Regulation of early endocytic vesicle motility and fission in a reconstituted system

Bananis, Eustratios; Murray, John W.; Stockert, Richard J.; Satir, Peter; Wolkoff, Allan W.

doi:10.1242/jcs.00478

Cited by 54 publications

(92 citation statements)

References 56 publications

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“…In vitro studies of endocytic vesicles from rat liver indicated an involvement of the minus-end-directed kinesin, KIFC2 (REF. 61). However, KIFC2-knockout mice are viable and reproduce normally, arguing against a crucial role of KIFC2 for cell viability 62 .…”

Section: Box 2 | Modes Of Motor-cargo Associationmentioning

confidence: 99%

“…Uploading of endosomes onto dynein is dependent on dynactin and LIS1 (a dynein activator that is defective in patients with the brain disorder lissencephaly 77,78 ), which both accumulate at microtubule plus ends. The functional significance of bidirectional endosome movement needs to be clarified, but it might be either to keep these organelles dispersed in the cytoplasm 79 , to enhance encounters between different compartments for subsequent fusion 68 , or to support fission 61 .…”

Section: Box 2 | Modes Of Motor-cargo Associationmentioning

confidence: 99%

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Powering membrane traffic in endocytosis and recycling

Soldati

Schliwa

2006

Nat Rev Mol Cell Biol

312

279

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| Early in evolution, the diversification of membrane-bound compartments that characterize eukaryotic cells was accompanied by the elaboration of molecular machineries that mediate intercompartmental communication and deliver materials to specific destinations. Molecular motors that move on tracks of actin filaments or microtubules mediate the movement of organelles and transport between compartments. The subjects of this review are the motors that power the transport steps along the endocytic and recycling pathways, their modes of attachment to cargo and their regulation.The emergence of eukaryotic cells was accompanied by the development of endomembrane systems that compartmentalize biochemical pathways and biosynthetic processes. An evolutionary trend towards increasing complexity and subcellular specialization necessitated the development of machineries for intercompartmental communication. Molecular assemblies evolved to confer specificity to the interactions of donor and acceptor compartments (budding, sorting, tethering and fusion). Cytoskeletal polymers such as actin filaments and microtubules, which help segregate genetic material and determine cell shape and subcellular architecture, were co-opted as tracks for transport. In animal cells, microtubules support long-range transport, whereas the more flexible actin filaments serve short-range movements both near the cell periphery and in the cell interior. Also, actin filaments can be woven into dense networks of short fibres through the action of crosslinkers and branchpromoting complexes. On the other hand, in many plant cells, bundled actin filaments can form extended tracks for long-distance transport. Owing to the gel-like nature of the cytoplasm, the Brownian movement of organelles is severely restricted and cargoes have to be transported to their destinations at the expense of energy. Furthermore, seemingly random, but motor-dependent, movement is proposed to increase the probability of vesicle collisions and therefore promote fusion events. Movement is powered by three ATP-dependent motors: myosin, kinesin and dynein. Over the course of eukaryotic evolution, these motors have diversified into a large number of families with specific tasks (FIG. 1).Here, we review the involvement of molecular motors in the movement of endosomes and in vesicular trafficking along the endocytic and recycling pathways. These pathways are summarized in FIG. 2. We do not, however,

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Section: Box 2 | Modes Of Motor-cargo Associationmentioning

confidence: 99%

Section: Box 2 | Modes Of Motor-cargo Associationmentioning

confidence: 99%

Powering membrane traffic in endocytosis and recycling

Soldati

Schliwa

2006

Nat Rev Mol Cell Biol

312

279

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“…Using these tools, we found that plus-end motility of early endocytic vesicles from rat liver was mediated by the conventional kinesin Kif5B (standardized nomenclature kinesin-1) (Miki et al, 2003(Miki et al, , 2005Lawrence et al, 2004), and minus-end motility was mediated by Kifc2 (standardized nomenclature kinesin-14B) (Bananis et al, , 2003(Bananis et al, , 2004Murray et al, 2000). Whereas Kifc2 was initially described as a brain-specific minus-enddirected kinesin Saito et al, 1997), our studies showed that it was highly associated with these vesicles prepared from rat liver (Bananis et al, 2003). Although the rat is a convenient experimental animal, the power of genetic models that have been established in the mouse led us, in the present study, to examine microtubulebased motility and processing of early endocytic vesicles derived from mouse liver.…”

