Glutamate and asparagine cataplerosis underlie glutamine addiction in melanoma

Glutamine dependence is a prominent feature of cancer metabolism, and here we show that melanoma cells, irrespective of their oncogenic background, depend on glutamine for growth. A quantitative audit of how carbon from glutamine is used showed that TCA-cycle-derived glutamate is, in most melanoma cells, the major glutamine-derived cataplerotic output and product of glutaminolysis. In the absence of glutamine, TCA cycle metabolites were liable to depletion through aminotransferase-mediated α-ketoglutarate-to-glutamate conversion and glutamate secretion. Aspartate was an essential cataplerotic output, as melanoma cells demonstrated a limited capacity to salvage external aspartate. Also, the absence of asparagine increased the glutamine requirement, pointing to vulnerability in the aspartate-asparagine biosynthetic pathway within melanoma metabolism. In contrast to melanoma cells, melanocytes could grow in the absence of glutamine. Melanocytes use more glutamine for protein synthesis rather than secreting it as glutamate and are less prone to loss of glutamate and TCA cycle metabolites when starved of glutamine.

[1]  R. Deberardinis,et al.  Beyond aerobic glycolysis: Transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis , 2007, Proceedings of the National Academy of Sciences.

[2]  B. Fuchs,et al.  Stressing out over survival: glutamine as an apoptotic modulator. , 2006, The Journal of surgical research.

[3]  K. Lanks End products of glucose and glutamine metabolism by L929 cells. , 1987, The Journal of biological chemistry.

[4]  V. Sondak,et al.  Targeted therapy in melanoma. , 2013, Clinics in dermatology.

[5]  R. Dellavalle,et al.  A Review of Novel Therapies for Melanoma , 2014, American Journal of Clinical Dermatology.

[6]  Jiangbin Ye,et al.  The GCN2‐ATF4 pathway is critical for tumour cell survival and proliferation in response to nutrient deprivation , 2010, The EMBO journal.

[7]  Nicola Zamboni,et al.  Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells , 2007, The Journal of cell biology.

[8]  Tomer Shlomi,et al.  Glutamine-driven oxidative phosphorylation is a major ATP source in transformed mammalian cells in both normoxia and hypoxia , 2013, Molecular systems biology.

[9]  Christian M. Metallo,et al.  Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia , 2011, Nature.

[10]  H. Eagle,et al.  The growth response of mammalian cells in tissue culture to L-glutamine and L-glutamic acid. , 1956, The Journal of biological chemistry.

[11]  D. Neuberg,et al.  Long-term results of Dana-Farber Cancer Institute ALL Consortium protocols for children with newly diagnosed acute lymphoblastic leukemia (1985–2000) , 2009, Leukemia.

[12]  B. Crabtree,et al.  Glutamine metabolism in lymphocytes: its biochemical, physiological and clinical importance. , 1985, Quarterly journal of experimental physiology.

[13]  Jeffrey W. Smith,et al.  Functional Specialization in Proline Biosynthesis of Melanoma , 2012, PloS one.

[14]  Anthony Mancuso,et al.  Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction , 2008, Proceedings of the National Academy of Sciences.

[15]  V. Mootha,et al.  Metabolite Profiling Identifies a Key Role for Glycine in Rapid Cancer Cell Proliferation , 2012, Science.

[16]  S. Kalhan,et al.  The Key Role of Anaplerosis and Cataplerosis for Citric Acid Cycle Function* , 2002, Journal of Biological Chemistry.

[17]  Jamey D. Young,et al.  Isotopically nonstationary 13C flux analysis of Myc-induced metabolic reprogramming in B-cells. , 2013, Metabolic engineering.

[18]  Takashi Tsukamoto,et al.  Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells. , 2012, Cell metabolism.

[19]  M. Badet-Denisot,et al.  The mechanism of glutamine-dependent amidotransferases , 1998, Cellular and Molecular Life Sciences CMLS.

[20]  Dieter Jahn,et al.  MetaQuant: a tool for the automatic quantification of GC/MS-based metabolome data , 2006, Bioinform..

[21]  F. Young Biochemistry , 1955, The Indian Medical Gazette.

[22]  H. Krebs,et al.  Isolation and metabolic characteristics of rat and chicken enterocytes. , 1979, The Biochemical journal.

[23]  E. Cheng,et al.  Asparagine plays a critical role in regulating cellular adaptation to glutamine depletion. , 2014, Molecular cell.

[24]  Jesse M. Platt,et al.  Hypoxia promotes isocitrate dehydrogenase-dependent carboxylation of α-ketoglutarate to citrate to support cell growth and viability , 2011, Proceedings of the National Academy of Sciences.

[25]  Andrei L Osterman,et al.  Comparative Metabolic Flux Profiling of Melanoma Cell Lines , 2011, The Journal of Biological Chemistry.

[26]  J. D. Benson,et al.  Single-vector inducible lentiviral RNAi system for oncology target validation , 2009, Cell cycle.

[27]  H. Kornberg Anaplerotic Sequences in Microbial Metabolism , 1965 .

[28]  David S. Wishart,et al.  HMDB 3.0—The Human Metabolome Database in 2013 , 2012, Nucleic Acids Res..

[29]  J. Maris,et al.  ATF4 regulates MYC-mediated neuroblastoma cell death upon glutamine deprivation. , 2012, Cancer cell.

[30]  A. Lane,et al.  Targeting aspartate aminotransferase in breast cancer , 2008, Breast Cancer Research.

[31]  John M. Asara,et al.  Glutamine supports pancreatic cancer growth through a Kras-regulated metabolic pathway , 2013, Nature.

[32]  Fabian V. Filipp,et al.  Reverse TCA cycle flux through isocitrate dehydrogenases 1 and 2 is required for lipogenesis in hypoxic melanoma cells , 2012, Pigment cell & melanoma research.

[33]  J. Tamburini,et al.  Inhibiting glutamine uptake represents an attractive new strategy for treating acute myeloid leukemia. , 2013, Blood.

[34]  Gregory Stephanopoulos,et al.  Molecular Systems Biology Peer Review Process File Oncogenic K-ras Decouples Glucose and Glutamine Metabolism to Support Cancer Cell Growth Transaction Report , 2022 .