puckered (puc) encodes a VH1-like phosphatase that down-regulates Jun kinase (JNK) activity during dorsal closure of the Drosophila embryo. We report a role for puc in follicle cell morphogenesis during oogenesis. puc mRNA accumulates preferentially in the centripetally migrating follicle cells and cells of the elongating dorsal appendages. Proper levels of Puc activity in the follicle cells are critical for the production of a normal egg: either reduced or increased Puc activity result in incomplete nurse cell dumping and aberrant dorsal appendages. Phenotypes associated with puc mutant follicle cells include altered DE-cadherin expression in the follicle cells and a failure of nurse cell dumping to coordinate with dorsal appendage elongation, leading to the formation of cup-shaped egg chambers. The JNK pathway target A251-lacZ showed cell-type-specific differences in its regulation by puc and by the small GTPase DRac1. puc mutant cells displayed region-specific ectopic expression of the A251-lacZ enhancer trap whereas overexpression of a transgene encoding Puc was sufficient to suppress lacZ expression in a cell autonomous fashion. Strikingly, decreased or increased puc function leads to a corresponding increase or decrease, respectively, of Fos and Jun protein levels. Taken together, these data indicate that puc modulates gene expression responses by antagonizing a Ρ GTPase signal transduction pathway that stabilizes the AP-1 transcription factor. Consistent with this, overexpression of a dominant negative DRac1 resulted in lower levels of Fos/Jun.
Reference
Agnes
F.
, Suzanne
M.
, Noselli
S.
(1999
) The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis.
Development
126
, 5453
–5462
Canman
C.
, Kastan
M.
(1996
) Three paths to stress relief.
Nature
384
, 213
–214
Chen
R. H.
, Juo
P. C.
, Curran
T.
, Blenis
J.
(1996
) Phosphorylation of c-Fos at the C-termnus enhances its transforming activity.
Oncogene
12
, 1493
–1502
Chou
T.-B.
, Noll
E.
, Perrimon
N.
(1993
) Autosomal P[ovoD1] dominant female-sterile insertions in Drosophila and their use in generating germ-line chimeras.
Development
119
, 1359
–1369
Cooley
L.
, Verheyen
E.
, Ayers
K.
(1992
) chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis.
Cell
69
, 173
–184
Coso
O.
, Chiariello
A. M.
, Yu
J. C.
, Teramoto
H.
, Crespo
P.
, Xu
N.
, Miki
T.
, Gutkind
J. S.
(1995
) The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway.
Cell
81
, 1137
–1146
Dobens
L. L.
, Hsu
T.
, Twombley
V.
, Gelbart
W. M.
, Raftery
L. A.
, Kafatos
F. C.
(1997
) The Drosophilabunched gene is a homologue of the growth factor stimulated mammalian TSC-22 sequence and is required during oogenesis.
Mech. Dev
65
, 197
–208
Dobens
L. L.
, Raftery
L. A.
(2000
) Integration of epithelial patterning and morphogenesis in Drosophila ovarian follicle cells.
Developmental Dynamics
218
, 80
–93
Duffy
J.
, Harrison
D.
, Perrimon
N.
(1998
) Identifying loci required for follicular patterning using directed mosaics.
Development
125
, 2263
–2271
Eaton
S.
(1997
) Planar polarization of Drosophila and vertebrate epithelia.
Curr. Opin. Cell. Biol
9
, 860
–866
Edwards
K.
, Kiehart
D.
(1996
) Drosophila non-muscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis.
Development
122
, 1499
–1511
Emery
I. F.
, Bedian
V.
, Guild
G. M.
(1994
) Differential expression of Broad-Complex transcription factors may forecast tissue-specific developmental fates during Drosophila metamorphosis.
Development
120
, 3275
–3287
FlyBase Consortium
(1999
) The FlyBase Database of the Drosophila Genome Projects and community literature.
Nuc. Acid Res
27
, 85
–88
Genova
J. L.
, Jong
S.
, Camp
J. T.
, Fehon
R. G.
(2000
) Functional analysis of Dcdc42 in actin filament assembly, epithelial morphogenesis and cell signaling during Drosophila development.
Dev. Biol
221
, 181
–194
Glise
B.
, Bourbon
H.
, Noselli.
S.
