Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster

doi:10.1016/0092-8674(81)90167-7

Cell

Volume 25, Issue 3, September 1981, Pages 591-602

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Abstract

An electron microscopic investigation of kinetochore structure during the first meiotic division in male Drosophila melanogaster is presented. The data suggest that the structure that is responsible for initial microtubule attachment and chromosome orientation is a single, bilaminar hemisphere on each half-bivalent. Following the initial attachment this structure undergoes morphogenesis to a double-disc structure that reflects the underlying duality of sister chromatids in the half-bivalent. Thus these data support Darlington's idea that sister chromatids disjoin to the same spindle pole because they share a single kinetochore. Additionally, these data suggest that the meiotic mutations ord and mei-S332 sometimes cause premature “doubling” of the kinetochore region though, as discussed, possibly for a trivial reason.

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Separase cleaves the kinetochore protein Meikin at the meiosis I/II transition
2021, Developmental Cell
Citation Excerpt :
During anaphase I, cohesin on the chromosome arms is removed to allow homolog separation, whereas cohesin complexes at pericentromeric regions are critical for holding sister chromatids together and must be retained until anaphase II (Marston and Amon, 2004). Third, instead of binding to opposing spindle poles as they do in mitosis, the kinetochores of sister chromatids co-orient, fusing into a single microtubule-binding entity, to connect to microtubules from the same spindle pole during meiosis I (Chiang et al., 2010; Goldstein, 1981; Li and Dawe, 2009; Sarangapani et al., 2014). The meiosis-specific proteins and activities that contribute to protecting pericentromeric cohesin and promoting sister kinetochore co-orientation to enable this alternative division strategy remain important areas of investigation.
To generate haploid gametes, germ cells undergo two consecutive meiotic divisions requiring key changes to the cell division machinery. Here, we demonstrate that the protease separase rewires key cell division processes at the meiosis I/II transition by cleaving the meiosis-specific protein Meikin. Separase proteolysis does not inactivate Meikin but instead alters its function to create a distinct activity state. Full-length Meikin and the C-terminal Meikin separase cleavage product both localize to kinetochores, bind to Plk1 kinase, and promote Rec8 cleavage, but our results reveal distinct roles for these proteins in controlling meiosis. Mutations that prevent Meikin cleavage or that conditionally inactivate Meikin at anaphase I result in defective meiosis II chromosome alignment in mouse oocytes. Finally, as oocytes exit meiosis, C-Meikin is eliminated by APC/C-mediated degradation prior to the first mitotic division. Thus, multiple regulatory events irreversibly modulate Meikin activity during successive meiotic divisions to rewire the cell division machinery at two distinct transitions.
Repositioning of aurora b promoted by chiasmata ensures sister chromatid mono-orientation in meiosis i
2011, Developmental Cell
Citation Excerpt :
Meiosis is a unique type of cell division that allows halving of the chromosome number (Page and Hawley, 2003). In meiosis I, the cohesin-dependent association of sister DNA at the core centromere causes close juxtaposition or fusion of sister kinetochores and biases them geometrically toward the same spindle pole (mono-orientation) (Goldstein, 1981; Li and Dawe, 2009; Sakuno et al., 2009). In fission yeast, this “kinetochore cohesion” is established depending on the meiotic kinetochore protein Moa1 as well as the meiotic cohesin complex including Rec8 (Sakuno et al., 2009; Yokobayashi and Watanabe, 2005).
During meiosis I, kinetochores of sister chromatids are juxtaposed or fused and mono-orient, while homologous chromosomes that are paired by chiasmata (bivalents) have to biorient. In the absence of chiasmata, biorientation of sister chromatids (univalents), which carries a risk of aneuploidy, has been occasionally detected in several species, including humans. We show in fission yeast that biorientation of fused sister kinetochores predominates during early prometaphase I. Without chiasmata, this undesirable biorientation of univalents persists and eventually evades the spindle assembly checkpoint, provoking abnormal anaphase. When univalents are connected by chiasmata or by an artificial tether, this erroneous attachment is converted to monopolar attachment and stabilized. This stabilization is apparently achieved by a chromosome configuration that brings kinetochores to the outer edge of the bivalent, while bringing Aurora B, a destabilizer of kinetochore-microtubule attachment, inward. Our results elucidate how chiasmata favor biorientation of bivalents over that of univalents at meiosis I.
The Four Causes: The Functional Architecture of Centromeres and Kinetochores
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Direct evaluation of cohesin-mediated sister kinetochore associations at meiosis I in fission yeast
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Meiosis I Kinase Regulators: Conserved Orchestrators of Reductional Chromosome Segregation
2020, BioEssays
Advances and surprises in a decade of oocyte meiosis research
2020, Essays in Biochemistry

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^∗: Present address: Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, Colorado 80309.

