Human apolipoprotein E isoform-specific differences in neuronal sprouting in organotypic hippocampal culture.
Abstract
The apolipoprotein E (ApoE) epsilon4 allele is a major risk factor for neurodegenerative conditions, including Alzheimer's disease. A role for ApoE is implicated in regeneration of synaptic circuitry after neural injury. In the in vitro mouse organotypic hippocampal slice culture system, we previously showed that cultures derived from ApoE-knockout mice are defective in mossy fiber sprouting into the dentate gyrus molecular layer. This sprouting defect was rescued in cultures from transgenic mice expressing ApoE3 under the control of the human promoter and in ApoE-knockout cultures treated with ApoE3-conditioned media. Although the ApoE3 transgene fully restored sprouting, ApoE4 restored sprouting to only 58% of ApoE3 levels. These data indicate that ApoE isoform-specific effects on neuroregeneration may contribute to its genetic risk for Alzheimer's disease.
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ApoE3 was shown to augment neuronal sprouting in a developing organotypic hippocampal slice system.
“apoE3 was shown to augment neuronal sprouting in a developing organotypic hippocampal slice system (Teter et al., 1999).”
From Apolipoprotein E in Synaptic Plasticity and Alzheimer’s Disease: Potential Cellular and Molecular Mechanisms (2014) · cites this paper as Teter et al., 1999
Cites
Corder, E. H., Saunders, A. M., Strittmatter, W. J., Schmechel, D. E., Gaskell, P. C., Small, G. W., Roses, A. D., Haines, J. L., & Pericak-Vance, M. A. (1993) · Science · doi:10.1126/science.8346443 · Cited by 9,429 · see citing works
Self-citationApolipoprotein E: Cholesterol Transport Protein with Expanding Role in Cell Biology
Mahley, R. W. (1988) · Science · doi:10.1126/science.3283935 · Cited by 4,028 · see citing works
A simple method for organotypic cultures of nervous tissue
Stoppini, L., Buchs, P., & Muller, D. (1991) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(91)90128-m · Cited by 3,097 · see citing works
Perforant pathway changes and the memory impairment of Alzheimer's disease
Hyman, B. T., Van Hoesen, G. W., Kromer, L. J., & Damasio, A. R. (1986) · Annals of Neurology · doi:10.1002/ana.410200406 · Cited by 672 · see citing works
Apolipoprotein E in animal models of CNS injury and in alzheimer's disease
Poirier, J. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90156-2 · Cited by 637 · see citing works
Boyles, J. K., Zoellner, C. D., Anderson, L. J., Kosik, L. M., Pitas, R. E., Weisgraber, K. H., Hui, D. Y., Mahley, R. W., Gebicke‐Haerter, P. J., & Ignatius, M. J. (1989) · Journal of Clinical Investigation · doi:10.1172/jci113943 · Cited by 533 · see citing works
Plasticity of Hippocampal Circuitry in Alzheimer's Disease
Geddes, J. W., Monaghan, D. T., Cotman, C. W., Lott, I. T., Kim, R. C., & Chui, H. C. (1985) · Science · doi:10.1126/science.4071042 · Cited by 461 · see citing works
Buttini, M., Orth, M., Bellosta, S., Akeefe, H., Pitas, R. E., Wyss‐Coray, T., Mucke, L., & Mahley, R. W. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-12-04867.1999 · Cited by 355 · see citing works
Holtzman, D. M., Pitas, R. E., Kilbridge, J., Nathan, B., Mahley, R. W., Bu, G., & Schwartz, A. L. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.21.9480 · Cited by 349 · see citing works
Arendt, T., Schindler, C., Brückner, M. K., Eschrich, K., Bigl, V., Zedlick, D., & Marcova, L. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-02-00516.1997 · Cited by 319 · see citing works
Bellosta, S., Nathan, B. P., Orth, M., Dong, L.-M., Mahley, R. W., & Pitas, R. E. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.45.27063 · Cited by 313 · see citing works
Organotypic cultures of neural tissue
Gähwiler, B. H. (1988) · Trends in Neurosciences · doi:10.1016/0166-2236(88)90007-0 · Cited by 253 · see citing works
Patterns of aberrant sprouting in alzheimer's disease
Masliah, E., Mallory, M. E., Hansen, L. A., Alford, M. F., Albright, T., DeTeresa, R. M., Terry, R. D., Baudier, J., & Saitoh, T. (1991) · Neuron · doi:10.1016/0896-6273(91)90170-5 · Cited by 245 · see citing works
