Innate immunity in the C. elegans intestine is programmed by a neuronal regulator of AWC olfactory neuron development
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ABSTRACT:
PROVIDER: PRJNA542089 | ENA |
REPOSITORIES: ENA
Dataset's files
| Action | DRS | |||
|---|---|---|---|---|
| SRR9034490.fastq.gz | Fastqsanger.gz | |||
| SRR9034491.fastq.gz | Fastqsanger.gz | |||
| SRR9034492.fastq.gz | Fastqsanger.gz | |||
| SRR9034493.fastq.gz | Fastqsanger.gz | |||
| SRR9034487.fastq.gz | Fastqsanger.gz |
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Project description:Olfactory neurons allow animals to discriminate nutritious food sources from potential pathogens. From a forward genetic screen, we uncovered a surprising requirement for the olfactory neuron gene olrn-1 in the regulation of intestinal epithelial immunity in Caenorhabditis elegans. During nematode development, olrn-1 is required to program the expression of odorant receptors in the AWC olfactory neuron pair. Here, we show that olrn-1 also functions in AWC neurons in the cell non-autonomous suppression of the canonical p38 MAPK PMK-1 immune pathway in the intestine. Low activity of OLRN-1, which activates the p38 MAPK signaling cassette in AWC neurons during larval development, also de-represses the p38 MAPK PMK-1 pathway in the intestine to promote immune effector transcription, increased clearance of an intestinal pathogen and resistance to bacterial infection. These data reveal an unexpected connection between olfactory receptor development and innate immunity, and show that anti-pathogen defenses in the intestine are developmentally programmed.
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Project description:Olfactory neurons allow animals to discriminate nutritious food sources from potential pathogens. From a forward genetic screen, we uncovered a surprising requirement for the olfactory neuron gene olrn-1 in the regulation of intestinal epithelial immunity in Caenorhabditis elegans. During nematode development, olrn-1 is required to program the expression of odorant receptors in the AWC olfactory neuron pair. Here, we show that olrn-1 also functions in AWC neurons in the cell non-autonomous suppression of the canonical p38 MAPK PMK-1 immune pathway in the intestine. Low activity of OLRN-1, which activates the p38 MAPK signaling cassette in AWC neurons during larval development, also de-represses the p38 MAPK PMK-1 pathway in the intestine to promote immune effector transcription, increased clearance of an intestinal pathogen, and resistance to bacterial infection. These data reveal an unexpected connection between olfactory receptor development and innate immunity and show that anti-pathogen defenses in the intestine are developmentally programmed.
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Project description:Sensory neuron diversity is required for organisms to decipher complex environmental cues. In Drosophila, olfactory environment is detected by 50 different olfactory receptor neuron (ORN) classes that are clustered in combinations within distinct sensilla subtypes. Each sensilla subtype houses stereotypically clustered 1-4 ORN identities that arise through asymmetric divisions from a single multipotent sensory organ precursor (SOP). How each class of SOPs acquires a unique differentiation potential that accounts for ORN diversity is unknown. Previously, we reported a critical component of SOP diversification program, Rotund (Rn), which functions to increase ORN diversity by generating novel developmental trajectories from existing precursors within each independent sensilla type lineages. Here, we show that Rn, along with BarH1/H2, Bric-Ã -brac (Bab), Apterous (Ap) and Dachshund (Dac), constitute a functionally conserved transcription factor (TF) network, previously shown to pattern the segmentation of the leg, that patterns the developing olfactory tissue. Precursors with diverse ORN differentiation potentials are selected from concentric rings defined by unique combinations of these TFs along the proximodistal axis of the developing antennal disc. The combinatorial code that demarcates each precursor field is set up by cross-regulatory interactions among different factors within the network. Modifications of this network lead to predictable changes in the diversity of sensilla subtypes and ORN pools. In light of our data, we propose a molecular map that defines Time-course RNAseq across 4 developmental stages, inlcuding flies mutant for rotund gene (rn), heterozygotes and wildtype
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Project description:How functional cellular heterogeneities are regulated is fundamental for understanding the molecular basis of complex organs. Olfactory sensory neurons (OSNs) are an ideal model to investigate the regulation of cellular heterogeneity. The “one-neuron-one-receptor” organization and topographical mapping ensure the detection and precise translation of odor signals to the central neural system. Besides the diversity of OR genes and other molecular guiding axon sorting processes, single-cell transcriptome analysis revealed an OSN subpopulation, defined by Cd36, a lipid receptor gene. The function study exhibited lipid odor identification was impaired in Cd36-deficient mice. In this study, we systematically depicted the transcriptome diversity, spatial distribution, and specific functions of Cd36+ OSNs in the mouse olfactory epithelium. The specific molecular features of Cd36+ OSN we revealed implemented the programmed cellular diversity may be driven by their olfaction function. Furthermore, with the integrative analysis of single-cell transcriptome and epigenome profiles, we revealed the cis and trans regulatory signatures in Cd36+ OSN and identified Tshz1 and Mef2 as the key regulators that may directly regulate and promote the expression of Cd36 and drive the cellular diversity of OSNs. Especially, we demonstrated that Tshz1 is expressed coordinately with the choices of ORs, earlier than the expression of Cd36, which indicates it may act as a pioneer factor that instructs the lineage-specific expression of Cd36 and other genes, eventually leading to the cellular diversity of Cd36+ OSN. Our results provide novel knowledge on the regulation mechanism of cellular diversity of complex organs.
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