Nuclear migration events throughout development

Bone, Courtney R.; Starr, Daniel A.

doi:10.1242/jcs.179788

Cited by 110 publications

(117 citation statements)

References 161 publications

(163 reference statements)

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“…Nuclear positioning plays a role in development of a variety of cell types in vertebrates (37). In developing neuroepithelia, for example, nuclei of undifferentiated progenitors oscillate between the apical and the basal surfaces of polarized epithelia in synchrony with the cell cycle progression as a regulatory mechanism of cell division and differentiation, a process known as interkinetic nuclear migration (38).…”

Section: Discussionmentioning

confidence: 99%

Maturation arrest in early postnatal sensory receptors by deletion of the miR-183/96/182 cluster in mouse

Fan

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The polycistronic miR-183/96/182 cluster is preferentially and abundantly expressed in terminally differentiating sensory epithelia. To clarify its roles in the terminal differentiation of sensory receptors in vivo, we deleted the entire gene cluster in mouse germline through homologous recombination. The miR-183/96/ 182 null mice display impairment of the visual, auditory, vestibular, and olfactory systems, attributable to profound defects in sensory receptor terminal differentiation. Maturation of sensory receptor precursors is delayed, and they never attain a fully differentiated state. In the retina, delay in up-regulation of key photoreceptor genes underlies delayed outer segment elongation and possibly mispositioning of cone nuclei in the retina. Incomplete maturation of photoreceptors is followed shortly afterward by early-onset degeneration. Cell biologic and transcriptome analyses implicate dysregulation of ciliogenesis, nuclear translocation, and an epigenetic mechanism that may control timing of terminal differentiation in developing photoreceptors. In both the organ of Corti and the vestibular organ, impaired terminal differentiation manifests as immature stereocilia and kinocilia on the apical surface of hair cells. Our study thus establishes a dedicated role of the miR-183/96/182 cluster in driving the terminal differentiation of multiple sensory receptor cells. M ammalian sensory epithelia, such as those underlying vison, hearing, smell, and balance, consist of ciliated sensory receptor cells. Although highly specialized, similarities in embryonic origin underlie common features in their development (1). Following specification, lineage-restricted postmitotic precursors become structurally and functionally mature through a series of cellular differentiation events, collectively described as terminal differentiation (2). During maturation, sensory receptor cells typically develop microtubule-based primary cilia and in some cases actin-based membrane protrusions on apical membranes, which are sensory organelles, while maintaining apical basal polarity within sensory epithelia. In photoreceptors, for example, the extension of outer segments (OSs), specialized sensory cilia, is central to postmitotic differentiation and necessary for light sensitivity (3). In auditory and vestibular hair cells, the proper formation of hair bundles is indispensable for detecting sound and head positions (4). Similarly, olfactory sensory neurons (OSNs), the odorant receptor cells in the olfactory epithelium, project multiple dendritic cilia into the mucous membrane of the nasal epithelium where olfactory signaling is initiated (5). Mature sensory epithelia are highly structured with specific spatial organization that is tied to their functions. Synchronized planar cell polarity (PCP) of hair cells in the inner ear, for example, provides their directional sensitivity (6), whereas the development of laminar architecture in the retina restricts photoreceptors to proper compartments for efficient wiring with secondary neuro...

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Section: Discussionmentioning

confidence: 99%

Maturation arrest in early postnatal sensory receptors by deletion of the miR-183/96/182 cluster in mouse

Fan

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Two major roles of the LINC complex are nuclear anchoring and nuclear migration, 10,11,12 which is fundamental step for directional cell migration. Expression of a dominant-negative KASH in mouse MEF cells decreased directional cell migration, 36 suggesting that interaction(s) between SUN and nesprin is important for cell migration.…”

Section: Depletion Of Sun1 Suppresses Cell Migrationmentioning

confidence: 99%

“…[5][6][7][8][9] LINC complexes and nuclear lamins form a solid scaffold for diverse functions including nuclear migration, 10 nuclear shaping and positioning,. 11,12 maintaining the centrosome-nucleus connection, 13,14 mechanotransduction, 15,16 DNA repair, 17,18 nuclear membrane spacing, cancer, and recessive cerebellar ataxia.…”

Section: Introductionmentioning

confidence: 99%

SUN1 splice variants, SUN1_888, SUN1_785, and predominant SUN1_916, variably function in directional cell migration

