Advertisement
JOURNAL ARTICLES
The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family
J. Chae, M.J. Kim, J.H. Goo, S. Collier, D. Gubb, J. Charlton, P.N. Adler, W.J. Park
Development 1999 126: 5421-5429;

Summary

The tissue polarity genes control the polarity of hairs, bristles and ommatidia in the adult epidermis of Drosophila. We report here the identification of a new tissue polarity gene named starry night (stan). Mutations in this essential gene alter the polarity of cuticular structures in all regions of the adult body. The detailed polarity phenotype of stan on the wing suggested that it is most likely a component of the frizzled (fz) pathway. Consistent with this hypothesis, stan appears to be downstream of and required for fz function. We molecularly cloned stan and found that it encodes a huge protocadherin containing nine cadherin motifs, four EGF-like motifs, two laminin G motifs, and seven transmembrane domains. This suggests that Stan functions in signal reception, perhaps together with Fz.

Reference

    1. Adler P. N.
    (1992) The genetic control of tissue polarity in Drosophila. BioEssays 14, 735–741
    OpenUrlCrossRefPubMedWeb of Science
    1. Adler P. N.,
    2. Charlton J.,
    3. Liu J.
    (1998) Mutations in the cadherin superfamily member gene dachsous cause a tissue polarity phenotype by altering frizzled signaling. Development 125, 959–968
    OpenUrlAbstract
    1. Adler P. N.,
    2. Charlton J.,
    3. Park W. J.
    (1994) The Drosophila tissue polarity gene inturned function prior to wing hair morphogenesis in the regulation of hair polarity and number. Genetics 137, 829–836
    OpenUrlAbstract/FREE Full Text
    1. Bairoch A.,
    2. Bucher P.,
    3. Hofmann K.
    (1997) The PROSITE database, its status in 1997. Nucl. Acids Res 25, 217–221
    OpenUrlAbstract/FREE Full Text
    1. Bhanot P.,
    2. Brink M.,
    3. Samos C. H.,
    4. Hsieh J. C.,
    5. Wang Y.,
    6. Macke J. P.,
    7. Andrew D.,
    8. Nathans J.,
    9. Nusse R.
    (1996) A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 382, 225–230
    OpenUrlCrossRefPubMedWeb of Science
    1. Brown N. H.,
    2. Kafatos F. C.
    (1988) Functional cDNA libraries from Drosophila embryos. J. Mol. Biol 203, 425–437
    OpenUrlCrossRefPubMedWeb of Science
    1. Clark H. F.,
    2. Brentrup D.,
    3. Schneitz K.,
    4. Bieber A.,
    5. Goodman C.,
    6. Noll M.
    (1995). Dachsous encodes a member of the cadherin superfamily that controls imaginal disc morphogenesis in Drosophila Genes Dev 9, 1530–1542
    OpenUrlAbstract/FREE Full Text
    1. Di Nocera P. P.,
    2. Casari G.
    (1987) Related polypeptides are encoded by Drosophila F elements, I factors, and mammalian L1 sequences. Proc. Natl. Acad. Sci. USA 84, 5843–5847
    OpenUrlAbstract/FREE Full Text
    1. Geiger B.,
    2. Ayalon O.
    (1992) Cadherins. Annu. Rev. Cell Biol 8, 307–332
    OpenUrlCrossRefWeb of Science
    1. Gho M.,
    2. Bellaiche Y.,
    3. Schweisguth F.
    (1999) Revisiting the Drosophila microchaete lineage: a novel intrinsically asymmetric cell division generates a glial cell. Development 126, 3573–3584
    OpenUrlAbstract
    1. Gubb D.
    (1993) Genes controlling cellular polarity in Drosophila. Development 1993, 269–277
    1. Gubb D.,
    2. Green C.,
    3. Huen D.,
    4. Coulson D.,
    5. Johnson G.,
    6. Tree D.,
    7. Collier S.,
    8. Roote J.
    (1999) The balance between isoforms of the Prickle LIM domain protein is critical for planar polarity in Drosophila imaginal discs. Genes Dev 13, 2315–2327
    OpenUrlAbstract/FREE Full Text
    1. Hadjantonakis A. K.,
    2. Formstone C. J.,
    3. Little P. F. R.
    (1998) mCelsr1 is an evolutionarily conserved seven-pass transmembrane receptor and is expressed during mouse embryonic development. Mech. Dev 78, 91–95
    OpenUrlCrossRefPubMedWeb of Science
    1. Hadjantonakis A. K.,
    2. Sheward W. J.,
    3. Harmar A. J.,
    4. de Galan L.,
    5. Hoovers J. M.,
    6. Little P. F.
    (1997) Celsr1, a neural-specific gene encoding an unusual seven-pass transmembrane receptor, maps to mouse chromosome 15 and human chromosome 22qter. Genomics 45, 97–104
    OpenUrlCrossRefPubMedWeb of Science
    1. Hartl D. L.,
    2. Nurminsky D. I.,
    3. Jones R. W.,
    4. Lozovskaya E. R.
    (1994) Genome structure and evolution in Drosophila: applications of the framework P1 map. Proc. Natl. Acad. Sci. USA 91, 6824–6829
    OpenUrlAbstract/FREE Full Text
    1. Johnston P. A.,
    2. Archer B. T.,
    3. Robinson K.,
    4. Mignery G. A.,
    5. Jahn R.,
    6. Sudhof T. C.
