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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,W, Kajimura,M, Tanaka,H, Hasegawa,K, Bell,JD, Toop,T, Donald,JA and Hyodo,S 2014, Urea-based osmoregulation in the developing embryo of oviparous cartilaginous fish (Callorhinchus milii) : contribution of the extraembryonic yolk sac during the early developmental period, The Journal of Experimental Biology, vol. 217, no. 8, pp. 1353-1362, doi: 10.1242/jeb.094649.

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Title Urea-based osmoregulation in the developing embryo of oviparous cartilaginous fish (Callorhinchus milii) : contribution of the extraembryonic yolk sac during the early developmental period
Author(s) Takagi,W
Kajimura,M
Tanaka,H
Hasegawa,K
Bell,JD
Toop,T
Donald,JAORCID iD for Donald,JA orcid.org/0000-0001-5930-2642
Hyodo,S
Journal name The Journal of Experimental Biology
Volume number 217
Issue number 8
Start page 1353
End page 1362
Total pages 10
Publisher Company of Biologists
Place of publication Cambridge, United Kingdom
Publication date 2014-04-01
ISSN 1477-9145
Keyword(s) Organogenesis
Ornithine urea cycle enzymes
Osmoregulation
Oviparous cartilaginous fish
Urea synthesis
Yolk sac membrane
Science & Technology
Life Sciences & Biomedicine
Biology
Life Sciences & Biomedicine - Other Topics
CARBAMOYL-PHOSPHATE SYNTHETASE
SCYLIORHINUS-CANICULA L
SKATE RAJA-ERINACEA
ELASMOBRANCH EMBRYOS
GLUTAMINE-SYNTHETASE
CARCHARHINUS-LEUCAS
NITROGEN-EXCRETION
NA+/K+-ATPASE
CYCLE ENZYMES
DOGFISH
Animals
Embryo, Nonmammalian
Embryonic Development
Fish Proteins
Fishes
Osmoregulation
Real-Time Polymerase Chain Reaction
Transcriptome
Urea
Yolk Sac
Summary 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.
Language eng
DOI 10.1242/jeb.094649
Field of Research 060807 Animal Structure and Function
Socio Economic Objective 970106 Expanding Knowledge in the Biological Sciences
HERDC Research category C1 Refereed article in a scholarly journal
ERA Research output type C Journal article
Copyright notice ©2014, Company of Biologists
Persistent URL http://hdl.handle.net/10536/DRO/DU:30071571

Document type: Journal Article
Collections: Faculty of Science, Engineering and Built Environment
School of Life and Environmental Sciences
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Citation counts: TR Web of Science Citation Count  Cited 10 times in TR Web of Science
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