User menu

Lactate promotes glutamine uptake and metabolism in oxidative cancer cells.

Bibliographic reference Perez Escuredo, Jhudit ; Dadhich, Rajesh Kumar ; Dhup, Suveera ; Cacace, Andrea ; Van Hee, Vincent F ; et. al. Lactate promotes glutamine uptake and metabolism in oxidative cancer cells.. In: Cell Cycle, Vol. 15, no. 1, p. 72-83 (2016)
Permanent URL http://hdl.handle.net/2078.1/170451
  1. Porporato Paolo E., Dhup Suveera, Dadhich Rajesh K., Copetti Tamara, Sonveaux Pierre, Anticancer Targets in the Glycolytic Metabolism of Tumors: A Comprehensive Review, 10.3389/fphar.2011.00049
  2. Ward Patrick S., Thompson Craig B., Metabolic Reprogramming: A Cancer Hallmark Even Warburg Did Not Anticipate, 10.1016/j.ccr.2012.02.014
  3. Wu R, J Biol Chem, 234, 1036 (1959)
  4. KOLOBOVA Elena, TUGANOVA Alina, BOULATNIKOV Igor, POPOV Kirill M., Regulation of pyruvate dehydrogenase activity through phosphorylation at multiple sites, 10.1042/bj3580069
  5. Papandreou Ioanna, Cairns Rob A., Fontana Lucrezia, Lim Ai Lin, Denko Nicholas C., HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption, 10.1016/j.cmet.2006.01.012
  6. Dewhirst Mark W., Cao Yiting, Moeller Benjamin, Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response, 10.1038/nrc2397
  7. Sowter HM, Cancer Res, 63, 6130 (2003)
  8. Bustamante E., Pedersen P. L., High aerobic glycolysis of rat hepatoma cells in culture: Role of mitochondrial hexokinase, 10.1073/pnas.74.9.3735
  9. Mathupala Saroj P., Rempel Annette, Pedersen Peter L., Glucose Catabolism in Cancer Cells : IDENTIFICATION AND CHARACTERIZATION OF A MARKED ACTIVATION RESPONSE OF THE TYPE II HEXOKINASE GENE TO HYPOXIC CONDITIONS, 10.1074/jbc.m108181200
  10. Mazurek Sybille, Boschek C. Bruce, Hugo Ferdinand, Eigenbrodt Erich, Pyruvate kinase type M2 and its role in tumor growth and spreading, 10.1016/j.semcancer.2005.04.009
  11. Christofk Heather R., Vander Heiden Matthew G., Harris Marian H., Ramanathan Arvind, Gerszten Robert E., Wei Ru, Fleming Mark D., Schreiber Stuart L., Cantley Lewis C., The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth, 10.1038/nature06734
  12. Mazurek Sybille, Pyruvate kinase type M2: A key regulator of the metabolic budget system in tumor cells, 10.1016/j.biocel.2010.02.005
  13. Vander Heiden M. G., Cantley L. C., Thompson C. B., Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation, 10.1126/science.1160809
  14. Hensley Christopher T., Wasti Ajla T., DeBerardinis Ralph J., Glutamine and cancer: cell biology, physiology, and clinical opportunities, 10.1172/jci69600
  15. Mullen AR, Nature, 481, 385 (2012)
  16. David Charles J., Chen Mo, Assanah Marcela, Canoll Peter, Manley James L., HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer, 10.1038/nature08697
  17. Wise D. R., DeBerardinis R. J., Mancuso A., Sayed N., Zhang X.-Y., Pfeiffer H. K., Nissim I., Daikhin E., Yudkoff M., McMahon S. B., Thompson C. B., Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction, 10.1073/pnas.0810199105
  18. Gao Ping, Tchernyshyov Irina, Chang Tsung-Cheng, Lee Yun-Sil, Kita Kayoko, Ochi Takafumi, Zeller Karen I., De Marzo Angelo M., Van Eyk Jennifer E., Mendell Joshua T., Dang Chi V., c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism, 10.1038/nature07823
  19. DeBerardinis R. J., Mancuso A., Daikhin E., Nissim I., Yudkoff M., Wehrli S., Thompson C. B., Beyond aerobic glycolysis: Transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis, 10.1073/pnas.0709747104
  20. Sonveaux Pierre, Végran Frédérique, Schroeder Thies, Wergin Melanie C., Verrax Julien, Rabbani Zahid N., De Saedeleer Christophe J., Kennedy Kelly M., Diepart Caroline, Jordan Bénédicte F., Kelley Michael J., Gallez Bernard, Wahl Miriam L., Feron Olivier, Dewhirst Mark W., Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice, 10.1172/jci36843
