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Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis

Bibliographic reference Sonveaux, Pierre ; Copetti, Tamara ; De Saedeleer, Christophe ; Végran, Frédérique ; Verrax, Julien ; et. al. Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis. In: PLoS One, Vol. 7, no.3, p. e33418 [1-13] (2012)
Permanent URL http://hdl.handle.net/2078.1/132225
  1. Hanahan Douglas, Weinberg Robert A., Hallmarks of Cancer: The Next Generation, 10.1016/j.cell.2011.02.013
  2. R Wu, J Biol Chem, 234, 1036 (1959)
  3. Semenza Gregg L, Hypoxia-inducible factor 1: master regulator of O2 homeostasis, 10.1016/s0959-437x(98)80016-6
  4. Elstrom Rebecca L., Bauer Daniel E., Buzzai Monica, Karnauskas Robyn, Harris Marian H., Plas David R., Zhuang Hongming, Cinalli Ryan M., Alavi Abass, Rudin Charles M., Thompson Craig B., Akt Stimulates Aerobic Glycolysis in Cancer Cells, 10.1158/0008-5472.can-03-2904
  5. Gordan John D., Thompson Craig B., Simon M. Celeste, HIF and c-Myc: Sibling Rivals for Control of Cancer Cell Metabolism and Proliferation, 10.1016/j.ccr.2007.07.006
  6. Carmeliet Peter, Jain Rakesh K., 10.1038/35025220
  7. Pugh Christopher W, Ratcliffe Peter J, Regulation of angiogenesis by hypoxia: role of the HIF system, 10.1038/nm0603-677
  8. Berra E., HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1  in normoxia, 10.1093/emboj/cdg392
  9. Hirsilä Maija, Koivunen Peppi, Günzler Volkmar, Kivirikko Kari I., Myllyharju Johanna, Characterization of the Human Prolyl 4-Hydroxylases That Modify the Hypoxia-inducible Factor, 10.1074/jbc.m304982200
  10. Ratcliffe Peter J., Maxwell Patrick H., Wiesener Michael S., Chang Gin-Wen, Clifford Steven C., Vaux Emma C., Cockman Matthew E., Wykoff Charles C., Pugh Christopher W., Maher Eamonn R., 10.1038/20459
  11. Semenza Gregg L., Targeting HIF-1 for cancer therapy, 10.1038/nrc1187
  12. Semenza Gregg L, HIF-1: upstream and downstream of cancer metabolism, 10.1016/j.gde.2009.10.009
  13. Unruh Annika, Ressel Anke, Mohamed Hamid G, Johnson Randall S, Nadrowitz Roger, Richter Eckart, Katschinski Dörthe M, Wenger Roland H, The hypoxia-inducible factor-1α is a negative factor for tumor therapy, 10.1038/sj.onc.1206385
  14. Brahimi-Horn M. Christiane, Chiche Johanna, Pouysségur Jacques, Hypoxia and cancer, 10.1007/s00109-007-0281-3
  15. Fraisl Peter, Mazzone Massimiliano, Schmidt Thomas, Carmeliet Peter, Regulation of Angiogenesis by Oxygen and Metabolism, 10.1016/j.devcel.2009.01.003
  16. GREEN HOWARD, GOLDBERG BURTON, Collagen and Cell Protein Synthesis by an Established Mammalian Fibroblast Line, 10.1038/204347a0
  17. Hunt Thomas K., Aslam Rummana S., Beckert Stefan, Wagner Silvia, Ghani Q. Perveen, Hussain M. Zamirul, Roy Sashwati, Sen Chandan K., Aerobically Derived Lactate Stimulates Revascularization and Tissue RepairviaRedox Mechanisms, 10.1089/ars.2007.1674
  18. Trabold Odilo, Wagner Silvia, Wicke Corinna, Scheuenstuhl Heinz, Hussain M. Zamirul, Rosen Noah, Seremetiev Alan, Becker Horst D., Hunt Thomas K., Lactate and oxygen constitute a fundamental regulatory mechanism in wound healing, 10.1046/j.1524-475x.2003.11621.x
  19. Constant James S, Feng John J, Zabel David D, Yuan Hui, Suh David Y, Scheuenstuhl Heinz, Hunt Thomas K, Hussain M. Zamirul, Lactate elicits vascular endothelial growth factor from macrophages: a possible alternative to hypoxia, 10.1111/j.1524-475x.2000.00353.x
  20. Xiong Ming, Elson Genie, Legarda Diana, Leibovich Samuel Joseph, Production of Vascular Endothelial Growth Factor by Murine Macrophages, 10.1016/s0002-9440(10)65601-5
  21. 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
  22. 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
