Development, Vol 121, Issue 10 3187-3195, Copyright © 1995 by Company of Biologists

JOURNAL ARTICLES

The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila

EP Spana and CQ Doe
Howard Hughes Medical Institute, Department of Cell and Structural Biology, University of Illinois, Urbana 61801, USA.

Both intrinsic and extrinsic factors are known to regulate sibling cell fate. Here we describe a novel mechanism for the asymmetric localization of a transcription factor to one daughter cell at mitosis. The Drosophila CNS develops from asymmetrically dividing neuroblasts, which give rise to a large neuroblast and a smaller ganglion mother cell (GMC). The prospero gene encodes a transcription factor necessary for proper GMC gene expression. We show that the prospero protein is synthesized in the neuroblast where it is localized to the F-actin cell cortex. At mitosis, prospero is asymmetrically localized to the budding GMC and excluded from the neuroblast. After cytokinesis, prospero is translocated from the GMC cortex into the nucleus. Asymmetric cortical localization of prospero in neuroblasts requires entry into mitosis; it does not depend on numb function. prospero is also observed in cortical crescents in dividing precursors of the peripheral nervous system and adult midgut. The asymmetric cortical localization of prospero at mitosis is a mechanism for rapidly establishing distinct sibling cell fates in the CNS and possibly other tissues.

This article has been cited by other articles:

				C. Q. Doe Neural stem cells: balancing self-renewal with differentiation Development, May 1, 2008; 135(9): 1575 - 1587. [Abstract] [Full Text] [PDF]

				S. E. Siegrist and C. Q. Doe Microtubule-induced cortical cell polarity Genes & Dev., March 1, 2007; 21(5): 483 - 496. [Abstract] [Full Text] [PDF]

				C.-Y. Lee, R. O. Andersen, C. Cabernard, L. Manning, K. D. Tran, M. J. Lanskey, A. Bashirullah, and C. Q. Doe Drosophila Aurora-A kinase inhibits neuroblast self-renewal by regulating aPKC/Numb cortical polarity and spindle orientation Genes & Dev., December 15, 2006; 20(24): 3464 - 3474. [Abstract] [Full Text] [PDF]

				S. G. Sprecher, R. Urbach, G. M. Technau, F. M. Rijli, H. Reichert, and F. Hirth The columnar gene vnd is required for tritocerebral neuromere formation during embryonic brain development of Drosophila Development, November 1, 2006; 133(21): 4331 - 4339. [Abstract] [Full Text] [PDF]

				C.-J. Chang, S. Goulding, R. R. Adams, W. C. Earnshaw, and M. Carmena Drosophila Incenp is required for cytokinesis and asymmetric cell division during development of the nervous system J. Cell Sci., March 15, 2006; 119(6): 1144 - 1153. [Abstract] [Full Text] [PDF]

				U. Mettler, G. Vogler, and J. Urban Timing of identity: spatiotemporal regulation of hunchback in neuroblast lineages of Drosophila by Seven-up and Prospero Development, February 1, 2006; 133(3): 429 - 437. [Abstract] [Full Text] [PDF]

				R. Albertson, C. Chabu, A. Sheehan, and C. Q. Doe Scribble protein domain mapping reveals a multistep localization mechanism and domains necessary for establishing cortical polarity J. Cell Sci., December 1, 2004; 117(25): 6061 - 6070. [Abstract] [Full Text] [PDF]

				S. E. Cheesman, M. J. Layden, T. Von Ohlen, C. Q. Doe, and J. S. Eisen Zebrafish and fly Nkx6 proteins have similar CNS expression patterns and regulate motoneuron formation Development, November 1, 2004; 131(21): 5221 - 5232. [Abstract] [Full Text] [PDF]

				Y. Izumi, N. Ohta, A. Itoh-Furuya, N. Fuse, and F. Matsuzaki Differential functions of G protein and Baz-aPKC signaling pathways in Drosophila neuroblast asymmetric division J. Cell Biol., March 1, 2004; 164(5): 729 - 738. [Abstract] [Full Text] [PDF]

