CARMIL3 is important for cell migration and morphogenesis during early development in zebrafish: CARMIL3 and early development

Benjamin C. Stark, Yuanyuan Gao, Diane S. Sepich, Lakyn Belk, Matthew A. Culver, Bo Hu, Marlene Mekel, Wyndham Ferris, Jimann Shin, Lilianna Solnica-Krezel, Fang Lin, John A. Cooper

Research output: Contribution to journalArticlepeer-review

Abstract

Cell migration is important during early animal embryogenesis. Cell migration and cell shape are controlled by actin assembly and dynamics, which depend on capping proteins, including the barbed-end heterodimeric actin capping protein (CP). CP activity can be regulated by capping-protein-interacting (CPI) motif proteins, including CARMIL (capping protein Arp2/3 myosin-I linker) family proteins. Previous studies of CARMIL3, one of the three highly conserved CARMIL genes in vertebrates, have largely been limited to cells in culture. Towards understanding CARMIL function during embryogenesis in vivo, we analyzed zebrafish lines carrying mutations of carmil3. Maternal-zygotic mutants showed impaired endodermal migration during gastrulation, along with defects in dorsal forerunner cell (DFC) cluster formation, which affected the morphogenesis of Kupffer's vesicle (KV). Mutant KVs were smaller, contained fewer cells and displayed decreased numbers of cilia, leading to defects in left/right (L/R) patterning with variable penetrance and expressivity. The penetrance and expressivity of the KV phenotype in carmil3 mutants correlated well with the L/R heart positioning defect at the end of embryogenesis. This in vivo animal study of CARMIL3 reveals its new role during morphogenesis of the vertebrate embryo. This role involves migration of endodermal cells and DFCs, along with subsequent morphogenesis of the KV and L/R asymmetry.

Original languageEnglish
Pages (from-to)148-159
Number of pages12
JournalDevelopmental Biology
Volume481
DOIs
StatePublished - Jan 2022

Keywords

  • Actin
  • Capping protein
  • Cell migration
  • Endoderm
  • Gastrulation
  • Kupffer's vesicle
  • Morphogenesis
  • Zebrafish

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