American Journal of Plant Sciences
Vol.06 No.13(2015), Article ID:59207,8 pages
10.4236/ajps.2015.613212
The Evolution of Microtubule End-Binding Protein 1 (EB1) and Roles in Regulating Microtubule Behavior
Jiayu Liu1,2, Rong Han1,2*
1School of Life Science, Shanxi Normal University, Linfen, China
2Higher Education Key Laboratory of Plant Molecular and Environmental Stress Response (Shanxi Normal University) in Shanxi Province, Linfen, China
Email: 619248095@qq.com, *hhwrsl@163.com
Copyright © 2015 by authors and Scientific Research Publishing Inc.
This work is licensed under the Creative Commons Attribution International License (CC BY).
http://creativecommons.org/licenses/by/4.0/
Received 28 July 2015; accepted 22 August 2015; published 27 August 2015
ABSTRACT
All organisms must transmit genetic information to offspring through cell division, and mitotic spindle participates in the process. Spindle dynamics through depolymerization or polymerization of microtubules generates the driving force required for chromosome movements in mitosis. To date, studies have shown that microtubule arrays control the directions of cell division and diverse microtubule-associated proteins regulate cell division. But a clear picture of how microtubules and microtubule-associated proteins modulate cell division remains unknown. Depletion of end-binding protein 1 by RNA-mediated inhibition shows that one of the microtubule-associated proteins, end-binding protein 1, plays a crucial role in mitotic spindle formation and promotes microtubule dynamics and is needed for the proper segregation of mitotic chromosomes during anaphase in Drosophila cells. Here, we review the properties of end-binding protein 1 and the roles of end-binding protein
Keywords:
Microtubules, End-Binding Protein 1, Chromosome Segregation
1. Introduction
The microtubule cytoskeleton is essential for a variety of essential processes such as intracellular organization, intracellular transport, cell motility, and mitosis of eukaryotic cells. This is possible because of the intrinsic dynamic properties of microtubules. Microtubules (MTs) are dynamic hollow tubes comprising α, β-tubulin dimers that disassemble and reassemble at two ends: the slow-growing (minus) and fast-growing (plus) ends. It is now widely known that MT behavior is modulated by a number of MT-associated proteins (MAPs), which can influence dynamic instability parameters and consequently impact on mitotic progression and fidelity. Many of these MAPs share the ability to recognize only the distal part of a polymerizing MT, known as the MT plus end. For this reason, these MAPs are currently known as MT plus-end-tracking proteins (+TIPs) [1] [2] . Recently, +TIPs have emerged as regulators of MT dynamics. The plus end explores the cell periphery and shows dynamic instability, switching rapidly between the two phases of growth and shrinkage. Thus this dynamic scaffold performs a variety of very different functions. Genetic and biochemical studies have shown that +TIPs interact with each other and form protein complexes [3] .
End-binding protein 1 (EB1) promotes MT polymerization and interacts directly with many other +TIPs and cytoskeletal proteins such as cytoplasmic linker protein 170 (CLIP-170) and the dynactin large subunit p150Glued, and mitotic centromere-associated kinesin, microtubule-actin crosslinking factor and adenomatous polyposis coli (APC) [4] [5] . Thus, EB1 has been proposed to form the core of the microtubule plus-end complex and act as a hub in interactions with +TIPs [6] [7] .
Division of one cell into two genetically identical daughter cells occurs through two coordinated processes which are known as mitosis (division of the nucleus) and cytokinesis (division of the cytoplasm). The transition from interphase to mitosis involves a dramatic reorganization of the MT cytoskeleton. In fact, there is an increase in MT dynamics which occurs concomitantly with NEB that could be important for spindle morphogenesis [8] [9] . Studies have shown that accurate segregation of the replicated genome during cell division depends on dynamic attachments between kinetochores, proteinaceous structures assembled on the centromeric regions of chromosomes, and spindle microtubules. Kinetochores harness the forces generated by microtubule dynamics to drive chromosome segregation and ensure chromosome biorientation [10] . EB1 localizes to the plus ends of polymerizing MTs, suggesting that it may regulate MT dynamics during mitosis [11] . Depletion of Dm EB1 affects microtubule dynamics but causes minimal perturbation of microtubule organization in interphase cells. This result indicates that Dm EB1 promotes microtubule dynamics in Drosophila cells. Moreover, Dm EB1 is necessary for proper chromosomal segregation and spindle elongation during anaphase [12] . And studies show that together with APC, EB1 regulates chromosomal stability during mitosis [13] . So, EB1 is important for driving chromosome segregation by promoting microtubule dynamics. But a clear picture of how EB1 regulate microtubule behavior to drive chromosome segregation has not still emerged.
