A multipotent transit-amplifying neuroblast lineage in the central brain gives rise to optic lobe glial cells in Drosophila

Developmental Biology

Volumn 379, Issue 2, 2013, Pages 182-194

  Viktorin, Gudrun ^a   Riebli, Nadia ^a   Reichert, Heinrich ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Drosophila; Glia; Neuroglioblast; Optic lobe; Type II neuroblast

Indexed keywords

ARTICLE; BRAIN CELL; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL LINEAGE; CELL MIGRATION; CELL STRAIN; CELL STRAIN DL1; CELL TYPE; CONTROLLED STUDY; DROSOPHILA; GLIA CELL; INNERVATION; INSECT DEVELOPMENT; INTERNEURON; LARVA; MULTIPOTENT STEM CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; OPTIC CHIASM; OPTIC LOBE; PRIORITY JOURNAL; ANIMAL; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; DROSOPHILA MELANOGASTER; FLUORESCENCE MICROSCOPY; GLIA; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; DROSOPHILA MELANOGASTER; IMMUNOHISTOCHEMISTRY; LARVA; MICROSCOPY, FLUORESCENCE; MULTIPOTENT STEM CELLS; NEURAL STEM CELLS; NEUROGLIA; OPTIC LOBE, NONMAMMALIAN;

MLCS; MLOWN;

EID: 84878861831     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.04.020     Document Type: Article

References (67)

