Cortisol reduces hippocampal glucose metabolism in normal elderly, but not in Alzheimer's disease

Journal of Clinical Endocrinology and Metabolism

Volumn 82, Issue 10, 1997, Pages 3251-3259

  De Leon, M J ^a,e,f   McRae, T ^a   Rusinek, H ^a   Convit, A ^a,e   De Santi, S ^a   Tarshish, C ^a   Golomb, J ^a   Volkow, N ^b   Daisley, K ^a   Orentreich, N ^a,c   McEwen, B ^d  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

^c Orentreich Foundation for the Advancement of Science Inc   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

^e NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^f NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; HYDROCORTISONE;

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN METABOLISM; BRAIN SCINTISCANNING; CLINICAL ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; HIPPOCAMPUS; HORMONAL REGULATION; HUMAN; MALE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL;

AGED; AGING; ALZHEIMER DISEASE; BLOOD GLUCOSE; BRAIN; FEMALE; FLUORODEOXYGLUCOSE F18; GLUCOSE; HIPPOCAMPUS; HUMANS; HYDROCORTISONE; MAGNETIC RESONANCE IMAGING; MALE; RADIOPHARMACEUTICALS; REFERENCE VALUES; TOMOGRAPHY, EMISSION-COMPUTED;

ANIMALIA;

EID: 9844264859     PISSN: 0021972X     EISSN: None     Source Type: Journal    
DOI: 10.1210/jc.82.10.3251     Document Type: Article

References (94)

