bims-glucam Biomed News
on Glutamine cancer metabolism
Issue of 2023‒06‒25
fifteen papers selected by
Sreeparna Banerjee
Middle East Technical University


  1. J Immunol. 2023 Jun 21. pii: ji2200715. [Epub ahead of print]
      Activated T cells undergo metabolic reprogramming to meet anabolic, differentiation, and functional demands. Glutamine supports many processes in activated T cells, and inhibition of glutamine metabolism alters T cell function in autoimmune disease and cancer. Multiple glutamine-targeting molecules are under investigation, yet the precise mechanisms of glutamine-dependent CD8 T cell differentiation remain unclear. We show that distinct strategies of glutamine inhibition by glutaminase-specific inhibition with small molecule CB-839, pan-glutamine inhibition with 6-diazo-5-oxo-l-norleucine (DON), or by glutamine-depleted conditions (No Q) produce distinct metabolic differentiation trajectories in murine CD8 T cells. T cell activation with CB-839 treatment had a milder effect than did DON or No Q treatment. A key difference was that CB-839-treated cells compensated with increased glycolytic metabolism, whereas DON and No Q-treated cells increased oxidative metabolism. However, all glutamine treatment strategies elevated CD8 T cell dependence on glucose metabolism, and No Q treatment caused adaptation toward reduced glutamine dependence. DON treatment reduced histone modifications and numbers of persisting cells in adoptive transfer studies, but those T cells that remained could expand normally upon secondary Ag encounter. In contrast, No Q-treated cells persisted well yet demonstrated decreased secondary expansion. Consistent with reduced persistence, CD8 T cells activated in the presence of DON had reduced ability to control tumor growth and reduced tumor infiltration in adoptive cell therapy. Overall, each approach to inhibit glutamine metabolism confers distinct effects on CD8 T cells and highlights that targeting the same pathway in different ways can elicit opposing metabolic and functional outcomes.
    DOI:  https://doi.org/10.4049/jimmunol.2200715
  2. Mol Cancer Ther. 2023 Jun 23. pii: MCT-23-0041. [Epub ahead of print]
      The ability of tumor cells to alter their metabolism to support survival and growth presents a challenge to effectively treat cancers. Carbonic anhydrase IX (CAIX) is a hypoxia-induced, metabolic enzyme that plays a crucial role in pH regulation in tumor cells. Recently, through a synthetic lethal screen, we identified CAIX to play an important role in redox homeostasis. In this study, we show that CAIX interacts with the glutamine transporter, solute carrier family 1 member 5 (SLC1A5), and coordinately functions to maintain redox homeostasis through the glutathione/glutathione peroxidase 4 (GSH/GPX4) axis. Inhibition of CAIX increases glutamine uptake by SLC1A5 and concomitantly increases GSH levels. The combined inhibition of CAIX activity and glutamine metabolism or the GSH/GPX4 axis results in an increase in lipid peroxidation and induces ferroptosis, both in vitro and in vivo. Thus, this study demonstrates co-targeting of CAIX and glutamine metabolism as a potential strategy to induce ferroptosis in tumor cells.
    DOI:  https://doi.org/10.1158/1535-7163.MCT-23-0041
  3. Small. 2023 Jun 17. e2303253
      Tumor-dependent glucose and glutamine metabolisms are essential for maintaining survival, while the accordingly metabolic suppressive therapy is limited by the compensatory metabolism and inefficient delivery efficiency. Herein, a functional metal-organic framework (MOF)-based nanosystem composed of the weakly acidic tumor microenvironment-activated detachable shell and reactive oxygen species (ROS)-responsive disassembled MOF nanoreactor core is designed to co-load glycolysis and glutamine metabolism inhibitors glucose oxidase (GOD) and bis-2-(5-phenylacetmido-1,2,4-thiadiazol-2-yl) ethyl sulfide (BPTES) for tumor dual-starvation therapy. The nanosystem excitingly improves tumor penetration and cellular uptake efficiency via integrating the pH-responsive size reduction and charge reversal and ROS-sensitive MOF disintegration and drug release strategy. Furthermore, the degradation of MOF and cargoes release can be self-amplified via additional self-generation H2 O2 mediated by GOD. Last, the released GOD and BPTES collaboratively cut off the energy supply of tumors and induce significant mitochondrial damage and cell cycle arrest via simultaneous restriction of glycolysis and compensatory glutamine metabolism pathways, consequently realizing the remarkable triple negative breast cancer killing effect in vivo with good biosafety via the dual starvation therapy.
