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J. Biol. Chem., Vol. 281, Issue 9, 5398-5405, March 3, 2006

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Follicular Fluid High Density Lipoprotein-associated Sphingosine 1-Phosphate Is a Novel Mediator of Ovarian Angiogenesis^*

Sören von Otte¹², Jürgen R. J. Paletta¹, Steffi Becker, Simone König^¶, Manfred Fobker^||, Robert R. Greb^**, Ludwig Kiesel^**, Gerd Assmann^||, Klaus Diedrich, and Jerzy-Roch Nofer^||

From the Klinik für Frauenheilkunde und Geburtshilfe, Universitätsklinikum Schleswig-Holstein, Campus Lübeck, Ratzeburger Allee 160, 23538 Lubeck, Germany, the Klinik und Poliklinik für Unfall-, Hand-, und Wiederherstellungschirurgie, ^||Institut für Klinische Chemie und Laboratoriumsmedizin, and ^**Klinik und Poliklinik für Frauenheilkunde und Geburtshilfe, Westfälische Wilhelms-Universität Münster, 48149 Münster, Germany, the ^¶Integrierte Funktionelle Genomik, Interdisziplinäres Zentrum für Klinische Forschung der Medizinischen Fakultät der Universität Münster, 48149 Münster, Germany, and the Leibniz Institut für Arterioskleroseforschung an der Universität Münster, 48149 Münster, Germany

Angiogenesis plays an important role in the development of the ovarian follicle and its subsequent transition into the corpus luteum. Accordingly, follicular fluid is a rich source of mitogenic and angiogenic factors such as basic fibroblast growth factor and vascular endothelial growth factor secreted by granulosa cells. In the present study, we show that follicular fluid deprived of basic fibroblast growth factor or vascular endothelial growth factor by means of thermal denaturation or antibody neutralization retains its capacity to stimulate endothelial proliferation and angiogenesis. Mass spectrometric analysis of chromatographic fractions stimulating endothelial growth obtained from follicular fluid revealed that the heat-stable mitogenic activity is identical with the subfraction of high density lipoproteins purified from follicular fluid (FF-HDL). Further investigations demonstrated that sphingosine 1-phosphate (S1P), one of the lysophospholipids associated with HDL, accounts for the capacity of this lipoprotein to stimulate endothelial growth and the formation of new vessels. Activation of mitogen-activated protein kinase (p42/44^ERK1/2), protein kinase C, and protein kinase Akt represent signaling pathways utilized by FF-HDL and S1P to induce endothelial proliferation and angiogenesis. We conclude that FF-HDL represents a novel mitogenic and angiogenic factor present in follicular fluid and that S1P is one of the FF-HDL lipid components accounting for this activity.

Received for publication, August 9, 2005 , and in revised form, December 12, 2005.

^* 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 two authors contributed equally to this work.

² To whom correspondence should be addressed. Tel.: 49-451-500-2134; Fax: 49-451-500-2430; E-mail: svonotte{at}gmx.de.

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