The Developing Chicken Yolk Sac Acquires Nutrient Transport Competence by an Orchestrated Differentiation Process of Its Endodermal Epithelial Cells

Bauer, Raimund; Plieschnig, Julia A.; Finkes, Thomas; Riegler, Barbara; Hermann, Marcela; Schneider, Wolfgang J.

doi:10.1074/jbc.m112.393090

Cited by 67 publications

(105 citation statements)

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“…Acquisition of this function is a process which is coordinated with that of vascularization of the YS [26]. MTP has been identified in chicken YS [26,27], but the expression of MTP in fetal tissues has not been studied in detail yet.…”

Section: Introductionmentioning

confidence: 99%

Expression of microsomal triglyceride transfer protein in lipoprotein-synthesizing tissues of the developing chicken embryo

et al. 2014

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In contrast to mammals, in the chicken major sites of lipoprotein synthesis and secretion are not only the liver and intestine, but also the kidney and the embryonic yolk sac. Two key components in the assembly of triglyceride-rich lipoproteins are the microsomal triglyceride transfer protein (MTP) and apolipoprotein B (apoB). We have analyzed the expression of MTP in the embryonic liver, small intestine, and kidney, and have studied the expression of MTP in, and the secretion of apoB from, the developing yolk sac (YS). Transcript and protein levels of MTP increase during embryogenesis in YS, liver, kidney, and small intestine, and decrease in YS, embryonic liver, and kidney after hatching. In small intestine, the MTP mRNA level rises sharply during the last trimester of embryo development (after day 15), while MTP protein is detectable only after hatching (day 21). In the YS of 15- and 20-day old embryos, apoB secretion was detected by pulse-chase metabolic radiolabeling experiments and subsequent immunoprecipitation. Taken together, our data reveal the importance of coordinated production of MTP and apoB in chicken tissues capable of secreting triglyceride-rich lipoproteins even before hatching.

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Section: Introductionmentioning

confidence: 99%

Expression of microsomal triglyceride transfer protein in lipoprotein-synthesizing tissues of the developing chicken embryo

et al. 2014

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“…Taken together, our findings indicate that urea is produced in the endodermal layer of the YSM, and is then excreted into nearby blood vessels, and subsequently transferred to the embryo in order to maintain a high concentration of urea in the body fluid. Yolk sacs are found in many vertebrates, and the extra-embryonic YSM has been considered to play a key role in the absorption of yolk nutrients (Lambson, 1970;Diez and Davenport, 1990;Lechenault et al, 1993;Zohn and Sarkar, 2010;Bauer et al, 2013). An intriguing finding on the role of the YSM in teleost fish is that it is involved in osmoregulation during early development .…”

Section: Research Articlementioning

confidence: 99%

Urea-based osmoregulation in the developing embryo of oviparous cartilaginous fish (Callorhinchus milii): contribution of the extraembryonic yolk sac during the early developmental period

Takagi

Kajimura

Tanaka

et al. 2013

Journal of Experimental Biology

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Marine cartilaginous fish retain a high concentration of urea to maintain the plasma slightly hyperosmotic to the surrounding seawater. In adult fish, urea is produced by hepatic and extrahepatic ornithine urea cycles (OUCs). However, little is known about the urea retention mechanism in developing cartilaginous fish embryos. In order to address the question as to the mechanism of urea-based osmoregulation in developing embryos, the present study examined the gene expression profiles of OUC enzymes in oviparous holocephalan elephant fish (Callorhinchus milii) embryos. We found that the yolk sac membrane (YSM) makes an important contribution to the ureosmotic strategy of the early embryonic period. The expression of OUC enzyme genes was detectable in the embryonic body from at least stage 28, and increased markedly during development to hatching, which is most probably due to growth of the liver. During the early developmental period, however, the expression of OUC enzyme genes was not prominent in the embryonic body. Meanwhile, we found that the mRNA expression of OUC enzymes was detected in the extra-embryonic YSM; the mRNA expression of cmcpsIII in the YSM was much higher than that in the embryonic body during stages 28-31. Significant levels of enzyme activity and the existence of mitochondrial-type cmgs1 transcripts in the YSM supported the mRNA findings. We also found that the cmcpsIII transcript is localized in the vascularized inner layer of the YSM. Taken together, our findings demonstrate for the first time that the YSM is involved in urea-based osmoregulation during the early to mid phase of development in oviparous cartilaginous fish.

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“…[1][2][3] In mammals, the yolk sac is of major importance before the formation and functional maturation of the chorioallantoic placenta, a highly critical time in embryonic development during which early organogenesis and neural tube closure occur. 5 In addition to a drastic morphological change of EECs during this transition, 6 a differentiation process accompanied by the increase in expression of genes involved in nutrient uptake and lipoprotein metabolism, including the LRP2-Cubilin-Amnionless receptor tricomplex, Apolipoprotein B (APOB), APOA1, and APOA5 occurs. Nevertheless, structural and functional features of the yolk sac are highly conserved between species, and comparative RNA sequencing data revealed a significant conservation of the yolk sac transcriptome from human, murine, and chicken embryos.…”

Section: Introductionmentioning

confidence: 99%

A differentiation program induced by bone morphogenetic proteins 4 and 7 in endodermal epithelial cells provides the molecular basis for efficient nutrient transport by the chicken yolk sac

Bauer

Tondl

Schneider

2019

Developmental Dynamics

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Background: The mammalian yolk sac provides nutrients for the growing fetus during critical early developmental processes such as neural tube closure, which precedes the functional maturation of the placenta. In contrast, oviparous species such as the chicken rely solely on the yolk sac for transfer of nutrients from the yolk to the developing embryo. However, the molecular mechanisms that provide the yolk sac with nutrient transfer competence remain poorly understood.Results: We demonstrate that the chicken endodermal epithelial cells (EEC), which are in close contact with the yolk, gain their nutrient-transport competence by a paracrine crosstalk with the blood-vessel forming mesodermal cell layer. Bone morphogenetic proteins (BMP) 4 and 7 produced by ectodermal and mesodermal cell layers likely initiate a differentiation program of EECs during the transition from the area vitellina to the area vasculosa. BMPs, by inducing SMAD signaling, promote the up-regulation of endocytic receptor expression and thereby provide the EECs with the molecular machinery to produce triglyceride-rich lipoprotein particles. Conclusion: This paracrine signaling cascade may constitute the basis for the EEC-mediated mechanism underlying the efficient uptake, degradation, resynthesis, and transfer of yolk-derived nutrients into the embryonic circulation, which assures proper energy supply and development of the growing fetus. K E Y W O R D Sarea vasculosa, feto-maternal interface, nutrient transfer, paracrine signaling, triglyceride-rich lipoproteins

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The Developing Chicken Yolk Sac Acquires Nutrient Transport Competence by an Orchestrated Differentiation Process of Its Endodermal Epithelial Cells

Cited by 67 publications

References 68 publications

Expression of microsomal triglyceride transfer protein in lipoprotein-synthesizing tissues of the developing chicken embryo

Expression of microsomal triglyceride transfer protein in lipoprotein-synthesizing tissues of the developing chicken embryo

Urea-based osmoregulation in the developing embryo of oviparous cartilaginous fish (Callorhinchus milii): contribution of the extraembryonic yolk sac during the early developmental period

A differentiation program induced by bone morphogenetic proteins 4 and 7 in endodermal epithelial cells provides the molecular basis for efficient nutrient transport by the chicken yolk sac

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