Effect of high-fat diet on metabolic indices, cognition, and neuronal physiology in aging F344 rats

Neurobiology of Aging

Volumn 34, Issue 8, 2013, Pages 1977-1987

  Pancani, Tristano ^a   Anderson, Katie L ^a   Brewer, Lawrence D ^a   Kadish, Inga ^b   DeMoll, Chris ^a   Landfield, Philip W ^a   Blalock, Eric M ^a   Porter, Nada M ^a   Thibault, Olivier ^a  

^a UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Adiponectin; Aging; AHP; Calcium; Hippocampus; Learning; Metabolism

Indexed keywords

ADIPONECTIN; FATTY ACID; HEMOGLOBIN A1C; INSULIN;

AFTERHYPERPOLARIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN ELECTROPHYSIOLOGY; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; FATTY ACID BLOOD LEVEL; FOOD INTAKE; GLUCOSE METABOLISM; GLUCOSE TOLERANCE TEST; HEMOGLOBIN BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LIPID DIET; MALE; MAZE TEST; MORRIS WATER MAZE TEST; NONHUMAN; ORGAN WEIGHT; PRIORITY JOURNAL; RAT; SPATIAL LEARNING; SPATIAL MEMORY; WESTERN BLOTTING;

ADIPONECTIN; AGING; ANIMALS; CALCIUM; COGNITION; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; DISEASE PROGRESSION; HIPPOCAMPUS; MALE; MEMORY DISORDERS; OBESITY; RATS; RATS, INBRED F344; RISK FACTORS;

EID: 84877634220     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.02.019     Document Type: Article

References (67)

