Howard Hughes Medical Institute and Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, CO 80309, USA
* Author for correspondence (e-mail: daniel.starr{at}colorado.edu)
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Summary |
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Key words: Nuclear migration, Nuclear anchorage, UNC-84, SUN domain, ANC-1, Muscular dystrophy, Nuclear envelope
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Introduction |
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A wide variety of organisms have syncytia, which are formed either when
multiple nuclear divisions occur without cell divisions or as a result of cell
fusion. Normally, syncytial nuclei are located in specific regions or evenly
spaced through the cytoplasm. For instance, a vertebrate myotube has hundreds
of nuclei; most are evenly spaced apart; however, a group of 4-8 cluster at
the neuromuscular junction (Couteaux,
1973). A second striking example is in the Drosophila
blastoderm, where over 6000 nuclei, derived from 14 rounds of nuclear division
without cytokinesis, are carefully positioned at the periphery of a single
cell. A disruption in the precise spacing of these nuclei at the cortex has
catastrophic results, including tripolar spindles and disruptions of
patterning (Foe and Alberts,
1983
).
Two related processes are required to control the specific positioning of
nuclei. First, nuclei must migrate through the cytoplasm to the appropriate
locales within a cell, and then they must be anchored at that position so they
do not drift. These processes are controlled by a combination of forces from
microtubule and actin-based networks. In most studied cases, microtubules and
associated dynein and kinesin motors play a central role in the positioning of
nuclei. For example, the female pro-nucleus migrates as a result of dynein on
the nuclear envelope pulling the nucleus towards the male centrosome. Since
the role of microtubules in nuclear migration and positioning has been
recently reviewed (e.g. Bloom,
2001; Suelmann and Fischer,
2000
; Morris,
2000
; Reinsch and Gonczy,
1998
), here we concentrate on the important contributions of
actin-based networks for positioning of nuclei. Specifically we focus on a
newly identified family of proteins, Syne/ANC-1.
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Examples of actin-based nuclear-positioning events |
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Actin networks can also function actively to reposition nuclei. Chytilova
et al. (Chytilova et al., 2000)
recently described a dramatic example. Actin depolymerizing drugs completely
abolished rapid, long-distance intracellular nuclear migration in
Arabidopsis root hairs, whereas drugs that disrupted microtubules had
no effect (Chytilova et al.,
2000
). Because of the speed and distance of the nuclear migrations
in these cells, the actin network must be functioning actively to move nuclei,
in contrast to the above examples of passive mechanisms. Budding yeast
provides another example: both actin filaments and microtubules are required
for proper localization of the nucleus and spindle at the bud neck to ensure
normal cell division (Palmer et al.,
1992
; Bloom,
2001
).
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C. elegans genes required for nuclear positioning |
---|
As in other systems, both actin filaments and microtubules probably work
together to position organelles in C. elegans. There is a large body
of evidence that microtubules play important roles in nuclear positioning in
the early embryo (reviewed by Reinsch and
Gonczy, 1998). In addition, a disruption in the actin cytoskelton
by a weak loss-of-function mutation in the C. elegans homologue of
cofilin, unc-60(r398) (Ono et
al., 1999
), leads to a defect in positioning of mitochondria
(Starr and Han, 2002
).
Although it has not been directly tested with pharmaceutical agents in C.
elegans, actin is also probably required for positioning of nuclei in a
variety of cell types.
Two genes, anc-1 and unc-84, are required in C.
elegans for proper nuclear anchorage in syncytial cells. Normally, nuclei
are evenly spaced throughout the hypodermal syncytia. They move slightly as
the underlying muscles of the worm move but return to their original position
when the worm relaxes. Mutations in anc-1 or unc-84 lead to
an Anc (nuclear anchorage defective) phenotype, in which the nuclei
float freely within the cytoplasm and multiple nuclei group together
(Hedgecock and Thomson, 1982;
Malone et al., 1999
).
Mitochondria also fail to localize properly in anc-1, but not
unc-84, mutant cells (Hedgecock
and Thomson, 1982
; Starr and
Han, 2002
). Both unc-84 and a third gene,
unc-83, are required for many nuclear migration events in C.
elegans. Null unc-83 or unc-84 mutations lead to an Unc
(uncoordinated) phenotype because failed nuclear migrations lead to
the death of P-cells, which normally give rise to ventral neurons
(Horvitz and Sulston, 1980
).
unc-83 encodes a novel protein; its transcripts are temporally and
spatially controlled. UNC-83 first appears during development at the nuclear
envelope of migrating nuclei (Starr et
al., 2001
).