2. Microtubule Structure and Dynamics
Microtubules are intrinsically dynamic structures. In cells they are usually found in states of either growth or shrinkage and they exhibit rapid transitions between the two phases. This feature, termed dynamic instability, underlies many aspects of microtubule function including the ability to rearrange into different arrays [14] [15] . Microtubules are polymeric cylinders composed of α and β tubulin dimers. Rows of tubulin subunits, protofilaments, associate with each other laterally to form the microtubule lattice. Because they are arranged head to tail into 13 protofilaments that are aligned longitudinally in the tubule wall, microtubules are intrinsically polar: the plus-end where β-tubulin monomer is exposed, is the fast-growing end in vitro and the only end that grows in cells. The opposite (minus) end can slowly grow in vitro, while in cells it is usually stabilized or serves as the site of disassembly [16] . Microtubules are structurally polar and dynamic filaments that grow by addition of guanosine triphosphate (GTP)-loaded tubulin subunits to their end. After complex, largely unknown structural rearrangements at the nanoscale, GTP hydrolysis and phosphate release lead to the formation of a guanosine diphosphate (GDP)-loaded microtubule lattice. The matured microtubule lattice is protected from depolymerization by a stabilizing structure at the growing microtubule end. Stochastic loss of this end structure leads to depolymerization (catastrophe) [17] .
In cells, MT dynamics are not only regulated by the intrinsic dynamic instability of the polymers, but also by stabilizing/destabilizing structural MT-associated proteins (MAPs) that play a role in MT organization [18] . Among these, a large number of MAPs specifically recognize the terminal portion of MT. These are collectively known as MT plus-end-tracking proteins or +TIPs [1] . These +TIPs appear as comets in the MT tip, moving throughout the cell as MT grows and disappearing when MT shrinks [19] . One of these +TIPs, EB1 recruits several other proteins to growing microtubule ends and EB1 as a microtubule maturation factor and provide a mechanistic explanation for its effects on microtubule growth and catastrophe frequency, which cause microtubules to be more dynamic. EB1 binding accelerates conformational maturation in the microtubule, most likely by promoting lateral protofilament interactions and by accelerating reactions of the guanosine triphosphate (GTP) hydrolysis cycle. The microtubule maturation time is directly linked to the duration of a growth pause just before microtubule depolymerization, indicating an important role of the maturation time for the control of dynamic instability [20] .
3. The Microtubule Plus-End Binding Protein 1 (EB1) and Localization of EB
The EB1 protein is a member of the exciting and enigmatic family of microtubule (MT) tip-tracking proteins. EB1 acts as an exquisite marker of dynamic MT plus ends in some cases, whereas in others EB1 is thought to directly dictate the behavior of the plus ends [6] . EB1 was the first member identified in a yeast two-hybrid screen as an interactor of the C-terminus of the adenomatous polyposis coli (APC) tumor suppressor protein [21] . EBs are relatively small, elongated proteins (around 32 kDa) with conserved structural features. All members have at the N-terminal region an MT-binding portion containing a calponin homology (CH) domain with a highly conserved fold [2] . It was shown that this CH domain was both required and sufficient for binding to MT plus ends [22] [23] . The C-terminal portion of EB1, on the other hand, contains a coiled-coil region which is necessary for EB dimerization. The EEY/F motif at the flexible tail region provides a binding site for CAP-Gly domains found in select cytoskeleton-associated proteins, including a +TIP p150Glued [4] [24] . Members of the EB1 family (EBs) are mostly known for recruiting a variety of other plus-end-tracking proteins through interactions with their C-terminal EB homology domain [4] [25] [26] . The N-terminal microtubule binding domains bind to the outer microtubule surface in the grooves between adjacent protofilaments, close to the exchangeable GTP binding site [27] . End binding (EB) proteins are part of a highly conserved family which, in mammalians, comprises three members encoded from three different genes: EB1, EB2 (RP1), and EB3 (EB
4. Roles of EB
The dynamic properties of microtubules are regulated by multiple proteins. Two of them, EB1 and XMAP215 (chTOG in humans), are special in that they accumulate autonomously at microtubule ends [37] . EB1 is selective for growing ends (not distinguishing between plus and minus ends). And recruits several other proteins to growing microtubule ends and has seemingly antagonistic effects on microtubule dynamics [38] [39] . The first report regarding the possible role of EB proteins in MT dynamics came from the observation that, when overexpressed, these proteins induced the formation of acetylated MT bundles that were resistant to nocodazole treatment [40] . In addition, their ability to tip-track MTs led to the possibility that they might be involved in MT dynamics regulation, particularly in promoting MT growth [41] . This was