    (1991) rab3A attachment to the synaptic vesicle membrane mediated by a conserved polyisoprenylated carboxy-terminal sequence. Neuron 7, 101–109
    OpenUrlCrossRefPubMedWeb of Science
    1. Mahoney P. A.,
    2. Weber U.,
    3. Onofrechuk P.,
    4. Biessmann H.,
    5. Bryant P. J.,
    6. Goodman C. S.
    (1991) The fat tumor suppressor gene in Drosophila encodes a novel member of the cadherin gene superfamily. Cell 67, 853–868
    OpenUrlCrossRefPubMedWeb of Science
    1. Nagafuchi A.,
    2. Takeichi M.
    (1988) Cell binding function of E-cadherin is regulated by the cytoplamic domain. EMBO J 7, 3679–3684
    OpenUrlPubMedWeb of Science
    1. Nakayama M.,
    2. Nakajima D.,
    3. Nagase T.,
    4. Nomura N.,
    5. Seki N.,
    6. Ohara O.
    (1998) Identification of high-molecular-weight proteins with multiple EGF-like motifs by motif-trap screening. Genomics 51, 27–34
    OpenUrlCrossRefPubMedWeb of Science
    1. Nielsen H.,
    2. Engelbrecht J.,
    3. Brunak S.,
    4. von Heijne G.
    (1997) A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int. J. Neural Syst 8, 581–599
    OpenUrlCrossRefPubMed
    1. Park W. J.,
    2. Liu J.,
    3. Sharp E. J.,
    4. Adler P. N.
    (1996) The Drosophila tissue polarity gene inturned acts cell autonomously and encodes a novel protein. Development 122, 961–969
    OpenUrlAbstract
    1. Peifer M.,
    2. Rauskolb C.,
    3. Williams M.,
    4. Riggleman B.,
    5. Wieschaus E.
    (1991) The segment polarity gene armadillo interacts with the wingless signaling pathway in both embryonic and adult pattern formation. Development 111, 1029–1043
    OpenUrlAbstract/FREE Full Text
    1. Reddy G. V.,
    2. Rodrigues V.
    (1999) Sibling cell fate in the Drosophila adult external sense organ lineage is specified by prospero function, which is regulated by Numb and Notch. Development 126, 2083–2092
    OpenUrlAbstract
    1. Reifegerste R.,
    2. Moses K.
    (1999) Genetics of epithelial polarity and pattern in the Drosophila retina. BioEssays 21, 275–285
    OpenUrlCrossRefPubMedWeb of Science
    1. Rost B.,
    2. Casadio R.,
    3. Fariselli P.,
    4. Sander C.
    (1995) Prediction of helical transmembrane segments at 95% accuracy. Protein Science 4, 521–533
    OpenUrlPubMedWeb of Science
    1. Smith R. F.,
    2. Wiese B. A.,
    3. Wojzynski M. K.,
    4. Davison D. B.,
    5. Worley K. C.
    (1996) BCM search launcher—an integrated interface to molecular biology data base search and analysis services available on the world wide web. Genome Res 6, 454–462
    OpenUrlAbstract/FREE Full Text
    1. Tautz D.,
    2. Pfeiffle C.
    (1989) A nonradioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals a translational control of the segmentation gene hunchback. Chromosoma 98, 81–85
    OpenUrlCrossRefPubMedWeb of Science
    1. Taylor J.,
    2. Abramova N.,
    3. Charlton J.,
    4. Adler P. N.
    (1998) Van Gogh: a new Drosophila tissue polarity gene. Genetics 150, 199–210
    OpenUrlAbstract/FREE Full Text
    1. Tepass U.,
    2. Gruszynski-Defeo E.,
    3. Haag T. A.,
    4. Omatyar L.,
    5. Torok T.,
    6. Hartenstein V.
    (1996) shotgun encodes Drosophila E-Cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev 10, 672–685
    OpenUrlAbstract/FREE Full Text
    1. Theisen H.,
    2. Purcell J.,
    3. Bennett M.,
    4. Kansagara D.,
    5. Sved A.,
    6. Marsh J. L.
    (1994) dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development 120, 347–360
    OpenUrlAbstract
    1. Uemura T.,
    2. Oda H.,
    3. Kraut R.,
    4. Hayashi S.,
    5. Kotaoka Y.,
    6. Takeichi M.
    (1996) Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev 10, 659–671
    OpenUrlAbstract/FREE Full Text
    1. Usui T.,
    2. Shima Y.,
    3. Shimada Y.,
    4. Hirono S.,
    5. Burgess R. W.,
    6. Schwarz T. L.,
    7. Takeichi M.,
    8. Uemura T.
    (1999) Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98, 585–595
    OpenUrlCrossRefPubMedWeb of Science
    1. Wherli M.,
    2. Tomlinson A.
    (1998) Independent regulation of anterior/posterior and equatorial/polar polarity in the Drosophila eye. Development 125, 1421–1432
    OpenUrlAbstract
    1. Wolff T.,
    2. Rubin G. M.
    (1998) s trabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 125, 1149–1159
    OpenUrlAbstract
    1. Wong L. L.,
    2. Adler P. N.
    (1993) Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells. J. Cell Biol 123, 209–221
    OpenUrlAbstract/FREE Full Text
    1. Xu T.,
    2. Rubin G. M.
    (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223–1237
    OpenUrlAbstract
Back to top