1. Asterholm I.W., Scherer P.E. Enhanced metabolic flexibility associated with elevated adiponectin levels. Am. J. Pathol. 2010, 176:1364-1376.
2. Barzilai N., Rossetti L. Relationship between changes in body composition and insulin responsiveness in models of the aging rat. Am. J. Physiol. 1995, 269:E591-E597.
3. Belanger A., Lavoie N., Trudeau F., Massicotte G., Gagnon S. Preserved LTP and water maze learning in hyperglycaemic-hyperinsulinemic ZDF rats. Physiol. Behav. 2004, 83:483-494.
4. Biessels G.J., Deary I.J., Ryan C.M. Cognition and diabetes: a lifespan perspective. Lancet Neurol. 2008, 7:184-190.
5. Blalock E.M., Phelps J.T., Pancani T., Searcy J.L., Anderson K.L., Gant J.C., Popovic J., Avdiushko M.G., Cohen D.A., Chen K.C., Porter N.M., Thibault O. Effects of long-term pioglitazone treatment on peripheral and central markers of aging. PLoS ONE 2010, 5:e10405.
6. Bracho-Romero E., Reaven G.M. Effect of age and weight on plasma glucose and insulin responses in the rat. J. Am. Geriatr. Soc. 1977, 25:299-302.
7. Buettner R., Scholmerich J., Bollheimer L.C. High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity (Silver Spring) 2007, 15:798-808.
8. Curtis R., Geesaman B.J., DiStefano P.S. Ageing and metabolism: drug discovery opportunities. Nat. Rev. Drug Discov. 2005, 4:569-580.
9. Disterhoft J.F., Oh M.M. Alterations in intrinsic neuronal excitability during normal aging. Aging Cell 2007, 6:327-336.
10. Dou J.T., Chen M., Dufour F., Alkon D.L., Zhao W.Q. Insulin receptor signaling in long-term memory consolidation following spatial learning. Learn. Mem. 2005, 12:646-655.
11. Duelli R., Maurer M.H., Staudt R., Heiland S., Duembgen L., Kuschinsky W. Increased cerebral glucose utilization and decreased glucose transporter Glut1 during chronic hyperglycemia in rat brain. Brain Res. 2000, 858:338-347.
12. Farr S.A., Yamada K.A., Butterfield D.A., Abdul H.M., Xu L., Miller N.E., Banks W.A., Morley J.E. Obesity and hypertriglyceridemia produce cognitive impairment. Endocrinology 2008, 149:2628-2636.
13. Frick K.M., Baxter M.G., Markowska A.L., Olton D.S., Price D.L. Age-related spatial reference and working memory deficits assessed in the water maze. Neurobiol. Aging 1995, 16:149-160.
14. Frisardi V., Solfrizzi V., Seripa D., Capurso C., Santamato A., Sancarlo D., Vendemiale G., Pilotto A., Panza F. Metabolic-cognitive syndrome: a cross-talk between metabolic syndrome and Alzheimer's disease. Ageing Res. Rev. 2010, 9:399-417.
15. Fruebis J., Tsao T.S., Javorschi S., Ebbets-Reed D., Erickson M.R., Yen F.T., Bihain B.E., Lodish H.F. Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:2005-2010.
16. Furuhashi M., Tuncman G., Gorgun C.Z., Makowski L., Atsumi G., Vaillancourt E., Kono K., Babaev V.R., Fazio S., Linton M.F., Sulsky R., Robl J.A., Parker R.A., Hotamisligil G.S. Treatment of diabetes and atherosclerosis by inhibiting fatty-acid-binding protein aP2. Nature 2007, 447:959-965.
17. Gallagher M., Burwell R., Burchinal M. Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris Water Maze. Behav. Neurosci. 1993, 107:618-626.
18. Gant J.C., Sama M.M., Landfield P.W., Thibault O. Early and simultaneous emergence of multiple hippocampal biomarkers of aging is mediated by Ca2+-induced Ca2+ release. J. Neurosci. 2006, 26:3482-3490.
19. Garekani E.T., Mohebbi H., Kraemer R.R., Fathi R. Exercise training intensity/volume affects plasma and tissue adiponectin concentrations in the male rat. Peptides 2011, 32:1008-1012.
20. Gasparini L., Netzer W.J., Greengard P., Xu H. Does insulin dysfunction play a role in Alzheimer's disease?. Trends Pharmacol. Sci. 2002, 23:288-293.
21. Greenwood C.E., Winocur G. Learning and memory impairment in rats fed a high saturated fat diet. Behav. Neural Biol. 1990, 53:74-87.
22. Gustafson D.R. Adiposity hormones and dementia. J. Neurol. Sci. 2010, 299:30-34.
23. Jurdak N., Lichtenstein A.H., Kanarek R.B. Diet-induced obesity and spatial cognition in young male rats. Nutr. Neurosci. 2008, 11:48-54.
24. Kalant N., Stewart J., Kaplan R. Effect of diet restriction on glucose metabolism and insulin responsiveness in aging rats. Mech. Ageing Dev. 1988, 46:89-104.
