Endocytosed Cation-Independent Mannose 6-Phosphate Receptor Traffics via the Endocytic Recycling Compartment en Route to the<i>trans</i>-Golgi Network and a Subpopulation of Late Endosomes

Lin, Sharron X.; Mallet, William; Huang, Amy Y.; Maxfield, Frederick R.

doi:10.1091/mbc.e03-07-0497

Cited by 107 publications

(120 citation statements)

References 61 publications

Supporting

Mentioning

112

Contrasting

Unclassified

Order By: Relevance

“…Briefly, CD8 WT (CD8-WT) contains no known sorting signals in its cytoplasmic tail, is therefore not subject to endocytosis and is resident at the plasma membrane (28). CD8-cation-independent mannose 6-phosphate receptor (CIMPR) contains the cytoplasmic domain of CIMPR, a wellcharacterized cargo that is efficiently internalized in clathrincoated vesicles before being trafficked to the trans-Golgi network (TGN) and a subset of late endosomes, via sorting and recycling endosomes (32,33). The remaining constructs contain "designer" tails that represent three well-established endocytic motifs: YXXΦ (CD8-YAAL), [DE]XXXL[LI] (CD8-EAAALL), and FXNPXY (CD8-FANPAY), all transposed on a background of eight alanines (CD8-8xA) (28).…”

Section: Resultsmentioning

confidence: 99%

“…This pool is likely due to different trafficking routes. Although proteins containing YXXΦ, [D/E]XXXL[L/I], or FXNPXY motifs typically show rapid recycling back to the plasma membrane after internalization, a proportion of CIMPR also traffics to the TGN and late endosomes (33). Recycling from here to the plasma membrane will necessarily take more time.…”

Section: Mitotic Inhibition Of Endocytosis Was Confirmed Using Fluorementioning

confidence: 99%

See 1 more Smart Citation

Clathrin-mediated endocytosis is inhibited during mitosis

Fielding

Willox

Okeke

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

A long-standing paradigm in cell biology is the shutdown of endocytosis during mitosis. There is consensus that transferrin uptake is inhibited after entry into prophase and that it resumes in telophase. A recent study proposed that endocytosis is continuous throughout the cell cycle and that the observed inhibition of transferrin uptake is due to a decrease in available transferrin receptor at the cell surface, and not to a shutdown of endocytosis. This challenge to the established view is gradually becoming accepted. Because of this controversy, we revisited the question of endocytic activity during mitosis. Using an antibody uptake assay and controlling for potential changes in surface receptor density, we demonstrate the strong inhibition of endocytosis in mitosis of CD8 chimeras containing any of the three major internalization motifs for clathrin-mediated endocytosis (YXXΦ, [DE]XXXL[LI], or FXNPXY) or a CD8 protein with the cytoplasmic tail of the cationindependent mannose 6-phosphate receptor. The shutdown is not gradual: We describe a binary switch from endocytosis being "on" in interphase to "off" in mitosis as cells traverse the G 2 /M checkpoint. In addition, we show that the inhibition of transferrin uptake in mitosis occurs despite abundant transferrin receptor at the surface of HeLa cells. Our study finds no support for the recent idea that endocytosis continues during mitosis, and we conclude that endocytosis is temporarily shutdown during early mitosis.

show abstract

Section: Resultsmentioning

confidence: 99%

Section: Mitotic Inhibition Of Endocytosis Was Confirmed Using Fluorementioning

confidence: 99%

Clathrin-mediated endocytosis is inhibited during mitosis

Fielding

Willox

Okeke

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…For instance, in mammalian cell pulse-chase experiments, TGN38 and Shiga toxin have been shown to be retrograde cargos that traverse the recycling endosome en route to the TGN (20,21,25). Canonical recycling endosome regulators Rab11, FIP1/RCP, and mRme-1/EHD1 have been shown to be important regulators of recycling endosome-to-TGN transport of retrograde cargo (23,25,54). However, the overall molecular mechanisms mediating this transport step have remained elusive.…”

Section: Discussionmentioning

confidence: 99%

A TOCA/CDC-42/PAR/WAVE functional module required for retrograde endocytic recycling

Bai

Grant

2015

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Endosome-to-Golgi transport is required for the function of many key membrane proteins and lipids, including signaling receptors, small-molecule transporters, and adhesion proteins. The retromer complex is well-known for its role in cargo sorting and vesicle budding from early endosomes, in most cases leading to cargo fusion with the trans-Golgi network (TGN). Transport from recycling endosomes to the TGN has also been reported, but much less is understood about the molecules that mediate this transport step. Here we provide evidence that the F-BAR domain proteins TOCA-1 and TOCA-2 (Transducer of Cdc42 dependent actin assembly), the small GTPase CDC-42 (Cell division control protein 42), associated polarity proteins PAR-6 (Partitioning defective 6) and PKC-3/atypical protein kinase C, and the WAVE actin nucleation complex mediate the transport of MIG-14/Wls and TGN-38/TGN38 cargo proteins from the recycling endosome to the TGN in Caenorhabditis elegans. Our results indicate that CDC-42, the TOCA proteins, and the WAVE component WVE-1 are enriched on RME-1-positive recycling endosomes in the intestine, unlike retromer components that act on early endosomes. Furthermore, we find that retrograde cargo TGN-38 is trapped in early endosomes after depletion of SNX-3 (a retromer component) but is mainly trapped in recycling endosomes after depletion of CDC-42, indicating that the CDC-42-associated complex functions after retromer in a distinct organelle. Thus, we identify a group of interacting proteins that mediate retrograde recycling, and link these proteins to a poorly understood trafficking step, recycling endosome-to-Golgi transport. We also provide evidence for the physiological importance of this pathway in WNT signaling.retromer | endocytic recycling | endosome | toca | wave