				B. Yedvobnick, A. Kumar, P. Chaudhury, J. Opraseuth, N. Mortimer, and K. M. Bhat Differential Effects of Drosophila Mastermind on Asymmetric Cell Fate Specification and Neuroblast Formation Genetics, March 1, 2004; 166(3): 1281 - 1289. [Abstract] [Full Text] [PDF]

				A. Inbal, D. Levanon, and A. Salzberg Multiple roles for u-turn/ventral veinless in the development of Drosophila PNS Development, June 1, 2003; 130(11): 2467 - 2478. [Abstract] [Full Text] [PDF]

				A. D. Ho and M. Punzel Hematopoietic stem cells: can old cells learn new tricks? J. Leukoc. Biol., May 1, 2003; 73(5): 547 - 555. [Abstract] [Full Text] [PDF]

				V. Orgogozo, F. Schweisguth, and Y. Bellaiche Binary cell death decision regulated by unequal partitioning of Numb at mitosis Development, March 12, 2003; 129(20): 4677 - 4684. [Abstract] [Full Text] [PDF]

				C. A. Meyer, I. Kramer, R. Dittrich, S. Marzodko, J. Emmerich, and C. F. Lehner Drosophila p27Dacapo expression during embryogenesis is controlled by a complex regulatory region independent of cell cycle progression Development, March 3, 2003; 129(2): 319 - 328. [Abstract] [Full Text] [PDF]

				F. Yu, X. Morin, R. Kaushik, S. Bahri, X. Yang, and W. Chia A mouse homologue of Drosophila pins can asymmetrically localize and substitute for pins function in Drosophila neuroblasts J. Cell Sci., March 1, 2003; 116(5): 887 - 896. [Abstract] [Full Text] [PDF]

				X. Bi, A. V. Kajava, T. Jones, Z. N. Demidenko, and M. A. Mortin The Carboxy Terminus of Prospero Regulates Its Subcellular Localization Mol. Cell. Biol., February 1, 2003; 23(3): 1014 - 1024. [Abstract] [Full Text]

				H.-J. Song, J.-C. Billeter, E. Reynaud, T. Carlo, E. P. Spana, N. Perrimon, S. F. Goodwin, B. S. Baker, and B. J. Taylor The fruitless Gene Is Required for the Proper Formation of Axonal Tracts in the Embryonic Central Nervous System of Drosophila Genetics, December 1, 2002; 162(4): 1703 - 1724. [Abstract] [Full Text] [PDF]

				E. L. Weiss, C. Kurischko, C. Zhang, K. Shokat, D. G. Drubin, and F. C. Luca The Saccharomyces cerevisiae Mob2p-Cbk1p kinase complex promotes polarized growth and acts with the mitotic exit network to facilitate daughter cell-specific localization of Ace2p transcription factor J. Cell Biol., September 3, 2002; 158(5): 885 - 900. [Abstract] [Full Text] [PDF]

				F. Yu, C. T. Ong, W. Chia, and X. Yang Membrane Targeting and Asymmetric Localization of Drosophila Partner of Inscuteable Are Discrete Steps Controlled by Distinct Regions of the Protein Mol. Cell. Biol., June 15, 2002; 22(12): 4230 - 4240. [Abstract] [Full Text] [PDF]

				S. Bulgheresi, E. Kleiner, and J. A. Knoblich Inscuteable-dependent apical localization of the microtubule-binding protein Cornetto suggests a role in asymmetric cell division J. Cell Sci., March 12, 2002; 114(20): 3655 - 3662. [Abstract] [Full Text] [PDF]

				G. Zhao and J. B. Skeath The Sox-domain containing gene Dichaete/fish-hook acts in concert with vnd and ind to regulate cell fate in the Drosophila neuroectoderm Development, January 3, 2002; 129(5): 1165 - 1174. [Abstract] [Full Text] [PDF]

