Neuroblast pattern and identity in the Drosophila tail region and role of doublesex in the survival of sex-specific precursors

Development (Cambridge)

Volumn 140, Issue 8, 2013, Pages 1830-1842

  Birkholz, Oliver ^a   Rickert, Christof ^a   Berger, Christian ^a   Urbach, Rolf ^a   Technau, Gerhard M ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

CNS development; Doublesex; Drosophila; Neuroblasts; Programmed cell death; Segmental patterning; Sex specific precursors and lineages

Indexed keywords

DOUBLESEX PROTEIN; DROSOPHILA PROTEIN; UNCLASSIFIED DRUG;

ABDOMEN; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL COMPARTMENTALIZATION; CELL COUNT; CELL FUNCTION; CELL LINEAGE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION; GENE PRODUCT; MARKER GENE; NEUROBLAST; NEUROMERE; NONHUMAN; PRIORITY JOURNAL; SEX DETERMINATION; THORAX;

ABDOMEN; ANIMALS; APOPTOSIS; BODY PATTERNING; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, CONFOCAL; NEURAL STEM CELLS; SEX CHARACTERISTICS;

EID: 84875436620     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.090043     Document Type: Article

References (97)

1. Baines, R. A., Robinson, S. G., Fujioka, M., Jaynes, J. B. and Bate, M. (1999). Postsynaptic expression of tetanus toxin light chain blocks synaptogenesis in Drosophila. Curr. Biol. 9, 1267-1270.
2. Baumgardt, M., Karlsson, D., Terriente, J., Díaz-Benjumea, F. J. and Thor, S. (2009). Neuronal subtype specification within a lineage by opposing temporal feed-forward loops. Cell 139, 969-982.
3. Baumgartner, S., Bopp, D., Burri, M. and Noll, M. (1987). Structure of two genes at the gooseberry locus related to the paired gene and their spatial expression during Drosophila embryogenesis. Genes Dev. 1, 1247-1267.
4. Bello, B., Holbro, N. and Reichert, H. (2007). Polycomb group genes are required for neural stem cell survival in postembryonic neurogenesis of Drosophila. Development 134, 1091-1099.
5. Betschinger, J., Mechtler, K. and Knoblich, J. A. (2006). Asymmetric segregation of the tumor suppressor brat regulates self-renewal in Drosophila neural stem cells. Cell 124, 1241-1253.
6. Bhat, K. M. (1996). The patched signaling pathway mediates repression of gooseberry allowing neuroblast specification by wingless during Drosophila neurogenesis. Development 122, 2921-2932.
7. Bhat, K. M. (1999). Segment polarity genes in neuroblast formation and identity specification during Drosophila neurogenesis. BioEssays 21, 472-485.
8. Bier, E., Vaessin, H., Younger-Shepherd, S., Jan, L. Y. and Jan, Y. N. (1992). deadpan, an essential pan-neural gene in Drosophila, encodes a helix-loop-helix protein similar to the hairy gene product. Genes Dev. 6, 2137-2151.
9. Billeter, J. C., Villella, A., Allendorfer, J. B., Dornan, A. J., Richardson, M., Gailey, D. A. and Goodwin, S. F. (2006). Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene. Curr. Biol. 16, 1063-1076.
10. Boll, W. and Noll, M. (2002). The Drosophila Pox neuro gene: control of male courtship behavior and fertility as revealed by a complete dissection of all enhancers. Development 129, 5667-5681.
11. Bopp, D., Bell, L. R., Cline, T. W. and Schedl, P. (1991). Developmental distribution of female-specific Sex-lethal proteins in Drosophila melanogaster. Genes Dev. 5, 403-415.
12. Bossing, T., Udolph, G., Doe, C. Q. and Technau, G. M. (1996). The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev. Biol. 179, 41-64.
13. Broadus, J., Skeath, J. B., Spana, E. P., Bossing, T., Technau, G. and Doe, C. Q. (1995). New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system. Mech. Dev. 53, 393-402.