1. Alfonso T.B., Jones B.W. gcm2 promotes glial cell differentiation and is required with glial cells missing for macrophage development in Drosophila. Dev. Biol. 2002, 248:369-383.
2. Awasaki T., Lai S.L., Ito K., Lee T. Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J. Neurosci. 2008, 28:13742-13753.
3. Bayraktar O.A., Boone J.Q., Drummond M.L., Doe C.Q. Drosophila type II neuroblast lineages keep Prospero levels low to generate large clones that contribute to the adult brain central complex. Neural Dev. 2010, 5:26.
4. Beckervordersandforth R.M., Rickert C., Altenhein B., Technau G.M. Subtypes of glial cells in the Drosophila embryonic ventral nerve cord as related to lineage and gene expression. Mech. Dev. 2008, 125:542-557.
5. Bello B.C., Hirth F., Gould A.P. A pulse of the Drosophila Hox protein Abdominal-A schedules the end of neural proliferation via neuroblast apoptosis. Neuron 2003, 37:209-219.
6. Bello B.C., Izergina N., Caussinus E., Reichert H. Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev. 2008, 3:5.
7. Bieber A.J., Snow P.M., Hortsch M., Patel N.H., Jacobs J.R., Traquina Z.R., Schilling J., Goodman C.S. Drosophila neuroglian: a member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell 1989, 59:447-460.
8. Boone J.Q., Doe C.Q. Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Dev. Neurobiol. 2008, 68:1185-1195.
9. Bossing T., Udolph G., Doe C.Q., Technau G.M. The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev. Biol. 1996, 179:41-64.
10. Bowman S.K., Rolland V., Betschinger J., Kinsey K.A., Emery G., Knoblich J.A. The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. Dev. Cell 2008, 14:535-546.
11. Boyan G.S., Reichert H. Mechanisms for complexity in the brain: Generating the insect central complex. Trends Neurosci. 2011, 34:247-257.
12. Brand A.H., Livesey F.J. Neural stem cell biology in vertebrates and invertebrates: more alike than different?. Neuron 2011, 70:719-729.
13. Broadus J., Skeath J.B., Spana E.P., Bossing T., Technau G., Doe C.Q. New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system. Mech. Dev. 1995, 53:393-402.
14. Campbell G., Goring H., Lin T., Spana E., Andersson S., Doe C.Q., Tomlinson A. RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability in Drosophila. Development 1994, 120:2957-2966.
15. Chotard C., Salecker I. Glial cell development and function in the Drosophila visual system. Neuron Glia Biol. 2007, 3:17-25.
16. Dearborn R., Kunes S. An axon scaffold induced by retinal axons directs glia to destinations in the Drosophila optic lobe. Development 2004, 131:2291-2303.
17. Doe C.Q. Neural stem cells: balancing self-renewal with differentiation. Development 2008, 135:1575-1587.
18. Edwards T.N., Meinertzhagen I.A. The functional organisation of glia in the adult brain of Drosophila and other insects. Prog. Neurobiol. 2010, 90:471-497.
19. Edwards T.N., Nuschke A.C., Nern A., Meinertzhagen I.A. Organization and metamorphosis of glia in the Drosophila visual system. J. Comp. Neurol. 2012, 520:2067-2085.
20. Egger B., Boone J.Q., Stevens N.R., Brand A.H., Doe C.Q. Regulation of spindle orientation and neural stem cell fate in the Drosophila optic lobe. Neural. Dev. 2007, 2:1.
21. Halter D.A., Urban J., Rickert C., Ner S.S., Ito K., Travers A.A., Technau G.M. The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 1995, 121:317-332.
22. Han C., Jan L.Y., Jan Y.N. Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron-glia interactions in Drosophila. Proc. Nat. Acad. Sci. U.S.A. 2011, 108:9673-9678.
23. Hartenstein V. Morphological diversity and development of glia in Drosophila. Glia 2011, 59:1237-1252.
24. Hartenstein V., Nassif C., Lekven A. Embryonic development of the Drosophila brain. II. Pattern of glial cells. J. Comp. Neurol. 1998, 402:32-47.
25. Hofmeyer K., Kretzschmar D., Pflugfelder G.O. Optomotor-blind expression in glial cells is required for correct axonal projection across the Drosophila inner optic chiasm. Dev. Biol. 2008, 315:28-41.
26. Homem C.C., Knoblich J.A. Drosophila neuroblasts: a model for stem cell biology. Development 2012, 139:4297-4310.
27. Hortsch M., Patel N.H., Bieber A.J., Traquina Z.R., Goodman C.S. Drosophila neurotactin, a surface glycoprotein with homology to serine esterases, is dynamically expressed during embryogenesis. Development 1990, 110:1327-1340.
28. Ito K., Awasaki T. Clonal unit architecture of the adult fly brain. Adv. Exp. Med. Biol. 2008, 628:137-158.
29. Ito, M., Masuda, N., Shinomiya, K., Endo, K., Ito, K., 2013. Systematic Analysis of Neural Projections Reveals Clonal Composition of the Drosophila Brain. Curr. Biol 23, 644-655.
30. Izergina N., Balmer J., Bello B., Reichert H. Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain. Neural. Dev. 2009, 4:44.
31. Jacobs J.R., Hiromi Y., Patel N.H., Goodman C.S. Lineage, migration, and morphogenesis of longitudinal glia in the Drosophila CNS as revealed by a molecular lineage marker. Neuron 1989, 2:1625-1631.
32. Jenett A., Rubin G.M., Ngo T.T., Shepherd D., Murphy C., Dionne H., Pfeiffer B.D., Cavallaro A., Hall D., Jeter J., Iyer N., Fetter D., Hausenfluck J.H., Peng H., Trautman E.T., Svirskas R.R., Myers E.W., Iwinski Z.R., Aso Y., Depasquale G.M., Enos A., Hulamm P., Lam S.C., Li H.H., Laverty T.R., Long F., Qu L., Murphy S.D., Rokicki K., Safford T., Shaw K., Simpson J.H., Sowell A., Tae S., Yu Y., Zugates C.T. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep. 2012, 2:991-1001.
33. Jiang Y., Reichert H. Programmed cell death in type II neuroblast lineages is required for central complex development in the Drosophila brain. Neural Dev. 2012, 7:3.
