- Email: [email protected]
A ran-binding motif in nuclear pore proteins
A Ran-binding motif in nuclear pore proteins The small CTP-binding
protein
is essential for the second
present in other proteins,
step: translocation through the pore7s8. This suggests a direct
including NPC proteins. These
interaction between Ran and
proteins are: (1) the Saccharomyces cerevisiae nuclear pore protein
nuclear pore proteins at some stage of nuclear protein
(2) a 5. cerevisiae protein
Nup2p (ACC X69964;
Ref. 15),
related to Nup2p (ACC Z38060),
import.
which displays the highest
A 27 kDa Ran-binding protein
expression library by probing with
homology to Nup2p within the rbpl motif, (3) a human sequence tag (ACC M79174; Ref. 16) that is
(RanBPl) specific for Ran-GTP has been identified from a mouse Ran loaded with labelled CTP13. In a
particularly closely related to the
separate study using the same technique, proteins of 28, 86, 100
sequence, (4) the Caenorhabditis
and 6 for reviews). In particular, it is
and 200-300
elegans
a key component
The 28 kDa protein is cytosolic and
Ran/TC4 has been implicated number of different nuclear functions (Refs l-4;
in a
see Refs 5
in nuclear
transport7,*. Proteins are imported into the nucleus through the nuclear pores in an active two-step process9,10 that requires soluble factors’
l. The first step is the
NLS-dependent
5. cerevisioe NupZp-related
kDa were detected14.
probably corresponds to RanBPl ; the others were found in the highsalt/Triton-soluble nuclear fraction,
By comparing
the recently identified S. cerevisiae homologue of RanBPl (ACC 233503; Ref. 18), which shares
which also includes nuclear pore proteins.
binding of the
protein encoded by the
open reading frame (ORF) F59A2.1 (ACC 234801; Ref. 17), which contains two rbpl motifs, and (5)
40% identity with the mouse
sequences in the
protein and shows 64% identity
import substrate to the cytoplasmic side of the nuclear pore complex
CenBank database, we have identified an approximately 75
(NPC). Recently, a 60 kDa
amino acid domain in mouse
within the rbpl motif. As the rbpl motif is the most highly conserved
protein - ‘importin’ -was found to be required for this step12. Ran
RanBPl (ACC L25255), referred to here as the rbpl motif, that is also
domain in RanBPl, it seems likely that it mediates its interaction with Ran. In turn one might conclude that proteins containing the rbpl
Mouse RanBPl
motif bind Ran in its CTP-bound form. The presence of Ran-binding
Yeast RanBPl horn
interest, because it suggests Nup2p
motifs in Nup2p is of particular might serve to integrate the functions of two soluble factors that are essential for nuclear protein Yeast Nup2p-rel
import in the vertebrate system: namely Ran and importin. Nup2p has been shown to interact genetically and physically19 with
Human HHCP045
Srpl p (Ref. 20), the yeast homologue of importin12. The presence of the rbpl motif in Nup2p now suggests that it also
Nematode F59A2.1
interacts with Ran. The observation that Nup2p is essential only in certain genetic backgrounds15
Yeast Nup2p
indicates that such a central function is backed up by more than FIGURE 1 Proteins that contain the rbpl motif: schematic presentation of RanBPl -related proteins found in the GenBank database (release BS+) using the TBLASTN program26 of the NCBI e-mail server. Darkly shaded boxes indicate rbpl motifs; the striped box represents the Nupl53p-like
zinc-finger domains; and the lightly
shaded boxes indicate regions of XFXFC-like repeats. Mouse RanBPl is the mouse Ran-binding protein 1 (ACC L25255); yeast RanBPl horn is the 5. cerevisiaeRanBPl homologue SCHTNl (ACC X65925); yeast NupZp-rel is the NupZp-related protein encoded by an ORF in the 5. cerevisiae DNA sequence SC561 0 (ACC 238060); human HHCP045
is a partial sequence from the human clone HHCP045
(ACC M79174); yeast Nup2p is from 5. cerevisiae (ACC X69964); nematode F59A2.1 is encoded by the C. elegans ORF F59A2.1 (ACC 234801).
cDNA
sequences coding for proteins that contain at least parts of the rbpl motif were also found in rice (ACC D22992, ACC D39320, ACC D15902) and Arabidopsis thaliana
192
(ACC 234627, ACC T22134).