(1995
) hemipterous encodes a novel Drosophila Map kinase kinase required for epithelial cell sheet movements.
Cell
83
, 451
–461
Glise
B.
, Noselli.
S.
(1997
) Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis.
Genes Dev
11
, 1738
–1747
González-Reyes
A.
, St. Johnston
D.
(1998
) Patterning of the follicle cell epithelium along the anterior-posterior axis during Drosophila oogenesis.
Development
125
, 2837
–2846
Grossniklaus
U.
, Bellen
H. J.
, Wilson
C.
, Gehring
W. J.
(1989
) P-element-mediated enhancer detection applied to the study of oogenesis in Drosophila.
Development
107
, 189
–200
Hall
A.
(1998
) Rho GTPases and the actin cytoskeleton.
Science
279
, 509
–514
Harden
N.
, Ricos
M.
, Ong
Y. M.
, Chia
W.
, Lim
L.
(1999
) Participation of small GTPases in dorsal closure of the Drosophila embryo: distinct roles for Rho subfamily proteins in epithelial morphogenesis.
J. Cell Sci
112
, 273
–84
Hou
X. S.
, Goldstein
E. S.
, Perrimon
N.
(1997
) Drosophila Jun relays the Jun amino-terminal kinase signal transduction pathway to the Decapentaplegic signal transduction pathway in regulating epithelial sheet movement.
Genes Dev
11
, 1728
–1737
Keyse
S. M.
(2000
) Protein phosphatases and the regulation of mitogen activated protein kinase signalling.
Curr. Op. Cell Biol
12
, 186
–192
Khosravi
F. R.
, Solski
P. A.
, Clark
G. J.
, Kinch
M. S.
, Der
C. J.
(1995
) Activation of Rac1, RhoA, and mitogen-activated protein-kinases is required for Ras transformation.
Mol. Cell. Biol
15
, 6443
–6453
Lee
J. K.
, Brandin
E.
, Branton
D.
, Goldstein
L. S. B.
(1997
) -spectrin is required for ovarian follicle monolayer integrity in Drosophila melanogaster.
Development
124
, 353
–362
Lu
Y.
, Settleman
J.
(1999
) The Drosophila PKN protein kinase is a Rho/Rac effector target required for dorsal closure during embryogenesis.
Genes Dev
13
, 1168
–1180
Luo
L.
, Liao
Y.
, Jan
L.
, Jan
Y.
(1994
) Distinct morphogenetic functions of similar small GTPases: DrosophilaDrac1 is involved in axonal outgrowth and myoblast fusion.
Genes Dev
8
, 1787
–1802
Martín-Blanco
E.
(1997
) Regulation of cell differentiation by the Drosophila Jun kinase cascade.
Curr. Op. Genet. Dev
7
, 666
–671
Martín-Blanco
E.
, Gampel
A.
, Ring
J.
, Virdee
K.
, Kirov
N.
, Tolkovsky
A.
, Martinez-Arias
A.
(1998
) puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure.
Genes Dev
12
, 557
–570
McEwen
D. G.
, Cox
R. T.
, Peifer
M.
(2000
) The canonical Wg and JNK signaling cascades collaborate to promote both dorsal closure and ventral patterning.
Development
127
, 3607
–3617
Minden
A.
, Lin
A.
, Claret
F. X.
, Abo
A.
, Karin
M.
(1995
) Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPase Rac and Cdc42Hs.
Cell
81
, 1147
–1157
Murphy
A.
, Montell
D.
(1996
) Cell type-specific roles for Cdc42, Rac, and RhoL in Drosophila oogenesis.
J. Cell Biol
133
, 617
–630
Musti
A. M.
, Trier
M.
, Bohmann
D.
(1997
) Reduced ubiquitin-dependent degradation of c-Jun after phosphorylation by MAP kinases.
Science
275
, 400
–402
Noselli
S.
(1998
) JNK signaling and morphogenesis in Drosophila.
Trends Genet
14
, 33
–38
Noselli
S.
, Agnes
F.
(1999
) Roles of the JNK signaling pathway in Drosophila morphogenesis.
Curr. Op. Gen. Dev
9
, 466
–472
Okazaki
K.
, Sagata
N.
(1995
) The Mos/MAP kinase pathway stablizes c-Fos by phosphorylation and augments its transforming activity in NIH 3T3 cells.
