Time-lapse imaging and cell-specific expression profiling reveal dynamic branching and molecular determinants of a multi-dendritic nociceptor in C. elegans

Developmental Biology
Cody J SmithDavid M Miller

Abstract

Nociceptive neurons innervate the skin with complex dendritic arbors that respond to pain-evoking stimuli such as harsh mechanical force or extreme temperatures. Here we describe the structure and development of a model nociceptor, the PVD neuron of C. elegans, and identify transcription factors that control morphogenesis of the PVD dendritic arbor. The two PVD neuron cell bodies occupy positions on either the right (PVDR) or left (PVDL) sides of the animal in posterior-lateral locations. Imaging with a GFP reporter revealed a single axon projecting from the PVD soma to the ventral cord and an elaborate, highly branched arbor of dendritic processes that envelop the animal with a web-like array directly beneath the skin. Dendritic branches emerge in a step-wise fashion during larval development and may use an existing network of peripheral nerve cords as guideposts for key branching decisions. Time-lapse imaging revealed that branching is highly dynamic with active extension and withdrawal and that PVD branch overlap is prevented by a contact-dependent self-avoidance, a mechanism that is also employed by sensory neurons in other organisms. With the goal of identifying genes that regulate dendritic morphogenesis, we used the mRNA...Continue Reading

References

Mar 1, 1977·Developmental Biology·J E Sulston, H R Horvitz
Mar 15, 1993·Proceedings of the National Academy of Sciences of the United States of America·J M Kaplan, H R Horvitz
Jun 25, 1996·Proceedings of the National Academy of Sciences of the United States of America·G GuMartin Chalfie
Sep 1, 1999·Proceedings of the National Academy of Sciences of the United States of America·N Wittenburg, R Baumeister
Mar 29, 2001·Genes & Development·J WuMartin Chalfie
Sep 13, 2002·Brain Research. Molecular Brain Research·H IchikawaT Sugimoto
Apr 23, 2003·Cell·W Daniel TraceySeymour Benzer
Jun 28, 2003·Methods : a Companion to Methods in Enzymology·Ravi S Kamath, Julie Ahringer
Oct 12, 2004·Neuron·Maria E Gallegos, Cornelia I Bargmann
Mar 8, 2005·Proceedings of the National Academy of Sciences of the United States of America·Takao InouePaul W Sternberg
Feb 8, 2006·Annual Review of Physiology·Amanda H Kahn-Kirby, Cornelia I Bargmann
Mar 8, 2006·Nature Neuroscience·Carolyn E AdlerCornelia I Bargmann
Aug 8, 2006·Trends in Neurosciences·John A WemmieMichael J Welsh
Oct 18, 2006·Genes & Development·Stephen T Crews, Jay E Brenman
Dec 27, 2006·Methods : a Companion to Methods in Enzymology·Andy Golden, Kevin F O'Connell
Feb 6, 2007·Current Biology : CB·Takaki Komiyama, Liqun Luo
Feb 10, 2007·Genes & Development·Stephen E Von StetinaDavid M Miller
Mar 24, 2007·Annual Review of Neuroscience·Jay Z ParrishYuh Nung Jan
May 8, 2007·Cell·Benjamin J MatthewsWesley B Grueber
Sep 13, 2007·Genome Biology·Rebecca M FoxDavid M Miller
Oct 16, 2007·Current Opinion in Neurobiology·Fen-Biao Gao
Dec 1, 2007·WormBook : the Online Review of C. Elegans Biology·David M Eisenmann
Feb 1, 2008·Developmental Biology·Michèle Crozatier, Alain Vincent
May 24, 2008·Current Biology : CB·Christopher C QuinnWilliam G Wadsworth
Aug 2, 2008·Science·Bjarke AbrahamsenJohn N Wood
Mar 10, 2009·Development·Megan M CortyWesley B Grueber
May 8, 2009·Pflügers Archiv : European journal of physiology·Rui Xiao, X Z Shawn Xu
Aug 29, 2009·Neuroscience and Biobehavioral Reviews·Francis McGlone, David Reilly
Sep 8, 2009·Neuroscience and Biobehavioral Reviews·Francis McGlone, Charles Spence
Nov 13, 2009·The Journal of Neuroscience : the Official Journal of the Society for Neuroscience·Kerry FergusonYong Rao
May 8, 2010·Science·Meital Oren-SuissaBenjamin Podbilewicz
Jun 1, 2010·Nature Neuroscience·Marios ChatzigeorgiouWilliam R Schafer
Nov 12, 1986·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·J G WhiteS Brenner

