Lactate administration reproduces specific brain and liver exercise-related changes

Journal of Neurochemistry

Volumn 127, Issue 1, 2013, Pages 91-100

  E, Lezi ^a   Lu, Jianghua ^a,b   Selfridge, J Eva ^b   Burns, Jeffrey M ^a,b   Swerdlow, Russell H ^a,b  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

brain; exercise; lactate; liver

Indexed keywords

GLUCOSE; INSULIN; LACTIC ACID; MESSENGER RNA; MITOCHONDRIAL DNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOENERGY; BRAIN METABOLISM; CONTROLLED STUDY; DOWN REGULATION; EXERCISE INTENSITY; EXHAUSTION; GENE DOSAGE; GENE EXPRESSION; GLUCONEOGENESIS; LACTATE BLOOD LEVEL; LIVER METABOLISM; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RESPIRATORY CHAIN; TREADMILL EXERCISE; UPREGULATION;

BRAIN; EXERCISE; LACTATE; LIVER;

ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; BRAIN; BRAIN CHEMISTRY; DNA, MITOCHONDRIAL; ENERGY METABOLISM; GENE DOSAGE; IMMUNOHISTOCHEMISTRY; INSULIN; LACTIC ACID; LIVER; MALE; MICE; MICE, INBRED C57BL; NUCLEAR RESPIRATORY FACTOR 1; PHYSICAL CONDITIONING, ANIMAL; POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84884896415     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12394     Document Type: Article

References (55)

