The novel homeodomain gene buttonless specifies differentiation and axonal guidance functions of Drosophila dorsal median cells
10.1242/dev.120.12.3581
Crossref journal-article
The Company of Biologists
Development (237)
Abstract

ABSTRACT We have identified a novel homeodomain gene, buttonless (btn), that is specifically expressed in 20 cells of a single type during Drosophila embryonic development. These cells, the dorsal median (DM) cells, are arranged as a single pair within each segment along the dorsal midline of the CNS. Distinctive features of the DM cells include a large cell body and a long thick process extending laterally to the muscle attachment site. In the absence of btn gene function the initial commitment to the DM cell fate is made but differentiation fails to occur and the DM cells are lost. The btn mutation thus specifically eliminates the DM cells, and this genetic ablation in turn reveals a requirement for DM cells as cellular cues for axonal guidance during transverse nerve outgrowth and bifurcation of the median nerve.

Bibliography

Chiang, C., Patel, N. H., Young, K. E., & Beachy, P. A. (1994). The novel homeodomain gene buttonless specifies differentiation and axonal guidance functions of Drosophila dorsal median cells. Development, 120(12), 3581–3593.

Authors 4
  1. Chin Chiang (first)
  2. Nipam H. Patel (additional)
  3. Keith E. Young (additional)
  4. Philip A. Beachy (additional)
References 62 Referenced 30
  1. 10.1242/dev.117.4.1183 / Development / Regulation of development and differentiation by the extracellular matrix by Adams (1993)
  2. {'key': '2024121723590742700_DEVELOP_120_12_3581C2', 'first-page': '1325', 'volume': '7', 'author': 'Azpiazu', 'year': '1993', 'journal-title': 'tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev'} / tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev by Azpiazu (1993)
  3. 10.1523/JNEUROSCI.05-07-01808.1985 / J. Neurosci / Development of neuromuscular specificity in the grasshopper embryo: guidance of motoneuron growth cones by muscle pioneers by Ball (1985)
  4. 10.1002/j.1460-2075.1988.tb03054.x / EMBO J / A novel, tissue-specific, Drosophila homeobox gene by Barad (1988)
  5. 10.1002/j.1460-2075.1987.tb04837.x / EMBO J / Isolation and nucleotide sequence of mouse N-CAM cDNA that codes for a Mr 79000 polypeptide without a membrane-spanning region by Barthels (1987)
  6. 10.1523/JNEUROSCI.06-12-03542.1986 / J. Neurosci / Guidance of neuronal growth cones in the grasshopper embryo. III. Recognition of specific glial pathways by Bastiani (1986)
  7. {'key': '2024121723590742700_DEVELOP_120_12_3581C7', 'first-page': '1013', 'article-title': 'The mesoderm and its derivatives', 'volume-title': 'The Development of Drosophila melanogaster', 'author': 'Bate', 'year': '1993'} / The Development of Drosophila melanogaster / The mesoderm and its derivatives by Bate (1993)
  8. 10.1007/BF00376346 / Roux’s Arch. Dev. Biol / Lineage analysis of transplanted individual cells in embryos of Drosophila melanogaster: IV commitment and proliferative capabilities of mesodermal cells by Beer (1987)
  9. 10.1016/0092-8674(89)90029-9 / Cell / Drosophila neuroglian: a member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1 by Bieber (1989)
  10. 10.1242/dev.110.3.661 / Development / A new homeobox-containing gene, msh-2, is transiently expressed early during mesoderm formation of Drosophila by Bodmer (1990)
  11. 10.1016/0022-2836(88)90010-1 / J. Mol. Biol / Functional cDNA libraries from Drosophila embryos by Brown (1988)
  12. 10.1038/341239a0 / Nature / Caenorhabditis elegans has scores of homoeobox-containing genes by Burglin (1989)