Citations

Jan 22, 2014·Microscopy and Microanalysis : the Official Journal of Microscopy Society of America, Microbeam Analysis Society, Microscopical Society of Canada·Yingjun YanChris Janetopoulos
Mar 29, 2014·Schizophrenia Bulletin·Shane McCarthyAiden Corvin
Oct 12, 2011·Annual Review of Cell and Developmental Biology·Oliver Hobert
Dec 24, 2010·Genome Research·W Clay SpencerDavid M Miller
Sep 29, 2011·PLoS Biology·Leonie KirszenblatMassimo A Hilliard
Dec 18, 2013·BMC Neuroscience·Jarred SandersDavid Biron
Jul 12, 2014·Biomedical Engineering Online·Ayala GreenblumJosué Sznitman
Mar 20, 2012·Nature Neuroscience·Cody J SmithDavid M Miller
Jul 5, 2013·BMC Neuroscience·Aylia MohammadiWilliam S Ryu
Oct 20, 2010·The Journal of Cell Biology·Ellen A LumpkinAislyn M Nelson
Aug 16, 2011·Trends in Neurosciences·David H Hall, Millet Treinin
Dec 12, 2013·Journal of Molecular Signaling·Chun-Hao ChenChun-Liang Pan
Jan 5, 2011·Wiley Interdisciplinary Reviews. Systems Biology and Medicine·Genevieve Konopka
Mar 30, 2013·Wiley Interdisciplinary Reviews. Developmental Biology·Andrew D Chisholm, Suhong Xu
Aug 15, 2015·Development Genes and Evolution·Logan T SchachtnerEugenia C Olesnicky
Oct 26, 2010·Molecular and Cellular Neurosciences·Adi AlbegMillet Treinin
Aug 24, 2010·Current Biology : CB·Brikha R Shrestha, Wesley B Grueber
Aug 13, 2013·Current Biology : CB·Nathan E SchroederMaureen M Barr
Feb 13, 2014·Molecular and Cellular Neurosciences·Emiliano CohenMillet Treinin
Nov 12, 2014·Annual Review of Physiology·Xintong DongHannes E Bülow
Jul 24, 2014·Pflügers Archiv : European journal of physiology·William R Schafer
Dec 4, 2015·PLoS Genetics·Caitlin A TaylorKang Shen
Jul 28, 2016·Current Biology : CB·Carlos Díaz-BalzacHannes E Bülow
Sep 14, 2016·BMC Bioinformatics·David Angeles-AlboresPaul W Sternberg
Nov 17, 2011·Proceedings of the National Academy of Sciences of the United States of America·Irini Topalidou, Martin Chalfie
Sep 24, 2015·PLoS Genetics·Wei ZouDavid R Sherwood
May 26, 2017·Wiley Interdisciplinary Reviews. Developmental Biology·Rebecca J AndrowskiNathan E Schroeder
Mar 28, 2019·Open Biology·Wei-Kang Yang, Cheng-Ting Chien
Jun 1, 2010·Nature Neuroscience·Marios ChatzigeorgiouWilliam R Schafer
Feb 1, 2013·Nature·Bertrand Coste, Ardem Patapoutian
Feb 1, 2013·Nature·Marios ChatzigeorgiouWilliam R Schafer
Feb 13, 2015·G3 : Genes - Genomes - Genetics·Simona AntonacciDarrell J Killian
Apr 3, 2019·Annual Review of Neuroscience·Sharon InbergBenjamin Podbilewicz
Feb 6, 2019·Nature Communications·Xianzhuang LiuKang Shen
Feb 5, 2020·Frontiers in Pharmacology·Emiliano CohenMillet Treinin

Related Concepts

Dendrites
Neurons
Nociceptors
Transcription Factor
Caenorhabditis elegans
Laser Scanning Microscopy
Microscopy, Video
Cdna Microarrays
MRNA Differential Display
Caenorhabditis elegans Proteins

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