Neurobiology of Aging
Volume 28, Issue 5 , Pages 677-686 , May 2007

Apolipoprotein E polymorphism and dendritic shape in hippocampal interneurons

Received 20 September 2005 ,Revised 16 March 2006 ,Accepted 31 March 2006.

References 

  1. Ackermann H. BIAS—a programme package for biometrical analysis of samples. Comp Stat. 1991;11:223–224
  2. Anderton BH, Callahan L, Coleman P, Davies P, Flood D, Jicha GA, et al. Dendritic changes in Alzheimer's disease and factors that may underlie these changes. Progr Neurobiol. 1998;55:595–609
  3. Arendt T, Schindler C, Brückner MK, Eschrich K, Bigl V, Zedlick D, et al. Plastic neuronal remodeling is impaired in patients with Alzheimer's disease carrying apolipoprotein e4 allele. J Neurosci. 1997;17:516–529
  4. Bancher C, Braak H, Fischer P, Jellinger KA. Neuropathological staging of Alzheimer lesions and intellectual status in Alzheimer's and Parkinson's disease patients. Neurosci Lett. 1993;162:179–182
  5. Bancher C, Egensperger R, Kosel S, Jellinger K, Graeber MB. Low prevalence of apolipoprotein E epsilon 4 allele in the neurofibrillary tangle predominant form of senile dementia. Acta Neuropathol Berl. 1997;94:403–409
  6. Bellosta S, Nathan BP, Orth M, Dong LM, Mahley RW, Pitas RE. Stable expression and secretion of apolipoproteins E3 and E4 in mouse neuroblastoma cells produces differential effects on neurite outgrowth. J Biol Chem. 1995;270:27063–27071
  7. Braak E, Braak H, Mandelkow EM. A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol Berl. 1994;87:554–567
  8. Braak E, Strotkamp B, Braak H. Parvalbumin-immunoreactive structures in the hippocampus of the human adult. Cell Tissue Res. 1991;264:33–48
  9. Braak H, Braak E . Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol Berl. 1991;82:239–259
  10. Braak H, Braak E, Ohm T, Bohl J. Alzheimer's disease: mismatch between amyloid plaques and neuritic plaques. Neurosci Lett. 1989;103:24–28
  11. Braak H, Duyckaerts C, Braak E, Piette F. Neuropathological staging of Alzheimer-related changes correlates with psychometrically assessed intellectual status. In:  Corain B,  Iqbal K,  Nicolini M,  Winblad B,  Wisniewski H,  Zatta P editor. Alzheimer's disease: advances in clinical and basic research. John Wiley & Sons Ltd.; 1993;p. 131–137
  12. Campbell S, Switzer RC, Martin TL. Alzheimer's plaques and tangles: a controlled and enhanced silver staining method. Soc Neurosci Abstr. 1987;13:678
  13. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Rimmler JB, et al. Apolipoproein E, survival in Alzheimer's disease patients, and the competing risks of death and Alzheimer's disease. Neurology. 1995;45:1323–1328
  14. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell P, Small GW, et al. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science. 1993;261:921–923[see comments]
  15. DeMattos RB, Rudel LL, Williams DL. Biochemical analysis of cell-derived apoE3 particles active in stimulating neurite outgrowth. J Lipid Res. 2001;42:976–987
  16. Emi M, Wu LL, Robertson MA, Myers RL, Hegele RA, Williams RR, et al. Genotyping and sequence analysis of apolipoprotein isoforms. Genomics. 1988;3:373–379
  17. Falke E, Nissanov J, Mitchell TW, Bennett DA, Trojanowski JQ, Arnold SE. Subicular dendritic arborization in Alzheimer's disease correlates with neurofibrillary tangle density. Am J Pathol. 2003;163:1615–1621
  18. Freund TF, Buzsaki G. Interneurons of the hippocampus. Hippocampus. 1996;6:347–470
  19. Gallyas F. Silver staining of Alzheimer's neurofibrillary changes by means of physical development. Acta Morphol Acad Sci Hung. 1971;19:1–8
  20. Ghebremedhin E, Schultz C, Thal DR, Rüb U, Ohm TG, Braak E, et al. Gender and age modify the association between ApoE and AD-related neuropathology. Neurology. 2001;56:1696–1701
  21. Glöckner F, Meske V, Ohm TG. Genotype-related differences of hippocampal apolipoprotein E levels only in early stages of neuropathological changes in Alzheimer's disease. Neuroscience. 2002;114:1103–1114
  22. Gomez Isla T, Price JL, McKeel DW, Morris JC, Growdon JH, Hyman BT. Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J Neurosci. 1996;16:4491–4500
  23. Guyton JR, Miller SE, Martin ME, Khan WA, Roses AD, Strittmatter W. Novel large apolipoprotein E-containing lipoproteins of density 1.006–1.060g/ml in human cerebrospinal fluid. J Neurochem. 1998;70:1235–1240
