Versican is crucial for the initiation of cardiovascular lumen development in medaka (Oryzias latipes)

Mittal, Nishant; Yoon, Sung Han; Enomoto, Hirokazu; Miyama, Hiroshi; Shimizu, Atsushi; Kawakami, Koichi; Fujita, Mitsuhiro; Watanabe, Hideto; Fukuda, Keiichi; Makino, Shinji

doi:10.1038/s41598-019-45851-3

Cited by 23 publications

(14 citation statements)

References 88 publications

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“…We have provided the first evidence that laminin restricts heart growth during looping morphogenesis by limiting the number of SHF cells incorporated into the venous pole of the heart. Previous studies have identified roles for ECM components such as Versican and Fibronectin in promoting SHF addition to the arterial pole of the heart [79][80][81][82][83], however we have identified an opposing role for Lamb1a in restricting excessive SHF addition to the venous pole. Highlighting the importance of cell-ECM interactions in the SHF loss of Tbx1, a master regulator of SHF addition, results in reduced expression of Integrin, loss of focal adhesion markers, and impaired filopodia formation in the SHF [84,85].…”

Section: Discussioncontrasting

confidence: 54%

Lamb1a regulates atrial growth by limiting excessive, contractility-dependent second heart field addition during zebrafish heart development

Derrick

Ejg

Ass

et al. 2021

Preprint

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During early vertebrate heart development, the heart transitions from a linear tube to a complex asymmetric structure. This process includes looping of the tube and ballooning of the emerging cardiac chambers, which occur simultaneously with growth of the heart. A key driver of cardiac growth is deployment of cells from the Second Heart Field (SHF) into both poles of the heart, with cardiac morphogenesis and growth intimately linked in heart development. Laminin is a core component of extracellular matrix (ECM) basement membranes, and although mutations in specific laminin subunits are linked with a variety of cardiac abnormalities, including congenital heart disease and dilated cardiomyopathy, no role for laminin has been identified in early vertebrate heart morphogenesis. We identified dynamic, tissue-specific expression of laminin subunit genes in the developing zebrafish heart, supporting a role for laminins in heart morphogenesis. lamb1a mutants exhibit cardiomegaly from 2dpf onwards, with subsequent progressive defects in cardiac morphogenesis characterised by a failure of the chambers to compact around the developing atrioventricular canal. We show that loss of lamb1a results in excess addition of SHF cells to the atrium, revealing that Lamb1a functions to limit heart size during cardiac development by restricting SHF addition to the venous pole. lamb1a mutants exhibit hallmarks of altered haemodynamics, and specifically blocking cardiac contractility in lamb1a mutants rescues heart size and atrial SHF addition. Furthermore, we identify that FGF and RA signalling, two conserved pathways promoting SHF addition, are regulated by heart contractility and are dysregulated in lamb1a mutants, suggesting that laminin mediates interactions between SHF deployment, heart biomechanics, and biochemical signalling during heart development. Together, this describes the first requirement for laminins in early vertebrate heart morphogenesis, reinforcing the importance of specialised ECM composition in cardiac development.

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Section: Discussioncontrasting

confidence: 54%

Lamb1a regulates atrial growth by limiting excessive, contractility-dependent second heart field addition during zebrafish heart development

Derrick

Ejg

Ass

et al. 2021

Preprint

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“…However, as G. holbrooki embryos develop, at later stages, the heart contractions show a more co-ordinated pattern as is also the case for zebrafish embryos [ 16 ], which is linked to a substantial increase in cardiomyocyte numbers [ 51 ]. This is also consistent with observations in medaka [ 27 , 29 ] and mammals including humans [ 52 ].…”

Section: Discussionsupporting

confidence: 93%

“…Although the teleost lineage exhibits morphological evolutionary novelty such as bulbus arteriosus, they express genes that are conserved across vertebrates [ 50 ]. Therefore, fish such as zebrafish [ 18 ] and medaka [ 28 , 29 ] have been used as the model for cardiovascular studies. However, these species do not appear to show cardiac-related sex-specific differences, unlike humans [ 14 , 26 ].…”

Section: Discussionmentioning

confidence: 99%

“…In higher vertebrates, sex-specific differences in cardiac performance and physiology are well documented [ 14 , 26 ]. Although cardiac studies have been conducted increasingly in zebrafish [ 16 , 18 ] and medaka [ 27 , 28 , 29 ], no study to date has examined sex-specific heart rates (HRs) in fish embryos. For instance, the influence of sex on ventricular function and size in juvenile and adult zebrafish [ 7 , 8 , 30 ], and HR in adult sockeye salmon, Oncorhynchus nerka [ 31 ] and rainbow trout, Oncorhynchus mykiss [ 32 ], have been reported.…”