    Keywords:  dual-starvation therapy; glucose metabolism suppression; glutamine metabolism suppression; metal-organic framework (MOF)-based nanoreactors; tumor penetration
    DOI:  https://doi.org/10.1002/smll.202303253
  4. Thorac Cancer. 2023 Jun 22.
      BACKGROUND: The deregulation of circular RNA (circRNA) is widely reported in carcinogenesis. The purpose of this study was to investigate the role of circRNA-PDZ domain containing 8 (circ-PDZD8) in non-small cell lung cancer (NSCLC) progression.METHODS: The histological structure of tissues was identified by hematoxylin-eosin (HE) staining analysis. The expression levels of circ-PDZD8, miR-330-5p and la ribonucleoprotein 1 (LARP1) mRNA were ascertained by qPCR. Cell counting kit-8, colony formation, flow cytometry, and transwell assays were employed for functional analysis. Glutamine metabolism was monitored by glutamine consumption, alpha ketoglutarate (α-KG) level and adenosine triphosphate (ATP) level. A xenograft model was established to ascertain the role of circ-PDZD8 in vivo. The putative binding relationships were verified by dual-luciferase and RIP studies.
    RESULTS: Circ-PDZD8 expression was highly increased in NSCLC. Circ-PDZD8 knockdown inhibited cell growth, migratory capacity, invasiveness and glutamine metabolism but enhanced cell apoptosis in NSCLC cells. Circ-PDZD8 blocked miR-330-5p expression, and miR-330-5p inhibition overturned the effects of circ-PDZD8 absence. LARP1 targeted by miR-330-5p, and miR-330-5p upregulation-impaired cell growth, motility and glutamine metabolism were recovered by LARP1 overexpression. Circ-PDZD8 knockdown was also shown to impede solid tumor growth.
    CONCLUSION: Circ-PDZD8 promotes NSCLC cell growth and glutamine metabolism by increasing LARP1 via competitively targeting miR-330-5p.
    Keywords:  LARP1; NSCLC; circ-PDZD8; miR-330-5p
    DOI:  https://doi.org/10.1111/1759-7714.15006
  5. Inflamm Res. 2023 Jun 21.
      OBJECTIVE AND DESIGN: Post-traumatic urethral stricture is a clinical challenge for both patients and clinicians. Targeting glutamine metabolism to suppress excessive activation of urethral fibroblasts (UFBs) is assumed to be a potent and attractive strategy for preventing urethral scarring and stricture.MATERIAL OR SUBJECTS: In cellular experiments, we explored whether glutaminolysis meets the bioenergetic and biosynthetic demands of quiescent UFBs converted into myofibroblasts. At the same time, we examined the specific effects of M2-polarized macrophages on glutaminolysis and activation of UFBs, as well as the mechanism of intercellular signaling. In addition, findings were further verified in vivo in New Zealand rabbits.
    RESULTS: It revealed that glutamine deprivation or knockdown of glutaminase 1 (GLS1) significantly inhibited UFB activation, proliferation, biosynthesis, and energy metabolism; however, these effects were rescued by cell-permeable dimethyl α-ketoglutarate. Moreover, we found that exosomal miR-381 derived from M2-polarized macrophages could be ingested by UFBs and inhibited GLS1-dependent glutaminolysis, thereby preventing excessive activation of UFBs. Mechanistically, miR-381 directly targets the 3'UTR of Yes-associated protein (YAP) mRNA to reduce its stability at the transcriptional level, ultimately downregulating expression of YAP, and GLS1. In vivo experiments revealed that treatment with either verteporfin or exosomes derived from M2-polarized macrophages significantly reduced urethral stricture in New Zealand rabbits after urethral trauma.