show abstract

“…Prior work has revealed that M6PR moves between the Golgi and endosomes along diverse recycling pathways (Ghosh et al, 2003;Bonifacino and Rojas, 2006). Recycling endosomes and late endosomes are among the endocytic compartments from which M6PR returns back to the Golgi complex (Klumperman et al, 1993;Hirst et al, 1998;Lin et al, 2004;Tortorella et al, 2007). Consequently, we analyzed the subcellular distribution of the mannose-6-phosphate receptor (M6PR) in control and hSPE-39 downregulated cells.…”

Section: Hspe-39 Is Required For M6pr-mediated Transportmentioning

confidence: 99%

SPE-39 Family Proteins Interact with the HOPS Complex and Function in Lysosomal Delivery

Zhu

Salazar²,

Zlatic³

et al. 2009

MBoC

View full text Add to dashboard Cite

Yeast and animal homotypic fusion and vacuole protein sorting (HOPS) complexes contain conserved subunits, but HOPS-mediated traffic in animals might require additional proteins. Here, we demonstrate that SPE-39 homologues, which are found only in animals, are present in RAB5-, RAB7-, and RAB11-positive endosomes where they play a conserved role in lysosomal delivery and probably function via their interaction with the core HOPS complex. Although Caenorhabditis elegans spe-39 mutants were initially identified as having abnormal vesicular biogenesis during spermatogenesis, we show that these mutants also have disrupted processing of endocytosed proteins in oocytes and coelomocytes. C. elegans SPE-39 interacts in vitro with both VPS33A and VPS33B, whereas RNA interference of VPS33B causes spe-39-like spermatogenesis defects. The human SPE-39 orthologue C14orf133 also interacts with VPS33 homologues and both coimmunoprecipitates and cosediments with other HOPS subunits. SPE-39 knockdown in cultured human cells altered the morphology of syntaxin 7-, syntaxin 8-, and syntaxin 13-positive endosomes. These effects occurred concomitantly with delayed mannose 6-phosphate receptor-mediated cathepsin D delivery and degradation of internalized epidermal growth factor receptors. Our findings establish that SPE-39 proteins are a previously unrecognized regulator of lysosomal delivery and that C. elegans spermatogenesis is an experimental system useful for identifying conserved regulators of metazoan lysosomal biogenesis. INTRODUCTIONLysosome biogenesis is mediated by multiple vesicular budding and fusion events that deliver components between subcellular compartments (Luzio et al., 2003). In Saccharomyces cerevisiae, vesicular fusion at the vacuole (the yeast equivalent of lysosomes) requires the homotypic fusion and vacuole protein sorting (HOPS) complex, which regulates vesicle docking through its interaction with soluble N-ethylmaleimide-sensitive factor-attachment protein receptors (SNAREs) and the Rab protein Ypt7p Sato et al., 2000;Wurmser et al., 2000). The yeast HOPS complex contains class C Vps proteins Vps11p, Vps16p, Vps18p, and Vps33p (Rieder and Emr, 1997) and class B Vps proteins Vps39p and Vps41p (Seals et al., 2000;Wurmser et al., 2000). In addition to vesicular fusion at the vacuole, the class C Vps proteins also function in Golgi-to-endosome transport and other steps in vacuolar delivery pathways (Srivastava et al., 2000;Peterson and Emr, 2001;Subramanian et al., 2004;Peplowska et al., 2007). Involvement of the class C Vps proteins at multiple stages has also been reported in mammalian cells (Kim et al., 2003;Richardson et al., 2004). Vesicular trafficking to the lysosome has been extensively described in yeast (Bowers and Stevens, 2005), but it is also known that this process is more complex in metazoans (Dell'Angelica, 2004). Yeast only has lysosomes of a single type, whereas animals have lysosomes and lysosome-related organelles that are functionally diverse. This diversity is evident when comparing th...

show abstract

Endocytosed Cation-Independent Mannose 6-Phosphate Receptor Traffics via the Endocytic Recycling Compartment en Route to thetrans-Golgi Network and a Subpopulation of Late Endosomes

Cited by 107 publications

References 61 publications

Clathrin-mediated endocytosis is inhibited during mitosis

Clathrin-mediated endocytosis is inhibited during mitosis

A TOCA/CDC-42/PAR/WAVE functional module required for retrograde endocytic recycling

SPE-39 Family Proteins Interact with the HOPS Complex and Function in Lysosomal Delivery

Contact Info

Product

Resources

About