Reeler/Disabled-like Disruption of Neuronal Migration in Knockout Mice Lacking the VLDL Receptor and ApoE Receptor 2
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Layering of neurons in the cerebral cortex and cerebellum requires Reelin, an extracellular matrix protein, and mammalian Disabled (mDab1), a cytosolic protein that activates tyrosine kinases. Here, we report the requirement for two other proteins, cell surface receptors termed very low density lipoprotein receptor (VLDLR) and apolipoprotein E receptor 2 (ApoER2). Both receptors can bind mDab1 on their cytoplasmic tails and are expressed in cortical and cerebellar layers adjacent to layers that express Reelin. mDab1 expression is upregulated in knockout mice that lack both VLDLR and ApoER2. Inversion of cortical layers and absence of cerebellar foliation in these animals precisely mimic the phenotype of mice lacking Reelin or mDab1. These findings suggest that VLDLR and ApoER2 participate in transmitting the extracellular Reelin signal to intracellular signaling processes initiated by mDab1.
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VLDLR and APOER2 mediate Reelin signaling, which is essential for neuronal migration during brain development.
“VLDLR and APOER2 mediate Reelin signaling, which is essential for neuronal migration during brain development.”
From Deletion of neuronal <i>Idol</i> ameliorates Alzheimer's disease–related pathologies via APOE receptors (2025) · cites this paper as [77]
Several non-apolipoprotein ligands have been proposed for VLDLR, including Reelin and F-spondin.
“Several non-apolipoprotein ligands have also been proposed for VLDLR, including Reelin2 and F-spondin55.”
From IDOL regulates systemic energy balance through control of neuronal VLDLR expression (2019) · cites this paper as [2]
Reelin interaction with the VLDLR and ApoER2 is critical during development because it properly directs the positioning of neurons.
“Reelin interaction with the VLDLR and ApoER2 is critical during development because it properly directs the positioning of neurons (16, 20, 21).”
From The E3 ubiquitin ligase IDOL induces the degradation of the low density lipoprotein receptor family members VLDLR and ApoER2 (2010) · cites this paper as [16]
The VLDLR and ApoER2 are critical for neuronal migration during development.
“In addition to their proposed roles in metabolism, the VLDLR and ApoER2 are critical for neuronal migration during development (16, 20, 21).”
From The E3 ubiquitin ligase IDOL induces the degradation of the low density lipoprotein receptor family members VLDLR and ApoER2 (2010) · cites this paper as [16]
VLDLR and ApoER2 have a critical role in the neuronal Reelin pathway essential for proper neuronal positioning and brain development.
“studies in recent years have established a critical role for VLDLR and ApoER2 in the neuronal Reelin pathway that is essential for proper neuronal positioning and brain development (16–19).”
From The E3 ubiquitin ligase IDOL induces the degradation of the low density lipoprotein receptor family members VLDLR and ApoER2 (2010) · cites this paper as [16]
Only the combined loss of both VLDLR and ApoER2 results in severely impaired neuronal positioning.
“Because only the combined loss of both receptors results in severely impaired neuronal positioning (16), the ability of IDOL to simultaneously target both receptors for degradation may allow it to modulate this pathway.”
From The E3 ubiquitin ligase IDOL induces the degradation of the low density lipoprotein receptor family members VLDLR and ApoER2 (2010) · cites this paper as [16]
The knockdown of both VLDLR and ApoER2 causes a Reeler-phenotype in mice, resulting in neuronal lamination defects in both cortex and cerebellum.
“The knockdown of both VLDLR and ApoER2 cause a Reeler-phenotype in mice, resulting in neuronal lamination defects in both the cortex and cerebellum [13].”
From PCSK9 regulates neuronal apoptosis by adjusting ApoER2 levels and signaling (2012) · cites this paper as [13]
Reelin and ApoE bind to and activate ApoER2 and VLDLR.
“Reelin and ApoE bind to and activate ApoER2 and VLDLR, controlling cortical and cerebellar development [13,14], promoting cell survival [15], and regulating N-methyl-D-aspartic acid (NMDA) receptor activity through phosphorylation [16,17].”
