DOI: 10.1242/dev.120.4.755. Muscle pattern diversification in <i>Drosophila</i> is determined by the autonomous function of homeotic genes in the embryonic mesoderm

Muscle pattern diversification in Drosophila is determined by the autonomous function of homeotic genes in the embryonic mesoderm

10.1242/dev.120.4.755

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT Muscle diversification in the Drosophila embryo is manifest in a stereotyped array of myofibers that exhibit distinct segment-specific patterns. Here it is shown that the homeotic genes of the Bithorax complex control the identities of abdominal somatic muscles and their precursors by functioning directly in cells of the mesoderm. Whereas Ultrabithorax (Ubx) and abdominal-A (abd-A) have equivalent functions in promoting the formation of particular muscle precursors in the anterior abdominal segments, Abdominal-B (Abd-B) suppresses the development of these same myogenic cells in the posterior region of the abdomen. When expressed in the same mesodermal cells, however, either UBX or ABD-A can override the inhibitory influence of ABD-B, suggesting that these factors may compete in the regulation of common downstream genes. Furthermore, targeted ectopic expression of Ubx or abd-A indicates that these homeotic genes influence muscle cell fates by autonomous action in mesodermal cells. Muscle identity also appears to be sensitive to the level of UBX in myogenic precursors. Finally, these experiments reveal that homeotic cues specific to both the mesoderm and the ectoderm cooperate to specify the pattern of muscle attachment sites.

Bibliography

Michelson, A. M. (1994). Muscle pattern diversification in Drosophila is determined by the autonomous function of homeotic genes in the embryonic mesoderm. Development, 120(4), 755â768.

Authors 1

Alan M. Michelson (first)

