Large‐scale analysis reveals spatiotemporal circadian patterns of cilia transcriptomes in the primate brain. Issue 10 (26th July 2021)

• Record Type: Journal Article
• Authors: Baldi, Pierre; Alhassen, Wedad; Chen, Siwei; Nguyen, Henry; Khoudari, Mohammad; Alachkar, Amal
• Other Names: Johnson Elizabeth guestEditor.; Jones Kevin guestEditor.
• Is Part Of: Journal of neuroscience research. Volume 99:Issue 10(2021)
• Page Start: 2610
• Page End: 2624
• Publication Date: 2021-07-26
• Subjects: brain -- cilia -- circadian -- rhythm -- transcriptome; Neurobiology -- Periodicals; 612
• DOI: 10.1002/jnr.24919
• Languages: English
• ISSNs: 0360-4012

Abstract

Abstract: Cilia are dynamic subcellular systems, with core structural and functional components operating in a highly coordinated manner. Since many environmental stimuli sensed by cilia are circadian in nature, it is reasonable to speculate that genes encoding cilia structural and functional components follow rhythmic circadian patterns of expression. Using computational methods and the largest spatiotemporal gene expression atlas of primates, we identified and analyzed the circadian rhythmic expression of cilia genes across 22 primate brain areas. We found that around 73% of cilia transcripts exhibited circadian rhythmicity across at least one of 22 brain regions. In 12 brain regions, cilia transcriptomes were significantly enriched with circadian oscillating transcripts, as compared to the rest of the transcriptome. The phase of the cilia circadian transcripts deviated from the phase of the majority of the background circadian transcripts, and transcripts coding for cilia basal body components accounted for the majority of cilia circadian transcripts. In addition, adjacent or functionally connected brain nuclei had large overlapping complements of circadian cilia genes. Most remarkably, cilia circadian transcripts shared across the basal ganglia nuclei and the prefrontal cortex peaked in these structures in sequential fashion that is similar to the sequential order of activation of the basal ganglia‐cortical circuitry in connection with movement coordination, albeit on completely different timescales. These findings support a role for the circadian spatiotemporal orchestration of cilia gene expression in the normal physiology of the basal ganglia‐cortical circuit and motor control. Studying orchestrated cilia rhythmicity in the basal ganglia‐cortical circuits and other brain circuits may help develop better functional models, and shed light on the causal effects cilia functions have on these circuits and on the regulation of movement and other behaviors. Abstract : Spatiotemporal circadian patterns of cilia transcriptomes in the primate brain. Top‐left: Distribution of the peak phase of expression of the circadian cilia genes, and cumulative distribution of overlapped genes in different brain regions. Bottom‐left: Heatmap of 24‐hr oscillation of circadian cilia genes. Top‐right: Distribution of the peak phase of expression of the cilia substructural components' transcripts. Bottom‐right: Sequential order of Information flow and orchestrated circadian rhythmicity of cilia transcripts in the cortical‐basal ganglia‐cortical circuit.