Microtubule-driven nuclear rotations promote meiotic chromosome dynamics

Christophorou, Nicolas; Rubin, Thomas; Bonnet, Isabelle; Piolot, Tristan; Arnaud, Marion; Huynh, Jean‐René

doi:10.1038/ncb3249

Cited by 64 publications

(83 citation statements)

References 72 publications

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“…Cytoskeletal network remodeling is critical for maintaining mechanical stability and implementing the biological function of cells that are exposed to gravity. In cell meiosis, microtubules can also drive the nuclear rotation, mainly via SUN (Sad1p, UNC-84) at the nuclear envelope (38). Compression-resisted microtubules are ductile materials with a self-healing feature and lattice plasticity, which enables the adaptation of microtubules to mechanical stress via forced softening or stiffening (39).…”

Section: Discussionmentioning

confidence: 99%

Mechanical remodeling of normally sized mammalian cells under a gravity vector

et al. 2016

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Translocation of the dense nucleus along a gravity vector initiates mechanical remodeling of a cell, but the underlying mechanisms of cytoskeletal network and focal adhesion complex (FAC) reorganization in a mammalian cell remain unclear. We quantified the remodeling of an MC3T3-E1 cell placed in upward-, downward-, or edgeon-orientated substrate. Nucleus longitudinal translocation presents a high value in downward orientation at 24 h or in edge-on orientation at 72 h, which is consistent with orientation-dependent distribution of perinuclear actin stress fibers and vimentin cords. Redistribution of total FAC area and fractionized super mature adhesion number coordinates this dependence at short duration. This orientation-dependent remodeling is associated with nucleus flattering and lamin A/C phosphorylation. Actin depolymerization or Rho-associated protein kinase signaling inhibition abolishes the orientation dependence of nucleus translocation, whereas tubulin polymerization inhibition or vimentin disruption reserves the dependence. A biomechanical model is therefore proposed for integrating the mechanosensing of nucleus translocation with cytoskeletal remodeling and FAC reorganization induced by a gravity vector.-Zhang, C., Zhou, L., Zhang, F., Lü, D., Li, N., Zheng, L., Xu, Y., Li, Z., Sun, S., Long, M. Mechanical remodeling of normally-sized mammalian cells under gravity vector. FASEB J. 31, 000-000 (2017). www.fasebj.org KEY WORDS: gravity-directed • mechanosensing • nucleus translocation • cytoskeletal remodeling • FAC reorganization Cells on Earth are subject to a variety of mechanical forces, including gravity. Statolith, or amyloplast, has long been assumed to be a gravity receptor for plant species to sense, transduce, and respond to altered gravity (1); however, little is known about mechanisms that underlie gravisensing and gravitransduction in mammalian cells, even though a body of evidence confirms the effect of gravity on their biological responses (2). Conceptual studies have indicated that the spreading and mitosis of normally sized (;10 1 mm) mammalian cells are sensitive to the change in gravity vector. For example, randomizing the direction of gravity has no effect on the division orientation of Chinese hamster ovary cells that are point-attached in a vertical plane (3). Inversion of culture substrate cannot alter the number and function of attached osteoblasts, even though an immediate response-diminished viable osteoblast number-is observed in sparse, early cultures (4). Cell area, nucleus translocation, cell cycle, and F-actin reorganization vary significantly in a duration-dependent manner when Ros 17/2.8 cells make up a monolayer and are spread on downward-or edge-on-orientated substrate compared with those on an upward orientation (5). More quantitative analysis is observed in large-sized Xenopus oocytes (;1 mm), where the nucleolus sedimentation is dominant compared with the thermal fluctuation at gravity potential . thermal energy scale (6), which implies that the sediment...

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Section: Discussionmentioning

confidence: 99%

Mechanical remodeling of normally sized mammalian cells under a gravity vector

et al. 2016

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“…Interestingly, some species have developed a variation on this zygotene bouquet theme. In Drosophila, chromosome pairing occurs during the mitotic divisions that precede meiosis and utilizes centromeres instead of telomeres (Christophorou et al, 2015; Christophorou et al, 2013; Lake & Hawley, 2012). In C. elegans , pairing occurs during meiosis, but telomeres are again replaced by other specialized chromosomal regions, called pairing centers (Sato et al, 2009).…”

