DOI: 10.1242/dev.129.12.2957. <i>abdominal A</i>specifies one cell type in<i>Drosophila</i>by regulating one principal target gene

abdominal Aspecifies one cell type inDrosophilaby regulating one principal target gene

10.1242/dev.129.12.2957

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

The Hox/homeotic genes encode transcription factors that generate segmental diversity during Drosophila development. At the level of the whole animal, they are believed to carry out this role by regulating a large number of downstream genes. Here we address the unresolved issue of how many Hox target genes are sufficient to define the identity of a single cell. We focus on the larval oenocyte, which is restricted to the abdomen and induced in response to a non-cell autonomous, transient and highly selective input from abdominal A (abdA). We use Hox mutant rescue assays to demonstrate that this function of abdA can be reconstituted by providing Rhomboid (Rho), a processing factor for the EGF receptor ligand, secreted Spitz. Thus, in order to make an oenocyte, abdA regulates just one principal target, rho, that acts at the top of a complex hierarchy of cell-differentiation genes. These studies strongly suggest that, in at least some contexts, Hox genes directly control only a few functional targets within each nucleus. This raises the possibility that much of the overall Hox downstream complexity results from cascades of indirect regulation and cell-to-cell heterogeneity.

Bibliography

Brodu, V., Elstob, P. R., & Gould, A. P. (2002). abdominal Aspecifies one cell type inDrosophilaby regulating one principal target gene. Development, 129(12), 2957â2963.

Authors 3

Véronique Brodu (first)
Philip R. Elstob (additional)
Alex P. Gould (additional)

References 40 Referenced 53

Dates

Type	When
Created	4 years, 4 months ago (April 26, 2021, 12:57 a.m.)
Deposited	2 years, 8 months ago (Dec. 25, 2022, 6:59 a.m.)
Indexed	1 month ago (Aug. 2, 2025, 1:14 a.m.)
Issued	23 years, 2 months ago (June 15, 2002)
Published	23 years, 2 months ago (June 15, 2002)
Published Print	23 years, 2 months ago (June 15, 2002)