  23. 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
  24. Walenta S., Schroeder T., Mueller-Klieser W., Lactate in Solid Malignant Tumors: Potential Basis of a Metabolic Classification in Clinical Oncology, 10.2174/0929867043364711
  25. Walenta Stefan, Snyder Stacey, Haroon Zishan A, Braun Rod D, Amin Khalid, Brizel David, Mueller-Klieser Wolfgang, Chance Britton, Dewhirst Mark W, Tissue gradients of energy metabolites mirror oxygen tension gradients in a rat mammary carcinoma model, 10.1016/s0360-3016(01)01700-x
  26. P Sonveaux, J Clin Invest, 118, 3930 (2008)
  27. Kerbel Robert S., Tumor Angiogenesis, 10.1056/nejmra0706596
  28. Forsythe J A, Jiang B H, Iyer N V, Agani F, Leung S W, Koos R D, Semenza G L, Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1., 10.1128/mcb.16.9.4604
  29. Calvani M., Hypoxic induction of an HIF-1 -dependent bFGF autocrine loop drives angiogenesis in human endothelial cells, 10.1182/blood-2005-09-3541
  30. Li Fang, Sonveaux Pierre, Rabbani Zahid N., Liu Shanling, Yan Bin, Huang Qian, Vujaskovic Zeljko, Dewhirst Mark W., Li Chuan-Yuan, Regulation of HIF-1α Stability through S-Nitrosylation, 10.1016/j.molcel.2007.02.024
  31. JH Wilkinson, Enzyme, 13, 170 (1972)
  32. HALESTRAP Andrew P., PRICE Nigel T., The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation, 10.1042/bj3430281
  33. Halestrap Andrew P., Meredith David, The SLC16 gene family?from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond, 10.1007/s00424-003-1067-2
  34. JE Manning Fox, J Physiol, 529 Pt 2, 285 (2000)
  35. Masson Véronique, Devy Laetitia, Grignet-Debrus Christine, Bernt Sarah, Bajou Khalid, Blacher Silvia, Roland Guy, Chang Yawen, Fong Timothy, Carmeliet Peter, Foidart Jean-Michel, Noël Agnès, Mouse aortic ring assay: A new approach of the molecular genetics of angiogenesis, 10.1251/bpo30
  36. Sonveaux P., Caveolin-1 Expression Is Critical for Vascular Endothelial Growth Factor-Induced Ischemic Hindlimb Collateralization and Nitric Oxide-Mediated Angiogenesis, 10.1161/01.res.0000136344.27825.72
  37. Tang Nan, Wang Lianchun, Esko Jeffrey, Giordano Frank J., Huang Yan, Gerber Hans-Peter, Ferrara Napoleone, Johnson Randall S., Loss of HIF-1α in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis, 10.1016/j.ccr.2004.09.026
  38. Deudero Juan José P., Caramelo Carlos, Castellanos María Carmen, Neria Fernando, Fernández-Sánchez Ruth, Calabia Olalla, Peñate Silvia, González-Pacheco Francisco Román, Induction of Hypoxia-inducible Factor 1α Gene Expression by Vascular Endothelial Growth Factor, 10.1074/jbc.m703875200
  39. Vander Heiden M. G., Cantley L. C., Thompson C. B., Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation, 10.1126/science.1160809
  40. Feron Olivier, Pyruvate into lactate and back: From the Warburg effect to symbiotic energy fuel exchange in cancer cells, 10.1016/j.radonc.2009.06.025
  41. DeBerardinis R J, Cheng T, Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer, 10.1038/onc.2009.358
  42. Koukourakis Michael I., Giatromanolaki Alexandra, Harris Adrian L., Sivridis Efthimios, Comparison of Metabolic Pathways between Cancer Cells and Stromal Cells in Colorectal Carcinomas: a Metabolic Survival Role for Tumor-Associated Stroma, 10.1158/0008-5472.can-05-3260
  43. C Julien, Br J Cancer, 91, 374 (2004)
  44. Rauch Cyril, Pluen Alain, Foster Neil, Loughna Paul, Mobasheri Ali, Lagadic-Gossmann Dominique, Counillon Laurent, On Some Aspects of the Thermodynamic of Membrane Recycling Mediated by Fluid Phase Endocytosis: Evaluation of Published Data and Perspectives, 10.1007/s12013-009-9072-5
