TRIP13 is a protein-remodeling AAA+ ATPase that catalyzes MAD2 conformation switching

Ye, Qiaozhen; Rosenberg, Scott; Moeller, Arne; Speir, Jeffrey A.; Su, Tiffany Y; Corbett, K.D.

doi:10.7554/elife.07367

Cited by 150 publications

(235 citation statements)

References 91 publications

(150 reference statements)

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“…These results clearly demonstrate that maintenance of the SAC is critical to prevent cancer formation. TRIP13 has been shown to promote the dissociation of the MCC complex (15)(16)(17), which subsequently inactivates the SAC to prevent the completion of mitosis (18). Thus, overexpression of TRIP13 and silencing of MCC components have similar effects on cells, since both can lead to dysregulation of the SAC.…”

Section: Discussionmentioning

confidence: 96%

“…TRIP13 forms a stable hexameric ring, and ATP binding, as well as ATP hydrolysis, are critical for the function of the protein (13). Previous studies have revealed that TRIP13 is a novel component of the spindle assembly checkpoint (SAC) pathway (14)(15)(16)(17), which is crucial for the accurate distribution of duplicated chromosomes (18). Defects in the SAC pathway induce failure in chromosome separation and result in aneuploidy, which eventually leads to cellular apoptosis or transformation (19).…”

Section: Introductionmentioning

confidence: 99%

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TRIP13 is expressed in colorectal cancer and promotes cancer cell invasion

et al. 2016

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Abstract. Thyroid hormone receptor interactor 13 (TRIP13) is a member of the ATPases associated with various cellular activities family of proteins and is highly conserved in a wide range of species. Recent studies have demonstrated that TRIP13 is critical for the inactivation of the spindle assembly checkpoint and is associated with the progression of certain cancers. In the present study, the role of TRIP13 in colorectal cancer (CRC) was examined. Reverse transcription-quantitative polymerase chain reaction analysis revealed that TRIP13 messenger RNA was highly expressed in multiple CRC tissues. The depletion of TRIP13 in CRC cells suppressed cell proliferation, migration and invasion. To determine whether the catalytic activity of TRIP13 was critical for cancer progression, an inactive mutant of TRIP13 was expressed in CRC cells. The invasion of cancer cells that expressed the mutant TRIP13 was significantly reduced compared with that of the wild type TRIP13-expressing cancer cells. These results indicate that TRIP13 could be a potential target for CRC treatment. IntroductionThe ATPases associated with various cellular activities (AAA+) family of proteins comprises a functionally different group of enzymes that are involved in an array of cellular processes, including protein degradation, protein-complex disassembly and DNA replication (1). The AAA+ proteins are present in all kingdoms, and are characterized by the presence of conserved AAA+ domains that contain Walker A and Walker B motifs, followed by a conserved region called second region of homology (2). The majority of AAA+ proteins form hexamers to exert their biological functions. The chemical energy generated by adenosine triphosphate (ATP) hydrolysis by this family of proteins induces conformational changes in the substrate proteins to modulate their functions (3,4).A previous study reported that certain AAA+ enzymes are associated with tumor progression (5). For example, reptin [also known as RuvB-like (RUVBL) 2] and pontin (RUVBL1) have been demonstrated to be overexpressed in several tumors (5). These proteins interact with c-Myc or β-catenin, thus modulating their transcriptional activities to promote tumor progression (6). AAA+ proteins hydrolyze ATP, and thus, chemical inhibitors that disrupt the activities of cancer-associated AAA+ proteins may represent promising anti-cancer drugs.Thyroid hormone receptor interactor 13 (TRIP13, also known as 16E1BP and pachytene checkpoint 2) is a member of the AAA+ family proteins and is conserved in a wide range of species (7). It was first identified as a protein that interacts with human papilloma virus E1 proteins by a yeast two-hybrid analysis, but the physiological function of the interaction remains unknown (7). Accumulating studies have demonstrated that TRIP13 plays pivotal roles in meiotic recombination and DNA repair in plants, yeast, worms and mice (8-12). TRIP13 forms a stable hexameric ring, and ATP binding, as well as ATP hydrolysis, are critical for the function of the protein (13). Previous...