one gene product. The C. elegans F59A2.1 protein not only contains two potential Ran-binding sites but also has two additional remarkable characteristics: like the nuclear pore protein Nupl53p
it has a conserved
domain that includes zinc finger motifs; and it contains 13 hydrophobic pentapeptide repeats, which resemble the XFXFC motif found in several nuclear pore proteins, such as Nupl p, NupZp, Nspl p, ~62, POMl21, rat INMACIA and also Nupl53p review). Nupl53p
(see Ref. 21 for a is a DNA-binding
TRENDS IN CELL BIOLOGY VOL. 5 MAY 1995
Mouse RanBPl
36
QEIKTLEEDEEELFKMRAKLFRFASENDLPEWKERGTGDVKLLK--HKEKG--TIRLLMRRDKTLKICANHYIT~~LK~
112
Yeast RanBPl horn
74
VDVKTMEEDEEVLYKVRAKLFRF--DADAKEWKERGTGDCKFLKN-KKTN---KVRILMRRDKTLKICANHIIAPRYTLKP
148
Yeast NupZp
597
INLQNGEEDEVALFSQKAKLTF--NAETKSYDSRGVGEMKLLK--KKDDPS-KVRLLCRSDGMGNVLLNATVVDSFKYRP
672
Nematode
F59A2.1_N
258
~EVKTGEEGEQTMFCNRSKLYIY--ANETKEWKERGTGELKVLY--NKDKK--SWRVVMRRDQVLKVCANFPILGSMTIQQ
332
Nematode
F59A2.1_C
729
~EVKTGEEDEEVMFSARCKLYKY--YSDLKENKERGLGDIKLLK--SNDN---KYRIVMRREQVHKLCANFRIEKSMRLSP
802
203
QEVKSGEESEECIYQVNAKLYQL--SNIKEGWKERGVGIIKINK--SKDDVE-KTRIVMRSRGILKVILNIQLVKGFTVQK
278
VEVITGRRAESNVLQMQCKLFVF--DKTSQSWVERGRGLLRLNDMASTDDGTLQSRLVMRTQGSLRLILNTKLWAQMQIDK
81
Yeast Nup2p-rel
3
Human HHCP045
Consensus
vevktgEEdEe..f..raKL..f--....kewkeRG.G Y
c
lk.caN..i...m...p
..kllk--.kd----k.R.lmRrd.. rn
fY Y
lf
il
IV i v
FIGURE 2 The rbpl motif: rbpl motifs are shown aligned in single-letter code. The protein sequences were aligned by using the MACAW program. Sequence names are explained in the legend to Fig. 1. F59A2.1_N and F59A2.1_C are the N-terminal and C-terminal rbpl motifs, respectively, in the F59A2.1 protein from C. elegans. A consensus rbpl motif was calculated from the shown sequences. Amino acids that are conserved in all sequences are shown in the consensus
as capital
letters.
Lower-case
letters
in the
upper
line indicate
conservation
in more
than
50%
of the
sequences. Similar amino acids in one position are shown in the lower lines. protein
exclusively
nucleoplasmic
found
4
on the
and is therefore implicated
5 6
motifs, nucleoporin-like
7 8
9 10
BLOBEL, G. (1993)
23
SUKEGAWA,
Cuff.
1. and BLOBEL, C. (1993)
GRUNDMANN,
U., NERLICH,
LOTTSPEICH, 1. Cell Biol. 123,
(1988) 24
659
C., REIN, T.,
F. and KUEPPER, H. A.
Nucleic Acids Res. 16, 4721
MOORE,
M. S. and
BLOBEL, G. (1994)
Proc. Nat/ Acad. Sci. USA 91, 10212-l
NEWMEYER,
D. D. and FORBES, D. J.
25
OHTSUBO,
26
ALTSCHUL,
Cell 52,641-653
RICHARDSON,
M. et al. (1987)
0216
Genes Dev. 1,
585-589
W. D., MILLS, A. D., 5. M., LASKEY, R. A.
ADAM,
C. (1988)
S. F., GISH, W., MILLER, W.,
MYERS, E. M. and LIPMAN,
Cell 52,
5. A., STERNE-MARR,
CORLICH,
D. 1. (1990)
/. Mol. Biol. 215, 403-410
Enno Hartmann
R. and
/. Cell Biol. 111,
Max-Delbriick-Centrum
D., PREHN, S., LASKEY, R. A.
and HARTMANN,
E. (1994)
Cell 79,
767-778 13
translocation step of nuclear
FABRE, E. and HURT, E. C. (1994)
Cell 72, 29-38
807-816 12
cytosolic protein that binds to and cooperates with Ran in the
COUTAVAS,
1. D., D’EUSTACHIO,
and RUSH, M. (1993)
factor
Medizin, Berlin,
ftir Molekulare
Robert-Rdssle-Str.