1. Simmons PS, Miles JM, Gerich JE, Haymond MW. 1984 Increased proteolysis. An effect of increases in plasma cortisol within the physiologic range. J Clin Invest. 73:412-420.
2. Munck A. 1971 Glucocorticoid inhibition of glucose uptake by peripheral tissues: old and new evidence, molecular mechanisms, and physiological significance. Perspect Biol Med. 14:265-289.
3. Shamoon H, Soman V, Sherwin RS. 1980 The influence of acute physiological increments of cortisol on fuel metabolism and insulin binding to monocytes in normal humans. J Clin Endocrinol Metab. 50:495-501.
4. Horner HC, Munck A, Lienhard GE. 1987 Dexamethasone causes translocation of glucose transporters from the plasma membrane to an intracellular site in human fibroblasts. J Biol Chem. 262:17696-17702.
5. Horner HC, Packan DR, Sapolsky RM. 1990 Glucocorticoids inhibit glucose transport in cultured hippocampal neurons and glia. Neuroendocrinology. 52:57-64.
6. Virgin CE, Ha TP-T, Packan DR, et al. 1991 Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: implications for glucocorticoid neurotoxicity. J Neurochem. 57:1422-1428.
7. 14C-glucose by rat bram under the influence of corticosterone. Endocrinol Exp. 12:119-129.
8. Freo U, Holloway HW, Kalogeras K, Rapoport SI, Soncrant TT. 1992 Adrenalectomy or metyrapone-pretreatment abolishes cerebral metabolic responses to the serotonin agonist 1-(2, 5-dimethoxy-4-iodophenyl)-2-aminopropane (DOI) in the hippocampus. Brain Res. 586:256-264.
9. Kadekaro M, Ito M, Gross PM. 1988 Local cerebral glucose utilization is increased in acutely adrenalectomized rats. Neuroendocrinology. 47:324-314.
10. Endo Y, Nishimura J, Kimura F. 1994 Adrenalectomy increases local cerebral blood flow in the rat hippocampus. Pflugers Arch. 426:183-188.
11. Sapolsky R, Krey LC, McEwen BS. 1986 The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Hndocr Rev. 7:284-301.
12. McEwen BS. 1988 Destructive hormonal influences on brain aging: the result of interacting modulators? In: Pepeu G, ed. New trends in aging research. Fidia, Abano Terme, Italy.
13. Uno H, Tarara R, Else JG, Suleman MA, Sapolsky RM. 1989 Hippocampal damage associated with prolonged and fatal stress in primates. J Neurosci. 9:1705-1711.
14. Dachir S, Kadar T, Robinzon B, Levy A. 1996 Cognitive deficits induced in young rats by long-term corticosterone administration. Behav Neural Biol. 60:103-109.
15. Landfield PW, Waymire JC, Lynch G. 1978 Hippocampal aging and adrenocorticoids: quantitative correlations. Science. 202:1098-3102.
16. Sapolsky RM. 1986 Glucocorticoid toxicity in the hippocampus. Neuroendocrinology. 43:440-444.
17. Sapolsky RM. 1986 Glucocorticoid toxicity in the hippocampus: reversal by supplementation with brain fuels. J Neurosci. 6:2240-2244.
18. O'Brien JT, Schweitzer I, Ames D, Mastwyk M, Colman P. 1994 The function of the hypothalamic-pituitary-adrenal axis in Alzheimer's disease. Br J Psychiatry. 165:650-657.
19. Meaney MJ, O'Donnell D, Rowe W, et al. 1995 Individual differences in hypothalamic-pituitary-adrenal activity in later life and hippocampal aging. Exp Gerontol. 30:229-251.
20. Orrel MW. 1996 Dementia, ageing, and the stress control system. Lancet. 345:666-667.
21. de Leon MJ, McRae T, Tsai JR, et al. 1988 Abnormal cortisol response in Alzheimer's disease linked to hippocampal atrophy. Lancet. 2(8607): 391-392.
22. Davis KL, Davis BM, Greenwald BS, et al. 1986 Cortisol and Alzheimer's disease. I. Basal studies. Am J Psychiatry. 143:300-305.
23. Swaab DF, Raadsheer FC, Endert E, Hofman MA, Kamphorst W, Ravid R. 1994 Increased cortisol levels in aging and Alzheimer's disease in postmortem cerebrospinal fluid. J Neuroendocrinol. 6:681-687.
24. Raskind MA, Peskind ER, Wilkinson CW. 1994 Hypothalamic-pituitary-adrenal axis regulation and human aging. In: de Kloet ER, Azmitia EC, Landfield PW, eds. Brain corticosteroid receptors: studies on the mechanism, function, and neurotoxicity of corticosteroid action. New York: New York Academy of Sciences; 327-335.
