DNA-Binding Properties of Mblk-1, a Putative Transcription Factor from the Honeybee

Park, Jung-Min; Kunieda, Takekazu; Takeuchi, Hideaki; Kubo, Takeo

doi:10.1006/bbrc.2002.6397

Cited by 24 publications

(21 citation statements)

References 13 publications

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“…The E93 protein contains a helix-turn-helix DNA binding domain of the Pipsqueak family (35). This 54-aa domain is highly conserved within the E93 family of orthologs and, for the honey bee ortholog (Mblk-1), has been shown to bind DNA (36). With one exception, all E93 orthologs contain nuclear receptor interaction motifs (LXXLL motifs) (37).…”

Section: Discussionmentioning

confidence: 99%

“…The biological roles of the E93 family have not been well characterized. The C. elegans ortholog (MBR-1) is required for the pruning of excess neurites during the larval stages (41), and Mblk-1 is expressed within the mushroom bodies, regions of the brain thought to be involved in learning, memory, and sensory integration (36). In humans, the roles of LCoR are not yet known, but its paralog LCoR-Like has been associated with control of height (42,43).…”

Section: Discussionmentioning

confidence: 99%

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Control of target gene specificity during metamorphosis by the steroid response gene E93

Mou

Duncan

Baehrecke

et al. 2012

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

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Hormonal control of sexual maturation is a common feature in animal development. A particularly dramatic example is the metamorphosis of insects, in which pulses of the steroid hormone ecdysone drive the wholesale transformation of the larva into an adult. The mechanisms responsible for this transformation are not well understood. Work in Drosophila indicates that the larval and adult forms are patterned by the same underlying sets of developmental regulators, but it is not understood how the same regulators pattern two distinct forms. Recent studies indicate that this ability is facilitated by a global change in the responsiveness of target genes during metamorphosis. Here we show that this shift is controlled in part by the ecdysone-induced transcription factor E93. Although long considered a dedicated regulator of larval cell death, we find that E93 is expressed widely in adult cells at the pupal stage and is required for many patterning processes at this time. To understand the role of E93 in adult patterning, we focused on a simple E93-dependent process, the induction of the Dll gene within bract cells of the pupal leg by EGF receptor signaling. In this system, we show that E93 functions to cause Dll to become responsive to EGF receptor signaling. We demonstrate that E93 is both necessary and sufficient for directing this switch. E93 likely controls the responsiveness of many other target genes because it is required broadly for patterning during metamorphosis. The wide conservation of E93 orthologs suggests that similar mechanisms control life-cycle transitions in other organisms, including vertebrates.Distal-less | Eip93F | epidermal growth factor receptor | ultraspiracle | heterochrony S teroid hormones control metabolism, reproduction, and development in many organisms and have been linked to numerous human health problems. Steroids often control major transitions in the life cycle, regulating distinct cell responses in a stage-specific manner. Despite their global importance in development, relatively little is known about how steroid hormones control such stage-specific responses. One of the most dramatic life-cycle transitions driven by steroids is the metamorphosis of insects, in which there is a wholesale transformation of the larva into the adult. In Drosophila, metamorphosis is triggered by pulses of the steroid hormone 20-OH ecdysone (ecdysone) (reviewed in refs. 1-4). A complex of ecdysone bound to its nuclear receptor, a heterodimer of the ecdysone receptor (EcR) and the RXR ortholog Ultraspiracle (Usp), directly activates a small number of primary response genes, including E93, which in turn regulate many secondary response genes that function more directly in controlling cell fate. The role of ecdysone signaling in early events of metamorphosis, such as the death of larval cells and the morphogenesis of adult structures, has been studied extensively. However, mechanisms underlying the control of adult cell fates by ecdysone have been poorly characterized.In adult cells, many genes seem to un...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Control of target gene specificity during metamorphosis by the steroid response gene E93

