A Genetically Encoded FRET Lactate Sensor and Its Use To Detect the Warburg Effect in Single Cancer Cells

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  San Martín, Alejandro ^a,b   Ceballo, Sebastián ^a,b   Ruminot, Iván ^a,b   Lerchundi, Rodrigo ^a,b   Frommer, Wolf B ^c   Barros, Luis Felipe ^a  

^a CENTRO DE ESTUDIOS CIENTÍFICOS CECS   (Chile)

^b UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^c GEOPHYSICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; 3 HYDROXYBUTYRIC ACID; ACETIC ACID; CITRIC ACID; GLUCOSE; GLUTAMIC ACID; LACTIC ACID; MALIC ACID; MONOCARBOXYLATE TRANSPORTER; OXALOACETIC ACID; PYRUVIC ACID; SODIUM AZIDE; SUCCINIC ACID;

ANIMAL CELL; ARTICLE; ASTROCYTE; CANCER CELL; CELL STRAIN HEK293; CONTROLLED STUDY; CYTOSOL; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLIOMA CELL; HUMAN; HUMAN CELL; METABOLISM; MITOCHONDRION; MOUSE; NONHUMAN; SENSOR; WARBURG EFFECT;

ANIMALS; BIOLOGICAL TRANSPORT; BIOSENSING TECHNIQUES; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLIOMA; HEK293 CELLS; HUMANS; LACTIC ACID; MALE; MICE; MODELS, MOLECULAR; PROTEIN CONFORMATION; SINGLE-CELL ANALYSIS; SPATIO-TEMPORAL ANALYSIS; TRANSCRIPTION FACTORS;

EID: 84874458753     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057712     Document Type: Article

References (52)