  13. 10.1242/dev.116.4.1123 / Development / Mox-1 and Mox-2 define a novel homeobox gene subfamily and are differentially expressed during early mesodermal patterning in mouse embryos by Candia (1992)
  14. 10.1016/0012-1606(88)90344-2 / Dev. Biol / Formation of the transverse nerve in moth embryos by Carr (1988)
  15. {'key': '2024121723590742700_DEVELOP_120_12_3581C15', 'first-page': '196', 'article-title': 'Pioneer pathfinding of segment boundary nerves by identified cells in Drosophila embryos', 'volume': '12', 'author': 'Caudy', 'year': '1986', 'journal-title': 'Soc. Neurosci. Abstr'} / Soc. Neurosci. Abstr / Pioneer pathfinding of segment boundary nerves by identified cells in Drosophila embryos by Caudy (1986)
  16. 10.1002/j.1460-2075.1992.tb05188.x / EMBO, J / Structural complexity and evolutionary conservation of the Drosophila homeotic gene proboscipedia by Cribbs (1992)
  17. 10.1126/science.3576199 / Science / Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative splicing by Cunningham (1987)
  18. 10.1002/j.1460-2075.1994.tb06662.x / EMBO J. in press / The degree of variation in DNA sequence recognition among four Drosophila homeotic proteins by Ekker (1994)
  19. {'key': '2024121723590742700_DEVELOP_120_12_3581C19', 'first-page': '3722', 'article-title': 'Molecular cloning of a diverged homeobox gene that is rapidly down-regulated during the G0/G1 transition in vascular smooth muscle cells', 'volume': '13', 'author': 'Gorski', 'year': '1993', 'journal-title': 'Mol. Cell. Biol'} / Mol. Cell. Biol / Molecular cloning of a diverged homeobox gene that is rapidly down-regulated during the G0/G1 transition in vascular smooth muscle cells by Gorski (1993)
  20. 10.1101/SQB.1990.055.01.034 / Cold Spring Harbor Symp. Quant. Biol / Molecular genetics of neuronal recognition in Drosophila: evolution and function of immunoglobulin superfamily cell adhesion molecules by Grenningloh (1990)
  21. 10.1016/0092-8674(91)90571-F / Cell / Genetic analysis of growth cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule by Grenningloh (1991)
  22. 10.1242/dev.116.4.1203 / Development / The functionof the neurogenic genes during epithelial development in the Drosophila embryo by Hartenstein (1992)
  23. 10.1007/BF00188752 / Roux’s Arch. Dev. Biol / Studying Drosophila embryogenesis with PlacZ enhancer trap lines by Hartenstein (1992)
  24. 10.1038/301066a0 / Nature / Muscle pioneers: large mesodermal cells that erect a scaffold for developing muscles and motoneurones in grasshopper embryos by Ho (1983)
  25. 10.1016/S0021-9258(18)34441-7 / J. Biol. Chem / Chemical characterization of a neural cell adhesion molecule purified from embryonic brain membranes by Hoffman (1982)
  26. {'key': '2024121723590742700_DEVELOP_120_12_3581C26', 'first-page': '15', 'article-title': 'The role of the dorsal morphogen gradient in Drosophila embryogenesis', 'volume': '3', 'author': 'Ip', 'year': '1992', 'journal-title': 'Sem. Dev. Biol'} / Sem. Dev. Biol / The role of the dorsal morphogen gradient in Drosophila embryogenesis by Ip (1992)
  27. {'key': '2024121723590742700_DEVELOP_120_12_3581C27', 'first-page': '1518', 'volume': '6', 'author': 'Ip', 'year': '1992', 'journal-title': 'dorsal-twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo. Genes Dev'} / dorsal-twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo. Genes Dev by Ip (1992)
  28. 10.1002/neu.480190205 / J. Neurobiol / An identified cell is required for the formation of a major nerve during embryogenesis in the leech by Jellies (1988)
  29. 10.1242/dev.117.2.793 / Development / A new Drosophila homeobox gene, bsh, is expressed in a subset of brain cells during embeyogenesis by Jones (1993)