From PCSK9 regulates neuronal apoptosis by adjusting ApoER2 levels and signaling (2012) · cites this paper as [13]
ApoER2 contains a multifunctional NPxY motif responsible for its signaling, endocytosis, and interaction with several adaptor proteins.
“Similar to other members of the LDL-R family, ApoER2 contains a multifunctional NPxY motif, which is responsible for its signaling [4], [11], endocytosis [24] and also the role of facilitating the interaction with several adaptor proteins [54], [55].”
From Sorting nexin 17 regulates ApoER2 recycling and reelin signaling (2014) · cites this paper as [4]
ApoER2 binds reelin during development, triggering a signaling pathway that regulates neuronal migration and the formation of laminated brain structures such as the cortex, hippocampus and cerebellum.
“ApoER2 binds the extracellular matrix protein reelin during development [4], [6], triggering a signaling pathway that regulates neuronal migration and the formation of laminated brain structures such as the cortex, hippocampus [7] and cerebellum [4]”
From Sorting nexin 17 regulates ApoER2 recycling and reelin signaling (2014) · cites this paper as [4]
Reelin controls neuronal migration and positioning by stimulating tyrosine phosphorylation of Dab1 via VLDLR, ApoER2, and CNR family proteins.
“These results suggest that Reelin controls neuronal migration and positioning by stimulating tyrosine phosphorylation of Dab1 via VLDLR, ApoER2, and CNR family proteins.”
From Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody (2000) · cites this paper as [34]
Lrp8-null mice show ectopic Purkinje cells similar to the Rbfox2-null mice.
“Consistently, Lrp8-null mice show ectopic Purkinje cells similar to the Rbfox2-null mice59,60.”
From The neurogenetics of alternative splicing (2016) · cites this paper as [59]
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LRP8-Reelin-regulated neuronal enhancer signature underlying learning and memory formation
Telese, F., Ma, Q., Perez, P. M., Notani, D., Oh, S., Li, W., Comoletti, D., Ohgi, K. A., Taylor, H., & Rosenfeld, M. G. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.033 · Cited by 166 · see citing works
DAB1 and Reelin effects on amyloid precursor protein and ApoE receptor 2 trafficking and processing
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Regulation of Protein Tyrosine Kinase Signaling by Substrate Degradation during Brain Development
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More than cholesterol transporters: lipoprotein receptors in CNS function and neurodegeneration
Lane-Donovan, C., Philips, G. T., & Herz, J. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.005 · Cited by 158 · see citing works
Self-citationDeletion of Macrophage LDL Receptor–Related Protein Increases Atherogenesis in the Mouse
Overton, C. D., Yancey, P. G., Major, A. S., Linton, M. F., & Fazio, S. (2007) · Circulation Research · doi:10.1161/01.res.0000260204.40510.aa · Cited by 159 · see citing works
Role for Reelin in stabilizing cortical architecture
Frotscher, M. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.06.001 · Cited by 157 · see citing works
Reelin Is a Serine Protease of the Extracellular Matrix
Quattrocchi, C. C., Wannenes, F., Persico, A. M., Ciafré, S. A., D'Arcangelo, G., Farace, M. G., & Keller, F. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m106996200 · Cited by 154 · see citing works
Reelin signaling antagonizes β-amyloid at the synapse
Durakoglugil, M. S., Chen, Y., White, C. L., Kavalali, E. T., & Herz, J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908176106 · Cited by 153 · see citing works
Self-citationLayer acquisition by cortical GABAergic interneurons is independent of Reelin signaling
Pla, R., Borrell, V., Flames, N., & Marín, O. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0245-06.2006 · Cited by 151 · see citing works
New insights into Reelin-mediated signaling pathways
Lee, G. H., & D’Arcangelo, G. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00122 · Cited by 144 · see citing works
Cullin 5 regulates Dab1 protein levels and neuron positioning during cortical development
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Differential glycosylation regulates processing of lipoprotein receptors by γ-secretase
May, P., Bock, H. H., Nimpf, J., & Herz, J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m305858200 · Cited by 142 · see citing works
Self-citationAbnormal development of the apical ectodermal ridge and polysyndactyly in Megf7-deficient mice