14. Buenzow, D. E. and Holmgren, R. (1995). Expression of the Drosophila gooseberry locus defines a subset of neuroblast lineages in the central nervous system. Dev. Biol. 170, 338-349.
15. Campos-Ortega, J. A. and Hartenstein, V. (1997). The Embryonic Development of Drosophila melanogaster. Berlin, Heidelberg, New York, NY: Springer Verlag.
16. 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.
17. Christiansen, A. E., Keisman, E. L., Ahmad, S. M. and Baker, B. S. (2002). Sex comes in from the cold: the integration of sex and pattern. Trends Genet. 18, 510-516.
18. Chu, H., Parras, C., White, K. and Jiménez, F. (1998). Formation and specification of ventral neuroblasts is controlled by vnd in Drosophila neurogenesis. Genes Dev. 12, 3613-3624.
19. Colomb, S., Joly, W., Bonneaud, N. and Maschat, F. (2008). A concerted action of Engrailed and Gooseberry-Neuro in neuroblast 6-4 is triggering the formation of embryonic posterior commissure bundles. PLoS ONE 3, e2197.
20. DeFalco, T. J., Verney, G., Jenkins, A. B., McCaffery, J. M., Russell, S. and Van Doren, M. (2003). Sex-specific apoptosis regulates sexual dimorphism in the Drosophila embryonic gonad. Dev. Cell 5, 205-216.
21. De Graeve, F., Jagla, T., Daponte, J. P., Rickert, C., Dastugue, B., Urban, J. and Jagla, K. (2004). The ladybird homeobox genes are essential for the specification of a subpopulation of neural cells. Dev. Biol. 270, 122-134.
22. DiNardo, S., Kuner, J. M., Theis, J. and O'Farrell, P. H. (1985). Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein. Cell 43, 59-69.
23. Dittrich, R., Bossing, T., Gould, A. P., Technau, G. M. and Urban, J. (1997). The differentiation of the serotonergic neurons in the Drosophila ventral nerve cord depends on the combined function of the zinc finger proteins Eagle and Huckebein. Development 124, 2515-2525.
24. Doe, C. Q. (1992). Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116, 855-863.
25. Dormand, E. L. and Brand, A. H. (1998). Runt determines cell fates in the Drosophila embryonic CNS. Development 125, 1659-1667.
26. Evans, C. J., Olson, J. M., Ngo, K. T., Kim, E., Lee, N. E., Kuoy, E., Patananan, A. N., Sitz, D., Tran, P., Do, M. T. et al. (2009). G-TRACE: rapid Gal4-based cell lineage analysis in Drosophila. Nat. Methods 6, 603-605.
27. Frasch, M., Hoey, T., Rushlow, C., Doyle, H. and Levine, M. (1987). Characterization and localization of the even-skipped protein of Drosophila. EMBO J. 6, 749-759.
28. Fujioka, M., Lear, B. C., Landgraf, M., Yusibova, G. L., Zhou, J., Riley, K. M., Patel, N. H. and Jaynes, J. B. (2003). Even-skipped, acting as a repressor, regulates axonal projections in Drosophila. Development 130, 5385-5400.
29. Gorfinkiel, N., Sánchez, L. and Guerrero, I. (1999). Drosophila terminalia as an appendage-like structure. Mech. Dev. 86, 113-123.
30. Gutjahr, T., Patel, N. H., Li, X., Goodman, C. S. and Noll, M. (1993). Analysis of the gooseberry locus in Drosophila embryos: gooseberry determines the cuticular pattern and activates gooseberry neuro. Development 118, 21-31.
31. Hadjieconomou, D., Rotkopf, S., Alexandre, C., Bell, D. M., Dickson, B. J. and Salecker, I. (2011). Flybow: genetic multicolor cell labeling for neural circuit analysis in Drosophila melanogaster. Nat. Methods 8, 260-266.
32. Hartenstein, V. and Campos-Ortega, J. A. (1984). Early neurogenesis in wild-type Drosophila melanogaster. Roux's Arch. Dev. Biol. 193, 308-325.
33. Hartmann, B., Hirth, F., Walldorf, U. and Reichert, H. (2000). Expression, regulation and function of the homeobox gene empty spiracles in brain and ventral nerve cord development of Drosophila. Mech. Dev. 90, 143-153.
34. Häsemeyer, M., Yapici, N., Heberlein, U. and Dickson, B. J. (2009). Sensory neurons in the Drosophila genital tract regulate female reproductive behavior. Neuron 61, 511-518.