				M. R. Freeman and C. Q. Doe Asymmetric Prospero localization is required to generate mixed neuronal/glial lineages in the Drosophila CNS Development, October 15, 2001; 128(20): 4103 - 4112. [Abstract] [Full Text] [PDF]

				Z Demidenko, P Badenhorst, T Jones, X Bi, and M. Mortin Regulated nuclear export of the homeodomain transcription factor Prospero Development, January 4, 2001; 128(8): 1359 - 1367. [Abstract] [PDF]

				V Van De Bor and A Giangrande Notch signaling represses the glial fate in fly PNS Development, January 4, 2001; 128(8): 1381 - 1390. [Abstract] [PDF]

				V Orgogozo, F Schweisguth, and Y Bellaiche Lineage, cell polarity and inscuteable function in the peripheral nervous system of the Drosophila embryo Development, January 3, 2001; 128(5): 631 - 643. [Abstract] [PDF]

				T. R. Sarafi-Reinach and P. Sengupta The forkhead domain gene unc-130 generates chemosensory neuron diversity in C. elegans Genes & Dev., October 1, 2000; 14(19): 2472 - 2485. [Abstract] [Full Text]

				S. Abdelilah-Seyfried, Y.-M. Chan, C. Zeng, N. J. Justice, S. Younger-Shepherd, L. E. Sharp, S. Barbel, S. A. Meadows, L. Y. Jan, and Y. N. Jan A Gain-of-Function Screen for Genes That Affect the Development of the Drosophila Adult External Sensory Organ Genetics, June 1, 2000; 155(2): 733 - 752. [Abstract] [Full Text]

				H. Knaut, F. Pelegri, K. Bohmann, H. Schwarz, and C. Nusslein-Volhard Zebrafish vasa RNA but Not Its Protein Is a Component of the Germ Plasm and Segregates Asymmetrically before Germline Specification J. Cell Biol., May 15, 2000; 149(4): 875 - 888. [Abstract] [Full Text] [PDF]

				L. Li and H. Vaessin Pan-neural Prospero terminates cell proliferation during Drosophila neurogenesis Genes & Dev., January 15, 2000; 14(2): 147 - 151. [Abstract] [Full Text]

				P. Cheah, W Chia, and X Yang Jumeaux, a novel Drosophila winged-helix family protein, is required for generating asymmetric sibling neuronal cell fates Development, January 8, 2000; 127(15): 3325 - 3335. [Abstract] [PDF]

				Y Akiyama-Oda, Y Hotta, S Tsukita, and H Oda Mechanism of glia-neuron cell-fate switch in the Drosophila thoracic neuroblast 6-4 lineage Development, January 8, 2000; 127(16): 3513 - 3522. [Abstract] [PDF]

				S. Huang, P. Law, K. Francis, B. O. Palsson, and A. D. Ho Symmetry of Initial Cell Divisions Among Primitive Hematopoietic Progenitors Is Independent of Ontogenic Age and Regulatory Molecules Blood, October 15, 1999; 94(8): 2595 - 2604. [Abstract] [Full Text] [PDF]

				M. P. Zeidler, N. Perrimon, and D. I. Strutt Polarity determination in the Drosophila eye: a novel role for Unpaired and JAK/STAT signaling Genes & Dev., May 15, 1999; 13(10): 1342 - 1353. [Abstract] [Full Text]

				M Gho, Y Bellaiche, and F Schweisguth Revisiting the Drosophila microchaete lineage: a novel intrinsically asymmetric cell division generates a glial cell Development, January 8, 1999; 126(16): 3573 - 3584. [Abstract] [PDF]

				D Arendt and K Nubler-Jung Comparison of early nerve cord development in insects and vertebrates Development, January 6, 1999; 126(11): 2309 - 2325. [Abstract] [PDF]