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The UNC-84/SUN proteins at the nuclear envelope |
---|
|
|
The switch between nuclear anchorage and nuclear migration must be a
tightly coordinated event. Before a nucleus can migrate through the cytoplasm
of the cell, the nuclear anchor must be released. Mutations in unc-84
disrupt both nuclear anchorage and migration, suggesting that UNC-84 is
intimately involved with this switch. Interestingly, the SUN domain of UNC-84
is required to target both ANC-1 (through an interaction that is not known to
be direct or indirect) and UNC-83 (through a direct interaction) to the
nuclear envelope (Starr and Han,
2002; Starr et al.,
2001
). It is not known whether ANC-1 and UNC-83 can interact with
UNC-84 simultaneously, although both antigens are detected at the nuclear
envelope of adult hypodermal cells. A simple model would be that, when UNC-83
binds to UNC-84, it displaces ANC-1, perhaps through an unknown mediating
protein or complex, which frees the nucleus and allows migration to proceed.
In reality, the mechanism is probably more complex, involving unknown
signaling molecules, since overexpression of UNC-83 or the KASH domain of
ANC-1 does not displace ANC-1 or UNC-83, respectively
(Starr et al., 2001
) (D.A.S.,
unpublished).
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The Syne/ANC-1 family of proteins |
---|
Two related proteins exist in mammals and have been called Syne-1 and -2
(Apel et al., 2000), Nesprin-1
and -2 (Zhang et al., 2001
),
Myne-1 and -2 (Mislow et al.,
2002a
), or NUANCE (Zhen et
al., 2002
). Since the same two genes appear to encode all of these
proteins, we use the original names, Syne-1 and -2 (for synaptic
nuclear envelope). Single homologues have been
identified in Drosophila, Msp-300
(Rosenberg-Hasson et al.,
1996
; Starr and Han,
2002
), and C. elegans, ANC-1
(Starr and Han, 2002
). A
second protein in Drosophila, Klarsicht, contains the conserved
C-terminal domain but has no additional features in common with the other
proteins. Klarsicht localizes to the nuclear envelope, where it has been
proposed to organize dynein and/or kinesin motors to control nuclear and lipid
vesicle migration along microtubules
(Mosley-Bishop et al., 1999
;
Welte et al., 1998
). We call
the conserved C-terminal 60 residues the KASH domain (for
Klarsicht/ANC-1/Syne-1 homology) and refer to this
family of proteins as the Syne/ANC-1 proteins.
Antibodies against Syne-1, Syne-2 and ANC-1 localize to the nuclear
envelope (Apel et al., 2000;
Mislow et al., 2002a
;
Starr and Han, 2002
;
Zhang et al., 2001
;
Zhen et al., 2002
). In
mammals, they specifically localize to the nuclear envelope of muscle cell
nuclei throughout development. Interestingly, Syne-1 is enriched at the
nuclear envelope of myonuclei clustered at the neuromuscular junction, which
suggests a role in positioning of nuclei towards the synapse
(Apel et al., 2000
). The KASH
domain probably localizes Syne/ANC-1 proteins to the nuclear envelope. The
C-terminal 64 and 59 residues of Syne-1 and Syne-2, respectively, are
sufficient to localize tags to the nuclear envelope of mammalian tissue
culture cells (Zhang et al.,
2001
; Zhen et al.,
2002
). The KASH domains of ANC-1 and Klarsicht are also been
sufficient for nuclear envelope localization. Furthermore, the predicted
trans-membrane region of the KASH domain is required for localization to the
nuclear envelope (Zhang et al.,
2001
).
