DOI: 10.1242/dev.121.9.2877. Expression of the <i>unc-4</i> homeoprotein in <i>Caenorhabditis elegans</i> motor neurons specifies presynaptic input

Expression of the unc-4 homeoprotein in Caenorhabditis elegans motor neurons specifies presynaptic input

10.1242/dev.121.9.2877

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT In the nematode, Caenorhabditis elegans, VA and VB motor neurons arise from a common precursor cell but adopt different morphologies and synapse with separate sets of interneurons in the ventral nerve cord. A mutation that inactivates the unc-4 homeodomain gene causes VA motor neurons to assume the VB pattern of synaptic input while retaining normal axonal polarity and output; the disconnection of VA motor neurons from their usual presynaptic partners blocks backward locomotion. We show that expression of a functional unc-4-β-galactosidase chimeric protein in VA motor neurons restores wild-type movement to an unc-4 mutant. We propose that unc-4 controls a differentiated characteristic of the VA motor neurons that distinguishes them from their VB sisters, thus dictating recognition by the appropriate interneurons. Our results show that synaptic choice can be controlled at the level of transcription in the post-synaptic neuron and identify a homeoprotein that defines a subset of cell-specific traits required for this choice.

Bibliography

Miller, D. M., & Niemeyer, C. J. (1995). Expression of the unc-4 homeoprotein in Caenorhabditis elegans motor neurons specifies presynaptic input. Development, 121(9), 2877â2886.

Authors 2

David M. Miller (first)
Charles J. Niemeyer (additional)

References 25 Referenced 92

10.1098/rstb.1976.0085 / Philos. Trans. R. Soc. Lond., B / The pharynx of Caenorhabditis elegans by Albertson (1976)
10.1093/genetics/77.1.71 / Genetics / The genetics of Caenorhabditis elegans by Brenner (1974)
10.1523/JNEUROSCI.05-04-00956.1985 / J. Neurosci / The neural circuit for touch sensitivity in Caenorhabditis elegans by Chalfie (1985)
10.1111/j.1432-1033.1990.tb15355.x / Eur. J. Biochem / Quantitative estimation of minor mRNAs by cDNA-polymerase chain reaction by Chelly (1990)
10.1038/333376a0 / Nature / Control of neuronal fate by the Drosophila segmentation gene even-skipped by Doe (1988)
10.1016/0092-8674(90)90493-X / Cell / The unc-86 gene product couples cell lineage and cell identity in C. elegans by Finney (1990)
10.1016/0378-1119(90)90224-F / Gene / A modular set of lacZ fusion vectors for studying gene expression in Caenhorhabditis elegans by Fire (1990)
10.1073/pnas.87.3.876 / Proc. Natl. Acad. Sci. USA / Modulation of muscle gene expression in Caenorhabditis elegans: Differential levels of transcripts, mRNAs, and polypeptides for thick filament proteins during nematode development by Honda (1990)
10.1073/pnas.80.14.4253 / Proc. Natl. Acad. Sci. USA / Protein structural domains in the Caenorhabditis elegans unc-54 myosin heavy chain gene are not separated by introns by Karn (1983)
{'key': '2025011515021332900_DEVELOP_121_9_2877C10', 'first-page': '21', 'article-title': 'Amplification of RNA', 'volume-title': 'In PCR Protocols', 'author': 'Kawasaki', 'year': '1990'} / In PCR Protocols / Amplification of RNA by Kawasaki (1990)
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 (1992)
10.1016/0896-6273(93)90174-P / Neuron / The role of the cut gene in the specification of central projections by sensory axons in Drosophila by Merrit (1993)
10.1038/355841a0 / Nature / C. elegans unc-4 gene encodes a homeodomain protein that determines the pattern of synaptic input to specific motor neurons by Miller (1992)
10.1093/genetics/135.3.741 / Genetics / Dominant unc-37 mutations suppress the movement defect of a homeodomain mutation in unc-4, a neural specificity gene in Caenorhabditis elegans by Miller (1993)
{'key': '2025011515021332900_DEVELOP_121_9_2877C15', 'first-page': '356', 'article-title': 'Immunofluorescence Microscopy. In C. elegans: Modern Biological Analysis of an Organism', 'volume-title': 'Methods in Cell Biology', 'author': 'Miller', 'year': '1995'} / Methods in Cell Biology / Immunofluorescence Microscopy. In C. elegans: Modern Biological Analysis of an Organism by Miller (1995)
10.1038/359829a0 / Nature / Connectivity of chemosensory neurons is controlled by the gene poxn in Drosophila by Nottebohm (1992)
{'volume-title': 'Molecular Cloning: A Laboratory Manual', 'year': '1989', 'author': 'Sambrook', 'key': '2025011515021332900_DEVELOP_121_9_2877C17'} / Molecular Cloning: A Laboratory Manual by Sambrook (1989)
10.1016/0896-6273(92)90063-J / Neuron / Formation of the Drosophila larval photoreceptor organ and its neuronal differentiation require continuous krüpple gene activity by Schmucker (1992)
10.1098/rstb.1976.0084 / Philos. Trans. R. Soc. Lond., B / Post-embryonic development in the ventral cord of Caenorhabditis elegans by Sulston (1976)
{'key': '2025011515021332900_DEVELOP_121_9_2877C20', 'first-page': '587', 'article-title': 'Methods', 'volume-title': 'In The Nematode Caenorhabditis elegans', 'author': 'Sulston', 'year': '1988'} / In The Nematode Caenorhabditis elegans / Methods by Sulston (1988)
10.1016/0012-1606(77)90158-0 / Dev. Biol / Post-embryonic cell lineages of the nematode, Caenorhabditis elegans by Sulston (1977)
10.1016/0012-1606(83)90201-4 / Dev. Biol / The embryonic cell lineage of the nematode Caenorhabditis elegans by Sulston (1983)
{'key': '2025011515021332900_DEVELOP_121_9_2877C23', 'first-page': '377', 'article-title': 'The Nervous System', 'volume-title': 'In The Nematode Caenorhabditis elegans', 'author': 'White and Chalfie', 'year': '1988'} / In The Nematode Caenorhabditis elegans / The Nervous System by White and Chalfie (1988)
10.1098/rstb.1986.0056 / Phil. Trans. R. Soc. Lond. B / The structure of the nervous system of the nematode Caenorhabditis elegans by White (1986)
10.1038/355838a0 / Nature / Mutations in the Caenorhabditis elegans unc-4 gene alter the synaptic input to ventral cord motor neurons by White (1992)

Dates

Type	When
Created	4 years, 3 months ago (April 25, 2021, 10:25 p.m.)
Deposited	7 months, 1 week ago (Jan. 15, 2025, 10:02 a.m.)
Indexed	1 week, 5 days ago (Aug. 12, 2025, 5:57 p.m.)
Issued	29 years, 11 months ago (Sept. 1, 1995)
Published	29 years, 11 months ago (Sept. 1, 1995)
Published Online	29 years, 11 months ago (Sept. 1, 1995)
Published Print	29 years, 11 months ago (Sept. 1, 1995)

Funders 0

None

BibTeX

@article{Miller_1995, title={Expression of the unc-4 homeoprotein in Caenorhabditis elegans motor neurons specifies presynaptic input}, volume={121}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.121.9.2877}, DOI={10.1242/dev.121.9.2877}, number={9}, journal={Development}, publisher={The Company of Biologists}, author={Miller, David M. and Niemeyer, Charles J.}, year={1995}, month=sep, pages={2877–2886} }

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