Section: The Zygotene Chromosomal Bouquetmentioning

confidence: 99%

“…In C. elegans , pairing occurs during meiosis, but telomeres are again replaced by other specialized chromosomal regions, called pairing centers (Sato et al, 2009). However, even in these non-conventional forms of pairing, chromosomal movements still depend on microtubules via the same chromosome-SUN/KASH-microtubule connection (Christophorou et al, 2015; Hiraoka & Dernburg, 2009; Penkner et al, 2009; Sato et al, 2009). An exception to this mechanism is exhibited in S. cerevisiae , where actin and not microtubules are required for bouquet formation and synapsis (Trelles-Sticken et al, 2005).…”

Section: The Zygotene Chromosomal Bouquetmentioning

confidence: 99%

Coordination of cellular differentiation, polarity, mitosis and meiosis – New findings from early vertebrate oogenesis

Elkouby

Mullins

2017

Developmental Biology

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A mechanistic dissection of early oocyte differentiation in vertebrates is key to advancing our knowledge of germline development, reproductive biology, the regulation of meiosis, and all of their associated disorders. Recent advances in the field include breakthroughs in the identification of germline stem cells in Medaka, in the cellular architecture of the germline cyst in mice, in a mechanistic dissection of chromosomal pairing and bouquet formation in meiosis in mice, in tracing oocyte symmetry breaking to the chromosomal bouquet of meiosis in zebrafish, and in the biology of the Balbiani body, a universal oocyte granule. Many of the major events in early oogenesis are universally conserved, and some are co-opted for species-specific needs. The chromosomal events of meiosis are of tremendous consequence to gamete formation and have been extensively studied. New light is now being shed on other aspects of early oocyte differentiation, which were traditionally considered outside the scope of meiosis, and their coordination with meiotic events. The emerging theme is of meiosis as a common groundwork for coordinating multifaceted processes of oocyte differentiation. In an accompanying manuscript we describe methods that allowed for investigations in the zebrafish ovary to contribute to these breakthroughs. Here, we review these advances mostly from the zebrafish and mouse. We discuss oogenesis concepts across established model organisms, and construct an inclusive paradigm for early oocyte differentiation in vertebrates.

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“…In addition to obstructing nucleus expansion, microtubules could be more directly involved in the regulation of chromatin rearrangements across the nuclear membrane. Mechanical forces can regulate chromatin organization (Miroshnikova et al, 2017), and microtubules can act specifically on chromatin across the nuclear membrane (Hampoelz et al, 2011;King et al, 2008), facilitating the pairing of homologous chromosomes (Christophorou et al, 2015), driving the positioning of chromosome territories and clustering of telomeres or centromeres beneath the centrosome (Elkouby et al, 2016;King et al, 2008). Thus, microtubules could direct chromatin reorganization during nucleus expansion in myeloid progenitors.…”

Section: Discussionmentioning

confidence: 99%

Microtubules deform the nucleus and force chromatin reorganization during early differentiation of human hematopoietic stem cells

Biedzinski

Faivre²,

Vianay

et al. 2019

Preprint

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Hematopoietic stem cells (HSC) can differentiate into all hematopoietic lineages to support hematopoiesis. Cells from the myeloid and lymphoid lineages fulfill distinct functions with specific shapes and intra-cellular architectures. The role of cytokines in the regulation of HSC differentiation has been intensively studied but our understanding of the potential contribution of inner cell architecture is relatively poor. Here we show that large invaginations are generated by microtubule constraints on the swelling nucleus of human HSCs during early commitment toward the myeloid lineage. These invaginations are associated with chromatin reorganization, local loss of H3K9 trimethylation and changes in expression of specific hematopoietic genes. This establishes the role of microtubules in defining the unique lobulated nuclear shape observed in myeloid progenitor cells and suggests that this shape is important to establish the gene expression profile specific to this hematopoietic lineage. It opens new perspectives on the implications of microtubule-generated forces, in the early specification of the myeloid lineage.

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Microtubule-driven nuclear rotations promote meiotic chromosome dynamics

Cited by 64 publications

References 72 publications

Mechanical remodeling of normally sized mammalian cells under a gravity vector

Mechanical remodeling of normally sized mammalian cells under a gravity vector

Coordination of cellular differentiation, polarity, mitosis and meiosis – New findings from early vertebrate oogenesis

Microtubules deform the nucleus and force chromatin reorganization during early differentiation of human hematopoietic stem cells

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