Whether Syne/ANC-1 proteins localize to the outer or inner nuclear membrane
is still a matter of debate. Most of the data suggest that Syne/ANC-1 proteins
localize to the outer nuclear envelope and the cytoplasm. Digitonin extraction
experiments that allow antibodies to detect epitopes on the outside of the
nuclear envelope, but block epitopes inside the nuclear envelope, indicate
that Syne-2 is a component of the outer nuclear envelope
(Zhen et al., 2002). This
evidence implicates the KASH domain in making Syne-2 the first protein to
localize to the outer nuclear envelope but not the connected endoplasmic
reticulim, although it does not address whether Syne-2 is also on the inside
of the nuclear envelpe. Furthermore, the vast majority of ANC-1 antibody
staining in C. elegans and MSP-300 antibody staining in
Drosophila is cytoplasmic and excluded from the nucleoplasm
(Volk, 1992
;
Starr and Han, 2002
). Other
data suggest that Syne-1 functions as part of the nuclear matrix scaffold as
an inner nuclear membrane component. Syne-1 interacts directly with lamin A
and nesprin, both components of the inner nuclear matrix, in in vitro protein
blot overlay experiments (Mislow et al.,
2002b
). Therefore, Syne/ANC-1 proteins could function both inside
and outside the nucleus. Further investigations, including immunoelectron
microscopy localization of endogenous protein, are required to demonstrate the
exact locations of Syne/ANC-1 proteins with respect to the nuclear
envelope.
In C. elegans, localization of ANC-1 to the nuclear envelope
requires UNC-84 (Starr and Han,
2002). This fact, taken in context of the above model for UNC-84
function at the nuclear envelope, suggests that Syne/ANC-1, UNC-84 and perhaps
other proteins effectively bridge both membranes of the nuclear envelope
(Fig. 2). In support of such a
bridge hypothesis, Syne-1 co-immunoprecipitates with the major nuclear matrix
component lamin A/C (Mislow et al.,
2002a
).
Overexpression of the C-terminal domain of ANC-1 causes an Anc phenotype as
severe as that of null alleles of anc-1
(Starr and Han, 2002). In
mammalian tissue culture cells, the overexpressed C-terminus of Syne-2 is able
to displace endogenous Syne-2 from docking sites at the nuclear envelope
(Zhen et al., 2002
).
Therefore, disrupting the localization of endogenous Syne proteins to the
nuclear envelope probably produces the dominant negative phenotype. Since no
direct physical interaction between UNC-84 and any Syne proteins has been
detected, UNC-84 may function through other proteins to recruit or maintain
Syne proteins at the nuclear envelope. It will be informative to investigate
whether overexpression of the KASH domains of Syne-1 or Msp-300 in mice or
flies causes a nuclear anchorage defect, and if so, to analyze the
consequences.
The second major feature of the Syne/ANC-1 proteins is the conserved
N-terminal CH domains. CH domains are found in a large family of proteins,
including dystrophin and -actinin; when found in pairs, as they are in
the Syne/ANC-1 proteins, they usually bind to actin
(Gimona et al., 2002
). The CH
domains of Syne-2 and ANC-1 have been shown to bind to actin in vitro and to
co-localize with actin in vivo (Starr and
Han, 2002
; Zhen et al.,
2002
). In addition, Msp-300 cosediments with actin out of an
embryonic extract and colocalizes with actin
(Volk, 1992
). Finally,
overexpression of the N-terminus of ANC-1 causes a weakly penetrant, dominant
negative Anc phenotype (Starr and Han,
2002
). Thus, when overexpressed, the N-terminus of ANC-1 can block
the function of endogenous ANC-1. These data and the high degree of
conservation of the CH domains suggest that binding to actin is critical for
the function of the Syne proteins.
The bulk of ANC-1 consists of vast stretches of repetitive, mostly helical
domains, with short stretches of predicted coiled-coil domains throughout the
protein (Starr and Han, 2002).
ANC-1 might thus fold to form an elongated myosintail-like structure. Syne-1,
Syne-2 and Msp-300 all have large central domains containing multiple
spectrin-like repeats (Apel et al.,
2000
; Mislow et al.,
2002a
; Volk, 1992
;
Zhang et al., 2001
;
Zhen et al., 2002
). Spectrin
repeats are
106 residues long and fold to form highly coiled, 5 nm long,
triple helical bundles (Yan et al.,
1993
). Syne-2 has 22 spectrin repeats interspersed with other
predicted coiled regions. Therefore, the central extended coiled domain of
Syne-2 could extend well over 150 nm, and Syne-1 and Msp-300 could be 25%
longer. Presumably, the spectrin repeats of the Syne and Msp-300 proteins
function analogously to the long coiled domains of ANC-1. Some of the Syne-1
spectrin repeats directly interact with each other in two-hybrid and
blot-overlay experiments, which suggests that at least Syne-1 forms
antiparallel dimers (Mislow et al.,
2002b
). In an experiment designed to test the requirement of the
large central region of Syne-2, Zhen et al.