Sun, Y., Wu, S., Bu, G., Onifade, M. K., Patel, S. N., LaDu, M. J., Fagan, A. M., & Holtzman, D. M. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-09-03261.1998 · Cited by 213 · see citing works
Apolipoprotein E and the CNS Response to Injury
Laskowitz, D. T., Horsburgh, K., & Roses, A. D. (1998) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199805000-00001 · Cited by 201 · see citing works
Self-citationHeinonen, O., Soininen, H., Sorvari, H., Kosunen, O., Paljärvi, L., Koivisto, E., & Riekkinen, P. J. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00422-2 · Cited by 186 · see citing works
Xu, P.-T., Schmechel, D., Rothrock-Christian, T., Burkhart, D. S., Qiu, H.-L., Popko, B., Sullivan, P., Maeda, N., Saunders, A. M., Roses, A. D., et al. (1996) · Neurobiology of Disease · doi:10.1006/nbdi.1996.0023 · Cited by 178 · cited 2× · see citing works
“Human ApoE3 and ApoE4 (driven by the human ApoE promoter) transgenic mice were made in the ApoE-ko background (Xu et al., 1996).”
Self-citationHead Injury and Risk of Alzheimer's Disease by Apolipoprotein E Genotype
O’Meara, E. S., Kukull, W. A., Sheppard, L. A., Bowen, J., McCormick, W. C., Teri, L. L., Pfanschmidt, M. L., Thompson, J. D., Schellenberg, G. D., & Larson, E. B. (1997) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a009290 · Cited by 165 · see citing works
Masliah, E., Samuel, W., Veinbergs, I., Mallory, M., Mante, M., & Saitoh, T. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01420-5 · Cited by 146 · see citing works
Apolipoprotein E Isoform-Specific Differences in Outcome from Focal Ischemia in Transgenic Mice
Sheng, H., Laskowitz, D. T., Bennett, E. R., Schmechel, D. E., Bart, R. D., Saunders, A. M., Pearlstein, R. D., Roses, A. D., & Warner, D. S. (1998) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199804000-00003 · Cited by 143 · see citing works
Self-citationThe role of apolipoprotein E in the nervous system
Weisgraber, K. H., Roses, A. D., & Strittmatter, W. J. (1994) · Current Opinion in Lipidology · doi:10.1097/00041433-199404000-00007 · Cited by 136 · see citing works
Self-citationDeMattos, R. B., Curtiss, L. K., & Williams, D. L. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.7.4206 · Cited by 123 · see citing works
Behavioural, physiological and morphological analysis of a line of apolipoprotein E knockout mouse
Anderson, R., Barnes, J. C., Bliss, T. V. P., Cain, D. P., Cambon, K., Davies, H. A., Errington, M. L., Fellows, L. A., Gray, R. A., Hoh, T., et al. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00598-8 · Cited by 119 · see citing works
The distribution of Timm's stain in the nonsulphide‐perfused human hippocampal formation
Cassell, M. D., & Brown, M. W. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902220311 · Cited by 98 · see citing works
Nerve Regeneration Occurs in the Absence of Apolipoprotein E in Mice
Popko, B., Goodrum, J. F., Bouldin, T. W., Zhang, S. H., & Maeda, N. (1993) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1993.tb03268.x · Cited by 80 · see citing works
Lesion-induced neurite sprouting and synapse formation in hippocampal organotypic cultures
Stoppini, L., Buchs, P., & Müller, D. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90043-f · Cited by 73 · see citing works
Role of apolipoprotein E and estrogen in mossy fiber sprouting in hippocampal slice cultures
Teter, B., Harris‐White, M. E., Frautschy, S. A., & Cole, G. M. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00630-7 · Cited by 70 · see citing works
Self-citationGrowth of hippocampal mossy fibers: A lesion and coculture study of organotypic slice cultures
Zimmer, J., & Gähwiler, B. H. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902640102 · Cited by 61 · see citing works
Masliah, E., Mallory, M. E., DeTeresa, R. M., Alford, M. F., & Hansen, L. A. (1993) · Brain Research · doi:10.1016/0006-8993(93)91093-8 · Cited by 58 · see citing works
Specific Neurochemical Derangements of Brain Projecting Neurons in Apolipoprotein E‐Deficient Mice
Chapman, S., & Michaelson, D. M. (1998) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1998.70020708.x · Cited by 52 · see citing works
Coltman, B. W., Earley, E. M., Shahar, A., Dudek, F. E., & Ide, C. F. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903620205 · Cited by 44 · see citing works
