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Early cardiac morphogenesis defects caused by loss of embryonic macrophage function in Xenopus.

ABSTRACT: The heart-forming mesoderm in Xenopus embryos lies adjacent to the source of the first embryonic population of macrophages. Such macrophages underlie the bilateral myocardial cell layers as they converge to form a linear heart tube. We have examined whether such macrophages participate in early cardiac morphogenesis, combining morpholino oligonucleotides that inhibit macrophage differentiation or function with transgenic reporters to assess macrophage numbers in living embryos. We show that loss of macrophage production through tadpole stages of development by morpholino-mediated knockdown of the spib transcription factor results in an arrest of heart formation. The myocardium fails to form the fused, wedge-shaped trough that precedes heart tube formation and in the most severe cases, myocardial differentiation is also impaired. Knockdown of the Ly6 protein lurp1, an early, secreted product from differentiated macrophages, produces a similar arrest to myocardial morphogenesis. Heart development can moreover be rescued by surgical-transfer of normal macrophage domains into morpholino-injected embryos. Together, these results demonstrate that amphibian heart formation depends on the presence and activity of the macrophage population, indicating that these cells may be an important source of growth cues necessary for early cardiac morphogenesis.

SUBMITTER: Smith SJ

PROVIDER: S-EPMC3157588 | biostudies-literature | 2011 May-Jun

REPOSITORIES: biostudies-literature

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Early cardiac morphogenesis defects caused by loss of embryonic macrophage function in Xenopus.

Smith Stuart J SJ Smith Stuart J SJ Mohun Timothy J TJ

Mechanisms of development 20110415 5-6

The heart-forming mesoderm in Xenopus embryos lies adjacent to the source of the first embryonic population of macrophages. Such macrophages underlie the bilateral myocardial cell layers as they converge to form a linear heart tube. We have examined whether such macrophages participate in early cardiac morphogenesis, combining morpholino oligonucleotides that inhibit macrophage differentiation or function with transgenic reporters to assess macrophage numbers in living embryos. We show that loss ...[more]

PMID: 21515365

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Project description:During early vertebrate embryogenesis, cell fate specification is often coupled with cell acquisition of specific adhesive, polar and/or motile behaviors. In Xenopus gastrulae, tissues fated to form different axial structures display distinct motility. The cells in the early organizer move collectively and directionally toward the animal pole and contribute to anterior mesendoderm, whereas the dorsal and the ventral-posterior trunk tissues surrounding the blastopore of mid-gastrula embryos undergo convergent extension and convergent thickening movements, respectively. While factors regulating cell lineage specification have been described in some detail, the molecular machinery that controls cell motility is not understood in depth. To gain insight into the gene battery that regulates both cell fates and motility in particular embryonic tissues, we performed RNA sequencing (RNA-seq) to investigate differentially expressed genes in the early organizer, the dorsal and the ventral marginal zone of Xenopus gastrulae. We uncovered many known signaling and transcription factors that have been reported to play roles in embryonic patterning during gastrulation. We also identified many uncharacterized genes as well as genes that encoded extracellular matrix (ECM) proteins or potential regulators of actin cytoskeleton. Co-expression of a selected subset of the differentially expressed genes with activin in animal caps revealed that they had distinct ability to block activin-induced animal cap elongation. Most of these factors did not interfere with mesodermal induction by activin, but an ECM protein, EFEMP2, inhibited activin signaling and acted downstream of the activated type I receptor. By focusing on a secreted protein kinase PKDCC1, we showed with overexpression and knockdown experiments that PKDCC1 regulated gastrulation movements as well as anterior neural patterning during early Xenopus development. Overall, our studies identify many differentially expressed signaling and cytoskeleton regulators in different embryonic regions of Xenopus gastrulae and imply their functions in regulating cell fates and/or behaviors during gastrulation.

Dataset Information

Early cardiac morphogenesis defects caused by loss of embryonic macrophage function in Xenopus.

Publications

Early cardiac morphogenesis defects caused by loss of embryonic macrophage function in Xenopus.

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