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

Research output: Contribution to journalArticle

16 Citations (Scopus)

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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Caenorhabditis elegans
Sensory Receptor Cells
Tubulin
Touch
Neurons
Protein Isoforms
Genetic Phenomena
Eukaryota
Microtubules
Cell Division
Genes
Dissection
Chromosomes
RNA

Cite this

Lockhead, Dean ; Schwarz, Erich M. ; O'Hagan, Robert ; Bellotti, Sebastian ; Krieg, Michael ; Barr, Maureen M. ; Dunn, Alexander R. ; Sternberg, Paul W. ; Goodman, Miriam B. / The tubulin repertoire of Caenorhabditis elegans sensory neurons and its context-dependent role in process outgrowth. In: Molecular Biology of the Cell. 2016 ; Vol. 27, No. 23. pp. 3717-3728.
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Lockhead, D, Schwarz, EM, O'Hagan, R, Bellotti, S, Krieg, M, Barr, MM, Dunn, AR, Sternberg, PW & Goodman, MB 2016, 'The tubulin repertoire of Caenorhabditis elegans sensory neurons and its context-dependent role in process outgrowth', Molecular Biology of the Cell, vol. 27, no. 23, pp. 3717-3728. https://doi.org/10.1091/mbc.E16-06-0473

The tubulin repertoire of Caenorhabditis elegans sensory neurons and its context-dependent role in process outgrowth. / Lockhead, Dean; Schwarz, Erich M.; O'Hagan, Robert; Bellotti, Sebastian; Krieg, Michael; Barr, Maureen M.; Dunn, Alexander R.; Sternberg, Paul W.; Goodman, Miriam B.

In: Molecular Biology of the Cell, Vol. 27, No. 23, 15.11.2016, p. 3717-3728.

Research output: Contribution to journalArticle

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