DOI: 10.1242/dev.121.8.2313. Invagination centers within the Drosophila stomatogastric nervous system anlage are positioned by Notch-mediated signaling which is spatially controlled through wingless

Invagination centers within the Drosophila stomatogastric nervous system anlage are positioned by Notch-mediated signaling which is spatially controlled through wingless

10.1242/dev.121.8.2313

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT The gut-innervating stomatogastric nervous system of Drosophila, unlike the central and the peripheral nervous system, derives from a compact, single layered epithelial anlage. Here we report how this anlage is initially defined during embryogenesis by the expression of proneural genes of the achaete-scute complex in response to the maternal terminal pattern forming system. Within the stomatogastric nervous system anlage, the wingless-dependent inter-cellular communication system adjusts the cellular range of Notch-dependent lateral inhibition to single-out three achaete-expressing cells. Those cells define distinct invagination centers which orchestrate the behavior of neighboring cells to form epithelial infoldings, each headed by an achaete-expressing tip cell. Our results suggest that the wingless pathway acts not as an instructive signal, but as a permissive factor which coordinates the spatial activity of morphoregulatory signals within the stomatogastric nervous system anlage.

Bibliography

GonzÃ¡lez-GaitÃ¡n, M., & JÃ¤ckle, H. (1995). Invagination centers within the Drosophila stomatogastric nervous system anlage are positioned by Notch-mediated signaling which is spatially controlled through wingless. Development, 121(8), 2313â2325.

Authors 2

Marcos González-Gaitán (first)
Herbert Jäckle (additional)