1. Arany Z., Foo S. Y., Ma Y., et al,. (2008) HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature 451, 1008-1012.
2. Bayod S., Del Valle J., Canudas A. M., Lalanza J. F., Sanchez-Roige S., Camins A., Escorihuela R. M., and, Pallas M., (2011) Long-term treadmill exercise induces neuroprotective molecular changes in rat brain. J. Appl. Physiol. 111, 1380-1390.
3. Bell J. E., Hume R., Busuttil A., and, Burchell A., (1993) Immunocytochemical detection of the microsomal glucose-6-phosphatase in human brain astrocytes. Neuropathol. Appl. Neurobiol. 19, 429-435.
4. Berthet C., Lei H., Thevenet J., Gruetter R., Magistretti P. J., and, Hirt L., (2009) Neuroprotective role of lactate after cerebral ischemia. J. Cereb. Blood Flow Metab. 29, 1780-1789.
5. Bhattacharya S. B., and, Datta A. G., (1993) Is brain a gluconeogenic organ? Mol. Cell. Biochem. 125, 51-57.
6. Billat V. L., Mouisel E., Roblot N., and, Melki J., (2005) Inter- and intrastrain variation in mouse critical running speed. J. Appl. Physiol. 98, 1258-1263.
7. Black J. E., Isaacs K. R., Anderson B. J., Alcantara A. A., and, Greenough W. T., (1990) Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc. Natl Acad. Sci. USA 87, 5568-5572.
8. Bonora E., Targher G., Alberiche M., Bonadonna R. C., Saggiani F., Zenere M. B., Monauni T., and, Muggeo M., (2000) Homeostasis model assessment closely mirrors the glucose clamp technique in the assessment of insulin sensitivity: studies in subjects with various degrees of glucose tolerance and insulin sensitivity. Diabetes Care 23, 57-63.
9. Boumezbeur F., Petersen K. F., Cline G. W., Mason G. F., Behar K. L., Shulman G. I., and, Rothman D. L., (2010) The contribution of blood lactate to brain energy metabolism in humans measured by dynamic 13C nuclear magnetic resonance spectroscopy. J. Neurosci. 30, 13983-13991.
10. Choi C. S., Kim Y. B., Lee F. N., Zabolotny J. M., Kahn B. B., and, Youn J. H., (2002) Lactate induces insulin resistance in skeletal muscle by suppressing glycolysis and impairing insulin signaling. Am. J. Physiol. Endocrinol. Metab. 283, E233-E240.
11. Cross M. J., Dixelius J., Matsumoto T., and, Claesson-Welsh L., (2003) VEGF-receptor signal transduction. Trends Biochem. Sci. 28, 488-494.
12. Duncan J. G., (2011) Mitochondrial dysfunction in diabetic cardio-myopathy. Biochim. Biophys. Acta 1813, 1351-1359.
13. E L., Lu J., Burns J. M., and, Swerdlow R. H,. (2013) Effect of exercise on mouse liver and brain bioenergetic infrastructures. Exp. Physiol. 98, 207-219.
14. Erlichman J. S., Hewitt A., Damon T. L., Hart M., Kurascz J., Li A., and, Leiter J. C., (2008) Inhibition of monocarboxylate transporter 2 in the retrotrapezoid nucleus in rats: a test of the astrocyte-neuron lactate-shuttle hypothesis. J. Neurosci. 28, 4888-4896.
15. Fabel K., Fabel K., Tam B., Kaufer D., Baiker A., Simmons N., Kuo C. J., and, Palmer T. D., (2003) VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur. J. Neurosci. 18, 2803-2812.
16. Fontan-Lozano A., Lopez-Lluch G., Delgado-Garcia J. M., Navas P., and, Carrion A. M., (2008) Molecular bases of caloric restriction regulation of neuronal synaptic plasticity. Mol. Neurobiol. 38, 167-177.
17. Gallagher C. N., Carpenter K. L., Grice P., et al,. (2009) The human brain utilizes lactate via the tricarboxylic acid cycle: a 13C-labelled microdialysis and high-resolution nuclear magnetic resonance study. Brain 132, 2839-2849.
18. Ghosh A., Cheung Y. Y., Mansfield B. C., and, Chou J. Y., (2005) Brain contains a functional glucose-6-phosphatase complex capable of endogenous glucose production. J. Biol. Chem. 280, 11114-11119.
19. Gotoh J., Itoh Y., Kuang T. Y., Cook M., Law M. J., and, Sokoloff L., (2000) Negligible glucose-6-phosphatase activity in cultured astroglia. J. Neurochem. 74, 1400-1408.
20. Guo W., Jiang L., Bhasin S., Khan S. M., and, Swerdlow R. H., (2009) DNA extraction procedures meaningfully influence qPCR-based mtDNA copy number determination. Mitochondrion 9, 261-265.
21. van Hall G., Stromstad M., Rasmussen P., Jans O., Zaar M., Gam C., Quistorff B., Secher N. H., and, Nielsen H. B., (2009) Blood lactate is an important energy source for the human brain. J. Cereb. Blood Flow Metab. 29, 1121-1129.
22. Herzig S., Long F., Jhala U. S., et al,. (2001) CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413, 179-183.
23. Hood D. A., Irrcher I., Ljubicic V., and, Joseph A. M., (2006) Coordination of metabolic plasticity in skeletal muscle. J. Exp. Biol. 209, 2265-2275.
24. Huang H. H., Farmer K., Windscheffel J., Yost K., Power M., Wright D. E., and, Stehno-Bittel L., (2011) Exercise increases insulin content and basal secretion in pancreatic islets in type 1 diabetic mice. Exp. Diabetes Res. 2011, 481427.
25. Jin K., Zhu Y., Sun Y., Mao X. O., Xie L., and, Greenberg D. A., (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl Acad. Sci. USA 99, 11946-11950.
26. Latimer C. S., Searcy J. L., Bridges M. T., Brewer L. D., Popovic J., Blalock E. M., Landfield P. W., Thibault O., and, Porter N. M., (2011) Reversal of glial and neurovascular markers of unhealthy brain aging by exercise in middle-aged female mice. PLoS ONE 6, e26812.
