Cerebral ketone body oxidation is facilitated by a high fat diet enriched with advanced glycation end products in normal and diabetic rats

Frontiers in Neuroscience

Volumn 10, Issue NOV, 2016, Pages

  de Assis, Adriano M ^a   da Silva, Jussemara S ^a   Rech, Anderson ^a   Longoni, Aline ^a   Nonose, Yasmine ^a   Repond, Cendrine ^b   de Bittencourt Pasquali, Matheus A ^a,c   Moreira, José C F ^a   Souza, Diogo O ^a   Pellerin, Luc ^b  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

Author keywords

AGEs; Brain energy metabolism; Diabetes mellitus; High fat diet; MCTs

Indexed keywords

3 HYDROXYBUTYRIC ACID; ADVANCED GLYCATION END PRODUCT; KETONE BODY; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 2;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOENERGY; BRAIN CORTEX; BRAIN CORTEX SLICE; BRAIN METABOLISM; CONTROLLED STUDY; DISEASE EXACERBATION; ENERGY METABOLISM; FATTY ACID BLOOD LEVEL; HIPPOCAMPUS; INSULIN DEPENDENT DIABETES MELLITUS; KETONE BODY BLOOD LEVEL; LIPID DIET; MALE; METABOLIC PARAMETERS; NONHUMAN; PROTEIN EXPRESSION; RAT;

EID: 85009727487     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2016.00509     Document Type: Article

References (50)