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confidence: 99%

“…Motility assays were performed in a 3-l chamber consisting of two pieces of double-sided tape sandwiched between optical glass as described previously (Murray et al, 2002). The chamber was coated with 0.03 mg/ml DEAE-dextran (GE Healthcare), and rhodamine-labeled, Taxol-stabilized microtubules were added and incubated for 3 min at room temperature (Bananis et al, , 2003(Bananis et al, , 2004. The chamber was washed three times with PMEE motility buffer (35 mM PIPES-K 2 , 5 mM MgCl 2 , 1 mM EGTA, 0.5 mM EDTA, 4 mM DTT, 20 M Taxol, and 2 mg/ml BSA) containing 5 mg/ml casein followed by three washes with PMEE motility buffer without casein.…”

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Kif5B and Kifc1 Interact and Are Required for Motility and Fission of Early Endocytic Vesicles in Mouse Liver

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Bananis

Sarkar

et al. 2007

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Early endocytic vesicles loaded with Texas Red asialoorosomucoid were prepared from mouse liver. These vesicles bound to microtubules in vitro, and upon ATP addition, they moved bidirectionally, frequently undergoing fission into two daughter vesicles. There was no effect of vanadate (inhibitor of dynein) on motility, whereas 5 -adenylylimido-diphosphate (kinesin inhibitor) was highly inhibitory. Studies with specific antibodies confirmed that dynein was not associated with these vesicles and that Kif5B and the minus-end kinesin Kifc1 mediated their plus-and minus-end motility, respectively. More than 90% of vesicles associated with Kifc1 also contained Kif5B, and inhibition of Kifc1 with antibody resulted in enhancement of plus-end-directed motility. There was reduced vesicle fission when either Kifc1 or Kif5B activity was inhibited by antibody, indicating that the opposing forces resulting from activity of both motors are required for fission to occur. Immunoprecipitation of native Kif5B by FLAG antibody after expression of FLAG-Kifc1 in 293T cells indicates that these two motors can interact with each other. Whether they interact directly or through a complex of potential regulatory proteins will need to be clarified in future studies. However, the present study shows that coordinated activity of these kinesins is essential for motility and processing of early endocytic vesicles. INTRODUCTIONReceptor-mediated endocytosis is a process in which ligands bind to specific cell surface receptors and internalize via clathrin-coated pits. After internalization the clathrin coat is released and uncoated vesicles mature into early endosomes (Mellman, 1996;Mukherjee et al., 1997;Marsh and McMahon, 1999;Higgins and McMahon, 2002;Perrais and Merrifield, 2005). After acidification of early endosomes, ligands such as asialoorosomucoid (ASOR) that are destined for lysosomes dissociate from their receptors (Harford et al., 1983a,b), and a series of fission events results in their segregation into separate daughter vesicles (Wolkoff et al., 1984;Mellman, 1996;Mukherjee et al., 1997;Murray and Wolkoff, 2003). The resulting ligand-enriched late endosomes traffic to lysosomes for degradation, whereas the receptor-containing daughter endosomes traffic back to the cell surface where receptor is reused (Harford et al., 1983a;Wolkoff et al., 1984;Mukherjee et al., 1997). Previous studies indicated that this segregation event requires an intact microtubule cytoskeleton (Goltz et al., 1992;Novikoff et al., 1996;Murray et al., 2000;Bananis et al., 2003Bananis et al., , 2004. In more recent studies, microtubule-based endosome motility and segregation were reconstituted in vitro using fluorescent early endosomes prepared from rat liver 5 min after portal venous injection of Texas Red-labeled ASOR, a substrate for the hepatocytespecific asialoglycoprotein receptor (ASGPR) (Bananis et al., , 2003(Bananis et al., , 2004Murray et al., 2000;Murray and Wolkoff, 2003). On addition of ATP to the in vitro assay, these vesicles moved bidirectionall...

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