1. Gladden LB, (2004) Lactate metabolism: a new paradigm for the third millennium. J Physiol 558: 5-30.
2. Brooks GA (2009) Cell-cell and intracellular lactate shuttles. J Physiol 587: 5591-5600. jphysiol.2009.178350 [pii];10.1113/jphysiol.2009.178350 [doi].
3. Pellerin L, Bouzier-Sore AK, Aubert A, Serres S, Merle M, et al. (2007) Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 55: 1251-1262.
4. Barros LF, Deitmer JW, (2010) Glucose and lactate supply to the synapse. Brain Res Rev 63: 149-159.
5. Belanger M, Allaman I, Magistretti PJ, (2011) Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab 14: 724-738 S1550-4131(11)00420-7 [pii];10.1016/j.cmet.2011.08.016.
6. Wyss MT, Jolivet R, Buck A, Magistretti PJ, Weber B, (2011) In vivo evidence for lactate as a neuronal energy source. J Neurosci 31: 7477-7485 31/20/7477 [pii];10.1523/JNEUROSCI.0415-11.2011 [doi].
7. Jolivet R, Allaman I, Pellerin L, Magistretti PJ, Weber B, (2010) Comment on recent modeling studies of astrocyte-neuron metabolic interactions. J Cereb Blood Flow Metab 30: 1982-1986 jcbfm2010132 [pii];10.1038/jcbfm.2010.132 [doi].
8. Rinholm JE, Hamilton NB, Kessaris N, Richardson WD, Bergersen LH, et al. (2011) Regulation of oligodendrocyte development and myelination by glucose and lactate. J Neurosci 31: 538-548 31/2/538 [pii];10.1523/JNEUROSCI.3516-10.2011 [doi].
9. Attwell D, Buchan AM, Charpak S, Lauritzen M, MacVicar BA, et al. (2010) Glial and neuronal control of brain blood flow. Nature 468: 232-243 nature09613 [pii];10.1038/nature09613 [doi].
10. Shimizu H, Watanabe E, Hiyama TY, Nagakura A, Fujikawa A, et al. (2007) Glial Nax channels control lactate signaling to neurons for brain [Na+] sensing. Neuron 54: 59-72.
11. Sotelo-Hitschfeld T, Fernandez-Moncada I, Barros LF, (2012) Acute feedback control of astrocytic glycolysis by lactate. Glia 60: 674-680 10.1002/glia.22304 [doi].
12. Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH, et al. (2011) Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144: 810-823 S0092-8674(11)00132-2 [pii];10.1016/j.cell.2011.02.018 [doi].
13. Newman LA, Korol DL, Gold PE, (2011) Lactate produced by glycogenolysis in astrocytes regulates memory processing. PLoS One 6: e28427 10.1371/journal.pone.0028427 [doi];PONE-D-11-12947 [pii].
14. Ganapathy V, Thangaraju M, Prasad PD, (2009) Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol Ther 121: 29-40.
15. Vander Heiden MG, Cantley LC, Thompson CB, (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033.
16. Tennant DA, Duran RV, Gottlieb E, (2010) Targeting metabolic transformation for cancer therapy. Nat Rev Cancer 10: 267-277 nrc2817 [pii];10.1038/nrc2817 [doi].
17. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, et al. (2012) Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487: 443-448 nature11314 [pii];10.1038/nature11314 [doi].
18. Funfschilling U, Supplie LM, Mahad D, Boretius S, Saab AS, et al. (2012) Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485: 517-521 nature11007 [pii];10.1038/nature11007 [doi].
19. Gao YG, Suzuki H, Itou H, Zhou Y, Tanaka Y, et al. (2008) Structural and functional characterization of the LldR from Corynebacterium glutamicum: a transcriptional repressor involved in L-lactate and sugar utilization. Nucleic Acids Res 36: 7110-7123 gkn827 [pii];10.1093/nar/gkn827 [doi].
20. Aguilera L, Campos E, Gimenez R, Badia J, Aguilar J, et al. (2008) Dual role of LldR in regulation of the lldPRD operon, involved in L-lactate metabolism in Escherichia coli. J Bacteriol 190: 2997-3005 JB.02013-07 [pii];10.1128/JB.02013-07 [doi].
21. Deuschle K, Okumoto S, Fehr M, Looger LL, Kozhukh L, et al. (2005) Construction and optimization of a family of genetically encoded metabolite sensors by semirational protein engineering. Protein Sci 14: 2304-2314.
22. Day RN, Booker CF, Periasamy A, (2008) Characterization of an improved donor fluorescent protein for Forster resonance energy transfer microscopy. J Biomed Opt 13: 031203 10.1117/1.2939094 [doi].
23. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, et al. (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20: 87-90 10.1038/nbt0102-87 [doi];nbt0102-87 [pii].
24. Takanaga H, Frommer WB, (2010) Facilitative plasma membrane transporters function during ER transit. FASEB J 24: 2849-2858 fj.09-146472 [pii];10.1096/fj.09-146472 [doi].
25. Siess EA, Brocks DG, Wieland OH, (1978) Distribution of metabolites between the cytosolic and mitochondrial compartments of hepatocytes isolated from fed rats. Hoppe Seylers Z Physiol Chem 359: 785-798.
26. Kauppinen RA, Hiltunen JK, Hassinen IE, (1982) Compartmentation of citrate in relation to the regulation of glycolysis and the mitochondrial transmembrane proton electrochemical potential gradient in isolated perfused rat heart. Biochim Biophys Acta 681: 286-291 0005-2728(82)90033-0 [pii].
27. Saha AK, Laybutt DR, Dean D, Vavvas D, Sebokova E, et al. (1999) Cytosolic citrate and malonyl-CoA regulation in rat muscle in vivo. Am J Physiol 276: E1030-E1037.
28. Hung YP, Albeck JG, Tantama M, Yellen G, (2011) Imaging cytosolic NADH-NAD(+) redox state with a genetically encoded fluorescent biosensor. Cell Metab 14: 545-554 S1550-4131(11)00342-1 [pii];10.1016/j.cmet.2011.08.012 [doi].