25. Braak H, Braak E, Bohl J. 1993 Staging of Alzheimer-related cortical destruction. Eur Neurol. 33:403-408.
26. Squire LR. 1992 Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev. 99:195-231.
27. Wolkowitz OM, Reus VI, Weingartner H, et al. 1990 Cognitive effects of corticosteroids. Am J Psychiatry. 147:1297-1303.
28. Newcomer JW, Craft S, Hershey T, Askins K, Bardgett ME. 1994 Glucocorticoid-induced impairment in declarative memory performance in adult humans. J Neurosci. 14:2047-2053.
29. Hall JL, Gonder-Frederick LA, Chewning WW, Silveira J, Gold PE. 1989 Glucose enhancement of performance on memory tests in young and aged humans. Neuropsychologia. 27:1129-1138.
30. Craft S, Dagogo-Jack SE, Wiethop BV, et al. 1943 Effects of hyperglycemia on memory and hormone levels in dementia of the Alzheimer type: a longitudinal study. Behav Neurosci. 107:426-440.
31. Manning CA, Ragozzino ME, Gold PE. 1993 Glucose enhancement of memory in patients with probable senile dementia of the Alzheimer's type. Neurobiol Aging. 14:523-528.
32. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. 1984 Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA work group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology. 34:939-944.
33. American Psychiatric Association. 1987 Diagnostic and statistical manual of mental disorders. Washington DC: American Psychiatric Association.
34. Rosen WG, Terry RD, Fuld PA, Katzman R, Peck A. 1980 Pathological verification of ischemia score in differentiation of dementias. Ann Neurol. 7:486-488.
35. Hamilton M. 1960 A rating scale for depression. J Neurol Neurosurg Psychiatry. 23:56-62.
36. Reisberg B, Ferris SH, de Leon MJ, Crook T. 1982 The Global Deterioration Scale for assessment of primary degenerative dementia. Am J Psychiatry. 139:1136-1139.
37. Folstein MF, Folstein SE, McHugh PR. 1975 Mini-mental state: a practical method for grading the cognitive state of patients for the clinician. J Psychiatry Res. 12:189-198.
38. Gilbert JG, Levee RF. 1971 Patterns of declining memory. J Gerontol. 26:70-75.
39. Gilbert JG, Levee RF, Catalano FL. 1968 A preliminary report on a new memory scale. Percept Mot Skills. 27:277-278.
40. Reivich M, Alavi A, Wolf A, et al. 1985 Glucose metabolic rate kinetic model parameter determination in humans: the lumped constants and rate constants for [18F]fluorodeoxyglucose and [11C]deoxyglucose. J Cereb Blood Flow Metab. 5:179-192.
41. Pelizzari CA, Chen GTY, Speibring DR, Weichselbaum RR, Chen CT. 1989 Accurate three-dimensional registration of CT, PET, and/or MR images of the brain. J Comput Assist Tomogr. 13:20-26.
42. Rusinek H, Tsui WH, Levy AV, Noz ME, de Leon MJ. 1993 Principal axes and surface fitting methods for three-dimensional image registration. J Nucl Med. 34:2019-2024.
43. Bendriem B, Dewey SL, Schlyer DJ, Wolf AP, Volkow ND. 1991 Quantitation of the human basal ganglia with positron emission tomography: a phantom study of the effect of contrast and axial positioning. IEEE Trans Nucl Sci. 10:216-222.
44. Smith GS, de Leon MJ, George AE, et al. 1992 Topography of cross-sectional and longitudinal glucose metabolic deficits in Alzheimer's disease: pathophysiologic implications. Arch Neurol. 49:1142-1150.
45. Kuhl DE, Metter EJ, Riege WH, Phelps ME. 1982 Effects of human aging on patterns of local cerebral glucose utilization determined by the [18F] fluorodeoxyglucose method. J Cereb Blood Flow Metab. 2:163-171.
46. de Leon MJ, George AE, Tomanelli J, et al. 1987 Positron emission tomography studies of normal aging: a replication of PET III and 18-FDG using PET VI and 11-C-2DG. Neurobiol Aging. 8:319-323.
47. Minoshima S, Frey KA, Foster NL, Kuhl DE. 1995 Preserved pontine glucose metabolism in Alzheimer's disease: a reference region for functional brain image (PET) analysis. J Comput Assist Tomogr. 19:541-547.
48. Roland PE, Levine B, Kawashima R, Akerman S. 1993 Three-dimensional analysis of clustered voxels in O-15-butanol brain activation images. Hum Brain Mapping. 1:3-19.