				P Wai, B Truong, and K. Bhat Cell division genes promote asymmetric interaction between Numb and Notch in the Drosophila CNS Development, January 6, 1999; 126(12): 2759 - 2770. [Abstract] [PDF]

				M Tio, M Zavortink, X Yang, and W Chia A functional analysis of inscuteable and its roles during Drosophila asymmetric cell divisions J. Cell Sci., January 5, 1999; 112(10): 1541 - 1551. [Abstract] [PDF]

				Y Akiyama-Oda, T Hosoya, and Y Hotta Asymmetric cell division of thoracic neuroblast 6-4 to bifurcate glial and neuronal lineage in Drosophila Development, January 5, 1999; 126(9): 1967 - 1974. [Abstract] [PDF]

				L Manning and C. Doe Prospero distinguishes sibling cell fate without asymmetric localization in the Drosophila adult external sense organ lineage Development, January 5, 1999; 126(10): 2063 - 2071. [Abstract] [PDF]

				M Crozatier and A Vincent Requirement for the Drosophila COE transcription factor Collier in formation of an embryonic muscle: transcriptional response to notch signalling Development, January 4, 1999; 126(7): 1495 - 1504. [Abstract] [PDF]

				N. Hawkins and G. Garriga Asymmetric cell division: from A to Z Genes & Dev., December 1, 1998; 12(23): 3625 - 3638. [Full Text]

				C.-P. Shen, J. A. Knoblich, Y.-M. Chan, M.-M. Jiang, L. Y. Jan, and Y. N. Jan Miranda as a multidomain adapter linking apically localized Inscuteable and basally localized Staufen and Prospero during asymmetric cell division in Drosophila Genes & Dev., June 15, 1998; 12(12): 1837 - 1846. [Abstract] [Full Text]

				A. J. Schuldt, J. H.J. Adams, C. M. Davidson, D. R. Micklem, J. Haseloff, D. S. Johnston, and A. H. Brand Miranda mediates asymmetric protein and RNA localization in the developing nervous system Genes & Dev., June 15, 1998; 12(12): 1847 - 1857. [Abstract] [Full Text]

				M. Buescher, S. L. Yeo, G. Udolph, M. Zavortink, X. Yang, G. Tear, and W. Chia Binary sibling neuronal cell fate decisions in the Drosophila embryonic central nervous system are nonstochastic and require inscuteable-mediated asymmetry of ganglion mother cells Genes & Dev., June 15, 1998; 12(12): 1858 - 1870. [Abstract] [Full Text]

				A. Carmena, B. Murugasu-Oei, D. Menon, F. Jiménez, and W. Chia inscuteable and numb mediate asymmetric muscle progenitor cell divisions during Drosophila myogenesis Genes & Dev., February 1, 1998; 12(3): 304 - 315. [Abstract] [Full Text]

				F Matsuzaki, T Ohshiro, H Ikeshima-Kataoka, and H Izumi miranda localizes staufen and prospero asymmetrically in mitotic neuroblasts and epithelial cells in early Drosophila embryogenesis Development, January 10, 1998; 125(20): 4089 - 4098. [Abstract] [PDF]

				J. Skeath The Drosophila EGF receptor controls the formation and specification of neuroblasts along the dorsal-ventral axis of the Drosophila embryo Development, January 9, 1998; 125(17): 3301 - 3312. [Abstract] [PDF]

				T Jagla, F Bellard, Y Lutz, G Dretzen, M Bellard, and K Jagla ladybird determines cell fate decisions during diversification of Drosophila somatic muscles Development, January 9, 1998; 125(18): 3699 - 3708. [Abstract] [PDF]

				X Qian, S. Goderie, Q Shen, J. Stern, and S Temple Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells Development, January 8, 1998; 125(16): 3143 - 3152. [Abstract] [PDF]

