Single-cell quantification of ribosome occupancy in early mouse development

Hakan Ozadam, Tori Tonn, Crystal M. Han, Alia Segura, Ian Hoskins, Shilpa Rao, Vighnesh Ghatpande, Duc Tran, David Catoe, Marc Salit and Can Cenik ()
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Hakan Ozadam: University of Texas at Austin
Tori Tonn: University of Texas at Austin
Crystal M. Han: San Jose State University
Alia Segura: University of Texas at Austin
Ian Hoskins: University of Texas at Austin
Shilpa Rao: University of Texas at Austin
Vighnesh Ghatpande: University of Texas at Austin
Duc Tran: San Jose State University
David Catoe: Joint Initiative for Metrology in Biology, SLAC National Accelerator Laboratory
Marc Salit: Joint Initiative for Metrology in Biology, SLAC National Accelerator Laboratory
Can Cenik: University of Texas at Austin

Nature, 2023, vol. 618, issue 7967, 1057-1064

Abstract: Abstract Translation regulation is critical for early mammalian embryonic development1. However, previous studies had been restricted to bulk measurements2, precluding precise determination of translation regulation including allele-specific analyses. Here, to address this challenge, we developed a novel microfluidic isotachophoresis (ITP) approach, named RIBOsome profiling via ITP (Ribo-ITP), and characterized translation in single oocytes and embryos during early mouse development. We identified differential translation efficiency as a key mechanism regulating genes involved in centrosome organization and N6-methyladenosine modification of RNAs. Our high-coverage measurements enabled, to our knowledge, the first analysis of allele-specific ribosome engagement in early development. These led to the discovery of stage-specific differential engagement of zygotic RNAs with ribosomes and reduced translation efficiency of transcripts exhibiting allele-biased expression. By integrating our measurements with proteomics data, we discovered that ribosome occupancy in germinal vesicle-stage oocytes is the predominant determinant of protein abundance in the zygote. The Ribo-ITP approach will enable numerous applications by providing high-coverage and high-resolution ribosome occupancy measurements from ultra-low input samples including single cells.

Date: 2023
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DOI: 10.1038/s41586-023-06228-9

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