confirmed in many independent studies using not only different model organisms such as budding and fission yeast, Drosophila, and human cells, but also in vitro systems [23] [42] [43] . Growing microtubule ends serve as transient binding platforms for essential proteins that regulate microtubule dynamics and their interactions with cellular substructures. End-binding proteins (EBs) autonomously recognize an extended region at growing microtubule ends with unknown structural characteristics and then recruit other factors to the dynamic end structure. The calponin homology (CH) domain of the fission yeast EB Mal3 bridges protofilaments except at the microtubule seam. By binding close to the exchangeable GTP-binding site, the CH domain is ideally positioned to sense the microtubule’s nucleotide state. The same microtubule-end region is also a stabilizing structural cap protecting the microtubule from depolymerization. This supports that there is a common structural link between microtubule dynamic instability and end tracking [27] . EB1 senses conformational changes within the microtubule lattice induced by reactions taking place as part of the GTP hydrolysis cycle [27] [44] . This leads to the well-known comet-like accumulation of EBs at the end region of growing microtubules where high-affinity binding sites are gradually lost with time [45] . The impact of EB proteins on interphase MT dynamics may also involve their interaction with other +TIPs. In fact, differences in the expression and regulation of several +TIPs in different cell types may be responsible for the observed differences in specific MT populations [46] . In addition, data derived from in vitro assays demonstrated that EB1 can act cooperatively with other +TIPs such as CLIP
5. Roles of Microtubule and EB1 in Cell Cycle
Proper regulation of MT (microtubule) dynamics is essential for various vital processes, including the segregation of chromosomes, directional cell migration and differentiation. Spindle dynamics through depolymerization or polymerization of microtubules (MT) generates the driving force required for chromosome movements in mitosis [55] . MT assembly and disassembly is modulated by a complex network of intracellular factors that co- operate or antagonize each other, are highly regulated in space and time and are thus attuned to the cell cycle and differentiation processes [56] . Cell-cycle progression is accompanied by changes in MT dynamics at very specific stages. This is accompanied by an increase in MT dynamics and an abrupt decrease in MT polymer level which tightly correlates with NEB [57] . So studies of roles of microtubule and EB1 are important to understand the life of plants.
Interactions between microtubules plus-end and the cell cortex are important for accurate positioning of the spindle [58] . During normal mitosis, the mitotic spindle positions itself at the geometric center of the cell. In S2 cells lacking Dm EB1, however, the spindle was frequently mis-positioned. This shows that mitotic spindle positioning requires EB1 activity. At the same time, the Loss of Dm EB1 function causes defects in mitotic spindle structure in metaphase cells that could be classified into four general categories. The most common defect was a complete loss of astral microtubules. The second class of defects lacked astral microtubules and exhibited an overall compaction of the spindle into a basket-like meshwork of microtubules surrounding the chromosomes. The third type of defect was a detachment of a spindle pole from the bundles of microtubules that were connected to the kinetochores. The fourth category of defect was “barrel-shaped” spindles that maintained their symmetry, but failed to focus the microtubules at the poles and also lacked astral microtubules [12] . So, will these prevent normal chromosome segregation during mitosis? Whether chromosome segregation will be abnormal in these cases remains unclear. Dm EB1 plays a crucial role in mitotic spindle formation and elongation and is needed for the proper segregation of mitotic chromosomes during anaphase, but how it to induce chromosome segregation by regulating spindle movement is still not fully clear. The first reports indicated that depletion of EB
Plants are prolific organisms covering the earth and are also irreplaceable partners for human beings. To enact morphogenesis, plants have evolved plant-specific MT arrays: cortical MTs, preprophase band, mitotic spindle, and phragmoplast. Plant microtubules (MTs) and MT-associated proteins (MAPs) are essential for fundamental morphogenesis, including controlling the direction of cell division and expansion, chromosome segregation, and cytokinesis. However, little is known about roles of EB
Acknowledgments
This work was supported by the National Nature Science Foundation of China under Grant number 30671061 and the Natural Science of Shanxi Province under Grant number 20081101, 2014011028-5.
Cite this paper
Jiayu Liu,Rong Han, (2015) The Evolution of Microtubule End-Binding Protein 1 (EB1) and Roles in Regulating Microtubule Behavior. American Journal of Plant Sciences,06,2114-2121. doi: 10.4236/ajps.2015.613212
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NOTES
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