Johnson, E. B., Hammer, R. E., & Herz, J. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi381 · Cited by 141 · see citing works
Self-citationHong, C., Duit, S., Jalonen, P., Out, R., Scheer, L., Sorrentino, V., Boyadjian, R., Rodenburg, K. W., Foley, E., Korhonen, L., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.123729 · Cited by 142 · see citing works
Self-citationGrehan, S., Tse, E., & Taylor, J. M. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-03-00812.2001 · Cited by 138 · see citing works
PCSK9 regulates neuronal apoptosis by adjusting ApoER2 levels and signaling
Kysenius, K., Muggalla, P., Mätlik, K., Arumäe, U., & Huttunen, H. J. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-0977-6 · Cited by 137 · see citing works
Feedback Regulation of Cholesterol Uptake by the LXR–IDOL–LDLR Axis
Zhang, L., Reue, K., Fong, L. G., Young, S. G., & Tontonoz, P. (2012) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.112.250571 · Cited by 137 · see citing works
Bal, M., Leitz, J., Reese, A. L., Ramirez, D. M. O., Durakoglugil, M., Herz, J., Monteggia, L. M., & Kavalali, E. T. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.024 · Cited by 131 · see citing works
Self-citationUtsunomiya-Tate, N., Kubo, K.-I., Tate, S.-I., Kainosho, M., Katayama, E., Nakajima, K., & Mikoshiba, K. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.160272497 · Cited by 131 · see citing works
Sinagra, M., Verrier, D., Frankova, D., Korwek, K. M., Blahos, J., Weeber, E. J., Manzoni, O. J., & Chavis, P. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1757-05.2005 · Cited by 128 · see citing works
Emerging topics in Reelin function
Förster, E., Bock, H. H., Herz, J., Chai, X., Frotscher, M., & Zhao, S. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07222.x · Cited by 130 · see citing works
Self-citationDorrell, M. I., Aguilar, E., Jacobson, R., Yanes, O., Gariano, R., Heckenlively, J., Banin, E., Ramirez, G. A., Gasmi, M., Bird, A., et al. (2009) · Journal of Clinical Investigation · doi:10.1172/jci35977 · Cited by 127 · see citing works
Reduced Blood Levels of Reelin as a Vulnerability Factor in Pathophysiology of Autistic Disorder
Fatemi, S. H., Stary, J. M., & Egan, E. A. (2002) · Cellular and Molecular Neurobiology · doi:10.1023/a:1019857620251 · Cited by 122 · see citing works
Reelin in the years: controlling neuronal migration and maturation in the mammalian brain
D'Arcangelo, G. (2014) · Advances in Neuroscience · doi:10.1155/2014/597395 · Cited by 120 · see citing works
Functional Roles of the Interaction of APP and Lipoprotein Receptors
Pohlkamp, T., Wasser, C. R., & Herz, J. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00054 · Cited by 92 · see citing works
Self-citationCanonical and non-canonical Reelin signaling
Bock, H. H., & May, P. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00166 · Cited by 107 · see citing works
Alzheimer disease pathology in cognitively healthy elderly: A genome-wide study
Kramer, P. L., Xu, H., Woltjer, R. L., Westaway, S. K., Clark, D., Erten-Lyons, D., Kaye, J. A., Welsh-Bohmer, K. A., Troncoso, J. C., Markesbery, W. R., et al. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.01.010 · Cited by 108 · see citing works
Bock, H. H., Jossin, Y., May, P., Bergner, O., & Herz, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m401770200 · Cited by 102 · see citing works
Self-citationReversal of ApoE4-induced recycling block as a novel prevention approach for Alzheimer’s disease
Xian, X., Pohlkamp, T., Durakoglugil, M. S., Wong, C. H., Beck, J. K., Lane-Donovan, C., Plattner, F., & Herz, J. (2018) · eLife · doi:10.7554/elife.40048 · Cited by 98 · see citing works
Self-citationReelin deficiency causes granule cell dispersion in epilepsy
Haas, C. A., & Frotscher, M. (2010) · Experimental Brain Research · doi:10.1007/s00221-009-1948-5 · Cited by 96 · see citing works
Reelin depletion is an early phenomenon of Alzheimer's pathology
Herring, A., Donath, A., Steiner, K. M., Widera, M. P., Hamzehian, S., Kanakis, D., Kölble, K., ElAli, A., Hermann, D. M., Paulus, W., et al. (2012) · Journal of Alzheimer's Disease · doi:10.3233/jad-2012-112069 · Cited by 92 · see citing works
Reelin protects against amyloid β toxicity in vivo
Lane-Donovan, C., Philips, G. T., Wasser, C. R., Durakoglugil, M. S., Masiulis, I., Upadhaya, A., Pohlkamp, T., Coskun, C., Kotti, T., Steller, L., et al. (2015) · Science Signaling · doi:10.1126/scisignal.aaa6674 · Cited by 96 · see citing works
