The tubulin repertoire of Caenorhabditis elegans sensory neurons and its context-dependent role in process outgrowth

Dean Lockhead, Erich M. Schwarz, Robert O'hagan, Sebastian Bellotti, Michael Krieg, Maureen M. Barr, Alexander R. Dunn, Paul W. Sternberg, Miriam B. Goodman

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17 Scopus citations

Abstract

Microtubules contribute to many cellular processes, including transport, signaling, and chromosome separation during cell division. They comprise αβ-Tubulin heterodimers arranged into linear protofilaments and assembled into tubes. Eukaryotes express multiple tubulin isoforms, and there has been a longstanding debate as to whether the isoforms are redundant or perform specialized roles as part of a tubulin code. Here we use the well-characterized touch receptor neurons (TRNs) of Caenorhabditis elegans to investigate this question through genetic dissection of process outgrowth both in vivo and in vitro. With single-cell RNA-seq, we compare transcription profiles for TRNs with those of two other sensory neurons and present evidence that each sensory neuron expresses a distinct palette of tubulin genes. In the TRNs, we analyze process outgrowth and show that four tubulins (tba-1, tba-2, tbb-1, and tbb-2) function partially or fully redundantly, whereas two others (mec-7 and mec-12) perform specialized, context-dependent roles. Our findings support a model in which sensory neurons express overlapping subsets of tubulin genes whose functional redundancy varies among cell types and in vivo and in vitro contexts.

Original languageEnglish
Pages (from-to)3717-3728
Number of pages12
JournalMolecular Biology of the Cell
Volume27
Issue number23
DOIs
StatePublished - 15 Nov 2016

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    Lockhead, D., Schwarz, E. M., O'hagan, R., Bellotti, S., Krieg, M., Barr, M. M., Dunn, A. R., Sternberg, P. W., & Goodman, M. B. (2016). The tubulin repertoire of Caenorhabditis elegans sensory neurons and its context-dependent role in process outgrowth. Molecular Biology of the Cell, 27(23), 3717-3728. https://doi.org/10.1091/mbc.E16-06-0473