journal article Mar 01, 2001

The novel C. elegans gene sop-3 modulates Wnt signaling to regulate Hox gene expression

Development Vol. 128 No. 5 pp. 767-777 · The Company of Biologists
View at Publisher Save 10.1242/dev.128.5.767
Abstract
ABSTRACT
We describe the properties of a new gene, sop-3, that is required for the regulated expression of a C. elegans Hox gene, egl-5, in a postembryonic neuroectodermal cell lineage. Regulated expression of egl-5 in this cell lineage is necessary for development of the sensory rays of the male tail. sop-3 encodes a predicted novel protein of 1475 amino acids without clear homologs in other organisms. However, the sequence contains motifs consisting of homopolymeric runs of amino acids found in several other transcriptional regulators, some of which also act in Hox gene regulatory pathways. The genetic properties of sop-3 are very similar to those of sop-1, which encodes a component of the transcriptional Mediator complex, and mutations in the two genes are synthetic lethal. This suggests that SOP-3 may act at the level of the Mediator complex in regulating transcription initiation. In a sop-3 loss-of-function background, egl-5 is expressed ectopically in lineage branches that normally do not express this gene. Such expression is dependent on the Hox gene mab-5, as it is in branches where egl-5 is normally expressed. Ectopic egl-5 expression is also dependent on the Wnt pathway. Thus, sop-3 contributes to the combinatorial control of egl-5 by blocking egl-5 activation by MAB-5 and the Wnt pathway in inappropriate lineage branches.
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References
46
[1]
Baird "Pattern formation in the nematode epidermis: determination of the spatial arrangement of peripheral sense organs in the C. elegans male tail" Development (1991) 10.1242/dev.113.2.515
[2]
Barr "A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans" Nature (1999) 10.1038/43913
[3]
Bjorklund "Global transcription regulators of eukaryotes" Cell (1999) 10.1016/s0092-8674(00)80586-3
[4]
Boyer "Mammalian Srb/Mediator complex is targeted by adenovirus E1A protein" Nature (1999) 10.1038/20466
[5]
THE GENETICS OF CAENORHABDITIS ELEGANS

S Brenner

Genetics 1974 10.1093/genetics/77.1.71
[6]
Castelli-Gair "The lines gene of Drosophila is required for specific functions of the Abdominal-B HOX protein" Development (1998) 10.1242/dev.125.7.1269
[7]
Cavallo "Drosophila Tcf and Groucho interact to repress Wingless signalling activity" Nature (1998) 10.1038/26982
[8]
Chisholm "Control of cell fate in the tail region of C. elegans by the gene egl-5" Development (1991) 10.1242/dev.111.4.921
[9]
Chow "HOM-C/Hox genes and four interacting loci determine the morphogenetic properties of single cells in the nematode male tail" Development (1994) 10.1242/dev.120.9.2579
[10]
Cosma "Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter" Cell (1999) 10.1016/s0092-8674(00)80740-0
[11]
de Zulueta. "Homeotic complex and teashirt genes co-operate to establish trunk segmental identities in Drosophila" Development (1994) 10.1242/dev.120.8.2287
[12]
Eisenmann "The beta-catenin homolog BAR-1 and LET-60 Ras coordinately regulate the Hox gene lin-39 during Caenorhabditis elegans vulval development" Development (1998) 10.1242/dev.125.18.3667
[14]
Fasano "The gene teashirt is required for the development of Drosophila embryonic trunk segments and encodes a protein with widely spaced zinc finger motifs" Cell (1991) 10.1016/0092-8674(91)90209-h
[15]
Ferreira "Patterning of Caenorhabditis elegans posterior structures by the Abdominal-B homolog, egl-5" Dev. Biol (1999) 10.1006/dbio.1998.9124
[16]
Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans

Andrew Fire, SiQun Xu, Mary K. Montgomery et al.