Funders 0

None

BibTeX

@article{Brodu_2002, title={abdominal Aspecifies one cell type inDrosophilaby regulating one principal target gene}, volume={129}, ISSN={0950-1991}, url={http://dx.doi.org/10.1242/dev.129.12.2957}, DOI={10.1242/dev.129.12.2957}, number={12}, journal={Development}, publisher={The Company of Biologists}, author={Brodu, Véronique and Elstob, Philip R. and Gould, Alex P.}, year={2002}, month=jun, pages={2957–2963} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        2
      ]
    ],
    "date-time": "2025-08-02T05:14:25Z",
    "timestamp": 1754111665605
  },
  "reference-count": 40,
  "publisher": "The Company of Biologists",
  "issue": "12",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2002,
        6,
        15
      ]
    ]
  },
  "abstract": "<jats:p>The Hox/homeotic genes encode transcription factors that generate segmental diversity during Drosophila development. At the level of the whole animal, they are believed to carry out this role by regulating a large number of downstream genes. Here we address the unresolved issue of how many Hox target genes are sufficient to define the identity of a single cell. We focus on the larval oenocyte, which is restricted to the abdomen and induced in response to a non-cell autonomous, transient and highly selective input from abdominal A (abdA). We use Hox mutant rescue assays to demonstrate that this function of abdA can be reconstituted by providing Rhomboid (Rho), a processing factor for the EGF receptor ligand, secreted Spitz. Thus, in order to make an oenocyte, abdA regulates just one principal target, rho, that acts at the top of a complex hierarchy of cell-differentiation genes. These studies strongly suggest that, in at least some contexts, Hox genes directly control only a few functional targets within each nucleus. This raises the possibility that much of the overall Hox downstream complexity results from cascades of indirect regulation and cell-to-cell heterogeneity.</jats:p>",
  "DOI": "10.1242/dev.129.12.2957",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2021,
        4,
        26
      ]
    ],
    "date-time": "2021-04-26T04:57:48Z",
    "timestamp": 1619413068000
  },
  "page": "2957-2963",
  "source": "Crossref",
  "is-referenced-by-count": 53,
  "title": "<i>abdominal A</i>specifies one cell type in<i>Drosophila</i>by regulating one principal target gene",
  "prefix": "10.1242",
  "volume": "129",
  "author": [
    {
      "given": "Ve\u0301ronique",
      "family": "Brodu",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Philip R.",
      "family": "Elstob",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Alex P.",
      "family": "Gould",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Medical Research Council, National Institute for Medical Research, Mill Hill, London NW7 1AA, UK"
        }
      ]
    }
  ],
  "member": "237",
  "reference": [
    {
      "key": "2021042604203740600_AKAM-1998",
      "doi-asserted-by": "crossref",
      "unstructured": "Akam, M. (1998). Hox genes: from master genes to micromanagers. Curr. Biol.8, R676-R678.",
      "DOI": "10.1016/S0960-9822(98)70433-6"
    },
    {
      "key": "2021042604203740600_BODENSTEIN-1950",
      "unstructured": "Bodenstein, D. (1950). The postembryonic development of Drosophila. In Biology of Drosophila (ed. M. Demerec). New York: John Wiley & Sons."
    },
    {
      "key": "2021042604203740600_BRAND-AND-PERRIMON-1993",
      "doi-asserted-by": "crossref",
      "unstructured": "Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development118, 401-415.",
      "DOI": "10.1242/dev.118.2.401"
    },
    {
      "key": "2021042604203740600_CASARES-ETAL-1996",
      "doi-asserted-by": "crossref",
      "unstructured": "Casares, F., Calleja, M. and Sanchez-Herrero, E. (1996). Functional similarity in appendage specification by the Ultrabithorax and abdominal-A Drosophila HOX genes. EMBO J.15, 3934-3942.",
      "DOI": "10.1002/j.1460-2075.1996.tb00767.x"
    },
    {
      "key": "2021042604203740600_CASARES-AND-MANN-2001",
      "doi-asserted-by": "crossref",
      "unstructured": "Casares, F. and Mann, R. S. (2001). The ground state of the ventral appendage in Drosophila. Science293, 1477-1480.",