27. Lehninger A. L., Nelson D. L., and, Cox M. M., (2005) Lehninger principles of biochemistry. W.H, Freeman, New York.
28. Lin J., Puigserver P., Donovan J., Tarr P., and, Spiegelman B. M., (2002) Peroxisome proliferator-activated receptor gamma coactivator 1beta (PGC-1beta), a novel PGC-1-related transcription coactivator associated with host cell factor. J. Biol. Chem. 277, 1645-1648.
29. Lin J., Tarr P. T., Yang R., Rhee J., Puigserver P., Newgard C. B., and, Spiegelman B. M., (2003) PGC-1beta in the regulation of hepatic glucose and energy metabolism. J. Biol. Chem. 278, 30843-30848.
30. Marosi K., Bori Z., Hart N., Sarga L., Koltai E., Radak Z., and, Nyakas C., (2012) Long-term exercise treatment reduces oxidative stress in the hippocampus of aging rats. Neuroscience.
31. Matthews D. R., Hosker J. P., Rudenski A. S., Naylor B. A., Treacher D. F., and, Turner R. C., (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412-419.
32. Meats J. E., Tuersley M. D., Best L., Lynch A. M., and, Tomlinson S., (1989) Lactate alters plasma membrane potential, increases the concentration of cytosolic Ca2+ and stimulates the secretion of insulin by the hamster beta-cell line HIT-T15. J. Mol. Endocrinol. 3, 121-128.
33. Mirebeau-Prunier D., Le Pennec S., Jacques C., Gueguen N., Poirier J., Malthiery Y., and, Savagner F., (2010) Estrogen-related receptor alpha and PGC-1-related coactivator constitute a novel complex mediating the biogenesis of functional mitochondria. FEBS J. 277, 713-725.
34. Newman L. A., Korol D. L., and, Gold P. E., (2011) Lactate produced by glycogenolysis in astrocytes regulates memory processing. PLoS ONE 6, e28427.
35. Pellerin L., and, Magistretti P. J., (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl Acad. Sci. USA 91, 10625-10629.
36. Pereira A. C., Huddleston D. E., Brickman A. M., et al,. (2007) An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc. Natl Acad. Sci. USA 104, 5638-5643.
37. Pierre K., and, Pellerin L., (2005) Monocarboxylate transporters in the central nervous system: distribution, regulation and function. J. Neurochem. 94, 1-14.
38. Pugh C. W., and, Ratcliffe P. J., (2003) Regulation of angiogenesis by hypoxia: role of the HIF system. Nat. Med. 9, 677-684.
39. Quistorff B., Secher N. H., and, Van Lieshout J. J., (2008) Lactate fuels the human brain during exercise. FASEB J. 22, 3443-3449.
40. Ren J., Pulakat L., Whaley-Connell A., and, Sowers J. R., (2010) Mitochondrial biogenesis in the metabolic syndrome and cardiovascular disease. J. Mol. Med. 88, 993-1001.
41. Rockwood K., and, Middleton L., (2007) Physical activity and the maintenance of cognitive function. Alzheimers Dement. 3, S38-S44.
42. Scarpulla R. C., (2008) Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol. Rev. 88, 611-638.
43. Secher N. H., Seifert T., and, Van Lieshout J. J., (2008) Cerebral blood flow and metabolism during exercise: implications for fatigue. J. Appl. Physiol. 104, 306-314.
44. Siemeister G., Martiny-Baron G., and, Marme D., (1998) The pivotal role of VEGF in tumor angiogenesis: molecular facts and therapeutic opportunities. Cancer Metastasis Rev. 17, 241-248.
45. Steiner J. L., Murphy E. A., McClellan J. L., Carmichael M. D., and, Davis J. M., (2011) Exercise training increases mitochondrial biogenesis in the brain. J. Appl. Physiol. 111, 1066-1071.
46. Stranahan A. M., Zhou Y., Martin B., and, Maudsley S., (2009) Pharmacomimetics of exercise: novel approaches for hippoc-ampally-targeted neuroprotective agents. Curr. Med. Chem. 16, 4668-4678.
47. Suzuki A., Stern S. A., Bozdagi O., Huntley G. W., Walker R. H., Magistretti P. J., and, Alberini C. M., (2011) Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144, 810-823.
48. Swerdlow R. H., (2011) Role and treatment of mitochondrial DNA-related mitochondrial dysfunction in sporadic neurodegenerative diseases. Curr. Pharm. Des. 17, 3356-3373.
49. Tang K., Xia F. C., Wagner P. D., and, Breen E. C., (2010) Exercise-induced VEGF transcriptional activation in brain, lung and skeletal muscle. Respir. Physiol. Neurobiol. 170, 16-22.
50. Vercauteren K., Gleyzer N., and, Scarpulla R. C., (2009) Short hairpin RNA-mediated silencing of PRC (PGC-1-related coactivator) results in a severe respiratory chain deficiency associated with the proliferation of aberrant mitochondria. J. Biol. Chem. 284, 2307-2319.
51. Vina J., Gomez-Cabrera M. C., Borras C., Froio T., Sanchis-Gomar F., Martinez-Bello V. E., and, Pallardo F. V., (2009) Mitochondrial biogenesis in exercise and in ageing. Adv. Drug Deliv. Rev. 61, 1369-1374.
52. Walenta S., and, Mueller-Klieser W. F., (2004) Lactate: mirror and motor of tumor malignancy. Semin. Radiat. Oncol. 14, 267-274.
53. Wyss M. T., Jolivet R., Buck A., Magistretti P. J., and, Weber B., (2011) In vivo evidence for lactate as a neuronal energy source. J. Neurosci. 31, 7477-7485.
54. Zhang Q., Wu Y., Sha H., Zhang P., Jia J., Hu Y., and, Zhu J., (2012a) Early exercise affects mitochondrial transcription factors expression after cerebral ischemia in rats. Int. J. Mol. Sci. 13, 1670-1679.
55. Zhang Q., Wu Y., Zhang P., Sha H., Jia J., Hu Y., and, Zhu J., (2012b) Exercise induces mitochondrial biogenesis after brain ischemia in rats. Neuroscience 205, 10-17.