RRC ID 46382
Author Kim S, Govindan JA, Tu ZJ, Greenstein D.
Title SACY-1 DEAD-Box helicase links the somatic control of oocyte meiotic maturation to the sperm-to-oocyte switch and gamete maintenance in Caenorhabditis elegans.
Journal Genetics
Abstract In sexually reproducing animals, oocytes arrest at diplotene or diakinesis and resume meiosis (meiotic maturation) in response to hormones. In Caenorhabditis elegans, major sperm protein triggers meiotic resumption through a mechanism involving somatic Gα(s)-adenylate cyclase signaling and soma-to-germline gap-junctional communication. Using genetic mosaic analysis, we show that the major effector of Gα(s)-adenylate cyclase signaling, protein kinase A (PKA), is required in gonadal sheath cells for oocyte meiotic maturation and dispensable in the germ line. This result rules out a model in which cyclic nucleotides must transit through sheath-oocyte gap junctions to activate PKA in the germ line, as proposed in vertebrate systems. We conducted a genetic screen to identify regulators of oocyte meiotic maturation functioning downstream of Gα(s)-adenylate cyclase-PKA signaling. We molecularly identified 10 regulatory loci, which include essential and nonessential factors. sacy-1, which encodes a highly conserved DEAD-box helicase, is an essential germline factor that negatively regulates meiotic maturation. SACY-1 is a multifunctional protein that establishes a mechanistic link connecting the somatic control of meiotic maturation to germline sex determination and gamete maintenance. Modulatory factors include multiple subunits of a CoREST-like complex and the TWK-1 two-pore potassium channel. These factors are not absolutely required for meiotic maturation or its negative regulation in the absence of sperm, but function cumulatively to enable somatic control of meiotic maturation. This work provides insights into the genetic control of meiotic maturation signaling in C. elegans, and the conserved factors identified here might inform analysis in other systems through either homology or analogy.
Volume 192(3)
Pages 905-28
Published 2012-11-1
DOI 10.1534/genetics.112.143271
PII genetics.112.143271
PMID 22887816
PMC PMC3522166
MeSH Amino Acid Sequence Animals Caenorhabditis elegans / genetics* Caenorhabditis elegans / metabolism Caenorhabditis elegans Proteins / genetics* Caenorhabditis elegans Proteins / metabolism Cyclic AMP / metabolism DEAD-box RNA Helicases / genetics* DEAD-box RNA Helicases / metabolism Female Gene Order Germ Cells / metabolism Gonads / metabolism Infertility / genetics Male Meiosis* Molecular Sequence Data Mutation Necrosis / genetics Oocytes / metabolism* Sequence Alignment Sex Determination Processes Signal Transduction Spermatozoa / metabolism*
IF 4.015
Times Cited 18
WOS Category GENETICS & HEREDITY
Resource
C.elegans tm4724 tm5503 tm4802 tm611 tm1661