The adult external sense organ precursor (SOP) lineage is a model system for studying asymmetric cell division. Adult SOPs divide asymmetrically to produce IIa and IIb daughter cells; IIa generates the external socket (tormogen) and hair (trichogen) cells, while IIb generates the internal neuron and sheath (thecogen) cells. Here we investigate the expression and function of prospero in the adult SOP lineage. Although Prospero is asymmetrically localized in embryonic SOP lineage, this is not observed in the adult SOP lineage: Prospero is first detected in the IIb nucleus and, during IIb division, it is cytoplasmic and inherited by both neuron and sheath cells. Subsequently, Prospero is downregulated in the neuron but maintained in the sheath cell. Loss of prospero function leads to ‘double bristle’ sense organs (reflecting a IIb-to-IIa transformation) or ‘single bristle’ sense organs with abnormal neuronal differentiation (reflecting defective IIb development). Conversely, ectopic prospero expression results in duplicate neurons and sheath cells and a complete absence of hair/socket cells (reflecting a IIa-to-IIb transformation). We conclude that (1) despite the absence of asymmetric protein localization, prospero expression is restricted to the IIb cell but not its IIa sibling, (2) prospero promotes IIb cell fate and inhibits IIa cell fate, and (3) prospero is required for proper axon and dendrite morphology of the neuron derived from the IIb cell. Thus, prospero plays a fundamental role in establishing binary IIa/IIb sibling cell fates without being asymmetrically localized during SOP division. Finally, in contrast to previous studies, we find that the IIb cell divides prior to the IIa cell in the SOP lineage.

Reference

Ajiro
K.
,
Yoda
K.
,
Utsumi
K.
,
Nishikawa
Y.
(
1996
)
Alteration of cell cycle-dependent histone mitosis-specific H3 phosphorylation and chromatin condensation in mammalian interphase cells.
J. Biol. Chem
271
,
13197
13201
Bier
E.
,
Ackerman
L.
,
Barbel
S.
,
Jan
L.
,
Jan
Y. N.
(
1988
)
Identification and characterization of a neuron-specific nuclear antigen in Drosophila.
Science
240
,
913
915
Bodmer
R.
,
Barbel
S.
,
Sheperd
S.
,
Jack
J.
,
Jan
L.
,
Jan
Y.
(
1987
)
Transformation of sensory organs by mutations of the cut locus of D. melanogaster.
Cell
51
,
293
307
Bodmer
R.
,
Carretto
R.
,
Jan
Y. N.
(
1989
)
Neurogenesis of the peripheral nervous system in Drosophila embryos: DNA replication patterns and cell lineages.
Neuron
3
,
21
32
Bray
S.
(
1998
)
A Notch Affair.
Cell
93
,
499
503
Broadus
J.
,
Doe
C. Q.
(
1997
)
Extrinsic cues, intrinsic cues, and microfilaments regulate asymmetric protein localization in Drosophila neuroblasts.
Curr. Biol
7
,
827
835
Campos-Ortega
J.
(
1996
)
Numb diverts notch pathway off the tramtrack.
Neuron
17
,
1
4
Doe
C. Q.
,
Chu-LaGraff
Q.
,
Wright
D. M.
,
Scott
M. P.
(
1991
)
The prospero gene specifies cell fates in the Drosophila central nervous system.
Cell
65
,
451
464
Gho
M.
,
Lecourtois
M.
,
Geraud
G.
,
Posakony
J.
,
Schweisguth
F.
(
1996
)
Subcellular localization of Suppressor of Hairless in Drosophila sense organ cells during Notch signalling.
Development
122
,
1673
1682
Gho
M.
,
Schweisguth
F.
(
1998
)
Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila.
Nature
393
,
178
181
Golic
K. G.
,
Lindquist
S.
(
1989
)
The FLP recombinase catalyzes site-specific recombination in the Drosophila genome.
Cell
59
,
499
509
Guo
M.
,
Bier
E.
,
Jan
L. Y.
,
Jan
Y. N.
(
1995
)
tramtrack acts downstream of numb to specify distinct daughter cell fates during asymmetric cell divisions in the Drosophila PNS.
Neuron
14
,
913
925
Guo
M.
,
Jan
L.
,
Jan
Y.
(
1996
)
Control of daughter cell fates during asymmetric division: Interaction of numb and notch.
Neuron
17
,
27
41
Hartenstein
V.
,
Posakony
J.W.
(
1989
)
Development of adult sensilla on the wing and notum of Drosophila melanogaster.
Development
107
,
389
405
Hartenstein
V.
,
Posakony
J. W.
(
1990
)
A dual function of the Notch gene in Drosophila sensillum development.
Dev. Biol
142
,
13
30
Hendzel
M.
,
Wei
Y.
,
Mancini
M.
,
Van Hooser
A.
,
Ranalli
T.
,
Brinkley
B.
,
Bazett-Jones
D.
,
Allis
C.
(
1997
)
Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation.
Chromosoma
106
,
348
360
Higashijima
S.
,
Michiue
T.
,
Emori
Y.
,
Saigo
K.
(
1992
)
Subtype determination of Drosophila embryonic external sensory organs by redundant homeo box genes BarH1 and BarH2.
