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PMID:24892953

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Citation

Du, TT, Xu, PF, Dong, ZW, Fan, HB, Jin, Y, Dong, M, Chen, Y, Pan, WJ, Ren, RB, Liu, TX, Deng, M and Huang, QH (2014) Setdb2 controls convergence and extension movements during zebrafish gastrulation by transcriptional regulation of dvr1. Dev. Biol. 392:233-44

Abstract

As the primary driving forces of gastrulation, convergence and extension (C&E) movements lead to a medio-lateral narrowing and an anterior-posterior elongation of the embryonic body axis. Histone methylation as a post-translational modification plays a critical role in early embryonic development, but its functions in C&E movements remain largely unknown. Here, we show that the setdb2-dvr1 transcriptional cascade plays a critical role in C&E movements during zebrafish gastrulation. Knockdown of Setdb2, a SET domain-containing protein possessing a potential histone H3K9 methyltransferase activity, induced abnormal C&E movements, resulting in anterior-posterior shortening and medio-lateral expansion of the embryonic axis, as well as abnormal notochord cell polarity. Furthermore, we found that Setdb2 functions through fine-tuning the expression of dvr1, a ligand of the TGF-β superfamily, to an appropriate level to ensure proper C&E movements in a non-cell-autonomous manner. In addition, both overexpression and knockdown of Dvr1 at the one-cell stage resulted in defects at epiboly and C&E. These data demonstrate that Setdb2 is a novel regulator for C&E movements and acts by modulating the expression level of dvr1, suggesting that Dvr1 acts as a direct and essential mediator for C&E cell movements.

Links

PubMed Online version:10.1016/j.ydbio.2014.05.022

Keywords

Animals; Blotting, Western; Cell Movement/physiology; Fluorescent Antibody Technique; Gastrulation/physiology; Gene Expression Regulation, Developmental/physiology; Gene Knockdown Techniques; Histone-Lysine N-Methyltransferase/metabolism; Histone-Lysine N-Methyltransferase/physiology; In Situ Hybridization; Microarray Analysis; Morpholinos/genetics; Real-Time Polymerase Chain Reaction; Transforming Growth Factor beta/genetics; Transforming Growth Factor beta/metabolism; Zebrafish/embryology; Zebrafish Proteins/genetics; Zebrafish Proteins/metabolism; Zebrafish Proteins/physiology

Significance

Annotations

Gene product Qualifier GO Term Evidence Code with/from Aspect Extension Notes Status

DANRE:DVR1

involved_in

GO:1904086: regulation of epiboly involved in gastrulation with mouth forming second

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

DANRE:DVR1

involved_in

GO:0060027: convergent extension involved in gastrulation

ECO:0000316: genetic interaction evidence used in manual assertion

ZFIN:ZDB-GENE-030131-7093

P

Seeded From UniProt

complete

DANRE:DVR1

involved_in

GO:0060027: convergent extension involved in gastrulation

ECO:0000315: mutant phenotype evidence used in manual assertion

ZFIN:ZDB-MRPHLNO-171103-2

P

Seeded From UniProt

complete

DANRE:DVR1

involved_in

GO:0060027: convergent extension involved in gastrulation

ECO:0000315: mutant phenotype evidence used in manual assertion

ZFIN:ZDB-MRPHLNO-100312-2

P

Seeded From UniProt

complete

DANRE:DVR1

GO:1904136: regulation of convergent extension involved in notochord morphogenesis

ECO:0000316:

UniProtKB:Q06ZW3


P

In Figure 2 G-I, injection of Setdb2 morpholino will result in a wider and shorter notochord, however, when Dvr1 morpholino is co-injected with Setdb2 morpholino, the effects of setdb2 morpholino are reversed.

complete
CACAO 10544

DANRE:DVR1

GO:1904103: regulation of convergent extension involved in gastrulation

ECO:0000316:

UniProtKB:Q06ZW3


P

In Figure 2 G-I injection of Setdb2 morpholino will result in a wider and shorter notochord, however, when Dvr1 morpholino is co-injected with Setdb2 morpholino, the effects of setdb2 morpholino are reversed.

complete
CACAO 10670

DANRE:DVR1

GO:1904086: regulation of epiboly involved in gastrulation with mouth forming second

ECO:0000315:

P

In Figure 3 A-F, varying amounts of dvr1 mRNA are injected into embryos and compared to a control embryo. With larger amounts of dvr1 mRNA injection there are higher percentages of delayed epiboly, leading to the conclusion that dvr1 is involved in epiboly.

complete
CACAO 10672

DANRE:DVR1

GO:1904130: regulation of convergent extension involved in neural plate elongation

ECO:0000315:

P

In figure 3 J and K, embryos injected with 10pg of DVR1 mRNA show broader neural plates than embryos not injected. This suggests involvement in neural plate morphogenesis.

complete
CACAO 10714

DANRE:DVR1

GO:1904127: regulation of convergent extension involved in somitogenesis

ECO:0000315:

P

In figure 3 L and M, embryos injected with 10pg of DVR1 mRNA show wider and slightly shorter somites than embryos not injected. This suggests involvement in somitogenesis.

complete
CACAO 10715

DANRE:SETB2

involved_in

GO:0060027: convergent extension involved in gastrulation

ECO:0000316: genetic interaction evidence used in manual assertion

ZFIN:ZDB-GENE-980526-389

P

Seeded From UniProt

complete

DANRE:SETB2

involved_in

GO:0060027: convergent extension involved in gastrulation

ECO:0000315: mutant phenotype evidence used in manual assertion

ZFIN:ZDB-MRPHLNO-110201-1

P

Seeded From UniProt

complete

DANRE:SETB2

GO:1904105: positive regulation of convergent extension involved in gastrulation

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Each section in Figure 1 shows observations of the effects of an injection of Setdb2 morpholino such as a wider and shorter notochord, broader neural plate, wider rhombomeres, and a slightly posteriorly located prechordal plate, which combined suggest that Setdb2 is involved in convergence and extension movements in gastrulation.

complete
CACAO 10547

DANRE:SETB2

GO:1904136: regulation of convergent extension involved in notochord morphogenesis

ECO:0000315:

P

In figure 1 A and B, Setdb2 morpholino shows a wider and shorter notochord than the control embryo. Figure 1 J shows the length to width ratio of notochord cells for the control and setdb2 morpholino embryos. For the Setdb2 morpholino embryo, the length to width ratio is much smaller than that of the control.

complete
CACAO 10548

DANRE:SETB2

GO:1904130: regulation of convergent extension involved in neural plate elongation

ECO:0000315:

P

In Figure 1 C,D,G neural plates are shown to be much wider in setdb2 morpholinos than in the control setdb2.

complete
CACAO 10711

DANRE:SETB2

GO:1904133: regulation of convergent extension involved in rhombomere morphogenesis

ECO:0000315:

P

In figure 1 E-G, the rhombomeres in Setdb2 morpholino groups are wider than in setdb2 control groups.

complete
CACAO 10712

Notes

See also

References

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