CFEOM1-Associated Kinesin KIF21A Is a Cortical Microtubule Growth Inhibitor

Vaart, Babet van der; Riel, Wilhelmina E. van; Doodhi, Harinath; Kevenaar, Josta T.; Katrukha, Eugene A.; Gumy, Laura F.; Bouchet, Benjamin Pierre; Grigoriev, Ilya; Spangler, Samantha A.; Yu, Ka Lou; Wulf, Phebe S.; Wu, Jingchao; Lansbergen, Gideon; Battum, Eljo Y. van; Pasterkamp, R. Jeroen; Mimori-Kiyosue, Yuko; Demmers, Jeroen; Olieric, Natacha; Maly, Ivan V.; Hoogenraad, Casper C.; Akhmanova, Anna

doi:10.1016/j.devcel.2013.09.010

Cited by 164 publications

(293 citation statements)

References 50 publications

(80 reference statements)

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“…We observed that it supressed microtubule growth velocities in a dose dependent manner with a minimal effect on catastrophe rate ( Figure S2E-H). The mode of action of kinesin-4 thus appeared to be conserved between animals and plants [21][22][23].…”

Section: Resultsmentioning

confidence: 99%

Shortening of Microtubule Overlap Regions Defines Membrane Delivery Sites during Plant Cytokinesis

et al. 2017

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SummaryDifferent from animal cells that divide by constriction of the cortex inwards, cells of land plants divide by initiating a new cell wall segment from their centre. For this, a disk-shaped, membrane-enclosed precursor termed the cell plate is formed that radially expands towards the parental cell wall [1][2][3]. The synthesis of the plate starts with the fusion of vesicles into a tubulo-vesicular network [4][5][6]. Vesicles are putatively delivered to the division plane by transport along microtubules of the bipolar phragmoplast network that guides plate assembly [7][8][9]. How vesicle immobilisation and fusion are then locally triggered is unclear. In general, a framework for how the cytoskeleton spatially defines cell plate formation is lacking. Here we show that membranous material for cell plate formation initially accumulates along regions of microtubule overlap in the phragmoplast of the moss Physcomitrella patens. Kinesin-4 mediated shortening of these overlaps at the onset of cytokinesis proved to be required to spatially confine membrane accumulation. Without shortening, the wider cell plate membrane depositions evolved into cell walls that were thick and irregularly shaped. Phragmoplast assembly thus provides a regular lattice of short overlaps on which a new cell wall segment can be scaffolded. Since similar patterns of overlaps form in central spindles of animal cells, involving the activity of orthologous proteins [10,11], we anticipate that our results will help uncover universal features underlying membrane-cytoskeleton coordination during cytokinesis. Results and DiscussionEarly ultrastructural work in the flowering plant Haemanthus katherinae has revealed that microtubules from the two halves of the phragmoplast interdigitate at the midplane where cell plate vesicles aggregate [12]. The same configuration exists in the phragmoplast of the moss Physcomitrella patens [13], indicating that it might be universally relevant for the spatial orchestration of cytokinesis in land plants. We therefore investigated whether regions of antiparallel microtubule overlap could have a direct role in determining the location of cell plate assembly in the genetically amenable moss P. patens ( Figure 1A). For this we imaged the conserved microtubule bundling protein MAP65c labelled with citrine (a GFP variant) as a marker for microtubule overlaps [14][15][16] in combination with the lipophilic dye FM4-64 that stained the membrane of the forming cell plate in life caulonema apical cells ( Figure 1A Whether kinesin-4 has a direct role in division plane reorientation is currently unclear because the underlying process is mechanistically not understood.The mechanism by which kinesin-4 induces overlap shortening was investigated using a purified recombinant N-terminal fragment of moss Kin4-Ic. We observed that it supressed microtubule growth velocities in a dose dependent manner with a minimal effect on catastrophe rate ( Figure S2E-H Having found a way to increase overlap length, we next examined the consequenc...

