The trithorax group gene brahma (brm) encodes the ATPase subunit of a chromatin-remodeling complex involved in homeotic gene regulation. We report here that brm interacts with another trithorax group gene, osa, to regulate the expression of the Antennapedia P2 promoter. Regulation of Antennapedia by BRM and OSA proteins requires sequences 5′ to the P2 promoter. Loss of maternal osa function causes severe segmentation defects, indicating that the function of osa is not limited to homeotic gene regulation. The OSA protein contains an ARID domain, a DNA-binding domain also present in the yeast SWI1 and Drosophila DRI proteins. We propose that the OSA protein may target the BRM complex to Antennapedia and other regulated genes.

Aasland
R.
,
Stewart
A. F.
,
Gibson
T. J.
(
1996
)
The SANT domain: a putative DNA binding domain in the SWI/SNF and ADA complexes, the transcriptional co-repressor N-CoR and TFIIIB.
Trends Biochem. Sci
21
,
87
88
Altschul
S. F.
,
Madden
T. L.
,
Schaffer
A. A.
,
Zhang
J.
,
Zhang
Z.
,
Miller
W.
,
Lipman
D. J.
(
1997
)
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
Nucleic Acids Res
25
,
3389
3402
Bienz
M.
,
Saari
G.
,
Tremml
G.
,
Muller
J.
,
Zust
B.
,
Lawrence
P. A.
(
1988
)
Differential regulation of Ultrabithorax in two germ layers of Drosophila.
Cell
53
,
567
576
Bode
J.
,
Stengert-Iber
M.
,
Kay
V.
,
Schlake
T.
,
Dietz-Pfeilstetter
A.
(
1996
)
Scaffold/matrix-attached regions: topological switches with multiple regulatory functions.
Crit. Rev. Eukaryot. Gene Expr
6
,
115
138
Boulet
A.
,
Scott
M. P.
(
1988
)
Control elements of the P2 promoter of the Antennapedia gene.
Genes Dev
2
,
1600
1614
Brizuela
B. J.
,
Elfring
L.
,
Ballard
J.
,
Tamkun
J. W.
,
Kennison
J. A.
(
1994
)
Genetic analysis of the brahma gene of Drosophilamelanogaster and polytene chromosome subdivisions 72AB.
Genetics
137
,
803
813
Brizuela
B. J.
,
Kennison
J. A.
(
1997
)
The Drosophila homeotic gene moira regulates expression of engrailed and HOM genes in imaginal tissues.
Mech. Dev
65
,
209
220
Burns
G. L.
,
Peterson
C. L.
(
1997
)
The yeast SWI-SNF complex facilitates binding of a transcriptional activator to nucleosomal sites in vivo.
Mol. Cell. Biol
17
,
4811
4819
Cairns
B. R.
,
Kim
Y.-J.
,
Sayer
M. H.
,
Laurent
B. C.
,
Kornberg
R. D.
(
1994
)
A multisubunit complex containing the SWI1/ADR6, SWI2/SNF2, SWI3, SNF5, and SNF6 gene products isolated from yeast.
Proc. Natl. Acad. Sci.USA
91
,
1950
1954
Cairns
B. R.
,
Levinson
R. S.
,
Yamamoto
K. R.
,
Kornberg
R. D.
(
1996
)
Essential role of Swp73p in the function of yeast Swi/Snf complex.
Genes Dev
10
,
2131
2144
Cairns
B. R.
,
Henry
L. N.
,
Kornberg
R. D.
(
1996
)
TFG3/TAF30/ANC1, a component of the yeast SWI/SNF complex that is similar to the leukemogenic proteins ENL and AF-9.
Mol. Cell. Biol
16
,
3308
3316
Carlson
M.
,
Laurent
B. C.
(
1994
)
The SNF/SWI family of global transcriptional activators.
Curr. Opin. Cell. Biol
6
,
396
402
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
Côte
J.
,
Quinn
J.
,
Workman
J. L.
,
Peterson
C. L.
(
1994
)
Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex.
Science
265
,
53
60
Dallas
P. B.
,
Cheney
I. W.
,
Liao
D.
,
Bowrin
V.
,
Byam
W.
,
Pacchione
S.
,
Kobayashi
R.
,
Yaciuk
P.
,
Moran
E.
(
1998
)
p300/CREB binding protein-related protein p270 is a component of mammalian SWI/SNF complexes.
Mol. Cell. Biol
18
,
3596
3603
Desplan
D.
,
Theis
J.
,
O'Farrell
P. H.
(
1988
)
The sequence specificity of homeodomain-DNA interaction.
Cell
54
,
1081
1090
Dingwall
A. K.
,
Beek
S. J.
,
McCallum
C. M.
,
Tamkun
J. W.
,
Kalpana
G. V.
,
Goff
S. P.
,
Scott
M. P.
(
1995
)
The Drosophila snr1 and Brm proteins are related to yeast SWI/SNF proteins and are components of a large protein complex.