Nishioka

Imaizumi

Imada

et al. 2016

Nucleus

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The LINC complex is a multifunctional protein complex that is involved in various processes at the nuclear envelope, such as nuclear migration, mechanotransduction and chromatin tethering in the meiotic phase. However, it remains unknown how these functions are regulated in different cell contexts. An inner nuclear membrane component of the LINC complex, SUN1, is ubiquitously expressed. The human SUN1 gene produces over 10 variants by alternative splicing. Although functions of SUN1 are relatively well characterized, functional differences among SUN1 splice variants are poorly characterized. LINC complex components are associated with a wide range of human diseases; therefore, it is important to understand the functional diversity among SUN1 splice variants. Here, we identified a novel human SUN1 splice variant, SUN1_888. overexpression of the SUN1 splice variants, SUN1_888 or SUN1_785, but not the predominant isoform, SUN1_916, activated directional cell migration. Knockdown of SUN1_888 suppressed cell migration; in contrast depletion of SUN1_916 activated cell migration. In addition, all of investigated SUN1 splicing variants rescued cell migration in SUN1 knock out cell. These results indicate that redundant and non-redundant functions of SUN1 splice variant in directional cell migration and suggest that variable LINC complexes with distinct task may exit. Furthermore, in contrast to previous studies, we showed association between SUN1 and B-type lamins. Interestingly, B-type lamin preferentially interacts with SUN1 but not SUN2. These results suggest that tissue-specific SUN1 variants variably interact with nucleoplasmic partners and allow variable assembly of LINC complexes that can be assigned to distinct tasks.

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“…These LINC complexes were shown to connect nuclei to elements of the cytoskeleton, with the cytoplasmic domains of KASH proteins binding to actin, a microtubule motor or intermediate filaments. On the nucleoplasmic side, SUN proteins bind to lamins, thus connecting the cytoskeleton to the nucleoskeleton (for recent reviews, see Tapley and Starr, 2013;Luxton and Starr, 2014;Kim et al, 2015;Bone and Starr, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…Their cytoplasmic domains consist of a variable length of spectrin-repeat domains, with some KASH proteins being very large, such as the giant isoforms of human nesprin-1 (Syne-1) with over 8000 amino acids. LINC complex functions in nuclear movement and positioning include pronuclear migration in fertilized eggs, cell-cycle-dependent nuclear oscillations during neuronal differentiation, nuclear repositioning during fibroblast migration, nuclear positioning during C. elegans embryo development, nuclear migration during Drosophila eye disk development, as well as meiotic chromosome movement to facilitate recombination (reviewed in Burke and Roux, 2009;Razafsky and Hodzic, 2009;Starr and Fridolfsson, 2010;Bone and Starr, 2016). There is also growing evidence that LINC complexes are connected to human diseases, such as Emery-Dreifuss muscular dystrophy, cerebellar ataxia, arthrogyrposis and hereditary hearing loss, and that they are involved in mechanical signal transduction (Lombardi and Lammerding, 2010;Banerjee et al, 2014;Guilluy et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

LINCing the eukaryotic tree of life – towards a broad evolutionary comparison of nucleocytoplasmic bridging complexes

Meier

2016

Journal of Cell Science

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The nuclear envelope is much more than a simple barrier between nucleoplasm and cytoplasm. Nuclear envelope bridging complexes are protein complexes spanning both the inner and outer nuclear envelope membranes, thus directly connecting the cytoplasm with the nucleoplasm. In metazoans, they are involved in connecting the cytoskeleton with the nucleoskeleton, and act as anchoring platforms at the nuclear envelope for the positioning and moving of both nuclei and chromosomes. Recently, nucleocytoplasmic bridging complexes have also been identified in more evolutionarily diverse organisms, including land plants. Here, I discuss similarities and differences among and between eukaryotic supergroups, specifically of the proteins forming the cytoplasmic surface of these complexes. I am proposing a structure and function for a hypothetical ancestral nucleocytoplasmic bridging complex in the last eukaryotic common ancestor, with the goal to stimulate research in more diverse emerging model organisms.

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Nuclear migration events throughout development

Cited by 110 publications

References 161 publications

Maturation arrest in early postnatal sensory receptors by deletion of the miR-183/96/182 cluster in mouse

Maturation arrest in early postnatal sensory receptors by deletion of the miR-183/96/182 cluster in mouse

SUN1 splice variants, SUN1_888, SUN1_785, and predominant SUN1_916, variably function in directional cell migration

LINCing the eukaryotic tree of life – towards a broad evolutionary comparison of nucleocytoplasmic bridging complexes

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