Published November 15, 2016 | Version Supplemental Material + Submitted + Published
Journal Article Open

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

  • 1. ROR icon Stanford University
  • 2. ROR icon Cornell University
  • 3. ROR icon Rutgers, The State University of New Jersey
  • 4. ROR icon Stanford Medicine
  • 5. ROR icon California Institute of Technology

Abstract

Microtubules contribute to many cellular processes, including transport, signaling, and chromosome separation during cell division (Kapitein and Hoogenraad, 2015). They are comprised of αβ‐tubulin heterodimers arranged into linear protofilaments and assembled into tubes. Eukaryotes express multiple tubulin isoforms (Gogonea et al., 1999), and there has been a longstanding debate as to whether the isoforms are redundant or perform specialized roles as part of a tubulin code (Fulton and Simpson, 1976). 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, while 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 between cell types and in vivo and in vitro contexts.

Additional Information

© 2016 The American Society for Cell Biology. Under the License and Publishing Agreement, authors grant to the general public, effective two months after publication of (i.e.,. the appearance of) the edited manuscript in an online issue of MBoC, the nonexclusive right to copy, distribute, or display the manuscript subject to the terms of the Creative Commons–Noncommercial–Share Alike 3.0 Unported license (http://creativecommons.org/licenses/by-nc-sa/3.0). Submitted July 1, 2016. Revised September 12, 2016. Accepted September 15, 2016. This article was published online ahead of print in MBoC in Press (http://www.molbiolcell.org/cgi/doi/10.1091/mbc.E16-06-0473) on September 21, 2016. This work was funded by: NIH research grants K99NS089942 (to M.K), R01NS047715 (to M.B.G.), R01GM084389 (to P.W.S.), R01DK059418 and R56DK074746 (to M.M.B); The New Jersey Commission on Spinal Cord Research Grant CSCR15IRG014 (to R.O.); and The Stanford Graduate Fellowship and the NIH's Cellular and Molecular Biology Training Program T32GM007276 (to D.L). P.W.S. is an investigator of the Howard Hughes Medical Institute. We thank the following: Beth Pruitt and Maria Gallegos for discussion and feedback, Zhiwen Liao for numerous microinjections; Chloé Girard for technical consultation; the Japanese Knockout Consortium, Martin Chalfie, and Chaogu Zheng for strains; Igor Antoshechkin at the Jacobs Genomics Laboratory (California Institute of Technology) for RNA-seq; WormBase; and the Goodman, Pruitt, and Dunn groups for insightful discussions regarding this work. Data availability: Sequence files for raw RNA-seq reads have been deposited in the National Center for Biotechnology Information Sequence Read Archive (www.ncbi.nlm.nih.gov/sra) under the accession numbers SRR3481679 (PLM neuron pool), SRR3481680 (AFD neuron pool), and SRR3481678 (ASER neuron pool). The authors declare no conflicting financial interests.

Attached Files

Published - 3717.full.pdf

Submitted - 075879.full.pdf

Supplemental Material - CombinedSupMats.pdf

Supplemental Material - mc-E16-06-0473-s02.xlsx

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Additional details

Additional titles

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

Identifiers

PMCID
PMC5170555
Eprint ID
70835
Resolver ID
CaltechAUTHORS:20161004-135532696

Related works

Describes
10.1101/075879 (DOI)

Funding

NIH
K99NS089942
NIH
R01NS047715
NIH
R01GM084389
NIH
R01DK059418
NIH
R56DK074746
New Jersey Commission on Spinal Cord Research
CSCR15IRG014
Stanford Graduate Fellowship
NIH Predoctoral Fellowship
T32GM007276
Howard Hughes Medical Institute (HHMI)

Dates

Created
2016-10-04
Created from EPrint's datestamp field
Updated
2022-04-08
Created from EPrint's last_modified field