Fujita Masahide, Sakabe Masahide, Ioka Tomoko, Watanabe Yusuke, Kinugasa-Katayama Yumi, Tsuchihashi Takatoshi, Utset Manuel F, Yamagishi Hiroyuki, Nakagawa Osamu
Laboratory for Cardiovascular System Research, Nara Medical University Advanced Medical Research Center, Kashihara, Nara, Japan; Department of Molecular Physiology, National Cerebral and Cardiovascular Center Research Institute, Suita, Osaka, Japan.
Department of Molecular Physiology, National Cerebral and Cardiovascular Center Research Institute, Suita, Osaka, Japan.
Mech Dev. 2016 Feb;139:65-73. doi: 10.1016/j.mod.2015.11.002. Epub 2015 Nov 11.
The aortic arch and major branch arteries are formed from the three pairs of pharyngeal arch arteries (PAAs) during embryonic development. Their morphological defects are clinically observed as isolated diseases, as a part of complicated cardiovascular anomalies or as a manifestation of multi-organ syndromes such as 22q11.2 deletion syndrome. Although numerous genes have been implicated in PAA formation and remodeling, detailed mechanisms remain poorly understood. Here we report that the mice null for Hrt1/Hey1, a gene encoding a downstream transcription factor of Notch and ALK1 signaling pathways, show perinatal lethality on the C57BL/6N, C57BL/6N × C57BL/6J or C57BL/6N × 129X1/SvJ background. Hrt1/Hey1 null embryos display abnormal development of the fourth PAA (PAA4), which results in congenital vascular defects including right-sided aortic arch, interruption of the aortic arch and aberrant origin of the right subclavian artery. Impaired vessel formation occurs randomly in PAA4 of Hrt1/Hey1 null embryos, which likely causes the variability of congenital malformations. Endothelial cells in PAA4 of null embryos differentiate normally but are structurally disorganized at embryonic day 10.5 and 11.5. Vascular smooth muscle cells are nearly absent in the structurally-defective PAA4, despite the appropriate migration of cardiac neural crest cells into the fourth pharyngeal arches. Endothelial expression of Jag1 is down-regulated in the structurally-defective PAA4 of null embryos, which may be one of the mechanisms underlying the suppression of vascular smooth muscle cell differentiation. While the direct downstream phenomena of the Hrt1/Hey1 deficiency remain to be clarified, we suggest that Hrt1/Hey1-dependent transcriptional regulation has an important role in PAA formation during embryonic development.
在胚胎发育过程中,主动脉弓和主要分支动脉由三对咽弓动脉(PAA)形成。它们的形态学缺陷在临床上可表现为孤立性疾病、复杂心血管畸形的一部分或多器官综合征(如22q11.2缺失综合征)的一种表现。尽管许多基因与PAA的形成和重塑有关,但详细机制仍知之甚少。在此,我们报告,在C57BL/6N、C57BL/6N×C57BL/6J或C57BL/6N×129X1/SvJ背景下,编码Notch和ALK1信号通路下游转录因子的基因Hrt1/Hey1缺失的小鼠表现出围产期致死性。Hrt1/Hey1缺失的胚胎显示第四对咽弓动脉(PAA4)发育异常,这导致先天性血管缺陷,包括右侧主动脉弓、主动脉弓中断和右锁骨下动脉异常起源。在Hrt1/Hey1缺失的胚胎的PAA4中,血管形成受损随机发生,这可能导致先天性畸形的变异性。缺失胚胎的PAA4中的内皮细胞正常分化,但在胚胎第10.5天和11.5天时结构紊乱。尽管心脏神经嵴细胞向第四咽弓适当迁移,但在结构缺陷的PAA4中几乎没有血管平滑肌细胞。在缺失胚胎的结构缺陷的PAA4中,Jag1的内皮表达下调,这可能是抑制血管平滑肌细胞分化的潜在机制之一。虽然Hrt1/Hey1缺乏的直接下游现象仍有待阐明,但我们认为Hrt1/Hey1依赖的转录调控在胚胎发育过程中PAA的形成中起重要作用。