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Section: Resultsmentioning

confidence: 99%

Shortening of Microtubule Overlap Regions Defines Membrane Delivery Sites during Plant Cytokinesis

et al. 2017

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“…focal adhesions (FAs), that was described in the late 1990s (Kaverina et al, 1998). Specialized cortical complexes that involve +TIPs were shown to modulate this interaction (Lansbergen et al, 2006;van der Vaart et al, 2013;Wu et al, 2008;Bouchet et al, 2016), and the majority of existing data suggest that microtubules promote FA turnover (Stehbens and Wittmann, 2012) (Fig. 1).…”

Section: Introductionmentioning

confidence: 99%

Microtubules in 3D cell motility

Bouchet

Akhmanova

2017

Journal of Cell Science

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101

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Three-dimensional (3D) cell motility underlies essential processes, such as embryonic development, tissue repair and immune surveillance, and is involved in cancer progression. Although the cytoskeleton is a well-studied regulator of cell migration, most of what we know about its functions originates from studies conducted in twodimensional (2D) cultures. This research established that the microtubule network mediates polarized trafficking and signaling that are crucial for cell shape and movement in 2D. In parallel, developments in light microscopy and 3D cell culture systems progressively allowed to investigate cytoskeletal functions in more physiologically relevant settings. Interestingly, several studies have demonstrated that microtubule involvement in cell morphogenesis and motility can differ in 2D and 3D environments. In this Commentary, we discuss these differences and their relevance for the understanding the role of microtubules in cell migration in vivo. We also provide an overview of microtubule functions that were shown to control cell shape and motility in 3D matrices and discuss how they can be investigated further by using physiologically relevant models.

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“…Recent studies have shown that KIF21A suppresses cortical microtubule dynamics in neurons (Cheng et al 2014;van der Vaart et al 2013). KIF21A was originally identified as a motor protein that is expressed in neurons (Marszalek et al 1999).…”

Section: Microtubule-stabilizing Kinesins In Neuronsmentioning

confidence: 97%

“…Moreover, KIF21A is genetically associated with MAP1B, supporting the notion that KIF21A regulates microtubule dynamics. CFEOM1-associated mutations disrupt the autoinhibition of KIF21A, which results in the hyperactivation of KIF21A (Cheng et al 2014;van der Vaart et al 2013). Thus, it is considered that these mutations change the microtubule dynamics, and the axon guidance of occulomotor neurons is affected in CFEOM1.…”

Section: Microtubule-stabilizing Kinesins In Neuronsmentioning

confidence: 98%

“…In addition to the roles as sources of the force in intracellular transport and cell division, it has been revealed that Kinesin-8 and Kinesin-13 family members (such as KIF18A, KIF19A, and KIF2A-C) have microtubule-depolymerizing activities (Walczak et al 2013). In contrast, Kinesin-4 and Kinesin-11 members (such as KIF21A and KIF26A) have microtubule-stabilizing activities (Zhou et al 2009;van der Vaart et al 2013). Recent studies have shown that these atypical KIFs play fundamental roles in cellular morphogenesis.…”

Section: Introductionmentioning

confidence: 94%

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Kinesin superfamily proteins and the regulation of microtubule dynamics in morphogenesis

Niwa

2014

Anat Sci Int

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Kinesin superfamily proteins (KIFs) are microtubule-dependent molecular motors that serve as sources of force for intracellular transport and cell division. Recent studies have revealed new roles of KIFs as microtubule stabilizers and depolymerizers, and these activities are fundamental to cellular morphogenesis and mammalian development. KIF2A and KIF19A have microtubule-depolymerizing activities and regulate the neuronal morphology and cilia length, respectively. KIF21A and KIF26A work as microtubule stabilizers that regulate axonal morphology. Morphological defects that are similar to human diseases are observed in mice in which these KIF genes have been deleted. Actually, KIF2A and KIF21A have been identified as causes of human neuronal diseases. In this review, the functions of these atypical KIFs that regulate microtubule dynamics are discussed. Moreover, some interesting unanswered questions and hypothetical answers to them are discussed.

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CFEOM1-Associated Kinesin KIF21A Is a Cortical Microtubule Growth Inhibitor

Cited by 164 publications

References 50 publications

Shortening of Microtubule Overlap Regions Defines Membrane Delivery Sites during Plant Cytokinesis

Shortening of Microtubule Overlap Regions Defines Membrane Delivery Sites during Plant Cytokinesis

Microtubules in 3D cell motility

Kinesin superfamily proteins and the regulation of microtubule dynamics in morphogenesis

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