34. Jones B.W., Fetter R.D., Tear G., Goodman C.S. Glial cells missing: A genetic switch that controls glial versus neuronal fate. Cell 1995, 82:1013-1023.
35. Klämbt C. Modes and regulation of glial migration in vertebrates and invertebrates. Nat. Rev. Neurosci. 2009, 10:769-779.
36. Klämbt C., Goodman C.S. Role of the midline glia and neurons in the formation of the axon commissures in the central nervous system of the Drosophila embryo. Ann. N.Y. Acad. Sci. 1991, 633:142-159.
37. Klämbt C., Jacobs J.R., Goodman C.S. The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell 1991, 64:801-815.
38. Knoblich J.A. Mechanisms of asymmetric stem cell division. Cell 2008, 132:583-597.
39. Kowalczyk T., Pontious A., Englund C., Daza R.A., Bedogni F., Hodge R., Attardo A., Bell C., Huttner W.B., Hevner R.F. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb. Cortex 2009, 19:2439-2450.
40. Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 2009, 32:149-184.
41. Lee T., Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999, 22:451-461.
42. Lui J.H., Hansen D.V., Kriegstein A.R. Development and evolution of the human neocortex. Cell 2011, 146:18-36.
43. Miyata T., Kawaguchi D., Kawaguchi A., Gotoh Y. Mechanisms that regulate the number of neurons during mouse neocortical development. Curr. Opin. Neurobiol. 2010, 20:22-28.
44. Newsome T.P., Asling B., Dickson B.J. Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 2000, 127:851-860.
45. Park Y., Filippov V., Gill S.S., Adams M.E. Deletion of the ecdysis-triggering hormone gene leads to lethal ecdysis deficiency. Development 2002, 129:493-503.
46. Patel N.H., Snow P.M., Goodman C.S. Characterization and cloning of fasciclin III: a glycoprotein expressed on a subset of neurons and axon pathways in Drosophila. Cell 1987, 48:975-988.
47. Pereanu W., Hartenstein V. Neural lineages of the Drosophila brain: a three-dimensional digital atlas of the pattern of lineage location and projection at the late larval stage. J. Neurosci. 2006, 26:5534-5553.
48. Pereanu W., Shy D., Hartenstein V. Morphogenesis and proliferation of the larval brain glia in Drosophila. Dev. Biol. 2005, 283:191-203.
49. Perez S.E., Steller H. Migration of glial cells into retinal axon target field in Drosophila melanogaster. J. Neurobiol. 1996, 30:359-373.
50. Pfeiffer B.D., Jenett A., Hammonds A.S., Ngo T.T., Misra S., Murphy C., Scully A., Carlson J.W., Wan K.H., Laverty T.R., Mungall C., Svirskas R., Kadonaga J.T., Doe C.Q., Eisen M.B., Celniker S.E., Rubin G.M. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:9715-9720.
51. Pignoni F., Zipursky S.L. Induction of Drosophila eye development by decapentaplegic. Development 1997, 124:271-278.
52. Poeck B., Fischer S., Gunning D., Zipursky S.L., Salecker I. Glial cells mediate target layer selection of retinal axons in the developing visual system of Drosophila. Neuron 2001, 29:99-113.
53. Saini N., Reichert H. Neural stem cells in Drosophila: molecular genetic mechanisms underlying normal neural proliferation and abnormal brain tumor formation. Stem Cells Int. 2012, 2012:486169.
54. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P., Cardona A. Fiji: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682.
55. Schmidt H., Rickert C., Bossing T., Vef O., Urban J., Technau G.M. The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev. Biol. 1997, 189:186-204.
56. Silies M., Yuva Y., Engelen D., Aho A., Stork T., Klämbt C. Glial cell migration in the eye disc. J. Neurosci. 2007, 27:13130-13139.
57. Soustelle L., Giangrande A. Novel gcm-dependent lineages in the postembryonic nervous system of Drosophila melanogaster. Dev. Dyn. 2007, 236:2101-2108.
58. Struhl G., Basler K. Organizing activity of wingless protein in Drosophila. Cell 1993, 72:527-540.
59. Tix S., Eule E., Fischbach K.F., Benzer S. Glia in the chiasms and medulla of the Drosophila melanogaster optic lobes. Cell Tissue Res. 1997, 289:397-409.
60. Unhavaithaya Y., Orr-Weaver T.L. Polyploidization of glia in neural development links tissue growth to blood-brain barrier integrity. Genes Dev. 2012, 26:31-36.
61. Viktorin G., Riebli N., Popkova A., Giangrande A., Reichert H. Multipotent neural stem cells generate glial cells of the central complex through transit amplifying intermediate progenitors in Drosophila brain development. Dev. Biol. 2011, 356:553-565.
62. Wagh D.A., Rasse T.M., Asan E., Hofbauer A., Schwenkert I., Durrbeck H., Buchner S., Dabauvalle M.C., Schmidt M., Qin G., Wichmann C., Kittel R., Sigrist S.J., Buchner E. Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 2006, 49:833-844.
63. Winberg M.L., Perez S.E., Steller H. Generation and early differentiation of glial cells in the first optic ganglion of Drosophila melanogaster. Development 1992, 115:903-911.
64. Weng M., Golden K.L., Lee C.Y. dFezf/Earmuff maintains the restricted developmental potential of intermediate neural progenitors in Drosophila. Dev. Cell 2010, 18:126-135.
65. Weng M., Lee C.Y. Keeping neural progenitor cells on a short leash during Drosophila neurogenesis. Curr. Opin. Neurobiol. 2011, 21:36-42.
66. Xiong W.C., Okano H., Patel N.H., Blendy J.A., Montell C. repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev. 1994, 8:981-994.
67. Yu, H.-H., Awasaki, T., Schroder, M.D., Long, F., Yang, J.S., He, Y., Ding, P., Kao, J.-C., Wu, G.Y.-Y., Peng, H., Myers, G., Lee, T., Clonal Development and Organization of the Adult Drosophila Central Brain. Curr. Biol. 23, 633-643.