DOI: 10.1242/dev.124.23.4769. The metalloprotease-disintegrin Kuzbanian participates in <i>Notch</i> activation during growth and patterning of <i>Drosophila</i> imaginal discs

The metalloprotease-disintegrin Kuzbanian participates in Notch activation during growth and patterning of Drosophila imaginal discs

10.1242/dev.124.23.4769

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT The Notch transmembrane protein is the receptor of an evolutionary conserved pathway that mediates intercellular signalling leading to the specification of different cell types during development. In this pathway, many aspects of the signal transduction mechanism remain poorly understood, especially the role of proteolytic processing of Notch. We present genetic evidence indicating that the met-alloprotease-disintegrin kuzbanian (J. Rooke, D. Pan, T. Xu and G. M. Rubin (1996) Science 273, 1227–1231) is a new component of the Notch signalling pathway and is involved in Notch activation. kuzbanian genetic mosaics demonstrate that, during neurogenesis, wing margin formation and vein width specification kuzbanian is autonomously required in the cell where Notch is activated. Genetic interactions between kuzbanian and different genes of the Notch pathway indicate that kuzbanian is required upstream of Suppressor of Hairless. Moreover, the requirement of kuzbanian for signalling by a ligand-dependent Abruptex receptor, but not by a constitutively activated form of Notch, suggests that kuzbanian is involved in the generation of a Notch functional receptor and/or in its activation. However, differences in the phenotypes of loss-of-function Notch and kuzbanian mutations suggest the existence of alternative Kuzbanian-independent mechanisms that generate Notch functional receptors.

Bibliography

Sotillos, S., Roch, F., & Campuzano, S. (1997). The metalloprotease-disintegrin Kuzbanian participates in Notch activation during growth and patterning of Drosophila imaginal discs. Development, 124(23), 4769â4779.

Authors 3

Sol Sotillos (first)
Fernando Roch (additional)
Sonsoles Campuzano (additional)

