In the Drosophila central nervous system (CNS) glial cells are known to be generated from glioblasts, which produce exclusively glia or neuroglioblasts that bifurcate to produce both neuronal and glial sublineages. We show that the genesis of a subset of glial cells, the subperineurial glia (SPGs), involves a new mechanism and requires Notch. We demonstrate that the SPGs share direct sibling relationships with neurones and are the products of asymmetric divisions. This mechanism of specifying glial cell fates within the CNS is novel and provides further insight into regulatory interactions leading to glial cell fate determination. Furthermore, we show that Notch signalling positively regulates glial cells missing (gcm) expression in the context of SPG development.
Reference
Akiyama-Oda
Y.
, Hosoya
T.
, Hotta
Y.
(1999
) Asymmetric cell division of thoracic neuroblast 6–4 to bifurcate glial and neuronal lineage in Drosophila.
Development
126
, 1967
–1974
Bernardoni
R.
, Kammerer
M.
, Vonesch
J. L.
, Giangrande
A.
(1999
) Gliogenesis depends on glide/gcm through asymmetric division of neuroglioblasts.
Dev. Biol
216
, 265
–275
Bossing
T.
, Udolph
G.
, Doe
C. Q.
, 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
Broadus
J.
, Skeath
J. B.
, Spana
E. P.
, Bossing
T.
, Technau
G. M.
, 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
Buenzow
D. E.
, 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
Buescher
M.
, Yeo
S. L.
, Udolph
G.
, Zavortink
M.
, Yang
X.
, Tear
G.
, Chia
W.
(1998
) Binary sibling neuronal cell fate in the Drosophila embryonic central nervous system are nonstochastic and require inscuteable-mediated asymmetry of ganglion mother cells.
Genes Dev
12
, 1858
–1870
Campell
G.
, Göring
H.
, Lin
T.
, Spana
E.
, Andersson
S.
, Doe
C. Q.
, Tomlinson
A.
(1994
) RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability in Drosophila.
Development
120
, 2957
–2966
Frasch
M.
, Hoey
T.
, Rushlow
H.
, Levine
M.
(1986
) Characterisation and localisation of the even-skipped protein of Drosophila.
EMBO J
6
, 749
–759
Giesen
K.
, Hummel
T.
, Stollewerk
A.
, Harrison
S.
, Travers
A.
, Klämbt
C.
(1997
) Glial development in the Drosophila CNS requires concomitant activation of glial and repression of neuronal differentiation genes.
Development
124
, 2307
–2311
Guo
M.
, Jan
L. Y.
, Jan
Y. N.
(1996
) Control of daughter cell fates during asymmetric division: interaction of Numb and Notch.
Neuron
17
, 27
–41
Halter
D. A.
, Urban
J.
, Rickert
C.
, Ner
S. S.
, Ito
K.
, Travers
A.
, Technau
G.
(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
Hirata
J.
, Nakagoshi
H.
, Nabeshima
Y.
, Matzuzaki
F.
(1995
) Asymmetric segregation of the homeodomain protein Prospero during Drosophila development.
Nature
377
, 627
–630
Hosoya
T.
, Takizawa
K.
, Nitta
K.
, Hotta
Y.
(1995
) glial cells missing: a binary switch between neuronal and glial determination in Drosophila.
Cell
82
, 1025
–1036
Jacobs
J. R.
, Hiromi
Y.
, Patel
N. P.
, Goodman
C. S.
(1989
) Lineage, migration, and morphogenesis of longitudinal glia in the Drosophila CNS as revealed by a molecular lineage marker.
Neuron
2
, 1625
–1631
Jones
B. W.
, Fetter
R. D.
, Tear
G.
, Goodman
C. S.
(1995
) glial cells missing: a genetic switch that controls glial versus neuronal fate.
Cell
82
, 1013
–1023
Klaes
A.
, Menne
T.
, Stollewerk
A.
, Scholz
H.
, Klämbt
C.
(1994
) The ETS transcription factors encoded by the Drosophila Gene pointed direct glial cell differentiation in the embryonic CNS.
Cell
78
, 149
–160
Klämbt
C.
(1993
) The Drosophila gene pointed encodes two ETS-like proteins which are involved in the development of the midline glia cells.
Development
117
, 163
–176
Klämbt
C.
, Goodman
C. S.
(1991
) The diversity and pattern of glia during axon pathway formation in the Drosophila embryo.
Glia
4
, 205
–213
Knoblich
J. A.
, Jan
L. Y.
, Jan
Y. N.
(1995
) Asymmetric segregation of Numb and Prospero during cell division.
Nature
377
, 624
–627
Kraut
R.
