Neurobiology of Aging
Volume 28, Issue 5 , Pages 693-703 , May 2007

Life-span influences of apoE4 on CNS function

  • Bruce Teter

      Affiliations

    • Corresponding Author InformationTel.: +1 818 891 7711x7481; fax: +1 818 895 5835.
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Received 22 June 2006 ,Accepted 22 June 2006.

References 

  1. Adams LA, Munoz DG. Differential incorporation of processes derived from different classes of neurons into senile plaques in Alzheimer's disease. Acta Neuropathol (Berl). 1993;86:365–370
  2. Aggarwal NT, Wilson RS, Beck TL, Bienias JL, Berry-Kravis E, Bennett DA. The apolipoprotein E epsilon4 allele and incident Alzheimer's disease in persons with mild cognitive impairment. Neurocase. 2005;11:3–7
  3. Aono M, Bennett ER, Kim KS, Lynch JR, Myers J, Pearlstein RD, et al. Protective effect of apolipoprotein E-mimetic peptides on N-methyl-d-aspartate excitotoxicity in primary rat neuronal-glial cell cultures. Neuroscience. 2003;116:437–445
  4. Aono M, Lee Y, Grant ER, Zivin RA, Pearlstein RD, Warner DS, et al. E protects against NMDA excitotoxicity. Neurobiol Dis. 2002;11:214–220
  5. Arendt T, Bruckner MK, Gertz HJ, Marcova L. Cortical distribution of neurofibrillary tangles in Alzheimer's disease matches the pattern of neurons that retain their capacity of plastic remodelling in the adult brain. Neuroscience. 1998;83:991–1002
  6. Arendt T, Schindler C, Bruckner MK, Eschrich K, Bigl V, Zedlick D, et al. Plastic neuronal remodeling is impaired in patients with Alzheimer's disease carrying apolipoprotein epsilon 4 allele. J Neurosci. 1997;17:516–529
  7. Ashford JW. APOE genotype effects on Alzheimer's disease onset and epidemiology. J Mol Neurosci. 2004;23:157–165
  8. Ashford JW, Atwood CS, Blass JP, Bowen RL, Finch CE, Iqbal K, et al. What is aging? What is its role in Alzheimer's disease? What can we do about it?. J Alzheimers Dis. 2005;7:247–253[discussion 255–62]
  9. Bacskai BJ, Xia MQ, Strickland DK, Rebeck GW, Hyman BT. The endocytic receptor protein LRP also mediates neuronal calcium signaling via N-methyl-d-aspartate receptors. Proc Natl Acad Sci USA. 2000;97:11551–11556
  10. Barger SW, Mattson MP. Isoform-specific modulation by apolipoprotein E of the activities of secreted beta-amyloid precursor protein. J Neurochem. 1997;69:60–67
  11. Bretsky P, Guralnik JM, Launer L, Albert M, Seeman TE. The role of APOE-epsilon4 in longitudinal cognitive decline: MacArthur studies of successful aging. Neurology. 2003;60:1077–1081
  12. Brzyska M, Elbaum D. Dysregulation of calcium in Alzheimer's disease. Acta Neurobiol Exp (Wars). 2003;63:171–183
  13. Buttini M, Akeefe H, Lin C, Mahley RW, Pitas RE, Wyss-Coray T, et al. Dominant negative effects of apolipoprotein E4 revealed in transgenic models of neurodegenerative disease. Neuroscience. 2000;97:207–210
  14. Buttini M, Orth M, Bellosta S, Akeefe H, Pitas RE, Wyss-Coray T, et al. Expression of human apolipoprotein E3 or E4 in the brains of Apoe-/-mice: isoform-specific effects on neurodegeneration. J Neurosci. 1999;19:4867–4880
  15. Carafoli E. Calcium signaling: a tale for all seasons. Proc Natl Acad Sci USA. 2002;99:1115–1122
  16. Codemo A, Mazzetto CM, Education G. APOE status and cognitive impairment in elderly. An epidemiological study in a rural setting. Neurobiol Aging. 2000;
