Chronic psychosocial stress accelerates impairment of long-term memory and late-phase long-term potentiation in an at-risk model of Alzheimer's disease

Hippocampus

Volumn 21, Issue 7, 2011, Pages 724-732

  Tran, Trinh T ^a   Srivareerat, Marisa ^a   Alkadhi, Karim A ^a  

^a UNIVERSITY OF HOUSTON   (United States)

Author keywords

Alzheimer's disease; Beta amyloid; CA1; Electrophysiology; Hippocampus; Late phase long term potentiation; Radial arm water maze; Stress

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; COGNITION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HIGH RISK POPULATION; IMMUNOBLOTTING; LEARNING; LONG TERM MEMORY; LONG TERM POTENTIATION; MAZE TEST; MEMORY DISORDER; MENTAL STRESS; NERVE CELL PLASTICITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CHRONIC DISEASE; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; LONG-TERM POTENTIATION; MALE; MEMORY, LONG-TERM; RATS; RATS, WISTAR; RISK FACTORS; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 79959559264     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20790     Document Type: Article

References (66)

1. Alamed J, Wilcock DM, Diamond DM, Gordon MN, Morgan D. 2006. Two-day radial-arm water maze learning and memory task; robust resolution of amyloid-related memory deficits in transgenic mice. Nat Protoc 1: 1671-1679.
2. Aleisa AM, Alzoubi KH, Alkadhi KA. 2006a. Chronic but not acute nicotine treatment reverses stress-induced impairment of LTP in anesthetized rats. Brain Res 1097: 78-84.
3. Aleisa AM, Alzoubi KH, Gerges NZ, Alkadhi KA. 2006b. Nicotine blocks stress-induced impairment of spatial memory and long-term potentiation of the hippocampal CA1 region. Int J Neuropsychopharmacol 9: 417-426.
4. Aleisa AM, Alzoubi KH, Gerges NZ, Alkadhi KA. 2006c. Chronic psychosocial stress-induced impairment of hippocampal LTP: Possible role of BDNF. Neurobiol Dis 22: 453-462.
5. Alkadhi KA, Alzoubi KH, Aleisa AM, Tanner FL, Nimer AS. 2005. Psychosocial stress-induced hypertension results from in vivo expression of long-term potentiation in sympathetic ganglia. Neurobiol Dis 20: 849-857.
6. Alzoubi KH, Aleisa AM, Alkadhi KA. 2007a. Adult-onset hypothyroidism facilitates and enhances LTD: Reversal by chronic nicotine treatment. Neurobiol Dis 26: 264-272.
7. Alzoubi KH, Aleisa AM, Alkadhi KA. 2007b. Nicotine prevents disruption of the late phase LTP-related molecular cascade in adult-onset hypothyroidism. Hippocampus 17: 654-664.
8. Alzoubi KH, Aleisa AM, Gerges NZ, Alkadhi KA. 2006. Nicotine reverses adult-onset hypothyroidism-induced impairment of learning and memory: Behavioral and electrophysiological studies. J Neurosci Res 84: 944-953.
9. Alzoubi KH, Abdul-Razzak KK, Khabour OF, Al-Tuweiq GM, Alzubi MA, Alkadhi KA. 2009. Adverse effect of combination of chronic psychosocial stress and high fat diet on hippocampus-dependent memory in rats. Behav Brain Res 204: 117-123.
10. Arvanitis DN, Ducatenzeiler A, Ou JN, Grodstein E, Andrews SD, Tendulkar SR, Ribeiro-da-Silva A, Szyf M, Cuello AC. 2007. High intracellular concentrations of amyloid-beta block nuclear translocation of phosphorylated CREB. J Neurochem 103: 216-228.
11. Assis-Nascimento P, Jarvis KM, Montague JR, Mudd LM. 2007. Beta-amyloid toxicity in embryonic rat astrocytes. Neurochem Res 32: 1476-1482.
12. Barco A, Alarcon JM, Kandel ER. 2002. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108: 689-703.
13. Barco A, Patterson S, Alarcon JM, Gromova P, Mata-Roig M, Morozov A, Kandel ER. 2005. Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP, its synaptic capture. Neuron 48: 123-137.
14. Bito H, Takemoto-Kimura S. 2003. Ca(2+)/CREB/CBP-dependent gene regulation: A shared mechanism critical in long-term synaptic plasticity and neuronal survival. Cell Calcium 34: 425-430.
15. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ. 1994. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79: 59-68.
16. Buhot MC, Wolff M, Benhassine N, Costet P, Hen R, Segu L. 2003. Spatial learning in the 5-HT1B receptor knockout mouse: Selective facilitation/impairment depending on the cognitive demand. Learn Mem 10: 466-477.