References 58 Referenced 112

{'key': '2024121805383239000_DEVELOP_120_4_755C1', 'article-title': 'nautilus, a Drosophila member of the myogenic regulatory gene family', 'volume-title': 'Neuromuscular Development and Disease', 'author': 'Abmayr', 'year': '1992'} / Neuromuscular Development and Disease / nautilus, a Drosophila member of the myogenic regulatory gene family by Abmayr (1992)
10.1002/j.1460-2075.1993.tb05751.x / EMBO J / Cell-type-specific mechanisms of transcriptional repression by the homeotic gene products UBX and ABD-A in Drosophila embryos by Appel (1993)
10.1242/dev.110.3.791 / Development / The embryonic development of larval muscles in Drosophila by Bate (1990)
10.1038/313545a0 / Nature / Segmental distribution of Bithorax complex proteins during Drosophila development by Beachy (1985)
10.1101/gad.4.2.190 / Genes Dev / rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster by Bier (1990)
10.1016/0168-9525(93)90012-7 / Trends Genet / Myoblasts in pattern formation and gene therapy by Blau (1993)
10.1242/dev.118.2.401 / Development / Targeted gene expression as a means of altering cell fates and generating dominant phenotypes by Brand (1993)
10.1242/dev.119.2.533 / Development / Muscle development is independent of innervation during Drosophila embryogenesis by Broadie (1993)
10.1016/0092-8674(86)90627-6 / Cell / Identification and characterization of a parasegment specific regulatory element of the Abdominal-B gene of Drosophila by Casanova (1986)
10.1523/JNEUROSCI.12-06-02051.1992 / J. Neurosci / Alternate neuromuscular target selection following the loss of single muscle fibers in Drosophila by Cash (1992)
10.1101/gad.3.9.1424 / Genes Dev / The molecular genetics of the Bithorax complex of Drosophila: Characterization of the products of the Abdominal-B domain by Celniker (1989)
10.1126/science.8392225 / Science / Separable regulatory elements governing myogenin transcription in mouse embryogenesis by Cheng (1993)
10.1523/JNEUROSCI.13-02-00714.1993 / J. Neurosci / Growth cone choices of Drosophila motoneurons in response to muscle fiber mismatch by Chiba (1993)
10.1242/dev.108.2.323 / Development / Expression of Abdominal-B homeoproteins in Drosophila embryos by Delorenzi (1990)
10.1016/0092-8674(92)90119-W / Cell / Mammalian muscle cells bear a cell-autonomous, heritable memory of their rostrocaudal position by Donoghue (1992)
10.1016/0092-8674(90)90533-K / Cell / The developmental effect of overexpressing a Ubx product in Drosophila embryos is dependent on its interactions with other homeotic products by Gonzalez-Reyes (1990)
10.1038/344078a0 / Nature / Are cross-regulatory interactions between homeotic genes functionally significant? by Gonzalez-Reyes (1990)
10.1038/362630a0 / Nature / Homeotic genes autonomously specify one aspect of pattern in the Drosophila mesoderm by Greig (1993)
10.1016/0092-8674(92)90120-2 / Cell / A transgene target for positional regulators marks early rostrocaudal specification of myogenic lineages by Grieshammer (1992)
10.1523/JNEUROSCI.11-10-03227.1991 / J. Neurosci / Growth cone behavior underlying the development of stereotypic synaptic connections in Drosophila embryos by Halpern (1991)
10.1002/j.1460-2075.1986.tb04500.x / EMBO J / Homeotic gene function In the muscles of Drosophila larvae by Hooper (1986)
10.1016/0092-8674(90)90364-K / Cell / Induction across germ layers in Drosophila mediated by a genetic cascade by Immergluck (1990)
10.1007/BF00863276 / Wilhelm Roux’s Archiv. Dev. Biol / A cell arrangement specific to thoracic ganglia in the central nervous system of the Drosophila embryo: Its behaviour in homeotic mutants by Jimenez (1981)
10.1523/JNEUROSCI.09-12-04318.1989 / J. Neurosci / Axonal guidance and the development of muscle fiber-specific innervation in Drosophila embryos by Johansen (1989)
10.1016/0092-8674(85)90014-5 / Cell / The abdominal region of the bithorax complex by Karch (1985)
10.1101/gad.4.9.1573 / Genes Dev / abdA expression in Drosophila embryos by Karch (1990)
10.1242/dev.116.4.841 / Development / Ectopic expression of UBX and ABD-B proteins during Drosophila embryogenesis: Competition, not a functional hierarchy, explains phenotypic suppression by Lamka (1992)
10.1101/SQB.1985.050.01.016 / Cold Spring Harbor Symp. Quant. Biol / Pattern formation in the muscles of Drosophila by Lawrence (1985)
10.1016/0092-8674(84)90357-X / Cell / The genetic specification of pattern in a Drosophila muscle by Lawrence (1984)
10.1016/0092-8674(86)90282-5 / Cell / The muscle pattern of a segment of Drosophila may be determined by neurons and not by contributing myoblasts by Lawrence (1986)
10.1038/276565a0 / Nature / A gene complex controlling segmentation in Drosophila by Lewis (1978)
10.1242/dev.110.4.1197 / Development / Expression and regulation of the abd-A gene of Drosophila by Macias (1990)
10.1016/0092-8674(90)90663-Y / Cell / Functional dissection of Ultrabithorax proteins in D. melanogaster by Mann (1990)
10.1016/0092-8674(92)90471-N / Cell / Homeobox genes and axial patterning by McGinnis (1992)
10.1101/gad.4.12a.2086 / Genes Dev / Expression of a MyoD family member prefigures muscle pattern in Drosophila embryos by Michelson (1990)
