Novel functions of the ubiquitin-independent proteasome system in regulating Xenopus germline development

Hyojeong Hwang, Zhigang Jin, Vishnu Vardhan Krishnamurthy, Anumita Saha, Peter S. Klein, Benjamin Garcia, Wenyan Mei, Mary Lou King, Kai Zhang, Jing Yang

Research output: Contribution to journalArticle

Abstract

In most species, early germline development occurs in the absence of transcription with germline determinants subject to complex translational and post-translational regulations. Here, we report for the first time that early germline development is influenced by dynamic regulation of the proteasome system, previously thought to be ubiquitously expressed and toserve’housekeeping’ roles in controlling protein homeostasis.We show that proteasomes are present in a gradient with the highest levels in the animal hemisphere and extending into the vegetal hemisphere of Xenopus oocytes. This distribution changes dramatically during the oocyte-to-embryo transition, with proteasomes becoming enriched in and restricted to the animal hemisphere and therefore separated from vegetally localized germline determinants. We identify Dead-end1 (Dnd1), a master regulator of vertebrate germline development, as a novel substrate of the ubiquitin-independent proteasomes. In the oocyte, ubiquitin-independent proteasomal degradation acts together with translational repression to prevent premature accumulation of Dnd1 protein. In the embryo, artificially increasing ubiquitin-independent proteasomal degradation in the vegetal pole interferes with germline development. Our work thus reveals novel inhibitory functions and spatial regulation of the ubiquitin-independent proteasome during vertebrate germline development.

Original languageEnglish (US)
Article numberdev172700
JournalDevelopment (Cambridge)
Volume146
Issue number8
DOIs
StatePublished - Apr 15 2019

Fingerprint

Proteasome Endopeptidase Complex
Ubiquitin
Xenopus
embryo
vertebrate
Oocytes
degradation
protein
regulation
animal
homeostasis
Vertebrates
Embryonic Structures
determinants
substrate
repression
Pole
Proteins
Homeostasis

Keywords

  • Dnd1
  • Germline development
  • Oocyte-to-embryo transition
  • Ubiquitin-independent proteasome
  • Xenopus

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology

Cite this

Novel functions of the ubiquitin-independent proteasome system in regulating Xenopus germline development. / Hwang, Hyojeong; Jin, Zhigang; Krishnamurthy, Vishnu Vardhan; Saha, Anumita; Klein, Peter S.; Garcia, Benjamin; Mei, Wenyan; King, Mary Lou; Zhang, Kai; Yang, Jing.

In: Development (Cambridge), Vol. 146, No. 8, dev172700, 15.04.2019.

Research output: Contribution to journalArticle

Hwang, Hyojeong ; Jin, Zhigang ; Krishnamurthy, Vishnu Vardhan ; Saha, Anumita ; Klein, Peter S. ; Garcia, Benjamin ; Mei, Wenyan ; King, Mary Lou ; Zhang, Kai ; Yang, Jing. / Novel functions of the ubiquitin-independent proteasome system in regulating Xenopus germline development. In: Development (Cambridge). 2019 ; Vol. 146, No. 8.
@article{58b8ca64f4cb4c289acb64860c50dcf3,
title = "Novel functions of the ubiquitin-independent proteasome system in regulating Xenopus germline development",
abstract = "In most species, early germline development occurs in the absence of transcription with germline determinants subject to complex translational and post-translational regulations. Here, we report for the first time that early germline development is influenced by dynamic regulation of the proteasome system, previously thought to be ubiquitously expressed and toserve’housekeeping’ roles in controlling protein homeostasis.We show that proteasomes are present in a gradient with the highest levels in the animal hemisphere and extending into the vegetal hemisphere of Xenopus oocytes. This distribution changes dramatically during the oocyte-to-embryo transition, with proteasomes becoming enriched in and restricted to the animal hemisphere and therefore separated from vegetally localized germline determinants. We identify Dead-end1 (Dnd1), a master regulator of vertebrate germline development, as a novel substrate of the ubiquitin-independent proteasomes. In the oocyte, ubiquitin-independent proteasomal degradation acts together with translational repression to prevent premature accumulation of Dnd1 protein. In the embryo, artificially increasing ubiquitin-independent proteasomal degradation in the vegetal pole interferes with germline development. Our work thus reveals novel inhibitory functions and spatial regulation of the ubiquitin-independent proteasome during vertebrate germline development.",
keywords = "Dnd1, Germline development, Oocyte-to-embryo transition, Ubiquitin-independent proteasome, Xenopus",
author = "Hyojeong Hwang and Zhigang Jin and Krishnamurthy, {Vishnu Vardhan} and Anumita Saha and Klein, {Peter S.} and Benjamin Garcia and Wenyan Mei and King, {Mary Lou} and Kai Zhang and Jing Yang",
year = "2019",
month = "4",
day = "15",
doi = "10.1242/dev.172700",
language = "English (US)",
volume = "146",
journal = "Development",
issn = "0950-1991",
publisher = "Company of Biologists Ltd",
number = "8",

