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J. Biol. Chem., Vol. 280, Issue 11, 10357-10367, March 18, 2005

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Prostaglandin F₂-mediated Activation of Apoptotic Signaling Cascades in the Corpus Luteum during Apoptosis

INVOLVEMENT OF CASPASE-ACTIVATED DNase^*

Vijay K. Yadav, Garimella Lakshmi, and Rudraiah Medhamurthy

From the Department of Molecular Reproduction, Development and Genetics, Indian Institute of Science, Bangalore 560 012, India

Prostaglandin F₂ (PGF₂) acting via a G protein-coupled receptor has been shown to induce apoptosis in the corpus luteum of many species. Studies were carried out to characterize changes in the apoptotic signaling cascade(s) culminating in luteal tissue apoptosis during PGF₂-induced luteolysis in the bovine species in which initiation of apoptosis was demonstrable at 18 h after exogenous PGF₂ treatment. An analysis of intrinsic arm of apoptotic signaling cascade elements revealed that PGF₂ injection triggered increased ratio of Bax to Bcl-2 in the luteal tissue as early as 4 h posttreatment that remained elevated until 18 h. This increase was associated with the elevation in the active caspase-9 and -3 protein levels and activity (p < 0.05) at 4–12 h, but a spurt in the activity was seen only at 18 h posttreatment that could not be accounted for by the changes in the Bax/Bcl-2 ratio or changes in translocation of Bax to mitochondria. Examination of luteal tissue for FasL/Fas death receptor cascade revealed increased expression of FasL and Fas at 18 h accompanied by a significant (p < 0.05) induction in the caspase-8 activity and truncated Bid levels. Furthermore, intrabursal administration of specific caspase inhibitors, downstream to the extrinsic and intrinsic apoptotic signaling cascades, in a pseudopregnant rat model revealed a greater importance of extrinsic apoptotic signaling cascade in mediating luteal tissue apoptosis during PGF₂ treatment. The DNase responsible for PGF₂-induced apoptotic DNA fragmentation was found to be Ca²⁺/Mg²⁺-dependent, temperature-sensitive DNase, and optimally active at neutral pH conditions. This putative DNase was inhibited by the recombinant inhibitor of caspase-activated DNase, and immunodepletion of caspase-activated DNase from luteal lysates abolished the observed DNA fragmentation activity. Together, these data demonstrate for the first time temporal and spatial changes in the apoptotic signaling cascades during PGF₂-in-duced apoptosis in the corpus luteum.

Received for publication, August 20, 2004 , and in revised form, December 20, 2004.

^* This work was supported in part by grants from the Council of Scientific and Industrial Research, Indian Council of Medical Research, and University Grants Commission (New Delhi, India). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains Supplemental Figs. 1–5.

Supported by fellowship from the Council of Scientific and Industrial Research (New Delhi, India).

To whom correspondence should be addressed: Dept. of Molecular Reproduction, Development and Genetics, Indian Institute of Science, Bangalore 560012, India. E-mail: rmm{at}mrdg.iisc.ernet.in.

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