Section: Introductionmentioning

confidence: 99%

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Embryonic Onset of Sexually Dimorphic Heart Rates in the Viviparous Fish, Gambusia holbrooki

2021

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In fish, little is known about sex-specific differences in physiology and performance of the heart and whether these differences manifest during development. Here for the first time, the sex-specific heart rates during embryogenesis of Gambusia holbrooki, from the onset of the heart rates (HRs) to just prior to parturition, was investigated using light cardiogram. The genetic sex of the embryos was post-verified using a sex-specific genetic marker. Results reveal that heart rates and resting time significantly increase (p < 0.05) with progressive embryonic development. Furthermore, both ventricular and atrial frequencies of female embryos were significantly higher (p < 0.05) than those of their male sibs at the corresponding developmental stages and remained so at all later developmental stages (p < 0.05). In concurrence, the heart rate and ventricular size of the adult females were also significantly (p < 0.05) higher and larger respectively than those of males. Collectively, the results suggest that the cardiac sex-dimorphism manifests as early as late-organogenesis and persists through adulthood in this species. These findings suggest that the cardiac measurements can be employed to non-invasively sex the developing embryos, well in advance of when their phenotypic sex is discernible. In addition, G. holbrooki could serve as a better model to study comparative vertebrate cardiovascular development as well as to investigate anthropogenic and climatic impacts on heart physiology of this species, that may be sex influenced.

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“…To investigate the effects of SNC on the vascular formation and embryonic developments of medaka, we employed epidermal growth factor‐like domain 7 (eg, fl7), a key marker of angiogenic signaling factor. EGFL7 is produced exclusively by vascular endothelial cells, 13 and egfl7 is expressed in vascular endothelial cells during medaka embryogenesis 14 . In addition, e gfl7 is important for regulating tubulogenesis in zebrafish 15 and for controlling vascular patterning and integrity in mice 16 .…”

Section: Introductionmentioning

confidence: 99%

Silver nanocolloid affects hindbrain vascular formation during medaka embryogenesis

Matsukura

Kataoka

Kawana

et al. 2020

Environmental Toxicology

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Angiogenesis is essential for the normal development of an embryo. Silver nanocolloid (SNC) is known to induce vascular malformation in the medaka embryo. We focused on the development of the central arteries (CtAs) in the hindbrain of Japanese medaka. The CtAs and the basilar artery from which they branch are essential for transporting the blood and nutrients necessary to support the hindbrain parenchyma and the development of the pons and cerebellum from the hindbrain. We exposed medaka embryos at developmental stage 21 (6 somite stage), to 0, 0.5, 5, or 10 mg/L SNC and evaluated hatching rate, number of thrombi per embryo, head size (length and width), body length, and angiogenesis. Although all SNC‐exposed embryos hatched, their head size and body length were small in comparison to controls; in addition, the number of thrombi in the head increased and head size and body length decreased as the SNC concentration increased. To evaluate vasculogenic abnormalities, we performed whole‐mount in situ hybridization using a vascular marker (eg, fl7) and visualized the CtAs in medaka embryos. In control embryos, CtAs started to sprout at stage 32 (somite completion stage) and their extension was complete by stage 35 (pectoral fin blood circulation stage). In contrast, CtAs failed to sprout in SNC‐exposed embryos, and thrombi were present. Furthermore, qRT‐PCR analysis showed that SNC significantly suppressed the egfl7 expression level at stage 35. Together, our findings suggest that SNC induced decreased developments of head and body in medaka embryos due to insufficient angiogenesis and hindbrain vascular formation.

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Versican is crucial for the initiation of cardiovascular lumen development in medaka (Oryzias latipes)

Cited by 23 publications

References 88 publications

Lamb1a regulates atrial growth by limiting excessive, contractility-dependent second heart field addition during zebrafish heart development

Lamb1a regulates atrial growth by limiting excessive, contractility-dependent second heart field addition during zebrafish heart development

Embryonic Onset of Sexually Dimorphic Heart Rates in the Viviparous Fish, Gambusia holbrooki

Silver nanocolloid affects hindbrain vascular formation during medaka embryogenesis

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