References 67 Referenced 45

10.1146/annurev.cb.07.110191.002235 / Ann. Rev. Cell Biol / The Notch locus and the cell biology of neuroblast segregation by Artavanis-Tsakonas (1991)
10.1002/j.1460-2075.1990.tb07477.x / EMBO J / An early embryonic product of the gene shaggy encodes a serine/threonine protein kinase related to the CDC28/cdc2 subfamily by Bourouis (1990)
10.1007/BF00385679 / Roux Arch. Dev. Biol / Two groups of interrelated genes regulate early neurogenesis in Drosophila melanogaster by Brand (1988)
10.1016/0092-8674(87)90496-X / Cell / The expression of three members of the achaete-scute gene complex correlates with neuroblast segregation in Drosophila by Cabrera (1987)
{'key': '2025011514563566300_DEVELOP_121_8_2313C5', 'first-page': '1091', 'volume-title': 'Early neurogenesis in Drosophila melanogaster. In The development of Drosophila melanogaster', 'author': 'Campos-Ortega', 'year': '1993'} / Early neurogenesis in Drosophila melanogaster. In The development of Drosophila melanogaster by Campos-Ortega (1993)
10.1007/978-3-662-02454-6 / The Embryonic Development of Drosophila melanogaster by Campos-Ortega (1985)
10.1101/gad.3.12b.2025 / Genes Dev / Localized surface activity of torso, a receptor tyrosine kinase, specifies terminal body pattern in Drosophila by Casanova (1989)
10.1126/science.8372355 / Science / Neuroblast specification and formation regulated by wingless in the Drosophila CNS by Chu-LaGraff (1993)
10.1126/science.8424170 / Science / A wingless-dependent polar coordinate system in Drosophila imaginal discs by Couso (1993)
10.1242/dev.120.3.621 / Development / The wingless signalling pathway and the patterning of the wing margin in Drosophila by Couso (1994)
10.1016/0092-8674(94)90195-3 / Cell / Notch is required for wingless signaling in the epidermis of Drosophila by Couso (1994)
10.1101/gad.5.6.996 / Genes Dev / Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc by Cubas (1991)
10.1101/gad.1.3.297 / Genes Dev / Independent subpatterns of sense organs require independent genes of the achaete-scute complex in Drosophila larvae by Dambly-Chaudiere (1987)
10.1242/dev.120.6.1661 / Development / wingless acts through the shaggy/zeste-white 3 kinase to direct dorsal-ventral axis formation in the Drosophila leg by Díaz-Benjumea (1994)
10.1016/0012-1606(85)90446-4 / Dev. Biol / Early events in insect neurogenesis. II. The role of cells interactions and cell lineages in the determination of neuronal precursor cells by Doe (1985)
10.1016/0092-8674(93)90611-S / Cell / Notch: neurogenesis is only part of the picture by Fortini (1993)
10.1073/pnas.79.24.7929 / Proc. Natl. Acad. Sci. USA / Monoclonal antibodies against the Drosophila nervous system by Fujita (1982)
10.1093/genetics/91.3.491 / Genetics / Genetic analysis of the achaete-scute system of Drosophila melanogaster by Garcia-Bellido (1979)
10.1016/0092-8674(87)90124-3 / Cell / Pole region-dependent repression of the Drosophila gap gene Krüppel by maternal gene products by Gaul (1987)
10.1016/0925-4773(90)90135-9 / Mech. Dev / Regulation of Krüppel expression in the anlage of the Malpighian tubules in the Drosophila embryo by Gaul (1990)
10.1016/0168-9525(89)90097-8 / Trends Genet / Genesis of the Drosophila peripheral nervous system by Ghysen (1989)
{'key': '2025011514563566300_DEVELOP_121_8_2313C22', 'first-page': '244', 'article-title': 'Early vertebrate development: Neurulation and the ectoderm', 'volume-title': 'Developmental Biology', 'author': 'Gilbert', 'year': '1994'} / Developmental Biology / Early vertebrate development: Neurulation and the ectoderm by Gilbert (1994)
10.1073/pnas.91.18.8567 / Proc. Natl. Acad. Sci. USA / Redundant functions of the genes knirps and knirps-related for the establishment of anterior Drosophila head structures by González-Gaitán (1994)
{'key': '2025011514563566300_DEVELOP_121_8_2313C24', 'first-page': '1131', 'volume-title': 'Embryonic development of the Drosophila central nervous system. In The Development of Drosophila melanogaster', 'author': 'Goodman', 'year': '1993'} / Embryonic development of the Drosophila central nervous system. In The Development of Drosophila melanogaster by Goodman (1993)
10.1242/dev.113.4.1395 / Development / The determination of sense organs in Drosophila: effect of the neurogenic mutations in the embryo by Goriely (1991)
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)
10.1002/cne.903500304 / J. Comp. Neurology / Embryonic development of the stomatogastric nervous system in Drosophila by Hartenstein (1994)
10.1016/0092-8674(91)90263-X / Cell / The choice of cell fate in the epidermis of Drosophila by Heitzler (1991)
10.1016/0092-8674(90)90364-K / Cell / Induction across germ layers in Drosophila mediated by a genetic cascade by Immerglück (1990)
{'key': '2025011514563566300_DEVELOP_121_8_2313C30', 'first-page': '1207', 'article-title': 'The peripheral nervous system', 'volume-title': 'The Development of Drosophila melanogaste', 'author': 'Jan', 'year': '1993'} / The Development of Drosophila melanogaste / The peripheral nervous system by Jan (1993)
10.1038/282310a0 / Nature / A region of the Drosophila genome necessary for CNS development by Jiménez (1979)
10.1016/0896-6273(90)90036-F / Neuron / Defective neuroblast commitment in mutants of the achaete-scute complex and adjacent genes of Drosophila melanogaster by Jiménez (1990)
10.1101/gad.8.1.118 / Genes Dev / The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal by Klingensmith (1994)
10.1007/BF00848307 / Roux Arch. Dev. Biol / Mutations of early neurogenesis in Drosophila by Lehmann (1981)
