Cognitive decline is associated with reduced reelin expression in the entorhinal cortex of aged rats

Cerebral Cortex

Volumn 21, Issue 2, 2011, Pages 392-400

  Stranahan, Alexis M ^a   Haberman, Rebecca P ^a   Gallagher, Michela ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

aging; Alzheimer's disease; lateral entorhinal cortex; learning; mild cognitive impairment

Indexed keywords

MESSENGER RNA; MOLECULAR MARKER; REELIN; SYNAPTOPHYSIN; TAU PROTEIN;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; DENSITOMETRY; ENTORHINAL CORTEX; IMMUNOCOMPETENT CELL; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; TEMPORAL LOBE;

AGE FACTORS; AGING; ANALYSIS OF VARIANCE; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ENTORHINAL CORTEX; EXTRACELLULAR MATRIX PROTEINS; MALE; NERVE TISSUE PROTEINS; NEUROPSYCHOLOGICAL TESTS; PHOSPHORYLATION; RATS; RATS, LONG-EVANS; RNA, MESSENGER; SERINE ENDOPEPTIDASES; SYNAPTOPHYSIN; TAU PROTEINS;

EID: 78651480561     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq106     Document Type: Article

References (44)

1. Arriagada PV, Marzloff K, Hyman BT. 1992. Distribution of Alzheimer-type pathologic changes in nondemented elderly individuals matches the pattern in Alzheimer's disease. Neurology. 42:1681-1688.
2. Baxter MG, Gallagher M. 1996. Neurobiological substrates of behavioral decline: models and data analytic strategies for individual differences in aging. Neurobiol Aging. 17:491-495.
3. Biernat J, Wu YZ, Timm T, Zheng-Fischhofer Q, Mandelkow E, Meijer L, Mandelkow EM. 2002. Protein kinase MARK/PAR-1 is required for neurite outgrowth and establishment of neuronal polarity. Mol Biol Cell. 13:4013-4028.
4. Boric K, Munoz P, Gallagher M, Kirkwood A. 2008. Potential adaptive function for altered long-term potentiation mechanisms in aging hippocampus. J Neurosci. 28:8034-8039.
5. Braak H, Braak E. 1995. Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol Aging. 16:271-278.
6. Chin J, Massaro CM, Palop JJ, Thwin MT, Yu GQ, Bien-Ly N, Bender A, Mucke L. 2007. Reelin depletion in the entorhinal cortex of human amyloid precursor protein transgenic mice and humans with Alzheimer's disease. J Neurosci. 27:2727-2733.
7. de Bergeyck V, Naerhuyzen B, Goffinet AM, Lambert de Rouvroit C. 1998. A panel of monoclonal antibodies against reelin, the extracellular matrix protein defective in reeler mutant mice. J Neurosci Methods. 82(1):17-24.
8. Djordjevic J, Jones-Gotman M, De Sousa K, Chertkow H. 2008. Olfaction in patients with mild cognitive impairment and Alzheimer's disease. Neurobiol Aging. 29:693-706.
9. Dong H, Martin MV, Chambers S, Csernansky JG. 2007. Spatial relationship between synapse loss and beta-amyloid deposition in Tg2576 mice. J Comp Neurol. 500:311-321.
10. Durakoglugil MS, Chen Y, White CL, Kavalali ET, Herz J. 2009. Reelin signaling antagonizes beta-amyloid at the synapse. Proc Natl Acad Sci USA. 106:15938-15943.
11. Froc DJ, Eadie B, Li AM, Wodtke K, Tse M, Christie BR. 2003. Reduced synaptic plasticity in the lateral perforant path input to the dentate gyrus of aged C57BL/6 mice. J Neurophysiol. 90(1):32-38.
12. Gallagher M, Burwell R, Burchinal M. 1993. Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav Neurosci. 107:618-626.
13. Gallagher M, Rapp PR. 1997. The use of animal models to study the effects of aging on cognition. Annu Rev Psychol. 48:339-370.
14. Geinisman Y, Bondareff W, Dodge JT. 1978. Dendritic atrophy in the dentate gyrus of the senescent rat. Am J Anat. 152:321-329.
15. Gomez-Isla T, Price JL, McKeel DW Jr, 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.
16. Haberman RP, Lee HJ, Colantuoni C, Koh MT, Gallagher M. 2008. Rapid encoding of new information alters the profile of plasticity-related mRNA transcripts in the hippocampal CA3 region. Proc Natl Acad Sci USA. 105:10601-10606.
17. Herz J, Chen Y. 2006. Reelin, lipoprotein receptors and synaptic plasticity. Nat Rev Neurosci. 7:850-859.
18. Hiesberger T, Trommsdorff M, Howell BW, Goffinet A, Mumby MC, Cooper JA, Herz J. 1999. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron. 24:481-489.
19. Hoe HS, Lee KJ, Carney RS, Lee J, Markova A, Lee JY, Howell BW, Hyman BT, Pak DT, Bu G, et al. 2009. Interaction of reelin with amyloid precursor protein promotes neurite outgrowth. J Neurosci. 29:7459-7473.
20. Insausti R, Herrero MT, Witter MP. 1997. Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus. 7:146-183.
