Blood—cerebrospinal fluid transfer of plasma proteins during fetal development in the sheep

Dzięgielewska, Katarzyna M.; Evans, Chris; Malinowska, Danuta H.; Møllgård, Kjeld; Reynolds, M. L.; Saunders, NR

doi:10.1113/jphysiol.1980.sp013172

Cited by 90 publications

(93 citation statements)

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“…On the other hand, E-CSF has a complex protein composition, and the exposure of the apical surface of neuroepithelial cells to this fluid could affect their behavior (Dziegielewska et al 1980a(Dziegielewska et al , 1980b(Dziegielewska et al , 1981(Dziegielewska et al , 1991(Dziegielewska et al , 2000Checiu et al, 1984;Gato et al, 2004). Experimental data demonstrate that the loss or modification of the composition of the E-CSF strongly decreases the neuronal cell population (Desmond and Jacobson, 1977;Desmond, 1985).…”

Section: E-csf Helps Control Cellular Behavior In Neuroepithelial Cellsmentioning

confidence: 95%

“…In this way, several studies have demonstrated that, during development, the most prevalent components of the E-CSF are proteins. Moreover, the fact that the protein fraction of the CSF is more complex in embryos than in adults, and that it is detected at higher concentrations, has led some authors to suggest that the E-CSF is involved in the regulation of neuroepithelial cell behavior (Dziegielewska et al, 1980b(Dziegielewska et al, , 2000Ojeda and Piedra, 2000;Miyan et al, 2003;Gato et al, 2004). In addition, it has been shown that E-CSF plays a key role in the expansion of the embryonic brain primordium at the earliest stages of development (Desmond and Jacobson, 1977;Desmond, 1985;Gato et al, 1993;Alonso et al, 1998Alonso et al, , 1999Desmond and Levitan, 2002).…”

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Embryonic cerebrospinal fluid regulates neuroepithelial survival, proliferation, and neurogenesis in chick embryos

et al. 2005

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Early in development, the behavior of neuroepithelial cells is controlled by several factors, which act in a developmentally regulated manner. Diffusible factors are secreted locally by the neuroepithelium itself, although other nearby structures may also be involved. Evidence suggests a physiological role for the cerebrospinal fluid in the development of the brain. Here, using organotypic cultures of chick embryo neuroepithelial explants from the mesencephalon, we show that the neuroepithelium in vitro is not able to self-induce cell survival, replication, and neurogenesis. We also show that the embryonic cerebrospinal fluid (E-CSF) promotes neuroepithelial stem cell survival and induces proliferation and neurogenesis in mesencephalic explants. These data strongly suggest that E-CSF is involved in the regulation of neuroepithelial cells behavior, supporting the hypothesis that this fluid plays a key role during the early development of the central nervous system.

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Section: E-csf Helps Control Cellular Behavior In Neuroepithelial Cellsmentioning

confidence: 95%

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confidence: 99%

Embryonic cerebrospinal fluid regulates neuroepithelial survival, proliferation, and neurogenesis in chick embryos

et al. 2005

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“…Thus in 60-day-old fetal sheep (Dziegielewska et al 1980 b) and in neonatal rats (Habgood, 1990), albumin CSF/plasma ratios are similar to those of inulin, but the molecular radius of albumin is some three times larger than inulin. Also the CSF/plasma ratios for individual proteins are not the same in spite of the fact that their molecular sizes are similar (Dziegielewska, Evans, Fossan, Lorscheider, Malinowska, M0llgard, Reynolds, Saunders & Wilkinson, 1980a;Dziegielewska et al 1980b). It has been noted in earlier experiments on developing sheep brain that different species of the same protein, e.g.…”

Section: Introductionmentioning

confidence: 99%

“…Most of the albumin permeability experiments were run for 3 h because previous studies in this preparation had shown that several exogenous proteins including human albumin approached a steady-state level in cisternal CSF by 3-6 h after i.v. injection of the protein solution (Dziegielewska et al 1980b (Fig. 2).…”

Section: Morphological Techniquesmentioning

confidence: 99%

“…It has been noted in earlier experiments on developing sheep brain that different species of the same protein, e.g. albumin, can be transferred across the choroid plexus to a different level (Dziegielewska et al 1980b). These observations imply that there may be a specific protein transfer mechanism present in the immature brain that disappears later in brain development.…”

Section: Introductionmentioning

confidence: 99%

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Species‐specific transfer of plasma albumin from blood into different cerebrospinal fluid compartments in the fetal sheep.