    CONCLUSION: Collectively, this study demonstrates that exosomal miR-381 from M2-polarized macrophages reduces myofibroblast formation of UFBs and urethral scarring and stricture by inhibiting YAP/GLS1-dependent glutaminolysis.
    Keywords:  Exosomes; Glutaminolysis; M2-polarized macrophages; Urethral stricture; miR-381
    DOI:  https://doi.org/10.1007/s00011-023-01735-x
  6. Trends Endocrinol Metab. 2023 Jun 20. pii: S1043-2760(23)00106-6. [Epub ahead of print]
      p62 is an important multifunctional adaptor protein participating in autophagy and many other activities. Many studies have revealed that p62 is highly expressed in multiple cancers and decreasing its level can effectively lower the proliferation ability of cancer cells. Moreover, much research has highlighted the significant role of the regulation of cancer cell metabolism in helping to treat tumors. Recent reports demonstrate that p62 could regulate cancer cell metabolism through various mechanisms. However, the relationship between p62 and cancer cell metabolism as well as the related mechanisms has not been fully elucidated. In this review, we describe glucose, glutamine, and fatty acid metabolism in tumor cells and some signaling pathways that can regulate cancer metabolism and are mediated by p62.
    Keywords:  autophagy; cancer cell metabolism; inhibitors; p62
    DOI:  https://doi.org/10.1016/j.tem.2023.05.004
  7. Front Endocrinol (Lausanne). 2023 ;14 1195500
      Clear cell renal cell carcinoma (ccRCC) is a malignancy that exhibits metabolic reprogramming as a result of genetic mutations. This reprogramming accommodates the energy and anabolic needs of the cancer cells, leading to changes in glucose, lipid, and bio-oxidative metabolism, and in some cases, the amino acid metabolism. Recent evidence suggests that ccRCC may be classified as a metabolic disease. The metabolic alterations provide potential targets for novel therapeutic interventions or biomarkers for monitoring tumor growth and prognosis. This literature review summarized recent discoveries of metabolic alterations in ccRCC, including changes in glucose, lipid, and amino acid metabolism. The development of metabolic drugs targeting these metabolic pathways was also discussed, such as HIF-2α inhibitors, fatty acid synthase (FAS) inhibitors, glutaminase (GLS) inhibitors, indoleamine 2,3-dioxygenase (IDO) inhibitors, and arginine depletion. Future trends in drug development are proposed, including the use of combination therapies and personalized medicine approaches. In conclusion, this review provides a comprehensive overview of the metabolic alterations in ccRCC and highlights the potential for developing new treatments for this disease.
    Keywords:  cancer; ccRCC; glucose; lipids; lipids ccRCC; metabolism; metabolism reprogramming
    DOI:  https://doi.org/10.3389/fendo.2023.1195500
  8. Theranostics. 2023 ;13(10): 3165-3187
      Rationale: Mitochondria generate ATP via the oxidative phosphorylation system, which mainly comprises five respiratory complexes found in the inner mitochondrial membrane. A high-order assembly of respiratory complexes is called a supercomplex. COX7A2L is a supercomplex assembly factor that has been well-investigated for studying supercomplex function and assembly. To date, the effects of mitochondrial supercomplexes on cell metabolism have not been elucidated. Methods: We depleted COX7A2L or Cox7a2l in human and mouse cells to generate cell models lacking mitochondrial supercomplexes as well as in DBA/2J mice as animal models. We tested the effect of impaired supercomplex assembly on cell proliferation with different nutrient supply. We profiled the metabolic features in COX7A2L-/- cells and Cox7a2l-/- mice via the combined use of targeted and untargeted metabolic profiling and metabolic flux analysis. We further tested the role of mitochondrial supercomplexes in pancreatic ductal adenocarcinoma (PDAC) through PDAC cell lines and a nude mouse model. Results: Impairing mitochondrial supercomplex assembly by depleting COX7A2L in human cells reprogrammed metabolic pathways toward anabolism and increased glutamine metabolism, cell proliferation and antioxidative defense. Similarly, knockout of Cox7a2l in DBA/2J mice promoted the use of proteins/amino acids as oxidative carbon sources. Mechanistically, impaired supercomplex assembly increased electron flux from CII to CIII/CIV and promoted CII-dependent respiration in COX7A2L-/- cells which further upregulated glutaminolysis and glutamine oxidation to accelerate the reactions of the tricarboxylic acid cycle. Moreover, the proliferation of PDAC cells lacking COX7A2L was inhibited by glutamine deprivation. Conclusion: Our results reveal the regulatory role of mitochondrial supercomplexes in glutaminolysis which may fine-tune the fate of cells with different nutrient availability.
