/10.1182/blood.2021013201
  11. Org Biomol Chem. 2021 Sep 15. 19(35): 7695-7700
      Fluorescent probes have become valuable tools in chemical biology, providing interesting inferences for unfolding the complexities of natural biochemical processes. In this study, we report the synthesis and characterization of fluorescent labelled glutamine (Gln) and asparagine (Asn) derivatives via traceless Staudinger ligation, which exhibited high fluorescence quantum yields, excellent photostabilities and emission of blue fluorescence in the visible region. The successful permeation of these fluorescent amino acids into cellular components proved their potential as fluorescent probes for chemical biology.
    DOI:  https://doi.org/10.1039/d1ob01029h
  12. Front Oncol. 2021 ;11 743814
      Glioma stem-like cells (GSCs) were first described as a population which may in part be resistant to traditional chemotherapeutic therapies and responsible for tumour regrowth. Knowledge of the underlying metabolic complexity governing GSC growth and function may point to potential differences between GSCs and the tumour bulk which could be harnessed clinically. There is an increasing interest in the direct/indirect targeting or reprogramming of GSC metabolism as a potential novel therapeutic approach in the adjuvant or recurrent setting to help overcome resistance which may be mediated by GSCs. In this review we will discuss stem-like models, interaction between metabolism and GSCs, and potential current and future strategies for overcoming GSC resistance.
    Keywords:  cancer metabolism; cancer stem cell (CSC); glioma stem-like cell; metabolic reprogramming; therapeutic strategies
    DOI:  https://doi.org/10.3389/fonc.2021.743814
  13. Cancer Res. 2021 Sep 13. pii: canres.3242.2020. [Epub ahead of print]
      Oxidative phosphorylation (OXPHOS) is an active metabolic pathway in many cancers. RNA from pre-treatment biopsies from patients with triple negative breast cancer (TNBC) who received neoadjuvant chemotherapy demonstrated that the top canonical pathway associated with worse outcome was higher expression of an OXPHOS signature. In multiple TNBC patient-derived xenografts (PDXs), treatment with IACS-10759, a novel inhibitor of OXPHOS, stabilized tumor growth. Gene expression profiling revealed that all sensitive models displayed a basal-like 1 TNBC subtype, and expression of mitochondrial genes was significantly higher in sensitive PDXs. An in vivo functional genomics screen in tumors treated with IACS-10759 found several potential synthetic lethal targets, including CDK4. A combination of palbociclib, a CDK4/6 inhibitor, and IACS-10759 exhibited significant anti-tumor efficacy in vitro and in vivo. In addition, the combination of IACS-10759 and multi-kinase inhibitor cabozantinib had improved antitumor efficacy compared to either single agent. Taken together, these data suggest that OXPHOS is a metabolic vulnerability in TNBC that may be leveraged with novel therapeutics in combination regimens.
    DOI:  https://doi.org/10.1158/0008-5472.CAN-20-3242
  14. Cancer Res. 2021 Sep 16. pii: canres.1606.2021. [Epub ahead of print]
      Cancer is a complex disease and cancer cells typically harbor multiple genetic and epigenetic alterations. Large-scale sequencing of patient-derived cancer samples has identified several druggable driver oncogenes. Many of these oncogenes can be pharmacologically targeted to provide effective therapies for breast cancer, leukemia, lung cancer, melanoma, lymphoma, and other cancer types. Initial responses to these agents can be robust in many cancer types and some cancer patients experience sustained tumor inhibition. However, resistance to these targeted therapeutics frequently emerges, either from intrinsic or acquired mechanisms, posing a major clinical hurdle for effective treatment. Several resistance mechanisms, both cell autonomous and cell non-autonomous, have been identified in different cancer types. Here we describe how alterations of the transcriptome, transcription factors, DNA, and chromatin regulatory proteins confer resistance to targeted therapeutic agents. We also elaborate on how these studies have identified underlying epigenetic factors that drive drug resistance and oncogenic pathways, with direct implications for the prevention and treatment of drug-resistant cancer.
    DOI:  https://doi.org/10.1158/0008-5472.CAN-21-1606