  30. 10.1016/0092-8674(84)90534-8 / Cell / Analysis of P-transposable element functions in Drosophila by Karess (1984)
  31. 10.1101/gad.2.12b.1745 / Genes Dev / A Drosophila rRNA gene located in euchromatin is active in transcription and nucleolus formation by Karpen (1988)
  32. 10.1016/0092-8674(90)90453-L / Cell / Crystal structure of an engrailed homeodomain/DNA complex at 2. 6 A resolution: a framework for understanding homeodomain/DNA interactions by Kissinger (1990)
  33. 10.1073/pnas.90.17.8145 / Proc. Natl. Acad. Sci. USA / Csx: A murine homeobox-containing gene specifically expressed in the developing heart by Komuro (1993)
  34. 10.1083/jcb.97.2.499 / J. Cell Biol / Reversible blockage of membrane retrieval and endocytosis in the garland cell of the temperature-sensitive mutant of Drosophila melanogaster, shibire(ts1) by Kosada (1983)
  35. 10.1073/pnas.79.14.4381 / Proc. Natl. Acad. Sci. USA / Immunological method for mapping genes on Drosophila polytene chromosomes by Langer-Safer (1982)
  36. 10.1038/310025a0 / Nature / Sequence of a Drosophila segmentation gene: protein structure homology with DNA-binding proteins by Laughon (1984)
  37. 10.1016/0092-8674(88)90209-7 / Cell / Homeobox proteins as sequence-specific transcription factors by Levine (1988)
  38. 10.1016/0092-8674(78)90036-3 / Cell / The isolation of structural genes from libraries of eucaryotic DNA by Maniatis (1978)
  39. 10.1016/0092-8674(92)90471-N / Cell / Homeobox genes and axial patterning by McGinnis (1992)
  40. 10.1083/jcb.109.5.2441 / J. Cell Biol / Drosophila laminin: sequence of B2 subunit and expression of all three subunits during embryogenesis by Montell (1989)
  41. 10.1038/334701a0 / Nature / Neural adhesion molecule L1 is a member of the immunoglobulin superfamily with binding domains similar to fibronectin by Moos (1988)
  42. 10.1007/BF00188733 / Roux’s Arch. Dev. Biol / Drosophila glial architecture and development: analysis using a collection of new cell-specific markers by Nelson (1993)
  43. {'key': '2024121723590742700_DEVELOP_120_12_3581C43', 'first-page': '219', 'article-title': 'Amplification of flanking sequences by Inverse PCR', 'volume-title': 'PCR Protocols', 'author': 'Ochman', 'year': '1990'} / PCR Protocols / Amplification of flanking sequences by Inverse PCR by Ochman (1990)
  44. 10.1002/j.1460-2075.1990.tb08229.x / EMBO J / Glutactin, a novel Drosophila basement membrane- related glycoprotein with sequence similarity to serine esterases by Olson (1990)
  45. 10.1016/S0091-679X(08)60927-9 / Methods in Cell Biology, Vol 44. Drosophila melanogaster: Practical Uses in Cell Biology / Imaging neuronal subsets and other cell types in whole mount Drosophila embryos and larvae using antibody probes by Patel (1994)
  46. 10.1002/j.1460-2075.1984.tb01753.x / EMBO J / Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion by Rathjen (1984)
  47. 10.1126/science.6289436 / Science / Genetic transformation of Drosophila with transposable element vectors by Rubin (1982)
  48. 10.1038/334151a0 / Nature / Pattern formation in the developing eye of Drosophila melanogaster is regulated by the homeo- box gene, rough by Saint (1988)
  49. {'volume-title': 'Molecular Cloning: a Laboratory Manual. 2nd edition. Cold Spring Harbor: Cold Spring Harbor Laboratory Publications', 'year': '1989', 'author': 'Sambrook', 'key': '2024121723590742700_DEVELOP_120_12_3581C49'} / Molecular Cloning: a Laboratory Manual. 2nd edition. Cold Spring Harbor: Cold Spring Harbor Laboratory Publications by Sambrook (1989)
  50. {'key': '2024121723590742700_DEVELOP_120_12_3581C50', 'first-page': '353', 'article-title': 'Cell lines derived from late embryonic stages of Drosophila melanogaster', 'volume': '27', 'author': 'Schneider', 'year': '1972', 'journal-title': 'J. Embryol. Exp. Morph'} / J. Embryol. Exp. Morph / Cell lines derived from late embryonic stages of Drosophila melanogaster by Schneider (1972)
  51. 10.1007/BF01534735 / Somatic Cell Mol. Genetics / Establishment and characterization of continuous cell lines derived from temperature senseitive mutants of Drosophila melanogaster by Simcox (1985)
  52. {'volume-title': 'Cell and nuclear determination of early Drosophila melanogaster embryos. Ph. D. these, Ohio State University, Columbus, Ohio', 'year': '1981', 'author': 'Simcox', 'key': '2024121723590742700_DEVELOP_120_12_3581C52'} / Cell and nuclear determination of early Drosophila melanogaster embryos. Ph. D. these, Ohio State University, Columbus, Ohio by Simcox (1981)
  53. {'key': '2024121723590742700_DEVELOP_120_12_3581C53', 'first-page': '692', 'volume': '238', 'author': 'Steward', 'year': '1987', 'journal-title': 'Dorsal, an embryonic polarity gene in Drosophila, is homologous to the vertebrate proto-oncogene, c-rel. Science'} / Dorsal, an embryonic polarity gene in Drosophila, is homologous to the vertebrate proto-oncogene, c-rel. Science by Steward (1987)
  54. 10.1007/BF00291041 / Chromosoma / A non-radioactive in situ hybridization method for the localization of specific RNAs in the Drosophila embryo reveals translational control of the segmentation gene hunchback by Tautz (1989)
  55. 10.1002/j.1460-2075.1988.tb03056.x / EMBO J / Sequence of the twist gene and nuclear localization of its protein in edomesodermal cells of early Drosophila embryos by Thisse (1988)
  56. 10.1016/0378-1119(88)90177-1 / Gene / Vectors for Drosophila P-element-mediated transformation and tissue culture transfection by Thummel (1988)
  57. 10.1016/0092-8674(88)90133-X / Cell / rough, a Drosophila homeobox gene required in photoreceptors R2 and R5 for inductive interactions in the developing eye by Tomlinson (1988)
  58. 10.1016/0092-8674(93)90643-5 / Cell / Genes that control neuromuscular specificity in Drosophila by Van Vactor (1993)
  59. 10.1016/0092-8674(90)90449-O / Cell / A role for integrin in the formation of sacomeric cytoarchitecture by Volk (1990)
  60. 10.1016/0092-8674(88)90174-2 / Cell / Mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans by Way (1988)
  61. 10.1016/0925-4773(93)90072-6 / Mech. Dev / CNS midline enhancers of the Drosophila slit and Toll genes by Wharton (1993)
  62. 10.1006/dbio.1993.1063 / Dev. Biol / Neurons producing specific neuropeptides in the central nervous system of normal and pupariation- delayed Drosophila by Zitnan (1993)
Dates
Type When
Created 4 years, 4 months ago (April 23, 2021, 2:39 p.m.)
Deposited 8 months, 2 weeks ago (Dec. 17, 2024, 7 p.m.)
Indexed 8 months, 2 weeks ago (Dec. 17, 2024, 7:40 p.m.)
Issued 30 years, 9 months ago (Dec. 1, 1994)
Published 30 years, 9 months ago (Dec. 1, 1994)
Published Online 30 years, 9 months ago (Dec. 1, 1994)
Published Print 30 years, 9 months ago (Dec. 1, 1994)
Funders 0

None

@article{Chiang_1994, title={The novel homeodomain gene buttonless specifies differentiation and axonal guidance functions of Drosophila dorsal median cells}, volume={120}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.120.12.3581}, DOI={10.1242/dev.120.12.3581}, number={12}, journal={Development}, publisher={The Company of Biologists}, author={Chiang, Chin and Patel, Nipam H. and Young, Keith E. and Beachy, Philip A.}, year={1994}, month=dec, pages={3581–3593} }