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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Mar 29;91(7):2664–2668. doi: 10.1073/pnas.91.7.2664

Chromophore-assisted laser inactivation of patched protein switches cell fate in the larval visual system of Drosophila.

D Schmucker 1, A L Su 1, A Beermann 1, H Jäckle 1, D G Jay 1
PMCID: PMC43430  PMID: 8146172

Abstract

The Drosophila segment-polarity gene patched (ptc) is an integral component of the segmentation gene cascade acting in the early embryo. At later stages of embryogenesis, ptc is expressed in the primordia of epithelial placodes of a specific portion of the brain, the optic lobes. Mutant analysis shows that the lack of ptc activity alters the fate of optic-lobe primordia precursors. In ptc mutants they give rise to supernumerary neurons in the larval light-sensory system, termed Bolwig organ, which is derived from precursor cells next to the optic-lobe anlagen. We specifically eliminated ptc protein by chromophore-assisted laser inactivation (CALI) in late wild-type embryos. Such embryos show a normal segment pattern, but they develop phenocopies equivalent to the phenotype of ptc mutant Bolwig organs. Our results demonstrate that the CALI technique can be applied to separate genetic functions at different developmental stages of a living organism and that the segment-polarity gene ptc is redeployed to functionally discriminate between distinct developmental pathways in adjacent pools of precursor cells.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Artavanis-Tsakonas S. The molecular biology of the Notch locus and the fine tuning of differentiation in Drosophila. Trends Genet. 1988 Apr;4(4):95–100. doi: 10.1016/0168-9525(88)90096-0. [DOI] [PubMed] [Google Scholar]
  2. Doe C. Q., Hiromi Y., Gehring W. J., Goodman C. S. Expression and function of the segmentation gene fushi tarazu during Drosophila neurogenesis. Science. 1988 Jan 8;239(4836):170–175. doi: 10.1126/science.2892267. [DOI] [PubMed] [Google Scholar]
  3. Doe C. Q., Scott M. P. Segmentation and homeotic gene function in the developing nervous system of Drosophila. Trends Neurosci. 1988 Mar;11(3):101–106. doi: 10.1016/0166-2236(88)90154-3. [DOI] [PubMed] [Google Scholar]
  4. Doe C. Q., Smouse D., Goodman C. S. Control of neuronal fate by the Drosophila segmentation gene even-skipped. Nature. 1988 May 26;333(6171):376–378. doi: 10.1038/333376a0. [DOI] [PubMed] [Google Scholar]
  5. Duffy J. B., Kania M. A., Gergen J. P. Expression and function of the Drosophila gene runt in early stages of neural development. Development. 1991 Dec;113(4):1223–1230. doi: 10.1242/dev.113.4.1223. [DOI] [PubMed] [Google Scholar]
  6. Fujita S. C., Zipursky S. L., Benzer S., Ferrús A., Shotwell S. L. Monoclonal antibodies against the Drosophila nervous system. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7929–7933. doi: 10.1073/pnas.79.24.7929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gaul U., Seifert E., Schuh R., Jäckle H. Analysis of Krüppel protein distribution during early Drosophila development reveals posttranscriptional regulation. Cell. 1987 Aug 14;50(4):639–647. doi: 10.1016/0092-8674(87)90037-7. [DOI] [PubMed] [Google Scholar]
  8. Green P., Hartenstein A. Y., Hartenstein V. The embryonic development of the Drosophila visual system. Cell Tissue Res. 1993 Sep;273(3):583–598. doi: 10.1007/BF00333712. [DOI] [PubMed] [Google Scholar]
  9. Gutjahr T., Patel N. H., Li X., Goodman C. S., Noll M. Analysis of the gooseberry locus in Drosophila embryos: gooseberry determines the cuticular pattern and activates gooseberry neuro. Development. 1993 May;118(1):21–31. doi: 10.1242/dev.118.1.21. [DOI] [PubMed] [Google Scholar]
  10. Heilig J. S., Freeman M., Laverty T., Lee K. J., Campos A. R., Rubin G. M., Steller H. Isolation and characterization of the disconnected gene of Drosophila melanogaster. EMBO J. 1991 Apr;10(4):809–815. doi: 10.1002/j.1460-2075.1991.tb08013.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Heitzler P., Simpson P. The choice of cell fate in the epidermis of Drosophila. Cell. 1991 Mar 22;64(6):1083–1092. doi: 10.1016/0092-8674(91)90263-x. [DOI] [PubMed] [Google Scholar]