Dzięgielewska

Habgood

Møllgård

et al. 1991

The Journal of Physiology

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SUMMARY1. The blood-cerebrospinal fluid (CSF) transfer of endogenous sheep albumin and several exogenous species of albumin has been investigated in different CSF compartments of the immature fetal sheep brain, at an early stage of development (60 days gestation, term is 150 days) when the CSF concentration of total protein is high.2. There were marked differences in the steady-state CSF/plasma ratios for all species of albumin (including endogenous sheep albumin) between different CSF compartments. Ratios measured in the cisterna magna were significantly higher than those in the dorsal subarachnoid space, which in turn were higher than those in the lateral ventricles. The ratios for endogenous sheep albumin were (%; mean + S.E.M.): lateral ventricle (LV), 4 0 + 0 03; dorsal subarachnoid (DSA), 61 + 10; cisterna magna (CM), 13-7+08. 3. Three hours after i.v. injection, the CSF/plasma ratios for bovine albumin (LV, 2 0 + 0-2; DSA, 2 4 + 0-1; CM, 7 2 + 0-7 %) were significantly lower than the ratio for endogenous sheep albumin in all three compartments. The ratios for human albumin (LV, 0 7 + 0 2; DSA, 1P0 + 0-2; CM, 3 9 + 0-4 %) were significantly lower than those for bovine albumin.4. In all three CSF compartments, the endogenous sheep albumin ratios were higher than would be expected on the basis of transfer by passive mechanisms.Conversely, steady-state CSF/plasma ratios for [3H]sucrose and [14C]inulin were consistent with passive transfer, and there were no differences between the ratios for these markers measured in each of the three CSF regions. 7. Immunocytochemical evidence suggests that the route of transfer from blood to CSF is transcellular, through the choroid plexus epithelial cells.8. Regional variations in albumin ratios are probably due to differences in specific transfer into each CSF compartment. This is reflected in a differential immunocytochemical staining for albumin in choroid plexus epithelial cells from different regions of the brain.9. The results are discussed in terms of differences in albumin amino acid sequences, structural homologies, and transfer by a specific transcellular mechanism.

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Development of the choroid plexus

Dzięgielewska

Habgood

et al. 2000

Microsc. Res. Tech.

207

103

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Mammalian choroid plexuses develop at four sites in the roof of the neural tube shortly after its closure, in the order IVth, lateral, and IIIrd ventricles. Bone morphogenetic proteins and tropomyosin are involved in early specification of these sites and in early plexus growth. Four stages of lateral ventricular plexus development have been defined, based on human and sheep fetuses; these depend mainly on the appearance of epithelial cells and presence or absence of glycogen. Other plexuses and other species are probably similar, although marsupials may lack glycogen. Choroid plexuses form one of the blood‐brain barrier interfaces that control the brain's internal environment. The mechanisms involved combine a structural diffusion restraint (tight junctions between the plexus epithelial cells) and specific exchange mechanisms. In this review, it is argued that barrier mechanisms in the developing brain are different in important respects from those in the adult brain, but these differences do not necessarily reflect immaturity of the system. Absence of a barrier mechanism or presence of one not found in the adult may be a specialisation that is appropriate for that stage of brain development. Emphasis is placed on determining which mechanisms are present in the immature brain and relating them to brain development. One mechanism unique to the developing brain transfers specific proteins from blood to cerebrospinal fluid (CSF), via tubulocisternal endoplasmic reticulum in plexus epithelial cells. This results in a high concentration of proteins in early CSF. These proteins do not penetrate into brain extracellular space because of “strap” junctions between adjacent neuroependymal cells, which disappear later in development, when the protein concentration in CSF is much lower. Functions of the proteins in early CSF are discussed in terms of generation of a “colloid” osmotic pressure that expands the ventricular system as the brain grows; the proteins may also act as specific carriers and growth factors in their own right. The pathway for low molecular weight compounds, which is much more permeable in the developing choroid plexuses, appears also to be a transcellular one, rather than paracellular via tight junctions. There is thus good evidence to support a novel view of the state of development and functional significance of barrier mechanisms in the immature brain. It grows in an environment that is different from that of the rest of the fetus/neonate and that is also different in some respects from that of the adult. But these differences reflect developmental specialisation rather than immaturity. Microsc. Res. Tech. 52:5–20, 2001. © 2001 Wiley‐Liss, Inc.

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Blood—cerebrospinal fluid transfer of plasma proteins during fetal development in the sheep

Cited by 90 publications

References 27 publications

Embryonic cerebrospinal fluid regulates neuroepithelial survival, proliferation, and neurogenesis in chick embryos

Embryonic cerebrospinal fluid regulates neuroepithelial survival, proliferation, and neurogenesis in chick embryos

Species‐specific transfer of plasma albumin from blood into different cerebrospinal fluid compartments in the fetal sheep.

Development of the choroid plexus

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