(Zhen et al., 2002
) fused the
N-terminal CH domain to the C-terminal KASH domain and transfected the chimera
into mammalian tissue culture cells. This resulted in an ectopic recruitment
of actin to the cytoplasmic side of the nuclear envelope
(Zhen et al., 2002
),
suggesting that the role of the huge central domain is to separate the
actin-binding domain from the nuclear envelope domain. Therefore, we
hypothesize that the evolutionary conservation of size in Syne/ANC-1 is due to
a selective advantage.
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The function of Syne proteins |
---|
Genetic studies in C. elegans and Drosophila have
provided the best insight into the function of the Syne proteins. As mentioned
above, null mutations in the C. elegans gene anc-1 disrupt
the uniform spacing of nuclei in multi-nucleated syncytial cells, leading to
an Anc phenotype (Hedgecock and Thomson,
1982). Therefore, ANC-1 is required for positioning of syncytial
nuclei. ANC-1 is also expressed in mononucleated cells, and its function is
required for anchorage of mitochondria
(Starr and Han, 2002
). It is
thus conceivable that it positions nuclei in a wide variety of cells. The
anc-1 nuclear anchorage defect does not have a drastic effect on the
animal. In contrast, mutations in the Drosophila gene
msp-300 are lethal. Embryos die because of a defect in muscle
morphogenesis (Rosenberg-Hasson et al.,
1996
; Volk, 1992
).
The exact nature of the lethal phenotype has not been completely described.
For instance, it is not known whether nuclei are properly positioned in mutant
muscles. In addition, owing to the maternal contribution, whether MSP-300
anchors nuclei during early embryogenesis or oogenesis has not been
examined.
Dystrophin and the associated dystrophin-glycoprotein complex (DGC) connect
the actin cytoskeleton to the extracellular matrix
(Ehmsen et al., 2002);
mutations in any of these components lead to Duchenne or Becker muscular
dytrophies (Burke et al., 2001
;
Rando, 2001
). Although
Syne/ANC-1 is proposed to connect the actin cytoskeleton to the nuclear
matrix, whereas dystrophin connects actin to the extracellular matrix, there
are some striking similarities between these two mechanisms
(Fig. 3). Dystrophin and
Syne/ANC-1 both bind to actin through an N-terminal CH domain and extend
through the cytoplasm towards the plasma or nuclear membranes, respectively.
Through associated proteins, the DGC or UNC-84/SUN and other proteins,
dystrophin and Syne/ANC-1 eventually connect to related underlying matrices,
either the basement membrane component laminin or the nuclear lamina. Compared
with dystrophin, which does not have a predicted transmembrane domain,
Syne/ANC-1 could circumvent the problem of the double membrane at the nuclear
envelope by using its own transmembrane domain to pass through the outer
nuclear membrane. Proteins associated with the KASH domain of Syne-1 are
likely eventually to bind lamin in the nuclear matrix, creating a bridge
across the nuclear envelope. Anti-Syne-1 antibodies co-immunoprecipitate a
component of the nuclear matrix, lamin A/C
(Mislow et al., 2002a
), which
suggests there is a more complete connection between the Syne proteins and the
nuclear matrix. We therefore propose that lamin, UNC-84/SUN, Syne/ANC-1 and
perhaps other proteins bridge the nuclear envelope and connect the nuclear
matrix to the actin cytoskeleton.
|
Mutations in lamin A/C or emerin lead to Emmery-Dreifuss muscular dystrophy
(Burke et al., 2001;
Burton and Davies, 2002
;
Hutchison et al., 2001
;
Nagano and Arahata, 2000
). An
expression array experiment that identified messages that were up- or
downregulated in tissue from Duchenne muscular dystrophy patients showed that
SUN-2 is downregulated an average of three to fourfold
(Chen et al., 2000
). Since,
lamin and UNC-84 have been linked to muscular dystrophy, it would be worth
investigating whether disruptions in the Syne/ANC-1 also contribute to
muscular dystrophy.
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Concluding remarks |
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Acknowledgments |
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