Mol. Biol. Cell
6
,
777
791
Duncan
I. M.
(
1987
)
The bithorax complex.
Annu. Rev. Genet
21
,
285
319
Elfring
L.
,
Daniel
C.
,
Papoulas
O.
,
Deuring
R.
,
Sarte
M.
,
Moseley
S.
,
Beek
S.
,
Waldrip
R.
,
Daubresse
G.
,
DePace
A.
,
Kennison
J.
,
Tamkun
J.
(
1998
)
Genetic analysis of brahma: the Drosophila homolog of the yeast chromatin remodeling factor SWI2/SNF2.
Genetics
148
,
251
265
Frischer
L. E.
,
Hagen
F. S.
,
Garber
R. L.
(
1986
)
An inversion that disrupts the Antennapedia gene causes abnormal structure and localization of RNAs.
Cell
47
,
1017
1023
Gaudreau
L.
,
Schmid
A.
,
Blaschke
D.
,
Ptashne
M.
,
Hörz
W.
(
1997
)
RNA polymerase II holoenzyme recruitment is sufficient to remodel chromatin at the yeast PHO5 promoter.
Cell
89
,
55
62
Gibson
G.
,
Gehring
W. J.
(
1988
)
Head and thoracic transformations caused by ectopic expression of Antennapedia during Drosophila development.
Development
102
,
657
675
Golic
K. G.
,
Lindquist
S.
(
1989
)
The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome.
Cell
59
,
499
509
Gregory
S. L.
,
Kortschak
R. D.
,
Kalionis
B.
,
Saint
R.
(
1996
)
Characterization of the dead ringer gene identifies a novel, highly conserved family of sequence-specific DNA-binding proteins.
Mol. Cell. Biol
16
,
792
799
Heery
D. M.
,
Kalkhoven
E.
,
Hoare
S.
,
Parker
M. G.
(
1997
)
A signature motif in transcriptional co-activators mediates binding to nuclear receptors.
Nature
387
,
733
736
Herrscher
R. F.
,
Kaplan
M. H.
,
Lelsz
D. L.
,
Das
C.
,
Scheuermann
R.
,
Tucker
P. W.
(
1995
)
The immunoglobulin heavy-chain matrix-associating regions are bound by Bright: a B cell-specific trans-activator that describes a new DNA-binding protein family.
Genes Dev
9
,
3067
3082
Hopmann
R.
,
Duncan
D.
,
Duncan
I.
(
1995
)
Transvection in the iab-5,6,7 region of the bithorax complex of Drosophila: homology independent interactions in trans.
Genetics
139
,
815
833
Ingham
P. W.
(
1983
)
Differential expression of bithorax complex genes in the absence of the extra sex combs and trithorax genes.
Nature
306
,
591
593
Ingham
P. W.
(
1985
)
A clonal analysis of the requirement for the trithorax gene in the diversification of segments in Drosophila.
J. Embryol. exp. Morph
89
,
349
365
Ingham
P. W.
,
Martínez Arias
A.
(
1992
)
Boundaries and fields in early embryos.
Cell
68
,
221
235
Jenuwein
T.
,
Forrester
W. C.
,
Fernández-Herrero
L. A.
,
Laible
G.
,
Dull
M.
,
Grosschedl
R.
(
1997
)
Extension of chromatin accessibility by nuclear matrix attachment regions.
Nature
385
,
269
272
Jorgensen
E. M.
,
Garber
R. L.
(
1987
)
Function and misfunction of the two promoters of the DrosophilaAntennapedia gene.
Genes Dev
1
,
544
555
Kalionis
B.
,
O'Farrell
P. H.
(
1993
)
A universal target sequence is bound in vitro by diverse homeodomains.
Mech. Dev
43
,
57
70
Karpen
G. H.
,
Spradling
A. C.
(
1992
)
Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P element insertional mutagenesis.
Genetics
132
,
737
753
Kaufman
T. C.
,
Seeger
M. A.
,
Olsen
G.
(
1990
)
Molecular and genetic organization of the Antennapedia gene complex of Drosophila melanogaster.
Adv. Genet
27
,
309
362
Kennison
J. A.
(
1993
)
Transcriptional activation of Drosophila homeotic genes from distant regulatory elements.
Trends Genet
9
,
75
79
Kennison
J. A.
(
1995
)
The Polycomb and trithorax group proteins of Drosophila: trans-regulators of homeotic gene function.
Ann. Rev. Genet
29
,
289
303
Kennison
J. A.
,
Tamkun
J. W.
(
1988
)
Dosage-dependent modifiers of Polycomb and Antennapedia mutations in Drosophila.
Proc. Natl. Acad. Sci. USA
85
,
8136
8140
Laurent
B. C.
,
Carlson
M.
(
1992
)
Yeast SNF2/SWI2, SNF5, and SNF6 proteins function coordinately with the gene-specific transcriptional activators GAL4 and Bicoid.
Genes Dev
6
,
1707
1715
Logie
C.
,
Peterson
C. L.
(
1997
)
Catalytic activity of the yeast SWI/SNF complex on reconstituted nucleosome arrays.