17. Carrotta R, Di Carlo M, Manno M, Montana G, Picone P, Romancino D, San Biagio PL. 2006. Toxicity of recombinant beta-amyloid prefibrillar oligomers on the morphogenesis of the sea urchin Paracentrotus lividus. FASEB J 20: 1916-1917.
18. Catania C, Sotiropoulos I, Silva R, Onofri C, Breen KC, Sousa N, Almeida OF. 2009. The amyloidogenic potential and behavioral correlates of stress. Mol Psychiatry 14: 95-105.
19. Connor B, Young D, Yan Q, Faull RL, Synek B, Dragunow M. 1997. Brain-derived neurotrophic factor is reduced in Alzheimer's disease. Brain Res Mol Brain Res 49: 71-81.
20. Devanand DP, Pradhaban G, Liu X, Khandji A, De Santi S, Segal S, Rusinek H, Pelton GH, Honig LS, Mayeux R, Stern Y, Tabert MH, de Leon MJ. 2007. Hippocampal and entorhinal atrophy in mild cognitive impairment: Prediction of Alzheimer disease. Neurology 68: 828-836.
21. Diamond DM, Park CR, Heman KL, Rose GM. 1999. Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9: 542-552.
22. Gerges NZ, Stringer JL, Alkadhi KA. 2001. Combination of hypothyroidism and stress abolishes early LTP in the CA1 but not dentate gyrus of hippocampus of adult rats. Brain Res 922: 250-260.
23. Gerges NZ, Alzoubi KH, Park CR, Diamond DM, Alkadhi KA. 2004. Adverse effect of the combination of hypothyroidism and chronic psychosocial stress on hippocampus-dependent memory in rats. Behav Brain Res 155: 77-84.
24. Goodman Y, Mattson MP. 1994. Secreted forms of beta-amyloid precursor protein protect hippocampal neurons against amyloid beta-peptide-induced oxidative injury. Exp Neurol 128: 1-12.
25. Hartmann A, Veldhuis JD, Deuschle M, Standhardt H, Heuser I. 1997. Twenty-four hour cortisol release profiles in patients with Alzheimer's and Parkinson's disease compared to normal controls: Ultradian secretory pulsatility and diurnal variation. Neurobiol Aging 18: 285-289.
26. Ingelsson M, Fukumoto H, Newell KL, Growdon JH, Hedley-Whyte ET, Frosch MP, Albert MS, Hyman BT, Irizarry MC. 2004. Early Abeta accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain. Neurology 62: 925-931.
27. Joels M. 2006. Corticosteroid effects in the brain: U-shape it. Trends Pharmacol Sci 27: 244-250.
28. Joels M, Karst H, Krugers HJ, Lucassen PJ. 2007. Chronic stress: Implications for neuronal morphology, function and neurogenesis. Front Neuroendocrinol 28: 72-96.
29. Kandel ER. 2001. The molecular biology of memory storage: A dialogue between genes and synapses. Science 294: 1030-1038.
30. Kang H, Welcher AA, Shelton D, Schuman EM. 1997. Neurotrophins and time: Different roles for TrkB signaling in hippocampal long-term potentiation. Neuron 19: 653-664.
31. Karnam HB, Zhou JL, Huang LT, Zhao Q, Shatskikh T, Holmes GL. 2009. Early life seizures cause long-standing impairment of the hippocampal map. Exp Neurol 217: 378-387.
32. Kim JJ, Yoon KS. 1998. Stress: Metaplastic effects in the hippocampus. Trends Neurosci 21: 505-509.
33. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL. 1998. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95: 6448-6453.
34. Lamprecht R. 1999. CREB: A message to remember. Cell Mol Life Sci 55: 554-563.
35. Landfield PW, Blalock EM, Chen KC, Porter NM. 2007. A new glucocorticoid hypothesis of brain aging: implications for Alzheimer's disease. Curr Alzheimer Res 4: 205-212.
36. Lipsky RH, Marini AM. 2007. Brain-derived neurotrophic factor in neuronal survival and behavior-related plasticity. Ann NY Acad Sci 1122: 130-143.
37. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, Sue L, Beach T, Kurth JH, Rydel RE, Rogers J. 1999. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 155: 853-862.
38. Ma QL, Harris-White ME, Ubeda OJ, Simmons M, Beech W, Lim GP, Teter B, Frautschy SA, Cole GM. 2007. Evidence of Abeta- and transgene-dependent defects in ERK-CREB signaling in Alzheimer's models. J Neurochem 103: 1594-1607.
39. McEwen BS. 2008. Central effects of stress hormones in health and disease: Understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol 583: 174-185.
