Targeting of Rough Endoplasmic Reticulum Membrane Proteins and Ribosomes in Invertebrate Neurons

Rolls, Melissa M.; Hall, David H.; Victor, Martin; Stelzer, Ernst H. K.; Rapoport, Tom A.

doi:10.1091/mbc.01-10-0514

Cited by 146 publications

(169 citation statements)

References 47 publications

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“…In rab-10 mutant animals, we observed an accumulation of GLR-1::GFP in large accretions running along the length of the ventral cord neurite bundle ( Figure 1B). The size of these accretions is reminiscent of the intracellular membrane-bound compartments observed in the neurites of the ventral cord (Rolls et al, 2002). The rab-10 mutant phenotype is similar to the phenotype resulting from mutations in LIN-10 ( Figure 1C), a PDZ domain protein of the Mint/X11 family (Borg et al, 1998;Butz et al, 1998;Rongo et al, 1998;Whitfield et al, 1999).…”

mentioning

confidence: 74%

“…In the neurites of the ventral nerve cord, RFP::RAB-10 -containing structures were variable in size and shape. Because the neurites of the command interneurons contain smooth membranes that resemble endosomes, but they lack clear Golgi and Golgi-resident markers, it is most likely that RFP::RAB-10 is decorating early endosomes in neurites, just as it does in epithelial cells (Rolls et al, 2002). We observed low levels of colocalization between GLR-1::GFP and RFP::RAB-10, consistent with the idea that, at any one point in time, most GLR-1 in the ventral nerve cord does not reside within early endosomes.…”

Section: Discussionmentioning

confidence: 99%

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RAB-10 Regulates Glutamate Receptor Recycling in a Cholesterol-dependent Endocytosis Pathway

Glodowski

Chen

Schaefer

et al. 2007

MBoC

104

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Regulated endocytosis of ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-type glutamate receptors (AMPARs) is critical for synaptic plasticity. However, the specific combination of clathrin-dependent and -independent mechanisms that mediate AMPAR trafficking in vivo have not been fully characterized. Here, we examine the trafficking of the AMPAR subunit GLR-1 in Caenorhabditis elegans. GLR-1 is localized on synaptic membranes, where it regulates reversals of locomotion in a simple behavioral circuit. Animals lacking RAB-10, a small GTPase required for endocytic recycling of intestinal cargo, are similar in phenotype to animals lacking LIN-10, a postsynaptic density 95/disc-large/zona occludensdomain containing protein: GLR-1 accumulates in large accretions and animals display a decreased frequency of reversals. Mutations in unc-11 (AP180) or itsn-1 (Intersectin 1), which reduce clathrin-dependent endocytosis, suppress the lin-10 but not rab-10 mutant phenotype, suggesting that LIN-10 functions after clathrin-mediated endocytosis. By contrast, cholesterol depletion, which impairs lipid raft formation and clathrin-independent endocytosis, suppresses the rab-10 but not the lin-10 phenotype, suggesting that RAB-10 functions after clathrin-independent endocytosis. Animals lacking both genes display additive GLR-1 trafficking defects. We propose that RAB-10 and LIN-10 recycle AMPARs from intracellular endosomal compartments to synapses along distinct pathways, each with distinct sensitivities to cholesterol and the clathrin-mediated endocytosis machinery. INTRODUCTIONContinuous movement of ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)-type glutamate receptors (AMPARs) into and out of synaptic membranes is a key mechanism for the regulation of excitatory synaptic strength. Previous work has shown that insertion of AMPARs into the plasma membrane strengthens synapses and that it is required to convert silent synapses into active synapses (Bredt and Nicoll, 2003;Malenka, 2003;Malinow, 2003;Sheng and Hyoung Lee, 2003;Gerges et al., 2005). Furthermore, it has recently been shown that recycling of AMPARs from internal endosomal compartments back to the plasma membrane is important for long-term potentiation (Park et al., 2004). By contrast, endocytosis of AMPARs at sites adjacent to the postsynaptic density is important for long-term depression (Carroll et al., 2001;Racz et al., 2004). Thus, molecular machinery required for endocytosis, as well as intracellular membrane trafficking processes, ultimately regulates the character of signal transmitted at each synapse.Multiple endocytosis trafficking pathways have been observed in cells. Clathrin-dependent endocytosis occurs at clathrin-coated pits, where transmembrane protein cargo and adaptor molecules recruit soluble clathrin (Le Roy and Wrana, 2005). Vesicles coated with a clathrin lattice are then pinched off from the membrane. Members of the Rab family of small guanosine triphosphate (GTP)ases mediate the intracellular membrane trafficking of endocytose...

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mentioning

confidence: 74%

Section: Discussionmentioning

confidence: 99%

RAB-10 Regulates Glutamate Receptor Recycling in a Cholesterol-dependent Endocytosis Pathway

Glodowski

Chen

Schaefer

et al. 2007

MBoC

104

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“…The genomic or cDNA sequences of C. elegans rab-5, rab-7, rab-10, rab-11, rme-1, or human Rab10 genes were cloned individually into entry vector pDONR221 and then transferred into vha-6-GFP (or RFP)-vectors by Gateway recombination cloning to generate N-terminal fusions. The human TfR (transferrin receptor), human TAC (alpha-chain of the IL-2 receptor), and a fragment of C. elegans alpha-mannosidase II (F58H1.1, first 82 aa including signal sequence/TM-anchor domain as in Rolls et al, 2002) were cloned into a similar vector upstream of GFP to generate Cterminal fusions. Complete plasmid sequences are available on request.…”

