Regulation of Drosophila Vasa in vivo through paralogous cullin-RING E3 ligase specificity receptors

Jan Michael Kugler, Jae Sung Woo, Byung Ha Oh, Paul Lasko

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

In Drosophila species, molecular asymmetries guiding embryonic development are established maternally. Vasa, a DEAD-box RNA helicase, accumulates in the posterior pole plasm, where it is required for embryonic germ cell specification. Maintenance of Vasa at the posterior pole requires the deubiquitinating enzyme Fat facets, which protects Vasa from degradation. Here, we found that Gustavus (Gus) and Fsn, two ubiquitin Cullin-RING E3 ligase specificity receptors, bind to the same motif on Vasa through their paralogous B30.2/SPRY domains. Both Gus and Fsn accumulate in the pole plasm in a Vasa-dependent manner. Posterior Vasa accumulation is precocious in Fsn mutant oocytes; Fsn overexpression reduces ovarian Vasa levels, and embryos from Fsn-overexpressing females form fewer primordial germ cells (PGCs); thus, Fsn destabilizes Vasa. In contrast, endogenous Gus may promote Vasa activity in the pole plasm, as gus females produce embryos with fewer PGCs, and posterior accumulation of Vas is delayed in gus mutant oocytes that also lack one copy of cullin-5. We propose that Fsn- and Gus-containing E3 ligase complexes contribute to establishing a fine-tuned steady state of Vasa ubiquitination that influences the kinetics of posterior Vasa deployment.

Original languageEnglish
Pages (from-to)1769-1782
Number of pages14
JournalMolecular and Cellular Biology
Volume30
Issue number7
DOIs
Publication statusPublished - 2010 Apr 1
Externally publishedYes

Fingerprint

Cullin Proteins
Ubiquitin-Protein Ligases
Germ Cells
Drosophila
Oocytes
DEAD-box RNA Helicases
Embryonic Structures
Ubiquitination
Ubiquitin
Embryonic Development
Fats
Maintenance

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

Cite this

Regulation of Drosophila Vasa in vivo through paralogous cullin-RING E3 ligase specificity receptors. / Kugler, Jan Michael; Woo, Jae Sung; Oh, Byung Ha; Lasko, Paul.

In: Molecular and Cellular Biology, Vol. 30, No. 7, 01.04.2010, p. 1769-1782.

Research output: Contribution to journalArticle

@article{413b959a1a3b45bcab2ce995aa634fab,
title = "Regulation of Drosophila Vasa in vivo through paralogous cullin-RING E3 ligase specificity receptors",
abstract = "In Drosophila species, molecular asymmetries guiding embryonic development are established maternally. Vasa, a DEAD-box RNA helicase, accumulates in the posterior pole plasm, where it is required for embryonic germ cell specification. Maintenance of Vasa at the posterior pole requires the deubiquitinating enzyme Fat facets, which protects Vasa from degradation. Here, we found that Gustavus (Gus) and Fsn, two ubiquitin Cullin-RING E3 ligase specificity receptors, bind to the same motif on Vasa through their paralogous B30.2/SPRY domains. Both Gus and Fsn accumulate in the pole plasm in a Vasa-dependent manner. Posterior Vasa accumulation is precocious in Fsn mutant oocytes; Fsn overexpression reduces ovarian Vasa levels, and embryos from Fsn-overexpressing females form fewer primordial germ cells (PGCs); thus, Fsn destabilizes Vasa. In contrast, endogenous Gus may promote Vasa activity in the pole plasm, as gus females produce embryos with fewer PGCs, and posterior accumulation of Vas is delayed in gus mutant oocytes that also lack one copy of cullin-5. We propose that Fsn- and Gus-containing E3 ligase complexes contribute to establishing a fine-tuned steady state of Vasa ubiquitination that influences the kinetics of posterior Vasa deployment.",
author = "Kugler, {Jan Michael} and Woo, {Jae Sung} and Oh, {Byung Ha} and Paul Lasko",
year = "2010",
month = "4",
day = "1",
doi = "10.1128/MCB.01100-09",
language = "English",
volume = "30",
pages = "1769--1782",
journal = "Molecular and Cellular Biology",
issn = "0270-7306",
publisher = "American Society for Microbiology",
number = "7",

}

TY - JOUR

T1 - Regulation of Drosophila Vasa in vivo through paralogous cullin-RING E3 ligase specificity receptors

AU - Kugler, Jan Michael

AU - Woo, Jae Sung

AU - Oh, Byung Ha

AU - Lasko, Paul

PY - 2010/4/1

Y1 - 2010/4/1

N2 - In Drosophila species, molecular asymmetries guiding embryonic development are established maternally. Vasa, a DEAD-box RNA helicase, accumulates in the posterior pole plasm, where it is required for embryonic germ cell specification. Maintenance of Vasa at the posterior pole requires the deubiquitinating enzyme Fat facets, which protects Vasa from degradation. Here, we found that Gustavus (Gus) and Fsn, two ubiquitin Cullin-RING E3 ligase specificity receptors, bind to the same motif on Vasa through their paralogous B30.2/SPRY domains. Both Gus and Fsn accumulate in the pole plasm in a Vasa-dependent manner. Posterior Vasa accumulation is precocious in Fsn mutant oocytes; Fsn overexpression reduces ovarian Vasa levels, and embryos from Fsn-overexpressing females form fewer primordial germ cells (PGCs); thus, Fsn destabilizes Vasa. In contrast, endogenous Gus may promote Vasa activity in the pole plasm, as gus females produce embryos with fewer PGCs, and posterior accumulation of Vas is delayed in gus mutant oocytes that also lack one copy of cullin-5. We propose that Fsn- and Gus-containing E3 ligase complexes contribute to establishing a fine-tuned steady state of Vasa ubiquitination that influences the kinetics of posterior Vasa deployment.

AB - In Drosophila species, molecular asymmetries guiding embryonic development are established maternally. Vasa, a DEAD-box RNA helicase, accumulates in the posterior pole plasm, where it is required for embryonic germ cell specification. Maintenance of Vasa at the posterior pole requires the deubiquitinating enzyme Fat facets, which protects Vasa from degradation. Here, we found that Gustavus (Gus) and Fsn, two ubiquitin Cullin-RING E3 ligase specificity receptors, bind to the same motif on Vasa through their paralogous B30.2/SPRY domains. Both Gus and Fsn accumulate in the pole plasm in a Vasa-dependent manner. Posterior Vasa accumulation is precocious in Fsn mutant oocytes; Fsn overexpression reduces ovarian Vasa levels, and embryos from Fsn-overexpressing females form fewer primordial germ cells (PGCs); thus, Fsn destabilizes Vasa. In contrast, endogenous Gus may promote Vasa activity in the pole plasm, as gus females produce embryos with fewer PGCs, and posterior accumulation of Vas is delayed in gus mutant oocytes that also lack one copy of cullin-5. We propose that Fsn- and Gus-containing E3 ligase complexes contribute to establishing a fine-tuned steady state of Vasa ubiquitination that influences the kinetics of posterior Vasa deployment.

UR - http://www.scopus.com/inward/record.url?scp=77949346488&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77949346488&partnerID=8YFLogxK

U2 - 10.1128/MCB.01100-09

DO - 10.1128/MCB.01100-09

M3 - Article

C2 - 20123973

AN - SCOPUS:77949346488

VL - 30

SP - 1769

EP - 1782

JO - Molecular and Cellular Biology

JF - Molecular and Cellular Biology

SN - 0270-7306

IS - 7

ER -