Epigenetic control of cardiomyocyte production in response to a stress during the medaka heart development

Abstract

The size and morphology of organs are largely determined by a genetic program. However in some cases, an epigenetic mechanism influences the process of organ development. Particularly, epigenetic factors such as hemodynamic stress and blood pressure affect the morphogenesis of cardiac chambers and valves. Here, we report that the epigenetic influences affect the cardiomyocyte production. Taking advantage of longer developmental period of medaka fish, we could examine the later emerging tissue responses to the defect of ventricular beating, which occurred in the hozuki (hoz) mutant that harbors the mutated ventricular myosin heavy chain (vmhc) gene. The mutant showed a remarkable ventricular enlargement, and we showed that this enlargement was due to an excess production of ventricular cardiomyocytes in addition to the lack of concentric chamber growth. By experimental blockade of blood flow, we demonstrated that an elevated cardiac pressure was responsible for the aberrant cardiomyocyte production. From these data, we propose that the epigenetic tissue response to a stressed situation controls the production of cardiomyocytes to attain a fine tuning of heart formation.

Regular heartbeat rhythm at the heartbeat initiation stage is essential for normal cardiogenesis at low temperature

“…However, the larvae exhibited retrograde flow and could not swim because of degeneration of the pectoral and tail fins, possibly because of the lack of blood flow, and they died around 3 days after hatching. Several medaka mutants lacking heart functions also died either around the time of, or soon after, hatching [12,18]. …”

Reciprocal analyses in zebrafish and medaka reveal that harnessing the immune response promotes cardiac regeneration

“…We used the zebrafish AB strain (RRID:ZIRC_ZL1) as well as the following transgenic lines Tg(mpeg1:EGFP) gl22 (Ellett et al, 2011), Tg(mpeg1.4:mCherry-F) ump2 (Bernut et al, 2014), and TgBAC(mpx:GFP) i114 (Renshaw et al, 2006). We used the medaka WT Cab strain as well as the following transgenic lines fli::GFP;gata1::GFP (Schaafhausen et al, 2013), fli1-GFP (Moriyama et al, 2010; Ito et al, 2014), and Cab-Tg(zfmlc2 5.1 k:DsRed2-nuc) TG1026 (Taneda et al, 2010). The two medaka fli alleles were generated independently using the same plasmid, and we did not observe any difference in expression between them.…”

Current Advances in Functional Genomics in Aquaculture

“…As a result of these advances, epigenetics studies in aquaculture have tremendously increased in the last decades with the view to identifying biological markers relevant for improving the production of farmed aquatic organisms. Technologies used for epigenetics analyses in aquaculture include (i) RNA-seq in Medaka [207] and Nile tilapia [208]; (ii) genome-wide methylated DNA immunoprecipitation sequencing (MeDIP-seq) in Nile tilapia [209] and Medaka [207]; (iii) bisulite sequencing (BS-seq) in smooth tongue sole (Cynoglossus semilaevis) [210,211], rainbow trout [212] and Nile tilapia [208]; (iv) genetic linkage map analysis using simple sequence length polymorphisms (SSLPs) in medaka [213,214]; (v) methylation sensitivity ampliied polymorphism (MSAP) in Atlantic salmon [18], grass carp [215], brown trout [17], sea urchin (Glyptocidaris crenularis) [216] and sea cucumber (Apostichopus japonicas) [217]; (vi) 5-methylcytosine immunolocation in sea lamprey (Petromyzon marinus) [218]; (vii) restriction endonuclease hydrolysis of DNA using methylation enzymes in Zebraish [219] and (viii) bisulite sequencing PCR in Paciic Oyster (Crassostrea gigas) [220] and grass carp [221]. As shown in Table 3, epigenetics studies carried out this far include studies on reproduction, growth and adaptation traits.…”

“…Zebraish (Danio rerio) Carcinogenesis [258] Zebraish (Danio rerio) Embryo development [219] Zebraish (Danio rerio) Embryonic cardiogenesis [259] Medaka (Oryzias latipes) Excision of ToL2 transposal [260] Medaka (Oryzias latipes) Control of cardiomyocyte production in response to stress [214] Medaka (Oryzias latipes) Hypoxia and transgenerational reproduction impairment [207] Nile tilapia (Oreochromis niloticus) High temperature induced masculinization of skeletal muscles [209] Nile tilapia (Oreochromis niloticus) Sexual dimorphism [208] Atlantic salmon (Salmo salar L.) Early maturation [18] European seabass (Dicentrarchus labrax) Temperature dependent sex ratio shift [222,223] Tongue sole (Cynoglossidae) Sex reversal [210,211] Senegalese sole (Solea senegalensis) Thermal epigenetic regulation of muscle growth [261] European eel (Anguillarum…”