EMBO J
16
,
6772
6782
O'Hara
P. J.
,
Horowitz
H.
,
Eichinger
G.
,
Young
E. T.
(
1988
)
The yeast ADR6 gene encodes homopolymeric amino acid sequences and a potential metal-binding domain.
Nucl. Acids Res
16
,
10153
10169
Ostlund-Farrants
A. K.
,
Blomquist
P.
,
Kwon
H.
,
Wrange
O.
(
1997
)
Glucocorticoid receptor-glucocorticoid response element binding stimulates nucleosome disruption by the SWI/SNF complex.
Mol. Cell. Biol
17
,
895
905
Peterson
C. L.
,
Dingwall
A.
,
Scott
M. P.
(
1994
)
Five SWI/SNF gene products are components of a large multisubunit required for transcriptional enhancement.
Proc. Natl. Acad. Sci.USA
91
,
2905
2908
Poole
S.
,
Kauvar
L. M.
,
Drees
B.
,
Kornberg
T.
(
1985
)
The engrailed locus of Drosophila: structural anlysis of an embryonic transcript.
Cell
40
,
37
43
Quinn
J.
,
Fryberg
A. M.
,
Ganster
R. W.
,
Schmidt
M. C.
,
Peterson
C. L.
(
1996
)
DNA-binding properties of the yeast SWI/SNF complex.
Nature
379
,
844
847
Schneuwly
S.
,
Kuroiwa
A.
,
Gehring
W. J.
(
1987
)
Molecular analysis of the dominant homeotic Antennapedia phenotype.
EMBO J
6
,
201
206
Schneuwly
S.
,
Klemenz
R.
,
Gehring
W. J.
(
1987
)
Redesigning the body plan of Drosophila by ectopic expression of the homeotic gene Antennapedia.
Nature
325
,
816
818
Scott
M. P.
,
Weiner
A. J.
,
Hazelrigg
T. I.
,
Polisky
B. A.
,
Pirrotta
V.
,
Scalenghe
F.
,
Kaufman
T. C.
(
1983
)
The molecular organization of the Antennapedia locus of Drosophila.
Cell
35
,
763
776
Simon
J.
(
1995
)
Locking in stable states of gene expression: transcriptional control during Drosophila development.
Curr. Opin. Cell. Biol
7
,
376
385
Spradling
A. C.
,
Stern
D. M.
,
Kiss
I.
,
Roote
J.
,
Laverty
T.
,
Rubin
G. M.
(
1995
)
Gene disruptions using P transposable elements: An integral component of the Drosophila genome project.
Proc. Natl. Acad. Sci.USA
92
,
10824
10830
Talbert
P. B.
,
Garber
R. L.
(
1994
)
The Drosophila homeotic mutation Nasobemia (AntpNs) and its revertants: and analysis of mutational reversion.
Genetics
138
,
709
720
Tamkun
J. W.
,
Deuring
R.
,
Scott
M. P.
,
Kissinger
M.
,
Pattatuci
A. M.
,
Kaufman
T. C.
,
Kennison
J. A.
(
1992
)
brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2.
Cell
68
,
561
572
Treich
I.
,
Cairns
B. R.
,
de los Santos
T.
,
Brewster
E. M.
,
Carlson
M.
(
1995
)
SNF11, a new component of the yeast SNF-SWI complex that interacts with a conserved region of SNF2.
Mol. Cell. Biol
15
,
4240
4248
Treisman
J. E.
,
Luk
A.
,
Rubin
G. M.
,
Heberlein
U.
(
1997
)
eyelid antagonizes wingless signaling during Drosophila development and has homology to the Bright family of DNA-binding proteins.
Genes Dev
11
,
1949
1962
Tripoulas
N. A.
,
Hersperger
E.
,
LaJeunesse
D.
,
Shearn
A.
(
1994
)
Molecular genetic analysis of the Drosophila melanogaster gene absent, small or homeotic discs 1 (ash1).
Genetics
137
,
1027
1038
Tripoulas
N. A.
,
LaJeunesse
D.
,
Gildea
J.
,
Shearn
A.
(
1996
)
The Drosophilaash1 gene product, which is localized at specific sites on polytene chromosomes, contains a SET domain and a PHD finger.
Genetics
143
,
913
928
Utley
R. T.
,
Côte
J.
,
Owen-Hughes
T.
,
Workman
J. L.
(
1997
)
SWI/SNF stimulates the formation of disparate activator-nucleosome complexes but is partially redundant with cooperative binding.
J. Biol. Chem
272
,
12642
12649
Winston
F.
,
Carlson
M.
(
1992
)
Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection.
Trends Genet
8
,
387
391
Yoshinaga
S. K.
,
Peterson
C. L.
,
Herskowitz
I.
,
Yamamoto
K. R.
(
1992
)
Roles of SWI1, SWI2, and SWI3 proteins for transcriptional enhancement by steroid receptors.
Science
258
,
1598
1604
This content is only available via PDF.