  17. Collin T, Chat M, Lucas MG, Moreno H, Racay P, Schwaller B, et al. Developmental changes in parvalbumin regulate presynaptic Ca2+ signaling. J Neurosci. 2005;25:96–107
  18. Cummings JL, Vinters HV, Cole GM, Khachaturian ZS. Alzheimer's disease: etiologies, pathophysiology, cognitive reserve, and treatment opportunities. Neurology. 1998;51:S2–S17[discussion S65–7]
  19. Deary IJ, Whiteman MC, Pattie A, Starr JM, Hayward C, Wright AF, et al. Cognitive change and the APOE epsilon 4 allele. Nature. 2002;418:932
  20. Dekroon RM, Armati PJ. The effects of oxidative stress and altered intracellular calcium levels on vesicular transport of apoE-EGFP. Cell Biol Int. 2002;26:407–420
  21. Fonseca M, Soriano E, Ferrer I, Martinez A, Tunon T. Chandelier cell axons identified by parvalbumin-immunoreactivity in the normal human temporal cortex and in Alzheimer's disease. Neuroscience. 1993;55:1107–1116
  22. Ghebremedhin E, Schultz C, Braak E, Braak H. High frequency of apolipoprotein E epsilon4 allele in young individuals with very mild Alzheimer's disease-related neurofibrillary changes. Exp Neurol. 1998;153:152–155
  23. Greenwood PM, Lambert C, Sunderland T, Parasuraman R. Effects of apolipoprotein E genotype on spatial attention, working memory, and their interaction in healthy, middle-aged adults: results from the National Institute of Mental Health's BIOCARD study. Neuropsychology. 2005;19:199–211
  24. Grootendorst J, Bour A, Vogel E, Kelche C, Sullivan PM, Dodart JC, et al. 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
  25. Grosse G, Djalali S, Deng DR, Holtje M, Hinz B, Schwartzkopff K, et al. Area-specific effects of brain-derived neurotrophic factor (BDNF) genetic ablation on various neuronal subtypes of the mouse brain. Brain Res Dev Brain Res. 2005;156:111–126
  26. Hartmann H, Eckert A, Muller WE. Apolipoprotein E and cholesterol affect neuronal calcium signalling: the possible relationship to beta-amyloid neurotoxicity. Biochem Biophys Res Commun. 1994;200:1185–1192
  27. Hoe HS, Harris DC, Rebeck GW. Multiple pathways of apolipoprotein E signaling in primary neurons. J Neurochem. 2005;93:145–155
  28. Hoe HS, Pocivavsek A, Chakraborty G, Fu Z, Vicini S, Ehlers MD, et al. Apolipoprotein E receptor 2 interactions with the N-methyl-d-aspartate receptor. J Biol Chem. 2006;281:3425–3431
  29. Hof PR, Cox K, Young WG, Celio MR, Rogers J, Morrison JH. Parvalbumin-immunoreactive neurons in the neocortex are resistant to degeneration in Alzheimer's disease. J Neuropathol Exp Neurol. 1991;50:451–462
  30. Huang DY, Weisgraber KH, Strittmatter WJ, Matthew WD. Interaction of apolipoprotein E with laminin increases neuronal adhesion and alters neurite morphology. Exp Neurol. 1995;136:251–257
  31. Ji Y, Gong Y, Gan W, Beach T, Holtzman DM, 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
  32. Juottonen K, Lehtovirta M, Helisalmi S, Riekkinen PJ, Soininen H. Major decrease in the volume of the entorhinal cortex in patients with Alzheimer's disease carrying the apolipoprotein E epsilon4 allele. J Neurol Neurosurg Psychiatry. 1998;65:322–327
  33. Kater SB, Mills LR. Regulation of growth cone behavior by calcium. J Neurosci. 1991;11:891–899
  34. Lavretsky H, Ercoli L, Siddarth P, Bookheimer S, Miller K, Small G. Apolipoprotein epsilon4 allele status, depressive symptoms, and cognitive decline in middle-aged and elderly persons without dementia. Am J Geriatr Psychiatry. 2003;11:667–673
