Abstract
Abstract lin-26, which encodes a unique Zn-finger protein, is required for differentiation of nonneuronal ectodermal cells in Caenorhabditis elegans. Here, we show that the two genes located immediately upstream of lin-26 encode LIN-26-like Zn-finger proteins; hence their names are lir-1 and lir-2 (lin-26 related). lir-2, lir-1, and lin-26 generate several isoforms by alternative splicing and/or trans-splicing at different positions. On the basis of their trans-splicing pattern, their intergenic distances, and their expression, we suggest that lir-2, lir-1, and lin-26 form two overlapping transcriptional operons. The first operon, which is expressed in virtually all cells, includes lir-2 and long lir-1 isoforms. The second operon, which is expressed in the nonneuronal ectoderm, includes short lir-1 isoforms, starting at exon 2 and lin-26. This unusual genomic organization has been conserved in C. briggsae, as shown by cloning the C. briggsae lir-2, lir-1, and lin-26 homologs. Particularly striking is the sequence conservation throughout the first lir-1 intron, which is very long in both species. Structural conservation is functionally meaningful as C. briggsae lin-26 is also expressed in the nonneuronal ectoderm and can complement a C. elegans lin-26 null mutation.
Bibliography
Dufourcq, P., Chanal, P., Vicaire, S., Camut, E., Quintin, S., Boer, B. G. W. den, Bosher, J. M., & Labouesse, M. (1999). lir-2, lir-1 and lin-26 Encode a New Class of Zinc-Finger Proteins and Are Organized in Two Overlapping Operons Both in Caenorhabditis elegans and in Caenorhabditis briggsae. Genetics, 152(1), 221â235.
References
45
Referenced
18
10.1016/S0021-9258(18)81782-3
/ J. Biol. Chem. / The basal component of the nematode dense-body is vinculin by Barstead (1989){'key': '2022010313504616300_R2', 'first-page': '117', 'article-title': 'RNA processing and gene structure', 'volume-title': 'C. elegans II', 'author': 'Blumenthal', 'year': '1997'}
/ C. elegans II / RNA processing and gene structure by Blumenthal (1997)10.1093/genetics/77.1.71
/ Genetics / The genetics of Caenorhabditis elegans by Brenner (1974)10.1096/fasebj.10.9.8801176
/ FASEB J. / A decade of molecular biology of retinoic acid receptors by Chambon (1996)10.1093/genetics/146.1.207
/ Genetics / A screen for genetic loci required for hypodermal cell and glial-like cell development during Caenorhabditis elegans embryogenesis by Chanal (1997)10.1242/dev.125.16.3213
/ Development / A tissue specific knock-out strategy reveals that lin-26 is required for the formation of the somatic gonad epithelium in C. elegans by den Boer (1998)10.1016/0378-1119(89)90223-0
/ Gene / Nucleotide sequence of the rat γ–crystallin gene region and comparison with an orthologous human region by den Dunnen (1989)10.1093/nar/12.1Part1.387
/ Nucleic Acids Res. / A comprehensive set of sequence analysis programs for VAX by Devereux (1984){'key': '2022010313504616300_R9', 'first-page': '583', 'article-title': 'ACeDB and Macace', 'volume-title': 'Methods in Cell Biology', 'author': 'Eeckman', 'year': '1995'}
/ Methods in Cell Biology / ACeDB and Macace by Eeckman (1995)10.1073/pnas.94.18.9751
/ Proc. Natl. Acad. Sci. USA / Operons and SL2 trans-splicing exist in nematodes outside the genus Caenorhabditis by Evans (1997)10.1038/326259a0
/ Nature / A genetic pathway for the specification of the vulval cell lineages of Caenorhabditis elegans by Ferguson (1987)10.1016/0022-2836(83)90056-6
/ J. Mol. Biol. / Actin gene family of Caenorhabditis elegans by Files (1983)10.1016/0378-1119(90)90224-F
/ Gene / A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans by Fire (1990)10.1083/jcb.114.3.465
/ J. Cell Biol. / Muscle cell attachment in Caenorhabditis elegans by Francis (1991)10.1242/dev.121.1.209
/ Development / DWnt-4, a novel Drosophila Wnt gene acts downstream of homeotic complex genes in the visceral mesoderm by Graba (1995)10.1093/genetics/142.3.893
/ Genetics / The Drosophila engrailed and invected genes: partners in regulation, expression and function by Gustavson (1996)10.1007/BF02101786
/ J. Mol. Evol. / Functional elements and domains inferred from sequence comparisons of a heat-shock gene in two nematodes by Heschl (1990)10.1093/genetics/132.2.453
/ Genetics / Comparative studies of Drosophila Antennapedia genes by Hooper (1992)10.1006/jmbi.1993.1094
/ J. Mol. Biol. / The gut esterase gene (ges-1) from the nematodes Caenorhabditis elegans and Caenorhabditis briggsae by Kennedy (1993)10.1038/ng0594-48
/ Nature Genet. / Striking sequence similarity over almost 100 kilobases of human and mouse T-cell receptor DNA by Koop (1994){'key': '2022010313504616300_R21', 'first-page': '513', 'article-title': 'Techniques for analyzing transcription and translation', 'volume-title': 'Methods in Cell Biology', 'author': 'Krause', 'year': '1995'}
/ Methods in Cell Biology / Techniques for analyzing transcription and translation by Krause (1995)10.1016/0092-8674(87)90613-1