References 57 Referenced 132

10.1126/science.7716513 / Science / Notch signaling by Artavanis-Tsakonas (1995)
{'volume-title': 'Drosophila A Laboratory Handbook', 'year': '1989', 'author': 'Ashburner', 'key': '2025021406033342600_DEVELOP_124_23_4769C2'} / Drosophila A Laboratory Handbook by Ashburner (1989)
10.1101/gad.9.21.2609 / Genes Dev / Suppressor of Hairless directly activates transcription of Enhancer of split Complex genes in response to Notch receptor activity by Bailey (1995)
10.1006/dbio.1995.8033 / Dev. Biol / Hairless promotes stable commitment to the sensory organ precursor cell fate by negatively regulating the activity of the Notch signaling pathway by Bang (1995)
10.1016/S0092-8674(00)80336-0 / Cell / Intracellular cleavage of Notch leads to a heterodimeric receptor on the plasma membrane by Blaumueller (1997)
10.1242/dev.118.2.401 / Development / Targeted gene expression as a means of altering cell fates and generating dominant phenotypes by Brand (1993)
10.1101/gad.8.20.2491 / Genes Dev / Inhibition of the DNA-binding activity of Drosophila Supressor of Hairless and of its human homolog, KBF2/RBP-Jk, by direct protein-protein interaction with Drosophila Hairless by Brou (1994)
10.1002/neu.480241005 / J. Neurobiol / Mechanisms of early neurogenesis in Drosophila melanogaster by Campos-Ortega (1993)
10.1038/375761a0 / Nature / Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogeneic gene Delta by Chitnis (1995)
10.1016/S0960-9822(95)00281-8 / C urrent Biol / Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila by Couso (1995)
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)
10.1073/pnas.88.2.632 / Proc. Natl. Acad. Sci. USA / Cell-autonomous role of Notch, an epidermal growth factor homologue, in sensory organ differentiation in Drosophila by de Celis (1991)
10.1093/genetics/136.1.183 / Genetics / Modifications of the Notch function by Abruptex mutations in Drosophila melanogaster by de Celis (1994)
10.1016/0925-4773(94)90080-9 / Mech. Dev / Roles of the Notch gene in Drosophila wing morphogenesis by de Celis (1994)
10.1242/dev.122.1.359 / Development / Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc by de Celis (1996)
10.1242/dev.122.9.2719 / Development / Functional relationships between Notch, Su(H) and the bHLH genes of the E(sp1) complex: the E(sp1) genes mediate only a subset of Notch activities during imaginal development by de Celis (1996)
10.1242/dev.124.10.1919 / Development / Notch signalling regulates veinlet expression and establishes boundaries between veins and interveins in the Drosophila wing by de Celis (1997)
10.1242/dev.124.6.1139 / Development / Conservation of the Notch signalling pathway in mammalian neurogenesis by de la Pompa (1997)
10.1093/nar/12.1Part1.387 / Nuc. Acids Res / A comprehensive set of sequence analysis programs for the VAX by Devereux (1984)
10.1242/dev.121.12.4215 / Development / Serrate signals through Notch to establish a Wingless-dependent organizer at the dorso-ventral compartment boundary of the Drosophila wing by Diaz-Benjumea (1995)
10.1101/gad.10.4.421 / Genes Dev / Delta is a ventral to dorsal signal complementary to Serrate, another Notch ligand, in Drosophila wing formation by Doherty (1996)
10.1016/0092-8674(91)90111-B / Cell / TAN-1, the human homologue of Drosophila Notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms by Ellisen (1991)
10.1073/pnas.93.23.13233 / Proc. Nat. Acad. Sci. USA / The cell surface metalloprotease/disintegrin Kuzbanian is required for axonal extension in Drosophila by Fambrough (1996)
{'key': '2025021406033342600_DEVELOP_124_23_4769C24', 'first-page': '423', 'article-title': 'Molecular interactions between the protein products of the neurogenic loci', 'volume': '61', 'author': 'Fehon', 'year': '1990', 'journal-title': 'Notch and Delta, two EGF-homologous genes in Drosophila. Cell'} / Notch and Delta, two EGF-homologous genes in Drosophila. Cell / Molecular interactions between the protein products of the neurogenic loci by Fehon (1990)
10.1016/0092-8674(94)90196-1 / Cell / The Suppressor of Hairless protein participates in Notch receptor signalling by Fortini (1994)
10.1242/dev.122.6.1673 / Development / Subcellular localization of Suppressor of Hairless in Drosophila sense organ cells during development by Gho (1996)
10.1016/S0092-8674(00)81085-5 / Cell / araucan and caupolican, two members of the novel Iroquois complex, encode homeoproteins that control proneural and vein forming genes by Gómez-Skarmeta (1996)
10.1016/0012-1606(90)90147-B / Dev. Biol / A dual function of the Notch gene in Drosophila sensillum development by Hartenstein (1990)
10.1242/dev.122.1.161 / Development / Genes of the Enhancer of split and achaete-scute complexes are required for a regulatory loop between Notch and Delta during lateral signalling in Drosophila by Heitzler (1996)
10.1016/0092-8674(91)90263-X / Cell / The choice of cell fate in the epidermis of Drosophila by Heitzler (1991)