  35. Lehtovirta M, Kuikka J, Helisalmi S, Hartikainen P, Mannermaa A, Ryynanen M, et al. Longitudinal SPECT study in Alzheimer's disease: relation to apolipoprotein E polymorphism. J Neurol Neurosurg Psychiatry. 1998;64:742–746
  36. Lendon CL, Han BH, Salimi K, Fagan AM, Behrens MI, Muller MC, et al. No effect of apolipoprotein E on neuronal cell death due to excitotoxic and apoptotic agents in vitro and neonatal hypoxic ischaemia in vivo. Eur J Neurosci. 2000;12:2235–2242
  37. Leuba G, Kraftsik R, Saini K. Quantitative distribution of parvalbumin, calretinin, and calbindin D-28k immunoreactive neurons in the visual cortex of normal and Alzheimer cases. Exp Neurol. 1998;152:278–291
  38. Levi O, Jongen-Relo AL, Feldon J, Roses AD, Michaelson DM. ApoE4 impairs hippocampal plasticity isoform-specifically and blocks the environmental stimulation of synaptogenesis and memory. Neurobiol Dis. 2003;13:273–282
  39. Manns M, Gunturkun O. Differential effects of ocular BDNF-injections onto the development of tectal cells characterized by calcium-binding proteins in pigeons. Brain Res Bull. 2005;66:475–478
  40. Masliah E, Mallory M, Ge N, Alford M, Veinbergs I, Roses AD. Neurodegeneration in the central nervous system of apoE-deficient mice. Exp Neurol. 1995;136:107–122
  41. Mattson MP, Chan SL. Neuronal and glial calcium signaling in Alzheimer's disease. Cell Calcium. 2003;34:385–397
  42. Meirelles Kalil Pessoa de Barr, Rodrigues CJ, de Barros TE, Bevilacqua RG. Presence of apolipoprotein E epsilon4 allele in cerebral palsy. J Pediatr Orthop 20 (2000) 786–789.
  43. Mikkonen M, Alafuzoff I, Tapiola T, Soininen H, Miettinen R. Subfield- and layer-specific changes in parvalbumin, calretinin and calbindin-D28K immunoreactivity in the entorhinal cortex in Alzheimer's disease. Neuroscience. 1999;92:515–532
  44. Miller KJ, Rogers SA, Siddarth P, Small GW. Object naming and semantic fluency among individuals with genetic risk for Alzheimer's disease. Int J Geriatr Psychiatry. 2005;20:128–136
  45. Misra UK, Adlakha CL, Gawdi G, McMillian MK, Pizzo SV, Laskowitz DT. Apolipoprotein E and mimetic peptide initiate a calcium-dependent signaling response in macrophages. J Leukoc Biol. 2001;70:677–683
  46. Moceri VM, Kukull WA, Emanual I, van Belle G, Starr JR, Schellenberg GD, et al. Using census data and birth certificates to reconstruct the early-life socioeconomic environment and the relation to the development of Alzheimer's disease. Epidemiology. 2001;12:383–389
  47. Moceri VM, Kukull WA, Emanuel I, van Belle G, Larson EB. Early-life risk factors and the development of Alzheimer's disease. Neurology. 2000;54:415–420
  48. Muller W, Meske V, Berlin K, Scharnagl H, Marz W, Ohm TG. Apolipoprotein E isoforms increase intracellular Ca2+ differentially through a omega-agatoxin IVa-sensitive Ca2+-channel. Brain Pathol. 1998;8:641–653
  49. Nathan BP, Bellosta S, Sanan DA, Weisgraber KH, Mahley RW, Pitas RE. Differential effects of apolipoproteins E3 and E4 on neuronal growth in vitro. Science. 1994;264:850–852
  50. Nelson PG. Activity-dependent synapse modulation and the pathogenesis of Alzheimer disease. Curr Alzheimer Res. 2005;2:497–506
  51. Ohkubo N, Mitsuda N, Tamatani M, Yamaguchi A, Lee YD, Ogihara T, et al. Apolipoprotein E4 stimulates cAMP response element-binding protein transcriptional activity through the extracellular signal-regulated kinase pathway. J Biol Chem. 2001;276:3046–3053