    Keywords:  COX7A2L; PDAC; SCAF1; metabolism; mitochondrial supercomplex
    DOI:  https://doi.org/10.7150/thno.78292
  9. bioRxiv. 2023 Jun 11. pii: 2023.06.09.544407. [Epub ahead of print]
      Infusion of 13C-labeled metabolites provides a gold-standard for understanding the metabolic processes used by T cells during immune responses in vivo . Through infusion of 13C-labeled metabolites (glucose, glutamine, acetate) in Listeria monocytogenes ( Lm )-infected mice, we demonstrate that CD8+ T effector (Teff) cells utilize metabolites for specific pathways during specific phases of activation. Highly proliferative early Teff cells in vivo shunt glucose primarily towards nucleotide synthesis and leverage glutamine anaplerosis in the tricarboxylic acid (TCA) cycle to support ATP and de novo pyrimidine synthesis. Additionally, early Teff cells rely on glutamic-oxaloacetic transaminase 1 (Got1)-which regulates de novo aspartate synthesis-for effector cell expansion in vivo . Importantly, Teff cells change fuel preference over the course of infection, switching from glutamine-to acetate-dependent TCA cycle metabolism late in infection. This study provides insights into the dynamics of Teff metabolism, illuminating distinct pathways of fuel consumption associated with Teff cell function in vivo .Teaser: Interrogating dynamics of fuel utilization by CD8 + T cells in vivo reveals new metabolic checkpoints for immune function in vivo .
    DOI:  https://doi.org/10.1101/2023.06.09.544407
  10. Br J Cancer. 2023 Jun 21.
      Altered cellular metabolism is a major mechanism by which tumours support nutrient consumption associated with increased cellular proliferation. Selective dependency on specific metabolic pathways provides a therapeutic vulnerability that can be targeted in cancer therapy. Anti-metabolites have been used clinically since the 1940s and several agents targeting nucleotide metabolism are now well established as standard of care treatment in a range of indications. However, despite great progress in our understanding of the metabolic requirements of cancer and non-cancer cells within the tumour microenvironment, there has been limited clinical success for novel agents targeting pathways outside of nucleotide metabolism. We believe that there is significant therapeutic potential in targeting metabolic processes within cancer that is yet to be fully realised. However, current approaches to identify novel targets, test novel therapies and select patient populations most likely to benefit are sub-optimal. We highlight recent advances in technologies and understanding that will support the identification and validation of novel targets, re-evaluation of existing targets and design of optimal clinical positioning strategies to deliver patient benefit.
    DOI:  https://doi.org/10.1038/s41416-023-02324-9
  11. Cell Rep. 2023 Jun 21. pii: S2211-1247(23)00677-0. [Epub ahead of print]42(7): 112666
      Protein lysine crotonylation has been recently identified as a vital posttranslational modification in cellular processes, particularly through the modification of histones. We show that lysine crotonylation is an important modification of the cytoplastic and mitochondria proteins. Enzymes in glycolysis, the tricarboxylic acid (TCA) cycle, fatty acid metabolism, glutamine metabolism, glutathione metabolism, the urea cycle, one-carbon metabolism, and mitochondrial fusion/fission dynamics are found to be extensively crotonylated in pancreatic cancer cells. This modulation is mainly controlled by a pair of crotonylation writers and erasers including CBP/p300, HDAC1, and HDAC3. The dynamic crotonylation of metabolic enzymes is involved in metabolism regulation, which is linked with tumor progression. Interestingly, the activation of MTHFD1 by decrotonylation at Lys354 and Lys553 promotes the development of pancreatic cancer by increasing resistance to ferroptosis. Our study suggests that crotonylation represents a metabolic regulatory mechanism in pancreatic cancer progression.
