Embryonic cholesterol esterification is regulated by a cyclic AMP-dependent pathway in yolk sac membrane-derived endodermal epithelial cells

Wang, Siou-Huei; Lin, Han‐Jen; Lin, Yu-Chuan; Chen, Yu-Jen; Pan, Yu-Hui; Tung, Cheng-Ting; Mersmann, Harry J.; Ding, Shih‐Torng

doi:10.1371/journal.pone.0187560

Cited by 3 publications

(8 citation statements)

References 35 publications

(41 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…(1993) demonstrated that increased activity of ACAT, which is also called sterol O-acyltransferase ( SOAT ) and decreased activity of cholesteryl hydrolase in the YS tissue promoted the conversion of cholesterol to cholesteryl ester. Wang et al. (2017) found that SOAT1 mRNA and protein were regulated by nutrients and hormones through a cAMP-dependent pathway in the YS tissue of quail.…”

Section: Functional Roles Of the Yolk Sacmentioning

confidence: 97%

Centennial Review: The chicken yolk sac is a multifunctional organ

Wong

Uni

2021

Poultry Science

View full text Add to dashboard Cite

The yolk sac ( YS ) consists of the yolk, which supplies nutrients, and the YS tissue, which surrounds the yolk and provides essential metabolic functions for the developing embryo. The YS tissue is derived from the midgut of the embryo and consists of a layer of endodermal epithelial cells ( EEC ) in contact with the yolk contents, a mesodermal layer that contains the vascular system and an outer ectodermal layer. The YS tissue is a multifunctional organ that provides essential functions such as host immunity, nutrient uptake, carbohydrate and lipid metabolism, and erythropoiesis. The YS tissue plays a role in immunity by the transport of maternal antibodies in the yolk to the embryonic circulation that feeds the developing embryo. In addition, the YS tissue expresses high mRNA levels of the host defense peptide, avian β-defensin 10 during mid embryogenesis. Owing to its origin, the YS EEC share some functional properties with intestinal epithelial cells such as expression of transporters for amino acids, peptides, monosaccharides, fatty acids, and minerals. The YS tissue stores glycogen and expresses enzymes for glycogen synthesis and breakdown and glucogenesis. This carbohydrate metabolism may play an important role in the hatching process. The mesodermal layer of the YS tissue is the site for erythropoiesis and provides erythrocytes before the maturation of the bone marrow. Other functions of the YS tissue involve synthesis of plasma proteins, lipid transport and cholesterol metabolism, and synthesis of thyroxine. Thus, the YS is an essential organ for the growth, development, and health of the developing embryo. This review will provide an overview of the studies that have investigated the functionalities of the YS tissue at the cellular and molecular levels with a focus on chickens.

show abstract

Section: Functional Roles Of the Yolk Sacmentioning

confidence: 97%

Centennial Review: The chicken yolk sac is a multifunctional organ

Wong

Uni

2021

Poultry Science

View full text Add to dashboard Cite

show abstract

“…The miRNA sequencing of YSMs revealed the miRNAs involvement during avian development. We demonstrated that SOAT1 is not only activated by a cAMP-dependent pathway [2], but also was modulated by the TGFβ signaling pathway. The current study was the first to provide direct evidence to demonstrate miRNA expression profiling in the developing YSM of avian species.…”

Section: Discussionmentioning

confidence: 99%

“…Yolk sac membrane (YSM), a three-layer extraembryonic tissue, serves crucial roles for avian embryos during the entirety of embryonic development. We demonstrated that SOAT1 activity in endodermal epithelial cells (EECs, the third layer of YSM) was activated by specific nutrients and hormones through the cAMP-dependent PKA signaling pathway, and accumulated more cholesterol ester in EECs [2].…”

Section: Introductionmentioning

confidence: 99%

“…This suggested that miRNA transport from laying hens into albumen or yolk would be efficient to facilitate normal embryonic development by continually supplying miRNAs to growing embryos during nutrient uptake [7]. Nutrient absorption and reassembly in YSM has been confirmed [2, 8]. However, the miRNA expression patterns of YSM and the crucial linkages between embryos and yolk remain unclear during development.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Sterol-O acyltransferase 1 is inhibited by gga-miR-181a-5p and gga-miR-429-3p through the TGFβ pathway in endodermal epithelial cells of Japanese quail

Lin

Mersmann

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

20Nutrients are utilized and re-constructed by endodermal epithelial cells (EECs) in yolk 21 sac membranes in avian species. Sterol-O acyltransferase 1 (SOAT1) is the key enzyme to 22 convert cholesterol to cholesteryl ester for delivery to growing embryos. During 23 development, absorption of yolk is matched with significant changes of SOAT1 mRNA 24 and enzyme activity. miRNAs regulate angiogenesis and metabolism during mammalian 25 development. However, the involvement of miRNAs in lipid utilization during avian 26 embryogenesis remains ambiguous. 27 Using a miRNA sequencing technique, we found several candidate miRNAs and 28 confirmed expression patterns with real time PCR. They were selected for as candidates 29 targeting the receptor (TGFβ receptor type 1, TGFBR1) that may regulate SOAT1. Similar 30 to SOAT1 mRNA accumulation, the gga-miR-181a-5p expression was gradually elevated 31 during development, but the concentration of gga-miR-429-3p was in the opposite 32 direction. Transfection with gga-miR-181a-5p or gga-miR-429-3p inhibited TGFBR1 and 33 SOAT1 in EECs. The 3' untranslated region (3'UTR) of TGFBR1 was then confirmed to 34 be one of the targets of gga-miR-181a-5p and gga-miR-429-3p. Taken together, expression 35 of miRNAs during embryonic development regulates SOAT1 expression by inhibiting the 36 3'UTR of TGFBR1. This is indicative of possible regulation of avian yolk lipid utilization 3 37 and modification of hatchability by changing miRNA expressions. 38 39 Introduction 40 SOAT1 (sterol-O acyltransferase 1), also named ACAT1 (acyl-Coenzyme A: 41 cholesterol acyltransferase 1), is the key enzyme to catalyze cholesterol conversion into 42 cholesteryl ester, by adding fatty acyl coenzyme A; thus, a less polar molecule is produced 43 [1]. Yolk sac membrane (YSM), a three-layer extraembryonic tissue, serves crucial roles 44 for avian embryos during the entirety of embryonic development. We demonstrated that 45 SOAT1 activity in endodermal epithelial cells (EECs, the third layer of YSM) was 46 activated by specific nutrients and hormones through the cAMP-dependent PKA signaling 47 pathway, and accumulated more cholesterol ester in EECs [2]. 48 The diversity of bio-functions and involvement of non-coding RNAs has raised 49 considerable issues. Non-coding RNAs include short (microRNAs, miRNAs) and long 50 non-coding (lncRNAs), ribosomal (rRNAs), transfer (tRNAs), small nuclear (snRNAs), 51 small nucleolar (snoRNAs), transfer-messenger (tmRNAs) and telomerase RNAs [3]. The 52 functions and regulations of miRNAs have been examined in mammalian species for 53 decades. Mainly, mature miRNAs are paired to 3' untranslated regions (UTR) or 5'UTR 54 by identifying seed regions of target genes [4]. 4 55 During avian embryonic development, the comprehensive whole mount in situ 56 hybridization expression analysis of 111 mature miRNA sequences in chicken embryos 57 revealed that miRNAs showed a variety of patterns in the early stages of development [5]. 58 Tissue specific-expressed miRNAs were also found to regul...

show abstract

Section: Introductionmentioning

confidence: 99%