, Campos-Ortega
J. A.
(1996
) inscuteable, a neural precursor gene of Drosophila, encodes a candidate for a cytoskeleton adapter protein.
Dev. Biol
174
, 65
–81
Kraut
R.
, Chia
W.
, Jan
L. Y.
, Jan
Y. N.
, Knoblich
J. A.
(1996
) Role of inscuteable in orienting asymmetric cell division in Drosophila.
Nature
383
, 50
–55
Morrison
S. J.
, Perez
S. E.
, Qiao
Z.
, Verdi
J. M.
, Hicks
C.
, Weinmaster
G.
, Anderson
D. J.
(2000
) Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells.
Cell
101
, 499
–510
Prokop
A.
, Technau
G. M.
(1994
) Early tagma specific commitment of Drosophila progenitor NB1-1.
Development
120
, 2567
–2578
Rhyu
M. S.
, Jan
L. Y.
, Jan
Y. N.
(1994
) Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells.
Cell
76
, 477
–491
Schaefer
M.
, Shevchenko
A.
, Knoblich
J. A.
(2000
) A protein complex containing Inscuteable and the Galpha-binding protein Pins orients asymmetric cell divisions in Drosophila.
Curr. Biol
10
, 353
–62
Schmid
A.
, Chiba
A.
, Doe
C. Q.
(1999
) Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets.
Development
126
, 4653
–4689
Schmidt
H.
, Rickert
C.
, Bossing
T.
, Vef
O.
, Urban
J.
, 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
Schmidt-Ott
U.
, Technau
G. M.
(1992
) Expression of en and wg in the embryonic head and brain of Drosophila indicates a refolded band of seven segment remnants.
Development
116
, 111
–125
Schober
M.
, Schaefer
M.
, Knoblich
J. A.
(1999
) Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts.
Nature
402
, 548
–551
Schuldt
A. J.
, Adams
J. H.
, Davidson
C. M.
, Micklem
D. R.
, Haseloff
J.
, St Johnston
D.
, Brand
A. H.
(1998
) Miranda mediates asymmetric protein and RNA localisation in the developing nervous system.
Genes Dev
12
, 1847
–1857
Schuldt
A. J.
, Brand
A. H.
(1999
) Mastermind acts downstream of Notch to specify neuronal cell fates in the Drosophila central nervous system.
Dev. Biol
205
, 287
–295
Skeath
J. B.
, Doe
C. Q.
(1998
) Sanpodo and Notch act in opposition to distinguish sibling neuron fates in the Drosophila CNS.
Development
125
, 1857
–1865
Spana
E. P.
, Doe
C. Q.
(1996
) Numb antagonises Notch signaling to specify sibling neuron cell fates.
Neuron
17
, 21
–26
Spana
E. P.
, Kopcynski
C.
, Goodman
C. S.
, Doe
C. Q.
(1995
) Asymmetric localisation of numb autonomously determines sibling neuron identity in the Drosophila CNS.
Development
121
, 3489
–3494
Udolph
G.
, Prokop
A.
, Bossing
T.
, Technau
G. M.
(1993
) A common precursor for glia and neurons in the embryonic CNS of Drosophila gives rise to segment-specific lineage variants.
Development
118
, 765
–775
Udolph
G.
, Urban
J.
, Ruesing
G.
, Luer
K.
, Technau
G. M.
(1998
) Differential effects of EGF receptor signalling on neuroblast lineages along the dorsoventral axis of the Drosophila CNS.
Development
125
, 3291
–3299
Vincent
S.
, Vonesch
J. L.
, Giangrande
A.
(1996
) Glide directs glial fate commitment and cell fate switch between neurones and glia.
Development
122
, 131
–139
Wang
S.
, Barres
B. A.
(2000
) Up a notch: instructing gliogenesis.
Neuron
27
, 197
–200
Wodarz
A.
, Ramrath
A.
, Kuchinke
U.
, Knust
E.
(1999
) Bazooka provides an apical cue for Inscuteable localisation in Drosophila neuroblasts.
Nature
402
, 544
–547
Xiong
W. C.
, Okano
H.
, Patel
N. H.
, Blendy
J. A.
, Montell
C.
(1994
) Repo encodes a glial-specific homeodomain protein required in the Drosophila nervous system.
Genes Dev
8
, 981
–894
Yu
F.
, Morin
X.
, Cai
Y.
, Yang
X.
, Chia
W.
(2000
) Analysis of partner of inscuteable, a novel player of Drosophila asymmetric divisions, reveals two distinct steps in inscuteable apical localisation.
Cell
100
, 399
–409
This content is only available via PDF.
© 2001 by Company of Biologists
2001
-HUBSwebinar.jpg?versionId=4486)
(update)-InPreprints.png?versionId=4486)