    Keywords:  CP: Cancer; CP: Molecular biology; MTHFD1; crotonylation; metabolism; pancreatic cancer; tumor progression
    DOI:  https://doi.org/10.1016/j.celrep.2023.112666
  12. Acta Biomater. 2023 Jun 19. pii: S1742-7061(23)00341-0. [Epub ahead of print]
      The solid tumors are characterized with oxidative stress and metabolic reprogramming, which has been independently used for targeted tumor monotherapy. However, the potential of targeting metabolism-redox circuit in tumor therapy has long been neglected. Herein, we report a hybrid nanocarrier for concurrent targeting of glycolysis and redox balance in the current work. The nanocarriers are made of pH- and ATP-responsive zeolitic imidazolate framework (ZIF-8) as the porous core that was further coated with poloxamer 407 as the steric stabilizer. Two active cargos, glucose oxidase (GOx) and 3-bromopyruvate (3-BrPA) were co-loaded in the core of nanocarrier. GOx is well-known for its ability of producing hydrogen peroxide at the expense of glucose and oxygen. 3-BrPA can reduce oxygen and glucose consumption through glycolysis, which sensitized cancer cells to GOx-induced apoptosis. At the cellular level, the hybrid nanocarrier significantly impaired the redox balance in the liver hepatocellular carcinoma cell line (HepG2), as evidenced by the depletion of glutathione and boost of reactive oxygen species. The potency of hybrid nanocarrier in terms of suppressing HepG2 cell energy metabolism was proven by the exhaustion of ATP. As a consequence, cell viability was greatly reduced. The in vivo efficacy of hybrid nanocarriers was demonstrated in HepG2 tumor-bearing mice. The current work presents an approach of targeting metabolism-redox circuit for tumor treatment, which may enrich the available anti-tumor strategies. STATEMENT OF SIGNIFICANCE: Metabolic alterations and elevated reactive oxygen species (ROS) are two characteristics of cancer. The metabolic patterns of cancer cells are elaborately reprogrammed to enable the rapid propagation of cancer cells. However, the potential of targeting the metabolism-redox circuit in anti-tumor therapy has long been neglected. As a proof-of-concept, we report an engineered stimuli-responsive nanomedicine that can eradicate cancer cells via cooperative glycolysis inhibition and redox impairment. The current work presents an approach of targeting the metabolism-redox circuit for tumor treatment, which may enrich the available anti-tumor strategies.
    Keywords:  Drug delivery; glycolysis; nanocarrier; redox homeostasis; tumor therapy
    DOI:  https://doi.org/10.1016/j.actbio.2023.06.016
  13. Pharmacol Rep. 2023 Jun 19.
      Although Warburg's discovery of intensive glucose uptake by tumors, followed by lactate fermentation in oxygen presence of oxygen was made a century ago, it is still an area of intense research and development of new hypotheses that, layer by layer, unravel the complexities of neoplastic transformation. This seemingly simple metabolic reprogramming of cancer cells reveals an intriguing, multi-faceted nature that may link various phenomena including cell signaling, cell proliferation, ROS generation, energy supply, macromolecules synthesis/biosynthetic precursor supply, immunosuppression, or cooperation of cancerous cells with cancer-associated fibroblasts (CAFs), known as reversed Warburg effect. According to the current perception of the causes and consequences of the Warburg effect, PI3K/Akt/mTOR are the main signaling pathways that, in concert with the transcription factors HIF-1, p53, and c-Myc, modulate the activity/expression of key regulatory enzymes, including PKM2, and PDK1 to tune in the most optimal metabolic setting for the cancer cell. This in turn secures adequate levels of biosynthetic precursors, NADPH, NAD+, and rapid ATP production to meet the increased demands of intensively proliferating tumor cells. The end-product of "aerobic glycolysis", lactate, an oncometabolite, may provide fuel to neighboring cancer cells, and facilitate metastasis and immunosuppression together enabling cancer progression. The importance and possible applicability of the presented issue are best illustrated by numerous trials with various agents targeting the Warburg effect, constituting a promising strategy in future anti-cancer regimens. In this review, we present the key aspects of this multifactorial phenomenon, depicting the mechanisms and benefits behind the Warburg effect, and also pointing to selected aspects in the field of anticancer therapy.