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Abstract

References (33)

Ultrastructure of cell division in insect spermatogenesis

J. Ultrastruc. Res.

The structure of the kinetochore in meiosis and mitosis in Urechis eggs

Exp. Cell Res.

Kinetochore-to-pole connections during prometaphase of the meiotic divisions in Urechis eggs

Exp. Cell Res.

Fine structure of meiotic chromosomes

Functional morphology of the kinetochore

Int. Rev. Cytol. Suppl.

The genetic control of meiosis

Ann. Rev. Genet.

Die Spermatocytenteilungen der Tipuliden: III. Das Fewegungsverhalten der Chromosomen in Translokation heterozygoten von Tipula oleracea

Chromosoma

Polarity of microtubules nucleated by centrosomes and chromosomes of Chinese hamster ovary cells in vitro

J. Cell Biol.

The ultrastructure of the kinetochores of Lilium longiflorum during the first meiotic division

Caryologia (Firenze)

Normal spermatogenesis in Drosophila

Recent advances in cytology

Genetic analysis of a meiotic mutant resulting in precocious sister-centromere separation in Drosophila melanogaster

Molec. Gen. Genet.

Bildung and Bedeutung der Zentriolen: Eine Studie und Neuinterpretation der Meiose von Drosophila melanogaster

Cytobiologie

Mechanisms of chromosome orientation revealed by two meiotic mutants in Drosophila melanogaster

Chromosoma

The lamellar systems of cytoplasmic membranes in dividing spermatogenic cells of Drosophila virilis

J. Biophys. Biochem. Cytol.

Cytological evaluation of differential radiosensitivity in spermatogenous cells in Drosophila

Cited by (101)

Separase cleaves the kinetochore protein Meikin at the meiosis I/II transition

Repositioning of aurora b promoted by chiasmata ensures sister chromatid mono-orientation in meiosis i

The Four Causes: The Functional Architecture of Centromeres and Kinetochores

Direct evaluation of cohesin-mediated sister kinetochore associations at meiosis I in fission yeast

Meiosis I Kinase Regulators: Conserved Orchestrators of Reductional Chromosome Segregation

Advances and surprises in a decade of oocyte meiosis research

Cell

ArticleKinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster

Abstract

J. Ultrastruc. Res.

Exp. Cell Res.

Exp. Cell Res.

Functional morphology of the kinetochore

Int. Rev. Cytol. Suppl.

The genetic control of meiosis

Ann. Rev. Genet.

Die Spermatocytenteilungen der Tipuliden: III. Das Fewegungsverhalten der Chromosomen in Translokation heterozygoten von Tipula oleracea

Chromosoma

Polarity of microtubules nucleated by centrosomes and chromosomes of Chinese hamster ovary cells in vitro

J. Cell Biol.

The ultrastructure of the kinetochores of Lilium longiflorum during the first meiotic division

Caryologia (Firenze)

Normal spermatogenesis in Drosophila

Recent advances in cytology

Genetic analysis of a meiotic mutant resulting in precocious sister-centromere separation in Drosophila melanogaster

Molec. Gen. Genet.

Bildung and Bedeutung der Zentriolen: Eine Studie und Neuinterpretation der Meiose von Drosophila melanogaster

Cytobiologie

Mechanisms of chromosome orientation revealed by two meiotic mutants in Drosophila melanogaster

Chromosoma

The lamellar systems of cytoplasmic membranes in dividing spermatogenic cells of Drosophila virilis

J. Biophys. Biochem. Cytol.

Cytological evaluation of differential radiosensitivity in spermatogenous cells in Drosophila

Article
Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster