The Chromosomal Passenger Protein Birc5b Organizes Microfilaments and Germ Plasm in the Zebrafish Embryo

Sreelaja Nair, Florence Marlow, Elliott Abrams, Lee Kapp, Mary C. Mullins, Francisco Pelegri

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Microtubule-microfilament interactions are important for cytokinesis and subcellular localization of proteins and mRNAs. In the early zebrafish embryo, astral microtubule-microfilament interactions also facilitate a stereotypic segregation pattern of germ plasm ribonucleoparticles (GP RNPs), which is critical for their eventual selective inheritance by germ cells. The precise mechanisms and molecular mediators for both cytoskeletal interactions and GP RNPs segregation are the focus of intense research. Here, we report the molecular identification of a zebrafish maternal-effect mutation motley as Birc5b, a homolog of the mammalian Chromosomal Passenger Complex (CPC) component Survivin. The meiosis and mitosis defects in motley/birc5b mutant embryos are consistent with failed CPC function, and additional defects in astral microtubule remodeling contribute to failures in the initiation of cytokinesis furrow ingression. Unexpectedly, the motley/birc5b mutation also disrupts cortical microfilaments and GP RNP aggregation during early cell divisions. Birc5b localizes to the tips of astral microtubules along with polymerizing cortical F-actin and the GP RNPs. Mutant Birc5b co-localizes with cortical F-actin and GP RNPs, but fails to associate with astral microtubule tips, leading to disorganized microfilaments and GP RNP aggregation defects. Thus, maternal Birc5b localizes to astral microtubule tips and associates with cortical F-actin and GP RNPs, potentially linking the two cytoskeletons to mediate microtubule-microfilament reorganization and GP RNP aggregation during early embryonic cell cycles in zebrafish. In addition to the known mitotic function of CPC components, our analyses reveal a non-canonical role for an evolutionarily conserved CPC protein in microfilament reorganization and germ plasm aggregation.

Original languageEnglish (US)
Article numbere1003448
JournalPLoS Genetics
Volume9
Issue number4
DOIs
StatePublished - Apr 2013
Externally publishedYes

Fingerprint

Zebrafish
microfilaments
Actin Cytoskeleton
Danio rerio
Microtubules
embryo
germplasm
Embryonic Structures
microtubules
protein
Proteins
proteins
Actins
Cytokinesis
actin
defect
cytokinesis
microfilament proteins
mutation
Microfilament Proteins

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics
  • Cancer Research
  • Genetics(clinical)

Cite this

The Chromosomal Passenger Protein Birc5b Organizes Microfilaments and Germ Plasm in the Zebrafish Embryo. / Nair, Sreelaja; Marlow, Florence; Abrams, Elliott; Kapp, Lee; Mullins, Mary C.; Pelegri, Francisco.

In: PLoS Genetics, Vol. 9, No. 4, e1003448, 04.2013.

Research output: Contribution to journalArticle

Nair, Sreelaja ; Marlow, Florence ; Abrams, Elliott ; Kapp, Lee ; Mullins, Mary C. ; Pelegri, Francisco. / The Chromosomal Passenger Protein Birc5b Organizes Microfilaments and Germ Plasm in the Zebrafish Embryo. In: PLoS Genetics. 2013 ; Vol. 9, No. 4.
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