10.1242/dev.111.4.1087 / Development / The emergence of sense organs in the wing disc of Drosophila by Huang (1991)
10.1038/377355a0 / Nature / Signalling downstream of activated mammalian Notch by Jarriault (1995)
10.1242/dev.121.11.3745 / Development / Role of Notch and achaete-scute complex in the expression of Enhancer of split bHLH proteins by Jennings (1995)
10.1038/382133a0 / Nature / Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene by Kim (1996)
10.1073/pnas.93.4.1683 / Proc. Natl. Acad. Sci. USA / Signal transduction by activated mNotch: Importance of proteolytic processing and its regulation by the extracellular domain by Kopan (1996)
10.1101/gad.9.21.2598 / Genes Dev / The neurogenic Suppressor of Hairless DNA-binding protein mediates transcriptional activation of the Enhancer of split Complex genes triggered by Notch signaling by Lecourtois (1995)
{'volume-title': 'The Genome of Drosophila melanogaster', 'year': '1992', 'author': 'Lindsley', 'key': '2025021406033342600_DEVELOP_124_23_4769C37'} / The Genome of Drosophila melanogaster by Lindsley (1992)
10.1242/dev.121.8.2633 / Development / Deltex acts as a positive regulator of Notch signaling through interaction with the Notch ankyrin repeats by Matsuno (1995)
{'key': '2025021406033342600_DEVELOP_124_23_4769C39', 'first-page': '285', 'article-title': 'Patterning of adult peripheral nervous system of Drosophila', 'volume': '4', 'author': 'Modolell', 'year': '1997', 'journal-title': 'Persp. Dev Neurobiol'} / Persp. Dev Neurobiol / Patterning of adult peripheral nervous system of Drosophila by Modolell (1997)
10.1016/S0896-6273(00)80046-X / Neuron / Persistent expression of genes of the Enhancer of Split complex suppresses neural development in Drosophila by Nakao (1996)
10.1016/S0092-8674(00)80335-9 / Cell / Kuzbanian controls proteolytic processing of Notch and mediates lateral inhibition during Drosophila and vertebrate neurogenesis by Pan (1997)
{'key': '2025021406033342600_DEVELOP_124_23_4769C42', 'article-title': 'Screening of larval/pupal P-element induced lethals of the second chromosome in Drosophila melanogaster: clonal analysis and morphology of imaginal discs', 'volume-title': 'Mol. Gen. Genet. in press', 'author': 'Roch', 'year': '1997'} / Mol. Gen. Genet. in press / Screening of larval/pupal P-element induced lethals of the second chromosome in Drosophila melanogaster: clonal analysis and morphology of imaginal discs by Roch (1997)
{'key': '2025021406033342600_DEVELOP_124_23_4769C43', 'first-page': '1227', 'article-title': 'tKUZ, a conserved metalloprotease-disintegrin protein with two roles in Drosophila neurogenesis', 'volume': '273', 'author': 'Rooke', 'year': '1996', 'journal-title': 'Sc ience'} / Sc ience / tKUZ, a conserved metalloprotease-disintegrin protein with two roles in Drosophila neurogenesis by Rooke (1996)
{'volume-title': 'Molecular Cloning', 'year': '1989', 'author': 'Sambrook', 'key': '2025021406033342600_DEVELOP_124_23_4769C44'} / Molecular Cloning by Sambrook (1989)
10.1242/dev.121.6.1875 / Development / Suppressor of Hairless is required for signal reception during lateral inhibition in the Drosophila pupal notum by Schweisguth (1995)
10.1016/0092-8674(92)90641-O / Cell / Suppressor of Hairless, the Drosophila homolog of the mouse recombination signal-binding protein regulates peripheral nervous system development by Schweisguth (1992)
10.1242/dev.120.6.1433 / Development / Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis by Schweisguth (1994)
10.1016/0012-1606(78)90226-9 / Dev. Biol / Temperature-sensitive periods and autonomy of pleiotropic effects of 1(1)Nts1, a conditional Notch lethal in Drosophila by Shellenbarger (1978)
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)
10.1101/gad.5.6.984 / Genes Dev / Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing by Skeath (1991)
10.1016/0092-8674(93)90424-O / Cell / Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo by Struhl (1993)
10.1016/0925-4773(95)00377-0 / Mech. Dev / Inhibition of cell fate in Drosophila by Enhancer of split genes by Tata (1995)
10.1242/dev.111.3.749 / Development / The Drosophila gene Serrate encodes an EGF-like transmembrane protein with a complex expression pattern in embryos and wing discs by Thomas (1991)
10.1093/genetics/135.1.71 / Genetics / P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: isolation of lethals with different overgrowth phenotypes by Torok (1993)
10.1083/jcb.131.2.275 / J. Cell. Biol / ADAM, a novel family of membrane proteins containing a disintegrin and metalloprotease domain: multipotential functions in cell-cell and cell-matrix interactions by Wolfsberg (1995)
10.1242/dev.117.4.1223 / Development / Analysis of genetic mosaics in developing and adult Drosophila tissues by Xu (1993)
10.1073/pnas.92.14.6414 / Proc. Natl. Acad. Sci. USA / Alterations in Notch signaling in neoplastic lesions of the human cervix by Zagouras (1995)