10, 13125
Acknowledgements
Germany.
We thank
P.
Nature 366,
Wellcome/CRC
constructive
Institute,
Road, Cambridge,
UK
Tennis
Court
comments
CB2 1 QR.
14
LOUNSBURY, MACARA,
whether a consensus for those proteins can also be found.
11285-l
A. L. and
/. Biol. Chem. 269,
1290
15
LOEB, D. 1. D., DAVIS, L. I. and FINK, C.
16
ADAMS,
References
R. (1993)
DRIVAS, G. T., SHIH, A.,
K. M., BEDDOWS,
I. C. (1994)
E., RUSH, M. G. and
Mol. Biol. Cell. 4, 209-222 M. D. et al. (1992)
Nature 355,
632-634
Mol. Cell. Biol.
WILSON,
R. et a/. (1994)
Nature
368,
NOTE ADDED IN PROOF
supported
Similarfindings to those detailed in this
Deutsche
letter have been described Dingwall mun.).
by Colin
and colleagues (pers. comAfter
this
manuscript
finished,
further
the rbpl
motif were reported.
was
proteins containing These
Forschungsgemeinthe Cancer Research Campaign
32-38
are RBPX [BISCHOFF, F.R., KREBBER,H.,
(SP1961)
BUTLER, C. and WOLFE, K. H. (1994)
SMIRNOVA,
E.,
and
long-term
(1991) Proc. Not/ Acod. SC;. USA 88,
Biochem. Biophys. Acta 1219,
PONSTINCL,
H. (1995)
EM80 /. 14,
fellowship
10830-l
711-712
705-7151
and RUSH, M. C. (1993)
P.
/. Cell Viol. 120,
619-630
313-323
TRENDS IN CELL BIOLOGY
BELANGER, K. D., KENNA, and DAVIS, L. I. (1994)
VOL. 5 MAY 1995
M. A., WEI, 5.
/. Cell B/o/. 126,
accession U10248 Nat/ Acad.
DONC,
W.
and two proteins with the numbers [BEDDOW,
U19240
and
A.L. et al. Proc.
Sci. USA (in press)]
by the
schaft (SFB366),
10, 1793-l 798
REN, M., DRIVAS, C., D’EUSTACHIO,
This
work was
BISCHOFF, F. R. and PONSTINCL, H. 0834
on the
manuscript.
585-587
RCCl (Ref. 25), contains this motif. It remains to be seen
Ron
Laskey for
Dirk GiWlich
E., REN, M.,
OPPENHEIM,
protein import24, nor the Ran
3
22
F., PASCHAL, B., EVANS, E.
GERACE, L. (1990)
mediates interaction with Ran. For example, neither PP15 (Ref. 23), a
P. (1990)
21
655-664
unlikely to be the only one that
2
MELCHIOR,
and DINGWALL, 11
It is also clear that this motif is
D’EUSTACHIO,
BLOBEL, C. (1994)
M. S. and
DILWORTH,
so far, it is likely
that more of these proteins will be found to contain the rbpl motif.
COUTAVAS,
M. 5. and
MOORE,
(1988)
As only a few nuclear pore proteins have been
1
MOORE,
1649-l
interactions.
M.,
M. (1992)
Opin. Cell Biol. 6, 335-342
and CERACE, L. (1993)
distinct from nuclear protein import, such as nuclear-pore-chromatin
guanine-nucleotide-exchange
Trends Biochem. SC;.
Nature 365, 661-663
(F59A2.1) suggests that it might mediate functions of Ran that are
J. A. and NOMURA,
Mol. Cell. Biol. 12, 5640-5651
DASSO, M. (1993)
Trends Biochem. SC;. 19, 2 1 l-21 6
repeats, and Nupl53p zinc finger motifs in one C. elegans protein
YANO, R., OAKES, M., YAMACHISHI, DODD,
/. Cell Biol. 125,
18, 96-l 01
interactionsz2. The combination
characterized
20
S., DASSO, M. and J. (1994)
705-719
in
nuclear-pore-chromatin of two rbpl
KORNBLUTH, NEWPORT,
side of the NPC,
and a of the
Human
Frontier
Science
Program
Organization (to D. C.).