40. McEwen BS, Sapolsky RM. 1995. Stress and cognitive function. Curr Opin Neurobiol 5: 205-216.
41. McLaughlin KJ, Gomez JL, Baran SE, Conrad CD. 2007. The effects of chronic stress on hippocampal morphology and function: An evaluation of chronic restraint paradigms. Brain Res 1161: 56-64.
42. Miller DB, O'Callaghan JP. 2002. Neuroendocrine aspects of the response to stress. Metabolism 51: 5-10.
43. Minichiello L, Calella AM, Medina DL, Bonhoeffer T, Klein R, Korte M. 2002. Mechanism of TrkB-mediated hippocampal long-term potentiation. Neuron 36: 121-137.
44. Pang PT, Lu B. 2004. Regulation of late-phase LTP, long-term memory in normal and aging hippocampus: role of secreted proteins tPA and BDNF. Ageing Res Rev 3: 407-430.
45. Papatheodoropoulos C, Kostopoulos G. 2000. Decreased ability of rat temporal hippocampal CA1 region to produce long-term potentiation. Neurosci Lett 279: 177-180.
46. Pavlides C, Watanabe Y, Magarinos AM, McEwen BS. 1995. Opposing roles of type I, type II adrenal steroid receptors in hippocampal long-term potentiation. Neuroscience 68: 387-394.
47. Paxinos G, Watson C. 1986. The Rat Brain in Stereotaxic Coordinates, 2nd ed. Sydney; New York: Academic Press.
48. Phillips HS, Hains JM, Armanini M, Laramee GR, Johnson SA, Winslow JW. 1991. BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease. Neuron 7: 695-702.
49. Rafii MS, Aisen PS. 2009. Recent developments in Alzheimer's disease therapeutics. BMC Med 7: 7.
50. Sandi C, Pinelo-Nava MT. 2007. Stress and memory: Behavioral effects and neurobiological mechanisms. Neural Plast 2007: 78970.
51. Sauro MD, Jorgensen RS, Pedlow CT. 2003. Stress, glucocorticoids, and memory: A meta-analytic review. Stress 6: 235-245.
52. Schindler BA. 1985. Stress, affective disorders, and immune function. Med Clin North Am 69: 585-597.
53. Schulman H. 1995. Protein phosphorylation in neuronal plasticity and gene expression. Curr Opin Neurobiol 5: 375-381.
54. Sotiropoulos I, Catania C, Riedemann T, Fry JP, Breen KC, Michaelidis TM, Almeida OF. 2008. Glucocorticoids trigger Alzheimer disease-like pathobiochemistry in rat neuronal cells expressing human tau. J Neurochem 107: 385-397.
55. Srivareerat M, Tran TT, Alzoubi KH, Alkadhi KA. 2009a. Chronic psychosocial stress exacerbates impairment of cognition and long-term potentiation in beta-amyloid rat model of Alzheimer's disease. Biol Psychiatry 65: 918-926.
56. Srivareerat M, Tran TT, Salim S, Aleisa AM, Alkadhi KA. 2009b. Chronic nicotine restores normal Abeta levels and prevents short-term memory and E-LTP impairment in Abeta rat model of Alzheimer's disease. Neurobiol Aging May 20 [Epub ahead of print].
57. Tsigos C, Chrousos GP. 2002. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res 53: 865-871.
58. Tran TT, Srivareerat M, Alkadhi KA. 2010. Chronic psychosocial stress triggers cognitive impairment in a novel at-risk model of Alzheimer's disease. Neurobiol Dis 37: 756-763.
59. Turner RS. 2006. Alzheimer's disease. Semin Neurol 26: 499-506.
60. Walker E, Mittal V, Tessner K. 2008. Stress and the hypothalamic pituitary adrenal axis in the developmental course of schizophrenia. Annu Rev Clin Psychol 4: 189-216.
61. Walton MR, Dragunow I. 2000. Is CREB a key to neuronal survival? Trends Neurosci 23: 48-53.
62. Whitworth JA, Mangos GJ, Kelly JJ. 2000. Cushing, cortisol, and cardiovascular disease. Hypertension 36: 912-916.
63. Wilson RS, Evans DA, Bienias JL, Mendes de Leon CF, Schneider JA, Bennett DA. 2003. Proneness to psychological distress is associated with risk of Alzheimer's disease. Neurology 61: 1479-1485.
64. Wilson RS, Schneider JA, Boyle PA, Arnold SE, Tang Y, Bennett DA. 2007. Chronic distress and incidence of mild cognitive impairment. Neurology 68: 2085-2092.
65. Yamin G. 2009. NMDA receptor-dependent signaling pathways that underlie amyloid beta-protein disruption of LTP in the hippocampus. J Neurosci Res 87: 1729-1736.
66. Yin JC, Del Vecchio M, Zhou H, Tully T. 1995. CREB as a memory modulator: Induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81: 107-115.