Mou

Duncan

Baehrecke

et al. 2012

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

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“…3). Kakugo RNA was not detected in the honeybee genome, whereas a single band was detected for the MB-preferential transcription factor Mblk-1 (26,27,33), indicating that Kakugo RNA is not encoded by the honeybee genome. Furthermore, the Kakugo RNA sequence is not included in the genomic sequences annotated and registered to date by the honeybee genome project (Human Genome Sequencing Center at Baylor College of Medicine [http:// hgsc.bcm.tmc.edu/projects/honeybee/]).…”

Section: Identification Ofmentioning

confidence: 91%

Novel Insect Picorna-Like Virus Identified in the Brains of Aggressive Worker Honeybees

Fujiyuki

Takeuchi²,

Ono

et al. 2004

J Virol

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149

141

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To identify candidate genes involved in the aggressive behavior of worker honeybees, we used the differential display method to search for RNAs exclusively detected in the brains of aggressive workers that had attacked a hornet. We identified a novel, 10,152-nucleotide RNA, termed Kakugo RNA. Kakugo RNA encodes a protein of 2,893 amino acid residues that shares structural features and sequence similarities with various picorna-like virus polyproteins, especially those from sacbrood virus, which infects honeybees. The Kakugo protein contains several domains that correspond to the virion protein, helicase, protease, and RNA-dependent RNA polymerase domains of various picorna-like virus polyproteins. When the worker bee tissue lysate was subjected to sucrose density gradient centrifugation, Kakugo RNA, except for the material at the bottom, was separated into two major peaks. One of the peaks corresponded to the position of Kakugo mRNA, and the other corresponded to the position of the poliovirus virion. These results suggest that the Kakugo RNA exists as an mRNA-like free RNA and virion RNA in the honeybee. Furthermore, injection of the lysate supernatant from the attacker heads into the heads of noninfected bees resulted in a marked increase in Kakugo RNA. These results demonstrate that Kakugo RNA is a plus-strand RNA of a novel picorna-like virus and that the brains of aggressive workers are infected by this novel virus. Kakugo RNA was detected in aggressive workers but not in nurse bees or foragers. In aggressive workers, Kakugo RNA was detected in the brain but not in the thorax or abdomen, indicating a close relation between viral infection in the brain and aggressive worker behaviors.The European honeybee Apis mellifera L. is a eusocial insect, and the workers perform diverse tasks to maintain colony activity, such as comb-building, nursing, guarding, and foraging, according to age after eclosion (age polyethism) (36). Guard bees gathering at the entrance of the hive are highly aggressive and often scramble to counterattack natural enemies, such as hornets, to protect the colony (4, 5). The worker honeybee stinger is part of a highly modified ovipositor that evolved for defensive functions. The stinger is hooked and the worker loses it after use, resulting in the death of the bee. The advantage of losing the stinger is that the venom sac is then activated to inject additional venom after the sac detaches from the abdomen of the workers. The attacking behavior of guard bees is self-sacrificing and is therefore considered to be a typical altruistic behavior exhibited by the workers (35). Thus, the honeybee is an attractive model for the study of altruistic aggressive behaviors. Quantitative trait locus analysis has been used to identify the loci related to aggressive worker behaviors (11, 12). The genes responsible for the aggressive behaviors, however, have not yet been identified.Previously, members of our laboratories used the differential display method to identify genes expressed preferentially in the mus...

