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J. Biol. Chem., Vol. 278, Issue 25, 22771-22780, June 20, 2003

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Binding and Internalization of Lipopolysaccharide by Cla-1, a Human Orthologue of Rodent Scavenger Receptor B1^*

Tatyana G. Vishnyakova , Alexander V. Bocharov  ¶, Irina N. Baranova , Zhigang Chen , Alan T. Remaley  , Gyorgy Csako , Thomas L. Eggerman  || and Amy P. Patterson 

From the NHLBI, National Institutes of Health, Bethesda, Maryland 20892, the Department of Laboratory Medicine, W. G. Magnuson Clinical Center, National Institutes of Health, Bethesda, Maryland 20892, and the ^||Division of Diabetes, Endocrinology and Metabolic Diseases, NIDDK, National Institutes of Health, Bethesda, Maryland 20892

Scavenger receptor, class B, type I (SR-BI) mediates selective uptake of high density lipoprotein (HDL) cholesteryl ester. SR-BI recognizes HDL, low density lipoprotein (LDL), exchangeable apolipoproteins, and protein-free lipid vesicles containing negatively charged phospholipids. Lipopolysaccharides (LPS) are highly glycosylated anionic phospholipids contributing to septic shock. Despite significant structural similarities between anionic phospholipids and LPS, the role of SR-BI in LPS uptake is unknown. Cla-1, the human SR-BI orthologue, was determined to be a LPS-binding protein and endocytic receptor mediating the binding and internalization of lipoprotein-free, monomerized LPS. LPS strongly competed with HDL, lipidfree apoA-I and apoA-II for HDL binding to the mouse RAW cells. Stably transfected HeLa cells expressing Cla-1-bound LPS with a K_d of about 16 µg/ml, and had a 3–4-fold increase in binding capacity and LPS uptake. Bodipy-labeled LPS uptake was found to initially accumulate in the plasma membrane and subsequently in a perinuclear region identified predominantly as the Golgi complex. Bodipy-LPS and Alexa-apoA-I had staining that colocalized on the cell surface and intracellularly indicating similar transport mechanisms. When associated with HDL, LPS uptake was increased in Cla-1 overexpressing HeLa cells by 5–10-fold. Cla-1-associated ³H-LPS uptake exceeded ¹²⁵I-apolipoprotein uptake by 5-fold indicating a selective LPS uptake. Upon interacting with Cla-1 overexpressing HeLa cells, the complex (Bodipy-LPS/Alexa 488 apolipoprotein-labeled HDL) bound and was internalized as a holoparticle. Intracellularly, LPS and apolipoproteins were sorted to different intracellular compartments. With LPS-associated HDL, intracellular LPS co-localized predominantly with transferrin, indicating delivery to an endocytic recycling compartment. Our study reveals a close similarity between Cla-1-mediated selective LPS uptake and the recently described selective lipid sorting by rodent SR-BI. In summary, Cla-1 was found to bind and internalize monomerized and HDL-associated LPS, indicating that Cla-1 may play important role in septic shock by affecting LPS cellular uptake and clearance.

Received for publication, October 29, 2002 , and in revised form, March 13, 2003.

^* 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.

^¶ During part of this study the author was a guest scientist at the Food and Drug Administration, Center for Biologics Evaluation and Research, Division of Cellular and Gene Therapies. To whom correspondence should be addressed.

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