Frotscher, M. (1992) · Microscopy Research and Technique · doi:10.1002/jemt.1070230406 · Cited by 34 · see citing works
The Role of Misdirected Plasticity in Plaque Biogenesis and Alzheimer’s Disease Pathology
Cotman, C. W., Cummings, B. J., & Whitson, J. S. (1991) · Springer eBooks · doi:10.1007/978-3-642-46722-6_19 · Cited by 27 · see citing works
Gracia, V., Fiol, C., Hurtado, I., Pintó, X., Argimón, J., & Castiñeiras, M. J. (1994) · Analytical Biochemistry · doi:10.1006/abio.1994.1576 · Cited by 20 · see citing works
Sekiguchi, M., Abe, H., Nagato, Y., Tanaka, O., Guo, H., & Nowakowski, R. S. (1996) · Developmental Brain Research · doi:10.1016/0165-3806(95)00195-6 · Cited by 15 · see citing works
Methods for Evaluating a Slice Culture Model of Alzheimer’s Disease
Harris‐White, M. E., Sigel, J. J., Frautschy, S. A., & Cole, G. M. (1999) · Springer eBooks · doi:10.1007/978-3-642-59916-3_4 · Cited by 6 · see citing works
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Kim, J., Basak, J. M., & Holtzman, D. M. (2009) · Neuron · doi:10.1016/j.neuron.2009.06.026 · Cited by 1,661 · see citing works
The Neuropathology and Neurobiology of Traumatic Brain Injury
Blennow, K., Hardy, J., & Zetterberg, H. (2012) · Neuron · doi:10.1016/j.neuron.2012.11.021 · Cited by 669 · see citing works
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Li, Z., Shue, F., Zhao, N., Shinohara, M., & Bu, G. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00413-4 · Cited by 306 · see citing works
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Bennett, D. A., Wilson, R. S., Schneider, J. A., Evans, D. A., Aggarwal, N. T., Arnold, S. E., Cochran, E. J., Berry-Kravis, E., & Bienias, J. L. (2003) · Neurology · doi:10.1212/01.wnl.0000042478.08543.f7 · Cited by 282 · see citing works
Fernández-Calle, R., Konings, S. C., Frontiñán-Rubio, J., García-Revilla, J., Camprubí-Ferrer, L., Svensson, M., Martinson, I., Boza-Serrano, A., Venero, J. L., Nielsen, H. M., et al. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00566-4 · Cited by 278 · see citing works
Shih, R. A., Hu, H., Weisskopf, M. G., & Schwartz, B. S. (2006) · Environmental Health Perspectives · doi:10.1289/ehp.9786 · Cited by 259 · see citing works
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Dumanis, S. B., Tesoriero, J. A., Babus, L. W., Nguyen, M. T., Trotter, J. H., Ladu, M. J., Weeber, E. J., Turner, R. S., Xu, B., Rebeck, G. W., et al. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4026-09.2009 · Cited by 220 · see citing works
Ji, Y., Gong, Y., Gan, W., Beach, T., Holtzman, D. M., & Wisniewski, T. (2003) · Neuroscience · doi:10.1016/j.neuroscience.2003.08.007 · Cited by 189 · see citing works
Suri, S., Heise, V., Trachtenberg, A. J., & Mackay, C. E. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.10.010 · Cited by 183 · see citing works
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Vance, J., & Hayashi, H. (2010) · Biochimica et Biophysica Acta · doi:10.1016/j.bbalip.2010.02.007 · Cited by 185 · see citing works
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Mayeux, R. P., Small, S. A., Tang, M., Tycko, B., & Stern, Y. (2001) · Neurobiology of Aging · doi:10.1016/s0197-4580(01)00223-8 · Cited by 156 · see citing works
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Wright, R. O., Hu, H., Silverman, E. K., Tsaih, S.-W., Schwartz, J. D., Bellinger, D. C., Palazuelos, E., Weiss, S. T., & Hernández‐Ávila, M. (2003) · Pediatric Research · doi:10.1203/01.pdr.0000090927.53818.de · Cited by 151 · see citing works
Alexander, D. M., Williams, L. M., Gatt, J. M., Dobson‐Stone, C., Kuan, S., Todd, E. G., Schofield, P. R., Cooper, N. J., & Gordon, E. (2007) · Biological Psychology · doi:10.1016/j.biopsycho.2007.03.001 · Cited by 148 · see citing works
Kim, J., Yoon, H., Basak, J., & Kim, J. (2014) · Molecules and Cells · doi:10.14348/molcells.2014.0248 · Cited by 141 · see citing works
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Roses, A. D. (2006) · Journal of Alzheimer's Disease · doi:10.3233/jad-2006-9s340 · Cited by 86 · see citing works
Self-citationIs Brain Amyloid Production a Cause or a Result of Dementia of The Alzheimer's Type?
