The mechanism and pattern of yolk consumption provide insight into embryonic nutrition inXenopus

Abstract

Little is known about how metabolism changes during development. For most animal embryos, yolk protein is a principal source of nutrition, particularly of essential amino acids. Within eggs, yolk is stored inside large organelles called yolk platelets (YPs). We have gained insight into embryonic nutrition in the African clawed frog Xenopus laevis by studying YPs. Amphibians follow the ancestral pattern in which all embryonic cells inherit YPs from the egg cytoplasm. These YPs are consumed intracellularly at some point during embryogenesis, but it was not known when, where or how yolk consumption occurs. We have identified the novel yolk protein Seryp by biochemical and mass spectrometric analyses of purified YPs. Within individual YPs, Seryp is degraded to completion earlier than the major yolk proteins, thereby providing a molecular marker for YPs engaged in yolk proteolysis. We demonstrate that yolk proteolysis is a quantal process in which a subset of dormant YPs within embryonic cells are reincorporated into the endocytic system and become terminal degradative compartments. Yolk consumption is amongst the earliest aspects of differentiation. The rate of yolk consumption is also highly tissue specific, suggesting that nutrition in early amphibian embryos is tissue autonomous. But yolk consumption does not appear to be triggered by embryonic cells declining to a critically small size. Frog embryos offer a promising platform for the in vivo analysis of metabolism.

Genetics of Lipid-Storage Management inCaenorhabditis elegansEmbryos

“…The precursors of the yolk proteins, vitellogenins, are typically synthesized in organs distant from the gonad and are then endocytosed by the developing oocytes (Mosconi et al 2002;Tufail and Takeda 2009). Here they are stored in yolk platelets until they are degraded (Reimer and Crawford 1995;Jorgensen et al 2009). In C. elegans, the cathepsin L-like cysteine protease CPL-1 is involved in the degradation of yolk proteins during embryogenesis (Hashmi et al 2002;Britton and Murray 2004).…”

Proteomics of M-phase entry: ‘Omen’ vs. ‘Omre’, the battle for oocyte quality and beyond

“…Jorgensen et al [27] and ourselves [24] have shown that EP45 is not synthesized in oocytes but in the liver and that it is delivered to the oocytes via blood and, probably, via follicular cells. We also have shown that over-expression of EP45 does not induce meiotic maturation either in stage IV or VI oocytes.…”

“…Indeed, a recent proteomic www.fhc.viamedica.pl study of yolk components in Xenopus laevis has shown that EP45 (under the new name of Seryp) is one of the major components of yolk granules and the major player in regulation of the source of energy necessary for embryo development [27]. On the basis of its amino acid sequence, EP45 was classified as a member of the serine protease inhibitors called Serpins [26,27]. EP45 has a histidine-rich N-terminus which determines its high affinity for nickel [28,29].…”

Similarities between oocytes and macrophages. An overview

“…Jorgensen et al [17] found a new class of proteins in Xenopus and named it seryp, which is a constituent of yolk protein massed in the yolk platelets. This protein acts as a signature protein of the yolk platelet as it is degraded earlier in the embryonic cells to provide nutrition.…”