  52. Ohm TG, Hamker U, Cedazo-Minguez A, Rockl W, Scharnagl H, Marz W, et al. Apolipoprotein E and beta A4-amyloid: signals and effects. Biochem Soc Symp. 2001;121–129
  53. Ohm TG, Scharnagl H, Marz 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
  54. Pei JJ, Braak H, An WL, Winblad B, Cowburn RF, Iqbal K, et al. Up-regulation of mitogen-activated protein kinases ERK1/2 and MEK1/2 is associated with the progression of neurofibrillary degeneration in Alzheimer's disease. Brain Res Mol Brain Res. 2002;109:45–55
  55. Plassman BL, Welsh-Bohmer KA, Bigler ED, Johnson SC, Anderson CV, Helms MJ, et al. Apolipoprotein E epsilon 4 allele and hippocampal volume in twins with normal cognition. Neurology. 1997;48:985–989
  56. Puttfarcken PS, Manelli AM, Falduto MT, Getz GS, LaDu MJ. Effect of apolipoprotein E on neurite outgrowth and beta-amyloid-induced toxicity in developing rat primary hippocampal cultures. J Neurochem. 1997;68:760–769
  57. Qiu C, Backman L, Winblad B, Aguero-Torres H, Fratiglioni L. The influence of education on clinically diagnosed dementia incidence and mortality data from the Kungsholmen Project. Arch Neurol. 2001;58:2034–2039
  58. Qiu Z, Crutcher KA, Hyman BT, Rebeck GW. ApoE isoforms affect neuronal N-methyl-d-aspartate calcium responses and toxicity via receptor-mediated processes. Neuroscience. 2003;122:291–303
  59. Qiu Z, Hyman BT, Rebeck GW. Apolipoprotein E receptors mediate neurite outgrowth through activation of p44/42 mitogen-activated protein kinase in primary neurons. J Biol Chem. 2004;279:34948–34956
  60. Qiu Z, Strickland DK, Hyman BT, Rebeck GW. alpha 2-Macroglobulin exposure reduces calcium responses to N-methyl-d-aspartate via low density lipoprotein receptor-related protein in cultured hippocampal neurons. J Biol Chem. 2002;277:14458–14466
  61. Raber J, Bongers G, LeFevour A, Buttini M, Mucke L. Androgens protect against apolipoprotein E4-induced cognitive deficits. J Neurosci. 2002;22:5204–5209
  62. Raber J, Huang Y, Ashford JW. ApoE genotype accounts for the vast majority of AD risk and AD pathology. Neurobiol Aging. 2004;25:641–650
  63. Raber J, Wong D, Buttini M, Orth M, Bellosta S, Pitas RE, et al. Isoform-specific effects of human apolipoprotein E on brain function revealed in ApoE knockout mice: increased susceptibility of females. Proc Natl Acad Sci USA. 1998;95:10914–10919
  64. Raber J, Wong D, Yu GQ, Buttini M, Mahley RW, Pitas RE, et al. Apolipoprotein E and cognitive performance. Nature. 2000;404:352–354
  65. Ramon y Cajal S., Degeneration and regeneration in the nervous system [R.M. May transl.]. Hafner; 1928, Oxford University Press, USA, 1991.
  66. Reiman EM, Chen K, Alexander GE, Caselli RJ, Bandy D, Osborne D, et al. Functional brain abnormalities in young adults at genetic risk for late-onset Alzheimer's dementia. Proc Natl Acad Sci USA. 2004;101:284–289
  67. Riley KP, Snowdon DA, Saunders AM, Roses AD, Mortimer JA, Nanayakkara N. Cognitive function and apolipoprotein E in very old adults: findings from the Nun study. J Gerontol B Psychol Sci Soc Sci. 2000;55:S69–S75
  68. Roses AD SA, Huang Y, Strum J, Weisgraber KH, Mahley RW. Complex disease-associatyed pharmacogenetics: drug efficacy, drug safety, and confirmation of a pathogenic hypothesis (Alzheimer's disease). Pharmacogenomics J, June 13 [Epub ahead of print].