49. Baxter JD, Tyrrell JB. 1987 The adrenal cortex. In: Felig P, Baxter JD, Broadus AE, Frohman LA, eds. Endocrinology and metabolism. New York: McGraw-Hill; 511-650.
50. Pfaff DW, Silva MTA, Weiss JM. 1971 Telemetered recording of hormone effects on hippocampal neurons. Science. 172:394-395.
51. Vidal C, Jordan W, Zieglgansberger W. 1986 Corticosterone reduces the excitability of hippocampal pyramidal cells in vitro. Brain Res. 383:54-59.
52. Convit A, de Leon MJ, Golomb J, et al. 1993 Hippocampal atrophy in early Alzheimer's disease: anatomic specificity and validation. Psychiatr Q. 64:371-387.
53. Diamond DM, Bennett MC, Fleshner M, Rose GM. 1992 Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus. 2:421-230.
54. Eldridge JC, Fleenor DG, Kerr DS, Landfield PW. 1989 Impaired up-regulation of type II corticosteroid receptors in hippocampus of aged rats. Brain Res. 478:248-256.
55. Eldridge JC, Brodish A, Kute TE, Landfield PW. 1989 Apparent age-related resistance of type II hippocampal corticosteroid receptors to down-regulation during chronic escape training. J Neurosci. 9:3237-3242.
56. Landfield PW, Eldridge JC. 1989 Increased affinity of type II corticosteroid binding in aged rat hippocampus. Exp Neurol. 106:110-113.
57. Wetzel DM, Bohn MC, Kazee AM, Hamill RW. 1995 Glucocorticoid receptor mRNA in Alzheimer's diseased hippocampus. Brain Res. 679:72-81.
58. Maeda K, Tanimoto K, Terada T, Shintani T, Kakigi T. 1991 Elevated urinary free cortisol in patients with dementia. Neurobiol Aging. 12:161-163.
59. Martignoni E, Petraglia F, Costa A, Bono G, Genazzani AR, Nappi G. 1990 Dementia of the Alzheimer type and hypothalamus-pituitary-adrenocortical axis: changes in cerebrospinal fluid corticotropin releasing factor and plasma cortisol levels. Acta Neurol Scand. 81:452-456.
60. Nasman B, Olsson T, Viitanen M, Carlstrom K. 1995 A subtle disturbance in the feedback regulation of the hypothalamic-pituitary-adrenal axis in the early phase of Alzheimer's disease. Psychoneuroendocrinology. 20:211-220.
61. Simpson IA, Chundu KR, Davies-Hill T, Honer WG, Davies P. 1994 Decreased concentrations of GLUT1 and GLUT3 glucose transporters in the brains of patients with Alzheimer's disease. Ann Neurol. 35:546-551.
62. Harr SD, Simonian NA, Hyman BT. 1995 Functional alterations in Alzheimer's disease: decreased glucose transporter 3 immunoreactivity in the perforant pathway terminal zone. J Neuropathol Exp Neurol. 54:38-41.
63. Jagust WJ, Seab JP, Huesman RH, et al. 1991 Diminished glucose transport in Alzheimer's disease: dynamic PET studies. J Cereb Blood Flow Metab. 11:323-330.
64. Piert M, Koeppe RA, Giordani B, Berent S, Kuhl DE. 1996 Diminished glucose transport and phosphorylation in Alzheimer's disease determined by dynamic FDG-PET. J Nucl Med. 37:202-208.
65. Taha C, Mitsumoto Y, Liu Z, Skolnik EY, Klip A. 1995 The insulin-dependent biosynthesis of GLUT1 and GLUT3 glucose transporters in L6 muscle cells is mediated by distinct pathways. J Biol Chem. 270:24678-24681.
66. Giorgino F, Almahfouz A, Goodyear LJ, Smith RJ. 1993 Glucocorticoid regulation of insulin receptor and substrate IRS-1 tyrosine phosphorylation in rat skeletal muscle in vivo. J Clin Invest. 91:2020-2030.
67. Saad MJA, Folli F, Kahn CR. 1995 Insulin and dexamethasone regulate insulin receptors, insulin receptor substrate-1, and phosphatidylinositol 3-kinase in fao hepatoma cells. Endocrinology. 136:1579-1588.
68. Weinstein SP, Paquin T, Pritsker A, Haber RS. 1995 Glucocorticoid-induced insulin resistance: dexamethasone inhibits the activation of glucose transport in rat skeletal muscle by both insulin- and non-insulin-related stimuli. Diabetes. 44:441-445.
69. Seab JP, Jagust WS, Wong SFS, Roos MS, Reed BR, Budinger TF. 1988 Quantitative NMR measurements of hippocampal atrophy in Alzheimer's disease. Magn Reson Med. 8:200-208.
70. Kesslak JP, Nalcioglu O, Cotman CW. 1991 Quantification of magnetic resonance scans for hippocampal and parahippocampal atrophy in Alzheimer's disease. Neurology. 41:51-54.
