Rapid diffusion-state switching underlies stable cytoplasmic gradients in the Caenorhabditis elegans zygote

Youjun Wu, Bingjie Han, Younan Li, Edwin Munro, David J. Odde, Erik E. Griffin

Research output: Contribution to journalArticlepeer-review

36 Scopus citations

Abstract

Protein concentration gradients organize cells and tissues and commonly form through diffusion away from a local source of protein. Interestingly, during the asymmetric division of the Caenorhabditis elegans zygote, the RNA-binding proteins MEX-5 and PIE-1 form opposing concentration gradients in the absence of a local source. In this study, we use near-total internal reflection fluorescence (TIRF) imaging and single-particle tracking to characterize the reaction/diffusion dynamics that maintain the MEX-5 and PIE-1 gradients. Our findings suggest that both proteins interconvert between fast-diffusing and slow-diffusing states on timescales that are much shorter (seconds) than the timescale of gradient formation (minutes). The kinetics of diffusion-state switching are strongly polarized along the anterior/posterior (A/ P) axis by the PAR polarity system such that fast-diffusing MEX-5 and PIE-1 particles are approximately symmetrically distributed, whereas slow-diffusing particles are highly enriched in the anterior and posterior cytoplasm, respectively. Using mathematical modeling, we show that local differences in the kinetics of diffusion-state switching can rapidly generate stable concentration gradients over a broad range of spatial and temporal scales.

Original languageEnglish (US)
Pages (from-to)E8440-E8449
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number36
DOIs
StatePublished - Sep 4 2018

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. We thank Katya Voronina, Jamie Moseley, Geraldine Seydoux, and E.E.G. laboratory members for comments. Research in the E.E.G. and D.J.O. laboratories is supported by NIH Grant R01GM110194 (to E.E.G.). Research in the E.M. laboratory is supported by NIH Grant R01GM098441 (to E.M.). The TIRF system used in this study is supported by NIH Grant S10OD018046.

Publisher Copyright:
© 2018 National Academy of Sciences. All Rights Reserved.

Keywords

  • C. elegans
  • Gradients
  • MEX-5
  • PIE-1
  • Polarity

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