Hypothalamic-pituitary-adrenal dysfunction in Apoe(-/-) mice: Possible role in behavioral and metabolic alterations

Journal of Neuroscience

Volumn 20, Issue 5, 2000, Pages 2064-2071

  Raber, Jacob ^a,b   Akana, Susan F ^c   Bhatnagar, Seema ^c   Dallman, Mary F ^c   Wong, Derek ^a   Mucke, Lennart ^a,b  

^a GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^b Department of Neurology ^*  (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ACTH; Adrenal gland; Anxiety; apoE; Corticosterone; HPA axis; Metabolism; Open field activity; Pituitary

Indexed keywords

APOLIPOPROTEIN E; CORTICOSTERONE; CORTICOTROPIN;

ADRENAL GLAND; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; MALE; MAZE TEST; MOUSE; NONHUMAN; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL;

EID: 0034161608     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-05-02064.2000     Document Type: Article

References (61)

1. Aguilera G (1994) Regulation of pituitary ACTH secretion during chronic stress. Front Neuroendocrinol 15:321-350.
2. Ahima RS, Prabakaran D, Mantzoros C, Qu D, Lowell B, Maratos-Flier E, Flier JS (1996) Role of leptin in the neuruendocrine re-sponse to fasting. Nature 382:250-252.
3. Akana SF (1999) Assessment of integrated endocrine responses to cold challenge in mice. Endocr Soc Ahstr V139A:364.
4. Akana SF, Strack AM, Hanson ES, Dallman MF (1994) Regulation of activity in the hypothalamo-pituitary-adrenal axis is integral to a larger hypothalamic system that determines caloric flow. Endocrinology 135:1125-1134.
5. Akana SF, Hanson ES, Horsley C, Strack AM, Bhatnagar S, Bradbury MJ, Milligan ED, Dallman MF (1996) Clamped corticosterone (B) reveals the effect of endogenous B on both facilitated responsivity to acute restraint and metabolic responses to chronic stress. Stress 1:33-49.
6. Akwa Y, Schumacher M, Jung-Testas I, Baulicu EE (1993) Neurosteroids in rat sciatic nerves and Schwann cells. C R Acad Sci III 316:410-414.
7. Anderson R, Barnes JC, Bliss TVP, Cain DP, Cambon K, Davies HA, Errington ML, Fellows LA, Gray RA, Hoh T, Stewart M, Large CH, Higgins GA (1998) Behavioral, physiological and morphological analysis of a line of apolipoprotein E knockout mouse. Neuroscience 85:93-110.
8. ob mice. Endocrinology 139:4000-4003.
9. Bitran D, Shickh M, Dowd JA, Dugan MM, Renda P (1998) Corticosterone is permissive to the anxiolytic effect that results from the blockade of hippocampal mineralocorticoid receptors. Pharmacol Biochem Behav 60:879-887.
10. Britton DR, Koob GF, Rivier J, Vale W (1982) Intraventricular corticotropin-releasing factor enhances behavioral effects of novelty. Life Sci 31:363-367.
11. -/- mice: isoform-specific effects on neurodegeneration. J Neurosci 19:4867-4880.
12. Byrnes SE, Baur LA, Bermingham M, Brock K, Steinbeck K (1999) Leptin and total cholesterol are predictors of weight gain in prepubertal children. Int J Obes Relat Metab Disord 23:146-150.
13. Dallman MF, Akana SF, Cascio CS, Darlington DN, Jacobson L, Levin N (1987) Regulation of ACTH secretion: variations on a theme of B. Recent Prog Horm Res 43:113-173.
14. Dallman MF, Akana SF, Levin N, Walker C-D, Bradbury MJ, Sucmaru S, Scribner KS (1994) Corticosteroids and the control of function in the hypothalamo-pituitary-adrenal (HPA) axis. Ann NY Acad Sci 746:22-32.
15. Davis KL, Davis BM, Greenwald BS, Mohs RC, Mathθ AA, Johns CA, Horvath TB (1986) Cortisol and Alzheimer's disease. I: basal studies. Am J Psychiatry 143:300-305.
16. Diorio D, Viau V, Meaney MJ (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci 13:3839-3847.