Dates

Type	When
Created	4 years, 3 months ago (April 25, 2021, 11:10 p.m.)
Deposited	6 months, 1 week ago (Feb. 14, 2025, 1:04 a.m.)
Indexed	4 weeks, 1 day ago (July 24, 2025, 7:06 a.m.)
Issued	27 years, 8 months ago (Dec. 1, 1997)
Published	27 years, 8 months ago (Dec. 1, 1997)
Published Online	27 years, 8 months ago (Dec. 1, 1997)
Published Print	27 years, 8 months ago (Dec. 1, 1997)

Funders 0

None

BibTeX

@article{Sotillos_1997, title={The metalloprotease-disintegrin Kuzbanian participates in Notch activation during growth and patterning of Drosophila imaginal discs}, volume={124}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.124.23.4769}, DOI={10.1242/dev.124.23.4769}, number={23}, journal={Development}, publisher={The Company of Biologists}, author={Sotillos, Sol and Roch, Fernando and Campuzano, Sonsoles}, year={1997}, month=dec, pages={4769–4779} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        24
      ]
    ],
    "date-time": "2025-07-24T11:06:54Z",
    "timestamp": 1753355214351,
    "version": "3.37.0"
  },
  "reference-count": 57,
  "publisher": "The Company of Biologists",
  "issue": "23",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1997,
            12,
            1
          ]
        ],
        "date-time": "1997-12-01T00:00:00Z",
        "timestamp": 880934400000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "http://www.biologists.com/user-licence-1-1/"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1997,
        12,
        1
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>The Notch transmembrane protein is the receptor of an evolutionary conserved pathway that mediates intercellular signalling leading to the specification of different cell types during development. In this pathway, many aspects of the signal transduction mechanism remain poorly understood, especially the role of proteolytic processing of Notch. We present genetic evidence indicating that the met-alloprotease-disintegrin kuzbanian (J. Rooke, D. Pan, T. Xu and G. M. Rubin (1996) Science 273, 1227\u20131231) is a new component of the Notch signalling pathway and is involved in Notch activation. kuzbanian genetic mosaics demonstrate that, during neurogenesis, wing margin formation and vein width specification kuzbanian is autonomously required in the cell where Notch is activated. Genetic interactions between kuzbanian and different genes of the Notch pathway indicate that kuzbanian is required upstream of Suppressor of Hairless. Moreover, the requirement of kuzbanian for signalling by a ligand-dependent Abruptex receptor, but not by a constitutively activated form of Notch, suggests that kuzbanian is involved in the generation of a Notch functional receptor and/or in its activation. However, differences in the phenotypes of loss-of-function Notch and kuzbanian mutations suggest the existence of alternative Kuzbanian-independent mechanisms that generate Notch functional receptors.</jats:p>",
  "DOI": "10.1242/dev.124.23.4769",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2021,
        4,
        26
      ]
    ],
    "date-time": "2021-04-26T03:10:53Z",
    "timestamp": 1619406653000
  },
  "page": "4769-4779",
  "source": "Crossref",
  "is-referenced-by-count": 132,
  "title": "The metalloprotease-disintegrin Kuzbanian participates in <i>Notch</i> activation during growth and patterning of <i>Drosophila</i> imaginal discs",
  "prefix": "10.1242",
  "volume": "124",
  "author": [
    {
      "given": "Sol",
      "family": "Sotillos",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Centro de Biologia Molecular Severo Ochoa, CSIC and UAM , 28049 Madrid, Spain"
        }
      ]
    },
    {
      "given": "Fernando",
      "family": "Roch",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Centro de Biologia Molecular Severo Ochoa, CSIC and UAM , 28049 Madrid, Spain"
        }
      ]
    },
    {
      "given": "Sonsoles",
      "family": "Campuzano",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Centro de Biologia Molecular Severo Ochoa, CSIC and UAM , 28049 Madrid, Spain"
        }
      ]
    }
  ],
  "member": "237",
  "published-online": {
    "date-parts": [
      [
        1997,
        12,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C1",
      "doi-asserted-by": "publisher",
      "first-page": "225",
      "DOI": "10.1126/science.7716513",
      "article-title": "Notch signaling",
      "volume": "268",
      "author": "Artavanis-Tsakonas",
      "year": "1995",
      "journal-title": "Science"
    },
    {
      "volume-title": "Drosophila A Laboratory Handbook",
      "year": "1989",
      "author": "Ashburner",
      "key": "2025021406033342600_DEVELOP_124_23_4769C2"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C3",
      "doi-asserted-by": "publisher",
      "first-page": "2609",
      "DOI": "10.1101/gad.9.21.2609",
      "article-title": "Suppressor of Hairless directly activates transcription of Enhancer of split Complex genes in response to Notch receptor activity",
      "volume": "9",
      "author": "Bailey",
