Peripheral adipose tissue insulin resistance alters lipid composition and function of hippocampal synapses

Journal of Neurochemistry

Volumn 133, Issue 1, 2015, Pages 125-133

  Sallam, Hanaa S ^a   Tumurbaatar, Batbayar ^a   Zhang, Wen Ru ^a   Tuvdendorj, Demidmaa ^a   Chandalia, Manisha ^a,b   Tempia, Filippo ^a   Laezza, Fernanda ^a   Taglialatela, Giulio ^a   Abate, Nicola ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

cognitive dysfunction; ENPP1; glutamate receptors; insulin resistance; lipids; synaptic transmission

Indexed keywords

ECTONUCLEOTIDE PYROPHOSPHATE PHOSPHODIESTERASE 1; FATTY ACID; G PROTEIN COUPLED RECEPTOR 40; INSULIN RECEPTOR; LIPID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; PHOSPHODIESTERASE; PHOSPHOLIPID; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ANTIDIABETIC AGENT; INSULIN;

ADIPOSE TISSUE; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SYNAPTOSOME; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; INSULIN RESISTANCE; LIPID COMPOSITION; LIPID DIET; LIPID STORAGE; MALE; METABOLIC SYNDROME X; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; BRAIN CHEMISTRY; C57BL MOUSE; DRUG EFFECTS; HIPPOCAMPUS; LIPID METABOLISM; METABOLISM; PHYSIOLOGY; SYNAPTOSOME; TRANSGENIC MOUSE;

ANIMALIA; MUS;

ADIPOSE TISSUE; ANIMALS; BRAIN CHEMISTRY; HIPPOCAMPUS; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN RESISTANCE; LIPID METABOLISM; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTOR, INSULIN; SYNAPSES; SYNAPTOSOMES;

EID: 84924598594     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13043     Document Type: Article

References (39)