35. Hay, B. A., Wolff, T. and Rubin, G. M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 120, 2121-2129.
36. 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.
37. Hoshijima, K., Inoue, K., Higuchi, I., Sakamoto, H. and Shimura, Y. (1991). Control of doublesex alternative splicing by transformer and transformer-2 in Drosophila. Science 252, 833-836.
38. Ikeshima-Kataoka, H., Skeath, J. B., Nabeshima, Y., Doe, C. Q. and Matsuzaki, F. (1997). Miranda directs Prospero to a daughter cell during Drosophila asymmetric divisions. Nature 390, 625-629.
39. Isshiki, T., Takeichi, M. and Nose, A. (1997). The role of the msh homeobox gene during Drosophila neurogenesis: implication for the dorsoventral specification of the neuroectoderm. Development 124, 3099-3109.
40. 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.
41. Jagla, K., Jagla, T., Heitzler, P., Dretzen, G., Bellard, F. and Bellard, M. (1997). ladybird, a tandem of homeobox genes that maintain late wingless expression in terminal and dorsal epidermis of the Drosophila embryo. Development 124, 91-100.
42. Juergens, G. (1987). Segmental organisation of the tail region in the embryo of Drosophila melanogaster. Roux's Arch. Dev. Biol. 196, 141-157.
43. Kambadur, R., Koizumi, K., Stivers, C., Nagle, J., Poole, S. J. and Odenwald, W. F. (1998). Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes Dev. 12, 246-260.
44. Kammermeier, L., Leemans, R., Hirth, F., Flister, S., Wenger, U., Walldorf, U., Gehring, W. J. and Reichert, H. (2001). Differential expression and function of the Drosophila Pax6 genes eyeless and twin of eyeless in embryonic central nervous system development. Mech. Dev. 103, 71-78.
45. Kimura, K., Hachiya, T., Koganezawa, M., Tazawa, T. and Yamamoto, D. (2008). Fruitless and doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 59, 759-769.
46. Kohatsu, S., Koganezawa, M. and Yamamoto, D. (2011). Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 69, 498-508.
47. Kosman, D., Small, S. and Reinitz, J. (1998). Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev. Genes Evol. 208, 290-294.
48. Kuhn, D. T., Sawyer, M., Packert, G., Turenchalk, G., Mack, J. A., Sprey, T. E., Gustavson, E. and Kornberg, T. B. (1992). Development of the D. melanogaster caudal segments involves suppression of the ventral regions of A8, A9 and A10. Development 116, 11-20.
49. Lacin, H., Zhu, Y., Wilson, B. A. and Skeath, J. B. (2009). DBX mediates neuronal specification and differentiation through cross-repressive, lineage-specific interactions with eve and hb9. Development 136, 3257-3266.
50. Landgraf, M., Jeffrey, V., Fujioka, M., Jaynes, J. B. and Bate, M. (2003a). Embryonic origins of a motor system: motor dendrites form a myotopic map in Drosophila. PLoS Biol. 1, e41.
51. Landgraf, M., Sánchez-Soriano, N., Technau, G. M., Urban, J. and Prokop, A. (2003b). Charting the Drosophila neuropile: a strategy for the standardized characterisation of genetically amenable neurites. Dev. Biol. 260, 207-225.
52. Lee, G., Hall, J. C. and Park, J. H. (2002). Doublesex gene expression in the central nervous system of Drosophila melanogaster. J. Neurogenet. 16, 229-248.
53. Lewis, E. B. (1978). A gene complex controlling segmentation in Drosophila. Nature 276, 565-570.
54. Luo, S. D., Shi, G. W. and Baker, B. S. (2011). Direct targets of the D. melanogaster DSXF protein and the evolution of sexual development. Development 138, 2761-2771.
55. McDonald, J. A., Holbrook, S., Isshiki, T., Weiss, J., Doe, C. Q. and Mellerick, D. M. (1998). Dorsoventral patterning in the Drosophila central nervous system: the vnd homeobox gene specifies ventral column identity. Genes Dev. 12, 3603-3612.
