Kinesin-mediated organelle translocation revealed by specific cellular manipulations.

Feiguin, Fabián; Ferreira, Adriana; Kosik, Kenneth S.; Cáceres, Alfredo

doi:10.1083/jcb.127.4.1021

Cited by 163 publications

(119 citation statements)

References 52 publications

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“…These contradictory movements of Golgi elements are mediated by distinct molecular motors. Consistent with earlier findings by Feiguin et al (1994), who found that the expression of kinesin antisense oligonucleotide rendered the Golgi apparatus more compact, microinjection of antikinesin antibodies inhibited Golgi dispersion along stable, nocodazole-resistant MTs (Minin, 1997). Conversely, the central localization of the Golgi apparatus involves cytoplasmic dynein (Corthésy-Theulaz et al, 1992;Fath et al, 1994;Burkhardt et al, 1997;Harada et al, 1998).…”

supporting

confidence: 80%

The Golgi Complex Is a Microtubule-organizing Organelle

Chabin-Brion

Marceiller

Perez

et al. 2001

MBoC

275

245

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We show that the Golgi complex can directly stimulate microtubule nucleation in vivo and in vitro and thus behaves as a potent microtubule-organizing organelle in interphase cells. With the use of nocodazole wash-out experiments in hepatic cells, we found that the occurrence of noncentrosomal, early stabilized microtubules is highly correlated with the subcellular localization of Golgi membranes. With the use of in vitro reconstituted microtubule assembly systems with or without cytosol, we also found that, in contrast to centrosomally attached microtubules, the distal ends of Golgi-attached microtubules are remotely stabilized in a way that requires additional cytosolic component (s). Finally, we demonstrate that Golgi-based microtubule nucleation is direct and involves a subset of ␥-tubulin bound to the cytoplasmic face of the organelle. INTRODUCTIONIn interphase cells, the microtubule (MT) network plays a major role in membrane dynamics and organelle localization. In this context, the interaction between the Golgi complex and the MT network has been extensively studied. The Golgi apparatus colocalizes with the minus ends of MTs, which are usually associated with the centrosome (for review see Kreis et al., 1997;Thyberg and Moskalewski, 1999). This localization actually results from an equilibrium between two contradictory movements that have been unraveled with the use of MT-depolymerizing drugs and probably occur on MT subpopulations with different dynamics. The dispersal of Golgi elements occurs along stable MTs after depolymerization of the most labile MT population (Minin, 1997), whereas their reclustering involves newly assembled MTs (Ho et al., 1989). These contradictory movements of Golgi elements are mediated by distinct molecular motors. Consistent with earlier findings by Feiguin et al. (1994), who found that the expression of kinesin antisense oligonucleotide rendered the Golgi apparatus more compact, microinjection of antikinesin antibodies inhibited Golgi dispersion along stable, nocodazole-resistant MTs (Minin, 1997). Conversely, the central localization of the Golgi apparatus involves cytoplasmic dynein (Corthésy-Theulaz et al., 1992;Fath et al., 1994;Burkhardt et al., 1997;Harada et al., 1998). It is also worth noting that, in addition to the kinesin-mediated disruption of the central Golgi complex during MT depolymerization, the dispersion of Golgi elements also relies on the reconstitution of mini Golgi stacks at endoplasmic reticulum (ER) exit sites (Cole et al., 1996;Storrie et al., 1998). Such data on the scattering and the reclustering of the Golgi complex have led to the view that Golgi membranes undergo an intimate relationship with MTs and especially with a population of nocodazole-resistant, stable MTs. Stable MTs are characterized by the occurrence of posttranslationally modified tubulin-especially detyrosinated and acetylated tubulin (for review, see MacRae, 1997), which is thought to accumulate in stable MTs because of their longer half-lives, but does not influence MT stability i...

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supporting

confidence: 80%

The Golgi Complex Is a Microtubule-organizing Organelle

Chabin-Brion

Marceiller

Perez

et al. 2001

MBoC

275

245

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“…However, function disruption tests have again yielded conflicting data. Antisense oligonucleotide inhibition of KHC in cultured rat astrocytes caused a retraction of the ER network (Feiguin et al, 1994). In contrast, antibody inhibition of KHC in sea urchin embryonic cells (Wright et al, 1993) or gene disruption in mouse extraembryonic cells (Tanaka et al, 1998) had no dramatic effects on ER organization.…”

Section: Discussionmentioning

confidence: 96%

“…For example, in a study of vesicle/ tubule transport in the recycling pathway, antibody inhibition of KHC blocked brefeldin A-induced movement of Golgi membranes into the ER in cultured NRK cells (Lippincott-Schwartz et al, 1995). Conversely, antisense oligonucleotide inhibition of KHC in cultured rat astrocytes (Feiguin et al, 1994) and gene disruption in cultured mouse extraembryonic cells (Tanaka et al, 1998) did not prevent brefeldin A-induced Golgi-to-ER membrane transfer. With regard to Golgi-to-plasma membrane vesicle transport, antisense oligonucleotide inhibition of KHC in cultured vertebrate neurons impaired delivery of vesicles containing certain synaptic proteins to axon terminals (Ferreira et al, 1992).…”

