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J. Biol. Chem., Vol. 280, Issue 50, 41171-41177, December 16, 2005

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Diacylglycerol Induces Fusion of Nuclear Envelope Membrane Precursor Vesicles^*

Teresa Barona1, Richard D. Byrne1, Trevor R. Pettitt¶, Michael J. O. Wakelam¶, Banafshe Larijani, and Dominic L. Poccia||2

From the Biology Department, Amherst College, Amherst, Massachusetts 01002, the Cell Biophysics Laboratory, Cancer Research UK (CRUK), London Research Institute (LRI), 44 Lincoln's Inn Fields, London WC2A 3PX, United Kingdom, the ^¶CRUK Institute of Cancer Studies, University of Birmingham, Birmingham, B15 2TT, United Kingdom, and the ^||Unidade de Investigação na Biologia do Desenvolvimento, Universidade Lusófona, 376 Campo Grande, 1749-024 Lisbon, Portugal

Purified membrane vesicles isolated from sea urchin eggs form nuclear envelopes around sperm nuclei following GTP hydrolysis in the presence of cytosol. A low density subfraction of these vesicles (MV1), highly enriched in phosphatidylinositol (PtdIns), is required for nuclear envelope formation. Membrane fusion of MV1 with a second fraction that contributes most of the nuclear envelope can be initiated without GTP by an exogenous bacterial PtdIns-specific phospholipase C (PI-PLC) which hydrolyzes PtdIns to form diacylglycerides and inositol 1-phosphate. This PI-PLC hydrolyzes a subset of sea urchin membrane vesicle PtdIns into diglycerides enriched in long chain, polyunsaturated species as revealed by a novel liquid chromatography-mass spectrometry analysis. Large unilammelar vesicles (LUVs) enriched in PtdIns can substitute for MV1 in PI-PLC induced nuclear envelope formation. Moreover, MV1 prehydrolyzed with PI-PLC and washed to remove inositols leads to spontaneous nuclear envelope formation with MV2 without further PI-PLC treatment. LUVs enriched in diacylglycerol mimic prehydrolyzed MV1. These results indicate that production of membrane-destabilizing diglycerides in membranes enriched in PtdIns may facilitate membrane fusion in a natural membrane system and suggest that MV1, which binds only to two places on the sperm nucleus, may initiate fusion locally.

Received for publication, November 15, 2004 , and in revised form, August 24, 2005.

^* This work was partially supported by Fundaçao para a Ciência e a Tecnologia PRAXIS XXI Grant BD-19568-99 (to T. B.), by an Amherst College Faculty Research Award of the H. Axel Schupf '57 Fund for Intellectual Life (to D. L. P.), and by The Wellcome Trust (to M. J. O. W.). 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.

¹ These authors contributed equally to this work.

² To whom correspondence should be addressed. Tel.: 413-542-2198; Fax: 413-542-7955; E-mail: dlpoccia{at}amherst.edu.

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