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

Lockhead, Dean and Schwarz, Erich M. and O'Hagan, Robert and Bellotti, Sebastian and Krieg, Michael and Barr, Maureen M. and Dunn, Alexander R. and Sternberg, Paul W. and Goodman, Miriam B. (2016) The tubulin repertoire of C. elegans sensory neurons and its context-dependent role in process outgrowth. Molecular Biology of the Cell, 27 (23). pp. 3717-3728. ISSN 1059-1524. PMCID PMC5170555. https://resolver.caltech.edu/CaltechAUTHORS:20161004-135532696

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://dx.doi.org/10.1091/mbc.E16-06-0473DOIArticle
http://www.molbiolcell.org/content/27/23/3717/suppl/DC1PublisherSupplemental Materials
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5170555/PubMed CentralArticle
https://doi.org/10.1101/075879DOIDiscussion Paper
ORCID:
AuthorORCID
Schwarz, Erich M.0000-0003-3151-4381
Sternberg, Paul W.0000-0002-7699-0173
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.
Funders:
Funding AgencyGrant Number
NIHK99NS089942
NIHR01NS047715
NIHR01GM084389
NIHR01DK059418
NIHR56DK074746
New Jersey Commission on Spinal Cord ResearchCSCR15IRG014
Stanford Graduate FellowshipUNSPECIFIED
NIH Predoctoral FellowshipT32GM007276
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Issue or Number:23
PubMed Central ID:PMC5170555
Record Number:CaltechAUTHORS:20161004-135532696
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20161004-135532696
Official Citation:Dean Lockhead, Erich M. Schwarz, Robert O’Hagan, Sebastian Bellotti, Michael Krieg, Maureen M. Barr, Alexander R. Dunn, Paul W. Sternberg, and Miriam B. Goodman The tubulin repertoire of Caenorhabditis elegans sensory neurons and its context‑dependent role in process outgrowth Mol. Biol. Cell 2016 27:23 3717-3728; First Published on September 21, 2016; doi:10.1091/mbc.E16-06-0473
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:70835
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:04 Oct 2016 21:09
Last Modified:29 Oct 2019 21:39

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