Self-citationAge-related accumulation of Reelin in amyloid-like deposits
Knuesel, I., Nyffeler, M., Mormède, C., Muhia, M., Meyer, U., Pietropaolo, S., Yee, B. K., Pryce, C. R., LaFerla, F. M., Marighetto, A., et al. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.08.011 · Cited by 94 · see citing works
Reduction of Crk and CrkL expression blocks reelin-induced dendritogenesis
Matsuki, T., Pramatarova, A., & Howell, B. W. (2008) · Journal of Cell Science · doi:10.1242/jcs.027334 · Cited by 92 · see citing works
Nakajima, C., Kulik, A., Frotscher, M., Herz, J., Schäfer, M., Bock, H. H., & May, P. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.444364 · Cited by 85 · see citing works
Self-citationReelin-mediated signaling in neuropsychiatric and neurodegenerative diseases
Knuesel, I. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.04.002 · Cited by 89 · see citing works
ApoE isoform-dependent changes in hippocampal synaptic function
Korwek, K. M., Trotter, J. H., LaDu, M. J., Sullivan, P. M., & Weeber, E. J. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-21 · Cited by 89 · see citing works
Unique Requirement for Rb/E2F3 in Neuronal Migration: Evidence for Cell Cycle-Independent Functions
McClellan, K. A., Ruzhynsky, V. A., Douda, D. N., Vanderluit, J. L., Ferguson, K. L., Chen, D., Bremner, R., Park, D. S., Leone, G., & Slack, R. S. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02100-06 · Cited by 88 · see citing works
Leemhuis, J., Bouché, E., Frotscher, M., Henle, F., Hein, L., Herz, J., Meyer, D. K., Pichler, M., Roth, G., Schwan, C., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4036-10.2010 · Cited by 80 · see citing works
Self-citationKoch, S., Strasser, V., Hauser, C., Fasching, D., Brandes, C., Bajari, T. M., Schneider, W. J., & Nimpf, J. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf599 · Cited by 80 · see citing works
Self-citationRole for Reelin in neurotransmitter release
Hellwig, S., Hack, I., Kowalski, J., Brunne, B., Jarowyj, J., Unger, A., Bock, H. H., Junghans, D., & Frotscher, M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3984-10.2011 · Cited by 74 · see citing works
Choi, H. Y., Liu, Y., Tennert, C., Sugiura, Y., Karakatsani, A., Kröger, S., Johnson, E. B., Hammer, R. E., Lin, W., & Herz, J. (2013) · eLife · doi:10.7554/elife.00220 · Cited by 71 · see citing works
Self-citationDuit, S., Mayer, H., Blake, S. M., Schneider, W. J., & Nimpf, J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.025973 · Cited by 71 · see citing works
Self-citationDing, Y., Huang, L., Xian, X., Yuhanna, I. S., Wasser, C. R., Frotscher, M., Mineo, C., Shaul, P. W., & Herz, J. (2016) · Science Signaling · doi:10.1126/scisignal.aad5578 · Cited by 72 · see citing works
Self-citationFuentealba, R. A., Barría, M. I., Lee, J., Cam, J., Araya, C., Escudero, C. A., Inestrosa, N. C., Bronfman, F. C., Bu, G., & Marzolo, M.-P. (2007) · Molecular Neurodegeneration · doi:10.1186/1750-1326-2-14 · Cited by 70 · see citing works
The generation and function of soluble apoE receptors in the CNS
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Tinnes, S., Schäfer, M. K. E., Flubacher, A., Münzner, G., Frotscher, M., & Haas, C. A. (2011) · The FASEB Journal · doi:10.1096/fj.10-168294 · Cited by 58 · see citing works
Differential splicing and glycosylation of Apoer2 alters synaptic plasticity and fear learning
Wasser, C. R., Masiulis, I., Durakoglugil, M. S., Lane-Donovan, C., Xian, X., Beffert, U., Agarwala, A., Hammer, R. E., & Herz, J. (2014) · Science Signaling · doi:10.1126/scisignal.2005438 · Cited by 48 · see citing works
Self-citationApoE receptor 2 regulates synapse and dendritic spine formation
Dumanis, S. B., Cha, H.-J., Song, J. M., Trotter, J. H., Spitzer, M., Lee, J.-Y., Weeber, E. J., Turner, R. S., Pak, D. T. S., Rebeck, G. W., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017203 · Cited by 45 · see citing works
Differential gene expression in migratory streams of cortical interneurons
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Zolochevska, O., & Taglialatela, G. (2016) · Current Pharmaceutical Design · doi:10.2174/1381612822666160518142110 · Cited by 49 · see citing works
Larouche, M., Beffert, U., Herz, J., & Hawkes, R. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001653 · Cited by 49 · see citing works
Self-citationSorting nexin 17 regulates ApoER2 recycling and reelin signaling
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Apolipoprotein E decreases tau kinases and phospho-tau levels in primary neurons.
