Download Centrosome Dynamics during the Meiotic Progression in the Mouse

Eur J Clin Chem Clin Biochem 1996; 34:659-660 © 1996 by Walter de Gruyter · Berlin · New York
LETTER TO THE EDITOR
Centrosome Dynamics during the Meiotic Progression
in the Mouse Oocyte
Sarah Baatout. Paul Jacqitet, Louis de Saint-Georges and Lucile Baugnet-Mahieu
Laboratory of Radiobiology, Belgian Nuclear Energy Study Centre, CEN-SCK, Mol, Belgium
Sir,
The centrosome is the most important microtubule organizing
centre and a major point for microtubule growth within the cell.
Because of their microtubule nucleating capacity, centrosomes are
responsible for many functions, such as the organization of the
interphase cytoskeleton and cytoplasm and the formation of the
mitotic spindle. Centrosomes are known to participate in the location of the cleavage furrow during cytokinesis (1). In this context,
it is useful to note that several types of proteins including motor
molecules such as kinesin (2) and dynein (3), microtubule-associated proteins such as the microtubule associated protein MAPI (4),
Ca/calmodulin kinase II (5), centractin and centrin (6) are associated with centrosomes.
In animals, almost all mitotic cells possess two centrosomes, one
at each spindle pole, consisting of a pair of centrioles surrounded
by osmiophilic material called pericentriolar material and which
contains the microtubule nucleating capacity of the centrosome.
However, plant cells, yeast and fungi, and most notably, mammalian oocytes are known to divide without centrioles (7). In the
mouse, centrioles are still present in oogonia and early oocytes.
With respect to cytoplasmic centrosomes, their consistent reduction
in number from the germinal vesicle stage to early diakinesis, coupled with their increase in size at this stage, suggest that centrosomal material aggregates at this early step of maturation. This is
followed in prometaphase by increased numbers of smaller
centrosomes that are no longer detectable in metaphase of meiosis-I
but reappear at anaphase. Coupled with the total absence of
immunodetectable centrosomes during telophase and their re-emergence at metaphase-II, cycles of aggregation, dispersion and reassembly seem to occur at specific cell cycle transitions. Unlike
mitotic cells, metaphase-II-arrested mouse oocytes contain, in addition to spindle pole-associated centrosomes, a population of nonspindle-associated microtubule organizing centres (8). After fertilization, those organizing centres nucleate microtubules and participate in pronuclear movement and in the formation of subsequent
mitotic spindles (8). In addition, it is not until the late morula and
early blastocyst that centrioles reappear during preimplantation development in the mouse.
In the oocyte, the ability to form asters is temporally correlated
with an increase in maturation promoting factor activity which occurs upon meiotic resumption (9). The cell cycle of eukaryotes is
regulated in part by the maturation promoting factor, which is a
complex formed by the cdc2 (a serine/threonine kinase) and cyclin
B (a protein which is synthesized and degraded in a cell cycle
dependent manner). The maturation promoting factor activity increases greatly from the beginning of mitosis, is maximal at metaphase, and thereafter abruptly decreases thus stimulating mitotic
events. In the mouse, it has been shown that maturation promoting
factor level peaks at metaphase of meiosis-I and -II, with low levels
detectable between these stages (10). When exogenous cdc2 kinase
is added to isolated centrosomes, both phosphorylation and Mphase microtubule growth dynamics result, suggesting that cdc2
can regulate changes in centrosome-directed microtubule dynamics
(11). Furthermore, investigations of Gotoh and colleagues have
shown that maturation promoting factor acts locally to regulate
spindle formation and that regulation of cdc2 itself is dependent
on microtubules (12). Immunodetectable centrosomes are always
phosphorylated at cell cycle steps characterized by high levels of
maturation promoting factor; conversely, at telophase, when
centrosomes are not immunodetectable, phosphorylated foci are absent when maturation promoting factor level is known to be low.
This suggests that the phosphorylation status of centrosomal material would determine the apparent assembly and disassembly dynamics of centrosomes correlated with specific cell cycle stage during meiotic maturation.
