Cell cycle roles for two 14-3-3 proteins during<i>Drosophila</i>development

Su, Tin Tin; Parry, Devin H.; Donahoe, Bryon; Chien, Cheng-Ting; O’Farrell, Patrick H.; Purdy, Amanda K.

doi:10.1242/jcs.114.19.3445

Cited by 58 publications

(9 citation statements)

References 38 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…As in the eye, we find that Tctp and 14-3-3 are required for the growth of the salivary gland. 14-3-3ε and 14-3-3ζ have redundant functions in imaginal discs [ 7 ], but have distinct roles in other tissues [ 9 , 28 ]. Our data show that 14-3-3ε, but not 14-3-3ζ, is essential for cell growth in salivary glands, providing additional evidence for isoform-specific functions of 14-3-3 proteins.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Tctp regulates the level and localization of Foxo for cell growth in Drosophila

Nam

Chung

et al. 2022

Cell Death Discov.

View full text Add to dashboard Cite

Regulation of cell size is crucial for organ development. Insulin signaling regulates organ size by antagonizing the subgroup O of forkhead box transcription factor (Foxo) through 14-3-3 in Drosophila. However, mechanisms for controlling the level and the nuclear localization of Foxo in developing organs are not well understood. Here, we investigate the role of Drosophila Translationally controlled tumor protein (Tctp) and its interacting partner 14-3-3 in Foxo regulation during organ development. Foxo overexpression in the developing eye disc results in growth inhibition. We show that Tctp overexpression antagonizes the Foxo effect by downregulating the Foxo level in the eye disc. Foxo overexpression or knockdown of Tctp in the larval salivary gland results in reduced gland size, mainly due to reduced cell size by defects in endoreplication. Whereas 14-3-3ζ knockdown has a negligible effect, knockdown of 14-3-3ε mimics the effect of Foxo overexpression or Tctp knockdown, suggesting an isoform-specific role of 14-3-3. Unlike nuclear enrichment of the endogenous Foxo in the salivary gland, overexpressed Foxo protein is largely distributed in the cytoplasm, and this mislocalization is restored by Tctp overexpression. Opposite to the effect of Tctp overexpression, Tctp knockdown increases cytoplasmic Foxo levels while decreasing nuclear Foxo levels. Together, our data suggest that Tctp and 14-3-3ε play critical roles in cell growth by reducing cytoplasmic Foxo levels. Knockdown of human TCTP also elevates the level of cytoplasmic FOXO1 in HeLa cells, suggesting that human TCTP may have a conserved role in downregulating FOXO in human cells.

show abstract

Section: Discussionmentioning

confidence: 99%

“…The main role of Foxo family proteins is to activate transcription [ 28 , 30 , 31 ]. However, our data show that the exogenous Foxo protein overexpressed in the salivary gland, which causes growth defects in the gland, is enriched in the cytoplasm (Fig.…”

Section: Discussionmentioning

confidence: 99%

Tctp regulates the level and localization of Foxo for cell growth in Drosophila

Nam

Chung

et al. 2022

Cell Death Discov.

View full text Add to dashboard Cite

show abstract

“…43 Similarly, the 14-3-3 protein has been implicated in the eye and the early neural development in Drosophila and mice. 44,45 On a different functional level, five of the detected pathways were also significant only in the eyed stage (Table 2). Again, the RAN pathway is involved in neural, brain and eye development.…”

Section: Resultsmentioning

confidence: 99%

Proteomic Profiling of Early Life Stages of European Grayling (Thymallus thymallus)

et al. 2010

View full text Add to dashboard Cite

Salmonids are teleost fish of profound research and economic interest. Embryonic development is a key aspect of salmonid biology that can be critically affected by environmental parameters. Still, their proteome during embryogenesis remains largely unexplored. This study investigates the proteome of the eyed-egg and hatching stages of embryonic development of a salmonid species, European grayling (Thymallus thymallus), using a shotgun proteomic approach. To deal with limited grayling protein resources, the generated spectra were compared against an all-salmonid database using search and multiple protein grouping algorithms to infer identifications. Functional enrichment analysis was carried out at different levels (gene ontologies, pathways, networks) using zebrafish as a reference genome. A total of 213 and 239 proteins were confidently detected in eyed and hatching stages, respectively. Cell cycle, energy, and protein metabolism were the major processes common to both stages. Nuclear activity and brain and eye development were the predominant functions in the eyed-stage proteome, while central nervous system, skeletal muscle, and heart development prevailed in the hatching stage. Overall, this research constitutes the first effort to describe the proteome during embryogenesis in grayling or any salmonid species. It also presents a systematic approach by which existing resources can enable proteome research in salmonids.