Section: Plasmids and Transgenic Strainsmentioning

confidence: 99%

“…Given previously published reports that mammalian Rab10 is Golgi localized (Chen et al, 1993) and given our own observations showing extensive colocalization of GFP-RAB-10 with RFP-RAB-11, we next tested RAB-10 for Golgi localization using a specific C. elegans Golgi marker alphamannosidase II-GFP (MANS-GFP; Rolls et al, 2002;Figure 7, A-F). Unlike vertebrate cells that contain one large juxtanuclear Golgi stack, most invertebrate cells such as those in C. elegans instead contain many small Golgi stacks per cell, with the individual "mini-stacks" dispersed throughout the cytoplasm (Figure 7, A and D).…”

Section: Rab-10 Is Associated With Endosomes and Golgi In The Intestinementioning

confidence: 99%

RAB-10 Is Required for Endocytic Recycling in theCaenorhabditis elegansIntestine

Chen

Schweinsberg

Vashist

et al. 2006

MBoC

185

385

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The endocytic pathway of eukaryotes is essential for the internalization and trafficking of macromolecules, fluid, membranes, and membrane proteins. One of the most enigmatic aspects of this process is endocytic recycling, the return of macromolecules (often receptors) and fluid from endosomes to the plasma membrane. We have previously shown that the EH-domain protein RME-1 is a critical regulator of endocytic recycling in worms and mammals. Here we identify the RAB-10 protein as a key regulator of endocytic recycling upstream of RME-1 in polarized epithelial cells of the Caenorhabditis elegans intestine. rab-10 null mutant intestinal cells accumulate abnormally abundant RAB-5-positive early endosomes, some of which are enlarged by more than 10-fold. Conversely most RME-1-positive recycling endosomes are lost in rab-10 mutants. The abnormal early endosomes in rab-10 mutants accumulate basolaterally recycling transmembrane cargo molecules and basolaterally recycling fluid, consistent with a block in basolateral transport. These results indicate a role for RAB-10 in basolateral recycling upstream of RME-1. We found that a functional GFP-RAB-10 reporter protein is localized to endosomes and Golgi in wild-type intestinal cells consistent with a direct role for RAB-10 in this transport pathway. INTRODUCTIONEndocytosis and endocytic trafficking controls the uptake and sorting of extracellular macromolecules as well as the components of the cell membrane itself, counterbalancing secretion and allowing a complex interplay between cells and their environment that is important for a myriad of cellular activities (Brodsky et al., 2001;Maxfield and McGraw, 2004). The steps involved in the uptake and trafficking of cargo within the endosomal system have been well described, but many of the components mediating these steps at the molecular level remain to be identified (Brodsky et al., 2001;Maxfield and McGraw, 2004). Many receptors and their associated ligands cluster into clathrincoated pits, whereas other types of cargo utilize clathrinindependent uptake mechanisms (Nichols, 2003;Gesbert et al., 2004). Plasma membrane invaginations pinch off into vesicles, uncoat, and then fuse with one another and with early endosomes. In early endosomes some ligand-receptor complexes dissociate because of the reduced pH of the endosomal lumen (Mukherjee et al., 1997). Many receptors then recycle to the plasma membrane (PM) either directly or indirectly via recycling endosomes (Mukherjee et al., 1997;Maxfield and McGraw, 2004). Many ligands do not recycle but instead are transported from early to late endosomes and eventually to lysosomes for degradation (Mukherjee et al., 1997). In polarized epithelial cells such as cultured Madin-Darby canine kidney (MDCK) cells, an additional layer of complexity in the endocytic pathway contributes to formation and/or maintenance of the specialized apical and basolateral domains (Nelson and Yeaman, 2001;Mostov et al., 2003;Hoekstra et al., 2004). Both the apical and basolateral membranes deliver cargo ...

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“…let-858 3Ј UTR sequences derived from pPD117.01 were present in all constructs. We generated Golgi-specific marker lin-44::mans-yfp (pSK224) using MANS-YFP sequences (Rolls et al, 2002) and lin-44::vps-35-mCherry using mCherry sequences (Shaner et al, 2004). -mCherry lines were generated and all showed comparable expression levels and patterns.…”

Section: Molecular Biologymentioning

confidence: 99%

Wnt signaling establishes anteroposterior neuronal polarity and requires retromer inC. elegans

2006

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Secreted Wnt proteins influence neural connectivity by regulating axon guidance, dendritic morphogenesis and synapse formation. We report a new role for Wnt and Frizzled proteins in establishing the anteroposterior polarity of the mechanosensory neurons ALM and PLM in C. elegans. Disruption of Wnt signaling leads to a complete inversion of ALM and PLM polarity: the anterior process adopts the length, branching pattern and synaptic properties of the wild-type posterior process, and vice versa. Different but overlapping sets of Wnt proteins regulate neuronal polarity in different body regions. Wnts act directly on PLM via the Frizzled LIN-17. In addition, we show that they are needed for axon branching and anteriorly directed axon growth. We also find that the retromer, a conserved protein complex that mediates transcytosis and endosome-to-Golgi protein trafficking, plays a key role in Wnt signaling. Deletion mutations of retromer subunits cause ALM and PLM polarity, and other Wnt-related defects. We show that retromer protein VPS-35 is required in Wnt-expressing cells and propose that retromer activity is needed to generate a fully active Wnt signal.

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Targeting of Rough Endoplasmic Reticulum Membrane Proteins and Ribosomes in Invertebrate Neurons

Cited by 146 publications

References 47 publications

RAB-10 Regulates Glutamate Receptor Recycling in a Cholesterol-dependent Endocytosis Pathway

RAB-10 Regulates Glutamate Receptor Recycling in a Cholesterol-dependent Endocytosis Pathway

RAB-10 Is Required for Endocytic Recycling in theCaenorhabditis elegansIntestine

Wnt signaling establishes anteroposterior neuronal polarity and requires retromer inC. elegans

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