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

“…Antibody inhibition of KHC in human fibroblasts (Rodionov et al, 1993) and gene disruption in mouse extraembryonic cells (Tanaka et al, 1998) caused mitochondria, which are normally dispersed throughout the cytoplasm, to cluster near the cell center. However, no effect on mitochondrial distribution was seen in rat astrocytes injected with Khc antisense oligonucleotides (Feiguin et al, 1994) or in mutant strains of C. elegans (Hall et al, 1991) and fungi (Lehmler et al, 1997;Seiler et al, 1997).In the studies mentioned above, some of the disagreements might be due to a lack of specificity in KHC function disruption, incomplete KHC inhibition, variability in the way brefeldin A perturbs different cell types, and variations in physiology caused by cell culture conditions. Attempting to minimize these potential caveats, we have studied the fates of clones of Khc null cells carried in otherwise healthy, intact Drosophila.…”

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confidence: 97%

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Clonal Tests of Conventional Kinesin Function during Cell Proliferation and Differentiation

Brendza

Sheehan

Turner

et al. 2000

MBoC

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Null mutations in the Drosophila Kinesin heavy chain gene (Khc), which are lethal during the second larval instar, have shown that conventional kinesin is critical for fast axonal transport in neurons, but its functions elsewhere are uncertain. To test other tissues, single imaginal cells in young larvae were rendered null for Khc by mitotic recombination. Surprisingly, the null cells produced large clones of adult tissue. The rates of cell proliferation were not reduced, indicating that conventional kinesin is not essential for cell growth or division. This suggests that in undifferentiated cells vesicle transport from the Golgi to either the endoplasmic reticulum or the plasma membrane can proceed at normal rates without conventional kinesin. In adult eye clones produced by null founder cells, there were some defects in differentiation that caused mild ultrastructural changes, but they were not consistent with serious problems in the positioning or transport of endoplasmic reticulum, mitochondria, or vesicles. In contrast, defective cuticle deposition by highly elongated Khc null bristle shafts suggests that conventional kinesin is critical for proper secretory vesicle transport in some cell types, particularly ones that must build and maintain long cytoplasmic extensions. The ubiquity and evolutionary conservation of kinesin heavy chain argue for functions in all cells. We suggest interphase organelle movements away from the cell center are driven by multilayered transport mechanisms; that is, individual organelles can use kinesin-related proteins and myosins, as well as conventional kinesin, to move toward the cell periphery. In this case, other motors can compensate for the loss of conventional kinesin except in cells that have extremely long transport tracks. INTRODUCTIONVesicle transport is important in eukaryotic cells for the addition of material to the plasma membrane, for secretion, and for cell polarity. Active vesicle transport is thought to be driven by mechanochemical enzymes (motor proteins). Motors attach to vesicle membranes and then use ATP hydrolysis to drive unidirectional movement along polar cytoskeletal filaments. Characterized members of the myosin family of motors move toward the barbed or fast-growing ends of actin filaments with the exception of myosin VI, which moves toward the pointed or slow-growing ends (Wells et al., 1999) (reviewed by Sellers and Goodson, 1995). Actin filaments in undifferentiated and in some differentiated cell types are highly concentrated in the cortex (WatermanStorer et al., 1998; reviewed by Cramer, 1999). Cytoplasmic myosins may therefore be important for anchoring or moving vesicles when they are near the plasma membrane (Fath et al., 1994). Motors in the kinesin and dynein families move along microtubules. Characterized dyneins and members of the C-terminal kinesin subfamily move toward microtubule minus ends, whereas other kinesins that act as motors move toward microtubule plus ends (reviewed by Vale and Fletterick, 1997;Hirokawa, 1998;Goldstein and Ya...

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A fission yeast kinesin affects Golgi membrane recycling

Brazer

Williams

Chappell

et al. 2000

Yeast

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We report here an in vivo study of kinesin heavy chain (KHC) functions in yeast. We have identified in Schizosaccharomyces pombe a kinesin motor gene, klp3+, which has the highest homology to the Neurospora crassa KHC. Using indirect immunofluorescence, HA epitope‐tagged Klp3 protein is cytoplasmic and appears as one to a few distinct patches that are coincident with microtubules. The klp3 null allele is viable. In klp3 deleted cells, ER, Golgi and mitochondrial distribution appear normal. Mitochondrial distribution in S. pombe is known to be microtubule‐associated. We show that latrunculin A does not cause mitochondria to aggregate, suggesting that mitochondrial distribution in fission yeast, unlike budding yeast, is not dependent upon actin‐based processes. Neither latrunculin A nor thiabendazole affects ER or Golgi distribution. We also used the vital dye FM4‐64 to visualize the internalization of the dye and its transport to vacuoles in fission yeast in the presence and absence of Klp3. We observed no significant difference between the wild‐type and Klp3 null cells in either the dynamics of endocytosis or the distribution and fusion of vacuoles. The drug brefeldin A causes Golgi‐to‐ER recycling in wild‐type fission yeast cells. Although recycling of Golgi to ER after brefeldin A treatment occurs in klp3 null cells, recycling is defective and the distribution pattern we see is different from that observed in the wild‐type strain. We conclude that Klp3 plays a role in BFA‐induced membrane transport. The nucleotide sequence of S. pombe klp3+ was submitted to GenBank under Accession No. AF154055. Copyright © 2000 John Wiley & Sons, Ltd.

show abstract

Kinesin-mediated organelle translocation revealed by specific cellular manipulations.

Cited by 163 publications

References 52 publications

The Golgi Complex Is a Microtubule-organizing Organelle

The Golgi Complex Is a Microtubule-organizing Organelle

Clonal Tests of Conventional Kinesin Function during Cell Proliferation and Differentiation

A fission yeast kinesin affects Golgi membrane recycling

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