Major sperm protein signaling promotes oocyte microtubule reorganization prior to fertilization in Caenorhabditis elegans

Jana E. Harris, J. Amaranath Govindan, Ikuko Yamamoto, Joel Schwartz, Irina Kaverina, David Greenstein

Research output: Contribution to journalArticlepeer-review

42 Scopus citations

Abstract

In most animals, female meiotic spindles assemble in the absence of centrosomes; instead, microtubule nucleation by chromatin, motor activity, and microtubule dynamics drive the self-organization of a bipolar meiotic spindle. Meiotic spindle assembly commences when microtubules gain access to chromatin after nuclear envelope breakdown (NEBD) during meiotic maturation. Although many studies have addressed the chromatin-based mechanism of female meiotic spindle assembly, it is less clear how signaling influences microtubule localization and dynamics prior to NEBD. Here we analyze microtubule behavior in Caenorhabditis elegans oocytes at early stages of the meiotic maturation process using confocal microscopy and live-cell imaging. In C. elegans, sperm trigger oocyte meiotic maturation and ovulation using the major sperm protein (MSP) as an extracellular signaling molecule. We show that MSP signaling reorganizes oocyte microtubules prior to NEBD and fertilization by affecting their localization and dynamics. We present evidence that MSP signaling reorganizes oocyte microtubules through a signaling network involving antagonistic Gαo/i and Gαs pathways and gap-junctional communication with somatic cells of the gonad. We propose that MSP-dependent microtubule reorganization promotes meiotic spindle assembly by facilitating the search and capture of microtubules by meiotic chromatin following NEBD.

Original languageEnglish (US)
Pages (from-to)105-121
Number of pages17
JournalDevelopmental Biology
Volume299
Issue number1
DOIs
StatePublished - Nov 1 2006
Externally publishedYes

Bibliographical note

Funding Information:
We are grateful to Al Reynolds and Nicole Lobdell for generously sharing their spinning disk confocal microscope and providing training and assistance. We thank Anne Kenworthy and Jeffrey Shawn Goodwin for advice on the FRAP analysis. Sam Wells and Sean Schaffer provided helpful suggestions for optimizing live-cell imaging. Bob Barstead, Gary Moulder, Martin Srayko, Geraldine Seydoux, and the Caenorhabditis Genetic Center kindly provided strains. We thank Karen Oegema and Tony Hyman for their gift of the CeGrip-1 antibodies and Byeong Cha and Barth Grant for critical reading of the manuscript. J.E.H. would like to thank Mary Kosinski and Brandon Lute for their ideas and encouragement. This work was supported by NIH grants GM65115 and GM57173 (D.G.) and an NIH Training Grant 2T32HD007043-31 (J.E.H.).

Keywords

  • C. elegans
  • G-protein
  • Meiosis
  • Meiotic maturation
  • Microtubule
  • Oocyte
  • Signaling
  • Somatic gonad

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