Role of Microtubules in the Organization of the Golgi Complex

Thyberg, Johan; Moskalewski, Stanisław

doi:10.1006/excr.1998.4326

Cited by 317 publications

(281 citation statements)

References 212 publications

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“…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.…”

Section: Introductionmentioning

confidence: 99%

The Golgi Complex Is a Microtubule-organizing Organelle

Chabin-Brion

Marceiller

Perez

et al. 2001

MBoC

272

243

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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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Section: Introductionmentioning

confidence: 99%

The Golgi Complex Is a Microtubule-organizing Organelle

Chabin-Brion

Marceiller

Perez

et al. 2001

MBoC

272

243

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“…The maintenance of the Golgi ribbon has been shown to require an intact MT network 11 . However, the underlying mechanism for maintaining this specific Golgi arrangement as well as its physiological significance had been unclear until the above-mentioned studies.…”

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confidence: 99%

MTCL1 crosslinks and stabilizes non-centrosomal microtubules on the Golgi membrane

et al. 2014

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Recent studies have revealed the presence of a microtubule subpopulation called Golgi-derived microtubules that support Golgi ribbon formation, which is required for maintaining polarized cell migration. CLASPs and AKAP450/CG-NAP are involved in their formation, but the underlying molecular mechanisms remain unclear. Here, we find that the microtubule-crosslinking protein, MTCL1, is recruited to the Golgi membranes through interactions with CLASPs and AKAP450/CG-NAP, and promotes microtubule growth from the Golgi membrane. Correspondingly, MTCL1 knockdown specifically impairs the formation of the stable perinuclear microtubule network to which the Golgi ribbon tethers and extends. Rescue experiments demonstrate that besides its crosslinking activity mediated by the N-terminal microtubule-binding region, the C-terminal microtubule-binding region plays essential roles in these MTCL1 functions through a novel microtubule-stabilizing activity. These results suggest that MTCL1 cooperates with CLASPs and AKAP450/CG-NAP in the formation of the Golgi-derived microtubules, and mediates their development into a stable microtubule network.

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“…The cytoskeleton 47 determines the location of the Golgi, and depending on the 48 cellular model, either microtubules or actin filaments have 49 the greater influence (Egea and Rios 2008), the impact of 50 intermediate filaments being very limited (Gao and Sztul 51 2001;Gao et al 2002;Styers et al 2006;Toivola et al 52 2005). Historically, microtubules were the first cytoskele-53 ton element to be linked to the Golgi structure and function 54 (Thyberg and Moskalewski 1999), and only later was it 55 firmly established that actin and associated proteins (actin 56 et al) also played a significant role (for recent reviews see Soldati and Schliwa 61 2006). Here, we provide an up-to-date overview of the 62 structural and transport consequences of the coupling 75 jasplakinolide and botulinum toxins and are known generi-76 cally as actin toxins or actin drugs ( Fig.…”

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confidence: 99%

Actin acting at the Golgi

Egea

Serra‐Peinado

Salcedo-Sicilia

et al. 2013

Histochem Cell Biol

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7 Abstract The organization, assembly and remodeling of 8 the actin cytoskeleton provide force and tracks for a variety 9 of (endo)membrane-associated events such as membrane 10 trafficking. This review illustrates in different cellular 11 models how actin and many of its numerous binding and 12 regulatory proteins (actin and co-workers) participate in the 13 structural organization of the Golgi apparatus and in traf-14 ficking-associated processes such as sorting, biogenesis and 15 motion of Golgi-derived transport carriers. 16 17 Keywords Golgi apparatus Á Cytoskeleton Á Actin Á 18 Spectrin Á Myosin Á Rho GTPases Introduction 20The function of the Golgi apparatus is the result of a 21 complex interaction between the molecules that establish 22 its architecture, those that determine protein transport and 23 those that integrate signals from either outside or inside the 24 cell. Cytoskeletal elements (microtubules, actin filaments 25 or microfilaments and intermediate filaments) integrate 26 these processes. Association and coordination between 27 them as well as their respective binding and regulatory 28 proteins are present in the majority of endomembrane 29 systems, including the Golgi apparatus. While its basic 30 function is highly conserved, the Golgi varies greatly in 31 shape and number from one organism to another. Briefly, it 32 ranges from dispersed cisternae or isolated tubular net-33 works as occurs in algae, protozoa and the yeast Saccha-34 romyces cerevisiae, to a pile of flattened cisternae aligned 35 in parallel and known as the Golgi stack. This, depending 36 on the organism examined, could be present in a single 37 (fungi and the yeast Pichia pastoris) or multiple copies, the 38 latter being scattered throughout the cytoplasm (plants and 39 Drosophila) or organized as a ribbon around centrioles 40 (vertebrates) (daSilva et al. 2004; Hawes and Satiat-Je-41 unemaitre 2005; He et al. 2004;He2007; Henderson et al. 42 2007; Kondylis and Rabouille 2003; Ladinsky et al. 1999; 43 Lowe 2011; Mogelsvang et al. 2003; Pelletier et al. 2002; 44 Preuss et al. 1992;Rambourg and Clermont 1986; Ram-45 bourg et al. 2001;Ramírez and Lowe 2009; Rios and 46 Bornens 2003; Rossanese et al. 1999). The cytoskeleton 47 determines the location of the Golgi, and depending on the 48 cellular model, either microtubules or actin filaments have 49 the greater influence (Egea and Rios 2008), the impact of 50 intermediate filaments being very limited (Gao and Sztul 51 2001; Gao et al. 2002;Styers et al. 2006; Toivola et al. 52 2005). Historically, microtubules were the first cytoskele-53 ton element to be linked to the Golgi structure and function 54 (Thyberg and Moskalewski 1999), and only later was it 55 firmly established that actin and associated proteins (actin 56 et al.) also played a significant role (for recent reviews see 44Histochem Cell Biol DOI 10.1007/s00418-013-1115 Author Proof U N C O R R E C T E D P R O O F63 between the actin-based cytoskeleton and the Golgi in a 64 variety of cellular models ...

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Role of Microtubules in the Organization of the Golgi Complex

Cited by 317 publications

References 212 publications

The Golgi Complex Is a Microtubule-organizing Organelle

The Golgi Complex Is a Microtubule-organizing Organelle

MTCL1 crosslinks and stabilizes non-centrosomal microtubules on the Golgi membrane

Actin acting at the Golgi

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