spacer gif spacer gif spacer gif spacer gif spacer gif
 QUICK SEARCH:   [advanced]


spacer gif
     Home     Help     Feedback     Subscriptions     Archive     Search     Table of Contents    


This Article
Right arrow Figures Only
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Altun-Gultekin, Z.
Right arrow Articles by Hobert, O.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Altun-Gultekin, Z.
Right arrow Articles by Hobert, O.
Social Bookmarking
 Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?
Development 128, 1951-1969 (2001)
© 2001 The Company of Biologists Limited

A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans

Zeynep Altun-Gultekin1, Yoshiki Andachi2, Ephraim L. Tsalik1, David Pilgrim3, Yuji Kohara2 and Oliver Hobert1,*

1 Department of Biochemistry and Molecular Biophysics, Center for Neurobiology and Behavior, Columbia University, College of Physicians and Surgeons, New York, NY 10032, USA
2 Genome Biology Lab, Center for Genetic Resource Information, National Institute of Genetics, Mishima, Shizuoka, 411-8540, Japan
3 Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada

*Author for correspondence (e-mail: or38{at}columbia.edu)

Accepted February 27, 2001

The development of the nervous system requires the coordinated activity of a variety of regulatory factors that define the individual properties of specific neuronal subtypes. We report a regulatory cascade composed of three homeodomain proteins that act to define the properties of a specific interneuron class in the nematode C. elegans. We describe a set of differentiation markers characteristic for the AIY interneuron class and show that the ceh-10 paired-type and ttx-3 LIM-type homeobox genes function to regulate all known subtype-specific features of the AIY interneurons. In contrast, the acquisition of several pan-neuronal features is unaffected in ceh-10 and ttx-3 mutants, suggesting that the activity of these homeobox genes separates pan-neuronal from subtype-specific differentiation programs. The LIM homeobox gene ttx-3 appears to play a central role in regulation of AIY differentiation. Not only are all AIY subtype characteristics lost in ttx-3 mutants, but ectopic misexpression of ttx-3 is also sufficient to induce AIY-like features in a restricted set of neurons. One of the targets of ceh-10 and ttx-3 is a novel type of homeobox gene, ceh-23. We show that ceh-23 is not required for the initial adoption of AIY differentiation characteristics, but instead is required to maintain the expression of one defined AIY differentiation feature. Finally, we demonstrate that the regulatory relationship between ceh-10, ttx-3 and ceh-23 is only partially conserved in other neurons in the nervous system. Our findings illustrate the complexity of transcriptional regulation in the nervous system and provide an example for the intricate interdependence of transcription factor action.

Key words: Homeobox, C. elegans, Neuronal differentiation


Add to CiteULike CiteULike   Add to Complore Complore   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati   Add to Twitter Twitter    What's this?


This article has been cited by other articles:


Home page
J. Cell Sci.Home page
B. Schaheen, H. Dang, and H. Fares
Derlin-dependent accumulation of integral membrane proteins at cell surfaces
J. Cell Sci., July 1, 2009; 122(13): 2228 - 2239.
[Abstract] [Full Text] [PDF]


Home page
J. Neurosci.Home page
Y. Iino and K. Yoshida
Parallel Use of Two Behavioral Mechanisms for Chemotaxis in Caenorhabditis elegans
J. Neurosci., April 29, 2009; 29(17): 5370 - 5380.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
K. Sato, G. G. Ernstrom, S. Watanabe, R. M. Weimer, C.-H. Chen, M. Sato, A. Siddiqui, E. M. Jorgensen, and B. D. Grant
Differential requirements for clathrin in receptor-mediated endocytosis and maintenance of synaptic vesicle pools
PNAS, January 27, 2009; 106(4): 1139 - 1144.
[Abstract] [Full Text] [PDF]


Home page
Hum Mol GenetHome page
M. Briese, B. Esmaeili, S. Fraboulet, E. C. Burt, S. Christodoulou, P. R. Towers, K. E. Davies, and D. B. Sattelle
Deletion of smn-1, the Caenorhabditis elegans ortholog of the spinal muscular atrophy gene, results in locomotor dysfunction and reduced lifespan
Hum. Mol. Genet., January 1, 2009; 18(1): 97 - 104.
[Abstract] [Full Text] [PDF]


Home page
Genes Dev.Home page
C. Kang and L. Avery
Systemic regulation of starvation response in Caenorhabditis elegans
Genes & Dev., January 1, 2009; 23(1): 12 - 17.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
O. Hobert
Gene Networks in Development and Evolution Special Feature Sackler Colloquium: Regulatory logic of neuronal diversity: Terminal selector genes and selector motifs
PNAS, December 23, 2008; 105(51): 20067 - 20071.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
S. Jarriault, Y. Schwab, and I. Greenwald
A Caenorhabditis elegans model for epithelial-neuronal transdifferentiation
PNAS, March 11, 2008; 105(10): 3790 - 3795.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
A. Mohri-Shiomi and D. A. Garsin
Insulin Signaling and the Heat Shock Response Modulate Protein Homeostasis in the Caenorhabditis elegans Intestine during Infection
J. Biol. Chem., January 4, 2008; 283(1): 194 - 201.
[Abstract] [Full Text] [PDF]


