Temporal and Spatial Expression of Homeotic Genes Is Important for Segment-specific Neuroblast 6-4 Lineage Formation in Drosophila

  • Kang, Sun-Young (Department of Biology Education, Seoul National University) ;
  • Kim, Su-Na (Department of Biology Education, Seoul National University) ;
  • Kim, Sang Hee (Department of Chemistry, Konkuk University) ;
  • Jeon, Sang-Hak (Department of Biology Education, Seoul National University)
  • Received : 2006.05.12
  • Accepted : 2006.06.19
  • Published : 2006.06.30

Abstract

Different proliferation of neuroblast 6-4 (NB6-4) in the thorax and abdomen produces segmental specific expression pattern of several neuroblast marker genes. NB6-4 is divided to form four medialmost cell body glia (MM-CBG) per segment in thorax and two MM-CBG per segment in abdomen. As homeotic genes determine the identities of embryonic segments along the A/P axis, we investigated if temporal and specific expression of homeotic genes affects MM-CBG patterns in thorax and abdomen. A Ubx loss-of-function mutation was found to hardly affect MM-CBG formation, whereas abd-A and Abd-B caused the transformation of abdominal MM-CBG to their thoracic counterparts. On the other hand, gain-of-function mutants of Ubx, abd-A and Abd-B genes reduced the number of thoracic MM-CBG, indicating that thoracic MM-CBG resembled abdominal MM-CBG. However, mutations in Polycomb group (PcG) genes, which are negative transregulators of homeotic genes, did not cause the thoracic to abdominal MM-CBG pattern transformation although the number of MM-CBG in a few percent of embryos were partially reduced or abnormally patterned. Our results indicate that temporal and spatial expression of the homeotic genes is important to determine segmental-specificity of NB6-4 daughter cells along the anterior-posterior (A/P) axis.

Keywords

abd-A;Abd-B;MM-CBG;Neuroblast;PcG Genes;Ubx;*

Acknowledgement

Supported by : Korean Science and Engineering Foundation (KOSEF)