56. Mettler, U., Vogler, G. and Urban, J. (2006). Timing of identity: spatiotemporal regulation of hunchback in neuroblast lineages of Drosophila by Seven-up and Prospero. Development 133, 429-437.
57. Monastirioti, M. (2003). Distinct octopamine cell population residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogaster. Dev. Biol. 264, 38-49.
58. Ni, J. Q., Liu, L. P., Binari, R., Hardy, R., Shim, H. S., Cavallaro, A., Booker, M., Pfeiffer, B. D., Markstein, M., Wang, H. et al. (2009). A Drosophila resource of transgenic RNAi lines for neurogenetics. Genetics 182, 1089-1100.
59. Noordermeer, J. N., Kopczynski, C. C., Fetter, R. D., Bland, K. S., Chen, W. Y. and Goodman, C. S. (1998). Wrapper, a novel member of the Ig superfamily, is expressed by midline glia and is required for them to ensheath commissural axons in Drosophila. Neuron 21, 991-1001.
60. Patel, N. H. (1994). Imaging neuronal subsets and other cell types in whole mount Drosophila embryos and larvae using antibody probes. In Methods in Cell Biology. Drosophila melanogaster: Practical Uses in Cell Biology, Vol. 44 (ed. L. S. Goldstein and E. Fyrberg), pp. 445-487. New York, NY: Academic Press.
61. Patel, N. H., Martin-Blanco, E., Coleman, K. G., Poole, S. J., Ellis, M. C., Kornberg, T. B. and Goodman, C. S. (1989). Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58, 955-968.
62. Plickert, G., Gajewski, M., Gehrke, G., Gausepohl, H., Schlossherr, J. and Ibrahim, H. (1997). Automated in situ detection (AISD) of biomolecules. Dev. Genes Evol. 207, 362-367.
63. Prokop, A. and Technau, G. M. (1991). The origin of postembryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster. Development 111, 79-88.
64. Rezával, C., Pavlou, H. J., Dornan, A. J., Chan, Y. B., Kravitz, E. A. and Goodwin, S. F. (2012). Neural circuitry underlying Drosophila female postmating behavioral responses. Curr. Biol. 22, 1155-1165.
65. Rideout, E. J., Billeter, J.-C. and Goodwin, S. F. (2007). The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr. Biol. 17, 1473-1478.
66. Rideout, E. J., Dornan, A. J., Neville, M. C., Eadie, S. and Goodwin, S. F. (2010). Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat. Neurosci. 13, 458-466.
67. Robinett, C. C., Vaughan, A. G., Knapp, J. M. and Baker, B. S. (2010). Sex and the single cell. II. There is a time and place for sex. PLoS Biol. 8, e1000365.
68. Rogulja-Ortmann, A. and Technau, G. M. (2008). Multiple roles for Hox genes in segment-specific shaping of CNS lineages. Fly (Austin) 2, 316-319.
69. Sanders, L. E. and Arbeitman, M. N. (2008). Doublesex establishes sexual dimorphism in the Drosophila central nervous system in an isoform-dependent manner by directing cell number. Dev. Biol. 320, 378-390.
70. Schmid, A., Chiba, A. and Doe, C. Q. (1999). Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126, 4653-4689.
71. Schmidt, H., Rickert, C., Bossing, T., Vef, O., Urban, J. and Technau, G. M. (1997). The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev. Biol. 189, 186-204.
72. Schütt, C. and Nöthiger, R. (2000). Structure, function and evolution of sex-determining systems in Dipteran insects. Development 127, 667-677.
73. Shen, C. P., Jan, L. Y. and Jan, Y. N. (1997). Miranda is required for the asymmetric localization of Prospero during mitosis in Drosophila. Cell 90, 449-458.
74. Skeath, J. B. (1999). At the nexus between pattern formation and cell-type specification: the generation of individual neuroblast fates in the Drosophila embryonic central nervous system. BioEssays 21, 922-931.
75. Skeath, J. B., Zhang, Y., Holmgren, R., Carroll, S. B. and Doe, C. Q. (1995). Specification of neuroblast identity in the Drosophila embryonic central nervous system by gooseberry-distal. Nature 376, 427-430.