21. Irizarry MC, Soriano F, McNamara M, Page KJ, Schenk D, Games D, Hyman BT. 1997. Abeta deposition is associated with neuropil changes, but not with overt neuronal loss in the human amyloid precursor protein V717F (PDAPP) transgenic mouse. J Neurosci. 17:7053-7059.
22. Jicha GA, Bowser R, Kazam IG, Davies P. 1997. Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau. J Neurosci Res. 48:128-132.
23. Kimura T, Yamashita S, Fukuda T, Park JM, Murayama M, Mizoroki T, Yoshiike Y, Sahara N, Takashima A. 2007. Hyperphosphorylated tau in parahippocampal cortex impairs place learning in aged mice expressing wild-type human tau. EMBO J. 26:5143-5152.
24. LaSarge CL, Montgomery KS, Tucker C, Slaton GS, Griffith WH, Setlow B, Bizon JL. 2007. Deficits across multiple cognitive domains in a subset of aged Fischer 344 rats. Neurobiol Aging. 28:928-936.
25. Martnez-Cerdeno V, Galazo MJ, Clasca F. 2003. Reelin-immunoreactive neurons, axons, and neuropil in the adult ferret brain: evidence for axonal secretion of reelin in long axonal pathways. J Comp Neurol. 463:92-116.
26. Merrill DA, Chiba AA, Tuszynski MH. 2001. Conservation of neuronal number and size in the entorhinal cortex of behaviorally characterized aged rats. J Comp Neurol. 438:445-456.
27. Niewiadomska G, Baksalerska-Pazera M, Riedel G. 2005. Altered cellular distribution of phospho-tau proteins coincides with impaired retrograde axonal transport in neurons of aged rats. Ann N Y Acad Sci. 1048:287-295.
28. Niu S, Yabut O, D'Arcangelo G. 2008. The Reelin signaling pathway promotes dendritic spine development in hippocampal neurons. J Neurosci. 28:10339-10348.
29. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. San Diego (CA): Academic Press, Inc.
30. Planel E, Richter KE, Nolan CE, Finley JE, Liu L, Wen Y, Krishnamurthy P, Herman M, Wang L, Schachter JB, et al. 2007. Anesthesia leads to tau hyperphosphorylation through inhibition of phosphatase activity by hypothermia. J Neurosci. 27:3090-3097.
31. Pujadas L, Gruart A, Bosch C, Delgado L, Teixeira CM, Rossi D, de Lecea L, Martnez A, Delgado-Garca JM, Soriano E. 2010. Reelin regulates postnatal neurogenesis and enhances spine hypertrophy and long-term potentiation. J Neurosci. 30:4636-4649.
32. Ramos-Moreno T, Galazo MJ, Porrero C, Martnez-Cerdeno V, Clasca F. 2006. Extracellular matrix molecules and synaptic plasticity: immunomapping of intracellular and secreted Reelin in the adult rat brain. Eur J Neurosci. 23:401-422.
33. Rapp PR, Deroche PS, Mao Y, Burwell RD. 2002. Neuron number in the parahippocampal region is preserved in aged rats with spatial learning deficits. Cereb Cortex. 12:1171-1179.
34. Rapp PR, Gallagher M. 1996. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc Natl Acad Sci USA. 93:9926-9930.
35. Reilly JF, Games D, Rydel RE, Freedman S, Schenk D, Young WG, Morrison JH, Bloom FE. 2003. Amyloid deposition in the hippocampus and entorhinal cortex: quantitative analysis of a transgenic mouse model. Proc Natl Acad Sci USA. 100:4837-4842.
36. Robitsek RJ, Fortin NJ, Koh MT, Gallagher M, Eichenbaum H. 2008. Cognitive aging: a common decline of episodic recollection and spatial memory in rats. J Neurosci. 28:8945-8954.
37. Scheff SW, Price DA, Schmitt FA, Mufson EJ. 2006. Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment. Neurobiol Aging. 27:1372-1384.
38. Smith TD, Adams MM, Gallagher M, Morrison JH, Rapp PR. 2000. Circuit-specific alterations in hippocampal synaptophysin immuno-reactivity predict spatial learning impairment in aged rats. J Neurosci. 20:6587-6593.
39. Spires-Jones TL, Stoothoff WH, de Calignon A, Jones PB, Hyman BT. 2009. Tau pathophysiology in neurodegeneration: a tangled issue. Trends Neurosci. 32:150-159.
40. Stranahan AM, Arumugam TV, Cutler RG, Lee K, Egan JM, Mattson MP. 2008. Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat Neurosci. 11:309-317.
41. TakumaH,ArawakaS,MoriH.2003. Isoforms changesoftau protein during development in various species. Brain Res Dev Brain Res. 142:121-127.
42. Van Strien NM, Cappaert NL, Witter MP. 2009. The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci. 10:272-282.
43. Wilson IA, Gallagher M, Eichenbaum H, Tanila H. 2006. Neurocognitive aging: prior memories hinder new hippocampal encoding. Trends Neurosci. 29:662-670.
44. Young BJ, Otto T, Fox GD, Eichenbaum H. 1997. Memory representation within the parahippocampal region. J Neurosci. 17:5183-5195.