      "DOI": "10.1126/science.1062542"
    },
    {
      "key": "2021042604203740600_CASTELLI-GAIR-ETAL-1994",
      "doi-asserted-by": "crossref",
      "unstructured": "Castelli-Gair, J., Greig, S., Micklem, G. and Akam, M. (1994). Dissecting the temporal requirements for homeotic gene function. Development120, 1983-1995.",
      "DOI": "10.1242/dev.120.7.1983"
    },
    {
      "key": "2021042604203740600_ELSTOB-ETAL-2001",
      "doi-asserted-by": "crossref",
      "unstructured": "Elstob, P. R., Brodu, V. and Gould, A. P. (2001). spalt-dependent switching between two cell fates that are induced by the Drosophila EGF receptor. Development128, 723-732.",
      "DOI": "10.1242/dev.128.5.723"
    },
    {
      "key": "2021042604203740600_GONZALEZ-CRESPO-AND-MORATA-1995",
      "doi-asserted-by": "crossref",
      "unstructured": "Gonzalez-Crespo, S. and Morata, G. (1995). Control of Drosophila adult pattern by extradenticle. Development121, 2117-2125.",
      "DOI": "10.1242/dev.121.7.2117"
    },
    {
      "key": "2021042604203740600_GOULD-ETAL-2001",
      "doi-asserted-by": "crossref",
      "unstructured": "Gould, A. P., Elstob, P. R. and Brodu, V. (2001). Insect oenocytes: a model system for studying cell-fate specification by Hox genes. J. Anat.199, 25-33.",
      "DOI": "10.1017/S0021878201008317"
    },
    {
      "key": "2021042604203740600_GRABA-ETAL-1997",
      "doi-asserted-by": "crossref",
      "unstructured": "Graba, Y., Aragnol, D. and Pradel, J. (1997). Drosophila Hox complex downstream targets and the function of homeotic genes. BioEssays19, 379-388.",
      "DOI": "10.1002/bies.950190505"
    },
    {
      "key": "2021042604203740600_HASSAN-ETAL-2000",
      "doi-asserted-by": "crossref",
      "unstructured": "Hassan, B. A., Bermingham, N. A., He, Y., Sun, Y., Jan, Y. N., Zoghbi, H. Y. and Bellen, H. J. (2000). atonal regulates neurite arborization but does not act as a proneural gene in the Drosophila brain. Neuron25, 549-561.",
      "DOI": "10.1016/S0896-6273(00)81059-4"
    },
    {
      "key": "2021042604203740600_HEUER-AND-KAUFMAN-1992",
      "doi-asserted-by": "crossref",
      "unstructured": "Heuer, J. G. and Kaufman, T. C. (1992). Homeotic genes have specific functional roles in the establishment of the Drosophila embryonic peripheral nervous system. Development115, 35-47.",
      "DOI": "10.1242/dev.115.1.35"
    },
    {
      "key": "2021042604203740600_HOPPLER-AND-BIENZ-1995",
      "doi-asserted-by": "crossref",
      "unstructured": "Hoppler, S. and Bienz, M. (1995). Two different thresholds of wingless signalling with distinct developmental consequences in the Drosophila midgut. EMBO J.14, 5016-5026.",
      "DOI": "10.1002/j.1460-2075.1995.tb00184.x"
    },
    {
      "key": "2021042604203740600_IMMERGLUCK-ETAL-1990",
      "doi-asserted-by": "crossref",
      "unstructured": "Immergluck, K., Lawrence, P. A. and Bienz, M. (1990). Induction across germ layers in Drosophila mediated by a genetic cascade. Cell62, 261-268.",
      "DOI": "10.1016/0092-8674(90)90364-K"
    },
    {
      "key": "2021042604203740600_JARMAN-ETAL-1993",
      "doi-asserted-by": "crossref",
      "unstructured": "Jarman, A. P., Grau, Y., Jan, L. Y. and Jan, Y. N. (1993). atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell73, 1307-1321.",
      "DOI": "10.1016/0092-8674(93)90358-W"
    },
    {
      "key": "2021042604203740600_JARMAN-ETAL-1995",
      "doi-asserted-by": "crossref",
      "unstructured": "Jarman, A. P., Sun, Y., Jan, L. Y. and Jan, Y. N. (1995). Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development121, 2019-2030.",
      "DOI": "10.1242/dev.121.7.2019"
    },
    {
      "key": "2021042604203740600_KELLERMAN-ETAL-1990",
      "doi-asserted-by": "crossref",
      "unstructured": "Kellerman, K. A., Mattson, D. M. and Duncan, I. (1990). Mutations affecting the stability of the fushi tarazu protein of Drosophila. Genes Dev.4, 1936-1950.",
      "DOI": "10.1101/gad.4.11.1936"
    },
    {
      "key": "2021042604203740600_LEE-ETAL-2001",
      "doi-asserted-by": "crossref",
      "unstructured": "Lee, J. R., Urban, S., Garvey, C. F. and Freeman, M. (2001). Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila. Cell107, 161-171.",