  45. Paulusma C.C., Oude Elferink R.P.J., The type 4 subfamily of P-type ATPases, putative aminophospholipid translocases with a role in human disease, 10.1016/j.bbadis.2005.04.006
  46. Wilbers K.H., Haest C.W.M., Von Benthem M., Deuticke B., Influence of enzymatic phospholipid cleavage on the permeability of the erythrocyte membrane. II. Protein-mediated transfer of monosaccharides and anions, 10.1016/0005-2736(79)90380-8
  47. Mahon P. C., FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity, 10.1101/gad.924501
  48. Elvidge Gareth P., Glenny Louisa, Appelhoff Rebecca J., Ratcliffe Peter J., Ragoussis Jiannis, Gleadle Jonathan M., Concordant Regulation of Gene Expression by Hypoxia and 2-Oxoglutarate-dependent Dioxygenase Inhibition : THE ROLE OF HIF-1α, HIF-2α, AND OTHER PATHWAYS, 10.1074/jbc.m511408200
  49. Semenza G. L., Involvement of oxygen-sensing pathways in physiologic and pathologic erythropoiesis, 10.1182/blood-2009-05-189985
  50. Carmeliet Peter, Dor Yuval, Herbert Jean-Marc, Fukumura Dai, Brusselmans Koen, Dewerchin Mieke, Neeman Michal, Bono Françoise, Abramovitch Rinat, Maxwell Patrick, Koch# Cameron J., Ratcliffe Peter, Moons Lieve, Jain Rakesh K., Collen Désiré, Keshet Eli, 10.1038/28867
  51. Iyer N. V., Kotch L. E., Agani F., Leung S. W., Laughner E., Wenger R. H., Gassmann M., Gearhart J. D., Lawler A. M., Yu A. Y., Semenza G. L., Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1alpha, 10.1101/gad.12.2.149
  52. Ryan H. E., HIF-1alpha is required for solid tumor formation and embryonic vascularization, 10.1093/emboj/17.11.3005
  53. Le Bras A, Lionneton F, Mattot V, Lelièvre E, Caetano B, Spruyt N, Soncin F, HIF-2α specifically activates the VE-cadherin promoter independently of hypoxia and in synergy with Ets-1 through two essential ETS-binding sites, 10.1038/sj.onc.1210566
  54. Bertram John S., Janik Przemyslaw, Establishment of a cloned line of Lewis lung carcinoma cells adapted to cell culture, 10.1016/0304-3835(80)90130-5
  55. HS Taper, Cancer Res, 26, 143 (1966)
  56. Martinive P., Reversal of temporal and spatial heterogeneities in tumor perfusion identifies the tumor vascular tone as a tunable variable to improve drug delivery, 10.1158/1535-7163.mct-05-0472
  57. Diepart Caroline, Verrax Julien, Calderon Pedro Buc, Feron Olivier, Jordan Bénédicte F., Gallez Bernard, Comparison of methods for measuring oxygen consumption in tumor cells in vitro, 10.1016/j.ab.2009.09.029
  58. P Sonveaux, Cancer Res, 63, 1012 (2003)
  59. Feron Olivier, Belhassen Laurent, Kobzik Lester, Smith Thomas W., Kelly Ralph A., Michel Thomas, Endothelial Nitric Oxide Synthase Targeting to Caveolae : SPECIFIC INTERACTIONS WITH CAVEOLIN ISOFORMS IN CARDIAC MYOCYTES AND ENDOTHELIAL CELLS, 10.1074/jbc.271.37.22810
  60. Quintero M., Colombo S. L., Godfrey A., Moncada S., Mitochondria as signaling organelles in the vascular endothelium, 10.1073/pnas.0601026103
  61. Bouzin C., Brouet A., De Vriese J., DeWever J., Feron O., 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, 10.4049/jimmunol.178.3.1505
  62. Dimmeler Stefanie, Dernbach Elisabeth, Zeiher Andreas M, Phosphorylation of the endothelial nitric oxide synthase at Ser-1177 is required for VEGF-induced endothelial cell migration, 10.1016/s0014-5793(00)01657-4
  63. Brouet A., Sonveaux P., Dessy C., Moniotte S., Balligand J.-L., Feron O., Hsp90 and Caveolin Are Key Targets for the Proangiogenic Nitric Oxide-Mediated Effects of Statins, 10.1161/hh2201.100319
  64. Del Prete E., Lutz T.A., Scharrer E., Inhibition of glucose oxidation by α-cyano-4-hydroxycinnamic acid stimulates feeding in rats, 10.1016/j.physbeh.2003.10.007
  65. MW Dewhirst, Br J Cancer, Suppl 27, S247 (1996)
  66. P Sonveaux, FASEB J, 16, 1979 (2002)