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PMID:15930113

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Citation

Maddox, AS, Habermann, B, Desai, A and Oegema, K (2005) Distinct roles for two C. elegans anillins in the gonad and early embryo. Development 132:2837-48

Abstract

Anillins are conserved proteins that are important for stabilizing and remodeling the actin cytoskeleton. Anillins have been implicated in cytokinesis in several systems and in cellularization of the syncytial Drosophila embryo. Here, we examine the functions of three C. elegans proteins with homology to anillin (ANI-1, ANI-2 and ANI-3). We show that ANI-1 and ANI-2 contribute to embryonic viability by performing distinct functions in the early embryo and gonad, respectively. By contrast, ANI-3 appears to be dispensable for embryonic development. ANI-1 is essential for cortical ruffling and pseudocleavage, contractile events that occur in embryos prior to mitosis. ANI-1 is also required for the highly asymmetric cytokinetic events that extrude the two polar bodies during oocyte meiosis, but is dispensable for cytokinesis following mitotic chromosome segregation. During both meiosis and mitosis, ANI-1 targets the septins, but not myosin II, to the contractile ring and does not require either for its own targeting. In contrast to ANI-1, ANI-2 functions during oogenesis to maintain the structure of the rachis, the central core of cytoplasm that connects the developing oocytes in the syncytial gonad. In ANI-2-depleted worms, oocytes disconnect prematurely from the defective rachis, generating embryos of varying sizes. Our results highlight specialization of divergent anillin family proteins in the C. elegans life cycle and reveal conserved roles for this protein family in organizing syncytial structures and cortical contractility.

Links

PubMed Online version:10.1242/dev.01828

Keywords

Animals; Caenorhabditis elegans/cytology; Caenorhabditis elegans/embryology; Caenorhabditis elegans/genetics; Caenorhabditis elegans/metabolism; Caenorhabditis elegans Proteins/genetics; Caenorhabditis elegans Proteins/metabolism; Cell Differentiation; Cell Membrane/genetics; Cell Membrane/metabolism; Cell Surface Extensions; Contractile Proteins/genetics; Contractile Proteins/metabolism; Cytokinesis; Embryo, Nonmammalian/cytology; Embryo, Nonmammalian/embryology; Embryo, Nonmammalian/metabolism; Gene Expression Regulation, Developmental; Genome; Gonads/cytology; Gonads/embryology; Gonads/metabolism; Meiosis; Microfilament Proteins/genetics; Microfilament Proteins/metabolism; Mitosis; Myosin Heavy Chains/metabolism; Myosin Type II/metabolism; Oocytes/cytology; Oocytes/metabolism; RNA Interference; Survival Rate; Time Factors

Significance

Annotations

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

CAEEL:ANI2

located_in

GO:0005737: cytoplasm

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

CAEEL:ANI2

involved_in

GO:0032504: multicellular organism reproduction

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI2

involved_in

GO:0008406: gonad development

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI2

involved_in

GO:0009792: embryo development ending in birth or egg hatching

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI2

involved_in

GO:0048477: oogenesis

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI1

located_in

GO:0032154: cleavage furrow

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

CAEEL:ANI1

located_in

GO:0005938: cell cortex

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

CAEEL:ANI1

involved_in

GO:0045138: nematode male tail tip morphogenesis

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI1

enables

GO:0051015: actin filament binding

ECO:0000250: sequence similarity evidence used in manual assertion

UniProtKB:Q9V4P1

F

Seeded From UniProt

complete

CAEEL:ANI1

involved_in

GO:0040038: polar body extrusion after meiotic divisions

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI1

involved_in

GO:0040035: hermaphrodite genitalia development

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI1

involved_in

GO:0040011: locomotion

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI1

involved_in

GO:0040002: collagen and cuticulin-based cuticle development

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI1

part_of

GO:0005938: cell cortex

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

CAEEL:ANI1

involved_in

GO:0008104: protein localization

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI1

involved_in

GO:0009792: embryo development ending in birth or egg hatching

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI1

involved_in

GO:0030590: first cell cycle pseudocleavage

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI1

involved_in

GO:0030865: cortical cytoskeleton organization

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI1

involved_in

GO:0031106: septin ring organization

ECO:0000315: mutant phenotype evidence used in manual assertion

P

Seeded From UniProt

complete

CAEEL:ANI1

part_of

GO:0032154: cleavage furrow

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

See also

References

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