Genes Dev
6
,
1005
1018
Hirata
J.
,
Nakaghoshi
H.
,
Nabeshima
Y.
,
Matsuzaki
F.
(
1995
)
Asymmetric segregation of the homeodomain protein Prospero during Drosophila development.
Nature
377
,
627
630
Huang
F.
,
Dambly-Chaudiee
C.
,
Ghysen
A.
(
1991
)
The emergence of sense organs in the wing disc of Drosophila.
Development
111
,
1087
1095
Ikeshima-Kataoka
H.
,
Skeath
J. B.
,
Nabeshima
Y.
,
Doe
C. Q.
,
Matsuzaki
F.
(
1997
)
Miranda directs Prospero to a daughter cell during Drosophila asymmetric divisions.
Nature
390
,
625
629
Jan
Y. N.
,
Jan
L. Y.
(
1995
)
Maggot's hair and bug's eye: role of cell interactions and intrinsic factors in cell fate specification.
Neuron
14
,
1
5
Jones
B. W.
,
Fetter
R. D.
,
Tear
G.
,
Goodman
C. S.
(
1995
)
glial cells missing: a genetic switch that controls glial vs. neural fate.
Cell
82
,
1013
1023
Kauffmann
R. C.
,
Gallagher
P. A.
,
Zhang
J.
,
Carthew
R. W.
(
1996
)
Ras1 signaling and transcriptional competence in the R7 cell of Drosophila.
Genes Dev
10
,
2167
2178
Knoblich
J. A.
,
Jan
L. Y.
,
Jan
Y. N.
(
1995
)
Asymmetric segregation of Numb and Prospero during cell division.
Nature
377
,
624
627
Leviten
M.W.
,
Posakony
J.W.
(
1996
)
Gain-of-function alleles of Bearded interfere with alternative cell fate decisions in Drosophila adult sensory organ development.
Dev. Biol
176
,
264
283
Li
S.
,
Li
Y.
,
Carthew
R.
,
Lai
Z.
(
1997
)
Photoreceptor cell differentiation requires regulated proteolysis of the transcriptional repressor Tramtrack.
Cell
90
,
469
478
Mahadevan
L.
,
Willis
A.
,
Barratt
M.
(
1991
)
Rapid histone H3 phosphorylation in response to growth factors, phorbol esters, okadaic acid, and protein synthesis inhibitors.
Cell
65
,
775
783
Nakamura
M.
,
Okano
H.
,
Blendy
J.
,
Montell
C.
(
1994
)
Musashi, a neural RNA-binding protein required for Drosophila adult external sensory organ development.
Neuron
13
,
67
81
Posakony
J. W.
(
1994
)
Nature versus nurture: asymmetric cell divisions in Drosophila bristle development.
Cell
76
,
415
418
Reddy
G. V.
,
Rodrigues
V.
(
1999
)
Clonal analysis of Prospero function in adult mechanosensory lineage and its regulation by Numb and Notch.
Development,
126
,
2083
2092
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
Shen
C.-P.
,
Jan
L. Y.
,
Jan
Y. N.
(
1997
)
Miranda is required for the asymmetric localization of Prospero during mitosis in Drosophila.
Cell
90
,
449
458
Shiomi
K.
,
Takeichi
M.
,
Nishida
Y.
,
Nishi
Y.
,
Uemura
T.
(
1994
)
Alternative cell fate choice induced by low-level expression of a regulator of protein phosphatase 2A in the Drosophila peripheral nervous system.
Development
120
,
1591
1599
Skeath
J.
,
Doe
C.
(
1998
)
Sanpodo and Notch act in opposition to Numb to distinguish sibling neuron fates in the Drosophila CNS.
Development
125
,
1857
1865
Spana
E.
,
Doe
C. Q.
(
1995
)
The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila.
Development
121
,
3187
3195
Spana
E. P.
,
Doe
C. Q.
(
1996
)
Numb antagonizes Notch signaling to specify sibling neuron cell fates.
Neuron
17
,
21
26
Spana
E. P.
,
Kopczynski
C.
,
Goodman
C. S.
,
Doe
C. Q.
(
1995
)
Asymmetric localization of numb autonomously determines sibling neuron identity in the Drosophila CNS.
Development
121
,
3489
3494
Tang
A.
,
Neufeld
T.
,
Kwan
E.
,
Rubin
G.
(
1997
)
PHYL acts to down-regulate TTK88, a transcriptional repressor of neuronal cell fates, by a SINA-dependent mechanism.
Cell
90
,
459
467
Uemura
T.
,
Sheperd
S.
,
Ackerman
L.
,
Jan
L. Y.
,
Jan
Y. N.
(
1989
)
numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos.
Cell
58
,
349
360
Vaessin
H.
,
Grell
E.
,
Wolff
E.
,
Bier
E.
,
Jan
L. Y.
,
Jan
Y. N.
(
1991
)
prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila.
Cell
67
,
941
953
Wang
S.
,
Younger-Shepherd
S.
,
Jan
L. Y.
,
Jan
Y. N.
(
1997
)
Only a subset of the binary cell fate decisions mediated by Numb/Notch signaling in Drosophila sensory organ lineage requires suppressor of hairless.
Development
124
,
4435
4446
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