17. -/-) mice but impaired clearance of axonal degeneration products following injury. Exp Neurol 151:314-325.
18. Fisher A, Brandeis R, Chapman S, Pittel Z, Michaelson DM (1998) M1 muscarinic agonist treatment reverses cognitive and cholinergic impairments of apolipoprotein E-deficient mice. J Neurochem 70:1991-1997.
19. Gold PW, Licinio J, Wong M-L, Chrousos GP (1995) Corticotropin releasing hormone in the pathophysiology of melancholic and atypical depression and in the mechanism of action of antidepressant drugs. Ann NY Acad Sci 771:716-729.
20. Gordon I, Grauer E, Genis I, Sehayek E, Michaelson DM (1995) Memory deficits and cholinergic impairments in apolipoprotein E-deficient mice. Neurosci Lett 199:1-4.
21. Gordon I, Ben-Eliyahu S, Rosenne E, Sehayek E, Michaelson DM (1996) Derangement in stress response of apolipoprotein E-deficient mice. Neurosci Lett 206:212-214.
22. Gray JA (1982) The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system. New York: Oxford UP.
23. Gray JA, McNaughton N (1983) Comparison between the behavioural effects of septal and hippocampal lesions: a review. Neurosci Biobehav Rev 7:119-188.
24. Hall PF, Almahbobi G (1997) Roles of microfilaments and intermediate filaments in adrenal steroidogenesis. Microsc Res Tech 36:463-479.
25. Hamilton RL, Wong JS, Guo LS, Krisans S, Havel RJ (1990) Apolipoprotein E localization in rat hepatocytes by immunogold labeling of cryothin sections. J Lipid Res 31:1589-1603.
26. Hatzinger M, Z'brun A, Hemmeter U, Seifritz E, Baumann F, Holsboer-Trachsler E, Heuser IJ (1995) Hypothalamic-pituitary-adrenal system function in patients with Alzheimer's disease. Neurobiol Aging 16:205-209.
27. Heiman ML, Ahima RS, Craft LS, Schoner B, Stephens TW, Flier JS (1997) Leptin inhibition of the hypothalamic-pituitary-adrenal axis in response to stress. Endocrinology 138:3859-3863.
28. Koob GF, Bloom FE (1985) Corticotropin-releasing factor and behavior. Fed Proc 44:259-263.
29. Korte SM, de Boer SF, de Kloet ER, Bonus B (1995) Anxiolytic-like effects of selective mineralocorticoid and glucocorticoid antagonists on fear-enhanced behavior in the elevated plus-maze. Psychoneuroendocrinology 20:385-394.
30. Kruse M, Bornstein SR, Uhlmann K, Paeth G, Scherbaum WA (1998) Leptin down-regulates the steroid producing system in the adrenal. Endocr Res 24:587-590.
31. Landfield PW, Baskin RK, Pitler TA (1981) Brain aging correlates: retardation by hormonal-pharmacological treatments. Science 214:581-584.
32. Liang KC, Lee EHY (1988) Intra-amygdala injections of corticotropin releasing factor facilitate inhibitory avoidance learning and reduce exploratory behavior in rats. Psychopharmacology 96:232-236.
33. Lupien SJ, McEwen BS (1997) The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Res Rev 24:1-27.
34. Lupien SJ, de Leon M, de Santi S, Convit A, Tarshish C, Nair NPV, Thakur M, McEwen BS, Hauger RL, Meaney MJ (1998) Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat Neurosci 1:69-73.
35. Magarin̄os AM, McEwen BS (1995) Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69:89-98.
36. Mahley RW (1988) Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240:622-630.
37. Masliah E, Mallory M, Ge N, Alford M, Veinbergs I, Roses AD (1995) Neurodegeneration in the central nervous system of apoE-deficient mice. Exp Neurol 136:107-122.
38. Masliah E, Samuel W, Veinbergs I, Mallory M, Mante M, Saitoh T (1997) Neurodegeneration and cognitive impairment in apoE-deficient mice is ameliorated by infusion of recombinant apoE. Brain Res 751:307-314.
39. McEwen BS, Sapolsky RM (1995) Stress and cognitve function. Curr Opin Neurobiol 5:205-216.
