Mutation in utp15 disrupts vascular patterning in a p53-dependent manner in zebrafish embryos

PLoS One. 2011;6(9):e25013. doi: 10.1371/journal.pone.0025013. Epub 2011 Sep 20.

Abstract

Background: Angiogenesis is the process by which the highly branched and functional vasculature arises from the major vessels, providing developing tissues with nutrients, oxygen, and removing metabolic waste. During embryogenesis, vascular patterning is dependent on a tightly regulated balance between pro- and anti-angiogenic signals, and failure of angiogenesis leads to embryonic lethality. Using the zebrafish as a model organism, we sought to identify genes that influence normal vascular patterning.

Methodology and principal findings: In a forward genetic screen, we identified mutant LA1908, which manifests massive apoptosis during early embryogenesis, abnormal expression of several markers of arterial-venous specification, delayed angiogenic sprouting of the intersegmental vessels (ISV), and malformation of the caudal vein plexus (CVP), indicating a critical role for LA1908 in cell survival and angiogenesis. Genetic mapping and sequencing identified a G to A transition in the splice site preceding exon 11 of utp15 in LA1908 mutant embryos. Overexpression of wild type utp15 mRNA suppresses all observed mutant phenotypes, demonstrating a causative relationship between utp15 and LA1908. Furthermore, we found that injecting morpholino oligonucleotides inhibiting p53 translation prevents cell death and rescues the vascular abnormalities, indicating that p53 is downstream of Utp15 deficiency in mediating the LA1908 phenotypes.

Conclusions and significance: Taken together, our data demonstrate an early embryonic effect of Utp15 deficiency on cell survival and the normal patterning of the vasculature and highlight an anti-angiogenic role of p53 in developing embryos.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Apoptosis
  • Blood Vessels / embryology*
  • Blood Vessels / metabolism
  • Cloning, Molecular
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / metabolism*
  • Embryonic Development
  • Gene Expression Regulation, Developmental
  • In Situ Hybridization
  • Mutation / genetics*
  • Neovascularization, Physiologic*
  • Phenotype
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Signal Transduction
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism*
  • Zebrafish / embryology
  • Zebrafish / genetics*
  • Zebrafish / metabolism
  • Zebrafish Proteins / physiology*

Substances

  • RNA, Messenger
  • Tumor Suppressor Protein p53
  • Zebrafish Proteins