      "DOI": "10.1016/S0092-8674(01)00526-8"
    },
    {
      "key": "2021042604203740600_LEWIS-1978",
      "doi-asserted-by": "crossref",
      "unstructured": "Lewis, E. B. (1978). A gene complex controlling segmentation in Drosophila. Nature276, 565-570.",
      "DOI": "10.1038/276565a0"
    },
    {
      "key": "2021042604203740600_MACIAS-ETAL-1990",
      "doi-asserted-by": "crossref",
      "unstructured": "Macias, A., Casanova, J. and Morata, G. (1990). Expression and regulation of the abd-A gene of Drosophila. Development110, 1197-1207.",
      "DOI": "10.1242/dev.110.4.1197"
    },
    {
      "key": "2021042604203740600_MACIAS-AND-MORATA-1996",
      "doi-asserted-by": "crossref",
      "unstructured": "Macias, A. and Morata, G. (1996). Functional hierarchy and phenotypic suppression among Drosophila homeotic genes: the labial and empty spiracles genes. EMBO J.15, 334-343.",
      "DOI": "10.1002/j.1460-2075.1996.tb00363.x"
    },
    {
      "key": "2021042604203740600_MANN-AND-CHAN-1996",
      "doi-asserted-by": "crossref",
      "unstructured": "Mann, R. and Chan, S.-K. (1996). Extra specificity from extradenticle: the partnership between HOX and PBX/EXD homeodomain proteins. Trends Genet.12, 258-262.",
      "DOI": "10.1016/0168-9525(96)10026-3"
    },
    {
      "key": "2021042604203740600_MANN-AND-MORATA-2000",
      "doi-asserted-by": "crossref",
      "unstructured": "Mann, R. S. and Morata, G. (2000). The developmental and molecular biology of genes that subdivide the body of Drosophila. Annu. Rev. Cell Dev. Biol.16, 243-271.",
      "DOI": "10.1146/annurev.cellbio.16.1.243"
    },
    {
      "key": "2021042604203740600_MCGINNIS-AND-KRUMLAUF-1992",
      "doi-asserted-by": "crossref",
      "unstructured": "McGinnis, W. and Krumlauf, R. (1992). Homeobox genes and axial patterning. Cell68, 283-302.",
      "DOI": "10.1016/0092-8674(92)90471-N"
    },
    {
      "key": "2021042604203740600_MICHELSON-1994",
      "doi-asserted-by": "crossref",
      "unstructured": "Michelson, A. M. (1994). Muscle pattern diversification in Drosophila is determined by the autonomous function of homeotic genes in the embryonic mesoderm. Development120, 755-768.",
      "DOI": "10.1242/dev.120.4.755"
    },
    {
      "key": "2021042604203740600_QUEENAN-ETAL-1997",
      "doi-asserted-by": "crossref",
      "unstructured": "Queenan, A. M., Ghabrial, A. and Schupbach, T. (1997). Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo. Development124, 3871-3880.",
      "DOI": "10.1242/dev.124.19.3871"
    },
    {
      "key": "2021042604203740600_RAUSKOLB-ETAL-1993",
      "doi-asserted-by": "crossref",
      "unstructured": "Rauskolb, C., Peifer, M. and Wieschaus, E. (1993). extradenticle, a regulator of homeotic gene activity, is a homolog of the homeobox-containing human proto-oncogene pbx1. Cell74, 1101-1112.",
      "DOI": "10.1016/0092-8674(93)90731-5"
    },
    {
      "key": "2021042604203740600_REUTER-ETAL-1990",
      "doi-asserted-by": "crossref",
      "unstructured": "Reuter, R., Panganiban, G. E. F., Hoffmann, F. M. and Scott, M. P. (1990). Homeotic genes regulate the spatial expression of putative growth factors in the visceral mesoderm of Drosophila embryos. Development110, 1031-1040.",
      "DOI": "10.1242/dev.110.4.1031"
    },
    {
      "key": "2021042604203740600_RUIZ-DE-MENA-ETAL-1999",
      "doi-asserted-by": "crossref",
      "unstructured": "Ruiz de Mena, I., Fernandez-Moreno, M. A., Bornstein, B., Kaguni, L. S. and Garesse, R. (1999). Structure and regulated expression of the delta-aminolevulinate synthase gene from Drosophila melanogaster. J. Biol. Chem.274, 37321-37328.",
      "DOI": "10.1074/jbc.274.52.37321"
    },
    {
      "key": "2021042604203740600_RUSTEN-ETAL-2001",
      "unstructured": "Rusten, T. E., Cantera, R., Urban, J., Technau, G., Kafatos, F. C. and Barrio, R. (2001). Spalt restricts EGFR mediated induction of chordotonal precursors in the embryonic PNS of Drosophila. Development128, 711-722."
    },
    {
      "key": "2021042604203740600_SCHWEITZER-ETAL-1995",
      "doi-asserted-by": "crossref",
