A Sterile 20 Family Kinase and Its Co-factor CCM-3 Regulate Contractile Ring Proteins on Germline Intercellular Bridges

Kathryn Rehain-Bell, Andrew Love, Michael E. Werner, Ian MacLeod, John R. Yates, Amy Shaub Maddox

Research output: Research - peer-reviewArticle

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Abstract

Germ cells in most animals are connected by intercellular bridges, actin-based rings that form stable cytoplasmic connections between cells promoting communication and coordination [1]. Moreover, these connections are required for fertility [1, 2]. Intercellular bridges are proposed to arise from stabilization of the cytokinetic ring during incomplete cytokinesis [1]. Paradoxically, proteins that promote closure of cytokinetic rings are enriched on stably open intercellular bridges [1, 3, 4]. Given this inconsistency, the mechanism of intercellular bridge stabilization is unclear. Here, we used the C. elegans germline as a model for identifying molecular mechanisms regulating intercellular bridges. We report that bridges are actually highly dynamic, changing size at precise times during germ cell development. We focused on the regulation of bridge stability by anillins, key regulators of cytokinetic rings and cytoplasmic bridges [1, 4–7]. We identified GCK-1, a conserved serine/threonine kinase [8], as a putative novel anillin interactor. GCK-1 works together with CCM-3, a known binding partner [9], to promote intercellular bridge stability and limit localization of both canonical anillin and non-muscle myosin II (NMM-II) to intercellular bridges. Additionally, we found that a shorter anillin, known to stabilize bridges [4, 7], also regulates NMM-II levels at bridges. Consistent with these results, negative regulators of NMM-II stabilize intercellular bridges in the Drosophila egg chamber [10, 11]. Together with our findings, this suggests that tuning of myosin levels is a conserved mechanism for the stabilization of intercellular bridges that can occur by diverse molecular mechanisms.

LanguageEnglish (US)
Pages860-867
Number of pages8
JournalCurrent Biology
Volume27
Issue number6
DOIs
StatePublished - Mar 20 2017

Fingerprint

Contractile Proteins
Phosphotransferases
anillin
myosin
germ cells
phosphotransferases (kinases)
proteins
Proteins
Myosin Type II
Germ Cells
Molecular Models
Cytokinesis
Protein-Serine-Threonine Kinases
Myosins
Cell Communication
Drosophila
Ovum
Fertility
Actins
molecular models

Keywords

  • anillin
  • C. elegans
  • CCM-3
  • cytokinesis
  • GCK III
  • GCK-1
  • intercellular bridge
  • rachis

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

A Sterile 20 Family Kinase and Its Co-factor CCM-3 Regulate Contractile Ring Proteins on Germline Intercellular Bridges. / Rehain-Bell, Kathryn; Love, Andrew; Werner, Michael E.; MacLeod, Ian; Yates, John R.; Maddox, Amy Shaub.

In: Current Biology, Vol. 27, No. 6, 20.03.2017, p. 860-867.

Research output: Research - peer-reviewArticle

Rehain-Bell, Kathryn ; Love, Andrew ; Werner, Michael E. ; MacLeod, Ian ; Yates, John R. ; Maddox, Amy Shaub. / A Sterile 20 Family Kinase and Its Co-factor CCM-3 Regulate Contractile Ring Proteins on Germline Intercellular Bridges. In: Current Biology. 2017 ; Vol. 27, No. 6. pp. 860-867
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