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Int J Mol Sci
2024 Feb 19;254:. doi: 10.3390/ijms25042412.
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The Molecular Mechanism of Body Axis Induction in Lampreys May Differ from That in Amphibians.
Ermakova GV
,
Kucheryavyy AV
,
Zaraisky AG
,
Bayramov AV
.
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Lamprey homologues of the classic embryonic inducer Noggin are similar in expression pattern and functional properties to Noggin homologues of jawed vertebrates. All noggin genes of vertebrates apparently originated from a single ancestral gene as a result of genome duplications. nogginA, nogginB and nogginC of lampreys, like noggin1 and noggin2 of gnathostomes, demonstrate the ability to induce complete secondary axes with forebrain and eye structures when overexpressed in Xenopus laevis embryos. According to current views, this finding indicates the ability of lamprey Noggin proteins to suppress the activity of the BMP, Nodal/Activin and Wnt/beta-catenin signaling pathways, as shown for Noggin proteins of gnathostomes. In this work, by analogy with experiments in Xenopus embryos, we attempted to induce secondary axes in the European river lamprey Lampetra fluviatilis by injecting noggin mRNAs into lamprey eggs in vivo. Surprisingly, unlike what occurs in amphibians, secondary axis induction in the lampreys either by noggin mRNAs or by chordin and cerberus mRNAs, the inductive properties of which have been described, was not observed. Only wnt8a mRNA demonstrated the ability to induce secondary axes in the lampreys. Such results may indicate that the mechanism of axial specification in lampreys, which represent jawless vertebrates, may differ in detail from that in the jawed clade.
Figure 1. Induction of secondary body axes upon injection of nogginA, nogginB, nogginC and wnt8a mRNAs in X. laevis and L. fluviatilis embryos. (A–F) Injections of lamprey nogginA, nogginB and nogginC mRNAs induce secondary axes in X. laevis. (G,H) Injections of lamprey nogginB mRNA do not induce secondary axes in L. fluviatilis embryos. (I,J) Injections of amphibian wnt8a mRNA induce secondary axes in L. fluviatilis embryos. (K) sonic hedgehog (shh) expression in L. fluviatilis embryos detected by ISH in an uninjected control embryo. (L,M) Detection of secondary axes in L. fluviatilis embryos by sonic hedgehog (shh) ISH. (N) Proteins, translated from injected Xl_noggin1-Myc and Lf_BMPa-Flag mRNAs, are detected in lamprey embryos at stages 17 and 21.
Figure 2. Hypothetical difference in the mechanism of BMP signaling between lamprey and amphibians. BMP2/4a expression by ISH (A–C) and antibody staining of Smad1/5 phosphorylation (D–F) in L. fluviatilis embryos. np—neural plate. (G) Smad1/5 phosphorylation might be modulated by factor(s) other than BMP, as injections of BMP inhibitors do not induce secondary axes in lamprey.
Supplementary Figure S1.
A - B – L. fluviatilis secondary axes diversity after injection of Xenopus wnt8a mRNA.
C - H – L. fluviatilis embryos injected with the indicated synthetic mRNAs showing no secondary axes.
Supplementary Figure S2.
A - C - qRT-PCR analysis of BMP2/4a, BMP2/4b and BMP2/4c expression at early embryonic stages of L. fluviatilis normalized by expression of housekeeping genes EF-1a and ODC.
D - F – approximate estimate of the total amount of RNA in embryos at early embryonic stages made by qRT-PCR of housekeeping genes ef-1a and odc at a series of stages (D, E) and by measuring of the amount of total mRNA isolated from 30 embryos at each stage using Implen NanoPhotometer (F).
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