76. Steinmann-Zwicky, M., Amrein, H. and Nöthiger, R. (1990). Genetic control of sex determination in Drosophila. Adv. Genet. 27, 189-237.
77. Tautz, D. and Pfeifle, C. (1989). A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81-85.
78. Taylor, B. J. and Truman, J. W. (1992). Commitment of abdominal neuroblasts in Drosophila to a male or female fate is dependent on genes of the sex-determining hierarchy. Development 114, 625-642.
79. Technau, G. M. (1984). Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J. Neurogenet. 1, 113-126.
80. Technau, G. M., Berger, C. and Urbach, R. (2006). Generation of cell diversity and segmental pattern in the embryonic central nervous system of Drosophila. Dev. Dyn. 235, 861-869.
81. Truman, J. W. and Bate, M. (1988). Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol. 125, 145-157.
82. Urbach, R. and Technau, G. M. (2003a). Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 130, 3621-3637.
83. Urbach, R. and Technau, G. M. (2003b). Segment polarity and DV patterning gene expression reveals segmental organization of the Drosophila brain. Development 130, 3607-3620.
84. Urbach, R. and Technau, G. M. (2004). Neuroblast formation and patterning during early brain development in Drosophila. BioEssays 26, 739-751.
85. Urbach, R., Schnabel, R. and Technau, G. M. (2003). The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development 130, 3589-3606.
86. von Hilchen, C. M., Beckervordersandforth, R. M., Rickert, C., Technau, G. M. and Altenhein, B. (2008). Identity, origin, and migration of peripheral glial cells in the Drosophila embryo. Mech. Dev. 125, 337-352.
87. von Hilchen, C. M., Hein, I., Technau, G. M. and Altenhein, B. (2010). Netrins guide migration of distinct glial cells in the Drosophila embryo. Development 137, 1251-1262.
88. von Philipsborn, A. C., Liu, T., Yu, J. Y., Masser, C., Bidaye, S. S. and Dickson, B. J. (2011). Neuronal control of Drosophila courtship song. Neuron 69, 509-522.
89. Walldorf, U. and Gehring, W. J. (1992). Empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. EMBO J. 11, 2247-2259.
90. Wang, W. and Yoder, J. H. (2012). Hox-mediated regulation of doublesex sculpts sex-specific abdomen morphology in Drosophila. Dev. Dyn. 241, 1076-1090.
91. Weiss, J. B., Von Ohlen, T., Mellerick, D. M., Dressler, G., Doe, C. Q. and Scott, M. P. (1998). Dorsoventral patterning in the Drosophila central nervous system: the intermediate neuroblasts defective homeobox gene specifies intermediate column identity. Genes Dev. 12, 3591-3602.
92. Wheeler, S. R., Kearney, J. B., Guardiola, A. R. and Crews, S. T. (2006). Single-cell mapping of neural and glial gene expression in the developing Drosophila CNS midline cells. Dev. Biol. 294, 509-524.
93. White, K., Grether, M. E., Abrams, J. M., Young, L., Farrell, K. and Steller, H. (1994). Genetic control of programmed cell death in Drosophila. Science 264, 677-683.
94. Williams, T. M., Selegue, J. E., Werner, T., Gompel, N., Kopp, A. and Carroll, S. B. (2008). The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134, 610-623.
95. Xie, B., Charlton-Perkins, M., McDonald, E., Gebelein, B. and Cook, T. (2007). Senseless functions as a molecular switch for color photoreceptor differentiation in Drosophila. Development 134, 4243-4253.
96. 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.
97. Zhang, Y., Ungar, A., Fresquez, C. and Holmgren, R. (1994). Ectopic expression of either the Drosophila gooseberry-distal or proximal gene causes alterations of cell fate in the epidermis and central nervous system. Development 120, 1151-1161.