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Hoe, H.-S., & Rebeck, G. W. (2005) · Molecular Brain Research · doi:10.1016/j.molbrainres.2005.02.013 · Cited by 85 · see citing works
Cao, J., Huang, M., Guo, L., Zhu, L., Hou, J., Zhang, L., Pero, A., Ng, S., Gaamouch, F. E., Elder, G. A., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0824-3 · Cited by 79 · see citing works
Brodbeck, J., Balestra, M. E., Saunders, A. M., Roses, A. D., Mahley, R. W., & Huang, Y. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709906104 · Cited by 86 · see citing works
Self-citationDefective neuronal sprouting by human apolipoprotein E4 is a gain-of-negative function.
Teter, B., Xu, P., Gilbert, J. R., Roses, A. D., Galasko, D., & Cole, G. M. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10221 · Cited by 74 · see citing works
Self-citationFrom degenerative disease to malignant tumors: Insight to the function of ApoE
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Horsburgh, K. J., McCulloch, J., Nilsen, M., Roses, A. D., & Nicoll, J. A. R. (2000) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2000.01339.x · Cited by 70 · see citing works
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Mortalin is regulated by APOE in hippocampus of AD patients and by human APOE in TR mice
Osorio, C., Sullivan, P. M., Dong, H., Mace, B. E., Ervin, J. F., Strittmatter, W. J., & Álzate, Ó. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.08.011 · Cited by 61 · see citing works
Gene-environment interaction of ApoE genotype and combat exposure on PTSD
Lyons, M. J., Genderson, M., Grant, M. D., Logue, M., Zink, T., McKenzie, R., Franz, C. E., Panizzon, M., Lohr, J. B., Jerskey, B., et al. (2013) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32154 · Cited by 60 · see citing works
ApoE-Dependent Plasticity in Alzheimer's Disease
Teter, B. (2004) · Journal of Molecular Neuroscience · doi:10.1385/jmn:23:3:167 · Cited by 56 · see citing works
Self-citationMolecular Insight into the Therapeutic Promise of TargetingAPOE4for Alzheimer’s Disease
Mamun, A. A., Uddin, M. S., Bashar, M. F. B., Zaman, S., Begum, Y., Bulbul, I. J., Islam, M. S., Sarwar, M. S., Mathew, B., Amran, M. S., et al. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/5086250 · Cited by 53 · see citing works
Cimarosti, H., & Henley, J. M. (2008) · The Neuroscientist · doi:10.1177/1073858408322677 · Cited by 52 · see citing works
Brain region‐specific up‐regulation of mouse apolipoprotein E by pharmacological estrogen treatments
Levin-Allerhand, J. A., McEwen, B. S., Lominska, C. E., Lubahn, D. B., Korach, K. S., & Smith, J. D. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00627.x · Cited by 52 · see citing works
Estradiol regulation of astroglia and apolipoprotein E: An important role in neuronal regeneration
Struble, R. G., Nathan, B. P., Cady, C., Cheng, X., & McAsey, M. E. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.05.013 · Cited by 51 · see citing works
Melemedjian, O. K., Yassine, H. N., Shy, A., & Price, T. J. (2013) · Molecular Pain · doi:10.1186/1744-8069-9-14 · Cited by 50 · see citing works
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Ophir, G., Meilin, S., Efrati, M., Chapman, J., Karussis, D., Roses, A. D., & Michaelson, D. M. (2003) · Neurobiology of Disease · doi:10.1016/s0969-9961(02)00005-0 · Cited by 48 · see citing works