      "unstructured": "Schweitzer, R., Shaharabany, M., Seger, R. and Shilo, B. Z. (1995). Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes Dev.9, 1518-1529.",
      "DOI": "10.1101/gad.9.12.1518"
    },
    {
      "key": "2021042604203740600_STRUHL-1983",
      "doi-asserted-by": "crossref",
      "unstructured": "Struhl, G. (1983). Role of the esc+ gene product in ensuring the selective expression of segment-specific homeotic genes in Drosophila. J. Embryol. Exp. Morphol.76, 297-331.",
      "DOI": "10.1242/dev.76.1.297"
    },
    {
      "key": "2021042604203740600_SZUTS-ETAL-1997",
      "doi-asserted-by": "crossref",
      "unstructured": "Szuts, D., Freeman, M. and Bienz, M. (1997). Antagonism between EGFR and Wingless signalling in the larval cuticle of Drosophila. Development124, 3209-3219.",
      "DOI": "10.1242/dev.124.16.3209"
    },
    {
      "key": "2021042604203740600_SZUTS-ETAL-1998",
      "doi-asserted-by": "crossref",
      "unstructured": "Szuts, D., Eresh, S. and Bienz, M. (1998). Functional intertwining of Dpp and EGFR signaling during Drosophila endoderm induction. Genes Dev.12, 2022-2035.",
      "DOI": "10.1101/gad.12.13.2022"
    },
    {
      "key": "2021042604203740600_VACHON-ETAL-1992",
      "doi-asserted-by": "crossref",
      "unstructured": "Vachon, G., Cohen, B., Pfeifle, C., McGuffin, M. E., Botas, J. and Cohen, S. M. (1992). Homeotic genes of the Bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene Distal-less. Cell71, 437-450.",
      "DOI": "10.1016/0092-8674(92)90513-C"
    },
    {
      "key": "2021042604203740600_WAKIMOTO-AND-KAUFMAN-1981",
      "doi-asserted-by": "crossref",
      "unstructured": "Wakimoto, B. T. and Kaufman, T. C. (1981). Analysis of larval segmentation in lethal genotypes associated with the Antennapedia gene complex in Drosophila melanogaster. Dev. Biol.81, 51-64.",
      "DOI": "10.1016/0012-1606(81)90347-X"
    },
    {
      "key": "2021042604203740600_WEATHERBEE-ETAL-1998",
      "doi-asserted-by": "crossref",
      "unstructured": "Weatherbee, S. D., Halder, G., Kim, J., Hudson, A. and Carroll, S. (1998). Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev.12, 1474-1482.",
      "DOI": "10.1101/gad.12.10.1474"
    },
    {
      "key": "2021042604203740600_WHITE-AND-WILCOX-1984",
      "doi-asserted-by": "crossref",
      "unstructured": "White, R. A. and Wilcox, M. (1984). Protein products of the bithorax complex in Drosophila. Cell39, 163-171.",
      "DOI": "10.1016/0092-8674(84)90202-2"
    },
    {
      "key": "2021042604203740600_WIELLETTE-AND-MCGINNIS-1999",
      "doi-asserted-by": "crossref",
      "unstructured": "Wiellette, E. L. and McGinnis, W. (1999). Hox genes differentially regulate Serrate to generate segment-specific structures. Development126, 1985-1995.",
      "DOI": "10.1242/dev.126.9.1985"
    },
    {
      "key": "2021042604203740600_YU-ETAL-1996",
      "doi-asserted-by": "crossref",
      "unstructured": "Yu, X., Hoppler, S., Eresh, S. and Bienz, M. (1996). decapentaplegic, a target gene of the wingless signalling pathway in the Drosophila midgut. Development122, 849-858.",
      "DOI": "10.1242/dev.122.3.849"
    }
  ],
  "container-title": "Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "http://journals.biologists.com/dev/article-pdf/129/12/2957/1205393/2957.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "http://journals.biologists.com/dev/article-pdf/129/12/2957/1205393/2957.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        12,
        25
      ]
    ],
    "date-time": "2022-12-25T11:59:28Z",
    "timestamp": 1671969568000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/dev/article/129/12/2957/41763/abdominal-A-specifies-one-cell-type-in-Drosophila"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2002,
        6,
        15
      ]
    ]
  },
  "references-count": 40,
  "journal-issue": {
    "issue": "12",
    "published-print": {
      "date-parts": [
        [
          2002,
          6,
          15
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/dev.129.12.2957",
  "relation": {},
  "ISSN": [
    "1477-9129",
    "0950-1991"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2002,
        6,
        15
      ]
    ]
  }
}