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ApoER2 processing by presenilin-1 modulates reelin expression
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Self-citationSelective expression of <i>LDLR</i> and <i>VLDLR</i> in myelinating oligodendrocytes
Zhao, S., Hu, X., Park, J., Zhu, Y., Zhu, Q., Li, H., Luo, C., Han, R., Cooper, N., & Qiu, M. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21283 · Cited by 39 · see citing works
Brosda, J., Dietz, F., & Koch, M. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.07.008 · Cited by 37 · see citing works
Reelin proteolysis affects signaling related to normal synapse function and neurodegeneration
Lussier, A. L., Weeber, E. J., & Rebeck, G. W. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00075 · Cited by 31 · see citing works
Lrp4 domains differentially regulate limb/brain development and synaptic plasticity
Pohlkamp, T., Durakoglugil, M., Lane-Donovan, C., Xian, X., Johnson, E. B., Hammer, R. E., & Herz, J. (2015) · PLOS ONE · doi:10.1371/journal.pone.0116701 · Cited by 28 · see citing works
Self-citationMinami, S. S., Sung, Y. M., Dumanis, S. B., Chi, S. H., Burns, M. P., Ann, E.-J., Suzuki, T., Turner, R. S., Park, H.-S., Pak, D. T. S., et al. (2010) · The FASEB Journal · doi:10.1096/fj.09-138123 · Cited by 28 · see citing works
- Authors
- Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., Hammer, R. E., Richardson, J. A., & Herz, J.
- Affiliations
- The University of Texas Southwestern Medical Center (US)
- University of Vienna (AT)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Herz, Joachim
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 1999-06
- Volume
- 97
- Issue
- 6
- Pages
- 689-701
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2079396188
- Cited by
- 1,261
- References
- 44
- Citations by year
- 2026: 8 · 2025: 28 · 2024: 16 · 2023: 24 · 2022: 23 · 2021: 32 · 2020: 30 · 2019: 27 · 2018: 30 · 2017: 49 · 2016: 42 · 2015: 32 · 2014: 38 · 2013: 47 · 2012: 57
- FWCI
- 27.71
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- Funders
- National Institute on Aging (P30AG012300, AG 12300)
- National Heart, Lung, and Blood Institute (HL-20948, R37HL063762, P01HL020948)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- reelin, VLDL receptor, neuronal migration, cortical lamination, cerebellar foliation, Reelin signaling, knockout mice, extracellular matrix, tyrosine kinase signaling
- MeSH terms
- Reelin Protein, Amino Acid Sequence, Animals, Cell Line, Cell Movement, Cerebral Cortex, Dendrites, Female, Mice, Mutant Strains, Molecular Sequence Data, Nerve Tissue Proteins, Purkinje Cells, Receptors, LDL, Recombinant Fusion Proteins, Serine Endopeptidases, Cell Adhesion Molecules, Neuronal, Up-Regulation, Extracellular Matrix Proteins, Receptors, Lipoprotein, Mice, Knockout, LDL-Receptor Related Proteins, Mice
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