25. Kamal A., Biessels G.J., Duis S.E., Gispen W.H. Learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: interaction of diabetes and ageing. Diabetologia 2000, 43:500-506.
26. Kamal A., Ramakers G.M., Gispen W.H., Biessels G.J. Effect of chronic intracerebroventricular insulin administration in rats on the peripheral glucose metabolism and synaptic plasticity of CA1 hippocampal neurons. Brain Res. 2012, 1435:99-104.
27. Keenan K.P., Soper K.A., Hertzog P.R., Gumprecht L.A., Smith P.F., Mattson B.A., Ballam G.C., Clark R.L. Diet, overfeeding, and moderate dietary restriction in control Sprague-Dawley rats: II. Effects on age-related proliferative and degenerative lesions. Toxicol. Pathol. 1995, 23:287-302.
28. Kerr D.S., Campbell L.W., Hao S.Y., Landfield P.W. Corticosteroid modulation of hippocampal potentials: increased effect with aging. Science 1989, 245:1505-1509.
29. Kim B., Feldman E.L. Insulin resistance in the nervous system. Trends Endocrinol. Metab. 2012, 23:133-141.
30. Kloting N., Fasshauer M., Dietrich A., Kovacs P., Schon M.R., Kern M., Stumvoll M., Bluher M. Insulin-sensitive obesity. Am. J. Physiol. Endocrinol. Metab. 2010, 299:E506-E515.
31. Launer L.J. Diabetes and brain aging: epidemiologic evidence. Curr. Diab. Rep. 2005, 5:59-63.
32. Levin B.E., Triscari J., Sullivan A.C. Relationship between sympathetic activity and diet-induced obesity in two rat strains. Am. J. Physiol. 1983, 245:R364-R371.
33. Levy J.R., Davenport B., Clore J.N., Stevens W. Lipid metabolism and resistin gene expression in insulin-resistant Fischer 344 rats. Am. J. Physiol. Endocrinol. Metab. 2002, 282:E626-E633.
34. Li Y.M., Steffes M., Donnelly T., Liu C., Fuh H., Basgen J., Bucala R., Vlassara H. Prevention of cardiovascular and renal pathology of aging by the advanced glycation inhibitor aminoguanidine. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:3902-3907.
35. Li X.L., Aou S., Oomura Y., Hori N., Fukunaga K., Hori T. Impairment of long-term potentiation and spatial memory in leptin receptor-deficient rodents. Neuroscience 2002, 113:607-615.
36. Luchsinger J.A., Cheng D., Tang M.X., Schupf N., Mayeux R. Central obesity in the elderly is related to late-onset alzheimer disease. Alzheimer Dis. Assoc. Disord. 2012, 26:101-105.
37. Malloy V.L., Krajcik R.A., Bailey S.J., Hristopoulos G., Plummer J.D., Orentreich N. Methionine restriction decreases visceral fat mass and preserves insulin action in aging male Fischer 344 rats independent of energy restriction. Aging Cell 2006, 5:305-314.
38. McNay E.C., Recknagel A.K. Brain insulin signaling: a key component of cognitive processes and a potential basis for cognitive impairment in type 2 diabetes. Neurobiol. Learn. Mem. 2011, 96:432-442.
39. McNay E.C. The impact of recurrent hypoglycemia on cognitive function in aging. Neurobiol. Aging 2005, 26(Suppl 1):76-79.
40. Mielke J.G., Nicolitch K., Avellaneda V., Earlam K., Ahuja T., Mealing G., Messier C. Longitudinal study of the effects of a high-fat diet on glucose regulation, hippocampal function, and cerebral insulin sensitivity in C57BL/6 mice. Behav. Brain. Res. 2006, 175:374-382.
41. Mooradian A.D., Albert S.G. The age-related changes in lipogenic enzymes: the role of dietary factors and thyroid hormone responsiveness. Mech. Ageing Dev. 1999, 108:139-149.
42. Mooradian A.D., Wong N.C., Shah G.N. Apolipoprotein A1 expression in young and aged rats is modulated by dietary carbohydrates. Metabolism 1997, 46:1132-1136.
43. Morley J.E. The metabolic syndrome and aging. J. Gerontol. A Biol. Sci. Med. Sci. 2004, 59:139-142.
44. Moyer J.R., Thompson L.T., Disterhoft J.F. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J. Neurosci. 1996, 16:5536-5546.
45. Narimiya M., Azhar S., Dolkas C.B., Mondon C.E., Sims C., Wright D.W., Reaven G.M. Insulin resistance in older rats. Am J Physiol. 1984, 246:E397-E404.
46. Pistell P.J., Morrison C.D., Gupta S., Knight A.G., Keller J.N., Ingram D.K., Bruce-Keller A.J. Cognitive impairment following high fat diet consumption is associated with brain inflammation. J. Neuroimmunol. 2010, 219:25-32.
47. Popovic M., Biessels G.J., Isaacson R.L., Gispen W.H. Learning and memory in streptozotocin-induced diabetic rats in a novel spatial/object discrimination task. Behav. Brain Res. 2001, 122:201-207.
