Interaction of reelin signaling and Lis1 in brain development

Assadi, Amir H.; Zhang, Guangcheng; Beffert, Uwe; McNeil, Robert S.; Renfro, Amy; Niu, Sanyong; Quattrocchi, Carlo Cosimo; Antalffy, Barbara; Sheldon, Michael; Armstrong, Dawna; Wynshaw‐Boris, Anthony; Herz, Joachim; D’Arcangelo, Gabriella; Clark, Gary D.

doi:10.1038/ng1257

Cited by 195 publications

(163 citation statements)

References 30 publications

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“…It has been well established that reelin-induced signaling through apoER2 and VLDLR, the intracellular adaptor protein Dab1, and Src family protein tyrosine kinases is critical in embryonic brain development (D'Arcangelo et al, 1995;Goffinet, 1995;Howell et al, 1997Howell et al, , 1999aBock and Herz, 2003;Kuo et al, 2005). Recent studies have shown that this system also interacts intracellularly with an array of signaling pathways involving cdk5 (cyclin-dependent kinase 5), JIP (c-Jun N-terminal kinase-interacting protein), PI3K, PKB, GSK-3␤ (glycogen synthase kinase-3␤), Lis-1 (lissencephaly 1), and CrK family adaptor proteins Arnaud et al, 2003;Assadi et al, 2003;Bock and Herz, 2003;Ballif et al, 2004), suggesting that reelin may be involved in multiple aspects of neuronal development and physiology. Moreover, reelin-lipoprotein receptor-mediated signaling also plays an important role in neuronal maturation, synaptic plasticity, and memory formation (Nimpf and Schneider, 2000;Weeber et al, 2002;Beffert et al, 2005;D'Arcangelo, 2005).…”

Section: Discussionmentioning

confidence: 99%

Differential Reelin-Induced Enhancement of NMDA and AMPA Receptor Activity in the Adult Hippocampus

Qiu¹,

Zhao²,

Korwek³

et al. 2006

J. Neurosci.

159

161

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The developmental lamination of the hippocampus and other cortical structures requires a signaling cascade initiated by reelin and its receptors, apoER2 (apolipoprotein E receptor 2) and VLDLR (very-low-density lipoprotein receptor). However, the functional significance of continued reelin expression in the postnatal brain remains poorly understood. Here, we show that reelin application to adult mice hippocampal slices leads to enhanced glutamatergic transmission mediated by NMDA receptors (NMDARs) and AMPA receptors (AMPARs) through distinct mechanisms. Application of recombinant reelin enhanced NMDAR-mediated currents through postsynaptic mechanisms, as revealed by the variance-mean analysis of synaptic NMDAR currents, assessment of spontaneous miniature events, and the levels of NMDAR subunits at synaptic surface. In comparison, nonstationary fluctuation analysis of miniature AMPAR currents and quantification of synaptic surface proteins revealed that reelin-induced enhancement of AMPAR responses was mediated by increased AMPAR numbers. Reelin enhancement of synaptic NMDAR currents was abolished when receptor-associated protein (RAP) or the Src inhibitor 4-amino-5-(4-methylphenyl)-7-(t-butyl)pyrazolo[3,4-d]-pyrimidine (PP1) was bath applied and was abrogated by includingPP1 in the recording electrodes. In comparison, including RAP or an inactive PP1 analog PP3 in the recording electrode was without effect. Interestingly, the increased AMPAR response after reelin application was not blocked by PP1 but was blocked by the phosphoinositide-3Ј kinase (PI3K) inhibitors wortmannin and LY294002 [2-(4-morpholinyl)-8-phenyl-1(4H)-benzopyran-4-one hydrochloride]. Furthermore, reelin-induced, PI3K-dependent AMPAR surface insertion was also observed in cultured hippocampal neurons. Together, these results reveal a differential functional coupling of reelin signaling with NMDAR and AMPAR function and define a novel mechanism for controlling synaptic strength and plasticity in the adult hippocampus.

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Section: Discussionmentioning

confidence: 99%

Differential Reelin-Induced Enhancement of NMDA and AMPA Receptor Activity in the Adult Hippocampus

Qiu¹,

Zhao²,

Korwek³

et al. 2006

J. Neurosci.

159

161

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“…Other potential mechanisms by which ApoE receptors may promote neuronal survival (Beffert et al 2006b) during aging involve signaling pathways that control microtubule and actin dynamics Assadi et al 2003;Brich et al 2003;Ohkubo et al 2003;Chai et al 2009;Forster et al 2010;Rust et al 2010), dendritogenesis (Niu et al 2004), spine formation (Niu et al 2008), glutamate receptor function and synaptic plasticity (Zhuo et al 2000;Weeber et al 2002;Beffert et al 2005;Chen et al 2005;D'Arcangelo 2005;Sinagra et al 2005;Groc et al 2007;Durakoglugil et al 2009;Korwek et al 2009;Chen et al 2010), as well as learning and memory (reviewed in Herz and Beffert 2000;Herz and Chen 2006;Bu 2009;Herz 2009). In this section we will mainly focus on the role of the ApoE receptors Apoer2 and Vldlr and their ligand Reelin in these processes.…”

Section: Apoe Receptors and Synaptic Plasticitymentioning

confidence: 99%

Apolipoprotein E and Apolipoprotein E Receptors: Normal Biology and Roles in Alzheimer Disease

Holtzman

Herz²,

2012

Cold Spring Harbor Perspectives in Medicine

661

602

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“…Third, Dab1 interacts with Lis1, a protein implicated in the human brain developmental disorder lissencephaly. This interaction depends on the tyrosine phosphorylation of Dab1 (Assadi et al 2003). Furthermore, Lis1 mutations associated with severe phenotypes in humans disrupt the Lis1-Dab1 interaction.…”

Section: Guiding Neuronal Cell Migrationsmentioning

confidence: 99%

Guiding Neuronal Cell Migrations

Marı́n¹,

Valiente²,

Ge³

et al. 2010

Cold Spring Harbor Perspectives in Biology

359

351

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Neuronal migration is, along with axon guidance, one of the fundamental mechanisms underlying the wiring of the brain. As other organs, the nervous system has acquired the ability to grow both in size and complexity by using migration as a strategy to position cell types from different origins into specific coordinates, allowing for the generation of brain circuitries. Guidance of migrating neurons shares many features with axon guidance, from the use of substrates to the specific cues regulating chemotaxis. There are, however, important differences in the cell biology of these two processes. The most evident case is nucleokinesis, which is an essential component of migration that needs to be integrated within the guidance of the cell. Perhaps more surprisingly, the cellular mechanisms underlying the response of the leading process of migrating cells to guidance cues might be different to those involved in growth cone steering, at least for some neuronal populations.

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Interaction of reelin signaling and Lis1 in brain development

Cited by 195 publications

References 30 publications

Differential Reelin-Induced Enhancement of NMDA and AMPA Receptor Activity in the Adult Hippocampus

Differential Reelin-Induced Enhancement of NMDA and AMPA Receptor Activity in the Adult Hippocampus

Apolipoprotein E and Apolipoprotein E Receptors: Normal Biology and Roles in Alzheimer Disease

Guiding Neuronal Cell Migrations

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