  69. Salehi A, Lucassen PJ, Pool CW, Gonatas NK, Ravid R, Swaab DF. Decreased neuronal activity in the nucleus basalis of Meynert in Alzheimer's disease as suggested by the size of the Golgi apparatus. Neuroscience. 1994;59:871–880
  70. Sampson VL, Morrison JH, Vickers JC. The cellular basis for the relative resistance of parvalbumin and calretinin immunoreactive neocortical neurons to the pathology of Alzheimer's disease. Exp Neurol. 1997;145:295–302
  71. Seeman TE, Huang MH, Bretsky P, Crimmins E, Launer L, Guralnik JM. Education and APOE-e4 in longitudinal cognitive decline: MacArthur studies of successful aging. J Gerontol B Psychol Sci Soc Sci. 2005;60:P74–P83
  72. Sheng H, Laskowitz DT, Bennett E, Schmechel DE, Bart RD, Saunders AM, et al. Apolipoprotein E isoform-specific differences in outcome from focal ischemia in transgenic mice. J Cereb Blood Flow Metab. 1998;18:361–366
  73. Siucinska E, Kossut M. Short-term sensory learning does not alter parvalbumin neurons in the barrel cortex of adult mice: a double-labeling study. Neuroscience. 2006;138:715–724
  74. Small BJ, Basun H, Backman L. Three-year changes in cognitive performance as a function of apolipoprotein E genotype: evidence from very old adults without dementia. Psychol Aging. 1998;13:80–87
  75. Small GW, Ercoli LM, Silverman DH, Huang SC, Komo S, Bookheimer SY, et al. Cerebral metabolic and cognitive decline in persons at genetic risk for Alzheimer's disease. Proc Natl Acad Sci USA. 2000;97:6037–6042
  76. Smith GE, Bohac DL, Waring SC, Kokmen E, Tangalos EG, Ivnik RJ, et al. Apolipoprotein E genotype influences cognitive ‘phenotype’ in patients with Alzheimer's disease but not in healthy control subjects. Neurology. 1998;50:355–362
  77. Solodkin A, Veldhuizen SD, Van Hoesen GW. Contingent vulnerability of entorhinal parvalbumin-containing neurons in Alzheimer's disease. J Neurosci. 1996;16:3311–3321
  78. Teasdale GM, Murray GD, Nicoll JA. The association between APOE epsilon4, age and outcome after head injury: a prospective cohort study. Brain. 2005;128:2556–2561
  79. Teter B, Ashford JW. Neuroplasticity in Alzheimer's disease. J Neurosci Res. 2002;70:402–437
  80. Teter B, Xu PT, Gilbert JR, Roses AD, Galasko D, Cole GM. Defective neuronal sprouting by human apolipoprotein E4 is a gain-of-negative function. J Neurosci Res. 2002;68:331–336
  81. 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
  82. Thal LJ. The Alzheimer's disease cooperative study in 2004. Alzheimer Dis Assoc Disord. 2004;18:183–185
  83. Tolar M, Keller JN, Chan S, Mattson MP, Marques MA, Crutcher KA. Truncated apolipoprotein E (ApoE) causes increased intracellular calcium and may mediate ApoE neurotoxicity. J Neurosci. 1999;19:7100–7110
  84. Tolar M, Marques MA, Harmony JA, Crutcher KA. Neurotoxicity of the 22kDa thrombin-cleavage fragment of apolipoprotein E and related synthetic peptides is receptor-mediated. J Neurosci. 1997;17:5678–5686
  85. Turic D, Fisher PJ, Plomin R, Owen MJ. No association between apolipoprotein E polymorphisms and general cognitive ability in children. Neurosci Lett. 2001;299:97–100
  86. Veinbergs I, Everson A, Sagara Y, Masliah E. Neurotoxic effects of apolipoprotein E4 are mediated via dysregulation of calcium homeostasis. J Neurosci Res. 2002;67:379–387
  87. Veinbergs I, Mallory M, Mante M, Rockenstein E, Gilbert JR, Masliah E. Differential neurotrophic effects of apolipoprotein E in aged transgenic mice. Neurosci Lett. 1999;265:218–222
  88. Vesalius A, De humani corporis fabrica (On the fabric of the human body), Book One, The things that sustain and support the entire body, and what braces and attaches them all (The bones and the ligaments that interconnect them), Johannes Oporinus, Basel, Drawing of the Bones of the Human Body, Seen from the Side, 1543, p. 164.