Home page
Toxicol SciHome page
G. C.-T. Jiang, K. Tidwell, B. A. McLaughlin, J. Cai, R. C. Gupta, D. Milatovic, R. Nass, and M. Aschner
Neurotoxic Potential of Depleted Uranium Effects in Primary Cortical Neuron Cultures and in Caenorhabditis elegans
Toxicol. Sci., October 1, 2007; 99(2): 553 - 565.
[Abstract] [Full Text] [PDF]


Home page
Genome ResHome page
V. Vermeirssen, M. I. Barrasa, C. A. Hidalgo, J. A. B. Babon, R. Sequerra, L. Doucette-Stamm, A.-L. Barabasi, and A. J.M. Walhout
Transcription factor modularity in a gene-centered C. elegans core neuronal protein-DNA interaction network
Genome Res., July 1, 2007; 17(7): 1061 - 1071.
[Abstract] [Full Text] [PDF]


Home page
J. Neurosci.Home page
H. R. Brignull, F. E. Moore, S. J. Tang, and R. I. Morimoto
Polyglutamine proteins at the pathogenic threshold display neuron-specific aggregation in a pan-neuronal Caenorhabditis elegans model.
J. Neurosci., July 19, 2006; 26(29): 7597 - 7606.
[Abstract] [Full Text] [PDF]


Home page
J. Neurophysiol.Home page
S. Faumont, T. Boulin, O. Hobert, and S. R. Lockery
Developmental Regulation of Whole Cell Capacitance and Membrane Current in Identified Interneurons in C. elegans
J Neurophysiol, June 1, 2006; 95(6): 3665 - 3673.
[Abstract] [Full Text] [PDF]


Home page
Cold Spring Harb Symp Quant BiolHome page
O. HOBERT
Architecture of a MicroRNA-controlled Gene Regulatory Network That Diversifies Neuronal Cell Fates
Cold Spring Harb Symp Quant Biol, January 1, 2006; 71(0): 181 - 188.
[Abstract] [PDF]


Home page
J. Exp. Biol.Home page
B. B. Shtonda and L. Avery
Dietary choice behavior in Caenorhabditis elegans
J. Exp. Biol., January 1, 2006; 209(1): 89 - 102.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
L. I. Grad, L. C. Sayles, and B. D. Lemire
Introduction of an additional pathway for lactate oxidation in the treatment of lactic acidosis and mitochondrial dysfunction in Caenorhabditis elegans
PNAS, December 20, 2005; 102(51): 18367 - 18372.
[Abstract] [Full Text] [PDF]


Home page
J. Cell Sci.Home page
J. A. Smith, P. McGarr, and J. S. Gilleard
The Caenorhabditis elegans GATA factor elt-1 is essential for differentiation and maintenance of hypodermal seam cells and for normal locomotion
J. Cell Sci., December 15, 2005; 118(24): 5709 - 5719.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
R. J. Johnston Jr and O. Hobert
A novel C. elegans zinc finger transcription factor, lsy-2, required for the cell type-specific expression of the lsy-6 microRNA
Development, December 15, 2005; 132(24): 5451 - 5460.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
R. Branicky and S. Hekimi
Specification of muscle neurotransmitter sensitivity by a Paired-like homeodomain protein in Caenorhabditis elegans
Development, November 15, 2005; 132(22): 4999 - 5009.
[Abstract] [Full Text] [PDF]


Home page
NeuroscientistHome page
M. Wines-Samuelson and J. Shen
Presenilins in the Developing, Adult, and Aging Cerebral Cortex
Neuroscientist, October 1, 2005; 11(5): 441 - 451.
[Abstract] [PDF]


Home page
J. Neurosci.Home page
B. D. Ackley, R. J. Harrington, M. L. Hudson, L. Williams, C. J. Kenyon, A. D. Chisholm, and Y. Jin
The Two Isoforms of the Caenorhabditis elegans Leukocyte-Common Antigen Related Receptor Tyrosine Phosphatase PTP-3 Function Independently in Axon Guidance and Synapse Formation
J. Neurosci., August 17, 2005; 25(33): 7517 - 7528.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
S. Ghenea, J. R. Boudreau, N. P. Lague, and I. D. Chin-Sang
The VAB-1 Eph receptor tyrosine kinase and SAX-3/Robo neuronal receptors function together during C. elegans embryonic morphogenesis
Development, August 15, 2005; 132(16): 3679 - 3690.
[Abstract] [Full Text] [PDF]


