The Chromosome Cycle and the Centrosome Cycle in the Mitotic Cycle

doi:10.1016/S0074-7696(08)61698-8

International Review of Cytology

Volume 100, 1987, Pages 49-92

https://doi.org/10.1016/S0074-7696(08)61698-8 Get rights and content

“Possible, but not interesting,” Lonnrot answered. “You'll reply that reality hasn't the least obligation to be interesting. And I'll answer you that reality may avoid that obligation but that hypotheses may not.”

Jorge Luis Borges, “Death and the Compass”

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The centrosome can and does change its molecular configuration. Besides serving as a MTOC and creating the mitotic spindle, there are several reasons to think that the centrosome/microtubule system controls the relationships between cell growth and cell division, just as Daniel Mazia hypothesized (Mazia, 1987, 1993; Hinchcliffe et al., 2001; Anastassiia et al., 2016; Lyons, 2020). In spite of a great deal of research on the centrosome and the cell cycle that supports the cell body concept, the use of the term is absent from the literature.
Symbiosis is a major evolutionary force, especially at the cellular level. Here we discuss several older and new discoveries suggesting that besides mitochondria and plastids, eukaryotic nuclei also have symbiotic origins. We propose an archaea-archaea scenario for the evolutionary origin of the eukaryotic cells. We suggest that two ancient archaea-like cells, one based on the actin cytoskeleton and another one based on the tubulin-centrin cytoskeleton, merged together to form the first nucleated eukaryotic cell. This archaeal endosymbiotic origin of eukaryotic cells and their nuclei explains several features of eukaryotic cells which are incompatible with the currently preferred autogenous scenarios of eukaryogenesis.
Centromere Dysfunction Compromises Mitotic Spindle Pole Integrity
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In any case, these mis-localized chromosomes would skip the opportunity to be incorporated into the main daughter nuclei and form MN. This surprising impact of centromere dysfunction on centrosome integrity offers new perspectives on the idea initially proposed by D. Mazia [28] on the coordination between the chromosome cycle with centrosomes and possibly other distant organelles even if in distinct compartments. Further information and requests for resources and reagents should be directed to and will be fulfilled by the Lead Contact, Renata Basto ([email protected]).
Centromeres and centrosomes are crucial mitotic players. Centromeres are unique chromosomal sites characterized by the presence of the histone H3-variant centromere protein A (CENP-A) [1]. CENP-A recruits the majority of centromere components, collectively named the constitutive centromere associated network (CCAN) [2]. The CCAN is necessary for kinetochore assembly, a multiprotein complex that attaches spindle microtubules (MTs) and is required for chromosome segregation [3]. In most animal cells, the dominant site for MT nucleation in mitosis are the centrosomes, which are composed of two centrioles, surrounded by a protein-rich matrix of electron-dense pericentriolar material (PCM) [4]. The PCM is the site of MT nucleation during mitosis [5]. Even if centromeres and centrosomes are connected via MTs in mitosis, it is not known whether defects in either one of the two structures have an impact on the function of the other. Here, using high-resolution microscopy combined with rapid removal of CENP-A in human cells, we found that perturbation of centromere function impacts mitotic spindle pole integrity. This includes release of MT minus-ends from the centrosome, leading to PCM dispersion and centriole mis-positioning at the spindle poles. Mechanistically, we show that these defects result from abnormal spindle MT dynamics due to defective kinetochore-MT attachments. Importantly, restoring mitotic spindle pole integrity following centromere inactivation lead to a decrease in the frequency of chromosome mis-segregation. Overall, our work identifies an unexpected relationship between centromeres and maintenance of the mitotic pole integrity necessary to ensure mitotic accuracy and thus to maintain genetic stability.
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Apoptosis, a form of programmed cell death, is responsible for eliminating damaged or unnecessary cells in multicellular organisms. Various types of intracellular stress trigger apoptosis by induction of cytochrome c release from mitochondria into the cytosol. Apoptotic protease activating factor-1 (Apaf-1) is a key molecule in the intrinsic or mitochondrial pathway of apoptosis, which oligomerizes in response to cytochrome c release and forms a large complex known as apoptosome. Procaspase-9, an initiator caspase in the mitochondrial pathway, is recruited and activated by the apoptosome leading to downstream caspase-3 processing. Various cellular proteins and small molecules can modulate apoptosome formation and function directly or indirectly. Despite recent progress in understanding the mitochondrial pathway of apoptosis, numerous questions such as the molecular mechanism of Apaf-1 oligomerization and caspase-9 activation remain poorly understood. In addition, reports have emerged showing non-apoptotic functions for Apaf-1. The current review summarizes the latest findings regarding structure-function relationship of Apaf-1 as well as its modifiers.
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The replication of these centrioles underlies the one-to-two duplication of the centrosome as a whole, and increases the amount of PCM present at the centrosome (Hinchcliffe and Sluder, 2001a; Nigg, 2007; Strnad and Gönczy, 2008). In preparation for mitosis, the pairs of duplicated centrioles split apart and separate (Figure 6.2), each daughter centrosome remains associated with at least some of the interphase microtubule network, causing this network to split into two (Mazia, 1987; Rosenblatt, 2005; Hinchcliffe, 2011). As the two centrosomes segregate apart, the single MTOC becomes two foci, and the nucleating capacity of each centrosome increases via a cell cycle-dependent accumulation of γ-TURCs (Dictenberg et al., 1998; Khodjakov and Rieder, 1999; Haren et al., 2009; Zhang et al., 2009; Lee and Rhee, 2011).
The assembly of a bipolar spindle lies at the heart of mitotic chromosome segregation. In animal somatic cells, the process of spindle assembly involves multiple complex interactions between various cellular compartments, including an emerging antiparallel microtubule network, microtubule-associated motor proteins and spindle assembly factors, the cell’s cortex, and the chromosomes themselves. The result is a dynamic structure capable of aligning pairs of sister chromatids, sensing chromosome misalignment, and generating force to segregate the replicated genome into two daughters. Because the centrosome lies at the center of the array of microtubule minus-ends, and the essential one-to-two duplication of the centrosome prior to mitosis is linked to cell cycle progression, this organelle has long been implicated as a device to generate spindle bipolarity. However, this classic model for spindle assembly is challenged by observations and experimental manipulations demonstrating that acentrosomal cells can and do form bipolar spindles, both mitotic and meiotic. Indeed, recent comprehensive proteomic analysis of centrosome-dependent versus independent mitotic spindle assembly mechanisms reveals a large, common set of genes required for both processes, with very few genes needed to differentiate between the two. While these studies cast doubt on an absolute role for the centrosome in establishing spindle polarity, it is clear that having too few or too many centrosomes results in abnormal chromosome segregation and aneuploidy. Here we review the case both for and against the role of the centrioles and centrosomes in ensuring proper assembly of a bipolar spindle, an essential element in the maintenance of genomic stability.
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The Chromosome Cycle and the Centrosome Cycle in the Mitotic Cycle