    Keywords:  Aerobic glycolysis; Metabolic adaptation of cancer cells; Reverse Warburg effect; Tumor metabolism; Warburg effect
    DOI:  https://doi.org/10.1007/s43440-023-00504-1
  14. Cancers (Basel). 2023 May 22. pii: 2862. [Epub ahead of print]15(10):
      Approximately a century ago, Otto Warburg discovered that cancer cells use a fermentative rather than oxidative metabolism even though the former is more inefficient in terms of energy production per molecule of glucose. Cancer cells increase the use of this fermentative metabolism even in the presence of oxygen, and this process is called aerobic glycolysis or the Warburg effect. This alternative metabolism is mainly characterized by higher glycolytic rates, which allow cancer cells to obtain higher amounts of total ATP, and the production of lactate, but there are also an activation of protumoral signaling pathways and the generation of molecules that favor cancer progression. One of these molecules is succinate, a Krebs cycle intermediate whose concentration is increased in cancer and which is considered an oncometabolite. Several protumoral actions have been associated to succinate and its role in several cancer types has been already described. Despite playing a major role in metabolism and cancer, so far, the potential of succinate as a target in cancer prevention and treatment has remained mostly unexplored, as most previous Warburg-directed anticancer strategies have focused on other intermediates. In this review, we aim to summarize succinate's protumoral functions and discuss the use of succinate expression regulators as a potential cancer therapy strategy.
    Keywords:  Warburg effect; cancer; glucose; glycolysis; lactate; metabolism; succinate
    DOI:  https://doi.org/10.3390/cancers15102862
  15. J Obstet Gynaecol Res. 2023 Jun 20.
      BACKGROUND: KIFC1 exerts an important function in centrosome aggregation in breast cancer (BC) cells and a variety of other cancer cells, but its potential mechanisms in BC pathogenesis are yet fully elucidated. The aim of this study was to investigate the effects of KIFC1 on BC progression and its underlying mechanisms.METHODS: Expression of ELK1 and KIFC1 in BC was analyzed by The Cancer Genome Atlas database and quantitative real-time polymerase chain reaction. Cell proliferative capacity was examined by CCK-8 and colony formation assays, respectively. Glutathione (GSH)/glutathione disulfide (GSSG) ratio and GSH level were measured using the kit. Expression of GSH metabolism-related enzymes (G6PD, GCLM, and GCLC) was detected by western blot. Intracellular reactive oxygen species (ROS) levels were measured by the ROS Assay Kit. The transcription factor ELK1 upstream of KIFC1 was identified by hTFtarget, KnockTFv2 database and Pearson correlation. Their interaction was validated by dual-luciferase reporter assay and chromatin immunoprecipitation.
    RESULTS: This study demonstrated the upregulation of ELK1 and KIFC1 in BC and found that ELK1 could bind to the KIFC1 promoter to promote KIFC1 transcription. KIFC1 overexpression increased cell proliferation and intracellular GSH levels, while decreasing intracellular ROS levels. The addition of the GSH metabolism inhibitor BSO attenuated the promotion of BC cell proliferation induced by KIFC1 overexpression. In addition, KIFC1 overexpression reversed the inhibitory effect of knockdown of ELK1 on BC cell proliferation.
    CONCLUSION: ELK1 was a transcriptional factor of KIFC1. ELK1/KIFC1 axis reduced ROS level by increasing GSH synthesis, thus facilitating BC cell proliferation. Current observations suggest that ELK1/ KIFC1 may be a potential therapeutic target for BC treatment.
    Keywords:  ELK1; KIFC1; breast cancer; glutathione metabolism
    DOI:  https://doi.org/10.1111/jog.15710