/ Cell / A trans-spliced leader sequence on actin mRNA in C. elegans by Krause (1987)10.1006/dbio.1994.1302
/ Dev. Biol. / Elements regulating cell- and stage-specific expression of the C. elegans MyoD family homolog hlh-1 by Krause (1994)10.1093/nar/22.21.4414
/ Nucleic Acids Res. / Cloning by synteny: identifying C. briggsae homologues of C. elegans genes by Kuwabara (1994)10.1242/dev.120.9.2359
/ Development / The Caenorhabditis elegans gene lin-26 is required to specify the fates of hypodermal cells and encodes a presumptive zinc-finger transcription factor by Labouesse (1994)10.1242/dev.122.9.2579
/ Development / The Caenorhabditis elegans LIN-26 protein is required to specify and/or maintain all non-neuronal ectodermal cell fates by Labouesse (1996)10.1016/0378-1119(92)90126-A
/ Gene / Conservation of gene organization and trans-splicing in the glyceraldehyde-3-phosphate dehydrogenase-encoding genes of Caenorhabditis briggsae by Lee (1992)10.1007/BF02407308
/ J. Mol. Evol. / Unbiased estimation of the rates of synonymous and nonsynonymous substitution by Li (1993){'key': '2022010313504616300_R29', 'first-page': '5749', 'article-title': 'Saccharomyces cerevisiae BUF protein binds to sequences participating in DNA replication in addition to those mediating transcriptional repression (URS1) and activation', 'volume': '13', 'author': 'Luche', 'year': '1993', 'journal-title': 'Mol. Cell Biol.'}
/ Mol. Cell Biol. / Saccharomyces cerevisiae BUF protein binds to sequences participating in DNA replication in addition to those mediating transcriptional repression (URS1) and activation by Luche (1993)10.1016/0925-4773(94)90024-8
/ Mech. Dev. / Regulatory and coding regions of the segmentation gene hunchback are functionally conserved between Drosophila virilis and Drosophila melanogaster by Lukowitz (1994)10.1016/0092-8674(87)90081-X
/ Cell / Deletion analysis of GAL4 defines two transcriptional activating segments by Ma (1987)10.1016/S0378-1119(96)00491-X
/ Gene / Conservation of function and expression of unc-119 from two Caenorhabditis species despite divergence of non-coding DNA by Maduro (1996)10.1002/j.1460-2075.1991.tb04966.x
/ EMBO J. / Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences by Mello (1991)10.1146/annurev.mi.47.100193.002213
/ Annu. Rev. Microbiol. / Trans-splicing of nematode premessenger RNA by Nilsen (1993)10.1016/0092-8674(86)90866-4
/ Cell / An underlying repeat in some transcriptional control sequences corresponding to half a double helical turn of DNA by Rhodes (1986)10.1074/jbc.270.37.22066
/ J. Biol. Chem. / Structure and expression of novel spliced leader RNA genes in Caenorhabditis elegans by Ross (1995){'key': '2022010313504616300_R37', 'volume-title': 'Molecular Cloning: A Laboratory Manual', 'author': 'Sambrook', 'year': '1989'}
/ Molecular Cloning: A Laboratory Manual by Sambrook (1989)10.1242/dev.120.10.2823
/ Development / Soma-germline asymmetry in the distributions of embryonic RNAs in Caenorhabditis elegans by Seydoux (1994)10.1096/fasebj.8.10.8050670
/ FASEB J. / The achaete-scute complex: generation of cellular pattern and fate within the Drosophila nervous system by Skeath (1994)10.1093/nar/22.13.2437
/ Nucleic Acids Res. / Codon usage in Caenorhabditis elegans: delineation of translational selection and mutational biases by Stenico (1994)10.1093/nar/25.24.4876
/ Nucleic Acids Res. / The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tool by Thompson (1997)10.1038/ng0592-114
/ Nature Genet. / A survey of expressed genes in Caenorhabditis elegans by Waterston (1992)10.1101/gad.5.12a.2199
/ Genes Dev. / The mec-3 gene contains cis-acting elements mediating positive and negative regulation in cells produced by asymmetric cell division in Caenorhabditis elegans by Way (1991)10.1038/368032a0
/ Nature / 2.2 Mb of contiguous nt sequence from chromosome III of C. elegans by Wilson (1994)10.1038/372270a0
/ Nature / Operons as a common form of chromosomal organization in C. elegans by Zorio (1994)
Dates
Type | When |
---|---|
Created | 4 years, 4 months ago (April 27, 2021, 10:48 p.m.) |
Deposited | 3 years, 8 months ago (Jan. 3, 2022, 12:04 p.m.) |
Indexed | 2 months, 2 weeks ago (June 23, 2025, 9:09 a.m.) |
Issued | 26 years, 4 months ago (May 1, 1999) |
Published | 26 years, 4 months ago (May 1, 1999) |
Published Online | 26 years, 4 months ago (May 1, 1999) |
Published Print | 26 years, 4 months ago (May 1, 1999) |
@article{Dufourcq_1999, title={lir-2, lir-1 and lin-26 Encode a New Class of Zinc-Finger Proteins and Are Organized in Two Overlapping Operons Both in Caenorhabditis elegans and in Caenorhabditis briggsae}, volume={152}, ISSN={1943-2631}, url={http://dx.doi.org/10.1093/genetics/152.1.221}, DOI={10.1093/genetics/152.1.221}, number={1}, journal={Genetics}, publisher={Oxford University Press (OUP)}, author={Dufourcq, Pascale and Chanal, Philippe and Vicaire, Serge and Camut, Elise and Quintin, Sophie and Boer, Bart G W den and Bosher, Julia M and Labouesse, Michel}, year={1999}, month=may, pages={221–235} }