The molecular signature and cis-regulatory architecture of a C-elegans gustatory neuron

被引:135
作者
Etchberger, John F.
Lorch, Adam
Sleumer, Monica C.
Zapf, Richard
Jones, Steven J.
Marra, Marco A.
Holt, Robert A.
Moerman, Donald G.
Hobert, Oliver [1 ]
机构
[1] Columbia Univ, Ctr Med, Howard Hughes Med Inst, Dept Biochem & Mol Biophys, New York, NY 10032 USA
[2] Univ British Columbia, Dept Zool, Vancouver, BC V6T 1Z4, Canada
[3] British Columbia Canc Agcy, Canadas Michael Smith Genome Sci Ctr, Vancouver, BC V5Z 4S6, Canada
关键词
Caenorhabditis elegans; development; gustatory neuron; transcription factor;
D O I
10.1101/gad.1560107
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Taste receptor cells constitute a highly specialized cell type that perceives and conveys specific sensory information to the brain. The detailed molecular composition of these cells and the mechanisms that program their fate are, in general, poorly understood. We have generated serial analysis of gene expression ( SAGE) libraries from two distinct populations of single, isolated sensory neuron classes, the gustatory neuron class ASE and the thermosensory neuron class AFD, from the nematode Caenorhabditis elegans. By comparing these two libraries, we have identified > 1000 genes that define the ASE gustatory neuron class on a molecular level. This set of genes contains determinants of the differentiated state of the ASE neuron, such as a surprisingly complex repertoire of transcription factors (TFs), ion channels, neurotransmitters, and receptors, as well as seven-transmembrane receptor (7TMR)-type putative gustatory receptor genes. Through the in vivo dissection of the cis-regulatory regions of several ASE-expressed genes, we identified a small cis-regulatory motif, the "ASE motif," that is required for the expression of many ASE-expressed genes. We demonstrate that the ASE motif is a binding site for the C2H2 zinc finger TF CHE-1, which is essential for the correct differentiation of the ASE gustatory neuron. Taken together, our results provide a unique view of the molecular landscape of a single neuron type and reveal an important aspect of the regulatory logic for gustatory neuron specification in C. elegans.
引用
收藏
页码:1653 / 1674
页数:22
相关论文
共 71 条
[1]   CHEMOSENSORY NEURONS WITH OVERLAPPING FUNCTIONS DIRECT CHEMOTAXIS TO MULTIPLE CHEMICALS IN C-ELEGANS [J].
BARGMANN, CI ;
HORVITZ, HR .
NEURON, 1991, 7 (05) :729-742
[2]   Probabilistic code for DNA recognition by proteins of the EGR family [J].
Benos, PV ;
Lapedes, AS ;
Stormo, GD .
JOURNAL OF MOLECULAR BIOLOGY, 2002, 323 (04) :701-727
[3]   Comprehensive analysis of photoreceptor gene expression and the identification of candidate retinal disease genes [J].
Blackshaw, S ;
Fraioli, RE ;
Furukawa, T ;
Cepko, CL .
CELL, 2001, 107 (05) :579-589
[4]   Functional genomics of the cilium, a sensory organelle [J].
Blacque, OE ;
Perens, EA ;
Boroevich, KA ;
Inglis, PN ;
Li, CM ;
Warner, A ;
Khattra, J ;
Holt, RA ;
Ou, GS ;
Mah, AK ;
McKay, SJ ;
Huang, P ;
Swoboda, P ;
Jones, SJM ;
Marra, MA ;
Baillie, DL ;
Moerman, DG ;
Shaham, S ;
Leroux, MR .
CURRENT BIOLOGY, 2005, 15 (10) :935-941
[5]   Specification of muscle neurotransmitter sensitivity by a paired-like homeodomain protein in Caenorhabditis elegans [J].
Branicky, R ;
Hekimi, S .
DEVELOPMENT, 2005, 132 (22) :4999-5009
[6]   Rapid expression screening of Caenorhabditis elegans homeobox open reading frames using a two-step polymerase chain reaction promoter-gfp reporter construction technique [J].
Cassata, G ;
Kagoshima, H ;
Prétôt, RF ;
Aspöck, G ;
Niklaus, G ;
Bürglin, TR .
GENE, 1998, 212 (01) :127-135
[7]   MicroRNAs act sequentially and asymmetrically to control chemosensory laterality in the nematode [J].
Chang, S ;
Johnston, RJ ;
Frokjær-Jensen, C ;
Lockery, S ;
Hobert, O .
NATURE, 2004, 430 (7001) :785-789
[8]   A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C-elegans [J].
Chang, S ;
Johnston, RJ ;
Hobert, O .
GENES & DEVELOPMENT, 2003, 17 (17) :2123-2137
[9]   Dachshund and eyes absent proteins form a complex and function synergistically to induce ectopic eye development in Drosophila [J].
Chen, R ;
Amoui, M ;
Zhang, ZH ;
Mardon, G .
CELL, 1997, 91 (07) :893-903
[10]   Expression profiling of GABAergic motor neurons in Caenorhabditis elegans [J].
Cinar, H ;
Keles, S ;
Jin, YS .
CURRENT BIOLOGY, 2005, 15 (04) :340-346