The suppression of centrosome-nucleated microtubule assembly
observed at metaphase-I and -II occurs when both maturation promoting factor and cytostatic factor levels are thought to be elevated. Purified centrosomes injected into unactivated metaphaseII-arrested Xenopus oocytes do not support microtubule growth.
However, when these eggs are artificially activated, microtubule
growth occurs. Since the increase in nucleation capacity appears
in conjunction with the loss of cytostatic factor, it is possible that
cytostatic factor is involved in the differential regulation of microtubule dynamics of the centrosome during both metaphase-ί and
-II. Cytostatic factor has been identified as the c-mos protooncogene product and its destruction at fertilization is dependent on the
calcium-activated enzyme, calpain (9). In addition, the interaction
between c-mos protein and tubulin suggests that c-mos protein may
bind to tubulin subunits and prevent assembly or it may act directly
on the centrosome to alter microtubule dynamics (13).
Vertebrate oocytes are also unique in exhibiting asymmetric cleavage at the time of polar body formation. The polarity exhibited by
the mammalian oocyte at the lime of polar body formation has
been thought to reflect the effect of the meiotic spindle on the
oocyte plasma membrane and subcortical cytoplasm. Documented
examples of this polarity include changes in the cortical organization of the oocyte membrane during maturation, with the establishment of an acttn-rich microvillus-free domain overlying the
spindle, that exhibit differences in lipid and protein mobility and
the exclusion of cortical granules (14). Whether a functional relationship exists between cytoplasmic centrosomes and polarity determination in the oocyte remains to be established. Since the
mouse oocyte appears to segregate its centrosomes into spindle
organizing and cytoplasmic components, it is possible that this
structural segregation is used to coordinate the unique demands of
karyokinesis and cytokinesis for asymmetric cleavage during meiotic progression. Further studies will be necessary in order to characterize the functional roles of centrosome populations during the
meiotic cell cycle.
Letter to the editor
660
References
1. Rappaport R. Establishment of the mechanism of cytokinesis
in animal cells. Int Rev Cytol 1986; 105:245-81.
2. Neighbors BW, Williams RC, Mclntosh JR. Localization of
kinesin in cultured cells. J Cell Biol 1988; 106:1193-204.
3. Pfarr CM, Cove M, Grisson PM, Hays TS, Porter ME, Mclntosh JR. Cytoplasmic dynein localizes to kinetochores during
mitosis. Nature 1990; 345:263-5.
4. Sherline P, Mascaro RN. Epidermal growth factor induces
rapid centrosomal separation in HeLa and 3T3 cells. J Cell
Biol 1982; 93:507-11.
5. Ohta Y, Ohta T, Miyamoto E. Ca/calmodulin-dependent protein kinase II: localisation in the interphase nucleus and the
mitotic apparatus of mammalian cells. Proc Natl Acad Sei
USA 1990; 87:5341-5.
6. Rout M, Kilmartin J. Components of the yeast spindle and
spindle pole body. J Cell Biol 1990; 111:1913-27.
7. Maro B, Karsenti E. Centrosomes and the spatial distribution
of microtubules in animal cells. Trends Biochem Sei 1986;
11:460-3.
8. Schatten H, Schatten G, Mazia D, Balczon R, Simerly C. Behavior of centrosomes during fertilization and cell division in
mouse oocytes and in sea urchin eggs. Proc Natl Acad Sei
USA 1986; 83:105-9.
9. Sagata N, Wanatabe N, Vande Woude GF, Ikawa Y. The c-mos
proto-oncogene product is a cytostatic factor responsible for
meiotic arrest in vertebrate eggs. Nature 1989; 342:512-8.
10. Hashimoto N, Kishimoto T. Regulation of meiotic metaphase
by a cytoplasmic maturation-promoting factor during mouse
oocyte maturation. Dev Biol 1988; 126:242-52.
11. Verde F, Berrez J, Antony C, Karsenti E. Taxol-induced microtubule asters in mitotic extracts of Xeriopus eggs: requirement
for phosphorylated factors and cytoplasmic dynein. J Cell Biol
1991; 112:1177-87.
12. Gotoh Y, Nisihia E, Matsuda S, Shiina N, Kosako H, Shiokawa
K, et al. In vitro effects on microtubule dynamics of purified
Xenopus M phase-activated MAP kinase. Nature 1991;
349:251-4.
