Motifs that mediate dendritic targeting in hippocampal neurons: A comparison with basolateral targeting signals

Silverman, Michael; Peck, Robert K.; Glover, Greta; He, Congcong; Carlin, C.; Banker, Gary

doi:10.1016/j.mcn.2005.02.008

Cited by 29 publications

(26 citation statements)

References 44 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This suggests that neurons cannot handle recessive apical information contained in these proteins. There is also evidence suggesting that neurons do not recognize dihydrophobic-based basolateral sorting signals (Silverman et al, 2005). However, the sorting behavior of wild type and all our mutant receptors expressed in hippocampal neurons show striking congruency with the sorting correspondence hypothesis.…”

Section: Discussionmentioning

confidence: 61%

“…However, there are also examples that do not fit into this pattern. For example, there is evidence suggesting that neurons cannot interpret dihydrophobic sorting signals as epithelial cells do (Silverman et al, 2005). Interestingly, even though neurons do not express AP1B , they still direct proteins to dendrites, such as the TfR (Bradke and Dotti, 1998), LDLR (Jareb and Banker, 1998), and LDLR-related protein 1 (LRP1; Brown et al, 1997), whose basolateral distribution in epithelial cells is AP1B-dependent (Folsch et al, 1999;Gan et al, 2002;Marzolo et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

“…All these aspects are less known in neurons, even though they are considered to share elements of the sorting machinery with epithelial cells (Horton and Ehlers, 2003;Silverman et al, 2005). There are several examples of apical and basolateral proteins handled, respectively, as axonal and somatodendritic proteins in neurons, and vice versa in epithelial cells (Dotti and Simons, 1990;Dotti et al, 1991;Pietrini et al, 1994;Bradke and Dotti, 1998).…”

Section: Introductionmentioning

confidence: 99%

“…Because the nonpolarized distribution of the endocytosis mutants is similar to the distribution of LRP1 in cells lacking 1B (Marzolo et al, 2003), the most plausible model is that Y 63 ATL and LL 86,87 motifs contribute to AP1B-dependent basolateral sorting of LRP1 in CRE compartment, both during post-TGN biosynthetic trafficking and post-SNX17 recycling trafficking. This model implies that AP1B and SNX17 sort LRP1 at different stations of its endocytic recycling itinerary recognizing distinct sorting motifs (see proposed model in Figure 14).A matter still under scrutiny and debate is the proposed correspondence between basolateral/apical sorting in epithelial cells and somatodendritic/axonal sorting in neurons (Dotti and Simons, 1990;Silverman et al, 2005). It could be dependent on the specific type of sorting signals possessed by individual proteins.…”

mentioning

confidence: 97%

“…AP1B has been localized in TfR-containing recycling endosomes as part of the sorting machinery operating in post-TGN biosynthetic and recycling pathways (Cancino et al, 2007;Gravotta et al, 2007). It is necessary to extend the analysis of the sorting signals that could operate at the TGN and/or endosomes and to search for additional decoding elements that might be involved in distinct endocytic compartments.All these aspects are less known in neurons, even though they are considered to share elements of the sorting machinery with epithelial cells (Horton and Ehlers, 2003;Silverman et al, 2005). There are several examples of apical and basolateral proteins handled, respectively, as axonal and somatodendritic proteins in neurons, and vice versa in epithelial cells (Dotti and Simons, 1990;Dotti et al, 1991;Pietrini et al, 1994;Bradke and Dotti, 1998).…”

mentioning

confidence: 99%

See 4 more Smart Citations

Polarized Traffic of LRP1 Involves AP1B and SNX17 Operating on Y-dependent Sorting Motifs in Different Pathways

Donoso

Cancino

Lee

et al. 2009

MBoC

View full text Add to dashboard Cite

Low-density lipoprotein receptor-related protein 1 (LRP1) is an endocytic recycling receptor with two cytoplasmic tyrosine-based basolateral sorting signals. Here we show that during biosynthetic trafficking LRP1 uses AP1B adaptor complex to move from a post-TGN recycling endosome (RE) to the basolateral membrane. Then it recycles basolaterally from the basolateral sorting endosome (BSE) involving recognition by sorting nexin 17 (SNX17).In the biosynthetic pathway, Y 29 but not N 26 from a proximal NPXY directs LRP1 basolateral sorting from the TGN. A N 26 A mutant revealed that this NPXY motif recognized by SNX17 is required for the receptor's exit from BSE. An endocytic Y 63 ATL 66 motif also functions in basolateral recycling, in concert with an additional endocytic motif (LL 86,87 ), by preventing LRP1 entry into the transcytotic apical pathway. All this sorting information operates similarly in hippocampal neurons to mediate LRP1 somatodendritic distribution regardless of the absence of AP1B in neurons. LRP1 basolateral distribution results then from spatially and temporally segregation steps mediated by recognition of distinct tyrosine-based motifs. We also demonstrate a novel function of SNX17 in basolateral/somatodendritic recycling from a different compartment than AP1B endosomes. INTRODUCTIONEpithelial cells posses functional, morphological, and biochemically distinct apical and basolateral cell surface domains and maintain this polarized phenotype addressing specific plasma membrane proteins into each domain (Yeaman et al., 1999;Mostov, 2003;Rodriguez-Boulan et al., 2005). Apical and basolateral proteins are sorted in the biosynthetic route at the level of the trans-Golgi network (TGN; Rindler et al., 1984;Fuller et al., 1985;Griffiths and Simons, 1986), and those proteins that undergo endocytosis can be additionally sorted in recycling endosomes (RE;Mostov and Cardone, 1995;Odorizzi and Trowbridge, 1997). Evidence accumulated over a decade and consolidated in the most recent studies (Ang et al., 2004;Lock and Stow, 2005;Cancino et al., 2007;Cresawn et al., 2007;Gravotta et al., 2007) have shown that the biosynthetic route of at least some proteins includes a post-TGN transit through RE. Under this scenery, it is now important to define the relative contribution of the TGN and RE in the polarized sorting mechanisms of different cargo and in different kind of polarized cells. Neurons, for instance, have to direct distinct proteins to somato-dendritic or axonal plasma membrane domains (Rodriguez-Boulan and Powell, 1992;Winckler and Mellman, 1999), yet their protein-sorting mechanisms remain less known than in epithelial cells. A comparative analysis in epithelial cells and neurons could indeed help to understand the underlying mechanisms of the polarized phenotype.Studies in MDCK cells, the most currently used model of cell polarity, settled the basics of apical and basolateral protein sorting (Rodriguez-Boulan et al., 2005). Apical membrane proteins possess sorting information located in their extracel...

