Lactate Activates HIF-1 in Oxidative but Not in Warburg-Phenotype Human Tumor Cells

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  de Saedeleer, Christophe J ^a   Copetti, Tamara ^a   Porporato, Paolo E ^a   Verrax, Julien ^a   Feron, Olivier ^a   Sonveaux, Pierre ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER 1; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROLYLHYDROXYLASE 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HYPOXIA; CELL RESPIRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENOTYPE; GLYCOLYSIS; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; METABOLIC REGULATION; MOUSE; NONHUMAN; OXIDATION; PARACRINE SIGNALING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR GROWTH; TUMOR VASCULARIZATION;

ANIMALS; ANTIGENS, CD147; CELL LINE, TUMOR; CELL MEMBRANE; CELL PROLIFERATION; GLYCOLYSIS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LACTIC ACID; MALE; MICE; MICE, NUDE; MONOCARBOXYLIC ACID TRANSPORTERS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; OXIDATION-REDUCTION; PHENOTYPE; PROCOLLAGEN-PROLINE DIOXYGENASE; PROTEIN STABILITY; SYMPORTERS;

EID: 84867660436     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046571     Document Type: Article

References (58)

1. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
2. Porporato PE, Dadhich RK, Dhup S, Copetti T, Sonveaux P, (2011) Anticancer targets in the glycolytic metabolism of tumors: a comprehensive review. Front Pharmacol 2: 49.
3. Wu R, Racker E, (1959) Regulatory mechanisms in carbohydrate metabolism. IV. Pasteur effect and Crabtree effect in ascites tumor cells. J Biol Chem 234: 1036-1041.
4. Warburg O, Wind F, Negelein E, (1927) The metabolism of tumors in the body. J Gen Physiol 8: 519-530.
5. Pollard PJ, Wortham NC, Tomlinson IP, (2003) The TCA cycle and tumorigenesis: the examples of fumarate hydratase and succinate dehydrogenase. Ann Med 35: 632-639.
6. Selak MA, Armour SM, MacKenzie ED, Boulahbel H, Watson DG, et al. (2005) Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7: 77-85.
7. Dang L, White DW, Gross S, Bennett BD, Bittinger MA, et al. (2009) Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462: 739-744.
8. Fantin VR, St Pierre J, Leder P, (2006) Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 9: 425-434.
9. Moreno-Sanchez R, Rodriguez-Enriquez S, Marin-Hernandez A, Saavedra E, (2007) Energy metabolism in tumor cells. FEBS J 274: 1393-1418.
10. Luo W, Hu H, Chang R, Zhong J, Knabel M, et al. (2011) Pyruvate Kinase M2 Is a PHD3-Stimulated Coactivator for Hypoxia-Inducible Factor 1. Cell 145: 732-744.
11. Semenza GL, (2003) Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732.
12. Semenza GL, (2010) HIF-1: upstream and downstream of cancer metabolism. Curr Opin Genet Dev 20: 51-56.
13. Pugh CW, Ratcliffe PJ, (2003) Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 9: 677-684.
14. Hirsila M, Koivunen P, Gunzler V, Kivirikko KI, Myllyharju J, (2003) Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. J Biol Chem 278: 30772-30780.
15. Berra E, Benizri E, Ginouves A, Volmat V, Roux D, et al. (2003) HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. EMBO J 22: 4082-4090.
16. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, et al. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275.
17. Li F, Sonveaux P, Rabbani ZN, Liu S, Yan B, et al. (2007) Regulation of HIF-1alpha stability through S-nitrosylation. Mol Cell 26: 63-74.
18. Lu H, Forbes RA, Verma A, (2002) Hypoxia-inducible factor 1 activation by aerobic glycolysis implicates the Warburg effect in carcinogenesis. J Biol Chem 277: 23111-23115.