Cell

Cell

Biophys. J.

Int. Rev. Cytol.

Biochim. Biophys. Acta

Exp. Cell Res.

Exp. Cell Res.

Exp. Cell Res.

Int. Rev. Cytol.

Exp. Cell Res.

Dev. Biol.

J. Biol. Chem.

Dev. Biol.

Cell

Cell Biol. Int. Rep.

Exp. Cell Res.

Int. Rev. Cytol.

Cell Biol. Int. Rep.

Exp. Cell Res.

Int. Rev. Cytol.

Int. Rev. Cytol.

Cell

Cell

Int. Rev. Cytol. Suppl.

Cold Spring Harbor Symp. Quant. Biol.

Cold Spring Harbor Symp. Quant. Biol.

“Zellen-studien II. Die Befruchtung und Teilung des Eies von Ascaris megalocephala.”

“Zellen-studien IV. Ueber die Natur der Centrosomen”

Cold Spring Harbor Symp. Quant. Biol.

J. Cell Biol.

Ann. Rev. Genet.

J. Cell Biol.

Cell

J. Cell Sci. Suppl.

Cell Struct. Fund.

Dev. Growth Differ.

J. Cell Biol.

Arch. Microsc. Anat.

Anatomiseher Anzeiger

Int. Rev. Cytol. Suppl.

J. Cell Biol.