48. Pratchayasakul W., Kerdphoo S., Petsophonsakul P., Pongchaidecha A., Chattipakorn N., Chattipakorn S.C. Effects of high-fat diet on insulin receptor function in rat hippocampus and the level of neuronal corticosterone. Life Sci. 2011, 88:619-627.
49. Qi Y., Takahashi N., Hileman S.M., Patel H.R., Berg A.H., Pajvani U.B., Scherer P.E., Ahima R.S. Adiponectin acts in the brain to decrease body weight. Nat. Med. 2004, 10:524-529.
50. Reaven E., Wright D., Mondon C.E., Solomon R., Ho H., Reaven G.M. Effect of age and diet on insulin secretion and insulin action in the rat. Diabetes 1983, 32:175-180.
51. Ross A.P., Bruggeman E.C., Kasumu A.W., Mielke J.G., Parent M.B. Non-alcoholic fatty liver disease impairs hippocampal-dependent memory in male rats. Physiol. Behav. 2012, 106:133-141.
52. Rowe W.B., Blalock E.M., Chen K.C., Kadish I., Wang D., Barrett J.E., Thibault O., Porter N.M., Rose G.M., Landfield P.W. Hippocampal expression analyses reveal selective association of immediate-early, neuroenergetic, and myelinogenic pathways with cognitive impairment in aged rats. J. Neurosci. 2007, 27:3098-3110.
53. Schioth H.B., Craft S., Brooks S.J., Frey W.H., Benedict C. Brain insulin signaling and Alzheimer's disease: current evidence and future directions. Mol Neurobiol. 2012, 46:4-10.
54. Song C., Detert J.A., Sehgal M., Moyer J.R. Trace fear conditioning enhances synaptic and intrinsic plasticity in rat hippocampus. J. Neurophysiol. 2012, 107:3397-3408.
55. Steen E., Terry B.M., Rivera E.J., Cannon J.L., Neely T.R., Tavares R., Xu X.J., Wands J.R., de la Monte S.M. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease-is this type 3 diabetes?. J. Alzheimers Dis. 2005, 7:63-80.
56. Stranahan A.M., Mattson M.P. Metabolic reserve as a determinant of cognitive aging. J. Alzheimers Dis 2012, 30 (Suppl 2):5-13.
57. Stranahan A.M., Norman E.D., Lee K., Cutler R.G., Telljohann R.S., Egan J.M., Mattson M.P. Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 2008, 18:1085-1088.
58. Talbot K., Wang H.Y., Kazi H., Han L.Y., Bakshi K.P., Stucky A., Fuino R.L., Kawaguchi K.R., Samoyedny A.J., Wilson R.S., Arvanitakis Z., Schneider J.A., Wolf B.A., Bennett D.A., Trojanowski J.Q., Arnold S.E. Demonstrated brain insulin resistance in Alzheimer's disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J. Clin. Invest. 2012, 122:1316-1338.
59. Teixeira A.L., Diniz B.S., Campos A.C., Miranda A.S., Rocha N.P., Talib L.L., Gattaz W.F., Forlenza O.V. Decreased levels of circulating adiponectin in mild cognitive impairment and Alzheimer's disease. Neuromol. Med 2013, 15:115-121.
60. Thibault O., Landfield P.W. Increase in single L-type calcium channels in hippocampal neurons during aging. Science 1996, 272:1017-1020.
61. Une K., Takei Y.A., Tomita N., Asamura T., Ohrui T., Furukawa K., Arai H. Adiponectin in plasma and cerebrospinal fluid in MCI and Alzheimer's disease. Eur. J. Neurol. 2011, 18:1006-1009.
62. Whitmer R.A., Gustafson D.R., Barrett-Connor E., Haan M.N., Gunderson E.P., Yaffe K. Central obesity and increased risk of dementia more than three decades later. Neurology 2008, 71:1057-1064.
63. Xu H., Barnes G.T., Yang Q., Tan G., Yang D., Chou C.J., Sole J., Nichols A., Ross J.S., Tartaglia L.A., Chen H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin. Investig. 2003, 112:1821-1830.
64. Zhang W., Liu C.Q., Wang P.W., Sun S.Y., Su W.J., Zhang H.J., Li X.J., Yang S.Y. Puerarin improves insulin resistance and modulates adipokine expression in rats fed a high-fat diet. Eur. J. Pharmacol. 2010, 649:398-402.
65. Zhang D., Guo M., Zhang W., Lu X.Y. Adiponectin stimulates proliferation of adult hippocampal neural stem/progenitor cells through activation of p38 mitogen-activated protein kinase (p38MAPK)/glycogen synthase kinase 3beta (GSK-3beta)/beta-catenin signaling cascade. J. Biol. Chem. 2011, 286:44913-44920.
66. Zhao W.Q., Chen H., Quon M.J., Alkon D.L. Insulin and the insulin receptor in experimental models of learning and memory. Eur. J. Pharmacol. 2004, 490:71-81.
67. Zhu M., Miura J., Lu L.X., Bernier M., DeCabo R., Lane M.A., Roth G.S., Ingram D.K. Circulating adiponectin levels increase in rats on caloric restriction: the potential for insulin sensitization. Exp. Gerontol. 2004, 39:1049-1059.