Cell News 2/2014
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Centrosomes in different eukaryotes
Centrosomes are tiny non-membranous organelles harboring
many different functions, most of which are somehow related
to microtubule organization. They generally consist of a cen-
tral, highly organized structure embedded in a matrix serving
as a scaffold for microtubule nucleation complexes. If present,
centrosomes serve as the main microtubule-organizing centers
(MTOCs) and thus they are essential for the whole cell architec-
ture in all organisms using the microtubule system to position
their organelles to the right place. Since the major function of
microtubule nucleation and organization is shared by all or-
ganisms containing an MTOC as a clearly discernable single
organelle, I use the term "centrosome" for all these kinds of
organelles whether they contain centrioles or not.
Mononucleated cells generally contain only one centrosome.
It duplicates once in each cell cycle and contributes to organi-
zation of the mitotic spindle, whereby each of the duplicated
centrosomes organizes microtubules at the two spindle poles.
Centrosomes or at least their precursors have been invented
very early in eukaryotic evolution since they are present in all
eukaryotes except higher plants (see Fig. 1 for a current model
of the eukaryotic tree of life). Eukaryotic evolution has engen-
dered different types of centrosomes. The most common type
is found among the opistokonts in animals, but also in unicel-
lular bikonts and lower plants. It is characterized by centrioles
consisting of a nine-fold symmetrical, cylindrical arrangement
of short microtubules and associated proteins (Fig. 2A). In G1
the centrosome contains two centrioles and after duplication
in S-phase, each centriole (now called mother centriole) has
born one premature daughter centriole in a perpendicular ori-
entation at its side. Thus, the centrioles are the duplicating unit
of the centrosome. They are embedded in a so-called pericen-
triolar matrix (PCM) mainly consisting of scaffolding proteins
that bind microtubule nucleation complexes and regulators of
microtubule dynamics. The presence of centrioles is inevitably
coupled to the existence of cilia or flagellae. This is because the
mother centriole also serves as the basal body of the prima-
ry cilium, which has signaling and sensory functions (Kim and
Dynlacht, 2013). Besides these non-motile primary cilia there
are also cells using single or several cilia for cell locomotion or
transport of fluids. Cells containing more than one cilium have
means to amplify centriole number independently of canonical,
cell cycle-synchronized centriole duplication.
Opposed to centriolar centrosomes are acentriolar centroso-
mes, sometimes also called nucleus associated bodies (NABs) or
spindle pole bodies (SPBs) found among the unikonts in fungi
and amoebozoans. These often possess layered core structu-
res instead of centrioles and are best characterized in yeasts
and Dictyostelium amoebae (Fig. 2B). In budding yeast the SPB
mainly consists of a stack of three plaques and is permanently
inserted into the nuclear envelope. It organizes a very simp-
le intra-nuclear and extra-nuclear microtubule cytoskeleton,
which is mainly required for nuclear positioning and chromo-
some segregation during mitosis. In the amoebozoan Dictyo-
stelium, the centrosome (NAB) also contains a three-layered
core structure, which in addition is surrounded by a corona
reminiscent of a PCM (Fig. 2B). Although being attached to
the nuclear envelope this centrosome is entirely located in the
cytosol during interphase by contrast to the budding yeast SPB.
The Dictyostelium centrosome enters the nuclear envelope only
upon centrosome duplication during mitosis, in a manner remi-
niscent of the situation in fission yeast (Ding et al., 1997; Ueda
et al., 1999). It organizes a radial microtubule cytoskeleton very
similar to that of animal cells. However, due to their amoebo -
id locomotion and the absence of ciliated gametes these cells
need no centrioles. Since their centrosomes seem to fulfill all
known functions of centrosomes except cilia formation, this
organism offers the possibility to use comparative biology to
identify the proteins essential for all those centrosomal
func-tions unrelated to cilia formation.
If different centrosome types of animals, yeasts and amoebozoa
are compared, a surprisingly short list of general centrosomal
components emerges. It includes the proteins of the
γ
-tubulin
small complex (
γ
-TuSC;
γ
-tubulin, gamma-tubulin complex-
associated proteins GCP2, GCP3) required for microtubule nuc-
leation, EB1, TACC and XMAP215 for microtubule dynamics and
stabilization, centrin, Cep192/SPD2, and centrosomin (Cnn) as
scaffolding proteins, kinases from the polo, aurora, NIMA and
Cdk family regulating duplication and spindle organization,
and the dynein motor protein (Still et al., 2004; Carvalho-San-
tos et al., 2010; Carvalho-Santos et al., 2011) suggesting that
these proteins comprise the most ancient centrosomal protein
inventory. I have added Cnn, which was originally identified
in Drosophila (Megraw et al., 1999; Lucas and Raff, 2007) to
the list, since recent experimental and database analyses in
Dictyostelium suggest that this protein is not only conserved
in humans (CDK5Rap2; (Fong et al., 2008)) and fission yeast
(mto1; (Samejima et al., 2005)) but also in Dictyostelium, whe-
re two putative orthologues, CP148 (Kuhnert et al., 2012) and
DDB_G0282851 (
, have been identified.
One of the intriguing questions is which of the extant centro-
some structures represents the most ancient type. For many
decades the amoeboid cell state was regarded as being ances-
tral and thus the acentriolar MTOCs in fungi and amoebozoans
were thought to represent a primitive centrosome type. Me-
anwhile, comparative biology has taught us that most likely
LECA (last eukaryotic common ancestor) already possessed one
or two centrioles associated with a cilium, since centrioles are
found in all major eukaryotic subgroups (Cavalier-Smith, 2010;
Hodges et al., 2010) (Fig. 1). Thus, the absence of centrioles
in higher plants, fungi and most amoebozoans is considered a
result of secondary loss due to abandonment of locomotion by
ciliary or flagellar beating in these organisms. In this light, the
most initial purpose of centrosomes was to initiate formation
of a cilium, whereby the centriole served as a basal body for
nucleation and tethering of ciliar microtubules and determined
the nine-fold symmetry of microtubule arrangements within
the cilium. Indeed, ciliates for example employ centrioles only
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