Home page
ScienceHome page
J.-J. Remy and O. Hobert
An Interneuronal Chemoreceptor Required for Olfactory Imprinting in C. elegans
Science, July 29, 2005; 309(5735): 787 - 790.
[Abstract] [Full Text] [PDF]


Home page
GENES CELLSHome page
T. Hirotsu and Y. Iino
Neural circuit-dependent odor adaptation in C. elegans is regulated by the Ras-MAPK pathway
Genes Cells, June 1, 2005; 10(6): 517 - 530.
[Abstract] [Full Text] [PDF]


Home page
J. Neurosci.Home page
E. Runko and Z. Kaprielian
Caenorhabditis elegans VEM-1, a Novel Membrane Protein, Regulates the Guidance of Ventral Nerve Cord-Associated Axons
J. Neurosci., October 13, 2004; 24(41): 9015 - 9026.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. Solomon, S. Bandhakavi, S. Jabbar, R. Shah, G. J. Beitel, and R. I. Morimoto
Caenorhabditis elegans OSR-1 Regulates Behavioral and Physiological Responses to Hyperosmotic Environments
Genetics, May 1, 2004; 167(1): 161 - 170.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
B. Gerisch and A. Antebi
Hormonal signals produced by DAF-9/cytochrome P450 regulate C. elegans dauer diapause in response to environmental cues
Development, April 15, 2004; 131(8): 1765 - 1776.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
N. Mehta, P. M. Loria, and O. Hobert
A Genetic Screen for Neurite Outgrowth Mutants in Caenorhabditis elegans Reveals a New Function for the F-box Ubiquitin Ligase Component LIN-23
Genetics, March 1, 2004; 166(3): 1253 - 1267.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
R. L. Chow, B. Volgyi, R. K. Szilard, D. Ng, C. McKerlie, S. A. Bloomfield, D. G. Birch, and R. R. McInnes
Control of late off-center cone bipolar cell differentiation and visual signaling by the homeobox gene Vsx1
PNAS, February 10, 2004; 101(6): 1754 - 1759.
[Abstract] [Full Text] [PDF]


Home page
Mol. Biol. CellHome page
J. F. Morley and R. I. Morimoto
Regulation of Longevity in Caenorhabditis elegans by Heat Shock Factor and Molecular Chaperones
Mol. Biol. Cell, February 1, 2004; 15(2): 657 - 664.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
H. Yu, R. F. Pretot, T. R. Burglin, and P. W. Sternberg
Distinct roles of transcription factors EGL-46 and DAF-19 in specifying the functionality of a polycystin-expressing sensory neuron necessary for C. elegans male vulva location behavior
Development, November 1, 2003; 130(21): 5217 - 5227.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
X. Huang, P. Huang, M. K. Robinson, M. J. Stern, and Y. Jin
UNC-71, a disintegrin and metalloprotease (ADAM) protein, regulates motor axon guidance and sex myoblast migration in C. elegans
Development, July 15, 2003; 130(14): 3147 - 3161.
[Abstract] [Full Text] [PDF]


Home page
J. Neurosci.Home page
H. A. Zariwala, A. C. Miller, S. Faumont, and S. R. Lockery
Step Response Analysis of Thermotaxis in Caenorhabditis elegans
J. Neurosci., May 15, 2003; 23(10): 4369 - 4377.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
O. Uchida, H. Nakano, M. Koga, and Y. Ohshima
The C. elegans che-1 gene encodes a zinc finger transcription factor required for specification of the ASE chemosensory neurons
Development, April 1, 2003; 130(7): 1215 - 1224.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
O. Aurelio, T. Boulin, and O. Hobert
Identification of spatial and temporal cues that regulate postembryonic expression of axon maintenance factors in the C. elegans ventral nerve cord
Development, February 1, 2003; 130(3): 599 - 610.
[Abstract] [Full Text] [PDF]


Home page
Genes Dev.Home page
R. Lints and S. W. Emmons
Regulation of sex-specific differentiation and mating behavior in C. elegans by a new member of the DM domain transcription factor family
Genes & Dev., September 15, 2002; 16(18): 2390 - 2402.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
H. E. Bulow, K. L. Berry, L. H. Topper, E. Peles, and O. Hobert
Heparan sulfate proteoglycan-dependent induction of axon branching and axon misrouting by the Kallmann syndrome gene kal-1
PNAS, April 30, 2002; 99(9): 6346 - 6351.
[Abstract] [Full Text] [PDF]


Home page
DevelopmentHome page
T. R. Sarafi-Reinach, T. Melkman, O. Hobert, and P. Sengupta
The lin-11 LIM homeobox gene specifies olfactory and chemosensory neuron fates in C. elegans
Development, September 1, 2001; 128(17): 3269 - 3281.
[Abstract] [Full Text] [PDF]




© The Company of Biologists Ltd 2001