Behavioral phenotype and BDNF differences related to apoE isoforms and sex in young transgenic mice

Experimental Neurology

Volumn 237, Issue 1, 2012, Pages 116-125

  Reverte, Ingrid ^a   Klein, Anders Bue ^b   Ratner, Cecilia ^b   Domingo, José L ^a   Colomina, Maria Teresa ^a  

^a UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^b Mental Health Services CPH   (Denmark)

Author keywords

Alzheimer's disease; Apolipoprotein E; BDNF; Gender differences; General activity; Memory; Spatial learning; TrkB

Indexed keywords

APOLIPOPROTEIN E2; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; BRAIN DERIVED NEUROTROPHIC FACTOR;

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; GENDER; GENOTYPE; LEARNING; MALE; MOUSE; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SEX DIFFERENCE; SPATIAL MEMORY;

AGE FACTORS; ANIMALS; APOLIPOPROTEIN E2; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; APOLIPOPROTEINS E; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; FEMALE; FRONTAL LOBE; GENOTYPE; HIPPOCAMPUS; MALE; MICE; MICE, TRANSGENIC; PHENOTYPE; PROTEIN ISOFORMS; SEX CHARACTERISTICS; SPATIAL BEHAVIOR;

EID: 84863824871     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.06.015     Document Type: Article

References (62)