Nature 1998 10.1038/35888
[17]
Gallet "Trunk-specific modulation of wingless signalling in Drosophila by teashirt binding to armadillo" Curr. Biol (1998) 10.1016/s0960-9822(07)00369-7
[18]
Gallet "The C-terminal domain of armadillo binds to hypophosphorylated teashirt to modulate wingless signalling in Drosophila" EMBO J (1999) 10.1093/emboj/18.8.2208
[19]
Gellon "Shaping animal body plans in development and evolution by modulation of Hox expression patterns" BioEssays (1998) 10.1002/(sici)1521-1878(199802)20:2<116::aid-bies4>3.0.co;2-r
[20]
Hanna-Rose "Active repression mechanisms of eukaryotic transcription repressors" Trends Genet (1996) 10.1016/0168-9525(96)10022-6
[21]
Hatini "Tissue- and stage-specific modulation of Wingless signaling by the segment polarity gene lines" Genes Dev (2000) 10.1101/gad.14.11.1364
[22]
Herman "The C. elegans gene lin-44, which controls the polarity of certain asymmetric cell divisions, encodes a Wnt protein and acts cell nonautonomously" Cell (1995) 10.1016/0092-8674(95)90238-4
[23]
Hunter "Hox gene expression in a single Caenorhabditis elegans cell is regulated by a caudal homolog and intercellular signals that inhibit Wnt signaling" Development (1999) 10.1242/dev.126.4.805
[24]
Ito "Identity between TRAP and SMCC complexes indicates novel pathways for the function of nuclear receptors and diverse mammalian activators" Mol. Cell (1999) 10.1016/s1097-2765(00)80463-3
[25]
Kornberg "Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome" Cell (1999) 10.1016/s0092-8674(00)81958-3
[26]
Korswagen "Distinct beta-catenins mediate adhesion and signalling functions in C. elegans" Nature (2000) 10.1038/35020099
[27]
Laughon "Common properties of proteins encoded by the Antennapedia complex genes of Drosophila melanogaster" Cold Spring Harb. Symp. Quant. Biol (1985) 10.1101/sqb.1985.050.01.032
[28]
Lin "POP-1 and anterior-posterior fate decisions in C. elegans embryos" Cell (1998) 10.1016/s0092-8674(00)80917-4
[29]
Lints "Patterning of dopaminergic neurotransmitter identity among Caenorhabditis elegans ray sensory neurons by a TGF-β family signaling pathway and a Hox gene" Development (1999) 10.1242/dev.126.24.5819
[30]
Maloof "A Wnt signaling pathway controls hox gene expression and neuroblast migration in C. elegans" Development (1999) 10.1242/dev.126.1.37
[31]
Mann "Nuclear import of the homeodomain protein Extradenticle in response to Wg and Dpp signalling" Nature (1996) 10.1038/383630a0
[32]
Marshall "Retinoids and Hox genes" FASEB J (1996) 10.1096/fasebj.10.9.8801179
[33]
McGinnis "A cap ‘n’ collar protein isoform contains a selective Hox repressor function" Development (1998) 10.1242/dev.125.22.4553
[34]
Mohler "Control of Drosophila head segment identity by the bZIP homeotic gene cnc" Development (1995) 10.1242/dev.121.1.237
[35]
Petcherski "LAG-3 is a putative transcriptional activator in the C. elegans Notch pathway" Nature (2000) 10.1038/35012645
[36]
Pflugrad "The Groucho-like transcription factor UNC-37 functions with the neural specificity gene unc-4 to govern motor neuron identity in C. elegans" Development (1997) 10.1242/dev.124.9.1699
[37]
Rieckhof "Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein" Cell (1997) 10.1016/s0092-8674(00)80400-6
[38]
Roose "The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors" Nature (1998) 10.1038/26989
[39]
Salser "A C. elegans Hox gene switches on, off, on and off again to regulate proliferation, differentiation and morphogenesis" Development (1996) 10.1242/dev.122.5.1651
[40]
Singh "sur-2, a novel gene, functions late in the let-60 ras-mediated signaling pathway during Caenorhabditis elegans vulval induction" Genes Dev (1995) 10.1101/gad.9.18.2251
[41]
Smoller "The Drosophila neurogenic locus mastermind encodes a nuclear protein unusually rich in amino acid homopolymers" Genes Dev (1990) 10.1101/gad.4.10.1688
[42]
Struhl "Fundamentally different logic of gene regulation in eukaryotes and prokaryotes" Cell (1999) 10.1016/s0092-8674(00)80599-1
[43]
Waring "Selective silencing of cell communication influences anteroposterior pattern formation in C. elegans" Cell (1990) 10.1016/0092-8674(90)90722-q
[44]
Waring "Regulation of cellular responsiveness to inductive signals in the developing C. elegans nervous system" Nature (1991) 10.1038/350712a0
[45]
Zhang "A C. elegans mediator protein confers regulatory selectivity on lineage-specific expression of a transcription factor gene" Genes Dev (2000) 10.1101/gad.814700
[46]
Zhao "A transcription factor controlling development of peripheral sense organs in C. elegans" Nature (1995) 10.1038/373074a0
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Published
Mar 01, 2001
Vol/Issue
128(5)
Pages
767-777
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Cite This Article
Hong Zhang, Scott W. Emmons (2001). The novel C. elegans gene sop-3 modulates Wnt signaling to regulate Hox gene expression. Development, 128(5), 767-777. https://doi.org/10.1242/dev.128.5.767
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