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2017 ; 6
(1
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Mechanisms of Chromosome Congression during Mitosis
#MMPMID28218637
Maiato H
; Gomes AM
; Sousa F
; Barisic M
Biology (Basel)
2017[Feb]; 6
(1
): ä PMID28218637
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Chromosome congression during prometaphase culminates with the establishment of a
metaphase plate, a hallmark of mitosis in metazoans. Classical views resulting
from more than 100 years of research on this topic have attempted to explain
chromosome congression based on the balance between opposing pulling and/or
pushing forces that reach an equilibrium near the spindle equator. However, in
mammalian cells, chromosome bi-orientation and force balance at kinetochores are
not required for chromosome congression, whereas the mechanisms of chromosome
congression are not necessarily involved in the maintenance of chromosome
alignment after congression. Thus, chromosome congression and maintenance of
alignment are determined by different principles. Moreover, it is now clear that
not all chromosomes use the same mechanism for congressing to the spindle
equator. Those chromosomes that are favorably positioned between both poles when
the nuclear envelope breaks down use the so-called "direct congression" pathway
in which chromosomes align after bi-orientation and the establishment of end-on
kinetochore-microtubule attachments. This favors the balanced action of
kinetochore pulling forces and polar ejection forces along chromosome arms that
drive chromosome oscillatory movements during and after congression. The other
pathway, which we call "peripheral congression", is independent of end-on
kinetochore microtubule-attachments and relies on the dominant and coordinated
action of the kinetochore motors Dynein and Centromere Protein E (CENP-E) that
mediate the lateral transport of peripheral chromosomes along microtubules, first
towards the poles and subsequently towards the equator. How the opposite
polarities of kinetochore motors are regulated in space and time to drive
congression of peripheral chromosomes only now starts to be understood. This
appears to be regulated by position-dependent phosphorylation of both Dynein and
CENP-E and by spindle microtubule diversity by means of tubulin
post-translational modifications. This so-called "tubulin code" might work as a
navigation system that selectively guides kinetochore motors with opposite
polarities along specific spindle microtubule populations, ultimately leading to
the congression of peripheral chromosomes. We propose an integrated model of
chromosome congression in mammalian cells that depends essentially on the
following parameters: (1) chromosome position relative to the spindle poles after
nuclear envelope breakdown; (2) establishment of stable end-on
kinetochore-microtubule attachments and bi-orientation; (3) coordination between
kinetochore- and arm-associated motors; and (4) spatial signatures associated
with post-translational modifications of specific spindle microtubule
populations. The physiological consequences of abnormal chromosome congression,
as well as the therapeutic potential of inhibiting chromosome congression are
also discussed.
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