      "year": "1995",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C4",
      "doi-asserted-by": "publisher",
      "first-page": "479494",
      "DOI": "10.1006/dbio.1995.8033",
      "article-title": "Hairless promotes stable commitment to the sensory organ precursor cell fate by negatively regulating the activity of the Notch signaling pathway",
      "volume": "172",
      "author": "Bang",
      "year": "1995",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C5",
      "doi-asserted-by": "publisher",
      "first-page": "281",
      "DOI": "10.1016/S0092-8674(00)80336-0",
      "article-title": "Intracellular cleavage of Notch leads to a heterodimeric receptor on the plasma membrane",
      "volume": "90",
      "author": "Blaumueller",
      "year": "1997",
      "journal-title": "Cell"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C6",
      "doi-asserted-by": "publisher",
      "first-page": "401",
      "DOI": "10.1242/dev.118.2.401",
      "article-title": "Targeted gene expression as a means of altering cell fates and generating dominant phenotypes",
      "volume": "118",
      "author": "Brand",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C7",
      "doi-asserted-by": "publisher",
      "first-page": "2491",
      "DOI": "10.1101/gad.8.20.2491",
      "article-title": "Inhibition of the DNA-binding activity of Drosophila Supressor of Hairless and of its human homolog, KBF2/RBP-Jk, by direct protein-protein interaction with Drosophila Hairless",
      "volume": "8",
      "author": "Brou",
      "year": "1994",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C8",
      "doi-asserted-by": "publisher",
      "first-page": "1305",
      "DOI": "10.1002/neu.480241005",
      "article-title": "Mechanisms of early neurogenesis in Drosophila melanogaster",
      "volume": "24",
      "author": "Campos-Ortega",
      "year": "1993",
      "journal-title": "J. Neurobiol"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C9",
      "doi-asserted-by": "publisher",
      "first-page": "761",
      "DOI": "10.1038/375761a0",
      "article-title": "Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogeneic gene Delta",
      "volume": "375",
      "author": "Chitnis",
      "year": "1995",
      "journal-title": "Nature"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C10",
      "doi-asserted-by": "publisher",
      "first-page": "1437",
      "DOI": "10.1016/S0960-9822(95)00281-8",
      "article-title": "Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila",
      "volume": "5",
      "author": "Couso",
      "year": "1995",
      "journal-title": "C urrent Biol"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C11",
      "doi-asserted-by": "publisher",
      "first-page": "996",
      "DOI": "10.1101/gad.5.6.996",
      "article-title": "Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc",
      "volume": "5",
      "author": "Cubas",
      "year": "1991",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C12",
      "doi-asserted-by": "publisher",
      "first-page": "632",
      "DOI": "10.1073/pnas.88.2.632",
      "article-title": "Cell-autonomous role of Notch, an epidermal growth factor homologue, in sensory organ differentiation in Drosophila",
      "volume": "88",
      "author": "de Celis",
      "year": "1991",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C13",
      "doi-asserted-by": "publisher",
      "first-page": "183",
      "DOI": "10.1093/genetics/136.1.183",
      "article-title": "Modifications of the Notch function by Abruptex mutations in Drosophila melanogaster",
      "volume": "136",
      "author": "de Celis",
      "year": "1994",
      "journal-title": "Genetics"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C14",
      "doi-asserted-by": "publisher",
      "first-page": "109",
      "DOI": "10.1016/0925-4773(94)90080-9",
      "article-title": "Roles of the Notch gene in Drosophila wing morphogenesis",
      "volume": "46",
      "author": "de Celis",
      "year": "1994",
      "journal-title": "Mech. Dev"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C15",
      "doi-asserted-by": "publisher",
      "first-page": "359",
      "DOI": "10.1242/dev.122.1.359",
      "article-title": "Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc",
      "volume": "122",
      "author": "de Celis",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C16",
      "doi-asserted-by": "publisher",
      "first-page": "2719",
      "DOI": "10.1242/dev.122.9.2719",
      "article-title": "Functional relationships between Notch, Su(H) and the bHLH genes of the E(sp1) complex: the E(sp1) genes mediate only a subset of Notch activities during imaginal development",
      "volume": "122",
      "author": "de Celis",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C17",
      "doi-asserted-by": "publisher",
      "first-page": "1919",
      "DOI": "10.1242/dev.124.10.1919",
      "article-title": "Notch signalling regulates veinlet expression and establishes boundaries between veins and interveins in the Drosophila wing",
      "volume": "124",