10.1007/BF00848493 / Wilhelm Roux’s Archiv. Dev. Biol / Preblastoderm mosaics of mutants of the Bithorax complex by Minana (1982)
{'key': '2024121805383239000_DEVELOP_120_4_755C37', 'first-page': '125', 'article-title': 'Developmental analysis of some mutants of the Bithorax system of Drosophila. Wilhelm Roux’s Archiv', 'volume': '179', 'author': 'Morata', 'year': '1976', 'journal-title': 'Dev. Biol'} / Dev. Biol / Developmental analysis of some mutants of the Bithorax system of Drosophila. Wilhelm Roux’s Archiv by Morata (1976)
10.1242/dev.110.4.1041 / Development / A Drosophila growth factor homolog, decapentaplegic, regulates homeotic gene expression within and across germ layers during midgut morphogenesis by Panganiban (1990)
10.1073/pnas.88.9.3782 / Proc. Natl. Acad. Sci. USA / The Drosophila homologue of vertebrate myogenic-determination genes encodes a transiently expressed nuclear protein marking primary myogenic cells by Paterson (1991)
10.1242/dev.110.4.1031 / Development / Homeotic genes regulate the spatial expression of putative growth factors in the visceral mesoderm of Drosophila embryos by Reuter (1990)
10.1242/dev.109.2.289 / Development / Expression and function of the homeotic genes Antennapedia and Sex combs reduced in the embryonic midgut of Drosophila by Reuter (1990)
10.1016/0092-8674(89)90342-5 / Cell / Gene activation and DNA binding by Drosophila Ubx and abd-A proteins by Samson (1989)
10.1038/313108a0 / Nature / Genetic organization of Drosophila Bithorax complex by Sanchez-Herrero (1985)
{'key': '2024121805383239000_DEVELOP_120_4_755C44', 'first-page': '25', 'article-title': 'The structure and function of the homeodomain', 'volume': '989', 'author': 'Scott', 'year': '1989', 'journal-title': 'Biochim. Biophys. Acta'} / Biochim. Biophys. Acta / The structure and function of the homeodomain by Scott (1989)
10.1242/dev.113.2.701 / Development / Early ablation of target muscles modulates the arborisation pattern of an identified embryonic Drosophila motor axon by Sink (1991)
10.1093/genetics/124.2.357 / Genetics / Dosage requirements of Ultrabithorax and bithoraxoid in the determination of segment identity in Drosophila melanogaster by Smolik-Utlaut (1990)
{'key': '2024121805383239000_DEVELOP_120_4_755C47', 'first-page': '175', 'article-title': 'P element-mediated transformation', 'volume-title': 'Drosophila: A Practical Approach', 'author': 'Spradling', 'year': '1986'} / Drosophila: A Practical Approach / P element-mediated transformation by Spradling (1986)
10.1101/gad.4.7.1114 / Genes Dev / Molecular organization of the decapentaplegic gene in Drosophila melanogaster by St. Johnston (1990)
10.1016/0012-1606(92)90068-R / Dev. Biol / Myogenic cell lineages by Stockdale (1992)
10.1007/BF00291041 / Chromosoma / A nonradioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals a translational control of the segmentation gene hunchback by Tautz (1989)
10.1038/314558a0 / Nature / Domains of action of Bithorax genes in Drosophila central nervous system by Teugels (1985)
10.1002/j.1460-2075.1989.tb08408.x / EMBO J / Homeotic gene expression in the visceral mesoderm of Drosophila embryos by Tremml (1989)
10.1016/0092-8674(92)90513-C / Cell / Homeotic genes of the Bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene distal-less by Vachon (1992)
10.1126/science.1846704 / Science / The MyoD gene family: Nodal point during specification of the muscle cell lineage by Weintraub (1991)
10.1101/gad.1.4.386 / Genes Dev / Ultrabithorax mutations in constant and variable regions of the protein coding sequence by Weinzierl (1987)
10.1002/j.1460-2075.1985.tb03889.x / EMBO J / Distribution of Ultrabithorax proteins in Drosophila by White (1985)
{'key': '2024121805383239000_DEVELOP_120_4_755C57', 'first-page': '199', 'article-title': 'Looking at embryos', 'volume-title': 'Drosophila: A Practical Approach', 'author': 'Wieschaus', 'year': '1986'} / Drosophila: A Practical Approach / Looking at embryos by Wieschaus (1986)
{'key': '2024121805383239000_DEVELOP_120_4_755C58', 'first-page': '35', 'article-title': 'A gradient of morphogenetic information involved in muscle patterning', 'volume': '58', 'author': 'Williams', 'year': '1980', 'journal-title': 'J. Embryol. Exp. Morph'} / J. Embryol. Exp. Morph / A gradient of morphogenetic information involved in muscle patterning by Williams (1980)

Dates

Type	When
Created	4 years, 4 months ago (April 23, 2021, 2:47 p.m.)
Deposited	8 months, 1 week ago (Dec. 18, 2024, 12:39 a.m.)
Indexed	1 month, 3 weeks ago (July 4, 2025, 8:47 a.m.)
Issued	31 years, 4 months ago (April 1, 1994)
Published	31 years, 4 months ago (April 1, 1994)
Published Online	31 years, 4 months ago (April 1, 1994)
Published Print	31 years, 4 months ago (April 1, 1994)

Funders 0

None

BibTeX

@article{Michelson_1994, title={Muscle pattern diversification in Drosophila is determined by the autonomous function of homeotic genes in the embryonic mesoderm}, volume={120}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.120.4.755}, DOI={10.1242/dev.120.4.755}, number={4}, journal={Development}, publisher={The Company of Biologists}, author={Michelson, Alan M.}, year={1994}, month=apr, pages={755–768} }

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