-r
13. Zhou R, Oskarsson M, Paules PS, Schulz N, Cleveland D,
Vande Woude GF. Ability of the c-mos product to associate
with and phosphorylate tubulin. Science 1991; 251:671-5.
14. Ducibella T, Anderson E, Albertini DF, Aalberg J, Rangarajan
S. Quantitative studies of changes in cortical granule number
and distribution in the mouse oocyte during meiotic maturation. Dev Biol 1988; 130:184-97.
Received April 4/May 27, 1996
Corresponding author: Sarah Baatout, Laboratory of
Radiobiology, Belgian Nuclear Study Energy Centre, CEN-SCK,
Boeretang 200, B-2400 Mol, Belgium
Eur J Clin Chem Clin Biochem 1996; 34:661 © 1996 by Waiter de Gruyter · Berlin · New York
LETTER TO THE EDITOR
Searching for an International Name for an Old Discipline
Xavier Fuentes-Arderiu
Servei de Bioquimica Clinica, Ciutat Sanitaria i Universitäria de Bellvitge, UHospitalet de Llobregat, Barcelona,
Spain
Sir,
The advancements in the European Union will it make necessary
to adapt and harmonize many areas, including the professional
fields of the scientific disciplines which have considerable differences among the European countries (1). This also applies, of
course, to the discipline corresponding to the activity carried out
in a general clinical laboratory.
This discipline may be defined as the branch of health sciences
devoted to the in vitro observation of biological properties useful
in prevention, diagnostics, prognostics and monitoring of diseases,
by means of the techniques of the basic sciences; in other words,
it is the set of knowledge, considered as a whole, belonging to the
individual disciplines Clinical Biochemistry, Clinical Immunology,
Clinical Microbiology, Clinical Parasitology and Laboratory Haematology (though in some countries Anatomical Pathology and Clinical Toxicology are also included).
But what is the name of this discipline? In the European Union
there are different names depending on the country. The most usual
names are: Clinical Analyses (e. g. in Spain), Clinical Biology (e. g.
in Belgium), Clinical Pathology (e.g. in Portugal), Laboratory
Diagnostic Pathology (e. g. in Italy), Laboratory Medicine (e. g. in
Germany), and Medical Biology (e. g. in France).
In my opinion, within the European Union — and ideally within
the world — a unique name to refer to this branch of scientific
knowledge should exist. This unique name should have two essential characteristics:
(i) to avoid any preponderance, it should be a name that is not
traditionally used in any country of the European Union, and
(ii) it should be a name not in conflict with the diversity of the
university background (graduates in biology, chemistry, medicine,
pharmacy, etc.) of the professionals of such activity.
A possible solution may be the name Clinical Laboratory Sciences. I strongly uphold this term because it has the above characteristics and is the most useful to describe this plural discipline.
This opinion is probably supported by many clinical laboratory professionals, as suggested from the public-opinion poll about the
preference between the slogans "Serving clinical laboratory science
worldwide" and "Serving laboratory medicine worldwide", proposed by the Journal of the International Federation of Clinical
Chemistry as a reaction to a Letter to the Editor (2). The votes
collected by H. J. Lin, chair of the Editorial Board of the journal,
were: 49 votes for "Serving clinical laboratory science worldwide",
and 10 votes for "Serving laboratory medicine worldwide" (Lin
HJ, personal communication, 1993).
Dealing with scientific matters, reason should always prevail
over sentiment!
References
1. Büttner J. Clinical chemistry: a professional field for physicians
and natural scientists in Europe. Eur J Clin Chem Clin Biochem
1991; 29:3-12.
2. Fuentes-Arderiu X, Castineiras-Lacambra MJ. Laboratory medicine or clinical laboratory sciences? J Int Fed Clin Chem
1992; 4:136.
Received October JO, 1995
Corresponding author: Dr. X. Fuentes-Arderiu, Servei de
Bioquimica Clinica, Ciutat Sanitaria i Universitaria de Bellvitge,
E-08907 L'Hospitalet de Llobregat, Barcelona, Spain