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Section: Discussionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

TRIP13 is expressed in colorectal cancer and promotes cancer cell invasion

et al. 2016

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“…The latter acts as a targeting protein for the binding of the ATPase to MCC (13,14). The energy of ATP hydrolysis is apparently used in this process to promote a conformational change of Mad2 back from C-Mad2 to O-Mad2, leading to loss of its affinity for Cdc20 in MCC and thus to Mad2 release.…”

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confidence: 99%

Role of CCT chaperonin in the disassembly of mitotic checkpoint complexes

Kaisari

Sitry-Shevah

Miniowitz-Shemtov

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The mitotic checkpoint system prevents premature separation of sister chromatids in mitosis and thus ensures the fidelity of chromosome segregation. When this checkpoint is active, a mitotic checkpoint complex (MCC), composed of the checkpoint proteins Mad2, BubR1, Bub3, and Cdc20, is assembled. MCC inhibits the ubiquitin ligase anaphase promoting complex/cyclosome (APC/C), whose action is necessary for anaphase initiation. When the checkpoint signal is turned off, MCC is disassembled, a process required for exit from checkpoint-arrested state. Different moieties of MCC are disassembled by different ATP-requiring processes. Previous work showed that Mad2 is released from MCC by the joint action of the TRIP13 AAA-ATPase and the Mad2-binding protein p31comet. Now we have isolated from extracts of HeLa cells an ATP-dependent factor that releases Cdc20 from MCC and identified it as chaperonin containing TCP1 or TCP1–Ring complex (CCT/TRiC chaperonin), a complex known to function in protein folding. Bacterially expressed CCT5 chaperonin subunits, which form biologically active homooligomers [Sergeeva, et al. (2013)J Biol Chem288(24):17734–17744], also promote the disassembly of MCC. CCT chaperonin further binds and disassembles subcomplexes of MCC that lack Mad2. Thus, the combined action of CCT chaperonin with that of TRIP13 ATPase promotes the complete disassembly of MCC, necessary for the inactivation of the mitotic checkpoint.

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“…Through analysis of conserved domains in the resulting proteins, we discovered that TSMS related genes often contain domains associated with sterility traits, including the AAA, AAI, BBOX, HLH, Knot1, RING, and SANT domains. The AAA domain confers ATPase activity, and correlates with abnormal development in plants (Ye et al, 2015). The AAI domain is found in the BcMF15 gene of B. oleracea, which is mainly expressed in the stamen, indicating that the AAI domain may participate in fertility regulation (Tian et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

“…The presence of the AAA domain defines the AAA family of proteins, which often perform chaperone-like functions to assist in the assembly, operation, or disassembly of proteins; these proteins exhibit high ATPase activity and oligomerization (Ye et al, 2015). The AAI domain is present in several crucial proteins involved in pollen development (Tian et al, 2009).…”

Section: Structure Of Tapetum Specific Male Sterility Related Proteinmentioning

confidence: 99%

Comparative sequence and expression analysis of tapetum specific male sterility related genes in Medicago truncatula

Lh¹,

Xw²,

Dx³

et al. 2016

Genet. Mol. Res.

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ABSTRACT. Heterosis, or enhancement through outbreeding, is one of the most promising approaches for increasing crop yield. Male sterility (MS), which promotes heterosis, has been widely applied in hybrid crop production. Medicago truncatula is a model legume species and is closely related to M. sativa, an important legume forage plant. Although the molecular mechanisms of MS in M. truncatula and M. sativa remain unclear, several studies of MS have been conducted in Arabidopsis thaliana. Previous research has shown that MS is associated with the destruction of tapetal cell layers. Disruption of tapetum developmental processes may result in pollen abortion. In an effort to identify genes useful for breeding in M. sativa, we identified MS related genes in M. truncatula using BLAST and homology to A. thaliana genes. In this study, we identified 63 tapetum specific male sterility (TSMS) related genes. The length of TSMS genes varied from 225 to 3747 bp. We identified 15 conserved domains and 8 cis-elements associated with TSMS related genes. Analysis of the phylogenetic relationships among these genes allowed them to be classified into three groups, MtTsms A, MtTsms B, and MtTsms C. Expression analyses revealed that these genes may be involved in developmental processes and response to abiotic stress.

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TRIP13 is a protein-remodeling AAA+ ATPase that catalyzes MAD2 conformation switching

Cited by 150 publications

References 91 publications

TRIP13 is expressed in colorectal cancer and promotes cancer cell invasion

TRIP13 is expressed in colorectal cancer and promotes cancer cell invasion

Role of CCT chaperonin in the disassembly of mitotic checkpoint complexes

Comparative sequence and expression analysis of tapetum specific male sterility related genes in Medicago truncatula

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