show abstract

Section: Discussionmentioning

confidence: 61%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 97%

mentioning

confidence: 99%

See 3 more Smart Citations

Polarized Traffic of LRP1 Involves AP1B and SNX17 Operating on Y-dependent Sorting Motifs in Different Pathways

Donoso

Cancino

Lee

et al. 2009

MBoC

View full text Add to dashboard Cite

show abstract

Expressing Optogenetic Actuators Fused to N‐terminal Mucin Motifs Delivers Targets to Specific Subcellular Compartments in Polarized Cells

Wang,

Platz‐Baudin,

Noetzel

et al. 2023

Advanced Biology

View full text Add to dashboard Cite

Optogenetics is a powerful approach in neuroscience research. However, other tissues of the body may benefit from controlled ion currents and neuroscience may benefit from more precise optogenetic expression. The present work constructs three subcellularly‐targeted optogenetic actuators based on the channelrhodopsin ChR2‐XXL, utilizing 5, 10, or 15 tandem repeats (TR) from mucin as N‐terminal targeting motifs and evaluates expression in several polarized and non‐polarized cell types. The modified channelrhodopsin maintains its electrophysiological properties, which can be used to produce continuous membrane depolarization, despite the expected size of the repeats. This work then shows that these actuators are subcellularly localized in polarized cells. In polarized epithelial cells, all three actuators localize to just the lateral membrane. The TR‐tagged constructs also express subcellularly in cortical neurons, where TR5‐ChR2XXL and TR10‐ChR2XXL mainly target the somatodendrites. Moreover, the transfection efficiencies are shown to be dependent on cell type and tandem repeat length. Overall, this work verifies that the targeting motifs from epithelial cells can be used to localize optogenetic actuators in both epithelia and neurons, opening epithelia processes to optogenetic manipulation and providing new possibilities to target optogenetic tools.

show abstract

A dual tyrosine‐leucine motif mediates myelin protein P₀ targeting in MDCK cells

Kidd

Yadav

Huang

et al. 2006

Glia

View full text Add to dashboard Cite

Differential targeting of myelin proteins to multiple, biochemically and functionally distinct Schwann cell plasma membrane domains is essential for myelin formation. In this study, we investigated whether the myelin protein P0 contains targeting signals using Madin-Darby canine kidney (MDCK) cells. By confocal microscopy, P0 was localized to MDCK cell basolateral membranes. C-terminal deletion resulted in apical accumulation, and stepwise deletions defined a 15-mer region that was required for basolateral targeting. Alanine substitutions within this region identified the YAML sequence as a functional tyrosine-based targeting signal, with the ML sequence serving as a secondary leucine-based signal. Replacement of the P0 ectodomain with green fluorescent protein altered the distribution of constructs lacking the YAML signal. Coexpression of the myelin-associated glycoprotein did not alter P0 distribution in MDCK cells. The results indicate that P0 contains a hierarchy of targeting signals, which may contribute to P0 localization in myelinating Schwann cells and the pathogenesis in human disease.

show abstract

Motifs that mediate dendritic targeting in hippocampal neurons: A comparison with basolateral targeting signals

Cited by 29 publications

References 44 publications

Polarized Traffic of LRP1 Involves AP1B and SNX17 Operating on Y-dependent Sorting Motifs in Different Pathways

Polarized Traffic of LRP1 Involves AP1B and SNX17 Operating on Y-dependent Sorting Motifs in Different Pathways

Expressing Optogenetic Actuators Fused to N‐terminal Mucin Motifs Delivers Targets to Specific Subcellular Compartments in Polarized Cells

A dual tyrosine‐leucine motif mediates myelin protein P₀ targeting in MDCK cells

Contact Info

Product

Resources

About

Motifs that mediate dendritic targeting in hippocampal neurons: A comparison with basolateral targeting signals

Cited by 29 publications

References 44 publications

Polarized Traffic of LRP1 Involves AP1B and SNX17 Operating on Y-dependent Sorting Motifs in Different Pathways

Polarized Traffic of LRP1 Involves AP1B and SNX17 Operating on Y-dependent Sorting Motifs in Different Pathways

Expressing Optogenetic Actuators Fused to N‐terminal Mucin Motifs Delivers Targets to Specific Subcellular Compartments in Polarized Cells

A dual tyrosine‐leucine motif mediates myelin protein P0 targeting in MDCK cells

Contact Info

Product

Resources

About

A dual tyrosine‐leucine motif mediates myelin protein P₀ targeting in MDCK cells