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Raber, J. (2004) · Science of Aging Knowledge Environment · doi:10.1126/sageke.2004.11.re2 · Cited by 46 · see citing works
McAsey, M. E., Cady, C., Jackson, L. M., Li, M., Randall, S., Nathan, B. P., & Struble, R. G. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2005.09.008 · Cited by 45 · see citing works
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Self-citationScarmeas, N., Habeck, C. G., Anderson, K. E., Hilton, J., Devanand, D. P., Pelton, G. H., Tabert, M. H., Flynn, J., Park, A., Ciappa, A., et al. (2004) · American Journal of Geriatric Psychiatry · doi:10.1176/appi.ajgp.12.6.596 · Cited by 37 · see citing works
Blain, J., Sullivan, P. M., & Poirier, J. (2005) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.08.010 · Cited by 35 · see citing works
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Matsuo, M., Campenot, R. B., Vance, D. E., Ueda, K., & Vance, J. E. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2010.10.004 · Cited by 30 · see citing works
Delayed olfactory nerve regeneration in ApoE-deficient mice
Nathan, B. P., Nisar, R., Short, J. L., Randall, S., Grissom, E. M., Griffin, G., Switzer, P. V., & Struble, R. G. (2005) · Brain Research · doi:10.1016/j.brainres.2005.02.011 · Cited by 30 · see citing works
Caliban's heritance and the genetics of neuronal aging
Teter, B., & Finch, C. E. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.08.005 · Cited by 26 · see citing works
Self-citationApolipoprotein E, Alzheimer disease, and African Americans
Mayeux, R. (2003) · Archives of Neurology · doi:10.1001/archneur.60.2.161 · Cited by 26 · see citing works
Victorov, I. V., Lyjin, A. A., & Aleksandrova, O. P. (2001) · Brain Research Protocols · doi:10.1016/s1385-299x(00)00059-3 · Cited by 23 · see citing works
Levi, O., Dolev, I., Belinson, H., & Michaelson, D. M. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04810.x · Cited by 22 · see citing works
Lanterna, L. A., & Biroli, F. (2009) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2008.09.006 · Cited by 19 · see citing works
Increased Vulnerability to Focal Ischemic Brain Injury in Human Apolipoprotein E4 Knock‐In Mice
Mori, T., Kobayashi, M., Town, T., Fujita, S., & Asano, T. (2003) · Journal of Neuropathology and Experimental Neurology · doi:10.1093/jnen/62.3.280 · Cited by 21 · see citing works
Apolipoprotein E-Related Neurotoxicity as a Therapeutic Target for Alzheimer's Disease
Marques, M. A., & Crutcher, K. A. (2003) · Journal of Molecular Neuroscience · doi:10.1385/jmn:20:3:327 · Cited by 17 · see citing works
Reconstitution of the olfactory epithelium following injury in ApoE-deficient mice
Nathan, B. P., Gairhe, S., Nwosu, I. C., Clark, S. J., & Struble, R. G. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.08.001 · Cited by 16 · see citing works
Patel, N. V., Wei, M., Wong, A., Finch, C. E., & Morgan, T. E. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.08.076 · Cited by 13 · see citing works
Zhou, R., Chen, H., Ye, F., Huang, S., & Zhang, J. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00085 · Cited by 10 · see citing works
Glucocorticoids and the Aging Brain: Cause or Consequence?