193
protein
is essential for the second
present in other proteins,
step: translocation through the pore7s8. This suggests a direct
including NPC proteins. These
interaction between Ran and
proteins are: (1) the Saccharomyces cerevisiae nuclear pore protein
nuclear pore proteins at some stage of nuclear protein
(2) a 5. cerevisiae protein
Nup2p (ACC X69964;
Ref. 15),
related to Nup2p (ACC Z38060),
import.
which displays the highest
A 27 kDa Ran-binding protein
expression library by probing with
homology to Nup2p within the rbpl motif, (3) a human sequence tag (ACC M79174; Ref. 16) that is
(RanBPl) specific for Ran-GTP has been identified from a mouse Ran loaded with labelled CTP13. In a
particularly closely related to the
separate study using the same technique, proteins of 28, 86, 100
sequence, (4) the Caenorhabditis
and 6 for reviews). In particular, it is
and 200-300
elegans
a key component
The 28 kDa protein is cytosolic and
Ran/TC4 has been implicated number of different nuclear functions (Refs l-4;
in a
see Refs 5
in nuclear
transport7,*. Proteins are imported into the nucleus through the nuclear pores in an active two-step process9,10 that requires soluble factors’
l. The first step is the
NLS-dependent
5. cerevisioe NupZp-related
kDa were detected14.
probably corresponds to RanBPl ; the others were found in the highsalt/Triton-soluble nuclear fraction,
By comparing
the recently identified S. cerevisiae homologue of RanBPl (ACC 233503; Ref. 18), which shares
which also includes nuclear pore proteins.
binding of the
protein encoded by the
open reading frame (ORF) F59A2.1 (ACC 234801; Ref. 17), which contains two rbpl motifs, and (5)
40% identity with the mouse
sequences in the
protein and shows 64% identity
import substrate to the cytoplasmic side of the nuclear pore complex
CenBank database, we have identified an approximately 75
(NPC). Recently, a 60 kDa
amino acid domain in mouse
within the rbpl motif. As the rbpl motif is the most highly conserved
protein - ‘importin’ -was found to be required for this step12. Ran
RanBPl (ACC L25255), referred to here as the rbpl motif, that is also
domain in RanBPl, it seems likely that it mediates its interaction with Ran. In turn one might conclude that proteins containing the rbpl
Mouse RanBPl
motif bind Ran in its CTP-bound form. The presence of Ran-binding
Yeast RanBPl horn
interest, because it suggests Nup2p
motifs in Nup2p is of particular might serve to integrate the functions of two soluble factors that are essential for nuclear protein Yeast Nup2p-rel
import in the vertebrate system: namely Ran and importin. Nup2p has been shown to interact genetically and physically19 with
Human HHCP045
Srpl p (Ref. 20), the yeast homologue of importin12. The presence of the rbpl motif in Nup2p now suggests that it also
Nematode F59A2.1
interacts with Ran. The observation that Nup2p is essential only in certain genetic backgrounds15
Yeast Nup2p
indicates that such a central function is backed up by more than FIGURE 1 Proteins that contain the rbpl motif: schematic presentation of RanBPl -related proteins found in the GenBank database (release BS+) using the TBLASTN program26 of the NCBI e-mail server. Darkly shaded boxes indicate rbpl motifs; the striped box represents the Nupl53p-like
zinc-finger domains; and the lightly
shaded boxes indicate regions of XFXFC-like repeats. Mouse RanBPl is the mouse Ran-binding protein 1 (ACC L25255); yeast RanBPl horn is the 5. cerevisiaeRanBPl homologue SCHTNl (ACC X65925); yeast NupZp-rel is the NupZp-related protein encoded by an ORF in the 5. cerevisiae DNA sequence SC561 0 (ACC 238060); human HHCP045
is a partial sequence from the human clone HHCP045
(ACC M79174); yeast Nup2p is from 5. cerevisiae (ACC X69964); nematode F59A2.1 is encoded by the C. elegans ORF F59A2.1 (ACC 234801).
cDNA
sequences coding for proteins that contain at least parts of the rbpl motif were also found in rice (ACC D22992, ACC D39320, ACC D15902) and Arabidopsis thaliana
192
(ACC 234627, ACC T22134).