  12. Hooper J. E., Scott M. P. The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell. 1989 Nov 17;59(4):751–765. doi: 10.1016/0092-8674(89)90021-4. [DOI] [PubMed] [Google Scholar]
  13. Ingham P. W., Taylor A. M., Nakano Y. Role of the Drosophila patched gene in positional signalling. Nature. 1991 Sep 12;353(6340):184–187. doi: 10.1038/353184a0. [DOI] [PubMed] [Google Scholar]
  14. Ingham P. W. The molecular genetics of embryonic pattern formation in Drosophila. Nature. 1988 Sep 1;335(6185):25–34. doi: 10.1038/335025a0. [DOI] [PubMed] [Google Scholar]
  15. Jay D. G., Keshishian H. Laser inactivation of fasciclin I disrupts axon adhesion of grasshopper pioneer neurons. Nature. 1990 Dec 6;348(6301):548–550. doi: 10.1038/348548a0. [DOI] [PubMed] [Google Scholar]
  16. Jay D. G. Selective destruction of protein function by chromophore-assisted laser inactivation. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5454–5458. doi: 10.1073/pnas.85.15.5454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Macdonald P. M., Struhl G. A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature. 1986 Dec 11;324(6097):537–545. doi: 10.1038/324537a0. [DOI] [PubMed] [Google Scholar]
  18. Martizez Arias A., Baker N. E., Ingham P. W. Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. Development. 1988 May;103(1):157–170. doi: 10.1242/dev.103.1.157. [DOI] [PubMed] [Google Scholar]
  19. Moses K., Rubin G. M. Glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes Dev. 1991 Apr;5(4):583–593. doi: 10.1101/gad.5.4.583. [DOI] [PubMed] [Google Scholar]
  20. Nakano Y., Guerrero I., Hidalgo A., Taylor A., Whittle J. R., Ingham P. W. A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched. Nature. 1989 Oct 12;341(6242):508–513. doi: 10.1038/341508a0. [DOI] [PubMed] [Google Scholar]
  21. Patel N. H., Schafer B., Goodman C. S., Holmgren R. The role of segment polarity genes during Drosophila neurogenesis. Genes Dev. 1989 Jun;3(6):890–904. doi: 10.1101/gad.3.6.890. [DOI] [PubMed] [Google Scholar]
  22. Schmidt-Ott U., Technau G. M. Expression of en and wg in the embryonic head and brain of Drosophila indicates a refolded band of seven segment remnants. Development. 1992 Sep;116(1):111–125. doi: 10.1242/dev.116.1.111. [DOI] [PubMed] [Google Scholar]
  23. Schmucker D., Taubert H., Jäckle H. Formation of the Drosophila larval photoreceptor organ and its neuronal differentiation require continuous Krüppel gene activity. Neuron. 1992 Dec;9(6):1025–1039. doi: 10.1016/0896-6273(92)90063-j. [DOI] [PubMed] [Google Scholar]
  24. St Johnston D., Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell. 1992 Jan 24;68(2):201–219. doi: 10.1016/0092-8674(92)90466-p. [DOI] [PubMed] [Google Scholar]
  25. Stein D., Roth S., Vogelsang E., Nüsslein-Volhard C. The polarity of the dorsoventral axis in the Drosophila embryo is defined by an extracellular signal. Cell. 1991 May 31;65(5):725–735. doi: 10.1016/0092-8674(91)90381-8. [DOI] [PubMed] [Google Scholar]
  26. Steller H., Fischbach K. F., Rubin G. M. Disconnected: a locus required for neuronal pathway formation in the visual system of Drosophila. Cell. 1987 Sep 25;50(7):1139–1153. doi: 10.1016/0092-8674(87)90180-2. [DOI] [PubMed] [Google Scholar]
  27. Taylor A. M., Nakano Y., Mohler J., Ingham P. W. Contrasting distributions of patched and hedgehog proteins in the Drosophila embryo. Mech Dev. 1993 Jul;42(1-2):89–96. doi: 10.1016/0925-4773(93)90101-3. [DOI] [PubMed] [Google Scholar]
  28. Tix S., Minden J. S., Technau G. M. Pre-existing neuronal pathways in the developing optic lobes of Drosophila. Development. 1989 Apr;105(4):739–746. doi: 10.1242/dev.105.4.739. [DOI] [PubMed] [Google Scholar]
  29. Van Vactor D., Jr, Krantz D. E., Reinke R., Zipursky S. L. Analysis of mutants in chaoptin, a photoreceptor cell-specific glycoprotein in Drosophila, reveals its role in cellular morphogenesis. Cell. 1988 Jan 29;52(2):281–290. doi: 10.1016/0092-8674(88)90517-x. [DOI] [PubMed] [Google Scholar]
  30. Weigel D., Seifert E., Reuter D., Jäckle H. Regulatory elements controlling expression of the Drosophila homeotic gene fork head. EMBO J. 1990 Apr;9(4):1199–1207. doi: 10.1002/j.1460-2075.1990.tb08227.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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