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Biology subjects

Sheets, M. D.

Publications and source records attributed to Sheets, M. D..

4 recordsLinked to original sources

An inducible tethered function assay reveals differential regulatory effects for the RNA-binding protein YBX3 and its domains.

RNA-binding protein (RBP) regulation is widespread across biology from development to learning and memory. Often RBPs contain multiple modular domains, which contribute to distinct RNA- binding activity or interactions necessary for regulation. However, assays to determine specific regulatory activity of individual domains are limited. The tethered function assay (TFA) provides a direct method to assess the functional activity of RBPs and their domains. The assay consists of two key components: (i) a reporter plasmid that encodes an mRNA, such as luciferase or GFP, engineered with high-affinity binding sites for an exogenous RNA-binding factor, and (ii) an effector construct that expresses a chimera of the RBP fused to the RNA-binding factor. Co- transfection of these constructs allows for measurement of reporter activity as a quantitative readout for RBP regulatory function. We developed an inducible TFA (iTFA) system through generation of a stable inducible mammalian cell line to express a reporter mRNA encoding nanoluciferase (nLuc) with six high-affinity MS2 binding sites within its 3 untranslated region. These cells can be transfected with a single plasmid that expresses an RBP fused to the MS2 coat protein. This approach enhances efficiency and reproducibility through reduction of transfection burden to a single plasmid and simplified normalization. We used this platform to dissect the individual and combined regulatory effects of YBX3 domains, a modular RBP with differential regulatory activity. The iTFA system provides a streamlined, tunable platform for functional analysis of RBPs that facilitates rapid interrogation of RBP or domain-specific activities in mammalian cells.

molecular biology↗

Conserved and diverged mechanisms for RNA target-site recognition by the multi KH-domain Bicaudal C protein

The Bicaudal-C (Bicc1) multi-KH domain RNA binding protein controls cell fates by binding and repressing the translation of specific target mRNAs. To provide new insights into Bicc1-RNA binding we used quantitative assays to analyze interactions between Xenopus Bicc1 protein and the 32-nt Bicc1 RNA target site from XlCripto-1 mRNA. High-affinity binding by XlBicc1(Kd=34nM) required both a 5 leader sequence and a 3loop sequence. Bicc1 proteins from humans (HsBicc1), zebrafish (DrBicc1) and fruit flies (DmBicc1) also bound the XlCripto-1 RNA with high-affinity via an interaction requiring the 5 leader sequence, providing evidence for a conserved mechanism of RNA recognition by Bicc1. However, in contrast to XlBicc1, each of the other species Bicc1s showed a significantly relaxed requirement for the 3 loop sequence. Analyses of mutant forms of XlBicc1, revealed that the KH1 domain promoted Bicc1s requirement for the loop sequence via a GXXG-independent mechanism. In addition, a fusion protein comprised of the XlKH1 and the DmBicc1-KH2-KH3 subdomains was sufficient to establish high-affinity, loop-sensitive Bicc1-binding to XlCripto-1 RNA. These data support a model wherein the KH2 domain interacts with the leader sequence via a GXXG-mediated KH-RNA interface, defining the conserved core of the metazoan Bicc1-RNA interaction, while the KH1 domain is required for the formation of a more flexible, secondary protein-RNA interface that allows recognition of the 3 loop sequence. This secondary interface differs between species and possibly between target mRNAs, establishing the potential for a range of translational repression activities for Bicc1 target mRNAs.

molecular biology↗

Frem1 activity regulated by Sonic Hedgehog signaling in the cranial neural crest mesenchyme guides midfacial morphogenesis

The Frem/Fras family of extracellular matrix proteins has been linked to human face shape variation and malformation, but little is known about their regulation and biological roles in facial development. During midfacial morphogenesis in mice, we observed Frem1 expression in the embryonic growth centers that form the median upper lip, nose, and palate. Expansive spatial gradients of Frem1 expression in the cranial neural crest cell (cNCC) mesenchyme of these tissues suggested transcriptional regulation by a secreted morphogen. Accordingly, Frem1 expression paralleled that of the conserved Sonic Hedgehog (Shh) target gene Gli1 in the cNCC mesenchyme. Suggesting direct transcriptional regulation by Shh signaling, we found that Frem1 expression is induced by SHH ligand stimulation or downstream pathway activation in cNCCs and observed GLI transcription factor binding at the Frem1 transcriptional start site during midfacial morphogenesis. Shh pathway antagonism reduced Frem1 expression during pathogenesis of midfacial hypoplasia, and FREM1 was sufficient to induce cNCC proliferation in a concentration-dependent manner. These findings provide novel insight into the mechanism by which the Shh pathway drives midfacial morphogenesis and reveal a functional role for Frem1 in cNCC biology that establishes the developmental basis for FREM1-associated face shape variation and malformation.

developmental biology↗

Bicc1 and dicer regulate left-right patterning through posttranscriptionalcontrol of the Nodal-inhibitor dand5

Rotating cilia at the vertebrate left-right organizer (LRO) generate an asymmetric leftward flow, which is sensed by cells at the left LRO margin. How the flow signal is processed and relayed to the laterality-determining Nodal cascade in the left lateral plate mesoderm (LPM) is largely unknown. We previously showed that flow down-regulates mRNA expression of the Nodal inhibitor Dand5 in left sensory cells. De-repression of the co-expressed Nodal drives LPM Nodal cascade induction. Here, we identify the mechanism of dand5 downregulation, finding that its posttranscriptional repression is a central process in symmetry breaking. Specifically, the RNA binding protein Bicc1 interacts with a proximal element in the 3-UTR of dand5 to repress translation in a dicer1-dependent manner. The bicc1/dicer1 module acts downstream of flow, as LRO ciliation was not affected upon its loss. Loss of bicc1 or dicer1 was rescued by parallel knockdown of dand5, placing both genes in the process of flow sensing.

developmental biology↗