      "author": "de Celis",
      "year": "1997",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C18",
      "doi-asserted-by": "publisher",
      "first-page": "1139",
      "DOI": "10.1242/dev.124.6.1139",
      "article-title": "Conservation of the Notch signalling pathway in mammalian neurogenesis",
      "volume": "124",
      "author": "de la Pompa",
      "year": "1997",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C19",
      "doi-asserted-by": "publisher",
      "first-page": "387",
      "DOI": "10.1093/nar/12.1Part1.387",
      "article-title": "A comprehensive set of sequence analysis programs for the VAX",
      "volume": "12",
      "author": "Devereux",
      "year": "1984",
      "journal-title": "Nuc. Acids Res"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C20",
      "doi-asserted-by": "publisher",
      "first-page": "42154225",
      "DOI": "10.1242/dev.121.12.4215",
      "article-title": "Serrate signals through Notch to establish a Wingless-dependent organizer at the dorso-ventral compartment boundary of the Drosophila wing",
      "volume": "121",
      "author": "Diaz-Benjumea",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C21",
      "doi-asserted-by": "publisher",
      "first-page": "421",
      "DOI": "10.1101/gad.10.4.421",
      "article-title": "Delta is a ventral to dorsal signal complementary to Serrate, another Notch ligand, in Drosophila wing formation",
      "volume": "10",
      "author": "Doherty",
      "year": "1996",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C22",
      "doi-asserted-by": "publisher",
      "first-page": "649661",
      "DOI": "10.1016/0092-8674(91)90111-B",
      "article-title": "TAN-1, the human homologue of Drosophila Notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms",
      "volume": "66",
      "author": "Ellisen",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C23",
      "doi-asserted-by": "publisher",
      "first-page": "13233",
      "DOI": "10.1073/pnas.93.23.13233",
      "article-title": "The cell surface metalloprotease/disintegrin Kuzbanian is required for axonal extension in Drosophila",
      "volume": "93",
      "author": "Fambrough",
      "year": "1996",
      "journal-title": "Proc. Nat. Acad. Sci. USA"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C24",
      "first-page": "423",
      "article-title": "Molecular interactions between the protein products of the neurogenic loci",
      "volume": "61",
      "author": "Fehon",
      "year": "1990",
      "journal-title": "Notch and Delta, two EGF-homologous genes in Drosophila. Cell"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C25",
      "doi-asserted-by": "publisher",
      "first-page": "273",
      "DOI": "10.1016/0092-8674(94)90196-1",
      "article-title": "The Suppressor of Hairless protein participates in Notch receptor signalling",
      "volume": "79",
      "author": "Fortini",
      "year": "1994",
      "journal-title": "Cell"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C26",
      "doi-asserted-by": "publisher",
      "first-page": "1673",
      "DOI": "10.1242/dev.122.6.1673",
      "article-title": "Subcellular localization of Suppressor of Hairless in Drosophila sense organ cells during development",
      "volume": "122",
      "author": "Gho",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C27",
      "doi-asserted-by": "publisher",
      "first-page": "95",
      "DOI": "10.1016/S0092-8674(00)81085-5",
      "article-title": "araucan and caupolican, two members of the novel Iroquois complex, encode homeoproteins that control proneural and vein forming genes",
      "volume": "85",
      "author": "G\u00f3mez-Skarmeta",
      "year": "1996",
      "journal-title": "Cell"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C28",
      "doi-asserted-by": "publisher",
      "first-page": "13",
      "DOI": "10.1016/0012-1606(90)90147-B",
      "article-title": "A dual function of the Notch gene in Drosophila sensillum development",
      "volume": "142",
      "author": "Hartenstein",
      "year": "1990",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C29",
      "doi-asserted-by": "publisher",
      "first-page": "161",
      "DOI": "10.1242/dev.122.1.161",
      "article-title": "Genes of the Enhancer of split and achaete-scute complexes are required for a regulatory loop between Notch and Delta during lateral signalling in Drosophila",
      "volume": "122",
      "author": "Heitzler",
      "year": "1996",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C30",
      "doi-asserted-by": "publisher",
      "first-page": "1083",
      "DOI": "10.1016/0092-8674(91)90263-X",
      "article-title": "The choice of cell fate in the epidermis of Drosophila",
      "volume": "64",
      "author": "Heitzler",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C31",
      "doi-asserted-by": "publisher",
      "first-page": "1087",
      "DOI": "10.1242/dev.111.4.1087",
      "article-title": "The emergence of sense organs in the wing disc of Drosophila",
      "volume": "111",