40. McEwen BS, De Kloet ER, Rostene W (1986) Adrenal steroid receptors and actions in the nervous system. Physiol Rev 66:1121-1188.
41. Mellon SH, Nussbaum S, Hochberg RB (1980) Biosynthesis of lipidal derivative of pregnenolone and hydroepiandrosterone by the adrenal. J Biol Chem 255:5566-5572.
42. Nicosia M, Prack MM, Williams DL (1992) Differential regulation of apolipoprotein-E messenger RNA in zona fasciculata cells of rat adrenal gland determined by in situ hybridization. Mol Endocrinol 6:288-298.
43. Oitzl MS, Fluttert M, de Kloet ER (1994) The effect of corticosterone on reactivity to spatial novelty is mediated by central mineralocorticosteroid receptors. Eur J Neurosci 6:1072-1079.
44. Oitzl MS, Mulder M, Lucassen PJ, Havekes LM, Grootendorst J, De Kloet ER (1997) Severe learning deficits in apolipoprotein E-knockout mice in a water maze task. Brain Res 752:189-196.
45. Piedrahita JA, Zhang SH, Hagaman JR, Oliver PM, Maeda N (1992) Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc Natl Acad Sci USA 89:4471-4475.
46. Plump AS, Smith JD, Hayek T, Aalto-Setala A, Walsh A, Verstuyft JG, Rubin EM, Breslow JL (1992) Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 71:343-353.
47. Porter NM, Landfield PW (1998) Stress hormones and brain aging: adding injury to insult? Nat Neurosci 1:3-4.
48. Prack MM, Nicosia M, Williams DL, Gwynne J (1991) Relationship between apolipoprotein E mRNA expression and tissue cholesterol content in rat adrenal gland. J Lipid Res 32:1611-1618.
49. Raber J (1998) Detrimental effects of chronic hypothalamic-pituitary-adrenal axis activation - from obesity to memory deficits. Mol Neurobiol 18:1-22.
50. Raber J, O'Shea RD, Bloom FE, Campbell IL (1997) Modulation of hypothalamic-pituitary-adrenal function by transgenic expression of interleukin-6 in the CNS of mice. J Neurosci 17:9473-9480.
51. Raber J, Wong D, Buttini M, Orth M, Bellosta S, Pitas RE, Mahley RW, Mucke L (1998) Isoform-specific effects of human apolipoprotein E on brain function revealed in ApoE knockout mice: increased susceptibility of females. Proc Natl Acad Sci USA 95:10914-10919.
52. Sapolsky RM (1996) Stress, glucocorticoids, and damage to the nervous system: the current state of confusion. Stress 1:1-19.
53. Sapolsky RM, Krey LC, McEwen BS (1985) Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J Neurosci 5:1222-1227.
54. Smythe JW, Murphy D, Timothy C, Costall B (1997) Hippocampal mineralocorticoid, but not glucocorticoid, receptors modulate anxiety-like behavior in rats. Pharmacol Biochem Behav 56:507-513.
55. Ströhle A, Poettig M, Barden N, Holsboer F, Montkowski A (1998) Age- and stimulus-dependent changes in anxiety-related behaviour of transgenic mice with GR dysfunction. NeuroReport 9:2099-2102.
56. Sutton RE, Koob GF, Moal ML, Rivier J, Vale W (1982) Corticotropin releasing factor produces behavioural activation in rats. Nature 297:331-333.
57. Watanabe Y, Gould E, Cameron HA, Daniels DC, McEwen BS (1992) Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus 2:431-435.
58. Weisgraber KH, Mahley RW (1996) Human apolipoprotein E: the Alzheimer's disease connection. FASEB J 10:1485-1494.
59. Woolley CS, Gould E, McEwen BS (1990) Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 531:225-231.
60. Zhang SH, Reddick RL, Piedrahita JA, Maeda N (1992) Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258:468-471.
61. Zhou Y, Elkins PD, Howell LA, Ryan DH, Harris RBS (1998) Apolipoprotein-E deficiency results in an altered stress responsiveness in addition to an impaired spatial memory in young mice. Brain Res 788:151-159.