29. Gao C, Hu C, Zheng Z, Ma C, Jiang T, et al. (2012) Lactate utilization is regulated by the FadR-type regulator LldR in Pseudomonas aeruginosa. J Bacteriol 194: 2687-2692 JB.06579-11 [pii];10.1128/JB.06579-11 [doi].
30. Brown MA, Brooks GA, (1994) Trans-stimulation of lactate transport from rat sarcolemmal membrane vesicles. Arch Biochem Biophys 313: 22-28 S0003-9861(84)71353-1 [pii];10.1006/abbi.1994.1353 [doi].
31. Zhao Y, Jin J, Hu Q, Zhou HM, Yi J, et al. (2011) Genetically encoded fluorescent sensors for intracellular NADH detection. Cell Metab 14: 555-566 S1550-4131(11)00350-0 [pii];10.1016/j.cmet.2011.09.004 [doi].
32. Maughan DW, Henkin JA, Vigoreaux JO, (2005) Concentrations of glycolytic enzymes and other cytosolic proteins in the diffusible fraction of a vertebrate muscle proteome. Mol Cell Proteomics 4: 1541-1549 M500053-MCP200 [pii];10.1074/mcp.M500053-MCP200 [doi].
33. Miyawaki A, Griesbeck O, Heim R, Tsien RY, (1999) Dynamic and quantitative Ca2+ measurements using improved cameleons. Proc Natl Acad Sci U S A 96: 2135-2140.
34. Bittner CX, Loaiza A, Ruminot I, Larenas V, Sotelo-Hitschfeld T, et al. (2010) High resolution measurement of the glycolytic rate. Front Neuroenergetics 2: 1-11 doi:10.3389/fnene.2010.00026. doi: 10.3389/fnene.2010.00026.
35. Bittner CX, Valdebenito R, Ruminot I, Loaiza A, Larenas V, et al. (2011) Fast and reversible stimulation of astrocytic glycolysis by K+ and a delayed and persistent effect of glutamate. J Neurosci 31: 4709-4713.
36. Ruminot I, Gutiérrez R, Peña-Munzenmeyer G, Añazco C, Sotelo-Hitschfeld T, et al. (2011) NBCe1 mediates the acute stimulation of astrocytic glycolysis by extracellular K+. J Neurosci 31: 14264-14271.
37. Takanaga H, Chaudhuri B, Frommer WB, (2008) GLUT1 and GLUT9 as major contributors to glucose influx in HepG2 cells identified by a high sensitivity intramolecular FRET glucose sensor. Biochim Biophys Acta 1778: 1091-1099.
38. Ovens MJ, Davies AJ, Wilson MC, Murray CM, Halestrap AP, (2010) AR-C155858 is a potent inhibitor of monocarboxylate transporters MCT1 and MCT2 that binds to an intracellular site involving transmembrane helices 7-10. Biochem J425: 523-530 BJ20091515 [pii];10.1042/BJ20091515 [doi].
39. Georgi T, Engels V, Wendisch VF, (2008) Regulation of L-lactate utilization by the FadR-type regulator LldR of Corynebacterium glutamicum. J Bacteriol 190: 963-971 JB.01147-07 [pii];10.1128/JB.01147-07 [doi].
40. Fehr M, Lalonde S, Lager I, Wolff MW, Frommer WB, (2003) In vivo imaging of the dynamics of glucose uptake in the cytosol of COS-7 cells by fluorescent nanosensors. J Biol Chem 278: 19127-19133.
41. Fehr M, Frommer WB, Lalonde S, (2002) Visualization of maltose uptake in living yeast cells by fluorescent nanosensors. Proc Natl Acad Sci U S A 99: 9846-9851 10.1073/pnas.142089199 [doi];142089199 [pii].
42. Okumoto S, Looger LL, Micheva KD, Reimer RJ, Smith SJ, et al. (2005) Detection of glutamate release from neurons by genetically encoded surface-displayed FRET nanosensors. Proc Natl Acad Sci U S A 102: 8740-8745 0503274102 [pii];10.1073/pnas.0503274102 [doi].
43. Lager I, Looger LL, Hilpert M, Lalonde S, Frommer WB, (2006) Conversion of a putative Agrobacterium sugar-binding protein into a FRET sensor with high selectivity for sucrose. J Biol Chem 281: 30875-30883 M605257200 [pii];10.1074/jbc.M605257200 [doi].
44. Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C, (2008) Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322: 1551-1555.
45. Hussien R, Brooks GA, (2011) Mitochondrial and plasma membrane lactate transporter and lactate dehydrogenase isoform expression in breast cancer cell lines. Physiol Genomics 43: 255-264 physiolgenomics.00177.2010 [pii];10.1152/physiolgenomics.00177.2010 [doi].
46. Hashimoto T, Hussien R, Cho HS, Kaufer D, Brooks GA, (2008) Evidence for the mitochondrial lactate oxidation complex in rat neurons: demonstration of an essential component of brain lactate shuttles. PLoS One 3: e2915 10.1371/journal.pone.0002915 [doi].
47. Dubouchaud H, Butterfield GE, Wolfel EE, Bergman BC, Brooks GA, (2000) Endurance training, expression, and physiology of LDH, MCT1, and MCT4 in human skeletal muscle. Am J Physiol Endocrinol Metab 278: E571-E579.
48. Marcillac F, Brix B, Repond C, Johren O, Pellerin L, (2011) Nitric oxide induces the expression of the monocarboxylate transporter MCT4 in cultured astrocytes by a cGMP-independent transcriptional activation. Glia 59: 1987-1995 10.1002/glia.21240 [doi].
49. 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 J350 Pt 1: 219-27.: 219-227.
50. Tennant DA, Duran RV, Boulahbel H, Gottlieb E, (2009) Metabolic transformation in cancer. Carcinogenesis 30: 1269-1280 bgp070 [pii];10.1093/carcin/bgp070 [doi].
51. Loaiza A, Porras OH, Barros LF, (2003) Glutamate triggers rapid glucose transport stimulation in astrocytes as evidenced by real-time confocal microscopy. J Neurosci 23: 7337-7342.
52. Schmidt MM, Dringen R, (2009) Differential effects of iodoacetamide and iodoacetate on glycolysis and glutathione metabolism of cultured astrocytes. Front Neuroenergetics 1: 1 10.3389/neuro.14.001.2009 [doi].