1. Aleeva, G. N., Kiyasov, A. P., Minnebaev, M. M., Burykin, I. M., and Khafiz'yanova, R. K. h. (2002). Changes in the count of pancreatic beta-and alpha-cells and blood glucose level in rats with alloxan-induced diabetes. Bull. Exp. Biol. Med. 133, 127-129.
2. Ahmed, N., and Zahra, N. (2011). Neurochemical correlates of alloxan diabetes: glucose and related brain metabolism in the rat. Neurochem. Res. 36, 494-505. doi: 10.1007/s11064-010-0369-y
3. Baud, O., Fayol, L., Gressens, P., Pellerin, L., Magistretti, P., Evrard, P., et al. (2003). Perinatal and early postnatal changes in the expression of monocarboxylate transporters MCT1 and MCT2 in the rat forebrain. J. Comp. Neurol. 465, 445-454. doi: 10.1002/cne.10853
4. Brands, A. M., Kessels, R. P., Hoogma, R. P., Henselmans, J. M., van der Beek Boter, J. W., Kappelle, L. J., et al. (2006). Cognitive performance, psychological well-being, and brain magnetic resonance imaging in older patients with type 1 diabetes. Diabetes 55, 1800-1806. doi: 10.2337/db05-1226
5. Brownlee, M. (2005). The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54, 1615-1625. doi: 10.2337/diabetes.54.6.1615
6. Cai, W., Uribarri, J., Zhu, L., Chen, X., Swamy, S., Zhao, Z., et al. (2014). Oral glycotoxins are a modifiable cause of dementia and the metabolic syndrome in mice and humans. Proc. Natl. Acad. Sci. U.S.A. 111, 4940-4945. doi: 10.1073/pnas.1316013111
7. Carneiro, L., and Pellerin, L. (2015). Monocarboxylate transporters: new players in body weight regulation. Obes. Rev. 16(Suppl. 1), 55-66. doi: 10.1111/obr.12256
8. Chenal, J., and Pellerin, L. (2007). Noradrenaline enhances the expression of the neuronal monocarboxylate transporter MCT2 by translational activation via stimulation of PI3K/Akt and the mTOR/S6K pathway. J. Neurochem. 102, 389-397. doi: 10.1111/j.1471-4159.2007.04495.x
9. Chenal, J., Pierre, K., and Pellerin, L. (2008). Insulin and IGF-1 enhance the expression of the neuronal monocarboxylate transporter MCT2 by translational activation via stimulation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin pathway. Eur. J. Neurosci. 27, 53-65. doi: 10.1111/j.1460-9568.2007.05981.x
10. Chiry, O., Pellerin, L., Monnet-Tschudi, F., Fishbein, W. N., Merezhinskaya, N., Magistretti, P. J., et al. (2006). Expression of the monocarboxylate transporter MCT1 in the adult human brain cortex. Brain Res. 1070, 65-70. doi: 10.1016/j.brainres.2005.11.064
11. Crane, S. C., and Morgan, B. L. (1983). The effect of alterations in ketone body availability on the utilization of beta-hydroxybutyrate by developing rat brain. J. Nutr. 113, 1063-1072.
12. de Assis, A. M., Rech, A., Longoni, A., da Silva Morrone, M., de Bittencourt Pasquali, M. A., Perry, M. L., et al. (2015). Dietary n-3 polyunsaturated fatty acids revert renal responses induced by a combination of 2 protocols that increase the amounts of advanced glycation end product in rats. Nutr. Res. 35, 512-522. doi: 10.1016/j.nutres.2015.04.013
13. de Assis, A. M., Rech, A., Longoni, A., Rotta, L. N., Denardin, C. C., Pasquali, M. A., et al. (2012). Omega3-Polyunsaturated fatty acids prevent lipoperoxidation, modulate antioxidant enzymes, and reduce lipid content but do not alter glycogen metabolism in the livers of diabetic rats fed on a high fat thermolyzed diet. Mol. Cell. Biochem. 361, 151-160. doi: 10.1007/s11010-011-1099-4
14. de Assis, A. M., Rieger, D. K., Longoni, A., Battu, C., Raymundi, S., da Rocha, R. F., et al. (2009). High fat and highly thermolyzed fat diets promote insulin resistance and increase DNA damage in rats. Exp. Biol. Med. 234, 1296-1304. doi: 10.3181/0904-RM-126
15. Duarte, J. M., Agostinho, P. M., Carvalho, R. A., and Cunha, R. A. (2012). Caffeine consumption prevents diabetes-induced memory impairment and synaptotoxicity in the hippocampus of NONcZNO10/LTJ mice. PLoS ONE 7:e21899. doi: 10.1371/journal.pone.0021899
