Cell and tissue morphology determine actin-dependent nuclear migration mechanisms in neuroepithelia

Yanakieva, Iskra; Erzberger, Anna; Matejčić, Marija; Modes, Carl D.; Norden, Caren

doi:10.1083/jcb.201901077

Cited by 47 publications

(55 citation statements)

References 67 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…(Bergert et al, 2015;Liu et al, 2015;Ruprecht et al, 2015). Similarly, neuroepithelial cells alter the subcellular distribution of actomyosin and adopt different force mechanisms during nuclear translocation depending on cell shape and tissue morphology (Yanakieva et al, 2019). It is thus possible that neurons might also adopt differential cytoskeletal dynamics depending on the extracellular mechanical environment.…”

Section: Actin-myosin Based Nuclear Translocationmentioning

confidence: 99%

Mechanical Regulation of Nuclear Translocation in Migratory Neurons

Nakazawa

Kengaku

2020

Front. Cell Dev. Biol.

View full text Add to dashboard Cite

Neuronal migration is a critical step during the formation of functional neural circuits in the brain. Newborn neurons need to move across long distances from the germinal zone to their individual sites of function; during their migration, they must often squeeze their large, stiff nuclei, against strong mechanical stresses, through narrow spaces in developing brain tissue. Recent studies have clarified how actomyosin and microtubule motors generate mechanical forces in specific subcellular compartments and synergistically drive nuclear translocation in neurons. On the other hand, the mechanical properties of the surrounding tissues also contribute to their function as an adhesive support for cytoskeletal force transmission, while they also serve as a physical barrier to nuclear translocation. In this review, we discuss recent studies on nuclear migration in developing neurons, from both cell and mechanobiological viewpoints.

show abstract

Section: Actin-myosin Based Nuclear Translocationmentioning

confidence: 99%

Mechanical Regulation of Nuclear Translocation in Migratory Neurons

Nakazawa

Kengaku

2020

Front. Cell Dev. Biol.

View full text Add to dashboard Cite

show abstract

“…Actin cables are utilized in other contexts, but in those cases nuclei are coupled to the actin cables used as tracks for nuclear transport (Folker et al, 2011;Luxton et al, 2010;Luxton et al, 2011). The retinal neuroepithelium in fish utilizes a different sort of formindependent actin network to push the nucleus apically, and cortex-anchored and bundled actin modulated by myosin may generate the pushing force (Yanakieva et al, 2019). Microtubule dependent pushing and pulling forces are also widely used to move nuclei (Adames and Cooper, 2000;Gönczy et al, 1999;Levy and Holzbaur, 2008;Tran et al, 2001;Zhao et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

A Diaphanous and Enabled dependent asymmetric actin cable array repositions nuclei during Drosophila oogenesis

McCartney

Logan

2020

Preprint

View full text Add to dashboard Cite

Cells reposition their nuclei for a diversity of specialized functions through a wide variety of cytoskeletal mechanisms. To complete oogenesis, Drosophila nurse cells employ novel actin cable arrays to reposition their nuclei. During oogenesis, 15 nurse cells connected by ring canals contract to dump their cytoplasmic contents into the oocyte. Just prior to dumping, actin cables initiate from the nurse cell cortex and elongate toward their nuclei, pushing them away from the ring canals to prevent obstruction. How the actin cable arrays generate directional nuclear movement is not known. We found regional differences in the actin cable growth rate that are dependent on the differential localization of the actin assembly factors Enabled (Ena) and Diaphanous (Dia). Mislocalization of Ena resulted in actin cable arrays with a uniform growth rate. In the absence of growth rate asymmetry, nuclear relocation was significantly altered and cytoplasmic dumping was incomplete. This novel mechanism for nuclear repositioning relies on the regulated cortical localization of Dia and Ena producing asymmetric actin cable arrays that push the nuclei away from the ring canals, enabling successful oogenesis.

show abstract

“…Recently, it has been shown that nuclei in the hindbrain start migrating from variable apicobasal positions and move toward the apical surface in a directed and smooth manner, and this movement is controlled by Rho-ROCK-dependent myosin contractility [27]. However, the mechanisms by which actin generates the forces required for apical nuclear movement and the link between forces and atoh1b are not understood.…”

Section: Discussionmentioning

confidence: 99%

The role ofatoh1genes in the development of the lower rhombic lip during zebrafish hindbrain morphogenesis

Belzunce

Pujades

2019

Preprint

View full text Add to dashboard Cite

BACKGROUND: The Lower Rhombic Lip (LRL) is a transient neuroepithelial structure of the dorsal hindbrain, which expands from r2 to r7, and gives rise to deep nuclei of the brainstem, such as the vestibular and auditory nuclei and most posteriorly the precerebellar nuclei. Although there is information about the contribution of specific proneural-progenitor populations to specific deep nuclei, and the distinct rhombomeric contribution, little is known about how progenitor cells from the LRL behave during neurogenesis and how their transition into differentiation is regulated. RESULTS:In this work, we investigated the atoh1 gene regulatory network operating in the specification of LRL cells, and the kinetics of cell proliferation and behavior of atoh1a-derivatives by using complementary strategies in the zebrafish embryo. We unveiled that atoh1a is necessary and sufficient for specification of LRL cells by activating atoh1b, which worked as a differentiation gene to transition progenitor cells towards neuron differentiation in a Notch-dependent manner. This cell state transition involved the release of atoh1a-derivatives from the LRL: atoh1a progenitors contributed first to atoh1b cells, which are committed non-proliferative precursors, and to the lhx2bneuronal lineage as demonstrated by cell fate studies and functional analyses. Using in vivo cell lineage approaches we showed that the proliferative cell capacity, as well as their mode of division, relied on the position of the atoh1a progenitors within the dorsoventral axis.CONCLUSIONS: Our data demonstrates that the zebrafish provides an excellent model to study the in vivo behavior of distinct progenitor populations to the final neuronal differentiated pools, and to reveal the subfunctionalization of ortholog genes. Here, we unveil that atoh1a behaves as the cell fate selector gene, whereas atoh1b functions as a neuronal differentiation gene, contributing to the lhx2b neuronal population. atoh1aprogenitor cell dynamics (cell proliferation, cell differentiation, and neuronal migration) relies on their position, demonstrating the challenges that progenitor cells face in computing positional information from a dynamic two-dimensional grid in order to generate the stereotyped neuronal structures in the embryonic hindbrain. BACKGROUNDThe assembly of functional neural circuits requires the specification of neuronal identities and the execution of developmental programs that establish precise neural network wiring. The generation of such cell diversity happens during embryogenesis, at the same time that the brain undergoes a dramatic transformation from a simple tubular structure, the neural tube, to a highly convoluted structure -the brain-, resulting in changes in the position of neuronal progenitors and their derivatives upon time. Thus, the coordination of progenitor proliferation and cell fate specification is central to tissue growth and maintenance. The comprehension of how neuronal heterogeneity is achieved implies the understanding of how the neurogenic capaci...

show abstract

Cell and tissue morphology determine actin-dependent nuclear migration mechanisms in neuroepithelia

Cited by 47 publications

References 67 publications

Mechanical Regulation of Nuclear Translocation in Migratory Neurons

Mechanical Regulation of Nuclear Translocation in Migratory Neurons

A Diaphanous and Enabled dependent asymmetric actin cable array repositions nuclei during Drosophila oogenesis

The role ofatoh1genes in the development of the lower rhombic lip during zebrafish hindbrain morphogenesis

Contact Info

Product

Resources

About