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Cumulus cell contact during oocyte maturation in mice regulates meiotic spindle positioning and enhances developmental competence

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Abstract

Purpose

To investigate the role of cumulus cell contact during oocyte maturation on meiotic spindle assembly and the acquisition of developmental competence.

Methods

Cumulus oocyte complexes isolated from mouse ovaries subjected to in vitro or in vivo maturation were analyzed by confocal microscopy with respect to oocyte somatic cell contacts and for their ability to develop after parthenogenic activation during embryo culture.

Results

Cell contact is maintained during maturation in vivo, predisposing oocytes to cortical meiotic spindle assembly and developmental competence acquisition. In contrast, oocytes matured in vitro lose cell contact coincident with central meiotic spindle assembly that results in cleavage delays upon egg activation and failure to form blastocysts. Experimental disruption of cell contact by the actin-depolymerizing agent latrunculin B results in the formation of enlarged meiotic spindles with dispersed chromosomes unlike the compact ordering of chromosomes observed on spindles formed after in vivo maturation, suggesting a link between cell contact and the acquisition of developmental competence.

Conclusions

Somatic cell contact optimizes oocyte quality during meiotic maturation by regulating the spatial organization and function of the meiotic spindle through actin-dependent mechanisms that enhance development.

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Abbreviations

TZP:

transzonal projections

GV:

germinal vesicle

COC:

cumulus oocyte complex

IVM:

in vitro maturation

IVO:

in vivo maturation

LatB:

Latrunculin B

MT:

microtubules

ICM:

inner cell mass

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Acknowledgments

We thank past and present members of the Albertini Laboratory for their guidance and support and Drs Stephen Palmer and Daniel DeMatos for advice and kind donations of the recombinant FSH used in these studies.

Author information

Authors and Affiliations

  1. Program in Cellular, Molecular and Developmental Biology, Tufts University, Boston, MA, 02111, USA

    Susan L. Barrett

  2. Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, KS, 66160, USA

    Susan L. Barrett & David F. Albertini

  3. Marine Biological Laboratory, Woods Hole, MA, USA

    David F. Albertini

  4. Northwestern University, 303 E. Superior Street, Chicago, IL, 69611, USA

    Susan L. Barrett

Authors
  1. Susan L. Barrett
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  2. David F. Albertini
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Corresponding author

Correspondence to Susan L. Barrett.

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Capsule

In vitro maturation of mouse COCs requires the maintenance of cumulus cell contact to achieve developmental competence through an actin dependent mechanism that mediates meiotic spindle anchoring to the oocyte cortex.

Funding

NIH (HD 42076), ESHE Fund, The Hall Family Foundation

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Barrett, S.L., Albertini, D.F. Cumulus cell contact during oocyte maturation in mice regulates meiotic spindle positioning and enhances developmental competence. J Assist Reprod Genet 27, 29–39 (2010). https://doi.org/10.1007/s10815-009-9376-9

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  • DOI: https://doi.org/10.1007/s10815-009-9376-9

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