Dataset Information

Transcriptomic dynamics control rapid transition of core crop functions in 'lactating' pigeon

ABSTRACT:

Pigeons (Columba livia) are widely kept as domesticated pets worldwide, and may have adapted to captivity through the evolutionarily specialized ability to produce ‘milk’ in the crops of both male and female parents via rapid proliferation and shedding of lipid- and protein-enriched epithelial cells. Given the implications for understanding evolution in atricial species, a comprehensive transcriptomic perspective of the pigeon crop spanning the complete breeding cycle is warranted. Here, we generated a de novo pigeon genome assembly to construct a high resolution spatio-temporal transcriptomic landscape of the crop epithelium across the entire breeding cycle. This multi-omics analysis identified a set of ‘lactation’-related genes involved in lipid and protein metabolism that are highly expressed in the crop. Spatial transcriptomics analysis revealed extensive reorganization of long-range promoter-enhancer interactions linked to the dynamic expression of these ‘lactation’-related genes between stages. Moreover, their expression is spatially localized in specific epithelial layers, and can be correlated with phenotypic changes in the crop. This study thus illustrates the preferential de novo synthesis of ‘milk’ lipids and proteins in the crop epithelium prior to shedding from the lumen, and provides candidate enhancer loci for further investigation of the regulatory elements controlling pigeon ‘lactation’. Furthermore, these comprehensive datasets provide a foundational resource for avian and evolutionary biology research, especially relevant to atricial reproductive biology.

INSTRUMENT(S): Liquid Chromatography MS - negative - reverse phase, Liquid Chromatography MS - positive - reverse phase

SUBMITTER: yujie wang

PROVIDER: MTBLS5195 | MetaboLights | 2023-02-13

REPOSITORIES: MetaboLights

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			Action	DRS
	MTBLS5195	Other
	FILES	Other
	a_MTBLS5195_LC-MS_negative_reverse-phase_metabolite_profiling.txt	Txt
	a_MTBLS5195_LC-MS_positive_reverse-phase_metabolite_profiling.txt	Txt
	files-all.json	Other

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Project description:Butyrophilin 1A1 (BTN1A1) was first identified as a major integral protein of both the apical surface of mammary epithelial cells during lactation and the surface membrane surrounding lipid droplets in milk. Current evidence supports a role for BTN1A1 in the secretion of milk lipids as a membrane receptor, which forms a secretion complex with the redox enzyme, xanthine oxidoreductase (XDH). Capping of cytoplasmic lipid droplets with BTN1A1 and XDH serves to envelop the droplets with cellular membranes at the cell apex as an initial step in their subsequent release from the cell. The first evidence that BTN1A1 functions in this process was the generation of Btn1a1-/- mice, in which lipid secretion was disrupted and large unstable droplets were released into alveolar spaces with fragmented surface membranes. We have revisited this mutant mouse line using RNAseq and proteomic analysis to fully assess the consequences of ablating the Btn1a1 gene on the expression of other genes and proteins. Disruption of Btn1a1 expression led to a large build-up of Xdh (6-fold over wild-type levels) in the cytoplasm, induction of acute phase response genes and Lif-activation of STAT3 phosphorylation. At peak lactation, approx. 10% of the cells were dying, as assessed by TUNEL-analysis of nuclear DNA. Cell death appeared to proceed through expression of caspase 8 and activated caspase 3 and not via lysosomal lysis, which is the principal route for elimination of cells during mammary involution in wild-type mice. Other potential death pathways include autophagy and Slc5a8-mediated inactivation of survivin (Birc5). Milk secretion was prolonged by renewal of the secretory epithelium, as evidenced by the expression of cyclins, Fos/Jun and upregulation of Ki67 in approx. 10% of secretory cell nuclei. Thus a 21-day lactation cycle can be maintained, despite significant cell death by compensatory cell division, provided a milking stimulus is maintained. These data highlight the importance of BTN1A1 expression for the maintenance of terminally differentiated mammary epithelial cells and optimal milk production throughout lactation. From a practical standpoint, the complimentary RNAseq and proteomics data should provide a useful reference database for gene and protein expression in C57/Bl6 mice at peak lactation.

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Transcriptomic dynamics control rapid transition of core crop functions in 'lactating' pigeon

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