 Download PDF

Email
JOURNAL ARTICLES
The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family
J. Chae, M.J. Kim, J.H. Goo, S. Collier, D. Gubb, J. Charlton, P.N. Adler, W.J. Park
Development 1999 126: 5421-5429;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

The Node is looking for a new Community Manager!

If you're interested in science communication, publishing and the developmental biology community, we're hiring for a new Community Manager for our community site, the Node.

The position is an exciting opportunity to develop an already successful and well-known site, engaging with the academic, publishing and online communities. Find out more and how to apply.

Upcoming special issue: call for papers

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

The special issue welcomes Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

The people behind the papers - Clément Dubois, Shivam Gupta, Andrew Mugler and Marie-Anne Félix

A new paper investigates the robustness of neuroblast migration in the C. elegans larva in the face of both genetic and environmental variation. In an interview, the paper's four authors tell us more about the story.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Every talk is recorded and since launching in August last year, the series has clocked up almost 10k views on YouTube.

Here, Swann Floc'hlay discusses her work modelling dorsal-ventral axis specification in the sea urchin embryo.

Save your spot at our next session:

14 April
Time: 17:00 BST
Chaired by: François Guillemot

12 May
Time: TBC
Chaired by: Paola Arlotta

Join our mailing list to receive news and updates on the series.