71. Jack CR, Petersen RC, O'Brien PC, Tangalos EG. 1992 MR-based hippocampal volumetry in the diagnosis of Alzheimer's disease. Neurology. 42:183-188.
72. Jernigan TL, Salmon DP, Butters N, Hesselink JR. 1991 Cerebral structure on MRI. II. Specific changes in Alzheimer's and Huntington's diseases. Biol Psychiatry. 29:68-81.
73. Deweer B, Lehericy S, Pillon B, et al. 1995 Memory disorders in probable Alzheimer's disease: the role of hippocampal atrophy as shown with MRI. J Neurol Neurosurg Psychiatry. 58:590-597.
74. Ikeda M, Tanabe H, Nakagawa Y, et al. 1994 MRI-based quantitative assessment of the hippocampal region in very mild to moderate Alzheimer's disease. Neuroradiology. 36:7-10.
75. Laakso MP, Soininen H, Partanen K, et al. 1995 Volumes of hippocampus, amygdala and frontal lobes in the MRI-based diagnosis of early Alzheimer's disease: correlation with memory functions. J Neural Transm. 9:73-86.
76. Lehericy S, Baulac M, Chiras J, et al. 1994 Amygdalohippocampal MR volume measurements in the early stages of Alzheimer disease. Am J Neuroradiol. 15:929-937.
77. Convit A, de Leon MJ, Tarshish C, et al. 1997 Specific hippocampal volume reductions in individuals at risk for Alzheimer's disease. Neurobiol Aging. 18:1-9.
78. de Leon MJ, George AE, Stylopoulos LA, Smith G, Miller DC. 1989 Early marker for Alzheimer's disease: the atrophic hippocampus. Lancet. 2(8664):672-673.
79. de Leon MJ, Golomb J, George AE, et al. 1993 The radiologic prediction of Alzheimer's disease: the atrophic hippocampal formation. Am J Neuroradiol. 14:897-906.
80. Convit A, de Leon MJ, Tarshish C, et al. 1995 Hippocampal volume losses in minimally impaired elderly. Lancet. 345(8944):266.
81. de Leon MJ, George AE, Golomb J, et al. 1997 Frequency of hippocampus atrophy in normal elderly and Alzheimer's disease patients. Neurobiol Aging. 18:1-11.
82. Jagust WJ, Friedland RP, Budinger TF, Koss E, Ober B. 1988 Longitudinal studies of regional cerebral metabolism in Alzheimer's disease. Neurology. 38:909-912.
83. Swanwick GRJ, Coen RF, Walsh JB, Coakley D, Lawlor BA. 1996 The predictive value of hypothalamic-pituitary-adrenal axis dysfunction in Alzheimer's disease. Soc Biol Psychiatry. 39:976-978.
84. Lupien S, Lecours AR, Lussier I, Schwartz G, Nair NPV, Meaney MJ. 1994 Basal cortisol levels and cognitive deficits in human aging. J Neurosci. 14:2893-2903.
85. West MJ, Coleman PD, Flood DG, Troncoso JC. 1994 Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet. 344:769-772.
86. Bobinski M, Wegiel J, Wisniewski HM, et al. 1995 Atrophy of hippocampal formation subdivisions correlates with stage and duration of Alzheimer disease. Dementia. 6:205-210.
87. Bobinski MJ, Wegiel J, Wisniewski HM, et al. 1996 Neurofibrillary pathology-correlation with hippocampal formation atrophy in Alzheimer disease. Neurobiol Aging. 17:909-919.
88. Gomez-Isla T, Price JL, McKeel Jr DW, Morris JC, Growdon JH, Hyman BT. 1996 Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J Neurosci. 16:4491-4500.
89. McEwen BS, Angulo J, Cameron H, et al. 1992 Paradoxical effects of adrenal steroids on the brain: protection versus degeneration. Biol Psychiatry. 31:177-199.
90. Wolkowitz OM, Coppola R, Breier A, et al. 1993 Quantitative electroencephalographic correlates of steroid administration in man. Neuropsychobiology. 27:224-230.
91. Starkman MN, Gebarski SS, Berent S, Schteingart DE. 1992 Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biol Psychiatry. 32:756-765.
92. Axelson DA, Doraiswamy PM, McDonald WM, et al. 1993 Hypercortisolemia and hippocampal changes in depression. Psychiatry Res. 47:163-173.
93. Oberfield SE, Cowan L, Levine LS, et al. 1996 Altered cortisol response and the hippocampal atrophy in pediatric HIV disease. J AIDS. 7:57-62.
94. Keenan PA, Jacobson MW, Soleymani RM, Mayes MD, Stress ME, Yaldoo DT. 1996 The effect on memory of chronic prednisone treatment in patients with systemic disease. Neurology. 47:1396-1402.