  89. Wahlund LO, Julin P, Lannfelt L, Lindqvist J, Svensson L. Inheritance of the ApoE epsilon4 allele increases the rate of brain atrophy in dementia patients. Dement Geriatr Cogn Disord. 1999;10:262–268
  90. Wang C, Wilson WA, Moore SD, Mace BE, Maeda N, Schmechel DE, et al. Human apoE4-targeted replacement mice display synaptic deficits in the absence of neuropathology. Neurobiol Dis. 2005;18:390–398
  91. Wang X, Luebbe P, Gruenstein E, Zemlan F. Apolipoprotein E (ApoE) peptide regulates tau phosphorylation via two different signaling pathways. J Neurosci Res. 1998;51:658–665
  92. Wang XS, Gruenstein E. Rapid elevation of neuronal cytoplasmic calcium by apolipoprotein E peptide. J Cell Physiol. 1997;173:73–83
  93. Winnock M, Letenneur L, Jacqmin-Gadda H, Dallongeville J, Amouyel P, Dartigues JF. Longitudinal analysis of the effect of apolipoprotein E epsilon4 and education on cognitive performance in elderly subjects: the PAQUID study. J Neurol Neurosurg Psychiatry. 2002;72:794–797
  94. Wright RO, Hu H, Silverman EK, Tsaih SW, Schwartz J, Bellinger D, et al. Apolipoprotein E genotype predicts 24-month bayley scales infant development score. Pediatr Res. 2003;54:819–825
  95. Xu PT, Li YJ, Qin XJ, Scherzer CR, Xu H, Schmechel DE, et al. Differences in apolipoprotein E3/3 and E4/4 allele-specific gene expression in hippocampus in Alzheimer disease. Neurobiol Dis. 2006;21:256–275
  96. 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
  97. De Mattos RD, Curtiss LK, Williams DL. A minimally lipidated form of cell-derived apolipoprotein E exhibits isoform-specific stimulation of neurite outgrowth in the absence of exogenous lipids or lipoproteins. J Biol Chem. 1998;273:4206–4212
  98. DeMattos RB, Brendza RP, Heuser JE, Kierson M, Cirrito JR, Fryer J, et al. Purification and characterization of astrocyte-secreted apolipoprotein E and J-containing lipoproteins from wild-type and human apoE transgenic mice. Neurochem Int. 2001;39:415–425
  99. Fagan AM, Bu G, Sun Y, Daugherty A, Holtzman DM. Apolipoprotein E-containing high density lipoprotein promotes neurite outgrowth and is a ligand for the low density lipoprotein receptor-related protein. J Biol Chem. 1996;271:30121–30125
  100. Handelmann GE, Boyles JK, Weisgraber KH, Mahley RW, Pitas RE. Effects of apolipoprotein E, b-very low density lipoproteins, and cholesterol on the extension of neurites by rabbit dorsal root ganglion neurons in vitro. J Lipid Res. 1992;33:1677–1688
  101. 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 Nat Acad Sci USA. 1995;92:9480–9484
  102. Maezawa I, Zaja-Milatovic S, Milatovic D, Stephen C, Sokal I, Maeda N, et al. Apolipoprotein E isoform-dependent dendritic recovery of hippocampal neurons following activation of innate immunity. J Neuroinflammation. 2006;3(1):21;[Epub ahead of print]
  103. Nathan BP, Chang K, Bellosta S, Brisch E, Ge N, Mahley RW, et al. The inhibitory effect of apolipoprotein E4 on neurite outgrowth is associated with microtubule depolymerization. J Biol Chem. 1995;270(34):19791–19799
  104. Nathan BP, Jiang Y, Wong GK, Shen F, Brewer G, Struble RG. Apolipoprotein E4 inhibits, and apolipoprotein E3 promotes neurite sprouting in cultured adult mouse cortical neurons through a low-density lipoprotin receptor-related protein. Brain Res. 2002;928:96–105
  105. Peng D, Song C, Reardon CA, Liao S, Getz GS. Lipoproteins produced by ApoE−/− astrocytes infected with adenovirus expressing human ApoE. J Neurochem. 2003;86(6):1391–1402
  106. Sun Y, Wu S, Bu G, Onifade MK, Patel SN, LaDu MJ, et al. Glial fibrillary acidic protein-apolipoprotein E transgenic mice: astrocyte-specific expression and differing biological effects of astrocyte-secreted apoE3 and apoE4 lipoproteins. J Neurosci. 1998;18:3261–3272

PII: S0197-4580(06)00337-X

doi: 10.1016/j.neurobiolaging.2006.06.028

Neurobiology of Aging
Volume 28, Issue 5 , Pages 693-703 , May 2007