References

  1. Carroll, S. B., Laymon, R. A., McCutcheon, M. A., Riley, P. D., and Scott, M. P. (1986) The localization and regulation of Antennapedia protein expression in Drosophila embryos. Cell 47, 113-122 https://doi.org/10.1016/0092-8674(86)90372-7
  2. Casanova, J., Sanchez-Herrero, E., Busturia, A., and Morata, G. (1987) Double and triple mutant combinations of bithorax complex of Drosophila. EMBO J. 6, 3103-3109
  3. Irish, V. F., Martinez-Arias, A., and Akam, M. (1989) Spatial regulation of the antennapedia and ultrabithorax homeotic genes during Drosophila early development. EMBO J. 8, 1527-1537
  4. Jurgens, G. (1985) A group of genes controlling the spatial expression of the bithorax complex in Drosophila. Nature 316, 153-155 https://doi.org/10.1038/316153a0
  5. Lewis, E. B. (1978) A gene complex controlling segmentation in Drosophila. Nature 276, 565-570 https://doi.org/10.1038/276565a0
  6. Simon, J., Chiang, A., and Bender, W. (1992) Ten different Polycomb group genes are required for spatial control of the abdA and AbdB homeotic products. Development 114, 493-505
  7. Struhl, G. (1981) A gene product required for correct initiation of segmental determination in Drosophila. Nature 293, 36-41 https://doi.org/10.1038/293036a0
  8. Breen, T. R. (1999) Mutant alleles of the Drosophila trithorax gene produce common and unusual homeotic and other developmental phenotypes. Genetics 152, 319-344
  9. Graba, Y., Aragnol, D., Laurenti, P., Garzino, V., Charmot, D., et al. (1992) Homeotic control in Drosophila; the scabrous gene is an in vivo target of ultrabithorax proteins. EMBO J. 11, 3375-3384
  10. Karch, F., Bender, W., and Weiffenbach, B. (1990) abdA expression in Drosophila embryos. Genes Dev. 4, 1573-1587 https://doi.org/10.1101/gad.4.9.1573
  11. Struhl, G. and White, R. A. (1985) Regulation of the Ultrabithorax gene of Drosophila by other bithorax complex genes. Cell 43, 507-519 https://doi.org/10.1016/0092-8674(85)90180-1
  12. Tautz, D. and Pfeifle, C. (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals transcriptional control of the segmentation gene hunchback. Chromosoma 98, 81-85 https://doi.org/10.1007/BF00291041
  13. Jacobs, J. J. and van Lohuizen, M. (2002) Polycomb repression: from cellular memory to cellular proliferation and cancer. Biochim. Biophys. Acta 1602, 151-161
  14. Beachy, P. A., Helfand, S. L., and Hogness, D. S. (1985) Segmental distribution of bithorax complex proteins during Drosophila development. Nature 313, 545-551 https://doi.org/10.1038/313545a0
  15. Jones, B. W., Abeysekera, M., Galinska, J., and Jolicoeur, E. M. (2004) Transcriptional control of glial and blood cell development in Drosophila: cis-regulatory elements of glial cells missing. Dev. Biol. 266, 374-387 https://doi.org/10.1016/j.ydbio.2003.10.013
  16. Higashijima, S., Shishido, E., Matsuzaki, M., and Saigo, K. (1996) eagle, a member of the steroid receptor gene superfamily, is expressed in a subset of neuroblasts and regulates the fate of their putative progeny in the Drosophila CNS. Development 122, 527-536
  17. Hosoya, T., Takizawa, K., Nitta, K., and Hotta, Y. (1995) glial cells missing: a binary switch between neuronal and glial determination in Drosophila. Cell 82, 1025-1036 https://doi.org/10.1016/0092-8674(95)90281-3
  18. Berger, C., Pallavi, S. K., Prasad, M., Shashidhara, L. S., and Technau, G. M. (2005) A critical role for cyclin E in cell fate determination in the central nervous system of Drosophila melanogaster. Nat. Cell Biol. 7, 56-62 https://doi.org/10.1038/ncb1203
  19. Halter, D. A., Urban, J., Rickert, C., Ner, S. S., Ito, K., et al. (1995) The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121, 317-332
  20. Orlando, V. and Paro, R. (1995) Chromatin multiprotein complexes involved in the maintenance of transcription patterns. Curr. Opin. Genet. Dev. 5, 174-179 https://doi.org/10.1016/0959-437X(95)80005-0
  21. Ingham, P. W. (1985) A clonal analysis of the requirement for the trithorax gene in the diversification of segments in Drosophila. J. Embryol. Exp. Morphol. 89, 349-365
  22. Xiong, W. C., Okano, H., Patel, N. H., Blendy, J. A., and Montell, C. (1994) repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev. 8, 981-994 https://doi.org/10.1101/gad.8.8.981
  23. Akiyama-Oda, Y., Hosoya, T., and Hotta, Y. (1999) Asymmetric cell division of thoracic neuroblast 6-4 to bifurcate glial and neuronal lineage in Drosophila. Development 126, 1967-1974
  24. Ito, K., Urban, J., and Technau, G. M. (1995) Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux's Arch. Dev. Biol. 204, 284-307 https://doi.org/10.1007/BF02179499
  25. Jones, B. W. (2001) Glial cell development in the Drosophila embryo. Bioessays 23, 877-887 https://doi.org/10.1002/bies.1129
  26. Lamka, M. L., Boulet, A. M., and Sakonju, S. (2002) Ectopic expression of Ubx and ABd-B proteins during Drosophila embryogenesis: competition, not a functinal hierachy, explains phenotypic suppression. Development 116, 841-854
  27. McKeon, J. and Brock, H. W. (1991) Interactions of the Polycomb group of genes with homeotic loci of Drosophila. Roux's Arch. Dev. Biol. 199, 387-396 https://doi.org/10.1007/BF01705848
  28. Doe, C. Q. (1992) Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116, 855-863
  29. Klambt, C. (1993) The Drosophila gene pointed encodes two ETS-like proteins which are involved in the development of the midline glial cells. Development 117, 163-176
  30. Sedkov, Y., Tillib, S., Mizrokhi, L., and Mazo, A. (1994) The bithorax complex is regulated by trithorax earlier during Drosophila embryogenesis than is the Antennapedia complex, correlating with a bithorax-like expression pattern of distinct early trithorax transcripts. Development 120, 1907-1917
  31. Celniker, S. E., Keelan, D. J., and Lewis, E. B. (1989) The molecular genetics of the bithorax complex of Drosophila: characterization of the products of the abdominal-B domain. Genes Dev. 3, 1424-1436
  32. Choi, S. H., Oh, C. T., Kim, S. H., Kim, Y. T., and Jeon, S. H. (2000) Effects of Polycomb group mutations on the expression of Ultrabithorax in the Drosophila visceral mesoderm. Mol. Cells 10, 156-161
  33. Egger, B., Leemans, R., Loop, T., Kammermeier, L., Fan Y., et al. (2002) Gliogenesis in Drosophila: genome-wide analysis of downstream genes of glial cells missing in the embryonic nervous system. Development 129, 3295-3309
  34. Mahmoudi, T. and Verrijzer, C. P. (2001) Chromatin silencing and activation by polycomb and trithorax group proteins. Oncogene 20, 3055-3066 https://doi.org/10.1038/sj.onc.1204330
  35. Lemke, G. (2001) Glial control of neuronal development. Annu. Rev. Neurosci. 24, 87-105 https://doi.org/10.1146/annurev.neuro.24.1.87
  36. Duncan, I. (1987) The bithorax complex. Annu. Rev. Genet. 21, 285-319 https://doi.org/10.1146/annurev.ge.21.120187.001441
  37. Girton, J. R. and Jeon, S. H. (1994) Novel embryonic and adult homeotic phenotypes are produced by pleiohomeotic mutations in Drosophila. Dev. Biol. 161, 393-407 https://doi.org/10.1006/dbio.1994.1040
  38. Kaufman, T. C., Seeger, M. A., and Olsen, G. (1990) Molecular and genetic organization of the antennapedia gene complex of Drosophila melanogaster. Adv. Genet. 27, 309-362 https://doi.org/10.1016/S0065-2660(08)60029-2