  24. Holtzman DM, Pitas RE, Kilbridge J, Nathan B, Mahley RW, Bu G, et al. Low density lipoprotein receptor-related protein mediates apolipoprotein E-dependent neurite outgrowth in a central nervous system-derived neuronal cell line. Proc Natl Acad Sci USA. 1995;92:9480–9484
  25. Ji Y, Gong Y, Gan W, Beach T, Holtzman DW, Wisniewski T. Apolipoprotein E isoform-specific regulation of dendritic spine morphology in apolipoprotein E transgenic mice and Alzheimer's disease patients. Neuroscience. 2003;122:305–315
  26. Laskowitz DT, Horsburgh K, Roses AD. Apolipoprotein E and the CNS response to injury. J Cereb Blood Flow Metab. 1998;18:465–471
  27. McBain CJ, Fisahn A. Interneurons unbound. Nat Rev Neurosci. 2001;2:11–23
  28. Miehe U, Leranth C, Ohm TG, Nitsch R. Long-lasting transneuronal dendritic changes of GABAergic neurons in the monkey dentate gyrus following entorhinal cortex lesion. Neurosci Lett. 1994;168:115–118
  29. Nagy Z, Esiri MM, Jobst KA, Johnston C, Litchfield S, Sim E, et al. Influence of the apolipoprotein E genotype on amyloid deposition and neurofibrillary tangle formation in Alzheimer's disease. Neuroscience. 1995;69:757–761
  30. Nathan BP, Bellosta S, Sanan DA, Weisgraber KH, Mahley RW, Pitas R. Differential effects of apolipoproteins E3 and E4 on neuronal growth in vitro. Science. 1994;264:850–852
  31. Nathan BP, Jiang Y, Wong GK, Shen F, Brewer GJ, Struble R. Apolipoprotein E4 inhibits, and apolipoprotein E3 promotes neurite outgrowth in cultured adult mouse cortical neurons through the low-density lipoprotein receptor-related protein. Brain Res. 2002;928:96–105
  32. Ohm TG, Braak E, Braak H. A competition between silver-stain and immunocytochemistry. Neural Transm (P-D Sect). 1989;1:111
  33. Ohm TG, Kirca M, Bohl J, Scharnagl H, Gross W, März W. Apolipoprotein E polymorphism influences not only cerebral senile plaque load but also Alzheimer-type neurofibrillary tangle formation. Neuroscience. 1995;66:583–587
  34. Ohm TG, Müller H, Ulfig N, Braak E. Glutamic acid decarboxylase- and Parvalbumin-like immunoreactive structures in the olfactory bulb of the human adult. J Comp Neurol. 1990;291:1–8
  35. Ohm TG, Münch S, Schönheit B, Zarski R, Nitsch R. Transneuronally altered dendritic processing of tangle-free neurons in Alzheimer's disease. Acta Neuropathol. 2002;103:437–443
  36. Ohm TG, Scharnagl H, März W, Bohl J. Apolipoprotein E isoforms and the development of low and high Braak stages of Alzheimer's disease-related lesions. Acta Neuropathol Berl. 1999;98:273–280
  37. Pitas RE, Boyles JK, Lee SH, Foss D, Mahley RW. Astrocytes synthesize apolipoprotein E and metabolize apolipoprotein E-containing lipoproteins. Biochim Biophys Acta. 1987;917:148–161
  38. Poirier J, Hess M, May PC, Finch CE. Astrocytic apolipoprotein E mRNA and GFAP mRNA in hippocampus after entorhinal cortex lesioning. Brain Res Mol Brain Res. 1991;11:97–106
  39. Roheim PS, Carey M, Forte T, Vega GL. Apolipoproteins in human cerebrospinal fluid. Proc Natl Acad Sci USA. 1979;76:4646–4649
  40. Saunders AM, Strittmatter WJ, Schmechel D, St. George-Hyslop PH, Pericak Vance MA, Joo SH, et al. Association of apolipoprotein E allele epsilon-4 with late-onset familial and sporadic Alzheimer's disease. Neurology. 1993;43:1467–1472
  41. Schönheit B, Döscher R, Ohm TG. Scientific progress and a hardy paradigm—the ‘amyloid cascade hypothesis’ revisited. Neurobiol Aging. 2004;25:743–746
  42. Schönheit B, Zarski R, Ohm TG. Spatial and temporal relationships between plaques and tangles in Alzheimer-pathology. Neurobiol Aging. 2004;25:697–711
  43. Teter B, Ashford JW. Neuroplasticity in Alzheimer's disease. J Neurosci Res. 2002;70:402–437
  44. Teter B, Harris-White ME, Frautschy SA, Cole GM. Role of apolipoprotein E and estrogen in mossy fiber sprouting in hippocampal slice cultures. Neuroscience. 1999;91:1009–1016
  45. Teter B, Xu PT, Gilbert JR, Roses AD, Galasko D, Cole GM. Human apolipoprotein E isoform-specific differences in neuronal sprouting in organotypic hippocampal culture. J Neurochem. 1999;73:2613–2616
  46. Weisgraber KH, Roses AD, Strittmatter WJ. The role of apolipoprotein E in the nervous system. Curr Opin Lipidol. 1994;5:110–116
  47. White F, Nicoll JA, Roses AD, Horsburgh K. Impaired neuronal plasticity in transgenic mice expressing human apolipoprotein E4 compared to E3 in a model of entorhinal cortex lesion. Neurobiol Dis. 2001;8:611–625

PII: S0197-4580(06)00332-0

doi: 10.1016/j.neurobiolaging.2006.03.016

Neurobiology of Aging
Volume 28, Issue 5 , Pages 677-686 , May 2007