  21. Van Hée Vincent F., Pérez-Escuredo Jhudit, Cacace Andrea, Copetti Tamara, Sonveaux Pierre, Lactate does not activate NF-κB in oxidative tumor cells, 10.3389/fphar.2015.00228
  22. Bonuccelli Gloria, Tsirigos Aristotelis, Whitaker-Menezes Diana, Pavlides Stephanos, Pestell Richard G., Chiavarina Barbara, Frank Philippe G., Flomenberg Neal, Howell Anthony, Martinez-Outschoorn Ubaldo E., Sotgia Federica, Lisanti Michael P., Ketones and lactate “fuel” tumor growth and metastasis : Evidence that epithelial cancer cells use oxidative mitochondrial metabolism, 10.4161/cc.9.17.12731
  23. Lu Huasheng, Forbes Robert A., Verma Ajay, Hypoxia-inducible Factor 1 Activation by Aerobic Glycolysis Implicates the Warburg Effect in Carcinogenesis, 10.1074/jbc.m202487200
  24. Lu Huasheng, Dalgard Clifton L., Mohyeldin Ahmed, McFate Thomas, Tait A. Sasha, Verma Ajay, Reversible Inactivation of HIF-1 Prolyl Hydroxylases Allows Cell Metabolism to Control Basal HIF-1, 10.1074/jbc.m508718200
  25. De Saedeleer Christophe J., Copetti Tamara, Porporato Paolo E., Verrax Julien, Feron Olivier, Sonveaux Pierre, Lactate Activates HIF-1 in Oxidative but Not in Warburg-Phenotype Human Tumor Cells, 10.1371/journal.pone.0046571
  26. DeBerardinis R J, Cheng T, Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer, 10.1038/onc.2009.358
  27. Leite Tiago C., Coelho Raquel G., Silva Daniel Da, Coelho Wagner S., Marinho-Carvalho Monica M., Sola-Penna Mauro, Lactate downregulates the glycolytic enzymes hexokinase and phosphofructokinase in diverse tissues from mice, 10.1016/j.febslet.2010.11.009
  28. Halestrap Andrew P., Wilson Marieangela C., The monocarboxylate transporter family-Role and regulation, 10.1002/iub.572
  29. Invernizzi F., D'Amato I., Jensen P.B., Ravaglia S., Zeviani M., Tiranti V., Microscale oxygraphy reveals OXPHOS impairment in MRC mutant cells, 10.1016/j.mito.2012.01.001
  30. Gatenby Robert A., Gillies Robert J., Why do cancers have high aerobic glycolysis?, 10.1038/nrc1478
  31. De Saedeleer C J, Porporato P E, Copetti T, Pérez-Escuredo J, Payen V L, Brisson L, Feron O, Sonveaux P, Glucose deprivation increases monocarboxylate transporter 1 (MCT1) expression and MCT1-dependent tumor cell migration, 10.1038/onc.2013.454
  32. Katt William P., Cerione Richard A., Glutaminase regulation in cancer cells: a druggable chain of events, 10.1016/j.drudis.2013.10.008
  33. Pappalardi Melissa B., McNulty Dean E., Martin John D., Fisher Kelly E., Jiang Yong, Burns Matthew C., Zhao Huizhen, Ho Thau, Sweitzer Sharon, Schwartz Benjamin, Annan Roland S., Copeland Robert A., Tummino Peter J., Luo Lusong, Biochemical characterization of human HIF hydroxylases using HIF protein substrates that contain all three hydroxylation sites, 10.1042/bj20101201
  34. Loboda Agnieszka, Jozkowicz Alicja, Dulak Jozef, HIF-1 and HIF-2 transcription factors — Similar but not identical, 10.1007/s10059-010-0067-2
  35. Corn Paul G., Ricci M. Stacey, Scata Kimberly A., Arsham Andrew M., Simon M. Celeste, Dicker David T., El-Deiry Wafik S., Mxi1 is induced by hypoxia in a HIF-1–dependent manner and protects cells from c-Myc-induced apoptosis, 10.4161/cbt.4.11.2299
  36. Zhang Huafeng, Gao Ping, Fukuda Ryo, Kumar Ganesh, Krishnamachary Balaji, Zeller Karen I., Dang Chi V., Semenza Gregg L., HIF-1 Inhibits Mitochondrial Biogenesis and Cellular Respiration in VHL-Deficient Renal Cell Carcinoma by Repression of C-MYC Activity, 10.1016/j.ccr.2007.04.001
  37. Walenta S., Schroeder T., Mueller-Klieser W., Lactate in Solid Malignant Tumors: Potential Basis of a Metabolic Classification in Clinical Oncology, 10.2174/0929867043364711
  38. Walenta Stefan, Mueller-Klieser Wolfgang F, Lactate: mirror and motor of tumor malignancy, 10.1016/j.semradonc.2004.04.004
