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Mol. Hum. Reprod. Advance Access published online on June 30, 2008
Molecular Human Reproduction, doi:10.1093/molehr/gan037
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© The Author 2008. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Regulation of Mitochondrial Polarity in Mouse and Human Oocytes: The Influence of Cumulus Derived Nitric Oxide

Jonathan Van Blerkom1,2, Patrick Davis1,2 and Verena Thalhammer1,3

1Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, Colorado, 80309 2Colorado Reproductive Endocrinology, The Rose Medical Center, Denver, Colorado, 80220 3Department of Biochemistry, Regensburg University, Regensburg, Germany

Correspondence address. E-mail: jonathan.vanblerkom{at}colorado.edu

Whether exogenous factors influenced the level of mitochondrial polarity ({Delta}{Psi}m) in the subplasmalemmal cytoplasm of the oocyte was investigated with denuded and cumulus-enclosed human and mouse oocytes between the germinal vesicle and metaphase II stage. Co-culture of denuded oocytes with cumulus masses or primary cumulus cell cultures demonstrated a ‘proximity’ effect with respect to the detectable level of {Delta}{Psi}m in the oocyte. The specificity and reversibility of this effect on subplasmalemmal mitochondria were shown by repeated repositioning between cellular and acellular regions, which sequentially down- or upregulated {Delta}{Psi}m. Experimental studies with a nitric oxide (NO) donor and inhibitor of NO synthase indicate that NO produced by cumulus cells has a regulatory influence on {Delta}{Psi}m in the subplasmalemmal cytoplasm of the corresponding oocyte. Culture of denuded and cumulus-enclosed (intact) oocytes in low and high oxygen atmospheres suggests that competition between oxygen and NO at the mitochondrial level may regulate the level of {Delta}{Psi}m and maintain mitochondria homeostasis in the preovulatory oocyte, with a shift to higher polarity occurring after ovulation. The role of exogenous influences on oocyte mitochondrial polarity is discussed with respect to the regulation of developmental processes in the oocyte and early embryo.

Key Words: Mitochondria/Mitochondrial Polarity/Nitric Oxide/Cumulus Cells/Regulation of Mitochondrial Activity

Submitted on March 4, 2008; resubmitted on June 4, 2008; accepted on June 12, 2008.


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