1. 2+ permeability. J. Biol. Chem. 289, 18805-18817. pii: jbc.M113.537282. [Epub ahead of print]
2. Bjorklund N. L., Reese L. C., Sadagoparamanujam V. M., Ghirardi V., Woltjer R. L., and, Taglialatela G., (2012) Absence of amyloid beta oligomers at the postsynapse and regulated synaptic Zn2+ in cognitively intact aged individuals with Alzheimer's disease neuropathology. Mol. Neurodegener. 7, 23.
3. Boden G., and, Chen X., (1995) Effects of fat on glucose uptake and utilization in patients with non-insulin-dependent diabetes. J. Clin. Invest. 96, 1261-1268.
4. Boden G., Chen X., Ruiz J., White J. V., and, Rossetti L., (1994) Mechanisms of fatty acid-induced inhibition of glucose uptake. J. Clin. Invest. 93, 2438-2446.
5. Brassard P., Frisch F., Lavoie F., Cyr D., Bourbonnais A., Cunnane S. C., Patterson B. W., Drouin R., Baillargeon J. P., and, Carpentier A. C., (2008) Impaired plasma nonesterified fatty acid tolerance is an early defect in the natural history of type 2 diabetes. J. Clin. Endocrinol. Metab. 93, 837-844.
6. Britton K. A., and, Fox C. S., (2011) Ectopic fat depots and cardiovascular disease. Circulation 124, e837-e841.
7. Calvo-Ochoa E., and, Arias C., (2015) Cellular and metabolic alterations in the hippocampus caused by insulin signaling dysfunction and its association with cognitive impairment during aging and Alzheimer's disease. Animal models of study. Diabetes Metab. Res. Rev. 31, 1-13.
8. Chandalia M., Davila H., Pan W., Szuszkiewicz M., Tuvdendorj D., Livingston E. H., and, Abate N., (2012) Adipose tissue dysfunction in humans: a potential role for the transmembrane protein ENPP1. J. Clin. Endocrinol. Metab. 97, 4663-4672.
9. Costello D. A., (2012) Brain deletion of insulin receptor substrate 2 disrupts hippocampal synaptic plasticity and metaplasticity. PLoS ONE 7, e31124.
10. Elias M. F., Elias P. K., Sullivan L. M., Wolf P. A., and, D'Agostino R. B., (2003) Lower cognitive function in the presence of obesity and hypertension: the Framingham heart study. Int. J. Obes. Relat. Metab. Disord. 27, 260-268.
11. Emamian E. S., Karayiorgou M., and, Gogos J. A., (2004) Decreased phosphorylation of NMDA receptor type 1 at serine 897 in brains of patients with Schizophrenia. J. Neurosci. 24, 1561-1564.
12. Emmanuel Y., Cochlin L. E., Tyler D. J., de Jager C. A., Smith A. D., and, Clarke K., (2013) Human hippocampal energy metabolism is impaired during cognitive activity in a lipid infusion model of insulin resistance. Brain Behav. 3, 134-144.
13. Granholm A. C., Bimonte-Nelson H. A., Moore A. B., Nelson M. E., Freeman L. R., and, Sambamurti K., (2008) Effects of a saturated fat and high cholesterol diet on memory and hippocampal morphology in the middle-aged rat. J. Alzheimers Dis. 14, 133-145.
14. Hassing L. B., Hofer S. M., Nilsson S. E., Berg S., Pedersen N. L., McClearn G., and, Johansson B., (2004) Comorbid type 2 diabetes mellitus and hypertension exacerbates cognitive decline: evidence from a longitudinal study. Age Ageing 33, 355-361.
15. Hei M. Y., Tao H. K., Tang Q., Yu B., and, Zhao L. L., (2012) Decreased levels of pNR1 S897 protein in the cortex of neonatal Sprague Dawley rats with hypoxic-ischemic or NMDA-induced brain damage. Braz. J. Med. Biol. Res. 45, 962-967.
16. van der Heide L. P., Kamal A., Artola A., Gispen W. H., and, Ramakers G. M., (2005) Insulin modulates hippocampal activity-dependent synaptic plasticity in a N-methyl-d-aspartate receptor and phosphatidyl-inositol-3-kinase-dependent manner. J. Neurochem. 94, 1158-1166.
17. Homko C. J., Cheung P., and, Boden G., (2003) Effects of free fatty acids on glucose uptake and utilization in healthy women. Diabetes 52, 487-491.
18. Itani S. I., Ruderman N. B., Schmieder F., and, Boden G., (2002) Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes 51, 2005-2011.
19. Li B., Devidze N., Barengolts D., Prostak N., Sphicas E., Apicella A. J., Malinow R., and, Emamian E. S., (2009) NMDA receptor phosphorylation at a site affected in schizophrenia controls synaptic and behavioral plasticity. J. Neurosci. 29, 11965-11972.
20. Liao G. Y., and, Leonard J. P., (1999) Insulin modulation of cloned mouse NMDA receptor currents in Xenopus oocytes. J. Neurochem. 73, 1510-1519.
21. Liu L., Brown J. C., 3rd, Webster W. W., Morrisett R. A., and, Monaghan D. T., (1995) Insulin potentiates N-methyl-D-aspartate receptor activity in Xenopus oocytes and rat hippocampus. Neurosci Lett. 192, 5-8.
22. Lomonaco R., Ortiz-Lopez C., Orsak B., et al,. (2012) Effect of adipose tissue insulin resistance on metabolic parameters and liver histology in obese patients with nonalcoholic fatty liver disease. Hepatology 55, 1389-1397.
23. Mapstone M., Cheema A. K., Fiandaca M. S., et al,. (2014) Plasma phospholipids identify antecedent memory impairment in older adults. Nat. Med. 20, 415-418.
24. McNay E. C., Ong C. T., McCrimmon R. J., Cresswell J., Bogan J. S., and, Sherwin R. S., (2010) Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiol. Learn. Mem. 93, 546-553.
25. Molteni R., Barnard R. J., Ying Z., Roberts C. K., and, Gomez-Pinilla F., (2002) A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 112, 803-814.
26. Morris R. G., (2013) NMDA receptors and memory encoding. Neuropharmacology 74, 32-40.
27. Muller D., Nitsch R. M., Wurtman R. J., and, Hoyer S., (1998) Streptozotocin increases free fatty acids and decreases phospholipids in rat brain. J. Neural. Transm. 105, 1271-1281.
28. Nowotny B., Zahiragic L., Krog D., et al,. (2013) Mechanisms underlying the onset of oral lipid-induced skeletal muscle insulin resistance in humans. Diabetes 62, 2240-2248.
29. Pan W., Ciociola E., Saraf M., Tumurbaatar B., Tuvdendorj D., Prasad S., Chandalia M., and, Abate N., (2011) Metabolic consequences of ENPP1 overexpression in adipose tissue. Am. J. Physiol. Endocrinol. Metab. 301, E901-E911.
30. Prasad M. R., Lovell M. A., Yatin M., Dhillon H., and, Markesbery W. R., (1998) Regional membrane phospholipid alterations in Alzheimer's disease. Neurochem. Res. 23, 81-88.
31. Ravussin E., and, Smith S. R., (2002) Increased fat intake, impaired fat oxidation, and failure of fat cell proliferation result in ectopic fat storage, insulin resistance, and type 2 diabetes mellitus. Ann. N. Y. Acad. Sci. 967, 363-378.
32. Ruddock M. W., Stein A., Landaker E., Park J., Cooksey R. C., McClain D., and, Patti M. E., (2008) Saturated fatty acids inhibit hepatic insulin action by modulating insulin receptor expression and post-receptor signaling. J. Biochem. 144, 599-607.
33. Samuel V. T., and, Shulman G. I., (2012) Mechanisms for insulin resistance: common threads and missing links. Cell 148, 852-871.
34. Schubert M., Gautam D., Surjo D., et al,. (2004) Role for neuronal insulin resistance in neurodegenerative diseases. Proc. Natl Acad. Sci. USA 101, 3100-3105.
35. Soderberg M., Edlund C., Kristensson K., and, Dallner G., (1991) Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease. Lipids 26, 421-425.
36. Tsien J. Z., Huerta P. T., and, Tonegawa S., (1996) The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87, 1327-1338.
37. 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.
38. Yu C., Chen Y., Cline G. W., et al,. (2002) Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J. Biol. Chem. 277, 50230-50236.
39. Zhang X. J., Rodriguez N. A., Wang L., Tuvdendorj D., Wu Z., Tan A., Herndon D. N., and, Wolfe R. R., (2012) Measurement of precursor enrichment for calculating intramuscular triglyceride fractional synthetic rate. J. Lipid Res. 53, 119-125.