centriole, and the older one as the mother centriole (figure 1
a
).
The mother centriole harbours distal and sub-distal appendages
whose distribution mirrors the ninefold symmetry of the cen-
triole, and which are acquired at the end of the cell cycle
following that in which the procentriole emerged. The distal
appendages mediate docking of the mother centriole to the
plasma membrane in cells that exit the cell cycle. Once docked
in that location, the mother centriole is referred to as the basal
body, and by some workers as the kinetosome [7], and serves
to template formation of the axoneme in cilia and flagella.
Note that nowadays the basal body is frequently referred to as
a centriole, both for simplicity and because basal bodies and cen-
trioles can interconvert in many cell types. Note also that often,
including in the present piece, the plural ‘centrioles’ is used to
refer indiscriminately to all centriolar cylinders (i.e. jointly to
centrioles and procentrioles).
Apart from centrioles, another main character in the plot is
the pericentriolar material (PCM), also known as the centro-
somal matrix, an electron-dense region that surrounds the
centriolar cylinders, particularly their proximal part, and
together with them constitutes the centrosome (figure 1
a
). It
is now clear that centrioles and PCM are intimately linked to
fulfil the numerous functions of the centrosome. However,
when the centrosome was equated to an MTOC—when micro-
tubule nucleation was the main function envisaged for the
entire organelle—the dominant view was that centrioles were
not important for centrosome function. That centrioles are
instrumental in maintaining centrosome integrity was demon-
strated in human cells by injection of monoclonal antibodies
against polyglutamylated tubulin, a post-translational modifi-
cation of
a
- and
b
-tubulin particularly prevalent in centrioles
[8]; see §5). This led to centriole loss and subsequent dissol-
ution of the entire centrosome. In
Caenorhabditis elegans
,
partial depletion of centriolar components by RNAi results in
smaller centrioles that recruit less PCM than in the wild-type,
further indicating that PCM-size scales with centriolar mate-
rial [9,10] . Therefore, centrioles play a fundamental role in
assembling the centrosome organelle.
There are other cast members that are neither centriolar nor
PCM components, yet clearly important for the overall archi-
tecture of the centrosome (figure 1
a
). These include the inter-
centriolar linker that connects the mother centriole and the
daughter centriole in G1, as well as the two diplosomes there-
after, as well as centriolar satellites, granules approximately
100 nm in diameter that remain incompletely described with
respect to their composition and function, apart from being
important for primary cilium assembly [11,12].
Besides knowing the cast of characters, it is also important
to ensure that the nomenclature of the molecular players that
participate in the play is accessible to a broad base of scien-
tists. Too many proteins have been referred to under more
than one name. For instance, the human protein related to
C. elegans
SAS-4 (Spindle ASsembly abnormal 4) has been
referred to as SAS4 (to indicate its relatedness with the
worm protein), as CPAP (for Centrosomal P4.1-Associated
Protein, as it was first named, before the relationship to
SAS-4 was known) or CENPJ (for Centromere Protein J, for
reasons that remain unclear). Although this naming plethora
is not an issue specific to the centrosome field, a concerted
effort would be welcome to clarify the language.
We hope that the reader of this Theme Issue will be in a pos-
ition to appreciate the fact that despite considerable progress in
understanding the molecular composition, the assembly
mechanisms and the numerous functions of centrosomes,
many fascinating questions remain open. The field is at an excit-
ing juncture: as many of the molecular mechanisms are being
unravelled, the time is ripe for addressing some of the impor-
tant long-standing questions, including ones that first
emerged when this remarkable organelle was discovered over
a century ago. We discuss below some of these questions, refer-
ring the reader to chapters of this Theme Issue for further
information when appropriate.
4. On the origin and evolution of the
centrosome
Some of the most pressing questions should probably be
posed from an evolutionary perspective: given that the cen-
trosome is not present in all multicellular organisms, nor in
all cells of a given organism, one must ask what this organelle
adds to the cell economy that explains its presence as well as
its specialization in different biological systems. It is now well
recognized that the centrosome evolved from an ancestral
basal body/flagellum [13]. Whatever the actual scenario for
the origin of the centrosome organelle in the Amorphea line-
age (see chapter by Juliette Azimzadeh) [14], it is interesting
to consider what consequences the many variations in centro-
some structure and composition observed in extant
eukaryotes may have on centrosome function. For instance,
what are the functional consequences associated with the
fact that many of the genes encoding centrosomal com-
ponents present in unicellular organisms and in vertebrate
species are missing in
Drosophila
or in
C. elegans
?
5. On centriolar microtubules
The microtubules that make up the walls of centrioles have a
unique organization, unlike that of any other microtubule in
the cell, except for the ones of the axoneme that they template.
In particular, centriolar microtubules have a very slow turn-
over and are resistant to microtubule-destabilizing drugs or
cold treatment [15]. Furthermore, centriolar microtubules can
apparently resist the mitotic state that dramatically increases
the turnover of cytoplasmic microtubules [16]. These proper-
ties are exhibited both by microtubule triplets (A, B and C
microtubules) present in the proximal part of centrioles and
microtubule doublets (A and B microtubules) found in the
distal part of centrioles as well as in axonemes (figure 1
a
,
b
).
Moreover, triplet microtubules, but not doublet microtubules,
resist treatments with high temperature or high pressure [17].
Perhaps the exceptional stability of triplet microtubules stems
from the short distance between the A microtubule of one tri-
plet and the C microtubule of the adjacent triplet, which could
provide additional mechanical strength. Moreover, triplet
microtubules could provide different surface properties from
that of doublets to associate with specific PCM proteins.
The mechanisms underlying the exceptional stability of
centriolar microtubules are not sufficiently understood, but
they are accompanied by the extensive post-translational
modifications of tubulin subunits, including polyglutamyla-
tion, detyrosination, acetylation and polyglycylation [18].
These modifications are thought to be important for centriole
integrity, as evidenced by the antibody injection experiments
described above. By analogy to the impact of post-
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