				F Hirth, B Hartmann, and H Reichert Homeotic gene action in embryonic brain development of Drosophila Development, January 5, 1998; 125(9): 1579 - 1589. [Abstract] [PDF]

				J. Skeath and C. Doe Sanpodo and Notch act in opposition to Numb to distinguish sibling neuron fates in the Drosophila CNS Development, January 5, 1998; 125(10): 1857 - 1865. [Abstract] [PDF]

				J. A. Knoblich, L. Y. Jan, and Y. N. Jan The N terminus of the Drosophila Numb protein directs membrane association and actin-dependent asymmetric localization PNAS, November 25, 1997; 94(24): 13005 - 13010. [Abstract] [Full Text] [PDF]

				B. Hassan, L. Li, K. A. Bremer, W. Chang, J. Pinsonneault, and H. Vaessin Prospero is a panneural transcription factor that modulates homeodomain protein activity PNAS, September 30, 1997; 94(20): 10991 - 10996. [Abstract] [Full Text] [PDF]

				X Yang, S Bahri, T Klein, and W Chia Klumpfuss, a putative Drosophila zinc finger transcription factor, acts to differentiate between the identities of two secondary precursor cells within one neuroblast lineage. Genes & Dev., June 1, 1997; 11(11): 1396 - 1408. [Abstract] [PDF]

				M. C. Mione, J. F. R. Cavanagh, B. Harris, and J. G. Parnavelas Cell Fate Specification and Symmetrical/Asymmetrical Divisions in the Developing Cerebral Cortex J. Neurosci., March 15, 1997; 17(6): 2018 - 2029. [Abstract] [Full Text] [PDF]

				T. Menne, K Luer, G. Technau, and C Klambt CNS midline cells in Drosophila induce the differentiation of lateral neural cells Development, January 12, 1997; 124(24): 4949 - 4958. [Abstract] [PDF]

				S Wang, S Younger-Shepherd, L. Jan, and Y. Jan Only a subset of the binary cell fate decisions mediated by Numb/Notch signaling in Drosophila sensory organ lineage requires Suppressor of Hairless Development, January 11, 1997; 124(22): 4435 - 4446. [Abstract] [PDF]

				B Ohlstein and D McKearin Ectopic expression of the Drosophila Bam protein eliminates oogenic germline stem cells Development, January 9, 1997; 124(18): 3651 - 3662. [Abstract] [PDF]

				H Sawa, L Lobel, and H R Horvitz The Caenorhabditis elegans gene lin-17, which is required for certain asymmetric cell divisions, encodes a putative seven-transmembrane protein similar to the Drosophila frizzled protein. Genes & Dev., September 1, 1996; 10(17): 2189 - 2197. [Abstract] [PDF]

				R Baumeister, Y Liu, and G Ruvkun Lineage-specific regulators couple cell lineage asymmetry to the transcription of the Caenorhabditis elegans POU gene unc-86 during neurogenesis. Genes & Dev., June 1, 1996; 10(11): 1395 - 1410. [Abstract] [PDF]

				C Guenther and G Garriga Asymmetric distribution of the C. elegans HAM-1 protein in neuroblasts enables daughter cells to adopt distinct fates Development, January 11, 1996; 122(11): 3509 - 3518. [Abstract] [PDF]

				L Boyd, S Guo, D Levitan, D. Stinchcomb, and K. Kemphues PAR-2 is asymmetrically distributed and promotes association of P granules and PAR-1 with the cortex in C. elegans embryos Development, January 10, 1996; 122(10): 3075 - 3084. [Abstract] [PDF]

				J Broadus and C. Doe Evolution of neuroblast identity: seven-up and prospero expression reveal homologous and divergent neuroblast fates in Drosophila and Schistocerca Development, January 12, 1995; 121(12): 3989 - 3996. [Abstract] [PDF]

E. Spana and C. Doe The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila Development, January 10, 1995; 121(10): 3187 - 3195. [Abstract]