1. Acevedo S.F., Piper B.J., Craytor M.J., Benice T.S., Raber J. Apolipoprotein E4 and sex affect neurobehavioral performance in primary school children. Pediatr. Res. 2010, 67:293-299.
2. Alexander D.M., Williams L.M., Gatt J.M., Dobson-Stone C., Kuan S.A., Todd E.G., Schofield P.R., Cooper N.J., Gordon E. The contribution of apolipoprotein E alleles on cognitive performance and dynamic neural activity over six decades. Biol. Psychol. 2007, 75:229-238.
3. Andersen, P.N., Egeland, J., Oie, M., in press. Learning and memory impairments in children and adolescents with attention-deficit/hyperactivity disorder. J. Learn. Disabil. http://dx.doi.org/10.1177/0022219412437040.
4. Andrews-Zwilling Y., Bien-Ly N., Xu Q., Li G., Bernardo A., Yoon S.Y., Zwilling D., Yan T.X., Chen L., Huang Y. Apolipoprotein E4 causes age- and Tau-dependent impairment of GABAergic interneurons, leading to learning and memory deficits in mice. J. Neurosci. 2010, 30:13707-13717.
5. Arendt T. Alzheimer's disease as a disorder of mechanisms underlying structural brain self-organization. Neuroscience 2001, 102:723-765.
6. Berteau-Pavy F., Park B., Raber J. Effects of sex and APOE epsilon4 on object recognition and spatial navigation in the elderly. Neuroscience 2007, 147:6-17.
7. Bour A., Grootendorst J., Vogel E., Kelche C., Dodart J.C., Bales K., Moreau P.H., Sullivan P.M., Mathis C. Middle-aged human apoE4 targeted-replacement mice show retention deficits on a wide range of spatial memory tasks. Behav. Brain Res. 2008, 193:174-182.
8. Bronfman F.C., Tesseur I., Hofker M.H., Havekens L.M., Van Leuven F. No evidence for cholinergic problems in apolipoprotein E knockout and apolipoprotein E4 transgenic mice. Neuroscience 2000, 97:411-418.
9. Brzyska M., Elbaum D. Dysregulation of calcium in Alzheimer's disease. Acta Neurobiol. Exp. (Wars) 2003, 63:171-183.
10. Champagne D., Dupuy J.B., Rochford J., Poirier J. Apolipoprotein E knockout mice display procedural deficits in the Morris water maze: analysis of learning strategies in three versions of the task. Neuroscience 2002, 114:641-654.
11. Colton C.A., Brown C.M., Vitek M.P. Sex steroids, APOE genotype and the innate immune system. Neurobiol. Aging 2005, 26:363-372.
12. Cunha C., Angelucci A., D'Antoni A., Dobrossy M.D., Dunnett S.B., Berardi N., Brambilla R. Brain-derived neurotrophic factor (BDNF) overexpression in the forebrain results in learning and memory impairments. Neurobiol. Dis. 2009, 33:358-368.
13. Dennis N.A., Browndyke J.N., Stokes J., Need A., Burke J.R., Welsh-Bohmer K.A., Cabeza R. Temporal lobe functional activity and connectivity in young adult APOE varepsilon4 carriers. Alzheimers Dement. 2010, 6:303-311.
14. D'Hooge R., De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res. Brain Res. Rev. 2001, 36:60-90.
15. Driscoll I., Espeland M.A., Wassertheil-Smoller S., Gaussoin S.A., Ding J., Granek I.A., Ockene J.K., Phillips L.S., Yaffe K., Resnick S.M., Women's Health Initiative Study of Cognitive Aging Weight change and cognitive function: findings from the Women's Health Initiative study of cognitive aging. Obesity (Silver Spring) 2011, 19:1595-1600.
16. Gomez-Pinilla F. Collaborative effects of diet and exercise on cognitive enhancement. Nutr. Health 2011, 20:165-169.
17. Grace A.A., Floresco S.B., Goto Y., Lodge D.J. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci. 2007, 30:220-227.
18. Grootendorst J., Bour A., Vogel E., Kelche C., Sullivan P.M., Dodart J.C., Bales K., Mathis C. Human apoE targeted replacement mouse lines: h-apoE4 and h-apoE3 mice differ on spatial memory performance and avoidance behavior. Behav. Brain Res. 2005, 159:1-14.
19. Hartman R.E., Wozniak D.F., Nardi A., Olney J.W., Sartorius L., Holtzman D.M. Behavioral phenotyping of GFAP-apoE3 and -apoE4 transgenic mice: apoE4 mice show profound working memory impairments in the absence of Alzheimer's-like neuropathology. Exp. Neurol. 2001, 170:326-344.
20. Hatters D.M., Peters-Libeu C.A., Weisgraber K.H. Apolipoprotein E structure: insights into function. Trends Biochem. Sci. 2006, 31:445-454.
21. Huang Y. Apolipoprotein E and Alzheimer disease. Neurology 2006, 66:S79-S85.
22. Kukolja J., Thiel C.M., Eggermann T., Zerres K., Fink G.R. Medial temporal lobe dysfunction during encoding and retrieval of episodic memory in non-demented APOE epsilon4 carriers. Neuroscience 2010, 168:487-497.
23. Legault M., Wise R.A. Novelty-evoked elevations of nucleus accumbens dopamine: dependence on impulse flow from the ventral subiculum and glutamatergic neurotransmission in the ventral tegmental area. Eur. J. Neurosci. 2001, 13:819-828.
24. Long J.R., Liu P.Y., Liu Y.J., Lu Y., Xiong D.H., Elze L., Recker R.R., Deng H.W. APOE and TGF-beta1 genes are associated with obesity phenotypes. J. Med. Genet. 2003, 40:918-924.
25. McLean C.P., Anderson E.R. Brave men and timid women? A review of the gender differences in fear and anxiety. Clin. Psychol. Rev. 2009, 29:496-505.
26. Minichiello L. TrkB signalling pathways in LTP and learning. Nat. Rev. Neurosci. 2009, 10:850-860.
27. Mondadori C.R., de Quervain D.J., Buchmann A., Mustovic H., Wollmer M.A., Schmidt C.F., Boesiger P., Hock C., Nitsch R.M., Papassotiropoulos A., Henke K. Better memory and neural efficiency in young apolipoprotein E epsilon4 carriers. Cereb. Cortex 2007, 17:1934-1947.
28. Nichol K., Deeny S.P., Seif J., Camaclang K., Cotman C.W. Exercise improves cognition and hippocampal plasticity in APOE epsilon4 mice. Alzheimers Dement. 2009, 5:287-294.
29. Noble E.E., Billington C.J., Kotz C.M., Wang C. The lighter side of BDNF. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300:R1053-R1069.
30. Papaleo F., Silverman J.L., Aney J., Tian Q., Barkan C.L., Chadman K.K., Crawley J.N. Working memory deficits, increased anxiety-like traits, and seizure susceptibility in BDNF overexpressing mice. Learn. Mem. 2011, 18:534-544.