one gene product. The C. elegans F59A2.1 protein not only contains two potential Ran-binding sites but also has two additional remarkable characteristics: like the nuclear pore protein Nupl53p
it has a conserved
domain that includes zinc finger motifs; and it contains 13 hydrophobic pentapeptide repeats, which resemble the XFXFC motif found in several nuclear pore proteins, such as Nupl p, NupZp, Nspl p, ~62, POMl21, rat INMACIA and also Nupl53p review). Nupl53p
(see Ref. 21 for a is a DNA-binding
TRENDS IN CELL BIOLOGY VOL. 5 MAY 1995
Mouse RanBPl
36
QEIKTLEEDEEELFKMRAKLFRFASENDLPEWKERGTGDVKLLK--HKEKG--TIRLLMRRDKTLKICANHYIT~~LK~
112
Yeast RanBPl horn
74
VDVKTMEEDEEVLYKVRAKLFRF--DADAKEWKERGTGDCKFLKN-KKTN---KVRILMRRDKTLKICANHIIAPRYTLKP
148
Yeast NupZp
597
INLQNGEEDEVALFSQKAKLTF--NAETKSYDSRGVGEMKLLK--KKDDPS-KVRLLCRSDGMGNVLLNATVVDSFKYRP
672
Nematode
F59A2.1_N
258
~EVKTGEEGEQTMFCNRSKLYIY--ANETKEWKERGTGELKVLY--NKDKK--SWRVVMRRDQVLKVCANFPILGSMTIQQ
332
Nematode
F59A2.1_C
729
~EVKTGEEDEEVMFSARCKLYKY--YSDLKENKERGLGDIKLLK--SNDN---KYRIVMRREQVHKLCANFRIEKSMRLSP
802
203
QEVKSGEESEECIYQVNAKLYQL--SNIKEGWKERGVGIIKINK--SKDDVE-KTRIVMRSRGILKVILNIQLVKGFTVQK
278
VEVITGRRAESNVLQMQCKLFVF--DKTSQSWVERGRGLLRLNDMASTDDGTLQSRLVMRTQGSLRLILNTKLWAQMQIDK
81
Yeast Nup2p-rel
3
Human HHCP045
Consensus
vevktgEEdEe..f..raKL..f--....kewkeRG.G Y
c
lk.caN..i...m...p
..kllk--.kd----k.R.lmRrd.. rn
fY Y
lf
il
IV i v
FIGURE 2 The rbpl motif: rbpl motifs are shown aligned in single-letter code. The protein sequences were aligned by using the MACAW program. Sequence names are explained in the legend to Fig. 1. F59A2.1_N and F59A2.1_C are the N-terminal and C-terminal rbpl motifs, respectively, in the F59A2.1 protein from C. elegans. A consensus rbpl motif was calculated from the shown sequences. Amino acids that are conserved in all sequences are shown in the consensus
as capital
letters.
Lower-case
letters
in the
upper
line indicate
conservation
in more
than
50%
of the
sequences. Similar amino acids in one position are shown in the lower lines. protein
exclusively
nucleoplasmic
found
4
on the
and is therefore implicated
5 6
motifs, nucleoporin-like
7 8
9 10
BLOBEL, G. (1993)
23
SUKEGAWA,
Cuff.
1. and BLOBEL, C. (1993)
GRUNDMANN,
U., NERLICH,
LOTTSPEICH, 1. Cell Biol. 123,
(1988) 24
659
C., REIN, T.,
F. and KUEPPER, H. A.
Nucleic Acids Res. 16, 4721
MOORE,
M. S. and
BLOBEL, G. (1994)
Proc. Nat/ Acad. Sci. USA 91, 10212-l
NEWMEYER,
D. D. and FORBES, D. J.
25
OHTSUBO,
26
ALTSCHUL,
Cell 52,641-653
RICHARDSON,
M. et al. (1987)
0216
Genes Dev. 1,
585-589
W. D., MILLS, A. D., 5. M., LASKEY, R. A.
ADAM,
C. (1988)
S. F., GISH, W., MILLER, W.,
MYERS, E. M. and LIPMAN,
Cell 52,
5. A., STERNE-MARR,
CORLICH,
D. 1. (1990)
/. Mol. Biol. 215, 403-410
Enno Hartmann
R. and
/. Cell Biol. 111,
Max-Delbriick-Centrum
D., PREHN, S., LASKEY, R. A.
and HARTMANN,
E. (1994)
Cell 79,
767-778 13
translocation step of nuclear
FABRE, E. and HURT, E. C. (1994)
Cell 72, 29-38
807-816 12
cytosolic protein that binds to and cooperates with Ran in the
COUTAVAS,
1. D., D’EUSTACHIO,
and RUSH, M. (1993)
factor
Medizin, Berlin,
ftir Molekulare
Robert-Rdssle-Str.