Lucassen, P. J., & de Kloet, E. R. (2001) · Elsevier eBooks · doi:10.1016/b978-012351830-9/50064-0 · Cited by 10 · see citing works
Dietary fat up-regulates the apolipoprotein E mRNA level in the Zucker lean rat brain
Knight, D. S., Mahajan, D. K., & Qiao, X. (2001) · Neuroreport · doi:10.1097/00001756-200110080-00026 · Cited by 9 · see citing works
Nontraditional Signaling Mechanisms of Lipoprotein Receptors
Rebeck, G. W. (2009) · Science Signaling · doi:10.1126/scisignal.268pe28 · Cited by 8 · see citing works
Apolipoprotein E influences neuronal death and repair
Horsburgh, K. J., McColl, B. W., White, F., & McCulloch, J. (2003) · International Congress Series · doi:10.1016/s0531-5131(03)00024-4 · Cited by 6 · see citing works
Life-span influences of apoE4 on CNS function
Teter, B. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.06.028 · Cited by 6 · see citing works
Self-citationApolipoprotein E polymorphism and dendritic shape in hippocampal interneurons
Schönheit, B., Glöckner, F., & Ohm, T. G. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.03.016 · Cited by 6 · see citing works
Altered lipid metabolic homeostasis in the pathogenesis of Alzheimer’s disease
Marian, O. C., Tran, C. L., & Don, A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-819404-1.00023-3 · Cited by 2 · see citing works
The Pathogenesis of Alzheimer’s Disease: General Overview
Apostolova, L. G., & Cummings, J. L. (2007) · Springer eBooks · doi:10.1007/978-0-387-36534-3_1 · Cited by 5 · see citing works
The Effects of Breast Milk Versus Infant Formulae on Cognitive Development
Yum, J. (2014) · Cited by 4 · see citing works
Electrophysiological Monitoring of Hippocampal Slice Cultures Using MEA on Porous Membrane
Hakkoum, D., Müller, D., & Stoppini, L. (2006) · Springer eBooks · doi:10.1007/0-387-25858-2_5 · Cited by 3 · see citing works
Imaging studies and APOE genotype in persons at risk for Alzheimer’s disease
Scarmeas, N., & Stern, Y. (1996) · Current Psychiatry Reports · doi:10.1007/s11920-996-0057-4 · Cited by 3 · see citing works
Alexander, S. A. (2004) · D-Scholarship@Pitt (University of Pittsburgh)
at college age APOE related alterations in cerebral activation even
Scarmeas, N., Habeck, C. G., Hilton, J., Anderson, K. E., Flynn, J., & Stern, Y. (2005)
Kerr, M. E., DeKosky, S. T., Kay, A., & Marion, D. W. (2001) · Springer eBooks · doi:10.1007/978-1-4615-1721-4_15
Elmassry, H., Nagy, N., Shorab, I., & Eid, M. (2015) · Activitas Nervosa Superior · doi:10.1007/bf03379625
Mondadori, C. R. A. (2006) · Zurich Open Repository and Archive (University of Zurich) · doi:10.5167/uzh-163345
Jasien, J., Stout, J. A., Mikati, M. A., Anderson, R. J., Nave, B., Fuchs, H. E., Smith, B., Badea, A., & Browndyke, J. N. (2025) · Annals of the Child Neurology Society · doi:10.1002/cns3.70016
Cole (2000) · doi:10.1002/1097-0029(20000815)50:4
- Authors
- Teter, B., Xu, P. ‐., Gilbert, J. R., Roses, A. D., Galasko, D., & Cole, G. M.
- Affiliations
- United States Department of Veterans Affairs (US)
- Duke University (US)
- GlaxoSmithKline (United Kingdom) (GB)
- University of California San Diego (US)
- University of California, Los Angeles (US)
- Corresponding author
- Teter, B.
- Venue
- Journal of Neurochemistry
- Publisher
- Wiley
- Published
- 1999-12
- Volume
- 73
- Issue
- 6
- Pages
- 2613-2616
- ISSN
- 0022-3042 (ISSN-L)
- 1471-4159
- OpenAlex
- W2088347760
- Cited by
- 88
- References
- 36
- Citations by year
- 2025: 2 · 2022: 2 · 2020: 5 · 2017: 1 · 2015: 1 · 2014: 3 · 2013: 5 · 2012: 1
- FWCI
- 3.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurochemistry (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (AG-10415, K01AG000962, P60AG010415)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Keywords
- apolipoprotein E, APOE isoforms, APOE ε4, APOE3, mossy fiber sprouting, neuronal regeneration, organotypic hippocampal slice cultures, dentate gyrus, Alzheimer's disease risk, nerve regeneration, conditioned medium
- MeSH terms
- Alzheimer Disease, Animals, Apolipoproteins E, Hippocampus, Humans, Mice, Inbred C57BL, Mice, Transgenic, Nerve Degeneration, Nerve Tissue Proteins, Organ Culture Techniques, Recombinant Fusion Proteins, Culture Media, Conditioned, Mossy Fibers, Hippocampal, Protein Isoforms, Mice, Apolipoprotein E3, Apolipoprotein E4
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