}

TY - JOUR

T1 - Novel functions of the ubiquitin-independent proteasome system in regulating Xenopus germline development

AU - Hwang, Hyojeong

AU - Jin, Zhigang

AU - Krishnamurthy, Vishnu Vardhan

AU - Saha, Anumita

AU - Klein, Peter S.

AU - Garcia, Benjamin

AU - Mei, Wenyan

AU - King, Mary Lou

AU - Zhang, Kai

AU - Yang, Jing

PY - 2019/4/15

Y1 - 2019/4/15

N2 - In most species, early germline development occurs in the absence of transcription with germline determinants subject to complex translational and post-translational regulations. Here, we report for the first time that early germline development is influenced by dynamic regulation of the proteasome system, previously thought to be ubiquitously expressed and toserve’housekeeping’ roles in controlling protein homeostasis.We show that proteasomes are present in a gradient with the highest levels in the animal hemisphere and extending into the vegetal hemisphere of Xenopus oocytes. This distribution changes dramatically during the oocyte-to-embryo transition, with proteasomes becoming enriched in and restricted to the animal hemisphere and therefore separated from vegetally localized germline determinants. We identify Dead-end1 (Dnd1), a master regulator of vertebrate germline development, as a novel substrate of the ubiquitin-independent proteasomes. In the oocyte, ubiquitin-independent proteasomal degradation acts together with translational repression to prevent premature accumulation of Dnd1 protein. In the embryo, artificially increasing ubiquitin-independent proteasomal degradation in the vegetal pole interferes with germline development. Our work thus reveals novel inhibitory functions and spatial regulation of the ubiquitin-independent proteasome during vertebrate germline development.

AB - In most species, early germline development occurs in the absence of transcription with germline determinants subject to complex translational and post-translational regulations. Here, we report for the first time that early germline development is influenced by dynamic regulation of the proteasome system, previously thought to be ubiquitously expressed and toserve’housekeeping’ roles in controlling protein homeostasis.We show that proteasomes are present in a gradient with the highest levels in the animal hemisphere and extending into the vegetal hemisphere of Xenopus oocytes. This distribution changes dramatically during the oocyte-to-embryo transition, with proteasomes becoming enriched in and restricted to the animal hemisphere and therefore separated from vegetally localized germline determinants. We identify Dead-end1 (Dnd1), a master regulator of vertebrate germline development, as a novel substrate of the ubiquitin-independent proteasomes. In the oocyte, ubiquitin-independent proteasomal degradation acts together with translational repression to prevent premature accumulation of Dnd1 protein. In the embryo, artificially increasing ubiquitin-independent proteasomal degradation in the vegetal pole interferes with germline development. Our work thus reveals novel inhibitory functions and spatial regulation of the ubiquitin-independent proteasome during vertebrate germline development.

KW - Dnd1

KW - Germline development

KW - Oocyte-to-embryo transition

KW - Ubiquitin-independent proteasome

KW - Xenopus

UR - http://www.scopus.com/inward/record.url?scp=85065347638&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85065347638&partnerID=8YFLogxK

U2 - 10.1242/dev.172700

DO - 10.1242/dev.172700

M3 - Article

C2 - 30910828

AN - SCOPUS:85065347638

VL - 146

JO - Development

JF - Development

SN - 0950-1991

IS - 8

M1 - dev172700

ER -