Focal adhesion kinase as a mechanotransducer during rapid brain growth of the chick embryo

Desmond, Mary E.; Knepper, Janice E.; DiBenedetto, Angela J.; Malaugh, Elizabeth; Callejo, Sagrario; Carretero, Raquel; Alonso, Manuel García; Gato, Á.

doi:10.1387/ijdb.130305md

Cited by 18 publications

(28 citation statements)

References 43 publications

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“…S2). We also note that uniform growth is not consistent with previously documented proliferation patterns (Gutzman and Sive, 2010; Layer and Sporns, 1987; Takamatsu and Fujita, 1987; Weikert et al, 1990), and predefined growth (uniform or patterned) does not predict documented increases in cell proliferation due to pressure (Desmond and Jacobson, 1977; Desmond et al, 2014, 2005). …”

Section: Discussioncontrasting

confidence: 75%

“…This idea is supported by multiple studies showing growth of the BT depends on eCSF pressure: Eliminating lumen pressure via intubation slows growth considerably (Desmond and Jacobson, 1977) (Fig. 5), and abnormally high pressure increases proliferation (Alonso et al, 1998; Desmond et al, 2014). Cell proliferation has been shown to increase with the degree of mechanical tension in tissues such as blood vessels and epithelia (Lehoux et al, 2005; Wyatt et al, 2015).…”

Section: Discussionmentioning

confidence: 74%

“…In Xenopus, Hens and DeSimone (1995) found FAK transcripts localized in the forebrain, midbrain, hindbrain, and optic vesicle. In the chick embryo, Desmond et al (2014) showed that FAK and cell proliferation were upregulated and activated by eCSF pressure. The stress and growth patterns predicted by our model are consistent with these data (Figs.…”

Section: Discussionmentioning

confidence: 99%

“…Yet evidence also suggests alternative or supplementary roles for pressure and growth (Gutzman and Sive, 2010; Lowery and Sive, 2009). Pressure from the eCSF inflates the brain tube viscoelastically and increases growth of the neuroepithelium (Alonso et al, 1998; Desmond and Jacobson, 1977; Desmond et al, 2014; Goodrum and Jacobson, 1981). Studies have also revealed increased proliferation in vesicles and dorsal regions of the normal embryonic chick brain (Layer and Sporns, 1987; Takamatsu and Fujita, 1987;Weikert et al, 1990).…”

Section: Introductionmentioning

confidence: 99%

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Contraction and stress-dependent growth shape the forebrain of the early chicken embryo

Garcia

Okamoto

Bayly

et al. 2017

Journal of the Mechanical Behavior of Biomedical Materials

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During early vertebrate development, local constrictions, or sulci, form to divide the forebrain into the diencephalon, telencephalon, and optic vesicles. These partitions are maintained and exaggerated as the brain tube inflates, grows, and bends. Combining quantitative experiments on chick embryos with computational modeling, we investigated the biophysical mechanisms that drive these changes in brain shape. Chemical perturbations of contractility indicated that actomyosin contraction plays a major role in the creation of initial constrictions (Hamburger-Hamilton stages HH11–12), and fluorescent staining revealed that F-actin is circumferentially aligned at all constrictions. A finite element model based on these findings shows that the observed shape changes are consistent with circumferential contraction in these regions. To explain why sulci continue to deepen as the forebrain expands (HH12–20), we speculate that growth depends on wall stress. This idea was examined by including stress-dependent growth in a model with cerebrospinal fluid pressure and bending (cephalic flexure). The results given by the model agree with observed morphological changes that occur in the brain tube under normal and reduced eCSF pressure, quantitative measurements of relative sulcal depth versus time, and previously published patterns of cell proliferation. Taken together, our results support a biphasic mechanism for forebrain morphogenesis consisting of differential contractility (early) and stress-dependent growth (late).

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Section: Discussioncontrasting

confidence: 75%

Section: Discussionmentioning

confidence: 74%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Contraction and stress-dependent growth shape the forebrain of the early chicken embryo

Garcia

Okamoto

Bayly

et al. 2017

Journal of the Mechanical Behavior of Biomedical Materials

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“…Further research should investigate how this osmotic mechanism is regulated during development and how it is coordinated with neuroepithelial growth in order to contribute to normal brain development. A recent study (27) made a step in this direction by proposing focal adhesion kinases (FAKs) as a link between CSF pressure and neuroepithelial precursors replication.…”

Section: Specific Roles Of Embryonic Csf: the Interaction With The Nementioning

confidence: 99%

Embryonic cerebrospinal fluid in brain development: neural progenitor control

et al. 2014

Self Cite

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Due to the effort of several research teams across the world, today we have a solid base of knowledge on the liquid contained in the brain cavities, its composition, and biological roles. Although the cerebrospinal fluid (CSF) is among the most relevant parts of the central nervous system from the physiological point of view, it seems that it is not a permanent and stable entity because its composition and biological properties evolve across life. So, we can talk about different CSFs during the vertebrate life span. In this review, we focus on the CSF in an interesting period, early in vertebrate development before the formation of the choroid plexus. This specific entity is called “embryonic CSF.” Based on the structure of the compartment, CSF composition, origin and circulation, and its interaction with neuroepithelial precursor cells (the target cells) we can conclude that embryonic CSF is different from the CSF in later developmental stages and from the adult CSF. This article presents arguments that support the singularity of the embryonic CSF, mainly focusing on its influence on neural precursor behavior during development and in adult life.

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FGF2/EGF contributes to brain neuroepithelial precursor proliferation and neurogenesis in rat embryos: the involvement of embryonic cerebrospinal fluid

Lamus

Martín

Carnicero

et al. 2019

Developmental Dynamics

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BackgroundAt the earliest stages of brain development, the neuroepithelium works as an interdependent functional entity together with cerebrospinal fluid, which plays a key regulatory role in neuroepithelial cell survival, replication and neurogenesis; however, the underlying mechanism remains unknown in mammals.ResultsWe show the presence of fibroblast growth factor 2 (FGF2) and epidermal growth factor (EGF), in 13.5‐day rat embryo cerebrospinal fluid (eCSF). Immunohistochemical detection of FGF2 expression localized this factor inside neuroepithelial precursors close to the neuroepithelial‐CSF interface, suggesting that FGF2 from eCSF could originate in the neuroepithelium by apical secretion. The colocalization of FGFR1 and FGF2 in some neuroepithelial cells close to the ventricular surface suggests they are target cells for eCSF FGF2. Brain neuroepithelium EGF expression was negative. By using a neuroepithelial organotypic culture, we demonstrate that FGF2 and EGF from eCSF plays a specific role in triggering the self‐renewal and are involved in neurogenetic induction of mesencephalic neuroepithelial precursor cells during rat development.ConclusionsWe propose eCSF as an intercommunication medium for neuroepithelial precursor behavior control during early rat brain development, and the neuroepithelial regulation of FGF2 and EGF presence in eCSF, as a regulative mechanism controlling precursor proliferation and neurogenesis.

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Focal adhesion kinase as a mechanotransducer during rapid brain growth of the chick embryo

Cited by 18 publications

References 43 publications

Contraction and stress-dependent growth shape the forebrain of the early chicken embryo

Contraction and stress-dependent growth shape the forebrain of the early chicken embryo

Embryonic cerebrospinal fluid in brain development: neural progenitor control

FGF2/EGF contributes to brain neuroepithelial precursor proliferation and neurogenesis in rat embryos: the involvement of embryonic cerebrospinal fluid

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