Plk1 negatively regulates PRC1 to prevent premature midzone formation before cytokinesis

Hu, Chi-Kuo; Özlü, Nurhan; Coughlin, Margaret; Steen, Judith Jebanathirajah; Mitchison, Timothy J.

doi:10.1091/mbc.e12-01-0058

Cited by 88 publications

(95 citation statements)

References 40 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This result suggests that establishment and maintenance of bipolarity in the preanaphase spindle are ensured by other proteins (e.g., kinesins), as is the case in animals or flowering plants (Bannigan et al, 2007). Human PRC1 is negatively regulated by Polo-like kinase1 in preanaphase to prevent premature midzone formation, and targeting of Arabidopsis MAP65-1 to the metaphase spindle is also inhibited by Cdk1 (Mao et al, 2005;Hu et al, 2012). Similar kinase-dependent regulation may be present in P. patens, possibly through the conserved Cdk1 site.…”

Section: Map65 Is Required For Bipolar Arrangement Of Phragmoplast Mtmentioning

confidence: 96%

MICROTUBULE-ASSOCIATED PROTEIN65 Is Essential for Maintenance of Phragmoplast Bipolarity and Formation of the Cell Plate inPhyscomitrella patens

et al. 2013

View full text Add to dashboard Cite

The phragmoplast, a plant-specific apparatus that mediates cytokinesis, mainly consists of microtubules (MTs) arranged in a bipolar fashion, such that their plus ends interdigitate at the equator. Membrane vesicles are thought to move along the MTs toward the equator and fuse to form the cell plate. Although several genes required for phragmoplast MT organization have been identified, the mechanisms that maintain the bipolarity of phragmoplasts remain poorly understood. Here, we show that engaging phragmoplast MTs in a bipolar fashion in protonemal cells of the moss Physcomitrella patens requires the conserved MT cross-linking protein MICROTUBULE-ASSOCIATED PROTEIN65 (MAP65). Simultaneous knockdown of the three MAP65s expressed in those cells severely compromised MT interdigitation at the phragmoplast equator after anaphase onset, resulting in the collapse of the phragmoplast in telophase. Cytokinetic vesicles initially localized to the anaphase midzone as normal but failed to further accumulate in the next several minutes, although the bipolarity of the MT array was preserved. Our data indicate that the presence of bipolar MT arrays is insufficient for vesicle accumulation at the equator and further suggest that MAP65-mediated MT interdigitation is a prerequisite for maintenance of bipolarity of the phragmoplast and accumulation and/or fusion of cell plate-destined vesicles at the equatorial plane.

show abstract

Section: Map65 Is Required For Bipolar Arrangement Of Phragmoplast Mtmentioning

confidence: 96%

MICROTUBULE-ASSOCIATED PROTEIN65 Is Essential for Maintenance of Phragmoplast Bipolarity and Formation of the Cell Plate inPhyscomitrella patens

et al. 2013

View full text Add to dashboard Cite

show abstract

“…The affinity of PRC1 to bind to microtubules is regulated by phosphorylation and dephosphorylation events precisely timed throughout mitosis 11, 20. Due to dephosphorylation, PRC1 forms dimers and binds to microtubules to form cross‐linkages between neighboring interdigitating fibers 11, 21.…”

Section: Introductionmentioning

confidence: 99%

PRC 1‐labeled microtubule bundles and kinetochore pairs show one‐to‐one association in metaphase

et al. 2016

View full text Add to dashboard Cite

In the mitotic spindle, kinetochore microtubules form k‐fibers, whereas overlap or interpolar microtubules form antiparallel arrays containing the cross‐linker protein regulator of cytokinesis 1 (PRC1). We have recently shown that an overlap bundle, termed bridging fiber, links outermost sister k‐fibers. However, the relationship between overlap bundles and k‐fibers throughout the spindle remained unknown. Here, we show that in a metaphase spindle more than 90% of overlap bundles act as a bridge between sister k‐fibers. We found that the number of PRC1‐GFP‐labeled bundles per spindle is nearly the same as the number of kinetochore pairs. Live‐cell imaging revealed that kinetochore movement in the equatorial plane of the spindle is highly correlated with the movement of the coupled PRC1‐GFP‐labeled fiber, whereas the correlation with other fibers decreases with increasing distance. Analysis of endogenous PRC1 localization confirmed the results obtained with PRC1‐GFP. PRC1 knockdown reduced the bridging fiber thickness and interkinetochore distance throughout the spindle, suggesting a function of PRC1 in bridging microtubule organization and force balance in the metaphase spindle.

show abstract

“…During mitosis, the cyclin-dependent kinase Cdk1-cyclin-B phosphorylates centralspindlin, inhibiting its association with the spindle (Mishima et al 2004), and Ect2, inhibiting its association with both the plasma membrane and centralspindlin (Yüce et al 2005;Su et al 2011). Similarly, inhibitory phosphorylation by Cdk1 and the polo-like kinase Plk1 on PRC1 limits PRC1 localization during the cell cycle (Zhu et al 2006;Hu et al 2012). PRC1 shows multiple modes of microtubule binding, depending on its interaction partners in the midzone, notably Kif4 (Subramanian et al 2013).…”

Section: Temporal Control In Metazoamentioning

confidence: 99%

Cytokinesis in Metazoa and Fungi

Glotzer

2016

Cold Spring Harb Perspect Biol

View full text Add to dashboard Cite

SUMMARYCell division-cytokinesis-involves large-scale rearrangements of the entire cell. Primarily driven by cytoskeletal proteins, cytokinesis also depends on topological rearrangements of the plasma membrane, which are coordinated with nuclear division in both space and time. Despite the fundamental nature of the process, different types of eukaryotic cells show variations in both the structural mechanisms of cytokinesis and the regulatory controls. In animal cells and fungi, a contractile actomyosin-based structure plays a central, albeit flexible, role. Here, the underlying molecular mechanisms are summarized and integrated and common themes are highlighted.

show abstract

Plk1 negatively regulates PRC1 to prevent premature midzone formation before cytokinesis

Abstract: Plk1, but not Cdk1, phosphorylates PRC1 on Thr-602 to prevent premature midzone assembly in metaphase. Microtubules enhance this phosphorylation. Plk1, PRC1, and microtubules together regulate homeostatic MT bundling throughout cell division.

Cited by 88 publications

References 40 publications

MICROTUBULE-ASSOCIATED PROTEIN65 Is Essential for Maintenance of Phragmoplast Bipolarity and Formation of the Cell Plate inPhyscomitrella patens

MICROTUBULE-ASSOCIATED PROTEIN65 Is Essential for Maintenance of Phragmoplast Bipolarity and Formation of the Cell Plate inPhyscomitrella patens

PRC 1‐labeled microtubule bundles and kinetochore pairs show one‐to‐one association in metaphase

Cytokinesis in Metazoa and Fungi

Contact Info

Product

Resources

About