16. Federiuk, I. F., Casey, H. M., Quinn, M. J., Wood, M. D., and Ward, W. K. (2004). Induction of type-1 diabetes mellitus in laboratory rats by use of alloxan: route of administration, pitfalls, and insulin treatment. Comp. Med. 54, 252-257.
17. Ferreira, G. C., Tonin, A., Schuck, P. F., Viegas, C. M., Ceolato, P. C., Latini, A., et al. (2007). Evidence for a synergistic action of glutaric and 3-hydroxyglutaric acids disturbing rat brain energy metabolism. Int. J. Dev. Neurosci. 25, 391-398. doi: 10.1016/j.ijdevneu.2007.05.009
18. Frier, B. M. (2011). Cognitive functioning in type 1 diabetes: the Diabetes Control and Complications Trial (DCCT) revisited. Diabetologia 54, 233-236. doi: 10.1007/s00125-010-1983-6
19. Froberg, M. K., Gerhart, D. Z., Enerson, B. E., Manivel, C., Guzman-Paz, M., Seacotte, N., et al. (2001). Expression of monocarboxylate transporter MCT1 in normal and neoplastic human CNS tissues. Neuroreport 12, 761-765. doi: 10.1097/00001756-200103260-00030
20. Greenwood, C. E., and Winocur, G. (2005). High-fat diets, insulin resistance and declining cognitive function. Neurobiol. Aging 26(Suppl. 1), 42-45. doi: 10.1016/j.neurobiolaging.2005.08.017
21. Hartman, A. L. (2012). Neuroprotection in metabolism-based therapy. Epilepsy Res. 100, 286-294. doi: 10.1016/j.eplepsyres.2011.04.016
22. Horwitz, W., Kamps, L. R., and Boyer, K. W. (1980). Quality assurance in the analysis of foods and trace constituents. J. Assoc. Off. Anal. Chem. 63, 1344-1354.
23. Hrynevich, S. V., Waseem, T. V., Hébert, A., Pellerin, L., and Fedorovich, S. V. (2016). beta-Hydroxybutyrate supports synaptic vesicle cycling but reduces endocytosis and exocytosis in rat brain synaptosomes. Neurochem. Int. 93, 73-81. doi: 10.1016/j.neuint.2015.12.014
24. Jacobson, A. M., Ryan, C. M., Cleary, P. A., Waberski, B. H., Weinger, K., Musen, G., et al. (2011). Biomedical risk factors for decreased cognitive functioning in type 1 diabetes: an 18 year follow-up of the Diabetes Control and Complications Trial (DCCT) cohort. Diabetologia 54, 245-255. doi: 10.1007/s00125-010-1883-9
25. Kante, A., Cherkaoui Malki, M., Coquard, C., and Latruffe, N. (1990). Metabolic control of the expression of mitochondrial D-beta-hydroxybutyrate dehydrogenase, a ketone body converting enzyme. Biochim. Biophys. Acta 1033, 291-297. doi: 10.1016/0304-4165(90)90136-K
26. Kaplan, R. J., and Greenwood, C. E. (1998). Dietary saturated fatty acids and brain function. Neurochem. Res. 23, 615-626. doi: 10.1023/A:1022478503367
27. Lee, Y., Morrison, B. M., Li, Y., Lengacher, S., Farah, M. H., Hoffman, P. N., et al. (2012). Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487, 443-448. doi: 10.1038/nature11314
28. Leino, R. L., Gerhart, D. Z., Duelli, R., Enerson, B. E., and Drewes, L. R. (2001). Diet-induced ketosis increases monocarboxylate transporter (MCT1) levels in rat brain. Neurochem. Int. 38, 519-527. doi: 10.1016/S0197-0186(00)00102-9
29. Lenzen, S. (2008). The mechanisms of alloxan-and streptozotocin-induced diabetes. Diabetologia 51, 216-226. doi: 10.1007/s00125-007-0886-7
30. Lombardo, Y. B., Hron, W. T., and Menahan, L. A. (1978). Effect of insulin in vitro on the isolated, perfused alloxan-diabetic rat liver. Diabetologia 14, 47-51. doi: 10.1007/BF00429707
31. Marcillac, F., Brix, B., Repond, C., Jöhren, O., and 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. doi: 10.1002/glia.21240
32. Mattson, M. P. (2012). Energy intake and exercise as determinants of brain health and vulnerability to injury and disease. Cell Metab. 16, 706-722. doi: 10.1016/j.cmet.2012.08.012
33. McCrimmon, R. J., Ryan, C. M., and Frier, B. M. (2012). Diabetes and cognitive dysfunction. Lancet 379, 2291-2299. doi: 10.1016/S0140-6736(12)60360-2
34. Mcnay, E. C., and Recknagel, A. K. (2011). Brain insulin signaling: a key component of cognitive processes and a potential basis for cognitive impairment in type 2 diabetes. Neurobiol. Learn. Mem. 96, 432-442. doi: 10.1016/j.nlm.2011.08.005