      "author": "Huang",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C32",
      "doi-asserted-by": "publisher",
      "first-page": "355",
      "DOI": "10.1038/377355a0",
      "article-title": "Signalling downstream of activated mammalian Notch",
      "volume": "377",
      "author": "Jarriault",
      "year": "1995",
      "journal-title": "Nature"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C33",
      "doi-asserted-by": "publisher",
      "first-page": "3745",
      "DOI": "10.1242/dev.121.11.3745",
      "article-title": "Role of Notch and achaete-scute complex in the expression of Enhancer of split bHLH proteins",
      "volume": "121",
      "author": "Jennings",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C34",
      "doi-asserted-by": "publisher",
      "first-page": "133",
      "DOI": "10.1038/382133a0",
      "article-title": "Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene",
      "volume": "382",
      "author": "Kim",
      "year": "1996",
      "journal-title": "Nature"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C35",
      "doi-asserted-by": "publisher",
      "first-page": "1683",
      "DOI": "10.1073/pnas.93.4.1683",
      "article-title": "Signal transduction by activated mNotch: Importance of proteolytic processing and its regulation by the extracellular domain",
      "volume": "93",
      "author": "Kopan",
      "year": "1996",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C36",
      "doi-asserted-by": "publisher",
      "first-page": "2598",
      "DOI": "10.1101/gad.9.21.2598",
      "article-title": "The neurogenic Suppressor of Hairless DNA-binding protein mediates transcriptional activation of the Enhancer of split Complex genes triggered by Notch signaling",
      "volume": "9",
      "author": "Lecourtois",
      "year": "1995",
      "journal-title": "Genes Dev"
    },
    {
      "volume-title": "The Genome of Drosophila melanogaster",
      "year": "1992",
      "author": "Lindsley",
      "key": "2025021406033342600_DEVELOP_124_23_4769C37"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C38",
      "doi-asserted-by": "publisher",
      "first-page": "26332644",
      "DOI": "10.1242/dev.121.8.2633",
      "article-title": "Deltex acts as a positive regulator of Notch signaling through interaction with the Notch ankyrin repeats",
      "volume": "121",
      "author": "Matsuno",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C39",
      "first-page": "285",
      "article-title": "Patterning of adult peripheral nervous system of Drosophila",
      "volume": "4",
      "author": "Modolell",
      "year": "1997",
      "journal-title": "Persp. Dev Neurobiol"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C40",
      "doi-asserted-by": "publisher",
      "first-page": "275",
      "DOI": "10.1016/S0896-6273(00)80046-X",
      "article-title": "Persistent expression of genes of the Enhancer of Split complex suppresses neural development in Drosophila",
      "volume": "16",
      "author": "Nakao",
      "year": "1996",
      "journal-title": "Neuron"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C41",
      "doi-asserted-by": "publisher",
      "first-page": "271",
      "DOI": "10.1016/S0092-8674(00)80335-9",
      "article-title": "Kuzbanian controls proteolytic processing of Notch and mediates lateral inhibition during Drosophila and vertebrate neurogenesis",
      "volume": "90",
      "author": "Pan",
      "year": "1997",
      "journal-title": "Cell"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C42",
      "article-title": "Screening of larval/pupal P-element induced lethals of the second chromosome in Drosophila melanogaster: clonal analysis and morphology of imaginal discs",
      "volume-title": "Mol. Gen. Genet. in press",
      "author": "Roch",
      "year": "1997"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C43",
      "first-page": "1227",
      "article-title": "tKUZ, a conserved metalloprotease-disintegrin protein with two roles in Drosophila neurogenesis",
      "volume": "273",
      "author": "Rooke",
      "year": "1996",
      "journal-title": "Sc ience"
    },
    {
      "volume-title": "Molecular Cloning",
      "year": "1989",
      "author": "Sambrook",
      "key": "2025021406033342600_DEVELOP_124_23_4769C44"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C45",
      "doi-asserted-by": "publisher",
      "first-page": "1875",
      "DOI": "10.1242/dev.121.6.1875",
      "article-title": "Suppressor of Hairless is required for signal reception during lateral inhibition in the Drosophila pupal notum",
      "volume": "121",
      "author": "Schweisguth",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C46",
      "doi-asserted-by": "publisher",
      "first-page": "1199",
      "DOI": "10.1016/0092-8674(92)90641-O",
      "article-title": "Suppressor of Hairless, the Drosophila homolog of the mouse recombination signal-binding protein regulates peripheral nervous system development",
      "volume": "69",
      "author": "Schweisguth",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C47",