  39. Kennedy Kelly M., Scarbrough Peter M., Ribeiro Anthony, Richardson Rachel, Yuan Hong, Sonveaux Pierre, Landon Chelsea D., Chi Jen-Tsan, Pizzo Salvatore, Schroeder Thies, Dewhirst Mark W., Catabolism of Exogenous Lactate Reveals It as a Legitimate Metabolic Substrate in Breast Cancer, 10.1371/journal.pone.0075154
  40. Busk Morten, Walenta Stefan, Mueller-Klieser Wolfgang, Steiniche Torben, Jakobsen Steen, Horsman Michael Robert, Overgaard Jens, Inhibition of tumor lactate oxidation: Consequences for the tumor microenvironment, 10.1016/j.radonc.2011.05.053
  41. Nakajima Erica C., Van Houten Bennett, Metabolic symbiosis in cancer: Refocusing the Warburg lens, 10.1002/mc.21863
  42. Guillaumond F., Leca J., Olivares O., Lavaut M.-N., Vidal N., Berthezene P., Dusetti N. J., Loncle C., Calvo E., Turrini O., Iovanna J. L., Tomasini R., Vasseur S., Strengthened glycolysis under hypoxia supports tumor symbiosis and hexosamine biosynthesis in pancreatic adenocarcinoma, 10.1073/pnas.1219555110
  43. McGillen Jessica B., Kelly Catherine J., Martínez-González Alicia, Martin Natasha K., Gaffney Eamonn A., Maini Philip K., Pérez-García Víctor M., Glucose–lactate metabolic cooperation in cancer: Insights from a spatial mathematical model and implications for targeted therapy, 10.1016/j.jtbi.2014.09.018
  44. Kianercy A., Veltri R., Pienta K. J., Critical transitions in a game theoretic model of tumour metabolism, 10.1098/rsfs.2014.0014
  45. Sonveaux Pierre, Copetti Tamara, De Saedeleer Christophe J., Végran Frédérique, Verrax Julien, Kennedy Kelly M., Moon Eui Jung, Dhup Suveera, Danhier Pierre, Frérart Françoise, Gallez Bernard, Ribeiro Anthony, Michiels Carine, Dewhirst Mark W., Feron Olivier, Targeting the Lactate Transporter MCT1 in Endothelial Cells Inhibits Lactate-Induced HIF-1 Activation and Tumor Angiogenesis, 10.1371/journal.pone.0033418
  46. Vegran F., Boidot R., Michiels C., Sonveaux P., Feron O., Lactate Influx through the Endothelial Cell Monocarboxylate Transporter MCT1 Supports an NF- B/IL-8 Pathway that Drives Tumor Angiogenesis, 10.1158/0008-5472.can-10-2828
  47. Roland C. L., Arumugam T., Deng D., Liu S. H., Philip B., Gomez S., Burns W. R., Ramachandran V., Wang H., Cruz-Monserrate Z., Logsdon C. D., Cell Surface Lactate Receptor GPR81 Is Crucial for Cancer Cell Survival, 10.1158/0008-5472.can-14-0319
  48. Appelhoff Rebecca J., Tian Ya-Min, Raval Raju R., Turley Helen, Harris Adrian L., Pugh Christopher W., Ratcliffe Peter J., Gleadle Jonathan M., Differential Function of the Prolyl Hydroxylases PHD1, PHD2, and PHD3 in the Regulation of Hypoxia-inducible Factor, 10.1074/jbc.m406026200
  49. DeBoer LW, Am J Physiol, 265, H1571 (1993)
  50. Russell RR, Am J Physiol, 261, H1756 (1991)
  51. Corbet C., Draoui N., Polet F., Pinto A., Drozak X., Riant O., Feron O., The SIRT1/HIF2  Axis Drives Reductive Glutamine Metabolism under Chronic Acidosis and Alters Tumor Response to Therapy, 10.1158/0008-5472.can-14-0705
  52. Reitzer LJ, J Biol Chem, 254, 2669 (1979)
  53. Cardaci S., Rizza S., Filomeni G., Bernardini R., Bertocchi F., Mattei M., Paci M., Rotilio G., Ciriolo M. R., Glutamine Deprivation Enhances Antitumor Activity of 3-Bromopyruvate through the Stabilization of Monocarboxylate Transporter-1, 10.1158/0008-5472.can-12-1741
  54. Doherty J. R., Yang C., Scott K. E. N., Cameron M. D., Fallahi M., Li W., Hall M. A., Amelio A. L., Mishra J. K., Li F., Tortosa M., Genau H. M., Rounbehler R. J., Lu Y., Dang C. V., Kumar K. G., Butler A. A., Bannister T. D., Hooper A. T., Unsal-Kacmaz K., Roush W. R., Cleveland J. L., Blocking Lactate Export by Inhibiting the Myc Target MCT1 Disables Glycolysis and Glutathione Synthesis, 10.1158/0008-5472.can-13-2034
  55. Söderberg Ola, Gullberg Mats, Jarvius Malin, Ridderstråle Karin, Leuchowius Karl-Johan, Jarvius Jonas, Wester Kenneth, Hydbring Per, Bahram Fuad, Larsson Lars-Gunnar, Landegren Ulf, Direct observation of individual endogenous protein complexes in situ by proximity ligation, 10.1038/nmeth947