10.1002/j.1460-2075.1993.tb06139.x / EMBO J / Role of the gooseberry gene in Drosophila embryos: maintenance of wingless expression by a wingless-gooseberry autoregulatory loop by Li (1993)
{'volume-title': 'The Genome of Drosophila melanogaster', 'year': '1992', 'author': 'Lindsley', 'key': '2025011514563566300_DEVELOP_121_8_2313C36'} / The Genome of Drosophila melanogaster by Lindsley (1992)
10.1038/324537a0 / Nature / A molecular gradient in early Drosophila embryos and its role in specifying the body pattern by Macdonald (1986)
10.1016/0168-9525(94)90153-8 / Trends Genet / Pathways of cell communication during development: signalling and epistases by Martínez Arias (1994)
10.1038/367080a0 / Nature / dishevelled and armadillo act in the wingless signalling pathway in Drosophila by Noordermeer (1994)
10.1101/gad.7.11.2181 / Genes Dev / Activity of Wnt-1 as a transmembrane protein by Parkin (1993)
10.1242/dev.119.Supplement.163 / Development / A model system for cell adhesion and signal transduction in Drosophila by Peifer (1993)
10.1016/0092-8674(90)90413-9 / Cell / The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin by Peifer (1990)
{'key': '2025011514563566300_DEVELOP_121_8_2313C43', 'first-page': '371', 'article-title': 'Stomatogastric nervous system', 'volume-title': 'Comprehensive Insect Physiology, Biochemistry and Pharmacology', 'author': 'Penzlin', 'year': '1985'} / Comprehensive Insect Physiology, Biochemistry and Pharmacology / Stomatogastric nervous system by Penzlin (1985)
10.1016/0092-8674(93)90412-J / Cell / The torso receptor protein-tyrosine kinase signaling pathway: an endless story by Perrimon (1993)
10.1016/0092-8674(94)90351-4 / Cell / The genetic basis of patterned baldness in Drosophila by Perrimon (1994)
10.1073/pnas.23.3.133 / Proc. Natl. Acad. Sci. USA / Chromosomal deficiencies and the embryonic development of Drosophila melanogaster by Poulson (1937)
10.1093/oso/9780199633913.003.0002 / Cellular Interactions in Development: A Practical Approach / Cell transplantation by Prokop (1993)
10.1002/j.1460-2075.1987.tb02474.x / EMBO J / The achaete-scute complex is expressed in neurogenic regions of Drosophila embryos by Romani (1987)
10.1038/362557a0 / Nature / The Drosophila shaggy kinase and rat glycogen synthase kinase-3 have conserved activities and act downstream of Notch by Ruel (1993)
10.1242/dev.117.2.677 / Development / A role for wingless in the segmental gradient of Drosophila by Sampedro (1993)
{'key': '2025011514563566300_DEVELOP_121_8_2313C51', 'first-page': '1', 'article-title': 'Recherches descriptives et expérimentales sur la céphalogenèse de Calliphora erytrocephala (Meigen) au cours des développements embryonnaire et postembryonnaire', 'volume': '103', 'author': 'Schoeller', 'year': '1964', 'journal-title': 'Arch. Zool. Exp. Gen'} / Arch. Zool. Exp. Gen / Recherches descriptives et expérimentales sur la céphalogenèse de Calliphora erytrocephala (Meigen) au cours des développements embryonnaire et postembryonnaire by Schoeller (1964)
10.1016/S0092-8674(05)80065-0 / Cell / wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate by Siegfried (1992)
10.1038/367076a0 / Nature / Components of wingless signalling in Drosophila by Siegfried (1994)
10.1242/dev.109.3.509 / Development / Lateral inhibition and the development of the sensory bristles of the adult peripheral nervous system of Drosophila by Simpson (1990)
10.1242/dev.119.Supplement.29 / Development / A dual role for the protein kinase shaggy in the repression of achaete-scute by Simpson (1993)
{'key': '2025011514563566300_DEVELOP_121_8_2313C56', 'first-page': '941', 'author': 'Skaer', 'year': '1993', 'journal-title': 'The alimentary canal. In The development of Drosophila melanogaster, M. Bate and A. Martinez Arias ed. (Cold Spring Harbor, NY, Cold Spring Harbor Laboratory Press.)'} / The alimentary canal. In The development of Drosophila melanogaster, M. Bate and A. Martinez Arias ed. (Cold Spring Harbor, NY, Cold Spring Harbor Laboratory Press.) by Skaer (1993)
10.1242/dev.114.4.939 / Development / Regulation of proneural gene expression and cell fate during neuroblast segregation in the Drosophila embryo by Skeath (1992)
10.1038/338478a0 / Nature / The Drosophila gene torso encodes a putative receptor tyrosine kinase by Sprenger (1989)
10.1016/0092-8674(93)90072-X / Cell / Organizing activity of wingless protein in Drosophila by Struhl (1993)
10.1007/BF00291041 / Chromosoma / A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback by Tautz (1989)
10.1006/dbio.1993.1243 / Dev. Biol / Crumbs and stardust act in a genetic pathway that controls the organization of epithelia in Drosophila melanogaster by Tepass (1993)
10.1016/0092-8674(89)90020-2 / Cell / Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication by van den Heuvel (1989)
10.1016/0092-8674(87)90495-8 / Cell / The achaete-scute gene complex of Drosophila melanogaster: conserved domains in a subset of genes required for neurogenesis and their homology to myc by Villares (1987)
10.1016/0092-8674(94)90139-2 / Cell / Drosophila wingless sustains engrailed expression only in adjoining cells: evidence from mosaic embryos by Vincent (1994)
10.1007/BF00375906 / Roux Arch. Dev. Biol / Primordium specific requirement of the homeotic gene fork head in the developing gut of the Drosophila embryo by Weigel (1989)
10.1016/0092-8674(89)90133-5 / Cell / The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo by Weigel (1989)
10.1126/science.2158673 / Science / Two gap genes mediate maternal terminal pattern information in Drosophila by Weigel (1990)

Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 10:24 p.m.)
Deposited	7 months, 2 weeks ago (Jan. 15, 2025, 9:58 a.m.)
Indexed	7 months, 2 weeks ago (Jan. 15, 2025, 10:40 a.m.)
Issued	30 years ago (Aug. 1, 1995)
Published	30 years ago (Aug. 1, 1995)
Published Online	30 years ago (Aug. 1, 1995)
Published Print	30 years ago (Aug. 1, 1995)

Funders 0

None

BibTeX

@article{Gonz_lez_Gait_n_1995, title={Invagination centers within the Drosophila stomatogastric nervous system anlage are positioned by Notch-mediated signaling which is spatially controlled through wingless}, volume={121}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.121.8.2313}, DOI={10.1242/dev.121.8.2313}, number={8}, journal={Development}, publisher={The Company of Biologists}, author={González-Gaitán, Marcos and Jäckle, Herbert}, year={1995}, month=aug, pages={2313–2325} }

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      "author": "Artavanis-Tsakonas",
      "year": "1991",
      "journal-title": "Ann. Rev. Cell Biol"
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      "doi-asserted-by": "publisher",
      "first-page": "2877",
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      "article-title": "An early embryonic product of the gene shaggy encodes a serine/threonine protein kinase related to the CDC28/cdc2 subfamily",
      "volume": "9",
      "author": "Bourouis",
      "year": "1990",
      "journal-title": "EMBO J"
    },
    {
      "key": "2025011514563566300_DEVELOP_121_8_2313C3",
      "doi-asserted-by": "publisher",
      "first-page": "457",
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      "article-title": "Two groups of interrelated genes regulate early neurogenesis in Drosophila melanogaster",
      "volume": "197",
      "author": "Brand",
      "year": "1988",
      "journal-title": "Roux Arch. Dev. Biol"
    },
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      "article-title": "The expression of three members of the achaete-scute gene complex correlates with neuroblast segregation in Drosophila",
      "volume": "50",
      "author": "Cabrera",
      "year": "1987",
      "journal-title": "Cell"
    },
    {
      "key": "2025011514563566300_DEVELOP_121_8_2313C5",
      "first-page": "1091",
      "volume-title": "Early neurogenesis in Drosophila melanogaster. In The development of Drosophila melanogaster",
      "author": "Campos-Ortega",
      "year": "1993"
    },
    {
      "key": "2025011514563566300_DEVELOP_121_8_2313C6",
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      "DOI": "10.1007/978-3-662-02454-6",
      "volume-title": "The Embryonic Development of Drosophila melanogaster",
      "author": "Campos-Ortega",
      "year": "1985"
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      "author": "Casanova",
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      "author": "Doe",
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      "author": "Fujita",
      "year": "1982",
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