31. Paratcha G., Ibáñez C.F. Lipid rafts and the control of neurotrophic factor signaling in the nervous system: variations on a theme. Curr. Opin. Neurobiol. 2002, 12:542-549.
32. Pendse A.A., Arbones-Mainar J.M., Johnson L.A., Altenburg M.K., Maeda N. Apolipoprotein E knock-out and knock-in mice: atherosclerosis, metabolic syndrome, and beyond. J. Lipid Res. 2009, 50:S178-S182. (Suppl.).
33. Pfankuch T., Rizk A., Olsen R., Poage C., Raber J. Role of circulating androgen levels in effects of apoE4 on cognitive function. Brain Res. 2005, 1053:88-96.
34. Profenno L.A., Faraone S.V. Diabetes and overweight associate with non-APOE4 genotype in an Alzheimer's disease population. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2008, 147B:822-829.
35. Raber J. Androgens, apoE, and Alzheimer's disease. Sci. Aging Knowledge Environ. 2004, re2.
36. Raber J. Role of apolipoprotein E in anxiety. Neural Plast. 2007, 2007:91236.
37. Raber J. AR, apoE, and cognitive function. Horm. Behav. 2008, 53:706-715.
38. Raber J., Wong D., Buttini M., Orth M., Bellosta S., Pitas R.E., Mahley R.W., Mucke L. Isoform-specific effects of human apolipoprotein E on brain function revealed in ApoE knockout mice: increased susceptibility of females. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:10914-10919.
39. Raber J., Wong D., Yu G.Q., Buttini M., Mahley R.W., Pitas R.E., Mucke L. Apolipoprotein E and cognitive performance. Nature 2000, 404:352-354.
40. Raber J., Huang Y., Ashford J.W. ApoE genotype accounts for the vast majority of AD risk and AD pathology. Neurobiol. Aging 2004, 25:641-650.
41. Raz N., Rodrigue K.M., Kennedy K.M., Land S. Genetic and vascular modifiers of age-sensitive cognitive skills: effects of COMT, BDNF, ApoE, and hypertension. Neuropsychology 2009, 23:105-116.
42. Reichardt L.F. Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006, 361:1545-1564.
43. Reiman E.M., Chen K., Alexander G.E., Caselli R.J., Bandy D., Osborne D., Saunders A.M., Hardy J. Functional brain abnormalities in young adults at genetic risk for late-onset Alzheimer's dementia. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:284-289.
44. Reitz C., Mayeux R. Endophenotypes in normal brain morphology and Alzheimer's disease: a review. Neuroscience 2009, 164:174-190.
45. Ribes D., Colomina M.T., Vicens P., Domingo J.L. Effects of oral aluminum exposure on behavior and neurogenesis in a transgenic mouse model of Alzheimer's disease. Exp. Neurol. 2008, 214:293-300.
46. Robertson J., Curley J., Kaye J., Quinn J., Pfankuch T., Raber J. apoE isoforms and measures of anxiety in probable AD patients and Apoe-/- mice. Neurobiol. Aging 2005, 26:637-643.
47. Sebastião A.M., Ribeiro J.A. Triggering neurotrophic factor actions through adenosine A2A receptor activation: implications for neuroprotection. Br. J. Pharmacol. 2009, 158:15-22.
48. Shen L., Tso P., Woods S.C., Clegg D.J., Barber K.L., Carey K., Liu M. Brain apolipoprotein E: an important regulator of food intake in rats. Diabetes 2008, 57:2092-2098.
49. Shepherd J.K., Grewal S.S., Fletcher A., Bill D.J., Dourish C.T. Behavioural and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacology (Berl) 1994, 116:56-64.
50. Siegel J.A., Benice T.S., Van Meer P., Park B.S., Raber J. Acetylcholine receptor and behavioral deficits in mice lacking apolipoprotein E. Neurobiol. Aging 2011, 32:75-84.
51. Siegel J.A., Haley G.E., Raber J. Apolipoprotein E isoform-dependent effects on anxiety and cognition in female TR mice. Neurobiol. Aging 2012, 33:345-358.
52. Sullivan P.M., Mezdour H., Aratani Y., Knouff C., Najib J., Reddick R.L., Quarfordt S.H., Maeda N. Targeted replacement of the mouse apolipoprotein E gene with the common human APOE3 allele enhances diet-induced hypercholesterolemia and atherosclerosis. J. Biol. Chem. 1997, 272:17972-17980.
53. Suzuki S., Kiyosue K., Hazama S., Ogura A., Kashihara M., Hara T., Koshimizu H., Kojima M. Brain-derived neurotrophic factor regulates cholesterol metabolism for synapse development. J. Neurosci. 2007, 27:6417-6427.
54. Tao M.H., Liu J.W., LaMonte M.J., Liu J., Wang L., He Y., Li X.Y., Wang L.N., Ye L. Different associations of apolipoprotein E polymorphism with metabolic syndrome by sex in an elderly Chinese population. Metabolism 2011, 60:1488-1496.
55. Thibault O., Gant J.C., Landfield P.W. Expansion of the calcium hypothesis of brain aging and Alzheimer's disease: minding the store. Aging Cell 2007, 6:307-317.
56. Toufexis D.J., Myers K.M., Davis M. The effect of gonadal hormones and gender on anxiety and emotional learning. Horm. Behav. 2006, 50:539-549.
57. Vaisi-Raygani A., Rahimi Z., Nomani H., Tavilani H., Pourmotabbed T. The presence of apolipoprotein epsilon4 and epsilon2 alleles augments the risk of coronary artery disease in type 2 diabetic patients. Clin. Biochem. 2007, 40:1150-1156.
58. Van Meer P., Acevedo S., Raber J. Impairments in spatial memory retention of GFAP-apoE4 female mice. Behav. Brain Res. 2007, 176:372-375.
59. Ṽikar V., K̃ks S., Vasar E., Rauvala H. Strain and gender differences in the behavior of mouse lines commonly used in transgenic studies. Physiol. Behav. 2001, 72:271-281.
60. Wetter S.R., Delis D.C., Houston W.S., Jacobson M.W., Lansing A., Cobell K., Salmon D.P., Bondi M.W. Deficits in inhibition and flexibility are associated with the APOE-E4 allele in nondemented older adults. J. Clin. Exp. Neuropsychol. 2005, 27:943-952.
61. Yun S.H., Park K.A., Sullivan P., Pasternak J.F., Ladu M.J., Trommer B.L. Blockade of nicotinic acetylcholine receptors suppresses hippocampal long-term potentiation in wild-type but not ApoE4 targeted replacement mice. J. Neurosci. Res. 2005, 82:771-777.
62. Zeljko H.M., Škarić-Jurić T., Narančić N.S., Tomas Ž., Barešić A., Salihović M.P., Starčević B., Janićijević B. E2 allele of the apolipoprotein E gene polymorphism is predictive for obesity status in Roma minority population of Croatia. Lipids Health Dis. 2011, 10:9.