show abstract

“…Immunoblotting of the WCE and NE with anti-14-3-3β, γ, , σ, and ζ antibodies revealed that the total expression of all these isoforms was higher at the G 1 /S and G 2 /M phases of the cell cycle, particularly the expression of the σ and γ isoforms (Figure 5B). In addition to their role in cell signaling pathways, which would require the cytoplasmic presence of these proteins at all phases of the cell cycle, their role as check-point proteins (18,19,(45)(46)(47)(48)(49)(50)(51) may explain this increased expression. On the other hand, expression of the human replication origin binding protein, hOrc2p, whose expression and chromatin-bound state have been shown to be stable throughout the cell cycle (35), was approximately the same in both the WCE and the NE at all phases of the cell cycle (Figure 5B).…”

Section: Discussionmentioning

confidence: 99%

Analysis of the Cruciform Binding Activity of Recombinant 14-3-3ζ-MBP Fusion Protein, Its Heterodimerization Profile with Endogenous 14-3-3 Isoforms, and Effect on Mammalian DNA Replication in Vitro

et al. 2003

View full text Add to dashboard Cite

The human cruciform binding protein (CBP), a member of the 14-3-3 protein family, has been recently identified as an origin of DNA replication binding protein and involved in DNA replication. Here, pure recombinant 14-3-3zeta tagged with maltose binding protein (r14-3-3zeta-MBP) at its N-terminus was tested for binding to cruciform DNA either in the absence or presence of F(TH), a CBP-enriched fraction, by electromobility shift assay (EMSA), followed by Western blot analysis of the electroeluted CBP-cruciform DNA complex. The r14-3-3zeta-MBP was found to have cruciform binding activity only after preincubation with F(TH). Anti-MBP antibody immunoprecipitation of F(TH) preincubated with r14-3-3zeta-MBP, followed by Western blot analysis with antibodies specific to the beta, gamma, epsilon, zeta, and sigma 14-3-3 isoforms showed that r14-3-3zeta-MBP heterodimerized with the endogenous beta, epsilon, and zeta isoforms present in the F(TH) but not with the gamma or sigma isoforms. Immunoprecipitation of endogenous 14-3-3zeta from nuclear extracts (NE) of HeLa cells that were either serum-starved (s-s) or blocked at the G(1)/S or G(2)/M phases of the cell cycle revealed that at G(1)/S and G(2)/M, the zeta isoform heterodimerized only with the beta and epsilon isoforms, while in s-s extracts, the 14-3-3zeta/epsilon heterodimer was never detected, and the 14-3-3zeta/beta heterodimer was seldom detected. Furthermore, addition of r14-3-3zeta-MBP to HeLa cell extracts used in a mammalian in vitro replication system increased the replication level of p186, a plasmid bearing the minimal 186-bp origin of the monkey origin of DNA replication ors8, by approximately 3.5-fold. The data suggest that specific dimeric combinations of the 14-3-3 isoforms have CBP activity and that upregulation of this activity leads to an increase in DNA replication.

show abstract

Cell cycle roles for two 14-3-3 proteins duringDrosophiladevelopment

Cited by 58 publications

References 38 publications

Tctp regulates the level and localization of Foxo for cell growth in Drosophila

Tctp regulates the level and localization of Foxo for cell growth in Drosophila

Proteomic Profiling of Early Life Stages of European Grayling (Thymallus thymallus)

Analysis of the Cruciform Binding Activity of Recombinant 14-3-3ζ-MBP Fusion Protein, Its Heterodimerization Profile with Endogenous 14-3-3 Isoforms, and Effect on Mammalian DNA Replication in Vitro

Contact Info

Product

Resources

About