      "doi-asserted-by": "publisher",
      "first-page": "1433",
      "DOI": "10.1242/dev.120.6.1433",
      "article-title": "Antagonistic activities of Suppressor of Hairless and Hairless control alternative cell fates in the Drosophila adult epidermis",
      "volume": "120",
      "author": "Schweisguth",
      "year": "1994",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C48",
      "doi-asserted-by": "publisher",
      "first-page": "432",
      "DOI": "10.1016/0012-1606(78)90226-9",
      "article-title": "Temperature-sensitive periods and autonomy of pleiotropic effects of 1(1)Nts1, a conditional Notch lethal in Drosophila",
      "volume": "62",
      "author": "Shellenbarger",
      "year": "1978",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C49",
      "doi-asserted-by": "publisher",
      "first-page": "509",
      "DOI": "10.1242/dev.109.3.509",
      "article-title": "Lateral inhibition and the development of the sensory bristles of the adult peripheral nervous system of Drosophila",
      "volume": "109",
      "author": "Simpson",
      "year": "1990",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C50",
      "doi-asserted-by": "publisher",
      "first-page": "984",
      "DOI": "10.1101/gad.5.6.984",
      "article-title": "Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing",
      "volume": "5",
      "author": "Skeath",
      "year": "1991",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C51",
      "doi-asserted-by": "publisher",
      "first-page": "331",
      "DOI": "10.1016/0092-8674(93)90424-O",
      "article-title": "Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo",
      "volume": "74",
      "author": "Struhl",
      "year": "1993",
      "journal-title": "Cell"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C52",
      "doi-asserted-by": "publisher",
      "first-page": "305",
      "DOI": "10.1016/0925-4773(95)00377-0",
      "article-title": "Inhibition of cell fate in Drosophila by Enhancer of split genes",
      "volume": "51",
      "author": "Tata",
      "year": "1995",
      "journal-title": "Mech. Dev"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C53",
      "doi-asserted-by": "publisher",
      "first-page": "749",
      "DOI": "10.1242/dev.111.3.749",
      "article-title": "The Drosophila gene Serrate encodes an EGF-like transmembrane protein with a complex expression pattern in embryos and wing discs",
      "volume": "111",
      "author": "Thomas",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C54",
      "doi-asserted-by": "publisher",
      "first-page": "7180",
      "DOI": "10.1093/genetics/135.1.71",
      "article-title": "P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: isolation of lethals with different overgrowth phenotypes",
      "volume": "135",
      "author": "Torok",
      "year": "1993",
      "journal-title": "Genetics"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C55",
      "doi-asserted-by": "publisher",
      "first-page": "275",
      "DOI": "10.1083/jcb.131.2.275",
      "article-title": "ADAM, a novel family of membrane proteins containing a disintegrin and metalloprotease domain: multipotential functions in cell-cell and cell-matrix interactions",
      "volume": "131",
      "author": "Wolfsberg",
      "year": "1995",
      "journal-title": "J. Cell. Biol"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C56",
      "doi-asserted-by": "publisher",
      "first-page": "1223",
      "DOI": "10.1242/dev.117.4.1223",
      "article-title": "Analysis of genetic mosaics in developing and adult Drosophila tissues",
      "volume": "117",
      "author": "Xu",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "2025021406033342600_DEVELOP_124_23_4769C57",
      "doi-asserted-by": "publisher",
      "first-page": "6414",
      "DOI": "10.1073/pnas.92.14.6414",
      "article-title": "Alterations in Notch signaling in neoplastic lesions of the human cervix",
      "volume": "92",
      "author": "Zagouras",
      "year": "1995",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    }
  ],
  "container-title": "Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/124/23/4769/3128223/develop_124_23_4769.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/124/23/4769/3128223/develop_124_23_4769.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2025,
        2,
        14
      ]
    ],
    "date-time": "2025-02-14T06:04:09Z",
    "timestamp": 1739513049000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/dev/article/124/23/4769/39666/The-metalloprotease-disintegrin-Kuzbanian"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1997,
        12,
        1
      ]
    ]
  },
  "references-count": 57,
  "journal-issue": {
    "issue": "23",
    "published-print": {
      "date-parts": [
        [
          1997,
          12,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/dev.124.23.4769",
  "relation": {},
  "ISSN": [
    "0950-1991",
    "1477-9129"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1997,
        12,
        1
      ]
    ]
  }
}