10, 13125
Acknowledgements
Germany.
We thank
P.
Nature 366,
Wellcome/CRC
constructive
Institute,
Road, Cambridge,
UK
Tennis
Court
comments
CB2 1 QR.
14
LOUNSBURY, MACARA,
whether a consensus for those proteins can also be found.
11285-l
A. L. and
/. Biol. Chem. 269,
1290
15
LOEB, D. 1. D., DAVIS, L. I. and FINK, C.
16
ADAMS,
References
R. (1993)
DRIVAS, G. T., SHIH, A.,
K. M., BEDDOWS,
I. C. (1994)
E., RUSH, M. G. and
Mol. Biol. Cell. 4, 209-222 M. D. et al. (1992)
Nature 355,
632-634
Mol. Cell. Biol.
WILSON,
R. et a/. (1994)
Nature
368,
NOTE ADDED IN PROOF
supported
Similarfindings to those detailed in this
Deutsche
letter have been described Dingwall mun.).
by Colin
and colleagues (pers. comAfter
this
manuscript
finished,
further
the rbpl
motif were reported.
was
proteins containing These
Forschungsgemeinthe Cancer Research Campaign
32-38
are RBPX [BISCHOFF, F.R., KREBBER,H.,
(SP1961)
BUTLER, C. and WOLFE, K. H. (1994)
SMIRNOVA,
E.,
and
long-term
(1991) Proc. Not/ Acod. SC;. USA 88,
Biochem. Biophys. Acta 1219,
PONSTINCL,
H. (1995)
EM80 /. 14,
fellowship
10830-l
711-712
705-7151
and RUSH, M. C. (1993)
P.
/. Cell Viol. 120,
619-630
313-323
TRENDS IN CELL BIOLOGY
BELANGER, K. D., KENNA, and DAVIS, L. I. (1994)
VOL. 5 MAY 1995
M. A., WEI, 5.
/. Cell B/o/. 126,
accession U10248 Nat/ Acad.
DONC,
W.
and two proteins with the numbers [BEDDOW,
U19240
and
A.L. et al. Proc.
Sci. USA (in press)]
by the
schaft (SFB366),
10, 1793-l 798
REN, M., DRIVAS, C., D’EUSTACHIO,
This
work was
BISCHOFF, F. R. and PONSTINCL, H. 0834
on the
manuscript.
585-587
RCCl (Ref. 25), contains this motif. It remains to be seen
Ron
Laskey for
Dirk GiWlich
E., REN, M.,
OPPENHEIM,
protein import24, nor the Ran
3
22
F., PASCHAL, B., EVANS, E.
GERACE, L. (1990)
mediates interaction with Ran. For example, neither PP15 (Ref. 23), a
P. (1990)
21
655-664
unlikely to be the only one that
2
MELCHIOR,
and DINGWALL, 11
It is also clear that this motif is
D’EUSTACHIO,
BLOBEL, C. (1994)
M. S. and
DILWORTH,
so far, it is likely
that more of these proteins will be found to contain the rbpl motif.
COUTAVAS,
M. 5. and
MOORE,
(1988)
As only a few nuclear pore proteins have been
1
MOORE,
1649-l
interactions.
M.,
M. (1992)
Opin. Cell Biol. 6, 335-342
and CERACE, L. (1993)
distinct from nuclear protein import, such as nuclear-pore-chromatin
guanine-nucleotide-exchange
Trends Biochem. SC;.
Nature 365, 661-663
(F59A2.1) suggests that it might mediate functions of Ran that are
J. A. and NOMURA,
Mol. Cell. Biol. 12, 5640-5651
DASSO, M. (1993)
Trends Biochem. SC;. 19, 2 1 l-21 6
repeats, and Nupl53p zinc finger motifs in one C. elegans protein
YANO, R., OAKES, M., YAMACHISHI, DODD,
/. Cell Biol. 125,
18, 96-l 01
interactionsz2. The combination
characterized
20
S., DASSO, M. and J. (1994)
705-719
in
nuclear-pore-chromatin of two rbpl
KORNBLUTH, NEWPORT,
side of the NPC,
and a of the
Human
Frontier
Science
Program
Organization (to D. C.).
193