EMBO J
14
, 5048
–5059
Pesacreta
T.
, Byers
T.
, Dubrueil
R.
, Kiehart
D.
, Branton
D.
(1989
) Drosophila spectrin: the membrane skeleton during embryogenesis.
J. Cell. Biol
108
, 1697
–1709
Peverali
F. A.
, Isaksson
A.
, Papavassiliou
A. A.
, Plastina
P.
, Staszewski
L. M.
, Mlodzik
M.
, Bohmann
D.
(1996
) Phosphorylation of Drosophila Jun by the MAP kinase rolled regulates photoreceptor differentiation.
EMBO J
15
, 3943
–3950
Pignoni
F.
, Zipursky
S. L.
(1997
) Induction of Drosophila eye development by Decapentaplegic.
Development
124
, 271
–278
Qiu
R. G.
, Abo
A.
, McCormick
F.
, Symons
M.
(1997
) Cdc42 regulates anchorage-independent growth and is necessary for Ras transformation.
Mol. Cell Biol
17
, 3449
–3458
Qiu
R. G.
, Chen
J.
, Kirn
D.
, McCormick
F.
, Symons
M.
(1995
) An essential role for Rac in Ras transformation.
Nature
374
, 457
–459
Qiu
R. G.
, Chen
J.
, McCormick
F.
, Symons
M.
(1995
) A role for Rho in Ras transformation.
Proc. Natl. Acad. Sci. USA
92
, 11781
–11785
Ricos
M. G.
, Harde
N.
, Sem
K. P.
, Lin
L.
, Chia
W.
(1999
) Dcdc42 acts in TGF-signaling during Drosophila morphogenesis: distinct roles for Drac1/JNK and Dcdc42/TGK- cascades in cytoskeletal regulation.
J. Cell Sci
112
, 1225
–1235
Riesgo-Escovar
J. R.
, Hafen
E.
(1997
) Common and distinct roles of DFos and DJun during Drosophila development.
Science
278
, 669
–672
Riesgo-Escovar
J. R.
, Hafen
E.
(1997
) Drosophila Jun kinase regulates expression of decapentaplegic via the ETS-domain protein Aop and the AP-1 transcription factor DJun during dorsal closure.
Genes Dev
11
, 1717
–1727
Robinson
D. N.
, Cooley
L.
(1997
) Genetic analysis of the actincytoskeleton in the Drosophila ovary.
Annu. Rev. Cell. Dev. Biol
13
, 147
–170
Schupbach
T.
, Wieschaus
E.
(1989
) Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations.
Genetics
121
, 101
–117
Teramoto
H.
, Crespo
P.
, Coso
O. A.
, Igishi
T.
, Xu
N.
, Gutkind
J. S.
(1996
) The small GTP-binding protein rho activates c-Jun N-terminal kinase/stress-activated protein kinases in human kidney 293T cells. Evidence for a Pak-independent signaling pathway.
J. Biol. Chem
271
, 25731
–25734
van Aelst
L.
, D'Souza-Schorey
C.
(1997
) Rho GTPases and signaling networks.
Genes Dev
11
, 2295
–2322
Wasserman
J.
, Freeman
M.
(1998
) An autoregulatory cascade of EGF receptor signaling patterns the Drosophila egg.
Cell
95
, 355
–364
Xu
T.
, Rubin
G. M.
(1993
) Analysis of genetic mosaics in developing and adult Drosophila tissues.
Development
117
, 1223
–1237
Young
P.
, Richman
A.
, Ketchum
A.
, Kiehart
D.
(1993
) Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function.
Genes Dev
7
, 29
–41
Zeitlinger
J.
, Kockel
L.
, Peverali
F. A.
, Jackson
D. B.
, Mlodzik
M.
, Bohmann
D.
(1997
) Defective dorsal closure and loss of epidermal decapentaplegic expression in Drosophilafos mutants.
EMBO J
16
, 7393
–7401
This content is only available via PDF.
© 2001 by Company of Biologists
2001
-JournalMeeting.png?versionId=3737)
(update)-ImmuneSI.png?versionId=3737)
-GSWorkshop.png?versionId=3737)
(update)-InPreprints.png?versionId=3737)
-FocalPlaneNetworkLaunch.png?versionId=3737)
