Deficiency of AP1 Complex Ap1g1 in Zebrafish Model Led to Perturbation of Neurodevelopment, Female and Male Fertility; New Insight to Understand Adaptinopathies

Int J Mol Sci. 2023 Apr 12;24(8):7108. doi: 10.3390/ijms24087108.

Abstract

In vertebrates, two homologous heterotetrameric AP1 complexes regulate the intracellular protein sorting via vesicles. AP-1 complexes are ubiquitously expressed and are composed of four different subunits: γ, β1, μ1 and σ1. Two different complexes are present in eukaryotic cells, AP1G1 (contains γ1 subunit) and AP1G2 (contains γ2 subunit); both are indispensable for development. One additional tissue-specific isoform exists for μ1A, the polarized epithelial cells specific to μ1B; two additional tissue-specific isoforms exist for σ1A: σ1B and σ1C. Both AP1 complexes fulfil specific functions at the trans-Golgi network and endosomes. The use of different animal models demonstrated their crucial role in the development of multicellular organisms and the specification of neuronal and epithelial cells. Ap1g1 (γ1) knockout mice cease development at the blastocyst stage, while Ap1m1 (μ1A) knockouts cease during mid-organogenesis. A growing number of human diseases have been associated with mutations in genes encoding for the subunits of adaptor protein complexes. Recently, a new class of neurocutaneous and neurometabolic disorders affecting intracellular vesicular traffic have been referred to as adaptinopathies. To better understand the functional role of AP1G1 in adaptinopathies, we generated a zebrafish ap1g1 knockout using CRISPR/Cas9 genome editing. Zebrafish ap1g1 knockout embryos cease their development at the blastula stage. Interestingly, heterozygous females and males have reduced fertility and showed morphological alterations in the brain, gonads and intestinal epithelium. An analysis of mRNA profiles of different marker proteins and altered tissue morphologies revealed dysregulated cadherin-mediated cell adhesion. These data demonstrate that the zebrafish model organism enables us to study the molecular details of adaptinopathies and thus also develop treatment strategies.

Keywords: CRISPR/Cas9 technique; adaptinopathies; embryonic development; intracellular vesicular trafficking.

MeSH terms

  • Animals
  • Endosomes / metabolism
  • Epithelial Cells / metabolism
  • Female
  • Humans
  • Male
  • Mice
  • Neurodevelopmental Disorders* / genetics
  • Protein Isoforms / metabolism
  • Transcription Factor AP-1* / metabolism
  • Zebrafish Proteins* / metabolism
  • Zebrafish* / genetics
  • Zebrafish* / metabolism
  • trans-Golgi Network / metabolism

Substances

  • Protein Isoforms
  • Transcription Factor AP-1
  • Zebrafish Proteins

Grants and funding

This research was funded by the University of Brescia (ex 60%2021-2022 funds from Dipartimento di Medicina Molecolare e Traslazionale-University of Brescia to D.Z., D.F. and G.B.); «PNRR M4C2-Investimento 1.4-CN00000041 finanziato dall’Unione Europea–NextGenerationEU» to S.M., M.V., L.M. and E.M. were supported by PhD Program in Molecular Genetics, Biotechnology and Experimental Medicine, from the University of Brescia.