19. Lu H, Dalgard CL, Mohyeldin A, McFate T, Tait AS, et al. (2005) Reversible inactivation of HIF-1 prolyl hydroxylases allows cell metabolism to control basal HIF-1. J Biol Chem 280: 41928-41939.
20. Elvidge GP, Glenny L, Appelhoff RJ, Ratcliffe PJ, Ragoussis J, et al. (2006) Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J Biol Chem 281: 15215-15226.
21. Vegran F, Boidot R, Michiels C, Sonveaux P, Feron O, (2011) Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-kappaB/IL-8 pathway that drives tumor angiogenesis. Cancer Res 71: 2550-2560.
22. Sonveaux P, Copetti T, De Saedeleer CJ, Vegran F, Verrax J, et al. (2012) Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis. PLoS ONE 7: e33418.
23. Hewitson KS, Lienard BM, McDonough MA, Clifton IJ, Butler D, et al. (2007) Structural and mechanistic studies on the inhibition of the hypoxia-inducible transcription factor hydroxylases by tricarboxylic acid cycle intermediates. J Biol Chem 282: 3293-3301.
24. Semenza GL, (2007) HIF-1 mediates the Warburg effect in clear cell renal carcinoma. J Bioenerg Biomembr 39: 231-234.
25. Walenta S, Schroeder T, Mueller-Klieser W, (2004) Lactate in solid malignant tumors: potential basis of a metabolic classification in clinical oncology. Curr Med Chem 11: 2195-2204.
26. Sonveaux P, Vegran F, Schroeder T, Wergin MC, Verrax J, et al. (2008) Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest 118: 3930-3942.
27. Walenta S, Snyder S, Haroon ZA, Braun RD, Amin K, et al. (2001) Tissue gradients of energy metabolites mirror oxygen tension gradients in a rat mammary carcinoma model. Int J Radiat Oncol Biol Phys 51: 840-848.
28. Reitzer LJ, Wice BM, Kennell D, (1979) Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells. J Biol Chem 254: 2669-2676.
29. Rideout D, Bustamante A, Patel J, (1994) Mechanism of inhibition of FaDu hypopharyngeal carcinoma cell growth by tetraphenylphosphonium chloride. Int J Cancer 57: 247-253.
30. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, et al. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613.
31. Kong D, Park EJ, Stephen AG, Calvani M, Cardellina JH, et al. (2005) Echinomycin, a small-molecule inhibitor of hypoxia-inducible factor-1 DNA-binding activity. Cancer Res 65: 9047-9055.
32. Halestrap AP, Price NT, (1999) The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem J 343 Pt 2: 281-299.
33. Halestrap AP, Meredith D, (2004) The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch 447: 619-628.
34. Whitaker-Menezes D, Martinez-Outschoorn UE, Lin Z, Ertel A, Flomenberg N, et al. (2011) Evidence for a stromal-epithelial "lactate shuttle" in human tumors: MCT4 is a marker of oxidative stress in cancer-associated fibroblasts. Cell Cycle 10: 1772-1783.
35. Ullah MS, Davies AJ, Halestrap AP, (2006) The plasma membrane lactate transporter MCT4, but not MCT1, is up-regulated by hypoxia through a HIF-1alpha-dependent mechanism. J Biol Chem 281: 9030-9037.
36. Dimmer KS, Friedrich B, Lang F, Deitmer JW, Broer S, (2000) The low-affinity monocarboxylate transporter MCT4 is adapted to the export of lactate in highly glycolytic cells. Biochem J 350 Pt 1: 219-227.
37. Dhup S, Dadhich RK, Porporato PE, Sonveaux P, (2012) Multiple biological activities of lactic acid in cancer: influences on tumor growth, angiogenesis and metastasis. Curr Pharm Des 18: 1319-1330.
