PCP and SAX-3/Robo Pathways Cooperate to Regulate Convergent Extension-Based Nerve Cord Assembly in C. elegans

Publication date: 24 April 2017
Source:Developmental Cell, Volume 41, Issue 2
Author(s): Pavak K. Shah, Matthew R. Tanner, Ismar Kovacevic, Aysha Rankin, Teagan E. Marshall, Nathaniel Noblett, Nhan Nguyen Tran, Tony Roenspies, Jeffrey Hung, Zheqian Chen, Cristina Slatculescu, Theodore J. Perkins, Zhirong Bao, Antonio Colavita
Formation and resolution of multicellular rosettes can drive convergent extension (CE) type cell rearrangements during tissue morphogenesis. Rosette dynamics are regulated by both planar cell polarity (PCP)-dependent and -independent pathways. Here we show that CE is involved in ventral nerve cord (VNC) assembly in Caenorhabditis elegans. We show that a VANG-1/Van Gogh and PRKL-1/Prickle containing PCP pathway and a Slit-independent SAX-3/Robo pathway cooperate to regulate, via rosette intermediaries, the intercalation of post-mitotic neuronal cell bodies during VNC formation. We show that VANG-1 and SAX-3 are localized to contracting edges and rosette foci and act to specify edge contraction during rosette formation and to mediate timely rosette resolution. Simultaneous loss of both pathways severely curtails CE resulting in a shortened, anteriorly displaced distribution of VNC neurons at hatching. Our results establish rosette-based CE as an evolutionarily conserved mechanism of nerve cord morphogenesis and reveal a role for SAX-3/Robo in this process.

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Teaser

Shah, Tanner, et al. show that the axon guidance factors SAX-3 and Robo also play a role in organizing the C. elegans ventral nerve cord (VNC) via convergent extension-type cell rearrangements. SAX-3 and Robo cooperate with the planar cell polarity pathway to promote intercalation of neuronal cell bodies during VNC formation.


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