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“…Truncated Mblk-1 protein that contains either RHF1 or RHF2 can also bind MBE but with much lower affinity than intact Mblk-1. An in vitro pull-down assay indicated that RHF1 and RHF2 afford homodimeric bindings, suggesting that Mblk-1 functions as a dimer (13). These results suggest that Mblk-1 is a transcription factor that functions in the MB neural circuits in the honeybee brain.…”

mentioning

confidence: 76%

“…Among them, RHF2 was necessary for Mblk-1 activity. Although truncated Mblk-1 containing RHF1 can also bind to MBE in vitro (13), there was no appreciable decrease in the transactivation activity of RHF1 deletion mutants in the luciferase assay. At present, it is not clear whether RHF1 has some functions in Mblk-1.…”

Section: Mblk-1-induced Transactivation Was Stimulated By the Ras/ Mamentioning

confidence: 87%

The Activity of Mblk-1, a Mushroom Body-selective Transcription Factor from the Honeybee, Is Modulated by the Ras/MAPK Pathway

Park

Kunieda

Kubo

2003

Journal of Biological Chemistry

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We previously identified a gene, termed Mblk-1, that encodes a putative transcription factor with two DNA-binding motifs expressed preferentially in the mushroom body of the honeybee brain, and its preferred binding sequence, termed Mblk-1-binding element (MBE) (Takeuchi, H., Kage, E., Sawata, M., Kamikouchi, A., Ohashi, K., Ohara, M., Fujiyuki, T., Kunieda, T., Sekimizu, K., Natori, S., and Kubo, T. The honeybee Apis mellifera L. is a social insect, and colony members perform various exquisite communications to maintain colony activities. Worker bees inform the other foragers of the direction and distance of a food source using dance language (1, 2), which might require complex processing of sensory information in their brains. Little is known, however, regarding the molecular basis of their highly advanced behavior.Mushroom bodies (MBs) 1 are believed to be involved in sensory integration, learning, and memory in insects (3, 4). The honeybee MBs are well developed when compared with those of other insects. In the honeybee, the ratio of volume of MBs to that of whole brain is ϳ12%, whereas that of Drosophila is ϳ2% (5). Moreover, each MB of the honeybee has two calyces composed of two morphologically distinct types of interneurons, the large-and small-type Kenyon cells (5-7). On the other hand, in Drosophila, there is only one calyx, and the Kenyon cells are morphologically indistinct (8). These observations suggest that MB function is closely associated with the advanced honeybee behaviors.To identify molecules involved in the highly advanced behaviors of the honeybees, we previously used the differential display method to identify a gene, termed Mblk-1, that is expressed preferentially in the large-type Kenyon cells of the honeybee brain (9). Mblk-1 encodes a novel protein consisting of 1598 amino acid residues with significant similarity to a nuclear factor encoded by the Drosophila melanogaster CG18389/E93 gene. The CG18389/E93 gene was identified previously as an ecdysone-inducible gene in the prepupal salivary gland (10) and was reported to encode a nuclear protein that is required for ecdysone-triggered programmed cell death during metamorphosis (11). The expression of CG18389/E93 in the adult and the biochemical characteristics of the protein, however, have not been examined.Two putative DNA-binding motifs, termed RHF (region conserved between honeybee and fruit fly) 1 and RHF2, a nuclear localization signal, and Gln run were conserved between Mblk-1 and Drosophila E93 protein (9). RHF2 has significant sequence homology with proteins encoded by genes from nematoda (a polypeptide predicted by an open reading frame of the Caenorhabditis elegans cosmid T01C1), human (three polypeptides predicted by open reading frames of the chromosome 4 clone RP11-173B23 map 4, chromosome 11 clone RP11-162M10 map 11, and chromosome 10 clone RP11-175019, respectively), mouse (12), and sea urchin (a polypeptide predicted by an open reading frame of the Strongylocentrotus purpuratus EST253 coelomocyte cDNA 5Ј-end), suggestin...

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DNA-Binding Properties of Mblk-1, a Putative Transcription Factor from the Honeybee

Cited by 24 publications

References 13 publications

Control of target gene specificity during metamorphosis by the steroid response gene E93

Control of target gene specificity during metamorphosis by the steroid response gene E93

Novel Insect Picorna-Like Virus Identified in the Brains of Aggressive Worker Honeybees

The Activity of Mblk-1, a Mushroom Body-selective Transcription Factor from the Honeybee, Is Modulated by the Ras/MAPK Pathway

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