38. Wilson MC, Meredith D, Fox JE, Manoharan C, Davies AJ, et al. (2005) Basigin (CD147) is the target for organomercurial inhibition of monocarboxylate transporter isoforms 1 and 4: the ancillary protein for the insensitive MCT2 is EMBIGIN (gp70). J Biol Chem 280: 27213-27221.
39. Finch NA, Linser PJ, Ochrietor JD, (2009) Hydrophobic interactions stabilize the basigin-MCT1 complex. Protein J 28: 362-368.
40. Fredriksson S, Gullberg M, Jarvius J, Olsson C, Pietras K, et al. (2002) Protein detection using proximity-dependent DNA ligation assays. Nat Biotechnol 20: 473-477.
41. Manning Fox JE, Meredith D, Halestrap AP, (2000) Characterisation of human monocarboxylate transporter 4 substantiates its role in lactic acid efflux from skeletal muscle. J Physiol 529 Pt 2: 285-293.
42. Weinberg F, Hamanaka R, Wheaton WW, Weinberg S, Joseph J, et al. (2010) Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proc Natl Acad Sci U S A 107: 8788-8793.
43. Unruh A, Ressel A, Mohamed HG, Johnson RS, Nadrowitz R, et al. (2003) The hypoxia-inducible factor-1 alpha is a negative factor for tumor therapy. Oncogene 22: 3213-3220.
44. Brahimi-Horn MC, Chiche J, Pouyssegur J, (2007) Hypoxia and cancer. J Mol Med 85: 1301-1307.
45. Martinez-Outschoorn UE, Pavlides S, Howell A, Pestell RG, Tanowitz HB, et al. (2011) Stromal-epithelial metabolic coupling in cancer: Integrating autophagy and metabolism in the tumor microenvironment. Int J Biochem Cell Biol 43: 1045-1051.
46. Fiaschi T, Marini A, Giannoni E, Taddei ML, Gandellini P, et al. (2012) Reciprocal metabolic reprogramming through lactate shuttle corrdinately influences tumor-stroma interplay. Cancer Res 10.1158/0008-5472.CAN-12-1949 [doi].
47. Gatenby RA, Gillies RJ, (2004) Why do cancers have high aerobic glycolysis? Nat Rev Cancer 4: 891-899.
48. Vander Heiden MG, Cantley LC, Thompson CB, (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033.
49. Onnis B, Rapisarda A, Melillo G, (2009) Development of HIF-1 inhibitors for cancer therapy. J Cell Mol Med 13: 2780-2786.
50. Semenza GL, (2009) Involvement of oxygen-sensing pathways in physiologic and pathologic erythropoiesis. Blood 114: 2015-2019.
51. King MP, Attardi G, (1989) Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 246: 500-503.
52. Feron O, Belhassen L, Kobzik L, Smith TW, Kelly RA, et al. (1996) Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J Biol Chem 271: 22810-22814.
53. Quintero M, Colombo SL, Godfrey A, Moncada S, (2006) Mitochondria as signaling organelles in the vascular endothelium. Proc Natl Acad Sci U S A 103: 5379-5384.
54. Sonveaux P, Brouet A, Havaux X, Gregoire V, Dessy C, et al. (2003) Irradiation-induced angiogenesis through the up-regulation of the nitric oxide pathway: implications for tumor radiotherapy. Cancer Res 63: 1012-1019.
55. Bouzin C, Brouet A, De Vriese J, DeWever J, Feron O, (2007) Effects of vascular endothelial growth factor on the lymphocyte-endothelium interactions: identification of caveolin-1 and nitric oxide as control points of endothelial cell anergy. J Immunol 178: 1505-1511.
56. Moon EJ, Sonveaux P, Porporato PE, Danhier P, Gallez B, et al. (2010) NADPH oxidase-mediated reactive oxygen species production activates hypoxia-inducible factor-1 (HIF-1) via the ERK pathway after hyperthermia treatment. Proc Natl Acad Sci U S A 107: 20477-20482.
57. Stragand JJ, Barlogie B, White RA, Drewinko B, (1981) Biological properties of the human colonic adenocarcinoma cell line SW 620 grown as a xenograft in the athymic mouse. Cancer Res 41: 3364-3369.
58. Tomayko MM, Reynolds CP, (1989) Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 24: 148-154.