35. Miethke, H., Wittig, B., Nath, A., and Jungermann, K. (1986). Gluconeogenic-glycolytic capacities and metabolic zonation in liver of rats with streptozotocin, non-ketotic as compared to alloxan, ketotic diabetes. Histochemistry 85, 483-489. doi: 10.1007/BF00508430
36. Miles, W. R., and Root, H. F. (1922). Psychological tests applied in diabetic patients. Arch. Intern. Med. 30, 11. doi: 10.1001/archinte.1922.00110120086003
37. Müller, A. P., Longoni, A., Farina, M., da Silveira, C. K. B., Souza, D. O., Perry, M. L. S., et al. (2013). Propylthiouracil-induced hypothyroidism during lactation alters leucine and mannose metabolism in rat cerebellar slices. Exp. Biol. Med. 238, 31-36. doi: 10.1258/ebm.2012.012255
38. Pellerin, L., Pellegri, G., Martin, J. L., and Magistretti, P. J. (1998). Expression of monocarboxylate transporter mRNAs in mouse brain: support for a distinct role of lactate as an energy substrate for the neonatal vs. adult brain. Proc. Natl. Acad. Sci. U.S.A. 95, 3990-3995. doi: 10.1073/pnas.95.7.3990
39. Pierre, K., Magistretti, P. J., and Pellerin, L. (2002). MCT2 is a major neuronal monocarboxylate transporter in the adult mouse brain. J. Cereb. Blood Flow Metab. 22, 586-595. doi: 10.1097/00004647-200205000-00010
40. Pierre, K., Parent, A., Jayet, P. Y., Halestrap, A. P., Scherrer, U., and Pellerin, L. (2007). Enhanced expression of three monocarboxylate transporter isoforms in the brain of obese mice. J. Physiol. 583, 469-486. doi: 10.1113/jphysiol.2007.138594
41. Pierre, K., and Pellerin, L. (2005). Monocarboxylate transporters in the central nervous system: distribution, regulation and function. J. Neurochem. 94, 1-14. doi: 10.1111/j.1471-4159.2005.03168.x
42. Pierre, K., Pellerin, L., Debernardi, R., Riederer, B. M., and Magistretti, P. J. (2000). Cell-specific localization of monocarboxylate transporters, MCT1 and MCT2, in the adult mouse brain revealed by double immunohistochemical labeling and confocal microscopy. Neuroscience 100, 617-627. doi: 10.1016/S0306-4522(00)00294-3
43. Puchowicz, M. A., Xu, K., Sun, X., Ivy, A., Emancipator, D., and Lamanna, J. C. (2007). Diet-induced ketosis increases capillary density without altered blood flow in rat brain. Am. J. Physiol. Endocrinol. Metab. 292, E1607-E1615. doi: 10.1152/ajpendo.00512.2006
44. Robinet, C., and Pellerin, L. (2010). Brain-derived neurotrophic factor enhances the expression of the monocarboxylate transporter 2 through translational activation in mouse cultured cortical neurons. J. Cereb. Blood Flow Metab. 30, 286-298. doi: 10.1038/jcbfm.2009.208
45. Robinet, C., and Pellerin, L. (2011). Brain-derived neurotrophic factor enhances the hippocampal expression of key postsynaptic proteins in vivo including the monocarboxylate transporter MCT2. Neuroscience 192, 155-163. doi: 10.1016/j.neuroscience.2011.06.059
46. Roman-Lopez, C. R., and Allred, J. B. (1987). Acute alloxan diabetes alters the activity but not the total quantity of acetyl CoA carboxylase in rat liver. J. Nutr. 117, 1976-1981.
47. Rösen, P., Windeck, P., Zimmer, H. G., Frenzel, H., Bürrig, K. F., and Reinauer, H. (1986). Myocardial performance and metabolism in non-ketotic, diabetic rat hearts: myocardial function and metabolism in vivo and in the isolated perfused heart under the influence of insulin and octanoate. Basic Res. Cardiol. 81, 620-635. doi: 10.1007/BF02005186
48. Ryan, C. M., Geckle, M. O., and Orchard, T. J. (2003). Cognitive efficiency declines over time in adults with Type 1 diabetes: effects of micro-and macrovascular complications. Diabetologia 46, 940-948. doi: 10.1007/s00125-003-1128-2
49. Wilson, G. L., Patton, N. J., McCord, J. M., Mullins, D. W., and Mossman, B. T. (1984). Mechanisms of streptozotocin-and alloxan-induced damage in rat B cells. Diabetologia 27, 587-591. doi: 10.1007/BF00276973
50. Winocur, G., and Greenwood, C. E. (2005). Studies of the effects of high fat diets on cognitive function in a rat model. Neurobiol. Aging 26(Suppl. 1), 46-49. doi: 10.1016/j.neurobiolaging.2005.09.003